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Dietary fiber intake, the gut microbiome, and chronic systemic inflammation in a cohort of adult men

BACKGROUND: A higher intake of dietary fiber is associated with a decreased risk of chronic inflammatory diseases such as cardiovascular disease and inflammatory bowel disease. This may function in part due to abrogation of chronic systemic inflammation induced by factors such as dysbiotic gut commu...

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Autores principales: Ma, Wenjie, Nguyen, Long H., Song, Mingyang, Wang, Dong D., Franzosa, Eric A., Cao, Yin, Joshi, Amit, Drew, David A., Mehta, Raaj, Ivey, Kerry L., Strate, Lisa L., Giovannucci, Edward L., Izard, Jacques, Garrett, Wendy, Rimm, Eric B., Huttenhower, Curtis, Chan, Andrew T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8212460/
https://www.ncbi.nlm.nih.gov/pubmed/34140026
http://dx.doi.org/10.1186/s13073-021-00921-y
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author Ma, Wenjie
Nguyen, Long H.
Song, Mingyang
Wang, Dong D.
Franzosa, Eric A.
Cao, Yin
Joshi, Amit
Drew, David A.
Mehta, Raaj
Ivey, Kerry L.
Strate, Lisa L.
Giovannucci, Edward L.
Izard, Jacques
Garrett, Wendy
Rimm, Eric B.
Huttenhower, Curtis
Chan, Andrew T.
author_facet Ma, Wenjie
Nguyen, Long H.
Song, Mingyang
Wang, Dong D.
Franzosa, Eric A.
Cao, Yin
Joshi, Amit
Drew, David A.
Mehta, Raaj
Ivey, Kerry L.
Strate, Lisa L.
Giovannucci, Edward L.
Izard, Jacques
Garrett, Wendy
Rimm, Eric B.
Huttenhower, Curtis
Chan, Andrew T.
author_sort Ma, Wenjie
collection PubMed
description BACKGROUND: A higher intake of dietary fiber is associated with a decreased risk of chronic inflammatory diseases such as cardiovascular disease and inflammatory bowel disease. This may function in part due to abrogation of chronic systemic inflammation induced by factors such as dysbiotic gut communities. Data regarding the detailed influences of long-term and recent intake of differing dietary fiber sources on the human gut microbiome are lacking. METHODS: In a cohort of 307 generally healthy men, we examined gut microbiomes, profiled by shotgun metagenomic and metatranscriptomic sequencing, and long-term and recent dietary fiber intake in relation to plasma levels of C-reactive protein (CRP), an established biomarker for chronic inflammation. Data were analyzed using multivariate linear mixed models. RESULTS: We found that inflammation-associated gut microbial configurations corresponded with higher CRP levels. A greater intake of dietary fiber was associated with shifts in gut microbiome composition, particularly Clostridiales, and their potential for carbohydrate utilization via polysaccharide degradation. This was particularly true for fruit fiber sources (i.e., pectin). Most striking, fiber intake was associated with significantly greater CRP reduction in individuals without substantial Prevotella copri carriage in the gut, whereas those with P. copri carriage maintained stable CRP levels regardless of fiber intake. CONCLUSIONS: Our findings offer human evidence supporting a fiber-gut microbiota interaction, as well as a potential specific mechanism by which gut-mediated systemic inflammation may be mitigated. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13073-021-00921-y.
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spelling pubmed-82124602021-06-22 Dietary fiber intake, the gut microbiome, and chronic systemic inflammation in a cohort of adult men Ma, Wenjie Nguyen, Long H. Song, Mingyang Wang, Dong D. Franzosa, Eric A. Cao, Yin Joshi, Amit Drew, David A. Mehta, Raaj Ivey, Kerry L. Strate, Lisa L. Giovannucci, Edward L. Izard, Jacques Garrett, Wendy Rimm, Eric B. Huttenhower, Curtis Chan, Andrew T. Genome Med Research BACKGROUND: A higher intake of dietary fiber is associated with a decreased risk of chronic inflammatory diseases such as cardiovascular disease and inflammatory bowel disease. This may function in part due to abrogation of chronic systemic inflammation induced by factors such as dysbiotic gut communities. Data regarding the detailed influences of long-term and recent intake of differing dietary fiber sources on the human gut microbiome are lacking. METHODS: In a cohort of 307 generally healthy men, we examined gut microbiomes, profiled by shotgun metagenomic and metatranscriptomic sequencing, and long-term and recent dietary fiber intake in relation to plasma levels of C-reactive protein (CRP), an established biomarker for chronic inflammation. Data were analyzed using multivariate linear mixed models. RESULTS: We found that inflammation-associated gut microbial configurations corresponded with higher CRP levels. A greater intake of dietary fiber was associated with shifts in gut microbiome composition, particularly Clostridiales, and their potential for carbohydrate utilization via polysaccharide degradation. This was particularly true for fruit fiber sources (i.e., pectin). Most striking, fiber intake was associated with significantly greater CRP reduction in individuals without substantial Prevotella copri carriage in the gut, whereas those with P. copri carriage maintained stable CRP levels regardless of fiber intake. CONCLUSIONS: Our findings offer human evidence supporting a fiber-gut microbiota interaction, as well as a potential specific mechanism by which gut-mediated systemic inflammation may be mitigated. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13073-021-00921-y. BioMed Central 2021-06-17 /pmc/articles/PMC8212460/ /pubmed/34140026 http://dx.doi.org/10.1186/s13073-021-00921-y Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Ma, Wenjie
Nguyen, Long H.
Song, Mingyang
Wang, Dong D.
Franzosa, Eric A.
Cao, Yin
Joshi, Amit
Drew, David A.
Mehta, Raaj
Ivey, Kerry L.
Strate, Lisa L.
Giovannucci, Edward L.
Izard, Jacques
Garrett, Wendy
Rimm, Eric B.
Huttenhower, Curtis
Chan, Andrew T.
Dietary fiber intake, the gut microbiome, and chronic systemic inflammation in a cohort of adult men
title Dietary fiber intake, the gut microbiome, and chronic systemic inflammation in a cohort of adult men
title_full Dietary fiber intake, the gut microbiome, and chronic systemic inflammation in a cohort of adult men
title_fullStr Dietary fiber intake, the gut microbiome, and chronic systemic inflammation in a cohort of adult men
title_full_unstemmed Dietary fiber intake, the gut microbiome, and chronic systemic inflammation in a cohort of adult men
title_short Dietary fiber intake, the gut microbiome, and chronic systemic inflammation in a cohort of adult men
title_sort dietary fiber intake, the gut microbiome, and chronic systemic inflammation in a cohort of adult men
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8212460/
https://www.ncbi.nlm.nih.gov/pubmed/34140026
http://dx.doi.org/10.1186/s13073-021-00921-y
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