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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
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.
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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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