Human Oral Bacterial Biofilms: Composition, Dynamics, and Pathogenesis

  • Robert J. PalmerJr
  • Richard Darveau
  • Richard J. Lamont
  • Bente Nyvad
  • Ricardo P. Teles


The oral cavity has a diverse and dynamic bacterial flora that is significantly more complex than other sites in and on the human body, with the exception of the gut. Bacterial communities differ in composition depending on location in the mouth. Spatial relationships within the communities seem to be important for their function. Composition of the communities varies temporally and spatially: Changes in composition drive oral disease such as caries and periodontitis. Host response is key in the latter disease.


Periodontal Tissue Gingival Crevicular Fluid Oral Bacterium Probe Pocket Depth Periodontal Pathogen 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Robert J. Palmer Jr. is supported by the Intramural Research Program, National Institute of Dental and Craniofacial Research, National Institutes of Health.


  1. Aas JA et al (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721–5732PubMedGoogle Scholar
  2. Aas JA et al (2008) Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol 46:1407–1417PubMedGoogle Scholar
  3. Årtun J, Thylstrup A (1989) A 3-year clinical and SEM study of surface changes of carious enamel lesions after inactivation. Am J Orthod Dentofacial Orthop 95:327–333PubMedGoogle Scholar
  4. Attström R, Schroeder HE (1979) Effect of experimental neutropenia on initial gingivitis in dogs. Scand J Dent Res 87:7–23PubMedGoogle Scholar
  5. Axelsson P et al (2004) The long-term effect of a plaque control program on tooth mortality, caries and periodontal disease in adults. Results after 30 years of maintenance. J Clin Periodontol 31:749–757PubMedGoogle Scholar
  6. Badersten A et al (1984) Effect of nonsurgical periodontal therapy. II. Severely advanced periodontitis. J Clin Periodontol 11:63–76PubMedGoogle Scholar
  7. Baelum V et al (2003) Application of survival analysis to carious lesion transitions in intervention trials. Community Dent Oral Epidemiol 31:252–260PubMedGoogle Scholar
  8. Baelum V et al (2006) Dental caries paradigms in diagnosis and diagnostic research. Eur J Oral Sciv 114:263–277Google Scholar
  9. Baelum V et al (2008) “for richer, for poorer, in sickness and in health…” the role of dentistry in controlling caries and periodontitis globally. In: Fejerskov O, Kidd E (ed) Dental caries: the disease and its clinical management, 2nd edn. Blackwell Munksgaard, OxfordGoogle Scholar
  10. Banas JA (2004) Virulence properties of Streptococcus mutans. Front Biosci 9:1267–1277PubMedGoogle Scholar
  11. Bardow A et al (2008) The role of saliva. In: Fejerskov O, Kidd E (ed) Dental caries: THE disease and its clinical management, 2nd edn. Blackwell Munksgaard, OxfordGoogle Scholar
  12. Becker MR et al (2002) Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 40:1001–1009PubMedGoogle Scholar
  13. Bergstrom J et al (1988) Influence of cigarette smoking on vascular reaction during experimental gingivitis. Scand J Dent Res 96:34–39PubMedGoogle Scholar
  14. Blehert DS et al (2003) Autoinducer 2 production by Streptococcus gordonii DL1 and the biofilm phenotype of a luxS mutant are influenced by nutritional conditions. J Bacteriol 185:4851–4860PubMedGoogle Scholar
  15. Brinig MM et al (2003) Prevalence of bacteria of division TM7 in human subgingival plaque and their association with disease. Appl Environ Microbiol 69:1687–1694PubMedGoogle Scholar
  16. Cebra JJ (1999) Influences of microbiota on intestinal immune system development. Am J Clin Nutr 69:1046S–1051SPubMedGoogle Scholar
  17. Chadwick VS, Anderson R P (1992) Microorganisms and their products in inflammatory bowel disease. In: Macdermott RP, Stenson WF (ed) Inflammatory bowel disease edn. Elseviere, AmsterdamGoogle Scholar
  18. Chalmers NI et al (2008) Characterization of a Streptococcus sp.–Veillonella sp. community micromanipulated from dental plaque. J Bacteriol 190:8145–8154PubMedGoogle Scholar
  19. Chong P et al (2008) LiaS regulates virulence factor expression in Streptococcus mutans. Infect Immun 76:3093–3099PubMedGoogle Scholar
  20. Christersson LA et al (1987) Tissue localization of Actinobacillus actinomycetemcomitans in human periodontitis. I. Light, immunofluorescence and electron microscopic studies. J Periodontol 58:529–539PubMedGoogle Scholar
  21. Chung WO, Dale BA (2008) Differential utilization of nuclear factor-kappaB signaling pathways for gingival epithelial cell responses to oral commensal and pathogenic bacteria. Oral Microbiol Immunol 23:119–126PubMedGoogle Scholar
  22. Cisar JO et al (1995) Lectin recognition of host-like saccharide motifs in streptococcal cell-wall polysaccharides. Glycobiology 5:655–662PubMedGoogle Scholar
  23. Cosseau C et al (2008) The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infect Immun 76:4163–4175PubMedGoogle Scholar
  24. Cotton SL et al (2009) Subgingival taxa in periodontal health and disease using HOMIM. Paper presented at the 87th General Session of the International Association for Dental Research. Miami FL, 1–4 April 2009Google Scholar
  25. Darveau RP et al (1997) The microbial challenge in periodontitis. Periodontol 2000 14:12–32PubMedGoogle Scholar
  26. Dawes C (2003) What is the critical pH and why does a tooth dissolve in acid? J Can Dent Assoc 69:722–724PubMedGoogle Scholar
  27. Dewhirst FE, et al (2010) The human oral microbiome. J Bacteriol, doi:10.1128/JB.00542-10, PMID 20656903Google Scholar
  28. Diaz PI et al (2006) Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl Environ Microbiol 72:2837–2848PubMedGoogle Scholar
  29. Dirks OB (1966) Posteruptive changes in dental enamel. J Dent Res 45:503–511Google Scholar
  30. Dixon DR et al (2004) Modulation of the innate immune response within the periodontium. Periodontol 2000 35:53–74PubMedGoogle Scholar
  31. Douglas CW et al (1993) Identity of viridans streptococci isolated from cases of infective endocarditis. J Med Microbiol 39:179–182PubMedGoogle Scholar
  32. Fejerskov O et al (1981) Rational use of fluorides in caries prevention. Acta Odontologica Scandinavica 39:241–249PubMedGoogle Scholar
  33. Fejerskov O, Manji F (1990) Risk assessment in dental caries. In: Bader JD (ed) Risk assessment in dentistry, University of North Carolina, Chapel Hill, NCGoogle Scholar
  34. Fejerskov O (1997) Concepts of dental caries and their consequences for understanding the disease. Community Dent Oral Epidemiol 25:5–12PubMedGoogle Scholar
  35. Fitzgerald RJ, Keyes PH (1960) Demonstration of the etiologic role of streptococci in experimental caries in the hamster. J Am Dent Assoc 61:9–19PubMedGoogle Scholar
  36. Flemmig TF (1999) Periodontitis. Ann Periodontol 4:32–37PubMedGoogle Scholar
  37. Fong KP et al (2006) Actinobacillus actinomycetemcomitans leukotoxin requires lipid microdomains for target cell cytotoxicity. Cell Microbiol 8:1753–1767PubMedGoogle Scholar
  38. Friedman MT et al (1992) The “Plaque-free zone” in health and disease: a scanning electron microscope study. J Periodontol 63:890–896PubMedGoogle Scholar
  39. Gallagher A et al (2003) Glycosylation of the Arg-gingipains of Porphyromonas gingivalis and comparison with glycoconjugate structure and synthesis in other bacteria. Curr Protein Pept Sci 4:427–441PubMedGoogle Scholar
  40. Garcia RI et al (2001) Relationship between periodontal disease and systemic health. Periodontol 2000 25:21–36Google Scholar
  41. Gemmell E, Seymour GJ (1993) Interleukin 1, interleukin 6 and transforming growth factor-beta production by human gingival mononuclear cells following stimulation with Porphyromonas gingivalis and Fusobacterium nucleatum. J Periodontal Res 28:122–129PubMedGoogle Scholar
  42. Gemmell E et al (1994) Adhesion molecule expression in chronic inflammatory periodontal disease tissue. J Periodont Res 29:46–53PubMedGoogle Scholar
  43. Gibbons RJ, Nygaard M (1970) Interbacterial aggregation of plaque bacteria. Arch Oral Biol 15:1397–1400PubMedGoogle Scholar
  44. Gordon HA, Pesti L (1971) The gnotobiotic animal as a tool in the study of host microbial relationships. Bacteriol Rev 35:390–429PubMedGoogle Scholar
  45. Groeneveld A (1985) Longitudinal study of prevalence of enamel lesions in a fluoridated and non-fluoridated area. Community Dent Oral Epidemiol 13:159–163PubMedGoogle Scholar
  46. Haffajee a D et al (2003) Systemic anti-infective periodontal therapy. A systematic review. Ann Periodontol 8:115–181PubMedGoogle Scholar
  47. Haffajee a D et al (2004) Clinical and microbiological changes associated with the use of combined antimicrobial therapies to treat “refractory” periodontitis. J Clin Periodontol 31:869–877PubMedGoogle Scholar
  48. Haffajee AD et al (2006a) The effect of periodontal therapy on the composition of the subgingival microbiota. Periodontol 2000 42:219–258Google Scholar
  49. Haffajee AD et al (2006b) Association of Eubacterium nodatum and Treponema denticola with human periodontitis lesions. Oral Microbiol Immunol 21:269–282PubMedGoogle Scholar
  50. Hart TC et al (1994) Neutrophil defects as risk factors for periodontal diseases. J Periodontol 65:521–529PubMedGoogle Scholar
  51. Heath JK et al (1987) Bacterial antigens induce collagenase and prostaglandin E2 synthesis in human gingival fibroblasts through a primary effect on circulating mononuclear cells. Infect Immun 55:2148–2154PubMedGoogle Scholar
  52. Heitz-Mayfield LJ et al (2003) Clinical course of chronic periodontitis. II. Incidence, characteristics and time of occurrence of the initial periodontal lesion. J Clin Periodontol 30:902–908PubMedGoogle Scholar
  53. Hemmerle J, Frank RM (1991) Bacterial invasion of periodontal tissues after experimental immunosuppression in rats. J Biol Buccale 19:271–282PubMedGoogle Scholar
  54. Henderson B et al (2003) Molecular pathogenicity of the oral opportunistic pathogen Actinobacillus actinomycetemcomitans. Annu Rev Microbiol 57:29–55PubMedGoogle Scholar
  55. Herrera D et al (2002) A systematic review on the effect of systemic antimicrobials as an adjunct to scaling and root planing in periodontitis patients. J Clin Periodontol 29 Suppl 3:136–159PubMedGoogle Scholar
  56. Herzberg MC et al (1997) Host-pathogen interactions in bacterial endocarditis: Streptococcal virulence in the host. Adv Dent Res 11:69–74PubMedGoogle Scholar
  57. Holmen L et al (1987) Clinical and histological features observed during arrestment of active enamel carious lesions in vivo. Caries Res 21:546–554PubMedGoogle Scholar
  58. Hooper LV et al (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884PubMedGoogle Scholar
  59. Hugoson A et al (2008) Trends over 30 years, 1973–2003, in the prevalence and severity of periodontal disease. J Clin Periodontol 35:405–414PubMedGoogle Scholar
  60. Imfeld T, Lutz F (1980) Intraplaque acid formation assessed in vivo in children and young adults. Pediatr Dent 2:87–93Google Scholar
  61. Jin L, Darveau RP (2001) Soluble CD14 levels in gingival crevicular fluid of subjects with untreated adult periodontitis. J Periodontol 72:634–640PubMedGoogle Scholar
  62. Jin L et al (2004) The in vivo expression of membrane-bound cd14 in periodontal health and disease. J Periodontol 75:578–585PubMedGoogle Scholar
  63. Keyes PH (1960) The infectious and transmissible nature of experimental dental caries – findings and implications. Arch Oral Biol 1:304–319PubMedGoogle Scholar
  64. Kigure T et al (1995) Distribution of Porphyromonas gingivalis and Treponema denticola in human subgingival plaque at different periodontal pocket depths examined by immunohistochemical methods. J Periodontal Res 30:332–341PubMedGoogle Scholar
  65. Kim J, Amar S (2006) Periodontal disease and systemic conditions: a bidirectional relationship. Odontology 94:10–21PubMedGoogle Scholar
  66. Kleinberg I (2002) A mixed-bacteria ecological approach to understanding the role of the oral bacteria in dental caries causation: an alternative to Streptococcus mutans and the specific-plaque hypothesis. Crit Rev Oral Biol Med 13:108–125PubMedGoogle Scholar
  67. Kolenbrander PE (1988) Intergeneric coaggregation among human oral bacteria and ecology of dental plaque. Annu Rev Microbiol 42:627–656PubMedGoogle Scholar
  68. Kolenbrander PE, Palmer RJ Jr (2004) Human oral bacterial biofilms. In: Ghannoum M, O’Toole GA (ed) Microbial biofilms, edn. ASM Press, Washington, DCGoogle Scholar
  69. Kornman KS et al (1997) The host response to the microbial challenge in periodontitis: assembling the players. Periodontol 2000 14:33–53Google Scholar
  70. Kreth J et al (2007) The response regulator comE in Streptococcus mutans functions both as a transcription activator of mutacin production and repressor of CSP biosynthesis. Microbiology (Reading, Engl) 153:1799–1807Google Scholar
  71. Kuboniwa M et al (2008) P. gingivalis accelerates gingival epithelial cell progression through the cell cycle. Microbes Infect 10:122–128PubMedGoogle Scholar
  72. Lamont RJ, Yilmaz O (2002) In or out: the invasiveness of oral bacteria. Periodontol 2000 30:61–69Google Scholar
  73. Larsen MJ (1990) Chemical events during tooth dissolution. J Dent Res 69:575–580PubMedGoogle Scholar
  74. Lemos JA, Burne RA (2008) A model of efficiency: stress tolerance by Streptococcus mutans. Microbiology (Reading, Engl) 154:3247–3255Google Scholar
  75. Lepp PW et al (2004) Methanogenic archaea and human periodontal disease. Proceedings of the National Academy of Sciences of the United States of America 101:6176–6181Google Scholar
  76. Lindemann RA et al (1995) Effect of whole oral bacteria and extracted lipopolysaccharides on peripheral blood leukocyte interleukin-2 receptor expression. J Periodontal Res 30:264–271PubMedGoogle Scholar
  77. Lindhe J et al (1983) Progression of periodontal disease in adult subjects in the absence of periodontal therapy. J Clin Periodontol 10:433–442PubMedGoogle Scholar
  78. Listgarten MA (1994) The structure of dental plaque. Periodontol 2000 5:52–65Google Scholar
  79. Lo ECM et al (1998) Arresting dentine caries in Chinese preschool children. Int J Paediatr Dent 8:253–260PubMedGoogle Scholar
  80. Loe H, Brown LJ (1991) Early onset periodontitis in the United States of America. J Periodontol 62:608–616PubMedGoogle Scholar
  81. Lopez NJ et al (2006) Effects of metronidazole plus amoxicillin as the only therapy on the microbiological and clinical parameters of untreated chronic periodontitis. J Clin Periodontol 33:648–660PubMedGoogle Scholar
  82. Lu Q et al (2004) Expression of human beta-defensins-1 and -2 peptides in unresolved chronic periodontitis. J Periodontal Res 39:221–227PubMedGoogle Scholar
  83. Lu Q et al (2005) Expression of human beta-defensin-3 in gingival epithelia. J Periodontal Res 40:474–481PubMedGoogle Scholar
  84. Macfarlane GD et al (1992) Refractory periodontitis associated with abnormal polymorphonuclear leukocyte phagocytosis and cigarette smoking. J Periodontol 63:908–913PubMedGoogle Scholar
  85. Macpherson AJ, Harris NL (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4:478–485PubMedGoogle Scholar
  86. Maeda K et al (2008) A Porphyromonas gingivalis tyrosine phosphatase is a multifunctional regulator of virulence attributes. Mol Microbiol 69:1153–1164PubMedGoogle Scholar
  87. Mager DL et al (2003) Distribution of selected bacterial species on intraoral surfaces. J Clin Periodontol 30:644–654PubMedGoogle Scholar
  88. Manji F et al (1991) A random effects model for some epidemiological features of dental caries. Community Dent Oral Epidemiol 19:324–328PubMedGoogle Scholar
  89. Marsh PD (2003) Are dental diseases examples of ecological catastrophes? Microbiology (Reading, Engl) 149:279–294Google Scholar
  90. Masada MP et al (1990) Measurement of interleukin-1 alpha and -1 beta in gingival crevicular fluid: implications for the pathogenesis of periodontal disease. J Periodontal Res 25:156–163PubMedGoogle Scholar
  91. McNab R et al (2003) LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185:274–284PubMedGoogle Scholar
  92. Merritt J et al (2003) Mutation of luxS affects biofilm formation in Streptococcus mutans. Infect Immun 71:1972–1979PubMedGoogle Scholar
  93. Moughal NA et al (1992) Endothelial cell leukocyte adhesion molecule-1 (ELAM-1) and intercellular adhesion molecule-1 (ICAM-1) expression in gingival tissue during health and experimentally-induced gingivitis. J Periodont Res 27:623–630PubMedGoogle Scholar
  94. Newman P et al (1979) An in-dwelling electrode for in-vivo measurement of the pH of dental plaque in man. Arch Oral Biol 24:501–507PubMedGoogle Scholar
  95. Noiri Y et al (1997) An immunohistochemical study on the localization of Porphyromonas gingivalis, Campylobacter rectus and Actinomyces viscosus in human periodontal pockets. J Periodontal Res 32:598–607PubMedGoogle Scholar
  96. Noiri Y, Ebisu S (2000) Identification of periodontal disease-associated bacteria in the “plaque-free zone”. J Periodontol 71:1319–1326PubMedGoogle Scholar
  97. Noiri Y et al (2001) The localization of periodontal-disease-associated bacteria in human periodontal pockets. J Dent Res 80:1930–1934PubMedGoogle Scholar
  98. Nylander K et al (1993) Expression of the endothelial leukocyte adhesion molecule-1 (ELAM-1) on endothelial cells in experimental gingivitis in humans. J Periodontol 64:355–357PubMedGoogle Scholar
  99. Nyvad B, Fejerskov O (1986) Active root surface caries converted into inactive caries as a response to oral hygiene. Scan J Dent Res 94:281–284Google Scholar
  100. Nyvad B, Fejerskov O (1987a) Transmission electron microscopy of early microbial colonization of human enamel and root surfaces in vivo. Scan J Dent Res 95:297–307Google Scholar
  101. Nyvad B, Fejerskov O (1987b) Scanning electron microscopy of early microbial colonization of human enamel and root surfaces in vivo. Scan J Dent Res 95:287–296Google Scholar
  102. Nyvad B, Kilian M (1987) Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand J Dent Res 95:369–380PubMedGoogle Scholar
  103. Nyvad B, Kilian M (1990) Comparison of the initial streptococcal microflora on dental enamel in caries-active and in caries-inactive individuals. Caries Res 24:267–272PubMedGoogle Scholar
  104. Nyvad B (1993) Microbial colonization of human tooth surfaces. APMIS 101:7–45Google Scholar
  105. Nyvad B, Fejerskov O (1997) Assessing the stage of caries lesion activity on the basis of clinical and microbiological examination. Community Dent Oral Epidemiol 25:69–75PubMedGoogle Scholar
  106. Nyvad B et al (1999) Reliability of a new caries diagnostic system differentiating between active and inactive caries lesions. Caries Res 33:252–260PubMedGoogle Scholar
  107. Nyvad B et al (2003) Construct and predictive validity of clinical caries diagnostic criteria assessing lesion activity. J Dent Res 82:117–122PubMedGoogle Scholar
  108. Nyvad B (2008) The role of oral hygiene. In: Fejerskov O, Kidd E (ed) Dental caries the disease and its clinical management, Blackwell Munksgaard, OxfordGoogle Scholar
  109. O’Brien-Simpson NM et al (2001) Role of RgpA, RgpB, and Kgp proteinases in virulence of Porphyromonas gingivalis W50 in a murine lesion model. Infect Immun 69:7527–7534PubMedGoogle Scholar
  110. Offenbacher S et al (1996) Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 67:1103–1113PubMedGoogle Scholar
  111. Page RC, Schroeder HE (1976) Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 33:235–249Google Scholar
  112. Page RC et al (1987) Molecular basis for the functional abnormality in neutrophils from patients with generalized prepubertal periodontitis. J Periodontal Res 22:182–183PubMedGoogle Scholar
  113. Page RC, Kornman KS (1997) The pathogenesis of human periodontitis: an introduction. Periodontol 2000 14:9–11Google Scholar
  114. Palmer RJ Jr et al (2003) Coaggregation-mediated interactions of streptococci and actinomyces detected in initial human dental plaque. J Bacteriol 185:3400–3409PubMedGoogle Scholar
  115. Papapanou PN (1996) Periodontal diseases: epidemiology. Ann Periodontol 1:1–36PubMedGoogle Scholar
  116. Papapanou PN (1999) Epidemiology of periodontal diseases: an update. J Int Acad Periodontol 1:110–116PubMedGoogle Scholar
  117. Paster BJ et al (1998) Identification of oral streptococci using PCR-based, reverse-capture, checkerboard hybridization. Methods Cell Sci 20:223–231Google Scholar
  118. Paster BJ et al (2006) The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol 2000 42:80–87Google Scholar
  119. Petersen PE (2003) The World Oral Health Report 2003: continuous improvement of oral health in the 21st century – The approach of the WHO Global Oral Health Programme. Community Dent Oral Epidemiol 31:3–24PubMedGoogle Scholar
  120. Potempa J et al (2003) Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes. Curr Protein Pept Sci 4:397–407PubMedGoogle Scholar
  121. Quirynen M et al (2005) Initial subgingival colonization of “pristine” pockets. J Dent Res 84:340–344PubMedGoogle Scholar
  122. Quivey RG Jr et al (2001) Genetics of acid adaptation in oral streptococci. Crit Rev Oral Biol Med 12:301–314PubMedGoogle Scholar
  123. Quivey RG Jr et al (2000) Adaptation of oral streptococci to low pH. Adv Microb Physiol 42:239–274PubMedGoogle Scholar
  124. Ren L et al (2004) Local expression of lipopolysaccharide-binding protein in human gingival tissues. J Periodontal Res 39:242–248PubMedGoogle Scholar
  125. Ren L et al (2005) The expression profile of lipopolysaccharide-binding protein, membrane-bound CD14, and toll-like receptors 2 and 4 in chronic periodontitis. J Periodontol 76:1950–1959PubMedGoogle Scholar
  126. Sallay K et al (1984) Bacterial invasion of oral tissues of immunosuppressed rats. Infect Immun 43:1091–1093PubMedGoogle Scholar
  127. Salvi GE et al (1997) Influence of risk factors on the pathogenesis of periodontitis. Periodontol 2000 14:173–201Google Scholar
  128. Senadheera D, Cvitkovitch DG (2008) Quorum sensing and biofilm formation by Streptococcus mutans. Adv Exp Med Biol 631:178–188PubMedGoogle Scholar
  129. Serino G et al (2001) Initial outcome and long-term effect of surgical and non-surgical treatment of advanced periodontal disease. J Clin Periodontol 28:910–916PubMedGoogle Scholar
  130. Shao H et al (2007) Autoinducer 2 is required for biofilm growth of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Infect Immun 75:4211–4218PubMedGoogle Scholar
  131. Sheets SM et al (2008) Gingipain-dependent interactions with the host are important for survival of Porphyromonas gingivalis. Front Biosci 13:3215–3238PubMedGoogle Scholar
  132. Shenker BJ et al (2001) Induction of apoptosis in human T cells by Actinobacillus actinomycetemcomitans cytolethal distending toxin is a consequence of G2 arrest of the cell cycle. J Immunol 167:435–441PubMedGoogle Scholar
  133. Simionato MR et al (2006) Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii. Infect Immun 74:6419–6428PubMedGoogle Scholar
  134. Socransky SS, Haffajee a D (1997) The nature of periodontal diseases. Ann Periodontol 2:3–10PubMedGoogle Scholar
  135. Socransky SS et al (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144PubMedGoogle Scholar
  136. Socransky SS, Haffajee AD (2002) Dental biofilms: difficult therapeutic targets. Periodontol 2000 28:12–55Google Scholar
  137. Socransky SS, Haffajee AD (2005) Periodontal microbial ecology. Periodontol 2000 38:135–187Google Scholar
  138. Springer TA (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76:301–314PubMedGoogle Scholar
  139. Stephan R (1940) Changes in hydrogen-ion concentration on tooth surfaces and in carious lesions. J Am Dent Assoc 27:718–723Google Scholar
  140. Sugawara Y et al (2006) Toll-like receptors, NOD1, and NOD2 in oral epithelial cells. J Dent Res 85:524–529PubMedGoogle Scholar
  141. Takahashi N, Nyvad B (2008) Caries ecology revisited: microbial dynamics and the caries process. Caries Res 42:409–418PubMedGoogle Scholar
  142. Teles RP et al (2006) Microbiological goals of periodontal therapy. Periodontol 2000 42:180–218PubMedGoogle Scholar
  143. Teles RP et al (2008) Disease progression in periodontally healthy and maintenance subjects. J Periodontol 79:784–794PubMedGoogle Scholar
  144. Thylstrup A et al (1994) In vivo caries models-mechanisms for caries initiation and arrestment. Adv Dent Res 8:144–157PubMedGoogle Scholar
  145. Tonetti MS et al (1994) Localized expression of mRNA for phagocyte-specific chemotactic cytokines in human periodontal infections. Infect Immun 62:4005–4014PubMedGoogle Scholar
  146. Tonetti MS (1997) Molecular factors associated with compartmentalization of gingival immune responses and transepithelial neutrophil migration. J Periodontal Res 32:104–109PubMedGoogle Scholar
  147. Tonetti MS et al (1998) Neutrophil migration into the gingival sulcus is associated with transepithelial gradients of interleukin-8 and ICAM-1. J Periodontol 69:1139–1147PubMedGoogle Scholar
  148. Tonetti MS, Mombelli A (1999) Early-onset periodontitis. Ann Periodontol 4:39–52PubMedGoogle Scholar
  149. Umesaki Y, Setoyama H (2000) Structure of the intestinal flora responsible for development of the gut immune system in a rodent model. Microbes Infect 2:1343–1351PubMedGoogle Scholar
  150. van Houte J et al (1996) The final pH of bacteria comprising the predominant flora on sound and carious human root and enamel surfaces. J Dent Res 75:1008–1014PubMedGoogle Scholar
  151. van Ruyven FO J et al (2000) Relationship among mutans streptococci, “low-pH” bacteria, and lodophilic polysaccharide-producing bacteria in dental plaque and early enamel caries in humans. J Dent Res 79:778–784PubMedGoogle Scholar
  152. Van Steenbergen TJ et al (1993) Microbiological and clinical monitoring of non-localized juvenile periodontitis in young adults: a report of 11 cases. J Periodontol 64:40–47PubMedGoogle Scholar
  153. Van Winkelhoff AJ et al (1996) Systemic antibiotic therapy in periodontics. Periodontol 2000 10:45–78Google Scholar
  154. Waldrop TC et al (1987) Periodontal manifestations of the heritable Mac-1, LFA-1, deficiency syndrome. Clinical, histopathologic and molecular characteristics. J Periodontol 58:400–416PubMedGoogle Scholar
  155. Wecke J et al (2000) A novel technique for monitoring the development of bacterial biofilms in human periodontal pockets. FEMS Microbiol Lett 191:95–101PubMedGoogle Scholar
  156. White DJ (1997) Dental calculus: recent insights into occurrence, formation, prevention, removal and oral health effects of supragingival and subgingival deposits. Eur J Oral Sci 105:508–522PubMedGoogle Scholar
  157. Whittaker CJ, Klier CM, Kolenbrander PE (1996) Annual Review of Microbiology 50:513–552Google Scholar
  158. Xie H et al (2000) Intergeneric communication in dental plaque biofilms. J Bacteriol 182:7067–7069PubMedGoogle Scholar
  159. Xie H et al (2007) Identification of a signalling molecule involved in bacterial intergeneric communication. Microbiology (Reading, Engl) 153:3228–3234Google Scholar
  160. Xu J, Gordon JI (2003) Inaugural article: honor thy symbionts. Proc Natl Acad Sci USA 100:10452–10459PubMedGoogle Scholar
  161. Yamazaki K et al (1992) Direct and indirect effects of Porphyromonas gingivalis lipopolysaccharide on interleukin-6 production by human gingival fibroblasts. Oral Microbiol Immunol 7:218–224PubMedGoogle Scholar
  162. Yilmaz O et al (2008) ATP scavenging by the intracellular pathogen Porphyromonas gingivalis inhibits P2X7-mediated host-cell apoptosis. Cell Microbiol 10:863–875PubMedGoogle Scholar
  163. Yoshinari N et al (1994) Effect of long-term methotrexate-induced neutropenia on experimental periodontal lesion in rats. J Periodontal Res 29:393–400PubMedGoogle Scholar
  164. Zambon JJ (1996) Periodontal diseases: microbial factors. Ann Periodontol 1:879–925PubMedGoogle Scholar
  165. Zero DT (2004) Sugars – the arch criminal? Caries Res 38:277–285PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Robert J. PalmerJr
    • 1
  • Richard Darveau
    • 2
  • Richard J. Lamont
    • 3
  • Bente Nyvad
    • 4
  • Ricardo P. Teles
    • 5
  1. 1.Oral Infection and Immunity Branch, National Institute of Dental and Craniofacial ResearchNational Institutes of HealthBethesdaUSA
  2. 2.Department of PeriodonticsUniversity of WashingtonSeattleUSA
  3. 3.Department of Oral BiologyUniversity of Florida College of DentistryGainesvilleUSA
  4. 4.School of Dentistry, Faculty of Health SciencesUniversity of AarhusAarhusDenmark
  5. 5.Department of PeriodontologyThe Forsyth InstituteBostonUSA

Personalised recommendations