Oral microbial communities in children, caregivers, and associations with salivary biomeasures and environmental tobacco smoke exposure

Author:

Rothman Jason A.12ORCID,Riis Jenna L.23,Hamilton Katrina R.24,Blair Clancy56,Granger Douglas A.278910,Whiteson Katrine L.12ORCID

Affiliation:

1. Department of Molecular Biology and Biochemistry, University of California , Irvine, California, USA

2. Institute for Interdisciplinary Salivary Bioscience Research, University of California , Irvine, California, USA

3. Department of Psychological Science, University of California , Irvine, California, USA

4. Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine , Baltimore, Maryland, USA

5. Department of Population Health, New York University , New York, New York, USA

6. Department of Applied Psychology, New York University , New York, New York, USA

7. Department of Acute and Chronic Care, Johns Hopkins University School of Nursing , Baltimore, Maryland, USA

8. Department of Pediatrics, Johns Hopkins University School of Medicine , Baltimore, Maryland, USA

9. Salivary Bioscience Laboratory, University of Nebraska , Lincoln, Nebraska, USA

10. Department of Psychology, University of Nebraska , Lincoln, Nebraska, USA

Abstract

ABSTRACTHuman oral microbial communities are diverse, with implications for oral and systemic health. Oral microbial communities change over time; thus, it is important to understand how healthy versus dysbiotic oral microbiomes differ, especially within and between families. There is also a need to understand how the oral microbiome composition is changed within an individual including by factors such as environmental tobacco smoke (ETS) exposure, metabolic regulation, inflammation, and antioxidant potential. Using archived saliva samples collected from caregivers and children during a 90-month follow-up assessment in a longitudinal study of child development in the context of rural poverty, we used 16S rRNA gene sequencing to determine the salivary microbiome. A total of 724 saliva samples were available, 448 of which were from caregiver/child dyads, an additional 70 from children and 206 from adults. We compared children’s and caregivers’ oral microbiomes, performed “stomatotype” analyses, and examined microbial relations with concentrations of salivary markers associated with ETS exposure, metabolic regulation, inflammation, and antioxidant potential (i.e., salivary cotinine, adiponectin, C-reactive protein, and uric acid) assayed from the same biospecimens. Our results indicate that children and caregivers share much of their oral microbiome diversity, but there are distinct differences. Microbiomes from intrafamily individuals are more similar than microbiomes from nonfamily individuals, with child/caregiver dyad explaining 52% of overall microbial variation. Notably, children harbor fewer potential pathogens than caregivers, and participants’ microbiomes clustered into two groups, with major differences being driven byStreptococcusspp. Differences in salivary microbiome composition associated with ETS exposure, and taxa associated with salivary analytes representing potential associations between antioxidant potential, metabolic regulation, and the oral microbiome.IMPORTANCEThe human oral cavity is a multi-environment habitat that harbors a diversity of microorganisms. This oral microbiome is often transmitted between cohabitating individuals, which may associate oral and systemic health within family members. Furthermore, family social ecology plays a significant role in childhood development, which may be associated with lifelong health outcomes. In this study, we collected saliva from children and their caregivers and used 16S rRNA gene sequencing to characterize their oral microbiomes. We also analyzed salivary biomeasures of environmental tobacco smoke exposure, metabolic regulation, inflammation, and antioxidant potential. We show there are differences in individuals’ oral microbiomes mainly due toStreptococcusspp. that family members share much of their microbes, and several bacterial taxa associate with the selected salivary biomeasures. Our results suggest there are large-scale oral microbiome patterns, and there are likely relationships between oral microbiomes and the social ecology of families.

Funder

HHS | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development

HHS | National Institutes of Health

George E. Hewitt Foundation for Medical Research

Publisher

American Society for Microbiology

Subject

Computer Science Applications,Genetics,Molecular Biology,Modeling and Simulation,Ecology, Evolution, Behavior and Systematics,Biochemistry,Physiology,Microbiology

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