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Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota
BACKGROUND: Roux-en-Y gastric bypass (RYGB) is an effective means to achieve sustained weight loss for morbidly obese individuals. Besides rapid weight reduction, patients achieve major improvements of insulin sensitivity and glucose homeostasis. Dysbiosis of gut microbiota has been associated with...
Autores principales: | , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2016
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4908688/ https://www.ncbi.nlm.nih.gov/pubmed/27306058 http://dx.doi.org/10.1186/s13073-016-0312-1 |
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author | Palleja, Albert Kashani, Alireza Allin, Kristine H. Nielsen, Trine Zhang, Chenchen Li, Yin Brach, Thorsten Liang, Suisha Feng, Qiang Jørgensen, Nils Bruun Bojsen-Møller, Kirstine N. Dirksen, Carsten Burgdorf, Kristoffer S. Holst, Jens J. Madsbad, Sten Wang, Jun Pedersen, Oluf Hansen, Torben Arumugam, Manimozhiyan |
author_facet | Palleja, Albert Kashani, Alireza Allin, Kristine H. Nielsen, Trine Zhang, Chenchen Li, Yin Brach, Thorsten Liang, Suisha Feng, Qiang Jørgensen, Nils Bruun Bojsen-Møller, Kirstine N. Dirksen, Carsten Burgdorf, Kristoffer S. Holst, Jens J. Madsbad, Sten Wang, Jun Pedersen, Oluf Hansen, Torben Arumugam, Manimozhiyan |
author_sort | Palleja, Albert |
collection | PubMed |
description | BACKGROUND: Roux-en-Y gastric bypass (RYGB) is an effective means to achieve sustained weight loss for morbidly obese individuals. Besides rapid weight reduction, patients achieve major improvements of insulin sensitivity and glucose homeostasis. Dysbiosis of gut microbiota has been associated with obesity and some of its co-morbidities, like type 2 diabetes, and major changes of gut microbial communities have been hypothesized to mediate part of the beneficial metabolic effects observed after RYGB. Here we describe changes in gut microbial taxonomic composition and functional potential following RYGB. METHODS: We recruited 13 morbidly obese patients who underwent RYGB, carefully phenotyped them, and had their gut microbiomes quantified before (n = 13) and 3 months (n = 12) and 12 months (n = 8) after RYGB. Following shotgun metagenomic sequencing of the fecal microbial DNA purified from stools, we characterized the gut microbial composition at species and gene levels followed by functional annotation. RESULTS: In parallel with the weight loss and metabolic improvements, gut microbial diversity increased within the first 3 months after RYGB and remained high 1 year later. RYGB led to altered relative abundances of 31 species (P < 0.05, q < 0.15) within the first 3 months, including those of Escherichia coli, Klebsiella pneumoniae, Veillonella spp., Streptococcus spp., Alistipes spp., and Akkermansia muciniphila. Sixteen of these species maintained their altered relative abundances during the following 9 months. Interestingly, Faecalibacterium prausnitzii was the only species that decreased in relative abundance. Fifty-three microbial functional modules increased their relative abundance between baseline and 3 months (P < 0.05, q < 0.17). These functional changes included increased potential (i) to assimilate multiple energy sources using transporters and phosphotransferase systems, (ii) to use aerobic respiration, (iii) to shift from protein degradation to putrefaction, and (iv) to use amino acids and fatty acids as energy sources. CONCLUSIONS: Within 3 months after morbidly obese individuals had undergone RYGB, their gut microbiota featured an increased diversity, an altered composition, an increased potential for oxygen tolerance, and an increased potential for microbial utilization of macro- and micro-nutrients. These changes were maintained for the first year post-RYGB. TRIAL REGISTRATION: Current controlled trials (ID NCT00810823, NCT01579981, and NCT01993511). ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13073-016-0312-1) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4908688 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-49086882016-06-16 Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota Palleja, Albert Kashani, Alireza Allin, Kristine H. Nielsen, Trine Zhang, Chenchen Li, Yin Brach, Thorsten Liang, Suisha Feng, Qiang Jørgensen, Nils Bruun Bojsen-Møller, Kirstine N. Dirksen, Carsten Burgdorf, Kristoffer S. Holst, Jens J. Madsbad, Sten Wang, Jun Pedersen, Oluf Hansen, Torben Arumugam, Manimozhiyan Genome Med Research BACKGROUND: Roux-en-Y gastric bypass (RYGB) is an effective means to achieve sustained weight loss for morbidly obese individuals. Besides rapid weight reduction, patients achieve major improvements of insulin sensitivity and glucose homeostasis. Dysbiosis of gut microbiota has been associated with obesity and some of its co-morbidities, like type 2 diabetes, and major changes of gut microbial communities have been hypothesized to mediate part of the beneficial metabolic effects observed after RYGB. Here we describe changes in gut microbial taxonomic composition and functional potential following RYGB. METHODS: We recruited 13 morbidly obese patients who underwent RYGB, carefully phenotyped them, and had their gut microbiomes quantified before (n = 13) and 3 months (n = 12) and 12 months (n = 8) after RYGB. Following shotgun metagenomic sequencing of the fecal microbial DNA purified from stools, we characterized the gut microbial composition at species and gene levels followed by functional annotation. RESULTS: In parallel with the weight loss and metabolic improvements, gut microbial diversity increased within the first 3 months after RYGB and remained high 1 year later. RYGB led to altered relative abundances of 31 species (P < 0.05, q < 0.15) within the first 3 months, including those of Escherichia coli, Klebsiella pneumoniae, Veillonella spp., Streptococcus spp., Alistipes spp., and Akkermansia muciniphila. Sixteen of these species maintained their altered relative abundances during the following 9 months. Interestingly, Faecalibacterium prausnitzii was the only species that decreased in relative abundance. Fifty-three microbial functional modules increased their relative abundance between baseline and 3 months (P < 0.05, q < 0.17). These functional changes included increased potential (i) to assimilate multiple energy sources using transporters and phosphotransferase systems, (ii) to use aerobic respiration, (iii) to shift from protein degradation to putrefaction, and (iv) to use amino acids and fatty acids as energy sources. CONCLUSIONS: Within 3 months after morbidly obese individuals had undergone RYGB, their gut microbiota featured an increased diversity, an altered composition, an increased potential for oxygen tolerance, and an increased potential for microbial utilization of macro- and micro-nutrients. These changes were maintained for the first year post-RYGB. TRIAL REGISTRATION: Current controlled trials (ID NCT00810823, NCT01579981, and NCT01993511). ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13073-016-0312-1) contains supplementary material, which is available to authorized users. BioMed Central 2016-06-15 /pmc/articles/PMC4908688/ /pubmed/27306058 http://dx.doi.org/10.1186/s13073-016-0312-1 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Palleja, Albert Kashani, Alireza Allin, Kristine H. Nielsen, Trine Zhang, Chenchen Li, Yin Brach, Thorsten Liang, Suisha Feng, Qiang Jørgensen, Nils Bruun Bojsen-Møller, Kirstine N. Dirksen, Carsten Burgdorf, Kristoffer S. Holst, Jens J. Madsbad, Sten Wang, Jun Pedersen, Oluf Hansen, Torben Arumugam, Manimozhiyan Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota |
title | Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota |
title_full | Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota |
title_fullStr | Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota |
title_full_unstemmed | Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota |
title_short | Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota |
title_sort | roux-en-y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4908688/ https://www.ncbi.nlm.nih.gov/pubmed/27306058 http://dx.doi.org/10.1186/s13073-016-0312-1 |
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