Folia Microbiologica

, Volume 60, Issue 1, pp 69–80 | Cite as

The oral microbiome diversity and its relation to human diseases

  • Jinzhi He
  • Yan Li
  • Yangpei Cao
  • Jin Xue
  • Xuedong Zhou
Article

Abstract

As one of the most clinically relevant human habitats, the human mouth is colonized by a set of microorganisms, including bacteria, archaea, fungi, and viruses. Increasing evidence has supported that these microbiota contribute to the two commonest oral diseases of man (dental caries and periodontal diseases), presenting significant risk factors to human health conditions, such as tumor, diabetes mellitus, cardiovascular diseases, bacteremia, preterm birth, and low birth weight in infants. It is widely accepted that oral microorganisms cause diseases mainly by a synergistic or cooperative way, and the interspecies interactions within the oral community play a crucial role in determining whether oral microbiota elicit diseases or not. Since a comprehensive understanding of the complex interspecies interactions within a community needs the knowledge of its endogenous residents, a plenty of research have been carried out to explore the oral microbial diversity. In this review, we focus on the recent progress in this field, including the oral microbiome composition and its association with human diseases.

References

  1. Aas JA, Paster BJ, Stokes LN et al (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721–5732PubMedCentralPubMedGoogle Scholar
  2. Aas JA, Griffen AL, Dardis SR et al (2008) Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol 46:1407–1417PubMedCentralPubMedGoogle Scholar
  3. Ahn J, Chen C, Hayes R (2012) Oral microbiome and oral and gastrointestinal cancer risk. Cancer Causes Control 23:399–404PubMedCentralPubMedGoogle Scholar
  4. Alberti KGMM, Zimmet PZ (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Diabet Med 15:539–553PubMedGoogle Scholar
  5. Allaker RP, Waite RD, Hickling J et al (2008) Topographic distribution of bacteria associated with oral malodour on the tongue. Arch Oral Biol 53(Supplement 1):8–12Google Scholar
  6. Allavena P, Garlanda C, Borrello MG et al (2008) Pathways connecting inflammation and cancer. Curr Opin Genet Dev 18:3–11PubMedGoogle Scholar
  7. Alves FRF, Siqueira JF Jr, Carmo FL et al (2009) Bacterial community profiling of cryogenically ground samples from the apical and coronal root segments of teeth with apical periodontitis. J Endod 35:486–492PubMedGoogle Scholar
  8. Bäckhed F, Ley RE, Sonnenburg JL et al (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920PubMedGoogle Scholar
  9. Bagan J, Sarrion G, Jimenez Y (2010) Oral cancer: clinical features. Oral Oncol 46:414–417PubMedGoogle Scholar
  10. Bahrani-Mougeot FK, Paster BJ, Coleman S et al (2008) Diverse and novel oral bacterial species in blood following dental procedures. J Clin Microbiol 46:2129–2132PubMedCentralPubMedGoogle Scholar
  11. Balakrishnan M, Simmonds RS, Tagg JR (2000) Dental caries is a preventable infectious disease. Aust Dent J 45:235–245PubMedGoogle Scholar
  12. Baumgartner JC, Watkins BJ, Bae KS et al (1999) Association of black-pigmented bacteria with endodontic infections. J Endod 25:413–415PubMedGoogle Scholar
  13. Becker MR, Paster BJ, Leys EJ et al (2002) Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 40:1001–1009PubMedCentralPubMedGoogle Scholar
  14. Belda-Ferre P, Alcaraz LD, Cabrera-Rubio R et al (2012) The oral metagenome in health and disease. ISME J 6:46–56PubMedCentralPubMedGoogle Scholar
  15. Bik EM, Long CD, Armitage GC et al (2010) Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J 4:962–974PubMedCentralPubMedGoogle Scholar
  16. Brogden KM, Guthmiller JM (2008) Polymicrobial diseases. ASM, WashingtonGoogle Scholar
  17. Byström A, Happonen R-P, Sjögren U et al (1987) Healing of periapical lesions of pulpless teeth after endodontic treatment with controlled asepsis. Dent Traumatol 3:58–63Google Scholar
  18. Campus G, Salem A, Uzzau S et al (2005) Diabetes and periodontal disease: a case–control study. J Periodontol 76:418–425PubMedGoogle Scholar
  19. Canabarro A, Valle C, Farias MR et al (2013) Association of subgingival colonization of Candida albicans and other yeasts with severity of chronic periodontitis. J Periodontal Res 48:428–432PubMedGoogle Scholar
  20. Cannon RD, Holmes AR, Mason AB et al (1995) Oral candida: clearance, colonization, or Candidiasis? J Dent Res 74:1152–1161PubMedGoogle Scholar
  21. Casarin RCV, Barbagallo A, Meulman T et al (2013) Subgingival biodiversity in subjects with uncontrolled type-2 diabetes and chronic periodontitis. J Periodontal Res 48:30–36PubMedGoogle Scholar
  22. Chiu B (1999) Multiple infections in carotid atherosclerotic plaques. Am Heart J 138:534–536Google Scholar
  23. Chugal N, Wang J, Wang R et al (2011) Molecular characterization of the microbial flora residing at the apical portion of infected root canals of human teeth. J Endod 37:1359–1364PubMedCentralPubMedGoogle Scholar
  24. Colombo APV, Boches SK, Cotton SL et al (2009) Comparisons of subgingival microbial profiles of refractory periodontitis, severe periodontitis, and periodontal health using the Human Oral Microbe Identification Microarray. J Periodontol 80:1421–1432PubMedCentralPubMedGoogle Scholar
  25. Colombo AP, Bennet S, Cotton SL et al (2012) Impact of periodontal therapy on the subgingival microbiota of severe periodontitis: comparison between good responders and individuals with refractory periodontitis using the human oral microbe identification microarray. J Periodontol 83:1279–1287PubMedCentralPubMedGoogle Scholar
  26. Contreras A, Falkler WA, Enwonwu CO et al (1997) Human Herpesviridae in acute necrotizing ulcerative gingivitis in children in Nigeria. Oral Microbiol Immunol 12:259–265PubMedGoogle Scholar
  27. Contreras A, Umeda M, Chen C et al (1999) Relationship between herpesviruses and adult periodontitis and periodontopathic bacteria. J Periodontol 70:478–484PubMedGoogle Scholar
  28. Contreras A, Mardirossian A, Slots J (2001) Herpesviruses in HIV-periodontitis. J Clin Periodontol 28:96–102PubMedGoogle Scholar
  29. Cooper GM (1992) Elements of human cancer. Jones and Bartlett, BostonGoogle Scholar
  30. Dahlén G, Leonhardt Å (2006) A new checkerboard panel for testing bacterial markers in periodontal disease. Oral Microbiol Immunol 21:6–11PubMedGoogle Scholar
  31. Darveau RP (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Micro 8:481–490Google Scholar
  32. Delima SL, McBride RK, Preshaw PM et al (2010) Response of subgingival bacteria to smoking cessation. J Clin Microbiol 48:2344–2349PubMedCentralPubMedGoogle Scholar
  33. Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human–microbe mutualism and disease. Nature 449:811–818PubMedGoogle Scholar
  34. Dewhirst FE, Chen T, Izard J et al (2010) The human oral microbiome. J Bacteriol 192:5002–5017PubMedCentralPubMedGoogle Scholar
  35. Docktor MJ, Paster BJ, Abramowicz S et al (2012) Alterations in diversity of the oral microbiome in pediatric inflammatory bowel disease. Inflamm Bowel Dis 18:935–942PubMedCentralPubMedGoogle Scholar
  36. Dridi B, Raoult D, Drancourt M (2011) Archaea as emerging organisms in complex human microbiomes. Anaerobe 17:56–63PubMedGoogle Scholar
  37. Drury TF, Horowitz AM, Ismail AI et al (1999) Diagnosing and reporting early childhood caries for research purposes: a report of a workshop sponsored by the National Institute of Dental and Craniofacial Research, the Health Resources and Services Administration, and the Health Care Financing Administration. J Public Health Dent 59:192–197PubMedGoogle Scholar
  38. Ebersole JL, Holt SC, Hansard R et al (2008) Microbiologic and immunologic characteristics of periodontal disease in Hispanic Americans with type 2 diabetes. J Periodontol 79:637–646PubMedGoogle Scholar
  39. Eckburg PB, Lepp PW, Relman DA (2003) Archaea and their potential role in human disease. Infect Immun 71:591–596PubMedCentralPubMedGoogle Scholar
  40. Fábián TK, Fejérdy P, Csermely P (2008) Salivary genomics, transcriptomics and proteomics: the emerging concept of the oral ecosystem and their use in the early diagnosis of cancer and other diseases. Curr Genomics 9:11–21PubMedCentralPubMedGoogle Scholar
  41. Fabricious L, Dahlen G, ÖHman AE et al (1982) Predominant indigenous oral bacteria isolated from infected root canals after varied times of closure. Eur J Oral Sci 90:134–144Google Scholar
  42. Farrell JJ, Zhang L, Zhou H et al (2011) Variations of oral microbiota are associated with pancreatic diseases including pancreatic cancer. Gut 61:582–588PubMedCentralPubMedGoogle Scholar
  43. Faveri M, Mayer MPA, Feres M et al (2008) Microbiological diversity of generalized aggressive periodontitis by 16S rRNA clonal analysis. Oral Microbiol Immunol 23:112–118PubMedGoogle Scholar
  44. Faveri M, Gonçalves LFH, Feres M et al (2011) Prevalence and microbiological diversity of Archaea in peri-implantitis subjects by 16S ribosomal RNA clonal analysis. J Periodontal Res 46:338–344PubMedGoogle Scholar
  45. Figuero E, Sánchez-Beltrán M, Cuesta-Frechoso S et al (2011) Detection of periodontal bacteria in atheromatous plaque by nested polymerase chain reaction. J Periodontol 82:1469–1477PubMedGoogle Scholar
  46. Filoche S, Wong L, Sissons CH (2010) Oral biofilms: emerging concepts in microbial ecology. J Dent Res 89:8–18PubMedGoogle Scholar
  47. Ford PJ, Gemmell E, Hamlet SM et al (2005) Cross-reactivity of GroEL antibodies with human heat shock protein 60 and quantification of pathogens in atherosclerosis. Oral Microbiol Immunol 20:296–302PubMedGoogle Scholar
  48. Forner L, Larsen T, Kilian M et al (2006) Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontol 33:401–407PubMedGoogle Scholar
  49. Gersdorf H, Pelz K, Göbel UB (1993) Fluorescence in situ hybridization for direct visualization of Gram-negative anaerobes in subgingival plaque samples. FEMS Immunol Med Microbiol 6:109–114PubMedGoogle Scholar
  50. Ghannoum MA, Jurevic RJ, Mukherjee PK et al (2010) Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 6:e1000713PubMedCentralPubMedGoogle Scholar
  51. Gill SR, Pop M, DeBoy RT et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359PubMedCentralPubMedGoogle Scholar
  52. Gomes BPFA, Drucker DB, Lilley JD (1994) Association of specific bacteria with some endodontic signs and symptoms. Int Endod J 27:291–298PubMedGoogle Scholar
  53. Goodson JM, Groppo D, Halem S et al (2009) Is obesity an oral bacterial disease? J Dent Res 88:519–523PubMedCentralPubMedGoogle Scholar
  54. Griffen AL, Beall CJ, Campbell JH et al (2012) Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 6:1176–1185PubMedCentralPubMedGoogle Scholar
  55. Gross EL, Leys EJ, Gasparovich SR et al (2010) Bacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol 48:4121–4128PubMedCentralPubMedGoogle Scholar
  56. Hajishengallis G, Lamont RJ (2012) Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27:409–419PubMedCentralPubMedGoogle Scholar
  57. Han YW, Fardini Y, Chen C et al (2010) Term stillbirth caused by oral Fusobacterium nucleatum. Obstet Gynecol 115:442–445PubMedCentralPubMedGoogle Scholar
  58. Hanookai D, Nowzari H, Contreras A et al (2000) Herpesviruses and periodontopathic bacteria in trisomy 21 periodontitis. J Periodontol 71:376–384PubMedGoogle Scholar
  59. Haraszthy VI, Zambon JJ, Sreenivasan PK et al (2007) Identification of oral bacterial species associated with halitosis. J Am Dent Assoc 138:1113–1120PubMedGoogle Scholar
  60. Haynes M, Rohwer F (2011) The Human virome. In: Nelson KE (ed) Metagenomics of the human body. Springer, New York, pp 63–77Google Scholar
  61. Heijtz RD, Wang S, Anuar F et al (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 108:3047–3052PubMedCentralGoogle Scholar
  62. Herzberg MC, Meyer MW (1996) Effects of oral flora on platelets: possible consequences in cardiovascular disease. J Periodontol 67:1138–1142PubMedGoogle Scholar
  63. Hintao J, Teanpaisan R, Chongsuvivatwong V et al (2007) The microbiological profiles of saliva, supragingival and subgingival plaque and dental caries in adults with and without type 2 diabetes mellitus. Oral Microbiol Immunol 22:175–181PubMedGoogle Scholar
  64. Hooper SJ, Crean SJ, Fardy MJ et al (2007) A molecular analysis of the bacteria present within oral squamous cell carcinoma. J Med Microbiol 56:1651–1659PubMedGoogle Scholar
  65. Hu YJ, Wang Q, Jiang YT et al (2013) Characterization of oral bacterial diversity of irradiated patients by high-throughput sequencing. Int J Oral Sci 5:21–25PubMedCentralPubMedGoogle Scholar
  66. Huang S, Yang F, Zeng X et al (2011) Preliminary characterization of the oral microbiota of Chinese adults with and without gingivitis. BMC Oral Health 11:33PubMedCentralPubMedGoogle Scholar
  67. Imbronito AV, Okuda OS, Maria de Freitas N et al (2008) Detection of herpesviruses and periodontal pathogens in subgingival plaque of patients with chronic periodontitis, generalized aggressive periodontitis, or gingivitis. J Periodontol 79:2313–2321PubMedGoogle Scholar
  68. Jiang YT, Xia WW, Li CL et al (2009) Preliminary study of the presence and association of bacteria and archaea in teeth with apical periodontitis. Int Endod J 42:1096–1103PubMedGoogle Scholar
  69. José FS Jr (2002) Endodontic infections: concepts, paradigms, and perspectives. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 94:281–293Google Scholar
  70. Kanasi E, Dewhirst FE, Chalmers NI et al (2010) Clonal analysis of the microbiota of severe early childhood caries. Caries Res 44:485–497PubMedCentralPubMedGoogle Scholar
  71. Kazor CE, Mitchell PM, Lee AM et al (2003) Diversity of bacterial populations on the tongue dorsa of patients with halitosis and healthy patients. J Clin Microbiol 41:558–563PubMedCentralPubMedGoogle Scholar
  72. Keijser BJF, Zaura E, Huse SM et al (2008) Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 87:1016–1020PubMedGoogle Scholar
  73. 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
  74. Kleinegger CL, Lockhart SR, Vargas K et al (1996) Frequency, intensity, species, and strains of oral Candida vary as a function of host age. J Clin Microbiol 34:2246–2254PubMedCentralPubMedGoogle Scholar
  75. Klinke T, Guggenheim B, Klimm W et al (2011) Dental caries in rats associated with Candida albicans. Caries Res 45:100–106PubMedGoogle Scholar
  76. Kononen E, Wade (2007) Manual of clinical microbiology. ASM, WashingtonGoogle Scholar
  77. Koren O, Spor A, Felin J et al (2011) Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci U S A 108:4592–4598PubMedCentralPubMedGoogle Scholar
  78. Kraneveld EA, Buijs MJ, Bonder MJ et al (2012) The relation between oral Candida load and bacterial microbiome profiles in Dutch older adults. PLoS ONE 7:e42770PubMedCentralPubMedGoogle Scholar
  79. Krishnan PA (2012) Fungal infections of the oral mucosa. Indian J Dent Res 23:650–659PubMedGoogle Scholar
  80. Kubar A, Saygun I, Özdemir A et al (2005) Real-time polymerase chain reaction quantification of human cytomegalovirus and Epstein-Barr virus in periodontal pockets and the adjacent gingiva of periodontitis lesions. J Periodontal Res 40:97–104PubMedGoogle Scholar
  81. Kumar PS, Griffen AL, Barton JA et al (2003) New bacterial species associated with chronic periodontitis. J Dent Res 82:338–344PubMedGoogle Scholar
  82. Kumar PS, Griffen AL, Moeschberger ML et al (2005) Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. J Clin Microbiol 43:3944–3955PubMedCentralPubMedGoogle Scholar
  83. Kumaraswamy KL, Vidhya M (2011) Human papilloma virus and oral infections: an update. J Cancer Res Ther 7:120–127PubMedGoogle Scholar
  84. Lalla E, Kaplan S, Chang SMJ et al (2006) Periodontal infection profiles in type 1 diabetes. J Clin Periodontol 33:855–862PubMedGoogle Scholar
  85. Lazarevic V, Whiteson K, Hernandez D et al (2010) Study of inter- and intra-individual variations in the salivary microbiota. BMC Genomics 11:523PubMedCentralPubMedGoogle Scholar
  86. Lederberg J, McCray AT (2001) ‘Ome sweet’omics—a genealogical treasury of words. Scientist 15:2–8Google Scholar
  87. Lepp PW, Brinig MM, Ouverney CC et al (2004) Methanogenic Archaea and human periodontal disease. Proc Natl Acad Sci U S A 101:6176–6181PubMedCentralPubMedGoogle Scholar
  88. Li M, Wang B, Zhang M et al (2008) Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci U S A 105:2117–2122PubMedCentralPubMedGoogle Scholar
  89. Li CL, Liu DL, Jiang YT et al (2009) Prevalence and molecular diversity of Archaea in subgingival pockets of periodontitis patients. Oral Microbiol Immunol 24:343–346PubMedGoogle Scholar
  90. Libby P, Ridker PM, Maseri A (2002) Inflammation and atherosclerosis. Circulation 105:1135–1143PubMedGoogle Scholar
  91. Lif Holgerson P, Harnevik L, Hernell O et al (2011) Mode of birth delivery affects oral microbiota in infants. J Dent Res 90:1183–1188PubMedCentralPubMedGoogle Scholar
  92. Ling LJ, Ho CC, Wu CY et al (2004) Association between human herpesviruses and the severity of periodontitis. J Periodontol 75:1479–1485PubMedGoogle Scholar
  93. Ling Z, Kong J, Jia P et al (2010) Analysis of oral microbiota in children with dental caries by PCR-DGGE and barcoded pyrosequencing. Microb Ecol 60:677–690PubMedGoogle Scholar
  94. Lira EAG, Ramiro FS, Chiarelli FM et al (2013) Reduction in prevalence of Archaea after periodontal therapy in subjects with generalized aggressive periodontitis. Aust Dent J 58:442–447PubMedGoogle Scholar
  95. Löe H (1993) Periodontal disease: the sixth complication of diabetes mellitus. Diabetes Care 16:329–334PubMedGoogle Scholar
  96. Machado de Oliveira JC, Siqueira JF, Rôças IN et al (2007) Bacterial community profiles of endodontic abscesses from Brazilian and USA subjects as compared by denaturing gradient gel electrophoresis analysis. Oral Microbiol Immunol 22:14–18PubMedGoogle Scholar
  97. Mager DL, Ximenez-Fyvie LA, Haffajee AD et al (2003) Distribution of selected bacterial species on intraoral surfaces. J Clin Periodontol 30:644–654PubMedGoogle Scholar
  98. Mager D, Haffajee A, Devlin P et al (2005) The salivary microbiota as a diagnostic indicator of oral cancer: a descriptive, non-randomized study of cancer-free and oral squamous cell carcinoma subjects. J Transl Med 3:27PubMedCentralPubMedGoogle Scholar
  99. Mansfield JM, Campbell JH, Bhandari AR et al (2012) Molecular analysis of 16S rRNA genes identifies potentially periodontal pathogenic bacteria and Archaea in the plaque of partially erupted third molars. J Oral Maxillofac Surg 70:1507–1514PubMedGoogle Scholar
  100. Marsh PD (2005) Dental plaque: biological significance of a biofilm and community life-style. J Clin Periodontol 32:7–15PubMedGoogle Scholar
  101. Masdea L, Kulik EM, Hauser-Gerspach I et al (2012) Antimicrobial activity of Streptococcus salivarius K12 on bacteria involved in oral malodour. Arch Oral Biol 57:1041–1047PubMedGoogle Scholar
  102. Matarazzo F, Ribeiro AC, Faveri M et al (2012) The domain Archaea in human mucosal surfaces. Clin Microbiol Infect 18:834–840PubMedGoogle Scholar
  103. Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449:819–826PubMedGoogle Scholar
  104. Metwalli KH, Khan SA, Krom BP et al (2013) Streptococcus mutans, Candida albicans, and the human mouth: a sticky situation. PLoS Pathog 9:e1003616PubMedCentralPubMedGoogle Scholar
  105. Meurman JH (2010) Oral microbiota and cancer. J Oral Microbiol. doi:10.3402/jom.v2i0.5195
  106. Mitchell-Lewis D, Engebretson SP, Chen J et al (2001) Periodontal infections and pre-term birth: early findings from a cohort of young minority women in New York. Eur J Oral Sci 109:34–39PubMedGoogle Scholar
  107. Moore LVH, Moore WEC, Cato EP et al (1987) Bacteriology of human gingivitis. J Dent Res 66:989–995PubMedGoogle Scholar
  108. Murata T, Yamaga T, Iida T et al (2002) Classification and examination of halitosis. Int Dent J 52:181–186PubMedGoogle Scholar
  109. Nagy KN, Sonkodi I, Szöke I et al (1998) The microflora associated with human oral carcinomas. Oral Oncol 34:304–308PubMedGoogle Scholar
  110. Napeñas JJ, Brennan MT, Coleman S et al (2010) Molecular methodology to assess the impact of cancer chemotherapy on the oral bacterial flora: a pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 109:554–560PubMedGoogle Scholar
  111. Nasidze I, Li J, Quinque D et al (2009) Global diversity in the human salivary microbiome. Genome Res 19:636–643PubMedCentralPubMedGoogle Scholar
  112. Nguyen-Hieu T, Khelaifia S, Aboudharam G et al (2013) Methanogenic archaea in subgingival sites: a review. APMIS 121:467–477PubMedGoogle Scholar
  113. Noguchi N, Noiri Y, Narimatsu M et al (2005) Identification and localization of extraradicular biofilm-forming bacteria associated with refractory endodontic pathogens. Appl Environ Microbiol 71:8738–8743PubMedCentralPubMedGoogle Scholar
  114. Offenbacher S, Lin D, Strauss R et al (2006) Effects of periodontal therapy during pregnancy on periodontal status, biologic parameters, and pregnancy outcomes: a pilot study. J Periodontol 77:2011–2024PubMedGoogle Scholar
  115. Ohki T, Itabashi Y, Kohno T et al (2012) Detection of periodontal bacteria in thrombi of patients with acute myocardial infarction by polymerase chain reaction. Am Heart J 163:164–167PubMedGoogle Scholar
  116. Ohlrich EJ, Cullinan MP, Leichter JW (2010) Diabetes, periodontitis, and the subgingival microbiota. J Oral Microbiol. doi:10.3402/jom.v2i0.5818
  117. Özok AR, Persoon IF, Huse SM et al (2012) Ecology of the microbiome of the infected root canal system: a comparison between apical and coronal root segments. Int Endod J 45:530–541PubMedGoogle Scholar
  118. Paster BJ, Olsen I, Aas JA et al (2006) The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol 2000(42):80–87Google Scholar
  119. Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366:1809–1820PubMedGoogle Scholar
  120. Porter SR, Scully C (2006) Oral malodour (halitosis). Brit Med J 333:632–635PubMedCentralPubMedGoogle Scholar
  121. Poveda-Roda R, Jimenez Y, Carbonell E et al (2008) Bacteremia originating in the oral cavity. A review. Med Oral Patol Oral Cir Bucal 13:E355–E362PubMedGoogle Scholar
  122. Preza D, Olsen I, Aas JA et al (2008) Bacterial profiles of root caries in elderly patients. J Clin Microbiol 46:2015–2021PubMedCentralPubMedGoogle Scholar
  123. Preza D, Olsen I, Willumsen T et al (2009) Microarray analysis of the microflora of root caries in elderly. Eur J Clin Microbiol Infect Dis 28:509–517PubMedCentralPubMedGoogle Scholar
  124. Pride DT, Salzman J, Haynes M et al (2012) Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J 6:915–926PubMedCentralPubMedGoogle Scholar
  125. Pucar A, Milasin J, Lekovic V et al (2007) Correlation between atherosclerosis and periodontal putative pathogenic bacterial infections in coronary and internal mammary arteries. J Periodontol 78:677–682PubMedGoogle Scholar
  126. Pushalkar S, Mane SP, Ji X et al (2011) Microbial diversity in saliva of oral squamous cell carcinoma. FEMS Immunol Med Microbiol 61:269–277PubMedCentralPubMedGoogle Scholar
  127. Qi QG, Hu T, Zhou XD (2005) Frequency, species and molecular characterization of oral Candida in hosts of different age in China. J Oral Pathol Med 34:352–356PubMedGoogle Scholar
  128. Raghunand N, Gatenby RA, Gillies RJ (2003) Microenvironmental and cellular consequences of altered blood flow in tumours. Br J Radiol 76:11–22Google Scholar
  129. Raja M, Hannan A, Ali K (2010) Association of oral candidal carriage with dental caries in children. Caries Res 44:272–276PubMedGoogle Scholar
  130. Riggio MP, Lennon A, Rolph HJ et al (2008) Molecular identification of bacteria on the tongue dorsum of subjects with and without halitosis. Oral Dis 14:251–258PubMedGoogle Scholar
  131. Roberts GJ (1999) Dentists are innocent! “Everyday” bacteremia is the real culprit: a review and assessment of the evidence that dental surgical procedures are a principal cause of bacterial endocarditis in children. Pediatr Cardiol 20:317–325PubMedGoogle Scholar
  132. Robles-Sikisaka R, Ly M, Boehm T et al (2013) Association between living environment and human oral viral ecology. ISME J 7:1710–1724PubMedCentralPubMedGoogle Scholar
  133. Rôças IN, Siqueira JF (2008) Root canal microbiota of teeth with chronic apical periodontitis. J Clin Microbiol 46:3599–3606PubMedCentralPubMedGoogle Scholar
  134. Rôças IN, Alves FRF, Santos AL et al (2010) Apical root canal microbiota as determined by reverse-capture checkerboard analysis of cryogenically ground root samples from teeth with apical periodontitis. J Endod 36:1617–1621PubMedGoogle Scholar
  135. Ross R (1999) Atherosclerosis— an inflammatory disease. New Engl J Med 340:115–126PubMedGoogle Scholar
  136. Sakamoto M, Umeda M, Ishikawa I et al (2000) Comparison of the oral bacterial flora in saliva from a healthy subject and two periodontitis patients by sequence analysis of 16S rDNA libraries. Microbiol Immunol 44:643–652PubMedGoogle Scholar
  137. Sakamoto M, Rôças IN, Siqueira JF et al (2006) Molecular analysis of bacteria in asymptomatic and symptomatic endodontic infections. Oral Microbiol Immunol 21:112–122PubMedGoogle Scholar
  138. Santos AL, Siqueira JF, Rôças JIN et al (2011) Comparing the bacterial diversity of acute and chronic dental root canal infections. PLoS One 6(11):e28088PubMedCentralPubMedGoogle Scholar
  139. Sardi JCO, Duque C, Camargo GACG et al (2011) Periodontal conditions and prevalence of putative periodontopathogens and Candida spp. in insulin-dependent type 2 diabetic and non-diabetic patients with chronic periodontitis—a pilot study. Arch Oral Biol 56:1098–1105PubMedGoogle Scholar
  140. Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107–133PubMedGoogle Scholar
  141. Saygun I, Şahin S, Özdemir A et al (2002) Detection of human viruses in patients with chronic periodontitis and the relationship between viruses and clinical parameters. J Periodontol 73:1437–1443PubMedGoogle Scholar
  142. Schacher B, Baron F, Roßberg M et al (2007) Aggregatibacter actinomycetemcomitans as indicator for aggressive periodontitis by two analysing strategies. J Clin Periodontol 34:566–573PubMedGoogle Scholar
  143. Selwitz RH, Ismail AI, Pitts NB (2007) Dental caries. Lancet 369:51–59PubMedGoogle Scholar
  144. Seymour GJ, Ford PJ, Cullinan MP et al (2007) Relationship between periodontal infections and systemic disease. Clin Microbiol Infect 13:3–10PubMedGoogle Scholar
  145. Shao ZY, Tang ZS, Yan C et al (2011) Effects of intensity-modulated radiotherapy on human oral microflora. J Radiat Res 52:834–839PubMedGoogle Scholar
  146. Shchipkova AY, Nagaraja HN, Kumar PS (2010) Subgingival microbial profiles of smokers with periodontitis. J Dent Res 89:1247–1253PubMedCentralPubMedGoogle Scholar
  147. Siqueira JFJ (2011) Treatment of endodontic infections. Quintessence, LondonGoogle Scholar
  148. Siqueira JF, Rôças IN (2005) Uncultivated phylotypes and newly named species associated with primary and persistent endodontic infections. J Clin Microbiol 43:3314–3319PubMedCentralPubMedGoogle Scholar
  149. Siqueira JF, Rôças IN (2009a) Community as the unit of pathogenicity: an emerging concept as to the microbial pathogenesis of apical periodontitis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 107:870–878PubMedGoogle Scholar
  150. Siqueira JF, Rôças IN (2009b) Diversity of endodontic microbiota revisited. J Dent Res 88:969–981PubMedGoogle Scholar
  151. Siqueira JF Jr, Rôças IN, Souto R et al (2000) Checkerboard DNA-DNA hybridization analysis of endodontic infections. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 89:744–748PubMedGoogle Scholar
  152. Siqueira JF, Rôças IN, Rosado AS (2004) Investigation of bacterial communities associated with asymptomatic and symptomatic endodontic infections by denaturing gradient gel electrophoresis fingerprinting approach. Oral Microbiol Immunol 19:363–370PubMedGoogle Scholar
  153. Siqueira JF, Rôças IN, Debelian GJ et al (2008) Profiling of root canal bacterial communities associated with chronic apical periodontitis from Brazilian and Norwegian subjects. J Endod 34:1457–1461PubMedGoogle Scholar
  154. Slots J (2010) Human viruses in periodontitis. Periodontol 2000(53):89–110Google Scholar
  155. Slots J, Contreras A (2000) Herpesviruses: a unifying causative factor in periodontitis? Oral Microbiol Immunol 15:277–280PubMedGoogle Scholar
  156. Socransky SS, Haffajee AD, Cugini MA et al (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144PubMedGoogle Scholar
  157. Stingu CS, Eschrich K, Rodloff AC et al (2008) Periodontitis is associated with a loss of colonization by Streptococcus sanguinis. J Med Microbiol 57:495–499PubMedGoogle Scholar
  158. Su L, Gao Y, Yu C et al (2010) Surgical endodontic treatment of refractory periapical periodontitis with extraradicular biofilm. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 110:40–44Google Scholar
  159. Sunde PT, Olsen I, Enersen M et al (2008) Human cytomegalovirus and Epstein–Barr virus in apical and marginal periodontitis: a role in pathology? J Med Virol 80:1007–1011PubMedGoogle Scholar
  160. Takahashi N, Nyvad B (2011) The role of bacteria in the caries process. J Dent Res 90:294–303PubMedGoogle Scholar
  161. Takeshita T, Nakano Y, Kumagai T et al (2008) The ecological proportion of indigenous bacterial populations in saliva is correlated with oral health status. ISME J 3:65–78PubMedGoogle Scholar
  162. Tanner ACR, Kent RL, Holgerson PL et al (2011) Microbiota of severe early childhood caries before and after therapy. J Dent Res 90:1298–1305PubMedCentralPubMedGoogle Scholar
  163. The Human Microbiome Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214Google Scholar
  164. Turnbaugh PJ, Ley RE, Hamady M et al (2007) The Human Microbiome Project. Nature 449:804–810PubMedCentralPubMedGoogle Scholar
  165. Van Hoogmoed CG, Geertsema-doornbusch GI, Teughels W et al (2008) Reduction of periodontal pathogens adhesion by antagonistic strains. Oral Microbiol Immunol 23:43–48PubMedGoogle Scholar
  166. Velazco CH, Coelho C, Salazar F et al (1999) Microbiological features of Papillon-Lefèvre syndrome periodontitis. J Clin Periodontol 26:622–627PubMedGoogle Scholar
  167. Vianna ME, Conrads G, Gomes BPFA et al (2006) Identification and quantification of Archaea involved in primary endodontic infections. J Clin Microbiol 44:1274–1282PubMedCentralPubMedGoogle Scholar
  168. Vianna ME, Holtgraewe S, Seyfarth I et al (2008) Quantitative analysis of three hydrogenotrophic microbial groups, methanogenic Archaea, sulfate-reducing bacteria, and acetogenic bacteria, within plaque biofilms associated with human periodontal diseases. J Bacteriol 190:3779–3785PubMedCentralPubMedGoogle Scholar
  169. Vianna ME, Conrads G, Gomes BPFA et al (2009) T-RFLP-based mcrA gene analysis of methanogenic archaea in association with oral infections and evidence of a novel Methanobrevibacter phylotype. Oral Microbiol Immunol 24:417–422PubMedGoogle Scholar
  170. Vickerman MM, Brossard KA, Funk DB et al (2007) Phylogenetic analysis of bacterial and archaeal species in symptomatic and asymptomatic endodontic infections. J Med Microbiol 56:110–118PubMedGoogle Scholar
  171. Wade WG (2011) Has the use of molecular methods for the characterization of the human oral microbiome changed our understanding of the role of bacteria in the pathogenesis of periodontal disease? J Clin Periodontol 38:7–16PubMedGoogle Scholar
  172. Whitley RJ, Roizman B (2001) Herpes simplex virus infections. Lancet 357:1513–1518PubMedGoogle Scholar
  173. Wilson M (2008) Bacteriology of humans: an ecological perspective. Blackwell, MaldenGoogle Scholar
  174. Xu Y, Teng F, Huang S et al (2014) Changes of saliva microbiota in nasopharyngeal carcinoma patients under chemoradiation therapy. Arch Oral Biol 59:176–186PubMedGoogle Scholar
  175. Yang F, Zeng X, Ning K et al (2011a) Saliva microbiomes distinguish caries-active from healthy human populations. ISME J 6:1–10PubMedCentralPubMedGoogle Scholar
  176. Yang L, Liu Y, Wu H et al (2011b) Current understanding of multispecies biofilms. Int J Oral Sci 3:74–81PubMedCentralPubMedGoogle Scholar
  177. Yang XQ, Zhang Q, Lu LY et al (2012) Genotypic distribution of Candida albicans in dental biofilm of Chinese children associated with severe early childhood caries. Arch Oral Biol 57:1048–1053PubMedGoogle Scholar
  178. Zaura E, Keijser BJ, Huse SM et al (2009) Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol 9:259–271PubMedCentralPubMedGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2014

Authors and Affiliations

  • Jinzhi He
    • 1
    • 2
  • Yan Li
    • 1
  • Yangpei Cao
    • 1
    • 2
  • Jin Xue
    • 1
    • 2
  • Xuedong Zhou
    • 1
    • 2
  1. 1.State Key Laboratory of Oral Diseases, West China Hospital of StomatologySichuan UniversityChengduChina
  2. 2.Department of Endodontics and Operative DentistryWest China Hospital of StomatologyChengduChina

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