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Volume 7 Number 2

Osteomyelitis Of The Jaw: A Retrospective Analysis

C Uche, R Mogyoros, A Chang, D Taub, J DeSimone

Citation
C Uche, R Mogyoros, A Chang, D Taub, J DeSimone. Osteomyelitis Of The Jaw: A Retrospective Analysis. The Internet
Journal of Infectious Diseases. 2008 Volume 7 Number 2.

Abstract
There is a paucity of recent data regarding osteomyelitis of the jaw (OMJ).Patients with inflammation of the jaw from Jan. 2000-
Dec. 2005 at TJUH underwent retrospective chart review. Forty-two patients met the criteria for OMJ (37 definite, 5 probable).
Mean age was 58 years. 78% were Caucasian. Most common risk factors associated with OMJ were tooth extraction, orofacial
malignancy and radiotherapy, and bisphosphonates use. Most common symptoms were pain, exposed bone/plate and cheek
swelling. Aerobic (GP 84%, GN 42%) and anaerobic (GP 53%, GN 27%) bacteria were identified. 34% of patients received > 4
weeks of IV antibiotics. Five patients achieved full recovery. Limited recovery was associated with orofacial malignancy and
radiotherapy (p= 0.06). Bisphosphonates use and radiotherapy for orofacial malignancy have emerged as major risk factors
associated with OMJ. Only orofacial malignancy and radiotherapy predicted limited recovery. Length of antibiotic therapy or
HBOT did not predict treatment outcome.

The article was previously presented in abstract/poster form 1991, Bernier et al 1995, Aitasalo et al 1998, Kushner et al
only at the 45th Annual Meeting of the Infectious Diseases 2004, Ruggiero et al 2004]. Risk factors associated with
Society of America in San Diego, CA on October 6, 2007. osteomyelitis of the jaw must be identified and modified if
possible. Known risk factors associate with osteomyelitis of
INTRODUCTION the jaw include diabetes mellitus, autoimmune diseases,
Osteomyelitis in the maxillofacial region has been a topic of malignancy, malnutrition, systemic steroids, chemotherapy,
discussion for many centuries. The unique environment of radiotherapy, bisphosphonates use, trauma, osteopetrosis,
the oral cavity and dentition in conjunction with a constantly acquired immunodeficiency disease, dental implant, sickle
changing intraoral environment has led to several cell anemia, alcoholism, intravenous drug abuse, renal or
classification schemes for mandibular and maxillofacial hepatic failure, chronic hypoxia, extremes of age and
osteomyelitis. Newer challenges have declared themselves tobacco abuse [Hudson 1993, Marx 1991, Bernier et al 1995,
with the emergence of osteoradionecrosis of the jaw Aitasalo et al 1998, Kushner et al 2004, Ruggiero et al 2004,
secondary to radiation to the head and neck as well as Lew et al 2004, Lew et al 1997].
osteonecrosis of the jaw as seen with bisphosphonates.
These new clinical entities may be different than traditional There has been, however, a paucity of studies on
osteomyelitis in terms of pathogenesis but are managed alike osteomyelitis of the jaw taking into account new risk factors.
in many respects. The presence of microorganisms in Hence a comprehensive review of the management of
osteoradionecrosis and osteonecrosis are thought to be osteomyelitis of the jaw as seen in an academic medical
secondary in their pathogenesis. center was undertaken. The objectives of the study were as
follows: to determine and update the risk factors associated
Numerous classification systems for osteomyelitis of the jaw with osteomyelitis of the jaw, to determine the clinical
exists [Hudson 1993], but regardless of the classification, the presentation and
goals of treatment always remain the same. The goals of
therapy are to remove dead bone and eliminate or at least microbiological etiology associated with osteomyelitis of the
attenuate the proliferating pathogenic microorganisms jaw, to determine treatment outcomes and which variables
through a combination of surgery and antibiotics, and then might impact the management of osteomyelitis of the jaw
give supportive care for healing. It is important to identify and to determine the morbidity and mortality associated with
the causative or associated pathogens [Hudson 1993, Marx osteomyelitis of the jaw.

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Osteomyelitis Of The Jaw: A Retrospective Analysis

METHODS of compared data. Data compared included outcomes and

A retrospective chart review was performed at Thomas other variables such as risk factors associated with
Jefferson University Hospital, Philadelphia, PA. Subjects osteomyelitis, antibiotic regimen, duration of symptoms,
included patients seen between January 1, 2000 and number of surgeries and demographic variables.
December 31, 2005 in the Department of Oral and
RESULTS
Maxillofacial Surgery. The International Classification of
Demographics. Three hundred patients were identified with
Diseases, Revision 9 (ICD-9) codes 526.4, 526.8 and 526.9
ICD-9 codes 526.4, 526.8 and 526.9. Forty two patients met
were used to initially select patients with possible
the criteria for definite or probable osteomyelitis (37
osteomyelitis. ICD-9 code 526.4 describes inflammatory jaw
definite, 5 probable). Forty one patients had one episode of
conditions. This category includes the diagnoses of abscess,
osteomyelitis and one patient had 4 episodes. Twenty three
osteitis, acute and chronic osteomyelitis, suppurative
patients (54.8%) were females. The mean age of the patients
osteomyelitis and periostitis. ICD-9 codes 526.8 and 526.9
and standard deviation (SD) was 58.3 ± 17.5 years (95% CI
describe other and unspecified diseases of the jaw.
53.11-63.21). Thirty three patients (78.6%) were Caucasian,
Individual patient charts were then reviewed for study
8 (19.0%) were African-Americans and one was Asian.
eligibility.
Risk Factors. Risk factors associated with osteomyelitis are
A definite diagnosis of osteomyelitis was given for biopsy
shown in table 1. The most frequent risk factors were tooth
proven osteomyelitis and as probable when one of the
extraction, orofacial malignancy and radiotherapy, use of
following three conditions was present: (i) positive cultures
bisphosphonates and nicotine abuse. Twenty nine patients
isolated from jaw during surgical debridement (deep bone
(69.0%) had more than one risk factor for osteomyelitis.
cultures), (ii) presence of exposed bone during examination,
or (iii) surgeon’s clinical impression of osteomyelitis. The Clinical Presentation. Twenty nine patients (69%) reported
University institutional review board (IRB) approved the pain. Other frequently encountered presentations were
study prior to chart review. exposed bone/reconstruction plate and check swelling in
42.9% and 38.1% of patients respectively. A summary of the
Data collection was performed by reviewing patient charts
clinical presentation is shown in Table 2. The duration of
and computer records. Data collected included
symptoms ranged from 1 week to 29 years. The mean
demographics, risk factors associated with osteomyelitis,
duration was 14.6 months. When the patient with the 29
clinical presentation (subjective complaints and physical
years of symptoms was omitted, the longest duration was 3.5
examination findings), treatment (type of surgery and details
years and the mean and standard deviation were 6.0 ± 8.1
of antibiotics), operating room cultures, imaging findings
months (95%CI 3.46-8.56). The location of lesions is
(MRI, CT and Xray findings), surgical pathology results and
presented in Table 3. The vast majority of lesions occurred
outcomes including complications.
in the mandibular body.
Adequate follow-up for this study was defined as physician-
Microbiological Data. Microbiological samples were
patient contact for at least three months post-operatively.
obtained during surgery in 45 culture specimens for 34
Targeted antibiotics were defined as antibiotic therapy based
patients. The most common isolates were streptococci (46),
on culture and sensitivity data (when available). An outcome
Actinomyces species (12) and prevotella species (11) were
was classified as follows: “Full recovery” was defined as
the most common anaerobes. A summary of microorganisms
resolution of all signs and symptoms of active infection with
is shown in table 4. Two surgical cultures were reported as
no residual disability. “Limited recovery” was defined as
normal flora (not included in table 4). The overwhelming
resolution of all signs and symptoms of infection, but
majority (94.1%) of patients had polymicrobial cultures.
persistence of clinically significant residual disability, such
Thirty eight cultures (84.4%) contained aerobic gram
as pain that limited activity or required analgesic therapy.
positive bacteria while aerobic gram negative bacteria were
Patients with limited recovery were compared with patients
obtained in nineteen cultures (42.2%). Twenty four cultures
who fully recovered. A relapse was defined as recurrence of
(53.3%) included anaerobic gram positive bacteria while
symptoms of infections after apparent resolution.
anaerobic gram negative bacteria was seen in twelve cultures
Descriptive analysis was used to present a set of data. Chi (26.7%). Candida species were seen in fifteen cultures
square, Fisher’s exact test and t-test were used for analysis (33.3%).

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Osteomyelitis Of The Jaw: A Retrospective Analysis

Therapy. (a) Surgical Procedures. Every patient had a least range of this subject matter in recent years. We anticipate
one surgical procedure. A total of 114 surgical procedures in that this study will enhance knowledge in this clinical entity
97 surgeries were performed with a mean and SD of 2.3 ± and assist clinicians in the management of osteomyelitis of
1.7 surgeries per patient. One patient with 29 years of the jaw.
symptoms had 11 surgeries during the time of our study. If
Much earlier studies in two centers in Nigeria revealed that
she was omitted, the mean and SD would be 2.1 ± 1.0
patients presented late in the natural history and the mean
surgeries. Almost half of the patients had debridement
age of patients was usually in the second to forth decade.
without continuity defect. See table 5 for types of surgery.
The major predisposing factor was advanced periodontal
(b) Antibiotic Therapy. A total of 67 courses of
disease or odontogenic infection [Daramola et al 1982,
antibiotics were ordered and received. The largest group of Adekeye et al 1985]. More recent studies in the United
patients (34.3%) received ≥ 4 weeks of IV targeted States had predominantly Caucasian patients with mean ages
antibiotics ± simultaneous or subsequent oral targeted of patients in the fifth and sixth decade like this study and
antibiotics. See table 6 for the classification and distribution recognized the emerging role of osteoradionecrosis [Calhoun
of antibiotic therapy. Peri-operative antibiotics are excluded et al 1988, Lobati et al 2001, Koorbusch et al 1992]. These
from this table. (c) Hyperbaric Oxygen. Twenty five patients previous studies were prior to the widespread use of
had hyperbaric oxygen therapy (HBOT). None of the bisphosphonates in the management of malignancies.
patients that received HBOT fully recovered. Sixteen
The three major risk factors in this study were tooth
patients (88.9%) with a history of orofacial malignancy and
extraction, radiotherapy for orofacial malignancy and use of
radiotherapy received HBOT.
bisphosphonates for the management of malignancies. These
Outcomes. The mean length of follow up was 13.1 ± 11.3 risk factors were not mutually exclusive. This is in sharp
months. Six patients had follow up for less than 3 months. contrast to the study by Calhoun et al which the top three
There were no deaths in this study. Five patients (11.9%) risk factors were post-radiation therapy (46.7%),
experienced full recovery while 37 patients (88.1%) posttraumatic (25%) and odontogenic infection (21.7%)
achieved limited recovery. There was no significant [Calhoun et al 1988]. Another study by Koorbusch et al
difference in outcomes when patients that received ≥ 4 showed odontogenic infections (36.1%), traumatic (fracture
weeks of antibiotics were compared with patients that related) (36.1%) and radiation and neoplasm (16.7%) as the
received less than 4 weeks (P = 0.57). The only risk factor most common risk factors [Koorbusch et al 1992]. Finally, a
associated with osteomyelitis of the jaw that approached Korean study in the late 1990s revealed that teeth-related
statistical significance for an adverse outcome (limited (38.5%), postextraction complications (33.3%) and
recovery) was orofacial malignancy and radiotherapy (P = periodontal disease (12.8%) were the most risk factors [Kim
0.06). None of these patients (n = 18) achieved a full et al 2001]. We can therefore conclude that osteonecrosis of
recovery. Outcome was not influenced by duration of the jaw which results from the use of bisphosphonates for
symptoms (P = 0.78), number of surgeries (P = 0.33) or type the management of malignancies has emerged as a
of microorganism obtained during surgery. A good outcome significant risk factor associated with the development of
was associated with the female sex (P = 0.04). Full recovery osteomyelitis of the jaw. Furthermore, we also conclude that
was more likely in a younger patient (mean age 40.8 ± 22.1 osteoradionecrosis that results from radiotherapy for
years) than an older patient (mean age 60.7 ± 15.7 years; P = orofacial malignancy continues to play a significant role as a
0.015). A total of 7 relapses and 8 complications (5 of which predisposing factor in the development of osteomyelitis of
were fistulae) were recorded. None of the patients with good the jaw in the United States.
outcomes had a relapse or complication.
Bisphosphonates inhibit osteoclast activity which negatively
DISCUSSION impact bone resorption and bone remodeling.
In this retrospective study, we sought to undertake a Bisphosphonates also have antiangiogenic properties which
comprehensive review of osteomyelitis of the jaw as seen in can delay wound healing [Ruggiero et al 2004, Migliorati et
Thomas Jefferson University Hospital, Philadelphia, al 2006]. Bisphosphonate-associated osteonecrosis can
Pennsylvania in a six-year period. This study is timely develop spontaneously [Migliorati et al 2006]. Irradiation
because there has been a dearth of studies exploring the full affects osteoblasts and consequently, decreases collagen
formation. Irradiation also affects osteoclast activity initially

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Osteomyelitis Of The Jaw: A Retrospective Analysis

and causes vascular injury ultimately leading to sclerosis of bone but not both, or if osteomyelitic changes did not
bone marrow connective tissues [Ruggiero et al 2004, Teng advance to the inferior margin of bone. If pathologic fracture
et al 2005]. With the compromised bone micro-environment occurred or if clear clinical and radiographic evidence was
described above in osteonecrosis and osteoradionecrosis and seen of bicortical osteomyelitis than a resection with
the continued oral contamination, it is not surprising that continuity defect was often used. Efforts were always made
even small insults such as dental extraction or ill-fitting to maintain a continuity of native bone and this is why the
dentures can result in such a protracted illness [Mortensen et vast majority of cases proved to have debridement without
al 2005, Teng et al 2005, Melo et al 2005]. However, a new continuity defect.
hypothesis proposes that osteoradionecrosis arises from a
Selecting antibiotics is based mostly on isolating bacteria
fibroatrophic process and new considerations for treatment
from these cultures [Hudson 1993, Marx 1991]. Empiric
include antioxidants and antifibrotic drugs [Teng et al 2005].
antibiotics are started pending cultures providing adequate
The most common symptoms and signs in the study were coverage for Streptococci and anaerobic bacteria such as
pain, exposed bone or reconstruction plate, cheek swelling Actinomyces and Prevotella. Penicillins remain the drug of
and discharge/drainage. Fever was seen in a minority of choice [Hudson 1992]. Other alternatives which may be used
patients. We noted that five of the seven patients with as a combination regimen include clindamycin,
maxillary lesions were on bisphosphonates. This was noted fluoroquinolones, metronidazole, a variety of
in previous studies [Mortensen et al 2007, Migliorati et al cephalosporins, carbapenems, vancomycin in combination
2005, Dimitrakopoulos et al 2006]. The clinical presentation with other antibiotics and tetracyclines. Methicillin resistant
and site of osteomyelitis is essentially similar to other Staphylococcus aureus (MRSA) is noted in only three
studies [Calhoun et al 1988, Koorbusch et al 1992, Kim et al cultures and does not appear to play a dominant role in this
2001]. condition. Candida species were largely ignored in the
selection of antimicrobials.
The polymicrobial nature of surgical specimens obtained
from osteomyelitis of the jaw has been recognized, largely HBOT is known to enhance collagen synthesis and
mimicking mouth flora. The spectrum of organisms in this angiogenesis leading to improved wound healing in
study is as seen in earlier studies [Aitasalo et al 1998, osteoradionecrosis. Therefore, at least theoretically, HBOT
Ruggiero et al 2004, Calhoun et al 1988, Koorbusch et al was felt to play an adjunctive role in the management of
1992, Kim et al 2001] These cultures are deep bone cultures osteoradionecrosis [Aitasalo et al 1998, Kushner et al 2004,
obtained in the operating room. The most common bacteria Teng et al 2005]. However, Annane et al in a prospective,
encountered are the Streptococci, Actinomyces and multicenter, randomized, double-blind, placebo-controlled
Prevotella species. Candida species are also seen. It is trial showed potentially worse outcomes in the HBO arm
important to note that while candida, corynbacteria, and the study was stopped early [Annane et al 2004].
enterococci and anaerobic streptococci are common in the Patients with overt mandibular osteoradionecrosis did not
mouth, they may not be pathogens in the bone. Calhoun et al benefit from hyperbaric oxygenation [Annane et al 2004].
had noted that the presence of Candida in cultures did not This was confirmed in this study. None of the 25 patients
affect outcome [Calhoun et al]. We found that patient who had HBOT had a full recovery.
outcome and type of microorganisms recovered during
Female patients were more likely to have a good outcome.
surgery were not statistically related.
The reason for this is unclear. Full recovery was also more
Surgical treatment options are decided based upon the likely in a younger patient as seen in an earlier study [Lobati
radiographic and clinical features of disease. At times a et al 2001]. The relationship between a limited recovery and
curative measure can be simply extraction of a tooth with the risk factor of orofacial malignancy and radiotherapy
local curettage while at other times a resection of the approached statistical significance. In this study, no patient
affected area may be needed. For purposes of clarification all with a risk factor of orofacial malignancy and radiotherapy
marginal debridements are classified as, “debridement achieved a full recovery. Calhoun et al showed cure was
without continuity defect.” This was by far the most widely more likely in the non-radiation group, although this
used surgical treatment both in this study and in the difference disappeared when followed up for more than six
literature. This surgical technique was used when months [Calhoun et al 1988]. There was no statistically
osteomyelitic changes extended through only one cortex of significant relationship between the use of bisphosphonates

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Osteomyelitis Of The Jaw: A Retrospective Analysis

and patient outcome in our study. The other risk factors {image:2}
associated with osteomyelitis of the jaw did not predict
{image:3}
patient outcome. The role of surgery in the management of
osteomyelitis is largely established. The confusion lies in {image:4}
determining the length of antibiotic therapy. Most clinicians
use antibiotics empirically for 4-6 weeks. Arguments for {image:5}
longer or shorter courses remain unresolved [Lew et al 2004,
{image:6}
Lew et al 1997, Calhoun et al 1988, Mader et al 1999,
McHenry et al 2002, Lazzarini et al 2005]. Patient outcome ACKNOWLEDGEMENTS
was not affected by length of appropriate antibiotic therapy.
We wish to acknowledge former Jefferson Medical College
Our study did not show any benefit with the use of HBOT.
students, John Ragsdale MD and Alan Riley MD for their
Other studies showed similar results [Calhoun et al 1988,
help with data collection.
Teng et al 2005, Annane et al 2004].
References
One male patient was the only patient with more than one
1. Adekeye EO, Cornah J (1983). Osteomyelitis of the jaws:
episode. He had 4 episodes during this study. He had a A review of 141 cases. Br J Oral Maxillofac Surg
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3. Annane D, Depondt J, Aubert P, et al (2004). Hyperbaric
also predisposes to osteomyelitis [Tolar et al 2004]. Another oxygen therapy for radio necrosis of the jaw: A randomized,
patient had symptoms dating back to a subperiosteal implant placebo-controlled, double-blind trial from the ORN96 study
group. J Clint Oncol 22(24):4893-900.
29 years prior to presentation. The hardware ultimately was 4. Bernier S, Clermont S, Maranda G, Turcotte JY (1995).
explanted. Osteomyelitis of the jaws. J Can Dent Assoc 61(5):441-2,
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Author Information
Chukwudum Uche, MD
Fellow, Division of Infectious Diseases, Thomas Jefferson University Hospital

Robert Mogyoros, DMD

Chief Resident, Department of Oral and Maxillofacial Surgery, Thomas Jefferson University Hospital

Amy Chang, MD
Resident, Department of Medicine, Thomas Jefferson University Hospital

Daniel Taub, MD DDS

Assistant Director and Instructor, Department of Oral and Maxillofacial Surgery, Thomas Jefferson University Hospital

Joseph DeSimone, MD
Clincal Associate Professor and Fellowship Program Director, Division of Infectious Diseases, Thomas Jefferson University
Hospital

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