Rehabilitation of Sports Injuries - Scientific Basis

REHABILITATION OF
SPORTS INJURIES:
SCIENTIFIC BASIS
VOLUME X OF THE ENCYLOPAEDIA OF SPORTS MEDICINE
AN IOC MEDICAL COMMITTEE PUBLICATION
IN COLLABORATION WITH THE
INTERNATIONAL FEDERATION OF SPORTS MEDICINE
EDITED BY
WALTER R. FRONTERA
Blackwell
Science
REHABILITATION OF SPORTS INJURIES:
SCIENTIFIC BASIS
IOC MEDICAL COMMISSION
SUB-COMMISSION ON PUBLICATIONS IN THE SPORT SCIENCES
Howard G. Knuttgen PhD (Co-ordinator)

Boston, Massachusetts, USA
Harm Kuipers MD, PhD
Maastricht, The Netherlands
Per A.F.H. Renström MD, PhD
Stockholm, Sweden
REHABILITATION OF
SPORTS INJURIES:
SCIENTIFIC BASIS
VOLUME X OF THE ENCYLOPAEDIA OF SPORTS MEDICINE
AN IOC MEDICAL COMMITTEE PUBLICATION
IN COLLABORATION WITH THE
INTERNATIONAL FEDERATION OF SPORTS MEDICINE
EDITED BY
WALTER R. FRONTERA
Blackwell
Science
© 2003 International Olympic Committee
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First published 2003
Library of Congress Cataloging-in-Publication Data
Rehabilitation of sports injuries : scientific basis / edited by

Walter R. Frontera.
p. cm. — (The Encyclopaedia of sports medicine ; v. 10)
“An IOC Medical Commission publication in collaboration
with the International Federation of Sports Medicine.”
Includes bibliographical references and index.
ISBN 0-632-05813-7
1. Sports injuries. 2. AthletesaRehabilitation.
I. Frontera, Walter R., 1955– II. IOC Medical Commission.
III. International Federation of Sports Medicine. IV. Series.
RD97 .R439 2002
617.1’027adc21
2002007253
ISBN 0-632-05813-7
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Contents
List of Contributors, vi 7 Physiological and Functional Implications

of Injury, 144
Forewords, viii c.j. standaert and s.a. herring
Preface, ix 8 Psychological Factors in Sports Injury

Rehabilitation, 160
Part 1: Epidemiology and b.w. brewer and a.e. cornelius
Pathology
1 Epidemiology of Sports Injuries: Part 4: Clinical Rehabilitation
Implications for Rehabilitation, 3 Interventions
w.r. frontera 9 Pharmacological Agents and Acupuncture
in Rehabilitation, 187
2 Pathophysiology of Injury, 10
j.k. silver and j. audette
m.l. schamblin and m.r. safran
10 Physical Modalities and Pain
Part 2: Basic Science of Tissue Management, 204
Healing and Repair j.m. press, c.t. plastaras and
3 Skeletal Muscle Regeneration After Injury: s.l. wiesner
Cellular and Molecular Events, 35
11 Flexibility and Joint Range of Motion, 232
a.-x. bigard and e. fink
m. schwellnus
4 Tissue Healing and Repair: Tendons and 12 Strength and Endurance, 258
Ligaments, 56 g. grimby and r. thomeé
b.w. oakes
13 Proprioception and Coordination, 274
5 Tissue Healing and Repair: Bone and j.j. gonzález iturri
Cartilage, 99
k.-m. chan, h.c.l. ho and 14 Functional Rehabilitation and Return to
c.w.c. tong Training and Competition, 288
w.b. kibler and t.j. chandler
Part 3: Practical Issues
15 Orthoses in the Prevention and
6 Physiological and Performance Rehabilitation of Injuries, 301
Consequences of Training Cessation in w. micheo and a. esquenazi
Athletes: Detraining, 117
i. mujika and s. padilla Index, 317
v
List of Contributors
J. AUDETTE MD, Instructor, Department of W.R. FRONTERA MD, PhD, Chairman,

Physical Medicine and Rehabilitation, Spaulding Department of Physical Medicine and Rehabilitation,
Rehabilitation Hospital, Harvard Medical School, Spaulding Rehabilitation Hospital, Harvard Medical
Boston MA, USA School, Boston MA, USA
A.-X. BIGARD MD, Department of Human J.J. GONZÁLEZ ITURRI MD, Department
Factors, Centre de Recherches du Service de Santé des of Physical Medicine and Rehabilitation, University of
Armées, BP 87 La Tronche, 38702, France Navarra, 31007 Pamploma, Spain
B.W. BREWER PhD, Associate Professor, G. GRIMBY MD, PhD, Professor Emeritus,
Department of Psychology, Springfield College, Department of Rehabilitation Medicine, Göteborg
Springfield, Massachusetts 01109, USA University, Göteborg, Sweden
K.-M. CHAN MD, Chair Professor and Chief of S.A. HERRING MD, Clinical Professor,
Service, Hong Kong Centre of Sports Medicine & Sports Departments of Orthopedics and Rehabilitation Medicine,
Science, Department of Orthopaedics & Traumatology, University of Washington, Seattle, Washington, USA
Chinese University of Hong Kong, Prince of Wales
Hospital, Hong Kong H.C.L. HO MBChB, Department of Orthopaedics
and Traumatology, The Chinese University of Hong
T.J. CHANDLER EdD, Associate Professor, Kong, Prince of Wales Hospital, Hong Kong
Exercise Science, Sport, and Recreation, Marshall
University, Huntington WV, USA W.B. KIBLER MD, Medical Director, Lexington
Sports Medicine Center, Lexington, KY 40504, USA
A.E. CORNELIUS PhD, Center for Performance
Enhancement and Applied Research, Department of W. MICHEO MD, University of Puerto Rico,
Psychology, Springfield College, 263 Alden Street, Medical Sciences Campus, School of Medicine,
Springfield, MA 01109, USA Department of Physical Medicine, Rehabilitation and
Sports Medicine, San Juan PR 00936-5067
A. ESQUENAZI MD, Director, Gait and Motion
Analysis Laboratory Moss Rehabilitation Hospital, I. MUJIKA PhD, Department of Research and
Department of Physical Medicine and Rehabilitation, Development, Medical Services, Athletic Club of Bilbao,
Jefferson College School of Medicine and Department of Basque Country, Spain
Bioengineering, Drexel University, Philadelphia PA, USA
B.W. OAKES MD, Associate Professor,
E. FINK PhD, Department of Human Factors, Centre Department of Anatomy and Cell Biology, Faculty
de Recherches du Service de Santé des Armées, BP87, of Medicine, Monash University, Clayton 3168,
La Tronche, 38702, France Melbourne, Australia
vi
list of contributors vii
S. PADILLA MD, PhD, Department of Research M. SCHWELLNUS MD, PhD, Associate

and Development, Medical Services, Athletic Club of Professor, Sports Science Institute of South Africa,
Bilbao, Basque Country, Spain The University of Cape Town, Cape Town, South Africa
C.T. PLASTARAS MD, Rehabilitation J.K. SILVER MD, Assistant Professor, Department
Institute of Chicago, Center for Spine, Sports and of Physical Medicine and Rehabilitation, Spaulding
Occupational Rehabilitation, 1030 N. Clark Street, Rehabilitation Hospital, Harvard Medical School,
Chicago, IL 60610, USA Boston, MA, USA
J.M. PRESS MD, Rehabilitation Institute of C.J. STANDAERT MD, Clinical Assistant
Chicago, Center for Spine, Sports and Occupational Professor, Department of Rehabilitation Medicine,
Rehabilitation, 1030 N. Clark Street, Chicago, IL 60610, University of Washington, Seattle, Washington, USA
USA
R. THOMEÉ PhD, Department of Rehabilitation
M.R. SAFRAN MD, Co-Director Sports Medicine, Medicine, Göteborg University, Göteborg, Sweden
Department of Orthopaedic Surgery, University of
California San Francisco, San Francisco, California C.W.C. TONG MBChB (Hons), Department of
94143, USA Orthopaedics and Traumatology, The Chinese University
of Hong Kong, Prince of Wales Hospital, Hong Kong
M.L. SCHAMBLIN MD, Department of
Orthopaedic Surgery, University of California, Irvine, S.L. WIESNER MD, Chief, Occupational Health
California, USA Department, The Permanente Medical Group, 280 West
MacArthur Boulevard, Oakland, California 94611-5693,
USA
Forewords
The sports medical care of athletes is often authoritative information available relative to a
wrongly assumed to comprise simply the im- broad range of topic areas included under the
mediate treatment of injuries and of systemic rubric of Sports Medicine. The earlier volumes of
medical problems. The considerable time and the the Encyclopaedia series have addressed a wide
extensive effort devoted by medical and allied variety of areas of interest relative to both sports
health personnel, both to the prevention of medicine and the sport sciences. Following the
injuries and to the rehabilitation of athletes from general interest publication of Vol. I, The Olympic
injuries which curtail or prevent training and Book of Sports Medicine, succeeding volumes
competition, are frequently overlooked. were devoted to the more definitive topics of
This new volume in the Encyclopaedia of endurance, strength and power, prevention and
Sports Medicine series addresses all of the treatment of injuries, the child and adolescent
important issues related to the rehabilitation of athlete, sports nutrition, women in sport, and
the injured athlete. Dr Frontera and his team of biomechanics.
expert contributing authors present the cutting The publication of this volume further rein-
edge of knowledge relative to the basic science forces the intense interest that the IOC Medical
and accompanying practical considerations Commission has in the health and welfare of
regarding tissue injury and repair. the athletes of the world. Not only does optimal
This volume provides an excellent comple- rehabilitation assist in returning an injured
ment to the volumes already published. The athlete to training and competition, but a care-
series now includes the preparation of an athlete fully administered programme of rehabilitation
for competition, the prevention of sports injuries, serves to prevent the recurrence of the same
the immediate treatment of injuries, and the injury or the occurrence of additional injuries.
rehabilitation that must occur to bring an athlete A high-quality programme of rehabilitation is of
back to training and competition. importance to all athletes, their coaches, and the
My congratulations go to the editor and authors teams and nations that they represent.
for their excellent work and to the IOC Medical This volume will stand for many years as the
Commission for providing this admirable contri- most comprehensive and authoritative reference
bution to sports medicine literature. on sports injury rehabilitation available both
for clinicians and sports scientists. I extend both
Dr Jacques ROGGE my appreciation and my congratulations to Dr
IOC President Frontera and each of the contributing authors.
The general aim of the Encyclopaedia of Sports Princes Alexandre de MERODE

Medicine series is to present the latest and most Chairman, IOC Medical Commission
viii
Preface
Conceptual framework
must take into account the fact that the objective
Rehabilitation is, by definition, the restoration of of the patient (the athlete) is to return to the same
optimal form (anatomy) and function (physiol- activity and environment in which the injury
ogy). It is a process designed to minimize the loss occurred. Functional capacity after rehabilitation
associated with acute injury or chronic disease, should be the same, if not better, than before in-
to promote recovery, and to maximize functional jury since avoiding the conditions associated with
capacity, fitness and performance. The process the injury is not, in many cases, an alternative.
of rehabilitation should start as early as possible The sequence of events resulting from a sports-
after an injury and form a continuum with other related injury that may lead to a reduction or
therapeutic interventions such as the use of inability to perform in sports can be framed
pharmacological agents. It can also start before using a disability model widely used in the field
or immediately after surgery when an injury of rehabilitation medicine (Fig. 1). In this context,
requires a surgical intervention. The rehabilita- the ultimate goal of the rehabilitation process is
tion of the injured athlete is managed by a multi- to limit the extent of the injury, reduce or reverse
disciplinary team with a physician functioning the impairment and functional loss, and prevent,
as the leader and coordinator of care. The team correct or eliminate altogether the disability.
includes, but is not limited to, athletic trainers, From a clinical perspective it is possible to
physiotherapists, psychologists, and nutrition- divide the rehabilitation process into three
ists. The rehabilitation team works closely with phases. The goals during the initial phase of the
the athlete and the coach to establish the rehab- rehabilitation process include limitation of tissue
ilitation goals, to discuss the progress resulting damage, pain relief, control of the inflammatory
from the various interventions, and to establish response to injury, and protection of the affected
the time frame for the return of the athletes to anatomical area. The pathological events that
training and competition. take place immediately after the injury could
Injuries during sports competitions may result lead to impairments such as muscle atrophy and
from high forces during actions or movements weakness and limitation in the joint range of
inherent to the sport. The rehabilitation plan motion. These impairments result in functional
Pathology (injury) Impairment Functional loss Disability

Strain Contracture Inability to Inability to
Sprain Muscle atrophy run, jump compete
Fracture and weakness in sports
Fig. 1
ix
x preface
losses, for example, inability to jump or lift an and/or cartilage. Section three includes three
object. The extent of the functional loss may be chapters on practical issues of great significance
influenced by the nature and timing of the thera- to the outcome of the rehabilitation process.
peutic and rehabilitative intervention during the The treatment and rehabilitation of injuries in
initial phase of the injury. If functional losses are athletes requires, in many cases, the reduction
severe or become permanent, the athlete now or complete cessation of training. Injuries and
with a disability may be unable to participate in detraining alter basic physiological mechanisms
his/her sport. and the functional capacity of the athlete. These
The goals during the second phase of rehabili- effects must be taken into consideration espe-
tation include the limitation of the impairment cially at the beginning of the second phase of the
and the recovery from the functional losses. A rehabilitation process. It is a common mistake to
number of physical modalities are used to en- consider the physical rehabilitation of the athlete
hance tissue healing. Exercise to regain flexibility, disconnected from the psychological recovery.
strength, endurance, balance, and coordination The last chapter of this section addresses relevant
become the central component of the interven- emotional and psychological aspects of sports
tion. To the extent that these impairments and rehabilitation.
functional losses were minimized by early inter- The last section of the book includes seven
vention, progress in this phase can be accelerated. chapters that discuss the most commonly used
The final phase of rehabilitation represents the interventions in clinical rehabilitation. The use
start of the conditioning process needed to return of pharmacological agents, physical modalities,
to sports training and competition. Understand- and the various types of therapeutic exercise are
ing the demands of the particular sport becomes all discussed in detail. Particular attention is
essential as well as communication with the given to the use of orthotic devices and to func-
coach. This phase also represents an opportunity tional rehabilitation and issues related to the
to identify and correct risk factors, thus reducing return to training and competition.
the possibility of re-injury. The use of orthotic All authors have made a serious attempt to
devices to support musculoskeletal function and summarize the relevant scientific literature. It is
the correction of muscle imbalances and inflexi- our interest to discuss the evidence, if any, that
bility in uninjured areas should receive the atten- supports current rehabilitative strategies.
tion of the rehabilitation team.
Acknowledgements
Structure of this volume
I would like to thank all authors for their time
This volume contains a total of 15 chapters and excellent contributions to this volume. I
divided into four sections. The first section cov- also wish to express special thanks to Professor
ers relevant basic concepts of the epidemiology Howard Knuttgen, Chair of the Sub-commission
and pathology of sports injuries. The implica- on Publications of the IOC Medical Commission
tions of the patterns of sports injury for rehabili- for his guidance. Final thanks to the IOC Medical
tation are discussed and the physiological and Commission and the International Federation
cellular response to tissue injury reviewed in of Sports Medicine for having established this
detail. The second section contains three chap- important Encyclopedia of Sports Medicine.
ters on the basic science of tissue healing and
repair of the five most frequently injured tissues Walter R. Frontera
in sports: muscles, tendons, ligaments, bones, Boston, Massachusetts
PA R T 1
EPIDEMIOLOGY AND
PAT H O L O G Y
Chapter 1
Epidemiology of Sports Injuries:

Implications for Rehabilitation
WALTER R. FRONTERA
in the identification of risk factors for sports

Introduction
injuries (Macera et al. 1989) and modifications in
The study of the relationships among the vari- the competitive rules in various sports. Although
ous factors determining the frequency and dis- research in epidemiology has proved essential for
tribution of diseases and/or injuries in a human the development of preventive and therapeutic
community is known as epidemiology. The basic interventions, the relationship between the epi-
elements of epidemiology have been applied to demiology of sports injuries and the process of
the study of a frequent, albeit unintended, con- rehabilitation of the injured athlete has not received
sequence of the practice of sport; i.e. injuries to similar attention.
the musculoskeletal system. Some authors have proposed a model that
Understanding the incidence and prevalence uses epidemiological information to generate
of injuries based on variables such as type and preventive strategies (Van Mechelen 1993). The
nature of the injury, age group, nature of the sport, sequence of prevention is illustrated in Fig. 1.1.
gender and time since the onset of symptoms, In this model, the identification of the problem
among others, has contributed to the develop- and description using epidemiological outcomes
ment of programmes aimed at the prevention and leads to the study of the mechanisms of injury
treatment of injured athletes (Walter & Hart 1990). and the naming and grouping of risk factors.
Most importantly, these studies have resulted Based on that information, preventive measures
1 Establishing the extent of the injury

problem: incidence and severity
2 Establishing aetiology and

mechanism of sports injuries
3a Introducing a 3b Introducing a
preventive measure rehabilitation programme
Fig. 1.1 The sequence of

prevention and rehabilitation. 4 Assessing the effectiveness by
(Adapted from Van Mechelen repeating step 1
1993.)
3
4 epidemiology and pathology
designed to reduce the risk and/or severity of a reasonable association between the two. Fur-
the injuries are designed and implemented. Fin- ther, most of the observations included in this
ally, the measures are evaluated by repeating chapter are descriptive of a sports injury clinic
the description of the problem (step 1) after the located in a sports training centre and not in
intervention. We suggest that this useful model a hospital or medical centre. The descriptive
could be expanded by including, as part of the nature of these observations limits the extent
intervention strategies, effective rehabilitation pro- to which we can draw conclusions and only
grammes that contribute to symptom resolution, allows us to make preliminary observations and
limit functional losses, and restore physiological speculations. Finally, it is not intended to present
function and performance. an analysis of the incidence of sports injuries
From a clinical point of view, an analysis of with considerations of the population at risk
sports injuries by pattern, type, incidence and or the difference in exposure (hours during
severity, together with an improved under- which an athlete risks injury) (Wallace 1988).
standing of the physiological losses associated These factors appear to be less relevant in clinical
with these injuries, could help us design better rehabilitation.
rehabilitative interventions. Further, this know-
ledge could help us explain the extent to which
Patterns of sports injuries
the lack of effective rehabilitation itself becomes
a risk factor predisposing injured athletes to the It is common to examine the distribution of injuries
recurrence of an existing injury or to new injuries in relation to other variables of interest like
in a different, but related, anatomical area. For age group, type of injury (traumatic vs. overuse),
example, a high incidence of chronic injuries time since onset of symptoms, whether the injury
could indicate that proper rehabilitation did occurred during training or competition, ana-
not follow the treatment of the symptoms in the tomical area, specific diagnosis and severity of
acute inflammatory phase. It should be under- injury. These variables are of significant interest
stood that, for the competitive athlete, resolution when rehabilitation is our main focus. Let us
of the acute symptoms, such as pain, and clinical examine briefly the influence of these factors on
signs, such as swelling, is not the goal of the our rehabilitation strategies.
sports medicine practitioner. Restoration of form,
and more importantly, function after resolution
Type of injury (traumatic vs. overuse)
of the symptoms is necessary for optimal sports
performance. Further, as our understanding of Roughly 45–60% of all injuries treated in a
the physiological losses associated with the most sports medicine clinic can be classified as over-
common sports injuries improves, it will be pos- use injuries. This is particularly true in sports like
sible to anticipate the functional deficits resulting gymnastics (Fig. 1.2) where soft tissues and joints
from those injuries. Thus, the implementation of are subject to unusual positions and stresses.
appropriate rehabilitation programmes will be Risk factors for overuse injuries include muscle
feasible. weakness, muscle strength imbalance and ana-
The purpose of this chapter is to illustrate tomical misalignment (Knapik et al. 1991). An
how data on the pattern of injuries in various examination of these risk factors suggests that
sports populations can help us restore form and properly designed rehabilitation programmes
function after injury. It is not the author’s inten- and the use of rehabilitation devices such as
tion to present an exhaustive and critical review foot orthotics could contribute to a reduction in
of the literature on the epidemiology of sports the incidence and prevalence of overuse sports
injuries but to interpret some existing data in injuries.
the context of the goals of a standard rehabilita- Clearly, the situation may be different when
tion programme. It will suffice to demonstrate the analysis is restricted to clinical encounters
epidemiology of injury 5
Time from onset
Epidemiological studies show that, when the

time from onset of symptoms is considered, most
(70.2% of a total of 1650) injuries treated in an
ambulatory sports medicine clinic are chronic
in nature (Frontera et al. 1994). In other words,
the time between the onset of symptoms and the
evaluation in the clinic is longer than 2 weeks.
There are several potential reasons or scenarios
that could explain this observation. As men-
tioned above, an insidious onset in the absence
of obvious trauma with a slow progression of
the injury could result in a delay in making a
clinic appointment to get the signs and symptoms
evaluated. This is typical of the overuse injuries
that have become so prevalent in sports like
running, swimming and baseball.
Another possibility could be that the symptoms
are not well defined, at least initially, making the
diagnosis by a physician difficult. It is also con-
Fig. 1.2 Repetitive stress associated with high-volume ceivable that the incorrect therapeutic modality
training results in overuse injuries in many athletes in or rehabilitation intervention was chosen to initi-
various sports including gymnastics. M.O. Huilan at
ate treatment or that the patient did not complete
Atlanta, 1996. (© Allsport, Doug Pensinger, 1996.)
the treatment as prescribed by the physician for
other reasons. These two situations could prolong
in an emergency department. Many traumatic the acute stage resulting in the persistence of
injuries (Fig. 1.3) are more acute and severe, symptoms. Moreover, many injuries occur dur-
resulting frequently in immobilization and pro- ing training sessions when health care profes-
longed rehabilitation. sionals may not be available to immediately treat
Fig. 1.3 Falls in cycling can result

in significant traumatic injuries.
the injured athlete. The athlete may delay seek- 100

84.8 86.6
ing help or may initiate treatment him/herself if 80.4
80 75.2
the symptoms are not severe or disabling, and
60
I/UI%
tissue damage may increase in the absence of
acute therapeutic intervention. Finally, it is also 40
possible that the correct treatment was applied 20
resulting in resolution of the symptoms but that
0
proper rehabilitation of impairments and func- Quadriceps Knee Fracture Ankle
tional losses did not follow the therapeutic inter- Type of injury
ventions. In other words, the athlete is allowed
back into training and competition based on the Fig. 1.4 Concentric peak torque of the knee extensors
absence of pain and inflammation but not on of the injured side measured at 30 degrees per second
and expressed as a percentage of the uninjured side
the recovery of strength, flexibility or endurance (I/UI) in subjects with different types of injuries. The
needed for successful performance in sports. injuries occurred an average of 9.7 years before the
In the absence of appropriate rehabilitation, evaluation. (Adapted from Holder-Powell &
acute, subacute or chronic injuries frequently Rutherford 1999.)
result in significant physiological and functional
losses that place the affected anatomical area have significant deficits complete a rehabilitation
(and adjacent tissues and joints) at risk for rein- programme, in this study consisting of isokinetic
jury. Recovery from these losses becomes one of strengthening concentric and eccentric exercises,
the most important goals of the rehabilitation muscle weakness is reversed. Further, the incid-
programme. The extent of these losses is illus- ence of postrehabilitation injuries in the 12 months
trated by a clinical epidemiology study published following return to their sport was zero.
by Holder-Powell and Rutherford in 1999. These
authors evaluated the strength of various muscle
Anatomical distribution of injuries
groups in asymptomatic subjects with history of
a sports injury. The injuries occurred between When the incidence of sports injuries is ana-
0.75 and 42 years before the evaluation (mean = lysed by anatomical region, the most frequently
9.7 ± 11 years). injured areas are the knee (Fig. 1.5), shoulder
The most important observation in that study and ankle (Garrick 1985; DeHaven & Lintner 1986;
was a decrement of concentric, eccentric and static Frontera et al. 1994). Of course the anatomical
strength in the knee extensor muscles of the in-
jured limb many years after the injury (Fig. 1.4).
This was the case even when the muscle group
was distant from the injured area. In other words,
the authors of the study observed weakness of
the knee extensors in patients with injuries such
as fractures of the leg and sprains of the ankle
ligaments. The degree of weakness present in
the hamstrings, on the other hand, was minor
in some cases and non-existent in others, sug-
gesting that the rehabilitation approach must be
muscle specific.
In another study, Croisier et al. (2002) demon-
strated that athletes with strains of the hamstrings Fig. 1.5 An acute knee injury in a judo player,
had significant strength deficits. More import- Girolamo Giovinazzo of Italy at Sydney, 2000.
antly, these investigators showed that if those that (© Allsport, Clive Brunskill, 2000.)
distribution of injuries in a particular sport rehabilitation. Clearly, when the severity is high,
can be very specific. In other words, basketball longer periods of immobilization or rest are
players may suffer more injuries to the knee than needed for tissue healing. As a result, larger
to the shoulder but the situation in swimmers is physiological losses are experienced by the
the reverse. athlete and deconditioning of uninjured areas
Knowledge of the anatomical distribution of is more extensive. Under these conditions, it
injuries in a particular sport is essential to develop should be anticipated that rehabilitation will last
a training programme that maximizes sport- longer.
specific conditioning and minimizes the risk of
injury. Further, because deconditioning associated
Rehabilitation and the
with rest could potentially affect muscle groups
preparticipation exam
proximal and distal to the injured area, know-
ledge of this anatomical distribution of injuries Every competitive athlete must undergo a pre-
by sport could be vital for the rehabilitation of participation medical examination on a regular
the injured athlete. A well-planned rehabilita- basis. The preparticipation exam is an ideal situ-
tion programme should include exercises for the ation in which to: (i) treat existing medical condi-
injured area as well as for those areas at risk of tions early before the competition; (ii) anticipate
injury in the specific sports activity. the health care needs of the athlete; (iii) educate
the athlete and his/her coach regarding health
issues such as vaccinations and prevention of
Most frequent diagnoses
disease and injury; and (iv) discuss topics such as
Most sports injuries are relatively mild and do not doping in sports.
require surgical intervention. Independent of the Another important element of the preparti-
level of competition, the most frequent diagnoses cipation exam is the identification of risk factors
are in descending order: tendonitis (or tendinosis), for medical conditions in general and for sports
first degree strains (muscle tendon unit), first injuries in particular. The process of identifying
degree sprains (ligament and capsular injuries), risk factors can make use of the epidemiologic-
patellofemoral pain and second degree sprains. al evidence published in the sports medicine
The best course of action in these cases is appro- literature. Findings such as joint contractures or
priate conservative intervention to control symp- reduced flexibility, muscle weakness and muscle
toms such as pain and swelling, followed by strength asymmetry represent ideal opportunit-
comprehensive rehabilitation. The indications ies to do ‘preventive rehabilitation’. The restora-
for surgery in these cases are few and rehabilitation of normal form and function in these cases
tion becomes the most effective intervention when does not necessarily follow a sports injury but may
fast return to practice or competition and preven- be important in the prevention of future injuries.
tion of future injuries are the most important goals In addition, rehabilitation may prove to be bene-
(DeHaven & Lintner 1986; Matheson et al. 1989). ficial for sports performance because an enhanced
level of flexibility, cardiovascular endurance and
muscle strength and endurance, alone or in com-
Severity of injury
bination, are required in almost any sport.
The severity of the injury can be judged by the
nature of the diagnosis, the duration and nature
Health services in international
of the treatment, the time lost from sports training
competitions
or competition, and/or the presence and degree
of permanent damage (Van Mechelen 1993). There The study of the pattern of disease and injuries
is usually a positive correlation between sever- in international sports competitions can help the
ity, functional loss and the need for extended team physician make plans regarding, among
MSK logical and functional capacity in later stages.

39.1% In fact, in the above study, typical rehabilitation
interventions such as physical therapy modalities
(cold packs, hot packs, ultrasound, transcutane-
ous electrical stimulation, massage, therapeutic
exercises) were needed in 23.1–36.9% of the total
number of cases.
Resp.
17.2% It is important to note that, just like in the case
of the sports injury clinic discussed above, the
onset of symptoms preceded the competition in
many cases. Thus many injuries could be classified
as chronic in nature. High-performance athletes
GI Other
often continue to train and compete even in the
12.2% 25.7% presence of symptoms and signs of injury, and
Skin may delay proper treatment and rehabilitation of
5.8% an injury to participate in important competitions.
Thus, it is reasonable to speculate that some of
Fig. 1.6 Distribution of diagnoses (n = 2468) in a health
clinic during international sports competitions by the injured athletes did not receive appropriate
system. GI, gastrointestinal; MSK, musculoskeletal. rehabilitation after the initial insult. These two
(Adapted from Frontera et al. 1997.) observations make the inclusion of rehabilitation
services in precompetition assessment and plans
other things, the composition of the health care for a sports delegation an absolute necessity.
team travelling with sports delegations, the equip-
ment and medical supplies necessary to deliver
Conclusion
health care (including rehabilitation services) in
an Olympic village, the most commonly used and The study of the epidemiology of sports injuries
permitted medications, and the therapy modalities can be as valuable to rehabilitation as it is to pre-
needed for rehabilitation (Frontera et al. 1997). vention. Many injuries may occur because the
As the number of athletes and competitions rehabilitation of a previous injury was not com-
increase and new transportation methods facilit- plete. Understanding risk factors associated with
ate travel, health professionals will be challenged sports injuries can help in the design of rehabil-
to respond to the needs of the travelling athlete itation strategies resulting in a lower incidence
exposed to different environmental conditions, and severity of injuries. Rehabilitation principles
pathogens and demanding training regimes. can be applied in a sports injury clinic but also as
Although disorders of the respiratory and part of the health care services for a travelling
gastrointestinal tracts are very common among team. The following chapters will discuss the
travelling athletes, the main cause of morbidity scientific basis of current rehabilitation practices.
during an international competition is injuries to Every sports medicine practitioner should be
the musculoskeletal system (Fig. 1.6). familiar with these principles and apply them in
The five most common injuries or disorders their work with athletes.
affecting the musculoskeletal system (total num-
ber of diagnoses = 966) include: first degree References
strains (23.1%), tendinitis/tendinosis (18.7%), con-
Croisier, J.-L., Forthomme, B., Namurois, M.-H.,
tusion (12.7%), myositis (10.9%) and first degree
Vanderhommen, M. & Crielaard, J.-M. (2002)
sprains (10%). All of these diagnoses could bene- Hamstring muscle strain recurrence and strength
fit from rehabilitative interventions to control the performance disorders. American Journal of Sports
symptoms in the acute stage and to restore physio- Medicine 30, 199–203.
DeHaven, K.E. & Lintner, D.M. (1986) Athletic injuries: collegiate athletes. American Journal of Sports Medicine
comparison by age, sport, and gender. American 19, 76–81.
Journal of Sports Medicine 14, 218–224. Macera, C.A., Pate, R.R., Powell, K.E., Jackson, K.L.,
Frontera, W.R., Micheo, W.F., Aguirre, G., Rivera- Kendrick, J.S. & Craven, T.E. (1989) Predicting
Brown, A. & Pabon, A. (1997) Patterns of disease and lower-extremity injuries among habitual runners.
utilization of health services during international Archives of Internal Medicine 149, 2565–2568.
sports competitions. Archivos de Medicina del Deporte Matheson, G.O., Macintyre, J.G., Taunton, J.E.,
14, 479–484. Clement, D.B. & Lloyd-Smith, R. (1989) Musculo-
Frontera, W.R., Micheo, W.F., Amy, E. et al. (1994) skeletal injuries associated with physical activity in
Patterns of injuries in athletes evaluated in an inter- older adults. Medicine and Science in Sports and Exercise
disciplinary clinic. Puerto Rico Health Sciences Journal 21, 379–385.
13, 165–170. Van Mechelen, W. (1993) Incidence and severity of sports
Garrick, J.G. (1985) Characterization of the patient injuries. In: Sports Injuries: Basic Principles of Preven-
population in a sports medicine facility. Physician and tion and Care (Renström, P.A.F.H., ed.). Blackwell
Sportsmedicine 13, 73–76. Scientific Publications, Oxford: 3–15.
Holder-Powell, H.M. & Rutherford, O. (1999) Unilateral Wallace, R.B. (1988) Application of epidemiologic prin-
lower limb injury: its long-term effects on quad- ciples to sports injury research. American Journal of
riceps, hamstring, and plantarflexor muscle strength. Sports Medicine 16 (Suppl. 1), 22–24.
Archives of Physical Medicine and Rehabilitation 80, Walter, S.D. & Hart, L.E. (1990) Application of epi-
717–720. demiological methodology to sports and exercise
Knapik, J.J., Bauman, C.L., Jones, B.H., Harris, J.M. & science research. In: Exercise and Sports Sciences Reviews
Vaughan, L. (1991) Preseason strength and flexibility (Pandolf, K.B. & Holloszy, J.O., eds). Williams &
imbalances associated with athletic injuries in female Wilkins, New York: 417–448.
Chapter 2
Pathophysiology of Injury
MARK L. SCHAMBLIN AND MARC R. SAFRAN
Although in the recent past, understanding of

Introduction
the mediators of inflammation has vastly im-
No matter what the age of an athlete, the level of proved, many factors responsible for induction,
competition or the sport, inflammation is likely to regulation and resolution remain indefinable.
affect an individual at some point in their endeav- This lack of understanding remains an elusive
ours. Whether an injury is one of chronicity, cornerstone in treatment for both the physician
related to repetitive movements, or one of acute and the athlete. The purpose of this chapter is to
onset, related to trauma, the detrimental effects on provide an understanding of our current know-
athletic performance are well documented. Too ledge of the complex nature of the pathophysi-
frequently the complexity of the inflammatory ological mechanisms, which function to mediate
process is not fully understood and inflammation a host’s response to tissue injury. This knowledge
is treated as an unwanted hindrance to athletic is then utilized in later chapters to understand
performance, however, it is truly a complex net- specific tissue responses to injury as related to
work of vascular and cellular responses designed the athlete.
to facilitate the repair of traumatized tissue (Bryant
1977; Gamble 1988; Martinez-Hernandez 1988).
Cytokines
The development of an inflammatory reaction
to an injury is complex, utilizing many of the Inflammation may be seen in a variety of circum-
body’s systems to mediate its purpose. The goal stances that affect the human body. It may occur
of any inflammatory reaction is to resolve the as a defensive response to foreign material or as
pathological insult and restore the anatomy to a response to mechanical trauma, toxins or in
a level of physiological function identical or the face of abnormalities such as neoplasia. The
nearly identical to preinjury status. Ideally this accumulation and activation of leucocytes seems
can be accomplished by removing diseased or to play an essential role in nearly all forms of
damaged tissue with the subsequent regenera- inflammation. Following the influx of leucocytes
tion of normal anatomical tissue. However, this in the acute phase of inflammation, its pro-
is often not the case. Too frequently the insult is pagation and amplification is mediated by both
far too great or perpetrated over too long a period, humoral and cellular components of the immune
resulting in increased tissue destruction. This system.
often leads to scar tissue formation that in turn Cytokines are cellular proteins that are the
may propagate a continued inflammatory reac- mediators of physiological activity, including
tion. A persistent inflammatory action, therefore, the inflammatory process. There are proinflam-
may be harmful to an individual’s athletic per- matory and anti-inflammatory cytokines, which
formance, as well as to the individual. modulate their effect by binding to receptors
10
pathophysiology of injury 11
on target cells. Through this interaction the up-

regulation or down-regulation of cellular activity
may be propagated. In the acute phase response
of inflammation, cytokines appear to be respons-
ible for a myriad of physiological modifications
occurring both locally at the site of the patho- (a) (b)
logy and also at regions distant from the insult
(Rosenberg & Gallin 1993).
The functions of cytokines are varied. A given
cytokine may initiate and regulate cellular activ-
ities in numerous cells simultaneously. At the
same time, more than one cytokine may induce
a particular biological activity (Table 2.1). Inter- (c)
leukin 1 (IL-1), a common cytokine seen in Fig. 2.1 Cytokines mediate their effects via three
inflammation, acts on virtually all leucocytes, mechanisms of action. (a) Autocrine: the release of
endothelial cells, monocytes and hepatocytes to cytokines by a cell allows binding to receptors on the
up-regulate the expression of adhesion mole- cell of origin. (b) Paracrine: most cytokines have a
small radius of activity and mediate their effects on
cules, cytokines and arachidonic acid meta-
adjacent cells. (c) Some cytokines (IL-1 and TNF)
bolites (Rosenberg & Gallin 1993). It results in mediate their activity via endocrine mechanisms.
neutrophil accumulation, fibroblast prolifera-
tion, angiogenesis, acute phase protein syn-
thesis and metabolic alterations such as fever. The regulation of cytokine function is of
Similar activity is seen in other proinflamma- critical importance. Secondary to a cytokine’s
tory cytokines, such as tumor necrosis factor powerful ability to modify biological behaviour,
alpha (TNF-α), IL-6, IL-4, IL-10 and transform- the body has evolved numerous cellular and
ing growth factor beta (TGF-β). An excellent molecular mechanisms to control their activity.
example of this biological redundancy can be The predominant mechanism of regulation occurs
seen with IL-1 and TNF-α. Both of these cyto- at the level of gene transcription. Cytokines
kines result in the up-regulation of adhesion are not stored, but rather created de novo fol-
molecules, accumulation of leucocytes, protein lowing cellular activation. Antigen stimulation
synthesis and angiogenesis (Rosenberg & Gallin leads to increased transcription within 30 min.
1993; Bemelmans et al. 1996). A steady-state level is seen in anywhere from 4
Local cytokines react with their receptors in to 8 h (McDonald et al. 1993; Jain et al. 1995;
an autocrine, paracrine and endocrine fashion Serhan 1997). With the cessation of the stimulus,
(Fig. 2.1). The autocrine pathway allows for the return to the baseline will usually occur in 24 h.
amplification of the cytokine-induced inflam- A second form of regulation is the conversion of
matory process. The paracrine pathway allows an inactive form of the cytokine to the active
cytokines to influence cells in the local environ- form. This mechanism is seen in the conversion
ment, leading to the accumulation of inflammat- of a procytokine within the cytosol to the cyto-
ory cells. The induction of acute phase protein kine IL-1β, as well as the formation of TNF-α,
synthesis in the hepatocytes is an example of an which is formed in its active state but limited to
endocrine mechanism of peripherally circulat- the cell membrane. Cleavage of the membrane-
ing cytokines (Akira et al. 1993; Dinarello 1996). bound TNF-α by converting enzymes facilitates
By utilizing these three mechanisms of action, secretion.
the cytokine is able to alter the local tissue as The ability to down-regulate the inflammatory
well as the acute phase response in the face of process is as important as the ability to initiate
inflammation. it. Chronic inflammation or failure to control an
Table 2.1 The actions of selected cytokines including source, targets and activities.
Cytokine Cell source Cell target Biological activity
IL-1α Monocytes All cells Up-regulation of adhesion molecule expression

IL-1β Macrophages Macrophage emigrations
Acute phase protein synthesis
IL-2 T-cells T-cells T-cell activation and proliferation
B-cells Enhanced monocyte and macrophage cytolytic activity
Monocytes
Macrophages
IL-3 T-cells Monocytes Stimulation of haematopoietic progenitors
Mast cells Macrophages
NK cells Mast cells
Eosinophils
IL-4 T-cells T-cells Stimulates T-cell and B-cell differentiation
Mast cells B-cells Anti-inflammatory action on T-cells, B-cells and monocytes
Basophils Monocytes
Macrophages
Neutrophils
Eosinophils
IL-5 T-cells Eosinophils Regulates eosinophil migration and activation
Mast cells Basophils
Eosinophil
IL-6 Monocytes T-cells Induction of acute phase proteins
Macrophages B-cells T-cell and B-cell differentiation
B-cells Epithelial cells
IL-8 Monocytes Neutrophils Induces neutrophil, monocyte and T-cell migration
Macrophages T-cells Neutrophil adherence
T-cells Monocytes Angiogenesis
Neutrophils Macrophages Histamine release
IL-10 Monocytes Monocytes Inhibits macrophage proinflammatory cytokine production
Macrophages Macrophages Inhibits differentiation of T-cells
T-cells B-cells Inhibits NK cells
B-cells T-cells
Mast cells
TNF-α Monocytes All cells Fever, anorexia and proinflammatory cytokine production
Macrophages Enhanced capillary permeability
Mast cells Acute phase protein synthesis
Basophils
NK cells
B-cells
T-cells
TNF-β T-cells All cells Cell cytotoxicity
B-cells
TGF-β Most cell types Most cell types Down-regulates T-cell and macrophage responses
Stimulates angiogenesis
IFN-α All cells All cells Stimulates T-cell, macrophage and NK cell activity
Direct antitumour effects
Antiviral activity
IFN-γ T-cells All cells Regulates macrophage and NK cell activation
NK cells T-cell differentiation
Immunoglobulin production by B-cells
IFN, interferon; IL, interleukin; NK, natural killer; TGF, transforming growth factor; TNF, tumour necrosis factor.
inflammatory process may lead to host tissue E2 via the enzyme cyclooxygenase (Goldblatt
damage. There are several mechanisms utilized 1933; Von Euler 1935; van der Pouw et al. 1995).
in the down-regulation of inflammation. These From this finding it was thought that essential
include production of activated complement fatty acids served merely as a precursor to pro-
inhibitors, apoptosis of inflammatory cells and staglandin synthesis. This has subsequently been
production of anti-inflammatory cytokines such shown to be only one of the many functions of
as IL-4, IL-10, IL-13 and TGF-β (Feng et al. 1996). fatty acids, albeit an important one.
IL-4 and IL-10, perhaps the best known of the There are many ways of inducing prosta-
anti-inflammatory cytokines, appear to mediate glandin synthesis that appear to be cell specific.
an anti-inflammatory effect on the T-cell pre- In macrophages, prostaglandin E2 (PGE2) and
dominantly, but also B-lymphocytes, mast cells, thromboxane A2 (TxA2) are stimulated by the pre-
basophils and endothelial cells, as well as a sence of antigen–antibody complexes (Poranova
variety of others (Feng et al. 1996). et al. 1996). Cytokine receptors on mast cells
Cytokines are potent proteins in the initiation, stimulate the synthesis and secretion of PGD2
propagation and regulation of the inflammatory (Murakami et al. 1994). IL-1 and TNF-α stimula-
process. In this regard they are not alone, as the tion of endothelial cells and fibroblasts leads to
body synthesizes various types of proteins to PGE2 as well as PGI2 production. The production
mediate these same functions. Among these are of prostaglandins is accomplished by the break-
prostaglandins and leukotrienes, which will be down of membrane phospholipids by phos-
discussed in the subsequent sections. pholipase A2 with the subsequent formation of
arachidonic acid. Arachidonic acid is then con-
verted to PGG2 via cyclooxygenase 1 and 2. PGG2
Prostaglandins
then may be converted into various prostaglandins
Along with cytokines, prostaglandins are amongst by prostaglandin synthase (Fig. 2.2).
the best-defined mediators of the inflammatory Investigations of the role of prostaglandins
response. Since their discovery in 1931, advances within the inflammatory cascade are extensive.
in their structure, function and physiological In general, their function has been delineated
mechanisms have afforded an increased under- by their injection into both animal and human
standing of these molecules (Kurzok & Lieb 1931). subjects with subsequent monitoring of their
Independent work by two groups demonstrated effects. Another area of focus is the role of non-
arachidonic acid conversion to prostaglandin steroidal, anti-inflammatories in the regulation
Membrane phospholipids
Phospholipase A2
Arachidonic acid
Cyclooxygenase 1 and 2
Prostaglandin G2
Cyclooxygenase 1 and 2
Prostaglandin H2
Fig. 2.2 The synthesis of
prostaglandins and thromboxane Prostaglandin synthases
A2 from the membrane
phospholipids, utilizing
phospholipase A2,
cyclooxygenase and Prostaglandin Prostaglandin Prostaglandin Prostaglandin Thromboxane
prostaglandin synthase. D2 G2 F2 I2 A2
of cyclooxygenase function. Throughout these oedema. In states of inflammation, however, an

studies, one thing has remained clear, the bio- increase in oedema is seen by the ability of pro-
logical responses instigated by the presence of staglandins to dilate the vasculature leading
prostaglandins are wide ranging and varied in to increased blood supply to traumatized areas
nature. In an attempt to simplify their function, (Moncada et al. 1973; Wheeldon & Vardey 1993).
their actions may be broken down into four In the presence of inflammation, increased vas-
general areas of the inflammatory process: fever, cular permeability is present secondary to the
pain, oedema and leucocyte regulation. action of many proinflammatory mediators; this
Fever appears to be a complex neuroendocrine increased permeability coupled with increased
response to both infection and inflammation. blood flow stimulates excessive oedema. Experi-
A variety of proinflammatory mediators appear mental models also support this finding, as
to serve as a stimulant to fever production. Vari- the injection of prostaglandins, specifically PGE2
ous cytokines, which will be discussed in later and PGI2, coupled with bradykinin or platelet-
sections, assist in the stimulation of the ther- aggregating factor (PAF) (powerful stimulants
moregulatory centre by stimulating both the syn- to increased permeability) stimulate oedematous
thesis of the PGE family as well as mediating states (Von Euler 1934).
a direct effect on the thermoregulatory centre In an apparent contradiction, the systemic
itself. Increased levels of PGE2 have been demon- administration of prostaglandins appears to medi-
strated in the cerebral spinal fluid of febrile ate an anti-inflammatory effect (Kunkel et al. 1979;
animals. This PGE2 is most probably synthesized Fantone et al. 1980). Circulating prostaglandins
within the central nervous system as a result of (PGE2 and PGD2) inhibit neutrophils, monocytes
bacterial-induced cytokine release. PGE2 appears and circulating T-lymphocytes. The inhibition
to modulate its effect on thermoregulatory centres of neutrophils is accomplished by inhibition of
within the hypothalamus; however, the specific activation as measured by chemotaxis and super-
receptor of action remains elusive (Feldberg & oxide production (Wedmore & Williams 1981).
Saxena 1971; Milton & Wendlandt 1971). Cyclo- The inhibition of monocytes is mediated via the
oxygenase inhibitors, specifically cyclooxygenase decreased production of various proinflamma-
2 inhibitors, given to human subjects modulate tory mediators such as TNF-α (Kunkel et al. 1986).
an antipyretic effect, lending further support to T-lymphocyte inhibition is seen as a decrease in
the role of prostaglandins in the induction of a T-cell proliferation, a decrease in released cyto-
febrile state. kines and a decrease in the number of migrating
In experimental models, the injection of pro- T-cells (Goodwin et al. 1977; Shaw et al. 1988; Betz
staglandins in itself does not induce a painful & Fox 1991; Trinchieri 1995). Through these three
response. However, in the presence of pro- mechanisms, systemic prostaglandins appear to
staglandins, particularly PGE2 and PGI2, the inhibit the inflammatory reaction, whereas, as
response to painful stimuli is greatly increased discussed previously, the local accumulation
(Ferreira et al. 1978). It is unclear which of these of prostaglandins accentuates the inflammatory
two prostaglandins serves to accentuate the response.
painful stimuli to the greatest extent or if differ- As one can see, in recent years, the role of
ent individuals respond to different stimuli in prostaglandins has been greatly elucidated and
altered manners. In some experimental studies, their involvement in the inflammatory reaction
PGE2 appears to predominate while in others has been well documented. Secondary to their
PGI2 appears to be the prime mediator of an complex nature, however, it is highly probable
increase in the nociceptive response (Mnich et al. that their involvement is even more signific-
1995; Plemons et al. 1996). ant than is currently known. Recent advances
Similar to the response seen in pain, the injec- in understanding the nature of these molecules
tion of prostaglandins alone does not stimulate have led to improved pharmacological agents,
such as specific cyclooxygenase inhibitors in anti-

inflammatory medications. Despite the success of
these agents, one thing is clearaprostaglandins
are merely a fraction of the known types of pro-
inflammatory mediators that affect the human
body in the face of pathology.
In addition to mediators such as cytokines
and prostaglandins, the body’s immune system
is composed of a highly complex series of cellular
and plasma-derived components. The cellular
component consists of a variety of cell types,
each with a specific function. These cells interact
in a well-orchestrated manner to improve the
Fig. 2.3 Electron micrograph of a macrophage.
efficiency of the immune response. The cell types
are variable and functions range from stimulat-
ing the aggregation of leucocytes to presenting
Macrophages
foreign material to the actual destruction and
removal of the offending pathogen. Some of Macrophages are present throughout a variety of
the more important cellular components of the host tissues (Fig. 2.3). These cells are able to react
inflammatory process will be outlined in the to abnormalities such as ischaemia or metabolic
following pages. disturbance by initiating an inflammatory reac-
tion. When local processes are insufficient and
unable to remove the host tissue of the initiat-
Mast cells and basophils
ing stimuli, macrophages along with other cells
Several components of the immune system play can mobilize other forms of leucocytes (poly-
a critical role in inflammatory reactions. Tissue morphonuclear neutophils in particular) by the
mast cells and circulating basophils are haemato- activation of local endothelium and by the pro-
poietically derived cells, which express a variety duction of a variety of chemokines, cytokines
of surface receptors that allow them to migrate and other lipid mediators of the inflammatory
to specific tissue locations, interact with cells reaction (Table 2.2) (Bacon & Schall 1996). If the
and tissues, and respond to activation molecules. pathology continues and becomes one of chron-
Both types of cells contain granules, which serve icity, macrophages are able to up-regulate their
as storage for histamine, serotonin, cytokines microbicidal activity (Bell et al. 1994). When con-
and proteases. When IgE-sensitized mast cells sidering the role of macrophages in the initiation,
or basophils are stimulated by either antigens propagation and resolution of inflammation, it
or C3a and C5a (complement anaphylatoxins), is important to remember that each macrophage
the granules are released resulting in the secre- contains variable receptors on its membrane,
tion of these mediators. These in turn induce a allowing it to regulate the biosynthesis and secre-
reversible cell contraction in the endothelium, tion of substances in response to stimuli from the
leading to the formation of gap junctions (Black host tissue (Peterson et al. 1987).
et al. 1972; Arrang et al. 1983). This increases As noted previously, macrophages interact with
the permeability of the vasculature leading to a variety of cells within the human body. These
increased tissue oedema. Both mast cells as well interactions are complex and reciprocal in nature.
as basophils may be induced to release histamine Non-haemopoietic cells, such as endothelium, are
and serotonin by other means, including phys- dramatically affected by the secretory products
ical stimuli such as trauma or proteins secreted of the macrophage, and in turn have a profound
by activated platelets and neutrophils. effect on the ever-adapting macrophage itself.
Table 2.2 Macrophage-derived secretory products.
Cytokines
IL-1 Multiple local and systemic host defence functions
TNF-α Multiple local and systemic host defence functions
IFN-α/β Antiviral, immune modulation
IL-6 Acute phase response
IL-10 Inhibits proinflammatory cytokines
TGF-β Inhibits activation of macrophages and other cells
Complement proteins
Most components Local opsonization and complement activation
Coagulation factors Initiation and regulation of clot formation
Adhesion and matrix molecules Localization and migration
Modulates cellular interactions and phagocytosis
Bioactive lipids
Cyclooxygenase, lipoxygenase Mediators of inflammation
Platelet-activating factor
Antimicrobic activity
Superoxide anion Killing and stasis of microbial targets
Hydrogen peroxide
Nitric oxide
In this way, one can see how the macrophage is Cowland 1997). The azurophil granules con-
an important component in the regulation of the tain myeloperoxidase (an antibacterial enzyme),
inflammatory process. lysozyme and lysosomal enzyme, as well as a
variety of other agents (Table 2.3) (Klebanoff &
Clark 1978). Specific granules by definition do not
Neutrophils
contain peroxidase (Cramer & Breton-Gorius 1987;
These cells maintain the ability to mobilize from Livesey et al. 1989; Mutasa 1989; Path et al. 1996).
the blood to the tissue with subsequent degranula- These granules contain numerous agents includ-
tion in a matter of seconds. Their major function ing lysozyme and lactoferrin (Bretz & Baggiolini
in the inflammatory cascade is one of endocytosis 1974). Gelatinase granules are subsets of specific
(eating) or exocytosis (secreting) (Bainton 1980). granules, and are therefore peroxidase negative
In the normal adult human, a polymorphonuclear (Borregaard & Cowland 1997). They are named
neutrophil is found in one of three environments: for their high content of gelatinase found in their
bone marrow, blood or tissues. The bone marrow granules (Borregaard et al. 1993; Kjelsen et al. 1993;
is the site where proliferation and maturation Borregaard & Cowland 1997). Secretory vesicles
occurs. Following the phase of proliferation and are a group of vesicles that are easily mobilized to
maturation, the neutrophils are released into the the surface; they are remarkable for the presence
blood where they circulate for approximately 10 of alkaline phosphatase within the membrane as
days. They then migrate into the tissues where well as the presence of albumin (Borregarrd et al.
they survive for approximately another 1–2 days. 1990; Borregaard 1996).
Their ultimate fate after this is unknown (Bainton The degranulation of neutrophils is mediated
1980). by the presence of an injury. The azurophil and
Four distinct populations of granules have been secretory granules can be released independ-
identified within neutrophils by cytochemical ently (Williams & Morley 1973; Wright et al.
and cell-fractionation procedures (Borregaard & 1977; Presentey 1984). However, depending on
Table 2.3 Contents of neutrophil granules and vesicles.
Azurophil granule Specific granule Gelatinase granule Secretory vesicle
Cd63 Cd66 Cd11b Alkaline phosphatase

Cd68 Cd67 Cytochrome b558 Cytochrome b558
β-glycerophosphatase Cytochrome b558 Diacylglycerol-deacylating enzyme Cd11b
Acid mucopolysaccharide Fibronectin-R Plasminogen activator-R Cd14
α1-antitrypsin G-protein subunit Acetyltransferase Cd16
α-mannosidase Laminin-R β2-microglobulin Plasminogen activator-R
Heparin-binding protein Thrombospondin-R Gelatinase Albumin
Bactericidal permeability Plasminogen Lysozyme Tetranectin
increasing protein activator-R
β-glycerophosphatase Collagenase
β-glucuronidase Gelatinase
Cathepsins Histaminase
Defensins Heparanase
Elastase Lactoferrin
Lysozyme Lysozyme
Myeloperoxidase Sialidase
Proteinase-3 β-microglobulin
Sialidase TNF-R
TNF, tumour necrosis factor.
the stimuli, concomitant release is required to granules and autophagia. Patients with this dis-
accentuate the bactericidal effects. There appears ease suffer severe life-threatening infections. In
to be a hierarchy in ability to mobilize granules Chediak–Higashi syndrome, a rare autosomal
(Borregaard et al. 1993). The hierarchy for recessive disease, there is a presence of abnorm-
mobilization for excretory function appears to be ally large inclusions within the neutrophil, which
secretory vesicles, gelatinase granules, specific appear to be abnormal azurophilic granules
granules and finally azurophilic granules being (Davis & Douglas 1971; Ohashi et al. 1992). These
the least likely to be mobilized (Borregaard 1996). patients demonstrate an increased susceptibility
When activated, the specific granules, gelatinase to infection.
granules and the secretory vesicles bind to the
plasma membrane via cytochrome b558 subunits.
Eosinophils
Their contents are readily released; however they
lack the ability to generate reactive oxygen mole- Eosinophils are a type of leucocyte identifi-
cules without the contents of the azurophilic able by its bilobed nuclei and large eosinophilic
granules, specifically myeloperoxidase (Klebanoff granules. The large granules in the eosinophil
& Clark 1978; Pryzwansky et al. 1979). contain peroxidase; however, this peroxidase is
The clinical importance of proper neutrophil chemically different than the peroxidase found in
function can be seen in a variety of hereditary neutrophils (Bujak & Root 1974). Eosinophil per-
disease states such as acute myelogenous leuk- oxidase appears to have no role in the bactericidal
aemia, congenital dysgranulopoietic neutropenia activity of eosinophils. The granules also contain
or Chediak–Higashi syndrome (Bainton 1975; a variety of proteins including major basic pro-
Bainton et al. 1977). In congenital dysgranulo- tein (MBP), an eosinophil cationic protein, which
poietic neutropenia there is a defective syn- does appear to be cytotoxic to either parasites or
thesis and degradation of azurophilic granules, mammalian cells. MBP is also responsible for the
an absence or marked deficiency of specific induction of histamine release by basophils and
mast cells (Peretz et al. 1994). There are four physiological reactions associated with platelet
known inherited abnormalities of eosinophils. function.
An absence of eosinophil peroxidase, an auto- Haemostasis is the culmination of three inter-
somal recessive trait, usually results in no clinic- active systems including vascular endothelium,
ally detectable symptoms (Wright & Gallin 1979; blood platelets and plasma proteins of both the
Pouliot et al. 1997). Chediak–Higashi syndrome intrinsic and extrinsic coagulation pathways. This
manifests with large abnormal granules, seen process serves to arrest the loss of blood from
in the eosinophil as well (Davis & Douglas 1971). vessels that have been mechanically traumatized,
A third type of abnormality was found in an for example in muscular sprains, strains and
individual family. It appears to be inherited in an fractures. When discontinuity of a vessel occurs, a
autosomal recessive fashion. Their eosinophils series of responses termed primary haemostasis
demonstrated large grey inclusion bodies; how- ensues. Following trauma, the vessel wall quickly
ever, they manifested without any clinical abnor- retracts and platelets immediately adhere to the
mality (Tisdale 1997). The fourth abnormality is subendothelial collagen. Adherence to the vessel
an absence of specific granules seen in both neu- wall prompts platelet activation, which leads
trophils as well as eosinophils, presenting with to propagation of the thrombus. This is con-
repeated infections (Roos et al. 1996). tinued until occlusion of the traumatized vessel
occurs. The initial adherence is mediated by von
Willebrand factor found in the plasma as well as
Platelets
von Willebrand factor released from activated
Platelets, with their lack of a nucleus, may appear platelet and endothelial cells. Following adhesion
to be simple in nature but they serve a pivotal and activation (i.e. granule release), P-selectin, a
role in the regulation of haemostasis, thrombosis platelet granule membrane glycoprotein, trans-
and inflammation. Platelet formation is accom- locates to the cellular surface (Berman et al. 1986;
plished by the fragmentation of megakaryocyte McEver 1991; Frenette & Wagner 1997). This
cytoplasm. In the circulatory system, platelets glycoprotein mediates the adhesion of leucocytes
appear to be passive, smooth discs. However, they such as monocytes and neutrophils. Activation
maintain the ability to recognize a site of injury, of the platelet eicosanoid pathway occurs, lead-
adhere to this site and serve in the activation and ing to the formation of arachidonic acid (Serhan
propagation of thrombus, as well as mediate the et al. 1996; Sarraf et al. 1997). Arachidonic acid
inflammatory pathway. Their lifespan is from 7 is released where it is immediately converted to
to 10 days and in a healthy individual their count PGH2. This is then converted to TxA2, a potent
can range from 150 000 to 440 000/μl. Platelets vasoconstrictor (O’Rourke et al. 1997). The activ-
contain a circumferential band of microtubules, ated platelet undergoes a change in shape with
which serve to maintain the discoid shape, as well the formation of spicules. This change allows
as an abundance of both actin and myosin within more effective binding between platelets as well
the platelet. These microtubules are responsible as increased binding to factor X and activation of
for the change in shape and spicule formation factor VII of the extrinsic coagulation cascade.
seen in platelets following activation. The platelet not only serves an important role
Platelets are noted to have granules containing in the regulation of the coagulation cascade,
histamine, serotonin and TxA2, amongst other but serves as an important source of vasoactive
proteins. It is unclear whether these mediators mediators as well. Following vascular injury, act-
are developed within the megakaryocyte and ivation of the coagulation cascade or exposure to
are transferred to the platelet via the frag- the basement membrane stimulates platelets to
mentation process or whether they are absorbed release a variety of factors. These factors include
from the plasma. Regardless, these factors, when serotonin, TxA2 and histamine. Serotonin and his-
released, serve to instigate and propagate many tamine are generally released from cytoplasmic
granules and serve as an immediate stimulant strate an overly aggressive nature to MHC mole-
to increase vascular permeability. Thromboxane cules are removed via a process termed negative
A2, an arachidonic acid derivative formed by the selection, leaving only the physiologically react-
breakdown of membrane phospholipids, serves ive T-cell progeny to survive in the post-thymic
as a stimulant to secondary clot formation as well environment. In contrast to the cortical location
as the aforementioned function of smooth muscle of positive selection, it is unclear where the pro-
vasoconstriction. Interestingly, the absence of cess of negative selection occurs. There is evid-
platelets appears to induce an increased state ence that supports both a cortical and medullary
of vascular permeability. The mechanism of this localization of these events (Snijdewint 1993;
is unclear, but in patients who are thrombocy- Neiman 1997). T-cell importance in the acute
topenic, spontaneous cutaneous as well mucosal inflammatory phase has not been well docu-
bleeds are frequent. mented although its absence has been shown to
decrease the strength of healing collagen, while
prolonged activation has been implicated in the
T-lymphocytes
formation of excessive scar tissue.
T-cells are vitally important in the normal func-
tioning of the human immune system. In the
B-lymphocytes
human body, T-cells develop in the thymus.
Utilizing the CD4 and CD8 receptor molecules B-cell lymphocytes are derived from the bone
expressed on the surface of T-cells, they can be marrow in humans. They are a key element in
divided into four subsets (Sprent & Webb 1987; immune responses to foreign antigens. There are
Fink & Bevan 1995). These include CD4+/CD8+, two types of B-cell immune responses to anti-
CD4+/CD8−, CD4−/CD8+ and CD4−/CD8−. Both gens: T-cell independent- and T-cell-dependent
CD4- and CD8-negative T-cells make up about responses. T-cell-independent responses are
2% of the total thymocytes. Their function remains accomplished by the binding of an antigen, lead-
unknown; however, they do seem to serve as ing to cross-linking of the B-cell receptors. This
precursors to the remaining subsets. T-cells are stimulates proliferation and differentiation of B-
uniqueathey must display maximal reactivity cells into antibody-secreting plasma cells (Nossal
to an infinite number of antigens but remain 1994; Doody et al. 1996). The majority of immune
complacent in the face of self-antigens. In order responses to antigens, however, are T-cell depend-
to facilitate this, intrathymic precursors undergo ent. In this process, the B-cells present antigens to
a complex process of both positive and negative T-cells in order to beseech their assistance. After
selection based on their reactivity to self-peptides being presented an antigen, the B-cell will either
bound to major histocompatibility complex pinocytose or endocytose it via receptors on the
(MHC) molecules. cellular membrane. In the B-cell, the antigen is
Positive selection occurs in the cortical region processed and broken down into peptides, which
of the thymus. Since MHC complexes are highly are then presented by the cell’s MHC molecules
polymorphic, each individual must create a to antigen-specific T-cells. Following recognition
population of T-cells that are capable of recogniz- of the peptide–MHC complex by the T-cell, a
ing these molecules and reacting to them if they complex interaction occurs between the T-cell and
are bound to an antigen (Sprent & Webb 1995). B-cell. This interaction requires cell-to-cell con-
The double positive cells are exposed to self– tact and involves multiple receptors and ligands
MHC complexes and those precursors to circu- on both cells (Oliver & Essner 1975; Mitchell et al.
lating T-cells that display the ability to recognize 1995). Signals within this interaction are critical
these complexes are retained. The cells that are in the development of further immune responses,
unable to recognize these cells are allowed to die such as immunoglobulin isotype class switching
in situ (Strang et al. 1988). The cells that demon- and the generation of memory B-cells.
In the athlete, the amount of B-lymphocytes as stimulates the release of cytokines that can exert
well as T-lymphocytes appears to be decreased a regulatory role in the immune response and
during and immediately following vigorous inflammation (Trinchieri 1989; Bellone et al. 1993).
exercise. Some researchers have speculated that
an increased incidence of upper respiratory tract
The complement system
infections seen in high-level endurance athletes
is a result of this decrease in lymphocytes The complement system is partially responsible
(Neiman 1997). The decrease in numbers is most for the recognition and destruction of pathogens
probably related to the secretion of exercise- and altered host cells. In this respect it is a highly
induced hormones such at cortisol (Neiman 1997). complex system that plays an imperative role
Although B-lymphocytes have been implicated in both the innate immune system as well as a
in such phenomenon as exercise-induced asthma primed immune system ready to react against
and upper airway disease in the athlete, their role a pathological insult. The complement system
in the acute phase of injury remains elusive. Con- possesses the ability to directly recognize and
sidering the complex interactions seen between eliminate pathogens or damaged host cells. The
both plasma and cellular mechanisms of inflam- mechanisms by which this is accomplished will
mation, one may speculate that B-lymphocytes be considered below.
serve an active role in the generation and/or The complement system is made up of more
regulation of the inflammatory response. Further than 30 plasma and cell membrane proteins. When
studies are needed, however, to define the exact activated by a pathogen or injury, a precisely
nature of their involvement. regulated series of interactions, not only within the
complement proteins but also with the pathogen
and cell membranes, initiates a series of reactions
Natural killer cells
that can be divided into three stages. The first is
Natural killer (NK) cells represent a discrete sub- the recognition and initiation of one of the two
set of the lymphoid population, differing from complement-activating pathways (classic path-
T-cells and B-cells in that they do not express or way and alternate pathway.) The second is C3
rearrange known receptors for antigens. NK cells binding and amplification; the third and final
can account for up to 20% of circulating lympho- phase is the membrane attack pathway. The pro-
cytes. NK cells appear to provide a first line of cess of activation of the classic pathway involves
defence against tumour cells and viral infections recognition of the inflammatory agent by the first
(Tracey & Smith 1978). They are characterized by component of complement (C1). The C1 compon-
the expression of two distinct membrane pro- ent consists of three distinct proteins: C1q, C1r
teins, the CD56 receptor and the CD16 receptor. and C1s. The C1q protein attaches itself to the Fc
CD16 is a low affinity receptor for the Fc portion component of the instigating immunoglobulin.
of immunoglobulin G, whereas CD56, which is C1r and C1s are activated with this binding
analogous to the neural cell adhesion molecule and in turn react with C4 and C2 forming two
(NCAM) (Tracey & Smith 1978). These cells were products, an anaphylatoxin C4a and C3 con-
found to propagate cytolytic cell destruction in vertase (C4b and C2a). Cs3 convertase cleaves
the absence of deliberate immunization and in the C3 molecule forming C3a and C3b (a second
the absence of MHC complexes. The recognition anaphylatoxin). The resulting complex binds to
of these foreign cells seems to be mediated by the C5 molecule initiating hydrolysis of this mole-
the absence of MHC class 1 molecule (Ljunggren cule forming C5a and C5b. C5b will attach itself
& Karre 1985; Sprent 1993). The presence of to target cell membranes and acts to facilitate
such molecules appears to serve as an inhibitory binding of C6, C7 and C8 as well as initiating the
stimulus to the NK cells. Activation of NK cells polymerization of multiple C9 molecules. This
not only results in their cytolytic activity, but also forms a macromolecule known as the membrane
Classic pathway with the release of histamine, PAF and serotonin.

Immune complexes These mediators serve to further increase vas-
C1-antigen cular permeability. The anaphylatoxins appear
C4 C2 to mediate the smooth muscle contraction seen
in bronchial spasm. This is accomplished by one
of two pathways, the degranulation of the mast
cell or a second pathway utilizing an arachidonic
C4a Alternative pathway
acid derivative. C5a also serves an important role
C4b C2a (C3 convertase) Bacteria
C3a Foreign material as a chemotactic agent for leucocytes. With the
C3BD initiation of the complement system, local pro-
C5a duction of C5a serves to recruit neutrophils and
C3b
monocytes to sites of tissue injury. This cleav-
C5
age component also has the ability to stimulate
Bb
neutrophil degranulation and superoxide anion
C5b-g (MAC) C3b C3 production (Jose et al. 1981).
Mechanical trauma to tissues such as fractures,
C3a muscular strains or sprains leads to the exposure
C5a
of the basement membranes, which in turn activ-
Fig. 2.4 Illustration of the complement pathway ates factor XII (Hageman factor). This activated
demonstrating both the classic and alternative
Hageman factor not only cleaves plasminogen
pathways. Note the formation of the membrane attack
complex (MAC, C5b) as well as the formation of and prekallikrein, generating plasmin and kalli-
anaphylaxins C4a, C3a and C5a. krein, respectively, but also has the capability
of activating the alternative complement path-
way. Plasmin maintains the capability to induce
attack complex (Fig. 2.4). Following the assembly increased vascular permeability as well as utiliz-
of the membrane attack complex on the cell mem- ing the anaphylatoxins C3a and C5a to induce
brane of the target cell, small cylindrical holes are changes in microvascular permeability. In this
formed within the membrane leading to cell lysis way, acute traumatic injuries utilize the com-
(Cooper 1985; Muller-Eberhard 1986). plement system to mediate acute changes in
Cell products, bacteria or foreign material may vascular permeability as well as to initiate the
also activate the alternative pathway. In this path- inflammatory response.
way, C3 binds with two plasma proteins, factor B The complement system is regulated by several
and factor D, with a resultant product Bb catalys- mechanisms including: (i) the spontaneous decay
ing the conversion of C3 to C3a and C3b. With of active complexes or cleavage products; (ii) the
the presence of Bb, C3b functions in an amplifica- inactivation of specific components by proteolysis;
tion reaction stimulating C3 convertase to form and (iii) the binding of active components by
more C3a and C3b. C5 convertase is formed with plasma proteins. Factor I, a plasma protein, is
the generation of C5a and C5b. The membrane responsible for the down-regulation of both C3b
attack complex is then formed as in the classic and C4b (Liszewski & Atkinson 1993). A second
pathway. plasma protein, C1 esterase inhibitor, serves to
When the classic pathway is utilized, the regulate the activation of the classic pathway
formation of anaphylatoxins (C3a, C4a and C5a) by binding to both C1r and C1s making them
is an important step. Each of these molecules is inactive (Liszewski & Atkinson 1993). Serum
capable of causing smooth muscle contraction carboxylase N can inactivate the anaphylatoxins
as well as increasing vascular permeability. C3a C4a, C3a and C5a. Factor H is another plasma
and C5a also possess the ability to activate mast protein, which binds to the C3b protein, making
cells and basophils leading to their degranulation, it more susceptible to cleavage by factor I.
Table 2.4 Patterns of disease in complement-deficient patients.
Deficient component Disease
C1q, C1r, C1s, C4, C2 SLE, autoimmune diseases and recurrent pyogenic infections
C3, factor H, factor I Recurrent pyogenic infections and immune complex diseases
C5, C6, C7, C8 Recurrent neisserial infections
C1 inhibitor Hereditary angioedema
CR3, CR4 Severe immunodeficiency, leucocyte disfunction and recurrent infections
SLE, systemic lupus erythematosus.
The importance of the complement system can anatomy consists of a layer of endothelium
be seen by examining patients with congenital connected by tight junctions and a basement
deficiencies. The absence of any of the classic membrane composed of type IV collagen, glyco-
complement pathway (CCP), components results saminoglycans and glycoproteins. This vascular
in systemic lupus erythematosus (SLE) (Liszewski anatomy serves to preserve the normal relation-
et al. 1989). In addition to SLE, the absence of C3, ship between the tissue and the circulating plasma
factor H and factor I appear to make an individual and cellular components, which is one of mutual
more susceptible to repeated pyogenic infections exclusion. After tissue injury, an initial rapid step
by strains of Staphylococcus, Streptococcus, pneumo- is activation of the endothelial cells. The endo-
coccus and other organisms (Morgan & Walport thelium, when activated, has the ability to change
1991). Whereas impaired CCP activation leads to its surface properties and become adhesive for
autoimmune disease, immune complex disease both platelets and leucocytes. Shortly after acute
and repeated infections, uncontrolled CCP activa- trauma, the endothelium expresses an adhesion
tion occurs in the absence of regulatory proteins. protein, P-selectin. This protein binds both poly-
It appears that an unregulated CCP is involved morphonuclear leucocytes and monocytes; it is
in the pathogenesis of hereditary angioedema this binding or tethering that accounts for the
(Table 2.4) (Storkus et al. 1987; Davis 1988). rolling of leucocytes along the endothelium. The
activated endothelium also stimulates the pro-
duction of PAF. The synthesized PAF is directed
Response to injury
towards the surface of the endothelial cell, but
Numerous changes occur within the human body is not released. This localization of PAF to the
after the onset of an inflammatory state. These surface induces tight binding of the leucocytes
changes are not only localized to the site of the with their subsequent emigration, and also primes
pathology but also involve numerous organ sys- them for degranulation. PAF has also been implic-
tems. The acute phase response represents a state ated in the activation of passing platelets by the
in which the body modifies its normal internal bound leucocytes. The platelets, once activated,
environment to appropriately respond to an release mediators such as TxA2, serotonin and
inciting pathology. Cytokine-induced changes in histamine, leading to the formation of gap junc-
plasma protein synthesis, the neuroendocrine tions in the endothelium and thus facilitating
and haematological systems, metabolic processes, leucocyte migration (Fig. 2.5). The formation of
and non-protein plasma components mediate gap junctions leads to a disruption of endothelial
these local as well as distant changes. continuity and exposing of the basement mem-
The initial response to tissue injury occurs brane, which in turn further activates platelets.
primarily in the vasculature, namely the capillar- This leads to a self-propagating cycle which is
ies and postcapillary venules. Normal vascular vital in the repair of damaged tissue.
Platelet aggregation and formation, whereas constriction leads to increased

leucocyte recruitment hydrostatic pressure in the capillaries and sub-
sequent increased tissue oedema.
Senotonin
The postcapillary venule appears to be the
T & A histamine
primary site of endothelial changes for many of
the vasoactive mediators. As mentioned above,
during the time immediately following an injury,
a complex cascade of biochemical events is initi-
Activated ated, leading to cell contraction, loss of tight
platelets
junctions and formation of endothelial gaps. This
Circulating Exposed basement series of events leads to increased vascular per-
leucocytes membrane and
meability with the subsequent extravasation of
secondary gap junctions
(a) intravascular fluids into the injured tissue. This
process is dynamic and reversible with maximal
Leucocyte migration
permeability occurring within 10–30 min after
Vasoconstriction (TRA) injury. Normal vascular anatomy is regained usu-
ally within an hour.
Several modalities have been demonstrated
to alter the course of inflammation, both in the
acute and chronic setting. Non-steroidal anti-
Migration of inflammatory drugs (NSAIDs) serve as mem-
Rolling circulating brane stabilizers, thus dampening the effects of
mediated via leucocytes
(b) selectin the arachidonic acid cascade. The use of NSAIDs
has not been proven to speed wound healing and
Fig. 2.5 Following tissue injury, exposed vascular in fact has proved to be of minimal benefit in the
collagen stimulates platelet aggregation and activation treatment of acute injuries. Corticosteroids act
(a). Activation stimulates the release of mediators
leading to gap junction formation as well as leucocyte
early in the inflammatory cascade by blocking the
aggregation to the site of injury, with subsequent release of arachidonic acid. There have been no
migration into the tissues (b). clinical studies that demonstrate the oral use of
corticosteroids in acute sports trauma to be bene-
ficial in the recovery of an athlete. Corticosteroid
The response of the vasculature to injury is injection therapy, on the other hand, has been
not only one of increased permeability, but also implied in animal models to be advantageous
one of dynamic vasodilatation and vasoconstric- to wound healing, but no conclusive data have
tion. At sites of injury, vasoactive mediators, both been obtained. Injection of corticosteroids should
cellular and plasma derived, bind to specific be limited in acute macrotrauma secondary to its
receptors located on the endothelial cells as well catabolic effect, and injections around tendinous
as the vasculature smooth muscle, propagating and ligamentous structures must be weighed
either vasoconstriction or dilatation. The effects carefully secondary to the deleterious effects on
of vasodilatation and constriction have variable those structures. Physical modalities such as
effects on the tissue, depending on their site of thermotherapy and cryotherapy have been used
action. Vasodilatation of the arterioles leads to in the treatment of acute inflammation. Thermo-
increased blood flow to a tissue, i.e. increased therapy, or heat application, has been shown
oedema, whereas constriction leads to decreased to relieve the secondary symptoms of inflamma-
blood flow, i.e. decreased oedema. Conversely, tion such as muscle spasm. Cryotherapy appears
dilatation of venules decreases capillary hydro- to reduce the local tissue temperature and local
static pressure leading to decreased oedema blood flow. This serves to decrease the subsequent
30 000
Change plasma concentration (%)
Serum amyloid A
300 Creactive
200 protein
C3'
100
0 Fig. 2.6 Changes seen in serum

Transferrin concentrations of acute phase
Albumin proteins during the inflammatory
0 7 14 21 response. (Modified from
Time (days) Kushner 1993.)
oedema and may alter secondary necrotic effects altered synthesis of endocrine hormones includ-
of the initial trauma. ing corticotrophin-releasing hormone (CRH),
Acute phase proteins are defined as plasma glucagon, insulin, adrenal catecholamines, growth
proteins whose amount of production is either hormone, adrenocorticotrophic hormone (ACTH),
increased or decreased by a factor of 25% in the thyroid-stimulating hormone, aldosterone and
face of an inflammatory stimulus (Izumi et al. vasopressin (Chrousos 1995; Boelen et al. 1997).
1994). Some of the well-known human plasma For the most part, these changes in the neuro-
proteins include ceruloplasmin, the complement endocrine system do not appear to be functional,
components C3 and C4, C-reactive protein (CRP) rather unwanted collateral effects of the medi-
and serum amyloid (Kushner 1982; McCarty 1982). ators of inflammation. Fever has been discussed
These proteins are termed positive acute phase in the previous section on prostaglandins, but in
proteins in that their production is markedly addition to the effect of PGE on the stimulation
increased. CRP and serum amyloid is usually of fever, it appears that the cytokine, IL-6, stimu-
present in plasma in trace amounts. After an lates the induction of fever via its effects on the
inflammatory insult their concentration may thermoregulatory centre (Dinarello 1997). The
increase 1000-fold (Fig. 2.6) (McCarty 1982). The production of IL-6 occurs in the endothelium of
synthesis of negative acute phase proteins is hypothalamic organs and is a response to IL-1α
by definition decreased by at least 25%. Long and TNF-α, common proinflammatory mediators
recognized negative acute phase proteins include (Lucino & Wong 1996).
transferin and albumin. The functions of these Not only the inflammatory process, but also the
acute phase proteins are as varied as the proteins stress experienced by the body, affects the neuro-
themselves. Some, such as complement pro- endocrine system. The endocrine abnormalities
teins, are essential in the elimination of foreign experienced by the body are the result of a com-
pathogens; the functions of other proteins, such plex interaction between inflammation-associated
as CRP, remain elusive, but do provide us with cytokinesapredominantly the hypothalamic–
an adequate marker of the inflammatory status. pituitary–adrenal axis (Chrousos 1995). Common
Neuroendocrine changes seen in the acute phase hormone increases are seen in insulin, glucagons,
response include fever, somnolence, anorexia and cortisol and ACTH, as well as others (Patel &
Neuberger 1993). IL-1, IL-6 and TNF-α appear Metabolic changes seen in the face of chronic
to be amongst the most potent stimulators of the inflammation include the loss of body mass and
hypothalamic–pituitary–adrenal axis by stimulat- altered lipid metabolism. As with neuroendocrine
ing the production of CRH and arginine vaso- changes, these are probably an untoward effect
pressin, with a consequent increased production of circulating cytokines rather than a desired
of ACTH and cortisol. The sympathetic and response. Decreases in the amount of skeletal
adrenomedullary systems respond to both pro- muscle, fat tissue and bone mass result from the
inflammatory mediators as well as to endocrine effects of numerous cytokines including IL-1, IL-
changes, with the secretion of neurotransmitters. 6, TNF-α and interferon gamma (IFN-γ) (Espat
These further lead to alterations in the neuro- et al. 1995; Takahashi et al. 1996). IL-1 and IL-6
endocrine environment associated with the acute appear to be the primary cytokines responsible
phase response. for the loss of skeletal muscle, which is a result of
Lethargy, anorexia and somnolence appear decreased protein synthesis as well as increased
to be common findings during the acute phase muscle proteolysis (Cannon 1995). Alterations
response. In experimental models IL-1 and TNF- in lipid metabolism results in the loss of fat
α both induce a somnogenic effect on rabbits when tissue and decreases in circulating high-density
injected into their cerebral ventricles (Surh & lipoproteins, as well as increases in serum trigly-
Sprent 1994). IL-1 has been demonstrated within cerides, very low-density lipoproteins and low-
the central nervous system of humans and appears density lipoproteins (Liao & Floren 1993; Feingold
to play a central role in the somnogenic response et al. 1994; Banka et al. 1995). Unlike the cytokines
in them as well (Surh & Sprent 1994; Leon et al. responsible for muscle degradation, the cytokines
1997). Several cytokines are implicated in the responsible for the altered lipid metabolism
pathogenesis of anorexia. In animal models, IL- remain elusive. Studies have demonstrated that
1-induced secretion of IL-6 appears to stimulate chronic injections of IL-6 in Rhesus monkeys
an anorexic state; however, clinical trials to appear to induce a state of hypocholesterolaemia,
support these findings are lacking in humans but the correlation to human lipid metabolism
(Zeidler et al. 1992; Fattori et al. 1994; Leon et al. remains unclear. Immunosuppression has also
1996). Other animal studies have implicated local been implicated as an acute phase phenomenon
production of TNF-α as well as IL-1α-induced (Ettinger et al. 1995).
secretion of leptin (an acute phase reactant) as a The onset of an inflammatory process is accom-
stimulant to anorexia (Zeidler et al. 1992; Ryan panied by numerous physiological reactions at
1997). In truth, as with most types of inflamma- sites distant from the initial insult. The acute phase
tory reactions, its causes are most likely multifac- response to injury represents a complex interaction
torial and remain unclear. of numerous organ systems. These interactions
Anaemia of chronic inflammation appears to be appear to be mediated by inflammation-associated
secondary to a decreased production of red blood cytokines and influenced by modulators of cyto-
cell progenitors, as well as a decrease in erythro- kine function as well as endocrine hormones and
poietin synthesis (Means 1995). Both of these other circulating factors. Although these changes
appear to be mediated somewhat by inflamma- are frequently seen in association with one
tory cytokines. Some of these cytokines decrease another, it is common to have variable responses
the response of the red blood cell progenitors to to inflammation on an individual basis.
erythropoietin, whereas others decrease the syn-
thesis of erythropoietin (Faquin et al. 1992). The
The process of tissue repair
major component may be the decreased produc-
tion of erythropoietin, since studies have shown When faced with inflammation, the body is
that anaemia secondary to chronic inflammation forced to initiate the reparative process. The re-
can be overcome with the administration of establishment of physiologically functional tissue
erythropoietin alone (Zabucchi et al. 1992). is imperative for the return to activity levels
similar to the preinjured state. A coordinated pro-

cess of cell migration and proliferation directed T-lymphocytes
by specific biochemical mediators facilitates this
repair of damaged tissue. This process utilizes
Leucocyte numbers
various aspects of the humeral and cellular
defence mechanisms to alleviate the inciting Macrophages
pathology.
Following an injury in which the vasculature
is disrupted, the process of tissue repair begins
Platelets
immediately. As mentioned above, platelet adher-
ence to the exposed collagen stimulates activation
with the subsequent release of mediators such
as serotonin, histamine and TxA2, among others.
1 2 3 4 5 6 7 8 9 10 11 12 13 14
Once the acute haemorrhage is controlled by
Days
the activated platelet and clotting pathways, the
migration of inflammatory cells into the region Fig. 2.7 Following an injury to biological tissue,
of damage begins. migration of characteristic leucocytes into the
In the immediate postinjury period, neutro- damaged tissue follows a consistent pattern. The
length of their presence depends on the amount
phils predominate the immigrating leucocytes.
of trauma.
They can be detected within 1 h after injury and
peak in approximately 24–48 h. Recruitment of
these cells is mediated by the process of roll- fibroblasts. Macrophages function in debridement
ing (via selectins), adhesion (via integrin) and of the pathology, recruitment of other inflam-
migration through the endothelium (Menger & matory cells, cell proliferation, and regrowth of
Vollmar 1996). Immigration into the site of injury peripheral nerves (Leibovitch & Ross 1975; Platt
is stimulated by complement components (C5) as et al. 1996; Fritsch et al. 1997).
well as factors released by the activated platelets T-lymphocytes have been shown to be pre-
(Marder et al. 1985). sent at sites of injury from the first hour post-
The function of these neutrophils is to clear injury and peaking between 7 and 14 days later
the wound of fibrin as well as the initiation of (Fig. 2.7) (Martin & Muir 1990). Their function
inflammation via the release of proinflammatory is not clearly understood, although their absence
cytokines (Grinnell & Zhu 1994). As mentioned has been shown to lead to decreased wound
earlier, the regulation of cytokines is primarily at strength and lower amounts of collagen deposi-
the transcription level. Messenger RNA of TNF-α tion. Conversely, prolonged activation of T-cells
is apparent at the site of injury within 12 h, peak- appears to lead to excessive fibrosis as seen in
ing at 72 h. This increase in mRNA may last for keloid formation (Borgognoni et al. 1995). This
up to 5 days after the injury (Feiken et al. 1995). can be logically expanded to areas of chronic in-
As the number of neutrophils begins to decrease, flammation, where increased amounts of fibrosis
a concomitant rise in the number of macrophages are seen, presumably secondary to prolonged T-
is seen. This increase in macrophages seems cell activation (Peters et al. 1986).
to peak in 5–7 days. The recruitment of these Following the recruitment of leucocytes and
circulating macrophages to the site of injury is fibroblasts, a tissue termed granulation tissue is
secondary to factors released by both platelets formed. This tissue was initially termed granula-
and neutrophils (Cromack et al. 1990; Ham et al. tion tissue secondary to the granular appearance
1991). These macrophages serve as a major of the newly forming blood vessels. Granula-
source of growth factors and cytokines that tion tissue develops from connective tissue sur-
recruit and activate additional macrophages and rounding the site of injury as well as the recently
immigrated leucocytes, fibroblasts and myofib- takes the form of collagen with the physiological
roblasts. Over a period of time, this granulation and histological appearance of fibrosis. If the
tissue is gradually replaced with more organized pathological insult is small, the ratio of fibrosis to
collagen, which remodels to eventually form normal tissue remains small and the functional-
organized scar tissue. ity of the original tissue is left intact. In instances
of prolonged pathological insult, the ratio of
fibrosis to normal tissue is elevated, thus com-
Conclusions
promising the host tissue function. It is for this
Although inflammation is often thought of as reason that the athlete as well as the physician
an unwanted effect of trauma or overtraining, attempt to minimize the amount of inflammation.
it represents a physiological state of repair that’s
purpose is to return the individual to a state
of functional recovery. The development of an References
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PA R T 2
BASIC SCIENCE OF
TISSUE HEALING
A N D R E PA I R
Chapter 3
Skeletal Muscle Regeneration After Injury:

Cellular and Molecular Events
ANDRÉ-XAVIER BIGARD AND EMMANUELLE FINK
tion (Hudgson & Field 1973). Discontinuous

Introduction
regeneration, of embryonic type, is characterized
Muscle damage is frequently observed after by the formation of newly regenerated myofibres
sports injuries. The ability of skeletal muscle to from myoblastic cells. In contrast, continuous
regenerate after injury is one of its major charac- regeneration, of budding type, results in the out-
teristics and myofibres are repeatedly damaged growth from the end of the section of a partially
and repaired during adult life. At the anatomical damaged myofibre. Continuous regeneration is
level, injuries are commonly divided into shear- less understood and will not be treated in this
ing injuries, in which both myofibres and frame- review.
work are torn, and injuries in situ, in which only Before describing the several phases of the
myofibres are damaged, such as after repeated healing process, it is important to summarize
eccentric contractions. Shearing injuries result some aspects of the structure of satellite cells
mainly from direct trauma to skeletal muscle or which represent stem cells providing myoblasts
strain injuries, while in situ injuries follow exhaust- for regeneration. We will pay particular atten-
ive exercise, the application of local anaesthetics tion to the molecular events of activation and
or are caused by diseases. The treatment and differentiation of satellite cells, and their clinical
prognosis of muscle injuries vary widely accord- relevance now and in the future.
ing to the severity and extent of the trauma, but
regardless of the origin of the injury, skeletal
Structure of adult skeletal muscle
muscle will regenerate.
In response to injury, skeletal muscle re- Muscle fibres are enveloped by the basal lamina.
generates following two types of regeneration. Between the basal lamina and the sarcolemma
Epimorphic regeneration is mainly found in of the myofibres, are the satellite cells (Fig. 3.1).
amphibians and gives rise to an entire new limb These unspecialized mononucleated cells, which
after amputation (Carlson 1970). In contrast to were first described by Mauro (1961) in frog
amphibians, skeletal muscle regenerates in muscle, are known to have myogenic potential
mammals utilizing the remnants of the original and to mediate the postnatal growth of skeletal
myofibre complex. Here we review and discuss muscle (Rosenblatt et al. 1994; Schultz 1996). In
some important cellular events which follow addition to their role in muscle hypertrophy and
muscle damage in mammals, and epimorphic postnatal growth, there is now a large body of
regeneration will not be treated further. Muscle evidence indicating that satellite cells function
regeneration has been broadly divided into two as stem cells that provide myoblasts for muscle
types: continuous and discontinuous regenera- regeneration in adults. The exact origin of satellite
35
36 basic science of tissue healing and repair
Sarcolemma
Basal lamina
Myofibril
Mitochondria
Satellite cell
nucleus
Fig. 3.1 Anatomical location of

satellite cells at the periphery of
mature myofibres. Note that the
basal lamina that surrounds the
Myonucleus
satellite cell and the associated
myofibre is continuous. (From
Carlson & Faulkner 1983.)
cells has not been clearly identified. However, demonstrated that satellite cells have intrinsic
it seems that these myogenic cells stem from properties dependent on their muscle origin, and
early myoblasts that were not incorporated in the independent of environmental cues (Dolenc et al.
developing syncitia, and remained in the surface 1994; Martelly et al. 2000). Satellite cells from
of all fibres (Schultz 1989). Satellite cells adja- either slow or fast muscles present significant
cent to mature myofibres do not express specific differences on the expression of several protein
markers of committed myoblasts such as early- families such as metabolic enzymes, hormonal
acting myogenic regulatory factors (MRFs), Myf- receptors or capacity to express MRFs. These
5 and MyoD, growth factors, or other known differences could have consequences on the
markers of terminal differentiation. This finding capacity of slow and fast muscles to regenerate
is consistent with the hypothesis that satellite after injury.
cells are stem cells with an identity distinct from Satellite cells are normally in a non-
that of myoblasts. The microenvironment of satel- proliferative, quiescent state, but are activated
lite cells, available growth factors and MRFs play in response to muscle injury (Schultz et al. 1985;
a pivotal role for the generation of committed Grounds 1998). Multiple rounds of prolifera-
myoblasts. tion of these stem cells occur after their activa-
There is now available evidence that satellite tion, giving rise to myogenic precursor cells
cells are divided into subclasses based on the (Grounds & Yablonka-Reuveni 1993). The num-
fibre type in which they lie. Moreover, there is ber of quiescent satellite cells is dependent on
also evidence that satellite cells form a hetero- age and muscle fibre type. Skeletal muscle in
geneous population based on their profile of gene young animals contains a higher concentration
expression (Cornelison & Wold 1997). It has been of satellite cells than in adults (Schultz 1989).
skeletal muscle regeneration 37
Degenerative phase Regenerative phase
Damaged
VLA-4/VCAM myofibre FGFs LIF
ligation PDGF IGF-1
MyoD TGF-β HGF
Myf-5 IL-6 NGF
Satellite
cells Myogenic
precursor cells
TGF-β
TNF-α
Infiltration of IL-1 Myogenin
neutrophils and IL-6 MRF4
mononucleated Invaded/resident
cells macrophages
bFGF
PDGF
Fig. 3.2 Schematic representation Differentiated
Myostatin
of the cellular and molecular myotubes
Cytokines, IL-1
events involved in satellite Regenerated
cell activation following my myofibres
ofibre injury, giving rise to
Maturation phase
regenerated fibres.
The percentage of satellite cells within muscles either early-acting MRFs, an asymmetrical satel-
decreases with age, and more rapidly from birth lite cell division and/or the de-differentiation of
through sexual maturity than in adults. The committed myogenic precursor cells (Seale &
decrease in the percentage of satellite cells with Rudnicki 2000).
ageing is the result of an increase in myonuclei Skeletal muscle injury is generally followed by
in both oxidative and glycolytic myofibres, and a series of processes included in three phases: a
a decrease in total number of satellite cells. On degenerative phase, a regenerative phase and a
the other hand, the satellite cell density is higher maturation phase (Fig. 3.2) (Plaghki 1985). Many
in oxidative than in glycolytic tissue, at both experimental results suggest that basic mechan-
whole muscle and single fibre levels (Gibson isms underlying the cellular responses to acute
& Schultz 1982, 1983). This heterogeneity in trauma are well conserved regardless of the
satellite cell content between muscle fibre types type of initial injury. Although the sequence of
has been related to an increase in satellite cell cellular responses of injured muscle regenera-
density with the proximity of capillaries and tion is roughly constant and well determined,
motor neurone junctions. While the population the time-course of muscle regeneration processes
of satellite cells decreases with age, their number are tightly related to the types of muscle injury
remains relatively constant over repeated cycles (Carlson 1973). Using drastic experimental models,
of degeneration–regeneration. This finding high- it has been shown that the regenerative process
lights the inherent capacity of these stem cells takes place earlier after in situ injuries without
for self-renewal (Gibson & Schultz 1983). At least destruction of the basement membrane, than
three models have been suggested to account after denervation/devascularization of muscle
for the self-renewal of satellite cells, involving (Lefaucheur & Sebille 1995).
The degenerative phase A

First phase of the degenerative process
This is also known as non-inflammatory or

intrinsic degeneration, and follows the initial
damage of the muscle fibres. An extensive dis-
ruption of the structural components of the
muscle is first observed at the site of injury. The
extent of anatomical damage of the muscle
tissue varies significantly according to the nature
of the injury and its severity. With regard to
exercise-induced muscle injury, many morpho-
logical studies showed that the Z-discs are
the most vulnerable structures (Fridén & Lieber
2001). Other intracellular anomalies have been
reported according to the severity of the injur-
ing process, and damage of the sarcolemma,
T-tubules and the cytoskeletal system are com-
monly observed after exercise-induced muscle
injuries. More severe trauma, including strains,
B
contusions, prolonged ischaemia and muscle
lacerations are associated with the crush and tear
of myofibres, and often the death of nearly all
myonuclei (Fig. 3.3).
The early responses to initial damage con-
sist of catabolic events that result in autolysis
of the damaged muscular components. A loss
of intracellular calcium homeostasis has been
shown to activate calcium-dependent proteases
referred to as calpains (Armstrong et al. 1991).
Such enzymes are able to cleave myosin, α-actinin, Fig. 3.3 Histological evidence of muscle damage.
vinculin and many other contractile filament com- (A) Longitudinal section of the median head of the
triceps brachii muscle immediately after running
ponents and metabolic proteins in the muscle
downhill, stained with toluidine blue O. Note the
cell. Calpain activation appears thus to be a widened I-bands (arrows). The scale bar represents
key occurrence of damaged muscle autolysis. 25 μm (from Armstrong et al. 1983). (B) Transmission
Most of these alterations become prominent electron micrograph showing sarcomeric dissolution
4–8 h after initial injury. Satellite cells, which and Z-line streaming in skeletal muscle after eccentric
contractions. The scale bar represents 1 μm (from
are dormant under the basement membrane of
Warren et al. 1993).
myofibres, withstand the initial damage and its
early consequences, and then enter into a cycle of
activation–proliferation.
all traces of the originally damaged myofibres.
This phase of muscle repair includes phagocy-
Second phase of muscle degeneration
tosis, which is secondary to an inflammatory cell
This phase is also called extrinsic or inflamma- response, and is dependent on the presence of
tory degeneration, and involves the removal of invading macrophages (Fig. 3.2).
thus unlikely that bFGF is a key chemoattract-

neutrophils and
ive stimulus for inflammatory cells. In contrast,
mononucleated cells
platelet-derived growth factor (PDGF), released
Neutrophils and mononucleated cells accumu- from injured muscle, is known as a mitogen and
late at muscle injury sites. Neutrophils respond chemoattractant for inflammatory cells. However,
early to muscle injury. The neutrophil population its low concentration in myofibres and short half-
increases significantly within 1–6 h and declines life make uncertain its role as a chemoattractant
9–12 h after damage (Orimo et al. 1991). In certain to mediate the inflammatory response to muscle
cases this rapid increase in the neutrophil popula- injury (Bowen-Pope et al. 1984). Myostatin, a new
tion endures for a few days (Fielding et al. 1993). muscle-specific growth-inhibiting factor, has been
This early increase in the number of inflamma- recently suggested to act as a chemoattractant
tory cells may result either from chemotaxis of for phagocytes and inflammatory cells (Kirk et al.
specific cells to the site of muscle damage and/or 2000). The specific role played by many other
from mitogenesis of inflammatory cells initially soluble factors such as cytokines as chemoat-
present in skeletal muscle near the myofibres. tractants in damaged muscle remains unknown
There is experimental evidence that chemotaxis to date. Additional data suggest that the early
is the primary mechanism by which the number activation of resident macrophages or fibroblasts
of inflammatory cells increases in injured muscle could initiate the release of other chemoattract-
(Bintliff & Walker 1960). ant substances, leading to the translocation of
The exact nature of the substances acting as inflammatory cells within injured muscle. Once
chemoattractants for inflammatory cells remains resident macrophages and/or fibroblasts are
a matter of debate (Tidball 1995). Several mole- activated by chemoattractant substances, these
cules released from injured muscles have been later inflammatory cells could initiate chemotaxis
viewed as active substances for leading inflam- of additional cells by a wound hormone uniden-
matory cells from the circulatory system to the tified to date.
injury site (Table 3.1) (Chen & Quinn 1992). Basic The inflammatory response to muscle injury
fibroblast growth factor (bFGF or FGF-2) may be is initiated by the local proteolysis of extra-
released through membrane lesions, but while cellular matrix molecules. Fibroblasts probably
it is capable of attracting myogenic cells, there play a significant role in degrading extracellu-
is no experimental evidence to support a role lar matrix molecules, mainly by an increase
in attracting inflammatory cells after injury. It is in collagenase expression. PDGF and cytokines
Table 3.1 The main effects of several growth factors and cytokines on chemotaxis, proliferation and differentiation
of satellite cells.
Basic effects on muscle

Growth factor or
cytokine Chemotaxis Proliferation Differentiation
bFGF +/− ++ −−
PDGF + ++ −−
IL-1 + (lymphocytes)
IL-6 ++
LIF ++
IGF-I, IGF-II ++ ++
TGF-β + +/− −−
TNF-α + − −−
NGF + + +
detected in injured muscle, such as interleukin-1

(IL-1), may stimulate collagenase secretion by
fibroblasts and thus contribute to the proteolysis
of extracellular matrix molecules (Dayer et al.
1986).
polymorphonuclear lymphocytes
and macrophages
Polymorphonuclear lymphocytes and macro-

phages migrate to sites of tissue damage within
a few hours of the injury (Fig. 3.4). Macrophages
constitute the major type of invading cell dur-
ing the inflammatory response to muscle injury.
They are the predominant inflammatory cell
type 1 day postinjury, and more than 50% of
inflammatory cells are macrophages following
exercise-induced injury (Round et al. 1987). Many
investigations have confirmed the marked increase
in macrophages within damaged muscle and
emphasized the major importance of these cells
in muscle inflammation. Distinct subclasses of
macrophages are involved in the development
of muscle inflammation. Macrophages normally
present in the circulatory system increase sig-
nificantly early after injury, while macrophages
normally resident in muscle tissue increase
thereafter (St Pierre & Tidball 1994). It is thus
likely that macrophages increase in damaged
tissue both by emigration from the circulatory
system (mainly by chemotaxis) and also by cell
division of resident tissue macrophages.
Functional role of inflammatory cells in

damaged muscle
Neutrophils rapidly invade the injury site and

are associated with early promotion of the in-
flammatory response. They are involved in the
Fig. 3.4 Light microscopy cross-sections of skeletal release of cytokines or soluble factors that can
muscle from a rat 48 h after a bout of prolonged attract and activate additional inflammatory cells.
downhill exercise (H&E staining). Details of the As discussed above, fibroblasts are candidates
muscle show: (A) a degenerative myofibre with
as mediators of the chemotaxis of inflammatory
altered cytoplasm and infiltration of mononuclear
cells, representative of an early stage of development; cells, but above all can cause proteolysis of extra-
(B) a myofibre invaded by mononuclear cells; and cellular matrix proteins, one of the early stages of
(C) a small-sized regenerative fibre with internalized inflammation. Two pivotal roles for macrophages
nuclei. The scale bars represent 50 μm. have been proposed based on observations that
myogenesis is markedly impaired in the absence

macrophages and the secretion of
of macrophage infiltration (Lescaudron et al.
growth factors and cytokines
1999).
The success of muscle regeneration also relies on
functions other than phagocytosis that may be
phagocytic role of macrophages
mediated by macrophages. Although restricted
Macrophages and inflammatory cells play a in number, resident macrophages could provide
prominent role in removing all traces of the growth factors and cytokines important for the
damaged myofibres and consensus has been early development of the inflammatory response
reached in considering that the phagocytic role in damaged muscle, such as transforming growth
of these inflammatory cells is their most promin- factor beta (TGF-β), IL-1, IL-6 and tumour necrosis
ent function during the recovery from muscle factor alpha (TNF-α) (Rappolee & Werb 1992).
injury. This response of inflammatory cells is an TNF-α is known to induce skeletal muscle pro-
important component of the successful repair tein breakdown, angiogenesis and the production
of injured muscle. Treatment with non-steroidal of components of inflammation. IL-1 is expected
anti-inflammatory drugs (NSAIDs) is known to to exert important influences on the development
impair the recovery of damaged muscles. It has of inflammation. This cytokine is a mitogen and
been shown that rats treated with NSAIDs exhibit chemoattractant for fibroblasts, T-lymphocytes
a slower muscle regeneration than animals and B-lymphocytes, and increases the cytotox-
receiving placebo (Almekinders & Gilbert 1986). icity of macrophages. IL-1 also induces the expres-
The impaired recovery in muscles of treated sion of other inflammatory cytokines such as IL-6
rats is mainly attributed to a less phagocytic and interferons. The postexercise increase in
activity in damaged muscle, a slow down in serum and muscle IL-1 is rapid, and suggests a
the removal of cellular debris and a decrease post-translational control of the secretion of this
in the synthesis of cytokines involved in success- inflammatory cytokine (Tidball 1995). The early
ful muscle repair. These data clearly demon- response of IL-1 to muscle damage appears to
strate that macrophages and neutrophils are be mainly attributable to an increase in its pro-
directly involved in the process of muscle repair, duction by each activated cell, rather than by a
and inhibiting the early activation and infiltra- proliferation of inflammatory cells.
tion of inflammatory cells affects muscle fibre Taken together, these findings show that besides
repair. As a consequence, the early treatment their role in phagocytosis, non-muscle cells such
with NSAIDs after muscle trauma has a bad as macrophages may play pivotal and essential
prognosis. Other situations where phagocytosis roles in mediating muscle repair. The first invad-
by macrophages is impaired, such as ageing, ing subpopulation of macrophages phagocytoses
affect the success of muscle regeneration (Zacks tissue debris, while together with neutrophils the
& Sheff 1982). macrophages are involved in the early inflam-
Macrophage populations comprise distinct matory response, mainly through the secretion
subclasses of cells. Macrophages, including the of soluble factors such as cytokines and local
ED1 antigen, which are associated with lysoso- growth factors.
mal membranes, also called ED1+ macrophages,
are present at high concentrations in areas that
Skeletal muscle regeneration
contain necrotic fibres. They have been shown to
have a high phagocytic activity and to remove The regeneration of myofibres begins after phago-
cellular debris in injured tissue (Honda et al. cytosis of cellular debris. The first step of regenera-
1990; McLennan 1993). This specialized sub- tion includes the activation of satellite cells from
population of macrophages declines in muscle their relatively dormant state, giving rise to myo-
after the phagocytic stage is completed. genic precursor cells (Fig. 3.2). Thereafter, they
proliferate, differentiate into myoblasts, and fuse VCAM-1, called very late antigen 4 (VLA-4), is
to form multinucleated myotubes that then differ- present in leucocytes infiltrating muscle early after
entiate into myofibres. Myoblasts are myogenic injury. Cell–cell interactions of infiltrating VLA-
precursor cells expressing myogenic markers. This 4(+) leucocytes and satellite cells, mediated by
later step of regeneration leads to mature fibres VCAM-1/VLA-4 ligation, mediates the recruit-
comprising adult isoforms of the several families ment of leucocytes to muscle after injury and
of proteins, consistent with the expected muscle focuses the invading leucocytes specifically to the
phenotype (Plaghki 1985). The activation of satel- sites of regeneration ( Jesse et al. 1998). Infiltrating
lite cells and their differentiation into myoblasts leucocytes may also initiate a series of molecular
does not begin until the necrotic debris within the events implicated in muscle regeneration. On the
regenerating basal lamina cylinders have been other hand, the activation of satellite cells seems
removed by macrophages (Hurme et al. 1991). to be dependent on factors either synthesized and
Most myoblasts giving rise to new myofibres arise secreted by macrophages, or released from the
from local satellite cells lying underneath the necrotic tissue by phagocytes (Hurme & Kalimo
basal lamina. Although this problem has not been 1992). These soluble factors have not been clearly
entirely settled, there appears to be little recruit- identified but could be growth factors released
ment of satellite cells from adjacent muscles and, either by neutrophils or invading macrophages.
in most cases, repair of a muscle is the respons- Several cytokines and growth factors have been
ibility of the intrinsic satellite cell population of shown to play key roles in the activation and pro-
the damaged muscle (Schultz et al. 1986). liferation of satellite cells (Table 3.1) (Husmann
et al. 1996).
Activation of satellite cells

growth factor and cytokine
After injury, the satellite cells take several hours
responses during myofibre
to be mobilized. Several non-selective markers are
regeneration
used to characterize the proliferating satellite cell
pool, such as the incorporation of 3H-thymidine
Fibroblast growth factors
or bromodeoxyuridine. Autoradiographic stud-
ies demonstrated that satellite cells were labelled The actions of FGFs on muscle precursor cell act-
by 3H-thymidine 15–20 h after crush injury ivation have been extensively studied (Sheehan
(Schultz et al. 1985). Activated satellite cells were & Allen 1999). FGFs exist as nine different iso-
not detected in damaged muscle before phagocy- forms but only FGF-1, -2, -4, -6 and -9 are active
tosis of the necrotic debris by macrophages had on satellite cells. In normal skeletal muscle, FGFs
begun. This finding clearly demonstrates that the are stored in the extracellular matrix and are
removal of the necrotic muscle debris by macro- bound to proteoheparan sulphates. After muscle
phages seems to be a prerequisite for the activa- injury, FGFs are released, and high levels of both
tion and proliferation of satellite cells. mRNA and protein have been reported in pro-
Diverse mechanisms have been assumed to be liferating satellite cells before the formation of
involved in the activation of satellite cells, includ- myotubes. High concentrations of FGF-1 have
ing events of the inflammatory response and the been previously correlated with a high level of
release of growth factors. myoblast proliferation in damaged muscles of
dystrophin-deficient mice that display persistent
cycles of myofibre degeneration–regeneration
leucocyte–satellite cell
(Dimario & Strohman 1988).
interactions during regeneration
It is thus very likely that FGFs contribute to the
Quiescent satellite cells express a cell-surface proliferation of satellite cells and are involved
adhesion molecule called vascular cell adhesion in the chemotaxis of further muscle precursor
molecule 1 (VCAM-1). The integrin receptor of cells. The main action of FGFs is the activation
of muscle precursor cell proliferation to provide in damaged muscle. This growth factor is chemo-
enough cells to allow regeneration to take place. tactic for adult muscle precursor cells and shows
Studies using mouse knockout models show the a highly stimulating effect on the proliferation
ability of redundant FGF family members to com- of satellite cells (Ross et al. 1986). Moreover,
pensate for one another to preserve the role of together with FGFs, PDGF exerts a strong inhibi-
these growth factors on satellite cell proliferation tion of the terminal differentiation of satellite
under pathological conditions. cells into myoblasts.
Moreover, the availability of basic FGF, also
called FGF-2, is of importance for capillary growth
transforming growth factor beta
during muscle regenerationaa key factor for the
success of muscle repair. Another member of Like PDGF, TGF-β is released from degranulat-
the FGF family, FGF-5, might be important for ing platelets after injury. This growth factor is
the reinnervation process, when the presence of chemotactic for macrophages and leucocytes,
nerve is important for recovering the expected contributes to the synthesis of proteins of the
contractile and metabolic phenotype. Even extracellular matrix, and plays a pivotal role in
bFGF can interact with other growth factors to angiogenesis. Many of the biological effects of
stimulate the secretion of nerve growth factor TGF-β concern the reorganization of the extra-
(NGF) and contribute to the survival of neurones cellular matrix, particularly the reconstruction
(Unsicker et al. 1992). of the basement membrane surrounding the
Collectively, FGFs are mainly involved in the regenerating myofibres. Those effects are medi-
activation and proliferation of satellite cells, in ated by the production of: (i) extracellular matrix
order to provide and activate stem cells to allow proteases; (ii) protease inhibitors such as plas-
regeneration to occur. The exact mechanisms by minogen activator inhibitor 1 (Laiho et al. 1986);
which FGFs push satellite cells towards prolifera- and (iii) extracellular matrix components. TGF-β
tion remain unknown, but it could be hypothes- plays an important role in regulating repair after
ized that FGFs promote satellite cell activation, muscle injury and it has been suggested that
at least partly, by inhibiting the differentiation excessive TGF-β-induced deposition of the extra-
of myoblasts into myotubes. This effect of FGFs cellular matrix can lead to fibrosis (Border &
could be mainly related through inhibition of Ruoslahti 1992). TGF-β regulates a subset of
the expression of insulin-like growth factor II genes that encode growth factors and their
(IGF-II) (Rosenthal et al. 1991) or MyoD, one of receptors, and this finding could help to explain
the mammalian MRFs (Vaidya et al. 1989). As a the varied cellular responses to TGF-β (Nielsen-
consequence, other factors must either repress Hamilton 1990). As for FGFs, TGF-β can be
FGF production and/or strongly promote the dif- stored in an inactive form in the extracellular
ferentiation of myoblasts, later during recovery, matrix and thus both are available for direct
in order to minimize the repressing activity of action after injury, without the need for new syn-
FGFs on the differentiation of muscle precursor thesis before their local action. Moreover, this
cells into myoblasts. growth factor exerts a control on satellite cells
During the period of satellite cell prolifera- by inhibiting their proliferation and terminal dif-
tion, the expression of FGF receptor 1 (FGF-R1) ferentiation, mainly by silencing the transcrip-
increases, and the decrease in FGF-R1 expression tional activation of the MyoD family members
is associated with a concomitant increase in satel- (Allen & Boxhorn 1989).
lite cell differentiation.
Other cytokines
Platelet-derived growth factor
Other cytokines such as IL-6 and leukaemia inhib-
PDGF is first released from degranulated platelets, itory factor (LIF) have been shown to stimulate
and later by activated macrophages and vessels the proliferation of myogenic precursor cells in
vitro (Kurek et al. 1996). LIF is markedly increased basement membrane and extracellular matrix
very early after muscle injury, probably prior (Husmann et al. 1996). HGF and its receptor
to infiltration of immune cells. The activating c-Met have been localized in satellite cells and
effect of LIF on the proliferation of myogenic pre- adjacent myofibres, and their expression has
cursor cells is additive to those of other growth been related to the extent of muscle injury
factors such as bFGF and TGF-β, which suggests (Hawke & Garry 2001). Furthermore, HGF has
different mechanisms of action (Husmann et al. been involved in the activation of satellite cells,
1996). LIF has been shown to be produced by as well as in the inhibition of myoblast differ-
both damaged muscle fibres and resident non- entiation, mainly by an inhibition of the expres-
muscle cells such as leucocytes and macrophages sion of myogenic regulatory factors. Clearly, the
(Kurek et al. 1996). efficiency of muscle regeneration is related to the
IL-6 appears later in damaged muscle, between fine growth factor interactions and to their role
12 and 24 h after injury. This cytokine, together in the expression of myogenic regulators and
with LIF, is one of the putative growth fac- extracellular matrix components.
tors secreted by macrophages, which accounts Furthermore, differentiation of myogenic pre-
for the role of these infiltrating monocytes on cursor cells has been shown to be regulated by a
the proliferation of myogenic precursor cells family of regulatory factors that can interact with
(Cantini et al. 1994). As discussed above, there certain of the growth factors mentioned above.
is clear evidence that besides their scavenger The molecular mechanisms involved in the con-
role, macrophages play a pivotal role in the trol of the differentiation of myogenic precursor
activation and proliferation of satellite cells and cells and the role of MRFs should be examined.
myogenic precursor cells during muscle regen-
eration. Moreover, IL-6 promotes the degrada-
Differentiation of myogenic precursor cells
tion of necrotic tissue and induces apoptosis of
macrophages following muscle injury (Cantini &
growth factors and muscle cell
Carraro 1996).
differentiation
Most growth factors involved in the activation

Insulin-like growth factors
and proliferation of satellite cells inhibit their
Another group of growth factors, IGF-I and IGF- differentiation into myoblasts, except for IGFs
II, also called somatomedins, has been shown which exert a stimulating effect on the differen-
to be mitogenic for satellite cells and myoblasts tiation and fusion of myogenic cells (Table 3.1).
(Florini et al. 1996). Besides these effects on It has been shown that IGF-I exerts less activa-
the proliferation of myogenic cells, IGF-II also tion of myoblast differentiation than IGF-II, but
shows a marked stimulating effect on myoblast taken together these growth factors play a key
differentiation. role at the onset of differentiation (Husmann
et al. 1996). Some experimental evidence suggests
that IGF-I acts first by stimulating muscle pre-
Other growth factors
cursor cell proliferation, subsequently activating
Many other growth factors are already known muscle cell differentiation. As specified above,
to play a role in the regulation of skeletal muscle several local growth factors inhibit muscle cell
regeneration. Heparine-affine regulatory peptide, differentiation; this is the case for FGFs and it
ciliary neurotrophic factor, NGF and hepato- has been suggested that this inhibitory effect is
cyte growth factor (HGF) can interact with the related to a down-regulation of the IGF-II gene. It
most potent growth factors discussed above, appears that a strong interaction exists between
to contribute in the activation of satellite cells, several growth factors such as FGFs, IGF-I and
their proliferation and the reconstruction of the IGF-II.
MRF mRNA is lacking in quiescent satellite cells

mrfs and muscle cell
and this finding is consistent with the hypothesis
differentiation
that these cells represent stem cells, distinct
Myogenic regulatory factors, members of the basic from myoblasts, that give rise to myogenic cells
helix–loop–helix family (bHLH), are expressed after the beginning of their proliferative phase. In
in the embryo during development. These mole- summary, an up-regulation of MyoD and Myf5
cular factors activate the myogenic programme appears to be required for satellite cells to enter
in embryonic precursor cells, thus initiating the proliferative phase, while MRF4 and myo-
muscle differentiation. This family of myogenic genin appear later to participate to the regulation
factors, which includes MyoD, Myf5, MRF4 and of their differentiation into myoblasts.
myogenin, forms dimers with ubiquitous proteins.
The heterodimeric complexes are transcription
Skeletal muscle maturation
factors that bind to the E-box consensus DNA
sequence that is found in the regulatory region The differentiation of myogenic precursor cells is
of many muscle-specific genes. Studies support characterized by the capability for myoblasts to
a role for MyoD and Myf5 in the determination synthesize muscle-specific proteins. Differenti-
of the myogenic cell fate and the formation of ated myoblasts then migrate side by side, loose
myoblasts, while myogenin and MRF4 appear their membranes and fuse to form multinucle-
to act later on muscle differentiation (Hawke & ated myotubes. The fusion of myoblasts to form
Garry 2001). Thus, these myogenic factors play a myotubes is associated with the expression of
pivotal role in the commitment and differentia- muscle-specific proteins. Striking changes of gene
tion of embryonic myoblasts during development expression occur with the fusion of myoblasts,
(Seale & Rudnicki 2000). and genes encoding muscle-specific proteins are
The MRF expression programme during returned on.
generation is similar to that observed during The presence of specific proteins in the tissue
embryonic development. Not detected in quies- is required to produce a viable cellular structure
cent satellite cells, MyoD is expressed very early, and/or to play a tissue-specific role account-
within 12 h after muscle injury, prior to molecular ing for the properties of a system. Thus, skeletal
markers of cell proliferation (Mendler et al. 1998; muscle can be approached from a molecular
Seale & Rudnicki 2000). The expression of MyoD viewpoint, particularly the contractile proteins
mRNA has been strongly related to the prolifera- which account for the mechanical function and
tion of satellite cells and the beginning of re- performance. Several families of proteins present
generation (Olson & Klein 1994). Satellite cells a high degree of molecular variability, due to the
entering the cell cycle express first either mainly existence of multiple isoforms. Some of the pro-
MyoD or more seldom Myf5, followed by the teins accounting for the contractile and metabolic
coexpression of these two factors. The expression properties exist as adult mature and develop-
of these two early acting factors is shown to have mental immature isoforms.
a similar time course in regenerating slow and Skeletal muscle is characterized by the exist-
fast muscle. Following proliferation, myogenin ence of numerous types of fibres and a highly
and MRF4 are expressed in cells during their organized arrangement, resulting in a variety of
differentiation and expression of muscle-specific functional capabilities. A high molecular variety
proteins. However, the expression of these late- of myofibrillar and enzymatic proteins, due to
acting MRFs changes in a different way in regen- the existence of multiple isoforms, accounts for
erating fast and slow muscles (Mendler et al. 1998). this myofibre diversity. Three isozymic systems
Levels of myogenin and MRF4 mRNA decrease are particularly relevant to the functional hetero-
transiently in slow muscle, while mRNA levels geneity of myofibre types: myosin and especially
remain relatively constant in fast-twitch muscles. the isoforms of myosin heavy chain (MHC), the
creatine kinase (CK) isozymes and the lactate slow, that is present in slow fibres (Schiaffino &
dehydrogenase (LDH) isozymes. Reggiani 1996).
Myosin transition in regenerating MHC expression during development

skeletal muscle
Muscle development is characterized by the
One of the most informative methods of delineat- asynchronous differentiation of successive fibre
ing muscle fibre types is based on the exam- generationsainto at least primary and secondary
ination of specific myosin profiles. Myosin is the generations of myofibres in rats. These sequential
most essential part of the contractile machinery events have been mainly described in rats and
and contributes to the functional diversity of mice, since in these species a more complete
myofibres. A strong correlation has been shown picture of MHC isoform expression is avail-
between myosin isoforms, contractile properties able. At early stages of embryonic development,
and physiological measurements of myofibres all fibres express high levels of MHC-emb and
(Schiaffino & Reggiani 1996). The myosin iso- low levels of MHC-neo and MHC-β/slow. By
form composition is thus a molecular marker days 16–17, MHC-β/slow and MHC-neo are
for different muscle fibres, for the physiological segregated in different myofibres, and fibre-
state of muscle tissue, and for the maturation type diversification is then detectable (Condon et
state of regenerated muscle. al. 1990). At this stage of muscle development,
It is a well-known fact, that muscle regenera- primary generation fibres express either MHC-
tion recapitulates the embryonic development emb and MHC-β/slow, or MHC-neo and MHC-
of skeletal muscle fibres. The new myogenesis emb. Secondary generation fibres express mainly
that takes place in regenerating muscles has been MHC-neo.
related to the myogenesis which occurs during The major phase of myofibre maturation
normal development. The major steps of re- occurs during the perinatal period, with the
generation closely recapitulate those of normal appearance of the adult fast MHC isoforms and
ontogenesis, and these two types of myogenesis the emergence of the definitive fibre types.
display many similar morphological and bio- Myofibres expressing MHC-emb and MHC-neo
chemical features (Swynghedauw 1986). How- undergo a further diversification process during
ever, the transition from the immature to adult the postnatal week in rats. They give rise to one
isoforms is more precocious in regenerating than of the four major fibre-type phenotypes, charac-
in developing muscles (d’Albis et al. 1988). terized by the expression of at least one of the
The sarcomeric myosin molecule is a hexamer, four adult MHC isoforms (Schiaffino & Reggiani
consisting of two MHCs, two essential or alkali 1996). These adult MHC isoforms are initially
myosin light chains (MLCs) and two regulat- coexpressed with MHC-emb and/or MHC-neo,
ory or phosphorylable MLCs. MHCs account which progressively disappear during the first
for about 85% of the myosin molecule. This month of life. The MHC isoform profile of
subunit has been found to be both highly con- myofibres is not definitively established during
served in structural terms and highly polymor- the early postnatal period but undergoes further
phic (i.e. present as numerous isoforms). Two changes with ageing.
developmental isoforms have been described in
rat and human skeletal muscle: MHC-emb, pre-
mhc isoform transitions in
dominant in embryonic stages, and MHC-neo,
regenerating muscles
predominant in perinatal stages (Whalen et al.
1981). Rat skeletal muscles contain three major New myofibres formed after muscle injury tran-
fast MHC isoforms, called MHC-IIa, MHC-IIx and siently express developmental myosin isoforms
MHC-IIb, and one slow isoform, called MHC-β/ before switching to adult isoforms. Immature
types of myosin are synthesized before a normal (d’Albis et al. 1987). It is thus clear that the pres-
adult pattern is achieved (Sartore et al. 1982; ence of motor nerves and the thyroid hormone
Whalen et al. 1990). However, embryonic and status play determinant roles in myosin isoform
neonatal isoforms disappear faster during regen- expression, with potential consequences on
eration than during normal myogenesis (d’Albis muscle function.
et al. 1988). Moreover, both fast- and slow-twitch Members of the bHLH family of transcriptional
regenerating muscles show the same transition, regulators probably play a role in the expression
first toward a predominantly fast-type isoform of the MHC isoforms during regeneration. The E-
profile, and secondly toward a slow-type profile box sequence, specific to the heterodimers made
for slow-twitch muscles. up of MRFs and E-proteins (see above), has been
It is not clear to date if satellite cells are profound in the regulatory regions of several genes
grammed to express specific myosin isoforms. encoding for phenotypic proteins, including fast
Some data suggest that satellite cells are not pre- MLCs and type I and type IIb MHCs (Talmadge
determined with respect to the type of adult 2000). The primary function of MRFs is to initiate
myosins which will accumulate in the fibres they the expression of muscle-specific proteins dur-
form (Whalen et al. 1990). This finding supports ing development and regeneration. Moreover,
the notion that the programme expressed by it has been suggested that myogenin and MyoD
satellite cells is not strictly determined and could could play a role in determining the slow and
be influenced by several factors, including the fast phenotype, based on the distribution of these
presence of nerve. More recent data clearly point two factors in slow and fast myofibres, respect-
to intrinsic differences between satellite cells ively (Hughes et al. 1993).
from fast and slow muscles (Düsterhoft & Pette
1993; Dolenc et al. 1994; Martelly et al. 2000).
Creatine kinase in regenerating
Two major controlling influences play a role in
skeletal muscle
determining the specific adult myosin type that
ultimately appears in mammalian muscle fibres. The enzyme CK has been involved in the main-
Continuous innervation is an important factor tenance of the intracellular energy supply of cells
for the maintenance of slow myosin expression with intermittently high and fluctuating energy
during regeneration in rats (d’Albis et al. 1988; requirements, such as skeletal muscle. It has been
Whalen et al. 1990). Innervation plays a clear suggested that CK, which catalyses the revers-
role in determining which adult myosin isoform ible reaction:
will accumulate in regenerated muscle. Slow
Phosphocreatine2– + MgADP– + H+ ↔ Creatine +
myosin is expressed in regenerated slow-twitch
MgATP2–,
muscles only in the presence of slow nerves. In
contrast, a switching of myosin from embryonic fulfils different roles in fast- and slow-twitch
and neonatal MHC isoforms toward fast, and muscles. This enzyme exists as multiple iso-
not slow, isoforms was observed in regenerated forms; cytosolic isoforms of CK are heterodimeric
slow muscle in the absence of nerve, suggesting associations of two types of monomer subunits,
the existence of a ‘default programme’ of MHC known as M, muscle, and B, brain (MM-, MB-
expression (Buttler-Browne et al. 1982). and BB-CK). The MM-CK isozyme is bound to
Thyroid hormone levels also contribute to myofilaments and rephosphorylates ADP pro-
the control of MHC isoform transitions during duced by myosin ATPase, contributing to main-
regeneration. Hypothyroidism has been shown tain a locally high ATP : ADP ratio during periods
to inhibit the replacement of neonatal myosin of muscle contractions. Moreover, two additional
by adult fast myosin isoforms during regen- CK isozymes have been detected in mitochon-
eration; conversely, hyperthyroidism induces a dria, either specific for striated muscle, called
precocious induction of fast myosin expression mia-CK, or ubiquitous, mib-CK. These isozymes
play pivotal roles in high oxidative muscles

Lactate dehydrogenase activity in
by favouring phosphocreatine resynthesis from
regenerating skeletal muscle
oxidative phosphorylation (Ventura-Clapier et al.
1994). The activity and pattern of this enzyme is Lactate dehydrogenase exists in multiple mole-
of functional relevance since resistance to fatigue cular forms as a tetrameric association of two
is partly related to the ability of skeletal muscle to types of monomer subunits, known as H (heart)
sustain ATP levels through increased oxidative and M (muscle), which may be combined in
metabolism. five different ways and result in five isozymes. A
During myogenesis, there is a progressive correlation between the LDH isozyme pattern
increase in the total activity of CK, as well as a and the anaerobic/aerobic glycolysis capacity
shift from BB- to MM-CK isozyme. The onset of of muscle has been suggested. Heart contains a
the expression of the M-subunit of CK and the predominantly H type of LDH subunit, while
increase in the specific activity of the MM-CK fast glycolytic muscle contains the M type. The
isozyme have been correlated with the develop- LDH isozyme pattern of slow oxidative skeletal
ment of functional muscle. Moreover, the M-CK muscles is roughly mixed with equal specific
promoter is under the control of MyoD, one of activities of H- and M-subunits.
the most early MRFs, and the expression of the During the fetal development, there a shift
M-subunit is associated with that of other muscle- from the H toward the M-subunit, while the
specific protein isoforms encoded by genes specific activity of the M-subunit increases dur-
having an E-box sequence in their regulatory ing postnatal development (Plaghki 1985). A
regions. The developmental pattern of expres- marked decrease in the total activity of LDH has
sion of the various isozymes has been studied been reported early after muscle injury. There-
in the heart, where this multienzyme system after, the activity of total LDH increases from the
appears to be essential for the adaptation to fusion of precursor myogenic cells to myotubes.
increased metabolic demand (Hoerter et al. 1994). As for the expression of MHC isoforms, regen-
However, little is known about the expression of eration recapitulates the events that normally
mi-CK during the development of slow oxidat- occur during myogenesis, and the pattern of
ive skeletal muscle. LDH isoforms shifts from a predominance of
Skeletal muscle degeneration using bupiva- H-subunits toward M-subunits in regenerated
cain is associated with a marked decrease in slow muscles. Regenerated fast skeletal muscles
the total activity of CK (Plaghki 1985), and an recovered a LDH isoform pattern similar to that
increase in the specific activity of the BB-CK expected by 2 months after initial injury (Bigard
isozyme. The CK isozyme composition recovers et al. 2000).
a pattern similar to that of control muscle 10
days after initial injury (Sadeh et al. 1984). The
Practical consequences for
specific activity of mi-CK isozyme, linked to the
muscle healing
site of production of energy, is similar in control
and regenerated skeletal muscle 8 weeks after Treatment of muscle injuries varies widely de-
infiltration with a myotoxin (Bigard et al. 2000). pending on the nature and severity of the trauma.
However, the time-course of expression of mi-CK Besides the classic treatment of injured muscle,
during regeneration remains to be examined. different biological approaches can be used to
This issue is of importance in slow oxidative enhance muscle healing. Recent advances in
muscles because mi-CK located in the inner knowledge of the mechanisms of muscle degen-
mitochondrial membranes couples ATP syn- eration and regeneration after injury highlight
thesized during oxidative phosphorylation with the functional importance of the inflammatory
creatine formed during muscle metabolism to response and support the therapeutic potential
produce phosphocreatine. of several growth factors to improve muscle
healing. On the other hand, the physical activity regeneration by producing specific soluble factors.
pattern is an environmental factor known to Whether the rest, ice, compression and/or eleva-
affect muscle growth and maturation during the tion components of the principal therapy affect
early phases of regeneration. Therefore, it is of the inflammatory response to acute muscle injury
clinical interest to determine the specific effects has not been determined to date. Immobilization
of exercise on muscle healing. after muscle injury has been shown to limit the
amount of connective tissue, but it is likely that
this beneficial effect is not directly related to the
Initial inflammatory response to muscle injury
inflammatory response.
As discussed above, the injured muscle first
undergoes necrosis and is infiltrated by macro-
Growth factors and muscle healing
phages and neutrophils. Inflammatory cells are
important components of the successful repair of The activation of satellite cells, and their prolifera-
injured muscle. The early use of NSAIDs, which tion, differentiation into myoblasts and fusion
inhibit the function of macrophages and neutro- to form myotubes and myofibres are under the
phils, leads to a slower muscle regeneration control of many soluble factors such as growth
than in untreated animals (Almekinders & Gilbert factors (see above). Many growth factors inter-
1986). The impaired recovery in the muscles of act to control the involvement of inflammatory
treated animals was attributed to both the slow and satellite cells in the healing process, and
removal of cellular debris and the decrease in to regulate the reorganization of the basement
synthesis and release of soluble factors import- membrane and the extracellular matrix. Several
ant for the activation of regenerative processes studies have previously shown that individual
by macrophages. Because the early response of or combined growth factors play specific roles
inflammatory cells to muscle injury is a deter- during regeneration and therefore are able to
mining factor in directing muscle repair, there is improve muscle healing. The number and the
an argument for not using anti-inflammatory mean diameter of regenerating fibres increased
drugs during this period. It appears especially in muscles receiving serial and direct injections of
important to respect the inflammatory response bFGF and IGF-I in comparison with non-treated
to acute muscle injury, with the aim of protect- muscles, reflecting improved healing (Fig. 3.5)
ing the macrophage invasion, first to remove (Kasemkijwattana et al. 2000; Menetrey et al. 2000).
cellular debris and second to promote the involve- At 1 month, and in contrast with non-treated
ment of activated macrophages in muscle fibre muscles, regenerating myofibres were uniformly
Diameter of regenerating myofibres (μm)
70 70
60 60
50 50
40 40
Fig. 3.5 Changes in the mean
diameter of regenerating 30 30
myofibres when basic fibroblast
growth factor (bFGF) and 20 20
insulin-like growth factor I
(IGF-I) are used to improve 10 10
muscle healing after strain
injury (P < 0.05). (From 0 0
Kasemkijwattana et al. 2000.) bFGF Control IGF-1 Control
3
Fast-twitch strength (N·g–1)
2
2
1
1
0 0
(a) bFGF Control IGF-I Control
8 8
Tetanic strength (N·g–1)
6 6
4 4
Fig. 3.6 Effects of basic fibroblast

growth factor (bFGF) and insulin-
2 2
like growth factor I (IGF-I) to
improve: (a) fast-twitch strength,
and (b) tetanic strength after
0 0 strain injury (P < 0.05). (From
(b) bFGF Control IGF-I Control Kasemkijwattana et al. 2000.)
located in the deep and superficial parts of the However, it is unlikely that a treating physician
muscle treated with bFGF and IGF-I, their mean or a patient will accept repeated intramuscular
diameter was similar to the surrounding normal injections or implanted perfusion pumps, par-
fibres, and many of their nuclei were already ticularly with the infection risk. Thus, other
peripherally located. Moreover, the development approaches have be considered to achieve a sus-
of fibroblastic tissue was also reduced in treated tained expression of exogenous genes to skeletal
muscles, suggesting that muscle healing was muscle, such as myoblast transplantation or gene
accelerated in these muscles when compared with therapy based on viral and non-viral vectors. The
non-treated muscles. A significant improvement application of these emerging technologies to
in fast-twitch and tetanic strength was observed deliver sustained expression of growth factors in
15 days after injury in muscles treated with growth the injured muscle has been previously examined
factors (bFGF and IGF-I) when compared with (Kasemkijwattana et al. 1998). In this study, the
sham injected injured muscles (Fig. 3.6). Taken ability of recombinant adeno-associated virus to
together, these studies demonstrated that selected mediate direct and ex vivo the transfer of a marker
growth factors properly applied and injected gene (β-galactosidase) within the contused injured
within injured muscle are able to enhance muscle muscle, suggested that this biological approach
healing after injury. could be able to deliver an efficient and persistent
100 Intact muscle

Day 16, RGTA11–
Day 16, RGTA11+
80
Fig. 3.7 Percentage of slow
myosin heavy chain positive
Slow fibres (%)

fibres in transverse sections of 60
intact muscles and at day 16 of
regeneration, in the presence (+)
or in the absence (–) of dextran 40
*
derivatives (RGTA11). EDL,
extensor digitorum longus;
SOL, soleus; *, significantly 20
different from intact and
regenerated muscles in the
absence of RGTA11, P < 0.05. 0
(From Aamiri et al. 1995. EDL SOL
expression of selected growth factors. It is likely muscle that had regenerated in the presence of
that the development of those vectors carrying dextran derivatives showed a fourfold increase
selected growth factors and the delivery of growth in the number of slow fibres, in comparison with
factors, using such new technologies, represent muscle regenerating in the absence of dextran
potential strategies in improving muscle healing derivatives (Fig. 3.7). It is thus likely that dextran
that will be available for humans in the near derivatives act by protecting and favouring the
future. effects of heparin-binding growth factors (FGFs
and TGF-β) involved in the process of muscle
regeneration. This family of polymers may there-
Heparin sulphate proteoglycans and
fore open a new therapeutic approach to acceler-
muscle repair
ate skeletal muscle repair after injury.
Growth factors such as FGFs and TGF-β are trans-
mitted to the cell either by one tyrosine kinase
Physical exercise and muscle regeneration
receptor or by binding to low-affinity heparan
sulphate proteoglycans located on the cell sur- To determine the impact of physical exercise
face and in the extracellular matrix. As for other and contractile activity on muscle regeneration
growth factors, the interaction between them requires the use of animal models. A decreased
and the heparan sulphate components of the mechanical load after the removal of weight-
extracellular matrix might play a pivotal role in bearing activity impairs the rate and degree
regeneration. Selected dextran derivatives have of growth and maturation during regeneration
been shown to mimic some properties of heparin (Esser & White 1995). The degree of restoration
and heparan sulphate to stabilize and protect to control adult protein concentration values
heparin-binding growth factors such as FGFs and of regenerating muscle is markedly altered by
TGF-β. A single injection of a dextran derivative decreased mechanical load. Even the timing of
was found to improve the regenerative pro- transitional expression of MHC isoforms is
cess in a fast skeletal muscle after a crush injury delayed in unweighted regenerating muscles
(Gautron et al. 1995). Besides clear positive (Esser & White 1995; Bigard et al. 1997). There are
effects on the histological structure of regener- thus experimental data suggesting that growth
ated muscle, dextran derivatives were shown to and maturation are impaired by a decreased
accelerate the shift from the neonatal to adult mechanical load on regenerating muscles. On
MHC isoforms (Aamiri et al. 1995). Crushed slow the other hand, increased mechanical load by
ablation of synergistic muscles enhances the these growth factors stimulate the proliferation
growth of regenerated muscle but not matura- of satellite cells and concomitantly inhibit their
tion (Esser & White 1995). While ablation of syn- differentiation and fusion, except for IGFs, which
ergistic muscles is a model of chronic mechanical promote the differentiation of the myogenic pre-
overload, it is of interest to evaluate the specific cursor cells. TGF-β also plays an important role
influence of the metabolic component by exam- in muscle regeneration in promoting the reorgan-
ining the response of regenerating muscle to ization of the basement membrane and extra-
running exercise. The growth of damaged muscle cellular matrix components. The interaction of
and its oxidative capacity are improved by run those growth factors during muscle regeneration
conditioning. On the other hand, the response of requires further investigation. A better under-
the MHC composition to endurance training has standing of growth factor interactions and their
been shown to be more marked in regenerated role in the expression of myogenic regulators and
muscle, at least for fast MHC isoforms (Bigard extracellular matrix components is needed to
et al. 1996). Taken together, these results clearly identify specific growth factors or cytokines able
demonstrate that the removal of contractile act- to improve skeletal muscle repair. Exercise rest-
ivity and mechanical load have deleterious effects ing with increased contractile activity but without
on muscle growth and maturation. It is thus sug- mechanical overload is good advice in promot-
gested that muscular activity plays a key role in ing efficient muscle healing after damage. On the
the recovery of damaged skeletal muscle. other hand, the improvement of muscle healing
after injury may be enhanced by the develop-
ment of new technologies, such as gene therapy,
Conclusions
that may be able to deliver target proteins to the
Although studies using laboratory animals amply damaged muscle without systemic side effects.
demonstrate that skeletal muscle can regener-
ate after injury, our knowledge of muscle regen-
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Chapter 4
Tissue Healing and Repair:

Tendons and Ligaments
BARRY W. OAKES
matrix (Fig. 4.1). This new information indicates

Introduction
the possibility of intercellular ‘talk’ between cells
This chapter will briefly review recent basic similar to that of osteocytes and hence that these
scientific information on the structure and bio- tendon cells may be able to sense and coordinate
mechanics of tendons and ligaments, discuss a response to mechanical load or lack of load.
mechanisms of injury to ligaments/tendons and Mature adult ligament and tendon are com-
their repair response, and attempt to relate this posed of large diameter type I collagen fibrils
to practical clinical patient rehabilitation man- (150 nm or more in diameter) tightly packed
agement. Several recent, excellent reviews are together in a rope-like configuration with a
available in this area: Benjamin et al. (1986, 1995), small amount of type III collagen dispersed in
Daniel et al. (1990), Kannus et al. (1992a, 1992b), an aqueous gel containing small amounts of
Jackson et al. (1993), Archambault et al. (1995),
Benjamin and Ralphs (1995), Viidik (1996), Frank
and Jackson (1997), Jozsa and Kannus (1997),
Frank (1999), Frank et al. (1999), Rodeo and Izawa
(1999) and Woo et al. (2000).
Structure and biomechanics of

ligaments and tendons
There are subtle differences between ligament
and tendon morphology (Amiel et al. 1983) but for
the sake of this discussion they will be treated as
very similar tissues.
The fibroblasts of mature tendons lie in lon-
gitudinal rows and are flat, very elongated cells
squeezed laterally between the collagen fibrils.
Recently McNeilly and associates (1996) have
demonstrated elegantly (using confocal micro-
scopy coupled with fluorescent dye cellular Fig. 4.1 Confocal microscope image of fluorescent
labelling techniques) that tendon fibroblasts membrane-labelled cryosections of a rat digital flexor
tendon. The cell bodies are brightly fluorescent and
communicate with one another via an extensive show a network of fluorescent lateral cell processes
three-dimensional network of long cell processes meeting those of adjacent cells. (From McNeilly et al.
and gap junctions ramifying between the collagen 1996, with permission from Journal of Anatomy).
56
repair of tendons and ligaments 57
proteoglycan and elastic fibres. (Figs 4.2 and 4.3).

The outstanding feature of both these unique
load-bearing tissues is the collagen ‘crimp’,
which is a planar wave pattern found extend-
ing in phase across the width of all ligaments
and tendons (Fig. 4.4) (Diamant et al. 1972). This
collagen ‘crimp’ appears to be built into the
tertiary structure of the collagen molecule and
is probably maintained in vivo by inter- and
intramolecular collagen cross-links as well as
a strategically placed elastic fibre network. The
‘crimp’ may help to attenuate muscle loading
forces at the tendoperiosteal junction as well as
at the musculotendinous junction.
Viidik (1996) has recently reviewed the basic
biomechanics of ligaments and tendons and the
reader is referred to this text for a more detailed
examination of structure–function relationships.
The basic function of tendons and ligaments is to
transmit force with ‘reasonable safety margins’
(Viidik 1996). The longitudinal array of collagen
fibrils converts externally applied axial loads
to internal lateral compression which results in
Fig. 4.2 Adult rat ACL collagen fixed with ruthenium interfibril friction and heat generation. This heat
red after treatment with elastase at pH 8.8. for 12 h. generation may be responsible for central fibro-
There is typical regular banding periodicity (labelled) blast death in thick tendons, which has recently
and linking filaments probably hyaluronate, which
been described as exercised-induced hyper-
link the fibrils between the c and d bands. The fibre
marked with the asterisk appears to be dividing into thermia (Wilson & Goodship 1994). Peak intra-
a smaller fibril. Proteoglycan granules are attached tendinous core temperatures in the range of
to the fibrils in the region of the c and d bands. 43–45°C have been recorded in race horse
(Magnification × 98 000.) tendons. Temperatures greater than 42.5°C are
known to cause fibroblast death in vitro.
Also of interest is the notion that the muscle–
By weight tendon unit can act as a spring and the tendon
can recoil after being eccentrically stretched, for
Water example during the landing phase of a hopping
kangaroo. During this landing phase the tendon
Dry stretch of the Achilles tendon is stored as elastic
Other energy which is then converted to add extra lift
Proteoglycans for the animal during the concentric phase of
Elastin the hop and hence leads to energy conservation
Collagen
(Morgan et al. 1978; Proske & Morgan 1987).
Indeed, in the slowly hopping wallaby, strain
energy storage in tendons and ligaments accounts
Fig. 4.3 Approximate amounts of main
tendon/ligament components by weight. Collagen
for 33% of the negative and positive work that is
forms the main protein component of the dry weight done whilst the feet are on the ground (Ker et al.
with smaller amounts of elastin and proteoglycans. 1986)!
Size scale
Tropocollagen 15 nm
X-ray
35 nm
Microfibril X-ray EM
35 nm staining sites
100–200 nm
Subfibril X-ray EM
Fibril 500–5000 nm
640 nm periodicity
X-ray EM SEM
Fibroblasts
Fasicicle 50–300μm
EM SEM OM
Planar waveform SEM OM

or crimp structure
Endotenon or
Fascicular membrane 100–500μm
Paratenon or
Reticular membrane
Fig. 4.4 Structural organization

of tendon and ligament. Note the
Tendon planar ‘crimp’ seen at the light
microscopic level. (Adapted
from Kastelic et al. 1978.)
Ligament and tendon injury can be closely cor- irreversible ligament/tendon elongation occurs
related with the load–deformation curve (Butler due to partial rupture of intermolecular cross-
et al. 1979; Oakes 1981). The load–strain curve can links. As the load is increased further intra- and
be divided into three regions (Fig. 4.5): intermolecular cross-links are disrupted until
1 The ‘toe’ region or initial concave region repres- macroscopic failure is evident clinically. Electron
ents the normal physiological range of ligament/ microscopic studies (Viidik & Ekholm 1968) have
tendon strain up to about 3–4% of initial length, shown the collagen fibrils are elongated in this
and is due to the flattening of the collagen ‘crimp’. phase and the periodicity increases from 67–
Repeated cycling within this ‘toe region’ or 68 nm to 72 nm and the banding pattern may
‘physiological strain range’ of 3–4% (which may become disjointed across the fibrils indicating
be up to near 10% in cruciate ligaments due to the intrafibril damage by molecular slippage under
intrinsic macrospiral of collagen cruciate fibre shear strain (Kastelic & Baer 1980). With con-
bundles) can normally occur without irreversible tinued loading into the third region, the band-
macroscopic or molecular damage to the tissue. ing pattern is completely lost and in immature
2 The second part of the load–deformation collagen no free ends are seen ultrastructurally.
curve is the linear region where pathological This suggests that damaged fibrils can still bear
Rupture this is a rough guide to the clinical severity of

the injury.
3 In the third region, if continued loading occurs,
the linear part of the curve flattens and then the
yield or failure point is reached at 10–20% strain,
depending on the ligament/tendon fibre bundle
Linear macro-organization. In this region, complete
Load
ligament tendon rupture occurs at ‘maximal

breaking load’ and this is the dangerous grade
3 ligament rupture seen on clinical testing. It
is ‘dangerous’ because the athlete has severe
momentary pain when the trauma is applied
and then little pain, and the athlete (and often
Toe inexperienced examiners) erroneously believe
the injury is trivial and treat it as such with dis-
0 4 10 astrous consequences.
Deformation (strain) (%) Tendons and ligaments behave as non-linear
elastic materials. Viscous and plastic behavi-
Normal physiological range our become obvious when cyclical loading–
1° Tear (mild) unloading protocols are used during laboratory
tensile testing. The laboratory testing protocols
2° Tear (moderate) can be similar to the cyclical loading imposed on
3° Tear rupture (severe) tendons and ligaments during running. During
such cyclical testing the load–strain curves
Fig. 4.5 Load–deformation (strain) curve for initially have a large hysteresis loop and as the
ligament/tendon and the clinical correlation with the
cycles progress with time this hysteresis loop
grading of the injury. The ‘toe’ region of the curve is
entirely within the normal physiological range; more is lost; this is thought to be due to squeezing of
than about a 4% strain causes tissue damage. water from the tissue and concurrently aligning
the collagen fibrils along the axis of loading. This
‘preconditioning’ cycling could be thought of as
load and may represent a form of work harden- an important part of the warm-up procedure in
ing. In mature tendon, ruptured collagen fibril athletes and is reversible during the non-running
ends can be observed. Elegant X-ray diffraction period as water and proteoglycans redistribute
and electron microscopic studies, coupled with amongst the non-loaded fibrils. If, whilst cycling
accurate fast and slow loading studies, of both testing a specimen of tendon in the laboratory,
rat tail and human finger tendons has confirmed the cycling is stopped two further protocols can
that initial damage to the fibril is an intrafibrillar be used. If the stress is kept constant by slowly
sliding process that occurs only a few milliseconds increasing the strain, a creep phenomenon results.
before macroscopic fibre slippage occurs (Knorzer If the strain or deformation is kept constant by
et al. 1986). The early part of the linear region increasing the load slowly, stress–relaxation of
corresponds to mild ligament tears or grade 1 the tissue occurs (Viidik 1996).
ligament tears (0–50% fibre disruption) and the An enormous amount of research has been
latter part to grade 2 (50–80% fibre disruption) performed on the biomechanical properties of
where there is obvious clinical laxity on stress the human knee ligaments, with the anterior
testing. Grade 1 and 2 injuries always have some cruciate ligament (ACL) dominating research
pain after the initial trauma, and usually with a because of its key role in anteroposterior stability
grade 2 injury the athlete cannot continue and of the knee. Rotational injury to the knee with the
foot fixed, as well as hyperextension of the knee,

appear to be the two key mechanisms involved
in human ACL disruption. Forces of the order of
2000 N are required to disrupt the ACL and are
even higher for the posterior cruciate ligament
(PCL). Direct falls onto the tibia or collisions with
opponents, such that a posterior displacement
force of the tibia occurs on the femur, appears to
be a common mechanism for PCL injury. Col-
lateral ligament injury involves excessive varus,
valgus or rotational forces. The ligament–bone
junction with its special fibrocartilage transi-
tion zone is a common region of clinical failure.
Recent experimental animal studies indicate that
ligament mid-substance strain is much lower
than at the insertion sites and this appears to be
due to a differing collagen-fibre crimp amplitude
and angle. This higher strain at the insertion sites,
together with ligament insertion geometry, could Fig. 4.6 The attachment zones studied are the
be an explanation of preferential failure of some insertion of the quadriceps (QT), the origin (OPL)
ligament insertion sitesaespecially the femoral and the insertion (IPL) of the patellar ligament. The
angles between the long axis of tendon or ligament
attachment of the medial collateral ligament of
and bone are α, β and γ. The change in these angles is
the knee, which has an almost 90° insertion into quite large during knee motion. The subdivision of
the region of the medial femoral epicondyle each attachment site into regions X, Y and Z and the
compared with its tibial periosteal insertion. major differences in the quantities and distribution
of uncalcified fibrocartilage (UF) are illustrated
diagrammatically in the drawings to the right of the
Ligament/tendon insertion to bone figure. B, bone; F, femur; P, patellar ligament; T, tibia.
(From Benjamin & Evans 1990, with permission from
Benjamin and his co-workers (Benjamin et al. 1986, Journal of Anatomy).
1995; Benjamin & Evans 1990; Evans et al. 1990;
Benjamin & Ralphs 1995) have recently studied
extensively tendon–bone junctions where the the Achilles tendon with some evidence of repair
fibrocartilage interface or enthesis exists between and also transverse tears at the bone–tendon
the tendon and the bone. The width of this junction that were filled with fat cells and no
unique fibrocartilage interface, they hypothesize, repair tissue (Rufai et al. 1995), which Frank et al.
is dependent upon the relative degree of move- (1999) recognize as mechanical ‘flaws’ during
ment that occurs between the tendon and its tendon repair (see below).
bone attachment (Fig. 4.6). They suggest that the
enthesis prevents collagen fibre bending and
Correlation of collagen fibril size with
perhaps undergoing shearing, fraying and fail-
mechanical properties of tissues
ure at this special junction region. They have
found the thickest fibrocartilage interface in the Parry et al. (1978) have completed detailed quant-
very mobile Achilles tendon and a lesser thick- itative morphometric ultrastructural analyses of
ness of this interface in tendons such as the tib- collagen fibrils from a large number of collagen-
ialis anterior posterior and very little in the long containing tissues in various species. They came
flexor tendons (Frowen & Benjamin 1995). It is of to a number of conclusions that can be summar-
interest that they observed longitudinal splits in ized as follows:
180
160
Collagen fibrils diameter (nm)

140
120
Separation force (N)

100 38
34
80 30
Fig. 4.7 Increase in diameter 26
60 22
of collagen fibrils (full curve
through mean diameters with 18
40 14
bars representing the largest
and smallest fibrils) and tensile 10
20
strength (dashed curve) with 6
age in the growing rat ACL. 2
Both curves reach a plateau at 0 2130 60 90 120 150 180
about 90 days postconception Age (days)
or about 70 days after birth. Birth
1 Type 1-orientated tissues, such as ligament and two curves closely coincide, indicating a close
tendon, have a bimodal distribution of collagen correlation between the size of the collagen fibrils
fibril diameters at maturity. and the ultimate tensile strength of the ACL as
2 The ultimate tensile strength and mechanical has been suggested by Parry et al. (1978). This
properties of connective tissues are positively rapid increase in collagen fibril size over 6 weeks
correlated with the mass average diameter of in the growing rat is not seen during normal
collagen fibrils. In the context of the response ligament tissue repair or remodelling (Matthew
of ligaments to exercise they also concluded that et al. 1987; Oakes et al. 1991).
the collagen fibril diameter distribution is closely Work by Shadwick (1986, 1990) has also demon-
correlated with the magnitude and duration of strated a clear correlation between collagen fibril
loading of tissues (Fig. 4.7). diameter and the tensile strength of tendons. He
determined that the tensile strength of pig flexor
tendons was greater than that of extensor ten-
Collagen fibril diameter quantification with
dons and that this greater flexor tendon tensile
age and correlation with ACL tensile strength
strength was correlated with a population of
Oakes (1988) measured collagen fibrils at various larger diameter collagen fibrils not present in the
ages of the rat from 14 days fetal to 2-year-old weaker extensor tendons. Also, studies by Oakes
senile adult rats. The mean diameter and the et al. (1998), using the rabbit patellar tendon, have
range of fibres from the largest to the smallest for demonstrated a high correlation between the
each time interval were plotted against age and area-weighted mean collagen fibril diameter
are shown in Fig. 4.7. The mean fibril diameter (this method adjusts for the varying numbers of
begins to plateau at about 7 weeks after birth. large and small fibrils within a tendon) and both
Also plotted on this figure is the separation force modulus (R = 0.79) and ultimate tensile strength
required to rupture the ACL in the rat with age. (R = 0.63) (Fig. 4.8).
Special grips were used in this study to obviate It should be noted here that the original large
epiphyseal separation and 70% of the failures collagen fibrils seen in normal tendons and liga-
occurred within the ACL. It can be seen that the ments are not replaced after ligament/tendon
80
Ultimate tensile strength (Mpa)
r=0.63
70
60
50
40
30
20
10
0
0 50 100 150 200 250 300
(a) Area-weighted mean diameter (nm)
Fig. 4.8 Area-weighted mean
400 collagen fibril diameter (nm)
r=0.79
350 across full width of rabbit patellar
tendon versus (a) patellar tendon
300 ultimate tensile strength, and
Modulus (MPa)
250 (b) patellar tendon modulus.

200 (a) The good correlation (r = 0.63)
should be noted and indicates an
150 important relation between mean
100 collagen fibril size and tensile
properties of tendons. (b) The
50
excellent correlation (r = 0.79)
0 indicates mean fibril diameter and
0 50 100 150 200 250 300 material properties are closely
(b) Area-weighted mean diameter (nm) related. (From Oakes et al. 1998.)
rupture or injury and this is the probable explana- cent boys), muscle fatigue and inadequate
tion for the poor material properties of repair muscle skills. It is also clear that most muscle
scars even 1 year after repair. They are also not injuries occur in the lower limb and most involve
replaced when ligament replacements are used two-joint muscles such as the hamstrings and the
as scaffolds, such as for the reconstruction of the rectus femoris, probably because of the complex
knee ACL when autograft or allograft tendons reflexes involved in simultaneous co-contraction
are used. This is a major explanation for the high and co-relaxation (Oakes 1984). An excellent
failure rate of such knee ACL reconstructions, review of current knowledge of muscle strain
apart from any surgical misadventure (see below injuries has been published by Garrett (1996).
for further discussion). Recently, Hartig and Henderson (1999) have
clearly demonstrated that increased hamstring
flexibility decreased lower limb overuse injuries
Basic biomechanics of tissue injury
in military basic trainees.
Both concentric and eccentric muscle–tendon
Muscle–tendon–bone injury
unit loading can cause muscle–tendon–bone
The basic causes of intrinsic muscle injury are junction injury. The use of eccentric muscle load-
still not entirely clear, but have been attributed ing to cause increased muscle hypertrophy, as
to inadequate muscle length and strength (for against the use of more conventional concentric
example tight hamstrings, especially in adoles- loading, has led to the phenomenon of eccentric
muscle soreness which is now known to be due in or arthroscopic patellar tenotomy, revealed that
part to muscle sarcomere disruption at the Z-lines about 40% of subjects could not return to their
(Friden et al. 1983). Eccentric muscle–tendon– previous level of sporting activity and that with
bone load can generate more force than concen- either form of patellar tenotomy could expect little
tric contractions and may be the mechanism by improvement in symptoms beyond 12 months
which the patellar tendon and its attachments postoperatively. In this study those patients that
lead to tendoperiosteal partial disruptions at both achieved postsurgical sporting success appeared
the superior and inferior poles of the patellar. to have an 80% chance of having prolonged
Studies by Chun et al. (1989) demonstrated that success. There was no difference in outcomes
the inferomedial collagen fibre bundles of the between the open or arthroscopic procedures
human patellar tendon, when subjected to (Coleman et al. 2000).
mechanical analysis, fail at loads which are much
less than the lateral fibre bundles. The biological
Muscle–tendon junction injury
reasons for this are not clear at the moment but it
helps to explain the prevalence of inferomedial Failure at this junctional region is common. There
tenderness, which is such a common cause of is an increased muscle cell membrane folding of
anteromedial knee pain or ‘jumper’s knee’. the terminal end of the last muscle sarcomere that
The bone–tendon junction or enthesis is one of has important mechanical implications for reduc-
the commonest sites for tissue injury, as is seen ing the stress at this critical junctional region. It
with the classic infrapatellar tendonitis which is has been determined that a typical vertebrate fast-
so refractory to treatment. Benjamin et al. (1986) twitch cell can generate about 0.33 MPa of stress
have suggested that the zone of fibrocartilage across the cell. The stress placed on the cell’s
at the enthesis minimizes local stress concentra- junctional complex at the muscle–tendon junction
tions and appears to be characteristic of tendons by the complex folding of the terminal sarcomeres
and ligaments where there is a great change experiences a maximal stress of 1.5 × 104 Pa,
in angle between the tendon or ligament and which is much less than 33 × 104 Pa, and this
bone during movement. It is of interest that the difference may determine whether mechanical
enthesis which gives the most problems in the failure occurs at this junctional region.
clinic (the inferior patellar pole and the patellar With muscle injury at this junctional site it
tendon) is the one with the least thickness of is probable that the complex sarcomere muscle
fibrocartilage (see Fig. 4.6). It is possible that a membrane infoldingato increase the surface area
major mechanism of failure at this very mobile and hence decrease substantially the stressais
enthesis may be collagen fibril shear. probably not reproduced following repair and
A study by Cooke et al. (1997) found that more this may be an explanation for the reccurence
than one-third of athletes with patellar tendino- of tears at this junction in athletes. A detailed
pathy were unable to return to sport for more comprehensive review has been published by
than 6 months because of recurrent or persistent Noonan and Garrett (1992). Kannus et al. (1992a)
pain and eventually required surgery, indicating (Kvist et al. 1991) have demonstrated in the rat
the difficulty of the reformation of a normal load- that type II (fast-twitch) fibres have a more com-
bearing enthesis after repeated tension–avulsion plex folding pattern than the type II (slow-
injury. Also it was clear from their studies that twitch) fibres. The type II fibres have an increase
imaging such as ultrasonograms and magnetic of 30–40% in contact surface area compared to
resonance imaging (MRI) scans do not always the type I fibres. In this way the larger forces
correlate with the clinical and histopathological transmitted via the myotendinous junction with
findings (Khan et al. 1998). type II muscle can be transmitted through this
A recent detailed study of chronic patellar junction without increasing the force applied per
tendinopathy treated surgically by either open surface unit of the junction (Fig. 4.9).
of 43.3°C and a maximum of 45.4°C in one

animal. They suggest these core temperatures or
T central tendon hyperthermia are not survivable
by tendon fibroblasts and may explain the central
lesions seen in the equine superficial digital flexor
tendon and also in the human Achilles tendon.
P Spontaneous tendon rupture is uncommon
in the young athlete and usually occurs in the
older sportsman (for example the long head of
the biceps brachii) and then is usually associ-
ated with degenerative pathology of the collagen
fibrils, although the biochemical detail has not
been delineated.
M Supraspinatus tendon rupture is common with
ageing and may be related to a decreased tendon
cross-sectional area and also to increased stiffness
of the tissue with increased collagen cross-links.
Fig. 4.9 Schematic figure of the ultrastructure of This increased ‘stiffness’ may be further aggrav-
the myotendinous junction. Dotted arrow, lamina ated by matrix changes such as fibrocartilage
lucida of the muscular basement membrane; solid transformation and frank intratendinous calcifica-
arrow, lamina densa of the muscular basement
tion. Recently, Katayose and Magee (2001) have
membrane; M, muscle cell; P, muscle cell processes;
T, tendon collagen fibrils. (From Kannus et al. 1991, performed an elegant and detailed study of the
with permission.) cross-sectional areas (CSAs) of the normal domin-
ant and non-dominant supraspinatus tendon as a
function of age using diagnostic ultrasound with
a high level of interobserver reliability. They found
Tendon injury
that the CSA of the dominant side was signific-
Tendon injury in sport is common because of antly larger than the non-dominant side and that
the large loads applied. Komi (1987) has meas- the CSA decreased significantly with ageing. They
ured the high forces generated in the human noted that the CSAs of the 70–79-year age group
Achilles tendon with the surgical introduction of were 82% of those in the 20–29-year age group.
a calibrated buckle transducer for short periods
of time. Forces of up to 4000 N were recorded
Ligament/tendon repair
in the Achilles tendon with toe running. Thus it
is not surprising that with repetitive loadings There are three main phases of ligament/tendon
of these magnitudes microfatigue failure could repair: inflammation, repair (or proliferation)
occur with long-distance running, especially in a and remodelling (see Figs 4.10–4.14).
tendon of small cross-sectional area (Engstrom
et al. 1985). Studies by Hasselman et al. (1995)
Acute inflammation
indicate that the proximal tendon of the rectus
femoris extends well distal into the muscle belly, The gap in the ligament/tendon is filled immedi-
and tears at this muscle–tendon junction can ately with erythrocytes and inflammatory cells,
appear as mid-muscle belly haematomata. especially polymorphonuclear leucocytes. Within
Wilson and Goodship (1994) have demon- 24 h, monocytes and macrophages are the pre-
strated a rise of the core temperature of the dominant cell and actively engage in phagocytosis
equine superficial digital flexor tendon under of debris and necrotic cells. These are gradually
galloping conditions to a mean peak temperature replaced by fibroblasts from either intrinsic or
Inflammation
phase
Repair Remodelling
phase phase
Injury
of response
Intensity
0 3 4 11 days 6 weeks 6 months
Myofibroblasts
Fig. 4.10 The three phases of Endothelial cells (EDGF)
healing and the cells involved. Fibroblasts
EDGF, endothelium-derived Polymorphonuclear leucocytes,
growth factor; MDGF, monocytes, lymphocytes,
macrophage-derived growth mast cells and macrophages
factor; PDGF, platelet-derived Erythrocytes
growth factor. Megacaryocytes platelets, PDGF, MDGF, etc.
extrinsic sources and the initial deposition of the weeks). Type I collagen now begins to predomin-
type III collagen scar is commenced. At this stage ate and GAG concentration remains high. The
collagen concentration may be normal or slightly increasing amount of scar collagen and reducible
decreased but the total mass of ligament colla- cross-link profile has been correlated with the
gen scar is increased. Glycosaminoglycan (GAG) increasing tensile strength of the ligament matrix.
content, water, fibronectin and DNA content are Recent quantitative collagen fibril orientation
increased (Fig. 4.11). studies indicate that early mobilization of a
ligament at this stage (within the first 3 weeks)
may be detrimental to collagen orientation. After
Proliferation
this time there is experimental evidence that
Fibroblasts predominate in this phase. Water mobilization increases the tensile strength of the
content remains increased and collagen content repair and probably enhances this phase and
increases and peaks during this phase (3–6 the next phase of remodelling and maturation
3
Normalized values
2 Type III collagen
Glycosaminoglycans
Type I collagen
Fig. 4.11 Ligament repair during 1 DNA
the phases of healing and the Water
‘normalized’ content of type I
and III collagen, water, DNA
and glycosaminoglycans.
Inflammatory Remodelling
(From Andriacchi et al. 1988, 0
with permission.) Normal Proliferative
0 hours 24 hours 3–6 weeks
Immediate Acute Mobilization

postinjury inflammatory collagen
ligament response repair &
rupture (2º) remodelling
= orientated
H2O Compression load-bearing
repair
without
ICE adhesions
H2O RICE
(a)
Immediate No rice, No rice & early

postinjury uncontrolled exercise, bulky,
ligament H2O bleeding & painful scar
rupture (2º) oedema collagen with
adhesions
Pain
H2O
(b)
Fig. 4.12 Ligament repair: (a) with and (b) without RICE (rest, ice, compression and elevation) management and
early mobilization.
(Figs 4.12 and 4.13) (Vailas et al. 1981; Hart & quadriceps muscle bulk. Patients are now usually
Danhers 1987; Woo et al. 1987b). mobilized in a limited motion cast for 3–6 weeks
With this basic biological knowledge there is rather than the previously empirical time of
now a rationale for the use of early controlled 6 weeks. An initial range of motion of 20–60° of
mobilization of patients with ligament/tendon flexion is used because this places minimal load-
trauma. The use of a limited motion cast with an ing on all knee ligaments (Helbing & Burri 1977).
adjustable double-action hinge for the knee joint The beneficial effects of functional tendon cast-
is now clinically accepted and enhances more ing versus rigid casting has also been recently
rapid repair and remodelling as well as preserving demonstrated in a rabbit Achilles tenotomy model
Immediate No No stretching
postinjury RICE No exercise
Moderate (2º) Bulky, painful
muscular repair with
tear adhesions
24 hours 3–6 weeks
Stretching
and exercise
Ice Orientated
stronger
painless
repair
RICE
Fig. 4.13 Muscle repair at the muscle–tendon junction with and without RICE (rest, ice, compression and
elevation) management and early mobilization.
that demonstrated a 60% increase in tendon col- synthesis. Water content returns to normal and
lagen and a 20% increase in maximum load and collagen concentration returns to slightly below
maximum stress compared with control rigid casts normal, but total collagen content remains slightly
when measured 15 days’ post-tenotomy (Stehno- increased. With further remodelling there is a
Bittel et al. 1998). Such basic science studies have trend for scar parameters to return to normal but
led to the earlier mobilization of human Achilles the matrix in the ligament scar region continues
tendons after surgical repair (Mandelbaum et al. to mature slowly over months or even years. Scar
1995; Aoki et al. 1998; Speck & Klaue 1998). collagen matrix and adjacent normal matrix may
actually shorten the repair region, perhaps by inter-
action of ligament/tendon myofibroblasts with
Remodelling and maturation
their surrounding collagen matrix (Danhers et al.
(6 weeks to 12 months)
1986). Collagen fibril alignment in the longitudinal
During this phase there is a decrease in cell num- axis of the ligament occurs even though small-
bers and hence a decreased collagen and GAG diameter fibrils are involved (Figs 4.14 and 4.15).
Stress
for the clinician in that they are often intractable
C
to reasonable short-term management although
Stanish et al. (1986) claim good clinical results from
B graded eccentric loading regimes for patellar
A tendonitis. The author has examined Achilles
A B C tendon biopsies of patients with chronic localized
Strain tears and more generalized thickened, tender,
chronic Achilles tendons. The feature which
Fig. 4.14 The effect of collagen repair with identical characterized the pathology ultrastructurally
fibrils but different geometry and the corresponding
was the persistence of small-diameter collagen
load–strain response to tensile testing. (Adapted from
Viidik 1980.) fibrils < 100 nm diameter. The large fibrils of the
original tendon do not appear to be replaced in
the mature adult in either a repairing tendon or
Occasionally calcium apatite crystals will be ligament (Fig. 4.15) (see below); increasing the
deposited in the damaged tissues and the classic collagen fibril diameters (and their alignment) is
site for this to occur is in the rotator cuff supra- needed to enhance the repair scar tensile strength.
spinatus tendoperiosteal attachment to the greater ACL injuries appear to be unique in that the
tubercule of the humerus. chondrocyte-like cells in this special ligament
Achilles tendon and infrapatellar tendon in- apparently have a limited capacity to proliferate
juries, especially partial tears, present a dilemma and synthesize a new collagen matrix and hence
1400
1200
Number of fibrils
1000
800
600
400
200
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
(a) Diameter X 150 nm
40
Area/diameter group (%)
35
30
25
20 Fig. 4.15 (a) Number of fibrils
15 versus fibril diameter in patients
with chronic Achilles tendonitis;
10
(b) expressed as per cent area
5 occupied for each diameter
0 group versus diameter. The
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 preponderance of small-diameter
(b) Diameter X 150 nm fibrils in ‘repairing’ chronic
Achilles tendonitis should be
Normal tendo Achilles Chronic Achilles tendonitis noted. The large-diameter normal
fibrils > 100 nm are not replaced.
200
Right/left UTS (%)

100
*
0
12 weeks 24 weeks 1 year 3 years
(b) (n=3) (n=3) (n=3) (n=2)
Time postsurgery
Fig. 4.17 The mean and standard deviations of

normalized (right/left ratio) percentage ultimate
tensile strength (UTS) for the posterolateral bundles
of hemisected ACLs at intervals after surgery.
*, significantly different from 3-year results. (From
Ng et al. 1996b, with permission from American Journal
(a) (c) of Sports Medicine.)
Fig. 4.16 The operative procedure for a

hemitransection injury to the ACL. (a and b) period, but the ultimate tensile strength and stiff-
A medial arthrotomy is performed and the patella ness at 3 years were significantly higher than at
is displaced laterally; a probe is inserted to separate 12 weeks (P < 0.05). Failure started at the repair
the anteromedial and posterolateral bundles. (c) The site for the 12-week group, but at 24 and 52 weeks
posterolateral bundle is completely severed, leaving
the failure occurred through the ligament. At
the anteromedial bundle intact as an internal splint,
and a black silk suture is placed on the anteromedial 3 years, the posterolateral bundle specimens
bundle opposite the cut level as a marker of the failed by bony avulsion, indicating the repaired
incision site. (From Ng et al. 1996b, with permission tissue was not the weakest link of the bone–
from American Journal of Sports Medicine.) ligament–bone complex.
This study showed that under the favourable
repair appears to be limited. Collagenase release biological conditions of the experiment, partial
may also affect the effectiveness of the repair ACL injuries in the goat are capable of adequate
process (Amiel et al. 1989). However Ng et al. mechanical repair. What is more important, the
(1996a, 1996b) have completed a long-term high ultimate tensile strength and stiffness of the
biomechanical study of the repair of the goat 3-year repaired tissue indicate that full structural
ACL after hemisection injury showing that, con- repair of such an artificial transection injury is
trary to the current orthopaedic dogma, the ACL possible (Figs 4.16–4.18).
can heal even after partial tears. To test the
healing capacity of the partially torn ACL, liga-
Clinical and ultrastructural
ments were tested at 12, 24 and 52 weeks and
observations of Achilles tendon
3 years after surgery (Fig. 4.16). As early as 12
injuries
weeks after surgery, a translucent fibrous tissue
covered the transected posterolateral bundle. In this section I will attempt to relate the three
A comparison of anteroposterior laxity between phases of healing of soft tissues with that seen in
the right and left knees measured at 45 and 90° Achilles tendon injuries. Achilles tendon injuries
of flexion showed no significant difference at can be classified as described above for ligament
each time period. Results of Instron testing of the injuries, i.e. grades 1–3 with the latter being com-
posterolateral bundle revealed that normalized plete rupture. Several patient histories will be
changes in load–relaxation and Young’s modulus used to illustrate these three phases of healing
were also not significantly different at each time and attempted repair.
Injury
Fibroblast activity increase
Fibroblast
feedback loop
New collagen deposition,

cross-linking and remodelling
Fig. 4.18 The hypothetical
feedback loop mechanism of
collagen deposition control
during ligament repair. (From
Scar size increase and stiffness Ng et al. 1995, with permission
Functional
increase but material strength is from Journal of Orthopaedic
loading
inferior to preinjury level Research.)
Grade 3: complete rupture
Australian Rules football rover, aged 26, powering

off to avoid an opponent. Clinical signs were a
palpable defect in the Achilles tendon as well as
a positive Thompson’s sign. A biopsy was taken
during surgical repair.
With this disastrous injury there is both col-
lagen bundle failure as well as vascular dis-
ruption and hence bleeding is a feature of these
injuries when seen at early surgical repair. This
trauma to the tendon initiates the acute inflam-
matory phase and hence microscopically there
is massive red cell extravasation, fibrin clot
formation and collagen fibril disruption. The
damaged tendon becomes oedematous and poly-
morphonuclear monocytes migrate into this area
and release their lysosomal contents as well as
actively phagocytosing cellular and other debris.
Macrophages also move into the rupture site
and commence phagocytosis of damaged cells
and tissue. This phase lasts 0–72 h or so and is
Fig. 4.19 Light micrograph of an acute Achilles
followed by the repair phase (Fig. 4.19).
tendon rupture at 1 week postinjury, showing red
cells extravascular together with many polymorphs
and macrophages. (Epon-araldite, Azure A-Methylene
Grade 2: tear
blue.) Australian Rules football ruckman with 6 months’
painful thickened Achilles tendon. The operation
involved the excision of paratenon and tendon
incision to remove damaged, haemorrhagic and
phase and lasts 72 h to 4–6 weeks; but in this

patient the repair phase had been perpetuated
because of continued activity by the athlete. In
other patients where there is less florid tendonitis
and the tendon is clinically painful but not obvi-
ously enlarged, discrete areas of increased cel-
lularity are seen in the tendon in the form of free
red cells, cell debris and viable fibroblasts sur-
rounded by both large- and many small-diameter
collagen fibres. These areas are almost ‘walled-
off’ from the densely packed collagen of the rest
of the tendon by a fibrin precipitate. These dis-
crete areas are probably due to collagen fibre
ruptures or microtears corresponding to the early
part of the second region of the load–deformation
curve. There is as yet no evidence that the use
of massage or deep friction enhances this repair
phase (Walker 1984).
Grade 1: injury
Runner, aged 25, with a painful tender lump in the

Achilles tendon for 18 months! A biopsy was obtained
Fig. 4.20 Light micrograph of an acute Achilles
at open operation.
tendon grade 2 partial tear after 6 months of pain and
swelling. The tendon is oedematous and very cellular The lump at operation was firmer than the rest
and the fibroblasts are dilated with enlarged rough of the tendon and was slightly darker in colour.
endoplasmic reticular indicative of active collagen On light microscopy of the biopsy taken from
synthesis. (Epon-araldite, Azure A, Methylene blue.) the nodule, the changes in the collagen bundles
were very subtle. There was less regular ‘crimp-
necrotic regions. A biopsy was taken for light ing’ of the collagen bundles and they were not
and electron microscopy. as tightly packed. However, ultrastructually the
Light microscopy demonstrated a thickened cause of this less regular collagen crimp was
paratenon and an oedematous thickened tendon obvious in that between the large-diameter fibrils
(Fig. 4.20). Ultrastructurally many fibroblasts had were many small-diameter fibrils that were
dilated rough endoplasmic reticulum and pro- less well orientated longitudinally (Fig. 4.15).
minent nucleoli indicative of increased collagen These tendons were interpreted as being in the
synthesis. Apart from the many free red cells, the remodelling phase as there were no increased
other feature was the prevalence of many small- fibroblast numbers in the nodules and no inflam-
diameter collagen fibrils not aligned or closely matory cells were observed (Fig. 4.15).
packed (18–20 nm diameter) in amongst the older,
larger, pre-existing fibrils ranging from 80 to The mechanism of acute complete rupture in
150 nm diameter. Polymorphonuclear monocytes young athletes ‘powering-off’ during sprinting
and macrophages were not common at this stage, indicates that the gastrocnemius–soleus complex
reflecting perhaps the slowness of repair in this can generate sufficient force to rupture the tendon.
unique tissue. However, tendon strength usually exceeds that
The biopsy demonstrated the features of the of its muscle by a factor of two and hence rupture
repair phase that follows the acute inflammatory is unusual. The mechanisms involved in partial
2.0 LDR
0.5 NR
1.5 LDAT
Area (cm2 )
Load (F/Fmax)
1.0
0.5
0
Groups
Fig. 4.22 Cross-sectional area (cm2) of human

0 Achilles tendons measured by ultrasound for two
0 0.5 running groups matched for age, weight and distance
Deformation (ΔI/ΔImax) compared with a sedentary control group (NR).
The smaller cross-sectional area of the Achilles
Fig. 4.21 The effect of ‘fatigue failure’ or ‘plasticity’ tendons in the LDAT group (P < 0.05) should be
of load–strain curves with repeated loadings of a noted. LDAT, runners with grade I Achilles
tendon to successively higher loads (the curve of the tendonitis; LDR, runners without Achilles tendonitis.
next loading is shifted to the right) within the ‘toe’ (Courtesy of Professor A.W. Parker.)
region of the curve and before the linear part of
the curve. This effect may be operating in chronic
human Achilles tendonitis, especially in those
CSA using cadaver Achilles tendons. Two groups
athletes with a small cross-sectional area tendon.
(Adapted from Viidik 1973.) of distance athletes with and without grade 1
Achilles tendonitis who were age, weight and
distance matched had their Achilles tendon
grade 1 and 2 tears in the Achilles tendon are CSA measured using the previously validated
not as obvious. Viidik (1973) has shown that rat ultrasound technique. They demonstrated that
tendons in vitro undergo increasing deforma- athletes with grade 1-type Achilles tendonitis
tion or ‘plasticity’ if cycled to loads of less than had about a 30% decrease in the CSAs of their
one-tenth of its failure load, and that the strain Achilles tendons (Fig. 4.22). This indicates that a
or deformation occurs well before region two or major mechanism in this type of common injury
the linear part of the load–strain curve begins may simply be fatigue creep failure of Achilles
(Fig. 4.21). Similar observations have been made tendon collagen as shown in Fig. 4.21. Komi et al.
both in vivo and in vitro for rat knee joint liga- (1987) have developed an in vivo buckle trans-
ments by Weisman et al. (1980). It is possible that ducer which they located around the Achilles
in distance runners a similar fatigue plasticity tendon in a number of subjects. Direct force
and elongation occurs in the tendon and this measurements were made on several subjects
causes the microruptures and the thickened repair who were involved in slow walking, sprinting,
nodules already described. jumping and hopping after calibration of the
The notion that some running athletes may transducer. During running and jumping forces
not have an Achilles tendon of sufficient CSA to close to the previous estimated ultimate tensile
sustain the repetitive tendon loading of distance strength of the tendon were recorded, indicat-
without injury has been investigated by Engstrom ing that fatigue creep in a small cross-sectional
et al. (1985). In an elegant study they used ultra- tendon is a possible mechanism of injury without
sound to measure the CSA of the human Achilles the need to invoke other lower limb biomechan-
tendon in vivo and validated this technique as a ical pathology as has been suggested by Clement
reliable method to measure the Achilles tendon et al. (1984) and Williams (1986).
in collagen deposition at the repair site. Previous

Use of physical modalities in attempts
studies using low-intensity laser did moderately
to increase collagen deposition for
increase the biomechanical load-bearing capacity
enhancing the tensile strength of soft
of healing rabbit Achilles tendons after 14 days
tissue repair: electrical, ultrasound
of treatment (Enwemeka et al. 1990).
and laserphoto stimulation
Clearly, more long-term studies need to be
The original in vitro work of Fitton-Jackson and done in this area to attempt to understand the
Bassett (1980), in which fibroblasts were stimu- biological mechanisms involved and also to deter-
lated to increase collagen synthesis under the mine the long-term therapeutic value of such
influence of pulsed magnetic fields, has been in treatments.
part confirmed by other workers. However, the
gains in increased ligament strength have been
Effects of immobilization on the
meagre compared to the dramatic 40% or so
capsule and synovial joints
reduction in healing times for fresh fractures of
the tibia and radius with the use of low-intensity Akeson et al. (1987) reviewed their work and
ultrasound applied to fracture healing as origin- others’ work on this important topic. There is
ally described in the human by Heckman et al. articular cartilage atrophy with proteoglycan loss
(1994), and recently reviewed by Rubin et al. (2001). and an associated fibrofatty connective tissue
In fracture repair, ultrasound was demonstrated that is synovial derived, which adheres to the
with substantive data to enhance the three basic articular cartilage. Ligament insertion sites are
stages of the healing process described above. weakened and the ligament itself has increased
Such observations have been also demonstrated compliance with reduced load to failure due to
in part in soft tissue repair, but not with the same loss of collagen mass, which may occur with only
large increases in matrix deposition (collagen) as 8–12 weeks’ immobilization but may take up to
for bone deposition. Frank et al. (1983a, 1983b) 1 year to recover after mobilization (Amiel et al.
demonstrated accelerated early healing of a rab- 1983). Capsular changes include loss of water
bit medial collateral ligament (MCL) to which a due to loss of GAGs and hyaluronic acid, leading
solid core electromagnet energized the tissues to joint stiffness. Clearly joint immobilization is
with a square wave of unidirectional current 7 h to be avoided if possible to prevent the above
per day for up to 6 weeks postinjury. An increased changes from occurring which take many months
tensile strength of almost double the control MCL to recover (Fig. 4.23). Similarly Steno-Bittel et al.
was observed at 21 days, but at 42 days there was (1998) have demonstrated that functional casting
no difference between the treated and control of rabbits after an Achilles tendon complete tran-
ligaments. section and surgical repair in a short-term experi-
Enwemeka (1989) applied therapeutic ultra- ment (15 days); increased collagen deposition
sound daily for 5 min for nine treatments to (60%) and increased maximum tensile strength
tenotomized rabbit Achilles tendons, and noted (20%) and maximum stress (21%) in the repairing
significant increases in tensile strength and energy tendon compared to complete Achilles teno-
absorption to failure in the early healing phase tomies and suture repair with classic immobiliz-
(10 days’ post-tenotomy). tation of the lower limb with non-functional load
Kesava Reddy et al. (1998) applied a combined bearing.
laser treatment and electrical stimulation to the Thus the thrust in recent years has been to
repairing rabbit Achilles tendon after complete minimize immobilization times and to avoid
tenotomy over a short 5-day period. No statistical soft and hard tissue immobilization if practically
difference was found between the experimental possible. With wounds to soft tissues and hard
and the control tenotomies in terms of mechanical tissue injuries, such as fractures to bone, it may
performance although there was a 32% increase be necessary to immobilize these tissues either
Exercise effect experiments was ligament failure as opposed

100 to avulsion fracture failure. The latter mode of
Ultimate strength (%)
3° Ruptu failure was more predominant in the immobil-
Im
80 ion
zat
m
li ized group due to resorption of Haversian bone
obi
ob
60 M at the ligament attachment; but after 5 months
. ation
obiliz
re
No m of reconditioning femoral avulsion fractures did

40
not occur. It should be noted that there was no
20 surgery, just simple immobilization.
Another important study with direct implica-
0
0 8 1 tions for clinical practice is that of Amiel et al.
weeks year (1985). Although this work was done in rabbits,
Time of recovery in the context of the previous work by Noyes, it is
Fig. 4.23 Effects of immobilization, mobilization
very relevant. The timeframes for the changes
and exercise on the recovery of ligament ultimate in ligament tensile strength are similar and hence
tensile strength. The loss in ligament tensile strength are applicable to clinical rehabilitation. These
after a relatively short period of immobilization (about investigators were able to show that 12 weeks of
8 weeks) requires many months to recoverawith no immobilization of the MCL in the growing rabbit
mobilization it may take up to 1 year. The effect of
exercise on ligament ultimate tensile strength is small.
led to profound atrophy, such that there was a
(Adapted from Woo et al. 1987a.) decrease of approximately 30% in collagen mass
as a result of increased collagen degradation.
Remarkably most of this atrophy occurred during
externally (or internally with surgery) until heal- weeks 9–12 of immobilization. Again, there was
ing is well underway. This is so these tissues no trauma or surgery to the MCL in this study.
will have developed enough intrinsic mechanical Hence it appears from the above two studies
strengthathrough neocollagen fibril deposition that prolonged immobilization, i.e. 6–12 weeks
aso as not to be disrupted by early mobilization without trauma, can itself lead to profound
and to allow the remodelling phase of the repair atrophy of both the collateral and cruciate liga-
process to be enhanced (Vailas et al. 1981; see ments of the knee joint and recovery may require
below). Both tensile-bearing soft tissues such as at least many months or even a year. This time-
tendon and ligament require regular minimal frame must be kept in mind when managing
loading to maintain their intrinsic mechanical patients after prolonged knee immobilization
tensile strength; they are similar to bone and and advising them when they can best return to
articular cartilage in this respect (Caterson & full competitive sport.
Lowther 1978; Rubin & Lanyon 1987). Amiel et al. (1985) have also shown that there is
a close relationship between joint stiffness induced
by immobilization and a decrease of total GAG in
Effect of immobilization and
the periarticular connective tissues. They demon-
mobilization on ligament
strated alleviation of this joint stiffness in a rabbit
tensile strength
model using intra-articular hyaluronate.
Apart from the original, classic work of Noyes
Effect of immobilization
et al. (1974) in which the effects of immobiliza-
The most important study in this context is that tion on the ACL of the primate were examined,
by Noyes et al. (1974) using the ACL in monkeys. there have been few investigations of the cause
They demonstrated clearly that 8 weeks of lower of the decreased strength and elastic stiffness of
limb cast immobilization led to a substantial loss the ACL in response to immobilization. Tipton
of ligament tensile strength which took 9 months et al. (1970) reported that collagen fibre bundles
to recover from, even with a reconditioning pro- (viewed with light microscopy) were decreased in
gramme. The predominant mode of failure in these number and size in immobilized dogs, suggesting
that this was the cause of the decreased CSA seen these ligaments with the intensive endurance
in immobilized rabbit MCLs (Woo et al. 1987a). exercise programme and to determine if this could
The explanation for the decreased strength and be explained at the level of the collagen fibril,
elastic stiffness in these immobilized ligaments which is the fundamental tensile unit of ligament.
may be found at the collagen fibril level. Binkley Five 30-day-old pubescent rats were placed
and Peat (1986) showed a decrease in the number on a progressive 4-week exercise programme
of small-diameter fibrils after 6 weeks of immobi- of alternating days of swimming and treadmill
lization in the rat MCL. running. At the conclusion of the exercise pro-
gramme the rats were running 60–80 min at
26 m·min–1 on a 10% treadmill gradient and on
Effect of mobilization (exercise)
alternate days swimming 60 min with a 3% body
There have been a large number of studies inves- weight attached to their tails. Five caged rats
tigating this area. The literature has been reviewed of similar age and commencing body weights
by Tipton et al. (1986) Tipton and Vailas (1989), were controls. Analysis of ultrathin transverse
Butler et al. (1979) and Parker and Larsen (1981). sections cut through collagen fibrils of the exer-
cised ACLs revealed: (i) a larger number of fibrils
per unit area examined (29% increase, P < 0.05)
normal ligaments
compared with the non-exercised caged control
The results in experimental animals generally ACLs; (ii) a fall in mean fibril diameter from 9.66
indicate an increase in bone–ligament–bone prep- ± 0.3 nm in the control ACLs to 8.30 ± 0.3 nm
aration strength as a response to endurance-type in the exercised ACLs (P < 0.05); and (iii) as a
exercise. However, no change in ligament or ten- consequence of (i) and (ii) the major CSA of col-
don strength has been recorded by some workers lagen fibrils was found in the 11.25 nm diameter
and this may reflect different exercise regimes, group in the exercised ACLs and in the 15 nm
methods of testing as well as species differences. diameter group in the control ACLs. However,
The observations by Tipton et al. (1970, 1975), total collagen fibril cross-section per unit area
Cabaud et al. (1980), Parker and Larsen (1981) examined was approximately the same in both
and others that ligament strength is dependent the exercised and the non-exercised control
on physical activity prompted an ultrastructural ACLs. Similar changes occurred in the exercised
investigation as to the mechanism of this increase and control PCLs. These results are shown in
in tensile strength. Increased collagen content was Figs 4.24–26. In the exercised PCL, collagen per
found in the ligaments of exercised dogs and this microgram of DNA was almost double that of
correlated with increased CSA and larger fibre the control suggesting that the PCL was more
bundles. This accounts for the increased liga- loaded with this exercise regime than the ACL.
ment tensile strength but whether this increased The conclusion from this study is that ACL and
collagen was due to the deposition of collagen PCL fibroblasts deposit tropocollagen as smaller
on existing fibres or due to the synthesis of new diameter fibrils when subjected to an intense
fibres was not investigated. Larsen and Parker 1 month’s intermittent loading (exercise) rather
(1982) had already shown that with a 4-week than the expected accretion and increase in size
intensive exercise programme in young male of the pre-existing larger diameter collagen fibrils.
Wistar rats, both the ACLs and PCLs showed a Very similar ultrastructural observations have
significant strength increase (P < 0.05). been made for collagen fibrils of exercised mice
Oakes et al. (1981) and Oakes (1988) quantified flexor tendons (Michna 1984).
the collagen fibril populations in young rat ACLs The mechanism of the change to a smaller
and PCLs subjected to an intensive 1-month alter- diameter collagen fibril population is of interest
nating treadmill and swimming exercise pro- and may be related to a change in the type of pro-
gramme. This study was performed in an attempt teoglycans synthesized by ligament fibroblasts in
to explain the increased tensile strength found in response to the intermittent loading of exercise.
Fig. 4.24 Transverse sections

through: (a) exercised anterior
cruciate ligament, and
(b) non-exercised control
anterior cruciate ligament.
(Magnification × 21 600.)
Control It is well recognized since the original work of

Exercise Toole and Lowther (1968) that GAGs have an
** * effect on determining collagen fibril size in vitro
**
ACL ACL and this has been confirmed in vivo by Parry et al.
PCL
60
Area occupied by each
(1982). Merrilees and Flint (1980) demonstrated

diameter group (%)
**
50 a change in collagen fibril diameters between the
PCL
40 compression and tension regions of the flexor
30 digitorum profundus tendon as it turns 90° around
the talus. Amiel et al. (1984) have also shown that
20 * PCL rabbit cruciate ligaments have more GAGs than
ACL
10 the patellar tendon and hence it is likely that
0 GAGs also play an important role in determining
125–625 750–1125 1250–1750
collagen fibril populations in cruciate ligaments
Diameters nm
(see below for further discussion).
Fig. 4.25 Comparison of per cent area occupied by
three diameter groupings used for statistical analysis
for exercised and control anterior cruciate ligament surgically repaired ligaments
(ACL) and posterior cruciate ligament (PCL).
Tipton et al. (1970) demonstrated a significant
*, p = 0.01; **, p = 0.05.
increase in the strength of surgically repaired
MCLs of dogs after treadmill exercise training
for 6 weeks, after 6 weeks’ cast immobilization.
125–625 nm 125–625 nm
9.42
14.96%
%
1250 1250 750–1125
nm 42.06% nm 59.52% 31.06% nm Fig. 4.26 Comparison of per cent
43.02% area occupied by the three
diameter groupings used for
750–1125 statistical analysis in exercised
nm and control posterior cruciate
Exercise Control ligaments.
However, they emphasized that at 12 weeks’ vention. Both the structural properties of the
postsurgery (6 weeks of immobilization and FMT complex and the material properties of the
6 weeks of exercise training) the repair was MCL were examined. After immobilization, there
only approximately 60% that of the normal dogs were significant reductions in the ultimate load
and results suggested that at least 15–18 weeks and energy-absorbing capabilities of the bone–
of exercise training may be required before a ligament–bone complex. The MCL became less
return to ‘normal’ tensile strength is achieved. stiff with immobilization and the femoral and
Similar observations have been made by Piper tibial insertion sites showed increased osteo-
and Whiteside (1980), using the MCL of dogs. clastic activity, bone resorption and disruption of
They observed that mobilized MCL repairs were the normal bone attachment to the MCL. With
stronger and stretched out less, i.e. less valgus mobilization, the ultimate load and energy-
laxity, than MCL repairs managed by casting and absorbing capabilities improved but did not
delayed mobilization. This conclusion is sup- return to normal. The stress–strain characteristics
ported by the work of Woo et al. (1987a, 1987b). of the MCL returned to normal, indicating that
Some insight into the biological mechanisms the material properties of the collagen in rabbit
involved in the repair response with exercise has MCL return relatively quickly after remobiliza-
come from the elegant work of Vailas et al. (1981). tion but that the ligament– bone junction strength
By using 3H-proline pulse labelling to measure return to normal may take many months (see
collagen synthesis in rat MCL surgical repairs Fig. 4.23).
and coupling this with DNA analyses and tensile The detailed biological cellular mechanisms
testing of repaired ligaments subjected to exer- involved in this enhancement and remodelling
cise and non-exercise regimes, they were able of the repair are not understood but may involve
to show that treadmill running exercise com- prostaglandin and cAMP synthesis by fibroblasts
mencing 2 weeks after surgical repair enhanced subjected to repeated mechanical deformation
the repair and remodelling phase by inducing by exercise.
a more rapid return of cellularity, collagen syn- Amiel et al. (1987) have shown that maximal
thesis and ligament tensile strength to within collagen deposition and turnover occurs dur-
normal limits. Further, Woo et al. (1987b) have ing the first 3–6 weeks postinjury in the rabbit.
demonstrated almost complete return (98%) of Chaudhuri et al. (1987) used a Fourier domain
structural properties of the transected canine directional filtering technique to quantify collagen
femoral–medial collateral ligament–tibial (FMT) fibril orientation in repairing ligaments. Results
complex at 12 weeks’ post-transection without indicated that ligament collagen fibril reorienta-
immobilization. Canines immobilized for 6 weeks tion does occur in the longitudinal axis of the liga-
with the FMT complex tested at 12 weeks, had ment during remodelling. MacFarlane et al. (1989)
mean loads to failure of 54% that of the controls. and Frank et al. (1991) have further shown that
However, the tensile strength of the MCL was collagen remodelling of the repairing rabbit MCL
only 62% of controls at 48 weeks. This appar- appears to be encouraged by early immobilization
ent paradox in the non-immobilized dogs was but after 3 weeks collagen alignment and remodel-
explained by the approximate doubling in CSA of ling appears to be favoured by mobilization.
the healing MCL (and hence increased collagen We have recently completed a study on the
deposition) during the early phases of healing. repair of the goat ACL. It has almost become an
This repair collagen was most probably small- axiom amongst orthopaedic surgeons that the
diameter fibrils and would account for the poor ACL does not repair after injury, even partial
strain performance of the MCL scar collagen and injury. This seems to be the case with complete
would be similar to the lower curve on Fig. 4.23. ACL rupture (Grontvedt et al. 1996) if there is no
Woo et al. (1987a) examined the effects of pro- continuity in either the synovial membrane ACL
longed immobilization and then mobilization sleeve or its contained collagen fibre bundles.
on the rabbit MCL without any surgical inter- However, the repair of partial tears of the ACL
(grade 1 and 2) has not been examined carefully

Collagen fibril populations in human
in the long term in large animals. To test the
knee ligaments and grafts
healing of the partially torn ACL, we transected
the posterolateral bundle of the ACL in 11 adult
Human ACL autograft quantitative
female goats and tested the ligaments at 12, 24
collagen fibril studies
and 52 weeks and 3 years after surgery as previ-
ously described on page 69. Translucent repair In order to gain some biological insight into
tissue was seen filling in the ‘wound’ region as collagen repair and remodelling mechanisms
early as 12 weeks post-hemisection. There was within human cruciate ligament grafts, biopsies
also no difference in the antero-posterior laxity were obtained from autogenous ACL grafts from
between the hemisected and normal control knees patients subsequently requiring arthroscopic
at each time period examined. Load-relaxation
and Young’s modulus also were not significantly
different at each time period; but surprisingly the
hemisected-ACL ultimate tensile strength and
stiffness at 3 years were significantly higher than
at 12 weeks (p < 0.05). Also surprising was the
fact that at 3 years, the ACL specimens all failed
with bone avulsion indicating the repair tissue
was very strong and not the weakest link of the
bone–ligament–bone complex as one might have
expected (see Figs 4.16 and 4.17).
This study emphasizes that under favourable
conditions, partial ACL injuries or tears are
capable of an adequate tensile strength repair.
Perhaps more importantly as far as athletes are
concerned the high ultimate tensile strength and
stiffness of the 3-year repaired tissue indicates
that full structural repair of such an artificial hemi-
transection injury model is possible (Ng et al.
1996). This work suggests such partial human
ACL injuries may be adequately repaired in ath-
letes, (if diagnosed early with MRI examination)
which is contrary to current orthopaedic opinion.
With this basic biological knowledge there
is now a rationale for the use of early controlled
mobilization of patients with ligament trauma.
The use of a limited motion cast with an adjust-
able double-action hinge for the knee joint is Fig. 4.27 Transverse sections through collagen fibrils
of: (a) normal young adult patellar tendon (mean of
now accepted in clinical practice and enhances six biopsies); (b) normal young adult ACL (mean of
more rapid repair and remodelling as well as six biopsies); and (c) Jones’ free graft (mean of nine
preserving quadriceps muscle bulk and strength. biopsies). (Magnification × 34 100.) The insets show:
Patients are now usually mobilized early in a on the left, the number of fibrils versus diameter;
limited motion cast for a minimum of 3 weeks and on the right, per cent area occupied/diameter
group. The preponderance of small-diameter fibrils
with a range of motion from 20 to 60° (Helbing & in the graft (c), and large fibrils in the patellar tendon
Burri 1977) rather than the previously empirical (a), which are not seen in the ‘normal’ ACL (b),
time of 6 weeks’ immobilization. should be noted.
Fig. 4.28 Summary and

comparison histograms of
collagen fibril profiles for normal
tissues used for anterior cruciate
ligament (ACL) grafting (patellar 45
tendon [PT, n = 7], iliotibial band 45
40
[ITB, n = 3] and semitendinosus 40
35
[ST, n = 1]) with ACL autografts 35
Area/diameter (%)
Area/diameter (%)
30
derived from the same tissues 30
25
expressed as per cent area per 25
diameter group. Large-diameter 20
20
fibrils > 100 nm are found 15
15
predominantly in the hamstring 10
(ham.), ST and to a lesser extent 10
5
5
in the normal PT. The ITB has ITB
0
0 -A
a profile not unlike that of the 0 AC AII h
0–10–30 0
CL
Me L g am , (n
normal ACL. All the autograftsa 2 0–5 70 No an raf . =1
5)
4 0– A ts,
6 0–90 0
Fib
No r ma C L (n=
patellar tendon Jones’ free ACL 8 –11 0 J 9)
ril
No rm l IT FG
s
100 20–13–150 0
al B, s, (
di
grafts (JFG, n = 39), hamstring rm ST (n= n= on

am
No
1 40 –17 rm al
PT , (n 3) 39
a ris
et
1 60 =1 )
mp
al , (n
ACL grafts (n = 9) and ITB
er
1 AC =7 )
co
(n
L< )
ft
m
30
ACL grafts (n = 15)ahave a
)
, (n r
-10 g
predominantly small-diameter )
a nd
al
fibrils. (From Oakes 1993, with rm
No
permission from Raven Press.)
intervention because of stiffness, meniscal and/ and also biopsies of ACLs from young (< 30 years,
or articular cartilage problems or removal of n = 5) people who had not sustained a recent ACL
prominent staples used for fixation. Most of the injury. Biopsies were also obtained from normal
ACL grafts were from the central one-third of patellar tendons at operation (n = 7) (Figs 4.27
the patellar tendon as a free graft (n = 39), or in and 4.28). Eighteen ACL graft biopsies have been
some left attached distally (n = 8) and in others obtained from other surgeons, both nationally
the hamstrings (n = 9, graft age 10 months to and internationally (Oakes et al. 1991; Oakes 1993).
6 years) or the iliotibial tract was used (n = 15, The results from the collagen fibril diameter
graft age 10 months to 6 years). These biopsies morphometric analysis in all ACL grafts clearly
represented approximately 20% of the total free indicated a predominance of small-diameter
grafts performed over the 3 years of this study. collagen fibrils (Figs 4.28–4.30). Absence of a
The clinical ACL stability of the biopsy group ‘regular crimping’ of collagen fibrils was observed
differed little from the remainder. All had a by both light and electron microscopy, as was
grade 2–3 pivot shift (jerk) preoperatively (10– a less ordered parallel arrangement of fibrils. In
15 mm anterior drawer neutral), eliminated most biopsies, capillaries were present and most
postoperatively in 87% of patients (0.5 mm). Sub- fibroblasts appeared viable.
sequent clinical review at 3 years showed an
increase in the anterior drawer with a return in
Collagen typing of normal human ACL and
20% of a grade 1 pivot shift.
ACL grafts
A total of 39 biopsies have been quantitatively
analysed for collagen fibril diameter popula- Recent biochemical analyses of human patellar
tions in patients aged 19–42 years. These data tendon autografts in situ for 2–10 years indicates
were compared with collagen fibril populations a large amount of type III as well as type V col-
obtained from biopsies of cadaver ACLs (n = 5) lagen. This confirmed our suspicion that a large
50 50
45
45
40 40
35
Area/diameter (%)
35
Area/diameter (%)
30 30
25
25 1
20 20
15 15
10 10
5 5
0 0
5–
0 9
0–1–30 0 3 3– 4–5y yr A
20 0–5 70 2 4
0– yr r A uto
4
21 –3 36 A ut
Fib 4 60– –90 15 18– –24 0m m A uto o JF JFG
ril d 0 20 9– 12–1 –18 21m m A Aut uto JFG G n n=4
iam 1810–01–14060 6
0– –9m12m 5m m
A Aut uto o JF JFG n=3 4
=
ete 13 50–1–180 0 6
No Norm m A Au Aut Autouto J o JF JFG G n= n=6 .
r nm 1 170 0–20 rm u to o F G n 5
19 al al PT to J JFG JFG JFG G n= n=1 =2
AC n FG n n= n=4 4 ting
2 Ln 7
=1
=
1
=
n= 3 2
o s t graf
0 ep Tim
Fig. 4.29 Summary histograms of all human anterior cruciate ligament (ACL) patellar tendon (PT) autografts
(n = 39) versus time postgrafting compared with normal young ACL (n = 10) and normal young PT (n = 7)
expressed as per cent area per diameter group. The presence of large fibrils (> 100 nm) in the older (5–9-year-old
grafts; arrow 1) and the rapid loss of < 100 nm fibrils in the 0–6-month postgraft group (arrow 2), which are present
in the donor PT (to the left of arrow 2) should be noted. (From Oakes 1993, with permission from Raven Press.)
Fig. 4.30 Summary histograms

of all human anterior cruciate
ligament (ACL) allografts versus
60 time postgrafting compared
with normal young ACL, normal
60 1 50 patellar tendon (PT), reconstituted
Area/diameter (%)
50 tibialis anterior (TA) and Achilles

40
Area/diameter (%)
tendons expressed as per cent area

40 2 30 per diameter group. The early
preponderance of the small fibrils
30 20 at 3 months postgraft (arrow 1)
20 and their persistence even at 96
10
months postgraft in the majority
10 9 0 of biopsies examined should be
89 6m
6 m A
00 6 6m
54 2m
AC CL noted. Some large fibrils are
A L A All
0–1 30 1
42 m
m
A C
AC CL A L All llog gra
o
present (arrow 2) at 96 months,
20– 0–50 0 10 2m A C LA ll og ra ft
Fi
9 m A
4 0–7 0 6m m A AC CL L Al llog ogra raft ft
b
6 0–9 0 but the majority of the large fibrils

ri
8 –11 0 3m A CL L A Allo log ra ft

ld
T
100 20–13 50 No end ACL CL A Allo llog gra raft ft g present in the donor tissues are
ia
1 40–1 0 N o l
No orm rmal Ac Allo logr graf raft t
f
tin
m
1 –17 f
160 0–190 ra
et
rm al TA hill gra aft t removed (to the right of arrow 3).

P es g
er
18 al ft t
AC T
os
nm
3 LS
hin ep (From Oakes 1993, with
o
T im permission from Raven Press.)
Table 4.1 Human ACL collagen typing.
Type I (+/− SD) Type III (+/− SD)
Normal ACL 71.13 +/− 9.77 28.1 +/− 10.18

(N = 10, age 16–40)
Acute ACL rupture 65.51 +/− 7.80 33.77 +/− 7.86
(n = 11, age 16–30, < 1-week-old)
Jones’ free ACL grafts 70.20 +/− 6.75 28.48 +/− 7.02
(n = 9, age 19–27, graft age 9–2yrs)
Iliotibial band ACL grafts 60.27 +/− 13.89 39.03 +/− 13.90
(n = 3, age 25–35, graft age 4–10yrs)
amount of collagen in these remodelled grafts tribution in the patellar tendon is skewed to the
at this age may be type III and not type I as is right with a small number of large fibrils not pres-
normally found in the patellar tendon and adult ent in the normal ACL (Figs 4.27–4.30). Elegant
ACL (Deacon et al. 1991). work by Butler et al. (1985) has shown that the
We have examined and quantified the types patellar tendon is significantly stronger than the
of collagen in the normal ACL and in ACL grafts human ACL, PCL and lateral collateral ligament
using quantitative sodium dodecyl sulphate gel from the same knee in terms of maximum stress,
densitometry of cyanogen bromide peptides linear modulus and energy density to maximum
derived from the tissue in question (Chan & Cole strength. The larger fibrils observed in the patellar
1984). Tissue was obtained from: 10 acute rup- tendon are not found in the ACL and are an obvi-
tured ACLs (< 1 week old), 10 normal ACLs and ous explanation for the stronger biomechanical
nine autogenous patellar tendon grafts (age 3 tensile properties of the normal patellar tendon.
months to 2 years.). The biopsies from the grafts were obtained
The normal ACL contained a mean type I from patients with a good to fair rating in terms
collagen content of 71.13 ± 9.77 (SD) and type III of a moderate anterior drawer (0–5 mm) and cor-
content of 28.1 ± 10.18. The acute ACL ruptures rection of the pivot shift, but both these tests of
had similar type I and III collagen contents as did ACL integrity showed an increasing laxity of the
the patellar tendon grafts (Table 4.1). ACL at the 3-year clinical review. The length of
The high content of type III collagen in the time the grafts were in vivo prior to biopsy varied
normal human ACL (28.1%) is surprising and from 6 months to 6 years. The collagen fibril
was similar to that found in the patellar tendon population did not alter that much for the older
autografts and the acute ACL ruptures. This is grafts (namely > 3 years), which is not what was
much higher than that reported by Amiel et al. hoped for or expected but is in keeping with
(1984) for normal rabbit ACL. They suggest the the observation clinically that the ACL grafts
high type III content may reflect a wide variety ‘stretched out’ postoperatively.
of force vectors that the rabbit ACL is subjected The most striking feature of all the biopsies
to. These new data may indicate unrecognized from the autografts, irrespective of whether they
or documented previous injury to the ‘normal’ were ‘free grafts’, Jones’ grafts, fascia lata, ham-
ACL tissue (Oakes 1993). string grafts, and independent of the surgeon,
Before discussing the biopsy data it is of was the invariable prevalence of small-diameter
interest to compare the collagen profiles for the fibrils in amongst a few larger fibrils that prob-
patellar tendon with the normal ACL. It can be ably were the original large-diameter patellar
seen that the profiles are different in that the dis- fibrils. The packing of the small fibrils in the
grafts was not as tight as is usually observed in diameter collagen fibrils (< 7.5 nm) and their poor
the normal patellar tendon (compare Figs 4.27a, c packing and alignment in all the ACL grafts, irre-
and 4.29, arrows 1 and 2). spective of the type of graft (auto- or allograft),
It appears from the quantitative collagen fibril their age and the surgeon, may explain the clinical
observations in this study that the large-diameter and experimental evidence of a decreased tensile
fibrils of the original graft are removed and almost strength in such grafts compared with normal
entirely replaced by smaller, less well-packed and ACL. It appears that in the adult, the replacement
less well-orientated fibrils than the larger diameter fibroblasts in the remodelled ACL graft cannot
fibrils found in the normal patellar tendon. The reform the large-diameter, regularly crimped and
smaller diameter fibrils are probably recently tightly packed fibrils seen in the normal ACL,
synthesized because they are of smaller diameter even after 6 years, which was the oldest graft
than those found in the original patellar tendon. analysed.
Hence the entire collagen matrix of the original The origin of the replacement fibroblasts which
patellar tendon is remodelled and replaced with remodel the ACL grafts is not known at the
newly synthesized small-diameter collagen fibrils. moment. It is the author’s hunch that they will not
Is gentle mechanical loading in the ACL grafts come from the actual graft itself although some
an important stimulus to fibroblast proliferation of these cells may survive due to diffusion. How-
and collagen deposition? Inadequate mechanical ever, the bulk of the stem cells involved in the
stimulus may occur, especially if grafts are non- remodelling process are probably derived from
isometric and are ‘stretched out’ by the patient the surrounding synovium and its vasculature.
before they have adequate tensile strength. A Beynon et al. (1997) mechanically tested a
lax ACL graft may not induce sufficient mechan- human patellar tendon ACL graft 8 months post-
ical loading on graft fibroblasts to alter the GAG surgery. The stiffness and the ultimate failure
or decorin/collagen biosynthesis ratios to favour load approached that of normal after 8 months
large-diameter fibril formation. Certainly in this of healing and graft remodelling. The antero-
study there was ACL graft laxity which increased posterior (AP) laxity was 1.85 and 1.26 that of the
postoperatively. This would lend credence to normal knee at 10 and 60° of knee flexion,
the above notion. However, use of continuous respectively. This increase in AP laxity (6.3 mm
passive motion in grafted primates does not greater than normal) was substantially greater
increase the strength of grafts. than the 2 mm right-to-left variation in AP laxity
Another more likely possibility is that the seen in subjects with healthy knees. This was also
replacement fibroblasts in the ACL grafts are reflected in greater strain values when compared
derived from stem cells from the synovium (and with the normal ACL. Also, energy absorbed to
synovial perivascular cells) which are known to failure was only 53% of the normal ACL. These
synthesize hyaluronate, which in turn favours values of increased strain, increased AP laxity
small-diameter fibril formation (Parry et al. 1982). and low energy to failure indicate the poor qual-
The strong correlation of small-diameter fibrils ity of the remodelled collagen matrix of this ACL
with a lower tensile strength has been observed and is similar to that of the scar seen in the repair-
by Parry et al. (1978) and Shadwick (1990), and ing dog (Woo et al. 1987b) and rabbit MCL (Frank
the observations in this study would confirm this. et al. 1999; see below).
Our observations also correlate with the observa-
tions of Clancy et al. (1981) and Arnoczky et al.
Human ACL allografts
(1986). The observations by Amiel et al. (1989)
indicate that collagenase may play a role in the Recent further studies of biopsies obtained from
remodelling of ACL tears/grafts. ACL human allografts utilizing fresh frozen
The conclusion from these ultrastructural Achilles or tibialis anterior tendons, ranging in
observations is that the predominance of small- age from 3 to 54 months, indicated a similar
predominance of small-diameter collagen fibrils The large fibrils constituted about 80% of the total
(Shino et al. 1990, 1991, 1995). fibril CSA. In contrast, the normal ACL had about
Human ACL allograft specimens were studied 85% of its total CSA composed of fibrils < 100 nm,
as above for the autografts with quantitative but there were a small number of large fibrils
collagen fibril analyses (Oakes 1993), and were which accounted for about 15% of its total CSA.
compared with ACL autografts. The allograft
specimens were procured at the time of second-
allograft results versus
look arthroscopy from the superficial region of
time (Fig. 4.30)
the mid-zone of ACL grafts after synovial clear-
age. The grafts used for the ACL reconstruction By 3 months postoperatively (n = 2), there was
were usually from fresh frozen allogeneic Achilles a predominance of small-diameter fibrils which
or tibialis posterior or anterior tendons and were accounted for > 85% of the total CSA of these
implanted 3–96 months prior to biopsy. biopsies with a ‘tail’ of larger fibrils making the
Thirty-eight patients who had undergone allo- fibril distribution bimodal in shape. At 6 months
graft ACL replacement and whose AP stability (n = 5), the fibril distribution was now unimodal
had been adequately restored were randomly with most (c. 90%) of the fibril CSA in the < 100 nm
selected. The restored stability of the involved diameter group. Fibrils of > 100 nm were obvi-
knees was carefully confirmed with both Lachman ously fewer than in the 3-month specimens. By
and pivot shift signs and an objective quantita- 12 months (n = 12) almost all the CSA resided in
tive knee instability testing apparatus. All of the < 100 nm diameter fibril group and there was
these patients were subjected to second-look almost complete absence of the large > 100 nm
arthroscopy as a part of the procedure to remove fibrils.
hardware installed for graft fixation. Thirty-five This profile persisted in the 13–96-month-old
graft biopsies were obtained from this patient allografts. However, there were two exceptions,
group. Their age ranged from 15 to 37 years at the where one 12-month-old and one 54-month-old
time of reconstruction. ACL allograft biopsy specimen had significant
ACL reconstruction was performed using fresh numbers of large-diameter fibrils in contrast to
frozen allografts, 8–9 mm in diameter; part of the the earlier observations. In these two specimens
Achilles tendon, the tibialis anterior or posterior, the large-diameter fibrils (> 100 nm) accounted for
peroneal or other thick flexor tendons without 40% of the total CSA of the collagen fibrils. How-
any bone attached to their ends were used as an ever, the large-diameter fibrils in these excep-
ACL substitute. Postoperatively, the knee was tional grafts were smaller in size and had more
immobilized for 2–5 weeks, then full weight irregular surfaces than those in the allografts prior
bearing allowed at 2–3 months, jogging recom- to implantation, suggesting perhaps a ‘collagenase
mended at 5–6 months, and full activity allowed sculpting’ of their exposed surface fibrils.
at 9–12 months. Parry et al. (1978) were the first to describe
The normal tissues used were compared with the bimodal distribution of the collagen fibrils in
the normal ACL and the ACL allografts. adult mature tendon collagen that is subjected to
high tensile loads. The reconstituted (treated by
freezing and thawing) human allografts (Achilles
normal tissues used for allografts
and tibialis tendons) and the normal ACL in this
The reconstituted Achilles tendon demonstrated study are also shown to have a bimodal distribu-
a large number of fibrils in the 90–140 nm range tion of small- and large-diameter fibrils similar to
(40% of total CSA) together with small-diameter that described by Parry and colleagues in a large
fibrils of 30–80 nm. The reconstituted tibialis range of other tissues.
anterior tendon showed larger diameter fibrils Most ACL allograft biopsies also demonstrated
and fewer smaller fibrils than the Achilles tendon. a bimodal distribution of large and small fibrils
similar to the ‘normal reconstituted’ tendons up Awaiting the appearence of large fibrils with
until about 6 months postimplantation. How- close packing (perhaps under a Wolff’s law
ever, after this time the distribution became more tensile stimulus) as seen in normal ligament and
unimodal, such that there was an increasing tendon is probably futile. There is no current
predominance of small-diameter fibrils with a ultrastructural evidence available that large-
concomitant and progressive loss of the larger diameter fibrils will eventually be formed and
‘host tendon’ fibrils. It is these larger fibrils in the become a large proportion of the CSA of long-
‘normal’ tendon that are responsible for a large term ACL grafts or even that the packing of
percentage of the tendon collagen CSA and for the small-diameter fibrils becomes closer within
the very high tensile strength of these tendons; these grafts. If denser collagen fibril packing
the tensile strength exhibited is probably due could be achieved, this might possibly enhance
to the high density of intermolecular collagen the collagen fibril CSA per unit area, which in
cross-links. These observations suggest, at the turn might possibly increase the tensile strength
least, that most of the original large-diameter of the graft by increased interfibril interactions
fibrils in the ACL allografts are replaced by newly as already discussed. The reason denser pack-
synthesized smaller diameter collagen fibrils ing of fibrils is not seen in allo- or autografts may
(or undergo disaggregation, see below). The loss be due to an increased synthesis of small pro-
of the large-diameter fibrils from 6 months and teoglycans, particularly decorin and hyaluronan,
older allografts and the predominance of the preventing large collagen fibril formation (Scott
small-diameter fibrils seen in this study is the 1990; see below).
most likely explanation for the dramatic reduc- It should be also mentioned that the con-
tion in tensile strength of ACL allografts, and clusions drawn in this discussion are based on
hence the observed increased AP laxity in a pre- the assumption that large collagen fibrils of the
vious animal study by Shino et al. (1984). allograft tendons do not undergo a process of
These observations parallel those described disaggregation into smaller fibrils similar to
above for ACL autografts, which also demon- that described by glycerol treatment of mature
strated within 6 months postimplantation the collagen fibrils, which is reversible (Leonardi
loss of large-diameter collagen fibrils of patellar et al. 1983). This is a possibility which must be
tendon origin. It could be concluded, therefore, seriously considered but is very difficult to verify
that the remodelling process has a similar time- experimentally without rigorous immuno-electron
frame in both ACL tendon allografts and patellar microscopy.
tendon ACL autografts. It further suggests that The remodelling of collagen in tendon auto-,
similar mechanisms of collagen degradation and allo- and xenografts has been elegantly quantified
neosynthesis of collagen may be occurring by the by the now classic work of Klein et al. (1972).
invading synovial stem cells which repopulate They noticed at 3 months that xenografts lost 99%,
the ACL graft almost immediately after surgery. allografts lost 63% and autografts 54% of their
A valid criticism of these studies could be that original collagen, demonstrating a clear anti-
all the biopsies were obtained from the super- genic influence on collagen turnover which was,
ficial region of the grafts and that this may not be however, still substantialaeven in the autografts
representative of the bulk of the graft collagen. at 3 months. The remodelling of collagen during
However, in the previous autograft study the medial ligament repair in the rabbit has also
biopsies were usually obtained from the middle been shown to be prolonged in that the collagen
of the autografts and the observations were no concentration takes many months to approach
different from those in this allograft study. This normal levels (Klein et al. 1972) and appears to be
suggests that the superficial region from which similar in larger animals (Woo et al. 1987a).
the biopsies were taken in this study is represen- The observations and conclusions in this auto/
tative of the graft collagen. allograft review throw into question the current
timeframes for rehabilitation. It is generally con- collagen fibril remodelling process in adult goat
cluded by most knee surgeons that the graft patellar tendon ACL autografts over a 3-year
tissue will eventually mature, given enough time, timeframe. Eleven mature female adult goats
and that graft tensile strength will also increase were used in this study. The middle one-third of
with time, especially if the athlete waits for up the right patellar tendon was harvested and used
to 1 year for graft maturation. The observations as an ACL graft. The animals were sacrificed at
in this study do not support this notion that the following time intervals: 6 weeks (n = 3), 12
graft tensile strength will gradually increase with weeks (n = 2), 24 weeks (n = 2), 52 weeks (n = 3)
time. However, collagen cross-link maturation and 3 years (n = 1). The ACL grafts were then
could be very important in these grafts and this obtained and prepared for quantitative ultra-
may be a mechanism for restoring some graft structural collagen fibril analyses.
tensile strength even when the collagen fibrils The normal ACL (t = 0, n = 5) and ACL patellar
remain of small diameter. Observations by Butler tendon grafts (n = 11) were divided into thirds
et al. (1987) that primate ACL autografts and and 1 mm thick sections were cut from the femoral,
ACL allografts using the patellar tendon were middle and tibial thirds. This section was then
only about 30% the strength of normal ACL at cut into a strip and four sections obtained: two
12 months postimplantation, strongly support were deemed superficial and contained a syn-
the quantitative fibril observations outlined in ovial surface and two were deemed deep. The col-
this human auto/allograft study. lagen fibril profiles were directly quantified from
Comprehensive detailed clinical studies by electron micrograph negatives using a specific-
Shelbourne (Shelbourne & Nitz 1990; Shelbourne ally designed software program for automated
& Davis 1999), and more recently by Barber- computerized image analysis. The frequency of
Westin et al. (1999), have demonstrated (contrary fibrils within 20 diameter size classes and the
to expectations with the preceeding ACL graft percentage area occupied for each diameter group
small fibril data) that early accelerated ACL of fibrils were automatically calculated as a mean
rehabilitation programmes have not led to (Fig. 4.31).
increased AP laxity, which is a paradox when The results of the study were as follows:
compared to the results of Beynon et al. (1997). 1 Normal adult goat ACL, t = 0. The distribution
It may be speculated that the early aggressive was clearly bimodal with a large number of small
ACL rehabilitation advocated by Shelbourne may fibrils < 100 nm in diameter and a group of larger
limit the collagen loss and may assist in early fibrils > 100 nm in diameter (Fig. 4.32a). A small
collagen fibril orientation and deposition, and number of large fibrils of > 100 nm contributed
hence may help to explain the lack of AP laxity about 45% of the total collagen fibril area; these
with these programmes. large fibrils seen in the adult goat ACL are not
Excellent comprehensive reviews of all aspects seen in the normal adult human ACL.
of human ACL reconstruction are recommended 2 Normal adult goat patellar tendon, t = 0. The
further reading of this complex topic (Frank & collagen fibril distribution was quite different
Jackson 1997; Fu et al. 1999, 2000). ACL graft selec- to the ACL with a more unimodal distribution.
tion has been recently reviewed by Bartlett et al. There were less small-diameter fibrils and more
(2001). larger diameter fibrils > 100 nm than in the ACL,
and these latter fibrils contributed 65% of the
total collagen fibril area (Fig. 4.32b).
Goat ACL patellar tendon autograft
3 Patellar tendon ACL graft: tibial region versus
collagen remodelling: quantitative
femoral region (Figs 4.33 and 4.34). At 6 weeks
collagen fibril analyses over 3 years
postsurgery there was a large increase in the num-
The aim of this study (Ng et al. 1995a, 1995b, ber of small-diameter collagen fibrils (< 100 nm)
1996a, 1996b) was to quantify in detail the which was greatest at the tibial end. This number
Fig. 4.31 The methodology of

sampling the goat ACL, as well as
tissue blocking and the electron
microscopic grid random
sampling technique.
Femoral
PLB
AMB
Middle
(a)
52 weeks
Tibial
Fig. 4.33 Summary diagram of goat ACL graft fibril

profiles at 12 months postgrafting. The preponderance
of small fibrils at the tibial end of the graft and some
large fibrils remaining in the femoral end of the graft
at 12 months postgrafting should be noted. AMB,
antero-medial bundle; PLB, postero-lateral bundle.
of small-diameter fibrils was increased at both

(b) ends of the graft at 52 weeks. There was a loss of
Fig. 4.32 Electron micrographs of: (a) normal adult the large-diameter fibrils (> 100 nm) which could
goat ACL, and (b) normal adult goat patellar tendon. be seen at 6 weeks, and at 52 weeks only a few
Fig. 4.34 Three-dimensional

histograms of normal goat
patellar tendon (PT) and anterior 1
cruciate ligament (ACL) patellar 0.6
tendon autografts at t = 0, 3, 6, 12, 0.6
24 and 48 weeks in relation to the 0.5
femoral, middle and tibial regions 0.5
0.4
Fibril ratio
of the ACL autografts. The
0.4
Fibril ratio
vertical axis is the ratio of large 2 0.3
fibrils (> 100 nm) to small fibrils 0.3
(< 100 nm). Large fibrils are lost 0.2
0.2
from the tibial end of the graft as 0.1
early as 6 weeks postgrafting but 0.1
some large fibrils still remain 0
0 Fem
0
at the femoral end of the graft T T= ks ora
at 48 weeks (arrow 2). The P
w ee eks Mi
dd
l
s
Tim 3 we nth hs le
o n
predominance of large fibrils in ep 6 o t Tib
ti
m on ths ial
si
po
er 3
the original PT used as the donor iod 6 m mon
CL
12
A
graft (arrow 1) should be noted.
1
30
30
25
Fig. 4.35 Three-dimensional 25
histograms of normal goat
20
Fibril area (%)

patellar tendon (PT), anterior
20
Fibril area (%)
cruciate ligament (ACL) and

ACL autografts expressed as 15
per cent area covered by the 15 2
collagen fibrils versus age and 10
fibril diameter. Again there is 10
progressive loss of the large- 5
diameter fibrils and the rapid 5
replacement of these large fibrils 0
0 12
(arrow 3) as early as 6 weeks after
10 6 m mon
grafting, with a predominance 0– 0–3050 3 on ths
2 40– –70 0
0 9 0 3 6 w mont ths
of small fibrils at 12 months Fib 6 8000––101–130150 70 3w eek
s
hs
ril d 1 12 40– 0–1 190 5 PT e
ft
postgrafting (arrow 1). The (T= eks

ra
iam 1 16 80–0–22 27525 Ori 0

g
lack of large fibrils at 12 months ete 1 20 250– 0–3 g. A )

st
r nm 30 CL
o
p
postgrafting (arrow 2) should

e
im
be noted.
T
large fibrils remained at the femoral region. This ber of small-diameter fibrils in the deep region at
is reflected if the ratio of large > 100 nm fibrils to 52 weeks not seen in the superficial regions. If one
small < 100 nm fibrils is plotted (Fig. 4.35). plots the ratio of large-diameter fibrils > 100 nm
4 Patellar tendon ACL graft superficial region to small-diameter fibrils < 100 nm, the major
versus deep region. The major observation was fall in the ratio is seen in the superficial region
the complete loss of the large-diameter fibrils at reflecting the complete removal of the large-
1 year from the superficial regions of the graft. diameter fibrils in the superficial regions of the
There was also a concomitant increase in the num- grafts at 52 weeks (Figs 4.32, 4.35 and 4.36).
This study has determined the anatomical

regions of the ACL graft that undergo remodel-
ling and that this process continues for up to
3 years postgrafting. This remodelling process
changes the collagen fibril profile of the original
patellar tendon to one containing a greater pro-
portion of small-diameter fibrils. The remodel-
ling process occurs from the most outer areas
inwards, and is more vigorous in the tibial region
of the graft. This would be consistent with syn-
ovial revascularization. The rapid depletion of
the large fibrils in the grafts as early as 6 weeks
is also consistent with the dramatic decrease
in mechanical and material properties of such
grafts (Fig. 4.35). This collagen fibril study in
the goat also parallels that in the human ACL
patellar tendon grafts and appears to be a use-
ful model to follow collagen remodelling in the
ACL graft.
A 3-year biomechanical and viscoelastic

study of patellar tendon autografts for
ACL reconstruction
In this study, 27 adult female goats were testeda

Fig. 4.36 Representative electron micrographs of four served as controls and the others received
ACL and patellar tendon autografts: (a) at 6 weeks, an autograft to the right knee with each left knee
(b) at 12 weeks, (c) at 24 weeks, and (d) at 52 weeks serving as an additional control (Ng et al. 1995a,
postgrafting. The progressive loss of the large-
1995b). The animals with grafts were tested at
diameter fibrils at t = 0 (see Fig. 4.32b) and the
accumulation of small-diameter fibrils with 0 weeks (n = 4), 6 weeks (n = 4), 12 weeks (n = 4),
increasing graft age should be noted. 24 weeks (n = 3), 1 year (n = 5) and 3 years (n = 3)
after surgery. The AP laxity of the knee joint,
The collagen fibril profile for each time group load–relaxation, and structural and mechanical
was compared to the control ACL and patellar properties of the graft were tested.
tendon with Kolomogorov–Smirnov analyses. The AP laxity was significantly greater than
Differences were found between the patellar that of the controls for all groups except at 3 years
tendon collagen profile with the ACL grafts with where the AP laxity almost approached normal.
the 12-, 24- and 52-week groups (P = 0.005, 0.07 The mechanism of this return of AP laxity to near
and 0.1, respectively). All the grafts except the normal is not known but may be due to stiffening
6-week group contained mainly small fibrils of the collateral ligament complexes or may be
(< 100 nm). The large fibrils were not repopulated due to tibial and femoral condyle remodelling.
in the 1-year grafts, but in the one graft studied Load–relaxation was greater than that of the
at 3 years large fibrils > 100 nm were present. A control ACLs, but in the 1- and 3-year grafts
positive correlation (r = 0.6, P = 0.07) was found load–relaxation was less than that of the patellar
between the percentage of fibrils of > 100 nm tendons with 5 min of sustained loading. Between
diameter with Young’s modulus of the grafts, 12 and 52 weeks, the stiffness and the modulus of
which was tested in a separate study. the grafts were 44 and 49% those of the control
140
120
R/L ultimate strength (%)

Fig. 4.37 Anterior cruciate
ligament (ACL) graft ultimate Control ACL mean ± 1 SD
100
tensile strength (mean and SD) of
the right side (R) expressed as a 80
percentage of that for the left side
(L) for control ACL and grafts at 60
different times after surgery. The a
symbols a and b indicate values 40
that are significantly different a
from the control and 3-year 20 ab
ab ab ab
groups, respectively (P < 0.05).
(From Ng et al. 1995b, with 0
permission from Journal of 0 weeks 6 weeks 12 weeks 24 weeks 1 year 3 years
Orthopaedic Research.) Time postsurgery
120
Fig. 4.38 Young’s modulus 100

(mean and SD) of the right side Control ACL mean ± 1 SD
R/L modulus (%)
(R) expressed as a percentage of 80

that of the left side (L) for control
anterior cruciate ligament (ACL)
60
and ACL grafts at different time a
intervals after surgery. The
40 a
symbols a and b indicate values a a
that are significantly different
20 a
from the control and 3-year a
groups, respectively (P < 0.05).
(From Ng et al. 1995b, with 0
permission from American Journal 0 weesk 6 weeks 12 weeks 24 weeks 1 year 3 years
of Sports Medicine.) Time postsurgery
ligaments, respectively; the modulus was 37 and fibril profile and biochemical changes are not
46% that of the control ACLs and patellar tendons, clear. This study examined goat ACL patellar
respectively (Figs 4.37 and 4.38). The persistent tendon autografts up to 3 years postsurgery for
inferior mechanical performance at 3 years sug- collagen type and hydroxypyridinium (HP)
gests that ACL grafts in the goat may never attain cross-link density (Ng et al. 1995a, 1996a).
normal ACL strength. Twenty-two mature female goats received
an ACL patellar tendon autograft to the right
knee and were tested at 6 weeks (n = 5), 12 weeks
A 3-year study of collagen type and
(n = 4), 24 weeks (n = 5), 1 year (n = 5) and 3 years
cross-links for ACL patellar tendon
(n = 3). Two in each group were assigned for
autografts in a goat model
collagen typing and HP analyses. Two normal
The collagen matrix provides the tensile strength animals served as controls for collagen typing
of ligaments. Previous animal studies have shown and HP analyses.
that ACL patellar tendon autografts contain Type III collagen analyses with SDS gel elec-
mainly small-diameter collagen fibrils (< 100 nm) trophoresis showed an increase from 6 to 24 weeks
at 1 year postsurgery. The long-term collagen and then decreased afterwards. At 3 years, the
500
y = 3.25x + 311.39
Fig. 4.39 The relationship
400
Young’s modulus (MPa)
between hydroxypyridinium
(HP) cross-link density and
Control
Young’s modulus of the ACL
300 Graft
autografts (r = 0.8) and control
y = 5.73x + 13.21 ACL (r = 0.7). A significant
200 positive correlation is shown for
both tissues. The linear regression
lines that predict the Young’s
100 moduli of ACL autografts and
ACL controls from HP cross-link
density are also shown. Hypro,
0 hydroxproline. (From Ng et al.
0 10 20 30 40 1996a, with permission from
HP density (nMHP/mgHypro) Journal of Orthopaedic Research.)
grafts contained similar type III collagen amounts The grafts and control ACLs had comparable
as the control ACL; the collagen was distributed mean hydroxypyridinium cross-link densities but
generally throughout the grafts (not just in the different Young’s moduli, which implies hydro-
perifascicular regions) as in the normal patellar xypyridinium cross-link density is not the only
tendon, as demonstrated by immunofluorescent determinant for material strength. Other factors
labelling of the grafts with specific type III col- such as collagen fibril size, density of packing
lagen antibodies. and orientation may affect the Young’s modulus.
The hydroxypyridinium cross-link density However, the good correlation on regression
was low in the 6-, 12- and 24-week groups, but analysis suggests the hydroxypyridinium cross-
increased in the 1- and 3-year groups. The mean link density may be an important indicator for
hydroxypyridinium cross-link density in the ACL material strength. A previous study in MCL
grafts was similar to the two control ACLs at less scars in rabbits has also demonstrated a positive
than 24 weeks, but at 1 and 3 years the hydro- relationship between hydroxypyridinium cross-
xypyridinium cross-link density was increased link density and the failure stress of ligament
(P < 0.09). The hydroxypyridinium cross-link scar (Frank et al. 1994, 1995). Chan et al. (1998)
density of the left ACL of the unoperated goats have also demonstrated a high correlation with
was higher than the two controls, which could pyridinoline content and failure loads with the
be due to the change in loading to the left knee healing patellar tendon in the rat.
in these animals (Fig. 4.39). A negative correla- These two similar observations in different
tion was found between the percentage type III species and different tissues indicates that hydro-
collagen and Young’s modulus, but this was not xypyridinium cross-link density is one of the
significant. important determinates for the tensile strength
A significant positive correlation (P = 0.01) was of ligament repair and during ACL graft remod-
found between the hydroxypyridinium cross-link elling. We currently do not understand the
density and Young’s modulus in both the ACL biological and mechanical factors that control
grafts (r = 0.8) and controls (r = 0.7). This is the collagen cross-linking and hence clinical therap-
first correlation to be made between a measur- ies to improve and enhance collagen cross-link
able biochemical parameter and a biomechanical density are not yet available. There have been
parameter for ACL grafts and is very important no studies on human ACL graft tissues and the
in determining ACL graft tensile strength. hydroxypyridinium cross-link density to date.
collagen deposition and its remodelling in the

Enhancement of ligament/tendon
early phases of the healing response. The use
repair using tissue engineering
of these cells is still in its early phases although
technologies
results are encouraging (Young et al. 1998; Awad
Because of the long delay in achieving adequate et al. 1999).
tensile strength in ligament and tendon repairs During the healing process in ligaments, Frank
to withstand the imposed tensile forces of daily et al. (1999) noted several specific problems with
living, researchers and clinicians have explored the rabbit MCL scar tissue, which appeared to
means to not only hasten the repair process in have mechanical implications (i.e. flaws, decreased
its three phases (as described above), but also collagen cross-links and persistence of small-
to improve the quality of the repair scar tissue, diameter collagen fibrils). The latter has been
which is known in the adult to be of poor mechan- identified in this chapter as the probable key
ical quality. For example the normal rabbit MCL explanation for the poor biomechanical per-
when cut surgically heals with the usual phases formance of human and goat ACL auto- and
and a hypervascular disorganized scar tissue is allografts. The role of the small leucine-rich pro-
left that is then remodelled over many weeks to teoglycans, such as decorin, fibromodulin and
years. Biomechanical testing of this scar tissue lumican, in controlling collagen fibrillogenesis in
even at 1 year postinjury reveals it to be per- vitro has been well documented. Decorin stands
manently weaker and less stiff than the normal out as an important molecule in controlling colla-
MCL on both a structural and material basis. gen fibril assembly (Vogel & Trotter 1987; Birk
If the two ends of the ligament are opposed by et al. 1995; Weber et al. 1996; Danielson et al. 1997).
sutures after severance and the gap minimized, Based on these and other observations, Frank
the MCL can heal structurally to about 70–80% and his co-workers hypothesized that inhibition
of the strength and structural stiffness of the of decorin expression during the early phases
normal MCL; but if a gap is left the healing is of ligament healing may enhance the size of
about 40–50% of the normal MCL. On a mater- newly synthesized collagen fibrils. They used an
ial basis (i.e. per CSA) in both the opposed and antisense method using binding of oligodeoxy-
gap situations, the scar tissue only reaches a nucleotides to target decorin mRNA in collabora-
maximum of about 30% of normal MCL strength tion with Nakamura et al. (1998). Remarkably,
after years of healing (Frank et al. 1999). using this technology they were able to demon-
The use of growth factors to attempt to enhance strate that most antisense-treated scars contained
the healing phases of ligament and tendon has bundles of aligned collagen with some restora-
been pursued over the last decade since the tion of the normal collagen crimp pattern. Even
isolation of growth factors such as transforming more remarkable was the appearance of large-
growth factor beta (TGF-β), insulin-like growth diameter collagen fibrils in five of the six
factor I (IGF-I) and IGF-II and also basic fibro- antisense-treated scars. Collagen fibril diameter
blast growth factor (bFGF). These growth factors analysis of average collagen fibril sizes for the
have been used both singly and in combinations antisense-treated scars, sense control scars, injec-
using various delivery modes. The results have tion control scars and normal MCL were: 104.7 ±
been rather disappointing in that more collagen 51.1, 74.8 ± 11.00, 78.2 ± 11.9 and 189.1 ± 104.0 nm,
can be deposited but it is not well organized and respectively (Fig. 4.40). Correlated with these
the collagen fibrils are usually of small diameter collagen fibril observations was an increase in
and hence does not lead to any long-term improve- the mechanical quality of the scar tissue. In
ment of the quality of the repair tissue. other words, antisense scars were significantly
The use of mesenchyme stem cells is a useful (18–22%) less susceptible to elongation (creep)
strategy if the matrix synthetic capacity of these during low stress creep testing than both sense
undifferentiated cells can be harnessed to enhance control and injection control scars. They failed at
Fig. 4.40 A composite TEM of

transverse sections of collagen
fibrils in normal adult rabbit MCL
(upper left) versus three 6-week
healing scar groups: injected
decorin ‘sense’ controls (upper
right), injected control scar
(bottom left) and antisense–
decorin treated experimentals
(bottom right). Note that five of
the six antisense-treated 6-week
MCL scars contained some
patches of larger fibrils, as shown
here, whilst none of the control
scars contained any large fibrils.
(From Frank et al. 1999, with
permission from Journal of Science
and Medicine in Sport.)
14.9 ± 6.62 MPa on average, which was signific-

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Chapter 5
Tissue Healing and Repair: Bone and Cartilage

K.-M. CHAN, HENRY C.L. HO AND CHRISTOPHER W.C. TONG
Healing and regeneration of bone ing arterioles, venules, capillaries, nerves and
lymphatics. These whorls are known as Haversian
Structure of bone
systems (Fig. 5.1). The osteocytes form connec-
Bone is a specialized form of connective tissue, tions with each other and are bathed in a limited
which serves the following purposes. and complex interconnecting fluid space called
1 It is a skeletal framework for the body. the canaliculi. In the metaphyseal portion of long
2 It allows the different parts of the body, such bone, the lamellae are also stress orientated but
as the appendages, to move in space through form interlacing pillars called trabeculae, rather
various degrees of freedom by means of joints than Haversian systems, to support loads. Like
controlled by the activity of their attached muscles many tissues in the body, bone is constantly
and stabilized by ligaments. undergoing remodelling in response to the loads
3 It protects the vital organs such as the heart, that it is subjected to. There is a delicate balance
lungs and abdominal viscera from external trauma. between bone formation by osteoblasts and bone
4 It is a source of production for the elements of removal (resorption) by osteoclasts. The rate of
blood.
5 It plays a major part in mineral metabolism.
6 The bone marrow is an important part of the
immune system.
The structure of bone, like that of other con-
nective tissues, is composed of cellular elements
and their surrounding matrix, which is unique
in that it has an organic as well as an inorganic
mineral component. The cells include bone-
forming cells (osteoblasts), bone-resorbing cells
(osteoclasts) and a stable population of main-
tenance cells (osteocytes). The relative activity of
each of these cell types depends on the physio-
logical or pathological state of this unique tissue.
Under normal circumstances, in the absence
of trauma, the osteocytes are lined up neatly in
layers, like the skin of an onion, in the line of
stress to form lamellar bone. In cortical bone of Fig. 5.1 Haversian canals consisting of well-organized
long bone diaphysis, these layers form whorls layers of osteocytes interconnected by a system of
surrounding a central vascular channel contain- canaliculi.
99
remodelling is more pronounced in trabecular cycling, Australian football, basketball, soccer,

bone and less in cortical bone. cricket, netball, rugby, roller skating/blading,
The cells are derived from osteoprogenitor cells, skateboarding and trampolining (Finch et al. 1998).
which are themselves derived from immature Furthermore, sports-related injuries cause signi-
mesenchymal cells of the inner cambium layer of ficant morbidity. In a retrospective study by Shaw
the periosteum and endosteum lining the exter- et al. (1997) on the epidemiology and outcome of
nal and internal surfaces of bone, respectively. 523 tibial diaphyseal fractures in footballers, only
Under special circumstances, such as fractures, 73.9% of the patients had unimpaired sporting
the rate of differentiation from osteoprogenitor function after the injury and the average time to
cells to osteoblasts and osteoclasts is dramatic- return to football was 7–8 months. Therefore, it
ally increased in an attempt to heal the fracture. is unlikely for a player to return to sport in the
The strength of bone is derived from its mat- same season. The crux of the problem lies in the
rix, which is produced and maintained by the optimal time to return to full sporting activity
osteoblasts and osteocytes. The matrix consists of without jeopardizing the structural integrity of
an organic (40% of dry weight) and an inorganic the bone. Fractures may occur in any part of the
(60%) component. The organic component is bone, but specific areas such as those around the
composed of mainly type 1 collagen fibres (90%), major joints will be discussed in greater detail
which are responsible for the tensile strength of since the interplay between early return of joint
bone, proteoglycans for its compressive strength, motion and perfect restoration and healing of the
and other matrix proteins such as osteocalcin articular surface are of paramount importance if
and osteonectin, which are important for the prolong-term osteoarthritis is to be avoided.
motion of bone mineralization. Also present in
trace amounts are growth factors and cytokines
aim and principle of fracture
such as transforming growth factor (TGF-β),
treatment
insulin-like growth factor (IGF) and interleukins
1 and 6 (IL-1 and IL-6), which aid the control of Fractures commonly encountered in athletic activ-
bone cell differentiation, activation, growth and ities, usually arise from repeated stress and are
turnover (Bostrom et al. 2000). commonly treated non-operatively. An example
The inorganic component is the mineral por- is the metatarsal fracture, also known as a march
tion consisting of calcium hydroxyapatite and fracture. However, fractures arising from more
osteocalcium phosphate (brushite), which are major injuries can result in disruptions of larger
trapped in and between collagen molecules. These structures such as the tibial plateau. The tibial
are responsible for the compressive strength of plateau fracture is a good example of an injury
bone. that can have a major impact on an athlete’s career
and can indeed equate to permanent disability.
The major concern here is to achieve accurate
Fractures in sports
reduction of the fracture to restore a normal
Fractures anywhere in the body have serious smooth articular surface followed by stable frac-
implications for the athlete since both the inhibi- ture fixation and to attain bone healing in as
tion from pain and the disruption of skeletal short a time as possible. As soon as bony integ-
framework significantly compromise the func- rity is achieved, weightbearing and mobilization
tion of the affected part. Fractures sustained dur- can begin. Range of motion exercises of the joint
ing sport are common. Templeton et al. (2000) should begin as soon as possible to prevent joint
found that sport accounted for 22.1% of all tibial stiffness; they also have the role of promoting
diaphyseal fractures, of which 79.5% were sus- nutritional delivery and healing in the articular
tained during soccer. In addition, the 10 activities cartilage. Early safe mobilization also promotes
that most commonly lead to injury for all ages are the return of muscle function. While these are the
repair of bone and cartilage 101
basic principles behind the management of more

complex periarticular fractures, the optimum
rehabilitation strategy is yet to be defined.
The healing process of fractures after injury
The process of healing in bone is one of regenera-

tion of bone, in contrast to healing in other tissues
such as muscle where the defective tissue may
be replaced to some degree by scar tissue. Frac-
ture healing is a complex and well-orchestrated
physiological process and much research has been
invested in this field to achieve a better under- Fig. 5.3 Cutting cone: an important functional unit
consisting of leading osteoclasts resorbing bone debris,
standing of the natural pathways so that potential
thus creating a pathway for trailing osteoblasts and
avenues of intervention to promote earlier frac- newly formed vessels to lay down immature bone.
ture healing can be exploited. This has important
therapeutic implications since the main concern
for the athlete is how soon he or she can return to with newly formed bone by the process of endo-
normal sport. chondral ossification. In the case of primary frac-
To understand fracture healing, it is important ture healing, osteoclasts and osteoblasts function
to appreciate the cellular events taking place at to remove bony debris and produce immature
the fracture site (Fig. 5.2). Fracture healing can bone, respectively. This is followed by a vascular
be broadly divided into primary and secondary ingrowth to form the so-called ‘cutting cone’
healing. Primary healing, also known as primary (Fig. 5.3), which eventually leads to the re-
cortical healing, involves a direct attempt by establishment of Haversian systems. This pro-
the cortex to re-establish mechanical continuity. cess of primary fracture healing only takes place
In secondary fracture healing, the periosteum when there is a minimal fracture gap and rigid
containing cells of osteogenic potential and the fracture fixation.
external soft tissues form a callus, which sub- On the other hand, secondary fracture heal-
sequently bridges the fracture gap and undergoes ing, which is the more common mode of healing
cartilaginous changes followed by replacement found in fractures, involves an initial stage of
fracture haematoma formation and the release
Periosteum of important signalling molecules including IL–1
and IL–6, TGF-β and platelet-derived growth
Internal callus Endosteum factor (PDGF). The bone itself also releases PDGF,
TGF-β, IGF-I, IGF-II and bone morphogenic pro-
tein (BMP). These function to orchestrate the vari-
ous complex cellular changes taking place, which
include the proliferation and differentiation of
mesenchymal stem cells found in the periosteum
into osteoblasts. During the first 10 days, these
form new bone directly opposed to the cortex, a
Fracture
Cortical bone process known as intramembranous ossification.
haematoma
External callus At the same time, the bridging callus, which is
Fig. 5.2 Callus at the fracture site consisting of
contributed by the periosteum and external soft
osteoblasts, osteoclasts, newly formed blood vessels tissues, undergoes cartilagenous transformation.
and immature bone and cartilage. At 2 weeks, calcification of the cartilage begins to
take place. This tissue then becomes the target In addition, the amount of strain and hydro-
tissue for vascular ingrowth delivering osteoblasts static pressure applied along the calcified surface
to the area. The extent of this vascular invasion of the fracture gap have also been found to affect
depends very much on the integrity of the sur- the type of bone healing taking place. Using
rounding blood supply to the periosteum, endo- animal models, Claes et al. (1998) discovered that
steum and soft tissue. Newly formed immature for strains of less than 5% and pressures of less
woven bone is laid down while the calcified than 0.15 MPa, predominantly intramembranous
cartilage matrix is digested away by chondroclasts. ossification was seen. Strains between 5 and 15%
With time, under the influence of loading during and hydrostatic pressures greater than 0.15 MPa
rehabilitation, remodelling takes place and woven stimulated endochondral ossification, and larger
bone becomes substituted by mechanically com- strains led to healing by fibrous connective
petent and stress-orientated lamellar bone. tissue. The amount of strain also affected the
production of TGF-β. Increased production was
found for strains of up to 5% and a subsequent
mechanical factors influencing
decrease for larger strains. The amount of strain
the healing process
taking place at the fracture site is clearly depend-
With the above knowledge in mind, one has ent on the type of fixation. A fracture fixed with
to have some evidence on which to devise a re- a plate is much more likely to demonstrate less
habilitation strategy. It is important to recognize strain compared with one fixed with an Ilizarov
those mechanical factors that can promote and ring fixator. Similarly, Augat et al. (1996) studied
retard the natural biology of fracture healing. the effects of early weightbearing after fracture
Only then can the clinician devise a well thought- fixation using more flexible devices in the sheep
out rehabilitation plan that is based on scientific long bone. Although there was an abundance of
rather than anecdotal evidence. early soft callus formation, there was a signific-
Investigators (Cunningham et al. 1998) have ant delay in the healing of the osteotomy site. On
studied the effects of strain rate and timing in the other hand, prevention of early full weight-
the mechanical modulation of fracture healing. bearing and delayed full weightbearing resulted
They studied the effects of applying cyclic inter- in a higher flexural rigidity of the fracture, an
fragmentary micromovement at high and low increased mechanical stiffness of the callus tissue,
strain rates at various stages of healing and dis- and an enhanced bone formation at the healing
covered that a high strain rate, similar to that front (Augat et al. 1996).
obtained during brisk walking, induces a greater The amount of stability that a fixation device
amount of callus formation during the early imparts to a fracture will determine the optimum
phase of healing but significantly inhibits heal- time to begin loading across the fractured bone.
ing in the later period (6 weeks after fracture). Sarmiento and Latta (1999) showed the beneficial
They also predict that in the later (hard callus) effects of early weightbearing on fracture heal-
phase, tissue damage may occur under abnor- ing in their studies on rats and indeed con-
mally high stresses and strains and recommend firmed Wolff’s hypothesis that mechanical loading
increasing the rigidity of fracture fixation until stimulates an osteogenic response in bone. The
the fracture has healed. It has been suggested exact mechanism by which such mechanical influ-
that as healing progresses, the rigidity of the ences act is still not defined but is certainly a
fixation system should be increased in order to fascinating area deserving further research. While
minimize such excessive strains (Kenwright & recognizing the limitations of research models, one
Gardener 1998). This can be achieved in clinical must remain critical about such data and question
practice by the process of dynamization, whereby their validity when applied to clinical situations.
the fracture ends are jammed together further For example, much of the research has been on
as the patient bears weight. animal experiments and the fracture pattern and
behaviour may be quite different to that occurring non-union in the relatively less well vascularized
in humans. The surgical method and technique distal tibial shaft fractures. The much better vas-
of fracture fixation also influence the stability cularized metaphysis, on the other hand, nearly
of the osteosynthesis and affects the surgeon’s always heals uneventfully.
preferred method of rehabilitation. Therefore, the Therefore, in a tibial plateau fracture, the fixa-
results of research experiments can only serve as tion method usually now involves arthroscopic-
a guide to the biological events taking place in a ally assisted reduction of the articular surface and
patient and cannot be strictly extrapolated. percutaneous screw fixation supplemented by an
The current practice of fracture fixation has external ring fixator. Few would advocate open
now moved away from absolute rigid fixation reduction and plating of such injuries. Indeed, if
using compression plates and rigid statically plating is necessary, such as in long bone frac-
locked intramedullary nails to one of stable fixa- tures of the forearm, minimally invasive tech-
tion allowing some micromovement to take place niques are being developed to slide the plate
to stimulate early callus formation (Fig. 5.4). under the soft tissue after making a much smaller
Indeed, some of the inherently more stable surgical wound. Plates such as the low-contact
fractures such as the simple and minimally com- dynamic compression plate have also been
minuted tibial shaft fractures may be treated designed with the aim of reducing the amount
primarily by a functional brace, allowing early of pressure applied to the underlying periosteum
weightbearing to stimulate micromotion. This and bone to minimize ischaemia.
method obviously spares the patient a surgical
procedure, such as intramedullary nail fixation,
Management of fracture
and its surgical risks and allows a shorter rehab-
ilitation time (Sarmiento & Latta 1999). Further- Although surgical stabilization and anatomical
more, the subsequent shortening and deformity realignment remain the mainstay of treatment
found when bracing is used in the treatment of of most displaced fractures, it is still important
less stable tibial fractures might be functionally to realize that the ultimate goal is to achieve
insignificant (Sarmiento & Latta 1999). solid bone union as early as possible. One must
have the armamentarium to treat delayed or
established non-unions and the assessment of
biological factors influencing the
such challenging problems is a test of one’s
healing process
understanding of the biological requirements of
In addition to using less rigid forms of fracture healing. Apart from surgical means of promoting
fixation, there is a growing trend towards using union, such as bone grafting and bone marrow
minimal fixation. Apart from the mechanical injection to reactivate the healing process, non-
factors mentioned above, it is important to bear surgical methods, if found to be equally effective,
in mind that the chosen method of fixation must would generally be the patient’s choice.
respect the local blood supply to the fracture Future research is directed at investigating such
because healing will not take place in the absence newer non-surgical methods. An example of an
of an adequate blood supply due to a paucity already widely used tool is ultrasound stimula-
of cellular elements and growth factors at the tion (US). This technique was first introduced
fracture site. The fixation device will ultimately by Duarte in 1983 and its effects have been con-
fail if there is non-union of the fracture. Minimal firmed in animal and clinical studies (Duarte 1983).
fixation preserves the possibly already trauma- However, the exact mechanism is still unknown,
tized soft tissue envelope to the underlying bone but a stimulation of the expression of numerous
and simultaneously allows more micromotion. genes involved in the healing process includ-
The importance of a good blood supply is ing those encoding for aggrecan, IGF and TGF-β
exemplified by the preponderance of fracture have been demonstrated (Hadjiargyrou et al.
(c)
(a)
(b) (d)
Fig. 5.4 (a) External fixator in situ to hold a comminuted tibial plateau fracture reduced. A minimally invasive
technique of stable fracture fixation. (b) External fixator holding tibial plateau fracture reduced. (c) Sarmiento
brace is useful for the treatment of tibial shaft fractures. (d) Intramedullary nail providing rigid internal fixation
for tibial shaft fracture.
1998). An increase in the formation of soft callus Similarly, using a rat model, Sakai et al. (1999)
formation and an earlier onset of endochondral applied a protein called activin, a member of
ossification have been observed (Wang et al. the TGF-β family, topically to fibular fractures
1994). In one animal study, US treatment resulted and demonstrated a dose-related increase in the
in a 1.5 times increase in the mean acceleration of callus volume and callus weight. An increase in
fracture healing (Pilla et al. 1990). Heckman et al. the callus strength was also observed.
(1994) reported a significant reduction in heal- Research is currently taking place in order to
ing time in their multicentre, randomized, con- discover the factors that have important signal-
trolled clinical trial using low-intensity ultrasound ling properties in these complex cellular events,
for 20 min per day during the first week after as these may lead to new insights into the future
a fracture. The use of ultrasound for the healing development of new techniques for promoting
of fresh fractures has been approved by the fracture healing. One such example is BMP, which
American Food and Drug Administration. appears to be a subset of the TGF superfamily,
Similarly, pulsed electromagnetic and elec- and has an important role in early intramem-
tric fields have also been found to accelerate branous ossification and in the differentiation of
fresh fracture healing and augment healing in mesenchymal cells into chondrocytes by yet to
delayed union. It is believed that an exogenous be defined mechanisms. BMPs were discovered
electrical field applied at the fracture site can by Urist in 1965 (Urist 1965). They are present in
induce a mechanotransductive effect similar to many tissues, such as the kidney, peripheral and
that observed when bone is subjected to mechan- central nervous systems and the cardiorespira-
ical stress. Its use in clinical practice began in the tory system. Johnson and colleagues demon-
1970s. Deibert et al. (1994) demonstrated a 55– strated encouraging clinical results in 30 patients
299% increase in strength of healed rabbit fibula for the treatment of non-union and segmental
that were subjected to daily ion resonance elec- bone defects using human BMP extracted from
tromagnetic field stimulation. The exact cellular human bone incorporated into allografts to form
pathways responsible for this effect have not been a composite (Johnson & Urist 2000). However,
well defined, but a stimulation of the secretion of large clinical trials are still lacking and the
numerous growth factors such as BMP-2, BMP-4, doses of BMP in these trials are far higher than
TGF-β and IGF-II in vitro have been demon- that found in bone, leading to fears of inducing
strated. Sedel et al. (1981) have extensively invest- malignant change.
igated the use of electromagnetic fields in the With so much still unknown to us, formulating
treatment of delayed union and non-union. Ryaby the perfect rehabilitation programme for a par-
(1998) achieved an efficacy rate of 64–87% in the ticular fracture is very difficult. It is still very
treatment of non-union of the tibia. However, much subject to the orthopaedic surgeon’s per-
large controlled, randomized, double-blind clin- sonal training and experience and the behaviour
ical trials are currently lacking. of the fracture as well as the patient’s compli-
In terms of pharmacological treatment, the ance. Understanding the complex cellular and
potential clinical application of L-dopa, parathy- biomechanical processes of fracture regeneration
roid hormone, bisphosphonates and zinc com- helps us institute rehabilitation based on con-
pounds, as well as the many different growth crete scientific evidence. However, there is no
factors, in promoting fracture regeneration are cookbook approach to any single fracture. The
under extensive investigation. To cite a few interpatient biology is bound to be different and,
examples, a study by Holzer et al. (1999) showed therefore, the healing ability is likely to be differ-
that parentally administered parathyroid hor- ent as well. Thus, the progress of any fracture heal-
mone to mid-diaphyseal fractures of rat femurs ing is still likely to be monitored by radiological
increased the callus area and strength and the means. However, the correlation between radio-
bone density, thus calling for clinical trials in its logica progress and actual mechanical strength
use in healing fractures that are slow to heal. of the bone may be difficult to establish. This, of
course, poses further problems when one is become chondrocytes when they become iso-
designing clinical studies comparing different lated in lacunae, and the chondrocytes receive
methods of rehabilitation. Furthermore, the their nutritional support from the surrounding
forces acting through any part of the body at any synovial fluid. Chondrocytes in skeletally mature
one time cannot be measured easily. Such uncer- articular cartilage do not divide but still remain
tainties are reflected by the numerous opinions alive via the glycolytic anaerobic metabolism path-
available regarding the rehabilitation of a fracture. way. As chondrocytes age, they exhibit a decrease
For example, for a given lower limb fracture, one in cellular activity, especially in the production
surgeon may advise non-weightbearing mobil- of collagen and proteoglycan. The function of
ization whilst another may advise touch-down chondrocytes is to maintain the correct internal
walking. To date, such advice cannot be sup- milieu of articular cartilage. They synthesize and
ported by any sound scientific evidence and to maintain the various components of the matrix of
conduct well-controlled prospective studies pre- articular cartilage. This includes the production
sents a major scientific challenge. of collagen, proteoglycans and non-collagenous
proteins as well as enzymes (Mankin et al. 1994).
They maintain the balance of synthesis and
Healing and regeneration of
degradation of the protein macromolecular com-
articular cartilage
plex (Buckwalter & Mankin 1997).
Structure of articular cartilage

collagen
Articular cartilage plays a vital role in the
function of the musculoskeletal system by allow- Collagen contributes around 10% of the wet
ing almost frictionless motion to occur between weight of articular cartilage. The predominant
the articular surfaces of a diarthrodial joint. collagen type in articular cartilage, accounting
Furthermore, articular cartilage distributes the for 90–95%, is type II collagen, while types VI,
loads of articulation over a larger contact area, XI, X and XI are also found to lesser extents.
thereby minimizing the contact stresses, and Collagen is spread throughout the ground sub-
dissipating the energy associated with the stance in the extracellular matrix and is formed
load. These properties also allow the potential by three polypeptide chains that are cross-linked
for articular cartilage to remain healthy and covalently (Eyre 1980). Collagen fibres do not have
fully functional throughout the decades of life a large resistance to compression due to their
despite the very slow turnover rate of its collagen slenderness ratio. However, they are very strong
matrix. in tension and are the primary component of
The composition of articular cartilage consists cartilage, responsible for providing its tensile
of cells (chondrocytes), matrix proteins includ- properties (Roth & Mow 1980) Articular cartilage
ing collagen and proteoglycans, non-collagenous is composed of distinct layers where the col-
proteins, water and electrolytes. lagen fibres have different patterns of orientation
(Fig. 5.5). These layers include the superficial
zone, middle zone, deep zone, tidemark and cal-
chondrocytes
cified zone. In the superficial zone, collagen fibres
The basic building blocks of the articular surface are arranged in a parallel fashion relative to the
are the chondrocytes, which constitute around joint surface. In the middle zone, collagen fibres
5–10% of the wet weight of articular cartilage. are arranged in a criss-cross oblique fashion. In
Chondrocytes originate from undifferentiated the deep zone collagen fibres are arranged per-
mesenchymal marrow stem cells. These cells in pendicular to the joint surface (Redler 1974). The
turn progress through the calcified cartilage zone tidemark is the boundary between the deep zone
to become chondroblasts. The chondroblasts and the zone of calcified cartilage.
Chondrocyte appearance Collagen orientation Zones
Superficial
Middle
Deep
Tidemark
Calcified
layer
Bone
Fig. 5.5 Basic microstructural
anatomy of articular cartilage.
Collagen fibril
proteoglycans
Proteoglycans contribute around 10% of the wet

weight of articular cartilage. Proteoglycans are
composed of a protein core to which are attached Aggrecan
many extended polysaccharide units called gly-
cosaminoglycans (Muir 1983). The two main
glycosaminoglycans found in articular cartilage
are chondroitin sulphate and keratan sulphate.
The vast majority of proteoglycans found in
articular cartilage are known as aggregans, which
bind with hyaluronan to form a large proteo-
glycan aggregate (Fig. 5.6). Chondrocytes produce
aggrecan, link protein and hyaluronan, which are
secreted into the extracellular matrix where they
aggregate spontaneously (Muir 1983). The pro-
teoglycan molecules contain repeating sulphate Hyaluronic acid
and carboxylate groups along their chains. These
Fig. 5.6 This schematic diagram illustrates the
groups become negatively charged when placed in interaction between the collagen molecules and the
an aqueous solution. This negative charge attracts proteoglycan molecules in the articular cartilage
water molecules, which exerts a large swelling extracellular matrix.
pressure and thus a tensile stress on the surround- Rosenwasser 1988). When a load is applied slowly
ing collagen network (Maroudas 1976). to the cartilage, the fluid movement within
The proteoglycan molecules are the main com- the cartilage allows the cartilage to deform and
ponents in articular cartilage, providing resist- decreases the force applied to the matrix macro-
ance to compression forces within the articular molecular framework. When a load is applied
cartilage. The balance of expanding total swell- too rapidly, as occurs with a sudden impact or
ing pressure exerted by the proteoglycans and torsional joint loading of the joint surface, it may
the constraining tensile force developed within rupture the matrix macromolecular framework,
the surrounding collagen network determines the damage cells and exceed the ability of articular
degree of hydration in cartilage. A disruption of cartilage to prevent subchondral bone damage
this balance, resulting from damage to the articu- by dampening and distributing loads.
lar surface collagen network, has been shown to Experimental studies have shown that blunt
cause increased tissue hydration and significantly trauma can damage articular cartilage and the
changes the ability of the articular cartilage to calcified cartilage–subchondral bone region, while
bear loads (Setton et al. 1993). leaving the articular surface intact (Donohue
et al. 1983). Physiological levels of joint loading
do not appear to cause joint injury, but impact
Mechanism of injury of articular cartilage
loading above that associated with normal activ-
Direct blunt trauma, indirect impact loading ities, but less than that required to produce
or torsional loading of a joint can damage the cartilage disruption, can cause alterations of the
articular cartilage and the calcified cartilage– cartilage matrix.
subchondral bone region without disrupting the
surrounding soft tissues. Examples of direct blunt
Types of chondral and osteochondral injury
trauma include falling from a height or striking a
and their potential for healing
joint with a large hard object. Examples of indir-
ect impact and torsional loading include a blow The response of articular cartilage to injury
to a bone that forms the subchondral part of a and the subsequent healing response incurred
joint or severe twisting of a joint that is loaded. depends to a large extent on the type of cartilage
Unfortunately, these injuries occur frequently injuries. Cartilage injuries can be divided into
in people taking part in sports and are hard to three main types: (i) chondral damage without
diagnose. The amount of cartilage damage from visible tissue disruption; (ii) disruption of the
a given load depends on how rapidly this load articular cartilage alone with sparing of the under-
is applied. Slowly applied loads and suddenly lying subchondral bone (an example of this would
applied loads differ considerably in their effects. be the chondral flap injury); and (iii) articular
As mentioned previously, the articular cartil- cartilage injury involving the underlying sub-
age extracellular matrix consists of water and a chondral bone (i.e. osteochondral fractures). The
macromolecular framework formed primarily of intensity and rate of muscle contraction affect the
collagens and large aggregating proteoglycans. transmission of force to the articular cartilage.
The collagens give the tissue its form and tensile Age and genetic factors may influence the type of
strength, and the interaction of aggregating pro- articular cartilage injury sustained by a particu-
teoglycans with water gives the articular cartilage lar individual (Buckwalter et al. 1996).
its stiffness to compression, resilience and prob-
ably its durability. When the cartilage surface is
matrix and cell injuries
loaded, fluid movement occurs within and out
of the cartilage matrix. This movement of fluid These are injuries where there is a damage to
serves to dampen and distribute loads within the the chondral matrix and/or cells and/or sub-
cartilage and to the subchondral bone (Mow & chondral bone without visible disruption of the
articular surface. The proteoglycan content may

Classification of articular cartilage injuries
decrease with a concomitant disruption of the
collagen fibril network. If the basic matrix struc- The grading system devised by Outerbridge
ture remains intact and enough viable cells (1961) is a simple working tool for describing
remain, the cells can restore the normal tissue chondral lesions (Fig. 5.7). In grade I, the articu-
composition. However, if there is significant lar surface is swollen and soft and may be
damage to the matrix or cell population, or if the blistered. Grade II is characterized by the pres-
tissue sustains further damage, then the lesion ence of fissures and clefts measuring less than
may progress to cartilage degeneration. 1 cm in diameter. Grade III is characterized by
the presence of deep fissures extending to the
subchondral bone and measuring more than
chondral fractures and
1 cm in diameter. Loose flaps and joint debris
chondral flaps
may also be noted. In grade IV, subchondral bone
These are macroscopic disruptions to the articu- is exposed.
lar cartilage tissue without involvement of the
subchondral bone. No fibrin clot or inflamma-
Treatment modalities of articular
tory responses occur. The chondrocytes, how-
cartilage injuries
ever, will proliferate and synthesize new matrix
macromolecules. New tissue does not fill the Various methods have been used to enhance
cartilage gap. Depending on the location and size the healing and repair of articular cartilage
of the lesion and the structural integrity, stability injuries. These include: (i) arthroscopic lavage
and alignment of the joint, the lesion may or may and debridement; (ii) marrow stimulation tech-
not progress to cartilage degeneration. niques such as drilling, abrasion arthroplasty and
microfracture; (iii) osteochondral autografting;
and (iv) autologous chondrocyte implantation.
osteochondral fractures
The postoperative rehabilitation programme will
Injuries which involve the articular cartilage and vary depending on the method of treatment for
the underlying subchondral bone will elicit an the articular cartilage defect.
inflammatory and bleeding response from the
injured subchondral bone (Buckwalter et al. 1990).
arthroscopic lavage and
A clot will form in the subchondral bone defect
debridement
and to various depths of the cartilage defect.
This fibrin clot consists of mesenchymal stems Arthroscopic lavage and debridement have been
cell that will differentiate into cartilage-forming shown to produce measurable symptomatic im-
cells. Platelets within the clot release vasoactive provement (Hubbard 1996, Levy et al. 1996). In
mediators and growth factors or cytokines, includ- a study by Levy et al. (1996), it was noted that
ing TGF-β and PDGF (Buckwalter et al. 1996). debridement for acute small lesions (average size
Release of these growth factors appears to have 42 mm2) in 15 young soccer players allowed all
an important role in the repair of osteochondral players to return to soccer at 10.8 weeks after
defects. In particular, they probably stimulate vas- surgery, with six excellent and nine good results.
cular invasion and migration of undifferentiated However, the follow-up was short: only 1 year.
cells into the clot and influence the proliferative Hubbard (1996) noted that grade IV femoral con-
and synthetic activities of the cells. However, dyle lesions randomized to arthroscopic lavage
the repair tissue formed by these cells does not versus debridement did better when debrided.
have the structural and biomechanical properties The Lysholm scale score increased 28 points at
of articular hyaline cartilage but rather has prop- 1 year and 21 points at 5 years in over 50% of
erties resembling those of fibrocartilage. patients. The defect size was not measured and
Grade I Grade II
Fig. 5.7 Outerbridge classification

of articular cartilage injury. Grade
I: Softening of the articular
cartilage. Grade II: Superficial
fibrillation of the articular
cartilage. Grade III: Deep fissures
extending to the subchondral
bone. Grade IV: Exposure of
Grade III Grade IV subchondral bone.
radiographic evidence of progression or follow- their function is to allow pluripotent cells from
up arthroscopy was not performed in this study. the underlying marrow to enter the defect and
initiate a repair process. The advantages of the
microfracture technique is that it is a simple
marrow stimulation procedures:
procedure amenable to all surgeons who per-
microfracture and drilling
form arthroscopic work. The cost is low as no
The underlying principles of the various marrow sophisticated instruments or laboratory proced-
stimulation techniques are similar. The concept ures are required. The use of a microfracture
is that the subchondral bone is breached (either pick to breach the subchondral bone rather than
with a drill or a microfracture pick) resulting in using a drill should result in less thermal damage
an inflammatory response; the resultant fibrin and cellular necrosis.
clot that forms will bring in mesenchymal stems Steadman reported his 3–5 year results using
cells, cytokines and growth factors, which will the microfracture technique (Steadman et al. 1997).
lead to a repair response in the articular cartilage He noted pain relief in 75% of patients with 20%
defect. The repair material, however, is primarily unchanged and 5% made worse. When it came
fibrocartilage. Recently, the technique of micro- to functionality and activities of daily living and
fracture has gained considerable popularity: the work, 67% improved, 20% were unchanged and
chondral defect is first debrided arthroscopically 13% were made worse. Sixty-five per cent were
to a stable cartilage rim and any loose flaps of able to return to strenuous work and sports.
cartilage are removed. The calcified cartilage layer Recommendations for postoperative rehabili-
is removed by means of a curette paying atten- tation programmes after microfracture include
tion not to violate the underlying subchondral protected weightbearing for 6–8 weeks and
bone. Arthroscopic surgical picks are then used to passive mobilization with a continuous passive
make multiple holes in the exposed subchondral mobilization (CPM) machine for 8 weeks. The
bone. These holes are made 2–3 mm apart and benefits of CPM in the treatment of chondral
defects using microfracture have been docu- Gambella and Glousman (1999) reported good
mented by Rodrigo and Steadman (1994) Post- to excellent results in a group of 150 patients
operative weightbearing status depends on the treated with osteochondral grafting who had
location of the lesion. Patellar and trochlear grove isolated medial and lateral femoral condyle
lesions may be weightbearing and can tolerate and trochlear lesions. All physical examination
a hinged knee brace with a 30° flexion stop. parameters, including range of motion, effu-
Patients come out of the brace when they are sion, tenderness and crepitation improved over
not weightbearing and go into a CPM machine time. Outcomes were adversely affected by
from 10° to 90° for at least 8 h·day–1 (mostly at poor mechanical alignment and patellofemoral
night). If the chondral defect is in the medial or chondromalacia. Second-look arthroscopies and
lateral compartment, the patient is kept strictly to histological biopsies were also performed and
touch-down weightbearing, with a similar CPM showed hyaline-like cartilage surfaces.
protocol as used in patellofemoral lesions. The After osteochondral autograft transplantation,
CPM machine is set at 1 cycle per minute with the the patient is encouraged to move the knee in
largest range of motion that the patient finds a hinged brace through an unrestricted range
comfortable. Following the 6–8-week period of of motion but is strictly non-weightbearing for
protected weightbearing, patients are instructed the first 6 weeks after surgery. After satisfactory
to begin active range of motion exercises and assessment the patient can begin to gradually
progress to full weightbearing. No cutting, twist- weightbear as tolerated. Graft healing is assessed
ing or jumping sports are allowed until at least both clinically and by 3-monthly serial cartilage-
4 months after surgery. specific magnetic resonance imaging (MRI) scans.
Patients are only allowed to return to full sport-
ing activities after MRI evidence of full healing
osteochondral autograft
has been obtained.
transplantation
Osteochondral autograft transplantation involves

autologous chondrocyte
the harvesting of small osteochondral plugs from
implantation
the non-weightbearing portions of the knee and
these plugs are transplanted into the cartilage In larger lesions, surgical resurfacing using
defect in the weightbearing part of the knee. Most autograft transfer can be a significant challenge.
investigators agree that lesions < 2 cm2 are most Restoration of articular surface in lesions > 2.5–
suitable so that donor site morbidity is avoided 3 cm2 and up to 10–15 cm2 can be accomplished
(Bobic 1996). The advantages of osteochondral by autologous chondrocyte implantation (ACI)
grafting include a mature cartilage–bone unit (Brittberg et al. 1994, Minas & Peterson 1999). The
transfer with rapid bone healing and a subsequent technique of ACI involves a two-stage operation
return to high-level function. The disadvant- in the treatment of articular cartilage lesions. The
ages include the technical difficulty in restoring first operation consists of arthroscopic surgery
the biconvex geometric congruity of the femoral where the cartilage lesion is clearly defined and a
condyle in the sagittal and coronal planes and sample of cartilage is harvested from the non-
the potential damage imparted to the cartilagin- weightbearing area of the knee (usually over the
ous cap of the individual plugs, dependent on lateral femoral ridge). This cartilage tissue is then
the force required for insertion. Other questions sent to the laboratory where cartilage cells are
regarding this technique remain unanswered. grown and multiplied. The patient then under-
Concerns include the possible donor site morbid- goes a second operation, which is an open pro-
ity relating to the harvest of the osteochondral cedure around 6 weeks after the first operation.
plugs, and the fact that the tissue formed between The harvested cells are then transplanted into
the osteochondral plugs is fibrocartilage rather the cartilage defect and the defect is covered
than articular cartilage. with a piece of periosteum harvested from the
proximal tibia. A hyaline cartilage repair tissue

eventually fills the cartilage defect. The advant-
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PA R T 3
PRACTICAL ISSUES
Chapter 6
Physiological and Performance Consequences of

Training Cessation in Athletes: Detraining
IÑIGO MUJIKA AND SABINO PADILLA
Athletes themelves, coaches, physicians and

Introduction
all professionals implicated in the process of
Sports injuries are an unwanted but often inevit- getting an injured athlete back on the sports
able component of competitive sports. Through- field should be aware of the physiological and
out their careers, most athletes will experience performance consequences of training stoppage.
sport-related injuries that will keep them away Keeping these in mind during all three phases of
from training and competition for variable the rehabilitation process contributes to limiting
periods of time. In addition to the injury-related the negative functional impact of the inactivity
functional impairment that the athlete will suf- associated with the sports injury, and therefore
fer, these periods of training cessation will also accelerates the recovery of preinjury fitness and
have a negative impact on his or her physiolo- performance level.
gical status and performance level. Indeed, the This chapter focuses on the detraining char-
principle of training reversibility or detraining acteristics of highly trained athletes. However,
implies that whereas regular exercise training when scientific data for highly trained athletes
brings about or preserves specific adaptations are lacking or insufficient, available results on
that enhance a subject’s ability to tolerate the moderately or recently trained subjects that might
stress factors arising from training, and ultim- shed some light on different detraining-related
ately athletic performance (Gollnick et al. 1984; issues will also be reported. In this respect,
Houston 1986; Coyle 1988; Tidow 1995), training readers should bear in mind that detraining
cessation results in a partial or complete reversal characteristics may not necessarily be identical in
of these adaptations, which compromise athletic these two types of population (Lacour & Denis
performance (Coyle 1988; Hawley & Burke 1998; 1984; Hawley 1987; Moore et al. 1987; Coyle 1988;
Mujika & Padilla 2000a, 2001a). Recent reviews Neufer 1989; Coyle 1990; Fleck 1994; Wilber
on detraining define this term as the partial or & Moffatt 1994; Mujika & Padilla 2000a, 2000b,
complete loss of training-induced anatomical, 2001a, 2001b), and that observations made on
physiological and performance adaptations, as laboratory-based training/detraining paradigms
a consequence of training reduction or cessation may not be directly extrapolated to athletes
(Mujika & Padilla 2000a, 2001a). This defini- approaching their higher limits of adaptation.
tion differentiates the process through which a
trained individual loses some or all of his or her
Cardiorespiratory consequences of
training-induced adaptations (e.g. reduced train-
training cessation
ing, training cessation, bed rest confinement) and
the lost adaptations themselves, which are the Athletes in general, and endurance-trained ath-
outcome of that process. letes in particular, are characterized by quite
117
118 practical issues
impressive functional adaptations of their cardio- that 3–8 weeks of physical deconditioning in
vascular and respiratory systems. However, it highly trained subjects brought about a 20%
has often been reported that when the training reduction of Vo2max. Similar results have been
stimulus is lacking or insufficient to maintain repeatedly reported in team sport athletes. Male
training-induced adaptations, such as during basketball players not training for 4 weeks once
phases one and two of the rehabilitation pro- their competitive season was over showed a
cess, there is a marked negative impact on 13.8% Vo2max reduction (Ghosh et al. 1987), and
these systems (Lacour & Denis 1984; Sjøgaard 11 college soccer players decreased their Vo2max
1984; Hawley 1987; Coyle 1988, 1990; Fleck 1994; by 6.9% during 5 weeks of training cessation
Wilber & Moffatt 1994; Mujika & Padilla 2000a, (Fardy 1969). Smorawinski et al. (2001) have
2000b, 2001a). recently shown a 16.5 and 10.4% Vo2max reduc-
tion in amateur cyclists and bodybuilders,
respectively, as a result of 3 days of bed rest.
Maximal oxygen uptake
Conflicting results, however, are not lacking in
Maximal oxygen uptake (Vo2max) is a function the exercise science literature. Fifteen distance
of maximal delivery and utilization of oxygen. runners were shown to maintain Vo2max after 10
‘Central’ oxygen delivery depends on maximal days of training cessation (Cullinane et al. 1986).
cardiac output and maximal arterial oxygen The same was proven true for a group of trained
content, whereas ‘peripheral’ extraction of the cyclists and runners who also stopped training
delivered oxygen is expressed as the arterial– for 10 days (Heath et al. 1983), a group of female
venous oxygen difference (Sutton 1992). All college swimmers not training for a similar period
‘central’ factors implicated in the oxygen trans- of time (Claude & Sharp 1991) and a group of
port system are likely to be affected by training soccer players after 3 weeks of training stoppage
cessation and suffer some degree of detraining. (Bangsbo & Mizuno 1988). These conflicting
According to data reported in the literature, results could be partly explained by the different
training cessation induces a rapid reduction levels of physical activity performed by the
in maximal oxygen uptake (Vo2max) in highly athletes during the period of training stoppage.
trained individuals with a large aerobic power Time and initial fitness level seem to deter-
(> 62 mL·kg–1·min–1) and an extensive training mine the Vo2max loss during periods of training
background (Moore et al. 1987), even when train- cessation. Indeed, seven endurance-trained sub-
ing stoppage lasts less than 4 weeks. Indeed, jects stopped training for 84 days, and their
Houston et al. (1979) showed that 15 days of Vo2max declined by 7 and 16% in 21 and 56 days,
inactivity (7 days of leg casting followed by respectively, it then stabilized at that level, which
8 days without training) led to 4% reductions was still 17.3% higher than that of sedentary con-
in Vo2max in well-trained endurance runners. trol subjects. A correlation of 0.93 was observed
Vo2max also decreased by 4.7% in a group of between Vo2max in the trained state and per cent
endurance-trained runners who refrained from Vo2max decline with inactivity (Coyle et al. 1984).
training for 14 days (Houmard et al. 1992, 1993). Pavlik et al. (1986a, 1986b) reported on 40 obser-
Coyle et al. (1986) studied eight endurance- vations referring to highly trained road cyclists
trained subjects who stopped training for 2 or and endurance runners who, for various reasons,
4 weeks, and reported 6% Vo2max declines during stopped training for 60 days. They observed a
upright exercise. Even more pronounced results linear decline in the athletes’ Vo2max (r = –0.55)
were observed by Mankowitz et al. (1992), who throughout the initial 45 days of training stop-
reported a 12% decline in Vo2max during 14–22 page, with no further change thereafter. Sinacore
days of training stoppage in a group of trained et al. (1993) reported on five male and one female
runners, and by Martin et al. (1986), who indicated endurance-trained subjects who stopped training
consequences of detraining 119
30 long-term training, but it might also be due to the

r = 0.84
Reduction in VO2max (%)
25 P < 0.0001 inherent, genetically determined physiological

capabilities of these athletes (Wilber & Moffatt
20 1994).
·
15
10 Blood volume
5 The observed reduction in cardiovascular func-
0 tion during short periods of training cessation
(see Fig. 6.2) can to a large extent be attributed
0 10 20 30 40 50 60 70 80 90 100
to a decline in blood volume, which may be
Days of training cessation
apparent within the first 2 days of inactivity
Fig. 6.1 Third degree polynomial regression (Thompson et al. 1984; Cullinane et al. 1986).
between the number of days of training cessation Houmard et al. (1992) considered that part of the
and the percentage loss in maximal oxygen uptake reduction in Vo2max observed in a group of dis-
(Vo2max) in athletes, according to data reported
in the literature.
tance runners after 14 days of training with-
drawal was due to a 5.1% reduction in estimated
resting plasma volume. Identical 5% decreases
for 12 weeks. Vo2max declined by 17.1%, and this in plasma volume have been observed by other
decline was greatest in those subjects with the authors in distance runners who ceased training
highest initial Vo2max values. Smorawinski et al. for 10 days (Thompson et al. 1984; Cullinane et al.
(2001) also observed a relationship between the 1986). Moreover, eight endurance athletes who
initial Vo2max and the decrement in its value refrained from training for 2 or 4 weeks were
(r = 0.73) in amateur cyclists and bodybuilders reported to suffer 9 and 12% declines in blood
confined to rest in bed for 3 days. Very long-term and plasma volumes during upright exercise,
(2 years) training cessation has also been shown respectively (Coyle et al. 1986).
to be characterized by Vo2max declines of 6.3% in The mechanisms responsible for these declines
college badminton players (Miyamura & Ishida have not been clearly established. However,
1990). marked reductions in plasma protein content are
These and other similar reported data likely to play an important part. In a study with
(Drinkwater & Horvath 1972; Nemeth & Lowry previously untrained individuals as subjects, 16
1984; Coyle et al. 1985; Martin et al. 1986; Allen young males underwent 4 weeks of endurance
1989; Giada et al. 1995; Katzel et al. 1997; Nichols training and heat acclimatization followed by
et al. 2000) indicate that the Vo2max of highly 4 weeks of training stoppage. The latter resulted
trained athletes decreases progressively and pro- in reduced Vo2max (3.6%) and blood volume
portionally to the initial Vo2max during the initial (4.7%). Red cell volume decreased by 98 mL,
8 weeks of training cessation, this decline usually plasma volume by 248 mL, total plasma protein
ranging between 4 and 20%. Most investigations, by 16 g and plasma albumin by 12 g. Moreover,
however, indicate that Vo2max ceases to decline plasma volume changes were directly related
thereafter (Fig. 6.1) and remains higher than that to plasma protein dynamics, as loss of protein
of untrained counterparts (Fardy 1969; Coyle appeared to be responsible for 97% of the reduc-
et al. 1984, 1985), although one study reported tion in plasma volume (Pivarnik & Senay 1986).
that their subjects’ Vo2max fell down to sedentary In addition, 6 days of training cessation have been
values (Drinkwater & Horvath 1972). This par- shown to fully reverse the effects of short-term
tial retention of Vo2max by highly trained ath- training (6 days) on resting plasma volume and
letes may be due to the accumulated effect of concentrations of aldosterone and adrenaline
(epinephrine) during submaximal intensity 90% of Vo2max) increased by 11 beats·min–1 in

exercise, but not those of arginine vasopressin. a group of endurance runners after 14 days
According to the authors of the study, these without training (Houmard et al. 1992). Madsen
observations implicate plasma volume as a signi- et al. (1993) also observed heart rates of 6–7
ficant variable in modifying the exercise response beats·min–1 higher at submaximal exercise intens-
of fluid and electrolyte hormones (Shoemaker ities after 4 weeks of insufficient training stimulus
et al. 1998). In contrast, Raven et al. (1998) reported in nine endurance athletes.
that a reduction of daily aerobic activity (active Changes in athletes’ submaximal exercise
deconditioning) for 8 weeks resulted in a signifi- heart rates have also been reported after longer
cant 7% Vo2max decrease in eight untrained women periods of training cessation. Seven endurance-
and 11 untrained men. None the less, total blood trained subjects exercised at the same absolute
volume (4.0%) and plasma volume (3.1%) did not submaximal intensity in a trained state and
decrease significantly, and the baseline haemo- during 84 days of no training. Their heart rates
dynamic variables analysed by the investigators increased from 84 to 93% of maximal values dur-
were unaltered by the deconditioning period. ing the initial 56 days of inactivity, but stabilized
These data suggest that some of the changes in thereafter. Exercise of the same relative sub-
Vo2max accompanying physical deconditioning maximal intensity, on the other hand, elicited
may be independent of changes in total blood almost identical percentages of maximal heart rate
volume and plasma volume (Raven et al. 1998). (Coyle et al. 1985). Eleven college soccer players
showed increased heart rate at submaximal exer-
cise intensities during 5 weeks without training
Heart rate
(Fardy 1969). This result, along with a shortened
length of the cardiac isovolumetric contraction
resting heart rate
phase at rest, led the author of the study to sug-
Whereas resting heart rate has been shown to gest that inactivity brought about an increase
increase significantly after only 3 days of bed rest in the sympathoadrenergic tone of the players.
in endurance athletes (Smorawinski et al. 2001), Increased submaximal heart rates were also
it has been reported not to change in athletes observed in adolescent (15–18 years) female
following short-term (10 days) training cessation athletes as a result of 12 (Drinkwater & Horvath
(Cullinane et al. 1986). Resting heart rate did not 1972) and 23 (Michael et al. 1972) weeks of
change in five Olympic rowers and one canoeist training cessation following the track season. In
during 6–34 weeks of training stoppage follow- addition, the latter investigators also observed a
ing the 1988 Seoul Olympic Games (Maron et al. progressive 16% increase in postexercise recovery
1993), but it increased by 6.4% in 2–12 weeks heart rate, but stated that both submaximal and
of injury-induced training cessation in physical recovery heart rate increases seemed to level off
education students (Bánhegyi et al. 1999). after the initial 7 weeks of training stoppage.
In line with the above results, six college football
players showed an increased heart rate during
submaximal heart rate
submaximal exercise after 9 weeks of training
As a consequence of the above-mentioned cessation following their competitive season. Their
reduction in blood volume, the heart rate at sub- values, nevertheless, remained lower than those
maximal exercise intensities increases by approx- of sedentary counterparts (Penny & Wells 1975).
imately 5–10%. Coyle et al. (1986), observed Giada et al. (1998) observed that heart rates at
an 11% higher heart rate during submaximal a power output of 100 W increased from 108 to
exercise after a group of endurance athletes 114 beats·min–1 in young cyclists, and from 100
spent 2–4 weeks away from training. Heart rate to 106 beats·min–1 in older cyclists after 2 months
while performing submaximal exercise (75 and of training cessation.
(Coyle et al. 1984). The same group reported

maximal heart rate
that 3–8 weeks of physical deconditioning in
The training stoppage also influences heart rate highly trained subjects, which brought about a
during maximal intensity exercise, increasing 20% reduction of Vo2max, resulted in a signifi-
it by about 5–10%. Cullinane et al. (1986) meas- cant 17.2% reduction in stroke volume during
ured a 5% increase in maximal heart rate in upright exercise (Martin et al. 1986). On the other
15 runners after 10 days of training cessation. hand, Pavlik et al. (1986a, 1986b) indicated that
Fourteen days of training cessation also resulted the resting stroke volume index (mL·beat–1·m–2)
in 9 beats·min–1 higher maximal heart rate in a and ejection fraction rose in a group of highly
group of endurance runners (Houmard et al. 1992). trained road cyclists and endurance runners dur-
Madsen et al. (1993), on the other hand, reported ing 60 days of training cessation. These changes
unchanged maximal heart rates after 4 weeks were paralleled by a linear decrease in Vo2max
of insufficient training stimulus in nine endur- until the 45th day of training withdrawal. In
ance athletes. In contrast, in an 84-day training contrast, Smorawinski et al. (2001) recently re-
cessation follow-up study on seven endurance- ported on a significant decrease in resting stroke
trained subjects, maximal heart rate increased volume in a group of endurance athletes after
by 4–5% after the initial 12–21 days without 3 days of bed rest, but not in bodybuilders. The
training, but it did not change thereafter (Coyle authors did not elucidate whether these differ-
et al. 1984). ences depended on the subjects’ habitual phys-
ical training mode and endurance activity level
or the genetic factors associated with aerobic
Stroke volume
capacity.
The reduced maximal aerobic capacity observed
in highly trained subjects after short periods of
Cardiac output
training cessation seems to be a consequence of
the decline in stroke volume arising from the Cardiac output decreases during exercise in
reduced blood volume that characterizes detrain- highly trained athletes during periods of training
ing (Coyle et al. 1984). Coyle et al. (1986) observed cessation. This decrease takes place because the
that stroke volume fell by 12% during upright above-mentioned increase in exercise heart rate
exercise in a group of endurance athletes who is not enough to counterbalance the decline in
stopped training for 2–4 weeks. This effect was stroke volume. Coyle et al. (1984) reported that
reversed after plasma volume expansion, but estimated maximal cardiac output stabilized at
this intervention did not restore Vo2max, which 8% below trained values after 21 days of train-
remained 3% lower than in the trained state. ing cessation in endurance athletes, not falling
This observation suggests that the reduction in beyond that level between the 21st and 84th days
blood volume associated with detraining limits without training. These authors also observed
ventricular filling during upright exercise and a progressive shift from 84 to 94% of maximal
is largely responsible for the inactivity-induced cardiac output between the trained and detrained
decline in cardiovascular function. Stroke volume (84 days without training) states when subjects
declined by 10% after the initial 12 of 84 days exercised at the same absolute submaximal
without training in seven endurance-trained sub- intensity, whereas exercise of the same relative
jects, and averaged 10–14% below trained levels submaximal intensity elicited almost identical
during 12–84 days of training stoppage. These percentages of cardiac output (Coyle et al. 1985).
values did not differ from the controls. The Slightly but significantly higher cardiac ouputs
authors indicated that the decline in Vo2max dur- were also elicited during submaximal supine
ing the initial 21 days of training cessation was exercise following 8 weeks of training cessation
associated with a decreased stroke volume in highly trained subjects (Martin et al. 1986).
Detrained cyclists’ and runners’ cardiac index mass (19.5%). The increased mean blood pressure
(L·m–2·min–1) increased at rest as a result of the during upright exercise measured by these and
increased stroke volume index (Pavlik et al. 1986a, other authors (Coyle et al. 1986) could indeed be
1986b). Also, resting cardiac output of 55 physical due to a reduced left ventricular mass, coupled
education students not training for 2–12 weeks with a higher total peripheral resistance, which
due to injury increased by 10.1% (Bánhegyi et al. increased by 8% after 2–4 weeks of training cessa-
1999). On the other hand, submaximal and max- tion (Coyle et al. 1986). Cullinane et al. (1986), on
imal cardiac output was unchanged in endurance the other hand, did not observe any change in the
athletes and bodybuilders as a result of 3 days of cardiac dimensions and the blood pressure of 15
bed rest (Smorawinski et al. 2001). distance runners following 10 days of training
stoppage. During longer periods of training cessa-
tion (8 weeks), the left ventricular end-diastolic
Cardiac dimensions and circulation
dimension of highly trained athletes declined in
Short-term training cessation has also been shown parallel with stroke volume when performing
to result in altered cardiac dimensions in highly upright exercise (Martin et al. 1986). Meanwhile,
trained athletes (Fig. 6.2). Martin et al. (1986), for left ventricular posterior wall thickness decreased
instance, reported significant reductions in left progressively by 25%, but left ventricular mass
ventricular end-diastolic dimension (11.8%), left was unaltered after the decline observed follow-
ventricular wall thickness (25.0%) and increased ing the first 3 weeks of deconditioning.
mean blood pressure during upright exercise in Six Olympic-level athletes (five rowers and one
athletes who did not take part in physical train- canoeist) were shown to decrease their maximal
ing for 3 weeks. These investigators attributed left ventricular wall thickness by 23% (range
these changes to a reduction in left ventricular 15–33%) and their left ventricular mass by 22%
Cardiac morphology Cardiac function
Left ventricular end-diastolic dimension Resting heart rate

(4–12%, 21 days) (0–7%, 14 days)
Left ventricular wall thickness Submaximal heart rate
Decrease
(7–33%, 21 days) (5–10%, 10–14 days)

Heart
Left ventricular mass Maximal heart rate
(8–37%, 21 days) (5–10%, 10–14 days)
Increase
Interventricular septal wall thickness Recovery heart rate

(7%, 60 days) (7–16%, 21 days)
Resting cardiac output
(10–30%, 14–21 days)
Submaximal cardiac output
(5–12%, 12–21 days)
Mean blood pressure
(8–12%, 21days)
Total peripheral resistance
(8%, 14–28 days)
Exercise stroke volume Fig. 6.2 Morphological and

(10–18%, 12 days) physiological changes most
Decrease
Maximal cardiac output

likely to occur at the cardiac level,
(8–10%, 12–21 days) and minimum reported time of
training cessation necessary
Blood and plasma volume
(5–12%, 2 days)
for these changes to take place
in athletes.
(range 8–37%) during 6–34 weeks of training and above control values in road cyclists and
stoppage following the 1988 Seoul Olympic endurance runners during 60 days of inactiv-
Games. No changes in blood pressure or resting ity. The same was true for end-diastolic and
heart rate were observed. It was concluded that end-systolic volumes. Small and opposite non-
deconditioning may be associated with a con- significant changes were observed in relative
siderable reduction in ventricular septal thickness left ventricular end-diastolic volume (which
in elite athletes, suggesting that this population tended to increase) and relative left ventricular
had a physiological form of left ventricular hyper- end-systolic volume (which tended to decrease),
trophy induced by training (Maron et al. 1993). resulting in a linearly increased ejection fraction
Studying a group of young (24 ± 6 years) and until the 30th day of no training (r = 0.40), which
a group of older (55 ± 5 years) amateur cyclists reached control level. The stroke volume index
during 2 months of training stoppage, Giada et al. also increased until the 40th day (r = 0.40). Since
(1998) reported a reduced posterior wall thickness the resting heart rate remained low throughout
index (6.6%) and interventricular septal wall the follow-up period, the resting cardiac index
thickness index (6.5%) in the young athletes. In grew linearly until day 40 (r = 0.47), reaching the
the older athletes, detraining was characterized control level by the third week, then exceeding
by a reduced left ventricular end-diastolic dia- it. No further change was observed between
meter index (3.4%), left ventricular end-diastolic the 45th and 60th days. Left ventricular mean
volume index (9.9%) and left ventricular mass circumferential shortening velocity followed a
index (15.7%). The authors concluded that in the similar increasing trend until day 30 (r = 0.44).
young athletes, thickness was greatly reduced Mean arterial blood pressure remained practic-
whereas ventricular cavities remained unchanged, ally stable throughout the study, but relative
the final result being a slight and non-significant total peripheral resistance declined continuously
reduction in left ventricular mass. Conversely, (r = –0.45). Based on their observations, these
in the older athletes, the significant reduction in authors concluded that the cardiovascular regu-
left ventricular mass was the result of reduced lation undergoes a peculiar shift during training
cardiac cavities, whereas thickness of the free cessation in that a persisting cardiac enlarge-
wall and septum remained unchanged. It was ment and bradycardia is associated with a
suggested that in the elderly subjects cardiac temporarily unstable autonomous control due
adaptation to aerobic training takes place mainly to relatively high levels of both sympathetic and
through a higher degree of diastolic filling of the parasympathetic activity. This imbalance often
left ventricle with a greater utilization of Starling’s leads to a hyperkinesis-like syndrome when
mechanism, which makes up for the reduced an athlete stops endurance training abruptly.
chronotropic capacity. These conclusions coincide with a clinical entity
Giannattasio et al. (1992) reported that former known as ‘detraining syndrome’ (also referred
professional sprint runners and hammer throwers to as ‘relaxation syndrome’), which arises when
had left ventricular end-diastolic diameter and athletes with a long endurance-training history
mass indexes similar to those of sedentary sub- suddenly abandon their regular physical activ-
jects after 4–5 years of training cessation. They ity (Mujika & Padilla 2000a). It is characterized
also indicated that the impairment of the cardio- by a tendency to dizziness and fainting, non-
pulmonary reflex that they observed in athletes systematic precordial disturbances, sensations
is to a great extent reversible with training of cardiac arrhythmia, extrasystolia and palpita-
cessation-induced regression of cardiac hyper- tion, headaches, loss of appetite, gastric dis-
trophy. Pavlik et al. (1986a, 1986b) observed that turbances, profuse sweating, insomnia, anxiety
diastolic relative muscular wall thickness, inter- and depression (Israel 1972; S’Jongers 1976).
ventricular septum thickness and left ventricular Bánhegyi et al. (1999), on the other hand, study-
posterior wall thickness remained unchanged ing a group of 22 female and 23 male physical
education students who were forced to stop exer- six endurance cyclists and runners (Martin et al.
cising due to injury, reported slight reductions in 1986) and in six college football players (Penny
relative left ventricular wall thickness and relat- & Wells 1975). The values of the latter, however,
ive left ventricular muscle mass (2.6 and 2.7%, remained lower than those of sedentary counter-
respectively). They also observed increased rest- parts. It should also be noted that there have been
ing heart rate (6.4%) and cardiac output (10.1%). reports of unchanged blood pressure in seven
When comparing these results with their own young female track athletes (aged 14–17 years)
previous observations on highly trained cyclists following 12 weeks of training cessation at the
(Pavlik et al. 1986a, 1986b), they concluded that end of their competitive season (Drinkwater
the earliest modifications in echocardiographic & Horvath 1972), and in Olympic rowers and
parameters are likely to appear in the autono- canoeists not training for 6–34 weeks (Maron
mous regulation of the heart, first in sympathetic et al. 1993).
activity, then in parasympathetic tone. The change
in morphological parameters, if any, would
Ventilatory function
appear much later. This time course would be
the result of the fast response of the nervous According to several reports in the literature,
regulatory component, and it would depend on ventilatory function suffers a rapid deterior-
the previous conditioning level of the athlete, as ation when highly trained athletes stop exercis-
athletes of excellent condition not training for ing. Maximal exercise ventilation decreased in
several weeks were only shown to increase rest- parallel with Vo2max (2–7%) in six runners after
ing sympathetic autonomous activity, whereas 15 days without training (Houston et al. 1979).
less well-trained athletes’ changes in the com- Also, male basketball players not training for
ponents of cardiac function occur sooner and in 4 weeks after their competitive season showed a
a faster sequence (an elevation of resting sym- deterioration of cardiorespiratory efficiency, as
pathetic activity becomes manifest in an in- indicated by reduced maximal ventilation (9.3%),
creased resting cardiac output, a drop in resting O2 pulse (12.7%) and increased ventilatory equi-
parasympathetic tone in a faster heart rate, and valent (3.9%) (Ghosh et al. 1987). In the above-
also some of the morphological parameters may mentioned investigations, maximal ventilatory
show modifications). volume decreased in parallel with Vo2max. A
Interestingly, three out of 10 highly trained much higher decline in maximal ventilation
masters athletes (59 ± 8 years) developed new (21.3%) has been observed in endurance athletes
asymptomatic ischaemic-appearing, exercise- after just 3 days of bed rest (Smorawinski et al.
induced ST segment depression on their exercise 2001). Cullinane et al. (1986) did not observe a
electrocardiogram (ECG) during 3 months of decreased maximal ventilatory volume in male
training stoppage (Katzel et al. 1997). After 5– long-distance runners after 10 days of inactivity,
8 years of follow-up, two of the three athletes but they did observe a significantly lower max-
with silent ischaemia experienced major cardiac imal O2 pulse.
events (sudden death, cardiac bypass surgery), Reports on the negative effects of longer pe-
whereas the other seven athletes did not have riods of training cessation on ventilatory volume
any cardiovascular events. These observations during maximal exercise have also been pub-
led the authors to suggest that silent ischaemia lished. Indeed, maximal ventilation decreased by
after a 3-month period of training stoppage in 10, 10.3 and 14.5% in 11 college soccer players in
highly trained older athletes may be a predictor 5 weeks (Fardy 1969), young female track ath-
of future cardiac events (Begum & Katzel 2000). letes in 12 weeks (Drinkwater & Horvath 1972)
Mean and systolic blood pressures have been and five badminton players in 2 years (Miyamura
shown to increase along with total peripheral & Ishida 1990), respectively. In addition, the
resistance during 9–12 weeks without training in latter athletes’ hypercapnic ventilatory respons-
iveness was shown to increase significantly. Also, at submaximal and maximal exercise intensities
ventilatory volume shifted from 53 to 71% of (Table 6.1). Moore et al. (1987) observed in an
the maximal after 56 days without training in athletic population that 3 weeks of training stop-
endurance athletes (Coyle et al. 1985). Drink- page brought about a shift in RER from 0.89 to
water and Horvath (1972) and Michael et al. 0.95 at an exercise intensity of 60% of Vo2max. In
(1972) also observed markedly increased sub- another investigation, seven endurance-trained
maximal ventilatory volume and ventilatory athletes exercised at the same absolute sub-
equivalent in female athletes during long-term maximal intensity when they trained and during
training cessation. 84 days of training cessation; the RER increased
from 0.93 to 1.00. Exercise of the same relative
submaximal intensity elicited almost identical
Metabolic consequences of
percentages of maximal heart rate, ventilation
training cessation
and cardiac output, but RER increased from 0.93
When an athlete reduces his or her habitual level to 0.96 (Coyle et al. 1985). Also, the RERs of nine
of physical training to a level which is insuffi- highly trained endurance athletes shifted from
cient to maintain previously acquired adaptations, 0.89 to 0.91 when cycling at 75% of Vo2max after
metabolic detraining occurs. This is primarily 4 weeks of insufficient training (Madsen et al.
characterized by marked changes in the pattern 1993). Maximal RER also increased from 1.03
of substrate availability and utilization dur- to 1.06 after 14 days without training in a group
ing exercise, which most often result in altered of endurance-trained runners (Houmard et al.
lactate kinetics that are detrimental to sports 1992). Finally, Drinkwater and Horvath (1972)
performance (Hawley 1987; Neufer 1989; Wilber reported higher RER values during submaximal
& Moffatt 1994; Mujika & Padilla 2000a&b, and maximal exercise in female athletes 12 weeks
2001a). after the end of the track season, and Smorawinski
et al. (2001) observed higher RER values both at
rest and at submaximal exercise intensities in
Substrate availability and utilization
endurance athletes confined to bed for 3 days.
Taken as a whole, these results clearly indicate a
respiratory exchange ratio
shift towards an increased reliance on carbohy-
One of the metabolic consequences of a short drate as an energy substrate for exercising mus-
period of insufficient training stimulus in athletes cles, concomitantly with a decreased contibution
is an increased respiratory exchange ratio (RER) from lipid metabolism.
Table 6.1 Studies reporting changes in the exercise respiratory exchange ratio (RER) as a result of training
cessation in athletes.
Days of training
cessation Exercise intensity Trained vs detrained RER Reference
12 74% Vo2max 0.93 vs 0.97 Coyle et al. 1985

14 100% Vo2max 1.03 vs 1.06 Houmard et al. 1992
21 60% Vo2max 0.89 vs 0.95 Moore et al. 1987
28 75% Vo2max 0.89 vs 0.91 Madsen et al. 1993
84 100% Vo2max 0.97 vs 1.10 Drinkwater & Horvath 1972
transporter protein were also reduced by 8–29

glucose and lipid metabolism
and 17.5%, respectively. These results indicated
There have been several reports of a rapid that short-term inactivity decreases insulin action
decline in sensitivity for insulin-mediated whole- in endurance runners, suggesting that a reduc-
body glucose uptake during short-term inactivity. tion in muscle GLUT-4 transporter level may
Burstein et al. (1985) studied insulin-stimulated play a role in the decrease in glucose disposal
glucose disposal and erythrocyte insulin recep- rates (Vukovich et al. 1996). McCoy et al. (1994)
tor binding in seven endurance-trained athletes reported that 10 days of training stoppage in
(six runners and one swimmer) after 12 h, 60 h trained triathletes resulted in a 43.3% increase in
and 7 days of training stoppage. Plasma glucose the area under the insulin response curve during
did not change throughout the study period, but an oral glucose tolerance test, but still remained
plasma insulin increased significantly between the 24.3% below values of untrained control sub-
second and seventh days without training. The jects. No change was observed following training
metabolic clearance rate of glucose, measured by cessation in the glucose response to the test, but
the euglycaemic clamp technique, decreased from GLUT-4 protein levels decreased by 33.2%, in
15.6 ± 1.8 mL·kg–1·min–1 at the 12 h time point after parallel with a 28.6% reduction in citrate synthase
the last training bout, to 10.1 ± 1.0 mL·kg–1·min–1 activity, suggesting that glucose transport and
at 60 h, and to 8.5 ± 0.5 mL·kg–1·min–1 after 7 days. oxidation are regulated by the muscle activity
The last two values were not different from those level. In keeping with the previous findings,
of the sedentary controls (7.8 ± 1.2 mL·kg–1·min–1). the area under the glucose and insulin curves
There was also a 21.4 ± 1.8% decrease in insulin increased, respectively, by 65 and 73% during
receptor binding to isolated young erythrocytes 7–10 days of training cessation in endurance-
between 12 and 60 h postexercise, apparently due trained athletes. Resting metabolic rate fell by 4%,
to a reduced receptor number, rather than the and the RER during the oral glucose tolerance
affinity. These authors concluded that the increase test increased by the same amount. However, no
in peripheral insulin action seen in trained change was observed in the calf and forearm
athletes is rapidly reversed, and that modulation blood flow. These data indicated a deterioration
of in vivo insulin response by training stoppage in glucose tolerance and energy metabolism, but
may be at least partially mediated by changes these changes did not seem to be mediated by
in insulin receptor number. Five days of training limb blood flow (Arciero et al. 1998).
stoppage were enough in endurance athletes Heath et al. (1983) also studied the effects of
to decrease insulin sensitivity to levels found in 10 days of training cessation on glucose toler-
untrained counterparts (Mikines et al. 1989a). ance and insulin sensitivity in a group of trained
These authors, using the sequential hypergly- cyclists and runners. Glucose tolerance was
caemic clamp technique, reported that glucose- significantly reduced, as shown by a 10–25%
induced β-cell secretion increased slightly towards increase in blood glucose concentration and a
untrained levels during the same period, indicat- 55–120% increase in plasma insulin concentra-
ing that β-cells are subjected to an adaptation tion in response to an oral glucose tolerance test.
during training (Mikines et al. 1989b). Hardman A single bout of exercise, however, returned post-
et al. (1998) measured a 15.8% higher postprandial glucose tolerance test glucose and insulin levels
serum insulin response in endurance athletes to almost initial trained values, giving support
after 6.5 days without exercise. to the authors’ hypothesis that residual effects
In a similar short-term inactivity study (6 days) of the last bouts of exercise play an important
in endurance runners, it was shown that glucose role in the trained individuals’ improved glucose
disposal rates after insulin infusion fell by 14.2– tolerance and blunted insulin response to a
29.5%, despite 10.0–21.9% higher plasma insulin. glucose load. Following 14 days of training cessa-
Insulin clearance and muscle GLUT-4 glucose tion, an increased area under the glucose curve
(14.8%) was observed in 12 endurance runners. letes (Thompson et al. 1984). Also, marathon run-
The insulin curve also increased in endurance ners have been shown to increase their plasma
(30.3%) and strength (23.3%) in athletes during levels of lipoprotein(a) and apolipoprotein A1
an oral glucose tolerance test. The insulin sensi- by 24.2 and 16.0%, respectively, during 1 month
tivity index decreased by 23.7% in the former, of suspended physical activity of all types.
and 16.0% in the latter. The authors, however, Moreover, high-density lipoprotein cholesterol
observed no change in GLUT-4 content, either in decreased by 14.6% as compared with post-
endurance runners or in weightlifters. This lack marathon race values (Bonetti et al. 1995). Giada
of change was evident despite a 25.3% decrease et al. (1995) studied the effects of 2 months of
in citrate synthase activity in the endurance training stoppage in a group of young (24 ±
runners. It was concluded that the decrement in 6 years) and a group of older (55 ± 5 years)
insulin sensitivity with training cessation was amateur cyclists. Compared with the values
not associated with a decrease in GLUT-4 protein recorded at the peak of their seasonal prepara-
content, and that muscle oxidative capacity does tion, body fat increased by 4 and 2% in young
not necessarily change in tandem with GLUT-4 and older athletes, respectively. Triglycerides
protein content (Houmard et al. 1993). (14.5 and 22.2%) and the low-density lipoprotein
On the other hand, 2 weeks of training cessa- cholesterol : high-density lipoprotein cholesterol
tion from endurance running has been shown ratio (21.4 and 26.3%) increased significantly in
to yield a condition that favours the storage of both groups, whereas apolipoprotein A1 (8.4
adipose tissue, as shown by a marked increase and 8.6%), high-density lipoprotein cholesterol
(86%) in adipose tissue lipoprotein lipase activ- (10.2 and 8.7%), high-density lipoprotein2
ity, coupled with a marked decrease (45–74%) in cholesterol (10.5 and 12%) and high-density
muscle lipoprotein lipase activity (Simsolo et al. lipoprotein3 cholesterol (7.7 and 4.5%) decreased
1993). Moreover, endurance-trained subjects in significantly. In addition, fibrinogen and very
the fasted state have been reported to increase low-density lipoprotein cholesterol also increased
their concentrations of triacylglycerol (47%), very in the group of young cyclists (5.2 and 34.0%,
low-density lipoprotein cholesterol (28.2%) and respectively). The authors of this study con-
the ratio of total cholesterol : high-density lipo- cluded that a 2-month interruption in aerobic
protein cholesterol (7.5%) during 6.5 days with- training changed antiatherogenic lipoprotein pro-
out exercise. Concentrations of non-esterified file and body composition unfavourably in both
fatty acids, on the other hand, decreased during groups, and, therefore, that age did not seem to
the same period by 43.5%. Due to a higher rate have a significant influence on the plasma lipid
of triacylglycerol removal, probably related to response to training stoppage.
their high lipoprotein lipase activity because Mankowitz et al. (1992) observed, in a group
of their well-vascularized skeletal muscle mass, of trained runners, that 14–22 days of training
endurance-trained subjects usually exhibit low stoppage resulted in a 7.7% reduction in fast-
levels of postprandial lipaemia. However, 6.5 days ing high-density lipoprotein cholesterol con-
without training increased postprandial lipaemia centration, and a 21% reduction in postheparin
by 42.2%, as shown by the increased area under lipoprotein lipase activity. No significant changes
the plasma triacylglycerol versus time curve, were observed in body fat, estimated plasma
indicating that frequent exercise is necessary to volume, lipoprotein(a), total cholesterol, trigly-
maintain a low level of postprandial lipaemia cerides and low-density lipoprotein cholesterol.
in endurance-trained subjects (Hardman et al. On the other hand, the mean areas under the
1998). Ten days of training cessation also resulted concentration versus time curves for chylomi-
in a 15% reduction in high-density lipoprotein cron-retinyl esters increased by 41% and for
cholesterol and a 10% increase in low-density chylomicron remnant-retinyl esters increased by
lipoprotein cholesterol in endurance-trained ath- 37% after training cessation. It was concluded
that detraining was characterized by reduced to suffer dramatic changes affecting blood lac-
fasting concentrations of high-density lipopro- tate kinetics in as little as 1–4 weeks of training
tein cholesterol and a decreased metabolism of cessation. Indeed, muscle respiratory capacity
chylomicronsachanges that are associated with decreased by 50% after 1 week of inactivity in a
an increased incidence of atherosclerosis. group of eight swimmers. When subjects per-
During 2 months of training stoppage, six formed a standardized 183 m submaximal swim,
highly trained female swimmers were shown to postswim blood lactate was 2.3 times higher, pH
have increased their body mass by 4.8 kg, of significantly lower (7.183 vs 7.259), bicarbonate
which 4.3 kg was fat mass. This represented an concentration 22.7% lower, and base deficit twice
increase in body fat of about 4%. Interestingly, no as high (Costill et al. 1985). A group of 24 college
change was observed in lipid and energy intake swimmers not training for 4 weeks after 5 months
during this period, and the energy equivalent of of competitive training showed a 5.5 mmol·L–1
the fat gain (170 MJ) closely matched the habitual increase in blood lactate concentration follow-
energy cost of daily training, suggesting that the ing a standardized 183 m submaximal swim,
fat gain was related to a failure to reduce energy which was also indicative of a reduction in the
and fat intake to a level commensurate with the muscle oxidative capacity, and/or a change in the
new energy and lipid expenditure, perhaps in swimmers’ mechanical efficiency (Neufer et al.
order to promote the restoration of lipid balance 1987). Similar results were observed by Claude
(Alméras et al. 1997). and Sharp (1991) in seven female swimmers who
refrained from training for 10 days.
Endurance runners and cyclists performing
resting metabolic rate
an exercise task of the same relative submaximal
The influence of training cessation on the resting intensity before and after 84 days of training
metabolic rate of athletes has not been clearly stoppage showed a shift in blood lactate con-
established. In one report, resting metabolic rate centration from 1.9 to 3.2 mmol·L–1, along with a
was shown to fall by 4% in a group of endurance- marked decline in the muscle respiratory capacity
trained athletes during 7–10 days without train- (Coyle et al. 1985). An increased blood lactate
ing, indicating a reduced energy metabolism concentration at submaximal exercise intensity
(Arciero et al. 1998). However, other authors has also been reported in six college American
reported that the resting metabolic rate was football players after 9 weeks of postseason break
not affected by 3 weeks of training stoppage in (Penny & Wells 1975). Moreover, the lactate
trained males, which led the authors to suggest threshold has been shown to decline with 84 days
that exercise training does not potentiate resting of inactivity from 79.3 to 74.7% of Vo2max, but
metabolic rate (LaForgia et al. 1999). to remain above sedentary control values of
62.2% (Coyle et al. 1985). Pavlik et al. (1986b)
reported on 40 observations on highly trained
Blood lactate kinetics
road cyclists and endurance runners who, for vari-
It has been clearly established that highly trained ous reasons, stopped training for 60 days. They
athletes respond to submaximal exercise of the observed a linear decline in the athletes’ lactate
same absolute intensity with higher blood lactate threshold (r = –0.58) throughout the initial 45 days
concentrations after only a few days of training of training stoppage, with no further change
cessation. In a recent investigation, the blood thereafter. Nichols et al. (2000) reported on a
lactate threshold of endurance athletes was negat- female masters athlete (49.5 years) who due to
ively affected after only 3 days of bed rest, falling injury was forced to refrain from training for a
from 71 to 60% of Vo2max (Smorawinski et al. period of 32 days. Compared to values assessed
2001). Competitive swimmers’ skeletal muscle 2 days preinjury, when the subject was at the
metabolic characteristics have been reported peak of her competitive season, power output
Table 6.2 Main metabolic changes most likely to occur, and minimum reported time of training cessation
necessary for these changes to take place in athletes.
Metabolic change Percentage change Minimum time (days)
↑ Maximal respiratory exchange ratio 3–13 14

↑ Submaximal respiratory exchange ratio 2–8 12
↓ Resting metabolic rate 0–4 7–10
↓ Insulin-mediated glucose uptake 14–46 2.5
↑ Postprandial insulin response 10–22 6.5
↓ Insulin clearance 8–29 6
↓ Muscle GLUT-4 protein content 0–33 6
↓ Muscle lipoprotein lipase activity 21–75 14
↑ Adipose tissue lipoprotein lipase activity 86 14
↑ Body fat 0–4 percentage points 60
↑ Postprandial lipaemia 42 6.5
↑ Triacylglycerol 0–47 6.5
↓ Non-esterified fatty acids 44 6.5
↓ High-density lipoprotein cholesterol 8–15 10
↑ Low-density lipoprotein cholesterol 0–10 10
↑ Very low-density lipoprotein cholesterol 28–34 6.5
↑ Lipoprotein(a) 0–24 30
↓ Chylomicron metabolism 37–41 14–22
↑ Submaximal blood lactate 150–231 7
↓ Lactate threshold 4–17 21
↓ Blood bicarbonate 8–24 7
↓ Muscle glycogen 20–39 7
at the lactate threshold decreased by 16.7%, and cyclists and runners undergoing 4 weeks of
power output at a blood lactate concentration insufficient training (Madsen et al. 1993). More-
of 4 mmol·L–1 by 18.9%. The athlete needed over, short-term (5 days) training stoppage has
approximately 11 weeks to return to her pre- been shown to be enough in seven endurance-
injury level of fitness. A meta-analysis study by trained athletes to decrease glucose to glycogen
Londeree (1997) has confirmed that there is a conversion and glycogen synthase activity towards
decline in the lactate threshold with training sedentary values (Mikines et al. 1989a).
cessation. A summary of the main metabolic consequences
of training cessation in athletes can be found in
Table 6.2.
Muscle glycogen
Muscle glycogen concentration declines rapidly

Muscular consequences of
with training cessation in highly trained athletes.
training cessation
This decline is associated with a rapid reduction in
glucose to glycogen conversion and glycogen syn- One of the most important characteristics of
thase activity. In eight competitive swimmers, the skeletal muscle is its dynamic nature. Skeletal
deltoid muscle glycogen concentration declined muscle tissue has an extraordinary plasticity that
by 20% in the first week of training cessation after enables it to adapt to variable states of functional
the competitive season, and by 8–10% per week demands, neuromuscular activity and hormonal
without training thereafter (Costill et al. 1985). signals, by reversibly changing its functional
Pre-exercise muscle glycogen has also been shown characteristics and structural composition (Saltin
to be reduced by 20% in a group of triathletes, & Gollnick 1983; Hoppeler 1986; Kannus et al.
Muscle morphology Muscle function
Capillary density Arteriovenous oxygen

(0–6%, 15 days) difference (4–7%, 56 days)
Oxidative fibres in endurance Oxidative enzyme activities
athletes (14–40%, 56–84 days) (23–45%, 10 days)
Decrease
Decrease
Mean fibre CSA Glycogen synthase activity

(6–37%, 14–21 days) (42%, 5 days)
FT : ST area ratio Skeletal EMG activity
(6–21%, 56 days) muscle (6–13%, 14 days)
Muscle mass Strength/power performance
(1–5%, 21 days) (7–14%, 28 days) Fig. 6.3 Morphological and
physiological changes most likely
Oxidative fibres in strength athletes to occur at the skeletal muscle
level, and minimum reported
Increase
(40%, 210 days)

Oxidative fibre CSA time of training cessation
in endurance athletes necessary for these changes to
(12–25%, 14 days) take place in athletes.
1992b; Gordon & Pattullo 1993). Training-induced as long as 84 days without training, and that
skeletal muscle adaptations are such that the capillarization in this population was about 50%
trained muscle increases its tolerance to exercise higher than in sedentary controls. These authors
(Houston 1986). On the other hand, as shown discussed that the retention of the increased
in Fig. 6.3, skeletal muscle tissue also readjusts capillary density contributed to the observed
to the reduced physiological stressors during partial maintenance of the ability to attain a high
periods of injury, when there is reduced training percentage of Vo2max without large increases in
or complete training cessation (Sjøgaard 1984; blood lactate concentration.
Houston 1986; Hawley 1987; Costill 1988; Coyle
1988, 1990; Fleck 1994; Wilber & Moffatt 1994;
muscle fibre distribution
Tidow 1995; Mujika & Padilla 2001b).
The consequences of training cessation on
muscle fibre distribution seem to depend on
Muscle structure
the duration of the inactive period. Six highly
trained distance runners wore a walking plaster
muscle capillarization
cast for 7 days, then refrained from training for
Given the contradictory results that have been 8 additional days, but this was not enough to
reported in the literature, it is fair to state that the induce any change in their muscle fibre dis-
effects of training stoppage on capillary density tribution (Houston et al. 1979). The same was
in athletes have not been clearly established. true in the case of four soccer players not train-
Houston et al. (1979) reported a 6.3% reduction ing for 3 weeks (Bangsbo & Mizuno 1988), and
in capillary density after only 15 days of train- 12 strength-trained athletes not training for 14
ing cessation in well-trained endurance runners. days (Hortobágyi et al. 1993). Longer periods
Similarly, in semiprofessional soccer players, the of training cessation, on the other hand, have
number of capillaries around ST fibres decreased been reported to induce significant changes in
significantly from 6.0 to 5.8 after 3 weeks of train- the fibre distribution of athletes participating
ing cessation (Bangsbo & Mizuno 1988). In con- in various sports. Coyle et al. (1985) observed a
trast with these results, Coyle et al. (1984) reported large progressive shift from FTa to FTb fibres
that seven endurance-trained subjects’ trained- in endurance runners and cyclists, the latter
state muscle capillarization was unchanged after increasing from 5% in the trained state to 19%
after 56 days of training cessation. Sinacore et al. testosterone : cortisol ratio (67.6%) increased
(1993) studied muscle fibre distribution in five during the study period, whereas cortisol and
male and one female endurance-trained sub- creatine kinase enzyme levels decreased, respect-
jects who stopped training for 12 weeks. They ively, by 21.5 and 82.3%. The investigators con-
observed a 26% increase in the proportion of FTb cluded, on the one hand, that short-term training
fibres, and a concomitant 40% decrease in the stoppage in strength athletes specifically affected
proportion of FTa fibres. Larsson and Ansved FT fibre size, and on the other hand, that changes
(1985) reported that the proportion of ST fibres in the hormonal milieu accompanying inactiv-
in four elite oarsmen decreased by 14–16% dur- ity were propitious for an enhanced anabolic
ing the 4-year period following their retirement process, but the absence of the overload training
from competition. An opposite tendency towards stimulus prevented the materialization of such
a higher oxidative fibre population has been changes at the tissue level (Hortobágyi et al.
observed in strength athletes. Indeed, a case 1993; Houmard et al. 1993). In contrast, 14 days of
study on one elite power lifter indicated that the training stoppage did not result in a changed
oxidative muscle fibre population was 1.4 times muscle fibre CSA in a group of endurance
greater after 7 months without training (Staron runners (Houmard et al. 1992); it even increased
et al. 1981), and Häkkinen and Alén (1986) reported slightly (from 4.05 to 4.52·103μm2 in ST fibres,
a reduction in percentage FT muscle fibres and from 4.20 to 5.22·103μm2 in FTa fibres) in
(from 66 to 60%) in an elite bodybuilder who a similar group of runners (Houston et al. 1979).
underwent training cessation for 13.5 months. This change can be considered a reversal of the
Nevertheless, 14–15-year-old soccer players training-induced reduction in oxidative fibre
showed unchanged muscle fibre distribution size which facilitates diffusion by reducing its
after 4–8 weeks of training cessation (Amigó et al. distance.
1998), and female dancers have also been shown Longer periods of training stoppage also
not to change their fibre type distribution after brought about declines in FT and ST fibre CSA,
long-term (32 weeks) training cessation, suggest- the FT : ST area ratio and muscle mass in athletes.
ing, beyond the possible limitations inherent to It has been shown that rugby league players’ CSA
the mucle biopsy technique, that their high per- of FT fibres decreased to a greater extent than
centage of ST fibres may have been the result of ST fibres, the former being 23% larger at the end
natural selection rather than a training-induced of the season, but only 9% larger after 6 weeks
adaptation (Dahlström et al. 1987). without training. Further, an atrophy of the
muscle bulk was suggested by the author in
view of the fact that body mass decreased from
muscle fibre size
79.8 to 76.0 kg, but body fat content remained
Mean fibre cross-sectional area (CSA) has been relatively constant during the inactive period
shown to change during short-term training (Allen 1989). A 49.5-year-old female masters
stoppage. Bangsbo and Mizuno (1988) studied athlete’s fat-free mass decreased by 1.8 kg and
samples of the gastrocnemius muscle of male body fat increased by 2.1% during 32 days of
soccer players undergoing 3 weeks of training training stoppage due to injury (Nichols et al.
cessation and reported a 7% decline in the mean 2000). In line with these reports, LaForgia et al.
fibre CSA. This change was primarily due to a (1999) observed a small (0.7 kg) decrease in
12.4% decline in FTa fibre area, from 6022 to 5278 fat-free mass during a 3-week period without
μm2. Similar results have been observed in training in trained males. After 7 months of
12 weightlifters, whose FT fibre CSA declined by training cessation, an average atrophy of 37.1%
6.4% in 14 days of training stoppage. It is worth was observed in all fibre types of a power lifter,
mentioning that plasma concentrations of growth along with a large fat–weight loss (Staron et al.
hormone (58.3%), testosterone (19.2%) and the 1981). Also, an elite bodybuilder’s fat-free mass,
thigh and arm girth, and average fibre area athletes during training cessation is due to a
decreased by 9.3, 0.5, 11.7 and 8.3%, respectively, decreased stroke volume, the decreased arterial–
after 13.5 months without training. In addition, mixed venous oxygen difference would be re-
the FT : ST fibre area ratio decreased from 1.32 sponsible for the reduction in Vo2max observed
to 1.04 (Häkkinen & Alén 1986). Häkkinen et al. between the third and 12th weeks of training
(1981) also observed a reduction in the FT : ST cessation (Coyle et al. 1984).
muscle fibre area ratio from 1.11 to 1.04, and a
reduced muscle mass following 8 weeks of train-
myoglobin concentration
ing stoppage in strength-trained athletes, as well
as decreased FT and ST fibre areas after 12 weeks In a 12-week training cessation study, Coyle et al.
without training (Häkkinen et al. 1985). Larsson (1984) reported that myoglobin concentration in
and Ansved (1985) observed a 10% decrease in the gastrocnemius muscle of seven endurance-
the relative area of ST fibres in oarsmen after trained runners and cyclists (43.3 mg·g protein–1)
long-term cessation of their athletic activity, and did not change significantly after 3 (41.0 mg·g
Amigó et al. (1998) reported a reduction in the protein–1) and 12 weeks (40.7 mg·g protein–1)
diameter of ST and FT muscle fibres in adoles- of training cessation. In addition, these muscle
cent soccer players 4–8 weeks after the competi- myoglobin concentrations were not different
tive season. Dahlström et al. (1987), on the other from those of eight sedentary controls (38.5 mg·g
hand, measured a large increase in fibre areas protein–1). In a case study, Nemeth and Lowry
after 32 weeks of training cessation in female (1984) reported on the myoglobin content in ST
dancers, suggesting again that smaller fibres were and FT fibres of the vastus lateralis muscle of a
an endurance training-induced adaptation to 47-year-old cyclist, at peak training and after
decrease the oxygen diffusion distance. 6 and 84 days of training cessation. The myo-
globin levels remained unchanged despite a
16.7% decline in Vo2max and a 15–35% decrease
Muscle function
in the activities of oxidative enzymes during the
period of training restriction. It was concluded
arteriovenous oxygen difference
that a change in training condition that leads
As stated above, in addition to the ‘central’ factors to changes in the oxidative enzymes of human
already discussed, Vo2max is also a function of the muscle fibres does not affect myoglobin levels of
maximal ‘peripheral’ extraction of the delivered the same cells.
oxygen, which is traditionally expressed as the
arteriovenous oxygen difference (Sutton 1992).
enzymatic activities
The authors are aware of only one study report-
ing data on the arteriovenous oxygen difference Skeletal muscle oxidative capacity decreases
during training cessation in highly trained indi- markedly as a consequence of training cessation,
viduals (Coyle et al. 1984). According to that as reflected by large reductions in mitochondrial
study, 21 days without training did not bring enzyme activities. Indeed, Coyle et al. (1984, 1985)
about any change in the maximal arteriovenous observed that seven endurance-trained subjects’
oxygen difference of seven endurance-trained citrate synthase activity declined from 10.0 to
athletes (15.1, 15.1 and 15.4 mL·100 mL–1 at days 7.7 mol·kg protein–1·h–1 during the initial 3 weeks
0, 12 and 21 of training cessation, respectively). of training cessation, then continued declining
After 56 and 84 days without training, on the to 6.0 mol·kg protein–1·h–1 by the 56th day, and
other hand, values fell to 14.5 (4% reduction) and stabilized thereafter. Succinate dehydrogenase,
14.1 mL·100 mL–1 (7% reduction), respectively. β-hydroxyacyl-coenzyme A (CoA) dehydrogen-
Based on these results, the authors suggested ase and malate dehydrogenase declined roughly
that whereas the initial Vo2max loss observed in in parallel with citrate synthase (i.e. by about
20% in 3 weeks and 40% in 56 days of train- days of training cessation in the vastus lateralis
ing stoppage), also stabilizing thereafter at that muscle of a masters cyclist. Moreover, 16 male
level, which was still 50% higher than that of and female runners’ skeletal muscle lipoprotein
sedentary counterparts. Very similar observa- lipase activity was reduced by 45–75% during 2
tions were made by Chi et al. (1983) after 42–84 weeks of training cessation, whereas this enzyme’s
days of training stoppage in endurance athletesa activity increased by 86% at the adipose tissue
where citrate synthase, succinate dehydrogenase, level. The adipose tissue lipoprotein lipase :
β-hydroxyacyl-CoA dehydrogenase, malate dehy- muscle lipoprotein lipase ratio increased from
drogenase and β-hydroxybutyrate dehydrogen- 0.51 to 4.45, which was indicative of a tendency
ase declined by an average of 36% during that for the storage of circulating lipids in the adipose
period. As in the previous study, detrained-state tissue (Simsolo et al. 1993). Houston (1986) sug-
oxidative enzyme values were also 40% higher gested that the observed declines in mitochondrial
than controls. Interestingly, these authors also enzymatic activities are primarily regulated by
showed that mitochondrial enzyme levels de- altered protein synthesis rates. Moreover, these
creased almost to untrained levels in ST fibres, declines appear to be associated with the con-
but remained 50–80% higher in FT fibres. During comitant long-term reductions in Vo2max and
7 weeks of training followed by 3 weeks of train- arteriovenous oxygen difference (Coyle et al.
ing cessation, Moore et al. (1987) observed a 45% 1984; Allen 1989).
decline in citrate synthase activity in previously Small non-systematic changes in glycolytic
trained athletes, even though pretraining citrate enzyme activities have also been reported during
synthase activity did not change in response periods of training cessation in highly trained
to the initial 7 weeks of training. Also, Houmard athletic populations. For instance, hexokinase
et al. (1992, 1993) reported a 25.3% decline in decreased significantly by about 17%, phosph-
citrate synthase activity in a group of 12 dis- orylase did not change, phosphofructokinase
tance runners who stopped training for 14 days. increased non-significantly (about 16%) and
Similar results (27% decline in citrate synthase lactate dehydrogenase increased significantly by
and β-hydroxyacyl-CoA dehydrogenase) have about 20% in endurance athletes not training for
been reported in soccer players not training for 84 days (Coyle et al. 1985). Chi et al. (1983) also
3 weeks (Bangsbo & Mizuno 1988), triathletes observed an identical 17% decline in hexokinase,
(28.6% decline in citrate synthase activity) not whereas phosphorylase, phosphofructokinase
training for 10 days (McCoy et al. 1994) and and lactate dehydrogenase increased by 3.6–
adolescent soccer players (37.5% decline in cit- 21.1% in 42–84 days without training. Houston
rate synthase activity) not training for 4–8 weeks et al. (1979), on the other hand, reported a
(Amigó et al. 1998). Madsen et al. (1993) reported 13% lower mean lactate dehydrogenase activity
a 12% lower β-hydroxyacyl-CoA dehydrogenase after 15 days of training cessation. Competitive
activity after 4 weeks of insufficient training swimmers not training for 4 weeks showed
in nine endurance athletes, and Houston et al. non-significant declines in phosphorylase and
(1979) measured a 24% lower succinate dehydro- phosphofructokinase activities in their posterior
genase in six distance runners who did not train deltoid muscle (Costill et al. 1985). Phospho-
for 15 days. A similar 25% lower succinate dehy- fructokinase has also been shown to decline by
drogenase has been observed in six rugby league 16% in rugby players not training for 6 weeks
players’ lateral head of the gastrocnemius muscle (Allen 1989), and by 54.5% in adolescent soccer
6 weeks after the end of their competitive season players 4–8 weeks after their competitive season
(Allen 1989). Nemeth and Lowry (1984) reported (Amigó et al. 1998). In addition, Mikines et al.
that the activities of β-hydroxyacyl-CoA dehy- (1989a) reported that glycogen synthase activity
drogenase, citrate synthase and malate dehydro- dropped by 42% after only 5 days without train-
genase fell by approximately 15–35% during 84 ing in seven endurance-trained subjects.
power output during a graded, incremental cycle

mitochondrial atp production
test to exhaustion declined by 14.3% in a group of
No studies reporting on the consequences of endurance athletes after only 3 days of bed rest,
training cessation on highly trained athletes’ and by 10% in strength-trained athletes. Female
mitochondrial ATP production rates seem to competitive swimmers were 2.6% slower in a
be available in the exercise science literature. 366 m swim after only 10 days without training
However, using recently trained individuals as (Claude & Sharp 1991). Exercise time to exhaus-
subjects, Wibom et al. (1992) reported a 12–28% tion has also been reported to be reduced during
decrease in mitochondrial ATP production rate training cessationaby 9.2% (Houmard et al. 1992,
during 3 weeks of training cessation consecutive 1993) and 25% (Houston et al. 1979) in 2 weeks,
to 6 weeks of endurance training. This decrease and by 7.6% (Coyle et al. 1986) and 21% (Madsen
was attributed to a 4–17% reduction in indi- et al. 1993) in 4 weeks. The latter investigators
vidual mitochondrial enzyme activities. Because suggested that altered substrate utilization and/
highly trained athletes’ mitochondrial enzyme or altered Mg2+ transport from the extracellular
activities are markedly affected by training to the intracellular area, which could inhibit Ca2+
stoppage (see above), it can be inferred that a release from the sarcoplasmic reticulum, could
marked reduction in mitochondrial ATP produc- have contributed to the reduced endurance
tion would also take place in athletes undergoing performance after training stoppage. Interest-
a training cessation period. It is worth noticing, ingly, Houmard et al. (1992) suggested that the
however, that the mitochondrial ATP produc- short-term training cessation-induced perform-
tion rate remained 37–70% above pretraining ance impairment observed in their 12 distance
levels in the above-mentioned study on previ- runners was primarily due to the loss in car-
ously sedentary subjects (Wibom et al. 1992). diorespiratory fitness they had suffered, rather
than to altered mechanical efficiency, because they
did not observe a decline in running economy at
Training cessation and endurance
submaximal exercise intensities (75 and 90% of
performance
Vo2max).
It has been repeatedly shown that the endurance Swimming performance (100 and 200 m) has
performance of highly trained athletes suffers a also been shown to drop by 3–13% in national and
rapid deterioration when the training stimulus international level swimmers during the inactive
disappears or is insufficient to maintain training- period in between two training seasons (Mujika
induced adaptations (Table 6.3). Smorawinski et al. 1995). Also, exercise time to exhaustion has
et al. (2001) have recently reported that peak been reported to decline by 23.8% in 5 weeks
Table 6.3 Studies reporting changes in endurance performance measures as a result of training
cessation in athletes.
Days of training
cessation Performance measure Percentage decrease Reference
10 366 m swim 2.6 Claude & Sharp 1991

14 Exercise time to exhaustion 9.2 Houmard et al. 1992, 1993
14 Exercise time to exhaustion 25 Houston et al. 1979
28 Exercise time to exhaustion 7.6 Coyle et al. 1986
28 Exercise time to exhaustion 21 Madsen et al. 1993
≈30 100, 200 m swim 3–13 Mujika et al. 1995
32 Peak power output 18.2 Nichols et al. 2000
35 Exercise time to exhaustion 23.8 Fardy 1969
60 Peak power output 3.5–8.8 Giada et al. 1998
of training cessation in 11 college soccer players been shown to maintain their muscular strength
(Fardy 1969), and endurance-trained female run- measured on a swim bench during 4 weeks of
ners’ oxygen uptake during a standardized sub- training cessation. However, their swim power,
maximal exercise task increased significantly by indicative of their ability to apply force during
about 3–8% after 12 weeks of training cessation swimming, declined by 13.6% (Neufer et al.
(Drinkwater & Horvath 1972). In line with 1987). Longer periods of training cessation result
these results, Coyle et al. (1985) observed that in more pronounced declines in the strength
a submaximal exercise bout requiring a Vo2 of performance of strength-trained athletes, but this
3.11 ± 0.23 L·min–1 (74 ± 2% of Vo2max) when loss is still limited to 7–12% during periods of
their athletes were trained, elicited a Vo2 of inactivity ranging from 8 to 12 weeks. Häkkinen
3.20 ± 0.25 L·min–1 (90 ± 3% of Vo2max) after 84 et al. (1981) reported 11.6 and 12.0% decreases in
days without training. Compared with values squat–lift and leg extension forces, respectively,
obtained at the peak of their training season, following 8 weeks of training stoppage. In addi-
amateur cyclists aged 24 ± 6 and 55 ± 5 years tion, maximal bilateral and unilateral isometric
have been shown to decrease their peak power force decreased by 7.4 and 7.6%, respectively. This
output by, respectively, 3.5 and 8.8% during was coupled with decreased averaged maximal
2 months without training (Giada et al. 1998). bilateral (5.6%) and unilateral (12.1%) integrated
Finally, an injured female masters athlete who EMG. The latter change took place within the
could not train for 32 days, decreased her peak first 4 weeks of training cessation (Häkkinen
power output by 18.2% and her muscular resis- & Komi 1983). Results from the same group
tance to fatigue measured by a timed ride to of investigators have shown that both muscle
exhaustion at 110% of peak power output by atrophy and a diminished neural activation are
16.6%, as compared with values assessed when responsible for the decline in maximal force that
she was at the peak of her competitive season, takes place during 12 weeks of training cessation,
2 days before getting injured (Nichols et al. 2000). because FT and ST fibre areas, muscle mass and
maximal integrated electrical activity were shown
to diminish with inactivity (Häkkinen et al. 1981,
Training cessation and strength
1985; Häkkinen & Komi 1983). Studying six
performance
endurance-trained subjects during 12 weeks of
According to the available body of data, athletes training cessation, Sinacore et al. (1993) observed
can maintain or suffer a limited decay in their a significant reduction in the percentage of initial
muscular strength during short periods of train- torque after 30 s of recovery following a 1 min
ing stoppage. Fourteen days of training cessation bout of fatiguing exercise of the quadriceps
did not significantly change 12 weightlifters’ one femoris. Changes in FTa and FTb fibre distribu-
repetition maximum bench press (–1.7%) and tions paralleled changes in the rate of torque
squat (–0.9%) performance, isometric (–7%) and recovery following the 12-week period of train-
isokinetic (–2.3%) concentric knee extension force, ing stoppage. The rate of torque recovery after a
and vertical jump (1.2%) values. On the other standard bout of fatiguing exercise was related
hand, isokinetic eccentric knee extension force to Vo2max and may have reflected local muscle
and surface electromyograph (EMG) activity of endurance exercise adaptations.
the vastus lateralis decreased by 12 and 8.4–
12.7%, respectively. These results lead to the
Retention of training-induced
conclusion that eccentric strength was specific-
adaptations
ally affected in strength athletes inactive for a
short period of time, but that other aspects Overuse or any other type of injury can keep
of neuromuscular performance were unaltered athletes from performing their habitual exercises
(Hortobágyi et al. 1993). College swimmers have and/or from maintaining their usual training
intensity level. In view of the negative effects Vo2max) RER can increase slightly during per-
on physiological characteristics and perform- iods of reduced training (Houmard et al. 1990b;
ance criteria induced by an insufficient training McConell et al. 1993). Exercise blood lactate
stimulus, any strategy aiming to avoid or reduce concentration has been reported not to change
detraining would seem worthwhile for the injured (Houmard et al. 1989, 1990b) or to increase (Neufer
or the less active athlete. These strategies, which et al. 1987; McConell et al. 1993). Unchanged
generally include performing either a reduced insulin action and GLUT-4 concentrations have
training programme or an alternative form of train- also been reported as a result of reduced training
ing (i.e. to cross-train), are briefly summarized in recently trained individuals (Houmard et al.
below. 1996).
At the muscle level, research indicates that
athletes can readily maintain their lean body mass
Reduced training
(Houmard et al. 1989, 1990a, 1990b; McConell et al.
Reduced training has recently been defined as 1993), oxidative enzyme activities (Houmard et al.
a non-progressive, standardized reduction in the 1990b) and muscular strength (Neufer et al. 1987;
quantity of training, which may maintain or even Houmard et al. 1990b; Tucci et al. 1992; Martin
improve many of the positive physiological and et al. 1994) by means of reduced training pro-
performance adaptations gained with training grammes. The retention of these characteristics
(Mujika & Padilla 2000a). From a cardiorespira- may be related to a stable hormonal milieu, as
tory viewpoint, this strategy has been shown to suggested by the unchanged testosterone, cortisol
be a valuable procedure to retain many of the and testosterone : cortisol ratio that have been
training-induced adaptations for at least 4 weeks observed in trained distance runners during 3
in highly trained athletes (Neufer et al. 1987; weeks of reduced training (Houmard et al. 1990a).
Houmard et al. 1989, 1990a, 1990b; McConell et al. A growing body of data in the exercise and
1993; Martin et al. 1994; Ciuti et al. 1996), and even sports science literature indicate that maintain-
longer in moderately trained individuals (Hickson ing training intensity during periods of reduced
& Rosenkoetter 1981; Hickson et al. 1982, 1985; training and tapering is of paramount importance
Houmard et al. 1996). As a matter of fact, during for athletes in order to retain training-induced
periods of reduced training not forced by injury, physiological and performance adaptations (Van
highly trained athletes have been shown to not Handel et al. 1988; Neufer 1989; Houmard 1991;
change their: Vo2max (Neufer et al. 1987; Houmard Shepley et al. 1992; McConell et al. 1993; Houmard
et al. 1989, 1990a, 1990b; Madsen et al. 1993; Martin & Johns 1994; Mujika 1998; Mujika et al. 2000,
et al. 1994); resting (McConell et al. 1993), sub- 2002). Training volume, on the other hand, can
maximal (Houmard et al. 1989, 1990b; McConell be reduced to a great extent without risking
et al. 1993) and maximal (Houmard et al. 1989; detraining effects. Indeed, it has been indicated
Madsen et al. 1993) heart rates; submaximal that this reduction can reach 60–90% of the previ-
(Houmard et al. 1989; McConell et al. 1993) and ous weekly volume, depending on the duration
maximal (Madsen et al. 1993; McConell et al. of the reduced training period (Costill et al. 1985,
1993) exercise ventilatory volumes; and exercise 1991; Cavanaugh & Musch 1989; Neufer 1989;
time to exhaustion (Houmard et al. 1989, 1990b; Houmard et al. 1990a, 1990b, 1994; Houmard 1991;
McConell et al. 1993; Martin et al. 1994). Specific D’Acquisto et al. 1992; Johns et al. 1992; Shepley
athletic performance, on the other hand, can et al. 1992; McConell et al. 1993; Gibala et al.
decline rapidly in highly trained athletes despite 1994; Houmard & Johns 1994; Martin et al. 1994;
the use of reduced training strategies (Neufer et al. Mujika et al. 1995, 1996, 2000, 2002; Mujika 1998).
1987; Madsen et al. 1993; McConell et al. 1993). Reports from the literature also indicate that if
From a metabolic perspective, it has been training-induced physiological and performance
shown that submaximal exercise (65, 85 and 95% adaptations are to be maintained by highly trained
athletes during periods of reduced training et al. 1979; Moritani & deVries 1979; Houston et al.
frequencies, these reductions should be moder- 1983; Narici et al. 1989; Kannus et al. 1992a; Housh
ate, not exceeding 20–30% (Neufer et al. 1987; & Housh 1993; Weir et al. 1994; Housh et al. 1996).
Houmard et al. 1989; Neufer 1989; Houmard 1991; This phenomenon has obvious implications in
Houmard & Johns 1994; Mujika 1998; Mujika limiting muscular detraining during periods of
et al., 2002). unilateral casting, rehabilitation from injuries or
For additional information on the physiolo- following joint surgery.
gical and performance consequences of periods
of reduced training stimulus, readers can consult
Conclusions
the reviews by Houmard (1991), Houmard and
Johns (1994), Mujika (1998) and Neufer (1989). Sports injuries imply periods of training cessation
or a marked reduction in the habitual physical
activity level of athletes, and an insufficient train-
Cross-training
ing stimulus brings about a partial or complete
It has been suggested that cross-training, defined loss of previously acquired physiological and
here as the participation in an alternative train- performance adaptations, i.e. detraining. Cardio-
ing mode exclusive to the one normally used respiratory consequences of training cessation
(Loy et al. 1995), could be a useful means to avoid in athletes include a rapid Vo2max decline, though
or limit detraining during recovery from a sport- it usually remains above values of sedentary con-
specific injury. The limited body of data available trols. The Vo2max loss results from an almost
in the literature on the effects of cross-training as immediate reduction in total blood and plasma
opposed to training cessation suggest that whereas volumes, the latter being caused by a reduced
moderately trained individuals may maintain plasma protein content. Exercise heart rate in-
fitness and delay deconditioning by performing creases during maximal and submaximal intens-
dissimilar training modes (Moroz & Houston ities, but not sufficiently to counterbalance the
1987; Claude & Sharp 1991), similar-mode cross- reduced stroke volume. Therefore, maximal and
training would be necessary in more highly submaximal cardiac output drops, whereas it
trained individuals (Loy et al. 1995). may increase at rest. Cardiac dimensions, includ-
Thorough information on the possible benefits ing ventricular volumes and wall thickness, often
and practical use of cross-training in sports can decrease. Blood pressure and total peripheral
be found in a review by Loy et al. (1995). resistance, on the other hand, increase, and venti-
latory efficiency is most usually impaired after
short periods of training cessation.
Cross-transfer effect
A shift towards a higher reliance on carbohy-
During prolonged periods of inactivity, neural drate as a fuel for exercising muscles is a primary
(increased motor unit synchronization and act- consequence of training cessation from a meta-
ivation) and muscular (hypertrophy, increased bolic standpoint. Even short-term insufficient train-
content of creatine phosphate and glycogen) ing results in an increased respiratory exchange
adaptations induced by strength training ratio at maximal and submaximal exercise intens-
(Häkkinen et al. 1985) may be in jeopardy. Inter- ities. Glucose tolerance and whole-body glucose
estingly, however, a cross-transfer effect (also uptake are rapidly and markedly reduced, due
referred to as cross-education and cross-training) to a decline in insulin sensitivity coupled with a
of training-induced strength gains between reduced muscle GLUT-4 transporter protein con-
ipsilateral (i.e. trained limb) and contralateral tent. Muscle lipoprotein lipase activity decreases
(i.e. untrained limb) limbs has been repeatedly while it increases at the adipose tissue level,
described in the literature (Hellenbrandt et al. thus favouring the storage of adipose tissue. In
1947; Coleman 1969; Shaver 1975; Krotkiewski addition, the training-induced antiatherogenic
lipoprotein profile is reversed. Blood lactate capacity results in a rapid decline in the trained
concentration increases at submaximal exercise athletes’ endurance performance. This has been
intensities, and the lactate threshold is apparent shown by impaired performance measures in
at a lower percentage of Vo2max. These changes, all-out swims, peak power output and time to
coupled with a base deficit, result in a higher exhaustion tests. In contrast, force production
postexercise acidosis. Trained muscle’s glycogen declines slowly and in relation to decreased
concentration suffers a rapid decline, reverting EMG activity. Strength performance in general is
to sedentary values within a few weeks of train- thus readily retained for up to 4 weeks of training
ing cessation. cessation, but highly trained athletes’ eccentric
Skeletal muscle tissue is characterized by force and sport-specific power may suffer sig-
its dynamic nature and extraordinary plasticity, nificant declines within this timeframe.
which allows it to adapt to variable levels of Reduced training strategies have been shown
functional demands. When these demands are to delay the onset of detraining at the cardiore-
insufficient to retain training-induced adapta- spiratory, metabolic and muscular levels in highly
tions, muscular detraining occurs. This implies trained athletes. A maintenance of training in-
alterations in both muscle structure and muscle tensity appears to be the key factor for an athlete
function. Muscle capillary density could decrease to retain training-induced physiological and per-
in athletes within 2–3 weeks of training cessa- formance adaptations during periods of reduced
tion, but this possibility has not been clearly training, whereas training volume can be reduced
established. Muscle fibre distribution remains by as much as 60–90%. Training frequency reduc-
unchanged during the initial weeks of training tions, on the other hand, should be more moderate,
cessation, but there may be a decreased propor- not exceeding 20–30%.
tion of ST fibres and a large shift from FTa to FTb Performing alternative training modes exclus-
fibres in endurance athletes, and an increased ive to the one normally used by an athlete (i.e.
oxidative fibre population in strength-trained cross-training) may delay detraining, as long as
athletes within 8 weeks of training stoppage. A similar-mode exercises are performed. However,
general decline in muscle fibre CSA is rapidly even dissimilar-mode cross-training may be bene-
measurable during training cessation in strength ficial to the moderately trained subject.
and sprint-orientated athletes, whereas fibre area Finally, given that a cross-transfer effect be-
may increase slightly in endurance athletes. The tween ipsilateral and contralateral limbs is often
arteriovenous oxygen difference, unchanged fol- observed during periods of unilateral strength
lowing 3 weeks without training, declines after training, exercising the healthy limb should be
8 weeks of continued inactivity. Myoglobin con- recommended during periods of unilateral cast-
centration, on the other hand, does not seem to ing, rehabilitation from injuries or following joint
be affected by training cessation. Rapid and pro- surgery.
gressive reductions in oxidative enzyme activities
result in a reduced mitochondrial ATP produc-
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training and detraining on lumbar extension strength. detraining. Journal of Applied Physiology 73, 2004–2010.
Spine 17, 1497–1501. Wilber, R.L. & Moffatt, R.J. (1994) Physiological and
Van Handel, P.J., Katz, A., Troup, J.P., Daniels, J.T. & biochemical consequences of detraining in aerobic-
Bradley, P.W. (1988) Oxygen consumption and blood ally trained individuals. Journal of Strength and Con-
lactic acid response to training and taper. In: Swimming ditioning Research 8, 110–124.
Chapter 7
Physiological and Functional

Implications of Injury
CHRISTOPHER J. STANDAERT AND STANLEY A. HERRING
efficiency of the task and cause overload on other

Introduction
areas with resultant dysfunction or tissue failure.
As even the casual reader of this text can discern, In considering the local and systemic effects of
musculoskeletal injury in the athlete can involve injury and inactivity, it becomes apparent that
a wide range of anatomical structures and physio- any element of the kinetic chain can either be a
logical variables. Understanding the ways in possible causative factor in injury or be at risk for
which injury and treatment affect the athlete’s the deleterious effects of injury. In the case of a
physical performance is central to developing baseball pitcher with a sore shoulder, for example,
both an acute treatment strategy and a long-term the local tissue injury in the shoulder may be
management plan for the athlete. Injury clearly partly related to relative muscular imbalance in
can involve significant tissue damage, resulting the shoulder or inflexibility in the lumbar spine.
in pain and reduced physical performance. How- Resting the pitcher with the intent of allowing the
ever, injury needs to be viewed in the setting of
the entire athlete, not just the local area of acute
tissue damage. Prior injuries, strength or flexibil- 2
ity imbalance, skill, technique, or any of a num-
ber of other factors affecting the full functional
kinetic chain can have a strong bearing on how to
approach rehabilitation in a given individual.
As described by Kibler (1998), the term ‘kinetic
chain’ refers to the sequencing of individual
body segments or joints that must be moved in a
specific order and manner to allow for the effici-
ent accomplishment of a given task. The task of
pitching a baseball is an example of one such task 1 2
(Fig. 7.1). This skill, along with most of those in
the throwing or hitting sports, actually involves 1
two separate chains of motion: one extends from
the ground and planting leg through the hip and Fig. 7.1 Illustration of the kinetic chains involved in
trunk to the landing leg; the other extends from pitching a baseball. The first chain extends from the
the ground and planting leg through the pelvis ground and planting leg to the hip, trunk and down
the landing leg. The second chain runs from the
and trunk to the shoulder, elbow, wrist and, ulti- ground and planting leg to the hip and trunk then to
mately, the hand (Kibler 1998). Injuries or deficits the shoulder, elbow, wrist and hand of the throwing
anywhere along these chains can decrease the arm. (Adapted from Kibler 1998.)
144
consequences of injury 145
acute inflammation in the shoulder to resolve may for the increased risk of reinjury are not entirely
result in numerous less desirable consequences. clear, but several possibilities exist, including
These might include reductions in endurance, incomplete recovery from the initial injury, incom-
strength, mobility or neuromuscular control, all of plete rehabilitation, uncorrected biomechanical
which are necessary for the production of appro- problems, or physiological, anthropomorphical
priate arm speed, positioning and release neces- or technique issues related to an individual
sary to achieve optimal ball speed and movement. athlete (Keller et al. 1987; Rutherford et al. 1990;
Awareness of the potential for these deficits is Macera 1992; Taylor et al. 1993; Jonhagen et al.
crucial in the rehabilitation of the athlete. This 1994). Clearly, athletic injuries have a significant
chapter will present a format for understanding impact on a large number of athletes, teams and
injury in this context and include a discussion of sporting events. Interventions that may lessen
the physiological and functional implications of the ultimate impact of an injury upon an athlete’s
injury as they relate to rehabilitation. performance, including comprehensive rehabil-
itation, may have a dramatic effect not just for the
individual athlete, but for sports competition as
Rehabilitation
a whole.
Sports injuries are an extremely common event The rehabilitation plan for an individual athlete
for athletes (see Chapter 1). Reports of injury is based upon an assessment of the athlete’s
rates and severity vary widely by sport and also specific injury and more global functional prop-
by methods of measurement (Henry et al. 1982; erties, along with an understanding of the func-
Keller et al. 1987; Saal 1991; Bennell & Crossley tional consequences of the injury and treatment.
1996; Murtaugh 2001). None the less, reported First, the actual tissue injury must be diagnosed
injury rates can be extremely high, including a accurately. The presentation of the injury, or
12.7% incidence of injury in adolescent wrestlers the clinical symptom complex (Herring 1990),
during participation in a single tournament (Lorish needs to be identified, as do the type of injury
et al. 1992), a greater than 50% injury rate for high and the physiological and biomechanical factors
school football players for a single season (DeLee associated with its occurrence. Finally, the acute
& Farney 1992), a 69% injury rate for a profes- method of treatment needs to be established with
sional basketball team over 7 years (Henry et al. a thorough knowledge of the local or systemic
1982) and a lifetime incidence of > 70% for inter- effects of the chosen modality (e.g. immobiliza-
fering shoulder pain in elite swimmers (McMaster tion, surgery, etc.). From this base, an appropriate
& Troup 1993). The natural history of soft tissue rehabilitation strategy can be developed that
injuries is not necessarily benign, eitheraa recent addresses the full functional capacity of the
study on ankle sprains in the general population athlete (Herring & Kibler 1998).
(the vast majority of which were not treated with Although injury is often associated with
extensive rehabilitation) reported that 72.6% of focal tissue damage, the goal of treatment for an
subjects had persisting symptoms 6–18 months injured athlete extends far beyond achieving
after injury (Braun 1999). An initial injury may tissue homeostasis. The athlete’s goal is to return
also have a significant impact on the risk of fur- to sport at the highest level of performance pos-
ther injury. A review on injuries in soccer players sible. This means that medical professionals have
noted that prior injury was one of the factors to deal with all aspects of the athlete’s function-
most strongly associated with new injury and ing. As will be discussed, injury and the sub-
that 20% of ‘minor’ injuries were followed by a sequent acute treatment can result in diminished
more severe injury within 2 months (Keller et al. soft tissue tensile strength, decreased aerobic
1987). Macera (1992) also noted that there is a capacity, cellular and neurological changes, and
strong effect of previous injury on the risk of residual disability even in the absence of symp-
further injury in runners. The precise reasons toms. Rehabilitation needs to address all of these
issues, with an initial goal of symptom resolution severity that exceeds the tissue’s ability to enact
and an ultimate goal of restored function and appropriate repair or maintenance. This can result
continued fitness to minimize the risk of recur- in weakening of the structural properties of the
rent injury and preserve long-term performance affected tissue, adaptations of function in adjac-
(Herring & Kibler 1998). This concept is import- ent or compensatory structures, pain, impaired
ant in understanding why rehabilitation is neces- performance and, potentially, tissue failure. There
sary in the first place and why ‘rehabilitation’ is a continuum of injury present between these
really refers to an ongoing process of training and two mechanisms of ‘acute’ and ‘chronic’ injury,
maintaining the injured athlete. however; many apparently acute or macro-
traumatic events causing disruption are strongly
related to underlying degeneration, weakness or
Injury
misuse resulting from a lengthier microtraumatic
Specific tissues respond differently to the stress process of tissue degeneration. The vast majority
and strain associated with trauma (see Chap- of acute tendon ruptures, in fact, are associated
ters 3–5). Generally speaking, however, injury with prior pathological change in the tendon
occurs when the forces applied to a given anatom- (Leadbetter 1994). This conceptual model rein-
ical structure exceed the physiological tolerance forces the concept that injury occurrence, preven-
or reparative capabilities of that structure. As a tion and treatment represent ongoing, dynamic
gross step in assessing injuries, they can be broken processes occurring within the body’s structural
down into two major types: macrotraumatic or and cellular balance (Fig. 7.2).
microtaumatic (Leadbetter 1994; Quillen et al. A structural format for approaching the treat-
1996; Herring & Kibler 1998). Macrotrauma refers ment of an athletic injury needs to include a full
to acute, extreme forces that overwhelm the understanding of the clinical and physiological
tensile or structural properties of a given tissue. alterations induced by or associated with injury
This is generally thought of as resulting in the (Table 7.1). The injured athlete is typically being
acute deformation or disruption of previously assessed by medical personnel for complaints
normal structures, such as might occur with an of pain, weakness, oedema or dysfunction. The
acute ankle fracture or anterior cruciate ligament presenting symptoms can be referred to as the
tear. Microtrauma, on the other hand, refers to clinical symptom complex. For a patient with a
smaller forces that cause lesser degrees of cellu- rotator cuff injury, there may be local complaints
lar or structural disruption and occur at a rate or of pain, weakness and diminished range of motion
Return to
participation
Musculotendinous
tensile overload
Healing Subclinical
Tissue injury
adaptations
Decreased
performance
Microtears Macrotears
Functional
Clinical symptoms biomechanical deficits
1 Pain 1 Muscular weakness Fig. 7.2 The injury cycle and
2 Instability 2 Inflexibility feedback mechanisms, illustrating
3 Dysfunction 3 Scar tissue the multifactorial nature of
4 Muscle strength athletic injury. (From Kibler et al.
imbalance 1992, with permission.)
Table 7.1 Complete diagnosis of rotator cuff tendonitis/impingement in a baseball pitcher.

(Adapted from Herring 1990.)
Clinical symptom complex Impingement symptom pattern

Anterior–superior glenohumeral instability
Decreased pitch velocity
Prolonged recovery time
Tissue injury complex Tear in posterior capsule
Tear in rotator cuff
Glenoid labral attrition
Tissue overload complex Tensile load on posterior shoulder capsule
Tensile load on posterior shoulder muscles
Tensile load on scapular stabilizing muscles
Functional biomechanical deficit complex Internal rotation inflexibility
External/internal rotation strength imbalance
Lateral scapular slide
Alteration of trunk motion with increased passive lumbar
lordosis and decreased lateral lumbar flexion
Decreased hip mobility
Subclinical adaptation complex Altered shoulder or elbow positioning
Decreased pitch velocity
all affecting the injured shoulder. The actual cant strength imbalance at the shoulder with a
tissue injury represents the tissue injury complex. relative increase in strength of the shoulder inter-
In the above-mentioned athlete with a rotator nal rotators compared with the external rotators
cuff injury, this may be a partial tear of the (McMaster et al. 1991; Chandler et al. 1992). This
supraspinatus tendon. Frequently, medical assess- relative imbalance has been hypothesized to
ment focuses on these two components of the be related to shoulder injuries in those athletes
injured athlete. The actual symptomatic tissue due to an alteration of the normal mechanics
injury, however, may be accompanied by prob- of the glenohumeral joint (McMaster et al.
lems with associated structures that have been 1991; Chandler et al. 1992). This is an example of
overloaded, suboptimally lengthened or other- the functional biomechanical deficit complex which
wise impaired by the acute injury, or that may be includes abnormalities in strength or flexibil-
contributing to the injury. These related prob- ity associated with injury. Finally, alterations
lems are referred to as the tissue overload complex in mechanics, motion or task performance may
(Herring 1990; Herring & Kibler 1998). In the result from injury or functional biomechanical
athlete with a shoulder injury, this may include deficits. These associated problems are referred
tensile load on the posterior shoulder capsule to as the subclinical adaptation complex. As this
due to dynamic instability of the glenohumeral name would imply, these adaptations may not
joint or excessive load on the rhomboids related be directly associated with symptoms but can
to relative lateral translation of the scapula. contribute to progression or perpetuation of injury
In looking beyond local tissue injury, the clini- and impaired performance (Herring 1990; Kibler
cian also has to assess underlying biomechanical et al. 1991; Herring & Kibler 1998). An example of
or technique issues involved with the perform- this would be a baseball pitcher who lowers the
ance of an injured athlete. Continuing with the elbow of his or her throwing arm and changes
shoulder example, studies of relative isokinetic the release point of the ball due to a combination
strength in uninjured elite water polo players of shoulder pain, dynamic instability and internal
and collegiate tennis players have shown signifi- rotation inflexibility.
Viewing injury in the context just described the stabilizing properties of an injured ligament.
allows medical personnel to fully evaluate all of The loss of joint stability associated with an acute
the contributing biomechanical and physiological ligament injury also needs to be considered dur-
factors affecting an athlete’s injury, impaired ing the early phase of rehabilitation in order to
performance and full symptom complex. Once avoid further injury to the ligament complex.
this is assessed, an appropriate strategy for Tendon injuries are slightly different from
correcting deficits in all relevant areas can be ligamentous injuries and, subsequently, pose dif-
addressed, and an acute injury treatment plan ferent issues in the rehabilitation process. Tendons
can advance to a full management programme may also be acutely injured due to macrotraum-
for the athlete. atic forces applied across the musculotendinous
unit. However, tendons are also the structures
most frequently involved in overuse, or, perhaps
Tissue damagecthe tissue
more appropriately termed, chronic overload
injury complex
syndromes, which involve repetitive loading
Although the general inflammatory cascade is with partial disruption of the tendon structure
similar in all acute soft tissue injuries, the distinct (Herring & Nilson 1987; Curwin 1996). In over-
structural and reparative properties of differ- load injuries, the forces applied to an injured
ent tissues impact on how this process affects tendon may be within a physiological range
recovery and performance. The injury and repair for the tendon but they occur at a frequency that
processes for specific tissues are well addressed prohibits adequate recovery or repair processes.
in other chapters in this book (see Chapters 3–5). This may ultimately lead to failure of the tendon
However, some specific aspects of soft tissue structure (Curwin 1996). Tendon repair mechan-
injury and repair will be briefly reviewed in isms would imply that progressive loading of
order to more fully develop the underpinnings the injured structure is necessary to optimize the
of rehabilitation treatment. restoration of the tensile strength. Given the fre-
Ligament injuries frequently occur as a result quency with which extrinsic factors are associated
of acute macrotraumatic forces applied to the with tendon injuries, it is also important to assess
ligament causing structural disruption of vary- an athlete for issues of flexibility, strength im-
ing degrees. The amount of force necessary to balance, equipment and technique in order to
cause ligamentous disruption is dependent upon minimize deleterious effects that may be associ-
the size of the ligament, the age of the individual ated with external appliances or maladaptive
and the joint position at the time of injury. The motion patterns. These issues could potentially
healing process results in scar formation with involve the tissue overload complex, the func-
collagen deposition but is frequently inad- tional biomechanical deficit complex or the sub-
equate to withstand future load bearing (Frank clinical adaptation complex, and illustrate the
1996). Even in the best of circumstances, maximal importance of recognizing how all of these areas
recovery may take more than 1 year and still contribute to the problems of an injured athlete.
result in a decrement of 30–50% in tensile strength Muscular injuries are, yet again, distinct
(Leadbetter 1994). Immobilization may addition- from isolated tendinous or ligamentous injuries.
ally impair the structural properties of an injured Muscle injuries may occur in the midsubstance
ligament (Frank 1996; Salter 1996). As the func- of the muscle proper, such as in a contusion, or
tional role of a ligament is to serve as a passive in the region of the myotendinous junction, as
support for joint positioning and to potentially in a strain. In considering differences between
provide proprioceptive feedback, the rehabilita- tendinous and muscular injuries, the region of
tion of ligamentous injuries needs to include work the musculotendinous junction warrants particu-
on restoring or improving dynamic joint control lar attention. Muscle strain injury is felt to occur
through the kinetic chain in order to reinforce during elongation of the muscle, typically during
forceful eccentric contraction, and is particularly 1994). The type of treatment chosen and the
common in sports involving sprinting or jump- length of immobilization may also have a signifi-
ing (Noonan & Garrett 1992; Taylor et al. 1993; cant impact on the actual reparative processes
Jonhagen et al. 1994; Bennell & Crossley 1996; within injured muscle and the degree to which
Garrett 1996; Jarvinen et al. 2000). The vast major- contractile elements penetrate the connective
ity of muscular strain injuries have been shown tissue (Jarvinen & Lehto 1993).
to occur at the region of the musculotendinous Accurately assessing the nature and severity
junction, generally affecting the muscle immedi- of the tissue injury in an affected athlete, i.e. the
ately adjacent to the junction rather than in the tissue injury complex, is crucial in determin-
junction itself (Taylor et al. 1993; Garrett 1996; ing an appropriate rehabilitation approach to the
Malone et al. 1996). ‘Two-joint’ muscles, such as patient. The type of tissue injured, the degree
the rectus femoris, gastrocnemius and hamstrings, of structural damage, the concurrent structures
are particularly vulnerable to this type of injury affected and the potentially deleterious effects of
(Noonan & Garrett 1992; Mair et al. 1996; Jarvinen immobilization on adjacent structures all need to
et al. 2000). The tensile forces generated by the be taken into account in treatment. Although dif-
muscle during maximal eccentric loading com- ferent tissues are discussed in isolation above, an
bined with the forces associated with elonga- injury frequently results in alterations to several
tion of the static viscoelastic components of the different tissue components. For example, a
muscle probably contribute to the frequency surgically treated acute tear of the anterior cruci-
with which strain injury occurs during moments ate ligament in an athlete may ultimately result
of forceful eccentric contraction of the muscle in alterations of bone, tendon and ligament with
(Malone et al. 1996). There are, additionally, additional components of muscular atrophy,
distinctive properties of the sarcomeres and capsular tightness, aerobic deconditioning and
membranous structures adjacent to the musculo- alterations in neural control. Understanding each
tendinous junction that may contribute to this of the individual components associated with
area being particularly vulnerable to strain injury an injury allows for a more comprehensive and
(Noonan & Garrett 1992). precise approach to treatment.
Healing of muscular strain injuries, as well
as of disruptions of the muscle more distant
Immobilization and rest
to the site of the musculotendinous junction,
consists of scar deposition with regeneration Acute injury of soft tissue or bone is frequently
and ingrowth of contractile elements and nerves managed by a period of immobilization of the
(Jarvinen et al. 2000). Acutely, there is a signifi- injured body part or by rest of the injured area
cant decline in contractile strength and peak load or the athlete as a whole. This is done to allow
tolerance in injured muscle, and the scar is at for adequate healing and restoration of tensile
its weakest point until 10–12 days after injury strength so that the injured structure may begin
(Taylor et al. 1993; Jarvinen et al. 2000). Tensile to bear physiological loads with less risk for
strength recovery also appears to lag behind the recurrent injury. Periods of immobilization
recovery of force-generating capacity (tension required for the treatment of different injuries
generation), making the muscle perhaps more can vary highly. For example, ankle or radial
vulnerable to repeat injury than it may appear fractures may frequently be immobilized in a
by tension-generating capacity alone (i.e. gross rigid cast for 4–6 weeks, acute spinal fractures
measures of ‘strength’) (Garrett 1996). Scar may be treated with a rigid brace for up to
formation may significantly impair the ability of 3 months, and some authors recommend the use
contractile elements in injured muscle to repair, of a rigid brace for 6–12 months in the manage-
and contractile ability may be reduced by 10– ment of spondylolysis (Steiner & Micheli 1985;
20% long term ( Jarvinen & Lehto 1993; Leadbetter Tropp & Norlin 1995; McDowell 1997; Byl et al.
1999). Although often viewed as a useful tool 250 Before immobilization

in the management of musculoskeletal injuries, 225 After immobilization
immobilization and inactivity can have signifi- 200
175
Torque (nm)
cant deleterious effects on the injured athlete.
150 **
These changes may affect how an athlete will 125 ** **
be able to progress through a rehabilitation pro- 100 ** **
gramme after injury. Understanding the scope 75
and time course of deficits involved with rest and 50
immobilization allows health care professionals 25
0
to apply both preventative and restorative care
60 120 180 240 300
in the course of recovery.
(a) Angular velocity (degree . s−1)
Muscle 200
175
At the muscular level, there are significant changes
150
in the function and structural properties of the
Torque (nm)
125 ** **
musculotendinous unit treated with immobiliza- **
**
tion. These changes include reductions in strength, 100 *
limb volume, limb weight and the cross-sectional 75
area of muscles as a whole and of individual 50
muscle fibres (Muller 1970; Wills et al. 1982; Booth 25
1987; Veldhuizen et al. 1993; Bloomfield 1997; 0
Zarzhevsky et al. 1999). There are, additionally, 60 120 180 240 300
selective changes in enzymatic function and pro- (b) Angular velocity (degree . s−1)
tein synthesis and alterations to the musculo-
Fig. 7.3 Peak torque of: (a) knee extension and
tendinous junction with reduced contact area (b) knee flexion before and after 4 weeks of cast
between the muscle cells and tendineal collagen immobilization in healthy volunteers. The bars
fibres (Wills et al. 1982; Appell 1990; Kannus et al. show the medians and 75th percentiles (n = 8).
1992; Hortobagyi et al. 2000). All of these factors *, P < 0.05; **, P < 0.01. (From Veldhuizen et al. 1993,
with permission.)
play a role in the functional implications for
managing patients with injuries treated with
immobilization.
When looking strictly at muscle strength, the 8 weeks after open reduction and internal fixation
losses associated with immobilization can be proof an ankle fracture found a reduction of about
found. A recent study by Hortobagyi et al. (2000) 50% for ankle plantar flexion peak isometric torque
found that healthy volunteers placed in a fibre- with reductions in isokinetic torque for all angular
glass cast for 3 weeks sustained an average 47% speeds and positions (Shaffer et al. 2000). The
decrease in eccentric, concentric and isometric strength losses seem to be more dramatic with
strength of knee extension. Similar decreases the use of rigid immobilization than with either
in peak isometric torque of 53% for knee exten- limb suspension or bed rest, although these also
sion and 26% for knee flexion were noted by result in dramatic reductions in strength over a
Veldhuizen et al. (1993) after 4 weeks of cast fairly rapid time course (Berg et al. 1991; Bloomfield
immobilization in healthy volunteers (Fig. 7.3) 1997). This may suggest that there is a beneficial
Geboers et al. (2000) found a 28% decrease in effect on relative strength loss by the preservation
dorsiflexion torque for individuals who under- of some degree of joint mobility, although the true
went cast immobilization for 4–6 weeks after magnitude of any such effect is not clear currently.
ankle fractures. A study of individuals casted for Declines in muscular strength with immobilization
Fig. 7.4 Magnetic resonance

imaging (MRI) of the bilateral
thighs (axial view) of an
otherwise healthy 36-year-old
female 8 weeks after arthroscopic
surgery on the right knee. Note
the prominent atrophy in the
quadriceps musculature on the
right. Atrophy in the hamstrings
is less pronounced. There was no
atrophy noted preoperatively.
VL, vastus lateralis; VI, vastus
intermedius; RF, rectus femoris;
BF, biceps femoris (long head);
ST, semitendinosis; SM,
semimembranosis.
or disuse appear to be most prominent in anti- months after immobilization (Grimby et al. 1980;
gravity extensor muscles such as the quadriceps Wills et al. 1982; Appell 1990; Tropp & Norlin
and gastrocnemius/soleus (Appell 1990; Dittmer 1995; Zarzhevsky et al. 1999; Cruz-Martinez et al.
& Teasell 1993; Veldhuizen et al. 1993; Bloomfield 2000). The rate and extent of recovery may be
1997; Hortobagyi et al. 2000). Overall, the most dependent upon the type and intensity of retrain-
rapid period of strength loss seems to be early in ing applied. Both the effects of immobilization
the course of immobilization with little additional and the response to training appear to be speed
loss occurring after the first week (Muller 1970; and task specific (Grimby et al. 1980; Wills et al.
Wills et al. 1982; Appell 1990). 1982; Rutherford 1988; Appell 1990; Zarzhevsky
The losses in strength are paralleled by muscle et al. 1999). These issues clearly have a major
atrophy and losses in muscle fibre size (Fig. 7.4). bearing upon any rehabilitation plan for an injured
Human studies have shown a decrease in fibre athlete who has been treated with rest and/or
size by up to 14–17% after 72 h of immobilization immobilization.
(Lindboe & Platou 1984; Booth 1987). In the study
mentioned previously by Veldhuizen et al. (1993),
Neural changes
healthy subjects who were placed in a long leg
cast for 4 weeks were found to have sustained Loss in muscle mass may not be the only factor
a 21% loss in quadriceps cross-sectional area by affecting muscular performance following rest
computed tomography and a 16% decrease in or immobilization. There appear to be neural
fibre diameter. changes that affect relative muscular efficiency.
Although the strength losses associated with This is suggested by changes in the relative elec-
immobilization occur rapidly, the recovery of tromyograph (EMG) activity per unit of force
strength and mass may take a very long time, and produced, a decrease in the number of function-
strength may never recover completely in some ing motor units and a decrease in reflex potentia-
cases. Rutherford et al. (1990) found a marked tion (Bloomfield 1997). Cruz-Martinez et al. (2000)
reduction in strength and cross-sectional area of found EMG abnormalities felt to be consistent
previously injured and immobilized limbs com- with quadriceps motor neurone inhibition in
pared with the contralateral, uninjured limbs in patients studied after 1–4 months of knee immo-
patients assessed 1–5 years after their injuries. bilization after injury. Seki et al. (2001a, 2000b)
Similarly, other authors report prolonged decre- studied the effects of 6 weeks of immobilization
ments in strength or muscle mass for weeks to on the function of the first dorsal interosseus
cm An additional factor affecting muscular effici-

ency after injury may be the influence of degen-
1 erative changes or joint effusion on muscular
4 5 6 function. It has been proposed that the presence
cm
of a joint effusion or degenerative joint changes
1 may cause reflex inhibition of certain muscle
groups or fibre types (Spencer et al. 1984; Young
et al. 1987; Hurley & Newham 1993; Young
3 1993; Hopkins et al. 2001). This concept is sup-
ported, in part, by work showing differential
reflex inhibition or relative excitability of selected
5
muscle groups at a joint affected by an effusion
(Young et al. 1987; Hopkins et al. 2001). Spencer
et al. (1984) studied the effects of progressive
instillation of fluid into the knee joints of healthy
Motor cortex area of the immobilized muscle volunteers in order to assess the effects of an
Motor cortex area of the unaffected muscle effusion on reflex inhibition. They found that
increasing volumes of fluid instilled into the
Fig. 7.5 Motor cortex areas of both tibialis anterior joint were associated with reductions in the H-
muscles in a patient with unilateral immobilization of
reflex amplitude recorded from the quadriceps
the ankle for 8 weeks. (From Liepert et al. 1995, with
permission from Elsevier Science.) muscles. The H (or Hoffman) reflex is felt to reflect
the relative excitability of the motor neurone
pool. The degree of change in the amplitude of
muscle of the hand and found that the maximal the evoked response was related to the volume
motor neurone firing rate was decreased tran- instilled in a linear manner (Fig. 7.6). The changes
siently. The changes in maximal firing rate were were not seen in anaesthetized joints, consistent
more profoundly affected during the first 3 weeks with a mechanism of motor neurone inhibition
of immobilization than in the latter 3 weeks mediated by afferent receptors in the knee joint
and seemed to recover close to normal after 6 or capsule.
weeks following the period of immobilization. The potential inhibitory effect of a joint effu-
The authors felt that changes in the contractile sion on motor neurone function may represent
properties of muscle after immobilization can be a confounding factor when comparing studies
causally related to the alterations in firing rate of that involve individuals treated with immob-
the motor neurones. ilization after an injury (in which there may
In addition to alterations at the spinal cord or well be an associated effusion) to those that
muscular level, there is evidence that immobil- involve the immobilization of healthy volun-
ization affects cortical function as well. A study by teers (who probably do not have an effusion
Liepert et al. (1995) using transcranial magnetic present). However, in clinical practice, immo-
stimulation identified a decrease in the motor bilized joints are very frequently associated
cortex area associated with tibialis anterior func- with an injury or surgical intervention that may
tion in patients immobilized at the ankle (Fig. 7.5). result in an effusion. Understanding the poten-
The cortical changes reversed rapidly after volun- tial for neurological changes seen with either
tary muscular function, but suggest that cortical immobilization alone or with an effusion may
reorganization may occur with immobilization. allow clinicians to better understand the func-
This may potentially play a role in reduced tional properties of the limb of an injured athlete
muscular efficiency and motor control following affected by an effusion, a period of immobiliza-
injury and disuse. tion, or both.
2
Vastus medialis Vascular changes
y = 1.6−0.01x
Along with muscular and neural changes associ-
H-reflex amplitude (mV)
ated with immobilization, there also appear to be

significant local vascular changes. Immobilization
affects both the vascular density in the muscle
1
and the three-dimensional structure of the vessels
themselves (Kvist et al. 1995; Oki et al. 1998). In a
study on the rat gastrocnemius, Kvist et al. (1995)
found that 3 weeks of immobilization resulted
in a 30% reduction in capillary density in the
0 musculotendinous junction of the immobilized
muscle. As most of the blood supply to a tendon
1
is felt to come from the muscle vasculature, a
Rectus femoris
y = 0.7−0.003x
decrease in the capillary bed at the musculo-
tendinous junction may be a contributing factor to

subsequent injury due to loss of tensile strength
in the tendon (Kvist et al. 1995). The potential for
recovery of the vascular system appears to be
good with remobilization and occurs much more
rapidly in muscles mobilized earlier and in those
subjected to progressively increased physical
training (Jarvinen & Lehto 1993; Kvist et al. 1995).
0
Joint function
1
Vastus lateralis Immobilized joints are subject to multiple poten-
y = 0.69−0.004x tial changes after immobilization, including con-
tracture, adhesions, cartilage atrophy, erosions at

areas of bony contact and reduced load tolerance
of ligamentous attachments (Akeson et al. 1987;
Dittmer & Teasell 1993). Loss of joint motion is
a significant concern following immobilization
for an injury. Human and animal studies have
shown significant deficits in motion of affected
joints following immobilization (Akeson et al.
0 1987; Tropp & Norlin 1995; Reynolds et al. 1996;
0 10 20 30 40 50 60 Salter 1996; Schollmeier et al. 1996; Byl et al. 1999;
Volume (ml) Trudel et al. 1999; Trudel & Uhthoff 2000). In a rat
Fig. 7.6 Reduction in H-reflex amplitudes in the
model using immobilization at the knee, Trudel
quadriceps muscles as a function of the volume of et al. (1999) found that joint contracture occurred
saline introduced into the knee joint. (From Spencer as little as 2 weeks after immobilization and pro-
et al. 1984, with permission.) gressed at an average rate of 3.8°·week–1 for
16 weeks with an apparent plateau reached after
that point (Fig. 7.7). In a study on the effects
of cast immobilization for distal radial fractures
treated non-operatively, Byl et al. (1999) found
160 were normalized by 12 weeks after cast removal.

150 In contrast to this, Tropp and Norlin (1995) found
140
significant declines in range of motion at the
130
ROM (degrees)
120 ankle 10 weeks after surgical treatment for ankle

110 fractures with motion close to normal by 12
100 months after injury. Significant joint dysfunction
90 * well beyond this timeframe following immobil-
80 *
70 ization has also been recognized in the medical
60 * literature for well over a century (Salter 1996).
* *
50 Beyond loss of range of motion, numerous
40 other aspects of joint function and structure are
0 5 10 15 20 25 30 35
affected by immobilization. It has been proposed
Duration of immobilization (weeks)
that joint function and homeostasis are depend-
Experimental ent upon motion and use (Akeson et al. 1987;
Control Salter 1996). In the absence of these factors (i.e.
Experimental contralateral with immobilization), the functional and structural
Control contralateral properties of the joint cannot be maintained. This
Control sham-operated
leads to a number of documented changes in the
joint structure. These include the degradation
Fig. 7.7 Total range of motion (ROM) as a function
of immobilization of the knee (in weeks) in a rat of articular cartilage, adherence of the synovial
model. By the time of the initial assessment at 2 weeks, membrane to the underlying cartilage and within
there had already been a loss of 29° of motion in the synovial folds, synovial hyperplasia, destruction
immobilized joints compared with controls. The lines of ligamentous attachment sites and proliferation
at the upper portion of the graph represent the various
of connective tissue into the joint space (Akeson
controls in the study and a combined comparison
group (dashed line) used for statistical comparisons. et al. 1987; Salter 1996; Schollmeier et al. 1996).
*, P < 0.001. (From Trudel et al. 1999, with permission.) Synovial fluid is also affected, with reductions in
hyaluronic acid levels noted following immobil-
ization in an animal model (Pitsillides et al. 1999).
marked reductions in range of motion after cast There is, additionally, degradation of the collagen
removal (average cast time = 4.1 weeks). Their fibre structure of associated ligaments, probably
results included losses of greater than 50% of presenting a potential source of recurrent injury
expected motion for all planes in the wrist and (Akeson et al. 1987).
restriction of pronation and supination to 40% of
normal.
Cardiovascular and aerobic capacity
Studies on the persistence of joint contracture
after immobilization and injury vary, and the In addition to changes in locally involved struc-
actual results in a given case are probably depend- tures, immobilization and rest can have profound
ent upon multiple issues including the actual effects on overall cardiovascular and aerobic cap-
nature of the injury and the extent and duration acity. Dramatic declines in Vo2 max and maximal
of immobilization. After 4 weeks of immobiliza- exercise performance can occur with extended
tion of the knee in a plaster cast in healthy human rest (Neufer 1989; Convertino 1997). The rate of
volunteers, Veldhuizen et al. (1993) found that loss of aerobic capacity has been estimated at
range of motion returned to normal within 3 days 0.9% per day for 30 days of bed rest (Convertino
after cast removal. In a canine model of shoulder 1997). The decline in Vo2 max initially appears to
immobilization, Schollmeier et al. (1996) found be due to a reduction in circulating blood volume
that 12 weeks of cast use resulted in significant and venous return with a subsequent decline in
losses in passive range of motion initially that cardiac output and stroke volume (Neufer 1989;
Convertino 1997). Peripheral mechanisms of de- global view of athletic function into a rehabili-
creased muscle capillarization, decreased vascu- tation plan from the onset of injury through
lar conductance and decreased muscular oxidative resumption of play.
enzyme capacity also occur with detraining but
do not seem to play a major role in initial declines
The kinetic chain and
in Vo2max. These changes may be more import-
muscular balance
ant in submaximal exercise tolerance, however
(Neufer 1989). Changes in Vo2max may be more As noted previously, comprehensive rehabilita-
profound in conditioned athletes, in part due tion of an injured athlete requires that a clinician
to their greater relative level of aerobic fitness assess the entire kinetic chain for problems that
compared to untrained individuals (Convertino may arise from or contribute to injury (Fig. 7.1).
1997). Two of the major issues that relate to the mech-
Losses in aerobic fitness are related to the anics of, and force transmission through, the
relative duration, frequency and intensity of kinetic chain are relative strength and flexibility
training levels that are retained during periods across regions of the chain. Determining the
of reduced activity that may follow an injury. optimal degree of flexibility or muscular balance
Vo2max can be maintained for up to 15 weeks with for a given athlete may not necessarily follow
reductions in training frequency of up to 66% if uniform parameters, however, and these factors
the training duration is held constant (Neufer need to be assessed in the context of a given indi-
1989). A combined reduction of training frequency vidual and the demands of his or her sport.
and duration that results in a 70% reduction The role of abnormalities in relative muscular
in energy demand can maintain Vo2max over a balance in the occurrence of athletic injuries has
period of 4 weeks (Neufer 1989). Maintaining the been debated in the literature. A review on the
intensity of exercise training during periods of topic by Grace (1985) noted that, although mus-
reduced frequency or duration of activity, how- cular imbalance as a causative factor in athletic
ever, is crucial to maintaining Vo2max (Neufer injury seemed logical, there was little definitive
1989). In the rehabilitation of an injured athlete, proof of this. Part of the problem arises from
attempts to modify exercise patterns, where the lack of any clear definition of ‘imbalance’ for
appropriate, to allow for continued limited train- a given muscular group. However, there are a
ing sessions with maintained cardiovascular number of reports since the date of that review
intensity may be helpful in the acute stage and to that have identified relative muscular imbalance
potentially reduce the systemic cardiovascular in studies of athletes postinjury, in screening of
effects of rest for a local tissue injury. uninjured athletes commonly at risk for par-
When viewing the changes that occur in ticular injuries, and as a significant risk factor
aerobic capacity with extended rest or reduced for injury in prospective studies (Fleck & Falkel
activity in conjunction with the effects of rest and 1986; Taimela et al. 1990; Kibler et al. 1991; Knapik
immobilization on joint function, and vascular, et al. 1991; McMaster et al. 1991; Chandler et al.
neural and muscular functioning, the need to 1992; Jonhagen et al. 1994; Baumhauer et al. 1995;
assess the athlete as a whole becomes more Orchard et al. 1997). Kibler et al. (1991) iden-
apparent. Local tissue injury combined with the tified relative ankle inflexibility and deficits in
wide-ranging effects frequently associated with peak plantar flexion torque in the affected legs
the required treatment can present significant of runners with plantar fasciitis. A prospective
challenges to obtaining optimal recovery and per- study on the risk of ankle injury in college athletes
formance following an athletic injury. Thoroughly found that injured and uninjured athletes dif-
understanding these issues and following the fered in relative dorsiflexion to plantar flexion and
approach to rehabilitation outlined previously eversion to inversion ratios as measured with
(Table 7.1) allows a clinician to incorporate a isokinetic testing (Baumhauer et al. 1995). Another
prospective study on college athletes by Knapik instances, lesser degrees of flexibility may, in fact,
et al. (1991) also found that muscular imbalance be beneficial in force production associated with
either across the knee or between sides in a given rapid muscular contraction (Gleim & McHugh
athlete or imbalance in hip motion between sides 1997). It is likely that a variety of physiological
was associated with a higher risk of injury. and anthropomorphic factors allow a given
Similarly, Orchard et al. (1997) identified low athlete to obtain an elite level of performance in
hamstring to quadriceps peak torque ratios as a a given task. Traits that are beneficial for some
risk factor for hamstring injury in a prospect- sport-specific tasks may actually be detrimental
ive study of professional Australian rules foot- to the performance of others. The function of an
ballers. Muscular imbalance about the shoulder athlete needs to be viewed in the context of that
has also been described in a variety of ‘overhead’ athlete’s particular sport and the entire motion
athletes, such as tennis players, swimmers and chain that allows for the performance of specific
water polo players (Fleck & Falkel 1986; McMaster skills. Injury and rehabilitation must encompass
et al. 1991; Chandler et al. 1992). this view, and deficits in flexibility (or the pres-
As with muscle imbalance, the role of flexi- ence of excessive laxity) need to be assessed in
bility in sports injuries remains debated. Issues the performance of a given task.
of flexibility are frequently cited as relating to Given the data available on muscular balance,
athletic injury (Keller et al. 1987; Taimela et al. injury and soft tissue physiology, restoration of
1990; Taylor et al. 1990; Kibler et al. 1991; Knapik balanced strength and flexibility along the kinetic
et al. 1991; Jonhagen et al. 1994; Worrell 1994; chain emerges as an important issue for rehabilita-
Baumhauer et al. 1995; Stocker et al. 1995; Bennell tion and injury prevention. The overload process
& Crossley 1996; Gleim & McHugh 1997). Sev- resulting in soft tissue injury and clinical symp-
eral studies have found a positive association toms is multifactorial. Aspects of technique and
between injury and greater overall flexibility or training clearly play a role, as do aspects of the
‘ligamentous laxity’, although other studies have functional kinetic chain affecting motion across a
failed to show an association between the two joint (Chandler & Kibler 1993). Addressing these
(Keller et al. 1987; Taimela et al. 1990; Baumhauer issues in a comprehensive fashion allows for
et al. 1995; Stocker et al. 1995; Bennell & Crossley appropriate interventions to optimize athletic
1996). Some authors note that relative inflexi- performance. For a detailed description of rehab-
bility of a particular muscular group may be a ilitation techniques utilizing this framework, the
predisposing factor to injury, particularly mus- reader is referred to Chapter 14 in this text that is
culotendinous strain (Keller et al. 1987; Knapik devoted to this very topic.
et al. 1991; Jonhagen et al. 1994; Worrell 1994).
Studies by Kibler et al. (1991) and Jonhagen et al.
Conclusions
(1994) have shown relative decreases in passive
range of motion measures compared with con- Injury and immobilization have wide-ranging
trols in athletes with either plantar fasciitis or physiological effects on the athlete. A comprehen-
prior hamstring strains, respectively. In a review sive understanding of these issues is crucial in the
of the role of flexibility in sports injury, Gleim management of an injured athlete. The athlete
and McHugh (1997) noted that, as with muscular should be assessed not only for the acutely injured
imbalance, there is a lack of any standard defini- tissue but also for underlying biomechanical
tion for ‘flexibility’ and that there are a variety of problems along the kinetic chain and subclinical
ways in which flexibility can be assessed (such as adaptations. Athletic injuries need to be seen
static vs dynamic and stretch tolerance vs muscle in the context of the entire athlete, including an
stiffness). They also noted that specific flexibil- accurate diagnosis of acute tissue injuries and
ity patterns are associated with specific sports an understanding of the individual’s clinical
or even positions within a given sport. In some symptoms. The athlete should be evaluated for
other potentially overloaded structures, func- Convertino, V.A. (1997) Cardiovascular consequences
tional deficits such as strength imbalance, and of bed rest: effect on maximal oxygen uptake. Medicine
for alterations in motion or technique that arise and Science in Sports and Exercise 29 (2), 191–196.
Cruz-Martinez, A., Ramirez, A. & Arpa, J. (2000) Quad-
from or contribute to injury. Using this type of riceps atrophy after knee traumatisms and immobil-
approach with a detailed knowledge of the issues ization: electrophysiological assessment. European
discussed in other chapters of this text, clinicians Neurology 43, 110–114.
can formulate a comprehensive rehabilitation Curwin, S.L. (1996) Tendon injuries: pathophysiology
strategy for the injured athlete that can restore and treatment. In: Athletic Injuries and Rehabilitation
(Zachazewski, J.E., Magee, D.J. & Quillen, W.S., eds).
function and provide long-term benefits in health W.B. Saunders, Philadelphia: 27–53.
and performance. DeLee, J.C. & Farney, W.C. (1992) Incidence of injury in
Texas high school football. American Journal of Sports
Medicine 20 (5), 575–580.
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Chapter 8
Psychological Factors in Sports Injury

Rehabilitation
BRITTON W. BREWER AND ALLEN E. CORNELIUS
Following the recommendations of Brewer

Introduction
(1994), researchers have: (i) advanced theory (e.g.
Rehabilitation of sports injuries involves more Evans & Hardy 1995; Johnston & Carroll 1998a;
than repairing the physical injury and regaining Wiese-Bjornstal et al. 1998; Brewer et al. 2002); (ii)
previous levels of physical performance. Optim- included both psychological and physical vari-
izing injury rehabilitation also includes under- ables in their analyses (e.g. LaMott 1994; Durso-
standing the psychological impact of the injury Cupal 1996; Ross & Berger 1996; Theodorakis
on the athlete and how psychological factors et al. 1996; Theodorakis et al. 1997a; Theodorakis
may interact with the rehabilitation process. The et al. 1997b; Niedfeldt 1998; Morrey et al. 1999;
purpose of this chapter is to review the research Brewer et al. 2000c); (iii) assessed the prevalence
examining psychological factors related to sports of clinical levels of psychological distress (Leddy
injury rehabilitation. et al. 1994; Brewer & Petrie 1995; Brewer et al.
Major advances have been made in recent 1995a, 1995b; Perna et al. 1998); (iv) implemented
years in our understanding of the range of psy- prospective, longitudinal research designs (e.g.
chological factors associated with sports injury Smith et al. 1993; LaMott 1994; Leddy et al. 1994;
rehabilitation. In the early 1990s, Williams and Ross & Berger 1996; Morrey 1997; Petrie et al.
Roepke et al. (1993) and Brewer (1994) made 1997b; Udry 1997a; Perna et al. 1998; Roh et al.
specific suggestions for improving the quality of 1998; Morrey et al. 1999; Brewer et al. 2000c);
psychological research on sports injury rehabilita- (v) conducted qualitative investigations (e.g.
tion. Fortunately, many of these recommenda- Shelley 1994; Gould et al. 1997a, 1997b; Udry et al.
tions have been heeded. Specifically, responding 1997a, 1997b; Johnston & Carroll 1998a, 1998b;
to the recommendations made by Williams and Bianco et al. 1999b); (vi) used control groups
Roepke, researchers have: (i) identified cognitive of athletes without injuries (e.g. LaMott 1994;
and emotional responses to injury that are char- Brewer & Petrie 1995; Petrie et al. 1997a; Perna
acteristic of athlete populations (e.g. Leddy et al. et al. 1999); and (vii) examined groups of athletes
1994; Quinn & Fallon 1999); (ii) investigated the that are homogeneous with respect to injury type,
effects of psychological interventions on sports severity and prognosis (e.g. LaMott 1994; Ross
injury rehabilitation (e.g. Ross & Berger 1996; & Berger 1996; Theodorakis et al. 1996, 1997a,
Theodorakis et al. 1996, 1997a, 1997b; Cupal & 1997b; Udry 1997a; Morrey et al. 1999; Brewer
Brewer 2001); and (iii) initiated the education of et al. 2000a, 2000b, 2000c; Cupal & Brewer 2001);
sports medicine practitioners on psychological and (viii) used experimental research designs
aspects of injury rehabilitation (e.g. Ford & Gordon (e.g. Ross & Berger 1996; Theodorakis et al. 1996,
1997, 1998; Gordon et al. 1998). 1997a, 1997b; Cupal & Brewer 2001).
160
psychological factors 161
To provide some structure for the voluminous come. For example, if the cognitive response to
amount of research that has been conducted on an injury is one of doubt and thoughts of nega-
psychological factors in sports injury rehabilitative outcomes, a negative emotional response is
tion, two models are presented that describe the likely to result. If the appraisal of the injury is
hypothesized relationships among psycholo- more positive, with thoughts of full recovery and
gical and other key variables in the sports injury confidence in rehabilitation, the model predicts
rehabilitation process. The first model, the integ- that a positive emotional reaction will be more
rated model developed by Wiese-Bjornstal et al. likely.
(1998), describes many of the psychological fac- There has been considerable empirical support
tors related to athletes’ reactions to injuries. The for cognitive appraisal models in general, and
second model is a biopsychosocial model devel- the integrated model in particular. Sports injury
oped by Brewer et al. (2002) that places sports has been identified as a significant source of
injury rehabilitation in a broad contextual frame- stress in several studies (Brewer & Petrie 1995;
work. Following descriptions of these models, Gould et al. 1997a; Bianco et al. 1999; Ford &
research examining the relationships predicted Gordon 1999; Heniff et al. 1999), and numerous
by these models is reviewed. personal and situational factors have been asso-
ciated with psychological responses to sports
injury (Brewer 1994, 1998, 1999a). Although some
Models of psychological response
of the more complex mediational relationships
to sports injury and sports injury
predicted by the integrated model have not yet
rehabilitation
found empirical support (Daly et al. 1995; Brewer
et al. 2000c), there is considerable research sup-
cognitive appraisal models
porting the usefulness of this model for under-
Cognitive appraisal models view an injury as a standing the diverse array of reactions to sports
stressor or a stimulus, and the response of the injuries. The integrated model (Wiese-Bjornstal
individual is dependent upon a variety of factors et al. 1998) also has the benefit of providing the-
that influence the interpretation of this stimulus. oretical guidance for interventions to improve
Several cognitive appraisal models have been rehabilitation outcomes, as many of the personal
developed to explain athletes’ reactions to sports and situational factors are subject to modification
injuries (e.g. Gordon 1986; Weiss & Troxel 1986; (e.g. improving social support systems).
Grove 1993; Wiese-Bjornstal et al. 1998), the most
comprehensive of which is the integrated model
biopsychosocial model
proposed by Wiese-Bjornstal et al. (1998) (Fig. 8.1).
This model proposes that many preinjury and The integrated model describes the complex
postinjury factors are related to how an indivi- relationships of psychological, situational and
dual reacts to a sports injury. Preinjury factors are cognitive variables to emotional and behavioural
personality, history of stressors, coping resources responses to sports injury, but it does not take
and interventions. Postinjury factors include into account the breadth of factors that can be
personal factors (e.g. type and severity of the related to sports injury rehabilitation processes
injury, general health status, demographic vari- and outcomes. Because of the multiplicity of
ables) and situational factors (e.g. sport played, factors that potentially interact during sports
social support system, accessibility to rehabilita- injury rehabilitation, a model that is compre-
tion). These factors combine to determine the hensive, yet conceptually grounded, is required.
cognitive appraisal of the injury, which in turn Borrowing from other health outcome research
affects the emotional and behavioural responses (Cohen & Rodriguez 1995; Matthews et al. 1997)
to injury, and, ultimately, the rehabilitation out- and existing models of sports injury rehabilitation
Preinjury Factors
Stress response
Personality History of Coping Interventions

Sports injury
stressors resources
Response to sports injury and rehabilitation process

Personal factors Situational factors
* Injury * Sport
-History -Type
-Severity -Level of competition
-Type -Time in season
-Perceived cause Cognitive appraisal -Playing status
-Recovery status -Practice vs. game
* Goal adjustment
* Individual differences -Scholarship status
-Psychological
* Rate of perceived recovery * Social
>personality * Self-perceptions -Team mate influences
>self-perceptions * Belief and attributions -Coach influences
>self-motivation * Sense of loss or relief -Family dynamics
>motivational orientation * Cognitive coping -Sports medicine team influences
>pain tolerance -Social support provision
>athletic identity -Sport ethic/philosophy
>coping skills * Environmental
>psychological skills - Rehabilitation environment
>history of stressors - Accessibility to rehabilitation
>mood states
-Demographic
>gender
>age
>ethnicity Recovery outcomes
>socioeconomic status
>prior sport experience
* Psychosocial
-Physical
>use of ergogenic aids
* Physical
>physical health status
>disordered eating
Behavioural response Emotional response

* Adherence to rehabilitation * Fear of unknown
* Use of PST strategies * Tension, anger, depression
* Use/disuse of social support * Frustration, boredom
* Risk-taking behaviours * Positive attitude/outlook
* Effort and intensity * Grief
* Malingering * Emotional coping
* Behavioural coping
Fig. 8.1 Integrated model of psychological response to the sports injury and rehabilitation process.
(From Wiese-Bjornstal et al. 1998, with permission. © 1998 by the Association for the Advancement of
Applied Sport Psychology.)
Injury characteristics Sociodemographic factors

type age
course gender
severity race/ethnicity
location socioeconomic status
history
Biological factors Psychological factors Social/contextual factors

endocrine sleep personality social network
metabolism circulation cognition life stress
neurochemistry respiration affect situational characteristics
tissue repair immune behaviour rehabilitation environment
nutrition functioning
Intermediate biopsychological
outcomes
range of motion
strength
joint laxity
pain
endurance
rate of recovery
Sports injury rehabilitation

outcomes
functional performance
quality of life
treatment satisfaction
readiness to return to sport
Fig. 8.2 A biopsychosocial model of sports injury rehabilitation. (From Brewer et al. 2002)
(Leadbetter 1994; Flint 1998; Wiese-Bjornstal et al. location and history of injury) and sociodemo-
1998), a model incorporating biological, social, graphic factors (e.g. age, gender, race/ethnicity,
medical and psychological factors has been socioeconomic status) are depicted as influen-
developed (Brewer et al. 2002). This biopsycho- cing biological factors (e.g. nutrition, sleep), psy-
social model, as depicted in Fig. 8.2, has seven chological factors (e.g. personality, cognition) and
interacting components: injury characteristics, social/contextual factors (e.g. social networks,
sociodemographic factors, biological factors, life stress). Psychological factors are the focal
psychological factors, social/contextual factors, point of this model, having reciprocal relation-
intermediate biopsychological outcomes and ships with both biological and social/contextual
sports injury rehabilitation outcomes. factors. Biological, psychological and social/con-
The biopsychosocial model proposes that the textual factors are thought to influence inter-
sports injury rehabilitation process begins with mediate biopsychological outcomes (e.g. strength,
the occurrence of an injury. The specific charac- rate of recovery), with psychological factors also
teristics of the injury (e.g. type, course, severity, being reciprocally affected by these outcomes.
The final component of the model, sports injury result of an event or process associated with
rehabilitation outcomes, consists of functional sports participation and disrupts subsequent
performance, quality of life, treatment satisfac- sports participation. The duration of such dis-
tion and readiness to return to sport. This phase ruption of involvement in sports may vary ex-
of the model is reciprocally related to both the tensively depending on the nature, course and
intermediate biopsychological outcomes and the severity of the injury. Emotional responses
psychological factors. refer to affective (i.e. feeling) states that are
The biopsychosocial model incorporates the experienced subsequent to injury onset, whereas
various factors that are potentially related to behavioural responses refer to overt actions that
sports injury rehabilitation outcomes, and offers are manifested following the occurrence of
a structure for examining the relationships of injury.
these factors in a contextually complete model.
Given that the model incorporates findings and
Emotional responses to sports injury
concepts from already established models of
injury rehabilitation (Leadbetter 1994; Flint 1998; Emotional responses to sports injury have been a
Wiese-Bjornstal et al. 1998), there is already sup- widely researched topic within the sports psy-
port for many of the hypothesized relationships. chology literature. A popular approach has been
However, the broad scope of the model will the application of stage theories that propose that
enable researchers to investigate a wider array of athletes experience an injury as a type of loss.
potential influences on the sports rehabilitation The injury is thought to be perceived by the
process. athlete as a loss of an aspect of the self, and there-
Given the centrality of the psychological fac- fore considered to elicit a reaction similar to that
tors in the integrated model (Wiese-Bjornstal exhibited by an individual who has experienced
et al. 1998) and the biopsychosocial model (Brewer a serious psychological loss (Peretz 1970; Rotella
et al. 2002), and the focus of this chapter, the & Heyman 1986). Stage models of grief and loss
following sections review the research that have proposed that individuals experience a
examines the relationships between the psycho- sequence of emotional responses to the loss,
logical factors depicted in these models and the leading to eventual adaptation. In perhaps the
other constructs in the models. Specifically, the best known description of these stages, Kubler-
next section reviews the research findings related Ross 1969) proposed that in response to a major
to psychological reactions to injury, and the loss, individuals commonly progress through
subsequent section examines the literature con- five stages: denial, anger, bargaining, depression
cerning psychological factors associated with and acceptance. Researchers have found that
sports injury rehabilitation outcomes. athletes experience many of these same emotions
following an injury (Rotella 1985; Astle 1986;
Lynch 1988; Silva & Hardy 1991).
Psychological responses to
Although the five-stage model developed by
sports injury
Kubler-Ross (1969) has been widely discussed by
The subject of psychological disturbance arising sport psychologists, research investigating ath-
from sports injury has been studied extensively letes’ reactions to injury has not fully supported
since Little (1969) first identified neurotic symp- this model. Kubler-Ross’s model was derived
toms in injured athletes. The following sections from her work with terminally ill patients, and
examine research concerning emotional and the experience of being terminally ill may not
behavioural responses to sports injury that has be similar enough to having a sports injury to
accrued since Little’s seminal work. For the be generalizable (Smith et al. 1990b). There is,
purposes of this discussion, sports injuries are however, support for emotional responses to
defined as physical damage that occurs as the injury being somewhat similar to grief reactions
(Shelley 1994; Macchi & Crossman 1996). In the sequential progression of emotions and behav-
initial time period following an injury, negative iours. Although most of the emotions identified
emotions such as depression, frustration, con- in stage models (Rotella 1985; Astle 1986; Lynch
fusion, anger and fear have been documented in 1988) are commonly experienced by the majority
several qualitative studies (Gordon & Lindgren of athletes with injuriesaconsistent with the
1990; Shelley & Carroll 1996; Shelley & Sherman findings on psychological reactions to undesir-
1996; Udry et al. 1997a; Johnston & Carroll 1998a; able events in general (for a review, see Silver &
Sparkes 1998; Bianco et al. 1999b). During the Wortman 1980)aempirical support for a stage-
middle phase of rehabilitation, depression and like progression of these emotional states is weak
frustration are commonly reported emotions, (Brewer 1994). The emotional reactions of athletes
with the source of these emotions shifting from with injuries are more varied and less sequential
concerns about the injury to rehabilitation-related than those postulated by stage models. The only
issues. As rehabilitation of the injury nears com- consistent change in emotions over time that
pletion, depression and frustration remain preva- has been documented is an overall pattern of
lent and a fear of reinjury emerges (Johnston & decreasing negative emotions and increasing
Carroll 1998a; Bianco et al. 1999b). positive emotions as rehabilitation progresses
Quantitative studies have also demonstrated (Grove et al. 1990; McDonald & Hardy 1990;
that athletes with injuries experience negative Smith et al. 1990a; Uemukai 1993; LaMott 1994;
emotions to a greater extent than athletes with- Leddy et al. 1994; Quackenbush & Crossman
out injuries (Chan & Grossman 1988; Pearson & 1994; Crossman et al. 1995; Macchi & Crossman
Jones 1992; Smith et al. 1993; Leddy et al. 1994; 1996; Dawes & Roach 1997; Laurence 1997;
Brewer & Petrie 1995; Johnson 1997, 1998; Petrie Morrey 1997; Miller 1998; Quinn & Fallon 1999).
et al. 1997a, 1997b; Miller 1998; Perna et al. 1998; A deviation from this pattern, which has been
Roh et al. 1998; Newcomer et al. 1999) and that documented in two studies (LaMott 1994; Morrey
emotional responses to injury tend to become et al. 1999), is a slight increase in negative emo-
more adaptive as time progresses (McDonald & tions and a slight decrease in positive emotions
Hardy 1990; Smith et al. 1990a; Uemukai 1993). as athletes near the end of rehabilitation follow-
There is also evidence that the emotional disturb- ing reconstructive knee surgery, possibly reflect-
ance of athletes is greater following injury than ing athletes’ apprehension about returning to
it is prior to the injury (Dubbels et al. 1992; Smith sports activity and fear of reinjury (Quinn 1996;
et al. 1993; Leddy et al. 1994; Miller 1998). Johnston & Carroll 1998a; Bianco et al. 1999b).
These emotional disturbances are, for the most Stage models ignore several important factors
part, not of a sufficient magnitude or duration related to how athletes respond to an injury, such
to be assigned a clinical diagnosis (Heil 1993). as their idiosyncratic perceptions of the injury,
Epidemiological studies, however, have shown and situational circumstances such as the sever-
that a substantial minority of injured athletes ity of the injury and sources of social support
(5–24%) experience clinical levels of emotional (Brewer 1994; Wiese-Bjornstal et al. 1998).
disturbance as determined by scores on psycho- The general lack of empirical support for stage
metric instruments and, in some cases, clinical models does not mean that they are completely
interviews (Leddy et al. 1994; Brewer & Petrie without merit. Recently proposed versions of
1995; Brewer et al. 1995a, 1995b; Perna et al. 1998). stage models have evolved from static and rigid
There are risks of suicide with athletes who stages of previous models to more flexible and
experience severe levels of postinjury emotional dynamic descriptions of psychological responses
disturbance, particularly depression (Smith & to sports injury, thereby allowing for more indi-
Milliner 1994). vidual variation in how the stages are experienced
Stage models suggest that psychological (Evans & Hardy 1995, 1999). Such modification
reactions to sports injuries are manifested in a muddles the simplicity of stage models, but
Table 8.1 Situational factors associated with postinjury emotional disturbance.
Variable Direction Reference
Current injury status + Alzate et al. 1998; Brewer et al. 1995a; Quinn 1996
Injury severity + Alzate et al. 1998; Pargman & Lunt 1989; Perna 1992;
Smith et al. 1990a, 1993; Uemukai, 1993
Impairment of daily activities + Crossman & Jamieson 1985
Life stress + Brewer 1993; Petrie et al. 1997b; Quinn 1996
Recovery progress + Quinn 1996
Impairment of sport activities − Brewer et al. 1995a
Level of sport involvement +/− Crossman et al. 1995; Meyers et al. 1991
Medical prognosis − Gordin et al. 1988
Recovery progress − McDonald & Hardy 1990; Quinn 1996; Smith et al. 1988
Social support for rehabilitation − Brewer et al. 1995a
Social support satisfaction − Green & Weinberg 1998
Direction refers to the positive (+) and negative (−) correlations with postinjury emotional disturbance.
reflects more accurately the dynamic nature of et al. 1997), investment in playing professional
the emotional experience of athletes who have sports (Kleiber & Brock 1992), level of sports
been injured. Stage models have provided im- involvement (Meyers et al. 1991), pessimistic
petus for the development of cognitive appraisal explanatory style (Grove et al. 1990) and previous
models of responses to injury, such as the integ- injury experience (Bianco et al. 1999b). Athletes
rated model (Wiese-Bjornstal et al. 1998), which with injuries have demonstrated negative rela-
identifies factors that mediate and moderate tionships between emotional distress and age
emotional responses to sports injury. (Smith et al. 1990a; Brewer et al. 1995a) and hardi-
ness (Grove et al. 1990; Miller 1998). Thus, the
individuals most likely to encounter difficulty
mediating and moderating factors
adjusting emotionally to injury are those who are
The integrated model (Wiese-Bjornstal et al. 1998) young, least hardy, most strongly identified with
posits cognitive, personal and situational factors the athlete role, most dispositionally anxious,
as influences on emotional and behavioural re- most invested in having a career as a professional
sponses to sports injury, with cognitive appraisals athlete, most experienced in the rigors of sports
mediating the relationships between personal injury rehabilitation, and most pessimistic. The
and situational factors and emotional and behav- relationship of emotional distress to age is poten-
ioural responses. However, most of the research tially more complex than a simple linear relation-
in this area has not addressed this mediational ship, as Meyers et al. (1991) obtained a curvilinear
effect, but has focused instead on direct associ- relationship between age and emotional dis-
ations between various personal and situational turbance for participants recovering from knee
factors and emotional and behavioural responses surgery. Participants of intermediate age (20–39
to injury. Therefore, only indirect evidence of the years) reported greater levels of emotional dis-
hypothesized mediational role of cognitive ap- turbance than younger (10–19 years) and older
praisals has been obtained. (40–49 years) participants. Injury-related charac-
Personal factors that have been identified as teristics and aspects of the social and physical
being positively related to postinjury emotional environments that can change over time are
disturbance include self-identification with the referred to as situational factors. As shown in
athlete role (Brewer 1993; Shelley & Carroll 1996; Table 8.1, numerous situational factors have been
Sparkes 1998), competitive trait anxiety (Petrie correlated with emotional distress in athletes
with injury. In general, research has indicated that discussed in the previous section. The two most
athletes are likely to experience greater postin- relevant behaviours, and the most researched,
jury emotional disturbance when they perceive are coping behaviours and adherence to sports
their injuries as serious, view themselves as hav- injury rehabilitation.
ing made little rehabilitative progress, and con-
sider themselves as weakly supported in their
coping behaviours
rehabilitative pursuits.
According to the integrated model (Wiese- In an effort to deal effectively with injuries and
Bjornstal et al. 1998), it is cognitive appraisals the related issues that may arise during rehabil-
made concerning the injury that have the most itation, athletes may engage in certain behaviours
direct effect on emotional and behavioural re- to help them cope with the situation. Specific
sponses. Numerous types of cognitive appraisals behavioural strategies that have been identified
have been correlated with emotional distress in athletes with injuries include an aggressive
in research studies. Greater emotional distress rehabilitation approach, avoiding others, build-
following injury has been associated with the ing strength, distracting oneself (e.g. keeping busy,
tendencies to interpret pain in a catastrophic seeking a change of scenery), ‘driving through’
manner (Tripp 2000) and to attribute the cause of (e.g. doing things normally, learning about their
sports injury to factors residing within oneself injuries, resting when tired, working hard to
(Tedder & Biddle 1998) and pertaining to all achieve rehabilitation goals), seeking out and
areas of one’s life (Brewer 1991). Lower levels of using social support networks, trying alternative
postinjury emotional distress have been found treatments, and working or training at their own
for individuals who: (i) think that they will be pace (Gould et al. 1997b; Bianco et al. 1999a).
able to cope with their injuries (Daly et al. 1995); Other studies have examined the use of specific
(ii) can readily imagine themselves functioning coping strategies, and have found that the most
favourably following injury (Fisk & King 1998); strongly endorsed coping behaviours assessed
(iii) have high general and physical self-esteem by the COPE inventory (Carver et al. 1989; Scheier
(Brewer 1993; Quinn 1996); and (iv) are confident et al. 1994) were active coping, which involves
in themselves and their ability to adhere to the initiating behaviours to deal directly with a stres-
rehabilitation protocol, recover fully from injury sor or its effects, and instrumental social support,
and succeed in sport (Quinn 1996). Also, in which pertains to seeking help or information
contrast to the findings of Tedder and Biddle, (Grove & Bahnsen 1997; Udry 1997a; Quinn &
athletes who attribute the cause of their injuries Fallon 1999).
to factors residing within themselves and likely
to occur have reported lower levels of postinjury
adherence to sports injury
emotional disturbance (Brewer 1999b). Thus,
rehabilitation
although it is unclear whether taking respon-
sibility for one’s injury is adaptive in terms of A behavioural response to sports injury that is of
emotional adjustment, there is little doubt that central focus to the rehabilitation of the injury is
cognitions indicating confidence in oneself, adherence to the recommended rehabilitation
one’s body and one’s recovery are associated protocol, which can involve a number of differ-
with more favourable emotional states following ent behaviours, including: (i) performing clinic-
sports injury. based activities, such as doing exercises designed
to increase strength, flexibility and endurance;
(ii) modifying physical activity, such as resting
Behavioural responses to sports injury
and limiting activity; (iii) taking medications;
A sports injury can elicit a number of behavioural and (iv) completing home-based activities, such
responses in addition to the emotional responses as cryotherapy and home rehabilitation exercises
(Brewer 1998, 1999a). This wide range of behav- Brewer et al. 2000b), which refers to the extent to
iours requires a correspondingly wide range of which a person believes that health outcomes are
assessment techniques for measuring adherence. under their own control; (ii) pain tolerance (Fisher
The most frequently used methods of assessing et al. 1988; Byerly et al. 1994; Fields et al. 1995); (iii)
adherence are documenting patient attendance self-motivation (Noyes et al. 1983; Fisher et al.
at clinic-based rehabilitation sessions, recording 1988; Duda et al. 1989; Brewer et al. 1994a; Fields
practitioner ratings of adherence during rehabilit- et al. 1995; Culpepper et al. 1996; Brewer et al.
ation sessions, and obtaining patient self-reports 2000c); (iv) task involvement (Duda et al. 1989),
of home exercise completion (Brewer 1999a). Com- which is the degree to which a person is motiv-
plicating this diversity of adherence measures is ated to improve against their own personal
a lack of consistent operationalization of adher- standards; and (v) tough mindedness (Wittig
ence behaviour, with some research reporting & Schurr 1994). Personal factors that have been
a percentage of adherent versus non-adherent shown to be negatively associated with adher-
individuals, and other research comparing actual ence to sports injury rehabilitation are: (i) a
adherence behaviour to that recommended by chance health locus of control (Brewer et al.
the practitioner. 2000b), which refers to the extent to which a per-
Recognizing this diversity of adherence meas- son believes that health outcomes are influenced
ures and conflicting operationalization of the by chance or luck; (ii) ego involvement (Duda
adherence construct, estimates of adherence to et al. 1989), which is the degree to which a per-
sports injury rehabilitation have ranged from son is motivated by comparisons with other
40 to 91% (Brewer 1998, 1999a). Adherence rates individuals; and (iii) trait anxiety (Eichenhofer
tend to be higher for continuous measures of et al. 1986). Thus, in terms of dispositional char-
adherence, such as attendance at rehabilitation acteristics, the athletes most likely to adhere to
sessions (e.g. Almekinders & Almekinders 1994; their rehabilitation programmes are those who
Daly et al. 1995; Laubach et al. 1996) or amount are self-motivated, strong-willed and tolerant of
of time spent on home rehabilitation activities discomfort.
(Penpraze & Mutrie 1999), than for more discrete As shown in Table 8.2, a diverse array of situ-
measures of adherence that categorize individuals ational factors has been found to correlate with
based on their level of adherence (e.g. Taylor & adherence to sports injury rehabilitation pro-
May 1996). Consistent with a cognitive appraisal grammes. In general, higher levels of adherence
approach and the integrated model (Wiese- have been associated with: (i) a supportive
Bjornstal et al. 1998), researchers have postulated clinical environment; and (ii) a rehabilitation
that adherence rates are related to personal and programme that is convenient, valued and per-
situational factors, as well as cognitive and emo- ceived as efficacious.
tional responses. However, as with emotional The integrated model (Wiese-Bjornstal et al.
responses to sports injury, there is little direct 1998) predicts that, as with personal and situ-
support for the hypothesized mediational role ational factors, cognitive variables should be
of cognitive appraisals in the relations between related to behaviours such as adherence to rehab-
personal and situational factors and adherence to ilitation. Research has shown that individuals
sports injury rehabilitation. But researchers have who have high adherence rates also report a high
identified many personal, situational and cogni- ability to cope with their injuries (Daly et al. 1995),
tive factors that are associated with sports injury have high rehabilitation self-efficacy (Taylor &
rehabilitation adherence. May 1996), perceive little threat to their self-esteem
Personal factors that have been identified as (Lampton et al. 1993), attribute their recovery to
having a positive relationship with sports injury stable and personally controllable factors (Laubach
rehabilitation adherence include: (i) an internal et al. 1996), set rehabilitation goals, use imagery
health locus of control (Murphy et al. 1999; and use positive self-talk (Scherzer et al. 1999).
Table 8.2 Situational factors associated with adherence to sports injury rehabilitation.
Academic class status + Culpepper et al. 1996; Shank 1988

Academic performance level + Shank 1988
Belief in the efficacy of the treatment + Duda et al. 1989; Noyes et al. 1983; Taylor & May 1996
Comfort of the clinical environment + Brewer et al. 1994a; Fields et al. 1995; Fisher et al. 1988
Convenience of rehabilitation scheduling + Fields et al. 1995; Fisher et al. 1988
Degree of career goal definition + Shank 1988
Importance or value of rehabilitation + Taylor & May 1996
Injury duration + Culpepper et al. 1996
Perceived academic load + Shank 1988
Perceived sports participation time + Shank 1988
Perceived time availability for rehabilitation + Shank 1988
Perceived exertion during rehabilitation + Brewer et al. 1994a; Fisher et al. 1988
Perceived susceptibility to further + Taylor & May 1996
complications without rehabilitation
Postcollegiate sports participation plans + Shank 1988
Rehabilitation practitioner expectancy + Taylor & May 1995
Social support for rehabilitation + Byerly et al. 1994; Duda et al. 1989; Finnie 1999;
Fisher et al. 1988
Direction refers to the positive (+) correlations with postinjury emotional disturbance.
Thus, athletes who are confident in their ability have examined such relationships. Mood disturb-
to meet the demands of rehabilitation, accept ance has been negatively related to adherence
responsibility for their rehabilitation, and alloc- in three (Daly et al. 1995; Brickner 1997; Alzate
ate mental effort to their rehabilitation tend to et al. 1998), but a fourth study found no associ-
exhibit the highest levels of adherence. ation between adherence levels and psycholo-
One of the few cognitive processes that has gical disturbance (Brewer et al. 2000c). The only
received any experimental attention with regard behavioural response that has been investigated
to sports injury rehabilitation adherence is goal in association with sports injury rehabilitation
setting. Penpraze and Mutrie (1999) assigned adherence has been the use of instrumental
athletes with injuries to either a group that was coping behaviours, which involve asking for
assigned specific rehabilitation goals or a group additional information about the injury or the
that received non-specific rehabilitation goals. rehabilitation programme (Udry 1997a). Instru-
Athletes in the specific goals group had a greater mental coping behaviours were positively related
understanding of, and adherence to, their rehab- to adherence levels for individuals who were
ilitation protocols than athletes in the non- undergoing rehabilitation following reconstruct-
specific goal group. These experimental findings ive knee surgery designed to facilitate a return to
extended earlier qualitative findings that task- sports participation.
orientated goal setting was related to a greater
perception of rehabilitation adherence in athletes
Psychological factors and sports
with injuries (Gilbourne & Taylor 1995, 1998;
injury rehabilitation outcomes
Gilbourne et al. 1996).
The integrated model also predicts that emo- In addition to psychological responses to sports
tional responses and other behavioural responses injury reviewed in the preceding section, the
will be associated with adherence to sports psychological correlates of sports injury rehabil-
injury rehabilitation, although only a few studies itation outcomes are also of vital interest. Both
the integrated model (Wiese-Bjornstal et al. 1998) social support, which refers to the quantity, qual-
and the biopsychosocial model (Brewer et al. ity and type of interactions that athletes have
2002) specify relationships between psycholo- with other people (Udry 1996). Social support
gical variables and sports injury rehabilitation is considered to be multidimensional, with the
outcomes. These models predict that the same structure proposed by Richman et al. (1993) the
clusters of personal, situational, cognitive, emo- most widely used in sports injury rehabilitation
tional and behavioural variables associated with research (Ford & Gordon 1993; Izzo 1994; LaMott
psychological responses to sports injury will also 1994; Bianco & Orlick 1996; Quinn 1996; Ford
be related to sports injury rehabilitation out- 1998; Johnston & Carroll 1998b). The Richman
comes. Research that has investigated relation- structure categorizes social support as one of
ships between psychological factors and sports eight types: listening support, emotional sup-
injury rehabilitation outcomes is discussed in the port, emotional challenge, task appreciation, task
next sections. For the purposes of this discussion, challenge, reality confirmation, material assist-
sports injury rehabilitation outcomes refer not ance and personal assistance. These different
only to the variables listed in the category of the types of social support may be provided by dif-
same name in the biopsychosocial model shown ferent members of an athlete’s social network,
in Fig. 8.2, but also to the variables listed in the including coaches, friends, relatives, team mates,
biopsychosocial model (Brewer et al. 2002) as sports administrators and medical personnel
‘intermediate biopsychological outcomes’, as these (Lewis & LaMott 1992; Izzo 1994; Bianco & Orlick
variables (e.g. endurance, joint laxity, pain, range 1996; Macchi & Crossman 1996; Peterson 1997;
of motion, recovery rate, strength) are often used Udry 1997b; Udry et al. 1997b; Ford 1998; Johnston
as indices of rehabilitation outcome in research & Carroll 1998b; Bianco et al. 1999a; Udry &
investigations. Singleton 1999). The needs for particular types
of social support and the ability of an athlete’s
social support network to provide certain types
personal factors
of support may vary during the rehabilitation
Personal factors related to sports injury rehabilita- process (Ford 1998; LaMott 1994; Quinn 1996;
tion outcomes have been a topic of interest since Udry 1997a; Johnston & Carroll 1998b).
Wise et al. (1979) discovered that two personality Given the complexity of social support net-
variables (i.e. hysteria and hypochondriasis) were works and the changing social support needs of
inversely related to recovery following knee sur- injured athletes over the course of rehabilitation,
gery. Subsequent studies have shown that being it is not surprising that research in this area has
optimistic (LaMott 1994), male (Johnson 1996, produced conflicting results. For example, social
1997) and strongly identified with the athlete support has been positively related (Tuffey 1991),
role (Brewer et al. 2000c) have all been positively not related (Brewer et al. 2000c) and negatively
related to rehabilitation outcomes following sports related (Quinn & Fallon 2000) to rehabilitation
injuries. Research has not yet uncovered the outcome. These inconsistencies are probably
mechanisms by which these personal factors may due to the way in which social support has been
influence outcome, or what other of the myriad differentially operationalized across different
personal factors may be related to sports injury studies. The importance of considering different
rehabilitation outcomes. aspects of social support and their potential
different relationships to rehabilitation outcome
is highlighted in a study of skiers (Gould et al.
situational factors
1997a). Skiers who experienced successful injury
The situational factor that has received the most rehabilitation were less likely to perceive a lack
amount of research attention with respect to of attention/empathy from others and less likely
sports injury rehabilitation outcomes has been to encounter negative social relationship, yet
Table 8.3 Cognitive factors associated with sports injury rehabilitation outcomes.
Attentional focus on healing + Loundagin & Fisher 1993

Attribution of recovery to stable and + Brewer et al. 2000a; Laubach et al. 1996
controllable factors
Cognitive appraisal of injury coping ability + Niedfeldt 1998
Cognitive appraisal of the injury situation + Johnson 1996, 1997
Denial +/– Quinn & Fallon 2000; Grove & Bahnsen 1997
Emotional focus/venting – Grove & Bahnsen 1997
Emotion-focused coping + Quinn 1996
Expected recovery rate + Laurence 1997
Management of thoughts and emotions + Gould et al. 1997b
Mental disengagement - Grove & Bahnsen 1997
Number of rehabilitation goals + Johnson 1996, 1997
Pain catastrophizing + Tripp 2000
Positive attitude toward rehabilitation + Johnson 1996, 1997
Positive reinterpretation – Grove & Bahnsen 1997
Recovery confidence + Niedfeldt 1998; Quinn & Fallon 2000
Rehabilitation self-efficacy + Shaffer 1992
Self-confidence + Johnson 1996, 1997
Use of goal setting + Gould et al. 1997b; Ievleva & Orlick 1991;
Loundagin & Fisher 1993
Use of healing/recovery imagery + Ievleva & Orlick 1991; Loundagin & Fisher 1993
Use of imagery/visualization + Gould et al. 1997b
Direction refers to the positive (+) and negative (–) correlations with sports injury rehabilitation outcomes.
were more likely to indicate feeling socially iso- 2000), are equivocal. These inconsistencies, along
lated than skiers who experienced unsuccessful with the retrospective and correlational nature
injury rehabilitation. Thus, when examining the of the majority of studies on cognitive factors
relationships between rehabilitation outcome associated with sports injury rehabilitation out-
and social support, it is imperative that that comes, indicate that more research (especially
the specific type of social support is considered. prospective and experimental research) is needed
Further research is needed to better understand in this area to better understand the role of cogni-
the roles of the different types of social support in tion in influencing rehabilitation outcomes.
the injury rehabilitation process.
emotional factors
cognitive factors
Only a few studies have examined relationships
As indicated in Table 8.3, research has identified between emotional variables and sport rehabili-
many cognitive factors that are associated with tation outcomes. Positive relationships to have
sports injury rehabilitation outcomes. Overall, been found between rehabilitation outcomes
the research in this area suggests that positive and general well-being (Johnson 1996, 1997) and
cognitions and the use of psychological skills will vigour (Quinn 1996), whereas negative associ-
enhance the rehabilitation process. Some of the ations have been documented for anger (LaMott
findings, however, such as those for denial and 1994; Alzate et al. 1998), anxiety (Johnson 1996,
emotion-focused coping/emotional focus (Quinn 1997), fear, frustration, relief (LaMott 1994), mood
1996; Grove & Bahnsen 1997; Quinn & Fallon disturbance, depression (Alzate et al. 1998; Tripp
2000), fatigue, tension (Alzate et al. 1998) and 1991; Treacy et al. 1997; Alzate et al. 1998; Brewer
psychological distress (Brewer et al. 2000c). et al. 2000c; Quinn & Fallon 2000), non-significant
Although all of the findings regarding the rela- (Noyes et al. 1983; Brewer et al. 2000c; Quinn
tionship between emotions and sports injury & Fallon 2000) and, surprisingly, negative
rehabilitation outcomes are purely correlational (Shelbourne & Wilckens 1990; Quinn & Fallon
in nature, most of the studies cited (i.e. Johnson 2000). These discrepant findings are probably
1996, 1997; Alzate et al. 1998; Brewer et al. 2000c; due to a variety of factors, including the nature of
Quinn & Fallon 2000) were prospective in that the injury studied, the specifics of the rehabilita-
emotions were measured at one point in time tion protocol, the phase of rehabilitation that was
(e.g. prior to surgery, at the beginning of rehab- the focus of study, and the particular measures of
ilitation) and sports injury rehabilitation out- adherence and outcome (Brewer 1999a).
comes were measured at a later point in time (e.g. Only a few behaviours other than adherence
at the end of rehabilitation). Consequently, there to rehabilitation have received any empirical
is evidence that for reasons not currently under- investigation. Better sports injury rehabilitation
stood, positive emotions may often precede outcomes have been found to be associated with
favourable rehabilitation outcomes. higher levels of active coping (Quinn & Fallon
1999), lower levels of physical activity (Gould
et al. 1997b) and higher levels of seeking social
behavioural factors
support (Johnson 1996, 1997; Gould et al. 1997b).
The behavioural factor examined most frequently
in reference to sports injury rehabilitation out-
psychological interventions to
comes has been adherence to rehabilitation. One
enhance rehabilitation outcomes
would assume that greater adherence to rehabil-
itation would be associated with better outcome, Support for the influence of a wide variety of
but this has not always been the case. The rela- psychological factors on sports injury rehabilita-
tionship between adherence to rehabilitation and tion outcomes can be inferred from the results
rehabilitation outcome has been found to be of experimental studies in which psychological
positive (Meani et al. 1986; Derscheid & Feiring interventions have been applied to athletes with
1987; Hawkins 1989; Satterfield et al. 1990; Tuffey injuries. As shown in Table 8.4, a number of
Table 8.4 Controlled studies examining the effects of psychological interventions on physical and psychological
rehabilitation outcomes.
Reference Intervention Effect(s) of intervention
Krebs 1981 Biofeedback Greater strength and EMG output

Draper 1990 Biofeedback Greater strength and ROM
Draper & Ballard 1991 Biofeedback Greater strength
Levitt et al. 1995 Biofeedback Greater extensor torque and
quadriceps fibre recruitment
Theodorakis et al. 1996 Goal setting Greater strength
Theodorakis et al. 1997b Goal setting Greater strength and self-efficacy
Ross & Berger 1996 Stress inoculation training Greater physical functioning, less
pain, less reinjury anxiety
Theodorakis et al. 1997b Self-talk Greater strength
Johnson 2000 Multimodal Greater positive mood and readiness
for competition
Cupal & Brewer 2001 Relaxation/guided imagery Greater strength, less pain, less
reinjury anxiety
interventions have been investigated experi- athletes with injuries. Relaxation protocols, which
mentally for their effects on physical and psy- are typically aimed at calming the muscles and
chological rehabilitation outcomes, including the mind, are frequently implemented just prior
biofeedback (Krebs 1981; Draper 1990; Draper to the use of imagery procedures, which gener-
& Ballard 1991; Levitt et al. 1995), goal setting ally feature mental rehearsal of motivational,
(Theodorakis et al. 1996, 1997b), imagery/ healing and performance aspects of rehabilitation.
relaxation (Cupal & Brewer 2001), self-talk Combining relaxation and imagery techniques
(Theodorakis et al. 1997a), stress inoculation is thought to affect rehabilitation outcomes by
training (Ross & Berger 1996) and a multimodal enhancing rehabilitation motivation and boost-
intervention consisting of goal setting, imagery, ing physiological processes such as tissue
relaxation and stress management ( Johnson regeneration/repair and immune/inflammatory
2000). Case study data have also supported the responses (Cupal & Brewer 2001). Self-talk
efficacy of interventions such as counselling, goal (or cognitive restructuring) interventions are
setting, hypnosis, positive self-talk, relaxation designed to alter athletes’ thoughts and, ulti-
and systematic desensitization for positively mately, feelings and behaviours, regarding their
effecting rehabilitation outcome variables such rehabilitation.
as confidence, motivation, perception of pain, Because research on psychological interven-
physical recovery, psychological adjustment, tions in sports injury rehabilitation has focused
reinjury anxiety and range of motion (Rotella primarily on documenting the effectiveness of
& Campbell 1983; Nicol 1993; Sthalekar 1993; such interventions, the processes by which these
Potter 1995; Brewer & Helledy 1998; Hartman & interventions exert their effect are not well under-
Finch 1999; Evans et al. 2000; Jevon & O’Donovan stood. Referring to the biopsychosocial model, it
2000). is postulated that psychological interventions may
Without exception, the psychological inter- affect rehabilitation outcome through a variety of
ventions that have been documented in the mechanisms, including a direct effect, indirect
scientific literature as having been used success- effects through intermediate biopsychological
fully in sports injury rehabilitation are cognitive– outcomes, and indirect effects through relation-
behavioural in nature and involve athletes ships with biological factors and social/contex-
learning new skills or behaviours to cope more tual factors. The complexities of these possible
effectively with the rehabilitation process, both relationships have yet to be adequately explored
physically and psychologically. Biofeedback, by researchers, but it is likely that psychological
for example, involves furnishing patients with interventions affect outcomes through a variety
physiological information (e.g. electromyographic of pathways.
activity in the quadriceps muscle group) and is
thought to produce therapeutic gains by enhan-
Implications for clinical practice
cing motivation for rehabilitation activities and
enhancing proprioceptive information process- The percentage of athletes who experience dif-
ing (Levitt et al. 1995). Similarly, goal setting, ficulties adjusting emotionally or behaviourally
which involves generating (short- and long-term) to injury furnishes evidence of the need to
personal standards of achievement in rehabili- consider psychological factors in planning,
tation activities, is posited to provide direction implementing and evaluating sports injury rehab-
to the athlete’s rehabilitation efforts, enhance ilitation protocols. Further rationale for incorpor-
persistence in rehabilitation and facilitate the ating psychological aspects into the treatment of
development of new rehabilitation strategies sports injuries is provided by the abundance
(Locke & Latham 1990). Although they are con- of psychological factors associated with sports
ceptually distinct interventions, relaxation and injury rehabilitation outcomes and the demon-
imagery are often used in conjunction to treat strated efficacy of psychological interventions in
producing desirable sports injury rehabilitation and comfort in identifying the warning signs
outcomes. Although the value of taking psy- of athletes who are experiencing problems in
chological factors into account in sports injury adjusting psychologically to their injuries.
rehabilitation is recognized, the ways in which In some cases, such as when high levels of
psychology should be included in the rehabilita- depression or anxiety are detected, referral to a
tion process and by whom is less clearly delineated. mental health practitioner is warranted (Brewer
Potential opportunities for clinical application of et al. 1999b). In most circumstances, though,
the research on psychological factors in sports sports injury rehabilitation practitioners can
injury rehabilitation exist for both sports injury facilitate a smooth navigation of the rehabilita-
rehabilitation practitioners and sport psychology tion process by educating athletes about their
professionals. injuries and likely challenges to be encountered
during rehabilitation and, when appropriate,
applying a simple psychological intervention
sports injury rehabilitation
such as goal setting (Gilbourne & Taylor 1995,
practitioners
1998; Gilbourne et al. 1996; Theodorakis et al.
A variety of medical professionals provide clin- 1996, 1997b; Penpraze & Mutrie 1999) to motivate
ical services to athletes with injuries, including and focus the rehabilitation efforts of athletes.
physicians, physiotherapists and athletic train- The importance of patient education and clear
ers. Depending on the frequency of their contact patient–practitioner communication is under-
with athletes during the injury rehabilitation scored by research demonstrating that athletes
process, sports injury rehabilitation practitioners with injuries often misperceive their interactions
can be in a strategic position to enhance the with rehabilitation practitioners (Kahanov &
adjustment of athletes to injury and promote Fairchild 1994) and misunderstand at least some
adherence to the treatment protocol. Indeed, portion of their prescribed rehabilitation regime
sports injury rehabilitation practitioners, in con- (Webborn et al. 1997).
stituting an important situational factor in the
integrated model (Wiese-Bjornstal et al. 1998)
sport psychology professionals
and social/contextual variable in the biopsy-
chosocial model (Brewer et al. 2002), have the Despite the growing body of literature docu-
potential to affect the psychological state of their menting the role of psychological factors in
patients regardless of their intent to do so. influencing sports injury rehabilitation processes
Surveys of sports injury rehabilitation practi- and outcomes, only rarely are sport psychology
tioners (e.g. Brewer et al. 1991; Gordon et al. 1991; professionals fully fledged members of the sports
Ford & Gordon 1993, 1997; Larson et al. 1996; medicine treatment team (Cerny et al. 1992; Larson
Ninedek & Kolt 2000) have indicated a general et al. 1996). The low level of involvement of sport
awareness of, and interest in, psychological psychology professionals in the rehabilitation of
aspects of rehabilitation. Despite this interest and athletes with injuries may be due, in part, to: (i)
awareness, sports injury practitioners may not the structure and restrictions of the health care
feel comfortable or qualified to make judge- systems in which athletes receive rehabilitation
ments or initiate interventions of a psychological for their injuries; (ii) the lack of standard pro-
nature. Research has indicated that sports injury cedures for rehabilitation practitioners to refer
rehabilitation practitioners may have difficulty athletes with injuries for counselling or psycho-
recognizing psychological distress among their therapy (Larson et al. 1996); and (iii) the reluct-
patients (Brewer et al. 1995b; Maniar et al. 1999). ance of athletes with injuries to participate in
With appropriate training (Ford & Gordon 1998; ‘extra’ therapeutic activity beyond their physical
Gordon et al. 1998), however, rehabilitation pro- rehabilitation even if they find the interventions
fessionals can increase their knowledge, skills sufficiently credible (Brewer et al. 1994b).
In circumstances where a sport psychology will influence emotions, behaviour, cognitions

professional is not involved in the day-to-day and, ultimately, rehabilitation outcome, most
assessment of athletes with injuries and in the studies have focused on highly specific psycho-
initiation of psychological interventions such logical factors and only one of these types of vari-
as imagery and relaxation, as seems to be the ables. This has led to a hodgepotch of direct
norm, sports injury rehabilitation practitioners relationships, with little comparability of the
are encouraged to identify sport psychology psychological factors studied across the different
professionals to serve as consultants, referral outcome measures. Both models also propose
targets and resources on psychological aspects that many psychological factors are related to
of rehabilitation. Some sport psychology profes- injury and injury rehabilitation processes as
sionals have clinical training and can work with mediating variables, and these mediating rela-
athletes who show signs of mental disorders or tionships have yet to be sufficiently investigated.
severe adjustment reactions. Unfortunately, when To examine these relationships, studies will have
sport psychology professionals are not integral to become more integrated, including measures
members of the sports medicine treatment team, of the multiple constructs of both the integrated
they are more likely to be contacted regarding model and the biopsychosocial model. It must
difficult patients than regarding routine ways also be recognized that the rehabilitation process
that psychology can be applied to enhance the is a dynamic one, and more frequent assessments
rehabilitation of athletes with injuries. Further of the psychological factors (as in time series
research documenting the role of psychological analysis) and intraindividual analyses are needed
factors and the efficacy of psychological inter- to examine the fluid and diverse nature of the
ventions in sports injury rehabilitation is needed constructs involved (Evans & Hardy 1999).
to advance the standing of sport psychology One area of research vital to ensure progress in
professionals in the enterprise of sports injury this area of enquiry is the development and stand-
rehabilitation. ardization of adequate measures of the specific
constructs involved. Diversity in measurement
methods and inconsistent operationalization of
Future research directions
constructs has led to difficulty in making com-
The proliferation of, and progress in, research parisons across studies. Increased standardization
concerning psychological correlates of sports of instruments and definitions of the constructs
injury rehabilitation parameters since the re- are likely to lead to a more consistent and unified
commendations made by Williams and Roepke body of research (Evans & Hardy 1999). How-
(1993) and Brewer (1994) has been heartening. ever, the development of adequate instruments
However, this body of research has only is a difficult and time-consuming endeavour, and
scratched the surface of the potential questions research on psychological aspects of sports injury
still in need of answers. The two models used as rehabilitation has suffered from instruments that
a framework for the review of literature in this have not demonstrated good psychometric prop-
chapter, the integrated model (Wiese-Bjornstal erties (Brewer et al. 1999a; Slattery 1999). Only
et al. 1998) and the biopsychosocial model with adequately designed and validated measures
(Brewer et al. 2002), have provided not only a can the various constructs involved in the psy-
structure for examining the literature to date, but chological aspects of sports injury be effectively
offer many suggestions for future research. As examined.
demonstrated by the research reviewed in this A further area of enquiry on which future
chapter, many of the postulated direct pathways research should focus is the specific processes
of both models have been supported, but many and effectiveness of psychological interventions
have yet to be examined. In particular, although in sports injury rehabilitation. Although a variety
both models predict that psychological factors of interventions have been found to be related
to better sports injury rehabilitation outcomes growth, psychosocial development and academic
(Cupal 1998), the specifics of the mechanisms performance as a result of their injuries (Rose
through which these interventions operate are & Jevne 1993; Udry et al. 1997a; Ford 1998;
not well understood. Only by clearly under- Niedfeldt 1998; Ford & Gordon 1999). However,
standing how these interventions work can the again, the specific personal, situational and psy-
interventions be tailored effectively to the multi- chological variables that are related to these
plicity of personal variables, situational variables benefits have not been identified, and further
and psychological variables implicated in the studies, both qualitative and quantitative, are
sports injury rehabilitation process. needed to expand our knowledge of this fas-
It will also be important to examine ways in cinating counter-intuitive line of research.
which psychological interventions interact with From a theoretical standpoint, explanatory
medical interventions (e.g. immobilization, med- models for psychological aspects of sports injury
ications, physical therapy, surgery, therapeutic are in their infancy. The integrated model
exercise) to influence emotional and behavioural (Wiese-Bjornstal et al. 1998) and the biopycho-
functioning during injury rehabilitation. Given social model (Brewer et al. 2002) described in
that, from a biopsychosocial perspective (Brewer this chapter have been proposed only recently,
et al. 2002), medical interventions may directly and although supported by a growing body of
affect both biological factors and intermediate research, there are still many predictions derived
biopsychosocial outcomes, it would not be sur- from these models that have not yet received
prising if certain psychological interventions empirical support. Further data gathered within
were found to be especially effective for some the contexts of these models will probably
injuries and in conjunction with particular inspire modification to the models as they
medical treatments. For example, a psycholog- currently exist. Additionally, there is evidence
ical intervention designed to enhance motivation indicating that psychological factors are related
might be more appropriate for injury rehabili- to the occurrence of injury (Meeuwisse & Fowler
tation protocols that have heavy behavioural 1988; Williams & Andersen 1998) and these
demands (e.g. extensive rehabilitation exercises) relationships could be incorporated into a model
than for those with more passive features (e.g. that could cover the entire spectrum of the injury
activity restriction, immobilization). Unquestion- process, from biopsychosocial factors related to
ably, the agenda for further research on psycholo- the likelihood of experiencing an injury to the
gical interventions in sports injury rehabilitation implications of these factors for the outcome of
should include randomized controlled clinical sports injury rehabilitation.
trials comparing frequently advocated psycholo-
gical interventions (e.g. cognitive restructuring,
Conclusions
counselling, goal setting, imagery, relaxation)
separately and in combination. Such research can The proliferation of research investigating the
help provide practitioners with more detailed psychological factors related to sports injury
information on what interventions, administered rehabilitation has demonstrated the importance
in which ways and by whom at which frequen- of these factors to rehabilitation outcome. De-
cies, are likely to be most effective for which scriptive, correlational, experimental, quantitative
athletes under what circumstances. and qualitative research has shown that a variety
A paradoxical direction for future research is of behavioural, cognitive, emotional and situ-
to explore the potential benefits of sports injury ational factors are involved in the sports injury
(Udry 1999). Some recent qualitative studies have rehabilitation process. Only through an adequate
documented that some athletes with injuries understanding of these factors and their inter-
have reported experiencing higher levels of life relationships can well-designed interventions be
satisfaction, performance enhancement, personal proposed to enhance the rehabilitation process
and, potentially, speed up or improve the out- Brewer, B.W. (1999b) Causal attribution dimensions
come of sports injury rehabilitation. and adjustment to sports injury. Journal of Personal
and Interpersonal Loss 4, 215–224.
Brewer, B.W. & Helledy, K.I. (1998) Off (to) the deep
Author note end: psychological skills training and water running.
Applied Research in Coaching and Athletics Annual 13,
Preparation of this chapter was supported in part 99–118.
by grant number R29 AR44484 from the National Brewer, B.W. & Petrie, T.A. (1995) A comparison
Institute of Arthritis and Musculoskeletal and between injured and uninjured football players on
selected psychosocial variables. Academic Athletic
Skin Diseases. Its contents are solely the respons- Journal 10, 11–18.
ibility of the authors and do not represent the Brewer, B.W., Van Raalte, J.L. & Linder, D.E. (1991) Role
official views of the National Institute of Arthritis of the sport psychologist in treating injured athletes:
and Musculoskeletal and Skin Diseases. a survey of sports medicine providers. Journal of
Applied Sport Psychology 3, 183–190.
Brewer, B.W., Daly, J.M., Van Raalte, J.L., Petitpas, A.J. &
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Sport Psychology, Banff, Alberta, Canada. teristics of women volleyball players: relationships
Udry, E., Gould, D., Bridges, D. & Beck, L. (1997a) Down with injuries, rehabilitation, and team success. Per-
but not out: athlete responses to season-ending sonality and Social Psychology Bulletin 20, 322–330.
PA R T 4
CLINICAL
R E H A B I L I TAT I O N
I N T E RV E N T I O N S
Chapter 9
Pharmacological Agents and Acupuncture

in Rehabilitation
JULIE K. SILVER AND JOSEPH AUDETTE
symbolizes the hallmarks of acute inflammation

Introduction
(Vertosick 2000). One thousand years later, the
Medications are a mainstay of treatment in the Greek physician Hippocrates coined the term
injured athleteaboth for their pain relief and ‘phlegmone’ which means ‘the burning thing’.
healing properties. Yet, despite the widespread Then, in the first century after the death of Christ,
use and acceptance of many medications, more the Roman author Cornelius Celsus provided
often than not there is little research to endorse what is the basis for our description of inflamma-
their use. In this chapter, we will focus on the tion today: rubor et tumour cum calore et dolore
primary medication classes that are used in (redness and swelling with heat and pain)
sports medicine, especially during the first stage (Vertosick 2000).
of rehabilitation. However, the reader is cau- It is not surprising that since our ancestral
tioned to recognize that the evidence that we rely healers were so cognizant of inflammation that
so heavily on is sparse in this area. Therefore, it they would also have found ways to treat it.
is recommended that all medications in athletes Indeed, ancient Egyptians and Assyrians used
be used judiciously with a distinct regard for willow extract to reduce the redness and pain of
the risks and side effects as well as the potential inflamed joints; however, the first description of
benefits, which include pain relief and early salicylate therapy did not come until several
return to play. thousand years later. One historian notes that the
‘story begins in modern times with a letter from
the Reverend Edward Stone of Chipping Norton
Non-steroidal anti-inflammatory
to the Royal Society in 1763. He wrote: “There is a
drugs
bark of an English tree which I have found by
experience to be a powerful astringent and very
A brief history
efficacious in curing anguish and intermitting
Inflammation has been around longer than doc- disorders” ’ (Wall 2000).
tors have known how to treat it. But since the Although there were various historical attempts
very first physicians began to record what makes to use willow bark and its derivatives, it was not
up the basis of our current medical knowledge, until Hermann Kolbe, a professor of chemistry at
they have described inflammation. In the oldest Marburg University, succeeded in synthesizing
known medical textbook, the Edwin Smith papyrus salicylic acid (the precursor to modern aspirin)
that was written by Egyptian healers 17 centuries that it became widely used. In what is described
before the birth of Christ, the body’s reaction to as ‘a strange twist of history’ (Vertosick 2000),
injury was called ‘shememet’. The term shememet one patient who was disgusted with Kolbe’s
is always followed by a hieroglyph for ‘fire’ that concoction of salicylic acid that caused severe
187
188 clinical rehabilitation interventions
gastrointestinal upset, approached his son, a but this is not usually a factor in their use for
chemist for the German manufacturer of chem- sports injuries. Because some of the NSAIDs are
ical dyes, Fredrich Bayer & Company, and easily available without a prescription, they are
together they synthesized acetylsalicylic acid. often used haphazardly and improperly. More-
They called this new drug Aspirin. Today there over, the literature has not clearly defined when
are more than 30 000 tons of aspirin sold NSAIDs should be used, what dose is most
worldwide, and aspirin and its cohorts in the appropriate and for what period of time they
non-steroidal anti-inflammatory drug (NSAID) should be used after an injury. Thus, even when
class are universally used to control both pain they are prescribed by skilled clinicians, NSAIDs
and inflammation. may cause more harm than good.
Inflammation is the normal response in tissue
to any traumaawhether it is acute (macrotruama)
Chemical properties and mechanism of action
or chronic (microtrauma, generally due to repeti-
Today there are dozens of NSAIDs available tive motion). The purpose of the inflammatory
commercially, which all have a common mech- response (see Chapter 2 for a more detailed dis-
anism of action (Huff & Prentice 1999). Some of cussion) is to contain the injury, remove the
the more common NSAIDs are listed in Table 9.1. irreparably injured (necrotic) tissue and restore
NSAIDs are widely used as first-line agents in function by re-establishing structural integrity.
sports injuries, particularly in soft tissue injuries The acute inflammatory response occurs most
that involve muscles, tendons and ligaments. significantly in the first 48 h after injury. During
These medications are used primarily for two this period of time, the inflammatory response is
reasons: (i) to decrease inflammation, and (ii) to mediated by local vasoactive products such as
reduce pain. NSAIDs also have antipyretic effects, histamine, bradykinin and serotonin, which are
Table 9.1 Dosage of currently available NSAIDs.
Generic name Common dose (mg) Usual dosing frequency
Aspirin 325 Q 2–4 h

Celecoxib 100 BID
Diclofenac 75 BID
Diflunisal 500 BID
Etodolac 400 BID
Fenoprofen 600 QID
Flurbiprofen 100 TID
Ibuprofen 800 QID
Indomethacin 25–50 TID
Ketoprofen 75 TID
Ketorolac 10 QID
Meclofenamate 100 TID
Nabumetone 500 2 QD
Naproxen 500 BID
Oxaprozin 600 2 QD
Piroxicam 20 QD
Rofecoxib 25 QD
Salicylsalicylic acid 750 QID
Sodium salicylate 650 Q4h
Sulindac 200 BID
Tolmetin 400 TID
BID, twice a day; Q 2–4 h, every 2–4 h; QD, each day; 2 QD, two once a day; Q 4 h,
every 4 h; QID, four times a day; TID, three times a day.
pharmacological agents and acupuncture 189
released from mast cells in order to increase There are studies that have tried to address
blood flow and permeability. Their effects pre- this, although the answer is not yet clear. For
dominate in the first hour after injury. example, in one study 24 white rabbits sustained
The acute inflammatory response is then par- injury to the medial collateral ligament of one
tially maintained by a class of mediators called hindleg (Moorman et al. 1999). The rabbits were
the eicosanoids, which leads to the formation of treated orally, twice daily, with a 2-week course
prostaglandins and leukotrienes. The primary of either ibuprofen or placebo. The ligaments
focus of medications to control inflammation (in were tested and there was no statistically signi-
particular NSAIDs) has been to control prosta- ficant difference in the values of the mechanical
glandin synthesis, which is in large part respons- properties of the ligaments in the rabbits treated
ible for the increased vascular permeability and with ibuprofen versus placebo. The authors con-
vasodilatation at the site of injury. What happens cluded that, under the conditions of the study,
in chronic injuries or those without a significant there was no deleterious effect of a short course
initial inflammatory phase is not well elucidated. of ibuprofen on the mechanical properties of
For example, lateral epicondylitis or ‘tennis elbow’ medial collateral ligaments. However, in con-
was long thought to be a ‘tendinitis’ that was tradistinction to this study, another study was
caused by an inflammatory condition. Not sur- done on male rats where they underwent sur-
prisingly, NSAIDs have been a first-line treatment gical transection of the medial collateral liga-
for this condition. However, more recent studies ment (Elder et al. 2001). Postoperatively, half the
reveal that microscopically the process is more rats were treated with celecoxib and the others
consistent with a tendinosisademonstrating angio- were not. This study found that ligaments in the
fibroblastic hyperplasia, hyaline degeneration, celecoxib-treated rats had a 32% lower load to
fibrinoid necrosis and granulation tissue with failure than the untreated ligaments. Needless
very few inflammatory cells (Nirschl 1992). to say a reduced ligamentous strength is an un-
After the initial 24–48 h, the cellular inflam- acceptable outcome in athletes eager to return to
matory response begins the ‘clean-up’ process. training and competition as early as possible.
This marks the beginning of the reparatory phase. Additionally, NSAIDs are known to affect the
The cells most involved in this process are macro- clotting process, and it is not clear in acute injury
phages and neutrophils that are responsible for what impact this has on the tissues and the
digesting and clearing away unusable products healing process. Unfortunately, studies have not
in order to promote healthy tissue healing. It is been done to clearly delineate: (i) whether
in this phase that much of the controversy over NSAIDs truly help to heal sports injuries or
NSAIDs occurs. The question that remains un- merely act as suppressers of the initial immune
answered to date is whether NSAIDs retard this response as well as pain modulators; (ii) if they
important phase of healing and whether this in do help initially, then at what point do they
fact might delay or impair the healing process become ineffective or even detrimental; and (iii)
(Leadbetter 1990). if they help for all injuries or just injuries in
Since the inflammatory response consists of which one would anticipate a lot of inflammation
vasodilatation with extravasation of blood that such as an acute contusion or sprain/strain injury.
carries blood cells and other products into the There is a paucity of literature that illustrates
area of injury, and this initial response is fol- when and how to use NSAIDs for sports-related
lowed by the recruitment of inflammatory cells injuries.
such as leucocytes and macrophages, then part of Regardless of the injury, NSAIDs have two
this process involves clearing the injured area of main functions in the treatment of sports injuries:
debris such as necrotic muscle tissue and dis- (i) to modify the inflammatory process; and (ii)
rupted connective tissues (Almekinders 1993). If to provide analgesia (Huff & Prentice 1999). The
the clean-up process is halted or impaired, it is primary mechanism of action of NSAIDs in the
not clear whether the healing process will suffer. inflammatory process is to inhibit prostaglandin
production. Prostaglandins are a group of fatty slow healing in some instances. Moreover, in some
acids that help to mediate the inflammatory injuries in which there is a marked inflammatory
response. A decrease in prostaglandin synthesis response, such as an acute contusion or sprain/
through the inhibition of cyclooxygenase (COX) strain injury, the effect of NSAIDs (either good or
is believed to significantly inhibit the inflamma- bad) may be more significant than in injuries
tory response (Vane 1971). There are at least two where there is less of an inflammatory response
forms of COX inhibitors present in humans (e.g. chronic repetitive strain injuries or delayed-
(Huskisson et al. 1973; Polisson 1996). These onset muscle soreness, DOMS). Yet, despite the
enzymes act differently in the body and their fact that compelling studies, which would sup-
actions in large part determine the side effects port the use of NSAIDs in athletes, are lacking,
of NSAIDs. There has been increasing interest there are studies that suggest a definite role for
in NSAIDs that selectively promote COX-1 their use. For example, in one study where 364
while inhibiting COX-2 (DeWitt et al. 1993). Australian Army recruits with ankle sprains
Examples of NSAIDs that selectively inhibit sustained during training were treated with
COX-2 are celecoxib and rofecoxib (see Table 9.1 placebo or piroxicam, the latter group had less
for dosing). pain and were able to resume training more
This fairly straightforward explanation of how rapidly than the placebo group (Slatyer et al.
NSAIDs work is probably more complex in 1997). Two other studies revealed that NSAIDs
reality and has been challenged by a number of in young adult males and in healthy older indi-
studies. Some investigators have suggested that viduals attenuated the exercise-induced inflam-
NSAIDs may act directly on the inflammatory mation, strength loss and soreness associated
cells (Wahl et al. 1977; Ceuppens et al. 1986) and with eccentric exercise (DOMS) (Dudley et al.
that perhaps some NSAIDs are fairly weak 1997; Baldwin et al. 2001).
inhibitors of prostaglandin synthesis but appear
to have a more pronounced analgesic effect
Dosing
(McCormack & Brune 1991). It is interesting to
note that aspirin is the only NSAID that irre- Table 9.1 lists the common NSAIDs and their
versibly inhibits COX; the other effects of other doses. When taken orally, NSAIDs typically reach
NSAIDs are reversible. steady-state concentrations in the serum after
The mechanism by which NSAIDs produce three to five half-lives (Stankus 1999). The clear-
analgesia appears to be multifactorial. Aspirin ance of these agents (usually via the liver) is
can interfere with the transmission of painful variable, which accounts for the wide spectrum
impulses in the thalamus (Moncada & Vane 1979). of elimination times. Thus, typically NSAIDs are
Blocking the inflammatory response is also prob- prescribed for 2–3 weeks and monitored for their
ably a factor in decreasing pain. Both effects on effectiveness. The use of multiple NSAIDs has
pain and inflammation are thought to be due to not been shown to be more effective than mono-
the blocking of proinflammatory prostaglandins therapy and increases the risk of adverse side
in the soft tissues. effects (Stankus 1999). However, NSAIDs can be
Despite numerous studies elaborating on the used safely with other analgesics if pain control
mechanism of action of NSAIDs, it is not entirely is an issue (e.g. acetaminophen or opioids).
clear whether they influence the outcome after Topical preparations of NSAIDs have been
sports injuries. Clearly, they attenuate the classic shown to have a more reduced blood concentra-
inflammatory response that consists of pain tion than after oral or intramuscular administra-
(dolor), heat (calor), redness (rubor), swelling tion (Doogan 1989; Heynemann 1995; Dominkus
(tumour) and loss of function ( functio laesa) et al. 1996). However, they do appear to reach their
(Leadbetter 1990). But the degree to which they target tissues and have been found in muscle and
affect healing is not clear. In fact, they may actually subcutaneous tissue after topical use (Dominkus
et al. 1996). Topical preparations of NSAIDs sports injuries’ (Griffiths 1992). This occurred
are gaining favour in sports medicine due to a when she was in a stressful situation in a differ-
number of promising studies that suggest object- ent country and was playing tennis for 4 h a day
ive and subjective improvement of symptoms in a hot climate. Thus, it is likely that dehydra-
(Akermark & Forsskahl 1990; Thorling et al. 1990; tion also contributed to her condition. There
Russell 1991; Airaksinen et al. 1993). is also some evidence to suggest that in runners
NSAIDs may be harmful due to a reduction
in renal blood flow (Walker et al. 1994). It is
Side effects
important to remember that renal blood flow is
The side effects of NSAIDs result primarily reduced during exercise in healthy athletes
from the inhibition of prostaglandin synthesis and that proteinuria and haematuria have been
and occur in the following systems (in order of reported after long-distance running and cycling
decreasing relative frequency): (i) gastrointestinal (Eichner 1990; Mittleman & Zambraski 1992).
(e.g. gastritis or ulceration); (ii) renal (interstitial Future studies are needed to investigate the
nephritis); (iii) dermatological (rash); and (iv) possible interactions of exercise and NSAIDs.
central nervous system (CNS) changes (Mortensen Rashes have been noted with both oral and
1989). topical NSAIDs. Typically these are benign
By far the most notable side effect of NSAIDs is urticarial rashes that resolve when the medication
the toxicity to the gastrointestinal tract. Typical is discontinued. But more severe dermatological
symptoms of gastric toxicity include heartburn rashes have been described, e.g. Stevens–Johnson
or dyspepsia, gastritis and, potentially, ulcera- syndrome and erythema multiforme (Stankus
tion. One-third to one-half of all patients who 1999). It is important to note that the triad of
die of ulcer-related complications have recently nasal polyposis, asthma and rhinitis may be an
been on NSAID therapy (Hollander 1994). Studies indication of increased risk of NSAID-induced
have demonstrated a markedly increased (4–30- hypersensitivity reaction (Stankus 1999).
fold) risk of developing ulcer disease associated Central nervous system side effects are un-
with NSAID use (Soll et al. 1991; Griffith et al. common but may include headache, tinnitus,
1991). Although the risk of gastrointestinal side depression, aseptic meningitis, mental status
effects is significant, it is important to note that changes and coma (Stankus 1999). NSAIDs may
most of the literature regarding this topic does alter blood pressure control or decrease the
not reflect its use in young, healthy athletes. Both effectiveness of antihypertensive medications.
topical NSAIDs and the oral selective COX-2 NSAIDs also impair the normal function of
inhibitors may be safer alternatives regarding platelets and may increase the bleeding time.
gastrointestinal toxicity than traditional oral Of note is that NSAIDs are not recommended
NSAIDs (Dominkus et al. 1996; DeWitt et al. in the pregnant athlete.
1993). Additionally, medications used concur-
rently with NSAIDs, such as omeprazole, may
Steroidal medications
provide some protection (Goodman & Simon
1994).
A brief history and forms of administration
Renal toxicity is also an important considera-
tion when using NSAIDs. Although serious renal Both corticosteroids and anabolic steroids have
complications are uncommon, there are ex- been used in the treatment of sports injuries.
amples of severe renal toxicity that have resulted However, since the International Olympic Com-
from NSAID use. In one case report a 20-year-old mittee (IOC) (see doping issues, p. 200) and most
female athlete developed end-stage renal fail- other agencies governing the use of drugs in
ure that was attributed to ‘regular use of anti- athletes ban anabolic steroids, this section will
inflammatory analgesic medication for minor be primarily devoted to corticosteroid useaboth
oral and injectable forms. Local anaesthetic med- Injections also have the advantage of being both
ications that are often used in conjunction with diagnostic and therapeutic. Favourable results
corticosteroid injections (but may be used alone) are common with injectable steroids (Kapetanos
will also be covered. The relevant restrictions on 1982; Wiggins et al. 1994; Holt et al. 1995). Ionto-
the use of local anaesthetics and glucocorticoids phoresis (using electrical stimulation) and phono-
are discussed in the section on doping (p. 200). phoresis (using ultrasound) are other methods of
The use of corticosteroids has a much more delivering corticosteroids locally and may prove
recent history than that of NSAIDs. It was not until to have some benefit (Franklin et al. 1995; Breen
the 1920s that Dr Philip Hench noted that patients 1996).
with hypoadrenalism had many of the same
symptoms as people with rheumatoid arthri-
Chemical properties and mechanism of action
tis. Dr Hench concluded that rheumatoid
arthritis must have a component of adrenal hor- The exact mechanism by which glucocorticoids
mone insufficiency and could be cured with work to mitigate inflammation is not entirely
hormone replacement. Hench’s theory could understood. Glucocorticoids are adrenocortical
not be tested until the 1930s when pure prepara- steroids that occur naturally and can be manu-
tions of adrenal hormones became available. factured synthetically (Physicians’ Desk Refererence
However, the hormone product that came from 2002). These drugs are readily absorbed from
human adrenal glands (called compound E) was the gastrointestinal tract. Prednisone is the most
still not readily available. Years later, in 1948, commonly prescribed synthetic oral glucocorti-
Hench conducted the first clinical trial and the coid and will be the model for this discussion. In
results were just as he suspectedapatients with athletes, prednisone and the other glucocorticoids
rheumatoid arthritis reacted miraculously to cor- are prescribed primarily for their powerful anti-
tisone (compound E). Hench and his co-worker inflammatory properties.
won the Nobel prize for medicine in 1950 and his Anabolic steroids are synthetic derivatives
Nobel address was titled, ‘The reversibility of of the hormone testosterone. The actions of
certain rheumatic and non-rheumatic conditions anabolic steroids are therefore similar to that
by the use of cortisone’ (Vertosick 2000). of testosterone. In spite of the widespread use
Although this finding was an important one, of adrenergic steroids by bodybuilders and other
it was not what many people had hopedaa cure athletes, the effects of these drugs are poorly
for rheumatoid arthritis and other medical con- understood. Testosterone is known to increase
ditions that involve inflammation. In fact, further muscle mass, but it is not known whether testos-
studies revealed that cortisone had very serious terone truly improves physical function and
side effects and could not be taken in large quan- health-related quality of life (Bhasin et al. 2001).
tities for long periods of time. It is now common Anabolic steroids are banned in Olympic com-
knowledge in the medical community and even petitions. However, in clinical medicine there are
in the public domain that corticosteroids pro- some legitimate uses for these drugs including
duce significant deleterious side effects when the promotion of weight gain after weight loss
taken orally. following extensive surgery, burns or severe
In the injectable forms, although there are trauma, to offset the side effects associated
fewer systemic side effects, there are some with prolonged corticosteroid use and for the
potential hazards that mandate that these med- relief of bone pain accompanying osteoporosis
ications be prescribed with caution. It is critical (Physicians’ Desk Reference 2002). More recently,
that steroids used in injectable forms are properly there has been increased interest in the effect of
delivered to the target site. Imaging techniques male hormones and the synthetic derivatives on
such as fluoroscopy are sometimes used to help the healing of skeletal muscle (Beiner et al. 1999;
guide the practitioner (Micheli & Solomon 1997). Bhasin et al. 2001).
Table 9.2 Common sites of injection in athletes. One per cent lidocaine or 0.25% bupivicaine should be used with
long-acting, insoluble steroid salts such as triamcinalone acetate or betamethasone acetate.
Injection sites Needle Volume (cm3) Comments
Joints
Ulnocarpal No. 25, 1.5 in 1–3 Steroid volume to anaesthetic ratio 1 : 1
Radiocarpal
Carpometacarpal
Elbow No. 25, 1.5 in 2–3 Steroid volume to anaesthetic ratio 1 : 2
Ankle
Shoulder No. 25, 1.5 in 7–10 Steroid volume to anaesthetic ratio 1 : 6–9
Knee
Sacroiliac joint
Bone–tendon
Med/lat epicondyle No. 27, 1.25 in 2–3 Steroid volume to anaesthetic ratio 1 : 1
Plantar fascia
Patellar tendon
Achilles tendon
Pubic symphysis No. 25, 1.5 in 3–5 Steroid volume to anaesthetic ratio 1 : 2–4
Hamstrings
Adductors
Tendon sheaths
Thumb extensor No. 27, 1.25 in 1–3 Steroid volume to anaesthetic ratio 1 : 1
Finger flexors
Posterior tibial No. 27, 1.25 in 3–5 Steroid volume to anaesthetic ratio 1 : 2–4
Biceps (long head)
Bursae If aspirating, will need No. 18–20 needle first
Prepatellar No. 25, 1.5 in 2–3 Steroid volume to anaesthetic ratio 1 : 1
Pes anserine
Olecranon
Subacromial No. 25, 1.5 in 7–10 Steroid volume to anaesthetic ratio 1 : 6–9
Greater trochanter
Perineural
Carpal tunnel No. 27, 1.25 in 2–5 Steroid volume to anaesthetic ratio 2 : 1
Tarsal tunnel
Suprascapular notch
Cubital tunnel
involves a more constant dose (e.g. 5 or 10 mg

Dosing
of prednisone daily), but is really practitioner-
Systemic corticosteroids are dosed in a variety dependent. This approach is rarely used, if ever,
of ways and the literature does not support a in sports injuries and the systemic use of gluco-
‘best way’ approach. Often in an acute injury, corticoids is banned by the IOC (see doping
corticosteroids are prescribed in a weaning fash- issues, p. 200).
ion with the highest dose taken on the first Injections can be done with corticosteroid alone
few days and then tapering off the medication or mixed with a local anaesthetic, at a number of
altogether within 1–2 weeks. There are commer- sites (Table 9.2). In joints or bursae, aspiration of
cially available ‘dose packs’ that are used for just fluid may be done prior to injecting the medica-
this purpose. Longer term steroid use typically tion. The dose and amount of injected material
depends on the medication used and the struct- clinician, side effects are rare. Postinjection
ure that is being injected. There are no hard and pain is rather common, however, and patients
fast rules on dosing, but some general guidelines should be cautioned that they may experience a
advocated in the literature include: using 2.5–10 slight increase in pain for 1–2 days following the
mg of prednisolone tebutate suspension in small injection.
joints (e.g. hand and foot), 10–25 mg in medium-
sized joints (e.g. wrist and elbow) and 20–40 mg
Muscle relaxants
in large joints (e.g. knee and shoulder) (Swain &
Kaplan 1995). The literature on the use of muscle relaxants in
athletes in practically non-existent. It is mentioned
here only because, anecdotally, physicians often
Side effects
do prescribe muscle relaxants for sprain/strain-
The side effects associated with systemic corti- type injuries. Whether muscle relaxants help or
costeroid use are many and often are associated hinder healing is unclear. Equally unknown is
with long-term use. Some of the more serious whether muscle relaxants provide any pain relief
side effects include fluid and electrolyte disturb- effect or whether they allow athletes to return to
ances, steroid myopathy, osteoporosis, aseptic their sport at an earlier date. What is known is
necrosis of the femoral and humeral heads, pep- that there are many different types of muscle
tic ulcer, pancreatitis, impaired wound healing, relaxants that work by different pathways. Many
headaches, convulsions, suppression of growth of these have CNS side effects and at best cause
in children, Cushingoid state, cataracts and glau- fatigue or dry mouth and at worst can cause
coma (Physicians’ Desk Reference 2002). serious illness or even death (Linden et al. 1983;
Injections carry the risk of injury to a blood Kovac 1999; Olcina & Simonart 1999).
vessel, nerve or other important structure. The
deleterious effects on articular cartilage, tendons
Opioids and inflammation
and the plantar fascia are somewhat disputed
(Read & Motto 1992; Shrier et al. 1996), but there The use of opioids to treat athletic injuries is a
is the possibility of tendon or plantar fascial rup- controversial area. The reluctance of physicians
ture following corticosteroid injection (Acevedo to use these agents in the arena of sports injuries
& Beskin 1998; Smith et al. 1999). An allergic reac- is due to a number of concerns that are both
tion to the medication used, vasovagal syncope clinically and behaviourally motivated (Stanley
and infection are also important considerations & Weaver 1998). From a clinical point of view,
(Table 9.3). Injectable steroids may also cause opioids, as potent analgesics, may prevent the
subcutaneous tissue atrophy and skin depig- normal interpretation of pain signals by athletes
mentation, which are both usually just cosmetic and thereby allow too quick a resumption of
concerns for the patient. When used by a skilled aggressive training following injury. This could
Table 9.3 Local and systemic complications with local injections of corticosteroids.
Local Systemic
Subcutaneous atrophy Transient hyperglycaemia in diabetics

Pigmentation abnormalities Vasovagal symptoms with syncope
Tendon/ligament rupture Cognitive effects, ‘steroid psychosis’
Accelerated joint destruction Allergic reactions
Local sterile abscess Systemic infection
Peripheral nerve injury Suppression of pituitary–adrenal axis
Muscle necrosis/vascular injury Avascular necrosis of hip
potentially lead to reinjury and further impair- In addition, inflammation causes the perineural
ment. From a biobehavioural point of view, treat- barrier to become more permeable, presumably
ing physicians must also be concerned about the exposing more opioid receptors on the sensory
inappropriate use of opioids to enhance perfor- axon to both exogenous and endogenous opioids
mance. In addition, prolonged use of opioids to (Coggeshall et al. 1997). This increased receptor
treat a more persistent injury can cause physical expression is stimulated by the release of endo-
dependence and in rare cases psychological genous opioid peptides such as β-endorphin
dependence, making cessation of the medication from CD4+ lymphocytes within inflamed tissue
problematic. (Mousa et al. 2001). The source of the endo-
Opioids or ‘narcotics’ are on the IOC list of pro- genous opioid seems to not be from pituitary
hibited substances (see p. 200) (Catlin & Murray secretion, but rather from circulating immune
1996). However, given the need for more potent cells that accumulate at the site of acute in-
analgesics in treating acute injuries in sports, flammation. In particular, β-endorphin and
physicians lobbied the IOC to change its policy met-enkaphalin have been found by radioim-
regarding opioids. As a result, in 1992, the IOC munoassay in immunocytes at the site of injury
removed both codeine and dihydrocodeine bit- in a rat paw model of acute inflammation (Cabot
artrate from the list of banned substances. It is et al. 2001).
interesting to note that codeine is a prodrug and In animal models, the evidence suggests that
is converted by the liver to morphine, which is part of the anti-inflammatory action of opioids is
the active form of the drug. However, approx- to reduce the release of proinflammatory medi-
imately 8–10% of the population are genetically ators by the axon terminals. Peripheral nocicep-
deficient in the hepatic enzyme needed to make tors are now understood to not only signal tissue
this conversion and thus receive no analgesic injury centrally, but they also act to release pep-
benefit from codeine (Gourlay 1999). As we learn tides in the periphery, such as substance P and
more about opioid physiology, especially with calcitonin gene-related peptide which promote
regard to pain and inflammation, it is likely that inflammatory cell activity at the site of injury.
in the future selective use of opioids will be This axonal reflex to injury is referred to as neuro-
approved to treat athletic injuries. genic inflammation and is also believed to be
There is increased appreciation of the role that responsible for tissue swelling and pain outside
both endogenous and exogenous opioids play the area of direct tissue injury. Excessive release
in controlling not just pain, but inflammation of these proinflammatory substances can lead
following injury. The pharmacological actions to peripheral sensitization of sensory afferents,
of opioids have long been thought to reside which is in part due to an increase in the expres-
exclusively within the CNS. Over the last 10 sion of sodium channels (Fig. 9.1) (Julius &
years, a growing understanding of the peripheral Basbaum 2001). This in turn leads clinically to
effect of opioid medications has developed. All hyperalgesia or an exaggerated response to min-
three opioid receptor subtypes (mu, delta and imally painful stimulation (Woolf & Salter 2000).
kappa) have been isolated on peripheral axon By diminishing the release of these proinflammat-
terminals of small-diameter, unmyelinated sensory peptides from the C-fibre terminals, opioids
ory neurones (nociceptors or C-fibres). The opi- may be important in limiting the volume and
ate receptors are manufactured in the dorsal root extent of such sensitization. In addition, opioid
ganglion and then transported both centrally receptors have been found on immune cells sug-
into the dorsal horn and peripherally to the gesting a mechanism for the effect of morphine
axon terminal. With inflammation, increased on suppressing lymphocyte proliferation and
axonal transport of receptor proteins occurs with diminishing the production of various cytokines
up-regulation of the expression of the receptors including interleukin-1β, an important immune
on the C-fibre nerve terminals (Stein et al. 2001). modulator (House et al. 2001).
Stimulus Representative
receptor
NGF TrkA Fig. 9.1 Schematic diagram of
Bradykinin BK2 the response of nociceptors to
Serotonin 5-HT3 tissue injury. ASIC3, proton
Mast cell or ATP P2X3 receptor; ATP, adenosine
neutrophil H4 ASIC3/VR1 triphosphate; BK2, bradykinin
Lipids PGF2/CB1/VR1 receptor 2; CB1, cannabinoid
Substance Heat VR1/VRL-1 receptor 1; CGRP, calcitonin-gene
P Pressure DEG/ENaC? related peptide; DEG, pressure
Histamine receptors; DRG, dorsal root
DRG cell body
Bradykinin NGF ganglion; ENaC, putative pressure
receptor; H, protons; 5-HT,
Tissue 5-HT serotonin (5-hydroxy-tryptophan;
injury Prostaglandin 5-HT3-serotonin receptor 3; NGF,
ATP H nerve growth factor; PGF2,
GGRP prostaglandin F-2 receptor; P2X3,
substance P purinergic receptor; TrkA,
tyrosine kinase receptor A; VR1,
vanilloid receptor 1; VRL-1,
Blood vessel vanilloid receptor like protein.
Spinal cord (From Julius & Basbaum 2001,
with permission.)
saline) in chronic arthritis patients, both produced

Clinical applications
a significant reduction of pain when compared
Use of intra-articular, preservative-free morphine with saline, and the morphine group had signi-
sulphate has become more prevalent after joint ficantly lower synovial leucocyte counts when
operations such as knee meniscectomy. The goal compared with the dexamethasone group (Stein
is to reduce postoperative pain and inflamma- et al. 1999).
tion and speed recovery. With meniscectomy, In a review by Kalso et al. (1997), 33 random-
the usual recovery time course can last up to 10 ized, controlled trials studying 1500 patients
weeks before resumption of athletic competition. were found comparing intra-articular morphine
In general, the more pain and swelling following following knee surgery with placebo treatments.
surgery or injury, the longer the time to recovery. Dose ranges of the morphine ranged from 0.5 to
In a recent study that had as outcome measures 5 mg and no additional benefit was seen with
(i) time to being pain free, (ii) time before cessa- doses above 1 mg per knee. Overall, the studies
tion of crutches, and (iii) time before return to suggest that there is a prolonged analgesic effect
work, the use of intra-articular morphine with and reduction in consumption of pain medica-
bupivicaine allowed a more than 50% reduction tions. However, various methodological prob-
in average time necessary to reach these end- lems with the study designs make it difficult to
points when compared to intra-articular saline conclude that the use of intra-articular morphine
injection (Rasmussen et al. 1998). The addition of has a significant, clinically relevant effect on post-
methylprednisolone to bupivicaine and free surgical outcomes.
morphine sulphate led to even greater shorten-
ing of the duration before full recovery. Similar
Side effects
findings have been reported following ankle
surgery in athletes (Rasmussen & Kehlet 2000). Side effects associated with short-term opioid use
In comparing intra-articular morphine (3 mg in mainly involve cognition and the gastrointestinal
3 cm3 saline) with dexamethasone (4 mg in 3 cm3 system. The side effects for all of the commonly
Table 9.4 Dosage of currently available opioids.
Morphine equivalent
Generic name dose, oral (mg) Starting dose Usual dosing frequency
Pentazocine 50–200 50 mg QID

(agonist/antagonist)
Propoxyphene 65 50–100 mg QID
Codeine 30–200 30–60 mg QID
Morphine 30 15 mg Q4h
Hydrocodone 10 5–7.5 mg Q4h
Meperidine 200 50 mg Q4h
Hydromorphone 2–4 1–2 mg Q 3–4 h
Fentanyl patch 25 μg/h 72 h
Oxycodone 30 5–10 mg Q4h
Methadone 8–10 2.5–5 mg Q 8–12 h
Levorphanol 4 2 mg Q 6–8 h
Q 3–4 h, every 3–4 h; Q 4 h , every 4 h; Q 8–12 h, every 8–12 h; Q 6–8 h, every 6–8 h; QID, four times a day.
prescribed opioid medications (Table 9.4) are particularly bad combination with opioid med-
essentially similar, although there is a great ications, as it metabolizes to meprobamate, which
degree of variation in the side effects caused by is a barbituate.
various opioid agents for a particular individual. Some individuals experience a mild euphoria
So whereas codeine may cause severe nausea and with the consumption of an opioid medication.
cognitive disorientation for a particular person, This response to opioids may be predictive of
hydrocodone may not. an individual being prone to develop addictive
Cognitively, opioid-naïve individuals may feel behaviours around the use of opioid medica-
disinhibited, with loss of cognitive acuity and tions; however, there is no well designed study
mild to moderate sedation when first taking a to make a definitive statement regarding this
potent narcotic. Usually these cognitive side issue. Of note is the fact that a small percentage of
effects dissipate with continued use. Associated individuals will experience extreme dysphoria,
with the cognitive side of sedation is respiratory to the point of depression, with the consumption
depression, especially in the postoperative set- of opioids. Often this will be accompanied by
ting. This is associated with a shift in the respons- some degree of agitation, both of which resolve
iveness of the respiratory drive to the carbon with cessation of the agent. Finally, prolonged use
dioxide concentration in the lungs, an important of opioid medications can cause reduced libido,
mechanism of respiratory regulation during but this is not usually a major issue with short-
exercise. Although pain is a potent stimulus to term use (Evans 1999).
overcome this opioid effect, use of other agents Gastrointestinal side-effects are extremely com-
to relieve pain, including spinally administered mon. Mild to severe nausea can occur, but the
anaesthetics, can at times lead to the sudden most common problem that uniformly affects
relief of pain and the rapid onset of respiratory individuals taking opioids is constipation. Appro-
depression if the dose of opioid medication is priate measures to increase water and fibre
not reduced. Other medications can act synergis- intake can usually overcome this problem, but
tically with opioids to cause respiratory depres- bowel obstruction can occur if left unattended.
sion, especially agents in the benzodiazepine and Less common problems include excessive sweat-
barbituate class. Carisoprodol is often used as ing, pruritis and urinary retention. Extremely high
a muscle relaxant for acute pain and can be a doses of any opioid, but particularly found with
meperidine, can lower seizure threshold and can becoming an option in many Western nations.
occasionally cause cardiac arrhythmias. However, At the Winter Olympics in Japan in 1998, inter-
this is usually not important with short-term use national exposure came when the acupuncturist
in the setting of injury (Bowdle 1998). Often, the in Nagano offered free treatments to Olympic ath-
most serious physiological side effect in the out- letes and officials, emphasizing that it is a drug-
patient setting from the use of high-dose opioids free way to treat injuries. Even more stunning
is hepatitis due to excessive acetaminophen intake was the near miraculous recovery in response to
found in the combination of short-acting opioids acupuncture by the Austrian, Hermann Maier.
such as oxycodone and hydrocodone. Maier won gold medals in the giant slalom and
Finally, the issue of addiction versus tolerance super G, 3 days following a dramatic fall and
must be raised when discussing the use of opi- injury that occurred during the downhill com-
oids in pain. Tolerance occurs with prolonged petition. Maier mentioned to the press that the
use of opioids uniformly in all patients and is due use of acupuncture to treat his shoulder and knee
to physiological changes in the CNS. Clinically, injuries following the fall helped him to recover
this is expressed as the need to increase the dose so quickly.
of opioid medication to achieve continued anal- Over the last 30 years, a great deal of scientific
gesia. Addiction is a biobehavioural phenomenon evidence has accumulated to substantiate that
and is described as a maladaptive, self-destructive acupuncture stimulation (AP) and electroacu-
activity to continue to obtain and seek more puncture stimulation (EA) have physiological
opioid medications despite progressive deteri- effects that strongly influence the neurohumoral
oration in function and social status. Surveys in systems that modulate pain. The evidence for the
the acute pain population, such as those with release of endogenous opioids with AP and EA
postoperative pain, show that it is extremely goes back to the seminal work of Pomeranz in
rare to see the onset of addictive behaviours animals and Mayer in humans in the early 1970s
with the appropriate use of opioid medications. (Pomeranz & Chiu 1976; Mayer et al. 1977). We
In the chronic pain population, estimates of the now know that acupuncture causes the release of
incidence varies from 3.2 to 18.9% (Fishbain et al. endorphins and enkephalins in the CNS and that
1992). these neuropeptides play a significant role in its
In the future, as we learn more about the effect analgesic efficacy. There is growing evidence that
of opioids on peripheral pain and the inflamma- the descending inhibitory control system also plays
tory transduction system of tissue injury, novel a role in acupuncture analgesia. This involves
methods of treating the pain and inflammation the activation of serotonergic neurones in the
associated with athletic injuries will probably midbrain, that in turn act to inhibit the transmis-
include agents that act on these opioid receptors. sion of nocioceptive information at the level of
Ideally, agents that do not have a significant CNS the dorsal horn (Fig. 9.2). Release of 5-hydroxy
effect could be used to modulate the immuno- tryptamine (5-HTP) in the raphe nucleus of the
inflammatory response to injury. midbrain has been shown with both EA and AP,
and acupuncture analgesia is attenuated with the
injection of a serotonin antagonist such as para-
Acupuncture in acute pain and
cholorophenylalanine (Debreceni 1993).
inflammation
Acupuncture has been shown in animal models
Discussion of the peripheral effects of endogenous to strongly influence the pituitary–hypothalamic
and exogenous opioids would be incomplete system as well. The arcuate nucleus of the
without some mention of the effect of acupuncture ventromedial hypothalamus contains the β-
on pain and tissue injury. The use of acupuncture endorphin-producing cells and lesions of this
by athletes to treat acute injuries is very common nucleus abolishes acupuncture analgesia in rats
in Asia and Eastern Europe and is increasingly (Debreceni 1993). The hypothalamus secretes
PAG
B
Substantia
Fig. 9.2 Schematic diagram C

of pain transmission and
modulation in the central nervous
system. A, nociceptive input into D
the dorsal horn. B, ascending pain
Dorsal horn
pathway via the spinothalamic Raphe
tract with synapse in the
periaquaductal grey area
(PAG) in the mesencephalon. C,
descending, excitatory pathway A
to the raphe magnus in the rostral
medulla. D, the serotonergic,
descending, pain-modulating
tract has an inhibitory action on
the dorsal horn.
β-endorphin into the blood, consistent with the

Clinical applications
elevated blood levels of endorphin found with
both AP and EA. Concurrent with the release of The use of acupuncture for acute injuries has not
β-endorphin, is the secretion of adrenocorticotro- been studied extensively in athletes. However,
phic hormone with acupuncture, which in turn a recent study of rotator cuff tendinitis in sub-
stimulates adrenal secretion of cortisol causing jects with sports-related injuries found that true
a general anti-inflammatory effect (Pomeranz acupuncture needling was significantly superior
1998). Given the previous discussion relative to when looking at both its analgesic effects as
the presence of peripheral opioid receptors on C- well as strength, range of motion and functional
fibres in inflammatory conditions, the elevation scores when compared to a placebo needling
of systemic β-endorphin with acupuncture may control group (Kleinhenz et al. 1999). Treatment
exert both an analgesic and an anti-inflammatory consisted of using a combination of points in the
effect in sports injuries. feet and hands, based on Chinese acupuncture
Recent studies indicate that acupuncture also principles, together with meridian-based local
influences the release of immune-modulating points around the shoulder based on tenderness.
cytokines from the hypothalamus such as Subjects received two 22 min treatments per
interleukin 1β and 6 during experimental models week for 4 weeks and had follow-up assessments
of fever (Son et al. 2002). The rise of blood β- at the end of the treatment period and again at 4
endorphin with acupuncture also influences months. Acupuncture has also shown efficacy in
peripheral cytokine production in the spleen by providing acute pain relief with a single 20 min
causing increases in interferon-γ and reduction treatment for chronic lateral epicondylitis (tennis
of natural killer cell activity (Yu et al. 1998). These elbow) when compared with placebo. A single
early data suggest that acupuncture has physi- treatment was given using only one point near
ological effects that go far beyond the release the fibular head (gallbladder 34) on the leg ipsi-
of endorphins in the CNS, and has important lateral to the elbow pain (Molsberger & Hille
immune-modulating effects that may prove to be 1994). Both of these studies used a placebo needle
important in the recovery from injury. device for the control group, where a blunt
needle presses on the point, but does not pene- Table 9.5 List of prohibited substances and methods
trate the skin. in sports according to the International Olympic
Committee.
In a randomized trial of acupuncture for
osteoarthritis of the knee, significant improve- I Prohibited classes of substances
ment in scores of pain and function were noted A. Stimulants
when compared with standard treatment on B. Narcotics
oral NSAIDs (Berman et al. 1999). In this study, C. Anabolic agents
1. Anabolic androgenic steroids
subjects received 20 min sessions of electroacu-
2. β2-agonists
puncture at 2.4–4 Hz for 8 weeks with outcome D. Diuretics
assessments at 4, 8 and 12 weeks. Finally, in a E. Peptide hormones, mimetics and analogues
meta-analysis of randomized controlled trials of II Prohibited methods
acupuncture for low back pain, it was concluded A. Blood doping
that acupuncture is superior to the various con- B. Artificial oxygen carriers or plasma expanders
trol treatments, but insufficient evidence was C. Pharmacological, chemical and physical
available to state whether it was better than manipulation
placebo needling methods (Ernst & White 1998). III Classes of prohibited substances in certain
In conclusion, acupuncture appears to be a circumstances
A. Alcohol
safe and potentially effective method of treating
B. Cannabinoids
the pain and inflammation of sports-related C. Local anaesthetics
injuries. There is sufficient evidence to suggest a D. Glucocorticosteroids
physiological mechanism of action that involves E. β-blockers
neurohumoral processes that have both a central
and peripheral effect. Better designed and more
specific studies are needed to assess the clinical Anabolic androgenic steroids are prohibited
efficacy of acupuncture in various sports injuries. in Olympic sports and there is no indication or
It is also important to understand how acupunc- exemption to this rule. Since the β2-agonists have
ture might affect human performance in athletic anabolic properties they have been included
competitions. in the list of prohibited substances. Some β2-
agonists like formoterol, salbutamol, salmeterol
and terbutaline are permitted by inhaler only to
Doping issues prevent and/or treat asthma and exercise-induced
It is very important for every sports medicine asthma. Written notification by a respiratory or
practitioner to become familiar with the list of team physician that the athlete has asthma and/
prohibited substances of the IOC (Table 9.5). or exercise-induced asthma, is necessary to the
Relevant to this chapter are sections IB, IC, IIIC relevant medical authority prior to competition.
and IIID. At the Olympic Games, athletes who request
Narcotics such as diamorphine (heroin), meth- permission to inhale a permitted β-agonist will
adone, morphine and related substances are probe assessed by an independent medical panel.
hibited in Olympic sports competitions. On the Local anaesthetics are permitted under certain
other hand, codeine, dextromethorphan, dextro- conditions. Bupivacaine, lidocaine, mepivacaine,
propoxyphene, dihydrocodeine, diphenoxylate, procaine and related substances can be used, but
ethylmorphine, propoxyphene and tramadol are not cocaine. Vasoconstrictor agents may be used
permitted. The sports physician must know the in conjunction with local anaesthetics but only local
content of various medications to avoid using or intra-articular injections may be administered,
prohibited substances. Clearly, the doping rules and only when medically justified. Notification
do not apply in an emergency when the life of an of administration may be necessary where the
athlete may be at risk. rules of a responsible authority so provide.
The systemic use of glucocorticoids is pro- Ceuppens, J.L., Rodriquez, M.A. & Goodwin, J.S. (1982)
hibited when administered orally, rectally or by Non-steroidal anti-inflammatory agents inhibit syn-
intravenous or intramuscular injection. When thesis of IgM rheumatoid factor in vitro. Lancet 1,
52–58.
medically necessary, local and intra-articular Coggeshall, R.E., Zhou, S. & Carlton, S.M. (1997)
injections of glucocorticoids are permitted. Noti- Opioid receptors on peripheral sensory axons. Brain
fication of administration may be necessary where Research 764 (1–2), 126–132.
the rules of a responsible authority so provide. Debreceni, L. (1993) Chemical releases associated with
acupuncture and electric stimulation. Critical Reviews
in Physical Rehabilitation Medicine 5 (3), 247–275.
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randomized controlled trial of piroxicam in the man- & Ragen, S.E. (1977) Prostaglandin regulation of
agement of acute ankle sprain in Australian regular macrophage collagenase production. Proceedings of
army recruits: the kapooka ankle sprain study. the National Academy of Sciences of the USA 74,
American Journal of Sports Medicine 25 (4), 544–553. 4955–4958.
Smith, A.G., Kosygan, K., Williams, H. & Newman, R.J. Walker, R.J., Fawcett, J.P., Flannery, E.M. & Gerrard,
(1999) Common extensor tendon rupture following D.F. (1994) Indomethacin potentiates exercise-
corticosteroid injection for lateral tendinosis of the induced reduction in renal hemodynamics in ath-
elbow. British Journal of Sports Medicine 33, 423–425. letes. Medicine and Science in Sports and Exercise 26
Soll, A.H., Weinstein, W.M., Durata, J. et al. (1991) (11), 1302–1306.
Nonsteroidal anti-inflammatory drugs and peptic Wall, P. (2000) Pain: the Science of Suffering. Columbia
ulcer disease. Annals of Internal Medicine 114, 307– University Press, New York.
319. Wiggins, M.E., Fadale, P.D. & Barrach, M. (1994)
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effects of acupuncture on the lipopolysaccharide- ture treated with corticosteroids. American Journal of
induced fever and expression of interleukin-6 and Sports Medicine 22 (2), 279–288.
interleukin-1β mRNAs in the hypothalamus of rats. Woolf, C.J. & Salter, M. (2000) Neuronal plasticity;
Neuroscience Letters 319, 45–48. increasing the gain in pain. Science 288 (5472),
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Chapter 10
Physical Modalities and Pain Management

JOEL M. PRESS, CHRISTOPHER T. PLASTARAS AND
STEVEN L. WIESNER
therapeutic heat, has the opposite effect on col-

Introduction
lagen extensibility. Cold increases connective
This chapter provides the reader with the funda- tissue stiffness and muscle viscosity, thereby
mentals of various modalities used in the treat- diminishing flexibility.
ment of sports-related injuries. Heat, cold and Based on these various physiological effects,
the use of electrical stimulation may be useful cryotherapy is most commonly used during the
adjunctive components of the rehabilitation first 48 h of acute musculoskeletal injuries such
programme. By understanding the physiological as sprains, strains and contusions (Grana et al.
basis of these modalities, a safe and appropriate 1986). Use beyond the acute phase is justified
treatment choice can be made. One must remem- for continued pain control, muscle re-education
ber, however, that the most effective modality and control of swelling when utilized with com-
used will ultimately depend upon the patient’s pression (Quillen & Rouillier 1982; Sloan et al.
individualized and subjective response to treat- 1988). Contraindications for cryotherapy include
ment. Lastly, and most importantly, the use of ischaemia, cold intolerance, Raynaud’s phenom-
therapeutic modalities is only one component of enon, cold allergy, inability to communicate and
a comprehensive rehabilitation programme. insensate skin (Basford 1998). Care must be taken
when using cold therapy over nerves due to the
potential development of neuropraxia (conduc-
Cryotherapy (cold therapy)
tion block). Recommendations to minimize this
As with heat, in order to safely apply and more complication include limiting ice application to
effectively utilize cryotherapy in the treatment of less than 30 min and protecting any peripheral
sports-related injuries, an understanding of the nerves in the region (Drez et al. 1981).
physiological effects is necessary. In comparison
with heat, cold produces vasoconstriction with
Techniques of application
vasodilatation following reflexively; it causes
decreased local metabolism; and it minimizes Ice packs, iced compression wraps, slushes, ice
enzymatic activity and the subsequent demand massage, ice whirlpools and vapocoolant sprays
for oxygen (Lehmann & de Lateur 1982a; Ork are some methods of cold application (Basford
1982). Cold diminishes muscle spindle activity 1998). Regardless of the method used, there is a
as well as slowing nerve conduction velocity. rapid drop in skin temperature with a delayed
As a result, cold is commonly used for pain effect on muscle. This depends on the amount of
control and decreasing muscle spasticity and overlying subcutaneous tissue, with maximum
muscle guarding (Chambers 1969; Mennell 1975; cooling occurring to a muscle depth of 1–2 cm
McMaster 1982). Cryotherapy, in comparison to (Halvorson 1989). Ice continues to be the safest
204
pain management 205
and most effective method of application. Care 40

ICN
Temperature (°C)
must be taken when using chemical or gel packs
due to the poor control of temperature and risk of 35 SPP
skin irritation should the envelope break and the
chemical come in contact with the individual’s
30
skin (Grant 1964; McMaster et al. 1978; Lehmann
& de Lateur 1982a). Cryostretch and cryokinetics a b c
refer to the use of cryotherapy to facilitate joint 5 10
movement. Decreasing pain and muscle guard- Time after surgery (h)
ing may lead to improved flexibility and muscle
function (Roy & Irvin 1983; Halvorson 1989). An Fig. 10.1 Time–course plot of the change in intra-
articular temperature after anterior cruciate ligament
additional method of cryotherapy involves the reconstruction in the 5°C group. a, low-temperature
use of vapocoolant sprays (fluori-methane and phase; b, temperature-rising phase; c, thermostatic
ethyl chloride), which provide very effective phase; ICN, intercondylar notch; SPP, suprapatellar
cutaneous local anaesthesia and are commonly pouch. (From Ohkoshi et al. 1999, with permission.)
used to treat myofascial trigger points. The use
of cryotherapy in this context promotes normal
muscle resting length by a ‘spray and stretch’ group. Both the cryotherapy groups showed a
technique rather than by cooling the muscle itself triphasic temperature curve with a low temperat-
(Mennell 1975). Fluori-Methane is less explosive, ure phase occurring immediately postoperatively
less flammable and produces less cooling than and lasting about 2 h; followed by a temperature
ethyl chloride (Travell & Simons 1983). Concerns, rising phase; then finally a thermostatic phase.
however, have been raised regarding the destruc- The control group, however, went immediately
tion of the ozone layer by the use of vapocoolant to a thermostatic phase. During the low temper-
sprays, some of which are considered to be ature phase the cryotherapy groups’ suprapatel-
chlorofluorocarbons (Vallentyne & Vallentyne lar pouch temperatures were significantly lower
1988; Simons et al. 1990). than the intercondylar notch temperaturesaboth
Schaubel (1946) showed that the use of ice sites being significantly lower than body temper-
in 345 patients decreased the need for analgesic ature. Only the suprapatellar pouch temperature
medication following assorted orthopaedic oper- remained significantly lower than body temper-
ations, as compared with controls. In a study ature during the thermostatic phase. Although
using both clinical and basic science models, the numbers were not large in this interesting
Ohkoshi et al. (1999) showed that cryotherapy study, it helps link the objective intra-articular
is helpful with pain scores and analgesic use in temperature changes to clinical outcomes (Fig.
postoperative anterior cruciate ligament recon- 10.1). Martin et al. (2001) also found reduced
struction patients. Twenty-one patients under- intra-articular knee temperatures with ice applica-
going reconstructive anterior cruciate ligament tion with compression.
reconstruction were randomized into three In a randomized, controlled study, Konrath
groups: cryotherapy at 5°C, cryotherapy at 10°C et al. (1996) did not find significant differences
and no cryotherapy for the first 48 postoperative in medication usage or range of motion in 100
hours. A temperature probe was placed intraop- postoperative anterior cruciate ligament recon-
eratively in the suprapatellar pouch and the struction patients treated with cryotherapy;
intercondylar notch through arthroscopic por- unfortunately, pain scores were not recorded.
tals. The cryotherapy groups reached 120° of Levy and Marmar (1993) reported less swelling,
knee flexion 4 days sooner than controls. The less pain and better range of motion with the use
10°C group had significantly lower pain scores of cryotherapy in patients following total knee
and analgesic use as compared with the control arthroplasty.
Levy et al. (1997) studied the effect of cryother- risk of frostbite if ice is used directly on the skin.
apy on temperatures in the glenohumeral joint In a review of cryotherapy in sports medicine,
and the subacromial space following shoulder Swenson et al. (1996) deemed cryotherapy as
arthroscopy in 15 patients. They found no signi- ‘effective and harmless’, as few complications
ficant differences in temperatures as compared are reported.
with controls; however, clinical information on
pain scores was not reported. Pain scores were
Contrast baths
reported in a randomized, controlled study of
cryotherapy in 50 postoperative shoulder pati- Contrast baths, which alternate the use of heat
ents done by Speer et al. (1996). The cryotherapy and cold, have been described as a form of
group reported decreased pain frequency and ‘vascular exercise’ due to alternating dilatation
intensity, less need to use medication, better sleep, and constriction of blood vessels. By alternating
less swelling and less pain with shoulder move- cycles of heat and cold, a hyperaemic response
ment. Karlsson et al. (1994) found significantly may by created, thereby improving circulation
improved pain scores with cryotherapy following and assisting in the healing response. Specific
arthroscopic anterior cruciate ligament reconstruc- indications would include improving range of
tion. Similarly, Lessard et al. (1997) also showed motion, controlling swelling and providing pain
decreased pain scores and analgesic use follow- control. Contraindications include those already
ing arthroscopic knee surgery in a randomized, discussed for therapeutic heat and cold, particu-
blinded, controlled study of 45 patients. larly active bleeding and vascular insufficiency.
Cryotherapy has been shown to help pati- A protocol commonly used is as follows (Lehmann
ents with sprained ankles return to activity an & de Lateur 1982a; Halvorson 1989):
average of 5.1 days more quickly (Basur et al. 1 The affected region is submerged in a warm
1976). Hocutt (1981) found that early cryother- bath of 38–43°C for 10 min.
apy returned patients with sprained ankles back 2 This is followed by a cold bath of half ice/half
to activity an average of 15 days earlier when water at 13–18°C for 1 min.
compared with late cryotherapy or heat therapy. 3 A warm bath is then used for 4 min.
Paddon-Jones and Quigley (1997) and Yackzan 4 This is followed by a cold bath for 1 min.
et al. (1984) did not find cryotherapy to be effect- 5 Steps 3 and 4 are then alternated for a total
ive in treating delayed onset muscle soreness. In treatment cycle of 20–30 min.
a study of rats, Fu et al. (1997) found that post- 6 The sequence ends with a cold bath.
endurance training cryotherapy may actually Exercising the area may occur during the heating
be deleterious by causing histological myofibril phase with rest during the cooling phase. A
damage. somewhat different protocol is described by Roy
Merrick et al. (1999) found that 5 h of continu- and Irvin (1983) in which the treatment begins
ous cryotherapy after a crush injury to the triceps and ends with cold immersion. However, it is not
surae of rats reduced biochemical secondary clear that this technique works better than cold
injury compared with no treatment. Ho et al. alone.
(1994) showed that 20 min of cryotherapy on the
knees was enough to reduce arterial blood flow,
Therapeutic heat modalities
soft tissue blood flow and bone uptake. MacAuley
(2001) reviewed 45 textbooks and found consider- In order to better understand the appropriate
able variation in the recommended duration and role for heat therapy, one needs to be aware of
frequency of the use of ice. Although there is no the various modes available. Heat can be trans-
definitive recommendation regarding the dura- ferred to tissue by three methods.
tion of treatment, cryotherapy is typically used 1 Conduction: Direct heat transfer from one
for a period of 20–30 min at a time. There is more surface to another due to direct contact. This
pain management 207
Table 10.1 Physiological effects of heat.
• Vasodilatation of arterioles and capillaries Improved oxygen delivery to tissues

• Increased diffusion across membranes Oedema formation
• Hyperaemia Removal of inflammatory substances
• Increased metabolic tissue demands Decreases muscle spindle sensitivity,
thereby encouraging muscle relaxation
is a form of superficial heat. Examples would substrates. Heat also acts directly on free nerve
include hydrocollator packs and paraffin baths. endings and provides muscle relaxation by
The penetration depth depends on the thickness decreasing the muscle spindle’s sensitivity to
of the subcutaneous tissue. stretch via the gamma system (Lehmann &
2 Convection: Heat transfer due to the movement de Lateur 1990). Inhibitory pathways can be
of air or water across a body surface. This, too, activated by the use of heat modalities with
is a form of superficial heat. Examples would subsequent muscle relaxation. Central processes
include hydrotherapy and fluidotherapy. may also provide for sedation and decreased
3 Conversion: Transfer of heat due to a change in pain awareness. Thus, therapeutic heat assists in
the form of energy. Examples of superficial heat altering the pain–muscle guarding (spasm) cycle
conversion would include radiant energy such as (Fountain et al. 1960).
that produced by infrared lamps. Deep heating, One of the most useful therapeutic effects
also known as diathermy, is due to conversion of heat includes improved collagen flexibility,
through the use of short waves, electromagnetic especially when accompanied by prolonged stret-
microwaves and ultrasound. ching, as well as a subjective decrease in joint
To best utilize therapeutic heat modalities, an stiffness. Lehmann et al. (1970) showed that
understanding of the physiological effects is lengthening of the tendon and decreasing tendon
necessary (Table 10.1). Heating can create changes tension occurred most effectively when the
which are both local and distant, with the far- tendon was loaded in an elevated temperature
field effects being less pronounced. A consensual bath of 45°C as compared with one at 25°C.
response may also be seen whereby heating one Furthermore, only when stretch was applied
part of the body creates an increase in blood in conjunction with heat did lengthening occur
flow in other regions. As heat is applied to a body (Warren et al. 1971, 1976b). There are some stud-
surface, circulatory changes occur which include ies, however, that do not support this. In a small
vasodilatation of the arterioles and capillaries. study of 24 subjects, Taylor et al. (1995) showed
As a result of increased metabolic tissue demands, that heat or cold modality made no significant
there is a subsequent increase in blood flow with difference in hamstring length when used in
the arrival of various leucocytes, improved de- conjunction with a sustained hamstring stretch.
livery of oxygen, increased capillary permeablity Based on the physiological effects of thera-
and hyperaemia. Due to the increased blood peutic heat, indications for heat modalities with
flow, diffusion across membranes occurs more specific attention to the injured athlete include
effectively leading to oedema formation, espe- pain, muscle spasm, contracture, bursitis and
cially during the acute process (Cox et al. 1986). tenosynovitis. Contraindications for heat include
Additional physiological effects include pain peripheral vascular disease, bleeding diathesis,
control through vasodilatation, which, when malignancy, acute trauma, sensory deficits or in
applied during the later stages of healing, leads patients that are unable to communicate about
to improved blood flow through the removal their sensation of pain (Basford 1998). Therapeut-
of pain-causing inflammatory substances such ic heat, like other modalities, can often provide
as bradykinins, prostaglandin and histamine short-term relief, but there is little evidence to
support long-lasting effects. Timm (1994) studied and chemical packs. The major disadvantage of
250 subjects who had persistent low back pain using these devices is limited temperature control.
following an L5 laminectomy in a randomized,
controlled trial. The subjects were randomized
Hydrotherapy
into five groups including: (i) control; (ii) mani-
pulation; (iii) simple home exercise programme;
exercise in water
(iv) supervised exercise programme; and (v)
physical agents, including hot packs, ultrasound Hydrotherapy is a term that can describe two dis-
and transcutaneous electrical nerve stimulation tinct entities: warm water immersion or exercise
(TENS). The physical agent group did no better performed in the water. Warm water immersion
than the control group on the functional Oswestry is discussed below.
scale, but was the most costly of all groups A patient exercising in the water can get
(US$1842 per subject). The exercise groups had the therapeutic benefit of exercise while using
the most improvement in the Oswestry disability the buoyancy principles of water to decrease the
scores and had fewer recurrences of low back biomechanical stresses on the musculoskeletal
pain; the simple home exercise programme was system. The temperature of the water can be
also the most economical (US$1392 per subject). modified to fulfil individual needs. Patients with
acute injuries and pregnant women are typically
treated in cooler pools of 28°C whereas subacute
Superficial heat modalities
or chronic injuries are treated in warmer temper-
The common denominator of superficial heat atures of 33–34.5°C (Konlian 1999). Water exer-
modalities is direct heat penetration. Penetration cises can also be used to cross-train patients who
is greatest within 0.5 cm from the skin surface, require weightbearing restrictions, such as those
depending on the amount of adipose tissue with stress fractures. Buoyancy-assisting devices
(Lehmann et al. 1966; Michlovitz 1986). The more can be used to allow patients to run in water
commonly used modes for sports rehabilitation (cooler temperatures of 29–29.5°C) and maintain
are hydrocollator packs, whirlpools and contrast cardiovascular fitness (Konlian 1999). Oxygen
baths (see above). Other forms of superficial heat consumption of an activity performed in water
include infrared lamps, paraffin baths, fluido- has been shown to be greater than oxygen con-
therapy and moist air. sumption of the same activity done on land
(Cassidy & Nielsen 1992; Fyestone et al. 1993;
Routi et al. 1994). Hall et al. (1996) compared water-
Hydrocollator packs
based exercise, land-based exercise, seated water
Hydrocollator packs serve to transfer heat via immersion and progressive relaxation in 139
conduction. These packs come in three standard chronic rheumatoid arthritis patients in a ran-
sizes and are heated in stainless steel containers domized trial. At 3 months, the water-based
containing water at temperatures between 65 exercise group maintained the most improve-
and 90°C (Griffin & Karselis 1982). After appro- ment in emotional and psychological scales. Post
priate heating, toweling is applied to the packs in anterior cruciate ligament repair patients obtained
order to minimize burning of the skin and to quicker range of motion gains with water-based
maintain heat insulation. The highest tempera- exercise when compared with conventional land-
tures produced by the hydrocollator packs are at based therapy (Norton et al. 1996). It is important
the skin surface. The pack is able to maintain heat to incorporate land-based as well as water-based
for approximately 30 min with treatment sessions exercises together in the rehabilitation programme.
lasting 20–30 min The goal is to prepare the body for function on
Other heating packs are also available and land because most people function in life on the
include hot water bottles, electric heating pads ground and do not live their life in the water.
pain management 209
hand or foot contractures, healed ankle or hand

warm water immersion
fractures, postoperative Achilles tendon recon-
Heating through the use of submersion in water struction and healed elbow dislocations. Paraffin
is a form of convection. Whirlpools are used baths are a mixture of paraffin and mineral oil
when a small area of the body is to be heated, which provide a useful means of delivering heat
such as a part of the upper or lower extremity, to the smaller joints of the body by conduction.
while Hubbard tanks are used to treat larger The addition of mineral oil creates a lower melt-
surface areas. The Hubbard tank, due to its larger ing point for the paraffin and therefore provides
size, also allows for range of motion manoeuvres. increased thermal energy release in comparison
Since larger body areas are exposed to heat dur- with water. The bath mixture is kept at a temper-
ing hydrotherapy, there is an increased risk of ature of 52–58°C for upper extremity use and a
elevation in core body temperature. Therefore, somewhat lower temperature (45–52°C) for lower
water temperature rarely exceeds 40°C for total extremity application (Griffin & Karselis 1982).
body immersion, whereas temperatures as high Two methods of heating are commonly employed:
as 43°C may be used for partial limb immersion. the dip/wrap method and the immersion method.
The benefits of whirlpool treatment stem from With dipping, the extremity is immersed in the
the principle of buoyancy, in which a gravity- bath and then withdrawn after a few seconds,
eliminated environment assists the patient in thereby allowing the wax to harden. This pro-
upward movement. An additional benefit comes cedure is then repeated until a glove of wax has
from the resistance to flow, which provides low been created. Wrapping follows dipping whereby
resistance for muscle strengthening and training. the extremity is enclosed within a plastic or terry
Agitation created by the water flow provides towel wrap to create an insulating effect. The
sensory input to the skin, assisting with pain con- glove is then removed after approximately 20
trol as well as maintaining appropriate water min. The immersion method keeps the extremity
temperature (Hayes 1984). within the paraffin bath for a period of 20–30 min.
As larger areas of the body are immersed in This provides for higher and more prolonged
the heated water, diminished regulation of core tissue temperatures than that created by the dip
body temperature occurs, as sweating and heat and wrap method. Contraindications to paraffin
exchange can only occur in the non-immersed bath use includes patients with open wounds
portions (Lehmann & de Lateur 1990). As an and severe peripheral vascular disease.
area with poor circulation is exposed to heat,
a greater demand for blood supply is created
Fluidotherapy
due to increased metabolic needs. However, this
demand for increased circulation may not be Although infrequently used today, fluidotherapy
adequately met, leading to ischaemic results. may sometimes be used for postoperative hand
Lowering of water temperature may limit such and ankle rehabilitation in conjunction with
adverse effects. The indications and contraindica- manual joint mobilization, scar desensitization,
tions to hydrotherapy are the same as for thera- scar mobilization and active range of motion
peutic heat. exercises. Fluidotherapy involves placement of
the extremity into a container through which hot
air is blown within a medium of dry powder
Paraffin baths
or glass beads (Borell et al. 1977). Treatment pro-
Paraffin baths are used in conjunction with vides both therapeutic heat with its associated
manual joint mobilization, scar desensitization, physiological responses, as well as mechanical
scar mobilization and active range of motion stimulation that may further assist with pain
exercises of the distal upper body or limbs of control. Borell et al. (1980) found that fluidother-
patients. This may include patients who have apy, in comparison with hydrotherapy and
paraffin wax, caused the most significant tem- with the potential for overheating (Lehmann &
perature rise in the joint capsule and muscle. de Lateur 1982b). Significant heating can occur
to depths up to 5 cm below the skin surface,
thereby providing therapeutic effects to bone,
Diathermy or deep heating modalities
joint capsule, tendons, ligaments and scar tissue
Diathermy utilizes the principle of conversion (Santiesteban 1985). In summary, ultrasound pro-
to heat deeper tissues. The most commonly used vides for the deepest penetration of all heating
deep heating agents include ultrasound and modalities since minimal energy is converted to
phonophoresis. Shortwave and microwave dia- heat in subcutaneous fat or muscle with most of
thermy are not used much anymore. Radiant the conversion occurring at the bone interface.
heat is not frequently used any more. The general In addition to the thermal effects, ultrasound
indications and contraindications are similar also has non-thermal effects, which do not relate
to those already discussed for superficial heat. to tissue temperature elevation but rather to
However, specific clinical uses and precautions molecular vibration. Although heat can increase
are presented here. membrane permeability, diffusion can also occur
due to the non-thermal streaming/stirring effect
of fluids created by the ultrasonic field. Gaseous
Ultrasound
cavitation is also a non-thermal ultrasonic event.
Ultrasound is defined as sound waves classified Gas bubbles are created as a result of acoustic
within the acoustic spectrum above 20 000 Hz rarefaction and compression causing subsequent
(cycles per second). It is unique among diathermy enlargement in bubble size and pressure changes
modalities in that the production of heat is due within the tissues. As the gas-filled cavity vibrates
to a high-frequency alternating electric current due to alternating compression and rarefaction,
(0.8–1.0 MHz) which is converted via a crystal surrounding fluid movement occurs with the
transducer to acoustic vibrations, rather than to potential for cell destruction. Cavitation can
electromagnetic energy. Energy transfer occurs be minimized by the application of external pres-
due to the piezoelectric effect whereby the crystal sure and the use of a stroking, rather than a
undergoes changes in shape when the voltage is stationary, technique, which will be discussed
applied. By altering the crystal’s configuration, shortly.
vibrations are created which then pass through
the tissues being treated. The heating effects
application methods
depend on the absorption and reflection of
ultrasonic energy based on the differences in Two primary methods of ultrasound application
the acoustic impedance at the tissue interface. may be used: continuous or stationary. A coup-
Selective heating is greatest when acoustic im- ling medium, such as mineral oil/gel or water
pedance is high, such as at the bone–muscle for irregular surfaces is utilized to ensure ade-
interface. On the other hand, ultrasonic energy is quate transmission of sound energy (Warren
readily conducted through homogeneous struc- et al. 1976a; Griffin 1980; Balmaseda et al. 1986).
tures such as subcutaneous fat or metal implants With the continuous method, the ultrasound
with minimal thermal effects due to the rapid head is moved in a stroking fashion over the area
removal of heat energy. Thus, ultrasound can be being treated. This provides for safer, more uni-
safely used in the presence of metal implants. form heating. The size of the applicator head
However, in the presence of methyl methacry- should be larger than the treatment field with
late and high-density polyethylene, which may common sizes ranging from 5 to 10 cm2. The
be used in total joint replacements, a greater stationary method, as the name implies, does
amount of ultrasound energy will be absorbed not involve the continuous movement of the
pain management 211
applicator head. Since a rapid rise in temperature

musculoskeletal conditions
is produced over a localized area with increased
risk of burning and gaseous cavitation, this method General indications and contraindications for
is less commonly used. When this method is ultrasound use in muskuloskeletal conditions
employed, intensity output is reduced. are the same as for therapeutic heat. Additional
Dosimetry is measured in watts per square precautions include ultrasound over laminectomy
centimetre (W·cm–2), which reflects the appli- sites, the heart, brain, cervical ganglia, tumours,
cator output divided by the surface area of the acute haemorrhage sites, pacemakers, infection
applicator. Intensities of 1–4 W·cm–2 are most sites and fluid-filled cavities such as the eyes
commonly used for the continuous method. (Basford 1998). In general, ultrasound may be
Treatment often begins at 0.5 W·cm–2 and the effective as a therapeutic modality in subacute
total output gradually increases. When using and chronic inflammation (Hayes 1984). Pain
the stationary head, a safe range would be 0.1– control may occur by both thermal and non-
1.0 W·cm–2 (Lehmann & de Lateur 1982b). The thermal effects. Various studies have shown
duration of most treatments is 5–10 min per site alteration in nerve conduction velocity after
based on the size of the treatment area, with 10– diathermy application, with the changes appear-
12 treatments per series (Hayes 1984). As with all ing to be related to energy intensity of the ultra-
therapeutic modalities, the patient’s subjective sound field (Madsen & Gersten 1961; Zankel
response to heating is the best guide for proper 1966; Currier et al. 1978; Halle et al. 1981). By
dosing. altering the conduction velocity, analgesic effects
A variation of the primary technique includes may occur.
ultrasound application under water to more Studies have also documented increased levels
effectively treat irregular surfaces. Care must be of cortisol following ultrasound application to
taken to minimize the development of gaseous peripheral nerves. This release may provide
cavitation over the body part by removing the increased anti-inflammatory effects (Griffin et al.
bubbles formed. Forrest and Rosen (1989) evalu- 1965). However, Gnatz (1989) found that ultra-
ated the effectiveness of heating tendons overly- sound applied to the backs of two patients
ing the lateral epicondyle of a pig by comparing with documented lumbar disc herniation caused
the application of the ultrasound/coupling agent increased pain in a radicular pattern. Thus, any
directly over the limb with limb immersion in pain-relieving effects secondary to cortisol release
a water bath with ultrasound application 2 cm may be overcome by the increased oedema due
from the skin surface. They concluded that the to the deep heating effects of ultrasound. Con-
tendon temperature reached the therapeutic range flicting results have also occurred with the use
when the ultrasound was used directly over the of ultrasound as a diagnostic technique in the
anatomical area rather than when given under evaluation of lumbosacral nerve root irritation.
water. Cole and Gossman (1980) concluded that ultra-
Pulsed application is a method of admin- sound application over an irritated nerve root
istering ultrasound waves whereby the energy provoked pain radiation, providing diagnostically
produced is intermittent. The purpose is to pro- useful results, whereas Reid et al. (1989) con-
duce the mechanical, non-thermal reactions of cluded that due to the low sensitivity, sonation of
ultrasound by allowing for rest periods and the lumbar nerve roots in patients with sciatica
subsequent cooling (Prentice 1986). However, was not useful as a screening test for nerve irrita-
evidence is lacking that the non-thermal effects tion secondary to disc disease.
produced by pulsing have any advantage over The literature is filled with uncontrolled, non-
the similar results produced by the continuous randomized studies that show only modest bene-
method (Lehmann & de Lateur 1982b). fit of ultrasound for musculoskeletal disorders
(Tiidus 1999; Baker et al. 2001; Robertson & Baker of life; however, there was no significant differ-
2001). A closer look at just the randomized, ence at the 9-month follow-up. Interestingly,
controlled studies, however, failed to produce 42% of the ultrasound-treated shoulders demon-
convincing evidence of the efficacy of ultrasound strated resolution of calcium deposits and 23%
(van der Windt et al. 1999). showed improvement. In contrast, the sham
Gam et al. (1998) studied the effects of ultra- group showed calcium deposit resolution in
sound, massage and exercise in 58 patients with only 8% and improvement in only 12% of sub-
neck and shoulder myofascial trigger points in jects (P = 0.002). Perron and Malouin (1997) did
a randomized, controlled study. The first group not, however, find improvement with ultra-
received all three treatments, the second group sound and acetic acid iontophoresis above the
received massage, exercise and sham ultrasound, control for their smaller group of 22 patients
and the third group was a control group receiv- with calcific shoulder tendinitis. Nykanen (1995)
ing no treatment. Both of the treatment groups also found no benefit in using ultrasound over
had significantly improved numbers of myofascial sham ultrasound in 72 inpatients with shoulder
trigger points compared with the non-treated pain in a randomized, double-blinded, sham-
control group, but there was no difference between controlled study. Downing and Weinstein (1986)
the therapeutic ultrasound and the sham ultra- also found no benefit from ultrasound in sub-
sound groups. acromial bursitis in a double-blinded, sham-
Van der Heijden et al. (1999) studied 180 pati- controlled study.
ents with soft tissue shoulder disorders in a Tiidus (1999) reviewed the literature and
randomized, blinded, controlled trial comparing found little data to support the use of ultrasound
bipolar interferential electrotherapy with ultra- for postexercise muscle damage.
sound as adjuvants to a supervised exercise There is some evidence to suggest that ultra-
programme. All 180 subjects received exercise sound may hasten the healing of bone and
therapy; 73 subjects received active treatments, tendon. Kristiansen et al. (1997) studied 61 distal
72 subjects received dummy ultrasound and radius fractures in a multicentre, prospective,
interferential electrotherapy, and 35 subjects randomized, double-blind clinical trial compar-
received no adjuvants. At the 6-week and 12- ing low intensity non-thermal pulsed ultrasound
month follow-ups, the ultrasound and elec- versus a placebo device. The ultrasound group
trotherapy groups had received no additional experienced significantly faster radiographic
benefit above the exercise programme alone. fracture healing (mean of 61 days in the treat-
Crawford and Snaith (1996) found no difference ment group vs 98 days in the placebo group).
between ultrasound and sham ultrasound in Ramirez et al. (1997) performed work with ultra-
patients with plantar heel pain. There is con- sound and Achilles tendon injuries of neonatal
flicting evidence whether ultrasound may be rats to suggest that ultrasound stimulates colla-
beneficial for delayed-onset muscle soreness gen synthesis in tendon fibroblasts and stimu-
(Hasson et al. 1990; Plaskett et al. 1999). lates cell division during phases of rapid cell
Ebenbichler et al. (1999) studied ultrasound growth. Jackson et al. (1991) also found that ultra-
therapy in 54 patients with radiographically sound facilitated the rate of rat Achilles tendon
confirmed calcific rotator cuff tendinitis in a repair by promoting synthesis of collagen which
randomized, double-blinded, sham-controlled also proved to have a greater breaking strength.
study. Thirty-two shoulders were treated with Enwemeka (1989) found similar increased tensile
ultrasound and 29 shoulders were treated with strength in the Achilles tendons of rabbits that
sham ultrasound five times a week for the first were treated with ultrasound.
3 weeks, then three times a week for the follow- Binder et al. (1986) reported statistically signifi-
ing 3 weeks. At 6 weeks, the treatment group cant results studying 38 patients having ultra-
reported greater improvement in pain and quality sound (1 MHz, 1–2 W·cm–2) versus 38 patients
pain management 213
receiving sham ultrasound for lateral epicondy- using 10% hydrocortisone demonstrated better
losis. Twenty-four subjects in the treatment subjective and objective outcomes as compared
group compared with only 11 in the sham group with phonophoresis using 1% hydrocortisone.
reported satisfactory results. Other studies evalu- Klaiman et al. (1998) studied phonophoresis
ating ultrasound as treatment for lateral epi- versus ultrasound in 49 patients with various
condylosis do not show statistically significant soft tissue injuries in a randomized, double-
improvement (Halle et al. 1986; Lundeberg et al. blinded, uncontrolled trial. Each group had
1988; Haker & Lundeberg 1991; Vasseljen 1992; treatments three times a week for 3 weeks; each
Pienimaki et al. 1996). group had decreased pain levels at the end of
Gam and Johannsen (1995) and van der Windt 3 weeks, but there was no significant difference
et al. (1999) reviewed well-designed trials evalu- between the groups.
ating ultrasound therapy and concluded that In summary, ultrasonic energy in conjunction
there is little evidence to show efficacy in the with topical hydrocortisone may produce some
treatment of musculoskeletal disorders. Taking anti-inflammatory effect, possibly related to the
the available literature as a whole, there is evid- use of ultrasound alone and in part as a result of
ence to support improved tendon and bone heal- the penetration of cortisone.
ing and only little evidence suggesting a modest
benefit of ultrasound in rotator cuff calcific ten-
Therapeutic electricity
donitis and lateral epicondylosis.
The use of therapeutic electricity dates back
many centuries. One of the earliest accounts of
Phonophoresis
the use of electricity for a musculoskeletal prob-
Phonophoresis is sometimes used as a thera- lem occurred in 1747 when a man with rheuma-
peutic modality in the rehabilitation of sports toid arthritis and involvement of the small joint
injuries. There are few good controlled studies in his hands received marked relief of his pain
documenting the clinical effectiveness of phono- symptoms through the use of electricity (Licht
phoresis. Griffin showed that it is possible to 1983). Today, different forms of therapeutic elec-
drive a cortisol ointment onto pig skin in situ and tricity are used in the treatment of musculoskel-
to drive it into underlying muscle with ultrasonic etal and sports injuries. Electric currents are used
energy using levels within the clinical range to promote healing of injured tissue, to stimulate
(Griffin & Touchstone 1963). Newman et al. (1958) muscles, to stimulate sensory nerves in treating
reported that hypospray injection of cortisol fol- pain or to create an electrical field on the skin
lowed by local application of ultrasonic energy surface to drive ions beneficial to the healing
showed an improvement in symptoms of shoul- process into or through the skin. This section
der bursitis compared with ultrasound used describes different forms of therapeutic electri-
alone. Davick et al. (1988) demonstrated that city, the scientific basis for their use, their indica-
ultrasonically treated topical application of triti- tions and contraindications, briefly describes the
ated cortisol can lead to significant increases in techniques used in their applications, and elab-
cortisol penetration beyond the stratum corneum orates on their use in sports medicine. Electrical
and into the viable epidermis as compared with devices can put out either alternating current
topical cortisol alone. They concluded that once (AC or faradic), which is the form usually found
beyond the stratum corneum, the cortisol may in household appliances, or direct current (DC
penetrate over time and be absorbed into the or galvanic), which is found in a generator or
deep soft tissue structures. battery. Direct current can be continuous or
In Kleinkort and Wood’s (1975) retrospective intermittent, and can have different waveforms,
study of 285 patients treated for a variety of com- frequencies, duration and amplitudes. Adjust-
mon inflammatory conditions, phonophoresis ments in any or all of these parameters will
have an effect on the quality, type and form of from accumulation of ions in the skin under the
stimulation received by the patient. Details of electrodes, which act as a physiological stimulus
these parameters can be found in the cited texts to the sensory nerve endings, producing reflex
(Prentice 1986). vasodilatation (Marino 1986).
It is important to note that the responses Direct, uninterrupted electric current tends to
muscle and nerve have to electricity vary. Nerve be quite uncomfortable and may cause superfi-
tissue accommodates rapidly to current. Nerve cial skin burns. For this reason, a modification of
stimulation requires a current which rises rapidly the technique has been developed whereby the
to maximum intensity. High frequencies and current is applied in an alternating or ‘pulsed’
short durations are used. Motor nerves respond manner, termed high-voltage pulsed galvanic
to 25 cycles·s–1 and 500 μs or shorter of stimulus stimulation (HVPGS). Although the main use
duration. Sensory nerves respond to 100–150 of HVPGS in sports rehabilitation is for relief of
cycles·s–1 and 100 μs or shorter stimulus dura- pain, it can also be used to aid in tissue healing
tion. Muscle tissue does not accommodate as (Ross & Segal 1981). Electrically induced muscle
rapidly. Muscle can be stimulated with very contraction, such as that obtained with direct
slowly rising currents. Lower frequency and current or HVPGS, can be used to duplicate regu-
longer duration stimuli are used in stimulating lar muscle contractions. These contractions help
muscle as compared with nerve. The various stimulate circulation by pumping blood through
forms of therapeutic electricity include TENS, venous and lymphatic channels after acute
muscle electrical stimulation, percutaneous elec- injuries, when fluid accumulation is signifi-
trical nerve stimulation, iontophoresis and inter- cant. Intermittent muscle contraction, which per-
ferential current. mits increased blood flow, may also produce
relaxation of the muscles. Electrical stimulation
of muscle contractions can allow resolution of
Electrical stimulation to promote tissue
inflammatory fluid, while keeping an injured
healing
joint protected. In order to be successful in redu-
Medical galvanism, or the use of galvanic stimu- cing swelling, the current intensity must be high
lation, uses direct current modalities that deliver enough to provide a strong, comfortable muscle
a unidirectional, uninterrupted current flow contraction, therefore interrupted or surge-type
within the tolerance of the patient and without pulses must be used (Prentice 1986).
the destruction of tissue. The action of direct There are a number of contraindications to the
current on the body is primarily chemical. This use of electrical current in sports rehabilitation.
type of modality can be used to directly stimulate Contraindications of electrical therapy include
muscle following a nerve injury, to produce stimulation over cardiac pacemakers, electrical
ionic changes within the tissues and to decrease implants, carotid sinus, epiglottis, abdomen and
oedema; or it can be used to introduce topically gravid uterus (Basford 1998). Treatment should
applied medications into the skin, when it is be avoided over any area that is anaesthetic to
termed iontophoresis (Hillman & Delforge 1985). avoid local burns. Recent scars in the area to
The purpose of this electrical stimulation is prim- be treated should also be avoided because of
arily for the vasomotor effects, i.e. increased the potential for wound dehiscence. Any area
circulation. These effects are most often seen where metal is embedded close to the skin in
in resolution of inflammation, relief of pain and the area to be treated should be avoided for fear
reduction of interstitial oedema through electro- of concentrating the heat source at the metal sur-
osmosis and the shifting of water toward the face. Any form of electricity should be avoided
electrical cathode (Prentice 1986). Motor nerves near an area of acute injury if active bleeding
are not stimulated by a steady flow of direct stimu- is still present to prevent worsening of the
lation. The sensations experienced result in part haemorrhage.
pain management 215
Without a control group, however, it is not known

Iontophoresis: driving ions with
whether these encouraging results are from treat-
electrical stimulation
ment effect or the natural course of heel pain.
Iontophoresis uses direct current to drive Perron and Malouin (1997) did not, however,
medicinal ions locally into the skin and mucous find improvement with ultrasound and acetic
membranes. Ions of the medicinal compounds acid iontophorosis above the control in their
are absorbed subcutaneously. This absorption small group of 22 patients with calcific shoulder
occurs slowly into the local soft tissue, while tendinitis. Gudeman et al. (1997) studied 0.4%
some is ultimately absorbed systemically. Evid- dexamethasone iontophoresis in the treatment
ence for penetration much beyond the skin is of 40 feet with plantar fasciitis in a randomized,
variable and may depend on the particular sub- double-blinded, placebo-controlled trial. After
stance (O’Malley & Oester 1955). James et al. six treatments over 2 weeks, the treatment group
(1986) showed that percutaneous iontophoresis significantly improved, but were no different than
of 1% prednisolone sodium phosphate through placebo at the 1-month follow-up. Taniguchi et
human skin and nails gives peak plasma levels of al. (1995) reported a significantly increased pain
about one-third that produced by oral ingestion threshold in 30 healthy volunteers with clonidine
of 10 mg prednisolone. Similarly, Zankel et al. iontophoresis, as compared with amitriptyline
(1959) showed that the absorption of the negative and imipramine iontophoresis; the clinical impli-
ion I through unbroken skin only occurred in cations of this finding are not known. Hasson et
those conditions which included iontophor- al. (1992) studied 18 females with delayed-onset
esis. Bertolucci (1982), in a double-blind study, muscle soreness with dexamethasone iontophor-
found that patients below the age of 45 years esis, placebo iontophoresis and no treatment.
with shoulder dysfunction related to primary Perceived muscle soreness was significantly less
tendonitis responded well to iontophoresis ster- in the treatment group 48 h later, but no change
oid administration, whereas the placebo group in strength was noted.
received no benefit from the iontophoretic treat- The clinical effectiveness of iontophoresis is
ment with sodium chloride. However, Chan- still debatable. Some of the claimed benefits for
traine et al. (1986), in studies done both in pain relief may be due to the effects of the direct
vivo and in vitro failed to demonstrate the trans- current used as opposed to the medicinal com-
cutaneous migration of corticosteroids with pounds purportedly driven into the circulation.
iontophoresis. Few side effects have been described other than
Iontophoresis has been used to drive multiple drug sensitivity and sensitive skin.
substances into the skin, some of which include
calcium chloride, hydrocortisone, lithium chlor-
Electrical stimulation of muscle
ide, lidocaine and acetic acid. Acetic acid theor-
etically replaces carbonate in calcium carbonate Electrical stimulation of muscle is accomplished
to become calcium acetate, which is blood sol- with either direct or alternating current, or a
uble, thereby leaching the calcium away from the combination of the two. Alternating current is
site of bony spur and inflammation. Japour et al. usually preferred to direct current because of
(1999) reported very encouraging results using greater patient comfort (Hillman & Delforge
acetic acid iontophoresis in 35 patients with 1985). Muscles are stimulated for one of four
chronic heel pain in an uncontrolled case series. reasons. The first is to aid in muscle pumping
Ninety-four per cent of patients reported relief of for oedema reduction and tissue healing as
heel pain, after an average of only 5.7 sessions, described in the previous section. The other
over an average 2.8-week treatment period. Pain reasons include re-educating muscle, retarding
scores decreased from 7.5 to 1.8, which continued atrophy in immobilized or partially denervated
to be low at 0.64 at the 27-month follow-up. muscle and enhancing strength.
Certain general principles need to be adhered (Fleury & Lagasse 1979) and in the abductor
to when performing electrical stimulation of hallicis (LeDoux & Quinones 1981).
muscle (Stillwell 1982). Good contact should be
maintained between the skin and the electrodes.
retardation of muscle atrophy
The active electrode should be placed over the
motor point of the muscle. The two electrodes Electrical muscle stimulation may help prevent
used should generally be placed on the same side strength losses (Eriksson & Haggmark 1979;
of the body. Finally, since denervated muscle does Godfrey et al. 1979; Gould et al. 1979; Grove-
not have a motor point, the active electrode may Lainey et al. 1983; Morrissey et al. 1985;
be placed at the point that gives the best motor Wigerstad-Lossing et al. 1988; Delitto et al. 1989;
response, or the two electrodes may be placed one Snyder-Mackler 1990; Abdel-Moty et al. 1994),
at each end of the muscle so that the current will as well as prevent muscular atrophy (Eriksson
pass through the muscle and stimulate all of it. & Haggmark 1979; Morrissey et al. 1985; Nitz
& Dobner 1987; Wigerstad-Lossing et al. 1988),
which occur when a limb is immobilized. Stanish
muscle re-education
et al. (1982) and Eriksson et al. (1981) have shown
Electrical muscle stimulation can be used for that the biomechanical changes occurring in
muscular re-education after sports injuries the muscles of immobilized limbs are retarded
(Amrein et al. 1971). Muscular inhibition is quite by electrical muscle stimulation. Eriksson and
common after traumatic injuries or surgery. Haggmark (1979) showed better muscle function
Central nervous system inhibition is often the in a group of patients after reconstruction of the
cause, as muscle contraction causes pain. This anterior cruciate ligament when treated with
then causes decreased contraction and ultimate electrical muscle stimulation and isometric exer-
immobilization of the affected muscle. The cise than with isometric exercise alone. However,
injured patient or athlete may have a difficult Halbach and Straus (1980) examined isokinetic
time initiating contraction of an injured muscle only and electrical stimulation only exercise pro-
because of the pain associated with movement grammes and found that the isokinetic workload
and the lack of sensory input from that muscle was greater than the electrical stimulation work-
due to disuse. Forcing the muscle to contract load after 3 weeks of training and stimulation.
causes an increase in the sensory input from the In general, it is agreed that electrical muscle
muscle, allowing the patient to see the muscle stimulation programmes are more effective than
contract, and then attempt to duplicate this mus- no exercise programme, but no more effective
cular response (Prentice 1986). The focus of this than traditional strengthening exercise pro-
type of training is on kinetic training and the grammes (Currier et al. 1979; Halbach & Straus
sensory awareness of muscular contraction. For 1980; Kramer & Mendryk 1982; Currier & Mann
muscle re-education to occur, the current intens- 1983; Kramer & Semple 1983; Laughman et al.
ity must be adequate for a muscle contrac- 1983; McMiken et al. 1983; Kubiak et al. 1987;
tion, but not too uncomfortable for the athlete. Lieber et al. 1996). Snyder-Mackler et al. (1995)
HVPGS or high-frequency alternating current showed there may be some functional benefit
may be most effective (Prentice 1986). Although from using high-intensity muscle stimulation in
the clinical implications are not clear, electrical addition to an exercise programme. They studied
muscle stimulation has been shown to selectively 110 patients following anterior cruciate ligament
increase strength when applied to the abdominal reconstruction and randomized them to receive
muscles (Alon et al. 1987), triceps brachii (Snyder- high-intensity neuromuscular electrical stimula-
Mackler et al. 1988) and erector spinae (Kahanovitz tion, high-level volitional exercise, low-intensity
et al. 1987). Improved motor performance was neuromuscular electrical stimulation, or com-
demonstrated in the deltoid and pectoralis major bined high- and low-intensity neuromuscular
pain management 217
95 current, the placement of the stimulating elec-

trode, the duration and number of treatment
sessions, the rest periods between the treatment
75
sessions and the resting length of the muscle dur-
ing stimulation. Further discussions of all these
Extension (degrees)
Involved knee
55 parameters are beyond the scope of this chapter,
but are well described by Licht (1983). Gibson
et al. (1988) suggest that electrical stimulation
35 seems to prevent the fall in muscle protein syn-
thesis that is related to immobility. Cabric et al.
(1987) found that lower frequency electrical stimu-
15
lation (50 Hz) of muscle increased muscle fibre
size, which was thought to be correlated to the
−5 proliferation of muscle cell nuclei.
0 50 100
Stance phase (%)
muscle strength gains
Fig. 10.2 Graph of the kinematics of the knee in the
sagittal plane, showing a lack of extension of the Increasing the strength of a muscle can be accom-
involved knee during stance. (From Snyder-Mackler plished by repeated maximal or submaximal
et al. 1995, with permission.) contractions of that muscle. The rationale behind
the strength enhancement is that electrical stimu-
stimulation in addition to a standard closed lation can either increase the maximum contrac-
kinetic chain strengthening programme. At 4 tile force in the muscle, or that it can recruit more
weeks, the high-intensity stimulation group fibres to contract with a given stimulus, thereby
enjoyed the best quadriceps strength gains of enhancing the strength of contraction (Singer
70% of the uninvolved side, as opposed to 57% et al. 1989). When done via electrical stimulation,
in the high-level volitional exercise group. With tetanic contractions, which are achieved at pulse
knee joint kinematic analysis, the high-intensity rates above 20–30 per second, are required for
stimulation group showed significantly more maximum muscle contraction. Electrical stimula-
normal knee flexion–extension sagittal plane tion is achieved by stimulating the motor nerve
excursions during the stance phase when com- to a muscle by means of electrodes placed on
pared with the other groups (Fig. 10.2). How- the skin. Most of the research done with muscle
ever, long-term benefits and other functional stimulation for strength gains has been done
outcomes were not studied. with electrical stimulation in the isometric mode.
In order to improve strength under any circum- Because of the many variables of stimulation
stances, either electrically stimulating muscle or of muscleaincluding frequency, duration, pulse
through voluntary contraction, maximal or near shape, intensity and chargeano studies exist that
maximal contractions must occur to the point of compare the effectiveness of these variables in
muscle fatigue. The discomfort of the stimula- inducing effective strength-improving muscle
tion remains a major limitation (Currier 1991). contractions (Singer et al. 1989).
Most research to date indicates that, with few Significant strength gains in normal muscles
exceptions, maximal contractile forces can be have been described by Kots (1977). Kots’ ‘Russian’
produced by voluntary contractions (Singer et al. stimulation used an alternating-type current of
1989). high pulse rate and high intensity to produce
Also, while electrical stimulation retards de- strong, involuntary muscle contractions with
nervation atrophy, its effect depends on the pulse associated stimulation of local blood flow (Hillman
duration, the frequency and intensity of the & Delforge 1985). The actual benefit of such a
programme is questionable as similar results large-diameter afferent nerve fibres are electrically
have not been duplicated. To date, there are no stimulated, painful stimuli arriving at the spinal
good studies to warrant electrical stimulation for cord through small fibres at the dorsal horn are
gaining strength in normal muscle. blocked from transmission to the central nervous
There has also been some suggestion that system where pain is perceived. By stimulating
neuromuscular electrical stimulation can help the large fibres, the ‘gate’ to allowing further
in controlling oedema after injury (Gould et al. impulses to be transmitted centrally is closed.
1979; Lake 1989; Griffin et al. 1990). Hsueh et al. The central biasing theory also uses the idea of
(1997) studied 60 patients with upper trapezius gating impulses. In this model, intense stimula-
myofascial trigger points in a randomized, tion of smaller fibres (C fibres or pain fibres) at
placebo-controlled trial. They found electrical peripheral sites, for short periods, causes stimu-
muscle stimulation significantly improved im- lation of the descending neurones, which then
mediate cervical range of motion over the placebo affects transmission of pain information by clos-
and electrical nerve stimulation groups. The elec- ing the gate at the spinal cord level (Prentice
trical nerve stimulation group, however, showed 1986).
significantly decreased immediate pain scores The opiate pain control theory is premised
when compared with the other two groups. Pope on the fact that endogenous opiate enkephalins
et al. (1994) showed no statistical difference in and β-endorphins exist in our systems. Electrical
physical measures in a randomized trial of 164 stimulation of sensory nerves may stimulate
patients with subacute low back pain who received the release of these compounds from local sites
3 weeks of electrical muscle stimulation, manual throughout the central nervous system, causing
manipulation, massage or corset wearing. pain relief.
In summary, the literature suggests that elec-
trical muscle stimulation may be helpful in
transcutaneous electrical nerve
strengthening normal muscle, preventing loss
stimulation (tens)
of muscle bulk and strength associated with
immobilization, selective strengthening, enhan- TENS is usually defined as the application of
cing motor control and controlling oedema after an electric current therapy through the skin to
injury (Lake 1992). a peripheral nerve or nerves for the control of
pain (Singer et al. 1989). TENS units are very
commonly used in sports rehabilitation (Roeser
Electrical stimulation of nerves
et al. 1976). There are a number of advantages
The use of alternating and direct current for pain of using TENS, including that it is comfortable,
reduction via nerve stimulation is commonly fast-acting, can be used in many types of pain
used in the rehabilitation of sports injuries. The problems, and can be used continuously. The
goal of nerve stimulation is to stimulate sensory disadvantages are that the carry-over is often
nerves to change the patient’s perception of a variable and adaptations may need to be made
painful stimulus coming from an injured area. for continued benefit, i.e. increasing the pulse
Nerves, being more sensitive to electric current width or amplitude.
than muscle, are usually stimulated at a high fre- There are two major forms of TENSahigh
quency and short duration. Three theories have frequency and low frequency. High-frequency
been put forward to explain the analgesic effects TENS stimulates sensory nerves and causes an
of electrical stimulationathe gate-control theory, increase in pain threshold, although it does
the central biasing theory and the opiate pain not stimulate the release of endorphins. Low-
control theory. frequency TENS will cause pain relief, which
Melzack and Wall (1965) proposed the gate- can be blocked by administration of opiate
control theory in 1965. It postulates that when antagonists, implicating the opiate theory of pain
pain management 219
control. It is sometimes likened to acupuncture. Deyo et al. (1990a) studied 145 volunteers with
Walsh et al. (1995) found that low-frequency chronic low back pain in a randomized trial com-
TENS (4 Hz) was the best in decreasing immedi- paring four groups: active TENS, sham TENS,
ate pain visual analogue scores for ischaemically active TENS with exercise and sham TENS with
induced pain in a randomized, double-blinded, exercise. At 8 weeks following the 4-week treat-
controlled trial of 32 subjects comparing 4 Hz ment period, there were no significant differ-
TENS, 110 Hz TENS, placebo and no treatment. ences between the active TENS groups and the
When applying electrodes for either type of sham TENS groups.
TENS, electrodes may be placed on or around the Marchand et al. (1993) studied 43 patients with
painful area, over specific dermatomes, myotomes chronic low back pain in a randomized sham
or sclerotomes that correspond to the painful TENS (placebo) and no intervention (‘nocebo’)
area, close to the spinal cord segment that inner- controlled study. Immediately after two treat-
vates an area that is painful, or over trigger or ments of 30 min each, the active TENS group
acupuncture points. showed a 43% reduction of pain intensity as com-
The efficacy of TENS is not clear-cut (Licht pared with a 17% reduction in the sham TENS
1983; Robinson 1996). Although it has been argued groupathis finding was statistically significant.
that blinding for TENS studies may be difficult Active TENS patients maintained significantly
to truly achieve (Deyo et al. 1990b), few studies decreased pain intensity scores at 1 week as com-
have been done in a double-blind manner (Gersh pared with sham TENS patients. Both sham and
1978; Robinson 1996). Thorsteinsson et al. (1977) active TENS groups’ pain intensity scores were
studied 93 patients with various disorders in significantly better than the no treatment group
a double-blind, randomized, sham-controlled, at the 3- and 6-month follow-ups, but there was
cross-over study. Forty-nine per cent of the TENS no statistically significant difference between the
group versus 32% of the sham group reported sham TENS and active TENS groups.
partial or complete pain relief, but this difference Herman et al. (1994) studied 58 work-related
was not statistically significant. acute low back injuries of 3–10 weeks duration in
Ordog (1987) studied 100 patients with acute a randomized study of active TENS versus sham
traumatic disordersaincluding sprains, fractures TENS. Both groups received the same exercise
and contusionsain a randomized study compar- programme. Outcome measures showed the active
ing four groups: active TENS plus acetaminophen/ TENS group produced a drop in visual analogue
codeine, sham TENS plus acetaminophen/ pain scores immediately after TENS but showed
codeine, active TENS and sham TENS. Pain no difference in disability, return to work rates or
levels in 2 days dropped 63% in the active TENS pain scores at the 4-week follow-up.
plus drug, 58% in the sham TENS plus drug, 45% Jensen et al. (1985) showed that a group of
in the active TENS, and 17% in the sham TENS patients treated with TENS following arthro-
groups. There was no statistical difference be- scopic surgery experienced less pain, required
tween the active TENS and the sham TENS plus less narcotics and regained strength more
drug groups suggesting that TENS may be as quickly than the control group. Sluka et al. (1998)
effective as acetaminophen/codeine for acute showed that high-intensity TENS was more
traumatic disorders. effective in providing immediate pain relief than
Lehmann et al. (1986) studied 54 patients with low-intensity TENS for induced knee pain fol-
chronic low back pain in a randomized study lowing injection.
of active subthreshold TENS, sham TENS or elec- Some studies have shown that TENS may pro-
troacupuncture. They found that although all vide short-term relief for delayed-onset muscle
groups improved from baseline, there were no soreness (Denegar & Huff 1988; Denegar et al.
statistically significant differences between the 1989; Denegar & Perrin 1992), but others have not
groups at 6 months. (Craig et al. 1996). TENS can also be helpful for
postoperative pain (Smith et al. 1983; Cornell et al.

percutaneous electrical nerve
1984; Jensen et al. 1985; Arvidsson & Eriksson
stimulation (pens)
1986; Carrol & Badura 2001).
Overall, clinical experiences seem to show that PENS combines the therapeutic effects of TENS
TENS appears to give the best benefit in the treat- and electroacupuncture by placing small-gauge
ment of early postoperative pain or pain from needles (32 gauge) 2–4 cm into soft tissues and
acute injuries; however, the response can be vari- muscles in a dermatomal distribution, with
able, unpredictable and short lived. There are no subsequent stimulation with electrical impulses
good studies to prove the benefits of TENS in (< 25 mA) at a frequency of around 4 Hz. Ghon-
chronic pain problems. It appears that TENS is ame et al. (1999b) investigated the efficacy of
not harmful, may sometimes provide pain relief PENS. They studied 60 patients with stable
above the placebo response, is more effective in chronic non-radicular low back pain from radio-
acute pain relief with short-term benefit, and is graphically confirmed degenerative disc disease
more effective at higher stimulation intensities in a randomized, single-blinded, sham-controlled,
(Robinson 1996). cross-over study. Each subject received all of the
No serious complications have been observed following four treatments in a randomized
from the use of TENS (Licht 1983). Hypersensi- order: sham PENS, PENS, TENS and exercise.
tivity of the skin has been observed in up to 10% Sham PENS consisted of needle placement but
of patients, either due to the electrode or the elec- no electrical stimulation. Exercise only consisted
trode jelly. Minor burns were observed when of one exercise where the patient performed
high-frequency stimulation and high-intensity spinal flexion and extension while sitting in a
stimulation were used at the same time. TENS chair. At 24 h, the PENS group showed signifi-
should not be used in patients with pacemakers, cant improvements on pain, activity, sleep, sense
stimulation should not be applied over the of well being and narcotic usage scores as com-
carotid sinus, and it should probably not be used pared with the other three groups. Ninety-one
during pregnancy, as the effects are unknown per cent identified the PENS treatment as the
(Singer et al. 1989). preferred pain therapy and 81% identified it as a
treatment for which they would be willing to pay
extra. Ghoname et al. (1999a) also found that a
interferential current
stimulus frequency of 15–30 Hz is more effective
Interferential current is another type of electrical than 4 or 100 Hz.
stimulation that is used to control pain. Electric There are numerous potential uses of thera-
signals from two sets of electrodes with the same peutic electricity in the rehabilitation of sports
waveform are applied so that they arrive at injuries. The most common indications are for
the point to be stimulated from two directions. stimulation of muscle to retard atrophy, to aid
The area where the current overlaps is called the in tissue healing and muscle re-education, the
interference pattern, and the intensity summates stimulation of nerves for pain modification, and
in a manner that can be effective in modifying to drive ions through the skin for their medicinal
pain (Singer et al. 1989). The frequency obtained effects (Table 10.2).
at the interference pattern, through cancellation
of some waveforms, allows stimulation of local
Traction
muscle and nerve at a greater depth than if
applied only from the surface at that point. Thus, Traction is the technique in which a distractive
interferential current uses high-frequency carrier force is applied to a part of the body to stretch
circuits to afford deeper penetration. The main soft tissues and to separate joint surfaces or bone
use of interferential currents in sports is for pain fragments (Hinterbucher 1985). Cyriax popular-
reduction. ized traction in the 1950s as a treatment for
pain management 221
Table 10.2 Types of therapeutic electricity and typical uses.
• Alternating current or faradic stimulation Muscle re-education

• Direct current or galvanic stimulation Retard muscle atrophy
• High-voltage pulsed galvanic stimulation Improve muscle strength
• Iontophoresis Pain control
• Transcutaneous electrical nerve stimulation Pain control
• Percutaneous electrical nerve stimulation Pain control
• Interferential current Pain control
lumbar disc lesions. Prior to that, traction was the patient for a few minutes to see what kind of
mainly used in the treatment of fractures. Over therapeutic response they can expect with traction.
the years, traction has gained some popularity in To achieve separation of the spinal segments,
the field of sports rehabilitation, particularly a force of significant magnitude and duration
with respect to cervical and lumbosacral spine must be exerted. Traction can be delivered
injuries. manually, through weights and pulleys or via a
mechanical device. The direction of pull can be
vertical, horizontal or at an angle. Traction can be
Cervical traction
performed while the patient is standing, sitting,
Cervical traction is used for a number of types lying on a horizontal or inclined plane, or in the
of injuries of the cervical spine including cer- prone or supine position. Traction can be con-
vical herniated nucleus pulposus, radiculopathy, tinuous, sustained, intermittent or intermittent/
strains, zygapophyseal joint syndromes and myo- pulsed. Surface resistance to traction is depend-
fascial pain. The main reason for its use is relief ent on the weight of the body or body segment
of pain. Pain relief may occur through one of undergoing traction and the size, quality, con-
several mechanisms, including rest through im- tour and texture of the two surfaces in contact
mobilization and support of the head, distrac- (Hinterbucher 1985).
tion of the zygapophyseal joints and associated With cervical traction, the optimal angle of
improved nutrition to the articular cartilage, pull to obtain the most distractive force with
tightening of the longitudinal ligament and the least weight is at 20–30° of head flexion (Fig.
decreasing the intradiscal pressure. The last two 10.3). The supine position may be more effective
both press a bulging disc more centrally, reliev- than sitting, as it allows more relaxation. In the
ing nerve root pressure via increased foraminal supine position the force must be sufficient
diameter, improving head posture, and elongat- enough to overcome friction and must have a
ing muscles to improve blood flow and reduce pull that is at least half the weight of the head;
spasm. 3.6–4.5 kg is a usual starting point. In sitting,
Determination as to whether the patient has the pull must be sufficient to support the head;
any contraindications is the first step in admin- usually 11–18 kg is necessary.
istering traction of the cervical spine. Contrain- Cervical traction can be continuous or inter-
dications to the use of spinal traction include mittent. Continuous traction will allow quieting
an unstable spine, ligamentous instability, verte- of the stretch reflex and decrease muscle guard-
brobasilar artery insufficiency, atlantoaxial instab- ing. It will also allow separation of the posterior
ility, rheumatoid arthritis, osteomyelitis, discitis, structures (zygapophyseal joints) if maintained
neoplasm, severe osteoporosis, untreated hyper- for at least 7 s at a time. Intermittent traction is
tension, severe anxiety, cauda equina syndrome believed to act by cyclically causing muscle con-
and myelopathy (Rechtein et al. 1998). Clinically, traction and relaxation, thereby increasing blood
the examiner can first try manual traction with flow in a ‘massage-like’ action.
Fig. 10.3 Cervical traction

mechanical unit.
Goldie and Landquist (1970) carried out a great amount of force necessary to obtain separa-
blind study of patients with cervical pain, using tion of even a small amount in the lumbar spine
traction, exercise and control groups. Results (Frazer 1954; Lawson & Godfrey 1958). Therefore,
showed no difference between the three groups, clinically, lumbar traction functions to limit the
although there were a somewhat larger number activity of the patient. It may assist to decrease
of improved patients among those who were muscle spasm by forcing rest. There is no evid-
subjected to traction. Zylbergold and Piper ence that lumbar traction facilitates nuclear
(1985) studied 100 patients with disorders of the migration of the disc.
cervical spine in a randomized, controlled trial Lumbar traction is set up in a similar manner
comparing static traction, intermittent traction, to cervical traction except that a corset rather
manual traction and no traction. At 6 weeks, all than a head halter is used. Various types of
groups improved significantly compared with lumbar traction are described including gravity
baseline, but the intermittent traction group inversion traction, gravity lumbar reduction and
scored significantly better than the no traction autotraction. Inversion traction must be avoided
group in pain and cervical range of motion meas- in patients with hypertension or retinal problems
ures. Swezey et al. (1999) showed that 81% of because of the potential for increasing blood and
their 58 patients with cervical spondylosis had retinal pressures. Generally, at least one-quarter
symptomatic relief with home cervical traction in of the bodyweight must be used just to overcome
a retrospective, uncontrolled study. the friction of lumbar traction. The maximum
force that a patient can tolerate is often used
(Hinterbucher 1985).
Lumbar traction
Although ample experimental evidence that a
The traction load necessary to produce vertebral traction force of sufficient magnitude and dura-
separation in the lumbar spine is much greater tion applied to the spine produces separation
than that required to produce vertebral separation of the vertebrae and zygapophyseal joints and
in the cervical spine. De Seze and Levernieux increases the size of the foramen, no clear sci-
(1951) estimated that a tractive force of 330 kg entific evidence of its therapeutic value has been
was required to obtain a separation of 1.5 mm at reported in the few controlled studies to date
the L4/5 vertebral level and that 365 kg were (Hinterbucher 1985). Christie’s (1955) controlled
required to obtain a separation of 2 mm at the study of traction in the treatment of acute and
L3/4 level. Numerous other studies discuss the chronic lumbar painawith and without root
pain management 223
signsashowed that traction, when effective, was (United Nations Environment Programme 1987).
most useful in patients with chronic backaches The mechanism of action of possible therapeutic
with root signs. Weber’s (1973) double-blinded, effects is unknown (Blank & Findl 1987; Ayr-
controlled study of patients with sciatica from a apetyan et al. 1994). Increased peripheral blood
prolapsed disc treated with traction or simulated flow has been proposed as a mechanism of action
traction failed to show any significant difference by Erdman (1960), Fenn (1969) and Ross (1990).
in pain, mobility of the lumbar spine or the pres- The increased blood flow may also be associated
ence of neurological signs in either group. with changes in fibroblast concentration, fibrin
Beurskens et al. (1997) studied 151 patients with fibres and collagen at wound sites (Goldin et al.
non-specific low back pain in a randomized, 1981). Other postulates include blockage of
sham-controlled trial which showed no differ- action potentials (McLean et al. 1995), the role
ence between the treatment and control groups. of water (Carpenter & Ayrapetyan 1994), reson-
Van der Heijden et al. (1995) reviewed only ance, ions, induction, subatomic magnetic field
randomized clinical trials studying traction. interactions, and closed electrical circuits within
Beneficial effects of lumbar traction were sug- endothelium (Hazlewood & VanZandt 1995).
gested in only three of 14 randomized studies Pulsating electromagnetic field therapy has
and in only one of the 11 studies that the authors shown some promise in the treatment of osteo-
considered to be of better quality. They concluded arthritis of the knee and spine (Miner & Markoll
that there was no evidence to support or refute 1993; Trock et al. 1994). Trock et al. (1994) studied
the use of traction. 86 subjects with knee osteoarthritis and 81 sub-
Although hard data supporting the use of jects with cervical spondylosis in a random-
traction are not available, many clinicians and ized, double-blinded, placebo-controlled trial. The
patients will speak of its benefits. Some of these group treated with pulsating electromagnetic
positive experiences may be related to enforced fields (10–20 G) showed significant changes from
bed rest or the effects of some active intervention baseline at a follow-up interval of 1 month; this
for their back complaints. Cheatle and Esterhai change was not seen in the placebo group. Foley-
(1990) surveyed 369 orthopaedic surgeons and Nolan et al. (1992) studied the use of pulsat-
165 physiatrists about their use of pelvic traction. ing electromagnetic therapy in acute whiplash
Twenty-eight per cent of the responding physi- syndrome in a double-blinded, randomized,
cians said they would prescribe traction; the controlled study. Twenty patients wore active
chief rationale (54% of respondents) of this pre- pulsed electromagnetic therapy collars and 20
scription was to ensure bed rest. Similarly, there patients wore placebo collars for 8 h·day–1. The
are a lack of scientific data that traction is not treatment group had statistically significant im-
physiologically sound or even harmful. proved visual analogue scales at 2 and 4 weeks
compared with placebo. Pujol et al. (1998) ran-
domized a small group of 30 patients to receive
Magnetic therapy
40 min of real or sham current magnetic coil
Magnetic therapy has been used for pain relief stimulation over localized tender body regions.
for centuries and is replete with anecdotal suc- Postprocedure pain scores decreased by 59% in
cesses. The strongest scientific evidence in sup- the treatment group versus only 14% in the sham
port of the therapeutic use of magnetic fields groupathis finding reached statistical significance.
in treating musculoskeletal disorders involves Non-union fracture rate healing can be im-
using pulsating magnetic fields of strengths over proved with pulsating high magnetic fields
10 G. The World Health Organization reported (O’Connor et al. 1990; Bassett 1994). Sharrard
that there is no available evidence to show ad- (1990) studied electromagnetic therapy in the
verse effects on humans exposed to static mag- treatment of delayed union tibial shaft fractures
netic fields up to 2 T, which is equal to 20 000 G using active electromagnetic stimulation units
in 20 patients versus dummy control units in 25 6 Pulsating high magnetic fields may be helpful
patients. Nine subjects in the treatment group in osteoarthritis and bone healing, but there are
and only three subjects in the control group few data to support the use of static magnets for
showed union of the fracture, which was a stat- musculoskeletal disorders.
istically significant finding. 7 Modalities may be used as an adjunct to the
There are fewer studies to support the use of rehabilitation of musculoskeletal injuries. There
static magnets placed over the skin of the affected are no definite scientific data to strongly support
areas. Washnis (1998) cites a multitude of studies their use, certainly not as a primary treatment
using static magnets, but few have been random- option. They may, however, help to decrease pain
ized, double-blinded, placebo-controlled trials and oedema to allow an exercise-based rehabili-
appearing in peer-reviewed journals (Vallbona tation programme to proceed.
& Richards 1999). No controlled studies have
been conducted in an athletic population.
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Chapter 11
Flexibility and Joint Range of Motion

MARTIN SCHWELLNUS
ranges of motion are present in females com-

Introduction
pared with males, and in younger compared
Musculoskeletal injuries form a large propor- with older individuals (Nicholas 1970). Other
tion of the injuries reported by athletes (Wang causes for hypermobility are an increased mus-
et al. 1993). There are many potential causes for culotendinous unit temperature (Wessling et al.
these injuries and these include muscle strength 1987; Anderson & Burke 1991) and, in some
imbalances, muscle fatigue, biomechanical abnor- instances, after injury or surgery, significant leng-
malities, incorrect training methods and muscu- thening of soft tissue structures can also result in
loskeletal inflexibility (Burkett 1970; Burry 1975; abnormally increased joint range of motion.
Cooper & Fair 1978; Zarins 1982; Agre 1985). The use of stretching techniques as a means
A decrease in musculoskeletal flexibility has of treating hypomobility is widely advocated, as
been associated with both the aetiology of these a means of preventing injuries, as well as form-
injuries, as well as a consequence of these injuries ing an important component in the design of a
(Nicholas 1970; Glick 1980; Toft et al. 1989; Wang rehabilitation programme following injury or
et al. 1993). Furthermore, it has been documented surgery (Cureton 1941; Weber & Kraus 1949; De
that flexibility training (stretching), using a variety Vries 1962; Nicholas 1970; Cahill & Griffith 1978;
of techniques, effectively increases musculo- Cooper & Fair 1978; Glick 1980; Beaulieu 1981;
tendinous unit (MTU) range of motion in human Wiktorsson-Moller et al. 1983; Hardy 1985; Etnyre
subjects (De Vries 1962; Tanigawa 1972; Medeiros & Abraham 1986; Williford et al. 1986; Toft et al.
et al. 1977; Henricson et al. 1984). 1989; Zachazewski 1990; Worrell et al. 1991, 1994).
Because there are established guidelines as to A number of health professionals are therefore
the norms for musculotendinous unit flexibility involved in the prescription of flexibility training
for most joints or groups of joints (Janda 1983; in the primary and secondary prevention of
Kendall & McCreary 1983; Travell & Simons injuries in athletes. These professionals include
1983; Clendaniel et al. 1984), range of motion sports physicians, physiatrists (rehabilitation
testing can reveal values that exceed the normal medicine practitioners), orthopaedists, physical
(hypermobility), or are less than the normal therapists, rehabilitation workers, physical edu-
(hypomobility or inflexibility). Hypermobility cators, athletic trainers, coaches and athletes.
will not be discussed in detail in this chapter. This chapter focuses on the role of flexibility
However, the causes for hypermobility are largely training in the rehabilitation of injuries. After
genetic. Also, there are instances where hyper- a brief review of definitions and terminology
mobility is related to certain athletic activities, pertaining to flexibility training, the general
such as gymnastics or ballet dancing (Grahame benefits of flexibility training and the pathophysi-
& Jenkins 1972). In addition, in general, larger ology of loss of range of motion after injury will
232
flexibility and joint range of motion 233
be briefly reviewed. Techniques for the meas- Measurement of joint range of motion is thereby
urement of flexibility, and the physiology of an indirect measure of the extensibility of the
stretching will be discussed. A scientific basis tissues that have an influence over that particular
for stretching will be presented, and practical joint. Joint range of motion is thus a functional
guidelines for the implementation of a flexibility measurement and not a measurement of the
training programme during rehabilitation will physical dimensions of the muscle or the length
be provided. of the musculotendinous unit (Toppenburg &
Bullock 1986). Measurements of the joint angle
provide an ‘index’ of musculotendinous unit length
Terminology and definitions
or flexibility (Bullock-Saxton & Bullock 1994).
The literature uses a variety of terms when flexi- For the purposes of this chapter, the term flexi-
bility training is discussed. It is therefore neces- bility will be used to indicate an increase in joint
sary to define these terms at the beginning of this range of motion.
chapter in order to clarify what will be referred Flexibility in the musculotendinous unit is
to in the text that follows. A summary of the directly related to tension in that musculotendin-
terminology and definitions used is depicted in ous unit (Starring et al. 1988; Taylor et al. 1990).
Table 11.1. Tension in the musculotendinous unit is made
The terms ‘musculotendinous unit length’, up of both a passive component and an active
‘joint range of motion’ and ‘musculotendinous component (Taylor et al. 1990). The passive com-
unit flexibility’ are often used interchangeably. ponent lies in the connective tissue while the
Flexibility can be defined as the range of motion active component lies in the reflex activity of the
available in a joint or in a group of joints that is muscle. The passive, connective tissue compon-
influenced by muscles, tendons and bones ent has both viscous and elastic properties and
(Anderson & Burke 1991). Flexibility has also therefore behaves in a viscoelastic fashion when
been described as the degree to which muscle subjected to a tensile force (Fung 1967; Ciullo
length permits movement over that which it & Zarins 1983; Herbert 1988; Taylor et al. 1990;
has an influence (Toppenburg & Bullock 1986). Kwan et al. 1992).
Table 11.1 Definitions and terminology.
Term Description
Flexibility The range of motion in a joint or in a group of joints that is influenced by muscles,
tendons and bones
Flexibility training A training programme that is aimed at increasing the range of motion of specific
joints or groups of joints (stretching programme)
Elasticity The property in tissues that refers to the return of the tissue to its original length
when the force is removed
Viscous The property in tissues that refers to the elongation of a tissue that remains once
the force applied to it is removed
Viscoelastic A tissue that exhibits both viscous and elastic properties
Extensibility The ability of a tissue to elongate
Stiffness The ratio of the change in stress (force per unit area) and the change in length (strain)
Stress relaxation The decline in tissue tension that results when a tissue is lengthened and then held
at that constant length
Creep The change in length of a tissue in response to a load that is applied and then
maintained at that constant magnitude
Hysteresis The change in length of a tissue in response to a load that is applied in a cyclic fashion
The elastic component of viscoelasticity implies and is then held at that constant length. The force
that length changes in the musculotendinous or stress in the tissue, which will gradually
unit are directly proportional to the loads imposed decline over time, is known as stress relaxation
on the musculotendinous unit (Halbertsma & (Taylor et al. 1990). In living soft tissue, this rela-
Goeken 1994). This is well described in Hooke’s tionship is non-linear (Fung 1967; Herbert 1988;
model of a perfect spring (Burns & MacDonald Taylor et al. 1990; Kwan et al. 1992). Generally, the
1975; Sapega et al. 1981; Taylor et al. 1990). Elasticity elasticity of living tissue is characterized by a
implies the ability of a structure to stretch when a very small stress even when it is subjected to a
force is applied to it, and then to return to the large strain. When this stress begins to rise, how-
original length when the force is removed. Extensi- ever, it does so rapidly and exponentially (Fung
bility and stiffness comprise elasticity (Cavagna 1967). Because the tension in the musculotendin-
1970; Halbertsma & Goeken 1994). Extensibility ous unit, when it is stretched, decreases over
refers to the ability, in this case of the musculo- time, the tissue exhibits viscous behaviour, and
tendinous unit, to lengthen. Stiffness refers to the because there is still a degree of tension present
ratio of change in muscle length to the change in it also exhibits elastic behaviour (Taylor et al.
muscle tension (Halbertsma & Goeken 1994). 1990).
Therefore, high stiffness implies a greater resis- When the musculotendinous unit is placed
tance to stretch. Thus, flexibility is comprised of under a constant force, the musculotendinous
two componentsatension and stiffness (Fung 1967; unit responds by lengthening in a viscous way.
Stromberg & Wiederheilm 1969; Herbert 1988). This implies an irreversible increase in musculo-
In muscles, flexibility can also be defined as the tendinous unit length. The deformation in the
point where tension first develops in the muscle musculotendinous unit occurs up to a point
when it is stretched passively. Stiffness is the where the increase plateaus at a new length. This
ratio between tension and the amount of leng- is known as ‘creep’ (LaBan 1962; Kottke et al. 1966;
thening. Stiffness can therefore also be defined Fung 1967; Warren et al. 1976; Taylor et al. 1990).
as the slope of the stress–strain curve (stress = Prolonged, low load stretching of the musculo-
tension/cross-sectional area; strain = change tendinous unit results in more viscous deforma-
in length/initial length) (Burns & MacDonald tion than short, high load stretching (LaBan
1975). The greater the stiffness, the steeper the 1962; Kottke et al. 1966; Fung 1967; Warren et al.
slope of the stress–strain curve. 1976).
The viscous component of viscoelasticity is When a musculotendinous unit is stretched, it
both rate change-dependent and time-dependent may not return to its original length or natural
(Taylor et al. 1990). The rate of deformation is state because of its deviation from an ideal elastic
directly proportional to the applied force. This is substance (Starring et al. 1988). When the loads
illustrated by Newton’s hydraulic piston known or stretches applied to the musculotendinous
as a dash pot (Burns & MacDonald 1975). The unit are cyclic, it becomes possible to predict
connective tissue in the musculotendinous unit the deformation to the musculotendinous unit.
responds as a viscoelastic material where the This is known as ‘hysteresis’ (Fung 1967). The
ground substances, collagen and elastin, which effect of hysteresis is progressive, and further
comprise the connective tissue, determine this changes can be expected with repeated stretch-
response (Sapega et al. 1981; Starring et al. 1988). ing (Starring et al. 1988).
The relationship between length and tension, Flexibility of the musculotendinous unit can,
which changes with time as stretch is applied, therefore, also be defined by the amount of exten-
implies viscoelasticity in the musculotendinous sibility and stiffness in that musculotendinous
unit (Herbert 1988). unit (Halbertsma & Goeken 1994). The degree to
Stress relaxation occurs in viscoelastic substances which the flexibility of the musculotendinous
when the tissue is stretched to a specified length unit increases when a stress or stretch is applied
to it, is determined by its viscoelasticity (Herbert before injury, compared to relatively stiff joints
1988). The viscoelasticity of the musculotendin- (Klafs & Arnheim 1981). It is important to con-
ous unit allows for stress relaxation, creep and sider independently whether increased flexi-
hysteresis to occur in that musculotendinous bility reduces the risk of new injuries (primary
unit, when forces are applied at varying magni- prevention) or reinjury (secondary prevention).
tudes, durations and repetitions (Kottke et al. The scientific evidence for each of these two pos-
1966; Fung 1967; Warren et al. 1976; Starring et al. sibilities will now be briefly reviewed.
1988; Taylor et al. 1990). Musculotendinous unit
flexibility is also described as musculotendinous
does flexibility training decrease
unit length and joint range of motion (ROM). The
the risk of injuries?
parameter, which is physically measurable, is
joint ROM and this term will therefore be used A number of authors have proposed that
to describe musculotendinous unit flexibility. An decreased flexibility results in musculotendin-
increase in joint ROM will indicate an increase in ous unit injuries (Liemohn 1978; Ekstrand &
musculotendinous unit flexibility of the muscu- Gillquist 1982; Ekstrand et al. 1983; Worrell et al.
lotendinous unit, which directly affects the joint 1991). It has been reported that hamstring
ROM (Anderson & Burke 1991; Toppenburg & flexibility was decreased in a group of injured
Bullock 1986). athletes compared with a non-injured group
participating in the same sport. Athletes with
decreased ROM are more likely to suffer from
General benefits of flexibility training
musculotendinous unit tears than their flexible
Athletes and trainers commonly perform flexi- counterparts (Nicholas 1970; Worrell et al. 1991).
bility training as part of regular training and in It has also been suggested that muscle inflexi-
preparation for competition. It is also an integral bility may predispose athletes to certain injuries
part of most rehabilitation programmes follow- (Ekstrand & Gillquist 1982; Ekstrand et al. 1983).
ing injury or surgery. The general benefits of These investigations were conducted on soccer
flexibility training are usually cited as decreas- players, where the incidence of injuries was
ing the risk of injury (primary and secondary related to measures of flexibility. In a more
prevention), decreasing muscle soreness and recently published prospective study in military
improving sports performance. Evidence that recruits, increased hamstring flexibility was
flexibility training does benefit the athlete will related to a decrease in the overall incidence
now be briefly reviewed. (% injuries in 13 weeks) (flexible group = 16.7%,
control group = 29.1%) of injuries (Hartig &
Henderson 1999).
Decreased risk of injury
However, there are studies that do not show
Flexibility training is routinely recommended to that increased flexibility reduces the risk of injury.
increase ROM and thereby to reduce the risk of An early study on badminton players showed
injury (Liemohn 1978; Glick 1980; Ekstrand & flexible players did not report less injuries than
Gillquist 1982; Ciullo & Zarins 1983; Ekstrand their inflexible team-mates (Henricson et al. 1983).
et al. 1983; Zachazewski 1990; Beaulieu 1991). The More recently, in a well-conducted randomized
rationale behind this recommendation is that prospective study, pre-exercise stretching did
musculotendinous units possessing greater flexi- not reduce lower limb soft tissue, bony or all-
bility are less likely to be overstretched, lessening injury risk in military recruits (Pope et al. 2000).
the likelihood of injury (Bryant 1984). It has also However, the stretching protocol used in this
been stated that increased flexibility decreases study group (one static stretch of 20 s prior to
the risk of injury, because flexible joints can training) may not have been sufficient to increase
withstand a greater amount of ‘stress of torque’ ROM.
60 of stretch was 5 min during the first 22 h post-

Cumulative injury
incidence (%)
50 exercise. Other reports of stretching to reduce
40
DOMS are purely anecdotal (Noakes 1992). Some
30
20 authors report that musculotendinous units that
10 are flexible before being subjected to vigorous
0 exercise, suffer less from DOMS than musculo-
1 (high) 2 3 4 5 (low) tendinous units that are inflexible before exercise
Quintiles of flexibility (Noakes 1992).
Fig. 11.1 The relationship between flexibility and the In a study conducted by Buroker and Schwane
cumulative incidence of lower extremity injuries in (1989), subjects stretched for a total time of 45
male military recruits. The relative risk of injury for min on the first day after exercise and for 25 min
quintile 1 compared with 3 was 2.2 (P < 0.05). on the second and third days, respectively.
McGlynn et al. (1979) stretched their subjects for
a total time of 10 min on the first day and for
Furthermore, a recently published compre- 20 min on the second and third days, respect-
hensive review of the literature has failed to pro- ively. Neither of the studies found a decrease in
duce strong evidence of a direct link to increased DOMS with the addition of stretching. Buroker
flexibility and a reduction in injuries (Shrier and Schwane (1989) mention that this may have
& Gossal 2000). Data from military populations been due to their stretch being held for too long.
seem to indicate that both increased flexibility as None of the above results proves that stretch-
well as reduced flexibility is related to increased ing is effective in alleviating DOMS. It is clear
risk of injury (Jones & Knapik 1999). The relation- that the conditions under which DOMS is de-
ship between injury risk and flexibility may well creased by stretching need to be investigated and
be a U-shaped curve with increased risk in both defined.
extremes (Fig. 11.1).
Despite these conflicting reports, stretching is
Improved performance
still widely advocated and used by sportspersons
and clinicians. In particular, the use of flexibility Improved athletic performance may be another
training to restore normal ROM following injury potential benefit of increased musculotendinous
or surgery is still sound clinical practice. How- unit flexibility (Bosco & Komi 1979; Godges et al.
ever, more studies are required to define the 1989; Zachazewski 1990; Noakes 1992; Wilson
precise role of flexibility training in the preven- et al. 1992; Norris 1993; Worrell et al. 1994). Indeed,
tion of injuries in sport. in Borms (1984) it has been suggested that a
limited ROM can reduce work efficiency. Two
possible explanations are given for the positive
Decreased muscle soreness
association between increased flexibility and
Muscle soreness, which follows vigorous or enhanced performance.
unaccustomed exercise, is known as delayed- The first explanation is that musculotendinous
onset muscle soreness (DOMS). Stretching has unit flexibility is necessary in order for a limb
been advocated as a method to decrease DOMS to move through its full ROM. This is a given
(De Vries 1962; Liemohn 1978; Bryant 1984; prerequisite for optimal performance (Ciullo &
Zachazewski 1990; Anderson & Burke 1991; Zarins 1983; Borms 1984; Shellock & Prentice
Norris 1993). Despite the widespread belief that 1985). The second explanation is that flexibility
stretching decreases DOMS, there are few studies training could reduce musculotendinous stiff-
to verify this. ness and enhance rebound performance (Wilson
De Vries (1962) reported a chronic reduction of et al. 1992). Mechanical work is absorbed by the
DOMS with repeated stretching. The total time series elastic component of the musculotendinous
unit during eccentric contraction and is stored (McKenzie 1985). Imbalance at the joints is the
as potential energy. This energy is then available result of one musculotendinous unit at a joint
for use during the subsequent concentric con- being either significantly weaker or significantly
traction (Cavagna 1970; Bosco & Komi 1979). less flexible than the other musculotendinous
Two studies have been conducted which units at that joint (Kendall & McCreary 1983).
investigate the effect of stretching on musculo-
tendinous unit performance (Wilson et al. 1992;
Summary
Worrell et al. 1994). Wilson et al. (1992) imple-
mented a static stretching programme twice Numerous authors, trainers and athletes advocate
weekly for 8 weeks in the pectoral musculo- the use of stretching to increase musculotendin-
tendinous unit complex. At the end of this time, ous unit ROM. The benefits of an increase in
the bench press performance of the subjects musculotendinous unit ROM are commonly
had improved significantly. Worrell et al. (1994) reported. These include decreased risk of mus-
determined the effect of hamstring stretching on culotendinous unit injury, decreased DOMS,
hamstring musculotendinous unit performance. enhanced performance, avoidance of joint dys-
The subjects stretched 5 days a week for 3 weeks. function, joint imbalance and scar tissue forma-
Static stretching and proprioceptive neuromus- tion, and increased general relaxation and well
cular facilitation (PNF) stretching were included being. There is, however, a paucity of scientific
as stretching methods. The results showed that research data to substantiate these postulated
both methods of stretching increased muscu- positive effects of flexibility training.
lotendinous unit flexibility. Selective torque There is some evidence that indicates that ath-
measurements were significantly improved for letic performance may be enhanced by increased
eccentric and concentric contractions of the ham- musculotendinous unit ROM. There is also an
string musculotendinous unit in both groups. association between decreased injury prevalence
It can be concluded that there is some scientific and increased musculotendinous unit ROM. By
evidence that increased flexibility enhances mus- all accounts, there are few, if any, negative side
culotendinous unit performance. This is most effects if stretching is implemented correctly.
probably because of the attainment of optimal Therefore, the use of stretching to increase mus-
ROM and the reduction of musculotendinous culotendinous unit ROM is likely to continue to
unit stiffness. Stored elastic strain energy is be supported by therapists, coaches and athletes.
thereby utilized well during musculotendinous
unit contractions.
Pathophysiology of soft tissue
contracture following injury
Other benefits of stretching
The biology of soft tissue repair following injury
Other reported benefits resulting from increased or surgery has been discussed in detail in Chap-
musculotendinous unit ROM are numerous. ters 3–5. However, in the context of flexibility
They include muscle relaxation (De Vries 1962), training as part of normal rehabilitation follow-
avoidance of skeletal dysfunction (Starring et al. ing injury or surgery, a brief review of the mech-
1988; Bullock-Saxton & Bullock 1994), prevention anisms associated with soft tissue contracture
of scar tissue formation in the musculotendinous is appropriate. A decrease in range of motion
unit’s shortened position (Reilly 1992) and pre- following injury and repair can be the result of a
vention of imbalance at the joints (Herbert 1988; number of mechanisms (Table 11.2).
Bullock-Saxton & Bullock 1994). Skeletal dys- The healing process in soft tissues follows a
function can be defined as the syndrome that is a continuous process consisting of four interwoven
result of prolonged incorrect biomechanical usage phases: immediate reaction to trauma (0–60 min),
of the joints that comprise the skeletal system acute inflammatory phase (0–72 h), repair phase
Table 11.2 Mechanisms responsible for decreased Excessive wound contraction can lead to contrac-
range of motion in soft tissues following injury or tures, which can result in decreased soft tissue
surgery.
flexibility. A detailed discussion on the control of
Increased fibrosis within the scar wound contraction is beyond the scope of this
Wound contraction chapter but has recently been reviewed (Nedelec
Immobilization et al. 2000).
Nerve root tension
Decreased tissue temperature
Increased age Other factors
Following an injury, a decrease in musculotendin-

ous unit flexibility may also be associated with
(2–42 days) and the remodelling phase (21 days other factors. These include: (i) increased nerve
to 1 year). During the late part of the inflamma- root tension (Gadjosik 1991); (ii) increased age
tory and early part of the repair phase, fibroblast (Norris 1993; Booth et al. 1994) and obesity
accumulation is evident in the wound (Wahl & (Norris 1993); (iii) decreased musculotendinous
Renström 1990). The repair process follows and unit temperature (Rigby 1964; Sapega et al. 1981;
is characterized by recruitment of fibroblasts, Norris 1993); and (iv) immobilization or pro-
proliferation of fibroblasts, collagen and matrix longed usage in a limited ROM (Herbert 1988;
synthesis, and later, tissue remodelling. Starring et al. 1988).
Increased fibrosis within the scar Measurement of flexibility

In normal tissue repair, matrix generation is The measurement of musculotendinous unit
self-limiting and minimal scar tissue formation flexibility is of importance in both the laboratory
occurs. However, in some wounds, scar tissue and in the clinical examination room. A brief
formation may become excessive. This process of discussion on the basic method that is used to
increased fibrosis may result from: (i) increased measure musculotendinous unit flexibility is
numbers (proliferation and recruitment) of col- therefore needed. Musculotendinous unit flexi-
lagen-synthesizing cells; (ii) increased matrix bility refers to its functional length (Toppenburg
synthesis by existing cells; (iii) deficient collagen & Bullock 1986), and represents the degree to
degradation; and (iv) continued collagen syn- which it permits a movement over which it has
thesis (Wahl & Renström 1990). In addition to a an influence (Bullock-Saxton & Bullock 1994). In
larger volume of fibrous tissue, the fibrous tissue clinical practice, the ROM of a joint or a group of
can also form adhesions and interfere with the joints is usually measured and then compared
normal function of adjacent tissue. with the normal values expected for a specific
population. It is also useful to measure the ROM
prior to starting flexibility training, in order to
Wound contraction
assess changes objectively. Practically, a clinical
Wound contraction refers to the inward move- test of flexibility will be done by a clinician who
ment of the wound edges by the action of cells will position a limb or a body segment, and then
known as myofibroblasts (Martinez-Hernandez gradually move the segment to an end point.
& Amenta 1990). It is postulated that myofibro- For example, a number of anatomical positions
blasts are derived from mesenchymal stem cells have been used to assess hamstring musculo-
or from perivascular cells. They appear at the tendinous flexibility. These include: (i) flexion at
wound site 3–4 days after the injury and become the hips in standing (Gadjosik et al. 1993); (ii)
prominent 6–7 days after the injury. Their con- extension of the knee with the hip flexed to 90°
traction can reduce wound size by up to 70%. while lying in the supine position (Gadjosik &
Lusin 1983; Gadjosik et al. 1993); and (iii) the The EMG detection of the end-point is the
straight leg raise (SLR) method (Fahrni 1966; most repeatable measurement of the end-point
Breig & Troup 1979; Goeken 1991, 1993; Gadjosik of the flexibility test (intratester correlation
et al. 1993; Cameron et al. 1994). The SLR method coefficient = 0.99) (Hughes 1996), and is recom-
is commonly used because it is relatively easy mended for research studies. The most repeat-
to measure (Janda 1983; Kendall & McCreary able clinical method of assessing end-point is
1983) and evidence indicates that it is a clinically the end-feel by the tester (intratester correlation
acceptable form of measurement (Gadjosik 1991; coefficient = 0.95). This method is recommended
Gadjosik et al. 1993). The SLR method has been for testing end-range in a clinical setting.
proven as a reliable, albeit indirect, measure of
hamstring musculotendinous unit flexibility
Physiology of stretching
(Gadjosik 1991; Gadjosik et al. 1993).
A number of methods have been used to Stretching implies that a force applied to the
determine the end-point for a clinical range of tissue elongates the tissue. The physiological
motion measurement. These include: (i) patient effects that stretching has on the musculotendin-
sensation of the end of range (as a tolerable, ous unit include neural effects (Beaulieu 1981;
uncomfortable, but not painful sensation) (Goeken Reilly 1992; Norris 1993; Vujnovich & Dawson
1991); (ii) subjective tester determination of 1994), plastic (viscous) effects (Sapega et al. 1981;
end-feel (Cyriax & Cyriax 1983; Maitland 1991); Starring et al. 1988) and elastic effects (Starring
(iii) the start of joint movement as felt by the et al. 1988; Taylor et al. 1990). The physiology of
tester (Bullock-Saxton & Bullock 1994; Hanten each of these effects is discussed briefly.
& Chandler 1994); (iv) measurement of resistance
to movement through objective force measures
Neural effects of stretching
(Gadjosik 1991); (v) the objective use of cine-
matography to measure a limb angle (Bohannon There are three reflexes that primarily control the
1982); and (vi) the use of the electromyogram neural effects of stretching. These are the stretch
(EMG) to objectively detect a sudden spike in reflex, inverse stretch reflex, and perception and
neuromuscular activity (Moore & Hutton 1980; control of pain by the Pacinian corpuscles.
Bohannon 1984; Condon & Hutton 1987; Kirsch When a stretch is applied to the musculotendin-
et al. 1993; Chequer et al. 1994). The repeatability ous unit, the first reflex evoked is the stretch
of the various measures of end-point in testing reflex. The origin of this reflex is situated in the
hamstring flexibility was evaluated recently in a intrafusal and extrafusal fibres of the muscle
controlled laboratory-based study. The repeat- spindle (Beaulieu 1981; Etnyre & Abraham 1986;
ability of the four common tests is depicted in Reilly 1992; Norris 1993; Vujnovich & Dawson
Table 11.3. 1994). The stretch reflex serves as a protective
measure by causing a reflex contraction of the
muscle to prevent overstretching of the muscu-
Table 11.3 The intratester repeatability of four lotendinous unit. The magnitude and rate of
common methods of assessing the end-point in contraction elicited by the stretch reflex in a
hamstring range of motion testing (Hughes 1996). musculotendinous unit are proportional to the
magnitude and rate of the stretch that is applied
Correlation
Test of end-point coefficient to that musculotendinous unit (Beaulieu 1981;
Matthews 1993). Both static and ballistic stretch-
Subject (patient sensation) 0.86 ing evoke a response in the stretch reflex when
Tester end-feel 0.95 the end-point of ROM is reached (Beaulieu 1981).
Knee bend 0.73
One method of observing the stretch reflex is
EMG spike 0.99
through the EMG device (Moore & Hutton 1980;
Condon & Hutton 1987). In this method, the stretch inputs can cause long-term changes in levels of
reflex causes a spiking of the neural activity, neuronal excitability and thereby, indirectly, on
which is reflected by measuring EMG activity. flexibility (Vujnovich & Dawson 1994). There-
The inverse stretch reflex applies both to fore, musculotendinous units that are exposed
prolonged contraction and stretching of the mus- to repetitive stretching demonstrate increased
culotendinous unit (Beaulieu 1981; Anderson & tolerance to the manoeuvre, resulting in an
Burke 1991). This reflex is responsible for pre- apparent increased ROM.
venting prolonged increased strain of the mus-
culotendinous unit, caused either by powerful
Plastic and elastic effects of stretching
active contraction or by overstretching of the
musculotendinous unit (Beaulieu 1981; Etnyre & Plastic deformation within the musculotendinous
Abraham 1986; Anderson & Burke 1991). The ori- unit has largely been ascribed to changes which
gin of the inverse stretch reflex is located in the occur in the non-contractile elements within the
Golgi tendon organ (GTO), which is comprised musculotendinous unit (Cavagna 1970; Sapega
of receptors situated in the musculotendinous et al. 1981; Vujnovich & Dawson 1994). The
junction of the musculotendinous unit. The GTO non-contractile elements (ligaments, tendons,
causes a dampening effect on the motor neuronal capsules, aponeuroses and fascial sheaths) are
discharges, thereby causing relaxation of the predominantly comprised of connective tissue.
musculotendinous unit by resetting its resting Connective tissue is made up of collagen fibres
length (Beaulieu 1981; Reilly 1992; Norris 1993; which vary in spatial arrangements and are
Vujnovich & Dawson 1994). This usually occurs of varying densities and strengths (Sapega et al.
6–20 s after commencement of the stretch (Norris 1981). The non-contractile element of the muscle
1993). tissue is also comprised of a connective tissue
The third reflex of the musculotendinous unit framework, which is responsible for its resistance
originates in the Pacinian corpuscles that are to stretch (Sapega et al. 1981). Scar tissue and
located throughout the musculotendinous unit. adhesions are also comprised of connective tissue
The Pacinian corpuscles serve as pressure sensors, (Sapega et al. 1981). Prolonged stretching results
and assist with the regulation of pain tolerance in in plastic elongation of the connective tissue
the musculotendinous unit (Beaulieu 1981; Reilly (Sapega et al. 1981; Starring et al. 1988). The
1992; Vujnovich & Dawson 1994). mechanisms of both increased plastic and elastic
The three reflexes together are responsible for deformation have already been defined and
the neural effects that regulate musculotendinous described above.
unit flexibility, and are active during the stretch-
ing of the musculotendinous unit. The normal
Methods of stretching
sequence of activation in a vigorous stretching
movement would therefore be stretch reflex Several stretching techniques have been devel-
activation, causing reflex contraction of the oped to increase joint ROM. These include PNF,
musculotendinous unit, and Pacinian corpuscle ballistic stretching and static stretching. Com-
activation, leading to a perception of pain. This binations of these techniques have also been
would be followed in a prolonged stretch by advocated. All these techniques rely on the neu-
GTO inhibitory effects and Pacinian corpuscle ral, plastic and elastic effects of deformation as
modification. The latter two reflexes will allow previously described for their effectiveness.
relaxation in musculotendinous unit tension and
decreased pain perception (Beaulieu 1981; Reilly
Proprioceptive neuromuscular facilitation
1992; Vujnovich & Dawson 1994).
It has also been suggested that prolonged ex- Proprioceptive neuromuscular facilitation is
posure to significantly large and unusual afferent based on the theory that maximal contraction of
Fig. 11.2 A typical position

for performing an assisted
proprioceptive neuromuscular
facilitation stretch technique.
the musculotendinous unit results in maximum method is that increased stress through contrac-
relaxation after active contraction of that muscu- tion of the musculotendinous unit will result in
lotendinous unit (Knott & Voss 1956; Sady et al. autogenic inhibition in the musculotendinous
1982; Voss 1985; Osternig et al. 1987; Anderson & unit. The GTO activity will decrease tension and
Burke 1991). The PNF stretches that are used in cause relaxation by resetting the musculotendin-
sports have been adapted from neurological ous unit length. This will facilitate the passive
physical therapy treatments. The two techniques stretch procedure applied by the clinician (Norris
that are commonly used are contract–relax (CR) 1993).
and contract–relax agonist–contract (CRAC). 2 Contract–relax agonist–contract. In CRAC, the
1 Contract–relax. In CR, a therapist stretches a musculotendinous unit is stretched as described
limb to the point where limitation of ROM is felt. above in the CR procedure. In addition to this,
The therapist then holds this stretched position the opposing musculotendinous unit (antagonist)
while the patient actively contracts the musculo- of the musculotendinous unit being stretched
tendinous unit against the resistance of the ther- (agonist) is contracted isometrically while the
apist (Fig. 11.2). stretch is applied. The stretch procedure applied
The muscle is then relaxed and moved pas- by the clinician is then aided by contraction of the
sively to the new lengthened position, until a opposing musculotendinous unit (antagonist).
stretch is felt in the new position (Hanten & This results in reciprocal inhibition of the muscu-
Chandler 1994; Voss 1967, 1985; Norris 1993). A lotendinous unit being stretched, in order to
rotational component which entails a move- reduce its tension (Voss 1985; Norris 1993).
ment in the horizontal plane may be added to the In one of the first studies on the role of PNF
resistance which is in the sagittal or longitudinal in flexibility training, PNF was compared with
plane (Hanten & Chandler 1994; Voss 1967, static stretching of the hamstring musculotendin-
1985). Modifications to this method include ous unit (Tanigawa 1972). In this study, subjects
contraction of the musculotendinous unit before were divided into two treatment groups, and
stretching and contracting as described above stretches were applied twice weekly for 4
(Beaulieu 1981; Taylor et al. 1990; Noakes 1992; consecutive weeks. The PNF stretch procedure
Bandy & Irion 1994). The rationale behind the CR involved taking the leg into SLR until the subject
detected a stretch sensation. In this position, an lotendinous unit ROM (Holt et al. 1970; Tanigawa
isometric contraction was held for 7 s and then 1972; Sady et al. 1982; Wallin et al. 1985; Etnyre &
allowed to rest in the neutral position for 5 s. This Abraham 1986; Osternig et al. 1987; Cobbing et al.
was then repeated three more times. The static 2001). However, if PNF is to be performed effect-
stretch procedure to the hamstring musculo- ively, it requires expertise in all the stretching
tendinous unit was applied to group 2 in the SLR techniques, as well as an experienced clinician.
position for 7 s and allowed to rest in the neutral These techniques, therefore, although effective,
position for 5 s. This static stretch was repeated are seldom prescribed to or administered by
three more times. The control group rested in the individual athletes (Bandy & Irion 1994).
neutral position for 45 s. The results indicated
that PNF was more effective than static stretch-
Ballistic stretching
ing for increasing hamstring musculotendinous
unit ROM. Static stretching was also more effect- During ballistic stretching, the limb is moved to
ive than the control group. Measurements were the end of its ROM where the stretch sensation is
taken after each stretching session and these felt, either passively by the clinician or actively
indicate that PNF resulted in greater increases by the subjects themselves (Fig. 11.3).
in ROM at each of the individual stretching Once this stretched position is achieved, repet-
sessions and over the 4-week period. itive bouncing or jerking movements are added
In another study the effects of PNF, ballistic (Schultz 1979; Sady et al. 1982; Hardy & Jones 1986;
and static stretching were compared (Sady et al. Anderson & Burke 1991). This jerking motion
1982). Subjects were divided into four groups: during ballistic stretching could theoretically
PNF, ballistic stretch, static stretch and controls. exceed the limit of available range and thereby
Measurements of musculotendinous unit ROM cause a strain injury or tear in the musculo-
were taken of the shoulder, hamstrings and trunk. tendinous unit (De Vries 1962; Anderson &
These measurements were repeated at the end of Burke 1991; Noakes 1992). In addition, this rapid
the 6-week programme. Stretch procedures were jerking movement also elicits the stretch reflex,
performed three times weekly. The PNF proced- which then causes a reflex contraction against the
ure consisted of a stretch of the musculotendin- direction of stretch in the musculotendinous
ous unit to end of range, an isometric contraction unit. The resulting increase in tension can there-
for 6 s, an unspecified relaxation period and a fore increase the risk of injury (Beaulieu 1981;
further unspecified stretch. This was repeated Anderson & Burke 1991; Norris 1993). Theoretic-
two more times. The ballistic stretch involved ally, this technique may not be as beneficial for
repeating the full ROM, rapidly, 20 times. The increasing ROM as the musculotendinous unit
static stretch involved reaching the musculo- would undergo a reflex contraction at each bounce
tendinous unit end of range, holding for 6 s, or jerk due to the stretch reflex. Relaxation, or
relaxing for an unspecified time and repeating lengthening, of the musculotendinous unit can
the procedure twice more. The control group’s therefore not be achieved (Beaulieu 1981; Voss
procedure was not specified. Results indicate 1985; Noakes 1992; Matthews 1993).
that only PNF stretching increased musculo- In one study, the effects of a combination of
tendinous unit ROM over the 6-week period, ballistic and static stretching with static stretch-
compared with the control group. This study ing alone on the ankle dorsiflexion musculo-
was limited because there was no reported detail tendinous unit were compared (Vujnovich &
in terms of the control group’s procedure and Dawson 1994). Subjects were divided into a static
individual measurements of musculotendinous (stretch applied to the musculotendinous unit for
unit ROM during the 6-week period. 160 s) and a static–ballistic stretch group (static
Other authors also reported that PNF stretch- stretch applied to the musculotendinous unit for
ing techniques are effective in increasing muscu- 160 s followed by 160 s of ballistic stretch). The
Fig. 11.3 A typical position

for ballistic stretching of the
hamstring muscles. The athlete
performs small oscillating
movements in this position.
control group was rested for an unspecified time

Static stretching
period. The results of this study showed that a
static stretch followed by ballistic stretching The most common method of stretching that
increased musculotendinous unit ROM more is used by athletes, coaches and therapists, is the
than static stretching alone. Given that all the static stretch (Zachazewski 1990; Anderson &
stretching techniques are reported to increase Burke 1991; Beaulieu 1991; Norris 1993). Static
musculotendinous unit ROM (Tanigawa 1972; stretching is characterized by the limb being
Sapega et al. 1981; Taylor et al. 1990; Vujnovich moved slowly and gently to the end of its avail-
& Dawson 1994), it is not surprising that the able ROM, in order to obtain a stretch sensation
addition of one technique to the other, thereby in the tissues (Fig. 11.4).
doubling the total stretching time, will result in This controlled stretch is maintained in this
greater increases in musculotendinous unit ROM position for an extended period (Beaulieu 1991;
than with one technique alone. In this study, the Norris 1993). The end of the available range is
one group was stretched for 160 s in total, determined by maximum tolerance of the subject
whereas the other group was stretched for a total to the stretch sensation just short of pain (Norris
of 320 s. The greater increases in ROM in the 1993; Bandy & Irion 1994).
static–ballistic group could not therefore be Static stretching is sometimes referred to as
explained by the stretch type only, but also by passive stretching. Where this occurs, the dis-
total duration of stretch. tinction referred to is the mode of application. If
The use of ballistic stretching would appear to the stretch is applied and held by the subject, it is
increase the risk of injury due to the increases in referred to as static stretching. If the static stretch
musculotendinous unit tension. Furthermore, procedure is applied by a therapist or another
due to the stretch reflex mechanism, it, indeed, person to the subject, it is sometimes referred to
may not be effective in increasing musculotend- as passive stretching (Beaulieu 1981; Noakes
inous unit ROM. Its use is therefore not widely 1992). The danger of the passive stretch is that
advocated as the technique of choice to improve when executed incorrectly by a team-mate or
musculotendinous unit ROM. partner, it has the potential to overstretch the
Fig. 11.4 A typical position for

an athlete to perform a static
stretch of the hamstring
musculotendinous unit.
musculotendinous unit. When administered by and held for 10 s. The limb was then moved into
an experienced clinician, though, passive stretch- a greater ROM for a further 10 s. This procedure
ing can be very useful and as effective as the was repeated for 15 min. Because the stretch was
standard static stretch (Beaulieu 1981; Noakes held statically for a period of time, this cyclic
1992). method of stretching is referred to as a repeated
When the static stretch position is obtained static stretch. The static stretch group had a con-
slowly and gently, the stretch reflex response is stant force applied to the hamstrings for 15 min.
dampened and occurs late in the movement. Hamstring musculotendinous unit ROM was
As the tension in the musculotendinous unit measured at the end of each treatment session.
from the stretch and from the reflex contraction The procedures were repeated daily for 5 con-
increases, the inverse stretch reflex initiated by secutive days. Another measurement was taken
the GTO is induced (Beaulieu 1981; Voss 1985). 5 days after the last stretching session.
This causes autogenic inhibition in the musculo- Results showed that hamstring musculo-
tendinous unit and allows a greater ROM to be tendinous unit ROM increased more in the cyclic
achieved in the musculotendinous unit (Voss stretch group compared to the static stretch
1985). The GTO, therefore, overrides the stretch group. Increases in musculotendinous unit ROM
reflex. In this way, both neural effects and plastic were recorded on day 5 compared with day 1, for
deformation are utilized to increase musculo- both groups. In both groups, there were still
tendinous unit ROM. increases in musculotendinous unit ROM at
In one study, variations of the static stretching 5 days after the last stretch session, compared
procedures were examined. The effect of cyclic with the measurements taken on day 1. These
stretch with static stretch on hamstring musculo- increases were, however, less on day 5 compared
tendinous unit ROM was studied (Starring et al. with those reported on day 1. The cyclic group
1988). Subjects were divided into two groups and maintained a significantly larger increase in ROM
the hamstring musculotendinous unit length than the static group. These results show that
was measured using the knee extension test with static stretching which is held, and then repeated
the hip in 90° flexion. The cyclic stretch entailed in the increased ROM, produces greater increases
the hamstring being stretched to the end of range in musculotendinous unit ROM than static
stretching sustained for long periods in one duration (5 min) stretch with low load (25% of
position. high load), long duration (50 min) stretch (Warren
Compared with other methods of stretching, et al. 1976). This study was conducted on rat tail
static stretching produces the least amount of tendon. The high load, short duration protocol
tension (Moore & Hutton 1980). Theoretically, it resulted in almost twice the elongation compared
therefore has the lowest risk of injury, and is to the low load, long duration group. However,
easy and safe to implement. The static stretching in the high load, short duration group, elongation
method is consequently the one most commonly was retained for only half as long as in the low
advocated for use in a flexibility training pro- load, long duration group.
gramme (Bass 1965; Burry 1975; Glick 1980; Lehmann et al. (1970) compared short-term
Beaulieu 1981; Leach 1982; Zarins 1982; Voss 1985; stretch (time not reported) with long-term stretch
Noakes 1992). (20 min) on rat tail tendon. This study found that
long duration stretches were more effective in
increasing tendon length. Both Lehmann et al.
Scientific basis of a stretching session
(1970) and Warren et al.’s (1976) studies did not
A number of factors are important in the suc- investigate some of the commonly used stretch-
cessful implementation of a stretching session ing durations and therefore offer limited informa-
or flexibility training programme, irrespective of tion on the optimum duration of static stretching.
the type of technique. These include: (i) the dura- In addition, both these studies were conducted
tion for which a stretch is held; (ii) the number of on animal tail tendon and therefore cannot be
times the stretch is repeated in one session; (iii) extrapolated to human musculotendinous units.
the number of times the session is repeated per In one animal study, performed on rabbit mus-
day or week; (iv) the effect of warm-up on the culotendinous units, stress relaxation was used
effect of stretching; and (v) the most effective to determine the effects of static stretch duration
anatomical position in which to stretch a particu- on musculotendinous unit ROM (Taylor et al.
lar musculotendinous unit. Despite the fact that 1990). In this study, the musculotendinous unit
there are guidelines in most sports medicine text- was taken to a predetermined tension of 78.4 N
books on the method of static and PNF stretching (this magnitude of force was selected on the basis
(Zachazewski 1990; Noakes 1992; Norris 1993), that it did not cause any irreversible damage but
there are very few clinical research data available resulted in significant elastic deformation of the
to support the currently advocated methods of musculotendinous unit) and held at that length
static and PNF stretching. This section will focus for 30 s. The stress relaxation was then measured
on the recently acquired data from research stud- by recording the change in tension in the muscu-
ies that identified the scientific basis for optimum lotendinous unit over that time period. It was
static and PNF stretching. documented that significant relaxation in the
musculotendinous unit occurred after 12–18 s,
although relaxation continued over the entire
Optimum duration of a stretch at one
30 s period. Because the measurements were only
stretching session
taken over 30 s, it is impossible to state whether
the same overall stress relaxation would have
static stretching
occurred if held for a period of 48–72 s (i.e. 4 ×
The duration of the force applied in static stretch- 12–18 s).
ing can be defined as the time for which a stretch The optimum duration of a static stretch that
is applied at a single stretching session. Invest- is to be used in the normal population, and in
igators have studied the effects of various dura- athletes in particular, has also been investigated
tions of passive stretch in animal models. One in human studies. The optimum duration of
study compared the effects of high load, short static stretching has been reported on numerous
Change in ROM (degrees) 10 12
Change in ROM (degrees)

Control * Control
8 Stretch 10 Stretch
*
6 # 8
#
4 6
2 4
0 2
–2 0
10 20 30 60 90 120 240 10 20 30 60
Stretch durations (s) Stretch durations (s)
Fig. 11.5 The effect of different static stretch durations
Fig. 11.6 The effect of different PNF stretch durations
on changes in hamstring ROM. All stretch durations
on changes in hamstring ROM. All stretch durations
(except the 10 s duration) were significantly different
were significantly different from controls. *, significant
from controls. *, significant difference from change in
difference from change in ROM between 10 and 30 s.
ROM after 20 s; #, significant difference from change in
(From Cobbing et al. 2001.)
ROM after 60 s. (From Hughes et al. 2001.)
pnf stretching
occasions and varies from 6 s to 20 min (De Vries
1962; Tanigawa 1972; Medeiros et al. 1977; Moore The precise duration of a PNF stretch on
& Hutton 1980; Beaulieu 1981; Klafs & Arnheim increases in hamstring ROM has only recently
1981; Sady et al. 1982; Bohannon 1984; Henricson been reported. In this study, human subjects
et al. 1984; Madding et al. 1987; Zachazewski (experimental and a control group) were sub-
1990; Bandy & Irion 1994). jected to durations of PNF stretch of 10, 20, 30
Until recently, only three studies have been and 60 s. The increases in hamstring ROM fol-
reported in humans where different durations lowing different durations of PNF stretches are
of static stretch were compared with another. depicted in Fig. 11.6.
Bohannon (1984) measured increases in muscu- The results of this study show that a 10 s PNF
lotendinous unit length at 15 s and then at 30 s stretch is as effective in increasing ROM as longer
intervals thereafter, for 8 min. Madding et al. durations, i.e. up to 60 s.
(1987) measured only at 15, 45 and 120 s. Bandy
and Irion (1994) measured at 12, 30 and 60 s over
Number of repetitions (frequency) of stretches
a 6-week period.
at one stretching session
A definitive study described by Hughes et al.
(2001) examined the effects of different durations
static stretching
of static stretching on hamstring musculotend-
inous unit ROM. In this study, 10 normal subjects The optimum number of repetitions that should
underwent static stretching durations of 10, 20, be performed at a single static stretching session
30, 60, 90, 120 and 240 s. ROM was measured has not been investigated until recently. In the
using EMG activity as the end-point. Three past, between one and 20 repetitions have been
stretches were applied with a 1 min rest in advocated to increase ROM (Beaulieu 1991;
between. The results of this study are depicted in Norris 1993). However, this advice has not been
Fig. 11.5. based on scientific data from human studies.
The results of this study clearly show that a In one animal study on rabbit musculotendin-
static stretch duration of 30–60 s is optimal to ous units, this parameter was investigated (Taylor
increase ROM in static stretching. et al. 1990). In this study, the stress–relaxation
procedure was used. This involved taking the 16

Control
musculotendinous unit to a predetermined 78.4 N 14 Stretch
point of tension. This point was determined as 12
10
the point where no irreparable damage was done
8
to the musculotendinous unit, but where leng- *
6
thening occurred. The length of the musculotend- 4
inous unit where this point of tension occurred 2
was maintained for 30 s. During the 30 s period, 0
the tension in the musculotendinous unit and its –2
1 2 3 4 5 7 9
length was measured. The tension decreased Number of repetitions
during the 30 s period. After 30 s, the musculo-
tendinous unit was returned to the initial resting Fig. 11.7 The effect of different static stretch
tension of the musculotendinous unit of 1.96 N. repetitions on changes in hamstring ROM. All stretch
repetitions were significantly different from controls.
This cycle of stretching was repeated 10 con-
*, significant difference from change in ROM from
secutive times for each musculotendinous unit. after repetitions. (From Hughes et al. 2001.)
Results showed significant increases in muscu-
lotendinous unit length during the first four 14 *
Control *
cycles, with cycles 1 and 2 showing the largest 12 Stretch
increments in increased musculotendinous unit 10
length. Cycles 5–10 also showed increases in 8
musculotendinous unit length, but these were 6
not as significant as those occurring during cycles 4
1–4. 2
This study indicates that the optimal number 0
of repetitions in a single stretching session is –2
1 2 3 4
four. However, because all the stretches were Number of repetitions
only held for 30 s, it was not possible to deter-
mine whether the same increases in ROM would Fig. 11. 8 The effect of different PNF stretch
repetitions on changes in hamstring ROM. All stretch
have been attained had the stretch been held for a
repetitions were significantly different from controls.
total of 48–72 s (i.e. 4 × 12–18 s) in one session. *, significant difference from change in ROM from
Although this was a very thorough and useful after two repetitions. (From Cobbing et al. 2001.)
study, it required validation in the human
model.
pnf stretching
It was therefore necessary to investigate the
number of repetitions in a static stretch session The optimum frequency of PNF stretches to
that are required to gain optimum increases in increase hamstring ROM has only very recently
ROM in the human musculotendinous unit. been reported. Healthy subjects underwent 10 s
Recently this study was undertaken, using nor- repeated PNF stretches of different frequencies.
mal subjects that were subjected to stretches of Hamstring ROM was assessed in a stretch and
30 s duration (Hughes 1996). The frequency of control group using EMG spikes as the end-point
stretches varied from one to 10 stretches. The to determine ROM. The results of this study are
results of this study are depicted in Fig. 11.7. depicted in Fig. 11.8.
The results of this study indicate that three The results of this study show that three PNF
stretches are optimum in increasing ROM and stretches result in the largest increase in ROM,
that additional stretches do not add any further but that this was not significantly more than
advantage to increasing the ROM. performing a single stretch.
based on recent scientific evidence, ROM is only

Retention of increased ROM after one
retained for 4–6 h. The practical implication is
stretching session
that the frequency with which stretch sessions
should be conducted during a day to achieve
static stretching
maximal benefit, is approximately every 6 h (dur-
Until recently, it had not been well documented ing awake hours).
how long the retention in increased ROM follow-
ing a static stretch session would last. A number
pnf stretching
of authors have suggested time periods for the
retention of ROM, but none of these have been The retention in ROM following a PNF stretch
tested in a well-conducted clinical trial. Sug- session has not been well investigated. In one
gested time periods for retention of ROM ranged study by Toft et al. (1989), it was documented that
from 3 h (Beaulieu 1981) to days (Atha & Wheatley there was a residual effect of increased musculo-
1976). Data on the retention of ROM after a static tendinous unit ROM for at least 90 min after a
stretching session are vitally important in order PNF stretching bout. In this study, measurements
to implement a scientifically based stretching of ankle dorsiflexion were taken. PNF stretching
programme. was obtained by maximal contraction of the
In a study on rat tail tendon by Warren et al. plantar flexors for 8 s in the stretched position,
(1976), it was demonstrated that the application followed by 2 s of relaxation and finally 8 s
of low load forces (25% of high load) for 50 min of slow static stretching. This procedure was
resulted in the retention of more than twice the repeated five times, and 90 min later ankle dorsi-
elongation compared with the high load, short flexion was remeasured. It was found that the
duration applied for 5 min. The retention of increases in musculotendinous unit ROM were
elongation was measured 10 min poststretch. maintained over this 90 min period. Here the
This study was conducted on animal tendon and static stretching procedure was administered
is therefore not representative of the complete for 40 s only in total (15 × 8 s) and was preceded
musculotendinous unit and may also not be by an isometric contraction before each stretch.
applicable to human subjects. The duration of retention of ROM following PNF
In a recent study (Hughes 1996), the retention stretching requires further investigation.
in ROM achieved by a static stretch session (3 ×
30 s stretches) was evaluated. Normal subjects
Cumulative effect of repeated static
underwent a static stretch session, and ROM was
stretching sessions
then measured over a 24 h period to determine
residual increases in ROM at periodic intervals.
static stretching
The results of this study are depicted in Fig. 11.9.
The results of this study indicate that follow- Until recently, there had been no studies that
ing a stretch session that is conducted optimally, documented the cumulative effect, if any, of
15 Control
Change in ROM
10 Stretch
(degrees)
Fig. 11.9 The retention in

5
hamstring ROM after a static
0* stretch session (3 × 30 s stretches).
*, significant difference from
–5 change in ROM from value
Immediately 1 2 3 4 5 6 12* 24* immediately poststretch.
post Time after session (h) (From Hughes et al. 2001.)
25

Control
20 Stretch * *
*
*
15 *
*
10
Fig. 11.10 The cumulative effects 5
of daily static stretching (3 × 30 s
every 6 h) on hamstring ROM. 0
*, significant difference from –5
change in ROM from day 1. 1 2 4 7 9 11 14 16 18 21
(From Hughes et al. 2001.) Days
repeated bouts of static stretching on joint ROM.

pnf stretching
In one study by Bandy and Irion (1994), subjects
were placed on a stretching programme for 3 Retention in ROM following PNF stretching has
weeks. Measurements of hamstring musculo- not been well investigated either. In one study, a
tendinous unit ROM were made before and after PNF stretching programme was implemented
the study. Subjects in the three experimental where subjects stretched twice daily for 3 weeks
groups performed one 15 s, one 30 s or one 60 s (Toft et al. 1989). Ankle dorsiflexion ROM was
static stretch. This static stretch was performed measured before implementing the stretch pro-
daily, 5 days a week, for 3 weeks. At the end of cedure and after 3 weeks of stretching. The stretch
this period, hamstring musculotendinous unit had procedure consisted of a maximal isometric
increased significantly in the groups stretching contraction of the plantar flexors for 8 s in the
for 30 and 60 s, but not in the group stretching for stretched position, followed by a 2 s rest period
15 s. However, because measurements were only and finally an 8 s slow static stretch of the plantar
taken prior to the onset of the study and after flexors. This was repeated five times. The whole
3 weeks, it was not possible to determine when procedure was carried out twice daily for 3
the changes in ROM occurred. weeks. No measurements of ankle ROM were
More recently, the cumulative effects of static taken during the 3-week period. Ankle ROM was
stretching were investigated. In this study healthy remeasured at the end of the 3-week period. At
subjects underwent daily stretching every six the final measurement, no stretching procedures
hours (3 × 30 s static stretches). ROM measure- were carried out for at least 20 h prior to meas-
ments of the hamstring musculotendinous unit urement. There were still large residual increases
were conducted over a 22-day period. The results in ankle musculotendinous unit ROM.
of this study are depicted in Fig. 11.10.
The results of this study indicate that daily
Role of warm-up prior to static stretching on
static stretching (every 6 h) can result in retention
musculotendinous unit ROM
of ROM after as short a period as 7 days. There
is also a progressive increase in ROM (approx- The inclusion of warm-up prior to stretching
imately 1% per degree, in general). From Fig. 11.10 is widely advocated (Dominguez 1982; Wathen
it can be seen that the increase in ROM achieved 1987; Zachazewski 1990). However, its role in
using this stretching programme is approximately altering the effectiveness of the stretching pro-
15–20%, and that a plateau effect had not yet cedure is not clear. It has been suggested that
been achieved after 3 weeks. increases in flexibility occur as a result of
increases in tissue temperatures (Cureton 1941; on musculotendinous unit ROM. Measurements

De Vries 1962; Lehmann et al. 1970; Nicholas of hip flexion, abduction and external rotation
1970; Warren et al. 1976). Other authors suggest were taken. Subjects were divided into three
that increased tissue temperatures do not result groups. The first group had an electric heat pad
in increases in musculotendinous unit flexibility applied for 20 min at 43°C. A second group had
(Halkovich et al. 1981; Wiktorsson-Moller et al. the electric heat pad applied as above and this
1983; Williford et al. 1986; Cornelius et al. 1988). was then followed by a modified PNF technique
It is also important to determine whether the consisting of 7 s isometric contraction of the mus-
warm-up is passive or active. Passive warm-up culotendinous unit, followed by 7 s relaxation,
occurs when the muscles are warmed by means followed by 7 s static stretching. The third group
of external heating such as direct heat applica- performed only the PNF technique of stretching.
tion (heat packs) or in the form of therapeutic Results show that no increases in ROM occurred
ultrasound. Active warm-up refers to a warm-up in the first (heating only) group. The other two
of the muscles by active contraction. This would groups showed significant increases in ROM,
be in the form of a jog or any other exercise where with the combined heat and PNF group showing
the muscles to be stretched are repeatedly con- the greatest increases in ROM. This study indi-
tracted prior to stretching. cates that passive heating alone is not effective in
increasing musculotendinous unit ROM. How-
ever, when combined with stretching, passive
passive warm-up
heating is more effective in increasing musculo-
It has been postulated that in passive warm-up, tendinous unit ROM than stretching alone. The
the increases in tissue temperatures increase the PNF stretching technique is notable in that it
extensibility to the musculotendinous unit. This includes a muscle contraction as well as a static
increased extensibility is due to the effects of heat stretch. Therefore, PNF techniques employ an
on the intermolecular bonding of collagenous element of active warm-up as well.
tissue. It is probable that heating of the muscu- In another human study, the effect of passive
lotendinous unit results in the collagen being heating on the stretching procedure was studied
partially destabilized and consequently more pli- (Wessling et al. 1987). In this study, the triceps
able and extensible (Rigby 1964; Lehmann et al. surae musculotendinous unit either had static
1970; Warren et al. 1976; Sapega et al. 1981; Ciullo stretching applied to it for 1 min, or 1 min of
& Zarins 1983). static stretching applied after 7 min of continu-
In an animal study, Warren et al. (1976), showed ous ultrasound. Ultrasound causes a deep heat-
that rat tail tendon extensibility was increased ing effect in tissues (Gerston 1955; Low & Reed
with the addition of heat prior to the static stretch 1990). This study showed that the addition of
procedure. The tendons were either exposed to deep heating to static stretching of the musculo-
temperatures of 25, 39 or 45°C. A load of 100 g tendinous unit resulted in greater increases in
was applied to all the tendons and increases in ROM than static stretching alone. The difference
length were measured. The groups exposed to between this study and the one conducted by
higher temperatures experienced significantly Henricson et al. (1984) may lie in the deep heating
greater increases in extensibility compared with effect of ultrasound compared with the more
the 25°C group at the load of 100 g. There was superficial heating of the heat pad.
also less resultant tissue damage in these two
groups than in the 25°C group.
active warm-up
Studies on the effects of passive warm-up on
static stretching have also been performed on Although knowledge of the effects of the addi-
human subjects. In 1984, Henricson et al. con- tion of passive heat to the effectiveness of stretch-
ducted a trial on the effects of heat and stretching ing in increasing musculotendinous unit ROM is
valuable to the clinician, active warm-up is more active warm-up consisting of 15 min of stationary
practical and of more value to the sportsperson. cycling. The second group received 15 min of
As muscles contract repeatedly, heat is produced warm-up as above and 12 min of massage. The
and the intramuscular temperature increases third group received 12 min of massage only.
(Zachazewski 1990). This process is known as The fourth group received warm-up as above
active warm-up or physiological precondition- and PNF stretching. The PNF stretch consisted
ing (Safran et al. 1988; Zachazewski 1990). There of a maximal isometric contraction for 4–6 s,
have been a number of studies conducted to followed by relaxation for 2 s and finally by a
determine the effect of active warm-up on mus- static stretch for 8 s. Results showed that other
culotendinous unit ROM. than for ankle dorsiflexion, warm-up alone, mas-
In an animal study conducted by Safran et al. sage alone and warm-up plus massage have no
(1988), the effect of active warm-up on the ROM effect on musculotendinous unit ROM. Warm-
of the musculotendinous unit was investigated up combined with stretching showed significant
in rabbits. In one group, musculotendinous unit increases in ROM for all joints. None of the
length was measured and then this musculo- groups showed any changes in muscle strength
tendinous unit was electrically stimulated to its with the intervention. No measurements were
maximum wave summated tension for 15 s. This done on the effects of stretching alone, and there-
was classified as the active warm-up period. The fore the effect of the addition of warm-up to
electrode was then removed and the musculo- stretching could not be determined.
tendinous unit was statically stretched to failure. In 1986, Williford et al. conducted a study on
In the second group the musculotendinous unit the effects of active warm-up on musculotendin-
length was measured and then statically stretched ous unit flexibility over a period of 9 weeks. The
to failure without active warm-up. An average of flexibility of the shoulder, hamstrings, trunk and
7% more force was needed to reach failure in the ankle were measured. The subjects were divided
active warm-up group. The actively warmed-up into two groups. The first group performed only
musculotendinous units could also be stretched static stretching that entailed a static stretch,
to a significantly greater length before reaching which was held for 30 s and then repeated once
failure. Intramuscular temperatures were recorded more, totalling 60 s of static stretching. The
to increase by 1°C in the actively warmed-up second group actively warmed-up by jogging
musculotendinous units. The results of this study lightly but progressively for 5 min, prior to per-
are valuable because they indicate that actively forming the same static stretching as in group 1.
warmed-up musculotendinous units obtain signi- The subjects performed their respective stretch-
ficant increases in musculotendinous unit ROM ing routines twice per week for 9 weeks. Results
and can absorb significantly higher forces before indicated that the active warm-up group gained
failure. This would indicate that actively warmed- significantly greater increases (approximately
up musculotendinous units would significantly 14%) in ROM than the stretching only group.
increase their musculotendinous unit ROM when Gains (approximately 11%) in ROM were also
statically stretched and also have a lower risk of documented in the stretching-only group.
injury. In another study, the effects of the placement
In another study, the effects of active warm- of a stretching session in a work-out in increasing
up, massage and stretching on ROM and muscle ROM was determined (Cornelius et al. 1988).
strength were conducted (Wiktorsson-Moller Subjects were divided into three groups. The
et al. 1983). In this study, hip flexion, hip exten- first group performed static stretching for 10 s
sion, hip abduction, knee flexion and ankle dorsi- before the exercise session, which consisted of
flexion ROM, and hamstring and quadriceps 20–30 min of jogging. The second group per-
strength were measured. There were four groups formed static stretching after the exercise ses-
that were compared. The first group received an sion described. The third group performed the
15 *
Control
Stretch *
10
5 Fig. 11.11 The effects of warm-

up alone, stretching alone
and combined warm-up and
0 stretching on hamstring ROM.
*, significant difference between
–5 two groups, and between
Warm-up Stretch Warm-up and warm-up alone. (From Hughes
stretch et al. 2001.)
stretching both before and after the exercise combined with static stretching on musculo-
session. The stretching and exercise sessions tendinous unit ROM were determined. Normal
were performed 3–5 times per week, for 6 weeks. subjects underwent either active warm-up only
Results showed increases in musculotendinous (running until 70% maximum heart rate was
unit ROM in all the groups, but no significant achieved), static stretching (3 × 30 s) only, or
differences between the groups. This study is combined active warm-up and then static stretch-
limited in its value because the stretching proce- ing. Hamstring ROM measurements were con-
dure was not well defined, and the subjects in ducted in all groups after the interventions, and
the groups were not well matched. There was a in a control group. The results of this study are
wide variation in the amount of stretching and depicted in Fig. 11.11. The results of this study
exercise that was performed by the subjects. indicate that active warm-up alone is not effec-
From the above studies, it is difficult to deter- tive in increasing ROM, but that it may have an
mine the effects of active warm-up on musculo- additive effect if it is performed prior to static
tendinous unit ROM. Passive warm-up appears stretching.
to have little effect on musculotendinous unit There have been no studies that compare
ROM (Henricson et al. 1984). When passive warm- active versus passive warm-up, with and with-
up is combined with stretching it appears to be out stretching.
more effective than stretching alone for increas-
ing musculotendinous unit ROM (Henricson
Effect of stretch position during the stretching
et al. 1984; Wessling et al. 1987). Active warm-up
session on musculotendinous unit ROM
before static stretching in human subjects appears
more beneficial in increasing musculotendinous It is a widely held belief that stretch position
unit ROM than static stretching alone, over a alters the efficacy of the stretching procedure
period of 9 weeks (Williford et al. 1986). The most (Voss 1985). For example, it is generally believed
valuable study on the effect of active warm-up that increased ROM in a musculotendinous unit
was conducted on rabbit musculotendinous cannot be achieved when the musculotendinous
units (Safran et al. 1988). However, the results of unit is contracting. In a recent study, the effect
this study cannot be directly extrapolated to of limb position on hamstring ROM has been
humans. In this study, active warm-up increased evaluated. Normal subjects underwent three
musculotendinous unit ROM, musculotendin- types of stretching procedures: (i) standing and
ous unit length to failure, and the force necessary stretching a weightbearing (contracting) ham-
to reach failure. string muscle; (ii) standing but stretching a
In a recent study, the effects of active warm-up non-weightbearing hamstring muscle; and (iii)
alone, static stretching alone and active warm-up lying supine and stretching a non-weightbearing
12 Control

10 Stretch
8
*
6 *
4
Fig. 11.12 The effect of limb 2
position and stretch procedure
on hamstring ROM. *, significant 0
difference from supine position. Standing and Standing and Supine
(From Hughes et al. 2001.) weightbearing non-weightbearing
hamstring muscle. The ROM immediately after • Static stretching is most commonly used, is
the stretches (3 × 30 s static stretches) was mea- safe and effective.
sured. The results are depicted in Fig. 11.12. • PNF is more effective than static stretching
The results of this study show that limb position but it requires some training to master the
is important when performing static stretch pro- technique and requires an assistant in some
cedures. It is advised that static stretching should instances.
take place in the relaxed, non-weightbearing • Ballistic stretching may be effective but it has
position. been postulated to increase the risk of injury
while performing the stretch.
• An optimum static stretch session should con-
Conclusions and practical guidelines
sist of three stretches lasting 30 s each.
for stretching
• Two to three static stretch sessions should be
• Musculoskeletal injuries are common in ath- performed daily for maximum benefit.
letes and require rehabilitation following injury • Static stretch sessions performed two or three
or surgery. times per day will result in a permanent increase
• Injury or surgery can result in decreased in joint range of motion after 7 days.
joint ROM mainly due to fibrosis and wound • A cumulated benefit to daily static stretches
contraction. (every 6 h) for up to 21 days has been demon-
• Flexibility training is an important compon- strated.
ent of rehabilitation in order to minimize the • A warm-up alone will not increase ROM but
decrease in joint ROM. has an additive effect if it precedes a static stretch
• Flexibility training should begin in the first session.
week following injury or surgery to prevent • A static stretch should be performed in the
decrease in ROM due to wound contraction non-weightbearing position with the muscle
and fibrosis. relaxed for maximum gain in ROM.
• The main postulated benefits of flexibility
training for the non-injured athlete are injury
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Chapter 12
Strength and Endurance

GUNNAR GRIMBY AND ROLAND THOMEÉ
Introduction Impaired muscular activation
Injuries to the musculoskeletal system could result An impaired muscular activation can depend on
in skeletal muscle hypotrophy and weakness, factors such as: (i) inhibition due to pain or other
loss of aerobic capacity and fatigability. Often afferent nerve influence; or (ii) reduced muscle
there is a combination of these negative effects of activity at immobilization and/or injury.
injuries and immobilization with usually one or Pain, joint effusion and knee angle are factors
the other dominating, depending on the type influencing the degree of inhibition. Pain from
of injury. This chapter will discuss the time a joint may result in involuntary inhibition of
sequence and extent of these changes in the activity in muscles acting across that joint, and a
perspective of rehabilitation measures. Rehabili- considerable lack of ability for muscle activation
tation techniques and exercise prescription will has been seen after knee pathologies and surgery
especially be described for resistance training (Hurley et al. 1994). However, the presence
and cardiovascular (aerobic) conditioning train- of pain is not necessary for inhibition to occur
ing during the second phase (after the acute (Stokes & Young 1984; Shakespeare et al. 1985).
phase with immobilization). There is not a direct relationship between the
degree of pain and the amount of muscle inhibi-
tion. Inhibition may be as severe in a later post-
Reduction in skeletal muscle strength
operative period as at the first postoperative day,
Reduction in skeletal muscle strength and even in a virtually pain-free state. The activity in
increased fatigue after injury and/or immobil- other receptors from the joint and adjacent struc-
ization with disuse depend on several factors tures may have similar effects as seen in animal
(Kannus et al. 1992b,c; Behm & St Pierre 1998). experiments and human studies. It has been
The specific effects of immobilization have been demonstrated that a very small amount of joint
described in detail in Chapter 6 and the physio- effusion will result in reflex inhibition of the
logical and functional implications of injury in musculature. The amount of quadriceps inhibi-
Chapter 7. In the clinical management nowa- tion after knee injury may partly be dependent
days, immobilization is avoided, if possible. The on the knee angle, with less inhibition in a flexed
reduction in muscle strength can in principle than in a fully extended position (Shakespeare
depend on impaired neuromuscular activation et al. 1985). There might be selective inhibitions
and/or reduced muscle volume, as it can be of motor units, which could explain part of the
assumed that the number of muscle fibers are dominant hypotrophy of a specific fibre type
protected. (see below), seen after joint damage. Selective
258
strength and endurance 259
Joint damage hypotrophy of slow-twitch type I fibres, as also

seen after immobilization with a short muscle
length. After general disuse, a reduction, especi-
ally of fast-twitch type II fibres, predominates.
Muscle Reflex A reduction of the muscle size of the quadri-
Immobilization
weakness inhibition
ceps equivalent to up to 30–40% may be seen after
knee injury. The wasting of quadriceps usually
dominates over the loss of hamstrings muscle
Muscle wasting volume.
Fig. 12.1 Schematic presentation of different

mechanisms leading to muscle wasting and muscle Assessing the degree of muscle wasting
weakness. (Redrawn from Stokes & Young 1984.)
The degree of muscle wasting can not be accur-
ately diagnosed by measurements of circumfer-
ence using a standard tapemeasure device and
inhibition of part of the quadriceps muscle has can in fact be grossly underestimated. The reason
also been noted among patients with patello- for this is that the fat and bones structures are
femoral pain syndrome (Thomée et al. 1996). practically constant. With a reduction of the cir-
There is a vicious cycle causing muscle cumference of the muscle tissue, there will be an
weakness. Figure 12.1 illustrates the relationship increase in the width of the subcutaneous fat
between joint damage, immobilization, reflex in- layer masking part of the effect of muscle wast-
hibition and muscle wasting. The reflex inhibition ing on the total circumference. Thus, it is difficult
can therefore result in an immediate reduction and often misleading to use changes in circum-
of voluntary muscle activation causing muscle ferences as indicators of gains in muscle tissue
weakness, early after an injury or surgery. In a during rehabilitation after injury or immobiliza-
longer perspective it will also cause muscle wast- tion. Other more exact means have to be used
ing resulting in further muscle weakness. including computed tomography (CT), magnetic
resonance imaging (MRI) or ultrasound. In clin-
ical practice one has often to rely on the indirect
Reduced muscle volume
measurement of muscle strength and the inter-
The other factor causing decreased muscular pretation of changes in muscle strength with
strength, besides inhibition, is the reduction in respect to muscle volume.
muscle volume that follows an injury. In rehabili-
tation, aspects to consider are the importance
Difference in strength between extremities
of the different patterns of muscle hypotrophy,
the difficulty in assessing the degree of muscle An important aspect when evaluating reduction
wasting, the difference in strength between in strength at follow-up, is that there may be a
extremities, and the strength relation between lack of perception of a moderate difference in
the agonist and the antagonist muscles (agonist– strength between the two extremities. Thus, a 20%
antagonist ratios). reduction, or even more, of quadriceps muscle
strength has been recorded in the previously
injured side compared with the non-injured side
Patterns of muscle hypotrophy
in persons who have returned to normal activ-
Different patterns of muscle hypotrophy may ity and considered themselves fully recovered
be seen depending on the type of immobilization (Grimby et al. 1980; Arvidsson et al. 1981). If such
and disuse (Appell 1990; Kannus et al. 1992b,c). differences are seen in athletes, objective evalu-
Patients with longstanding pain may show ation and further rehabilitation are needed.
and different aspects may be of importance,

Agonist–antagonist ratios
depending on the type of training, the muscles
Assessment of the ratio of the agonist–antagonist involved, and the pretraining status.
strength, as the quadriceps–hamstrings ratio, The mechanisms of adaptation may include
may also result in recommendations for further increased activity of the prime movers for a
training, but a comparison between injured and specific movement and changes in the activation
non-injured sides is of more importance in clin- of synergists and antagonists (Sale 1988). There
ical practice. The knowledge of the prevalence of may be an increased activation of the number
muscular imbalance and its functional signifi- of motor units at maximal effort and/or an
cance is, however, rather poor. increased firing rate. The relative importance
of these factors may vary between muscles and
type of muscle activation. Motor units may be
Reduction in muscle endurance
better synchronized. There may be facilitation
Parallel with the reduction in muscle strength of reflexes as well as reduction of inhibitory
there will usually be a reduction in muscle influence. Parallel to the activation of the prime
endurance. A given level of force production will mover, activation of the antagonist may also
now be closer to the maximal force output of occur, having a functional positive or negative
the muscle, and therefore will need a relatively effect. A reduction in the activation of the antag-
higher proportion of the muscle strength. There onist during training may lead to greater activa-
are a number of factors which may reduce mus- tion of the prime mover, reducing any reciprocal
cle endurance following disuse (Kannus et al. inhibition, and alsoathrough less force produced
1992b,c; Behm & St Pierre 1998), including a by the antagonistsaan increased net output of
reduction in mitochondrial enzymes necessary force in the direction of the movement.
for the oxidative process in the muscle and a
reduction in capillarization with less ability to
time aspects
transport oxygen and energy supply to the mus-
cle cell. On the other hand, a reduction in muscle Early after an injury and/or immobilization there
fibre cross-sectional area with disuse will reduce is most likely to be reduced neuromuscular
the diffusion distances. With training these fac- activation (Sale 1988; Häkkinen 1994). Strength
tors will be reversed. An increase in mitochon- training effects will then mainly depend on
drial enzymes will be seen quite quickly during neural factors and may be limited to the type of
adequate training emphasizing the endurance training exercise, both with respect to speed dur-
adaptation. ing dynamic exercise and joint angle during
static exercises (Kraemer et al. 1996). The length
of this initial period may vary depending on the
Background for resistance training
type and degree of injury and disuse. For train-
There are different aspects of resistance training ing from an initial moderately untrained state,
depending upon whether an improved neuro- it has been estimated to be in the order of 6–10
muscular activation or increase in muscle volume weeks. The initial training effect may be quite
are given priority. large, providing that there are no major inhibi-
tory factors, as discussed earlier.
Neuromuscular activation
assessment of neuromuscular
Important points to consider are time, assess-
activation
ment of the degree of neuromuscular activation,
contralateral effects of resistance training, and One way in the laboratory setting to identify lack
speed of force development. The specific nature of neuromuscular activation is the use of single
of the neural adaptation is relatively unknown superimposed twitch electrical stimulation (Behm
et al. 1996; Thomée et al. 1996). After identifying
Progress
the maximal intensity of the stimulus for a single Strength
twitch by successively increasing the signal dur-
ing resting conditions to get a plateau, one or
several single-twitch stimuli are given during
muscle actions with maximal voluntary effort. Hypertrophy
Electrical stimulation has mainly been used
during static muscle activity, whereas our know-
ledge is more limited concerning optimal neuro- Neural adaptation
muscular activation during dynamic muscle
actions. During these conditions, electrical stimu-
lation with tetanic trains has been used; however,
this requires considerably cooperation from the
subject due to the discomfort involved. It has
Time
been used to demonstrate the lack of maximal
activation at eccentric muscle actions (Westing Fig. 12.2 Schematic illustration of the contribution to
et al. 1990). increased strength from neural adaptation and
muscular hypertrophy. (Redrawn from Sale 1988.)
contralateral effects of
neural adaptation. In contrast, in the later stages
resistance training
of resistance training increases in muscle strength
It has been reported that by training one leg, the occur mainly by increases in muscle volume (Fig.
other leg also may improve and show strength 12.2) (Sale 1988). There is an increase in the size
gains. Improvements can be in the order of (cross-section) of the individual muscle fibres
35–60% of that attained in the trained limb leading to an increase in the total muscle cross-
(Kannus et al. 1992a). Such a possible effect of sectional area. Whether there will also be hyper-
contralateral training should be recognized and plasia (an increase in the number of muscle
possibly be used during rehabilitation after injury fibres) is more questionable, unless there is an
and immobilization of one extremity. injury of the muscle tissue. Besides an increase in
cross-sectional area, there may be other structural
changes of importance for force development
speed of force development
such as increases in: (i) the length of muscle fibres
Another aspect of muscle force development is due to an increase in the number of sarcomeres;
a shortening of the time for tension development (ii) the density of contractile proteins; and (iii) the
after activation (electromechanical delay). Speed intra- and extracellular connective tissue matrix,
of force development may decrease after immo- enhancing the proportion of the sarcomere force
bilization or surgery (Komi 1984) and can increase that can be transmitted to the skeletal system
with specific training. The force–time relation- (Enoka 1988).
ship may change using power training with high-
velocity contractions or explosive training models,
Muscle training methods
so that there will be a relatively faster force rise
early in the muscle activation (Häkkinen 1994). In principle, resistance exercise can be performed
with static (isometric) or dynamic muscle actions.
Dynamic exercise can be performed at a constant
Muscle volume
velocity throughout the range of motion, isokin-
As mentioned earlier, in the initial stages of weight etic action, or with a constant or variable load,
training for sports or rehabilitation purposes, but without control of movement velocity. The
increases in strength occur mainly because of activity can be concentric or eccentric. In addition,
electrical muscle stimulation can be used. The (Appell 1990). This might be explained by a
advantages of static exercise are that it can be maintained effect on the adaptation of the
used in the presence of limited joint mobility and muscle and may have clinical implications for
also that a pain-free joint angle can be chosen. elective surgical procedures. However, the clin-
However, there will be no training through the ical relevance and usefulness has to be studied
full range of motion and static exercises are often further.
considered ‘non-functional’.
Dynamic exercise with a constant weight can
Electrical stimulation
be easy to arrange, but will not match the pattern
of maximal torque through the range of motion Electrical muscle stimulation in the early phase
and may not accommodate resistance to pain. of strength training or during immobilization
Eccentric exercise, if not wanted, cannot easily be may promote neural activation by the afferent
avoided. During dynamic exercise with variable signals, reducing any pain and preventing or
resistance, the load and muscle torque can be overriding reflex inhibition. However, in order
matched and it may, thus, be very efficient. to enhance the central neural drive to the muscle,
However, special considerations may be needed electrical muscle stimulation has to be combined
to accommodate the resistance to pain as, for with voluntary muscle activation. At voluntary
example, only using part of the range of motion. activation the low-threshold motor units inner-
Isokinetic exerciseaconcentric or eccentricais vating slow-twitch type I muscle fibres will be
sometimes considered non-functional, but is a activated first, followed by the high-threshold
well-controlled method of activating the muscle fast-twitch type II fibres at a higher stimulus
through the full range of motion, reducing the intensity (Gollnick et al. 1974). During direct nerve
risk for overload. However, at the end of the stimulation, however, larger axons belonging
movement there will no load and thus no train- to the fast-twitch type II fibres will be activated
ing effect, for example, for end of knee extension. first, as they have the lowest excitability. Com-
Eccentric muscle action results in higher bining electrical nerve stimulation and voluntary
maximal torque than concentric muscle action muscle activation may have a synergistic effect.
(Westing et al. 1988). Neural activation is, how- However, no convincing evidence is available of
ever, not larger with eccentric muscle action as the recruitment order of motor units, and in fact
indicated by maximal electromyographic (EMG) during surface stimulation no difference from
activity, which may be lower than in concentric pure voluntary activation has been seen (Knaflitz
actions. Eccentric muscle actions increase the et al. 1990).
risk for muscle soreness, as demonstrated in a The order of motor unit activation with elect-
number of studies (Fridén et al. 1983). However, rical muscle stimulation depends on at least three
by producing greater muscle tension, eccentric factors: (i) the diameter of the motor axon; (ii)
muscle actions may enhance protein synthesis in the distance between the axon and the active
muscles and contractile tissues. The soreness electrode; and (iii) the effect of input to motor
after eccentric exercise will lessen over the first neurones from cutaneous afferents by the elec-
week of continuous training (Fridén et al. 1983). trical muscle stimulation. It has been demon-
As eccentric muscle action is part of many nat- strated in a number of studies that a combination
ural movement patterns, especially when the of electrical muscle stimulation and voluntary
stretch–shortening cycle is used, as in running, muscle activation may limit strength reduction
jumping or throwing, they should be included in during immobilization and in the early post-
training programmes at some point. operative phase (Arvidsson et al. 1986; DeLitto
It has been demonstrated that a short train- et al. 1988; Wigerstad-Lossing et al. 1988). It will
ing period before immobilization may help to also act to maintain muscle oxidative enzymatic
prevent muscle hypotrophy and loss of strength capacity (Wigerstad-Lossing et al. 1988).
with a specific speed. Another aspect is the eco-

Gender differences
nomy for body movement, as for running, with
There are indications that the effect of neural less energy consumption at a more economic
adaptation in strength training would plateau movement pattern.
somewhat earlier in women than in men There are many factors contributing to endur-
(Häkkinen 1994). The effect on muscle volume is, ance for whole body exercise, including the
however, more dominant in men than in women capacity of the heart with respect to maximal car-
reflecting different hormonal influences. In diac output and stroke volume, the distribution
women there may still be rather large interindi- of blood flow to active muscles and the ventilat-
vidual differences in training-induced muscle ory function and blood–gas exchange in the lung.
hypertrophy, depending on the actual serum Coupled to these is the metabolic capacity for
testosterone level (Häkkinen 1994). Even if cer- aerobic metabolism in the muscles. It is now well
tain specific aspects may be taken into considera- established that the maximal perfusion capa-
tion when training men and women, the general city of particular skeletal muscles is well above
principles and the phases during rehabilitation that which can be used for exercise with larger
are the same, with similar recommendations. muscle groups (whole body exercise) (Andersen
& Saltin 1985) and that the regulation of the peri-
pheral blood flow in relation to the pumping capa-
Strength training for children and adolescents
city of the heart is essential (Saltin et al. 1998).
No convincing scientific evidence supports Capillary density, leg blood flow and maximal
beneficial effects of using strength training for oxygen uptake all increase in similar proportion
prepubescent children. Until more convincing after physical conditioning (Saltin & Rowell 1980).
studies are presented strength training should be With immobilization there will be a rather
avoided in this age group or used with low intens- rapid reduction in the activity of the mitochon-
ity. Reasons for this are the imbalances between drial enzymes in the muscles (Appell 1990),
the maturation of the muscle, tendon and skel- which would also have an impact on the regula-
etal tissues. Using too heavy loads often results in tion of the central circulation contributing to the
frustrating set-backs due to overuse or overload increased heart rate at a certain submaximal
pain symptoms. To this can be added the absence exercise level. There will successively be a reduc-
of strength gains compared with non-strength- tion in the circulatory capacity towards the
training peers. Strength training can slowly be untrained state. Studies of immobilization and
added to postpubescent children but the training training of one leg have demonstrated the inter-
should be carefully monitored to avoid excessive action between peripheral and central adapta-
overload or overuse. tion to exercise at immobilization and training
(Saltin 1986).
Cardiovascular endurance
Training of cardiovascular endurance after
This section deals with endurance for more
sports injury
prolonged exercise, which is dependent on the
function of the cardiovascular and respiratory Endurance training should include activities
systems. The overall capacity of the system can that are easy to perform despite the presence
be defined as the aerobic capacity (maximal of any local body restrictions, such as remain-
oxygen uptake). Endurance is defined as the ing pain, limited joint motion, reduced muscle
ability to sustain prolonged aerobic exercise with strength and local muscular fatigability. By tradi-
an acceptable level of homeostasis, expressed, tion, exercises where the effect of bodyweight
for example, as a percentage of maximal oxygen is reduced, such as swimming, pool exercises,
uptake or absolute power output or distance bicycling and rowing machines, are used.
An important consideration is the possible • Increase the circulation of blood and joint fluid
interaction of concurrent strength and endur- with low loading exercises performed several
ance training (Leveritt et al. 1999). During such a times daily to aid in the healing process, to pre-
training regime the increase in strength may be serve range of motion and to accustom the
reduced or limited compared with pure strength tissues to an increasing load.
training, but the understanding of such an inhibi- • Maintain strength, endurance, range of motion
tion is limited at present. Various combinations and function for the rest of the body.
of resistance and endurance training have to be
studied to further understand the interactions.
rehabilitation techniques
Whether, and to what extent, this also applies to
training starting from an immobilized state, During the first phase emphasis should be on the
as after an injury or surgery, is not well known. reduction or elimination of any reflex inhibition.
Hypotheses based on acute (caused by residual Pain, joint effusion and inflammation should
fatigue after endurance training) and chronic (lack be addressed with proper clinical management.
of possibility to adapt metabolically and morpho- Therefore local anaesthesia, analgesics, transcu-
logically to both strength and endurance train- taneous electrical nerve stimulation (TENS) and
ing simultaneously) effects have been suggested. acupuncture may serve an important role during
Endurance training even with resistance training this phase.
superimposed may tend to reduce or limit the The last decade has also shown that physical
increase in muscle fibre size seen after resistance exercises can be used with good results during
training alone. These aspects have to be taken the acute phase (Kannus et al. 1992b, 1998). Thus
into consideration when designing training pro- immobilization can be replaced with specific
grammes, especially in the later stages after range of motion exercises and active muscle act-
immobilization and sports injuries in athletes ivation exercises. Three to five specific exercises
participating in sports that require both strength with a low load (0–30% of 1 RM) and with many
and endurance. repetitions (20–50) could be recommended. These
exercises should be performed several times per
day.
Principal rehabilitation techniques
There are several factors that can explain the
A gradually increasing training programme, beneficial effects of an early active mobiliza-
with appropriate and continuously adjusted tion after injury. With exercise there is an
exercises, is probably the most important tool increase in blood flow, increasing the exchange
during rehabilitation after a sports injury. The of nutrients and removing waste products
rehabilitation programme can be divided into from the injury site. The tension created in the
three different phases, not rigidly separated from injured tissue serves as a positive stimulation
each other, but with a more or less obvious over- for tissue repair. The neuromuscular activa-
lap of different treatment approaches between tion from exercises used in early mobilization
the different phases. preserves coordination. Tension, compression,
torsion, distraction and angular displacements
at various speeds are necessary to maintain
First phase (acute phase)
proprioceptive functions. The triggering of
endorphin release achieved with active muscle
rehabilitation goals during
activation can be beneficial, resulting in pain
the first phase
reduction and subsequent improved neuromus-
• Minimize the magnitude of the injury by cor- cular activation (Thorén et al. 1990). With early
rect acute management. mobilization, range of motion can be preserved
• Reduce or minimize loading of the injured and, for example, joint fibrosis can be avoided or
tissue. minimized.
To achieve a more than voluntary activated training sessions per week are recommended.
muscle force, superimposed electrical stimula- At the same time the load is gradually increased
tion can be used during early immobilization. with a goal to reach 70–80% of maximal. At this
For optimal muscle effect the electrical stimula- level an optimal muscle hypertrophy can be
tion should be given simultaneously with max- anticipated. No major inhibitory influences should
imal voluntary activation, as discussed above. No be present and an adequate motor recruitment is
randomized and double-blind studies are found necessary. Therefore, at this stage, the training
in the literature studying the effects of electrical can be non-specific and various weight-training
muscle stimulation during sports injury rehab- equipment can be used, such as leg-extension,
ilitation. However, superimposed electrical leg-curl and leg-press weight machines. The use
stimulation has been suggested for the recovery of repetition maximum (RM, the maximal load
of quadriceps and hamstring muscle strength that can be lifted a given number of repetitions
during rehabilitation after reconstruction of the within one set) is a common method of determin-
anterior cruciate ligament (Arvidsson et al. 1986; ing the load used in resistance training. For
Wigerstad-Lossing et al. 1988; Snyder-Mackler increased maximal strength 1–5 RM are used,
et al. 1995). It should be recognized that the whereas 8–12 RM results in muscle hypertrophy.
placebo effect may have contributed to these During the late phases of anterior cruciate liga-
effects. Also, the positive effect of increased ment (ACL) rehabilitation, slow and moderate
motivation, with increased training effort and improvements of quadriceps muscle strength
compliance, may have contributed to the results. and size have been reported (Risberg et al.
1999). This may indicate that rehabilitation pro-
grammes should have a greater emphasis on
Second phase (training phase)
training for muscle volume and strength (i.e.
high-intensity weight training using heavy loads
which activate both high- and low-threshold
the second phase
motor units). Restoring muscle volume and
• Increase load tolerance of injured tissues. strength is a cornerstone in rehabilitation, there-
• Improve balance and coordination. fore weight training, with the optimal amount of
• Improve muscle strength and power and resistance required for a maximal muscle growth
muscular endurance by gradually increasing process to occur, must be considered an essential
loads and degree of difficulty regarding balance training programme variable.
and coordination, using more demanding sport- Interestingly, in sports training, as opposed to
specific exercises. the rehabilitation field, a number of empirically
• A gradual change from one to two training based strategies have been developed through
sessions per day at the beginning of this phase to the years to maintain a positive response to long-
three or four highly demanding sessions per term weight training (Fleck & Kraemer 1997).
week at the end of the phase. Thus, in advanced weight training various systems
(e.g. periodization or organization of training into
distinct periods) and methods (e.g. supersets,
forced repetitions, power factor training and pre-
In the second phase the injured tissue and exhaustion) are used to avoid performance to
surrounding muscles can withstand higher loads plateau, and for bringing about optimal gains of
and thus be more actively mobilized. The treat- strength and muscle hypertrophy (Sisco & Little
ment programme should be concentrated on the 1997; Bompa & Cornacchia 1998). However,
recovery of muscle mass. The number of repeti- current scientific knowledge of these practical
tions used in the various exercises during the strength- and power-training principles is poor.
first phase is therefore gradually lowered to Isokinetic training and testing equipment has
8–12. Two to three sets per exercise and three been recommended for many years. However,
the validity, reliability and sensitivity has been (e.g. axial loading) and joint geometry probably
strongly questioned during recent years (Gleeson play integral roles in knee joint stability during
& Mercer 1996; Stone et al. 2000). In well- closed kinetic chain exercise (Isear et al. 1997).
controlled studies, isokinetic training, previously Significant coactivation of the antagonists during
thought to be superior, has been found to be infer- maximal knee flexion/extension, indicating an
ior to other training modes (Stone et al. 2000). inhibitory mechanism which prevents overload-
Isokinetic testing is still the most commonly used ing of the joint and contributes to joint stabiliza-
strength testing procedure, but it is suggested tion (Kellis & Baltzopoulos 1998), would explain
that greater familiarization with the technique is the low ACL tension forces during open kinetic
needed, and several pre- and postevaluations, in chain exercise.
order to improve testing reliability and sensitiv-
ity (Gleeson & Mercer 1996; Stone et al. 2000).
Free weights and weight machines
Most athletes use resistance training, involving

Closed and open kinetic chain exercises
both free weights and weight machines, to im-
There is a debate concerning the use of closed prove strength and power. The pros and cons
versus open kinetic chain lower limb exercises of training with free weights versus weight
during rehabilitation. Studies have compared the machines are, as closed and open kinetic chain
effect of closed versus open kinetic chain lower training, widely discussed among athletes and
limb exercises on knee ligament strain (Henning coaches, among physical therapists, as well as
et al. 1985; Yack et al. 1993), anteroposterior in sports science. Differences of opinion exist as
tibiofemoral translation (Panariello et al. 1994) to which method results in optimal performance
and patellofemoral compression forces (Gooch gains. Proponents of free weights emphasize
et al. 1993; Steinkamp et al. 1993). The import- functionality and a direct application to sporting
ance of using closed kinetic chain rehabilitation activities (Panariello et al. 1994). Conversely, the
(De Carlo et al. 1992; Shelbourne et al. 1995) and advocators of weight machines stress safety and
evaluation (Wilk et al. 1994; Greenberger & less requirements of coordination as compared
Paterno 1995) has been stressed. However, few with free weight training (Kraemer & Fleck
studies have investigated whether the effect of 1993).
closed versus open kinetic chain weight training In studies comparing free weights versus
on strength and performance differs. weight machines or closed versus open kinetic
Despite several studies (Yack et al. 1993; chain weight training, a dilemma exists in creat-
Beynnon et al. 1997) concerning safety issues ing matching training conditions, e.g. equating
of closed and open kinetic chain exercises in ACL total volume of training, total work and total
rehabilitation, and although some authors have training time. Moreover, as the weight does
advocated the sole use of closed kinetic chain not vary in free weight exercise, the resultant
exercises (Shelbourne & Nitz 1992; Bynum et al. torque, and therefore the required muscular con-
1995), it is concluded that both types of exercises traction, does vary according to the mechanics of
can be performed in ways that do not place the specific exercise. Weight machines, on the
excessive strain on the ACL (Fitzgerald 1997). other hand, operating through, for example, a
Escamilla et al. (1998), comparing knee joint cam, enable variable resistance throughout the
biomechanics while performing closed and open range of motion of an exercise. This is an attempt
kinetic chain weight training at a 12 RM load, to approximate the strength curve of the exercise,
reported that peak ACL tension forces in open thus forcing the muscle to contract maximally
kinetic chain exercise were only 0.2 times body- throughout the range of movement.
weight, and non-existent in closed kinetic chain A barbell squat is a free weight, closed kinetic
exercise. Factors such as joint compressive forces chain exercise, involving muscles working across
r = 0.64
(41%)
r = 0.51 r = 0.57
(26%) (32%)
Fig. 12.3 Correlation between a closed kinetic chain test (barbell squat 3 RM) and an open kinetic chain test
(concentric isokinetic knee extension), respectively, and the test of functional performance (vertical jump) in
healthy male subjects. (From Augustsson & Thomeé 2000.)
multiple joints. Athletes using resistance train- sporting activities. However, the isokinetic knee
ing often include a barbell squat programme extension exercise, though not activating the
to improve lower extremity strength. Several stretch–shortening cycle, has advantages such
studies have shown positive effects from a bar- as greater control over velocity of motion, tech-
bell squat exercise programme on strength and nique and extraneous movement, which facil-
athletic performance (Thorstensson et al. 1976; itates measurement reliability and objectivity
Fry et al. 1991; Hickson et al. 1994). (Abernethy et al. 1995). Augustsson and Thomeé
Weight machine exercises, using muscles work- (2000) showed that a similar correlation existed
ing across only single joints in an open kinetic for both closed (r = 0.51) and open (r = 0.57) chain
chain, are also commonly used to improve lower testing with a vertical jump. However only
extremity strength. The specificity of free weight 26–32% of jumping ability was explained by the
and weight machine training is a critical issue, strength in the closed (r 2 = 0.26) and open (r 2 =
demanding accurate and sensitive tests to prove 0.32) chain tests (Fig. 12.3).
the superiority of one method over another. Dyn- Much time and effort is initially spent learn-
amic (isotonic) testing such as a barbell squat or a ing proper technique when training with free
vertical jump, activating the stretch–shortening weights. Conversely, weight machines are prob-
cycle (Komi 1987), could be argued to be more ably less difficult to master as they allow move-
valid than isokinetic testing when assessing ment in only one plane and direction. Therefore,
it is theorized that weight machines cause greater

gains of training load in short-term weight-
training programmes. According to Sale (1988),
increased performance as a result of weight
training that lasts less than 20 weeks is asso-
ciated mainly with neural adaptation, such as
increased motor unit activity of prime mover
muscles, and improved coordination, i.e. appro-
priate changes in the activation of synergists and
antagonists.
Single-joint weight machine exercises allow a
superior function of synergists and antagonists,
enabling a high activation of motor units in Up on both feet! Slowly down
prime mover muscles, as opposed to complex, on one foot!
multi-joint free weight exercises where full
Fig. 12.4 Eccentric strength training for the ankle
motor activation is probably more difficult to
plantor flexors.
achieve due to greater demands of coordination.
This theory is supported by recent studies in
which open kinetic chain training resulted in
larger increases of training load (Augustsson eccentric training and higher concentric strength
et al. 1998) and muscle hypertrophy (Chilibeck gains using concentric training. A more interest-
et al. 1998) than closed kinetic chain training in ing issue is, however, if eccentric strength train-
short-term weight training. ing results in higher or faster strength gains,
eccentrically or concentrically, than traditional
concentric/eccentric training. No definite answer
Eccentric training
can be found in the literature, thus more research
Eccentric training is different from traditional is needed. However, some studies, randomized
concentric/eccentric training in that a higher and controlled, show better results with eccentric
load is possible during eccentric training. How- training programmes compared with concen-
ever, the same types of exercises, with the same tric/eccentric training programmes for patients
number of repetitions, sets and frequency of with chronic pain from the Achilles tendon (Mafi
training, can be used. The higher load can be et al. 2000; Grävare Silbernagel et al. 2001).
accomplished in different ways. For example,
in the sitting knee extension exercise the weight
Muscle power training
can be lifted concentrically with both legs and
lowered eccentrically with one leg. The same As muscle strength and load tolerance increases,
principle applies to exercise in the standing posi- the total load on the musculoskeletal system
tion (Fig. 12.4). Another way is to have a train- can be further increased. When close to normal
ing partner help during the concentric phase. strength is achieved, muscle power training
Current isokinetic dynamometers allow specific and plyometrics (mainly reactive throwing and
heavy eccentric loading. jumping exercises) can gradually be added to
During normal concentric/eccentric weight the rehabilitation programme, stressing time to
training higher improvements have been noticed peak muscular tension as well as stressing the
both in concentric and eccentric strength gains stretch–shortening cycle. It is recommended that
compared with concentric-only weight training maximal or close to maximal muscle power
(Dudley et al. 1991). Further, Higbie et al. (1996) training and plyometrics (Fig. 12.5) are added to
reported higher eccentric strength gains using the training programme once or twice per week.
Fig. 12.5 Examples of a plyometric exercise for muscle power training.
Three to five exercises with two to three sets of

Third phase (return to sports phase)
10–15 repetitions and with a total training time of
10–15 min is sufficient. Thus the rehabilitation
programme should use free weights (barbells
the third phase
and dumbbells), medicine balls, throwing imple-
ments and various jumping exercises. Häkkinen • Regain maximal balance and coordination
(1994) showed that explosive-type training (i.e. during maximally loading exercises as well as
power training and plyometrics) had a positive maximal endurance exercises.
effect on the maximal average integrated elec- • Regain maximal running, jumping and throw-
tromyography (IEMG)–time curve of the leg ing capacity.
extensor muscles. Also, positive effects were • Resume sports activity by implementing sport-
shown with explosive-type training on the aver- specific exercises with maximal loading and
age isometric force–time curve with a higher maximal demand on range of motion, strength,
speed of force development, compared with endurance and coordination.
heavy resistance training.
Muscular endurance
The third phase can be arbitrarily defined to start
If the general overall goal during the second when the muscle has regained sufficient volume,
phase is to also improve muscular endurance, strength and endurance to approach a minimal
many repetitions should be used with very short level needed for various functional activities.
rest pauses of only a few seconds in between sets. Individuals have different functional needs, and
This type of muscular endurance training can be the limitations will therefore vary according to
performed daily with close to maximal intensity. the sport. A common feature, however, is the
Such a programme may increase endurance need for further improvement in muscle struc-
as well as strength and aerobic capacity of the ture and activation, as well as improved motor
muscle (Grimby et al. 1973). control and coordination.
It has been noticed that despite ‘aggressive’ maintained with a circuit weight programme
rehabilitation with early mobilization, full strength (Gettman et al. 1979, 1982; Haennel et al. 1989).
and muscle mass is not achieved 1 year after ACL In these studies the participants trained 8–12
surgery (Arangio et al. 1997; Pfeifer & Banzer 1999). weeks, three times a week, using three circuits,
Pfeifer and Banzer (1999) concluded, in their with 8–10 exercises and with 20–30 s work and
study of 39 patients with arthroscopically assisted rest periods. Thus, an athlete sustaining an injury
ACL reconstruction, that insufficient rehabilita- can maintain certain aspects of cardiovascular
tion schemes and not inhibition explained the endurance by replacing, for example, running
large strength deficits seen 10–16 months after with an alternative form of cardiovascular
surgery. Despite this, many athletes resume their endurance training. However, the peripheral
sports at 6 months and sometimes earlier after muscular endurance close to the injury is more
ACL reconstruction. It is thus not surprising that difficult to maintain and is limited to the recov-
reinjury is common or that a new injury occurs. ery of the injury.
In many sports the musculoskeletal system is
exposed to extreme loads. For example, during
References
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Chapter 13
Proprioception and Coordination

JUAN JOSÉ GONZÁLEZ ITURRI
Sherrington’s contributions are fundamental

Introduction
due to his classification of sensitivity (Asirón
Proprioception can be defined as ‘a special type Yribarren 1991):
of sensitivity that informs about the sensations of 1 Exteroceptive sensation. This is external surface
the deep organs and of the relationship between sensation. It includes touch, pressure, pain, and
muscles and joints’. Coordination can be defined hot and cold temperatures, which are globally
as ‘the capacity to perform movements in a known as general exteroceptive sensations; it
smooth, precise and controlled manner’. also includes other more specialized sensations
Rehabilitation techniques increasingly refer such as sight, hearing and smell, which together
to neuromuscular re-education. These methods form special exteroceptive sensation.
have provided evidence of their efficacy and 2 Proprioceptive sensation. This covers a series of
reliability in athletes, where just recovering the impressions on the functional state of the joints
function of an injured joint is not sufficient, and muscles. If the individual is aware of these
and perfect rehabilitation is required. Muscle- impressions, this is conscious proprioceptive sensa-
strengthening techniques are not sufficient since tion (awareness of passive and active movements,
the neuromuscular and neuroarticular functions and the attitude or position of a somatic part of
need to be re-educated. It is therefore time for the body, kinaesthesia); if he or she is unaware of
rehabilitation to have a proprioceptive objective. them, this is called unconscious proprioceptive
Ligaments, tendons and joint capsules do not sensation (relating to balance, tone and muscular
just perform mechanical support functions or coordination). There is also a special propriocep-
induce movement. They are also the bearers of tive sensation, called labyrinthine.
deep sensitivity mechanoreceptors that gather 3 Interoceptive sensation. This is found in the
information on the position of the joints, or how viscera and vessels (pain, oppression, etc.) and
tendons and ligaments are stretched, and this is of a general nature; it can be divided in areas
information is sent to the base of the encephalon such as gustatory and olfactory.
through the upper cord, initiating an effective There are three types of sensation:
response, resulting in dynamic stabilization and 1 Deep sensation. This is the source of profound
therefore a balanced reaction. sensations, from pain to pressure, or sensations
of movement.
2 Epicritical superficial sensation. This corresponds
Neurological proprioception
to fine contacts, the special difference between
mechanisms
sensations, the perception of temperature and
With regard to proprioception, as in many other the location of painful and temperature-related
fields associated with the nervous system, sensations.
274
proprioception and coordination 275
3 Protopathic superficial sensation. This produces muscular rigidity beforehand could protect this
sensations of extreme pain and temperatures. joint against a ligament injury.
However, it is preferable to use less topo- For Strumpell (1924) the nerve endings in
graphic and more functional classifications and the skin are sensitive to stimulant disorders:
descriptions. Gley (1914) talks of the sensation mechanical, temperature-related and pain. He
of attitudes and movements as a synonym for claims that the deep parts of the muscles, fasciae,
muscular sensationsaawareness of the position periosteum and joints can only feel mechanical
of muscles in space and the sensation of passive pressure and distension stimuli, in particular
movements, together with active movements and tactile sensation referring to heat and cold, pain,
resistance. He establishes a series of divisions: pressure, mechanical distension, electrocutane-
• Kinetic impressions, sensations of attitude, ous sensation or sense of vibrations, and stereo-
continuous, articular and muscular sensations. gnostic sensation, which recognizes objects from
• Kinetic impressions, sensation of passive their size, shape, hardness, etc.
movement. The perception of passive movements For Sonjen (1986) the term exteroceptive is
depends on articular sensitivity. Nevertheless, obsolete, whereas proprioceptive is used extens-
according to Gley, it is very difficult for joint ively. He points out the utility of classifying
sensations alone to determine the perception somatic sensation as superficial or deep, cor-
of passive movements. responding to the excitation of cutaneous sense
• Kinetic impressions, sensation of active organs and proprioceptors.
movements. Perception is a complex phenom-
enon combining tactile, joint and muscular
Sensitive receptor organs
impressions.
The afferent nerves responsible for kinetic im- Superficial somatic sensation is caused by extero-
pressions are cutaneous, articular and muscular: ceptors, including: Pacinian corpuscles, mech-
• Cutaneous: these nerves are found in the fold anoreceptors for rapid, tactile and vibratory
and tension of the skin, and vary with the speed, adaptations; Merkel’s disks, mechanoreceptors
energy and length of the contraction. for slow adaptations, tactile and pressure sensi-
• Articular: articular anaesthesia reduces the tivity; Meissner corpuscles, also for rapid adap-
perception of active and passive movements. tations and tactile sensation; Krause bulbs or
• Muscular: these nerves arise in the Golgi tendon heat receptors; Ruffini corpuscles, slow adapta-
organs and in the bones. The latter sense move- tion mechanoreceptors for sustained pressure;
ment and the former sense tension (Grigg et al. and free endings for nociception and intense
1982). tactile and temperature stimuli (Burgess & Clark
• Feelings of central enervation, an efferent 1969; Burgess & Wei 1982).
nerve, which comes from the brain and precedes Deep somatic sensation is due to proprio-
the contraction. This is the sensation that an ceptors, found in articular receptors like the
effort has to be made, of force released in the Golgi organs, Ruffini corpuscles, Pacinian
brain to provoke a movement. corpuscles, free endings and Krause’s end bulbs;
Thounnard et al. (1986), in a critical study of and in muscular receptors like the laminated
the pathogenesis of a sprained ankle, reported Pacinian corpuscles, Kühne’s neuromuscular
that the passive structures are incapable of spindles, Golgi–Mazzoni tendinous organs and
absorbing the energy produced when jumping free endings (Table 13.1).
on to an unstable surface. The time required to
reach the calcaneotibial varus angle that causes
Spinal level
the capsuloligamentous rupture is less than the
reflex latencies observed in the muscles that stab- As afferent elements in the spine, we have those
ilize the ankle, so it is assumed that only active already described, and as efferent elements, the
Table 13.1 Sensory receptor organs.
Receptors Location Function
Superficial somatic sensation Pacinian corpuscles Rapid adaptations, touch, vibration

(exteroceptive) Merkel’s disks Slow adaptations, tactile sensation, pressure
Meissner corpuscles Rapid adaptations, tactile sensation
Krause bulbs Temperature receptors
Ruffini corpuscles Rapid adaptations, sustained pressure
Free nerve endings Nociception, tactile stimuli, endings
Profound somatic sensation
(proprioceptors)
Articular receptors Golgi receptors
Ruffini corpuscles
Pacinian corpuscles
Krause’s free endings Deep sensation
Muscular receptors Pacinian corpuscles
Kühne’s spindles
Golgi organs
Free nerve endings
final common pathway and as a response to the means of an interneurone. Sherrington’s law of
segmental and suprasegmental reflexes and vol- successive induction, a sequence of reciprocal
untary impulses, the motoneuron axonal process inhibition, expresses the ease of contraction of a
located in the anterior horn of the spine contri- muscular group when antagonist contraction
buting muscle fibres and provoking contraction. ceases.
The flexor withdrawal, or proprioceptive
reflex, response to the nociceptive afferences on
Reflexes
any structure, activating the flexor muscles and
In humans, the medullar reflex circuits play a inhibiting the extensors, which provokes bend-
decisive role in the control of movement. Some of ing of the stimulated limb and the extension of
them are monosynaptic, including the stretching the contralateral muscle.
reflex and passive muscular stretching, which
excite the annulospiral endings.
Cerebral cortex
When walking, monosynaptic stretching re-
flexes are inhibited. This has been verified by At the head of the hierarchy is the cerebral cortex,
examining the behaviour of the potentials evoked with two relief stations: the somatosensory area
when walking or standing; when walking, the and the motor areas, through which a transcor-
group I afferent signals are blocked, both on the tical loop of variable gain and relatively slow
segmentary and supraspinal levels. execution is established, unlike the segmen-
On the other hand, and unlike what happens tary loops of less improvement but much faster
when walking, segmentary stretching reflex activ- execution.
ity helps to activate the muscles that stretch the For afferent nerves, there are two ways in
legs during rapid movements such as running or which sensations reach the cerebral cortex to
jumping. become consciousathey are the lemniscal sys-
Polysynaptic reflexes are mutually inhibitory, tem that carries precise time and space informa-
since the same afferent nerves that determine the tion, and the indirect extralemniscal system,
myotatic reflex provoke antagonist inhibition by with imprecise space and time characteristics.
For efferent nerves, there is the pyramidal

Motor control and coordination
path, a prolongation of the pyramidal neurones
of the motor cortex that is directly and indi- How the nervous system is organized to control
rectly projected onto the motor neurones of and coordinate the neuromuscular function is
the anterior horn of the medulla, to which the much discussed and as yet unknown. It is an
voluntary motorial function is attributed (Dietz extraordinarily complex system, the capacity of
1987). which exceeds the most perfect of computers,
Finally, we have the extrapyramidal pathways and hypotheses on conscience, the thought pro-
that are projected on to the thalamus, nucleus cess, motor planning and execution are impos-
basalis, red nucleus and pontine nuclei; they are sible to prove. Such a complete organizational
involved in muscular tone, the regulation of process involves structures such as: the cerebral
movement and the regulation of posture. cortex, which inhibits and excites the lower
levels; the extrapyramidal system in charge
of integrating the excitation and inhibition
Conclusions
components, making them automatic by repeti-
Proprioception can be considered as the indi- tion; the corticospinal pyramidal path used to
vidual’s capacity to be aware of and recognize repeatedly excite the desired activity; and the
the instantaneous, static or dynamic situation of basic spinal reflexes, which are the origin of all
his/her body. According to classic propriocep- motor functions and sensitive feedback.
tion classifications, it is responsible for capturing The human brain, unremarkable in appear-
tension, force, spatial position, passive and ance, and weighing approximately 1500 g, is
active movements with speed, acceleration and evidently the most complex organization in the
amplitude, and the sensation of the structures, universe (Eccles 1969).
their situation and body limits (body schema). When referring to neuromuscular function, it
All nerve endings, both superficialageneral is common to use the terms motor control, to
exteroceptive and special (sight and hearing) define the excitation that voluntarily activates an
aand deepageneral proprioceptive (articular isolated muscle, and motor coordination, a more
and muscular), visceral, general interoceptive complex neuromuscular activity that needs to
and special (taste and smell)aare involved in integrate several elements to excite some mus-
proprioception. cles and inhibit others, to create patterns and
The nervous levels used include: the medullar sequences and thus to achieve functional body
segmentary level; the suprasegmentary level with movementsasomething that is very important in
the brainstem; and the cortical level, the activity sport.
of which is conditioned by specific and non- The literature uses the terms motor control and
specific sensory afferent nerves, as well as the coordination indistinctly, and includes many
reticular thalamic system, or humoral regulation, common models and theories concerning how it
cortical regulation or feedback. is organized and learned. In any circumstance,
Cutaneous, articular, tendinous and muscular however, motor control is the result of a very
afferent nerves follow the lemniscal path to the important interaction between the individual,
somatognosic areas, alert the cerebral cortex and the activity and the surroundings (Fig. 13.1)
produce proprioceptive sensation. (Acebes et al. 1996).
The use of proprioceptive mechanisms helps to
correct or perfect motorial abilities (propriocep-
Measuring proprioceptive
tive facilitation) and conscious proprioceptive
performance
perception provides awareness of posture and
recognition of the body schema, allowing for Proprioceptive afferent signals take place and
their eventual correction. influence the motor response on several different
Electromyography can provide an orientated

analysis of muscular function as the end-point of
Task
regulatory proprioceptive function. Conclusions
concerning possible influences can be obtained
by observing muscular movement within the
framework of the sensory motor function, but it
Motor
does not measure an immediate proprioceptive
control
function. However, it does have some advant-
Person Environment ages, because:
• studies can be performed under conditions
involving effort;
• the impact of training and the application of
Fig. 13.1 Different elements that have an influence on external stabilization aids, such as bandaging,
motor control. can be studied by their effect on muscular action
and regulation performance; and
levels. Modulator influxes are added in the pro- • the pathological parameters of activation can
cess of propagating and generating stimuli by be defined and identified.
means of the downward paths. Most of the inter- Up to now, recognition procedure results have
action between motor and sensory responses takes shown a decrease in the proprioception of major
place outside the voluntary perception level. joints in relation to typical injuries and dysfunc-
Psychophysical tests such as measuring the tions of the locomotive apparatus. It is difficult to
movement threshold or the capacity to repro- evaluate the role of proprioception in the origin
duce an actively and passively preorientated of injuries, since there are a lack of data con-
angle are the test procedures used to assess pro- cerning the proprioceptive situation before the
prioception. However, in sports our knowledge injuries occured.
of proprioception is highly limited, for several Studying the use of proprioception in sport, it
reasons: is possible to obtain epidemiological data and
• It is not known how isolated proprioception results from prior examinations:
mechanisms influence these tests. There are lim- • From the findings of psychophysical and elec-
ited conclusions, for example, an improvement tromyographic examinations, it can be deduced
in a test result does not necessarily mean that that injuries produce alterations to the special
there is a useful improvement in a person’s somatosensory and proprioceptive character-
proprioceptive function. istics of performance.
• The tests are performed while resting. It is not • Before a major injury occurs, there are fre-
possible to measure the possible proprioceptive quently earlier injuries that have been damaging
function that the individual is capable of under the proprioceptive structures.
effort. • Directed proprioceptive training essentially
• To what extent are the tests understandable reduces the frequency of injuries.
outside voluntary perception?
• Angular reproduction tests are not constant
The effect of an injury on
for individuals.
proprioception
• Training has a partially paradoxical impact.
It can worsen test results or influence different The natural history of, for example, the rupture
psychophysical test procedures in opposite ways. of the anterior cruciate ligament of an athlete’s
Training can also influence the results of psy- knee shows that, in spite of reconstructive surg-
chophysical test procedures. ical techniques and a good rehabilitation process
Table 13.2 Knee joint receptors.
Receptors Location Function
Ruffini corpuscles Capsule Stable and dynamic mechanoreceptors

Ligaments: LLI/LCA Information on:
Cartilage joint position
amplitude and speed of movement
intra-articular pressure
Slow adaptation
Pacinian corpuscles Intra and extra-articular fatty tissue Stable and dynamic mechanoreceptors
Capsule Information on:
Internal meniscus end of the movement
LLI sensitivity to acceleration and deceleration
Cartilage Rapid adaptation
Golgi–Mazzoni corpuscles LCA/LCP/LLI/LLE Dynamic mechanoreceptors
Internal meniscus Information on external joint positions
Slow adaptation
Free nerve endings Capsule Pain receptors
Ligaments Information on mechanical stimuli
Fatty tissue Slow adaptation
leading to a correct muscular situation, there is

Proprioceptive re-education
no guarantee that the treatment will be success-
techniques
ful. This leads us to consider that there must be
other factors, such as the enervation of the knee The treatments traditionally used for the
and the proprioceptive mechanisms, that are lost recovery of injured athletes reprogramme the
when the injury occurs (Table 13.2). proprioceptive receptors and their afferent and
Capsular ligamentous elements, as primary efferent pathways. This is specifically the case
passive structures, provide stability and normal for traditional kinesiotherapy, massage or mod-
kinematics to the knee joint. The presence of ern isokinetic methods. They all stimulate the
these receptor elements also means that, in addi- exteroceptive and proprioceptive systems.
tion to their mechanical function, they can act In all these techniques, stretching, when cor-
as dynamic organs by causing reflex synergic rectly applied, has an important proprioceptive
muscular activities. effect on the injured area, whether it be articular
The ligament injury, the resulting effusion, the or muscular. Stretching not only gets the muscu-
immobilization required for treatment, and the lar receptors working, but also the articular level,
following surgical trauma all produce alterations improving integration of the body, which is
to proprioceptive sensitivity, creating confusing fundamental in normal daily activities and sport
afferent messages that inhibit motor control and (Commandre et al. 1996).
sensory motor programming, thus increasing
the lack of stability by creating incorrect muscu-
Proprioceptive techniques
lar responses. Knee stability cannot be restored
without taking enervation into consideration Proprioceptive reprogramming can be achieved
(Jerosch & Prymka 1996; Lephart et al. 1997). using the following techniques.
(a) (b) (c)
Fig. 13.2 Different proprioceptive training situations.

(a) Balancing on unstable planes; (b) balancing on one
foot; (c) balancing whilst sitting; (d) sliding the foot
(d) along an unstable plane.
• The use of unbalancing forces, using either at the work of the strongest muscle groups and
unstable planes or applying destabilizers to an leading to the functional improvement of other
individual supported by a stable plane (Fig. 13.2). weaker, normally inhibited, groups.
Both these kinds of imbalance are involved in Individuals make integrated movements that
sport, since the articular segment and the entire affect muscle groups that are used to working
articular apparatus become involved in situ- together. Complete kinetic chains work together
ations with components of either. following a series of rules: movement of the seg-
• Reprogramming can also be achieved with the ments on the diagonal plane; a spiral component
proprioceptive neuromuscular facilitation tech- associated with each movement; and stretching
niques proposed by Kabat at the beginning of the stimuli which are used when applying maximum
1950s, consisting of the use of superficial and manual resistance.
deep information, such as the position of joints, For years, this method was essentially only used
tendons and muscles, contact with the therapist’s on patients with neurological disorders, but it is
hand, verbal orders and visual stimuli, all aimed now frequently used in sports-relate pathologies.
ball against a wall, forcing the individual to work

t h e u p p e r l imb s
to receive it.
The proprioceptive re-education of a limb is
always global, integrating the joints and the
Semiclosed and open kinetic chain exercises
entire limb in the locomotive apparatus, and
taking into consideration the limb’s function. Exercises using a stick held in both hands, while
Upper limbs are used for holding, picking up the physiotherapist unbalances it, are practical,
and throwing and lower limbs for walking, run- very simple and can be graduated as required.
ning, jumping and pushing oneself upwards. It This stimulates different positions, particularly
is necessary to analyse what the segment has to in relation to the shoulder. This exercise can also
achieve in each sport. Reprogramming a javelin be performed in a unilateral fashion.
thrower’s arm is not the same as reprogramming
a swimmer’s arm (Fig. 13.3).
The Kabat method
A basic exercise for the upper limbs is Kabat’s
Exercises on unstable planes
diagonal movements, using the scapulohumeral
Any of these exercises can be used, working in a joint as a pivot and starting with a flexion and
closed kinetic chain. To increase the lack of stab- cubital inclination of the wrist, a pronation of the
ility, pressure is brought to bear on a Freeman forearm, an extension of the elbow and with the
board, and the exercise is performed in the shoulder positioned with extension, abduction
quadruped position. Another variant is the use and internal rotation. Applying manual resist-
of a ball as a source of instability, while the indi- ance, the movement is towards a radial extensi
vidual is either standing or in a quadruped posi- on and inclination of the wrist, supination of
tion. On occasion it is fundamental to throw the the forearm, with the elbow continuing to be
(a) (b)
Fig. 13.3 (a) Proprioceptive training of the shoulder. (b) Proprioceptive training of the shoulder by pushing against
the physiotherapist.
extended, and the shoulder moving towards in the original position, and the hip with flexion
flexion, adduction and internal rotation. and external rotation (Blanc & Piur 1984; Bernier
The second starting position can be a radial & Perrin 1998).
extension and inclination of the wrist, a prona- The second diagonal starts with a sole flexion
tion of the forearm, extension of the elbow, and inversion of the foot, with the knee either
extension, adduction and internal rotation of bent or extended, and the hip extended with
the shoulder, moving towards a flexion and external rotation, moving towards an eversion
cubital inclination of the wrist, maintaining the and dorsal flexion of the foot, and flexion and
elbow extended, and with the shoulder moving internal rotation of the hip (Fig. 13.4).
towards flexion, external rotation and adduction. Initially, the therapy starts with a perimaleolar
massage, as there will probably be oedema, con-
tinuing with mobilization of the scar, if there is
the lower limbs
a scar, since scar tissue is occasionally adhered.
Using the Kabat technique with the upper limbs, Passive kinesiotherapy is then applied to all the
two basic diagonal movements are used on ankle and foot joints, which helps to assess the
which variations are then introduced. Something state of the articular movements so that the ath-
similar can be used after injuries to the lower lete becomes aware of the state of his/her injured
limbs (Knoff & Voss 1968). joint. These mobilizations should be smooth and
The first situation starts with a sole flexion and never exceed the pain limit.
an eversion of the foot (with the knee bent or This is followed by active and selective
extended) with the hip extended with internal unloaded work with the anterior tibial (flexion
rotation, moving towards a dorsal flexion and of the toes, varus of the foot and dorsal flexion
inversion of the foot, and maintaining the knee of the ankle) and peroneals (plantar flexion of
Fig. 13.4 (a) General

proprioceptive training acting on
a lower limb with upper limb
work. (b) Standing proprioceptive
(a) (b) work.
the ankle, flexion of the toes and varus of the

foot). These exercises are performed both freely
and with manual counter-resistance. The athlete
should always perform the entire exercise in bare
feet (Freeman 1965; Herveou & Messeau 1976;
Herveou & Messeau 1981).
Stage 1
This exercise starts with learning crispation of

the toes. The athlete should stand with the knees
extended, trunk straight, feet parallel and in line
with the coxofemoral joints and perpendicular
to the frontal plane. The movement is towards a
position in which the knees are extended and the
trunk is straight and bent forwards, following a
theoretical axis that passes through the malleoli.
The purpose of this exercise is to work the mus-
culature of the foot and adherence to the ground.
It is the first level of proprioceptive information
and the first state of alert.
Control of the anterior tibial is learned in the
same way. The initial position is the same as Fig. 13.5 Proprioceptive training on unstable planes
for the previous exercise, but with a 30° flexion of with the physiotherapist’s help.
the knees. The athlete bends forwards, imitating
the initial stages of a fall, positioning the lower
joints in an outwards turn. The physiotherapist
should make sure that the contraction of the cises reproduce all the situations of the foot when
anterior tibial is intense and that the outer edge it is in contact with the ground when walking,
of the foot is supported (Fig. 13.5). The purpose running and jumping. Therefore, the position of
of this exercise is the active maintenance of the the foot during the exercises is very important,
internal longitudinal arch of the foot. It is the with unipodal support during the first half step,
second level of proprioceptive information and which is when the load is greatest.
the second state of alert. The toes are crispated, the anterior tibial is
Another exercise is with the two feet on the tensed to maintain the internal longitudinal arch,
ground, knees extended, trunk straight, feet the big toe is firmly positioned on the ground
parallel and in line with the coxofemorals. The and the foot is perpendicular to the frontal plane.
physiotherapist is positioned behind the athlete Contact with the ground is thus at the heel, the
and on the side opposite the injury, pressing outer edge of the foot, the metatarsal heads, the
forwards and outwards. tips of the toes and the entire plantar face of
the big toe. Cutaneous information is maximal
and reproduces the foot’s three support phases
Stage 2
when walking. The knee is bent outwards at
What we have described above is the prepara- 30° to maximize the information captured by
tory phase for the remaining exercises that work the proprioceptive mechanoreceptors, with the
proprioceptively on the ankle, stimulating all the ligaments relaxed and maximum dynamic ankle
mechanoreceptors as much as possible. The exer- stability.
Work with unipodal support starts at the sec- Unbalanced surfaces can be grouped together,
ond or third session of treatment. The athlete and when athletes have good stability on this
positions the injured limb in front of the healthy equipment they can go on to other surfaces
one, separated by a normal step length, repro- where the instability is greater. At the end of the
ducing the correction position of the foot (toes progression, unipodal exercises can be performed
crispated, the anterior tibial tensed and the foot with a ball, medicine ball and/or sandbag.
perpendicular to the frontal plane), with the knee The material required is commonly found in
bent to 30°, then returning to the initial position. rehabilitation centres:
The difficulty of the exercise can be increased by • A rectangular board on two hemispheres,
increasing the angle at which the knee is bent or which will selectively work on the internal,
extended. external and anteroposterior muscular groups
of the lower limb, depending on the position
adopted.
Stage 3
• A circular board with a central spherical wedge,
At the third session, the athlete progressively which works on proprioception in a broader
starts the Freeman (BAPS) board exercises on the sense. It regulates lack of balance, depending on
three axes of the rectangular plane. When the the size of the hemisphere. It is even better if it is
exercises on the rectangular plane are no longer coated with a kind of synthetic lawn material,
difficult, work should start on the circular plane which adds cutaneous information to the pro-
(Gagey 1993). prioceptive reflex.
After the second week of therapy (after • A hanging balancing board, which provides
approximately 10 sessions of rehabilitation) the maximum difficulty both for the lower limbs and
athlete should start jumping, first on the floor, for the trunk.
then from the floor to the board and then from Within this framework, the athlete could work
board to board, adding exercises involving for 5 min on the balancing boards, going from
catching a ball on the floor and on the Freeman the simplest to the most complex, ending with
board (Freeman 1965; Heurte et al. 1991). unipodal support and catching a ball. The train-
At the last therapy sessions the athlete can run ing could continue with unipodal exercises on a
on a treadmill, beginning sports training com- soft carpet, where the athlete moves forward on
bined with continuation of medical rehabilitation. the balancing bench to jump on a trampoline.
From here he or she might move to the circum-
flex boards, after crossing a common area jump-
Adapting proprioception to training
ing from platform to platform.
Medicine’s role in sport is the treatment and,
above all, prevention of athletic injuries. We
Coordination training
must attempt, therefore, to adapt propriocep-
tion to training systems (Raybaud et al. 1988; Improving coordination depends on repeating
Caraffa et al. 1996). Individual attention is not the positions and movements associated with
always possible or desirable for athletes; a struc- different sports and correct training. It has to
ture accessible to several athletes at the same begin with simple activities, performed slowly
time needs to be considered. It is possible to and perfectly executed, gradually increasing in
combine sports training and proprioceptive speed and complexity. The technician should
training by installing an ‘athlete’s programme make sure that the athlete performs these move-
area’ next to the usual training area. These ments unconsciously, until they finally become
programme areas, which use proprioceptive re- automatic.
education methods and techniques, can vary in In the first place, coordination training requires
infinite ways and be adapted to different sports. the athlete to be willing to undertake the activity
(a)
Fig. 13.6 (a) Spinal column

proprioceptive training whilst
lying on one side. (b) Spinal
column proprioceptive exercise
whilst crawling. (b)
or to rest whenever he/she wishes; continuous precisely executing certain activities. For this
perception information of the activity is needed, training, the individual has to be old enough to
with perfect peripheral sensitive receptors from understand and follow instructions, be capable
the subcortical centres. This creation of an auto- of learning and cooperating, and be capable of
matic movement can only be achieved by volun- concentrating and avoiding fatigue. The recep-
tary repetition. tors, paths and centres have to be intact and there
The basis of coordination training is the inhibi- must be a movement span of at least 30°, free
tion of the motor neurones that are not involved of pain, at the joint affected by the muscle. Pain
in the movement desired. Although direct train- will lead to inhibition and, therefore, lack of
ing is not possible, this can be maintained by coordination (Cerda et al. 1996).
Burgess, R.C. & Clark, F.J. (1969) Characteristics of

Conclusions
knee joint receptors in the cat. Journal of Physiological
For treatment to be effective it has to be applied (London) 203, 317.
early. The purpose of re-education, depending Burgess, R.C. & Wei, J.Y. (1982) Signaling of kinesthetic
information by peripheral sensory receptors. Annual
on the aetiology and severity of the injury, is Review of Neuroscience 5, 171–187.
to restore the athlete’s functional possibilities. It Caraffa, A., Cerulli, G., Projetti, M., Aisa, G.Y., Rizzo,
has to lead to a rapid return to physical activity A. (1996) Prevention of anterior cruciate ligament
compatible with the competition level. injuries in soccer. A prospective controlled study
Proprioceptive re-education has to get the of proprioceptive training. Knee Surgergy, Sports
Traumatology, Arthroscopy 4 (1), 19–21.
muscular receptors working, in order to provide Cerda, M., Abril, C., Puig, J.M., San Segundo, R.
a rapid motor response (Scott et al. 2000). The & Aguilar, J.J. (1996) Ejercicios terapéuticos para
treatment has to be adapted to each individual, tratamiento del control y la coordinación motora.
considering the type of injury and the stress to Rehabilitación 30, 436–442.
which the athlete will be exposed when practis- Coarasa Lirón de Robles, A. (2001) Propiocepción en la
rehabilitación del LCA. In: Minutes of the 8th FEMEDE
ing his or her sport. Congress, Zaragoza. Spanish Federation of Sports
There is no test for proprioceptive training. Its Medicine, Pamplona: 137–142.
success can only be measured under controlled Commandre, F.A., Fourre, J.M., Davarend, J.P.,
conditions in which the training is assessed and a Raybaud, A. & Formanirs, E. (1996) Re-education
reduction of the injury is confirmed (Quante & and rehabilitation of the lesions of the athletes
locomotive system. Cinesiologie 35, 9–23.
Hille 1999; Coarasa Lirón de Robles 2001). Dietz, V. (1987) Role des afferences péripheriques
Proprioceptive re-education is not a synonym et des reflexes spinaux dans la fonction locomotrice
of exercises on unstable planes. It re-educates humaine normale et pathologique. Revue de Neurologie
‘unstable’ athletes who are going to practise 143 (4), 241–254.
sport on unstable planes (Lorza 1991, 1998; Eccles, J.C. (1969) The dynamic loop hypothesis of
movements control. In: Information Processing in
Lephart et al. 1997; Guegan & Nicolas 1999; the Nervous System (Leibovic, K.N., ed.). Springer-
Romano 1999). Verlag, New York: 245–269.
It is important to use proprioception when Freeman, M. (1965) Coordination exercises the treat-
treating athletic injuries (Fig. 13.6). Global work ment of functional instability of the foot. Physiother-
has to be carried out on the injured limb, using apy 5, 393–395.
Gagey, P.-M. (1993) La plate-forme de rééducation pos-
the body’s own mechanisms, which are capable turale. Annales de Kinesitherapie 6 (20), 331–334.
of being reprogrammed when practising sport Gley, E. (1914) Tratado de Fisiología. Edition Salvat,
again. It has to be carried out in an early stage Barcelona.
and cannot guarantee that there will be no fur- Grigg, P., Hoffman, A.H. & Fogarty, K.E. (1982) Pro-
ther relapses. perties of Golgi-Mazzoni afferents in cat knee joint
capsule, as revealed by mechanical studies of isolated
joint capsule. Journal of Neurophysiology 47, 31–40.
Guegan, C. & Nicolas, K. (1999) Propioception. EPS
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(1997) The role of proprioception in the management ‘el recorrido del deportista’. Archivos de Medicina del
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Chapter 14
Functional Rehabilitation and Return to

Training and Competition
W. BEN KIBLER AND T. JEFF CHANDLER
and biomechanics to interact optimally with the

Introduction
sport-specific demands.
The goal of function-based rehabilitation pro- Rehabilitation protocols are structured around
grammes is the return of the athlete to optimum frameworks of progressions of exercises, loads
athletic function. Optimal athletic function is the and applied and generated forces as the athlete
result of physiological motor activations creating improves his or her ability to generate and
specific biomechanical motions and positions control sport-specific forces. Our rehabilitation
using intact anatomical structures to generate protocol includes three phases: acute, recovery
forces and actions. Sport-specific function occurs and functional (Fig. 14.2) (Kibler et al. 1992). The
when the activations, motions and resultant patient progresses through each phase in a ‘flow’
forces are specific and efficient for the needs of dependent upon reaching certain criteria of injury
that sport. We use the ‘critical point’ framework healing and achievement of control of certain
(Fig. 14.1) to understand sport specificity. Every physiological and biomechanical functions. The
sport has metabolic, physiological and biomech- acute phase is a broad, relatively non-specific
anical demands inherent in the way the sport phase with goals of:
is played, at whatever level of skill or intensity. 1 Protection or healing of injured tissues.
Every athlete brings a specific musculoskeletal 2 Improvement of general flexibility and
base to interact with the demands. Performance strength.
in the sport and injury risk are the results of the 3 Improvement in the distant links in the kinetic
interaction. Sport-specific functional rehabilita- chains involved in the sport or activity.
tion should focus on restoration of the injured
athlete’s ability to have sport-specific physiology
Power Functional
Strength Sport specific
Inherent Endurance fitness
sport-specific Sports Flexibility
demands performance
Flexibility Recovery
Critical
Strength Power General sport
Individual point
Kinetic Chain Endurance fitness
Injury
musculoskeletal
risk Injury Surgery Acute
base
Modalities Bracing Injury healing
Fig. 14.1 The ‘critical point’ framework showing
the relationship between sports demands and the Fig. 14.2 Phases of the rehabilitation process. The start
musculoskeletal base in determining performance of rehabilitation includes all causes of injury, but the
and injury risk. end focuses on return to function.
288
functional rehabilitation 289
The recovery phase is a relatively long phase The other two phases have been discussed in
with goals of: earlier chapters.
1 Preparation for maximum physical activity. Upon entry into the functional phase, the
2 Improvement in kinetic chain linkage athlete must have healing of the anatomical
sequencing. lesion, restoration of the distant links in the
3 Normalization of any distant kinetic chain break- kinetic chain, general flexibility, endurance and
ages such as inflexibility or strength imbalance. strength, and be able to achieve the motions and
4 Setting up the strength and power base for positions necessary to play the sport or activity.
sport-specific progressions. The therapist and doctor must also know the
The functional phase is a focused phase, with demands of the sport or activity and the level
the goals of sport-specific flexibility, strength, of preparedness of the musculoskeletal base to
physiological activations, biomechanical motions work towards sport-specific progressions.
and functional progressions.
The functional progressions should simulate
Sport-specific demands
the actual activities required in the sport. Return
to play criteria are based on successful comple- There are many similarities in the demands
tion of the functional phase goals. The functional sporting activities in general place on athletes.
phase marks a transition between rehabilitation Most sports require some level of energy expend-
and prehabilitation, which can be defined as iture to generate the forces necessary to move the
conditioning strategies in the formerly injured body, ball or other object toward a certain goal
athlete to prepare him or her for the stresses and (Fig. 14.3). Most require some stability of one
demands inherent in the sport, and which must part of the body to achieve some move-
be faced in return to sport (Kibler & Chandler ment of another part (Fig. 14.4). Most require
1994). Prehabilitation focuses on sport-specific some degree of flexibility of some body parts
musculoskeletal areas that have been shown to (Fig. 14.5). However, each sport has its own set
be weak or susceptible to injury, or have actually of inherent demands, and these demands may
been injured, in a specific sport (Chandler 1995). change with the level of skill, intensity or fre-
In some sports, the musculoskeletal system adapts quency with which the sport is played. Thera-
to repetitive use by manifesting areas of muscle pists and doctors need to know these parameters
weakness or muscle tightness, or both. For ex- in order to prehabilitate the athlete properly.
ample, long-distance runners frequently are found Many different systems may be set up to profile
to have hamstring and gastrocnemius inflexibil- sports and their demands. They may be based
ity, baseball and tennis players are found to have on anatomical requirements (range of motion
shoulder internal rotation deficits, and female required, strength required), metabolic require-
soccer and basketball players have weakness of ments (aerobic or anaerobic activity) or amount
their glutei and hamstrings. These deficits are of contact (collision, frequent contact or minimal
still present after injury, and may be even worse contact).
as a result of the injury or treatment. The purpose We use an evaluation system that profiles
of the prospective programme is to condition the physiological requirements and the biome-
those areas of high tensile load and high injury chanical kinetic chains necessary to play the
risk, or those that are the ‘weak link’ after injury, sport (Kibler 1990). This method allows good
in a particular sport. Prehabilitation exercises discrimination between sports and generates
consist of strength, power, range of motion and enough information about the specific sport to
endurance exercises for the musculoskeletal plan an adequate prehabilitation programme
areas and movements identified in a particular that will be sufficiently specific for the sport.
sport. This chapter will describe the activities The five physiological parameters we use in-
that should take place in the functional phase. clude flexibility, strength, power (force × distance
Fig. 14.3 Team handball: Atlanta

1996, Korea versus Denmark.
(© Doug Pensinger, Allsport.)
Fig. 14.5 Gymnastics: Atlanta 1996, Shannon Miller

(USA). (© Allsport.)
(e.g. aerobic endurance in golf); 2, the parameter

is important in performance or injury risk reduc-
tion (e.g. flexibility in tennis or basketball); and
3, the parameter is essential for maximum per-
formance (e.g. aerobic endurance in running,
Fig. 14.4 Discus: Sydney 2000, Franz Kruger of South
strength in weightlifting). Each sport will then
Africa in the men’s discus final. (© Matthew Stockman, have a profile that can be used to meet the
Allsport.) demands. Table 14.1 lists some sports and their
resulting profiles.
per unit of time), anaerobic and aerobic endur- Similarly, each sport can be characterized
ance. We grade each sport from 1 to 3 based on by the kinetic chains necessary to perform the
the parameter’s importance in the sport: 1, the sport. Kinetic chains are patterned, coordinated
parameter is important for general body fitness sequences of body segment activation and motion
Table 14.1 Individual sport profile.
Flexibility Strength Power Anaerobic Aerobic
Basketball 2 2 3 3 3
Tennis 3 2 3 3 2
Golf 3 2 3 1 1
Soccer 2 2 3 3 3
Swimming 2 2 3 3 3
Running 2 1 2 1 3
Sprinting 3 2 3 3 1
Bicycling 2 2 3 3 3
Volleyball 2 2 3 3 1
Table 14.2 Sport kinetic chains.
Running Ground → Leg → Hip/trunk → Opposite leg → Ground

Throwing Ground → Leg → Hip/trunk/opposite leg → Shoulder → Arm
Serving Ground → Legs → Trunk → Shoulder → Arm
Golf Ground → Legs → Trunk → Shoulder/arm → Wrist
Kicking Ground → Plant leg → Trunk/opposite hip → Kick leg → Ball
Swimming Water → Hand/wrist → Arm/shoulder → Trunk/legs → Arm → Water
Shooting ball Ground → Legs → Arm/wrist → Ball
that are used to accomplish athletic tasks. Run- Functional musculoskeletal prehabilitation
ning has a slightly different kinetic chain than exercises can be strenuous as they replicate the
sprinting. Tennis has a different kinetic chain motions, positions, forces, intensities and muscle
than baseball pitching. Kicking a soccer ball has activations inherent in the sport. The athlete’s
a different kinetic chain than jumping after a body should have enough general athletic fitness
basketball. Table 14.2 lists some of the most com- to allow these vigorous activities without undue
mon sports and their predominant kinetic chain injury risk. The anatomical lesion should be healed.
patterns. The physiological muscle activations, flexibility
When the physiological and biomechanical and endurance capabilities should be capable of
requirements of the sport or activity are cat- withstanding the strength and power exercises.
egorized, exercises and progressions of load and The physician and therapist should monitor
intensity can be employed to prepare the body and test for these parameters as rehabilitation
for the sport. A runner will need back and leg progresses and as the athlete goes into the pre-
flexibility exercises, progressive aerobic train- habilitation protocols. For throwing athletes, the
ing with longer duration of training bouts, and general criteria should include hip and trunk
eccentric strength training of the legs to absorb control over the planted leg, trunk rotational
the closed chain loads in the stance phase. An flexibility and strength, control of scapular eleva-
ice hockey player will need anaerobic training tion and protraction, functional glenohumeral
for short bursts of activity and power training internal rotation, and rotator cuff co-contraction
in both the arms and legs. A baseball pitcher strength (Kibler et al. 2000). For running athletes,
will need arm and back flexibility, lower body general criteria should include gastrocnemius,
strength, power training to develop force, and quadriceps and hamstring flexibility, hip and
eccentric training for the arm to control decelera- trunk control over the planted leg, trunk extensor
tion loads. strength and aerobic capacity.
Athletes frequently have areas of inflexibility increasing internal rotation range of motion and
and weakness in other parts of the kinetic chain external rotation strength. Flexibility exercises
that may contribute to the injury or to decreased are performed after the throwing activity is com-
performance, and should be included in the plete for the day. Due to the high tensile loads
prehabilitation exercises. The frequency of these developed in the shoulder external rotators
distant alterations may be as high as 50–85% in and due to the inflexibility of the athlete in this
association with injury (Ekstrand & Gilquist area, a flexibility programme is warranted. For
1982; Kibler et al. 1991; Knapik et al. 1991; Warner strengthening, the goals of the training pro-
et al. 1992; Burkhart et al. 2000). gramme are to increase the strength of the scapu-
lar stabilizers and shoulder external rotators
while maintaining explosiveness in those mus-
Specific examplescprehabilitation
cles. Plyometric/agility drills are incorporated
protocols
into the prehabilitation programme as they may
The prehabilitation protocols should be based on reduce the risk of injuries related to these ballistic
progressions of flexibility, strength exercises, in- movements. In addition to the prehabilitation
creasing loads and durations, and progress from programme, it is assumed the athlete partici-
closed chain to open chain configurations. This is pates in a general resistance training programme
illustrated by specific protocols for: (i) tennis/ two or three times per week.
baseball, for overhead activities; (ii) running, for At this stage of healing and rehabilitation,
long distance and long duration; and (iii) soccer, physical therapy modalities (heat, ice, ultra-
for high-intensity power running and jumping. sound, stimulation) are usually not indicated.
Very little tissue alteration is expected at this
stage of healing that would be modified by these
Tennis/baseball
modalities. Some heat may be used to help in
increasing tissue pliability before the exercise
prehabilitation plan
bout, and cold may be occasionally used if there
The athlete should begin a shoulder flexibility is some swelling postexercise.
and strengthening programme focusing on
weeks 1–2
Flexibility (daily, after activity):

Cross body stretch, scapula stabilized 3 × 30 s
Internal rotation, scapula stabilized 3 × 30 s
Triceps stretch 3 × 30 s
Racquet stretch (Fig. 14.6) 3 × 30 s
Strength (3–5 × week):

Shoulder external rotators/scapula 3 × 25 reps (moderate speed)
retraction with tubing
Rows with dumbbells/tubing, elbows down 3 × 15 reps
Reverse flies with dumbbells/tubing 3 × 15 reps
Plyometric/agility (3–5 × week):

Five dot drill (Fig. 14.7) 2 × 20 foot contacts
Hexagon drill (Fig. 14.8) 3 × 15 s, double leg
The hexagon drill
6 2
Racquet stretch
Use racquet as
rigid rod between
both hands to 5 3
rotate shoulder
4
Fig. 14.8 The hexagon drill. Do in the sequence shown

and repeat three times.
Fig. 14.6 The racquet stretch. Use the racquet as a lever

to rotate the shoulder into internal and external
rotation (figure seen from behind).
Line drill (Fig. 14.9) 2 × 20 double leg foot contacts

2 × 20 single leg foot contacts
Footwork ladder, bounding (Fig. 14.10) 2 × 20 double leg foot contacts
Footwork ladder, quick feet 4 × 20 low-intensity foot contacts
Footwork sprints (carioca, shuffle, back pedal, 5–8 × 9 m
cross-over step, skip, high knee, etc.)
weeks 3–4

Cross body stretch, scapula stabilized 2 × 30 s
Triceps stretch 2 × 30 s
Racquet stretch 2 × 30 s
5-dot drill 1 2 Right leg 3 Left leg 4 Both feet

1–2 2 1 1
4 5
3 3 3 3 3
1m
1 2 5 5 4 5
0.5m 4 5 4
3 3 3
Fig. 14.7 The five dot drill. Each
1 2 2 sequence should be done in the
order listed and completed five
Do each sequence with 5 repetitions
times.
Ladder drill
Line drill Use a rope or other material, or
Any 'line' will do; tennis court side line, draw on the surface to make
baseball foul line, soccer touch line, the 'ladder'. Jump in and out
basketball side line. May go forwards of the squares, there are many
or backwards, landing on one foot or variations possible for this drill
both feet, or jump over/jump back
across the line
Fig. 14.9 The line drill. Jump back and forth across a
line, which could be a tennis court side line, baseball
foul line, soccer touch line, etc. Land on both feet
(double leg) or one foot (single leg).
Fig. 14.10 (right) The footwork ladder drill. Use a rope,

some other material or draw on the surface to make a
‘ladder’. Jump in and out of the rectangular areas;
many different drills can be done.

Shoulder external rotation/scapula 4 × 25 reps (high speed)
retraction with tubing
Rows with dumbbells/tubing, elbows down 4 × 25 reps (high speed)
Shoulder internal rotators with tubing 4 × 25 reps (high speed)
Medicine ball forehand 2 × 25 reps
Medicine ball backhand 2 × 25 reps
Medicine ball serve 2 × 25 reps
Plyometric/agility:
Five dot drill 2 × 20 foot contacts
Hexagon drill 4 × 10 s, single and double leg
Line drill 2 × 20 double leg foot contacts
Footwork ladder, bounding 2 × 20 double leg foot contacts
Footwork sprints (carioca, shuffle, back pedal, 10–15 × 4.5 m
weeks 5–6

Racquet stretch 2 × 30 s

Shoulder external rotation/scapula retraction 2 × 25 reps (high speed)
with tubing
Shoulder internal rotation with tubing 2 × 25 reps (high speed)
Plyometrics/agility:
Hexagon drill 5 × 10 s, single and double leg
Footwork sprints (carioca, shuffle, back pedal, 10 × 4.5 m
10–25% increases in work load, which are usu-

Running
ally safe progressions. Strengthening the ankle
while trying to improve ankle range of motion is
warranted. Flexibility of the hamstrings and gas-
It is suggested that the athlete should start prehab- trocnemius is stressed. Low-intensity plyometric
ilitation on a more forgiving surface for training and eccentric activities may help prepare the
purposes whenever possible, such as grass or a athlete to withstand the repetitive loads of run-
rubber track. The main goal of the prehabilitation ning, as well as improve explosiveness for the
programme is to allow the athlete to progress at kick at the end of the race.
weeks 1–4
The athlete is running 1.6–4.8 km, 3–4 days per week.

Lying hamstring stretch 3 × 30 s
Standing quadriceps stretch 3 × 30 s
Leg twists for iliotibial band 3 × 30 s
Wall calf stretch 3 × 30 s
Trunk sit and reach 3 × 30 s

Squats (light resistance) 3 × 20 reps
Lunges with light dumbbells 3 × 20 reps
Weighted heel raise 3 × 20 reps
Plyometrics/agility (3 × week, non-running days on grass):

weeks 5–8
The athlete is running 4.8–8 km on Monday and Wednesday and 8 km on Friday and Saturday.

Leg twists 3 × 30 s

Plyometrics/agility (non-running days on grass):

Line drill 2 × 20 single leg foot contacts
Bounding drill 2 × 10–15 foot contacts
weeks 9–10
The athlete is running 8–16 km on Monday and Wednesday and 16–24 on Saturday.

Strength (2 × week):
Plyometrics/agility (non-running days on grass):

Fartlek progressionsaalternating low-intensity/high-intensity running bouts (20 m jog → 10 m run →
10 m sprint)
Soccer
may recur if prehabilitation is not complete,
Soccer requires aerobic endurance, anaerobic because of the varied and large loads inherent in
capacity and power. It is common that injuries the demands.
weeks 1–3

Leg twists 2 × 30 s
Strength (3 × week, bodyweight as resistance):

Squats 2 × 20 reps
Forward lunges 2 × 20 reps
Side step/cross step lunges 2 × 20 reps
Heel raise 2 × 20 reps
Plyometrics/agility (3 × week):
weeks 4–6

Standing knee to chest 2 × 30 s
Strength (medicine ball or dumbbells as resistance):

Squats 3 × 15 reps
Heel raises 3 × 15 reps
Footwork springs (carioca, shuffle, back pedal, 5–8 × 18 m
weeks 7–10

Standing knee to chest 2 × 30 s
Strength (3 × week, medicine ball or dumbbells as resistance):

Squats 2 × 10 reps
Heel raises 2 × 10 reps
but do not represent total capabilities, and should

Criteria for return to sports
not be used as sole determinants of return to play.
The injured athlete must be anatomically healed It is more important to know if the athlete can do
and must complete all of the rehabilitation stages all of the functions required in play, rather than if
to be considered for return to sport. Understand- the athlete can generate torque at one joint.
ing the inherent demands allows an objective set It may appear that the criteria for return to
of criteria for return. Throwers must have sport- sport are rigid or easily determined. Actually,
specific functional range of motion of arm joints, the criteria should be employed with some lee-
stable scapula, trunk core stability and plyometric way, based on the athlete and the situation. The
power development in the leg, no matter where athlete should not be allowed to ‘play yourself
their original injury occurred. Runners must have into shape’, with no guidelines or input. This
leg flexibility, trunk core stability and aerobic allows deleterious kinetic chain substitutions and
endurance, no matter where their original injury increases the chances of reinjury (Devlin 2000).
occurred (Kibler et al. 2000). All injured athletes However, the athlete should not be ‘rushed’
must then complete sport-specific functional pro- through the prehabilitation protocol, because
gressions of throwing, running, jumping, kick- the sport-specific exercises do impose significant
ing or swimming. These exercises demonstrate demands, once again increasing the chances of
that the athlete has the physiology and biome- reinjury.
chanics necessary to withstand the inherent Experience has taught us the value of gradual
demands of the sport. return to play, with emphasis on steady pro-
Some authors have advocated return to sport gression of exercises, strict attention to the pre-
based on quantitative criteria such as quadri- paredness of the musculoskeletal base for new
ceps/hamstring ratios in runners or internal exercises, involvement of the kinetic chain, and
rotation/external rotation ratios in throwers. resolution of both the local and distant altera-
These ratios are usually based on isokinetic data, tions that may exist in association with the injury
which have not been conclusively shown to be (Kibler et al. 1991, 1992).
associated with true muscle capability. These Return to play is completed by a sport-specific
ratios can be helpful in determining weaknesses, functional progression of doing the specific
Table 14.3 Interval throwing programme starting off the mound.
Stage 1: fastball only Use interval throwing to 36 m phase as warm-up

Step 1: Interval throwing
15 throws off mound 50%
Step 3: Interval throwing All throwing off the mound should be done in
45 throws off mound 50% the presence of your pitching coach to stress
Step 4: Interval throwing proper throwing mechanics
Step 6: 30 throws off mound 75% Use speed gun to aid in effort control
Step 7: 45 throws off mound 75%
Stage 2: fastball only

15 throws in batting practice
Stage 3
Step 12: 30 throws off mound 75% warm-up
15 throws off mound 50% breaking balls
45–60 throws in batting practice (fastball only)
30 breaking balls 75%
60–90 throws in batting practice 25% breaking balls
Step 15: Simulated game: progressing by 15 throws per
work-out
activity. Table 14.3 illustrates a sport-specific gramme requires knowing the end-point—the
throwing progression (Andrews & Wilk 1996), set of anatomical, physiological and biomechan-
while Fig. 14.11 illustrates a sport-specific soccer ical parameters the athlete will need in order to
progression (Kibler & Naessens 1996). meet the demands inherent in participation in
that sport. Sport profiling is key to this know-
ledge. The functional phase of the rehabilitation
Conclusions
protocol must emphasize acquisition of sport-
Optimal return to sport requires not only rehabili- specific parameters, and then shades into prehab-
tation of the general athletic fitness parameters ilitation, a maintenance programme to continue
for sport, but also the specific parameters for to improve sport-specific fitness. Criteria for
fitness in a particular sport or sporting activ- return to play must emphasize gradual return to
ity. Devising a sport-specific rehabilitation pro- sport-specific functional progressions.
Soccer field run
6
9 1 Sprint
4
2 Jump and head a ball
3 Run around cones
4 Run backwards
5 Pick up soccer ball
6 Dribble around cones
8 7 Three running jumps
3 8 Plyometric jumps over lines
7
9 Sprint
1 Fig. 14.11 Return to soccer

2 functional programme. The
drill encompasses all of the
Start soccer-specific demands.
Medicine Book (Garrett, W.E., Kirkendall, D.T. &

References
Contigulia, S.R., eds). US Soccer Federation,
Andrews, J.R. & Wilk, K.E. (1996) Throwing Progressions Chicago, Illinois: 147–167.
for Return to Baseball. American Sports Medicine Kibler, W.B., Goldberg, C. & Chandler, T.J. (1991)
Institute, Birmingham, Alabama. Functional biomechanical deficits in running ath-
Burkhart, S.S., Morgan, C.D. & Kibler, W.B. (2000) letes with plantar fasciitis. American Journal of Sports
Shoulder injuries in overhead athletes. The ‘dead Medicine 19, 66–71.
arm’ revisited. Clinical Sports Medicine 19, 125–159. Kibler, W.B., Chandler, T.J. & Pace, B.K. (1992) Prin-
Chandler, T.J. (1995) Exercise training for tennis. ciples of rehabilitation after chronic tendon injuries.
Clinical Sports Medicine 14, 33–46. Clinical Sports Medicine 11, 661–673.
Devlin, L. (2000) Recurrent hamstring symptoms in Kibler, W.B., McMullen, J. & Uhl, T.L. (2000) Shoulder
rugby. Sports Medicine 29, 279–287. rehabilitation strategies, guidelines, and practice.
Ekstrand, J. & Gilquist, J. (1982) The frequency of mus- Operative Techniques in Sports Medicine 8, 258–267.
cle tightness and injuries in soccer players. American Knapik, J.J., Bauman, C.L., Jones, B.H. et al. (1991)
Journal of Sports Medicine 10, 75–78. Preseason strength and flexibility imbalances associ-
Kibler, W.B. (1990) The Sports Preparticipation Exam. ated with athletic injuries in female college athletes.
Human Kinetics, Champaign, IL. American Journal of Sports Medicine 19, 76–81.
Kibler, W.B. & Chandler, T.J. (1994) Sports specific Warner, J.J.P., Micheli, L., Arslenian, L.E. et al. (1992)
conditioning. American Journal of Sports Medicine 22, Scapulothoracic motion in normal shoulders and
424–432. shoulders with glenohumeral instability and impinge-
Kibler, W.B. & Naessens, G.C. (1996) Soccer pre- ment syndrome. Clinical Orthopaedics and Related
participation physical exam. In: The US Soccer Sports Research 285, 199–210.
Chapter 15
Orthoses in the Prevention and

Rehabilitation of Injuries
WILLIAM MICHEO AND ALBERTO ESQUENAZI
prescribed to enhance mediolateral joint stability

Introduction
may produce a compensatory overactivation of
Advances in fabrication, increased availability the hamstrings that increases the likelihood of
and patient interest over the past few decades tendonitis (Esquenazi & Talaty 1996). In addition,
have contributed to the proliferation of orthotic they may increase energy expenditure or raise
use in sports and other areas of medicine. At intramuscular pressure in the anterior leg com-
the present time a more complete scientific partments of the athletes that use them (High-
understanding of the functional mechanism of genboten et al. 1991; Styf et al. 1992).
orthoses and how the body responds to them is The process of orthotic prescription is still sub-
needed to further increase the efficacy of this jective and evolving; it is dependent on the clini-
intervention. The usefulness of bracing for the cian’s understanding of the injury, acquired skill
prevention or treatment of lower limb joint in- and knowledge of the principles of physics and
stability, particularly of the knee, has been con- biomechanics. In addition, it requires a working
troversial, with clinical and biomechanical data knowledge of brace types, materials, functional
pointing in opposite directions (Cawley et al. design and the requirement of the sport, which in
1991). In addition, a lot of the information avail- general are not part of routine clinical training.
able to the clinicians about orthotics and their use Development of new materials and fabrica-
in sports medicine is provided by the manufac- tion techniques in the last decade have greatly
turers of the devices. increased the range of applicability of orthoses
Advances in applied biomechanics, motion to a wide variety of clinical situations in sports
and gait analysis have helped considerably by medicine. Due to this, braces are lighter, stronger,
allowing critical parameters to be accurately better fitting, more durable and perhaps more
measured in the athlete, thus infusing objectivity effective. These advances in brace construction
in the process of orthotic prescription and the allow clinicians to generate almost any com-
clinical management of injury (Esquenazi & Talaty bination of biomechanical features, that may be
1996; Zheng & Barrentine 2000). specific for a particular clinical problem and
However, the question of exactly what is the most beneficial for the athlete (Esquenazi &
best orthotic device for a given injury, and how a Talaty 1996).
brace may provide improved function for an ath-
lete participating in sport, is still not completely
Terminology and classification
clear. Prescribed orthoses may impair some of
the normal biomechanical functions that coexist The International Standards Organization of the
in the injured limb or may force compensation in International Society of Prosthetics and Orthotics
other anatomical sites. For example, a knee brace has defined an orthosis as ‘an externally applied
301
device used to modify structural and functional Table 15.1 Classification of orthotics.
characteristics of the neuromusculoskeletal sys-
Biomechanical
tem’. Orthoses are applied to the external sur-
Design characteristics Clinical function
face of the body to achieve one or more of the
following: to relieve pain, resist abnormal joint Static Corrective Preventive
motion, reduce axial load, stabilize musculoskel- Dynamic Accommodative Functional
etal segments, prevent or correct joint deformity Rehabilitation
and improve function while permitting joint(s)
movement (Redford 2000).
Orthotics in the past have been classified into Rehabilitation braces are primarily intended to
two major categories: static and dynamic. Static reduce pain and protect the joint immediately
orthoses are rigid and give support without after an injury or during the initial postoperative
allowing movement. Dynamic orthoses allow a period. These braces attempt to control the joint
certain degree of movement and are fabricated range of motion and provide protection in case
with a combination of rigid materials and mov- of inadvertent loading that may result in injury
able parts such as joint, cables, rubber bands or (Wirth & DeLee 1990). These types of orthoses,
springs. Sometimes, dynamic orthoses are also along with early functional rehabilitation, have
termed functional orthoses (Redford 2000). been used for the management of the injured
Depending on the clinical situation, the desired medial collateral ligament of the knee (Reider
effect and the biomechanical characteristics, et al. 1993).
orthoses are considered corrective or accommodat- In 1975 orthotic terminology was formally
ive. Corrective devices are used to improve the adopted to allow a simplified, standard, clear com-
position of the joint by modifying the alignment munication language among different clinicians.
of skeletal structures. Accommodative devices The terminology adopted encourages anatom-
attempt to maintain a given position and prevent ical level description starting with the most pro-
further joint deterioration. ximal joint, followed by the orthotic adjective,
Furthermore, orthoses for use in sportsa rather than eponyms or proper names. If the
particularly those for the knee and ankleahave orthosis is to involve the foot, ankle and knee
been classified as either prophylactic, functional or it is termed knee–ankle–foot orthosis (KAFO).
rehabilitative depending on the clinical situation The particular material used and the desired
in which they are used (Wirth & DeLee 1990) functional effect of the orthoses should also be
(Table 15.1). Prophylactic bracing is intended included as part of the design (Goldber & Hsu
to prevent or reduce the severity of injury to 1997).
healthy joints. Ankle prophylactic bracing has
been used in basketball, volleyball and soccer
Biomechanics
(Thacker et al. 1999).
Functional braces are designed to control nor- The major joints of the body can be seen as semi-
mal joint motion as well as to attempt to resist constrained motion units with feedback control
abnormal joint rotation and translation (Wirth & that respond to internal and external forces and
DeLee 1990; Cawley et al. 1991). Most functional allow a stable, complex, three-dimensional joint
braces are intended to address knee or ankle joint motion in both the loaded and unloaded condi-
instability caused by ligamentous injury. A com- tions. During dynamic activity, powerful oppos-
mon clinical situation in which a functional brace ing muscle groups (flexors and extensors) exert
is used is in the patient with a non-operated anter- moments of force working synergistically with
ior cruciate ligament (ACL) injury who desires soft tissue restraints (ligaments, capsule and
to continue to participate in sports (Micheo et al. tendons) as well as the surface geometry of the
1995). bones to position the joint for optimal loading
orthoses 303
(Esquenazi et al. 1997; Zheng & Barrentine 2000). design. The latter, when used for sports orthotics,
Orthotic systems usually function with a three- results in a lighter, stronger and more durable
point force system in order to control joint move- device. The choice of materials in the fabrication
ment (Buttler et al. 1983). Devices with a long of orthotics is expanding rapidly and a detailed
lever arm and wide, close-fitting cuffs which dis- review of them is beyond the scope of this chapter.
tribute force over a large area have improved Orthotics can be custom fabricated or bought
physical characteristics to control joint transla- off the shelf, with off-the-shelf orthotics being
tion (Redford 2000). For example, a knee orthosis the most commonly prescribed braces today. In
that extends up in the thigh and distally to the some cases, because of the patient’s anatomy,
calf will restrain the flexion or extension motion difficulties with fit, size of the individual and
based on its alignment. Rotational, translation joint incongruity, custom orthoses are required
and transverse forces are difficult to control with (Esquenazi & Talaty 1996).
an orthotic system since orthoses achieve joint When fabricating orthoses attention should
motion control through force transmission from be given to accommodating bony prominences,
the bone to the soft tissue and on to the brace to alignment with the anatomical axis and to
structure, which allows brace migration and reducing ligamentous stress. The difficulty of
makes the system not rigid. These limitations in application, maintaining adequate suspension
force control about a joint are particularly trouble- and comfort are also of importance in achieving
some in patients with injury-related strength or compliance with the use of these devices (Loke
proprioception loss (Janshen 2000). 2000).
Brace design should allow forces to be dis- A complete orthotic prescription should in-
tributed over the largest area possible in order to clude the patient’s diagnosis, consider the type
reduce pressure concentration (force over area) of footwear to be used, include the joints it
and potential secondary soft tissue injuries (Buttler encompasses and specify the desired biomech-
et al. 1983). Friction and shear stress should anical alignment, as well as the materials for
be controlled by appropriate construction and fabrication. Communication with the orthotist,
accommodating the soft tissue which interfaces who will fabricate or fit the brace, is of utmost
between the brace and the joint it will act upon. importance in order to obtain a good clinical
result.
Fabrication
Clinical application
Materials for fabrication include metal, leather,
elastic fabrics, low temperature thermoplastics, The successful use of an orthotic device depends
high temperature thermoplastics, composites and on matching brace function with the patient’s
graphite. Plastics have the benefit of being light- functional needs. Appropriate orthotic applica-
weight, adjustable, cosmetic and having total con- tion will result in restraint forces that oppose
tact in custom braces. Total contact construction an undesired motion (Kilmartin & Wallace 1994).
is important to reduce an undesirable concen- Often pathology of the muscle, tendon or liga-
tration of forces over soft tissues or pressure- ment results in multiple deviations of the normal
intolerant areas such as bony prominences. joint movement process. Primary causes are often
Composite materials and metal orthoses have masked by compensations and secondary devi-
the advantage of increased durability and, in the ations, which sometimes makes the clinical inter-
hands of a skilled orthotist, still maintain built-in vention difficult. Emphasis has been placed on
adjustability. With the advent of new products initially identifying the primary causes of the
such as carbon graphite and extruded plastic particular disorder as the point from which to
materials, we now have the additional advantage begin the clinical intervention (Esquenazi &
of maximum tension strength with lightweight Talaty 1996; Esquenazi et al. 1997).
Understanding clearly the pathology and the

resultant compensations, the orthotic needs for a
specific sport, how a brace may be used to meet
these needs, and what effect the brace exerts on
the overall performance of the mechanical sys-
tem and the athlete are areas where research is in
progress. The potential, protective and preven-
tive use of orthoses in the athlete who has not
been injured is controversial and further investi-
gation is needed to clarify their role in this area.
Foot orthotics
Heel cord and/or plantar fascia tightness, calf
weakness, increased pronation or a high arch are
all conditions that alone or in combination can
increase the likelihood of foot- and knee-related
injuries in athletes (Fig. 15.1). At high risk for these
injuries are athletes who participate in sports that
require running or jumping (Frontera et al. 1994).
Optimizing the biomechanical posture of the
foot structures, improving lower limb flexibility Fig. 15.1 A pronated foot.
and strength, correcting or accommodating the
presence of any abnormality in the architecture
of the foot and improving shock absorption are
all key interventions to prevent disabling injuries Prefabricated orthoses (off the shelf) are less
(Lee et al. 1987; Schwellnus et al. 1990; Redford expensive devices that can be adjusted to pro-
2000). Although statistics are not available, it is vide adequate control or correction. In the hands
plausible that more prescriptions are written for of the experienced practitioner prefabricated
foot orthotics than for all other orthoses com- orthotics are a very effective tool in the manage-
bined. The use of orthoses has been advocated to ment of abnormal biomechanics of the foot. In
improve foot posture and reduce the incidence of some instances because of the wide variation in
lower limb injuries during running or jumping foot configuration, size and pathology, and when
(Fig. 15.2) (Orteza et al. 1992; Kilmartin & Wallace time and economic factors permit, custom ortho-
1994). Limited information is available in the tics should be considered as a better treatment
scientific literature to prove or refute the efficacy option. As the name indicates custom orthotics
of foot orthotics for this type of activity. are made specifically for an individual with their
Fig. 15.2 Corrected foot

pronation with moulded carbon
graphite foot orthoses.
orthoses 305
particular functional needs in mind. On-site

fabrication by a skilled, certified orthotist or
other trained clinician is preferable to referral to
an outside site.
When prescribing foot orthotics for sports,
knowledge of the patient’s complaint, the path-
ology in question, functional anatomy, biome-
chanics, orthotic components, materials, sport
requirements and, finally, recognition of the anti-
cipated functional outcomes are essential for
proper prescription (Orteza et al. 1992). Consid-
eration should be given to the fact that external
loads act as dynamic forces that may require
different orthotic prescription and materials for
different activities (Cornwall & McPoil 1999;
Hertel et al. 2001; Subotnick 2001).
Foot orthoses are designed to be corrective or
accommodative devices. Corrective devices that
are meant to improve the position of the foot by
correcting the alignment of skeletal structures
can be manufactured from a variety of materials.
Rigid materials such as thermoplastics, acrylic Fig. 15.3 (a) A carbon graphite corrective foot orthosis,
laminates and carbon graphite composites are and (b) a moulded accommodative foot orthosis.
used frequently for this (Fig. 15.3a). Cork and
polyethylene are examples of materials used for
semirigid orthotic devices (Hertel et al. 2001). device, can be integrated in the design and com-
The patient with a pronated flexible foot and bined at the time of fabrication (Subotnick 2001).
metatarsal stress fracture may benefit from the There are several factors to consider when select-
use of a semirigid orthotic device as part of a ing materials used in custom orthotic fabrication;
complete rehabilitation programme (Chandler & these include the type of sport, the physical de-
Kibler 1993; Cornwall & McPoil 1999). mands and the length of time the orthosis is to be
Accommodative devices made of soft, open used. For example, a triathlete or long-distance
or closed cell foams alone or in combination runner may need a device that is rustproof and
with semiflexible materials are meant to provide designed to function with perspiration or wet skin.
cushioning and support to an already deformed If the brace is intended for use for a few weeks a
limb structure (Fig. 15.3b) (Subotnick 2001). They prefabricated device may suffice; however, if in-
prevent further deformity while attemping to tended for longer term use (several months) then
improve function and to control the direction a more durable custom brace constructed out of
and/or alignment of the joint movement. Indi- carbon graphite may need to be considered.
viduals with rigid high arched feet and recurrent The amount of corrective or controlling forces
injury such as Achilles tendonitis or plantar to be applied and the amount of axial loading, as
fascitis are candidates for a soft orthotic device well as the amount of cushioning that is desirable
(Mascaro & Swanson 1994). without introducing mediolateral ankle instabi-
Appropriate posting, longitudinal or transverse lity, should be considered (Schwellnus et al. 1990;
arch build-ups, heel lifts, pressure relief areas or Brown et al. 1996; Hertel et al. 2001). One example
other special modifications, as well as applica- of this custom application is the use of TPE®
tion of different materials in the same orthotic (thermoplastic elastomer) for the longitudinal
Uppers
Sockliner
Bottoms
Midsole
Outersole
Fig. 15.4 Computer-aided foot orthotic design.
Tongue Achilles notch

Quarlet
arch, Pelite® as a moulded substrate and Poron®
Stabilizing strap
for shock absorption, all in the same foot orthotic.
Toe box
In the very active athlete, accommodative
orthoses may need to be replaced often to adjust
for material deterioration, while in the child or
teenager, replacement should be done to accom-
modate for growth. The cost of these custom- Toe cap Heel
made devices, depending on regional variations Vamp counter
and availability, has a wide spectrum. For the Outersole Midsole
less complex accommodative devices price is not
Fig. 15.5 Components of an athletic shoe.
significantly different to that for prefabricated
ones. In some areas, fabrication and delivery from
the time of moulding can be accomplished in less toe break (Fig. 15.5) (Janisse 1993; Johnson 2001).
than 48 h. This time may be further reduced with The users of fluid-filled heel chambers should
the use of computerized design and manufactur- keep in mind the possibility of increased ankle
ing systems (Fig. 15.4). These two factorsacost mediolateral instability. A removable insert with
and fabrication timeaneed to be considered in longitudinal arch support is a good option, and
the selection of custom orthotics. if a foot orthosis is to be used, the shoe insole
The shoe is an integral part of any lower should be removed.
extremity orthotic that includes the foot, as it will When a custom orthosis is ready it should
serve as the foundation for the device and will be evaluated on the patient to assure proper fit
directly impact on its function. The correct shoe and function. When these characteristics are
size should be measured with the athlete stand- achieved, supervised wearing time should be
ing after a period of exercise, since with weight- gradually increased.
bearing and exercise the foot configuration will In prescribing orthotics for paediatric patients,
change. The shoe should be manufactured out of such as in runners, tennis or soccer players,
a breathable material, have a supportive counter consideration should be given to the fact that
and deep toe box with a wide heel and a flexible throughout childhood growth and development
orthoses 307
act as dynamic forces that require frequent orth- increased proprioception that allows the per-
otic re-evaluation and modification. Not infre- oneal muscles to react more rapidly to inhibit
quently, as the patient approaches adolescence, extreme ankle inversion.
cosmetic considerations and peer pressure super- Clinical studies have not shown that the height
sede functional considerations, which impacts of the shoe affects the incidence of ankle injury
on orthotic use, compliance and function. (Barrett et al. 1993). This, in addition to the high
cost of taping to prevent ankle injury, has led to
the widespread use of ankle orthoses in the treat-
Ankle orthotics
ment and prevention of ankle injury. Semirigid
The ankle sprain is one of the most common orthoses provide external support, may enhance
injuries in athletes, particularly in sports where proprioception and may be adjusted more easily
participants frequently jump and land on one than tape (Thonnard et al. 1996; Baier & Hopf
foot or are expected to make sharp cutting man- 1998). Data from randomized controlled trials
oeuvres, for example basketball, soccer, football demonstrate the effectiveness of some of these
and volleyball (Lee et al. 1987; Frontera et al. devices, especially for the prevention of rein-
1994). Because ankle sprains are common and juries, although clinical research indicates that
may result in days or weeks lost from practice some devices will be more effective or more
and competition, efforts have been made to pre- acceptable to athletes than others (Thacker et al.
vent such injuries through directly protecting the 1999). For example, lace-up (Fig. 15.6a) or elastic
athlete with better shoes, ankle wrapping, taping ankle supports are inexpensive and reusable but
or bracing (Tropp et al. 1985; Thacker et al. 1999). may be uncomfortable and do not provide uni-
Ankle braces range from simple off-the-shelf form compression. Stirrup-type orthoses have
models that provide light support to custom been effective in reducing the recurrence of ankle
hinged models that help control significant ankle injury and are acceptable to wearers (Fig. 15.6b)
instability. The important function is to limit (Surve et al. 1994). However, they may be ex-
plantar flexion and inversion, which is the pensive and because of difficulty with fit may
position of instability for the ankle. For example, decrease performance levels.
an articulated ankle foot orthosis with plastic Based on the available medical literature as
moulded side pieces allows dorsiflexion and well as the clinical experience of the authors,
plantar flexion but very little inversion or ever- athletes who suffer an ankle sprain should com-
sion (Wilkerson 1992). plete supervised rehabilitation before returning
Several interventions that could lower the rate to practice or competition, and those athletes suf-
of occurrence of ankle sprains in a variety of sports fering a moderate or severe sprain should wear
have undergone scientific review (Tropp et al. an appropriate orthosis for at least 6 months.
1985). Clinical trials in soccer and volleyball play- Research suggests that the benefit of the orthosis
ers suggest that training agility, flexibility, special- may persist for up to 1 year after injury (Thacker
ized ankle disc training and education reduce the et al. 1999). It is not clear that there is a benefit of
risk of ankle sprain (Thacker et al. 1999). using an orthosis if the athlete has not been
In the past, taping the ankle has been the injured.
preventive method of choice for coaches and
trainers in many sports. Data from controlled
Knee orthoses
trials indicate that taping can prevent ankle
sprains, despite the fact that tape loosens in In the autumn of 1984, the Sports Medicine Com-
approximately 10 min and provides little or no mittee of the American Academy of Orthopa-
measurable support to the inverting ankle within edic Surgeons conducted a symposium on knee
30 min (Liu & Jason 1994; Manfroy et al. 1997). bracing to classify the types of knee braces avail-
This residual protection may be associated with able and to review the existing research. The Sports
(a) (b)
Fig. 15.6 (a) An ankle–foot leather lace-up orthosis, and (b) a stirrup ankle orthosis.
Medicine Committee developed three categories injury at other joints of the extremity such as the
to describe the various types of knee braces avail- ankle.
able: prophylactic, rehabilitative and functional Rehabilitation braces or postoperative knee
(Wirth & DeLee 1990; Cawley et al. 1991). braces are those braces designed to be applied
Prophylactic knee braces are those that are immediately following injury or ligament recon-
designed specifically to prevent or reduce the struction (Wirth & DeLee 1990; Munns 2000).
severity of injury to the knee resulting from an These braces are characterized by greater length
externally applied force. They are not designed and usually incorporate a means for providing
to provide increased knee stability in the knee selective range of motion control by the use of
with a disrupted ligament. These braces are used hinges that can limit motion or be locked in one
almost exclusively in American football in an position (Reider et al. 1993). Typically, they con-
attempt to prevent ligament injuries. They are sist of circumferential wraps and straps attached
designed either with lateral or bilateral uprights, to medial and lateral side bars with a hinge
hinges and thigh as well as calf bands (Osternig attachment at the level of the knee joint line. If
& Robertson 1993; Munns 2000). Though pro- rotational control is desired they may require
phylactic braces are used to protect the medial attachment to a footplate. These devices are com-
collateral ligament they may preferentially pro- monly used and are widely accepted within the
tect the ACL (Paulos et al. 1991). Prophylactic sports medicine community. A note of caution
braces continue to be manufactured and used; for the prescriber of the brace is that motion at the
however, their efficacy for use in Olympic sports knee joint may exceed the limits set by the hinges
has yet to be resolved in the minds of many clini- by 10–20° and this needs to be considered in
cians. In addition, they may increase the risk of managing the patient.
orthoses 309
authors have commented in the literature that

functional knee braces do not provide increased
mechanical stability under higher loads such as
the physiological loads associated with sport
(Cherf & Paulos 1990; Cawley et al. 1991).
It is interesting that in clinical and biomechan-
ical studies that also conducted a subjective
evaluation of the orthoses, over 90% of the pati-
ents reported significant functional improvement
when using a functional knee brace (Cook et al.
1989; Cawley et al. 1991; Anderson et al. 1992).
This is despite the fact that laboratory research
clearly shows that the use of a functional knee
brace may not protect the ligament at the physio-
logical loads associated with sports, will have
a significant cost in terms of energy expenditure
and may lead to reduced performance (High-
genboten et al. 1991).
Cook et al. (1989) found that the application
of a functional knee brace to an ACL-deficient
Fig. 15.7 A functional knee orthosis. knee enabled patients to generate torque and
shear forces during a cutting manoeuvre that
Functional knee braces are those orthoses that were near those generated by normal, non-ACL-
are designed specifically to provide mechanical deficient subjects and significantly better than
stability in knees with disrupted ligaments (Fig. cutting manoeuveres performed by unbraced
15.7). These braces have straps or cuffs and knee ACL-deficient limbs (Cherf & Paulos 1990; Hertel
hinges, and function by limiting anterior tibial et al. 2001).
translation, knee hyperextension and, to a lesser The stabilizing effect of functional knee braces
degree, rotation. These functional knee braces has been correlated with knee stability and mus-
are routinely used in the chronically unstable cle firing patterns (Anderson et al. 1992; Wojtys
knee and most physicians recommend their use 1993). When anterior tibial translation loads
in this application (Bonamo et al. 1990; Gotlin were applied to the partially loaded limb, reduc-
& Huie 2000). While functional knee braces tions in tibial translation of 15–30% with muscles
continue to be applied on ligament-deficient relaxed and 60–80% with the muscles contracted
knees, they are also commonly used in knees were documented. In addition, a slowing of mus-
with reconstructed ligaments. Thus, functional cle reaction time or a latent period between the
knee braces are applied as prophylactic devices onset of the load and the firing of the muscles
to provide strain or overload protection to recon- was reported (Cawley et al. 1991; Wojtys 1993).
structed, healing ligaments or grafts. It is interesting that the braces, which best
The preponderance of existing brace research controlled tibial translation, also exhibited the
addresses functional knee braces. It has attempted longest latent period for muscle firing.
to measure tibial translation using a variety of Many clinicians are in agreement that func-
methods including both manual displacements tional knee bracing serves an important role
and knee arthrometer systems. Many published in the treatment of non-reconstructed knee liga-
studies demonstrate that knee bracing does reduce ment injuries (Bonamo et al. 1990; Micheo et al.
anterior tibial translation in varying degrees under 1995). In general, studies that performed subjec-
low, non-physiological loading conditions. Many tive evaluation of functional knee braces found
a positive response in those patients wearing

orthoses.
Proprioception and proprioceptive deficits
resulting from disruption of the knee ligaments
has been a hotly debated topic within the ortho-
paedic and sports medicine community since the
discovery of mechanoreceptors within the sub-
stance of both the ACL and the medial collateral
ligament of the knee as well as the joint capsule
(McNair et al. 1996; Birmingham et al. 2000). While
there may be an interrelationship between neuro-
sensory and neuromuscular control systems,
and proprioception may provide positional joint
awareness, it is not clear what is the mechanism
for this phenomenon in the injured athlete. In
theory, functional knee bracing may enhance
position sense until the intrinsic neurosensory
mechanisms are re-established and provide
overload protection to the healing tissues.
For conditions that involve the patellofemoral
joint, such as runner’s knee, a pullover knee
sleeve with various types of cut-outs that are Fig. 15.8 An intrapatellar counterforce orthosis.
designed to support or stabilize the patella can be
helpful (Paluska & McKeag 1999). For patellar
Low back orthoses
dislocation or subluxation, a patellar-stabilizing
brace that has a cut-out sleeve and heavier Low back pain is very common with a high
buttressing is indicated (Cherf & Paulos 1990). incidence reported in men and women. The
In patients with patellar tendonitis or jumper’s incidence of spinal injuries related to sporting
knee, an infrapatellar counterforce orthosis may activities has been estimated at 10 –15%. Sports in
be used (Fig. 15.8). The theory behind the use of which back injuries are among the most frequent
this type of counterforce bracing is that it inhibits reported injuries include golf, gymnastics, foot-
full muscular contraction and decreases the force ball, rowing, wrestling, weightlifting and tennis
on the partially injured musculotendinous unit (Tall & DeVault 1993). The prevalence, however,
(Crossley et al. 2001). varies with the patient’s age, the sport played
A treatment modality for patellofemoral pain and with the position played. In gymnastics, the
that has gained recent acceptance is patellar incidence of back injuries is estimated to be 11%
taping. This technique tries to correct patellar (D’Hemecourt et al. 2000).
malalignment, including subluxation, tilt and The most common injury site has been reported
rotation, permitting progression in a rehabilita- to be the soft tissues. However, depending on the
tion programme of quadriceps muscle strength- biomechanical demands of the sport, discogenic
ening. Some clinical studies have shown good or posterior element injuries have also been
results in pain reduction and quadriceps muscle described. Sports that place repeated flexion and
recruitment; however, radiological studies show rotation demands on the spine may lead to disc-
that although the technique appears to position related symptoms, while those that place repeated
the patella medially this position is not main- hyperextension demands on the spine may lead
tained after exercise (Larsen et al. 1995; Kowall to posterior element injury such as spondylolysis
et al. 1996). (Kaul & Herring 1994; Standaert et al. 2000).
orthoses 311
may be used in the initial stages for patient com-

fort with correction of posture and reduction of
gross motion as the mechanism of action of the
orthosis. If the patient’s symptoms are severe
and worsen with a flexed posture, the use of a
brace in 5° of extension has been advocated by
some clinicians (Gerbino & Micheli 1996).
Treatment of stable compression vertebral
fractures routinely includes the use of exten-
sion bracing. Depending on the location of the
fracture, a thoracolumbar–sacral (TLSO) or
lumbar–sacral orthosis (LSO) in extension is
used. A custom-made TLSO or a Jewett-type
extension brace may be used from 4 to 12 weeks
depending on bony healing (Nachemson 1987).
Upper extremity orthoses

Hand and upper extremity injuries are among
Fig. 15.9 A lumbosacral overlap orthosis.
the most common injuries sustained by athletes.
Unfortunately, there is a tendency to minimize
Young patients usually present with injury to the their severity as the hand does not bear weight
posterior elements while older athletes present and the injuries rarely render the athlete unable
with injury to the disc (Blanda et al. 1993; Gerbino to compete (Alexy & De Carlo 1998). Wrist and
& Micheli 1996; Young et al. 1997). hand injuries are fairly common and described
Bracing has been routinely used for manage- to occur in 3–9% of all athletic injuries (Rettig &
ment of spondylolysis (Blanda et al. 1993; Stinson Patel 1995).
1993; Kaul & Herring 1994). Micheli has recom- Injuries can be traumatic or related to overuse.
mended the use of a rigid polypropylene brace The most common problems of the elbow include
(modified Boston overlap brace) constructed in tendonitis (lateral, medial and posterior), nerve
0° of lumbar flexion, prescribed for 23 h per day dysfunction and ligamentous injuries. Lateral
for up to 6 months (Fig. 15.9) (Gerbino & Micheli epicondylitis or tennis elbow is the most common
1996). In the case of an acute spondylolysis, or overuse problem about the elbow in athletes
even in chronic cases, where immobilization was (Plancher et al. 1996a; Sánchez 2001). Tenosyno-
attempted in order to achieve healing, his proto- vitis of the wrist is quite common in sports; de
col has recently been modified to weaning from Quervain’s syndrome (tenosynovitis of the first
the brace as early as 4 months if there is evidence dorsal compartment) and extensor carpi ulnaris
of healing by computed tomography scanning tendonitis are commonly seen in racquet sports
(D’Hemecourt et al. 2000). The use of less rigid and weightlifting (Rettig & Patel 1995).
materials, in combination with the avoidance The scaphoid is the most commonly injured
of repeated hyperextension until the patient is carpal bone, accounting for 70% of all carpal frac-
asymptomatic, has been advocated by others, tures (Alexy & De Carlo 1998). The injury results
including our own clinical group with good from a fall on the hand with the wrist dorsiflexed
results (Standaert et al. 2000). greater than 90° and may be seen in a variety
The use of bracing for the treatment of disco- of sports. Dislocation of the proximal interpha-
genic symptoms is more controversial (Stillo et al. langeal joint is also a common traumatic injury of
1992; Young et al. 1997). A soft brace or corset the hand.
Nerve injuries can also occur associated with

overhead sports, for example volleyball. Ulnar
neuropathy at the level of the elbow can be seen
in baseball pitchers, and median neuropathy at
the level of the carpal tunnel can occur in racquet
sports such as tennis and racquetball (Plancher
et al. 1996b).
Orthoses can be used to manage acute and
overuse injuries of the wrist and hand. Stable
scaphoid fractures can be managed with a short
forearm to thumb spica cast followed by the use
of a thumb spica splint. Some athletes can return
to sports participation with the use of a playing
cast or a padded thermoplastic splint if there
is evidence of healing (Alexy & De Carlo 1998).
Dislocations of the proximal interphalangeal
joint can be treated with closed reduction and the
use of a digital extension block splint in approx-
Fig. 15.10 An elbow counterforce orthosis.
imately 30° of flexion (Sailer & Lewis 1995). After
3 weeks the patient may progress to the use of
buddy taping until the patient has pain-free full made of rigid thermoplastic material in 45° of
range of motion. flexion. In the early stages of recovery the orthosis
Tendonitis of the first dorsal compartment can should be worn during most of the day and as the
be treated with the use of a thumb spica splint in patient’s symptoms improve it should be used
combination with steroid injection and physical only at night (Plancher et al. 1996a). Median entrap-
therapy. A short course of immobilization with a ment at the level of the wrist should be treated
wrist–hand orthosis in 15–20° of wrist extension with a splint that immobilizes the wrist in 0–5° of
can be considered for other types of acute ten- wrist extension. The orthosis should be worn
donitis of the wrist. at night and during the day when performing
Counterforce bracing with the use of a forearm provocative activities that increase symptoms.
support band may be used for the treatment of
lateral epicondylitis. The orthosis should be used
Future research
just distal to the elbow to alter the tension forces
on the wrist extensor muscles (Fig. 15.10) (Tropp Research is underway with a different focus,
et al. 1985; Plancher et al. 1996a). As previously which considers the effect of the orthotic inter-
stated, the counterforce brace inhibits full muscle vention on each segment of the whole body, as
contraction thus decreasing the forces applied to well as on the total body response. This will help
the partially injured musculotendinous unit. It to clarify the brace–body interaction. Questions
has also been shown to decrease elbow angular are being addressed such as what is the best
acceleration and decrease electromyographic orthotic alignment (arc of motion allowed), what
muscle activity of the forearm muscles (Sailer & is the global effect of the brace on the body, how
Lewis 1995; Plancher et al. 1996a). does the body response to a brace change over
Ulnar neuropathy at the level of the elbow time, and how do subject perceptions correlate to
cubital tunnel can be treated with protection using more quantitative outcome measures? Research
an elbow pad to avoid direct pressure over the can play an important role in advancing the use
nerve, or in severe cases with an elbow orthosis of orthoses by: (i) isolating key facets of orthotic
orthoses 313
function; (ii) the introduction and refinement of

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Index
Page numbers in italics refer to age, emotional response to injury goat, hemitransection injury–69
figures; those in bold to tables. and–166 healing–68 –9
ageing immobilization–74
acetaminophen–198 satellite cell changes–37 mechanisms of injury–59 – 60
acetic acid iontophoresis–215 tendon injury and–64 mobilization
acetylsalicylic acid (aspirin)–188, aggrecans–107– 8 normal ligament–75, 76
190 agility training protocols see postsurgical–77– 8
Achilles tendon plyometrics/agility reconstruction–62, 78 – 85
ACL allografts–82– 3 protocols cryotherapy–205
elastic energy storage–57 agonist–antagonist ratios–260, 298 electrical muscle stimulation–
fatigue failure or plasticity–72 albumin–24 216 –17
grade 1 tendonitis–68, 71, 72 aldosterone–24, 119 –20 rehabilitation–85, 265, 266, 270
grade 2 partial tear–70 –2 alkaline phosphatase–16 antigens–19
grade 3 acute rupture–70, 71 alternating current (AC)–213, 215, antisense therapy, decorin–91–2,
injuries 216 93
biomechanics–64, 71–2 American football–308 apolipoprotein A1–127
healing–68, 69 –72 amyloid, serum–24 arachidonic acid–13, 18
physical modalities–73, 212 anabolic steroids–191–2, 200 arcuate nucleus–198 –9
insertion–60 anaemia, of chronic inflammation– arginine vasopressin–24, 25
surgery, functional casting after– 25 arteriovenous oxygen difference–
66–7 analgesia 132
ACL see anterior cruciate ligament acupuncture–198 –9 arthroscopic lavage, cartilage
activin–105 NSAIDs–189 –90 injuries–109 –10
acupuncture–198 –200 opioid–196 aspirin–188, 190
clinical applications–199 –200 anaphylotoxins–20, 21 asthma–200
mechanism of action–198 –9 anger–165 ATP, mitochondrial production–
acute injury–5, 146, 149 angioedema, hereditary–22 134
cryotherapy–204 ankle
NSAIDs–41, 49, 189 effects of stretching–249 back pain, low
rehabilitation–264 – 5, 288 injuries–6, 155 – 6 electrical therapy–218
TENS–219 orthotics–302, 307 lumbar traction–222– 3
acute phase proteins–24 sprains–206, 307 orthoses–310 –11
acute phase response–11, 22– 4 anorexia–25 percutaneous electrical nerve
addiction–198 anterior cruciate ligament (ACL) stimulation–220
adherence to rehabilitation–167–9 allografts–82– 5 TENS–219
assessment–168 autografts–78 – 82, 84 – 5 ultrasound therapy–211
factors affecting–168 –9 collagen fibril size distribution balancing board–285
impact on outcome–172 78 –9, 80, 81–2 ballistic stretching–242– 3, 253
adolescents, strength training–263 collagen typing–79 – 82, 89 –90 barbell squat–267
adrenaline–119–20 remodelling in goats–85 –90 baseball pitcher–291
adrenocorticotrophic hormone collagen fibril size distribution diagnosis of rotator cuff injury–
(ACTH)–24 – 5, 199 animal studies–61, 85, 86 147
aerobic capacity, maximal see in humans–78, 79, 83 kinetic chain–144 – 5
V̇ O 2max collagen typing–79 – 82 prehabilitation–292– 5
afferent nerves–275 functional knee braces–302, 309 return to sports–299
317
318 index
basic helix–loop–helix family cardiovascular adaptations cross-links

(bHLH)–45, 47 effects of detraining–117–25, 137, in ACL autografts–89 –90
basketball–7, 291 154 – 5 mechanical disruption–58
basophils–15 reduced training and–136 effects of heat–207
behavioural factors, rehabilitation cardiovascular endurance–263 – 4, effects of stretching–240
outcomes–172 270 ligament/tendon–56 –7, 58
behavioural responses to injury– carisoprodol–197 effects of immobilization–74 – 5
167–9 carpal tunnel syndrome–312 normal ACL and ACL
β2-agonists–200 cartilage, articular–106 –12 autografts–79 – 82
β-endorphin–195, 198 –9 effects of immobilization–73, 154 synthesis/deposition
betamethasone acetate–193 injuries effects of mobilization–75, 77
biofeedback–172, 173 classification–109, 110 in ligament/tendon repair–65,
biomechanics mechanism–108 67, 68 –9, 70
Achilles tendon injuries–64, 71–2 treatment–109 –12 physical modalities and–73
ACL autografts–88 –9 types and healing–108 –9 in tissue repair–27
collagen fibril size distribution structure–106 – 8 type I–56, 65, 81, 100
and–60–2 celecoxib–188, 189, 190 type III–56, 65, 79 – 81, 89 –90
ligament/tendon–57– 60 central biasing theory–218 type V–79 – 81
see also tensile strength, cerebral cortex–276 –7 typing, ACL grafts–79 – 82, 89 –90
ligament/tendon ceruloplasmin–24 collagenase–39 – 40
orthoses–302–3 cervical spondylosis–223 collagen fibrils
tissue injury–62– 4 cervical traction–221–2 biomechanics–57, 58 –9
biopsychosocial model–161– 4, 175, Chediak–Higashi syndrome–17, 18 in healing ligament/tendon–65,
176 children 67, 68
blood pressure–124 orthotics–306 –7 mechanisms of damage–58 –9
mean–122, 123, 124 strength training–263 remodelling, healing ligaments–
blood volume–119 –20, 121, 122 chondral injuries–108 –9 77, 84, 85 –90
B-lymphocytes–19 –20 classification–109, 110 size distribution
body mass, effects of detraining– flap injuries–108, 109 in ACL allografts–83 – 5
128, 131–2 fractures–109 in ACL autografts–78 –9, 80,
bone–99–106 matrix and cell–108 –9 81–2, 85 –90
fractures see fractures chondrocytes–106 in chronic Achilles tendonitis–
ligament/tendon insertion–60, 63 autologous transplantation– 68
remodelling–99 –100, 102 111–12 decorin antisense therapy and–
structure–99–100 chondroitin sulphate–107 91–2
subchondral, drilling–110 –11 chronic injuries–4, 5 – 6, 146 exercised ligaments–75 – 6
woven–102 cryotherapy–204 immobilized ligaments–74 – 5
bone marrow stimulation NSAIDs–189 injured ligament/tendon–
procedures, cartilage injuries see also overuse injuries 61–2
110–11 chronic overload syndromes–148 mechanical properties and–
bone morphogenetic protein (BMP) chylomicron-retinyl esters–127– 8 60 –2, 82, 84
101, 105 circulation–122– 4 reconstructed ligament/
braces see orthoses citrate synthase–126, 132– 3 tendon–62
bradykinin–14 clinical symptom complex–146 –7 communication, patient–
bupivacaine–193, 200 clinics, sports injuries–4 practitioner–174
bursae, corticosteroid injections– clonidine iontophoresis–215 complement system–20 –2
193–4 coagulation cascade–18 –19 concentric exercise–262
cocaine–200 conduction, heat–206 –7
C1 esterase inhibitor–21 codeine–195, 197, 200 confusion–165
calcium apatite deposition–68 cognitive appraisals connective tissue, effects of
callus–101, 102 models–161, 162 stretching–240
calpains–38 sports injury–166, 167 constipation, opioid-induced–
capillaries, response to injury–22–3 cognitive-behavioural 197– 8
capillarization, muscle–130, 153, interventions–172– 3 continuous passive mobilization
260 cognitive factors (CPM), in chondral injuries–
carbohydrate utilization–125 adherence to rehabilitation– 111
carbon graphite–303 168 –9 contracture, after injury–153 – 4,
cardiac dimensions–122– 4 rehabilitation outcomes–171 237– 8
cardiac function–120 –2 cold therapy see cryotherapy contrast baths–206
cardiac index–122, 123 collagen contusion–8
cardiac output–121–2 articular cartilage–106, 107, 108 convection, heat–207
cardiopulmonary reflex–123 ‘crimp’–57, 58 conversion, heat–207
index 319
coordination–277 TENS–219 –20 immobilization-related changes–

definition–274 ultrasound therapy–212 151–2
training–285 depression–165 emotional factors, rehabilitation
coping behaviours–167, 169 detraining–117– 38 outcomes–171–2
corticosteroids–191– 4 avoiding/reducing effects– emotional responses to injury–
history–191–2 135 –7 164 –7
injections–192, 193 – 4, 196, 201 cardiorespiratory effects–117–25, mediating/moderating factors–
iontophoresis–214 –15 154 – 5 166 –7
mechanism of action–23, 192 definition–117 β-endorphin–195, 198 –9
phonophoresis–213 endurance performance and– endorphins–218 –19
routes of administration–192 134 – 5 endothelial cells–22, 27
side effects–194 metabolic effects–125 –9 endurance–258 –70
systemic–193, 201 muscular effects–129 – 34 cardiovascular–263 – 4, 270
corticotrophin-releasing hormone strength performance and–135 definition–263
(CRH)–24, 25 syndrome–123 muscle–260, 269
cortisol–24–5, 131, 136 see also immobilization performance, detraining effects–
phonophoresis–213 dexamethasone iontophoresis–215 134 – 5, 138
ultrasound therapy and–211 dextran derivatives–51 training, after injury–263 – 4, 270
cortisone–192 dextromethorphan–200 enkephalins–195, 198
counselling–174 dextropropoxyphene–200 enthesis–60, 63
C-reactive protein (CRP)–24 diamorphine–200 eosinophils–17–18
creatine kinase (CK)–47– 8, 131 diathermy–207, 210 –13 epicritical superficial sensation–274
creep–59, 233, 234 diclofenac–188 epidemiology of sports injuries–
critical point framework–288 diflunisal–188 3 – 8, 145
cross-training–137, 138 dihydrocodeine–195, 200 in international competitions–
in water–208 diphenoxylate–200 7– 8
cross-transfer effect–137, 138, 261 direct current (DC)–213, 215 patterns of injuries–4 –7
cruciate ligaments see anterior doping–200 –1 epinephrine (adrenaline)–119 –20
cruciate ligament; posterior dynamization–102 erythropoietin–25
cruciate ligament ethyl chloride spray–205
cryokinetics–205 eccentric exercise–62– 3, 262, 268 etodolac–188
cryostretch–205 eccentric strength, training exercise
cryotherapy–204 – 6, 224 cessation and–135 ligament tensile strength and–
application techniques–204 – 6 eicosanoids–189 75 – 8
mechanisms of action–23 – 4, 204 elastic energy, storage–57, 236 –7 muscle regeneration and–51–2
‘cutting cone’–101 elastic fibres (elastin)–56, 57 see also mobilization; training
cycling–291 elasticity–233, 234 explosive-type training–269
cyclooxygenase (COX)–13 effects of stretching–240 extensibility
inhibitors–15, 190 elbow definition–233, 234
type 2 (COX-2) inhibitors–14, injuries–311, 312 effects of warm-up–250
190 orthoses–312 exteroceptive sensation–274, 275
cytokines–10–13, 25, 27 tennis see lateral epicondylitis extracellular matrix
in acupuncture–199 electrical stimulation articular cartilage–106 – 8
anti-inflammatory–10 –11, 13 muscle–215 –18, 262, 265 proteolysis–39 – 40
bone–100 nerves–214, 218 –20, 262 TGF-β actions–43
in muscle injury–39, 41, 42– 4 to promote tissue healing–214 extrapyramidal system–277
proinflammatory–10 –11, 14 single twitch–260 –1
in tissue repair–26 with tetanic trains–261 factor XII–21
electrical therapy–213 –20, 224 factor H–21
dash pot–234 contraindications–214 factor I–21
debridement, cartilage injuries– fracture healing and–105 faradic stimulation (alternating
109–10 indications–220, 221 current)–213, 215, 216
decorin antisense therapy–91–2, 93 soft tissue repair and–73 fat, body, effects of detraining–128,
deep heating (diathermy)–207, electric heating pads–208 131
210–13 electroacupuncture stimulation fatigue, after injury–258
deep sensation–274 (EA)–198 fatigue failure, Achilles tendon–72
delayed-onset muscle soreness electrocardiogram (ECG)–124 fear–165
(DOMS)–62– 3, 262 electromagnetic field therapy–73, femoral–medial collateral
cryotherapy–206 223 – 4 ligament–tibial (FMT)
flexibility training and–236 electromyography (EMG)–278 complex–77
iontophoresis–215 in flexibility testing–239 fenoprofen–188
NSAIDs–190 in flexibility training–239 – 40 fentanyl patch–197
320 index
fever–14, 24 fractures–100 –6 haemostasis–18

fibrinogen–127 aim and principle of treatment– Hageman factor–21
fibroblast growth factor (FGF)– 100 –1 hamstring flexibility
42–3, 44, 51 fixation methods–102– 3, 104 injury risk and–235
basic (bFGF, FGF-2)–39, 43, healing–101– 3 methods of increasing
49–50 biological influences–103 (stretching)–241–2, 244
receptor 1 (FGF-R1)–43 mechanical influences–102– 3 stretching studies–246, 247, 248,
type 1 (FGF-1)–42 primary and secondary–101 249, 252, 253
type 5 (FGF-5)–43 management–103 – 6, 149, 212, testing–238 –9
fibroblasts 223 – 4 hand
in ACL autografts–82 sports-related–100 injuries–311–12
tendon–56 Freeman (BAPS) board exercises– orthoses–312
heat-induced death–57, 64 281, 284 Haversian systems–99
in tissue repair–39 – 40, 64 – 5, frustration–165 healing see tissue repair/healing
238 functional biomechanical deficit health services, international
fibrocartilage–60, 63 complex–147 competitions–7– 8
fibrosis–26, 27, 238 functional rehabilitation–288 –97 heart dimensions–122– 4
five dot drill–293 heart rate
flexibility–232–53 galvanic stimulation–214 detraining effects–120 –1
components–233 – 4 gap junctions–22, 23 maximal–121, 122
definition–233 gaseous cavitation–210, 211 recovery–122
effects of heat–207 gastrointestinal disorders–8 reduced training and–136
injury risk and–156, 235 – 6 gastrointestinal effects resting–120, 122
measurement–238 –9 NSAIDs–191 submaximal–120, 122
terminology–233 – 5 opioids–197– 8 heat
flexibility training (stretching)– gate-control theory–218 physiological effects–207, 234
232–3 gelatinase–16 transfer–206 –7
definition–233 gender differences, resistance heat therapy–206 –13, 224
general benefits–235 –7 training effects–263 deep (diathermy)–207, 210 –13
decreased muscle soreness– gene therapy–50 –1 indications–207– 8
236 glucagon–24 –5 prior to stretching–250
decreased risk of injury–235 – 6 glucocorticoids see corticosteroids superficial modalities–208 –10
improved performance–236 –7 glucose metabolism–126 – 8 heel pain–212, 215
methods–240–5 GLUT-4 transporter–126, 127, 136 helix–loop–helix family, basic
ballistic stretching–242– 3 glycogen, muscle–129 (bHLH)–45, 47
passive stretching–243 – 4 glycogen synthase–133 heparin sulphate proteoglycans–51
proprioceptive neuromuscular glycolytic enzymes–133 hepatocyte growth factor (HGF)–44
facilitation see glycosaminoglycans (GAG) hexagon drill–293
proprioceptive articular cartilage–107– 8 hexokinase–133
neuromuscular facilitation ligament/tendon–65, 74, 76 high-density lipoprotein
static stretching see static goal setting–169, 172, 173 cholesterol–127, 128
stretching goals, rehabilitation–4, 145 – 6 high-voltage pulsed galvanic
physiology–239 – 40 acute phase–264, 288 stimulation (HVPGS)–214,
practical guidelines–253 functional phase–289 216
proprioceptive effects–279 recovery phase–289 histamine–15, 18 –19
scientific basis–245 – 53 return to sport phase–269 Hoffman (H) reflex–152, 153
effect of stretch position–252– 3 training phase–265 hormones–24 – 5
efficacy of one session–248 golf–291 hot water bottles–208
efficacy of repeated sessions– Golgi–Mazzoni corpuscles–279 H reflex–152, 153
248–9 Golgi tendon organ (GTO)–240, Hubbard tanks–209
frequency–246 –7 241, 244 hyaluronate, intra-articular–74
optimum duration–245 – 6 granulation tissue–26 –7 hydrocodone–197, 198
warm-up prior to–249 – 52 grief reactions–164 – 5 hydrocollator packs–208
sport-specific protocols growth factors hydrocortisone phonophoresis–213
running–295, 296 bone–100 hydromorphone–197
soccer–297, 298 in fracture healing–101, 105 hydrotherapy–208 –9
tennis/baseball–292, 293, 294 in muscle injury–39, 41, 42– 5, β-hydroxyacyl-coenzyme A (CoA)
fluidotherapy–209 –10 52 dehydrogenase–132– 3
fluori-methane–205 in osteochondral fractures–109 β-hydroxybutyrate dehydrogenase
flurbiprofen–188 therapy–49 – 51, 91 133
foot orthotics–304 –7 growth hormone–24, 131 5-hydroxytryptamine (5-HTP)–198
formoterol–200 gymnastics–4, 5, 310 hyperalgesia–195
index 321
hypermobility–232 interleukin 1 (IL-1)–11, 12, 13 after repeated stretching

hyperthermia, tendon–57, 64 in fracture healing–101 sessions–248 –9
hyperthyroidism–47 in inflammation–25 terminology–233 – 5
hypothalamic–pituitary–adrenal in muscle injury–39, 41 warm-up effects–249 – 52
axis–24–5 interleukin 1α (IL-1α)–12, 24 see also flexibility
hypothyroidism–47 interleukin 1β (IL-1β)–11, 12, 199 jumper’s knee–63, 310
hysteresis–59, 233, 234 interleukin 2 (IL-2)–12
interleukin 3 (IL-3)–12 Kabat technique see proprioceptive
ibuprofen–188, 189 interleukin 4 (IL-4)–11, 12 neuromuscular facilitation
ice–204–5 interleukin 5 (IL-5)–12 kallikrein–21
ice hockey–291 interleukin 6 (IL-6)–11, 12, 199 keratan sulphate–107
identification, with athlete role–166, in fracture healing–101 ketoprofen–188
170 in inflammation–24, 25 ketorolac–188
IL see interleukin in muscle injury–39, 41, 43 – 4 kicking–291
iliotibial band, ACL autografts–79 interleukin 8 (IL-8)–12 kinaesthesia–274
imagery, guided–172, 173 interleukin 10 (IL-10)–11, 12 kinetic chain–144 – 5, 280 –1
immobilization–149 – 55, 258 internal rotation/external rotation exercises, closed and open–266,
cardiovascular changes–154 – 5 ratio–298 281
joint changes–73 – 4, 153 – 4 international competitions–7– 8 muscular balance and–155 – 6
ligament tensile strength and– International Olympic Committee sport-specific–290 –1
74–5 (IOC), prohibited substances knee
muscle changes–150 –1 191–2, 195, 200 anteromedial pain (jumper’s
in muscle injury–49 interoceptive sensation–274 knee)–63, 310
neural changes–151–2 intersegmental dynamic analysis– immobilization, effects–74 – 5
vascular changes–153 313 injuries–6
see also detraining; mobilization interventricular septal wall limited motion casting–66, 78
immune system–15 –22 thickness–122, 123 mechanisms–59 – 60
indomethacin–188 inverse stretch reflex–240, 244 proprioceptive effects–278 –9,
infections, repeated pyogenic–22 iontophoresis–192, 215 310
inflammation–10 –27 isokinetic exercise–262, 266, 267 strength deficits after–6, 258 –9
acute–22–5 isokinetic testing–266, 267 orthoses (braces)–301, 302, 303,
chronic–10, 25 isometric muscle action–261 307–10
components–10 –22 sensory receptors–279, 310
corticosteroid actions–192 joint see also anterior cruciate ligament;
in muscle injury–38 – 40, 49 corticosteroid/local anaesthetic medial collateral ligament,
neurogenic–195 injections–193 – 4 knee; posterior cruciate
NSAID actions–188 –90 effusion, reflex muscle inhibition ligament
opioids and–195 152, 153, 258 Krause bulbs–275, 276
process–22–5 immobilization-induced changes
in tendon/ligament injury–64 – 5 73 – 4, 153 – 4 lactate, blood–128 –9, 136
tissue repair–25 –7 sensory receptors–275, 276 lactate dehydrogenase (LDH)–48,
inflammatory cells–15 –20 joint capsule 133
in muscle injury–38 – 41 effects of immobilization–73 – 4 ladder drill–294
in tissue injury–22 mechanoreceptors–274 laser photostimulation–73
inflammatory mediators–10 –15 joint range of motion (ROM)– lateral epicondylitis (tennis elbow)–
injections, corticosteroid/local 232– 53 189, 311
anaesthetic–192, 193 – 4 athletic performance and–236 –7 acupuncture–199 –200
insulin–24–5 decreased (contracture), after counterforce orthosis–312
action–126, 127, 136 injury–153 – 4, 237– 8 ultrasound therapy–212–13
insulin-like growth factor I (IGF-I)– definition–233, 235 left ventricular end-diastolic
39, 44 duration of stretching and–245, dimension–122, 123
in fracture healing–101 246 left ventricular mass–122, 123, 124
therapeutic potential–49 – 50 effects of immobilization–153 – 5 left ventricular wall thickness–
insulin-like growth factor II (IGF-II) end-point detection–239 122– 3, 124
39, 43, 44 excess (hypermobility)–232 leptin–25
in fracture healing–101 frequency of stretching and– lethargy–25
integrated model of psychological 246 –7 leucocytes
responses–161, 162, 175, measurement–238 –9 in inflammatory response–22, 23
176 methods of increasing–240 – 5 in muscle injury–42
interferential current–220 retention in tissue repair–26
interferon-α (IFN-α)–12 after one stretching session– see also inflammatory cells;
interferon-γ (IFN-γ)–12, 25, 199 248 macrophages; neutrophils
322 index
leukaemia inhibitory factor (LIF)– macrophages–15 –16, 26 in fractures–100 –1, 102– 3

39, 43–4 ED1+–41 in ligament/tendon injuries–
levorphanol–197 in muscle injury–40 –1, 44 65 –7, 78
lidocaine–193, 200 phagocytosis–41 ligament tensile strength and–
ligament–56–92 macrotrauma–146, 148 75 – 8
biomechanics–57– 60 magnetic therapy–73, 223 – 4 normal ligaments–75 – 6
effects of immobilization–73, 74, major basic protein (MBP)–17–18 surgically repaired ligaments–
154 major histocompatibility complex 76 – 8
injury–148 (MHC)–19 monocytes–14, 22
collagen fibril size distribution malate dehydrogenase–132– 3 mononucleated cells–39 – 40
after–61–2 march fracture–100 morphine–196, 197, 200
early controlled mobilization– marrow stimulation procedures, motor control–277, 278
65–6, 78 cartilage injuries–110 –11 see also coordination
grade 1 tears–59 mast cells–15 motor cortex–152, 276
grade 2 tears–59 maximal oxygen uptake see V̇ O 2max motor neurones, immobilization-
grade 3 rupture–59 mechanical factors, fracture healing related changes–151–2
mechanisms–59 – 60 102– 3 MRF4–45
rehabilitation–148 mechanoreceptors–274, 275, 276 muscle–259
insertion to bone–60 meclofenamate–188 activation, impaired–258 –9
mechanoreceptors–274 medial collateral ligament (MCL), agonist–antagonist ratios–260,
repair/healing–64 –9 knee 298
acute inflammatory phase– decorin antisense therapy–91–2, atrophy/hypotrophy/
64–5 93 wasting–259
effects of NSAIDs–189 effect of immobilization–74 – 5 assessment–259
phases–64, 65 electromagnetic stimulation of electrical stimulation–215–17
proliferative phase–65 –7 healing–73 immobilization-induced–151
remodelling and maturation functional knee braces–302 capillarization–130, 153, 260
phase–67–9 mechanism of injury–60 circumference measurement–259
tissue engineering approaches mobilization of surgically effects of detraining–129 – 34, 138
91–2 repaired–76 –7 electrical stimulation–214,
structure–56–7, 58 NSAID therapy and healing–189 215 –18, 262, 265
tensile strength see tensile scar tissue–91–2, 93 endurance–260, 269
strength, ligament/ medical examination, enzymatic activities–132– 3, 136,
tendon preparticipation–7 260
ligamentous laxity–156 Meissner corpuscles–275, 276 force development, speed of–261
line drill–294 membrane attack complex (MAC)– glycogen–129
lipid metabolism–25, 126 – 8 20 –1 healing/repair–37– 52, 149
lipoprotein(a)–127 meniscectomy–196 biological treatment
lipoprotein lipase–127, 133 mental health practitioner, referral approaches–48 – 52
load–deformation (strain) curve to–174 degeneration phase–25, 37,
Achilles tendon ‘fatigue failure’– meperidine–197, 198 38 – 41
72 mepivacaine–200 maturation phase–37, 45 – 8
tendon/ligament–57–9 meprobamate–197 regeneration phase–35, 37,
loading, mechanical Merkel’s disks–240, 275, 276 41– 5
ACL autografts–82 mesenchyme stem cells–91 imbalance, relative–155 – 6
articular cartilage injuries–108 metabolic adaptations immobilization-related changes–
fracture healing and–102– 3 effect of detraining–125 –9, 137– 8 150 –1
muscle regeneration and–51–2 reduced training and–136 injury–35 – 52, 148 –9
see also exercise; immobilization; metabolic rate, resting–128 biomechanics–62– 3
mobilization metatarsal fracture–100 in situ–35
local anaesthetic injections–192, met-enkephalin–195 shearing–35
193–4, 200 methadone–197, 200 mass
locus of control–168 microfracture technique, cartilage detraining effects–131–2
loss, injury as–164 injuries–110 –11 immobilization-induced loss–
low back pain see back pain, low microtrauma–146, 148 151
low-density lipoprotein cholesterol mitochondria reduced training and–136
127 ATP production–134 myoglobin–132
lower limb enzymatic activities–132– 3 power training–268 –9
orthoses–304–10 mobilization reduced training and–136
proprioceptive re-education– continuous passive (CPM), in re-education–216
282–4 chondral injuries–111 reflex inhibition–152, 216, 258 –9
lymphocytes–19–20, 40 early–264 sensory receptors–275, 276
index 323
soreness, delayed-onset see myosin heavy chain (MHC) endogenous–195, 198

delayed-onset muscle isoforms–46 –7 side effects–196 – 8
soreness myosin light chains (MLC)–46, 47 orthoses–301–13
specific proteins–45 – 8 myositis–8 accommodative–302
strength see strength, muscle myostatin–39 ankle–302, 307
structure–35–7 myotendinous junction injury see biomechanics–302– 3
volume muscle–tendon junction clinical application–303 – 4
postinjury reduction–259 injury corrective–302
resistance training effects–261, myotubes–45 custom made–303, 304 – 6
265 dynamic–302
muscle fibre (myofibre) nabumetone–188 fabrication–303
damage–35, 38 naproxen–188 foot–304 –7
distribution, detraining effects– narcotics see opioids functional–302
130–1 natural killer (NK) cells–20 future research–312–13
fast-twitch (FT, type II) nerve endings, free–276, 279 knee–301, 302, 303, 307–10
detraining effects–130 –1, 132 nerve growth factor (NGF)–39, 43, low back–310 –11
effects of injury–259 44 prophylactic–302
myosin isoforms–46 nerve injuries, upper extremity–312 rehabilitative–302
myotendinous junction–63 nerves static–302
regeneration–47 afferent–275 terminology and classification–
maturation–45– 8 electrical stimulation–214, 301–2
regeneration–35, 37, 41– 5 218 –20, 262 upper extremity–311–12
size neural activation osteoarthritis–223
detraining effects–131–2 electrical stimulation and–262 osteoblasts–99 –100, 101, 102
immobilization-induced losses flexibility training–239 – 40 osteochondral autograft
151 immobilization and–151–2 transplantation–111
slow-twitch (ST, type I) neuroendocrine system–24 – 5 osteochondral fractures–108, 109
detraining effects–131, 132 neurogenic inflammation–195 osteoclasts–99 –100, 101
effects of injury–259 neuromuscular activation–260 –1 osteocytes–99
myosin isoforms–46 assessment–260 –1 osteoprogenitor cells–100
regeneration–47 effects of injury–260 overload syndromes, chronic–148
muscle relaxants–194 neuromuscular re-education–274 overuse injuries–4 – 5, 148
muscle–tendon–bone injury–62– 3 neuropraxia–204 see also chronic injuries
muscle–tendon junction injury– neutropenia, congenital oxaprozin–188
148–9 dysgranulopoietic–17 oxidative enzymes, muscle–132– 3,
biomechanics–63, 64 neutrophils–14, 16 –17 136
tissue repair–67 in inflammatory response–22 oxycodone–197, 198
musculotendinous unit in muscle injury–39 – 40 oxygen difference, arteriovenous–
elastic energy storage–57, 236 –7 in tissue repair–26 132
flexibility see flexibility nociceptors, peripheral–195, 196 oxygen uptake, maximal see V̇ O 2max
length–233, 235, 238 non-steroidal anti-inflammatory
ROM see joint range of motion drugs (NSAIDs)–187–91 Pacinian corpuscles–240, 275, 276,
stiffness–234 dosing–188, 190 –1 279
tension–233–4 effects on healing–41, 49, 189, 190 pain
myeloperoxidase–16 history–187– 8 management–204 –24
Myf5–45 mechanism of action–13 –14, 15, see also analgesia
myoblasts 23, 188 –90 mechanisms–14
differentiation into–42, 44 – 5 side effects–191 pathways–199
fusion–45 topical–190 –1 paracetamol (acetaminophen)–198
myocardial ischaemia, silent–124 non-union, fracture–103 paraffin baths–209
MyoD–43, 45, 47, 48 NSAIDs see non-steroidal parasympathetic tone–124
myofascial trigger points–205, 212, anti-inflammatory drugs parathyroid hormone–105
218 passive stretching–243 – 4
myofibre see muscle fibre oedema patellar dislocation/subluxation–
myofibroblasts–238 electrical stimulation and–218 310
myogenic precursor cells–36, 41–2, pathophysiology–14, 23 patellar taping–310
44–5 omeprazole–191 patellar tendinopathy–63, 310
myogenic regulatory factors opiate pain control theory–218 patellar tendon
(MRFs)–36, 45, 47 opioid receptors–195 ACL autografts
myogenin–45, 47 opioids (narcotics)–194 – 8, 200 goat studies–85 –90
myoglobin, muscle–132 clinical applications–196 human studies–79 – 81, 82
myosin–46–7 dosage–197 biomechanics of injury–63
324 index
patellar tendon (cont.) prednisone–192, 193 psychologists, sports–174 – 5

collagen fibril size distribution prehabilitation–289 psychotherapy–174
goat–85, 86 exercises–291–2 pyramidal system–277
human–78, 79 protocols for specific sports–292–8
rabbit–61, 62 preparticipation exam–7 quadriceps–hamstrings ratio–260,
healing–68 prevention of injury model–3 – 4 298
insertion–60 preventive rehabilitation–7 quadriceps muscle
origin–60 procaine–200 reflex inhibition–258 –9
patellofemoral pain syndrome–259, propoxyphene–197, 200 strength differences between
310 proprioception–274 – 86 limbs–259
pathophysiology of injuries–10 –27 definition–274 wasting after injury–259
PCL see posterior cruciate ligament effect of injury–278 –9, 310 quadriceps tendon, insertion–60
pentazocine–197 measuring performance–277– 8
percutaneous electrical nerve neurological mechanisms–274 –7 racquet stretch–293
stimulation (PENS)–220 re-education–279 – 84, 285 – 6 range of motion (ROM) see joint
performance, athletic adaptation to training–284 range of motion
flexibility and–236 –7 lower limbs–282– 4 rectus femoris tendon injury–64
training cessation and–134 – 5 upper limbs–281–2 reflexes, proprioceptive–276
peripheral resistance, total–122, proprioceptive neuromuscular reflex inhibition–152, 216, 258 –9
123, 124 facilitation (PNF, Kabat rehabilitation–145 – 6, 264 –70
peroxidase–16, 17 method)–240 –2, 280–2 adherence–167–9, 172
personal factors contract–relax (CR)–241 first (acute) phase–264 – 5, 288
psychological responses to injury contract–relax–agonist contract functional–288 –97
166, 168 (CRAC)–241–2 functional phase–288, 289
rehabilitation outcomes–170 efficacy of one session–248 goals see goals, rehabilitation
personality–170 efficacy of repeated sessions–249 lack of effective–4, 6
phagocytosis, in muscle injury–41 lower limb–282– 4 phases–288
pharmacological agents–187–98 number of repetitions–247 plan–45
phonophoresis–192, 213 optimum duration–246 preventive–7
phosphofructokinase–133 upper limb–281–2 psychological influences on
phosphorylase–133 warm-up before–250, 251 outcome–169 –73
physical modalities–204 –24 proprioceptive reflexes–276 recovery phase–288, 289
fracture healing and–103 – 5 proprioceptive sensation–274 second (training) phase–265 –9
mechanisms of action–23 – 4 proprioceptors–275, 276 third (return to sport) phase–
in prehabilitation–292 prostaglandin E 2 (PGE 2)–13, 14 269 –70
soft tissue healing and–73 prostaglandin I 2 (PGI 2)–13, 14 reinjury risks–145, 270
piroxicam–188, 190 prostaglandins–13 –15, 189, 190 relaxation–172, 173
plantar fascia, corticosteroid prostaglandin synthase–13 relaxation syndrome–123
injection–194 proteins, plasma–119 renal toxicity, NSAIDs–191
plantar fasciitis–215 proteoglycans repetition maximum (RM)–264, 265
plasma volume–119 –20, 122 articular cartilage–107– 8 repetitions, number of–264, 265, 269
plasmin–21 bone–100 resistance/strength training–260 – 3
plasticity ligament and tendon–56, 57, children and adolescents–263
Achilles tendon–72 75 – 6, 91 contralateral effects–261
effects of stretching–240 muscle repair and–51 dynamic–261–2
plate fixation, fractures–103 protopathic superficial sensation 275 electrical muscle stimulation and
platelet-activating factor (PAF)–14, proximal interphalangeal joint, 262
22 dislocation–311, 312 endurance training interaction 264
platelet-derived growth factor P-selectin–18, 22 gender differences–263
(PDGF)–39 – 40, 43, 101 psychological factors–160 –77 methods–261–2
platelets–18–19, 22, 27 future research directions 175–6 muscle volume increase–261
plyometrics–268–9 implications–173 – 5 neuromuscular activation–260 –1
plyometrics/agility protocols in injury occurrence–176 prehabilitation protocols
running–295, 296 in rehabilitation outcomes running–295, 296
soccer–297, 298 169 –73 soccer–297, 298
tennis/baseball–292– 3, 294, 295 psychological interventions–172– 3, tennis/baseball–292, 294, 295
PNF see proprioceptive 175 – 6 in rehabilitation–264, 265 – 8
neuromuscular facilitation psychological responses to injury– static–261, 262
postcapillary venules–23 161–9 respiratory adaptations
posterior cruciate ligament (PCL) behavioural–167–9 effects of detraining–117–25
effect of mobilization–75, 76 emotional–164 –7 reduced training and–136
mechanisms of injury–60 explanatory models–161– 4, 175, respiratory depression, opioid-
prednisolone iontophoresis–214 –15 176 induced–197
index 325
respiratory disorders–8 skeletal dysfunction, flexibility and strength, muscle–258 –70

respiratory exchange ratio (RER)– 237 cross-transfer effect–137, 261
125, 136 soccer–291 detraining effects–135, 138
respiratory tract infections, upper– prehabilitation–296 – 8 difference between two limbs–
20 return to sport programme–299, 259
rest–149–55 300 electrical muscle stimulation and
see also detraining; social support–170 –1 217–18
immobilization sodium salicylate–188 immobilization-related loss–
rest, ice, compression and/or somatosensory cortex–276 150 –1
elevation (RICE) somnolence–25 postinjury reduction–6, 258 – 60,
in ligament/tendon injuries 66, 67 spondylolysis–149, 311 270
in muscle injuries–49 sport profiling–289 –90, 291, 299 reduced training and–136
return to sports–269 –70, 289 sports injuries–4 –7 training see resistance/strength
criteria–298–9 acute see acute injury training
functional programmes–299, 300 anatomical distribution–6 –7 stress
RICE see rest, ice, compression benefits–176 fractures–100
and/or elevation chronic see chronic injuries neuroendocrine response–24 – 5
rofecoxib–190 diagnostic context–146 – 8 psychological, injury-related–
role, identification with athlete–166, epidemiology–3 – 8, 145 161
170 flexibility in prevention–235 – 6 stress inoculation training–172, 173
ROM see joint range of motion frequent diagnoses–7 stress relaxation
rotator cuff disorders multifactorial nature–146 definition–233, 234
acupuncture–199 pathophysiology–10 –27 procedure–245, 246 –7
diagnosis–146–7 physiological/functional effects– stretching see flexibility training
physical modalities–212, 215 144 – 57 stretch reflex–239 – 40, 242, 244, 276
Ruffini corpuscles–275, 276, 279 psychological responses–161– 4 inverse–240, 244
runner’s knee–310 reinjury risk–145, 270 stroke volume–121, 122
running–291 severity–7 ST segment depression–124
prehabilitation–295 – 6 time from onset–5 – 6 subclinical adaptation complex–
return to sports–298 types–4 – 5 147
sports psychology professionals– substrate availability/utilization–
salbutamol–200 174 – 5 125 – 8
salicylic acid–187– 8 sports-specific demands–289 –92 succinate dehydrogenase–132– 3
salmeterol–200 critical point framework–288 suicide risk–165
satellite cells–35–7, 52 prehabilitation exercises– sulindac–188
activation–37, 42– 4 291–2 superficial digital flexor tendon,
ageing changes–37 sprains–7, 8 equine–64
differentiation into myoblasts– spray and stretch technique–205 supraspinatus tendon–64, 68
42, 44–5 sprinting–291 swimming–7, 291
growth factors/cytokines static stretching–243 – 5 sympathoadrenergic tone–120, 124
affecting–39 efficacy of one session–248 synovial fluid, immobilized joints–
myogenic regulatory factors–36, efficacy of repeated sessions– 154
45 248 –9 synovial hyperplasia, immobilized
scaphoid fractures–311, 312 number of repetitions–246 –7 joints–154
scar tissue–238 optimum duration–245 – 6 systemic lupus erythematosus
decorin antisense therapy and– position effects–252– 3 (SLE)–22
91–2, 93 practical guidelines–253
effect of stretching–240 repeated–244 – 5 temperature
in ligament/tendon healing–66, 67 by therapist (passive)–243 – 4 intramuscular, after warm-up–
sedation, opioid-induced–197 warm-up prior to–249 – 52 251
self-talk–172, 173 active warm-up–250 –2 intratendinous–57, 64
sensation, classification–274 – 5 passive warm-up–250 tissue, flexibility and–249 – 50
sensory receptor organs–275, 276 stem cells, mesenchyme–91 tendon–56 –92
serotonin–15, 18–19 steroidal medications–191– 4 biomechanics–57– 60
severity of injury–7 see also anabolic steroids; corticosteroid injection–194
shoe, athletic–306 corticosteroids hyperthermia–57, 64
shoulder stiffness injury–146, 148
injuries–6, 146–7, 212 after ACL injury–69 biomechanics–64
prehabilitation–292– 5 definitions–233, 234 collagen fibril size distribution
situational factors straight leg raise (SLR)–239 after–61–2
psychological responses to injury strain, mechanical, fracture healing rehabilitation–148
166–7, 168, 169 and–102 ultrasound therapy–212
rehabilitation outcomes–170 –1 strains–7, 8 insertion to bone–60, 63
326 index
tendon (cont.) tissue repair/healing–25 –7 upper limb

mechanoreceptors–274 bone–100 – 6 orthoses–311–12
repair/healing–64 –9 cartilage–108 –12 proprioceptive re-education–
acute inflammatory phase– effects of NSAIDs–41, 49, 189, 190 281–2
64–5 electrical stimulation and–214
phases–64, 65 physical modalities and–73 vapocoolant sprays–205
proliferative phase–65 –7 skeletal muscle–35 – 52 vascular cell adhesion molecule 1
remodelling and maturation soft tissue contracture after– (VCAM-1)–42
phase–67–9 237– 8 vascular permeability–23
tissue engineering approaches tendons and ligaments–64 –92 vasculature
91–2 T-lymphocytes–14, 19, 20, 26 immobilization-related changes–
rupture, spontaneous–64 tolerance, opioid–198 153
structure–56–7, 58 tolmetin–188 injury–18 –19
tensile strength see tensile total peripheral resistance–122, 123, response to injury–22– 3
strength, ligament/tendon 124 vasoconstriction–23, 27
tendonitis (tendinosis)–7, 8 trabeculae–99 vasoconstrictor agents–200
tennis–291 traction–220 – 3, 224 vasodilatation–23
prehabilitation–292– 5 cervical–221–2 vasopressin–24, 25
upper limb injuries–311, 312 lumbar–222– 3 ventilatory function–124 – 5
tennis elbow see lateral training very late antigen 4 (VLA-4)–42
epicondylitis adaptations, retention–135 –7 very low-density lipoprotein
tensile strength cessation see detraining cholesterol–127
ligament/tendon–74 – 8 coordination–284 –5 viscoelasticity–233 – 4, 235
ACL auto/allografts–82, 84, 85 cross- see cross-training ACL autografts–88 –9
collagen fibril size distribution endurance, postinjury–263 – 4 viscous (properties)–233, 234
and–61, 62, 82, 84 reduced–136 –7, 138, 155 V̇ O 2max
effect of immobilization–74 – 5 unilateral, cross-transfer–137, arteriovenous oxygen difference
effect of mobilization–65 – 6, 138, 261 and–132
75–8 see also flexibility training; blood volume and–119 –20
postsurgery–69 resistance/strength effects of detraining–118 –19,
surgical repaired ligaments– training 154 – 5
76–8 transcutaneous electrical nerve reduced training and–136
muscle, recovery after injury–149 stimulation (TENS)–218 –20 stroke volume and–121
tension, musculotendinous unit– transferrin–24 volleyball–291, 312
233–4 transforming growth factor beta von Willebrand factor–18
TENS (transcutaneous electrical (TGF-β)–11, 12
nerve stimulation)–218 –20 in fracture healing–101, 102 warm-up
terbutaline–200 in muscle injury–39, 43, 51, 52 active–250 –2
testosterone–131, 136, 192 traumatic injuries–4 – 5 passive–250, 252
testosterone:cortisol ratio–131, triacylglycerol–127 prior to static stretching–249 – 52,
136 triamcinolone acetate–193 253
TGF-β see transforming growth triceps surae stretching–250 tendon/ligament changes–59
factor beta trigger points, myofascial–205, 212, warm water immersion–209
thermotherapy see heat therapy 218 water
thromboxane A 2 (TxA 2)–13, 18 –19 triglycerides–127 in articular cartilage–107– 8
throwing–291 tumour necrosis factor alpha exercise in–208 –9
return to sports programme–298, (TNF-α)–11, 12, 13, 14 in ligament/tendon repair–65, 67
299 in inflammation–24, 25 warm, immersion–209
thyroid hormone–47 in muscle injury–39, 41 weightbearing
thyroid-stimulating hormone–24 in tissue repair–26 in chondral injuries–111
tibialis anterior tendon, ACL tumour necrosis factor beta (TNF-β) early, in fractures–102– 3
allografts–82– 3 12 weight-training–265
tibialis posterior tendon, ACL circuit–270
allografts–83 ulnar neuropathy–312 closed and open kinetic chain–
tibial plateau fracture–100, 103, ultrasound therapy–210 –13 266
104 application methods–210 –11 free weights vs weight machines–
tissue engineering, ligament/ clinical applications–211–13 266 – 8
tendon repair–91–2 fracture healing and–103 – 5 see also resistance/strength training
tissue injury prior to stretching–250 whirlpools–209
biomechanics–62– 4 soft tissue repair and–73 wound contraction–238
complex–147, 148 –9 see also phonophoresis wrist
inflammatory response–22– 5 unstable planes, exercises on–280, injuries–311, 312
tissue overload complex–147 281, 284 – 5 orthoses–312

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REHABILITATION OF

AN IOC MEDICAL COMMITTEE PUBLICATION

IN COLLABORATION WITH THE

INTERNATIONAL FEDERATION OF SPORTS MEDICINE

SUB-COMMISSION ON PUBLICATIONS IN THE SPORT SCIENCES

Howard G. Knuttgen PhD (Co-ordinator)

AN IOC MEDICAL COMMITTEE PUBLICATION

IN COLLABORATION WITH THE

INTERNATIONAL FEDERATION OF SPORTS MEDICINE

First published 2003

Library of Congress Cataloging-in-Publication Data

Rehabilitation of sports injuries : scientiﬁc basis / edited by

Set in 9/12 Palatino by Graphicraft Limited, Hong Kong

Commissioning Editor: Andrew Robinson

For further information on Blackwell Science, visit our website:

List of Contributors, vi 7 Physiological and Functional Implications

Preface, ix 8 Psychological Factors in Sports Injury

J. AUDETTE MD, Instructor, Department of W.R. FRONTERA MD, PhD, Chairman,

S. PADILLA MD, PhD, Department of Research M. SCHWELLNUS MD, PhD, Associate

The general aim of the Encyclopaedia of Sports Princes Alexandre de MERODE

Pathology (injury) Impairment Functional loss Disability

Epidemiology of Sports Injuries:

in the identiﬁcation of risk factors for sports

1 Establishing the extent of the injury

2 Establishing aetiology and

Fig. 1.1 The sequence of

Time from onset

Epidemiological studies show that, when the

Fig. 1.3 Falls in cycling can result

the injured athlete. The athlete may delay seek- 100

MSK logical and functional capacity in later stages.

Although in the recent past, understanding of

on target cells. Through this interaction the up-

Cytokine Cell source Cell target Biological activity

IL-1α Monocytes All cells Up-regulation of adhesion molecule expression

of cyclooxygenase function. Throughout these oedema. In states of inﬂammation, however, an

such as speciﬁc cyclooxygenase inhibitors in anti-

Table 2.2 Macrophage-derived secretory products.

Table 2.3 Contents of neutrophil granules and vesicles.

Azurophil granule Speciﬁc granule Gelatinase granule Secretory vesicle

Cd63 Cd66 Cd11b Alkaline phosphatase

TNF, tumour necrosis factor.

Classic pathway with the release of histamine, PAF and serotonin.

Table 2.4 Patterns of disease in complement-deﬁcient patients.

Deﬁcient component Disease

SLE, systemic lupus erythematosus.

Platelet aggregation and formation, whereas constriction leads to increased

0 Fig. 2.6 Changes seen in serum

similar to the preinjured state. A coordinated pro-

Skeletal Muscle Regeneration After Injury:

tion (Hudgson & Field 1973). Discontinuous

Fig. 3.1 Anatomical location of

Degenerative phase Regenerative phase

The degenerative phase A

This is also known as non-inﬂammatory or

thus unlikely that bFGF is a key chemoattract-