A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis
IntroductionUlcerative 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....
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Frontiers Media S.A.
2023-04-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1018242/full |
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| author | Farhad M. Panah Katrine D. Nielsen Gavin L. Simpson Anna Schönherz Andreas Schramm Charlotte Lauridsen Tina S. Nielsen Ole Højberg Marlene Fredborg Stig Purup Nuria Canibe |
| author_facet | Farhad M. Panah Katrine D. Nielsen Gavin L. Simpson Anna Schönherz Andreas Schramm Charlotte Lauridsen Tina S. Nielsen Ole Højberg Marlene Fredborg Stig Purup Nuria Canibe |
| author_sort | Farhad M. Panah |
| collection | DOAJ |
| description | IntroductionUlcerative 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.MethodsThe 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 discussionBacterial 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. |
| first_indexed | 2024-03-13T02:58:35Z |
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| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-13T02:58:35Z |
| publishDate | 2023-04-01 |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-6ab91318fb8744f4a02f7c2c83e37dc32023-06-27T18:36:43ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.10182421018242A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitisFarhad M. Panah0Katrine D. Nielsen1Gavin L. Simpson2Anna Schönherz3Andreas Schramm4Charlotte Lauridsen5Tina S. Nielsen6Ole Højberg7Marlene Fredborg8Stig Purup9Nuria Canibe10Department of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkDepartment of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkDepartment of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkDepartment of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkDepartment of Biology, Aarhus University, Aarhus, DenmarkDepartment of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkDepartment of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkDepartment of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkDepartment of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkDepartment of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkDepartment of Veterinary and Animal Sciences, Aarhus University, Tjele, DenmarkIntroductionUlcerative 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.MethodsThe 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 discussionBacterial 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.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1018242/fullinflammatory bowel diseaseulcerative colitismeat consumptioncolonic inflammationporcine model16S rRNA gut metagenomics |
| spellingShingle | Farhad M. Panah Katrine D. Nielsen Gavin L. Simpson Anna Schönherz Andreas Schramm Charlotte Lauridsen Tina S. Nielsen Ole Højberg Marlene Fredborg Stig Purup Nuria Canibe A westernized diet changed the colonic bacterial composition and metabolite concentration in a dextran sulfate sodium pig model for ulcerative colitis Frontiers in Microbiology inflammatory bowel disease ulcerative colitis meat consumption colonic inflammation porcine model 16S rRNA gut metagenomics |
| 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 | inflammatory bowel disease ulcerative colitis meat consumption colonic inflammation porcine model 16S rRNA gut metagenomics |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1018242/full |
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