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A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis

INTRODUCTION: Ulcerative colitis (UC) is characterized by chronic inflammation in the colonic epithelium and has a blurred etiology. A western diet and microbial dysbiosis in the colon were reported to play a role in UC development. In this study, we investigated the effect of a westernized diet, i....

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Autores principales: Panah, Farhad M., Nielsen, Katrine D., Simpson, Gavin L., Schönherz, Anna, Schramm, Andreas, Lauridsen, Charlotte, Nielsen, Tina S., Højberg, Ole, Fredborg, Marlene, Purup, Stig, Canibe, Nuria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10150118/
https://www.ncbi.nlm.nih.gov/pubmed/37138607
http://dx.doi.org/10.3389/fmicb.2023.1018242
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author Panah, Farhad M.
Nielsen, Katrine D.
Simpson, Gavin L.
Schönherz, Anna
Schramm, Andreas
Lauridsen, Charlotte
Nielsen, Tina S.
Højberg, Ole
Fredborg, Marlene
Purup, Stig
Canibe, Nuria
author_facet Panah, Farhad M.
Nielsen, Katrine D.
Simpson, Gavin L.
Schönherz, Anna
Schramm, Andreas
Lauridsen, Charlotte
Nielsen, Tina S.
Højberg, Ole
Fredborg, Marlene
Purup, Stig
Canibe, Nuria
author_sort Panah, Farhad M.
collection PubMed
description INTRODUCTION: Ulcerative colitis (UC) is characterized by chronic inflammation in the colonic epithelium and has a blurred etiology. A western diet and microbial dysbiosis in the colon were reported to play a role in UC development. In this study, we investigated the effect of a westernized diet, i.e., increasing fat and protein content by including ground beef, on the colonic bacterial composition in a dextran sulfate sodium (DexSS) challenged pig study. METHODS: The experiment was carried out in three complete blocks following a 2×2 factorial design including 24 six-week old pigs, fed either a standard diet (CT) or the standard diet substituted with 15% ground beef to simulate a typical westernized diet (WD). Colitis was induced in half of the pigs on each dietary treatment by oral administration of DexSS (DSS and WD+DSS, respectively). Samples from proximal and distal colon and feces were collected. RESULTS AND DISCUSSION: Bacterial alpha diversity was unaffected by experimental block, and sample type. In proximal colon, WD group had similar alpha diversity to CT group and the WD+DSS group showed the lowest alpha diversity compared to the other treatment groups. There was a significant interaction between western diet and DexSS for beta diversity, based on Bray-Curtis dissimilarly. The westernized diet and DexSS resulted in three and seven differentially abundant phyla, 21 and 65 species, respectively, mainly associated with the Firmicutes and Bacteroidota phyla followed by Spirochaetota, Desulfobacterota, and Proteobacteria. The concentration of short-chain fatty acids (SCFA) was lowest in the distal colon. Treatment had a slight effect on the estimates for microbial metabolites that might have valuable biological relevance for future studies. The concentration of putrescine in the colon and feces and that of total biogenic amines was highest in the WD+DSS group. We conclude that a westernized diet could be a potential risk factor and an exacerbating agent for UC by reducing the abundance of SCFA-producing bacteria, increasing the abundance of pathogens such as Helicobacter trogontum, and by increasing the concentration of microbial proteolytic-derived metabolites in the colon.
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spelling pubmed-101501182023-05-02 A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis Panah, Farhad M. Nielsen, Katrine D. Simpson, Gavin L. Schönherz, Anna Schramm, Andreas Lauridsen, Charlotte Nielsen, Tina S. Højberg, Ole Fredborg, Marlene Purup, Stig Canibe, Nuria Front Microbiol Microbiology INTRODUCTION: Ulcerative colitis (UC) is characterized by chronic inflammation in the colonic epithelium and has a blurred etiology. A western diet and microbial dysbiosis in the colon were reported to play a role in UC development. In this study, we investigated the effect of a westernized diet, i.e., increasing fat and protein content by including ground beef, on the colonic bacterial composition in a dextran sulfate sodium (DexSS) challenged pig study. METHODS: The experiment was carried out in three complete blocks following a 2×2 factorial design including 24 six-week old pigs, fed either a standard diet (CT) or the standard diet substituted with 15% ground beef to simulate a typical westernized diet (WD). Colitis was induced in half of the pigs on each dietary treatment by oral administration of DexSS (DSS and WD+DSS, respectively). Samples from proximal and distal colon and feces were collected. RESULTS AND DISCUSSION: Bacterial alpha diversity was unaffected by experimental block, and sample type. In proximal colon, WD group had similar alpha diversity to CT group and the WD+DSS group showed the lowest alpha diversity compared to the other treatment groups. There was a significant interaction between western diet and DexSS for beta diversity, based on Bray-Curtis dissimilarly. The westernized diet and DexSS resulted in three and seven differentially abundant phyla, 21 and 65 species, respectively, mainly associated with the Firmicutes and Bacteroidota phyla followed by Spirochaetota, Desulfobacterota, and Proteobacteria. The concentration of short-chain fatty acids (SCFA) was lowest in the distal colon. Treatment had a slight effect on the estimates for microbial metabolites that might have valuable biological relevance for future studies. The concentration of putrescine in the colon and feces and that of total biogenic amines was highest in the WD+DSS group. We conclude that a westernized diet could be a potential risk factor and an exacerbating agent for UC by reducing the abundance of SCFA-producing bacteria, increasing the abundance of pathogens such as Helicobacter trogontum, and by increasing the concentration of microbial proteolytic-derived metabolites in the colon. Frontiers Media S.A. 2023-04-17 /pmc/articles/PMC10150118/ /pubmed/37138607 http://dx.doi.org/10.3389/fmicb.2023.1018242 Text en Copyright © 2023 Panah, Nielsen, Simpson, Schönherz, Schramm, Lauridsen, Nielsen, Højberg, Fredborg, Purup and Canibe. 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 Microbiology
Panah, Farhad M.
Nielsen, Katrine D.
Simpson, Gavin L.
Schönherz, Anna
Schramm, Andreas
Lauridsen, Charlotte
Nielsen, Tina S.
Højberg, Ole
Fredborg, Marlene
Purup, Stig
Canibe, Nuria
A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis
title A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis
title_full A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis
title_fullStr A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis
title_full_unstemmed A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis
title_short A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis
title_sort westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10150118/
https://www.ncbi.nlm.nih.gov/pubmed/37138607
http://dx.doi.org/10.3389/fmicb.2023.1018242
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