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Markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies

AIMS/HYPOTHESIS: The gut microbiome is hypothesised to be related to insulin resistance and other metabolic variables. However, data from population-based studies are limited. We investigated associations between serologic measures of metabolic health and the gut microbiome in the Northern Finland B...

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Autores principales: Zouiouich, Semi, Loftfield, Erikka, Huybrechts, Inge, Viallon, Vivian, Louca, Panayiotis, Vogtmann, Emily, Wells, Philippa M., Steves, Claire J., Herzig, Karl-Heinz, Menni, Cristina, Jarvelin, Marjo-Riitta, Sinha, Rashmi, Gunter, Marc J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8245388/
https://www.ncbi.nlm.nih.gov/pubmed/34110438
http://dx.doi.org/10.1007/s00125-021-05464-w
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author Zouiouich, Semi
Loftfield, Erikka
Huybrechts, Inge
Viallon, Vivian
Louca, Panayiotis
Vogtmann, Emily
Wells, Philippa M.
Steves, Claire J.
Herzig, Karl-Heinz
Menni, Cristina
Jarvelin, Marjo-Riitta
Sinha, Rashmi
Gunter, Marc J.
author_facet Zouiouich, Semi
Loftfield, Erikka
Huybrechts, Inge
Viallon, Vivian
Louca, Panayiotis
Vogtmann, Emily
Wells, Philippa M.
Steves, Claire J.
Herzig, Karl-Heinz
Menni, Cristina
Jarvelin, Marjo-Riitta
Sinha, Rashmi
Gunter, Marc J.
author_sort Zouiouich, Semi
collection PubMed
description AIMS/HYPOTHESIS: The gut microbiome is hypothesised to be related to insulin resistance and other metabolic variables. However, data from population-based studies are limited. We investigated associations between serologic measures of metabolic health and the gut microbiome in the Northern Finland Birth Cohort 1966 (NFBC1966) and the TwinsUK cohort. METHODS: Among 506 individuals from the NFBC1966 with available faecal microbiome (16S rRNA gene sequence) data, we estimated associations between gut microbiome diversity metrics and serologic levels of HOMA for insulin resistance (HOMA-IR), HbA(1c) and C-reactive protein (CRP) using multivariable linear regression models adjusted for sex, smoking status and BMI. Associations between gut microbiome diversity measures and HOMA-IR and CRP were replicated in 1140 adult participants from TwinsUK, with available faecal microbiome (16S rRNA gene sequence) data. For both cohorts, we used general linear models with a quasi-Poisson distribution and Microbiome Regression-based Kernel Association Test (MiRKAT) to estimate associations of metabolic variables with alpha- and beta diversity metrics, respectively, and generalised additive models for location scale and shape (GAMLSS) fitted with the zero-inflated beta distribution to identify taxa associated with the metabolic markers. RESULTS: In NFBC1966, alpha diversity was lower in individuals with higher HOMA-IR with a mean of 74.4 (95% CI 70.7, 78.3) amplicon sequence variants (ASVs) for the first quartile of HOMA-IR and 66.6 (95% CI 62.9, 70.4) for the fourth quartile of HOMA-IR. Alpha diversity was also lower with higher HbA(1c) (number of ASVs and Shannon’s diversity, p < 0.001 and p = 0.003, respectively) and higher CRP (number of ASVs, p = 0.025), even after adjustment for BMI and other potential confounders. In TwinsUK, alpha diversity measures were also lower among participants with higher measures of HOMA-IR and CRP. When considering beta diversity measures, we found that microbial community profiles were associated with HOMA-IR in NFBC1966 and TwinsUK, using multivariate MiRKAT models, with binomial deviance dissimilarity p values of <0.001. In GAMLSS models, the relative abundances of individual genera Prevotella and Blautia were associated with HOMA-IR in both cohorts. CONCLUSIONS/INTERPRETATION: Overall, higher levels of HOMA-IR, CRP and HbA(1c) were associated with lower microbiome diversity in both the NFBC1966 and TwinsUK cohorts, even after adjustment for BMI and other variables. These results from two distinct population-based cohorts provide evidence for an association between metabolic variables and gut microbial diversity. Further experimental and mechanistic insights are now needed to provide understanding of the potential causal mechanisms that may link the gut microbiota with metabolic health. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains peer-reviewed but unedited supplementary material available at 10.1007/s00125-021-05464-w.
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spelling pubmed-82453882021-07-14 Markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies Zouiouich, Semi Loftfield, Erikka Huybrechts, Inge Viallon, Vivian Louca, Panayiotis Vogtmann, Emily Wells, Philippa M. Steves, Claire J. Herzig, Karl-Heinz Menni, Cristina Jarvelin, Marjo-Riitta Sinha, Rashmi Gunter, Marc J. Diabetologia Article AIMS/HYPOTHESIS: The gut microbiome is hypothesised to be related to insulin resistance and other metabolic variables. However, data from population-based studies are limited. We investigated associations between serologic measures of metabolic health and the gut microbiome in the Northern Finland Birth Cohort 1966 (NFBC1966) and the TwinsUK cohort. METHODS: Among 506 individuals from the NFBC1966 with available faecal microbiome (16S rRNA gene sequence) data, we estimated associations between gut microbiome diversity metrics and serologic levels of HOMA for insulin resistance (HOMA-IR), HbA(1c) and C-reactive protein (CRP) using multivariable linear regression models adjusted for sex, smoking status and BMI. Associations between gut microbiome diversity measures and HOMA-IR and CRP were replicated in 1140 adult participants from TwinsUK, with available faecal microbiome (16S rRNA gene sequence) data. For both cohorts, we used general linear models with a quasi-Poisson distribution and Microbiome Regression-based Kernel Association Test (MiRKAT) to estimate associations of metabolic variables with alpha- and beta diversity metrics, respectively, and generalised additive models for location scale and shape (GAMLSS) fitted with the zero-inflated beta distribution to identify taxa associated with the metabolic markers. RESULTS: In NFBC1966, alpha diversity was lower in individuals with higher HOMA-IR with a mean of 74.4 (95% CI 70.7, 78.3) amplicon sequence variants (ASVs) for the first quartile of HOMA-IR and 66.6 (95% CI 62.9, 70.4) for the fourth quartile of HOMA-IR. Alpha diversity was also lower with higher HbA(1c) (number of ASVs and Shannon’s diversity, p < 0.001 and p = 0.003, respectively) and higher CRP (number of ASVs, p = 0.025), even after adjustment for BMI and other potential confounders. In TwinsUK, alpha diversity measures were also lower among participants with higher measures of HOMA-IR and CRP. When considering beta diversity measures, we found that microbial community profiles were associated with HOMA-IR in NFBC1966 and TwinsUK, using multivariate MiRKAT models, with binomial deviance dissimilarity p values of <0.001. In GAMLSS models, the relative abundances of individual genera Prevotella and Blautia were associated with HOMA-IR in both cohorts. CONCLUSIONS/INTERPRETATION: Overall, higher levels of HOMA-IR, CRP and HbA(1c) were associated with lower microbiome diversity in both the NFBC1966 and TwinsUK cohorts, even after adjustment for BMI and other variables. These results from two distinct population-based cohorts provide evidence for an association between metabolic variables and gut microbial diversity. Further experimental and mechanistic insights are now needed to provide understanding of the potential causal mechanisms that may link the gut microbiota with metabolic health. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains peer-reviewed but unedited supplementary material available at 10.1007/s00125-021-05464-w. Springer Berlin Heidelberg 2021-06-10 2021 /pmc/articles/PMC8245388/ /pubmed/34110438 http://dx.doi.org/10.1007/s00125-021-05464-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This 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/) .
spellingShingle Article
Zouiouich, Semi
Loftfield, Erikka
Huybrechts, Inge
Viallon, Vivian
Louca, Panayiotis
Vogtmann, Emily
Wells, Philippa M.
Steves, Claire J.
Herzig, Karl-Heinz
Menni, Cristina
Jarvelin, Marjo-Riitta
Sinha, Rashmi
Gunter, Marc J.
Markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies
title Markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies
title_full Markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies
title_fullStr Markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies
title_full_unstemmed Markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies
title_short Markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies
title_sort markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8245388/
https://www.ncbi.nlm.nih.gov/pubmed/34110438
http://dx.doi.org/10.1007/s00125-021-05464-w
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