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

Human 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 underst...

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Autores principales: Rothman, Jason A., Riis, Jenna L., Hamilton, Katrina R., Blair, Clancy, Granger, Douglas A., Whiteson, Katrine L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470043/
https://www.ncbi.nlm.nih.gov/pubmed/37338237
http://dx.doi.org/10.1128/msystems.00036-23
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author Rothman, Jason A.
Riis, Jenna L.
Hamilton, Katrina R.
Blair, Clancy
Granger, Douglas A.
Whiteson, Katrine L.
author_facet Rothman, Jason A.
Riis, Jenna L.
Hamilton, Katrina R.
Blair, Clancy
Granger, Douglas A.
Whiteson, Katrine L.
author_sort Rothman, Jason A.
collection PubMed
description Human 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 by Streptococcus spp. 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. IMPORTANCE: The 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 to Streptococcus spp. 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.
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spelling pubmed-104700432023-09-01 Oral microbial communities in children, caregivers, and associations with salivary biomeasures and environmental tobacco smoke exposure Rothman, Jason A. Riis, Jenna L. Hamilton, Katrina R. Blair, Clancy Granger, Douglas A. Whiteson, Katrine L. mSystems Research Article Human 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 by Streptococcus spp. 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. IMPORTANCE: The 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 to Streptococcus spp. 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. American Society for Microbiology 2023-06-20 /pmc/articles/PMC10470043/ /pubmed/37338237 http://dx.doi.org/10.1128/msystems.00036-23 Text en Copyright © 2023 Rothman et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Rothman, Jason A.
Riis, Jenna L.
Hamilton, Katrina R.
Blair, Clancy
Granger, Douglas A.
Whiteson, Katrine L.
Oral microbial communities in children, caregivers, and associations with salivary biomeasures and environmental tobacco smoke exposure
title Oral microbial communities in children, caregivers, and associations with salivary biomeasures and environmental tobacco smoke exposure
title_full Oral microbial communities in children, caregivers, and associations with salivary biomeasures and environmental tobacco smoke exposure
title_fullStr Oral microbial communities in children, caregivers, and associations with salivary biomeasures and environmental tobacco smoke exposure
title_full_unstemmed Oral microbial communities in children, caregivers, and associations with salivary biomeasures and environmental tobacco smoke exposure
title_short Oral microbial communities in children, caregivers, and associations with salivary biomeasures and environmental tobacco smoke exposure
title_sort oral microbial communities in children, caregivers, and associations with salivary biomeasures and environmental tobacco smoke exposure
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470043/
https://www.ncbi.nlm.nih.gov/pubmed/37338237
http://dx.doi.org/10.1128/msystems.00036-23
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