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Distinctive patterns of sulfide- and butyrate-metabolizing bacteria after bariatric surgery: potential implications for colorectal cancer risk

Despite improved cardiometabolic outcomes following bariatric surgery, its long-term impact on colorectal cancer (CRC) risk remains uncertain. In parallel, the influence of bariatric surgery on the host microbiome and relationships with disease outcomes is beginning to be appreciated. Therefore, we...

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Autores principales: Hussan, Hisham, Clinton, Steven K., Grainger, Elizabeth M., Webb, Maxine, Wang, Cankun, Webb, Amy, Needleman, Bradley, Noria, Sabrena, Zhu, Jiangjiang, Choueiry, Fouad, Pietrzak, Maciej, Bailey, Michael T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10501170/
https://www.ncbi.nlm.nih.gov/pubmed/37702461
http://dx.doi.org/10.1080/19490976.2023.2255345
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author Hussan, Hisham
Clinton, Steven K.
Grainger, Elizabeth M.
Webb, Maxine
Wang, Cankun
Webb, Amy
Needleman, Bradley
Noria, Sabrena
Zhu, Jiangjiang
Choueiry, Fouad
Pietrzak, Maciej
Bailey, Michael T.
author_facet Hussan, Hisham
Clinton, Steven K.
Grainger, Elizabeth M.
Webb, Maxine
Wang, Cankun
Webb, Amy
Needleman, Bradley
Noria, Sabrena
Zhu, Jiangjiang
Choueiry, Fouad
Pietrzak, Maciej
Bailey, Michael T.
author_sort Hussan, Hisham
collection PubMed
description Despite improved cardiometabolic outcomes following bariatric surgery, its long-term impact on colorectal cancer (CRC) risk remains uncertain. In parallel, the influence of bariatric surgery on the host microbiome and relationships with disease outcomes is beginning to be appreciated. Therefore, we investigated the impact of Roux-en-Y gastric bypass (RYGB) and vertical sleeve gastrectomy (VSG) on the patterns of sulfide-reducing and butyrate-producing bacteria, which are hypothesized to modulate CRC risk after bariatric surgery. In this single-center, cross-sectional study, we included 15 pre-surgery subjects with severe obesity and patients who are at a median (range) of 25.6 (9.9–46.5) months after RYGB (n = 16) or VSG (n = 10). The DNA abundance of fecal bacteria and enzymes involved in butyrate and sulfide metabolism were identified using metagenomic sequencing. Differences between pre-surgery and post-RYGB or post-VSG cohorts were quantified using the linear discriminant analysis (LDA) effect size (LEfSe) method. Our sample was predominantly female (87%) with a median (range) age of 46 (23–71) years. Post-RYGB and post-VSG patients had a higher DNA abundance of fecal sulfide-reducing bacteria than pre-surgery controls (LDA = 1.3–4.4, p < .05). The most significant enrichments were for fecal E. coli, Acidaminococcus and A. finegoldii after RYGB, and for A. finegoldii, S. vestibularis, V. parvula after VSG. As for butyrate-producing bacteria, R. faecis was more abundant, whereas B. dentium and A. hardus were lower post-RYGB vs. pre-surgery. B. dentium was also lower in post-VSG vs. pre-surgery. Consistent with these findings, our analysis showed a greater enrichment of sulfide-reducing enzymes after bariatric surgery, especially RYGB, vs. pre-surgery. The DNA abundance of butyrate-producing enzymes was lower post-RYGB. In conclusion, the two most used bariatric surgeries, RYGB and VSG, are associated with microbiome patterns that are potentially implicated in CRC risk. Future studies are needed to validate and understand the impact of these microbiome changes on CRC risk after bariatric surgery.
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spelling pubmed-105011702023-09-15 Distinctive patterns of sulfide- and butyrate-metabolizing bacteria after bariatric surgery: potential implications for colorectal cancer risk Hussan, Hisham Clinton, Steven K. Grainger, Elizabeth M. Webb, Maxine Wang, Cankun Webb, Amy Needleman, Bradley Noria, Sabrena Zhu, Jiangjiang Choueiry, Fouad Pietrzak, Maciej Bailey, Michael T. Gut Microbes Brief Report Despite improved cardiometabolic outcomes following bariatric surgery, its long-term impact on colorectal cancer (CRC) risk remains uncertain. In parallel, the influence of bariatric surgery on the host microbiome and relationships with disease outcomes is beginning to be appreciated. Therefore, we investigated the impact of Roux-en-Y gastric bypass (RYGB) and vertical sleeve gastrectomy (VSG) on the patterns of sulfide-reducing and butyrate-producing bacteria, which are hypothesized to modulate CRC risk after bariatric surgery. In this single-center, cross-sectional study, we included 15 pre-surgery subjects with severe obesity and patients who are at a median (range) of 25.6 (9.9–46.5) months after RYGB (n = 16) or VSG (n = 10). The DNA abundance of fecal bacteria and enzymes involved in butyrate and sulfide metabolism were identified using metagenomic sequencing. Differences between pre-surgery and post-RYGB or post-VSG cohorts were quantified using the linear discriminant analysis (LDA) effect size (LEfSe) method. Our sample was predominantly female (87%) with a median (range) age of 46 (23–71) years. Post-RYGB and post-VSG patients had a higher DNA abundance of fecal sulfide-reducing bacteria than pre-surgery controls (LDA = 1.3–4.4, p < .05). The most significant enrichments were for fecal E. coli, Acidaminococcus and A. finegoldii after RYGB, and for A. finegoldii, S. vestibularis, V. parvula after VSG. As for butyrate-producing bacteria, R. faecis was more abundant, whereas B. dentium and A. hardus were lower post-RYGB vs. pre-surgery. B. dentium was also lower in post-VSG vs. pre-surgery. Consistent with these findings, our analysis showed a greater enrichment of sulfide-reducing enzymes after bariatric surgery, especially RYGB, vs. pre-surgery. The DNA abundance of butyrate-producing enzymes was lower post-RYGB. In conclusion, the two most used bariatric surgeries, RYGB and VSG, are associated with microbiome patterns that are potentially implicated in CRC risk. Future studies are needed to validate and understand the impact of these microbiome changes on CRC risk after bariatric surgery. Taylor & Francis 2023-09-13 /pmc/articles/PMC10501170/ /pubmed/37702461 http://dx.doi.org/10.1080/19490976.2023.2255345 Text en © 2023 The Author(s). Published with license by Taylor & Francis Group, LLC. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the Accepted Manuscript in a repository by the author(s) or with their consent.
spellingShingle Brief Report
Hussan, Hisham
Clinton, Steven K.
Grainger, Elizabeth M.
Webb, Maxine
Wang, Cankun
Webb, Amy
Needleman, Bradley
Noria, Sabrena
Zhu, Jiangjiang
Choueiry, Fouad
Pietrzak, Maciej
Bailey, Michael T.
Distinctive patterns of sulfide- and butyrate-metabolizing bacteria after bariatric surgery: potential implications for colorectal cancer risk
title Distinctive patterns of sulfide- and butyrate-metabolizing bacteria after bariatric surgery: potential implications for colorectal cancer risk
title_full Distinctive patterns of sulfide- and butyrate-metabolizing bacteria after bariatric surgery: potential implications for colorectal cancer risk
title_fullStr Distinctive patterns of sulfide- and butyrate-metabolizing bacteria after bariatric surgery: potential implications for colorectal cancer risk
title_full_unstemmed Distinctive patterns of sulfide- and butyrate-metabolizing bacteria after bariatric surgery: potential implications for colorectal cancer risk
title_short Distinctive patterns of sulfide- and butyrate-metabolizing bacteria after bariatric surgery: potential implications for colorectal cancer risk
title_sort distinctive patterns of sulfide- and butyrate-metabolizing bacteria after bariatric surgery: potential implications for colorectal cancer risk
topic Brief Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10501170/
https://www.ncbi.nlm.nih.gov/pubmed/37702461
http://dx.doi.org/10.1080/19490976.2023.2255345
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