Gut microbiota differs a decade after bariatric surgery relative to a nonsurgical comparison group



      Few studies have assessed differences in the gut microbiota composition after bariatric surgery in the long term or whether differences are correlated with remission of type 2 diabetes.


      This observational study assessed differences in the gut microbiota between individuals at up to 13 years after surgery and a comparison group of individuals with severe obesity. The relationship between type 2 diabetes remission and the gut microbiota was also assessed.




      Stool samples were collected from individuals completing bariatric surgery (surgery group; n = 16) and individuals with severe obesity that did not receive surgery (nonsurgery group; n = 19) as part of the 12-year follow-up in the Utah Obesity Study. Metabolic health data were collected at baseline and the follow-up examination. The gut microbiota was quantified by sequencing the V4 region of the 16 S rRNA gene. Significant differences in microbiota composition with surgery and other covariates were determined by Unifrac distance analysis and permutational multivariate analysis of variance. Significant differences in the relative abundance of individual bacterial taxa were assessed using analysis of composition of microbiomes software.


      The surgery group had higher relative abundances of Verrucomicrobiaceae (5.7 ± 1.3% versus 1.1 ± .3%) and Streptococcaceae (6.3 ± 1.0% versus 3.2 ± .8%), but lower relative abundances of Bacteroidaceae (8.8 ± 1.8% versus 18.6 ± 2.3%) 10.6 years after surgery. In a small subset of 8 individuals, a higher relative abundance of Akkermansia muciniphila was correlated with type 2 diabetes remission.


      Differences in the gut microbiota are evident a decade after bariatric surgery compared with individuals with severe obesity that did not undergo surgery. The observed long-term differences are consistent with previous findings.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Surgery for Obesity and Related Diseases
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Anhe F.F.
        • Varin T.V.
        • Schertzer J.D.
        • Marette A.
        The gut microbiota as a mediator of metabolic benefits after bariatric surgery.
        Can J Diabetes. 2017; 41: 439-447
        • Davies N.K.
        • O’Sullivan J.M.
        • Plank L.D.
        • Murphy R.
        Altered gut microbiome after bariatric surgery and its association with metabolic benefits: a systematic review.
        Surg Obes Relat Dis. 2019; 15: 656-665
        • Kong L.C.
        • Tap J.
        • Aron-Wisnewsky J.
        • et al.
        Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes.
        Am J Clin Nutr. 2013; 98: 16-24
        • Palleja A.
        • Kashani A.
        • Allin K.H.
        • et al.
        Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota.
        Genome Med. 2016; 8: 67
        • Shen N.
        • Caixas A.
        • Ahlers M.
        • et al.
        Longitudinal changes of microbiome composition and microbial metabolomics after surgical weight loss in individuals with obesity.
        Surg Obes Relat Dis. 2019; 15: 1367-1373
        • Tremaroli V.
        • Karlsson F.
        • Werling M.
        • et al.
        Roux-en-Y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation.
        Cell Metab. 2015; 22: 228-238
        • Adams T.D.
        • Pendleton R.C.
        • Strong M.B.
        • et al.
        Health outcomes of gastric bypass patients compared to nonsurgical, nonintervened severely obese.
        Obesity (Silver Spring). 2010; 18: 121-130
        • Cummings D.E.
        • Arterburn D.E.
        • Westbrook E.O.
        • et al.
        Gastric bypass surgery vs intensive lifestyle and medical intervention for type 2 diabetes: the CROSSROADS randomised controlled trial.
        Diabetologia. 2016; 59: 945-953
        • Sjostrom L.
        • Lindroos A.
        • Peltonen M.
        • et al.
        • for the Swedish Obese Subjects Study Scientific Group
        Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery.
        N Engl J Med. 2004; 351: 2683-2693
        • Adams T.D.
        • Davidson L.E.
        • Litwin S.E.
        • et al.
        Weight and metabolic outcomes 12 years after gastric bypass.
        N Engl J Med. 2017; 377: 1143-1155
        • Sjostrom L.
        Review of the key results from the Swedish Obese Subjects (SOS) trial - a prospective controlled intervention study of bariatric surgery.
        J Intern Med. 2013; 273: 219-234
        • Karlsson F.H.
        • Tremaroli V.
        • Nookaew I.
        • et al.
        Gut metagenome in European women with normal, impaired and diabetic glucose control.
        Nature. 2013; 498: 99-103
        • Qin J.
        • Li Y.
        • Cai Z.
        • et al.
        A metagenome-wide association study of gut microbiota in type 2 diabetes.
        Nature. 2012; 490: 55-60
        • Murphy R.
        • Tsai P.
        • Jullig M.
        • et al.
        Differential changes in gut microbiota after gastric bypass and sleeve gastrectomy bariatric surgery vary according to diabetes remission.
        Obes Surg. 2017; 27: 917-925
        • Williams R.R.
        • Hunt S.C.
        • Barlow G.K.
        • et al.
        Health family trees: a tool for finding and helping young family members of coronary and cancer prone pedigrees in Texas and Utah.
        Am J Public Health. 1988; 78: 1283-1286
        • Adams T.D.
        • Avelar E.
        • Cloward T.
        • et al.
        Design and rationale of the Utah obesity study. A study to assess morbidity following gastric bypass surgery.
        Contemp Clin Trials. 2005; 26: 534-551
        • Adams T.D.
        • Davidson L.E.
        • Litwin S.
        • et al.
        Health benefits of gastric bypass surgery after 6 years.
        JAMA. 2012; 308: 1122-1131
        • Smith S.C.
        • Edwards C.B.
        • Goodman G.N.
        • Halversen R.C.
        • Simper S.C.
        Open vs laparoscopic Roux-en-Y gastric bypass: comparison of operative morbidity and mortality.
        Obes Surg. 2004; 14: 73-76
        • Smith S.C.
        • Goodman G.N.
        • Edwards C.B.
        Roux-en-Y gastric bypass: a 7-year retrospective review of 3,855 patients.
        Obes Surg. 1995; 5: 314-318
        • Kozich J.J.
        • Westcott S.L.
        • Baxter N.T.
        • Highlander S.K.
        • Schloss P.D.
        Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform.
        Appl Environ Microbiol. 2013; 79: 5112-5120
        • Bolyen E.
        • Rideout J.R.
        • Dillon M.R.
        • et al.
        Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.
        Nat Biotechnol. 2019; 37: 852-857
        • McDonald D.
        • Price M.N.
        • Goodrich J.
        • et al.
        An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea.
        ISME J. 2012; 6: 610-618
        • Okasen J.
        • Blanchet F.G.
        • Friendly M.
        • et al.
        Vegan: community ecology package.
        R Project for Statistical Computing, Vienna2019
        • Mandal S.
        • Van Treuren W.
        • White R.A.
        • et al.
        Analysis of composition of microbiomes: a novel method for studying microbial composition.
        Microb Ecol Health Dis. 2015; 26: 27663
        • Graessler J.
        • Qin Y.
        • Zhong H.
        • et al.
        Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters.
        Pharmacogenomics J. 2013; 13: 514-522
        • Zhang H.
        • DiBaise J.K.
        • Zuccolo A.
        • et al.
        Human gut microbiota in obesity and after gastric bypass.
        Proc Natl Acad Sci U S A. 2009; 106: 2365-2370
        • Derrien M.
        • Vaughan E.E.
        • Plugge C.M.
        • de Vos W.M.
        Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium.
        Int J Syst Evol Microbiol. 2004; 54: 1469-1476
        • Celiker H.
        A new proposed mechanism of action for gastric bypass surgery: air hypothesis.
        Med Hypotheses. 2017; 107: 81-89
        • Golzarand M.
        • Toolabi K.
        • Djafarian K.
        Changes in body composition, dietary intake, and substrate oxidation in patients underwent laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy: a comparative prospective study.
        Obes Surg. 2019; 29: 406-413
        • Kanerva N.
        • Larsson I.
        • Peltonen M.
        • Lindroos A.K.
        • Carlsson L.M.
        Changes in total energy intake and macronutrient composition after bariatric surgery predict long-term weight outcome: findings from the Swedish Obese Subjects (SOS) study.
        Am J Clin Nutr. 2017; 106: 136-145
        • Eid H.M.
        • Wright M.L.
        • Anil Kumar N.V.
        • et al.
        Significance of microbiota in obesity and metabolic diseases and the modulatory potential by medicinal plant and food ingredients.
        Front Pharmacol. 2017; 8: 387
        • Chelakkot C.
        • Choi Y.
        • Kim D.K.
        • et al.
        Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions.
        Exp Mol Med. 2018; 50e450
        • Belzer C.
        • de Vos W.M.
        Microbes inside–from diversity to function: the case of Akkermansia.
        ISME J. 2012; 6: 1449-1458
        • Guo Y.
        • Huang Z.P.
        • Liu C.Q.
        • et al.
        Modulation of the gut microbiome: a systematic review of the effect of bariatric surgery.
        Eur J Endocrinol. 2018; 178: 43-56
        • Dao M.C.
        • Everard A.
        • Aron-Wisnewsky J.
        • et al.
        Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology.
        Gut. 2016; 65: 426-436
        • Everard A.
        • Belzer C.
        • Geurts L.
        • et al.
        Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity.
        Proc Natl Acad Sci U S A. 2013; 110: 9066-9071
        • de la Cuesta-Zuluaga J.
        • Mueller N.T.
        • Corrales-Agudelo V.
        • et al.
        Metformin is associated with higher relative abundance of mucin-degrading Akkermansia muciniphila and several short-chain fatty acid-producing microbiota in the gut.
        Diabetes Care. 2017; 40: 54-62
        • Forslund K.
        • Hildebrand F.
        • Nielsen T.
        • et al.
        Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota.
        Nature. 2015; 528: 262-266
        • Shin N.R.
        • Lee J.C.
        • Lee H.Y.
        • et al.
        An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice.
        Gut. 2014; 63: 727-735
        • Debedat J.
        • Amouyal C.
        • Aron-Wisnewsky J.
        • Clement K.
        Impact of bariatric surgery on type 2 diabetes: contribution of inflammation and gut microbiome?.
        Semin Immunopathol. 2019; 41: 461-475
        • Cani P.D.
        • de Vos W.M.
        Next-generation beneficial microbes: the case of Akkermansia muciniphila.
        Front Microbiol. 2017; 8: 1765
        • Naito Y.
        • Uchiyama K.
        • Takagi T.
        A next-generation beneficial microbe: Akkermansia muciniphila.
        J Clin Biochem Nutr. 2018; 63: 33-35
        • Depommier C.
        • Everard A.
        • Druart C.
        • et al.
        Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study.
        Nat Med. 2019; 25: 1096-1103
        • Federico A.
        • Dallio M.
        • Tolone S.
        • et al.
        Gastrointestinal hormones, intestinal microbiota and metabolic homeostasis in obese patients: effect of bariatric surgery.
        Vivo. 2016; 30: 321-330