Oral Microbiota Development in Early Childhood

Early life determinants of the oral microbiota have not been thoroughly elucidated. We studied the association of birth and early childhood characteristics with oral microbiota composition using 16 S ribosomal RNA (rRNA) gene sequencing in a population-based Swedish cohort of 59 children sampled at 6, 12 and 24 months of age. Repeated-measurement regression models adjusted for potential confounders confirmed and expanded previous knowledge about the profound shift of oral microbiota composition in early life. These alterations included increased alpha diversity, decreased beta diversity and alteration of bacterial composition with changes in relative abundance of 14 of the 20 most common operational taxonomic units (OTUs). We also found that birth characteristics, breastfeeding and antibiotic use were associated with overall phyla distribution and/or with the relative abundance of specific OTUs. Further, we detected a novel link between morning salivary cortisol level, a physiological marker of neuroendocrine activity and stress, and overall phyla distribution as well as with decreased abundance of the most common OTU mapped to the Streptococcaceae family. In conclusion, a major part of the maturation of the oral microbiome occurs during the first two years of life, and this development may be influenced by early life circumstances.

[1]  Yanhuizhi Feng,et al.  Alterations of oral microbiota distinguish children with autism spectrum disorders from healthy controls , 2018, Scientific Reports.

[2]  P. François,et al.  Effects of amoxicillin treatment on the salivary microbiota in children with acute otitis media. , 2013, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[3]  Sarah L. Westcott,et al.  Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform , 2013, Applied and Environmental Microbiology.

[4]  R. Knight,et al.  Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns , 2010, Proceedings of the National Academy of Sciences.

[5]  E. H. Simpson.  Measurement of Diversity , 1949, Nature.

[6]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[7]  Martin J. Blaser,et al.  Antibiotics, birth mode, and diet shape microbiome maturation during early life , 2016, Science Translational Medicine.

[8]  J. Duley,et al.  Deep sequencing of the 16S ribosomal RNA of the neonatal oral microbiome: a comparison of breast-fed and formula-fed infants , 2016, Scientific Reports.

[9]  A. Schuller,et al.  Exploring the oral microbiota of children at various developmental stages of their dentition in the relation to their oral health , 2011, BMC Medical Genomics.

[10]  J. Ludvigsson,et al.  Introduction of complementary foods in Sweden and impact of maternal education on feeding practices , 2016, Public Health Nutrition.

[11]  Patrick F. Sullivan,et al.  LifeGene—a large prospective population-based study of global relevance , 2010, European Journal of Epidemiology.

[12]  J. Clemente,et al.  Human gut microbiome viewed across age and geography , 2012, Nature.

[13]  T. Dinan,et al.  Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders , 2015, Front. Cell. Neurosci..

[14]  Ian Shrier,et al.  Reducing bias through directed acyclic graphs , 2008 .

[15]  I. Johansson,et al.  Maturation of Oral Microbiota in Children with or without Dental Caries , 2015, PloS one.

[16]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[17]  Sunil J Rao,et al.  Regression Modeling Strategies: With Applications to Linear Models, Logistic Regression, and Survival Analysis , 2003 .

[18]  E. Steyerberg,et al.  [Regression modeling strategies]. , 2011, Revista espanola de cardiologia.

[19]  M. André,et al.  The management of infections in children in general practice in Sweden: A repeated 1-week diagnosis-prescribing study in 5 counties in 2000 and 2002 , 2005, Scandinavian journal of infectious diseases.

[20]  Frank E. Harrell,et al.  Regression Modeling Strategies: With Applications to Linear Models, Logistic Regression, and Survival Analysis , 2001 .

[21]  K. Aagaard,et al.  Maturation of the Infant Microbiome Community Structure and Function Across Multiple Body Sites and in Relation to Mode of Delivery , 2017, Nature Medicine.

[22]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[23]  R. Gibbs,et al.  Temporal development of the gut microbiome in early childhood from the TEDDY study , 2018, Nature.

[24]  L. Engstrand,et al.  Impact of lifestyle on the gut microbiota of healthy infants and their mothers—the ALADDIN birth cohort. , 2014, FEMS microbiology ecology.

[25]  G. Shaw,et al.  Maternal pesticide exposure from multiple sources and selected congenital anomalies. , 1999 .

[26]  Ben Nichols,et al.  VSEARCH: a versatile open source tool for metagenomics , 2016, PeerJ.

[27]  M. Jenmalm,et al.  Oral microbiome development during childhood: an ecological succession influenced by postnatal factors and associated with tooth decay , 2018, The ISME Journal.

[28]  K. Kalanetra,et al.  Buccal administration of human colostrum: impact on the oral microbiota of premature infants , 2016, Journal of Perinatology.

[29]  James M. Robins,et al.  Causal diagrams for epidemiologic research. , 1999 .

[30]  Maarten L. Buis.  FMLOGIT: Stata module fitting a fractional multinomial logit model by quasi maximum likelihood , 2008 .

[31]  V. Tillmann,et al.  The Influence of Different Maternal Microbial Communities on the Development of Infant Gut and Oral Microbiota , 2017, Scientific Reports.

[32]  Rudolf P. Rohr,et al.  Including community composition in biodiversity–productivity models , 2014 .

[33]  H. Jentsch,et al.  The effects of stress hormones on growth of selected periodontitis related bacteria. , 2013, Anaerobe.

[34]  C. Genco,et al.  Immune dysregulation mediated by the oral microbiome: potential link to chronic inflammation and atherosclerosis , 2016, Journal of internal medicine.

[35]  G. Kulekci,et al.  Salivary detection of periodontopathic bacteria in periodontally healthy children. , 2008, Anaerobe.

[36]  D. Brandon,et al.  Early-life skin microbiota in hospitalized preterm and full-term infants , 2018, Microbiome.

[37]  Leslie E. Papke,et al.  Econometric Methods for Fractional Response Variables with an Application to 401(K) Plan Participation Rates , 1993 .

[38]  Xuedong Zhou,et al.  Oral cavity contains distinct niches with dynamic microbial communities. , 2015, Environmental microbiology.

[39]  Sasha Matthewman,et al.  Ecological perspectives , 2017 .

[40]  M. B. Gavião,et al.  Associations between oral health-related quality of life and emotional statuses in children and preadolescents. , 2012, Oral diseases.

[41]  Gerhard G. Thallinger,et al.  Wx Scout Fashion Sneaker Splash Navy Women's Keds qAS4tR1wn4 for bawln.com , 2009 .

[42]  I. Johansson,et al.  Mode of Birth Delivery Affects Oral Microbiota in Infants , 2011, Journal of dental research.

[43]  David A. Spratt,et al.  Same Exposure but Two Radically Different Responses to Antibiotics: Resilience of the Salivary Microbiome versus Long-Term Microbial Shifts in Feces , 2015, mBio.

[44]  Carlos Garbisu,et al.  Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient , 2016, Scientific Reports.

[45]  Cindy J. Castelle,et al.  Major New Microbial Groups Expand Diversity and Alter our Understanding of the Tree of Life , 2018, Cell.

[46]  M. Jenmalm,et al.  Oral microbiota maturation during the first 7 years of life in relation to allergy development , 2018, Allergy.

[47]  M. Nitert,et al.  Antibiotic treatment at delivery shapes the initial oral microbiome in neonates , 2017, Scientific Reports.

[48]  Anton Nekrutenko,et al.  Child Weight Gain Trajectories Linked To Oral Microbiota Composition , 2018, Scientific Reports.

[49]  B. McEwen.  Protective and damaging effects of stress mediators. , 1998, The New England journal of medicine.

[50]  B. Nyvad,et al.  The Role of Bacteria in the Caries Process , 2011, Journal of dental research.

[51]  Lie-Min Ruan,et al.  Current Understanding of Gut Microbiota in Mood Disorders: An Update of Human Studies , 2019, Front. Genet..

[52]  P. Pérez-Rodríguez,et al.  Beta-Diversity Modeling and Mapping with LiDAR and Multispectral Sensors in a Semi-Evergreen Tropical Forest , 2019, Forests.

[53]  K. Carlsen,et al.  Morning Salivary Cortisol in Young Children: Reference Values and the Effects of Age, Sex, and Acute Bronchiolitis , 2017, The Journal of pediatrics.

[54]  G. Pershagen,et al.  Limited association between markers of stress during pregnancy and fetal growth in ‘Born into Life’, a new prospective birth cohort , 2018, Acta paediatrica.

[55]  A. Dalpke,et al.  Bacterial biofilm composition in healthy subjects with and without caries experience. , 2019, Journal of oral microbiology.

[56]  C. Huttenhower,et al.  Metagenomic biomarker discovery and explanation , 2011, Genome Biology.

[57]  N. Adler,et al.  Social inequalities in childhood dental caries: the convergent roles of stress, bacteria and disadvantage. , 2010, Social science & medicine.

[58]  Vincent Gau,et al.  Matrix Effects—A Challenge toward Automation of Molecular Analysis , 2010 .

[59]  X. Xiong,et al.  Bidirectional gut-brain-microbiota axis as a potential link between inflammatory bowel disease and ischemic stroke , 2018, Journal of Neuroinflammation.

[60]  X. Liang,et al.  The impacts of delivery mode on infant’s oral microflora , 2018, Scientific Reports.

[61]  S. Pani,et al.  Salivary Cortisol as a Biomarker to Explore the Role of Maternal Stress in Early Childhood Caries , 2013, International journal of dentistry.

[62]  W. Garrett,et al.  Fusobacterium nucleatum — symbiont, opportunist and oncobacterium , 2018, Nature Reviews Microbiology.

[63]  I. Johansson,et al.  Oral Microbial Profile Discriminates Breast-fed From Formula-fed Infants , 2013, Journal of pediatric gastroenterology and nutrition.

[64]  E. Könönen.  Development of oral bacterial flora in young children , 2000, Annals of medicine.

[65]  P. Holzer,et al.  Gut Microbiota and the Neuroendocrine System , 2018, Neurotherapeutics.

[66]  J. Hellman,et al.  Antibiotic consumption among a Swedish cohort of children born in 2006 , 2015, Acta paediatrica.