Asian J Oral Maxillofac Surg. 2008;20:189-192.

CASE REPORT

Chronic Refractory Osteomyelitis of the Mandible and

Maxilla Related to Dental Implant Placement
Young-Kyun Kim,1 Ghee-Young Choe,2 Dal-Ho Lee,3 Pil-Young Yun1
Department of Oral and Maxillofacial Surgery, Section of Dentistry and 2Department of Pathology, Seoul National University
Bundang Hospital, Bundang, and 3Bangbae Boston Dental Private Office, Seoul, Korea

Abstract
A 68-year-old diabetic woman with chronic refractory osteomyelitis involving the mandible and
maxilla following dental implant placement is presented. The inflammatory lesion showed actinomycotic findings histopathologically and refractory responses to several surgical and medical treatments
for over 2 years. A periapical lesion on an adjacent tooth was overlooked as a possible source of
infection. The lesion was cured after complete surgical debridement in combination with long-term
antibiotic therapy.
Key words: Actinomycosis, Dental implants, Diabetes mellitus, Osteomyelitis

Introduction
Dental implant surgery is a reliable and safe procedure,1
but there are potential complications associated with it.
Postoperative infection, although uncommon, is one of the
most troublesome complications. Usually, infection in the
early phase may be well controlled by surgical and medical
intervention. However, if not adequately diagnosed and
treated, long-term and complicated therapy becomes necessary irrespective of the removal of the engaged implant.
Peri-implantitis is an inflammatory process on tissues
around already osseointegrated implants.2 Microbiological
studies have shown similar findings for peri-implantitis and
advanced stages of periodontitis.3 Plaque-associated lesions
that occupy a larger portion of the peri-implant cause extensive spread of infection to deeper tissues.4 Osteomyelitis
is defined as an inflammatory condition of the bone that
originates as an infection of the medullary space and has
extended to the cortical bone and periosteum. In the absence
of adequate treatment, the lesion may become refractory.
Few cases of osteomyelitis associated with implant therapy
have been reported; some of these reveal an aggressive destructive process. Esposito et al, who examined early oral
implant failures histopathologically, found that the clinical
conditions varied from osteomyelitis to a symptom-free state.5
We report a woman with chronic refractory osteomyelitis
following implant surgery in the molar area of the left mandible
Correspondence: Pil-Young Yun, DDS, MSD, PhD, Department of Oral
and Maxillofacial Surgery, Section of Dentistry, Seoul National University
Bundang Hospital 300, Gumi-dong, Bundang-gu, Seongnam-si, Gyeonggi-do
463-707, Korea.
Tel: (82 31) 787 2780 or 787 7545; Fax: (82 31) 787 4055;
E-mail: pilyoung@snubh.org

2008 Asian Association of Oral and Maxillofacial Surgeons.

and maxilla that remained uncontrolled for over 2 years in spite

of repeated surgical intervention and antibiotic therapy.

Case Report
A 68-year-old woman visited the Seoul National University
Bundang Hospital, Bundang, Korea, with pain and denudation of an implant site in the lower left second molar area
in August 2004. The patient had been undergoing dental
implantation in the left mandibular and maxillary areas at a
private dental clinic since April 2003. Gingival swelling and
pus discharge were detected at the implant site in the lower
left second molar area in April 2004. A clinical diagnosis
of peri-implantitis was made at the dental clinic, where the
patient underwent curettage and was given a 1-week postoperative course of antibiotics, which did not have any effect.
The patient was subsequently referred to the Department of
Oral and Maxillofacial Surgery in our hospital.
Careful history taking revealed diabetes mellitus and
osteoporosis. Laboratory investigations indicated that her
fasting blood glucose was >145 mg/dL and her postprandial
blood glucose at 2 hours was around 210 mg/dL. The glycosylated haemoglobin level (Hb A1c) was above 7.4 mg/%.
Clinical examination showed gingival swelling, with denudation of the implant site in the upper right canine to the
second premolar area, and necrotic change of the surrounding bone and gingiva of the implant site at the lower left
second molar area (Figure 1). Foul odour and tenderness of
the left posterior mandibular area were noted. Radiographic
examination showed a radiolucent lesion extending to the
mandibular canal in the left posterior mandibular area (Figure
2). Bone scintigraphy using technetium-99-m-diphosphonate
189

Mandibular and Maxillary Osteomyelitis

Figure 1. Necrosis and denudation of the mandibular buccal gingiva

in the lower left second molar area surrounding the implant.

Figure 2. Panoramic radiograph shows a radiolucent lesion,

extending to the mandibular canal, around the implant at the lower
left second molar area.

Figure 3. Initial bone scintigraphy demonstrated hot uptake in the

left mandibular and anterior maxillary areas.

demonstrated abnormal isotope accumulation in the left

mandibular body and anterior maxilla (Figure 3).
Saucerisation and sequestrectomy with implant removal
from the lower left second molar area were performed under
general anaesthesia in August 2004. During the procedure,
the lesion was found to extend to the ascending ramus and
mandibular canal. Also, severe bone destruction of the lower
left second premolar distal areas was found. In the maxilla,
saucerisation, sequestrectomy, and curettage with implant
removal from the upper right second premolar area were done.
A biopsy of the extirpated necrotic bone lead to a pathological diagnosis of chronic osteomyelitis showing dead
190

Figure 4. Pathology results showed chronic osteomyelitis, with dead

bone fragments, and bacterial colonies with suppurative exudates.

bone fragments and bacterial colonies with suppurative exudates (Figure 4). Small-sized colonies of bacterial organisms
were present, but no characteristic actinomycotic sulphur
granules were noted. Nitrofrazone gauze was changed at
3-day intervals postoperatively.
As pus discharge and necrotic bone exposure were detected in the residual right maxillary implant area in September
2004, curettage with drain insertion was done. Pathologic examination of the granulation tissues removed showed severe
chronic inflammation with dead bone fragments and new
bone formation. As the wound healed favourably, an overdenture was made using the 3 remaining implants in the maxilla.
The suppurative swelling and pain recurred in December
2004. A periapical radiolucency was detected in the lower
left second premolar area spreading to the apical area of
the lower left canine. The periapical lesion in the lower
left second premolar was suspected as the original focus of
osteomyelitis. The suspected tooth was extracted and curettage executed.
The patient was referred again due to pus discharge in the
lower left molar area in September 2005. Bone scan showed
a high concentration of radioisotope in the left mandible and
right anterior maxilla. Saucerisation and sequestrectomy,
inclusive of the mandibular canal area, was repeated in
November 2005. Histopathological examination revealed
characteristic actinomycotic sulphur granules with chronic
active inflammation and dead bone fragments. The sulphur
granules consisted of a mass of filamentous branching
bacteria enmeshed in an eosinophilic matrix of uncertain
composition. Polymorphonuclear neutrophils were clinging
to the edges of the sulphur granules (Figure 5). A pathologic
diagnosis of actinomycosis was made. However, anerobic
Actinomyces israelii was not confirmed.
Although symptoms in the lower left molar area were
controlled completely in November 2005, pus discharge and
tenderness remained in the gingival sulcus surrounding the
implants in the upper right canine, upper left canine, and
Asian J Oral Maxillofac Surg. Vol 20, No 4, 2008

Kim, Choe, Lee, et al

Figure 5. Histopathological examination showed characteristic

actinomycotic sulphur granules surrounded by polymorphonuclear
neutrophils. The sulphur granules consisted of a mass of thin,
delicate branching bacilli enmeshed in an eosinophilic matrix.

Figure 6. Bone scintigraphy confirmed nearly complete resolution

of the lesions.

upper left second premolar areas. Saucerisation, curettage,

and implant surface detoxification with tetracycline solution
were done in December 2005. The wound was dressed and
antibiotics prescribed. There was no evidence of bony infection at the last follow-up in April 2006 and the patient has
remained free of symptoms. Bone scintigraphy confirmed
nearly complete resolution of the lesions (Figure 6).

Discussion
Considering the many sources of infection in the oral cavity,
including dental infection, traumatic fracture, acute necrotic
ulcerative gingivitis, or stomatitis, it is remarkable that the
incidence of osteomyelitis of the jaw is relatively low. Host
resistance is regarded as one of the most important factors in
the incidence and course of osteomyelitis. However, patients
with chronic wasting diseases, deficient immune function,
and bone metabolic diseases are prone to osteomyelitis.6,7
Previously, Staphylococcus aureus was believed to be
the main causative organism of osteomyelitis. However,
Asian J Oral Maxillofac Surg. Vol 20, No 4, 2008

A-haemolytic streptococci and oral anaerobes are currently regarded as the primary causative microorganisms of
osteomyelitis of the jaw, particularly Peptostreptococcus,
Fusobacterium, and Bacteroides, which are related to odontogenic infections.8 In addition, various other organisms, such
as Actinomyces spp. and Treponema pallidum, cause special
types of osteomyelitis.
There are several controversial opinions on the classification of osteomyelitis.9,10 Radiographic examinations
are not helpful in acute osteomyelitis. A central radiopaque
sequestrum, with irregular ragged radiolucent margins is
usually found in chronic osteomyelitis. Extended follow-up is
necessary to evaluate clinical outcome in chronic osteomyelitis
as it may remain quiescent for longer periods.11 Normal endogenous antioxidant capability is often overwhelmed when there
are periods of sustained ischemia and hypoxia followed by
reperfusion. This may be an unrecognised contributing factor
to the destructive inflammation seen during the osteomyelitic
process.12,13 Adjunctive hyperbaric oxygen therapy is recommended in the refractory forms of osteomyelitis to enhance the
regional immune response of the jaws as well as to produce
microvascular neoangiogenesis for reperfusion support.14
Several refractory forms of osteomyelitis should be
considered during differential diagnosis, and chronic refractory multifocal osteomyelitis (CRMO) should be ruled out.
The multifocality of disease involvement and the typically
negative cultures of bone distinguish CRMO from bacterial osteomyelititis.15-17 Actinomycosis is a chronic, slowprogressing, infectious disease with both granulomatous
and supprative features. The dosage and duration of antimicrobial therapy effective for most infections may result in
only temporary resolution followed by recurrence for actinomycosis. Therefore, for actinomycosis, antibiotics must
be administered intravenously for 4 to 6 weeks, followed by
oral therapy for 6 to 12 months. Yenson et al reported a case
of actinomycotic osteomyelitis of the facial bones, including
the mandible, maxilla, and right zygoma.18 The lesion had
developed after extraction of a mandibular tooth.
In this patient, concomitant secondary actinomycosis
was suspected along with chronic osteomyelitis, in the
later period of treatment, due to a tendency for repetitive
osteomyelitic recurrences. Treatment was completed after
long-term antibiotic therapy, although no typical clinical
features of actinomycosis were found during the initial
treatment period. Actinomycotic bacteria are detectable in
anaerobic cultures for 4 to 6 days.8 However, false-negative
results in bacteriological examinations are frequently caused
by incorrectly collecting or transporting specimens for the
studies.8 Bartkowski et al analysed 15 cases of actinomycotic
osteomyelitis of the mandible,19 where the diagnoses was
established on the basis of clinical examinations confirmed
by bacteriological and histopathological tests. In this patient,
actinomycosis could not be confirmed from the pus culture,
191

Mandibular and Maxillary Osteomyelitis

but was suspected based on the result of a biopsy specimen

that contained actinomycotic colonies.
There were several problems associated with the current
patient. Firstly, the periapical lesion in the adjacent tooth, which
was the source of infection, was ignored during the initial
period of treatment. The treatment was at first focused on the
management of the peri-implantitis and adjacent osteomyelitis
lesion. After several recurrences, the osteomyelitic lesion was
controlled following the extraction of the suspected tooth.
Secondly, aggressive resection of the mandible was not
performed during early operations, and all implants at the
infection site were not removed entirely. The maxillary recurrences of osteomyelitis may have been associated with these
implants. Osteomyelitis of the maxilla is less frequent than
that of the mandible due to a different pattern of blood supply
in the maxilla. However, the chronic and refractory course of
the original mandibular lesion may have contributed to the
occurrence of maxillary osteomyelitis via haematogenous
spread of the lesion from the mandible to maxilla.
Lastly, other related factors may have contributed to the
chronic refractory osteomyelitis. In this patient, there was a
history of uncontrolled diabetes mellitus, which may have
caused subsequent immunosuppression, with obstructed
microcirculation and delayed healing. Therefore, the identification and correction of immunocompromising conditions,
such as diabetes mellitus, should be attempted. Although
diabetes has in the past been considered as a contraindication
for dental implants,20,21 a patient with well-controlled diabetes has no contraindications provided that careful preoperative assessment of blood glucose levels is done and there
is motivation for oral hygiene procedures. Few definitive
guidelines have been proposed in the literature for implant
surgery, and it has been suggested that strict protocols should
be enforced for better results.22 Some researchers recommend HbA1c levels <7.0 mg/% as the baseline for implant
surgery.23,24
In conclusion, accurate and early diagnosis based on
clinical, histological and microbiological findings, and
supported by thorough surgical debridement and long-term
antibiotic therapy are essential for predictable and favourable
results in the management of suppurative lesions of the jaw.
Early identification and elimination of any predisposing or
contributory factors will help in the effective treatment and
prevention of complications.

implant surfaces. Clin Oral Implants Res. 1993;4:53-64.

4.

Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Marinello C. Experimental breakdown of peri-implant and periodontal tissues. A study in
the beagle dog. Clin Oral Implants Res. 1992;3:9-16.

5.

Esposito M, Thomsen P, Ericson LE, Lekholm U. Histopathologic observations on early oral implant failures. Int J Oral Maxillofac Implants.
1999;14:798-810.

6.

Adekeye EO, Cornah J. Osteomyelitis of the jaws: a review of 141

cases. Br J Oral Maxillofac Surg. 1985;23:24-35.

7.

Bar T, Mishal J, Lewkowicz A, Nahlieli O. Osteomyelitis of the mandible due to Mycobacterium abscessus: a case report. J Oral Maxillofac
Surg. 2005;63:841-4.

8.

Peterson LJ. Microbiology of head and neck infections. Oral

9.

Daramola JO, Ajagbe HA. Chronic osteomyelitis of the mandible in

Maxillofac Clin North Am. 1991;3:247-57.

adults: a clinical study of 34 cases. Br J Oral Surg. 1982;20:58-62.
10. Marx RE. Chronic osteomyelitis of the jaws. Oral Maxillofac Clin
North Am. 1991;3:367-81.
11. van Merkesteyn JP, Groot RH, van den Akker HP, Bakker DJ,
Borgmeijer-Hoelen AM. Treatment of chronic suppurative osteomyelitis of the mandible. Int J Oral Maxillofac Surg. 1997;26:450-4.
12. Parks DA, Bulkley GB, Granger DN. Role of oxygen free radicals in
shock, ischemia, and organ preservation. Surgery. 1983;94:428-32.
13. Manson PN, Anthenelli RM, Im MJ, Bulkley GB, Hoopes JE. The role
of oxygen-free radicals in ischemic tissue injury in island skin flaps.
Ann Surg. 1983;198:87-90.
14. Hudson JW. Osteomyelitis of the jaws: a 50-year perspective. J Oral
Maxillofac Surg. 1993;51:1294-301.
15. Gamble JG, Rinsky LA. Chronic recurrent multifocal osteomyelitis: a
distinct clinical entity. J Pediatr Orthop. 1986;6:579-84.
16. Manson D, Wilmot DM, King S, Laxer RM. Physeal involvement in
chronic recurrent multifocal osteomyelitis. Pediatr Radiol. 1989;20:76-9.
17. Flygare L, Norderyd J, Kubista J, Ohlsson J, Vallo-Christiansen J,
Magnusson B. Chronic recurrent multifocal osteomyelitis involving
both jaws: report of a case including magnetic resonance correlation.
Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1997;83:300-5.
18. Yenson A, deFries HO, Deeb ZE. Actinomycotic osteomyelitis of the
facial bones and mandible. Otolaryngol Head Neck Surg. 1983;91:173-6.
19. Bartkowski SB, Zapala J, Heczko P, Szuta M. Actinomycotic osteomyelitis of the mandible: review of 15 cases. J Craniomaxillofac Surg.
1998;26:63-7.
20. Smith RA, Berger R, Dodson TB. Risk factors associated with dental
implants in healthy and medically compromised patients. Int J Oral
Maxillofac Implants. 1992;7:367-72.
21. Balshi TJ, Wolfinger GJ. Dental implants in the diabetic patient: a

References
1.

Weyant RJ, Burt BA. An assessment of survival rates and within-patient

2.

Quirynen M, Teughels W. Microbiologically compromised patients and

3.

Gatewood RR, Cobb CM, Killoy WJ. Microbial colonization on natural

clustering of failures for endosseous oral implants. J Dent Res. 1993;72:2-8.

impact on oral implants. Periodontol 2000. 2003;33:119-28.
tooth structure compared with smooth and plasma-sprayed dental

192

retrospective study. Implant Dent. 1999;8:355-9.

22. Abdulwassie H, Dhanrajani PJ. Diabetes mellitus and dental implants:
a clinical study. Implant Dent. 2002;11:83-6.
23. Blanchaert RH. Implants in the medically challenged patient. Dent Clin
North Am. 1998;42:35-45.
24. Beikler T, Flemmig TF. Implants in the medically compromised patient.
Crit Rev Oral Biol Med. 2003;14:305-16.

Asian J Oral Maxillofac Surg. Vol 20, No 4, 2008