INFECTION AND IMMUNITY, JUlY 1986, p. 149-153 0019-9567/86/070149-05$02.

00/0 Copyright C) 1986, American Society for Microbiology

Vol. 53, No. 1

Black-Pigmented Bacteroides

spp.

in Human Apical Periodontitis

MARKUS HAAPASALO,l 2* HELENA RANTA," 3 KARI RANTA,' AND HAROUN SHAH4 Departments of Cariology,' and Bacteriology and Immunology,2 University of Helsinki, and National Public Health Institute,3 SF-00280 Helsinki 28, Finland; and Department of Oral Microbiology, London Hospital Medical College, London El 2AD, United Kingdom4

Received 10 February 1986/Accepted 11 April 1986

The incidence of black-pigmented (BP) Bacteroides spp. in 62 human dental root canal infections (35 acute and 27 clinically asymptomatic cases of apical periodontitis) in 57 adults was studied. Altogether 37 strains of BP Bacteroides were found in 31 infections, always in mixed anaerobic infections. Two different BP Bacteroides species were present in six infections. B. intermedius was most frequently isolated (15 of 62 canals; 24%) followed by B. denticola which was present in 12 cases. Asaccharolytic BP Bacteroides species, B. gingivalis and B. endodontalis, were found in eight cases. BP Bacteroides species were found both from symptomatic and asymptomatic infections, but there were also several symptomatic cases from which BP Bacteroides species were not isolated. B. gingivalis and B. endodontalis were present only in acute infections, B. intermedius was found both in symptomatic and asymptomatic infections, and B. denticolk occurred mostly in asymptomatic infections. BP Bacteroides species were isolated initially from 9 of the 11 teeth with symptoms at 1 week, but only from 22 of the 51 teeth that were symptomless at 1 week. Two strains of B. denticola were resistant to penicillin G at a concentration of 2.4 ,ug/ml, but the MIC of penicillin G for all other strains was 0.6 ,ug/ml or lower. Forty-two randomly selected patients received penicillin V (oral administration, 650 mg, three times daily) during the first week of endodontic therapy. Penicillin had no effect on the occurrence of symptoms after 1 week compared with the control group (20 patients).

Black-pigmented (BP) Bacteroides species are normal inhabitants of the gastrointestinal tract and oral cavity of humans and are also commonly present in mixed anaerobic infections (5). The essential role of BP Bacteroides species in human opportunistic infections has long been established (15, 24, 28). Their pathogenic potential may be related to the production of hydrolytic enzymes such as collagenase and endotoxin and inhibition of the phagocytic function of polymorphonuclear leukocytes (8, 10, 25-27). Results of studies in animals indicate interspecies differences in the virulence potential of BP Bacteroides species (20, 29). The asaccharolytic species B. gingivalis and B. asaccharolyticus and the weakly saccharolytic species B. intermedius have been shown to induce more severe infections than strains previously classified as B. melaninogenicus subsp. melaninogenicus. Advances in the taxonomy of anaerobic bacteria and especially of BP Bacteriodes species, however, have brought some uncertainty to the evaluation of the virulence of these bacteria. Originally one species, B. melaninogenicus is now known to comprise eight species (human strains) on the basis of differences in biochemical characteristics, lipid analyses, DNA base composition, and DNA homology (3, 9, 11, 30). The occurrence of the newly described species of BP Bacteroides in endodontic infections, however, is not known. The virulence potential of bacteria in vivo is difficult to assess. In many respects dental root canal infections offer good conditions for studying the relative significance of a single bacterial species or combinations of species. Because of its anatomy, the root canal lacks normal flora, and specimens can be successfully obtained without mucosal or salivary contamination. Also, the number of different species in root canal infections is relatively low (12, 17, 23, 35).
*

Information has accumulated about the diversity of the flora, but it is only recently that the root canal has been used as a model for opportunistic infection. Induced root canal infections have been studied in animals (4). In studies on human infections the composition of the flora have been compared with the severity of infection. It has been suggested that the occurrence of BP Bacteroides species and symptoms may be closely related (G. Sundqvist, Ph.D. thesis, University of Umea, Umea, Sweden, 1976). Griffee et al. (6) also found a good correlation between the occurrence of symptoms and BP Bacteroides species in periapical osteitis. Whether interspecies differences do occur is not clear because of the diagnostic methods used (6) and the small number of infections studied. Penicillin has been the drug of choice in the treatment of endodontic infections. Recent studies, however, have demonstrated high frequencies of resistant strains also in bilesensitive Bacteroides species, including BP Bacteroides species (16, 18, 21). However, susceptibilities of the different species of BP Bacteroides are usually not given. The aim of this study was to examine the occurrence of BP Bacteroides species and symptoms in human root canal infections with special reference to recent taxonomic advances. Also, the sensitivity patterns of BP Bacteroides spp. to penicillin as well as the effectiveness of orally administered penicillin V in the treatment of apical periodontitis were studied.
MATERIAL AND METHODS

Subjects. Fifty-seven adult patients referred to the Department of Cariology and Endodontics, University of Helsinki, participated in the study. Teeth with one root canal and with diagnosed apical periodontitis were included (62 teeth). Informed consent was obtained. Reasons for exclusion were (i) antibiotic therapy within the previous 3 months, (ii) a periodontal pocket over 4 mm deep, (iii) previous endodontic therapy of the affected tooth, (iv) previous
149

Corresponding author.

Sample collection and bacterial diagnosis. Mueller-Hinton agar (BBL). Oxoid]. sensitivity to kanamycin (100 jig. 0. The mean ages of men and women were 36 and 42 years. Cockeysville. B. (ii) a nonselective medium containing horse blood (5%). gingivalis B. The G+C content was calculated from the following equation: mol% G+C = 50. gingivalis was found together with B. Denmark) and vancomycin (5 pig. and IsoVitaleX (10 mi/liter. intermedius was found in three canals. Montalieu-Vercieu. vancomycin (7.6.150 HAAPASALO ET AL.0) with a Gilford model 240 spectrophotometer and a Gilford 2527 temperature programmer. Sigma]. and B.4 jig/ml. of E. Occurrence of symptoms in 31 cases in which BP Bacteroides species (37 strains) were isolated Species Species erating kit. Merck AG Darmstadt. 10% H202 and 0. Agglutination tests for the asaccharolytic strains were performed with washed human types A. denticola. Cells of all asaccharolytic and saccharolytic indole-negative strains grown either in BM medium (liquid medium containing Trypticase [10 g/liter. production of indole (19). Rosco). Penicillin (penicillin G) concentrations were 0 (control plate). For disinfection of the teeth and the rubber dam. KVLB and MCGP plates were prereduced and used within 3 days after preparation. Apollonia. 1. Penicillin sensitivity tests. After perforation of the cavum.2. Louis. Dental therapy. Esch- erichia coli B (Sigma Chemical Co.05 M Tris-0. and 0 and sheep erythrocytes. denticola B. and 2. API. Frequency of isolation and key characteristics used in the identification of BP Bacteroides species in 62 cases of apical periodontitiSa Species Aggluti. Slides were occasionally rotated. and suspended in the same buffer containing 50 jig of proteinase K (B. BBL).3.5 jig/ml). 0. ~~~No.5 mg/liter. A total of 25 jil of a 2% (vol/vol) suspension of erythrocytes in phosphate-buffered saline was pipetted on microscope slides (kept on ice).15. Lab-Lemco powder (10 g/liter. peptone (15 g/liter.036. colony morphology. hemin [5 mg/liter. DNA base composition. intermedius was isolated in three cases together with B. Federal Republic of Germany) per ml. Not tested. Anaerobic jars were opened after 7 days. Trypticase soy agar (BBL Microbiology Systems. endodontalis. France). and subcultures were made. and B. gingivalis. Staphylococcus aureus ATCC 29213 and Enterococcus faecalis ATCC 29212 were used as controls. England). Patients with any generalized disorders were also excluded. menadione (0. Gram stain. Primary plates were incubated for up to 3 weeks.Tm. and in one case with B. Lysis was achieved with sodium dodecyl sulfate (final concentration. INFECT. CopenTABLE 2. TES buffer). DNA isolation and determination of base composition. intermedius + B. St. yeast extract [5 g/liter. pigmentation patterns. and hemagglutination was registered after 30 min. B. B. intermedius B. The following media were used for initial cultivation: (i) kanamycin (75 jiglml). laked blood (sheep blood) agar (KVLB) (19). or natrium chloride in the medium). the paper point was inserted into the canal to the approximate apex region. 1 mg/ml) treatment for 20 min at 60'C. glucose (2 g/liter). agglutination tests.49 51-52 NT 51-54 48 Saccharolytic B. gingivalis each in one canal. B. 0. and bacteria harvested from MCG plates after 3 days of anaerobic incubation were added. B. and bovine serum [20 mi/liter. Oxoid) at 370C. intermedius + B. contamination of the root canal by saliva (perforated canals). B. 0. peptone. B. b Occurrence of symptoms at 1 week. B. BBL]. bHuman type A. A single colony of a pure culture was used as an inoculum. gingivalis Ioescheii endodontalis intermedius denticola 2 10a" 3 1 9 1 9C BP Bacteroides species presentb 22 BP Bacteroides species not presentb 2 29 aIn three cases B. IMMUN. with symptoms B. Paper points (Maillefer. yeast extract (10 g/liter. [melting temperature] of test strain . in two cases with B. bacteriological agar no. and the DNA was purified by the method of Marmur (14). strains were grown on MCG plates (similar to MCGP but without Lab-Lemco powder. Sensitivity testing was performed in duplicate in an anaerobic chamber (model 1024 anaerobic system. gingiv'alis. which was spread with a platinum loop on the penicillin plate. Oxoid). and N2 (85%).05 M NaCl (pH 8.5% chlorhexidine gluconate in 70% ethanol were used. Cultures were inoculated onto Mueller-Hinton agar (BBL) containing 8% hemolyzed horse blood. denticola in two canals. B. and IsoVitaleX (10 mg/liter.. fermentation of carbohydrates (API 20A.9 + 2. loescheii 15 12 2 - + aA total of 37 strains were isolated from 31 canals (50%).).CelloG +C Indole biose No. Switzerland) were washed with chloroform before sterilization to avoid the possible inhibitory effect of unsaturated fatty acids to the bacterial growth. Oxoid). Sensitivity of BP Bacteroides species to penicillin was determined by the agar dilution method. washed twice with 0. Sigma]. an electrical apex meter (Dahlin Dentometer. The results were recorded under a stereo microscope at low magnification after 2 and 3 days of incubation. and (iii) chocolate agar containing hemolyzed horse blood (8%). hydrolysis of starch and esculin (19).. CO2 (5%). hemin (33 mg/liter). of produc.) was used as a reference DNA. To locate the apical constriction. BBL). natrium chloride [5 g/liter]. Hampshire. respectively. and (v) hypersensitivity to penicillin.005 M EDTA-0. loescheii. B. Oxoid). and natrium chloride (5 g/liter) (MCGP medium). The plates were immediately placed in an anaerobic jar (BBL) and incubated in an anaerobic atmosphere (gas gen- Agglutination tests. B. Forma Scientific) containing H2 (10%). . with ~~~symptoms 6 no No. The tooth was cleaned with pumice and isolated from the oral cavity with a rubber dam. cystein (500 mg/liter).5 mg/liter).44 x (Tm. The mole percent of G+C of purified DNA samples was estimated in triplicate by thermal denaturation in standard saline citrate (pH 7. endodontalis 6 2 + + + + + + + NT NT NT 45-. 0. For inoculum for biochemical tests. coli B). TABLE 1. intermedius. but BP Bacteroides species were isolated at week 0.0. Taastrup.Starch nation of hydrostrains fermen. Oxoid]. menadione [0. The infectious material was immediately spread over the agar plates with the paper point.content tion lysis erythrocyteSb tain(mol%) tto NTc NT NT - Asaccharolytic B.072. proteose peptone [10 g/liter. 1 (Oxoid Ltd. Md. The identification of species of BP Bacteroides was based on the following tests: aerotolerance. Rosco. Oxoid]) or on blood agar plates were collected by centrifugation. Bellaigues. Mo. denticola. and 0 and sheep erythrocytes. NT.

in which nearly half of the cases were asymptomatic. BP Bacteroides species were isolated from nine of these teeth at the beginning of the treatment (Table 2). melaninogenicus is very similar to B. (13) studied the susceptibilities of only oral BP Bacteroides species. RESULTS Frequencies of isolation. (2) found 9 BP Bacteroides strains in 12 cases. the characteristic pigmentation was no longer observed on horse blood agar. In our experience.3 0. denticola were found to be resistant.6 . and tenderness to percussion were regarded as signs of an acute infection. One or more species of BP Bacteroides were found in 19 (54%) of the symptomatic cases and in 12 (44%) of the asymptomatic cases. Symptoms were present in 11 teeth 1 week after the first examination. it is probable that the term clinical material used in many reports refers to nonoral strains. are usually not reported. Ioescheii in root canal infections usually have not been reported. Colonies of slowly pigmenting BP Bacteroides species have no other characteristics different from many other Bacteroides species. After repeated subcultures on MCG medium with sheep blood. All BP Bacteroides strains were isolated from mixed anaerobic infections. as well as the sources of isolates.4 >2. B. The number of anaerobic species usually varied from three to seven. denticola. and the measurement was confirmed radiographically. B. MICs for penicillin G of oral BP Bacteroides strains No. together with prolonged incubation of the primary plates to detect delayed pigmentation. In this study sheep blood was used only in the KVLB medium for initial cultivation. while horse blood was used for other media at this stage. Symptoms were registered in 35 teeth (56%). open sinus tract. 23. loescheii. all strains except one showed the characteristic pigmentation. 53.ug/ml. may partly explain the high frequency of BP Bacteroides species in our material. and the diagnostic precedures that were employed. Symptoms were registered at the beginning (0 weeks) and at 1 week. We also noticed that many BP Bacteroides strains pigmented readily on the primary plate when they were adjacent to colonies of other species. It should be emphasized that not all species of BP Bacteroides readily pigment on horse blood agar. (17) reported two B. 35). On laked rabbit blood agar. Only two strains of B. Laatsch et al. and B. In this study one or two species of BP Bacteroides were isolated in 31 of 62 teeth (50%) with apical periodontitis. When only acute dentogenous abscesses have been studied. 9 periodontal. Whether the presence of BP Bacteroides species always results in an acute infection cannot be evaluated from the results of these studies because only acute infections were included. more BP Bacteroides species were isolated from the MCGP and chocolate agar media than from the KVLB plates. asaccharolyticus. (1) studied acute dentogenous abscess aspirates and isolated BP Bacteroides species in 34 of 50 cases (68%). This. (34) found four strains of BP Bacteroides species in 3 of 10 dental abscesses studied. and the occurrence of symptoms when BP Bacteroides species were present are given in Tables 1 and 2. 22. three times daily) for 7 days. One explanation for this is that vancomycin is inhibitory to some BP Bacteroides species (32). while B. denticola. of strains penicillin G concn (. and 18 strains were not identified to the species level. and Williams et al. but these two species can be readily identified by the difference in the DNA base composition (9). one strain was identified as B. gingivalis endodontalis intermedius denticola Ioescheii 6 2 12 12 2 0. Results of several studies during the last few years have shown resistance to penicillin among BP Bacteroides species (16. Pain. denticola was by far the most common representative of this group. and the number of facultative species varied from zero to one. After the second examination all patients became symptomless. B. Sampling and cultivation onto the agar plates were performed at chairside. denticola if only conventional biochemical tests are used. melaninogenicus have. of strains inhibited at the following Species No. melaninogenicus subsp. melaninogenicus often require rabbit or sheep blood to show the characteristic pigmentation (9). Also in this study only a few strains were diagnosed to the species level.ug/ml): B. 1986 ROLE OF DIFFERENT BP BACTEROIDES SPP. Canals were filled with calcium hydroxide and sealed with a temporary filling between appointments.2 2. denticola. 151 hagen. B. In this study B.036 0. One of these four strains was identified as B. The proportions of acute infections declined from 55 to 19% in the penicillin group and from 30 to 15% in the control group. or both. sample processing.15 0. in fact. The great differences in the frequencies of BP Bacteroides species in these studies may partly reflect differences in sampling. Forty-two randomly selected patients received penicillin V (650 mg. B. Oguntebi et al. swelling. Our strains were all sensitive at a concentration of 0. intermedius strains from 10 periapical abscesses. 15 were identified as B. The frequencies of B. The interspecies differences. However. and B.4 3 3 1 1 7 5 2 1 1 5 3 2 DISCUSSION In previous reports of root canal infections the incidence of BP Bacteroides species ranges from 6 to 38% (6. In the tenth tooth a radicular cyst was diagnosed by the radiograph. melaninogenicus was totally absent. It is possible that some strains presented earlier under the name of B. the pigmentation of asaccharolytic species may also be delayed.6 1. the pigmentation of most B. Susceptibilities of BP Bacteroides species to penicillin are given in Table 3. Yet. Von Konow et al. When pure cultures of the indole-negative saccharoclastic BP Bacteroides species were obtained. higher frequencies also have been found. and the color of single colonies varies from light grey to dark brown. been B. key biochemical characteristics. although BP Bacteroides species are often isolated from acute dentogenous infections. Aderholt et al. with the exception of two strains of B. they . 12. 21). asaccharolyticus. B. melaninogenicus. there are also other species or combinations of species capable of inducing an acute phase of infection. Ioescheii was isolated from only two canals. 18. denticola. (33) studied needle aspirates of 57 dentoalveolar abscesses (39 periapical.VOL. denticola strains reappeared. In a study of acute periapical abscesses of children (5 to 16 years old) Brook et al. The reduction in the number of symptomatic cases was comparable in the penicillin (42 teeth) and control (20 teeth) groups between the first and second examinations. Of their strains. intermedius. However. TABLE 3. Denmark) was used. B.072 0. B. and 9 surgical infections) and found BP Bacteroides species in only three cases. B.

We previously reported our B. Sisson. J.. and N. Johnson. L. 1961. B. 2. 30:559-564. 4th ed. LITERATURE CITED Moore 1970). K. A. Antimicrobial susceptibilities of gram-negative anaerobes. American Society for Microbiology. Histopathological effects in the palate of the rat induced by injection with different black-pigmented Bacteroides strains. compared with the control group. endodontalis was isolated in 9 of 17 abscesses of endodontic origin. Aderholt. F. and K. 20. Hausler. dentalis (7). R. Oguntebi... Kielich. Jr. Oral Biol. Lett. nov. 19. 1981. Holdeman. Antibiotic susceptibility of black-pigmented Bacteroides isolates from the human oral cavity. I.). S. S. Socransky. the asaccharolytic oral species B. Bacteriol. (6). and R. de Graaf. Grigsby. Finegold. 11. V. and G. Sabiston. Antimicrob. M. 19:292-302.125 . L. and J. W. and K. 1981. de Jong. H. thesis) and Griffee et al. and emendation of the descriptions of Bacteroides melaninogenicus (Oliver and Wherry) Roy and Kelly 1939 and Bacteroides denticola Shah and Collins. E. intermedius. 22. Murray. and A. G. Oral Surg. Our results are in good agreement with the virulence tests of BP Bacteroides species in animals (20. 1981. L. Predominant microflora associated with human dental periapical abscesses. Percival. S. and Bacteroides macacae (Slots and Genco) comb. Ranta. J. W. P. J. 1984.152 HAAPASALO ET AL.. 14:153-156. gingivalis is the most virulent BP Bacteroides species. Our strains seem to be phenotypically indistinguishable from B. 18. The bacteriology of dentogenous pyogenic infections. Laatsch. 1984. Syst. and D. and the overall isolation frequency of BP Bacteroides species in our material was high. p. gingivalis was isolated more frequently than B. and E. Manual of clinical microbiology. 1980. Selkon. J. 50:457-461. The presence of symptoms 1 week after the beginning of treatment appeared to be related to the occurrence of BP Bacteroides species in these teeth when therapy was started. Agents Chemother. 6. Tharagonnet. Roeterink. intermedius. Gibbons. Hentges. J. Inhibition of phagocytosis in vitro by obligate anaerobes. 26. 11:605-608. M. P. but while our paper was in press the description of B.. Influence of combinations of oral bacteria on periapical tissues of monkeys. A procedure for the isolation of deoxyribonucleic acid from micro-organisms. Enberg. J. endodontalis in necrotic root canal is closely related to an acute infection and that fermentative BP Bacteroides species. and J. 19:91-96. 1974. and C. Isolation and characterization of a new variant of black pigmented Bacteroides. Griffee. Rosenblatt. S. S. It is also possible that the risk for persisting symptoms may be greater when BP Bacteroides species are part of the infective flora. nov. Patterson. Dis. Lennette. gingivalis was isolated in only 2 of 17 cases. J. It is possible that the resistance to phagocytosis by BP Bacteroides species (10. M. 14. The relationship of Bacteroides melaninogenicus to symptoms associated with pulpal necrosis. In our study B. Brook. are frequently present both in symptomatic and asymptomatic infections. Mayrand. A. 1977.5 ugIml. A. It was not only that symptoms were present without BP Bacteroides species but we also found an equal amount of symptomless teeth with BP Bacteroides species. Johnson. 6:242-248.J.. Miller. who suggested that there is a relationship between symptoms and BP Bacteroides species in human periapical osteitis. found that half of the strains had a MIC of less than 0. and of them a minority were abscesses. 23: 269-274. C. Academic Press. In a recent study on odontogenic abscesses. Slee. Biological activities of endotoxin from Bacte- roides melaninogenicus. Steffen. Mol. E. 1982. of 0. endodontalis was published (30). and N. McBride. 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Codd. 15:964-966. Dent. Balows. D. We were not able to confirm the findings of Sundqvist (G. Antimicrobial susceptibility testing of anaerobic bacteria. nov. B. J. V. gingivalis and B. B. However. Fabricius. W. Newton. B.ug/ml. E. Dis. and A. Immun. Scand. Required role of Bacteroides melaninogenicus in mixed anaerobic infections. J.. 21. 29). H. Isolation and classification of anaerobic bacteria from intact chambers of nonvital teeth in man. Shadomy (ed. J. endodontalis were found only in acute infections. Inc.. Marmur. Lancet ii:1252-1254. 24.. Arch. Segerstrom.. Coykendall. even with careful cleaning of the root canal space.. H. A. and B. Microbiol. S. and L. nov. 8. Rev.D. H. S. A.. L.. E. L. J. Kos. R. Genetic heterogeneity in Bacteroides asaccharolyticus (Holdeman and Infect. 1980. Periodontal Res. Kafrawy. 1982.. 4. A. J. New York. 1976. Henry. 32:399-409. L. endodontalis. R. 52:583-587. R. Oral Surg. 3:208-218. and descriptions of Bacteroides corporis sp. Bacteroides intermedius comb. and Bacteroides levii sp. G. Haapasalo. Agents Chemother. 1051-1092. H. in cases of uncomplicated periapical infections. Ranta. and C. Int. H. B. Moller. 115:247-253. 1982. C. Bloom. nov. W. endodontalis was the most frequently isolated BP Bacteroides species after B. and H. Sundqvist. endodontalis in this report to avoid confusion. Culture media. and W. Rosenblatt. C. M.. Res. The results of this study also suggest that penicillin therapy has no substantial effect on the occurrence of symptoms 1 week after the beginning of the treatment. Description of Bacteroides loescheii sp. Syst. Microbiol. In E. Holdeman. Int. Van Winkelhoffet al. 26) may partly explain the slower disappearance of the symptoms. 15:343-348. and P. but comparisons between these two studies are difficult to make because different materials were used. F. Johansson. 7:378-380. Cumberland. J. Frenkel. IMMUN. FEMS Microbiol. INFECT. Arch. A. S.. Ph. 9. Ingham.. Nash. Dahlen. 1983. 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