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The human microbiota is associated with cardiometabolic risk across the epidemiologic transition

Oral and fecal microbial biomarkers have previously been associated with cardiometabolic (CM) risk, however, no comprehensive attempt has been made to explore this association in minority populations or across different geographic regions. We characterized gut- and oral-associated microbiota and CM...

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Autores principales: Fei, Na, Bernabé, Beatriz Peñalver, Lie, Louise, Baghdan, Danny, Bedu-Addo, Kweku, Plange-Rhule, Jacob, Forrester, Terrence E., Lambert, Estelle V., Bovet, Pascal, Gottel, Neil, Riesen, Walter, Korte, Wolfgang, Luke, Amy, Kliethermes, Stephanie A., Layden, Brian T., Gilbert, Jack A., Dugas, Lara R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6656343/
https://www.ncbi.nlm.nih.gov/pubmed/31339887
http://dx.doi.org/10.1371/journal.pone.0215262
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author Fei, Na
Bernabé, Beatriz Peñalver
Lie, Louise
Baghdan, Danny
Bedu-Addo, Kweku
Plange-Rhule, Jacob
Forrester, Terrence E.
Lambert, Estelle V.
Bovet, Pascal
Gottel, Neil
Riesen, Walter
Korte, Wolfgang
Luke, Amy
Kliethermes, Stephanie A.
Layden, Brian T.
Gilbert, Jack A.
Dugas, Lara R.
author_facet Fei, Na
Bernabé, Beatriz Peñalver
Lie, Louise
Baghdan, Danny
Bedu-Addo, Kweku
Plange-Rhule, Jacob
Forrester, Terrence E.
Lambert, Estelle V.
Bovet, Pascal
Gottel, Neil
Riesen, Walter
Korte, Wolfgang
Luke, Amy
Kliethermes, Stephanie A.
Layden, Brian T.
Gilbert, Jack A.
Dugas, Lara R.
author_sort Fei, Na
collection PubMed
description Oral and fecal microbial biomarkers have previously been associated with cardiometabolic (CM) risk, however, no comprehensive attempt has been made to explore this association in minority populations or across different geographic regions. We characterized gut- and oral-associated microbiota and CM risk in 655 participants of African-origin, aged 25–45, from Ghana, South Africa, Jamaica, and the United States (US). CM risk was classified using the CM risk cut-points for elevated waist circumference, elevated blood pressure and elevated fasted blood glucose, low high-density lipoprotein (HDL), and elevated triglycerides. Gut-associated bacterial alpha diversity negatively correlated with elevated blood pressure and elevated fasted blood glucose. Similarly, gut bacterial beta diversity was also significantly differentiated by waist circumference, blood pressure, triglyceridemia and HDL-cholesterolemia. Notably, differences in inter- and intra-personal gut microbial diversity were geographic-region specific. Participants meeting the cut-points for 3 out of the 5 CM risk factors were significantly more enriched with Lachnospiraceae, and were significantly depleted of Clostridiaceae, Peptostreptococcaceae, and Prevotella. The predicted relative proportions of the genes involved in the pathways for lipopolysaccharides (LPS) and butyrate synthesis were also significantly differentiated by the CM risk phenotype, whereby genes involved in the butyrate synthesis via lysine, glutarate and 4-aminobutyrate/succinate pathways and LPS synthesis pathway were enriched in participants with greater CM risk. Furthermore, inter-individual oral microbiota diversity was also significantly associated with the CM risk factors, and oral-associated Streptococcus, Prevotella, and Veillonella were enriched in participants with 3 out of the 5 CM risk factors. We demonstrate that in a diverse cohort of African-origin adults, CM risk is significantly associated with reduced microbial diversity, and the enrichment of specific bacterial taxa and predicted functional traits in both gut and oral environments. As well as providing new insights into the associations between the gut and oral microbiota and CM risk, this study also highlights the potential for novel therapeutic discoveries which target the oral and gut microbiota in CM risk.
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spelling pubmed-66563432019-08-07 The human microbiota is associated with cardiometabolic risk across the epidemiologic transition Fei, Na Bernabé, Beatriz Peñalver Lie, Louise Baghdan, Danny Bedu-Addo, Kweku Plange-Rhule, Jacob Forrester, Terrence E. Lambert, Estelle V. Bovet, Pascal Gottel, Neil Riesen, Walter Korte, Wolfgang Luke, Amy Kliethermes, Stephanie A. Layden, Brian T. Gilbert, Jack A. Dugas, Lara R. PLoS One Research Article Oral and fecal microbial biomarkers have previously been associated with cardiometabolic (CM) risk, however, no comprehensive attempt has been made to explore this association in minority populations or across different geographic regions. We characterized gut- and oral-associated microbiota and CM risk in 655 participants of African-origin, aged 25–45, from Ghana, South Africa, Jamaica, and the United States (US). CM risk was classified using the CM risk cut-points for elevated waist circumference, elevated blood pressure and elevated fasted blood glucose, low high-density lipoprotein (HDL), and elevated triglycerides. Gut-associated bacterial alpha diversity negatively correlated with elevated blood pressure and elevated fasted blood glucose. Similarly, gut bacterial beta diversity was also significantly differentiated by waist circumference, blood pressure, triglyceridemia and HDL-cholesterolemia. Notably, differences in inter- and intra-personal gut microbial diversity were geographic-region specific. Participants meeting the cut-points for 3 out of the 5 CM risk factors were significantly more enriched with Lachnospiraceae, and were significantly depleted of Clostridiaceae, Peptostreptococcaceae, and Prevotella. The predicted relative proportions of the genes involved in the pathways for lipopolysaccharides (LPS) and butyrate synthesis were also significantly differentiated by the CM risk phenotype, whereby genes involved in the butyrate synthesis via lysine, glutarate and 4-aminobutyrate/succinate pathways and LPS synthesis pathway were enriched in participants with greater CM risk. Furthermore, inter-individual oral microbiota diversity was also significantly associated with the CM risk factors, and oral-associated Streptococcus, Prevotella, and Veillonella were enriched in participants with 3 out of the 5 CM risk factors. We demonstrate that in a diverse cohort of African-origin adults, CM risk is significantly associated with reduced microbial diversity, and the enrichment of specific bacterial taxa and predicted functional traits in both gut and oral environments. As well as providing new insights into the associations between the gut and oral microbiota and CM risk, this study also highlights the potential for novel therapeutic discoveries which target the oral and gut microbiota in CM risk. Public Library of Science 2019-07-24 /pmc/articles/PMC6656343/ /pubmed/31339887 http://dx.doi.org/10.1371/journal.pone.0215262 Text en © 2019 Fei et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Fei, Na
Bernabé, Beatriz Peñalver
Lie, Louise
Baghdan, Danny
Bedu-Addo, Kweku
Plange-Rhule, Jacob
Forrester, Terrence E.
Lambert, Estelle V.
Bovet, Pascal
Gottel, Neil
Riesen, Walter
Korte, Wolfgang
Luke, Amy
Kliethermes, Stephanie A.
Layden, Brian T.
Gilbert, Jack A.
Dugas, Lara R.
The human microbiota is associated with cardiometabolic risk across the epidemiologic transition
title The human microbiota is associated with cardiometabolic risk across the epidemiologic transition
title_full The human microbiota is associated with cardiometabolic risk across the epidemiologic transition
title_fullStr The human microbiota is associated with cardiometabolic risk across the epidemiologic transition
title_full_unstemmed The human microbiota is associated with cardiometabolic risk across the epidemiologic transition
title_short The human microbiota is associated with cardiometabolic risk across the epidemiologic transition
title_sort human microbiota is associated with cardiometabolic risk across the epidemiologic transition
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6656343/
https://www.ncbi.nlm.nih.gov/pubmed/31339887
http://dx.doi.org/10.1371/journal.pone.0215262
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