Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota.

Nils Bruun Jørgensen, Manimozhiyan Arumugam, Torben Hansen, Oluf Pedersen, Jun Wang, Sten Madsbad, Jens J Holst, Kristoffer S Burgdorf, Carsten Dirksen, Kirstine N Bojsen-Møller, Albert Palleja, Qiang Feng, Suisha Liang, Thorsten Brach, Yin Li, Chenchen Zhang, Trine Nielsen, Kristine H Allin, Alireza Kashani

Journal: Genome medicine 2017;8(1):67

PMID: 27306058

Plain Language Summary

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Roux-en-Y gastric bypass (RYGB) has been shown to cause quick and sustained weight loss, improvements to insulin sensitivity and reduced inflammation. However, the mechanisms resulting in these improvements are poorly understood. This longitudinal study explored the short and long term impact of RYGB on gut microbial composition with 13 morbidly obese people. The gut microbiomes were measured before surgery, and three months and 12 months after. Gut microbiota were categorised by species and gene levels. The study found that gut microbiota diversity increased in the first three months after RYGB surgery and still remained high 12 months later. This was inline with metabolic improvements (such as fasting blood glucose). There was also a change in microbiota composition including an increased potential for use of micro and macro nutrients.

Abstract

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 ).

Address: The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, 2200, Copenhagen, Denmark.; Danish Diabetes Academy, 5000, Odense, Denmark.; BGI-Shenzhen, Shenzhen, 518083, China.; Department of Endocrinology, Hvidovre Hospital, 2650, Hvidovre, Denmark.; Department of Biomedical Sciences, Faculty of Health Sciences, University of Copenhagen, 2200, Copenhagen, Denmark.; iCarbonX, Shenzhen, 518083, China.; Beijing Advanced Innovation Center for Food Nutrition and Human Health, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 10083, China.; Department of Biology, University of Copenhagen, 2200, Copenhagen, Denmark.; The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, 2200, Copenhagen, Denmark. [email protected].; The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, 2200, Copenhagen, Denmark. [email protected].; Faculty of Health Sciences, University of Southern Denmark, 5000, Odense, Denmark. [email protected].; The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, 2200, Copenhagen, Denmark. [email protected].

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