Chronic osteomyelitis of mandible caused by penicillin-resistant Bacteroides ruminicola Report of a case Bradley G. Seto, D.D.S.* Steven R. Lynch, D.D.S..** Los Angeles and Vacaville, C.alif SCHOOL
OF DENTISTRY,
UNIVERSITY
OF CALIFORNIA,
and Peter K. May. D.M.D.,***
LOS ANGELES
Osteomyelitis of the jaws caused by a Bacteroides species is uncommon. A case of osteomyelitis of the mandible caused by penicillin-resistant Bacteroides ruminicola is reported. The diagnosis was confirmed by isolation of the organism and bone scan eSmTc medronate disodium) of the mandible. Clindamycin and hyperbaric oxygen therapy resolved the infection. (ORAL SURC. ORAL MED. ORAL PATHOL. 61:29-31, 1986)
B acteroides
species are normal inhabitants of the oral cavity.le4Although Bacteroides melaninogenicus is probably the commonest variety, other species belonging to the normal oral flora of healthy individuals include Bacteroides oralis, Bacteroides ovatus, Bacteroides multiascides, Bacteroides hypermegis, and Bacteroides ruminicola.5
Recent reports have emphasized the participation of bacteroides in orofacial infections,6-9 including some penicillin-resistant strains reported in patients previously treated with penicillin.10-‘2 Bacteroides have been associated with mandibular osteomyelitisL3.14but are not usually considered the primary pathogen.15A caseof chronic mandibular osteomyelitis due to penicillin-resistant B. ruminicola follows. CASE REPORT
On May 17, 1980, a 47-year-old Mexican-American man came to the UCLA Hospital Dental Clinic complaining of pain in the left mandible. The pain had been present since the extraction of the mandibular left second molar 6 months earlier. Two weeks before the initial visit to our clinic, a submandibular swelling and gingival purulence appeared in association with the mandibular left first molar. The tooth was extracted; this was followed by incision and drainage of the submandibular swelling. Penicillin V was prescribed postoperatively. Alpha hemo*Hospital Dental Service. **In private practice, Vacaville, Calif ***Oral and Maxillofacial Surgery.
lytic streptococci and Staphylococcus epidermidis were isolated. Persistence of the pain and purulence caused the patient to seek further care. The past medical history was positive for adult-onset diabetes (controlled by diet) and rheumatoid arthritis (treated with prednisone, oxyphenbutazone, and ibuprofen). The remainder of the medical history was noncontributory. The clinical examination revealed an indurated left submandibular swelling with an associatedextraoral fistula. Purulent drainage was also noted in the extraction site of the lower left first molar. A panoramic radiograph demonstrated no significant pathologic condition. The purulent discharge from the extraoral tract was obtained for culture and sensitivity testing. There were no signs of systemic infection. The patient was placed on penicillin V and followed up as an outpatient. During the next 2 weeks the patient’s condition improved only slightly. The extraoral swelling decreased but purulent drainage continued intraorally. An incision and drainage were performed and the antibiotic regimen was changed to cephalexin. The lower left secondpremolar was found to be nonvital despite being unrestored. Root canal therapy was performed, and this was followed by apicoectomy because of the unresolved periapical abscess.All symptoms had subsided 2
monthsafter the patient first cameto the clinic. On November 6, 1980, the patient returned, complaining of a severe,dull, aching pain in the right mandibular parasymphyseal region. There was no swelling, erythema, trismus, or percussion sensitivity. All mandibular anterior teeth exhibited severe attrition. A panoramic radiograph revealedmultiple lytic areasof the anterior mandible.The lower right lateral incisor was found to be nonvital. Endodontic therapy was initiated and the patient received 29
30 Seto, Lynch, and May another regimen of penicillin V. The patient experienced continued swelling and drainage from the apex of lower right lateral incisor; therefore an apicoectomy was performed. Histopathologic analysis revealed a periapical granuloma, the cultures of which were negative. All symptoms resolved in 1 week. On December 22, 1980, the patient came to the clinic with pain and swelling involving the right submandibular space and right mandibnlar buccal vestibule. Vitality tests showed that the lower right first molar was nonvital. Endodontic therapy was initiated, and the patient was placed on penicillin V. All symptoms resolved within 3 weeks. Because of the developing history of multiple mandibular infections without obvious cause, the patient was referred to a physician to rule out systemic causes.The results of the physical examination and laboratory analyses were negative. However, the prednisone dosage was reduced. On March 10, 1981, the patient developed another swelling of the right submandibular space. Deep, intraosseous pain was accompanied by intermittent paresthesias of the right lower lip. Intraorally, the lower right first molar exhibited gingival purulence that was associated with a 12 mm pocket buccally at the furcation. A panoramic radiograph showed multiple changes of the trabecular pattern in the anterior and right mandibular body. The lower right first molar was extracted at this time. The extraoral swelling was incised and cultured under sterile conditions. Penicillin V was prescribed. A bone scan (99mT~ medronate disodium) of the mandible was obtained, and this confirmed the diagnosis of osteomyelitis. Anaerobic cultures grew a pure isolate of B. ruminicola resistant to penicillin and sensitive to clindamycin. The antibiotic was changed to clindamycin, 300 mg four times a day for 4 weeks, and was combined with 50 hours of hyperbaric oxygen treatments. After the substitution of clindamycin for penicillin the patient’s condition rapidly improved. The submandibular swelling decreased, with a slight discharge from the incision site continuing for 2 more days. One week later all clinical signs of infection were absent. In June 1981 a second bone scan confirmed the resolution of the osteomyelitis. No new symptoms have appeared and a follow-up panoramic radiograph 18 months later showed that the osseouslesions had healed. DISCUSSION
Mandibular osteomyelitis caused by B. ruminicola resistant to penicillin is exceedingly rare. The uncommon association of bacteroides with osteomyelitis of the jaws may be because of the difficulty in isolation.‘6 The diabetes and steroid therapy may have contributed to the persistence of the infection despite endodontics, extractions, and antibiotics.v Pain, radiographic changes, and acute exacerbations with associated swelling of soft tissue were consistent with osteomyelitis.16However, the expected sequestration of nonvital bone was absent. Since
Oral Surg. January, 1986
no other cause of the pulpal necrosis was found, it
follows that the infection within the body of the mandible caused devitalization of teeth. It is difficult to link radiographic changes to osteomyelitis unless
more significant symptoms, such as paresthesia, are present. The bone scan was invaluable in the confirmation of osteomyelitis.
Penicillin generally is the drug of choice in most orofacial infections.7*v. I’, ‘s However, there is an increasing amount of information indicating that a
high percentage of bacteroides organisms are resistant to penicillin.6~s~“~‘2~1v It has been well documented that resistance to penicillin can result from repeated penicillin courses.‘S’2 Thus, alternative antibiotics should be employed when infections are persistent despite proper penicillin
use. This unusual
case also reinforces the importance of culture and sensitivity testing. Clindamycin is a drug of choice for penicillinresistant bacteroides infections, along with cefoxitin and metronidazole. Clindamycin is a semisynthetic modification of lincomycin, with the same spectrum but four times the potency. It is considered bacteriostatic but becomes bacteriocidal in high doses.2o Adequate serum levels are attainable by means of oral administration, with peak concentrations being reached in 90 minutes.2’ The ability to penetrate various tissues, including
bone, makes it well suited
for use in osteomyelitis. The usual oral dosageof clindamycin is 150 to 300 mg every 6 hours. For severe infections the dosage can be increased to 450 mg every 6 hours.20Clindamycin is generally safe to dispense on an outpatient basis; frequent blood studies and intravenous admin-
istration are not required. The major adverse effects associated with the use of clindamycin involve the gastrointestinal tract. Among these, diarrhea and antibiotic-associated colitis have generated the greatest concern. The incidence of diarrhea is higher in females, in patients more than 20 years of age, and with oral administration.22 Clindamycin-associated colitis can produce
pronounced and persistent diarrhea, severe abdominal cramps, fever, and the appearance of blood and mucus in the stools. There is evidence that the colitis
is attributable to an overgrowth of Cfostridium di$kile.20 The incidence of clindamycin-associated colitis is 1 in 10,000.23 If colitis is suspected, the
clindamycin should be discontinued. Vancomycin and other supportive therapy may be required in severe cases.2o Combining hyperbaric oxygen therapy with antibiotics for patients with osteomyelitis can markedly improve resolution of the infection and healing over
Volume 61 Number 1
antibiotics alone. Hyperbaric oxygen increasescapillary proliferation (improving blood supply) and promotes collagen synthesis (repair).24 It can also enhance oxygen-dependent leukocyte function and osteoclast activity,25 which in turn increases phagocytosis and the removal of osseousdebris. CONCLUSION
A case of mandibular osteomyelitis caused by penicillin-resistant B. ruminicola is presented. Adult-onset diabetes and chronic steroid treatment may have contributed to the pathogenicity of the infection. Previous penicillin therapy probably selected for the resistant bacteria. Migrating soft tissue infections, tooth devitalization, and radiographic changes made it extremely difficult to make a diagnosis, until paresthesia began and a pure isolate of B. ruminicola was obtained. A bone scan (99mT~medronate disodium) confirmed the final diagnosis. The infection was rapidly resolved with a combination of clindamycin and hyperbaric oxygen therapy. We wish to thank Terry Jones of the UCLA School of
Dentistry Word Processing Center for preparation of this article and Dr. John Yagiela for his editorial comments. REFERENCES 1. Gibbons RJ, Socransky SS, De Araujo WC, Van Houte J: Studies of the predominant cultivable microbiota of dental plaque. Arch Oral Biol 9: 365370, 1964. 2. Gordon DF, Gibbons RJ: Studies of the predominant cultivable micro-organisms from the human tongue. Arch Oral Biol 11: 627-632,1966. Socransky SS: Relationship of bacteria to the etiology of oeriodontal disease. J Dent Res 49: 203-222, 1970. Socransky SS, Manganiello SD: The oral microbiota of man from birth to senility. J Periodontol 42: 485-496, 1971. Bisset KA, Davies GH: The microbial flora of the mouth. London, 1960, Heywood and Company. Bahn SL, Ciola B, Segal AC: Penicillin-resistant Bacteroides melaninogenicus infection of the mandible. J Oral Surg 39: 221-223, 1981. 7. Heimdahl A, Nord CE, Weilander K: Effects of phenoxymethylpenicillin, bacampicillin, and clindamycin in the oral, throat and colon microflora of man. Swed Dent J 4: 39-52, 1980. 8. Kannangara DW, Thadepalli H, McQuirter JL: Bacteriology and treatment of dental infections. Oral Surg 50: 103-109, 1980.
Chronic osteomyelitis
of mandible
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9. Chow AW, Roser SM, Brady FA: Orofacial odontogenic infections. Ann Intern Med 88: 392-402, 1978. 10. Heimdahl A, von Konow L, Nord CE: Beta-lactamase producing Bacteroides species in the oral cavity in relation to I penicillin therapy. J Antimicrob Chemother 8: 225-229, 1981. 11. Murray PR, Rosenblatt JE: Penicillin resistance and penicillinase production in clinical isolates of Bacteroides melaninogenicus. Antimicrob Agents Chemother 11: 605-608, 1977. bacteria in the 12. Naiman RA, Barrow JG: Penicillin-resistant mouths and throats of children receiving continuous prophylaxis for rheumatic fever. Ann Intern Med 58: 768-772, 1963. 13. Leake DL: Bacteroides osteomyelitis of the mandible: A report of two cases. ,Oral Surg 34: 585-588, 1972. 14. Monaldo LJ, Bellome J, Zegarelli DJ, Ragaini UE: Bacteroides infection of the mandible with secondary spread to the neck. J Oral Surg 32: 370-372, 1974. 15. Kholsa VM: Current concepts in the treatment of acute and chronic osteomyelitis: Review and report of four cases. J Oral Surg 28: 209-214, 1970. 16. Daramola JO, Ajagbe HA: Chronic osteomyelitis of the mandible in adults: A clinical study of 34 cases. Br J Oral Surg 20: 58-62, 1982. 17. Quayle AA: Bacteroides infections in oral surgery. J Oral Surg 32: 91-99, 1974. I8 Finegold SM, Bartlett JG, Chow AW, Flora DJ, Gorbach SL, Harder EJ, Tally FP: Management of anaerobic infections. Ann intern Med 83: 375-389, 1975 19. Heimdahl A, von Konow L, Nord CE: Isolation of betalactamase producing Bacteroides strains associated with clinical failures with penicillin treatment of human orofacial infections. Arch Oral Biol 25: 689-692, 1980. 20. Physician’s desk reference, ed 36, Oradell, N.J., 1982, Medical Economics Company, Inc., pp. 1930-32. 21. Bystedt H, Dahlblck A, Dornbusch K, Nord CE: Concentrations of azidocillin, erythromycin, doxycycline, and clindamytin in human mandibular bone. Int J Oral Surg 7: 442-449, 1978. 22. Swartzberg JE, Maresca RM, Remington JS: Clinical study of gastrointestinal complications associated with clindamycin therapy. J Infect Dis 135(Suppl):99-103, 1977. CH: Incidence of clindamycin-associated 23. Ramirez-Ronda colitis. Comments and corrections. Ann Intern Med 81: 860, 1974. 24. Marx RE, Ames JR: The use of hyperbaric oxygen therapy in bony reconstruction of the irradiated and tissue deficient patient. J Oral Maxillofac Surg 40: 412-420, 1982. 25. Strauss MB: Chronic refractory osteomyelitis: Review and role of hyperbaric oxygen. HBO review, Vol. I. No. 4, 1980, New York, Plenum Publishing Corp. Reprint requests to: Bradley G. Seto, D.D.S., Hospital Dental Service, School of Dentistry, Room 13, 089CHS. University of California, Los Angeles, Los Angeles, CA 90024.