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Anthocyanin-rich blue potato meals protect against polychlorinated biphenyl-mediated disruption of short-chain fatty acid production and gut microbiota profiles in a simulated human digestion model

BACKGROUND: Polychlorinated biphenyls (PCBs) are ubiquitous environmental pollutants associated with a wide variety of adverse human health outcomes. PCB 126 and PCB 153 are among the most prevalent congeners associated with human exposure. Emerging studies have suggested that PCB exposure leads to...

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Autores principales: Lu, Fang, MacPherson, Chad W., Tremblay, Julien, Iskandar, Michèle M., Kubow, Stan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10266533/
https://www.ncbi.nlm.nih.gov/pubmed/37324735
http://dx.doi.org/10.3389/fnut.2023.1130841
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author Lu, Fang
MacPherson, Chad W.
Tremblay, Julien
Iskandar, Michèle M.
Kubow, Stan
author_facet Lu, Fang
MacPherson, Chad W.
Tremblay, Julien
Iskandar, Michèle M.
Kubow, Stan
author_sort Lu, Fang
collection PubMed
description BACKGROUND: Polychlorinated biphenyls (PCBs) are ubiquitous environmental pollutants associated with a wide variety of adverse human health outcomes. PCB 126 and PCB 153 are among the most prevalent congeners associated with human exposure. Emerging studies have suggested that PCB exposure leads to lower gut microbial diversity although their effects on microbial production of health promoting short-chain fatty acids (SCFAs) has been scarcely studied. Blue potatoes are rich in anthocyanins (ACNs), which is a class of polyphenols that promote the growth of beneficial intestinal bacteria such as Bifidobacterium and Lactobacillus and increase the generation of SCFAs. A batch-culture, pH-controlled, stirred system containing human fecal microbial communities was utilized to assess whether human gut microbiota composition and SCFA production are affected by: (a) PCB 126 and PCB 153 exposure; and (b) ACN-rich digests in the presence and absence of the PCB congeners. METHODS: Anthocyanin-rich blue potato meals (11.03 g) were digested over 12 h with and without PCB 126 (0.5 mM) and PCB 153 (0.5 mM) using an in vitro simulated gut digestion model involving upper gastrointestinal digestion followed by metabolism by human fecal microbiota. Fecal digests were collected for analysis of gut microbial and SCFA profiles. RESULTS: Polychlorinated biphenyl-exposed fecal samples showed a significant (p < 0.05) decrease in species richness and a significantly (p < 0.05) different microbial community structure. PCB treatment was associated with an increased (p < 0.05) relative abundance of Akkermansia, Eggerthella, and Bifidobacterium and a decreased (p < 0.05) relative abundance of Veillonella, Streptococcus, and Holdemanella. ACN digests counteracted the altered abundances of Akkermansia and Bifidobacterium seen with the PCB treatment. PCB exposure was associated with a significant (p < 0.05) decrease in total SCFA and acetate concentrations. ACN digests were associated with significantly (p < 0.05) higher SCFA and acetate concentrations in the presence and absence of PCBs. CONCLUSION: Human fecal matter exposed to PCB 126 and PCB 153 led to decreased abundance and altered gut microbiota profiles as well as lowered SCFA and acetate levels. Importantly, this study showed that prebiotic ACN-rich potatoes counteract PCB-mediated disruptions in human gut microbiota profiles and SCFA production.
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spelling pubmed-102665332023-06-15 Anthocyanin-rich blue potato meals protect against polychlorinated biphenyl-mediated disruption of short-chain fatty acid production and gut microbiota profiles in a simulated human digestion model Lu, Fang MacPherson, Chad W. Tremblay, Julien Iskandar, Michèle M. Kubow, Stan Front Nutr Nutrition BACKGROUND: Polychlorinated biphenyls (PCBs) are ubiquitous environmental pollutants associated with a wide variety of adverse human health outcomes. PCB 126 and PCB 153 are among the most prevalent congeners associated with human exposure. Emerging studies have suggested that PCB exposure leads to lower gut microbial diversity although their effects on microbial production of health promoting short-chain fatty acids (SCFAs) has been scarcely studied. Blue potatoes are rich in anthocyanins (ACNs), which is a class of polyphenols that promote the growth of beneficial intestinal bacteria such as Bifidobacterium and Lactobacillus and increase the generation of SCFAs. A batch-culture, pH-controlled, stirred system containing human fecal microbial communities was utilized to assess whether human gut microbiota composition and SCFA production are affected by: (a) PCB 126 and PCB 153 exposure; and (b) ACN-rich digests in the presence and absence of the PCB congeners. METHODS: Anthocyanin-rich blue potato meals (11.03 g) were digested over 12 h with and without PCB 126 (0.5 mM) and PCB 153 (0.5 mM) using an in vitro simulated gut digestion model involving upper gastrointestinal digestion followed by metabolism by human fecal microbiota. Fecal digests were collected for analysis of gut microbial and SCFA profiles. RESULTS: Polychlorinated biphenyl-exposed fecal samples showed a significant (p < 0.05) decrease in species richness and a significantly (p < 0.05) different microbial community structure. PCB treatment was associated with an increased (p < 0.05) relative abundance of Akkermansia, Eggerthella, and Bifidobacterium and a decreased (p < 0.05) relative abundance of Veillonella, Streptococcus, and Holdemanella. ACN digests counteracted the altered abundances of Akkermansia and Bifidobacterium seen with the PCB treatment. PCB exposure was associated with a significant (p < 0.05) decrease in total SCFA and acetate concentrations. ACN digests were associated with significantly (p < 0.05) higher SCFA and acetate concentrations in the presence and absence of PCBs. CONCLUSION: Human fecal matter exposed to PCB 126 and PCB 153 led to decreased abundance and altered gut microbiota profiles as well as lowered SCFA and acetate levels. Importantly, this study showed that prebiotic ACN-rich potatoes counteract PCB-mediated disruptions in human gut microbiota profiles and SCFA production. Frontiers Media S.A. 2023-05-31 /pmc/articles/PMC10266533/ /pubmed/37324735 http://dx.doi.org/10.3389/fnut.2023.1130841 Text en Copyright © 2023 Lu, MacPherson, Tremblay, Iskandar and Kubow. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Nutrition
Lu, Fang
MacPherson, Chad W.
Tremblay, Julien
Iskandar, Michèle M.
Kubow, Stan
Anthocyanin-rich blue potato meals protect against polychlorinated biphenyl-mediated disruption of short-chain fatty acid production and gut microbiota profiles in a simulated human digestion model
title Anthocyanin-rich blue potato meals protect against polychlorinated biphenyl-mediated disruption of short-chain fatty acid production and gut microbiota profiles in a simulated human digestion model
title_full Anthocyanin-rich blue potato meals protect against polychlorinated biphenyl-mediated disruption of short-chain fatty acid production and gut microbiota profiles in a simulated human digestion model
title_fullStr Anthocyanin-rich blue potato meals protect against polychlorinated biphenyl-mediated disruption of short-chain fatty acid production and gut microbiota profiles in a simulated human digestion model
title_full_unstemmed Anthocyanin-rich blue potato meals protect against polychlorinated biphenyl-mediated disruption of short-chain fatty acid production and gut microbiota profiles in a simulated human digestion model
title_short Anthocyanin-rich blue potato meals protect against polychlorinated biphenyl-mediated disruption of short-chain fatty acid production and gut microbiota profiles in a simulated human digestion model
title_sort anthocyanin-rich blue potato meals protect against polychlorinated biphenyl-mediated disruption of short-chain fatty acid production and gut microbiota profiles in a simulated human digestion model
topic Nutrition
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10266533/
https://www.ncbi.nlm.nih.gov/pubmed/37324735
http://dx.doi.org/10.3389/fnut.2023.1130841
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