Skip to main content
SpringerLink
Log in

Pathogenic synergy: mixed infections in the oral cavity

  • Oral Microbiology
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

In almost all infections in the oral cavity, mixed populations of bacteria are present. However, recent evidence points to a certain specificity in these infections:Streptococcus mutans is related to caries and black-pigmentedBacteroides species are suspected pathogens in periodontal disease. Periodontal diseases, endodontic infections and submucous abscesses in the oral cavity are probably mixed infections in which anaerobic bacteria together with facultatives or other anaerobes are present. In experimental mixed anaerobic infections black-pigmentedBacteroides strains have been shown to play a key role. Little is known about the pathogenic synergy between the bacteria involved in mixed infections. Important mechanisms could be nutritional interrelationships and interactions with the host defense. Within the group of black-pigmentedBacteroides B. gingivalis seems to be the most virulent species. These bacteria possess a great number of virulence factors, which might be important in the pathogenesis of oral infections.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aderhold, L., Knothe, H. andFrenkel, G. 1981. The bacteriology of dentogenous pyogenic infections. — Oral Surg. Oral Med. Oral Pathol.52: 583–587.

    Article  CAS  PubMed  Google Scholar 

  • Brook, I., Gillmore, J. D., Coolbaugh, J. C. andWalker, R. I. 1983. Pathogenicity of encapsulatedBacteroides melaninogenicus group,B. oralis andB. ruminicola subsp.brevis in abscesses in mice. — J. Infect.7: 218–226.

    Article  CAS  PubMed  Google Scholar 

  • Brook, I., Grimm, S., andKielich, R. B. 1981. Bacteriology of acute periapical abscess in children. — J. Endodontics7: 378–380.

    CAS  Google Scholar 

  • Burdon, J. L. 1932. Isolation and cultivation ofBacterium melaninogenicum. — Proc. Soc. Exp. Biol. NY29: 1144–1145.

    Google Scholar 

  • Gibbons, R. J. andMacDonald, J. B. 1960. Hemin and vitamin K compounds as required factors for the cultivation of certain strains ofBacteroides melaninogenicus. — J. Bacteriol.80: 164–170.

    CAS  PubMed  Google Scholar 

  • Gibbons, R. J. andMacDonald, J. B. 1961. Degradation of collagenous substrates byBacteroides melaninogenicus. — J. Bacteriol.81: 614–621.

    CAS  PubMed  Google Scholar 

  • Grenier, D. andMayrand, D. 1983. Etudes d’infections mixtes anaérobies comportantBacteroides gingivalis. — Can. J. Microbiol.29: 612–618.

    CAS  PubMed  Google Scholar 

  • Griffee, M. B., Petterson, S. S., Miller, C. H., Kafrawy, A. H. andNewton, C. W. 1980. The relationship ofBacteroides melaninogenicus to symptoms associated with pulpal necrosis. — Oral Surg. Oral Med. Oral Pathol.50: 457–461.

    CAS  PubMed  Google Scholar 

  • Hammond, B. F. andStevens, R. H. 1982.Capnocytophaga andActinobacillus actinomycetemcomitans: occurrence and pathogenic potential in juvenile periodontitis. p. 46–61.In R. J. Genco and S. E. Mergenhagen (eds), Host-parasite Interactions in Periodontal Disease. — American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • Holdeman, L. V., Kelley, R. W. andMoore, W. E. C. 1984. Genus I.Bacteroides, Castellani and Chalmers 1919, 959. p. 604–631.In N. R. Krieg and J. G. Holt (eds), Bergey’s Manual of Systematic Bacteriology. — The Williams and Wilkins Co., Baltimore.

    Google Scholar 

  • Kantz, W. E. andHenry, C. A. 1974. Isolation and classification of anaerobic bacteria from intact pulp chambers of non-vital teeth in man. — Arch. Oral Biol.19: 91–96.

    CAS  PubMed  Google Scholar 

  • Kastelein, P., Van Steenbergen, T. J. M., Bras, J. M. andDe Graaff, J. 1981. An experimentally induced phlegmonous abscess by a strain ofBacteroides gingivalis in guinea pigs and mice. — Antonie van Leeuwenhoek47: 1–9.

    Article  CAS  PubMed  Google Scholar 

  • Kilian, M. 1981. Degradation of immunoglobulins A1, A2, and G by suspected principal periodontal pathogens. — Infect. Immun.34: 757–765.

    CAS  PubMed  Google Scholar 

  • Kornman, K. S. andLoesche, W. J. 1980. The subgingival microbial flora during pregnancy. — J. Periodontal Res.15: 111–122.

    CAS  PubMed  Google Scholar 

  • Labriola, J. D., Mascaro, J. andAlpert, B. 1983. The microbiologic flora of orofacial abscesses. — J. Oral Maxillofac. Surg.41: 711–714.

    CAS  PubMed  Google Scholar 

  • Laughon, B. E., Syed, S. A. andLoesche, W. J. 1982. API ZYM system for identification ofBacteroides spp.,Capnocytophaga spp., and spirochaetes of oral origin. — J. Clin. Microbiol.15: 97–102.

    CAS  PubMed  Google Scholar 

  • Loesche, W. J. 1976. Chemotherapy of dental plaque infections. — Oral Sci. Rev.9: 63–105.

    Google Scholar 

  • Loesche, W. J. 1980. The role of anaerobes in periodontal disease. p. 61–71.In G. Gottschalk, N. Pfennig and H. Werner (eds), Anaerobes and Anaerobic Infections. — Gustav Fischer Verlag, Stuttgart.

    Google Scholar 

  • Loesche, W. J. andLaughon, B. E. 1982. Role of spirochetes in periodontal disease. p. 62–75.In R. J. Genco and S. E. Mergenhagen (eds), Host-parasite Interactions in Periodontal Disease. — American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • Loesche, W. J., Syed, S. A., Laughon, B. E. andStoll, J. 1982. The bacteriology of acute necrotizing ulcerative gingivitis. — J. Periodontol.53: 223–230.

    CAS  PubMed  Google Scholar 

  • MacDonald, J. B., Socransky, S. S. andGibbons, R. J. 1963. Aspects of the pathogenesis of mixed anaerobic infections of mucous membranes. — J. Dent. Res.42: 529–544.

    Google Scholar 

  • MacLaren, D. M., Namavar, F., Verweij-Van Vught, A. M. J. J., Vel, W. A. C. andKaan, J. A. 1984. Pathogenic synergy: mixed intra-abdominal infections. — Antonie van Leeuwenhoek50: 775–787.

    Article  CAS  PubMed  Google Scholar 

  • Mayrand, D. andMcBride, B. C. 1980. Ecological relationships of bacteria involved in a simple, mixed anaerobic infection. — Infect. Immun.27: 44–50.

    CAS  PubMed  Google Scholar 

  • Mayrand, D., McBride, B. C., Edwards, T. andJensen, S. 1980. Characterization ofBacteroides asaccharolyticus andB. melaninogenicus oral isolates. — Can. J. Microbiol.26: 1178–1183.

    CAS  PubMed  Google Scholar 

  • Mayrand, D. andWhite, D. 1983. Proportion et fréquence de trois genres bactériens anaerobies en fonction de l’indice gingival. — J. Biol. Buccale11: 271–278.

    CAS  PubMed  Google Scholar 

  • Namavar, F., Verweij, A. M. J. J., Bal, M., Van Steenbergen, T. J. M., De Graaff, J. andMacLaren, D. M. 1983. Effect of anaerobic bacteria on killing ofProteus mirabilis by human polymorphonuclear leukocytes. — Infect. Immun.40: 930–935.

    CAS  PubMed  Google Scholar 

  • Newman, M. G. 1979. The role ofBacteroides melaninogenicus and other anaerobes in periodontal infections. — Rev. Infect. Dis.1: 313–323.

    CAS  PubMed  Google Scholar 

  • Oguntebi, B., Slee, A. M., Tanzer, J. M. andLangeland, K. 1982. Predominant microflora associated with human dental periapical abscesses. — J. Clin. Microbiol.15: 964–966.

    CAS  PubMed  Google Scholar 

  • Okuda, K., Slots, J. andGenco, R. J. 1981.Bacteroides gingivalis, Bacteroides asaccharolyticus, andBacteroides melaninogenicus subspecies: cell surface morphology and adherence to erythrocytes and human buccal epithelial cells. — Curr. Microbiol.6: 7–12.

    Article  Google Scholar 

  • Pulverer, G. andHeinrich, S. 1960. Infektionsversuche an Laboratoriumstieren und in vitro-Untersuchungen zur Fermentausstattung desBacteroides melaninogenicus. — Z. Hyg. Infektionskr.146: 341–349.

    CAS  PubMed  Google Scholar 

  • Pulverer, G., Ko, H. L., Wegrzynowicz, Z. andJeljaszewicz, J. 1977. Clotting and fibrinolytic activities ofBacteroides melaninogenicus. — Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. 1: Orig. Reihe A:239: 510–513.

    CAS  Google Scholar 

  • Robertson, P. B., Lantz, M., Marucha, P. T., Kornman, K. S., Trummel, C. L. andHolt, S. C. 1982. Collagenolytic activity associated withBacteroides species andActinobacillus actinomycetemcomitans. — J. Periodontal Res.17: 275–283.

    CAS  PubMed  Google Scholar 

  • Roeterink, C. H., Van Steenbergen, T. J. M., De Jong, W. F. B. andDe Graaff, J. 1984. Histopathological effects in the palate of the rat induced by injection with different black-pigmentedBacteroides strains. — J. Periodontal Res.19: 292–302.

    CAS  PubMed  Google Scholar 

  • Rudek, W. andHaque, R. U. 1976. Extracellular enzymes of the genusBacteroides. — J. Clin. Microbiol.4: 458–460.

    CAS  PubMed  Google Scholar 

  • Sabiston, C. B., Grigsby, W. R. andSegerstrom, N. 1976. Bacterial study of pyogenic infections of dental origin. — Oral Surg. Oral Med. Oral Pathol.41: 430–435.

    PubMed  Google Scholar 

  • Saywer, S. J., MacDonald, J. B. andGibbons, R. J. 1962. Biochemical characterization ofBacteroides melaninogenicus. — Arch. Oral Biol.7: 685–691.

    Google Scholar 

  • Slots, J. 1977. The predominant cultivable microflora of advanced periodontitis. — Scand. J. Dent. Res.85: 114–121.

    CAS  PubMed  Google Scholar 

  • Slots, J. 1979. Subgingival microflora and periodontal disease. — J. Clin. Periodontol.6: 351–382.

    Article  CAS  PubMed  Google Scholar 

  • Slots, J. 1981. Enzymatic characterization of some oral and nonoral gram-negative bacteria with the API ZYM system. — J. Clin. Microbiol.14: 288–294.

    CAS  PubMed  Google Scholar 

  • Slots, J. 1982. Importance of black-pigmentedBacteroides in human periodontal disease. p. 27–45.In R. J. Genco and S. E. Mergenhagen (eds), Host-parasite Interactions in Periodontal Disease. — American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • Slots, J. andGenco, R. J. 1979. Direct hemagglutination technique for differentiatingBacteroides asaccharolyticus oral strains from nonoral strains. — J. Clin. Microbiol.10: 371–373.

    CAS  PubMed  Google Scholar 

  • Slots, J. andGenco, R. J. 1984. Black-pigmentedBacteroides species,Capnocytophaga species, andActinobacillus actinomycetemcomitans in human periodontal disease: virulence factors in colonization, survival and tissue destruction. — J. Dent. Res.63: 412–421.

    CAS  PubMed  Google Scholar 

  • Slots, J. andGibbons, R. J. 1978. Attachment ofBacteroides melaninogenicus subsp.asaccharolyticus to oral surfaces and its possible role in colonization of the mouth and of periodontal pockets. — Infect. Immun.19: 254–264.

    CAS  PubMed  Google Scholar 

  • Socransky, S. S. 1977. Microbiology of periodontal disease — present status and future considerations. — J. Periodontal Res.48: 497–504.

    CAS  Google Scholar 

  • Socransky, S. S. andGibbons, R. J. 1965. Required role ofBacteroides melaninogenicus in mixed anaerobic infections. — J. Infect. Dis.115: 247–252.

    CAS  PubMed  Google Scholar 

  • Socransky, S. S., Tanner, A. C. R., Haffajee, A. D., Hillman, J. D. andGoodson, J. M. 1982. Present status of studies on the microbial etiology of periodontal diseases. p. 1–12.In R. J. Genco and S. E. Mergenhagen (eds), Host-parasite Interactions in Periodontal Disease. — American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • Spiegel, C. A., Hayduk, S. E., Minah, G. E. andKrywolap, G. N. 1979. Black-pigmentedBacteroides from clinically characterized periodontal sites. — J. Periodontal Res.14: 376–382.

    CAS  PubMed  Google Scholar 

  • Steffen, E. K. andHentges, D. J. 1981. Hydrolytic enzymes of anaerobic bacteria isolated from human infections. — J. Clin. Microbiol.14: 153–156.

    CAS  PubMed  Google Scholar 

  • Sundqvist, G. K. 1976. Bacteriological studies of necrotic dental pulps. — Ph.D. Thesis, University of Umea, Umea.

    Google Scholar 

  • Sundqvist, G. K., Carlsson, J., Herrmann, B. F., Höfling, J. F. andVäätäinen, A. 1984. Degradation in vivo of the C3 protein of guinea-pig complement by a pathogenic strain ofBacteroides gingivalis. — Scand. J. Dent. Res.92: 14–24.

    CAS  PubMed  Google Scholar 

  • Sundqvist, G. K., Eckerbom, M. I., Larsson, A. P. andSjögren, U. T. 1979. Capacity of anaerobic bacteria from necrotic dental pulps to induce purulent infections. — Infect. Immun.25: 685–693.

    CAS  PubMed  Google Scholar 

  • Takazoe, I., Tanaka, M. andHomma, T. 1971. A pathogenic strain ofBacteroides melaninogenicus. — Arch. Oral Biol.16: 817–822.

    CAS  PubMed  Google Scholar 

  • Tanner, A. C. R., Haffer, C., Brathall, G. T., Visconti, R. A. andSocransky, S. S., 1979. A study of the bacteria associated with advancing periodontitis in man. — J. Clin. Periodontol.6: 278–307.

    Article  CAS  PubMed  Google Scholar 

  • Touw, J. J. A., Van Kampen, G. P. J., Van Steenbergen, T. J. M., Veldhuijzen, J. P. andDe Graaff, J. 1982a. The effect of culture filtrates of oral strains of black-pigmentedBacteroides on the matrix production of chick embryo cartilage cells in vitro. — J. Periodontal Res.17: 351–357.

    CAS  PubMed  Google Scholar 

  • Touw, J. J. A., Van Steenbergen, T. J. M. andDe Graaff, J. 1982b. Butyrate: a cytotoxin for Vero cells produced byBacteroides gingivalis andBacteroides asaccharolyticus. — Antonie van Leeuwenhoek48: 315–325.

    CAS  PubMed  Google Scholar 

  • Van Steenbergen, T. J. M. 1981. Classification and virulence of black-pigmentedBacteroides strains. — Thesis, Vrije Universiteit, Amsterdam.

    Google Scholar 

  • Van Steenbergen, T. J. M., Kastelein, P., Touw, J. J. A. andDe Graaff, J. 1982. Virulence of black-pigmentedBacteroides strains from periodontal pockets and other sites in experimentally induced skin lesions in mice. — J. Periodontal Res.17: 41–49.

    PubMed  Google Scholar 

  • Van Steenbergen, T. J. M., Van Winkelhoff, A. J., Mayrand, D., Grenier, D. andDe Graaff, J. 1984.Bacteroides endodontalis sp. nov., an asaccharolytic black-pigmentedBacteroides species from infected dental root canals. — Int. J. Syst. Bacteriol.34: 118–120.

    Google Scholar 

  • Van Winkelhoff, A. J., Van Steenbergen, T. J. M. andDe Graaff, J. 1983. The role of oralBacteroides in mixed infections. — Antonie van Leeuwenhoek49: 606.

    Article  Google Scholar 

  • Weiss, C. 1943. The pathogenicity ofBacteroides melaninogenicus and its importance in surgical infections. — Surgery13: 683–691.

    Google Scholar 

  • Williams, B. L., McCann, G. F., andSchoenknecht, F. D. 1983. Bacteriology of dental abscesses of endodontic origin. — J. Clin. Microbiol.18: 770–774.

    CAS  PubMed  Google Scholar 

  • Zambon, J. J., Christersson, L. A. andSlots, J. 1983.Actinobacillus actinomycetemcomitans in human periodontal disease: prevalence in patient groups and distribution of biotypes and serotypes within families. — J. Periodontol.54: 707–711.

    CAS  PubMed  Google Scholar 

  • Zambon, J. J., Reynolds, H. S. andSlots, J. 1981. Black-pigmentedBacteroides spp. in the human oral cavity. — Infect. Immun.32: 198–203.

    CAS  PubMed  Google Scholar 

  • Zavistoski, J., Dzink, J. A., Onderdonk A. andBartlett, J. 1980. Quantitative bacteriology of endodontic infections. — Oral Surg. Oral Med. Oral Pathol.49: 171–174.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Research Group for Commensal Infections, Departments of Oral and Medical Microbiology, Schools of Dentistry and Medicine, Vrije Universiteit, Van der Boechorststraat 7, 1081 BT, Amsterdam, The Netherlands

    T. J. M. van Steenbergen, A. J. van Winkelhoff & J. de Graaff

Authors
  1. T. J. M. van Steenbergen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. J. van Winkelhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. de Graaff
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Steenbergen, T.J.M., van Winkelhoff, A.J. & de Graaff, J. Pathogenic synergy: mixed infections in the oral cavity. Antonie van Leeuwenhoek 50, 789–798 (1984). https://doi.org/10.1007/BF02386241

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02386241

Keywords

Search

Navigation