Evaluating the Ecological Hypothesis: Early Life Salivary Microbiome Assembly Predicts Dental Caries in a Longitudinal Case-Control Study

Details

• Personal Author:
  Bakulski KM ; Bhaumik D ; Blostein F ; Davis E ; Duhaime M ; Foxman B ; Marazita ML ; McNeil DW ; Salzman E ; Shedden K
• Description:
  Background: Early childhood caries (ECC)-dental caries (cavities) occurring in primary teeth up to age 6 years-is a prevalent childhood oral disease with a microbial etiology. Streptococcus mutans was previously considered a primary cause, but recent research promotes the ecologic hypothesis, in which a dysbiosis in the oral microbial community leads to caries. In this incident, density sampled case-control study of 189 children followed from 2 months to 5 years, we use the salivary bacteriome to (1) prospectively test the ecological hypothesis of ECC in salivary bacteriome communities and (2) identify co-occurring salivary bacterial communities predicting future ECC. Results: Supervised classification of future ECC case status using salivary samples from age 12 months using bacteriome-wide data (AUC-ROC 0.78 95% CI (0.71-0.85)) predicts future ECC status before S. mutans can be detected. Dirichlet multinomial community state typing and co-occurrence network analysis identified similar robust and replicable groups of co-occurring taxa. Mean relative abundance of a Haemophilus parainfluenzae/Neisseria/Fusobacterium periodonticum group was lower in future ECC cases (0.14) than controls (0.23, P value < 0.001) in pre-incident visits, positively correlated with saliva pH (Pearson rho = 0.33, P value < 0.001) and reduced in individuals who had acquired S. mutans by the next study visit (0.13) versus those who did not (0.20, P value < 0.01). In a subset of whole genome shotgun sequenced samples (n = 30), case plaque had higher abundances of antibiotic production and resistance gene orthologs, including a major facilitator superfamily multidrug resistance transporter (MFS DHA2 family PBH value = 1.9 × 10-28), lantibiotic transport system permease protein (PBH value = 6.0 × 10-6) and bacitracin synthase I (PBH value = 5.6 × 10-6). The oxidative phosphorylation KEGG pathway was enriched in case plaque (PBH value = 1.2 × 10-8), while the ABC transporter pathway was depleted (PBH value = 3.6 × 10-3). Conclusions: Early-life bacterial interactions predisposed children to ECC, supporting a time-dependent interpretation of the ecological hypothesis. Bacterial communities which assemble before 12 months of age can promote or inhibit an ecological succession to S. mutans dominance and cariogenesis. Intragenera competitions and intergenera cooperation between oral taxa may shape the emergence of these communities, providing points for preventive interventions. [Description provided by NIOSH]
• Subjects:
  Dental Offices Epidemiology Occupational Health Safety
• Keywords:
  16S RRNA Gene Author Keywords: Oral Microbiome Bacterial Cultures Case Control Studies Children Dental Health Dentistry Early Childhood Early Childhood Caries Ecological Hypothesis Ecological Systems Genomics Longitudinal Study Whole Genome Shotgun Metagenomics

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• ISSN:
  2049-2618
• Document Type:
  Text
• Funding:
  Grant
• Genre:
  Journal Article
• Place as Subject:
  Michigan ; OSHA Region 3 ; OSHA Region 5 ; Pennsylvania ; West Virginia
• CIO:
  National Institute for Occupational Safety and Health (NIOSH)
• Topic:
  Workplace Safety & Health
• Location:
  North America
• Volume:
  10
• NIOSHTIC Number:
  nn:20070608
• Citation:
  Microbiome 2022 Dec; 10:240
• Contact Point Address:
  Betsy Foxman, Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA
• Email:
  bfoxman@umich.edu
• Federal Fiscal Year:
  2023
• Performing Organization:
  University of Michigan, Ann Arbor
• Peer Reviewed:
  True
• Start Date:
  20050701
• Source Full Name:
  Microbiome
• End Date:
  20280630
• Collection(s):
  National Institute for Occupational Safety and Health
• Main Document Checksum:
  urn:sha-512:02fcb1290d06fe35bb2115b67c371a4367a3fbb48244eba41ff4193e47eb0888c3d592e55b4af587d587a9a4d7031549f71cf51f89be02c299835f7e02c08e27
• Download URL:
  https://stacks.cdc.gov/view/cdc/208787/cdc_208787_DS1.pdf
• File Type:
  [PDF - 3.66 MB ]