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THE THERAPEUTIC POSSIBILITIES OF SURGICAL

BIO-ENGINEERING IN INCOMPLETE SPINAL CORD LESIONS

(SPINAL CORD RELAXATION IN THE SURGICAL TREATMENT OF


INCOMPLETE SPINAL CORD LESIONS)
By ALF BREIG, M.D.
Sjukhuset, Stockholm, Sweden

THE aspect of bio-engineering I am going to describe can be described briefly as


spinal cord relaxation.
In surgical operations on the skeletal system our approach is governed by well
understood principles. In the case of the spinal cord, however, our knowledge of
the effect of pathological changes on the nerve parenchyma, unfortunately, leaves
much to be desired.
It is a generally accepted fact that mechanical stress on the ulnar nerve can be
relieved by transposition and that here the underlying mechanism is relaxation of
the nerve tissue. On the other hand, no one appears to have considered the
possibility that the detrimental forces acting on the soft parenchyma of the spinal
cord can also be eliminated by corrective surgery. It is true that in surgery today
there is a tendency to intervene and correct anomalous functional processes in soft
tissue organs, for instance, heart valve surgery and in various shunt operations for
hydrocephalus.
To visualise the kinds of pathological stress in the cord tissue that occurs in
practice I have recently reproduced as accurately as possible in situ in the cadaver
the forces to which the cord is subjected, when the vertebral column is (a) dorsi­
flexed and (b) ventriflexed. While subjected to stress, the cord, whose blood
vessels had previously been filled with radio-opaque medium, was fixed with
formalin. In this way it was possible to conduct a thorough examination of the
deformation of the cord tissue and its blood vessels, which gives an indication of
the forces to which these structures were exposed.
It was found that tensile, compressive and torsional forces invariably produce a
pathological tensile stress field within the cord parenchyma.
Our knowledge of the existence of these stress fields is now sufficient to afford
a guide to the appropriate surgical measures by means of which the stress acting
within the cord parenchyma can be counteracted or eliminated, thereby promoting
the blood circulation and improving neural conductivity. It would seem evident
that it is the deformation within the conducting axon cylinders that is the prime
cause of reversible neurological symptoms.
An outline of our present knowledge of the biomechanical behaviour of the
cord is now given to illustrate my thesis. It is the movement of the cord that in the
presence of pathological processes are ultimately responsible for neurological
symptoms. The pons, medulla oblongata and the cord, with their cranial and
spinal nerve roots, may be regarded as a continuous tissue tract, which is firmly
anchored rostrally at the mesencephalon and caudally by the attachments of the
nerve roots. As a result of this anchorage, the tract adapts itself immediately and
173
174 PARAPLEGIA

continuously to the shortening and elongation of the spinal canal during dorsi­
flexion and ventriflexion respectively. This adaptation occurs through internal
changes in the shape of the component structures of the parenchyma. Regarding
the many structures involved in this process of adaptation, reference will only be
made to the fact that the collagenous elements are arranged in a rhomboid structure,
whose angles of intersection change during elongation of the canal and hence
enable the cord to lengthen. When the head and spinal column are in the erect
position, all the elastic components that have become folded and have thus formed
a 'tissue reserve' during dorsiflexion, are pulled out smoothly. When the head and
column are ventriflexed the elastic components are further extended, and their
elasticity is now exploited. In Figure I, the folding of the axis cylinders is seen as

FIG. 1
Sagittal section through the cervical spinal cord at the level of C6,
Dorsal aspect. Palmgren's stain. x 370. A, On ventriflexion of the
cervical spine the parenchymal network is drawn out and the axis
cylinders straighten. B, On dorsiflexion the axis cylinders fold three-
dimensionally (Breig, 1960).

the tract comprising the pons and cord is shortened (fig. I, A), and their extension
as the tract lengthens again (fig. I, B).
An observation of major practical significance is the slackening of the pons­
spinal cord with their nerve roots, as the spinal canal is shortened. The fact that
the slackness is not evident to the naked eye would account for it having been over­
looked for so long. From the neurosurgical literature it is evident that the opposite
process, namely the stretching of the cervical cord when the head and cervical
column are flexed forwards, has long been recognised; in fact, many authors have
complained that this is a source of difficulty in operations on the ventral aspect of
the cervical canal, and incurs a risk of damage to the cord. As we now know today,
this can easily be avoided altogether by simply dorsiflexing the cervical spine, so
that both the cervical cord and its nerve roots are slackened. In this state the cord
THERAPEUTIC POSSIBILITIES OF SURGICAL BIO-ENGINEERING 175

can be raised from the canal and drawn to the side to the full extent permitted by
the nerve roots.
Although the author described the slackening phenomenon as long ago as
1957, it was only in 1960 that he required to test it in practice in an operation for a
clivus meningioma. In 1956, Dodge in the Mayo Clinic wrote that 'although most
tumours in the foramen magnum region are benign, any attempt to remove them
may result in no more than a Pyrrhic victory'. In our case the meningioma was an
extremely large one, as was seen in the air myelogram. The tumour forced the
pons and the medulla oblongata backwards in a large arc. It appeared obvious to
us that this displacement set up powerful tensions in the pons and medulla
oblongata in both axial and transverse directions. After removing the bone and
uncovering the dura we dorsiflexed the head and neck, a manipulation that now is
greatly facilitated by a specially designed head support. Apart from the fact that
the space available for surgery became more restricted, nothing in particular could
be seen with the naked eye, but on insertion of brain spatulae it appeared to be
much easier to move the pons and medulla oblongata to the side. The tumour
could then be removed by piecemeal extirpation without difficulty. After the
operation, spontaneous respiration was resumed, though it had been expected that
respirator treatment might be necessary. After about 14 days the patient had
almost fully recovered from her tetraspasticity, defective sensibility and urinary
incontinence. During the past decade we have used this spinal cord relaxation
technique with advantage to both patient and surgeon in operations at sites located
from the posterior cranial fossa to the sacral end of the spinal canal.
A long-standing impediment to the recognition of the nature of the forces
acting on both the spinal cord and the nerve roots in the individual situation has
been the view, still adhered to today, that all mechanical stresses on the spinal cord
and nerve roots is compressive. This myth was finally exploded in 1963 by Marions
and the author in the examination of 120 patients with a suspected intervertebral
disc herniation, by means of a water-soluble contrast medium which was injected
into the lumbosacral canal. To ascertain what actually happens to the spinal cord
and its nerve roots as a consequence of the forces set up by the herniation, the con­
ventional radiographs were supplemented by two extra radiographs of the lumbar
region, with the cervical spine firstly in dorsiflexion and then in ventriflexion
(fig. 2). It was then clearly seen that during dorsiflexion the medullary cone fell
some millimetres in the caudal direction owing to the relaxation of the spinal cord
and the simultaneous slackening of the nerve roots, (a) , while on ventriflexion of
the head and the cervical spine the cone and the nerve roots were straightened (b).
In disc herniation the nerve root is pulled against the disc protrusion and at the
same time stretched over it; and what is just as important, within the spinal canal
in these studies there was no evidence of any osseous or other structure opposite the
protrusion that could have involved the nerve root in a 'pincer action'. This
prompted us to carry out our first examination of the type of mechanical stress that
is exerted by a disc protrusion on the parenchyma of a nerve root or of the spinal
cord under the conditions just outlined. The macroscopic changes and effects will
be considered first. During the phase when the spinal canal is undergoing elon­
gation, any ventrally or anterolaterally located protrusion exerts a pressure on the
nearest section of the pons-spinal cord-nerve root structures: this pressure is greatest
in the region or plane of contact and diminishes to zero on the opposite free surface
of the section of the structures in question. At the same time the protrusion exerts
PARAPLEGIA

a tension on the section of the neural structures that are curved and stretched over
it. This tension is least along the aspect in contact with the protrusion and greatest
along its free aspect. From an analysis of a large number of pathological changes
that exert a unilateral pressure on some part of the stretched pons-spinal cord

FIG. 2

The propagation of the pons-spinal cord tissue


tract's slackening and stretching to the lumbo­
sacral nerve roots visualised by water-soluble
contrast injection into the lumbar subarachnoidal
space. A, In dorsiflexion of the cervical spine the
nerve roots form a smaller angle with the margins
of the vertebral bodies than in ventriflexion (B).
The nerve roots are respectively slackened and
stretched.

system it would appear that the stress can invariably be reduced to what might be
described as the thrust effect of an impinging body.
Histological sections through an arbitrary area of the pons and spinal cord
show that when they are stretched all unyielding pathological changes that are
located outside, or more accurately ventral to, or within its parenchyma (from the
region of the incisura tentorii to the sacral canal), give rise to the same phenomenon,
namely pressure on and vaulted narrowing of the extended nerve tissue. As a
THERAPEUTIC POSSIBILITIES OF SURGICAL BIO-ENGINEERING 177

result of this thrust the strata running parallel to the transverse or sagittal sectors of
the impinging body move closer to one another, while their tendency to crowd
together decreases with the distance from the impinging body. The effect of an
inclusion body has been studied by inserting a small metal cone in the cord tissue

FIG. 3
Tensile stress field within the cervical spinal cord artificially pro­
duced by inserting a small metal cone into the cord tissue and
fixing it' in situ by injection of formalin into the subarachnoidal
space. Section in front of the coronal mid-plane. Numerous
branches of the central arteries with their surrounding Virchow­
Robin's space are met. A, On ventriflexion of the cervical spine
the fibres bend and stretch over the cone. x 19'4. B, On dorsi­
flexion of the cervical spine (in another case) the fibres slacken
and leave their contact with the cone. The tensile stress field is
then dissolved. x 10'0.

in situ (fig. 3). Histological studies show that it is possible to follow the whole of a
typical tensile stress field set up on ventriflexion of the spinal column. The field is
indicated by the decreasing extent to which the fibres are packed and by the reduc­
tion in their bending with the distance from the impinging body towards the peri­
phery. In the present ideal case (so far as the visible manifestations of the
histodynamic stress are concerned) the direction of the tissue fibres corresponds to
the lines of force of the stress field. All the evidence indicates that it is the tension
PARAPLEGIA

in, and bending of, the conducting nerve elements with the accompanying decrease
in their cross-section and the corresponding increase in their resistance to conduc­
tion that account for the neurological symptoms. When the spinal canal is elon­
gated the deformation of the parenchyma usually increases directly as the tension in
the cord, and as we know symptoms can sometimes derive from adjacent pathways.
As has already been stated above, the neurological symptoms may often disappear;
that is to say, when the fibres slacken and the tensile and bending strain has been
relieved their conductivity can recover. The return of conductivity of the ulnar
nerve that may be achieved by its relaxation by operative transposition demonstrates
a familiar parallel in the peripheral nervous system.
It is, however, not only the strain in the actual conducting nerve elements
that accounts for the neurological symptoms, but also the hypoxia of the nerve cells
that occurs when the lumen of their supplying blood vessels (as integral compo­
nents of the parenchyma) are reduced by being stretched, if they happen to run
parallel to the axis of the tension strain field. A typical example where the symp­
toms of neurological deficit are evoked by a critical reduction of the lumen of blood
vessels is found in the atrophy of nerve cells of the lateral pyramidal tracts, a
process that sometimes occurs in cervical spondylotic myelopathy. These cells
are, of course, located quite a distance from the osteophytes on the ventral aspect of
the cervical canal that are responsible for the stress in question. In a study that
Turnbull and the author made in 1966 to analyse this situation, it was found that
the branches of the central arteries that supply the pyramidal tracts happen to run
parallel to the axis of a tension strain field oriented in the transverse direction of the
cervical cord. If the tension in the parenchyma is great enough and the resulting
narrowing of the blood vessels has led to protracted hypoxia within the corres­
ponding region, the hypoxia can ultimately lead to atrophic changes of the lateral
pyramidal tracts. This would seem to afford a plausible explanation of the impair­
ment of an area of parenchyma remote from the osteophytes that are responsible for
the pathodynamic strain.
The tensile stress field mentioned earlier in this paper can be resolved by the
relaxation of the pons-spinal cord complex, as is evident from, for instance, the
rapid regression of the neurological symptoms following removal of a clivus
meningioma. In the case of smaller lesions the relaxation of the tract required for
relief of the tensile and bending stress can be procured by simply dorsiflexing the
cervical spine.
The tension in the nerve fibres produced by the unilateral thrust of an
impinging body acting on the parenchyma of a stretched spinal cord either from
without or from within towards the pia is usually of moderate degree. In the case
shown in Figure 4, the tensile stress has been exerted by an osteophyte located
ventrally in the cervical canal. In the histological section through the coronal
plane of the cervical spinal cord in the specimen (see fig. 3), the thrust of the nerve
fibres exerted by an intraparenchymally located unyielding body has been repro­
duced by inserting a small metal cone in the cord tissue. The effect of this cone
and that of the osteophytes on the parenchyma during physiological stretching of
the spinal cord, when the spine was flexed forwards is shown (fig. 4); Etissues fixed
by subarachnoidal formalin injection in situ).
In contrast to a thrust's moderate tensile and bending stress that can usually
be resolved by slackening the spinal cord, bilateral constriction of nerval tissue
through compression, or more obviously, a pincer action always produces an
THERAPEUTIC POSSIBILITIES OF SURGICAL BIO-ENGINEERING 179

extremely high axial tension (the resultants of which are directed in cranial and
caudal directions) in a limited section of the tissue. Under certain conditions, this
tension will inevitably result in rupture of the cord substance. This has not
hitherto been fully explained.
The mechanical effect of a pincer action on an elastic body may be examined by
means of a stress optical model. As is indicated in the isochromes in a photograph,

FIG. 4
A, (upper); Transverse section through a tensile stress field in
the right side of the cervical spinal cord (left side disregarded)
produced by the unilateral thrust of the right part of a dumb­
bell shaped osteophyte located ventral to the cord. Lower: mag­
nified (framed) part of the tensile stress field from above. x 80.
B, (upper and lower); Transverse section through cervical spinal
cord parenchyma at the identical segmental level as in specimen
(A), but formalin fixated in the erect position. Normal histologic
picture without evidence of any mechanical stress. Lower left and
right specimen; Whilst in the unloaded state the parenchyma has a
honeycomb-like appearance, the laterad-towards the dentate
ligament-directed tension in the left specimen has led to a clear
stratification. In spite of the fact that the layers are more packed
in the left specimen, there appears a clearly visible intercellular
space and due to the transverse widening a bigger interspace can
be discerned between cell-bodies and transversally cut axis
cylinders.

taken of the compressed body through a polarising glass plate, an axial tension is
set up in a short segment of the body (the information provided by the isochromes
concerning differences in the material can be transposed into a graph).
To examine the effect on the parenchyma of a pincer action on the spinal cord
the following experiment has been performed. By means of the registration
technique mentioned above in a few of the 21 post-mortem specimens with the
cervical spine in the dorsiflexed position, the cervical cord was compressed to exert
180 PARAPLEGIA

a pincer action. This was achieved by pushing a round wooden plug towards
the anterior aspect of the dura and cord through a hole drilled between the C5 and
C6 vertebrae; in others of these specimens a similar pincer action on the cervical
cord was exerted by inserting the plug from
behind. Pressure great enough to reduce the
diameter of the cervical cord by about 20 per
cent. usually tore the parenchyma, irrespective
of whether the compression had been exerted
extremely slowly or as rapidly as the method
permitted.
When the plug was pushed in from behind
towards the anterior wall of the cervical canal
tearing of the ventral aspect of the cervical cord
always occurred. This contradicts the view held
hitherto that in the so called hyperextension injury
it is the flaval ligaments that are responsible for
the tearing of the dorsal aspect of the cervical
spinal cord. In fact, this must be due to an un­
yielding body moving in the anteroposterior
direction and consisting either of an intervertebral
disc or of an increased volume of cerebrospinal
fluid (fig. 5). The unyielding body can be reliably
identified only by means of rapid cinematography.
The material in which it has been possible to
obtain clinical experience of the special thera­
peutic possibilities offered by slackening of the
spinal cord is limited to 4 patients; 3 of them
suffered from cervical spondylotic myelopathy
and I from the sequelae of a central spinal cord
injury. This latter patient has been operated
upon too recently to warrant inclusion in the
survey of the results.
FIG. 5
In 2 of these patients within a few days after
Tearing of the dorsal aspect of a surgery tetraspasticity diminished markedly and
cervical spinal cord specimen
sensibility and bladder continence returned. In
produced in situ by a wooden
plug moving in the antero­ the other 2, central hemiparesis improved, and
posterior direction with the cer­ there was better control of bowel function.
vical spine kept in maximum Regarding the occurrence of a complete
dorsiflexion. Only one-eighth of
interruption of conductivity of certain spinal cord
the width of the parenchyma at
the ventral aspect of the cervical
pathways the myelopathy cases do not meet the
spinal cord still consists of criteria that one usually places on the term
coherent (undamaged) fibres. 'incomplete cord lesions'. But the neurological
This type of damage has hitherto symptoms in these cases are due to histodynamic
been ascribed to a protruding
stress similar in principle to that which would be
flaval ligament.
expected in incomplete or seemingly complete
transverse lesions. For recovery of the conductivity of certain neural pathways due
both to spinal cord injury and cervical myelopathy the nerve fibres must not, of
course, be tom. It is thus the preserved anatomical continuity of some or all of the
nerve fibres and the increased tension in these fibres with subsequent impairment of
THERAPEUTIC POSSIBILITIES OF SURGICAL BIO-ENGINEERING 181

conductivity that are the common factors in these heterogeneous cord affections. If
the respective nerve fibres in these two types of lesion are neither torn nor atrophied
but their conductivity is still reduced or abolished completely, there will probably
be a histodynamic strain similar to that produced by a unilateral thrust. On the
basis of these experimental and clinical observations it would appear to be justified
today to infer that under these particular conditions of histodynamic strain that
there is a theoretical chance that recovery of the conductivity of the neural
parenchyma can be secured by relaxation.
An outline of the essentials of the surgical technique for relaxing the pons and
spinal cord will now be given. Gas myelography is carried out prior to operation
to rule out or demonstrate the presence of pathological formation within the spinal

� BII� a b

c
FIG. 6
Schematic representation of the amount of resection of the upper rim of the
vertebral arch (arco-cristectomy) necessary for alleviation of its pincer action
on the spinal cord in the presence of another encroaching protrusion ( osteophyte)
in the ventral wall of the canal. The part of the vertebral arch shaded in the
diagrams must be incised and then lifted up from the dura. No instrument is
to be inserted between the bone and the dura mater as any further encroachment
on the nerval elements immediately increases the tensile stress in the parenchyma
with irreversible damage as the inevitable consequence.

canal that may be compressing the cord or nerve roots or that may do so on dorsi­
flexion of the cervical column; or to show cervical spinal canal stenosis. If such
formations are found, selective resection by a special conservative method (arco­
cristectomy) must be performed at the appropriate level. This operation can be
limited to removing the body, even just the upper border of a vertebral arch, which
is responsible for a pincer action (fig. 6). In accordance with the view just expressed
regarding the histodynamic tension it is felt that it may be eliminated simply by a
transplant of fascia lata and anchoring it between the external occipital protuber­
ance and the spinous process of the TI. For the sake of histocompatibility auto­
grafts have been used exclusively. In 2 of the patients available for follow-up
examination, the slight dorsiflexion of the cervical column was retained for more
than 3 years by means of a fascial graft. It would thus seem that this method is
also mechanically successful. If we accept the reduction or the disappearance
of neurological symptoms such as spasticity, impaired sensibility and urinary
182 PARAPLEGIA

incontinence as criteria of the therapeutic result, then those obtained with this
method so far may be classed as 'satisfactory' to 'extremely good'.
With a special instrument the degree of dorsiflexion of the cervical spine
required to obtain a slack cord can be determined. This was demonstrated in 1 of
the 3 patients with cervical myelopathy operated on in April 1970. He had had a
spastic hemiparesis and a corresponding spastic gait, impaired sensibility below the
iliac crests and slight urinary incontinence. A few days after the operation these
manifestations had appreciably diminished, and after a fortnight they had dis­
appeared almost completely. The patient is very satisfied with the result.
When the patient was trying to bend his cervical spine forwards as far as
possible, the head could be brought into the erect posture, which is slightly forward
of the intended position.
This surgical method constitutes a new active conservative measure for the
treatment of spinal cord disorders, both those caused by extramedullary unyielding
processes in the spinal canal, and intraparenchymal changes including the scarring
resulting from spinal cord trauma. This surgical approach is fully consistent with
the conservative principles adopted by Sir Ludwig Guttmann. But I venture to
suggest that it is more direct, and more far reaching and radical, since it effectively
eliminates any harmful tensile stress in the spinal cord parenchyma that must in­
evitably arise from the lengthening of the cervical spinal canal that occurs when the
neck is flexed forwards.

SUMMARY

The author is firmly convinced that by relaxing the pons and the spinal cord
a number of disorders of the central nervous system are rendered accessible for
symptomatic treatment, amongst them, intraparenchymal affections. Just which of
them, and how many cases of, for instance, multiple sclerosis and sequelae of spinal
cord injury can benefit from this method can only be established by practical
experience. The accumulation of such experience is a challenging task.
A number of misconceptions have hitherto stood in the way of a realistic assess­
ment of the tensile forces to which spinal cord tissue is submitted during functional
movements of the spine in the presence of unyielding pathological changes. An
insight into what happens in reality opens up a new practical approach to treatment,
namely relaxation of the spinal cord by a fascia lata graft and where necessary,
elimination of the pincer action by resection of the offending structure.

REFERENCES

BREIG, A. (1960). Biomechanics of the Central Nervous System. Stockholm, Sweden:


Almqvist & Wiksell.
BREIG, A. (1970). J. Biomech. 3,7-9.
BREIG, A. & MAruONS, O. (1963). Acta rad., I, 6, 1141-1160.
BREIG, A., TURNBULL, 1. & HASSLER, O. (1966). J. Neurosurg. 25, I, 45-56.
DODGE, 1. W. 1. (1956). J. Neurosurg. 13, 603.

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