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The Oral Microbiome of Children: Development, Disease, and Implications Beyond Oral Health

  • Human Microbiome
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Abstract

In the era of applied meta-omics and personalized medicine, the oral microbiome is a valuable asset. From biomarker discovery to being a powerful source of therapeutic targets and to presenting an opportunity for developing non-invasive approaches to health care, it has become clear that oral microbes may hold the answer for understanding disease, even beyond the oral cavity. Although our understanding of oral microbiome diversity has come a long way in the past 50 years, there are still many areas that need to be fine-tuned for better risk assessment and diagnosis, especially in early developmental stages of human life. Here, we discuss the factors that impact development of the oral microbiome and explore oral markers of disease, with a focus on the early oral cavity. Our ultimate goal is to put different experimental and methodological views into perspective for better assessment of early oral and systemic disease at an early age and discuss how oral microbiomes—at the community level—could provide improved assessment in individuals and populations at risk.

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References

  1. Miller WD (1892) Die Mikroorganismen der Mundhöhle. DMW-Deutsche Medizinische Wochenschrift 18:1016–1018

    Article  Google Scholar 

  2. Kligler IJ, Gies WJ (1915) A biochemical study and differentiation of oral bacteria with special reference to dental caries. J Allied Dental Soc 10:445–458

  3. Dewhirst FE, Chen T, Izard J et al (2010) The human oral microbiome. J Bacteriol 192:5002–5017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Nasidze I, Li J, Quinque D et al (2009) Global diversity in the human salivary microbiome. Genome Res 19:636–643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. 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 60:677–690

    Article  CAS  PubMed  Google Scholar 

  6. Bik EM, Long CD, Armitage GC et al (2010) Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J 4:962–974

    Article  PubMed  PubMed Central  Google Scholar 

  7. Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214

    Article  CAS  Google Scholar 

  8. Zaura E, Keijser BJF, Huse SM, Crielaard W (2009) Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol 9:1–12

    Article  CAS  Google Scholar 

  9. Keijser BJF, Zaura E, Huse SM et al (2008) Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 87:1016–1020

    Article  CAS  PubMed  Google Scholar 

  10. Becker MR, Paster BJ, Leys EJ et al (2002) Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 40:1001–1009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Zarco MF, Vess TJ, Ginsburg GS (2012) The oral microbiome in health and disease and the potential impact on personalized dental medicine. Oral Dis 18:109–120

    Article  CAS  PubMed  Google Scholar 

  12. Wade WG (2013) The oral microbiome in health and disease. Pharmacol Res 69:137–143

    Article  CAS  PubMed  Google Scholar 

  13. Costalonga M, Herzberg MC (2014) The oral microbiome and the immunobiology of periodontal disease and caries. Immunol Lett 162:22–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Paster BJ, Olsen I, Aas JA, Dewhirst FE (2006) The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol 42:80–87

    Article  Google Scholar 

  15. Dominguez-Bello MG, Costello EK, Contreras M et al (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 107:11971–11975

    Article  PubMed  PubMed Central  Google Scholar 

  16. Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP (2002) Possible association between amniotic fluid micro-organism infection and microflora in the mouth. BJOG 109:527–533

    Article  PubMed  Google Scholar 

  17. Fardini Y, Chung P, Dumm R et al (2010) Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection. Infect Immun 78:1789–1796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Aagaard K, Ma J, Antony KM, et al. (2014) The placenta harbors a unique microbiome. Sci Transl Med 6:237ra65.

  19. Goldenberg RL, Hauth JC, Andrews WW (2000) Intrauterine infection and preterm delivery. N Engl J Med 342:1500–1507

    Article  CAS  PubMed  Google Scholar 

  20. Han YW, Redline RW, Li M et al (2004) Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect Immun 72:2272–2279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Han YW, Ikegami A, Bissada NF et al (2006) Transmission of an uncultivated Bergeyella strain from the oral cavity to amniotic fluid in a case of preterm birth. J Clin Microbiol 44:1475–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Han YW, Shen T, Chung P et al (2009) Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J Clin Microbiol 47:38–47

    Article  PubMed  CAS  Google Scholar 

  23. Lif Holgerson P, Harnevik L, Hernell O et al (2011) Mode of birth delivery affects oral microbiota in infants. J Dent Res 90:1183–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kliman HJ (2014) Comment on “The placenta harbors a unique microbiome.” Sci Transl Med 6:254le4–254le4.

  25. Costello EK, Stagaman K, Dethlefsen L et al (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336:1255–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Isolauri E (2012) Development of healthy gut microbiota early in life. J Paediatr Child Health 48(Suppl 3):1–6

    Article  PubMed  Google Scholar 

  27. Munyaka PM, Khafipour E, Ghia J-E (2014) External influence of early childhood establishment of gut microbiota and subsequent health implications. Front Pediatr 2:109

    Article  PubMed  PubMed Central  Google Scholar 

  28. Hegde S, Munshi AK (1998) Influence of the maternal vaginal microbiota on the oral microbiota of the newborn. J Clin Pediatr Dent 22:317–321

    CAS  PubMed  Google Scholar 

  29. Merglova V, Polenik P (2016) Early colonization of the oral cavity in 6- and 12-month-old infants by cariogenic and periodontal pathogens: a case-control study. Folia Microbiol . doi:10.1007/s12223-016-0453-z

  30. Wan AK, Seow WK, Purdie DM et al (2001) Oral colonization of Streptococcus mutans in six-month-old predentate infants. J Dent Res 80:2060–2065

    Article  CAS  PubMed  Google Scholar 

  31. Carlsson J, Grahnén H, Jonsson G, Wikner S (1970) Early establishment of Streptococcus salivarius in the mouths of infants. J Dent Res 49:415–418

    Article  CAS  PubMed  Google Scholar 

  32. Cole MF, Evans M, Fitzsimmons S et al (1994) Pioneer oral streptococci produce immunoglobulin A1 protease. Infect Immun 62:2165–2168

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Hanson LA, Söderström T (1981) Human milk: defense against infection. Prog Clin Biol Res 61:147–159

    CAS  PubMed  Google Scholar 

  34. Lif Holgerson P, Öhman C, Rönnlund A, Johansson I (2015) Maturation of oral microbiota in children with or without dental caries. PLoS One 10:e0128534

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Cephas KD, Kim J, Mathai RA et al (2011) Comparative analysis of salivary bacterial microbiome diversity in edentulous infants and their mothers or primary care givers using pyrosequencing. PLoS One 6:e23503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Ward TL, Hosid S, Ioshikhes I, Altosaar I (2013) Human milk metagenome: a functional capacity analysis. BMC Microbiol 13:116

    Article  PubMed  PubMed Central  Google Scholar 

  37. Martín R, Langa S, Reviriego C et al (2003) Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr 143:754–758

    Article  PubMed  Google Scholar 

  38. Jost T, Lacroix C, Braegger C, Chassard C (2013) Assessment of bacterial diversity in breast milk using culture-dependent and culture-independent approaches. Br J Nutr 110:1253–1262

    Article  CAS  PubMed  Google Scholar 

  39. Yang F, Zeng X, Ning K et al (2012) Saliva microbiomes distinguish caries-active from healthy human populations. ISME J 6:1–10

    Article  PubMed  CAS  Google Scholar 

  40. Struzycka I (2014) The oral microbiome in dental caries. Pol J Microbiol 63:127–135

    PubMed  Google Scholar 

  41. Rôças IN, Alves FRF, Rachid CTCC et al (2016) Microbiome of deep dentinal caries lesions in teeth with symptomatic irreversible pulpitis. PLoS One 11:e0154653

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Crielaard W, Zaura E, Schuller AA et al (2011) Exploring the oral microbiota of children at various developmental stages of their dentition in the relation to their oral health. BMC Med Genomics 4:22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Goodrich JK, Waters JL, Poole AC et al (2014) Human genetics shape the gut microbiome. Cell 159:789–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Goodrich JK, Davenport ER, Beaumont M et al (2016) Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19:731–743

    Article  CAS  PubMed  Google Scholar 

  45. Blekhman R, Goodrich JK, Huang K et al (2015) Host genetic variation impacts microbiome composition across human body sites. Genome Biol 16:191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Stahringer SS, Clemente JC, Corley RP et al (2012) Nurture trumps nature in a longitudinal survey of salivary bacterial communities in twins from early adolescence to early adulthood. Genome Res 22:2146–2152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Papapostolou A, Kroffke B, Tatakis DN et al (2011) Contribution of host genotype to the composition of health-associated supragingival and subgingival microbiomes. J Clin Periodontol 38:517–524

    Article  PubMed  Google Scholar 

  48. Corby PM, Bretz WA, Hart TC et al (2007) Heritability of oral microbial species in caries-active and caries-free twins. Twin Res Hum Genet 10:821–828

    Article  PubMed  PubMed Central  Google Scholar 

  49. Corby PMA, Bretz WA, Hart TC et al (2005) Mutans streptococci in preschool twins. Arch Oral Biol 50:347–351

    Article  CAS  PubMed  Google Scholar 

  50. Acton RT, Dasanayake AP, Harrison RA et al (1999) Associations of MHC genes with levels of caries-inducing organisms and caries severity in African-American women. Hum Immunol 60:984–989

    Article  CAS  PubMed  Google Scholar 

  51. Ozawa Y, Chiba J, Sakamoto S (2001) HLA class II alleles and salivary numbers of mutans streptococci and lactobacilli among young adults in Japan. Oral Microbiol Immunol 16:353–357

    Article  CAS  PubMed  Google Scholar 

  52. Gizani S, Papaioannou W, Haffajee AD et al (2009) Distribution of selected cariogenic bacteria in five different intra-oral habitats in young children. Int J Paediatr Dent 19:193–200

    Article  PubMed  Google Scholar 

  53. Kianoush N, Nguyen K-AT, Browne GV, et al. (2014) pH gradient and distribution of streptococci, lactobacilli, prevotellae, and fusobacteria in carious dentine. Clin Oral Investig 18:659–669.

  54. Takahashi N, Nyvad B (2011) The role of bacteria in the caries process: ecological perspectives. J Dent Res 90:294–303

    Article  CAS  PubMed  Google Scholar 

  55. Burne RA, Marquis RE (2000) Alkali production by oral bacteria and protection against dental caries. FEMS Microbiol Lett 193:1–6

    Article  CAS  PubMed  Google Scholar 

  56. Avila WM, Pordeus IA, Paiva SM, Martins CC (2015) Breast and bottle feeding as risk factors for dental caries: a systematic review and meta-analysis. PLoS One 10:e0142922

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Holgerson PL, Vestman NR, Claesson R et al (2013) Oral microbial profile discriminates breast-fed from formula-fed infants. J Pediatr Gastroenterol Nutr 56:127–136

    Article  PubMed  PubMed Central  Google Scholar 

  58. Iida H, Auinger P, Billings RJ, Weitzman M (2007) Association between infant breastfeeding and early childhood caries in the United States. Pediatrics 120:e944–52.

  59. Alaluusua S, Mättö J, Grönroos L et al (1996) Oral colonization by more than one clonal type of mutans streptococcus in children with nursing-bottle dental caries. Arch Oral Biol 41:167–173

    Article  CAS  PubMed  Google Scholar 

  60. Burt BA, Eklund SA, Morgan KJ et al (1988) The effects of sugars intake and frequency of ingestion on dental caries increment in a three-year longitudinal study. J Dent Res 67:1422–1429

    Article  CAS  PubMed  Google Scholar 

  61. Naidu R, Nunn J, Kelly A (2013) Socio-behavioural factors and early childhood caries: a cross-sectional study of preschool children in central Trinidad. BMC Oral Health 13:30

    Article  PubMed  PubMed Central  Google Scholar 

  62. Kanasi E, Dewhirst FE, Chalmers NI et al (2010) Clonal analysis of the microbiota of severe early childhood caries. Caries Res 44:485–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Harris R, Nicoll AD, Adair PM, Pine CM (2004) Risk factors for dental caries in young children: a systematic review of the literature. Community Dent Health 21:71–85

    PubMed  Google Scholar 

  64. Edlund A, Yang Y, Yooseph S et al (2015) Meta-omics uncover temporal regulation of pathways across oral microbiome genera during in vitro sugar metabolism. ISME J 9:2605–2619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. McLean JS (2014) Advancements toward a systems level understanding of the human oral microbiome. Front Cell Infect Microbiol 4:98

    PubMed  PubMed Central  Google Scholar 

  66. Leme AFP, Koo H, Bellato CM et al (2006) The role of sucrose in cariogenic dental biofilm formation—new insight. J Dent Res 85:878–887

    Article  CAS  PubMed Central  Google Scholar 

  67. Krzyściak W, Jurczak A, Kościelniak D et al (2014) The virulence of Streptococcus mutans and the ability to form biofilms. Eur J Clin Microbiol Infect Dis 33:499–515

    Article  PubMed  Google Scholar 

  68. Nobre dos Santos M, Melo dos Santos L, Francisco SB, Cury JA (2002) Relationship among dental plaque composition, daily sugar exposure and caries in the primary dentition. Caries Res 36:347–352

    Article  CAS  PubMed  Google Scholar 

  69. Mattos-Graner RO, Smith DJ, King WF, Mayer MP (2000) Water-insoluble glucan synthesis by mutans streptococcal strains correlates with caries incidence in 12- to 30-month-old children. J Dent Res 79:1371–1377

    Article  CAS  PubMed  Google Scholar 

  70. Stephan RM, Miller BF (1943) A quantitative method for evaluating physical and chemical agents which modify production of acids in bacterial plaques on human teeth. J Dent Res 22:45–51

    Article  Google Scholar 

  71. Marsh PD (1994) Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res 8:263–271

    Article  CAS  PubMed  Google Scholar 

  72. Marsh PD (2016) Dental biofilms in health and disease. In: Goldberg M (ed) Understanding Dental Caries. Springer International Publishing, pp 41–52

  73. Matsui R, Cvitkovitch D (2010) Acid tolerance mechanisms utilized by Streptococcus mutans. Future Microbiol 5:403–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Forssten SD, Björklund M, Ouwehand AC (2010) Streptococcus mutans, caries and simulation models. Nutrients 2:290–298

    Article  PubMed  PubMed Central  Google Scholar 

  75. Marsh PD (2003) Are dental diseases examples of ecological catastrophes? Microbiology 149:279–294

    Article  CAS  PubMed  Google Scholar 

  76. Bradshaw DJ, McKee AS, Marsh PD (1989) Effects of carbohydrate pulses and pH on population shifts within oral microbial communities in vitro. J Dent Res 68:1298–1302

    Article  CAS  PubMed  Google Scholar 

  77. Bradshaw D, Marsh PD (1998) Analysis of pH-driven disruption of oral microbial communities in vitro. Caries Res 32:456–462

    Article  CAS  PubMed  Google Scholar 

  78. Jiang W, Zhang J, Chen H (2013) Pyrosequencing analysis of oral microbiota in children with severe early childhood dental caries. Curr Microbiol 67:537–542

    Article  CAS  PubMed  Google Scholar 

  79. Tanner ACR, Kent RL Jr, Holgerson PL et al (2011) Microbiota of severe early childhood caries before and after therapy. J Dent Res 90:1298–1305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Gross EL, Leys EJ, Gasparovich SR et al (2010) Bacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol 48:4121–4128

    Article  PubMed  PubMed Central  Google Scholar 

  81. Xu H, Hao W, Zhou Q et al (2014) Plaque bacterial microbiome diversity in children younger than 30 months with or without caries prior to eruption of second primary molars. PLoS One 9:e89269

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. 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 46:1407–1417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Divaris K (2015) Predicting dental caries outcomes in children: a “risky” concept. J Dent Res. doi:10.1177/0022034515620779

  84. Li Y, Ge Y, Saxena D, Caufield PW (2007) Genetic profiling of the oral microbiota associated with severe early-childhood caries. J Clin Microbiol 45:81–87

    Article  CAS  PubMed  Google Scholar 

  85. Luo AH, Yang DQ, Xin BC et al (2012) Microbial profiles in saliva from children with and without caries in mixed dentition. Oral Dis 18:595–601

    Article  CAS  PubMed  Google Scholar 

  86. Theilade E (1986) The non-specific theory in microbial etiology of inflammatory periodontal diseases. J Clin Periodontol 13:905–911

    Article  CAS  PubMed  Google Scholar 

  87. Morou-Bermudez E, Rodriguez S, Bello AS, Dominguez-Bello MG (2015) Urease and dental plaque microbial profiles in children. PLoS One 10:e0139315

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Morou-Bermudez E, Elias-Boneta A, Billings RJ et al (2011) Urease activity in dental plaque and saliva of children during a three-year study period and its relationship with other caries risk factors. Arch Oral Biol 56:1282–1289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Morou-Bermudez E, Elias-Boneta A, Billings RJ et al (2011) Urease activity as a risk factor for caries development in children during a three-year study period: a survival analysis approach. Arch Oral Biol 56:1560–1568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Fidalgo TKS, Freitas-Fernandes LB, Angeli R et al (2012) Salivary metabolite signatures of children with and without dental caries lesions. Metabolomics 9:657–666

    Article  CAS  Google Scholar 

  91. Fidalgo TKS, Freitas-Fernandes LB, Almeida FCL et al (2014) Longitudinal evaluation of salivary profile from children with dental caries before and after treatment. Metabolomics 11:583–593

    Article  CAS  Google Scholar 

  92. McLean JS, Fansler SJ, Majors PD et al (2012) Identifying low pH active and lactate-utilizing taxa within oral microbiome communities from healthy children using stable isotope probing techniques. PLoS One 7:e32219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Takahashi N, Washio J, Mayanagi G (2012) Metabolomic approach to oral biofilm characterization—a future direction of biofilm research. J Oral Biosci 54:138–143

    Article  CAS  Google Scholar 

  94. Foxman B, Srinivasan U, Wen A et al (2014) Exploring the effect of dentition, dental decay and familiality on oral health using metabolomics. Infect Genet Evol 22:201–207

    Article  CAS  PubMed  Google Scholar 

  95. Belda-Ferre P, Williamson J, Simón-Soro Á et al (2015) The human oral metaproteome reveals potential biomarkers for caries disease. Proteomics 15:3497–3507

    Article  CAS  PubMed  Google Scholar 

  96. Simón-Soro A, Tomás I, Cabrera-Rubio R et al (2013) Microbial geography of the oral cavity. J Dent Res 92:616–621

    Article  PubMed  Google Scholar 

  97. Sato Y, Yamagishi J, Yamashita R et al (2015) Inter-individual differences in the oral bacteriome are greater than intra-day fluctuations in individuals. PLoS One 10:e0131607

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Simón-Soro A, Guillen-Navarro M, Mira A (2014) Metatranscriptomics reveals overall active bacterial composition in caries lesions. J Oral Microbiol 6:25443

    Article  PubMed  CAS  Google Scholar 

  99. Shi W, Qin M, Chen F, Xia B (2016) Supragingival microbial profiles of permanent and deciduous teeth in children with mixed dentition. PLoS One 11:e0146938

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Afroughi S, Faghihzadeh S, Khaledi MJ, Motlagh MG (2010/5) Dental caries analysis in 3–5 years old children: a spatial modelling. Arch Oral Biol 55:374–378.

  101. Teng F, Yang F, Huang S et al (2015) Prediction of early childhood caries via spatial-temporal variations of oral microbiota. Cell Host Microbe 18:296–306

    Article  CAS  PubMed  Google Scholar 

  102. Li X, Kolltveit KM, Tronstad L, Olsen I (2000) Systemic diseases caused by oral infection. Clin Microbiol Rev 13:547–558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Beck JD, Slade G, Offenbacher S (2000) Oral disease, cardiovascular disease and systemic inflammation. Periodontol 23:110–120

    Article  CAS  Google Scholar 

  104. Seymour GJ, Ford PJ, Cullinan MP et al (2007) Relationship between periodontal infections and systemic disease. Clin Microbiol Infect 13(Suppl 4):3–10

    Article  CAS  PubMed  Google Scholar 

  105. Iacopino AM, Cutler CW (2000) Pathophysiological relationships between periodontitis and systemic disease: recent concepts involving serum lipids. J Periodontol 71:1375–1384

    Article  CAS  PubMed  Google Scholar 

  106. Shen H, Ye F, Xie L et al (2015) Metagenomic sequencing of bile from gallstone patients to identify different microbial community patterns and novel biliary bacteria. Sci Rep 5:17450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Slots J, Rams TE (1991) New views on periodontal microbiota in special patient categories. J Clin Periodontol 18:411–420

    Article  CAS  PubMed  Google Scholar 

  108. Tanaka S, Murakami Y, Seto K et al (2003) The detection of Porphyromonas gingivalis, Prevotella intermedia, and Actinobacillus actinomycetemcomitans in the supragingival plaque of children with and without caries. Pediatr Dent 25:143–148

    PubMed  Google Scholar 

  109. Merchant AT (2012) Periodontitis and dental caries occur together. J Evid Based Dent Pract 12:18–19

    Article  PubMed  Google Scholar 

  110. Lange L, Thiele GM, McCracken C et al (2016) Symptoms of periodontitis and antibody responses to Porphyromonas gingivalis in juvenile idiopathic arthritis. Pediatr Rheumatol Online J 14:8

    Article  PubMed  PubMed Central  Google Scholar 

  111. Francavilla R, Ercolini D, Piccolo M et al (2014) Salivary microbiota and metabolome associated with celiac disease. Appl Environ Microbiol 80:3416–3425

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Di Cagno R, De Angelis M, De Pasquale I et al (2011) Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization. BMC Microbiol 11:219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. Docktor MJ, Paster BJ, Abramowicz S et al (2012) Alterations in diversity of the oral microbiome in pediatric inflammatory bowel disease. Inflamm Bowel Dis 18:935–942

    Article  PubMed  Google Scholar 

  114. Hicks MJ, Carter AB, Rossmann SN et al (1998) Detection of fungal organisms in saliva from HIV-infected children: a preliminary cytologic analysis. Pediatr Dent 20:162–168

    CAS  PubMed  Google Scholar 

  115. Roberts GJ, Holzel HS, Sury MR et al (1997) Dental bacteremia in children. Pediatr Cardiol 18:24–27

    Article  CAS  PubMed  Google Scholar 

  116. Joshipura K, Ritchie C, Douglass C (2000) Strength of evidence linking oral conditions and systemic disease. Compend Contin Educ Dent Suppl 12–23; quiz 65.

  117. 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 9:11–21

    Article  PubMed  PubMed Central  Google Scholar 

  118. Gao S, Li S, Ma Z et al (2016) Presence of Porphyromonas gingivalis in esophagus and its association with the clinicopathological characteristics and survival in patients with esophageal cancer. Infect Agent Cancer 11:3

    Article  PubMed  PubMed Central  Google Scholar 

  119. Nakajima M, Arimatsu K, Kato T et al (2015) Oral administration of P. gingivalis induces dysbiosis of gut microbiota and impaired barrier function leading to dissemination of enterobacteria to the liver. PLoS One 10:e0134234

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Ibrahim R, Pasic M, Yousef GM (2016) Omics for personalized medicine: defining the current we swim in. Expert Rev Mol Diagn 16(7):719–722

  121. Lee JY, Divaris K (2014) The ethical imperative of addressing oral health disparities: a unifying framework. J Dent Res 93:224–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Mougeot J-LC, Stevens CB, Cotton SL, et al. (2016) Concordance of HOMIM and HOMI N GS technologies in the microbiome analysis of clinical samples. J Oral Microbiol. doi:10.3402/jom.v8.30379

  123. Duran-Pinedo AE, Frias-Lopez J (2015) Beyond microbial community composition: functional activities of the oral microbiome in health and disease. Microbes Infect 17:505–516

    Article  PubMed  PubMed Central  Google Scholar 

  124. Wong DTW (2012) Salivaomics. J Am Dent Assoc 143:19S–24S.

  125. Vayssier-Taussat M, Albina E, Citti C et al (2014) Shifting the paradigm from pathogens to pathobiome: new concepts in the light of meta-omics. Front Cell Infect Microbiol 4:29

    Article  PubMed  PubMed Central  Google Scholar 

  126. Hart TC, Corby PM, Hauskrecht M, et al. (2011) Identification of microbial and proteomic biomarkers in early childhood caries. Int J Dent 2011:196721

  127. Gehlenborg N, O’Donoghue SI, Baliga NS et al (2010) Visualization of omics data for systems biology. Nat Methods 7:S56–S68

    Article  CAS  PubMed  Google Scholar 

  128. Dimitrov DV, Hoeng J (2013) Systems approaches to computational modeling of the oral microbiome. Front Physiol 4:172

    Article  PubMed  PubMed Central  Google Scholar 

  129. Bartel J, Krumsiek J, Schramm K et al (2015) The human blood metabolome-transcriptome interface. PLoS Genet 11:e1005274

    Article  PubMed  PubMed Central  Google Scholar 

  130. Ferreira Zandoná A, Ando M, Gomez GF, et al. (2013) Longitudinal analyses of early lesions by fluorescence: an observational study. J Dent Res 92:84S–9S.

  131. Härkäne T, Larmas MA, Virtanen JI, Arjas E (2002) Applying modern survival analysis methods to longitudinal dental caries studies. J Dent Res 81:144–148

    Article  PubMed  Google Scholar 

  132. Nasidze I, Li J, Schroeder R et al (2011) High diversity of the saliva microbiome in Batwa Pygmies. PLoS One 6:e23352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Hamady M, Knight R (2009) Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res 19:1141–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Nunes AP, Oliveira IO, Santos BR et al (2012) Quality of DNA extracted from saliva samples collected with the Oragene\texttrademark DNA self-collection kit. BMC Med Res Methodol 12:1–6

    Article  CAS  Google Scholar 

  135. Rogers NL, Cole SA, Lan H-C et al (2007) New saliva DNA collection method compared to buccal cell collection techniques for epidemiological studies. Am J Hum Biol 19:319–326

    Article  PubMed  PubMed Central  Google Scholar 

  136. Ng DPK, Koh D, Choo SGL et al (2004) Effect of storage conditions on the extraction of PCR-quality genomic DNA from saliva. Clin Chim Acta 343:191–194

    Article  CAS  PubMed  Google Scholar 

  137. Quinque D, Kittler R, Kayser M et al (2006) Evaluation of saliva as a source of human DNA for population and association studies. Anal Biochem 353:272–277

    Article  CAS  PubMed  Google Scholar 

  138. Ahn J, Yang L, Paster BJ et al (2011) Oral microbiome profiles: 16S rRNA pyrosequencing and microarray assay comparison. PLoS One 6:e22788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Chen T, Yu W-H, Izard J, et al. (2010) The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database 2010:baq013.

  140. Griffen AL, Beall CJ, Firestone ND et al (2011) CORE: a phylogenetically-curated 16S rDNA database of the core oral microbiome. PLoS One 6:e19051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

Research supported in this publication was supported by the National Institute of Dental and Craniofacial Research of the National Institutes of Health under Award Number R01DE019665. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Correspondence to Andres Gomez.

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Gomez, A., Nelson, K.E. The Oral Microbiome of Children: Development, Disease, and Implications Beyond Oral Health. Microb Ecol 73, 492–503 (2017). https://doi.org/10.1007/s00248-016-0854-1

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