Actinomyces odontolyticus infections: review of six patients

Journal of Infection (1985) 1I, 125-129

Actinornyces odontolyticus

infections: review o f six patients

Y. P e l o u x , * D. R a o u l t , t H. C h a r d o n $ a n d J. P. E s c a r g u e l ~

* Bacteriology Laboratory, I-I6pital de la Conception, 13005 Marseille, France. "~Unit of Infectious Diseases, H3pital Houphouet-Boigny, 13015 Marseille, France. $ Bacteriology Laboratory, H~pital d'Aix en Provence, I3616 France. ~ Bacteriology Laboratory, H~pital d'Hy~res, 83000 France. Accepted for publication 15 November 1984 Introduction

Actinomyces may be found in the normal human buccal flora) Actinomyces odontolyticus was first described in I958 by Battyfl who isolated it from the site of dental caries. Since then, the organism has been isolated from patients with various infections 3-9 and reported without details in nine other cases. 1°, 11 We have previously reported three cases. 12,13 Since then we have observed three others. T h e purpose of this paper is to review our six cases together. T h e y comprise patients with the following: septicaemia, an abscess of a finger, pelvic peritonitis associated with an intra-uterine device (I.U.D.), an abscess of the arm and a submaxillary abscess. None of these was typical ofactinomycotic infection. Actinomyces odontolyticus was found in several samples from each of the patients except one who had been previously treated with antibiotics.

Case reports Case x This previously reported case 13 is one of a man, aged I9 years, without a history of previous illness. He was admitted to hospital on I7 August I981 with fever, confusion and jaundice. His temperature was 40 °C, blood pressure I5O/7O m m H g and pulse rate I3o/min. Angina had been diagnosed 3 days before admission. T h e red blood cell count (RBC) was 4"6 x lO6/1, haemoglobin I2 g/dl, platelets: zo × IO6/1, white blood cell count (WBC) : 5"4 x Io6/l. From I5 blood cultures, performed over a period of 3 days, two organisms were isolated: A. odontolyticus and Fusobacterium necrophorum. T h e course of the illness was gradually favourable during 6 weeks of treatment with penicillin sodium (30 g / d a y (IV)) and ornidazole (3 g/day IV). Bilateral serofibrinous pleural exudate was observed on day I5 of the illness and was aspirated. T h e state of his mouth and teeth was satisfactory. No immunosuppressive cause was found and the patient has remained in good health.

Case 2 A 4o-year-old man, a heavy smoker, was admitted to hospital on 9 October 1981 for an abscess of the right thumb which had appeared after puncture by o163-4453/85/o5o125 + 05 $02.oo/0

© 1985 The British Society for the Study of Infection

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Y. P E L O U X E T A L .

a fish bone. Physical examination was normal (temperature 37 °C, pulse rate 8o/min, blood pressure 12o/8o m m H g ) . This patient's m o u t h and teeth appeared very unhealthy. T h e blood count was: R B C 5 x io9/1, haemoglobin 15 g/d1, platelets 3 4 o x loS/l, W B C i o x io6/1 (70% polymorphonuclear: P M N ) . T h e abscess was opened. A sample of the pus contained both Klebsiella pneurnoniae and A. odontolyticus. T r e a t m e n t with cephalothin was given for 7 days with success. Case 3

A 54-year-old woman, an alcoholic, was admitted to hospital on 16 March 1982 for pelvic pain and fever of 38 °C that she had had for IO days. She was nulliparous and post-menopausal (since 1978 ). Physical examination revealed a painful suprapubic swelling. An X-ray of the chest was normal. T h e blood count was: R B C 4"5 x lO9/1, haemoglobin 12 g/dl, platelets 500 x lO8/1, W B C 20 x lO6/1 ( P M N 84%). T h r e e blood cultures and urine cultures remained sterile. Exploratory surgery revealed two infected ovarian cysts as well as pelvic peritonitis requiring hysterectomy. A sample of the peritoneal fluid yielded E. coli and A. odontolyticus. T h e outcome of the illness was favourable after 15 days of treatment with ampicillin (6 g/day IV), tobramycin (15o m g / d a y IV) and metronidazole (2 g/day IV). Case 4

A 3o-year-old woman was seen with infection associated with an I.U.D. Her temperature was normal. T h e device was taken out on II June 1982 and cultured. Haemophilus influenzae and A. odontolyticus were isolated. N o other therapy was required for her cure. Case 5

A 47-year-old man, a schizophrenic, was admitted to hospital for an abscess of the arm on IO September I982. His temperature was 39 °C, pulse rate I i o / m i n and blood pressure 13o/7o m m H g . T h e physical examination revealed a hot, red and painful swelling of the arm. T h e blood count was: R B C 4"6 x lO9/1, haemoglobin 14.2 g/dl, W B C 19.1 x lO8/1 ( P M N : 80%). Puncture of the abscess revealed pus containing Streptococcus milleri 2, Haemophilus aphrophilus and A. odontolyticus. T h e outcome was good, following I0 days of penicillin sodium (20 g/day IV), gentamicin sulphate (24o m g / d a y IM) and ornidazole (I g/day IV). Case 6

A 65-year-old m a n was admitted to hospital on 27 December I982 for a painful submaxillary swelling with enlarged submaxillary l y m p h nodes. His temperature was normal, pulse rate 7 o / m i n and blood pressure 12o/7o m m H g . An X-ray of the chest was normal. T h e blood count was: R B C 4"5 x lO9/1, haemoglobin 14 g/dl, platelets 289 x io~/1, W B C 9"3 x lO6/1 ( P M N : 75%). Tetracycline had been prescribed for 4 days before the patient's admission to hospital. Incision of the abscess on the following day revealed pus yielding only A. odontolyticus. No further treatment was required.

Actinomyces odontolyticus infections

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Bacteriology1, 14--17

Actinomyces odontolyticus is a Gram-positive, irregularly staining bacterium, non-acid-fast, non-spore-forming and non-motile. Microcolonies, after 48 h growth on brain-heart infusion agar, are usually smooth, with an entire edge, and may have a dense centre. On blood agar, small colonies are irregular, smooth to slightly granular and with an entire edge. An area of greening may appear around the colonies so that they resemble a-haemolytic streptococci. Macrocolonies on brain-heart infusion agar after 7-r5 days' incubation are I-2 m m in diameter, circular to irregular, raised, convex or umbonate, smooth or granular with an entire or irregular edge, opaque, white and soft. On blood agar mature colonies produce a dark red pigment. This may appear in 2 - I 4 days and may develop best when an anaerobically grown culture is allowed to stand aerobically at room temperature. This feature is very important in the presumptive identification. Definitive identification is based on: negative catalase and oxidase tests, reduction of nitrate to nitrite, filamentation of microcolonies (sometimes absent), absence of growth at p H 5"5 and absence of propionic acid in the end-products of glucose fermentation (different from `4rachnia sp. and Propionibacterium sp.). Our strains produced only small quantities of acetic and succinic acid (different from Bifidobacterium sp.). Otherwise the fermentation reactions of ,4. odontolyticus are variable. With a micromethod (API system) we found fermentation of glucose, maltose and lactose; glycerol and mannose were slowly and little acidified. In all of our cases (except case I) a Gram-positive bacterium was shown by direct staining of pus. Antibiotic susceptibility tests were performed under anaerobic conditions by a disc diffusion technique except for that of metronidazole, for which a tube dilution technique with Schaeddler broth was used. Our strains were susceptible to penicillin, ampicillin, cephalothin, tetracycline, erythromycin, clindamycin and chloramphenicol. T h e y were resistant to aminoglycosides as well as to colistin. While susceptibility to metronidazole is variable, 18 our strains were resistant to this agent. Discussion

Since its isolation from the dental arch by Batty in I958, ,4. odontolyticus has often been identifed in the mouth. One of us (Y.P.) found it in 35 of 78 samples 19-2° in cases of granulomas, pulpitis and periodontitis. Its exact role is still under discussion, but it would seem that it participates in the genesis of dental plaque. ~,19,21.-2~ Its implication in periodontitis has also been considered. 26 T h e organism has rarely been found outside the mouth, its natural habitat, except in cases of bacteraemia after scalingY Gerencser and Slack in I9585 first suggested that it might be pathogenic when they found it associated with ,4rachnia propionica in a patient with dacryocystitis. Since then it has been mentioned in various pathological conditions: malar mass, 6 4 cases of cervical actinomycosis9 and one case of hepatic actinomycosis. 8 In addition, it has been found in pus in: lung abscess 3, pleural empyema (associated with Streptococcus faecalis), 4 and thoracic abscess. 7

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Y. PELOUX E T A L .

E l s e w h e r e the or ga ni s m has been m e n t i o n e d in nine o t h e r cases. 1°-11 N o detail was given. I n hal f o f the cases, o t h e r t h a n those o f actinomycosis, r e p o r t e d it is m e n t i o n e d as being in pus. T h e organi sm is associated with o t h e r p a t h o g e n s in five o f o u r cases. T h e sixth pat i ent had b e e n previ ousl y t reat ed with antibiotics. It appears that this organism c a n n o t be p a t h o g e n i c on its own. E x p e r i m e n t a l l y , it is n o n - p a t h o g e n i c in p u r e cul t ure in animalsfl b u t it is able to p o t e n t i a t e the virulence o f a n o t h e r organism. In o u r first case we verified the absence o f p a t h o g e n i c i t y ofFusobacterium necrophorum and A. odontolyticus in mice w h e n separately injected intra-peritoneally. W h e n b o t h were injected simultaneously, h o w e v e r , t h e y killed the mice. la As to the portal o f ent ry, the m o u t h is p r o b a b l y implicated in m o s t cases. It is possible that o t h e r m u c o u s m e m b r a n e s carry this organism, as suggested in o u r observat i on o f an I . U . D . infection. O t h e r I . U . D . infections have b e e n r e p o r t e d with various species o f Actin o my ces fl s-33 b u t n o t with A . odontolyticus. T h e status of patients w ho c o n t r a c t such infections in sites o t h e r t h a n the m o u t h is interesting. T w o patients 3, 4 were i m m u n o s u p p r e s s e d , and in o u r observations we n o t e d an alcoholic and a s c h i z o p h r e n i c patient. P e r h a p s such conditions encourage the infection. T h e r a p e u t i c a l l y , the p r o n o u n c e d susceptibility o f A . odontolyticus to m o s t antibiotics (except aminoglycosides and colistin) facilitates treatm e n t . M e t r o n i d a z o l e is rarely effective and c a n n o t be r e c o m m e n d e d . Conclusion W e believe that A. odontolyticus generally acts as a p y o g e n i c organism. It is quite o f ten f o u n d in m i x e d infections as are o t h e r Actinomyces spp. References I. Slack JM. In Buchanan RE Gibbons NEed., Bergey's manual of determinative bacteriology, 8th ed. Baltimore: Williams & Wilkins I974, 659-664. 2. Batty I. Actinomycesodontolyticus. A new species ofactinomyceteregularly isolated from deep carious dentine. J Pathol I958; 75: 455-459. 3. Baron EJ, Angevine J, Sundstrom W. Actinomycotic pulmonary abscess in an immunosuppressed patient. Am J Clin Pathol I979; 72: 637-639. 4. Dublanchet A, Durieux R, Guillou JP, Chevrier L, Beucl~re A. Un cas de pleur6sie purulente h Actinomyces odontolyticus. Med Mal Inf I978; 8: I25--I26. 5. Gerencser MA, Slack JM. Isolation and characterisation of Actinomyces propionicus. J Baet I967; 94: Io9-II5. 6. Mitchell PD, Hintz CZ, Haselby RC. Malar mass due to Actinomyces odontolyticus. J Clin Microbiol I977; 5: 658-66o. 7. Morris JF, Kilbourn P. Systemic actinomycosis caused by Actinomyces odontolyticus. Ann Int Med I974; 8x : 7oo. 8. Ruutu P, Pentikainen P], Larinkari U, Lempinen M. Hepatic actinomycosis presenting as repeated cholestatic reactions. Scand J Infect Dis 1982; x4: 235-238. 9. Pulverer G, Schaal KP. Treatment of actinomycosis. Proceedings of the z3th International Congress of Chemotherapy (S.Y. 46-8), Vienna I983. io. Georg LK. The agents of human actinomycosis. In Balows A. ed., Anaerobic bacteria Springfield, Illinois: Thomas, I974; 237-256xI. Rose I-I, Varkey B, Kesavakutty C. Thoracic actinomycosis caused by Actinomyces meyeri. Am Rev Resp Dis I982; I25: 251--254. I2. Peloux Y, Chardon H, Lagier E, Jauffret P, Latil G, De Cuttoli JP. Le r61e pathog~ne des Actinomyces en dehors de l'actinomycose. Apropos de deux cas de suppurations aigues contenant Actinomyces odontolyticus. Sem H~p Paris I983 ; 59: 3o63-3o64.

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I3. Raoult D, Kohler JL, Gallais H, Estrangin E, Peloux Y, Casanova P. Fusobacterium necrophorum associated with Actinomyces odontolyticus septicemia. Pathol Biol 1982; 3o: 576-580. 14. Guillou JP, Durieux R, Dublanchet A, Chevrier L. Actinomyces odontolyticus; first study in France. CR Acad Sci Paris 1977; 285: 156I-I564. 15. Holdeman LV, Cato EP, Moore WEC. Anaerobe laboratory manual, 4th ed. Blacksburg, Virginia 14o6i : Virginia Polytechnic Institute and State University, 1977. 16. Marucha PT, Keyes P, Wittenberger C, Ondon J. Rapid method for identification and enumeration of oral Actinomyces. Infect Immunol 1978; 2 1 : 786-791. 17. Smith LDS. The pathogenic anaerobic bacteria. Springfield, Illinois: Thomas, I975. 18. Wusr J. Susceptibility of anaerobic bacteria to metronidazole, ornidazole and tinidazole and routine susceptibility testing by standardized methods. Antimicrob Agent Chemother 1977; I I : 631-637. 19. Peloux Y, Rocca JP, Levy G, Estrangin E. La plaque dentaire humaine: confrontation des r6sultats bact6riologiques et anatomopathologiques. Rev Inst Pasteur Lyon 1981 ~ I4: 267-277. zo. Rocca JP, Peloux Y, Levy G. Bacteriological investigation on one type of apical granuloma. J Dent Res 1981; 6o : 77. 2 I. Borssen E, Sundquist G. Actinomyces of infected root canals. Oral Surg 1981 ; 5x: 643-648. z2. Edwardson S. Bacteriological studies on deep areas of carious dentine. Odontol Rev 1975; 25: 143. z 3. Holmberg K. Isolation and identification of gram positive rods in human dental plaque. Arch Oral Biol 1976; 21: 153-I6O. 24. Jordan HV, Hammond BF. Filamentous bacteria isolated from human rootsurface caries. Arch Oral Biol 1972; x7: 1333-134z. z5. MacNamara TF, Friedman BK, Kleinberg I. The microbial composition of human incisor tooth plaque. Arch Oral Biol I979; 24: 91-95. 26. Moore WE, Holdeman LV, Smibert RM, Good J, Burmeister JA, Palcanis KG, Ranney RR. Bacteriology of experimental gingivitis in young adult humans. Infect Immun I98Z; 38: 651-667. 27. Conner D, I-Iabermann S~ Collings K, Winford T. Bacteremias following periodontal scaling in patients with healthy appearing ~gingiva. J Periodontol 1967; 38: 466-471. 28. Duguid H, Duncan I, Paratt D, Traynor R. Actinomyces and intrauterine devices. J A M A I982; 248: t579-I58o. 29. Behbehani MJ, Jordan HV. Comparative pathogenicity of Actinomyces in mice. J Med Microbiol 1982; x5: 465-473. 3o. Hager WD, Douglas B, Majmudar B. Pelvic colonisation with Actinomyces in women using intrauterine device. Am ff Obstet Gynecol I979; I35: 680-684. 31. Traynor RM, Paratt D, Duguid H. Isolation of Actinomycetes from cervical specimens. J Clin Pathol I98I ; 34:914-9 I8. 32. Valicenti JF, Pappas AA, Graber CD, Williamson O, Fowler Willis N. Detection and prevalence of I.U.D. associated Actinomyees colonization and related morbidity. J A M A I982; 247: 1149--II5Z. 33. Burkman R, Schlesselman S, McCaffrey L. The relationship of genital tract Actinomyces and the development of pelvic inflammatory disease. Am J Obstet Gynecol 1982; x43: 585-589.