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The Importance of the Microbiome in Bariatric Surgery: a Systematic Review

  • Josianne C. H. B. M. Luijten
  • Guusje Vugts
  • Grard A. P. Nieuwenhuijzen
  • Misha D. P. LuyerEmail author
Review Article

Abstract

Bariatric surgery results in sustained weight loss, improvement of metabolic and hormonal changes, and reduction of comorbidities in obese patients. However, beneficial effects of bariatric surgery are not solely explained by restriction and malabsorption induced by surgery itself. Changes in the microbiome might play a role in this mechanism. A systematic review was performed in which 21 studies were included. The microbiome was affected by surgery and profound changes occurred in the first year of follow-up. An increase in Bacteroides and Proteobacteria and a decrease in Firmicutes were observed postoperatively in most studies. These changes were associated with weight loss. Bariatric surgery induces profound changes in the microbiome. This may be related to the beneficial effect of bariatric surgery on comorbidities associated with obesity.

Keywords

Gut microbiome Bariatric surgery Comorbidities Type 2 diabetes Weight loss Roux-en-Y gastric bypass (RYGB) Sleeve gastrectomy (SG) 

Notes

Author Contributions

All authors equally contributed to this paper. Conception and design of the study: ML and GN; literature review and analysis: JL and GV; drafting and critical revision and editing, and final approval of the final version: JL, GV, ML, and GN.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Statements Regarding Ethics and Consent

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Flegal KM. Epidemiologic aspects of overweight and obesity in the United States. Physiol Behav. 2005;86:599–602.CrossRefGoogle Scholar
  2. 2.
    Sturm R, Hattori A. Morbid obesity rates continue to rise rapidly in the United States. Int J Obes. 2013;37:889–91.CrossRefGoogle Scholar
  3. 3.
    Kushner RF, Kahan S. Introduction: the state of obesity in 2017. Med Clin North Am. 2018;102:1–11.Google Scholar
  4. 4.
    Lazzati A, Guy-Lachuer R, Delaunay V, et al. Bariatric surgery trends in France: 2005-2011. Surg Obes Relat Dis. 2014;10:328–34.CrossRefGoogle Scholar
  5. 5.
    Tadross JA, le Roux CW. The mechanisms of weight loss after bariatric surgery. Int J Obes. 2009;33(Suppl 1):S28–32.CrossRefGoogle Scholar
  6. 6.
    Federico A, Dallio M, Tolone S, et al. Gastrointestinal hormones, intestinal microbiota and metabolic homeostasis in obese patients: effect of bariatric surgery. In vivo. 2016;30:321–30.Google Scholar
  7. 7.
    Reames BN, Finks JF, Bacal D, et al. Changes in bariatric surgery procedure use in Michigan, 2006-2013. JAMA. 2014;312:959–61.CrossRefGoogle Scholar
  8. 8.
    Memarian E, Calling S, Sundquist K, et al. Sociodemographic differences and time trends of bariatric surgery in Sweden 1990-2010. Obes Surg. 2014;24:2109–16.CrossRefGoogle Scholar
  9. 9.
    Cani PD, Delzenne NM. Gut microflora as a target for energy and metabolic homeostasis. Curr Opin Clin Nutr Metab Care. 2007;10:729–34.CrossRefGoogle Scholar
  10. 10.
    Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.CrossRefGoogle Scholar
  11. 11.
    Liou AP, Paziuk M, Luevano Jr JM, et al. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5:178ra41.CrossRefGoogle Scholar
  12. 12.
    Haskins IN, Corcelles R, Froylich D, et al. Primary inadequate weight loss after Roux-en-Y gastric bypass is not associated with poor cardiovascular or metabolic outcomes: experience from a single institution. Obes Surg. 2017;27:676–80.CrossRefGoogle Scholar
  13. 13.
    Furet JP, Kong LC, Tap J, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010;59:3049–57.CrossRefGoogle Scholar
  14. 14.
    Akbay E, Yetkin I, Ersoy R, et al. The relationship between levels of alpha1-acid glycoprotein and metabolic parameters of diabetes mellitus. Diabetes Nutr Metab. 2004;17:331–5.Google Scholar
  15. 15.
    Kang Y, Cai Y. Gut microbiota and obesity: implications for fecal microbiota transplantation therapy. Hormones. 2017;16:223–34.CrossRefGoogle Scholar
  16. 16.
    Swank GM, Deitch EA. Role of the gut in multiple organ failure: bacterial translocation and permeability changes. World J Surg. 1996;20:411–7.CrossRefGoogle Scholar
  17. 17.
    Ley RE, Backhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070–5.CrossRefGoogle Scholar
  18. 18.
    Le Chatelier E, Nielsen T, Qin J, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500:541–6.CrossRefGoogle Scholar
  19. 19.
    Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.CrossRefGoogle Scholar
  20. 20.
    Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009;106:2365–70.CrossRefGoogle Scholar
  21. 21.
    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;13:514–22.CrossRefGoogle Scholar
  22. 22.
    Kong LC, 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.CrossRefGoogle Scholar
  23. 23.
    Damms-Machado A, Mitra S, Schollenberger AE, et al. Effects of surgical and dietary weight loss therapy for obesity on gut microbiota composition and nutrient absorption. Biomed Res Int. 2015;2015:806248.CrossRefGoogle Scholar
  24. 24.
    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;22:228–38.CrossRefGoogle Scholar
  25. 25.
    Patrone V, Vajana E, Minuti A, et al. Postoperative changes in fecal bacterial communities and fermentation products in obese patients undergoing bilio-intestinal bypass. Front Microbiol. 2016;7:200.CrossRefGoogle Scholar
  26. 26.
    Palleja A, Kashani A, Allin KH, 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.CrossRefGoogle Scholar
  27. 27.
    Murphy R, Evennett NJ, Clarke MG, et al. Sleeve gastrectomy versus Roux-en-Y gastric bypass for type 2 diabetes and morbid obesity: double-blind randomised clinical trial protocol. BMJ Open. 2016;6:e011416.CrossRefGoogle Scholar
  28. 28.
    Ilhan ZE, DiBaise JK, Isern NG, et al. Distinctive microbiomes and metabolites linked with weight loss after gastric bypass, but not gastric banding. ISME J. 2017;11:2047–58.CrossRefGoogle Scholar
  29. 29.
    Sanmiguel CP, Jacobs J, Gupta A, et al. Surgically induced changes in gut microbiome and hedonic eating as related to weight loss: preliminary findings in obese women undergoing bariatric surgery. Psychosom Med. 2017;79:880–7.CrossRefGoogle Scholar
  30. 30.
    Medina DA, Pedreros JP, Turiel D, et al. Distinct patterns in the gut microbiota after surgical or medical therapy in obese patients. PeerJ. 2017;5:e3443.CrossRefGoogle Scholar
  31. 31.
    Liu R, Hong J, Xu X, et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nat Med. 2017;23:859–68.CrossRefGoogle Scholar
  32. 32.
    Chen H, Qian L, Lv Q, et al. Change in gut microbiota is correlated with alterations in the surface molecule expression of monocytes after Roux-en-Y gastric bypass surgery in obese type 2 diabetic patients. Am J Transl Res. 2017;9:1243–54.Google Scholar
  33. 33.
    Campisciano G, Cason C, Palmisano S, et al. Bariatric surgery drives major rearrangements of the intestinal microbiota including the biofilm composition. Front Biosci (Elite Ed). 2018;10:495–505.Google Scholar
  34. 34.
    Campisciano G, Palmisano S, Cason C, et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benefic Microbes. 2018;9:367–73.CrossRefGoogle Scholar
  35. 35.
    Aron-Wisnewsky J, Prifti E, Belda E, Ichou F, Kayser BD, Dao MC, et al. Major microbiota dysbiosis in severe obesity: fate after bariatric surgery. Gut. 2019;68(1):70–82Google Scholar
  36. 36.
    Kikuchi R, Irie J, Yamada-Goto N, et al. The impact of laparoscopic sleeve gastrectomy with duodenojejunal bypass on intestinal microbiota differs from that of laparoscopic sleeve gastrectomy in Japanese patients with obesity. Clin Drug Investig. 2018;38:545–52.CrossRefGoogle Scholar
  37. 37.
    Kumar R, Grams J, Chu DI, et al. New microbe genomic variants in patients fecal community following surgical disruption of the upper human gastrointestinal tract. HUMIC. 2018;10:37–42.Google Scholar
  38. 38.
    Cortez RV, Petry T, Caravatto P, et al. Shifts in intestinal microbiota after duodenal exclusion favor glycemic control and weight loss: a randomized controlled trial. Surg Obes Relat Dis. 2018;14:1748–54.CrossRefGoogle Scholar
  39. 39.
    Hong S-H, Bunge J, Jeon S-O, et al. Predicting microbial species richness. Proc Natl Acad Sci U S A. 2006;103:117–22.CrossRefGoogle Scholar
  40. 40.
    Li M, Wang B, Zhang M, et al. Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci U S A. 2008;105:2117–22.CrossRefGoogle Scholar
  41. 41.
    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;27:917–25.CrossRefGoogle Scholar
  42. 42.
    Backhed F, Manchester JK, Semenkovich CF, et al. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A. 2007;104:979–84.CrossRefGoogle Scholar
  43. 43.
    Gagliardi A, Totino V, Cacciotti F, et al. Rebuilding the gut microbiota ecosystem. Int J Environ Res Public Health. 2018;15(8)Google Scholar
  44. 44.
    Nishida A, Inoue R, Inatomi O, et al. Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol. 2018;11:1–10.CrossRefGoogle Scholar
  45. 45.
    Costello SP, Waters O, Bryant RV, et al. Short duration, low intensity, pooled fecal microbiota transplantation induces remission in patients with mild-moderately active ulcerative colitis: a randomised controlled trial. Gastroenterology. 2017;152:S198–S9.CrossRefGoogle Scholar
  46. 46.
    Paramsothy S, Kamm MA, Kaakoush NO, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017;389:1218–28.CrossRefGoogle Scholar
  47. 47.
    Khanna S, Vazquez-Baeza Y, Gonzalez A, et al. Changes in microbial ecology after fecal microbiota transplantation for recurrent C difficile infection affected by underlying inflammatory bowel disease. Microbiome. 2017;5:55.CrossRefGoogle Scholar
  48. 48.
    van Praagh JB, de Goffau MC, Bakker IS, et al. Intestinal microbiota and anastomotic leakage of stapled colorectal anastomoses: a pilot study. Surg Endosc. 2016;30:2259–65.CrossRefGoogle Scholar
  49. 49.
    van Praagh JB, de Goffau MC, Bakker IS, van Goor H, Harmsen HJM, Olinga P, et al. Mucus microbiome of anastomotic tissue during surgery has predictive value for colorectal anastomotic leakage. Ann Surg. 2018. [ePub ahead of print]Google Scholar
  50. 50.
    Reddy RM, Weir WB, Barnett S, et al. Increased variance in oral and gastric microbiome correlates with esophagectomy anastomotic leak. Ann Thorac Surg. 2018;105:865–70.CrossRefGoogle Scholar
  51. 51.
    Castaner O, Goday A, Park YM, et al. The gut microbiome profile in obesity: a systematic review. Int J Endocrinol. 2018;2018:4095789.Google Scholar
  52. 52.
    Liu H, Hu C, Zhang X, et al. Role of gut microbiota, bile acids and their cross-talk in the effects of bariatric surgery on obesity and type 2 diabetes. J Diabetes Investig. 2018;9:13–20.CrossRefGoogle Scholar
  53. 53.
    Guo Y, Huang ZP, Liu CQ, et al. Modulation of the gut microbiome: a systematic review of the effect of bariatric surgery. Eur J Endocrinol. 2018;178:43–56.CrossRefGoogle Scholar
  54. 54.
    Ejtahed HS, Angoorani P, Hasani-Ranjbar S, et al. Adaptation of human gut microbiota to bariatric surgeries in morbidly obese patients: a systematic review. Microb Pathog. 2018;116:13–21.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of ResearchNetherlands Comprehensive Cancer Organization (IKNL)UtrechtThe Netherlands
  2. 2.Department of SurgeryCatharina HospitalEindhovenThe Netherlands

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