The role of bacteria in the caries process: Ecological perspectives

Journal of Dental Research

Volumn 90, Issue 3, 2011, Pages 294-303

  Takahashi, N ^a   Nyvad, B ^b  

^a TOHOKU UNIVERSITY   (Japan)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

acid induced adaptation; acid induced selection; acidogenicity; acidurance; Actinomyces; Bifidobacterium; caries process; caries associated bacteria; extended caries ecological hypothesis; Lactobacillus; mutans streptococci; non mutans streptococci

Indexed keywords

ACTINOMYCES; ANIMAL; BIFIDOBACTERIUM; BIOFILM; DENTAL CARIES; ECOSYSTEM; GLYCOLYSIS; HOST PATHOGEN INTERACTION; HUMAN; LACTOBACILLUS; METABOLISM; MICROBIOLOGY; PH; REVIEW; STREPTOCOCCUS; TOOTH PLAQUE;

ACTINOMYCES; ANIMALS; BIFIDOBACTERIUM; BIOFILMS; DENTAL CARIES; DENTAL PLAQUE; ECOSYSTEM; GLYCOLYSIS; HOST-PATHOGEN INTERACTIONS; HUMANS; HYDROGEN-ION CONCENTRATION; LACTOBACILLUS; STREPTOCOCCUS;

EID: 79952065856     PISSN: 00220345     EISSN: 15440591     Source Type: Journal    
DOI: 10.1177/0022034510379602     Document Type: Review

References (102)

1. AAPD (American Academy of Pediatric Dentistry) (2008). Policy on early childhood caries (ECC): classifications, consequences, and preventive strategies. Available at: http://www.aapd.org/media/Policies-Guidelines/P- ECCClassifications.pdf (accessed July 7, 2010).
2. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005). Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721-5732. (Pubitemid 41612354)
3. Aas JA, Griffen AL, Dardis SR, Lee AM, Olsen I, Dewhirst FE, et al. (2008). Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol 46:1407-1417. (Pubitemid 351563587)
4. Becker MR, Paster BJ, Leys EJ, Moeschberger ML, Kenyon SG, Galvin JL, et al. (2002). Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 40:1001-1009. (Pubitemid 34208659)
5. Beighton D, Whiley RA (1990). Sialidase activity of the "Streptococcus milleri group" and other viridans group streptococci. J Clin Microbiol 28:1431-1433. (Pubitemid 20194445)
6. Belli WA, Marquis RE (1991). Adaptation of Streptococcus mutans and Enterococcus hirae to acid stress in continuous culture. Appl Environ Microbiol 57:1134-1138.
7. Boue D, Armau E, Tiraby G (1987). A bacteriological study of rampant caries in children. J Dent Res 66:23-28.
8. Boyar RM, Thylstrup A, Holmen L, Bowden GH (1989). The microflora associated with the development of initial enamel decalcification below orthodontic bands in vivo in children living in a water-fluoridated area. J Dent Res 68:1734-1738.
9. Bowden GH (1990). Microbiology of root-surface caries in humans. J Dent Res 69:1205-1210.
10. Bowden GH, Hardie JM, Slack GL (1975). Microbial variations in approximal dental plaque. Caries Res 9:253-277.
11. Bradshaw DJ, Marsh PD (1998). Analysis of pH-driven disruption of oral microbial communities in vitro. Caries Res 32:456-462. (Pubitemid 128526881)
12. Bradshaw DJ, Homer KA, Marsh PD, Beighton D (1994). Metabolic cooperation in oral microbial communities during growth on mucin. Microbiology 140(Pt 12):3407-3412.
13. Brailsford SR, Shah B, Simons D, Gilbert S, Clark D, Ines I, et al. (2001). The predominant aciduric microflora of root-caries lesions. J Dent Res 80:1828-1833.
14. Brown LR, Dreizen S, Handler S (1976). Effects of selected caries preventive regimens on microbial changes following irradiation-induced xerostomia in cancer patients. In: Microbial aspects of dental caries: workshop proceedings. Stiles HM, Loesche WJ, O'Brien TC, editors. Washington, DC, USA: Information Retrieval Inc (Spec Suppl, Microbiology Abstracts), Vol. 1, pp. 275-290.
15. Burne RA, Marquis RE (2000). Alkali production by oral bacteria and protection against dental caries. FEMS Microbiol Lett 193:1-6.
16. Budtz-Jörgensen E (1990). Etiology, pathogenesis, therapy, and prophylaxis of oral yeast infections. Acta Odontol Scand 48:61-69.
17. Byers HL, Homer KA, Beighton D (1996). Utilization of sialic acid by viridans streptococci. J Dent Res 75:1564-1571. (Pubitemid 32770462)
18. Byers HL, Tarelli E, Homer KA, Beighton D (1999). Sequential deglycosylation and utilization of the N-linked, complex-type glycans of human a1-acid glycoprotein mediates growth of Streptococcus oralis. Glycobiology 9:469-479. (Pubitemid 29240344)
19. Carlsson J (1997). Bacterial metabolism in dental biofilms. Adv Dent Res 11:75-80.
20. Chhour KL, Nadkarni MA, Byun R, Martin FE, Jacques NA, Hunter N (2005). Molecular analysis of microbial diversity in advanced caries. J Clin Microbiol 43:843-849. (Pubitemid 40256044)
21. Corby PM, Lyons-Weiler J, Bretz WA, Hart TC, Aas JA, Boumenna T, et al. (2005). Microbial risk indicators of early childhood caries. J Clin Microbiol 43:5753-5759. (Pubitemid 41612357)
22. Dige I, Raarup MK, Nyengaard JR, Kilian M, Nyvad B (2009). Actinomyces in initial dental biofilm formation. Microbiology 155(Pt 7):2116-2126.
23. Dirksen TR, Little MF, Bibby BG, Crump SL (1962). The pH of carious cavities. 1. The effect of glucose and phosphate buffer on cavity pH. Arch Oral Biol 7:49-57.
24. Edwardsson S (1974). Bacteriological studies of deep areas of carious dentine. Odontol Revy 25(Suppl 32):1-143.
25. Eliasson L, Carlén A, Almståhl A, Wikström M, Lingström P (2006). Dental plaque pH and micro-organisms during hyposalivation. J Dent Res 85:334-338. (Pubitemid 43672442)
26. Fejerskov O, Scheie AA, Manji F (1992). The effect of sucrose on plaque pH in the primary and permanent dentition of caries-inactive and -active Kenyan children. J Dent Res 71:25-31.
27. Fejerskov O, Nyvad B, Larsen MJ (1994). Human experimental caries models - intra-oral environmental variability. Adv Dent Res 8:134-143.
28. Gianoulis TA, Raes J, Patel PV, Bjornson R, Korbelc JO, Letunic I, et al. (2009). Quantifying environmental adaptation of metabolic pathways in metagenomics. Proc Natl Acad Sci USA 106:1374-1379.
29. Haffajee AD, Teles RP, Patel MR, Song X, Yaskell T, Socransky SS (2009). Factors affecting human supragingival biofilm composition. II. Tooth position. J Periodontal Res 44:520-528.
30. Hamada S, Slade HD (1980). Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol Rev 44:331-384. (Pubitemid 11128312)
31. Hamilton IR (1976). Intracellular polysaccharide synthesis by cariogenic microorganisms. In: Microbial aspects of dental caries: workshop proceedings (Spec suppl, Microbiology Abstracts). Stiles HM, Loesche WJ, O'Brien TC, editors. Washington, DC, USA: Information Retrieval Inc, Vol. 3, pp.683-701.
32. Hamilton IR, Ellwood DC (1983). Carbohydrate metabolism by Actinomyces viscosus growing in continuous culture. Infect Immun 42:19-26. (Pubitemid 13012429)
33. Haukioja A, Söderling E, Tenovuo J (2008). Acid production from sugars and sugar alcohols by probiotic lactobacilli and bifidobacteria in vitro. Caries Res 42:449-453.
34. Hojo S, Komatsu M, Okuda R, Takahashi N, Yamada T (1994). Acid profiles and pH of carious dentin in active and arrested lesions. J Dent Res 73:1853-1857.
35. Holt JG, editor (1984). Bergey's manual of systematic bacteriology. Baltimore, MD: Williams & Wilkins.
36. Homer KA, Roberts G, Byers HL, Tarelli E, Whiley RA, Beighton D, et al. (2001). Mannosidase production by viridans group streptococci. J Clin Microbiol 39:995-1001. (Pubitemid 32209712)
37. Horiuchi M, Washio J, Mayanagi H, Takahashi N (2009). Transient acid-impairment of growth ability of oral Streptococcus, Actinomyces, and Lactobacillus: a possible ecological determinant in dental plaque. Oral Microbiol Immunol 24:319-324.
38. Johnson JL, Moore LV, Kaneko B, Moore WE (1990). Actinomyces georgiae sp. nov., Actinomyces gerencseriae sp. nov., designation of two genospecies of Actinomyces naeslundii, and inclusion of A. naeslundii serotypes II and III and Actinomyces viscosus serotype II in A. naeslundii genospecies 2. Int J Syst Bacteriol 40:273-286. (Pubitemid 20216937)
39. Jordan HV, Hammond BF (1972). Filamentous bacteria isolated from human root surface caries. Arch Oral Biol 17:1333-1342.
40. Kawamura Y, Hou XG, Sultana F, Miura H, Ezaki T (1995). Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus. Int J Syst Bacteriol 45:406-408.
41. 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 13:108-125.
42. Kleinberg I, Jenkins GN (1964). The pH of dental plaques in the different areas of the mouth before and after meals and their relationship to the pH and rate of flow of resting saliva. Arch Oral Biol 9:493-516.
43. Klinke T, Kneist S, de Soet JJ, Kuhlisch E, Mauersberger S, Forster A, et al. (2009). Acid production by oral strains of Candida albicans and lactobacilli. Caries Res 43:83-91.
44. Komiyama K, Khandelwal RL, Heinrich SE (1988). Glycogen synthetic and degradative activities by Actinomyces viscosus and Actinomyces naeslundii of root surface caries and noncaries sites. Caries Res 22:217-225.
45. Li J, Helmerhorst EJ, Leone CW, Troxler RF, Yaskell T, Haffajee AD, et al. (2004). Identification of early microbial colonizers in human dental biofilm. J Appl Microbiol 97:1311-1318. (Pubitemid 39573955)
46. Liu Y, Tao H, Zhang J, Zhou X (2006). Characterization of the Actinomyces naeslundii ureolysis and its role in bacterial acidurity and capacity to modulate pH homeostasis. Microbiol Res 161:304-310. (Pubitemid 44740278)
47. Loesche WJ (1986). Role of Streptococcus mutans in human dental decay. Microbiol Rev 50:353-380.
48. Loesche WJ, Eklund S, Earnest R, Burt B (1984). Longitudinal investigation of bacteriology of human fissure decay: epidemiological studies on molars shortly after eruption. Infect Immun 46:765-772. (Pubitemid 15211081)
49. Ma Y, Curran TM, Marquis RE (1997). Rapid procedure for acid adaptation of oral lactic-acid bacteria and further characterization of the response. Can J Microbiol 43:143-148. (Pubitemid 27119773)
50. Manji F, Fejerskov O, Nagelkerke NJ, Baelum V (1991). A random effects model for some epidemiological features of dental caries. Community Dent Oral Epidemiol 19:324-328.
51. Mantzourani M, Gilbert SC, Sulong HN, Sheehy EC, Tank S, Fenlon M, et al. (2009a). The isolation of Bifidobacteria from occlusal carious lesions in children and adults. Caries Res 43:308-313.
52. Mantzourani M, Fenlon M, Beighton D (2009b). Association between Bifidobacteriaceae and the clinical severity of root caries lesions. Oral Microbiol Immunol 24:32-37.
53. Marsh PD (1994). Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res 8:263-271.
54. Marsh PD, Martin VM (1999). Dental plaque. In:Oral microbiology . 4th ed. Marsh PD, Martin VM, editors. Oxford: Wright, pp. 58-81.
55. Marsh PD, Nyvad B (2008). The oral microflora and biofilms on teeth. In:Dental caries: the disease and its clinical management . 2nd ed. Fejerskov O, Kidd EAM, editors. Oxford, UK: Blackwell Munksgaard, pp. 163-187.
56. Martin FE, Nadkarni MA, Jacques NA, Hunter N (2002). Quantitative microbiological study of human carious dentine by culture and realtime PCR: association of anaerobes with histopathological changes in chronic pulpitis. J Clin Microbiol 40:1698-1704. (Pubitemid 34493143)
57. Milnes AR (1996). Description and epidemiology of nursing caries. J Public Health Dent 56:38-50.
58. Milnes AR, Bowden GH (1985). The microflora associated with developing lesions of nursing caries. Caries Res 19:289-297. (Pubitemid 15058594)
59. Munson MA, Banerjee A, Watson TF, Wade WG (2004). Molecular analysis of the microflora associated with dental caries. J Clin Microbiol 42:3023-3029. (Pubitemid 38938052)
60. Nakajo K, Takahashi N, Beighton D (2010). Resistance to acidic environments by the caries-associated bacteria: Bifidobacterium dentium and Bifidobacterium longum. Caries Res (in press).
61. Nunn ME, Braunstein NS, Krall Kaye EA, Dietrich T, Garcia RI, Henshaw MM (2009). Healthy eating index is a predictor of early childhood caries. J Dent Res 88:361-366.
62. Nyvad B (1993). Microbial colonization of human tooth surfaces. APMIS 32(Suppl):1-45.
63. Nyvad B, Fejerskov O (1990). An ultrastructural study of bacterial invasion and tissue break-down in human experimental root surface caries. J Dent Res 69:1118-1125.
64. Nyvad B, Kilian M (1987). Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand J Dent Res 95:369-380.
65. Nyvad B, Kilian M (1990). Comparison of the initial streptococcal microflora on dental enamel in caries-active and caries-inactive individuals. Caries Res 24:267-272.
66. Nyvad B, Machiulskiene V, Baelum V (1999). Reliability of a new caries diagnostic system differentiating between active and inactive caries lesions. Caries Res 33:252-260.
67. Nyvad B, Machiulskiene V, Baelum V (2003). Construct and predictive validity of caries diagnostic criteria assessing lesion activity. J Dent Res 82:117-122. (Pubitemid 41764122)
68. Paddick JS, Brailsford SR, Kidd EA, Beighton D (2005). Phenotypic and genotypic selection of microbiota surviving under dental restorations. Appl Environ Microbiol 71:2467-2472. (Pubitemid 40646990)
69. Plutzer K, Spencer AJ (2008). Efficacy of an oral health promotion intervention in the prevention of early childhood caries. Community Dent Oral Epidemiol 36:335-346.
70. Preza D, Olsen I, Willumsen T, Boches SK, Cotton SL, Grinde B, et al. (2009). Microarray analysis of the microflora of root caries in elderly. Eur J Clin Microbial Infect Dis 28:509-517.
71. Quivey RG Jr, Kuhnert WL, Hahn K (2000). Adaptation of oral streptococci to low pH. Adv Microb Physiol 42:239-274. (Pubitemid 30465953)
72. Rosebury T (1962). Microorganisms indigenous to man. New York, USA: McGraw-Hill.
73. Ruby J, Goldner M (2007). Nature of symbiosis in oral disease. J Dent Res 86:8-11.
74. Samaranayake LP, Hughes A, Weetman DA, MacFarlane TW (1986). Growth and acid production of Candida species in human saliva supplemented with glucose. J Oral Pathol 15:251-254.
75. Sansone C, van Houte J, Joshipura K, Kent R, Margolis HC (1993). The association of mutans streptococci and non-mutans streptococci capable of acidogenesis at a low pH with dental caries on enamel and root surfaces. J Dent Res 72:508-516.
76. Schaal KP (1984). Genus Actinomyces. In: Bergey's manual of systematic bacteriology. Holt JG, editor. Baltimore, MD: Williams & Wilkins, pp. 1383-1418.
77. Stanier R, Doudoroff M, Adelberg E (1970). The microbial world. 3rd ed. Englewood Cliffs, NJ: Prentice-Hall.
78. Sumney DL, Jordan HV (1974). Characterization of bacteria isolated from human root surface carious lesions. J Dent Res 53:343-351.
79. Svensäter G, Larsson UB, Greif EC, Cvitkovitch DG, Hamilton IR (1997). Acid tolerance response and survival by oral bacteria. Oral Microbiol Immunol 12:266-273. (Pubitemid 27409005)
80. Syed SA, Loesche WJ (1978). Bacteriology of human experimental gingivitis: effect of plaque age. Infect Immun 21:821-829. (Pubitemid 9011178)
81. Takahashi N, Nyvad B (2008). Caries ecology revisited: microbial dynamics and the caries process. Caries Res 42:409-418.
82. Takahashi N, Yamada T (1996). Catabolic pathway for aerobic degradation of lactate by Actinomyces naeslundii. Oral Microbiol Immunol 11:193-198. (Pubitemid 26369969)
83. Takahashi N, Yamada T (1999a). Acid-induced acidogenicity and acid tolerance of non-mutans streptococci. Oral Microbiol Immunol 14:43-48. (Pubitemid 29042967)
84. Takahashi N, Yamada T (1999b). Glucose and lactate metabolism by Actinomyces naeslundii. Crit Rev Oral Biol Med 10:487-503.
85. Takahashi N, Iwami Y, Yamada T (1991). Metabolism of intracellular polysaccharide in the cells of Streptococcus mutans under strictly anaerobic conditions. Oral Microbiol Immunol 6:299-304.
86. Takahashi N, Kalfas S, Yamada T (1995). Phosphorylating enzymes involved in glucose fermentation of Actinomyces naeslundii. J Bacteriol 177:5806-5811.
87. Takahashi N, Horiuchi M, Yamada T (1997). Effects of acidification on growth and glycolysis of Streptococcus sanguis and Streptococcus mutans. Oral Microbiol Immunol 12:72-76. (Pubitemid 27324331)
88. Takahashi N, Washio J, Mayanagi G (2010). Metabolomics of supragingival plaque and oral bacteria. J Dent Res (in press).
89. Tanzer JM, Livingston J, Thompson AM (2001). The microbiology of primary dental caries in humans. J Dent Educ 65:1028-1037.
90. Thenisch NL, Bachmann LM, Imfeld T, Leisebach Minder T, Steurer J (2006). Are mutans streptococci detected in preschool children a reliable predictive factor for dental caries risk? A systematic review. Caries Res 40:366-374. (Pubitemid 44329044)
91. Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, et al. (2005). Comparative metagenomics of microbial communities. Science 308:554-557. (Pubitemid 40570586)
92. van Palenstein Helderman WH (1981). Longitudinal microbial changes in developing human supragingival and subgingival plaque. Arch Oral Biol 26:7-12.
93. van Houte J (1994). Role of micro-organisms in caries etiology. J Dent Res 73:672-681.
94. van Houte J, de Moor CE, Jansen HM (1970). Synthesis of iodophilic polysaccharide by human oral streptococci. Arch Oral Biol 15:263-266.
95. van Houte J, Gibbs G, Butera C (1982). Oral flora of children with "nursing bottle caries". J Dent Res 61:382-285.
96. van Houte J, Sansone C, Joshipura K, Kent R (1991a). In vitro acidogenic potential and mutans streptococci of human smooth-surface plaque associated with initial caries lesions and sound enamel. J Dent Res 70:1497-1502.
97. van Houte J, Sansone C, Joshipura K, Kent R (1991b). Mutans streptococci and non-mutans streptococci acidogenic at low pH, and in vitro acidogenic potential of dental plaque in two different areas of the human dentition. J Dent Res 70:1503-1507.
98. van Houte J, Lopman J, Kent R (1996). The final pH of bacteria comprising the predominant flora on sound and carious human root and enamel surfaces. J Dent Res 75:1008-1014. (Pubitemid 32763588)
99. van Ruyven FO, Lingström P, van Houte J, Kent R (2000). Relationship among mutans streptococci, "low-pH" bacteria, and iodophilic polysaccharide- producing bacteria in dental plaque and early enamel caries in humans. J Dent Res 79:778-784.
100. Whiley RA, Beighton D (1998). Current classification of the oral streptococci. Oral Microbiol Immunol 13:195-216. (Pubitemid 28348826)
101. Ximénez-Fyvie LA, Haffajee AD, Socransky SS (2000). Microbial composition of supra- and subgingival plaque in subjects with adult periodontitis. J Clin Periodontol 27:722-732.
102. Zijnge V, van Leeuwen MBM, Degener JE, Abbas F, Thurnheer T, Gmür R, et al. (2010). Oral biofilm architecture on natural teeth. PLoS ONE 5:e9321.