The importance of the gut microbiota after bariatric surgery

Abstract

The gut microbiota is recognized to have an important role in energy storage and the subsequent development of obesity. To date, bariatric surgery (indicated for severe obesity) represents the only treatment that enables substantial and sustained weight loss. Bariatric surgery is also a good model to study not only the pathophysiology of obesity and its related diseases but also the mechanisms involved in their improvement after weight reduction. Scarce data from humans and animal models have demonstrated that gut microbiota composition is modified after Roux-en-Y gastric bypass (RYGB), suggesting that weight reduction could affect gut microbiota composition. However, weight loss might not be the only factor responsible for those modifications. Indeed, bariatric surgery not only improves hormonal and inflammatory status, but also induces numerous changes in the digestive tract that might account for the observed modifications of microbiota ecology. In future bariatric surgery studies in humans or mice, these major surgery-induced modifications will need to be taken into account when analyzing the link between gut microbiota composition, obesity, its complications and their improvement after bariatric surgery. This Review outlines the potential mechanisms by which the major changes in the digestive tract after bariatric surgery can affect the gut microbiota.

Key Points

  • Obesity is associated with dysbiosis of the gut microbiota, in particular with decreased bacterial diversity

  • Bariatric surgery represents a successful treatment option for severe obesity, and is also a good model to study the mechanisms involved in weight reduction and obesity-related disease improvement

  • Bariatric surgery is associated with major modifications in microbiota composition and function; to date, however, only limited data are available concerning gut microbiota composition after bariatric surgery

  • In particular, RYGB induces important changes in the digestive tract, namely gastric-pouch narrowing, decreased acid production and anatomical gut rearrangement, which might have an affect on the gut microbiota

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Characteristics of the normal gastrointestinal tract.
Figure 2: The three main bariatric surgical interventions.
Figure 3: Roux-en-Y gastric bypass induces various environmental, systemic and anatomical changes that might directly or indirectly affect the composition of the gut microbiota.

References

  1. 1

    Penders, J. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118, 511–521 (2006).

    Article  PubMed  Google Scholar 

  2. 2

    Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A. & Brown, P. O. Development of the human infant intestinal microbiota. PLoS Biol. 5, e177 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 3

    Marchesi, J. R. Human distal gut microbiome. Environ. Microbiol. 13, 3088–3102 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  4. 4

    Shendure, J. & Ji, H. Next-generation DNA sequencing. Nat. Biotechnol. 26, 1135–1145 (2008).

    Article  CAS  PubMed  Google Scholar 

  5. 5

    DiBaise, J. K. et al. Gut microbiota and its possible relationship with obesity. Mayo Clin. Proc. 83, 460–469 (2008).

    Article  PubMed  Google Scholar 

  6. 6

    Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 7

    Clemente, J. C., Ursell, L. K., Parfrey, L. W. & Knight, R. The impact of the gut microbiota on human health: an integrative view. Cell 148, 1258–1270 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 8

    Turnbaugh, P. J. et al. The human microbiome project. Nature 449, 804–810 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Tap, J. et al. Towards the human intestinal microbiota phylogenetic core. Environ. Microbiol. 11, 2574–2584 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10

    Flegal, K. M., Carroll, M. D., Ogden, C. L. & Curtin, L. R. Prevalence and trends in obesity among US adults, 1999–2008. JAMA 303, 235–241 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Kopelman, P. G. Obesity as a medical problem. Nature 404, 635–643 (2000).

    Article  CAS  PubMed  Google Scholar 

  12. 12

    Backhed, F. et al. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl Acad. Sci. USA 101, 15718–15723 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    Backhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A. & Gordon, J. I. Host-bacterial mutualism in the human intestine. Science 307, 1915–1920 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    Backhed, F., Manchester, J. K., Semenkovich, C. F. & Gordon, J. I. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl Acad. Sci. USA 104, 979–984 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    Cani, P. D., Delzenne, N. M., Amar, J. & Burcelin, R. Role of gut microflora in the development of obesity and insulin resistance following high-fat diet feeding. Pathol. Biol. (Paris) 56, 305–309 (2008).

    Article  CAS  Google Scholar 

  16. 16

    Henao-Mejia, J. et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482, 179–185 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    Serino, M. et al. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut 61, 543–553 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 18

    Hildebrandt, M. A. et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137, 1716–1724 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 19

    Turnbaugh, P. J., Backhed, F., Fulton, L. & Gordon, J. I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213–223 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 20

    Astrup, A., Dyerberg, J., Selleck, M. & Stender, S. Nutrition transition and its relationship to the development of obesity and related chronic diseases. Obes. Rev. 9 (Suppl. 1), 48–52 (2008).

    Article  PubMed  Google Scholar 

  21. 21

    Santacruz, A. et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring) 17, 1906–1915 (2009).

    Article  Google Scholar 

  22. 22

    Tilg, H. & Kaser, A. Gut microbiome, obesity, and metabolic dysfunction. J. Clin. Invest. 121, 2126–2132 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. 23

    Prakash, S., Tomaro-Duchesneau, C., Saha, S. & Cantor, A. The gut microbiota and human health with an emphasis on the use of microencapsulated bacterial cells. J. Biomed. Biotechnol. 981214 (2011).

  24. 24

    Dicksved, J. et al. Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls. J. Med. Microbiol. 58 (Pt 4), 509–516 (2009).

    Article  CAS  PubMed  Google Scholar 

  25. 25

    Guarner, F. & Malagelada, J. R. Gut flora in health and disease. Lancet 361, 512–519 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  26. 26

    Midtvedt, T. Microbial bile acid transformation. Am. J. Clin. Nutr. 27, 1341–1347 (1974).

    Article  CAS  PubMed  Google Scholar 

  27. 27

    Ridlon, J. M., Kang, D. J. & Hylemon, P. B. Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47, 241–259 (2006).

    Article  CAS  PubMed  Google Scholar 

  28. 28

    Kurdi, P., Kawanishi, K., Mizutani, K. & Yokota, A. Mechanism of growth inhibition by free bile acids in lactobacilli and bifidobacteria. J. Bacteriol. 188, 1979–1986 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  30. 30

    Sonnenburg, J. L. et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307, 1955–1959 (2005).

    Article  CAS  PubMed  Google Scholar 

  31. 31

    Gill, S. R. et al. Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 32

    Topping, D. L. & Clifton, P. M. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 81, 1031–1064 (2001).

    Article  CAS  PubMed  Google Scholar 

  33. 33

    Schwiertz, A. et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring) 18, 190–195 (2010).

    Article  Google Scholar 

  34. 34

    Ley, R. E. et al. Obesity alters gut microbial ecology. Proc. Natl Acad. Sci. USA 102, 11070–11075 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 35

    Clarke, S. et al. The gut microbiota and its relationship to diet and obesity: new insights. Gut Microbes 3 (2012).

  36. 36

    Armougom, F., Henry, M., Vialettes, B., Raccah, D. & Raoult, D. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PLoS ONE 4, e7125 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 37

    Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 38

    Duncan, S. H. et al. Human colonic microbiota associated with diet, obesity and weight loss. Int. J. Obes. (Lond.) 32, 1720–1724 (2008).

    Article  CAS  Google Scholar 

  39. 39

    Duncan, S. H. et al. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 73, 1073–1078 (2007).

    Article  CAS  Google Scholar 

  40. 40

    Jumpertz, R. et al. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am. J. Clin. Nutr. 94, 58–65 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 41

    Harris, K., Kassis, A., Major, G. & Chou, C. J. Is the gut microbiota a new factor contributing to obesity and its metabolic disorders? J. Obes. 879151 (2012).

  42. 42

    Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 43

    Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174–180 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 44

    Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105–108 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. 45

    Yatsunenko, T. et al. human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 46

    Dyson, P. A. The therapeutics of lifestyle management on obesity. Diabetes Obes. Metab. 12, 941–946 (2010).

    Article  CAS  PubMed  Google Scholar 

  47. 47

    Wing, R. R. & Phelan, S. Long-term weight loss maintenance. Am. J. Clin. Nutr. 82 (1 Suppl.), 222S–225S (2005).

    Article  CAS  PubMed  Google Scholar 

  48. 48

    Sjöström, L. et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N. Engl. J. Med. 351, 2683–2693 (2004).

    Article  PubMed  Google Scholar 

  49. 49

    Ioannides-Demos, L. L., Piccenna, L. & McNeil, J. J. Pharmacotherapies for obesity: past, current, and future therapies. J. Obes. 179674 (2011).

  50. 50

    Frachon, I. et al. Benfluorex and unexplained valvular heart disease: a case-control study. PLoS ONE 5, e10128 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 51

    Sachdev, M., Miller, W. C., Ryan, T. & Jollis, J. G. Effect of fenfluramine-derivative diet pills on cardiac valves: a meta-analysis of observational studies. Am. Heart J. 144, 1065–1073 (2002).

    Article  CAS  PubMed  Google Scholar 

  52. 52

    Rich, S., Rubin, L., Walker, A. M., Schneeweiss, S. & Abenhaim, L. Anorexigens and pulmonary hypertension in the United States: results from the surveillance of North American pulmonary hypertension. Chest 117, 870–874 (2000).

    Article  CAS  PubMed  Google Scholar 

  53. 53

    Sjostrom, L. et al. Bariatric surgery and long-term cardiovascular events. JAMA 307, 56–65 (2012).

    Article  PubMed  Google Scholar 

  54. 54

    Buchwald, H. et al. Bariatric surgery: a systematic review and meta-analysis. JAMA 292, 1724–1737 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. 55

    Dixon, J. B., Straznicky, N. E., Lambert, E. A., Schlaich, M. P. & Lambert, G. W. Surgical approaches to the treatment of obesity. Nat. Rev. Gastroenterol. Hepatol. 8, 429–437 (2011).

    Article  PubMed  Google Scholar 

  56. 56

    Buchwald, H. Consensus Conference Panel. Consensus conference statement bariatric surgery for morbid obesity: health implications for patients, health professionals, and third-party payers. Surg. Obes. Relat. Dis. 1, 371–381 (2005).

    Article  PubMed  Google Scholar 

  57. 57

    Sandoval, D. Bariatric surgeries: beyond restriction and malabsorption. Int. J. Obes. (Lond.) 35 (Suppl. 3), S45–S49 (2011).

    Article  Google Scholar 

  58. 58

    Chopra, T., Zhao, J. J., Alangaden, G., Wood, M. H. & Kaye, K. S. Preventing surgical site infections after bariatric surgery: value of perioperative antibiotic regimens. Expert Rev. Pharmacoecon. Outcomes Res. 10, 317–328 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59

    No authors listed] ASHP Therapeutic Guidelines on Antimicrobial Prophylaxis in Surgery. American Society of Health-System Pharmacists. Am. J. Health Syst. Pharm. 56, 1839–1888 (1999).

  60. 60

    Favretti, F., O'Brien, P. E. & Dixon, J. B. Patient management after LAP-BAND placement. Am. J. Surg. 184, 38S–41S (2002).

    Article  PubMed  Google Scholar 

  61. 61

    Godlewski, A. E. et al. Effect of dental status on changes in mastication in patients with obesity following bariatric surgery. PLoS ONE 6, e22324 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 62

    Brunault, P. et al. Observations regarding 'quality of life' and 'comfort with food' after bariatric surgery: comparison between laparoscopic adjustable gastric banding and sleeve gastrectomy. Obes. Surg. 21, 1225–1231 (2011).

    Article  PubMed  Google Scholar 

  63. 63

    Peterli, R. et al. Metabolic and hormonal changes after laparoscopic Roux-en-Y gastric bypass and sleeve gastrectomy: a randomized, prospective trial. Obes. Surg. 22, 740–748 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  64. 64

    Basso, N. et al. First-phase insulin secretion, insulin sensitivity, ghrelin, GLP-1, and PYY changes 72 h after sleeve gastrectomy in obese diabetic patients: the gastric hypothesis. Surg. Endosc. 25, 3540–3550 (2011).

    Article  CAS  PubMed  Google Scholar 

  65. 65

    El Oufir, L. et al. Relations between transit time, fermentation products, and hydrogen consuming flora in healthy humans. Gut 38, 870–877 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. 66

    Laferrère, B. et al. Effect of weight loss by gastric bypass surgery versus hypocaloric diet on glucose and incretin levels in patients with type 2 diabetes. J. Clin. Endocrinol. Metab. 93, 2479–2485 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 67

    Reed, M. A. et al. Roux-en-Y gastric bypass corrects hyperinsulinemia implications for the remission of type 2 diabetes. J. Clin. Endocrinol. Metab. 96, 2525–2531 (2011).

    Article  CAS  PubMed  Google Scholar 

  68. 68

    Laferrère, B. et al. Incretin levels and effect are markedly enhanced 1 month after Roux-en-Y gastric bypass surgery in obese patients with type 2 diabetes. Diabetes Care 30, 1709–1716 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 69

    Beckman, L. M., Beckman, T. R. & Earthman, C. P. Changes in gastrointestinal hormones and leptin after Roux-en-Y gastric bypass procedure: a review. J. Am. Diet. Assoc. 110, 571–584 (2010).

    CAS  Google Scholar 

  70. 70

    Ashrafian, H. et al. Diabetes resolution and hyperinsulinaemia after metabolic Roux-en-Y gastric bypass. Obes. Rev. 12, e257–272 (2011).

    Article  CAS  PubMed  Google Scholar 

  71. 71

    Ashrafian, H. et al. Metabolic surgery: an evolution through bariatric animal models. Obes. Rev. 11, 907–920 (2010).

    Article  CAS  PubMed  Google Scholar 

  72. 72

    Ciangura, C. et al. Dynamics of change in total and regional body composition after gastric bypass in obese patients. Obesity (Silver Spring) 18, 760–765 (2010).

    Article  Google Scholar 

  73. 73

    Dalmas, E. et al. Variations in circulating inflammatory factors are related to changes in calorie and carbohydrate intakes early in the course of surgery-induced weight reduction. Am. J. Clin. Nutr. 94, 450–458 (2011).

    Article  CAS  PubMed  Google Scholar 

  74. 74

    Aron-Wisnewsky, J. et al. Human adipose tissue macrophages: m1 and m2 cell surface markers in subcutaneous and omental depots and after weight loss. J. Clin. Endocrinol. Metab. 94, 4619–4623 (2009).

    Article  CAS  PubMed  Google Scholar 

  75. 75

    Cancello, R. et al. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 54, 2277–2286 (2005).

    Article  CAS  PubMed  Google Scholar 

  76. 76

    Poitou, C. et al. CD14dimCD16+ and CD14+CD16+ monocytes in obesity and during weight loss: relationships with fat mass and subclinical atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 31, 2322–2330 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. 77

    Shin, A. C., Zheng, H., Pistell, P. J. & Berthoud, H. R. Roux-en-Y gastric bypass surgery changes food reward in rats. Int. J. Obes. (Lond.) 35, 642–651 (2011).

    Article  CAS  Google Scholar 

  78. 78

    le Roux, C. W. et al. Gastric bypass reduces fat intake and preference. Am. J. Physiol. Regul. Integr Comp. Physiol. 301, R1057–R1066 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. 79

    Zhang, H. et al. Human gut microbiota in obesity and after gastric bypass. Proc. Natl Acad. Sci. USA 106, 2365–2370 (2009).

    Article  Google Scholar 

  80. 80

    Furet, J. P. et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59, 3049–3057 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. 81

    US National Library of Medicine. Adaptation of Human Gut Microbiota to Energetic Restriction (microbaria). ClinicalTrials.gov[online], (2011).

  82. 82

    Li, J. V. et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut 60, 1214–1223 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. 83

    Li, J. V. et al. Experimental bariatric surgery in rats generates a cytotoxic chemical environment in the gut contents. Front. Microbiol. 2, 183 (2011).

    PubMed  PubMed Central  Google Scholar 

  84. 84

    Smith, C. D. et al. Gastric acid secretion and vitamin B12 absorption after vertical Roux-en-Y gastric bypass for morbid obesity. Ann. Surg. 218, 91–96 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. 85

    Ishida, R. K. et al. Microbial flora of the stomach after gastric bypass for morbid obesity. Obes. Surg. 17, 752–758 (2007).

    Article  PubMed  Google Scholar 

  86. 86

    Prachand, V. N. & Alverdy, J. C. Gastroesophageal reflux disease and severe obesity: Fundoplication or bariatric surgery? World J. Gastroenterol. 16, 3757–3761 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  87. 87

    Frezza, E. E. et al. Symptomatic improvement in gastroesophageal reflux disease (GERD) following laparoscopic Roux-en-Y gastric bypass. Surg. Endosc. 16, 1027–1031 (2002).

    Article  CAS  PubMed  Google Scholar 

  88. 88

    O'May, G. A., Reynolds, N. & Macfarlane, G. T. Effect of pH on an in vitro model of gastric microbiota in enteral nutrition patients. Appl. Environ. Microbiol. 71, 4777–4783 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. 89

    Giannella, R. A., Broitman, S. A. & Zamcheck, N. Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13, 251–256 (1972).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. 90

    O'May, G. A., Reynolds, N., Smith, A. R., Kennedy, A. & Macfarlane, G. T. Effect of pH and antibiotics on microbial overgrowth in the stomachs and duodena of patients undergoing percutaneous endoscopic gastrostomy feeding. J. Clin. Microbiol. 43, 3059–3065 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  91. 91

    Williams, C. Occurrence and significance of gastric colonization during acid-inhibitory therapy. Best Pract. Res. Clin. Gastroenterol. 15, 511–521 (2001).

    Article  CAS  PubMed  Google Scholar 

  92. 92

    Theisen, J. et al. Suppression of gastric acid secretion in patients with gastroesophageal reflux disease results in gastric bacterial overgrowth and deconjugation of bile acids. J. Gastrointest. Surg. 4, 50–54 (2000).

    Article  CAS  PubMed  Google Scholar 

  93. 93

    Fried, M. et al. Duodenal bacterial overgrowth during treatment in outpatients with omeprazole. Gut 35, 23–26 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. 94

    Walker, A. W. et al. pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl. Environ. Microbiol. 71, 3692–3700 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. 95

    Midtvedt, T., Norman, A. & Nygaard, K. Bile acid transforming micro-organisms in rats with an intestinal blind segment. Acta Pathol. Microbiol. Scand. 77, 162–166 (1969).

    Article  CAS  PubMed  Google Scholar 

  96. 96

    Swann, J. R. et al. Systemic gut microbial modulation of bile acid metabolism in host tissue compartments. Proc. Natl Acad. Sci. USA 108 (Suppl. 1), 4523–4530 (2011).

    Article  PubMed  Google Scholar 

  97. 97

    Patti, M. E. et al. Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity (Silver Spring) 17, 1671–1677 (2009).

    Article  CAS  Google Scholar 

  98. 98

    Islam, K. B. et al. Bile acid is a host factor that regulates the composition of the cecal microbiota in rats. Gastroenterology 141, 1773–1781 (2011).

    Article  CAS  PubMed  Google Scholar 

  99. 99

    Binder, H. J., Filburn, B. & Floch, M. Bile acid inhibition of intestinal anaerobic organisms. Am. J. Clin. Nutr. 28, 119–125 (1975).

    Article  CAS  PubMed  Google Scholar 

  100. 100

    Dorman, R. B. et al. Risk for hospital readmission following bariatric surgery. PLoS ONE 7, e32506 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. 101

    Cotter, P. D., Stanton, C., Ross, R. P. & Hill, C. The impact of antibiotics on the gut microbiota as revealed by high throughput DNA sequencing. Discov. Med. 13, 193–199 (2012).

    PubMed  Google Scholar 

  102. 102

    Antonopoulos, D. A. et al. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect. Immun. 77, 2367–2375 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. 103

    Ubeda, C. et al. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J. Clin. Invest. 120, 4332–4341 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. 104

    Dethlefsen, L., Huse, S., Sogin, M. L. & Relman, D. A. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6, e280 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. 105

    Claesson, M. J. et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc. Natl Acad. Sci. USA 108 (Suppl. 1), 4586–4591 (2011).

    Article  PubMed  Google Scholar 

  106. 106

    Dethlefsen, L. & Relman, D. A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl Acad. Sci. USA 108 (Suppl. 1), 4554–4561 (2011).

    Article  PubMed  Google Scholar 

  107. 107

    Miras, A. D. & le Roux, C. W. Bariatric surgery and taste: novel mechanisms of weight loss. Curr. Opin. Gastroenterol. 26, 140–145 (2010).

    Article  PubMed  Google Scholar 

  108. 108

    Cani, P. D. et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761–1772 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. 109

    Turnbaugh, P. J. et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1, 6ra14 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. 110

    Ravussin, Y. et al. Responses of gut microbiota to diet composition and weight loss in lean and obese mice. Obesity (Silver Spring) 20, 738–747 (2012).

    Article  CAS  Google Scholar 

  111. 111

    Nadal, I. et al. Shifts in clostridia, bacteroides and immunoglobulin-coating fecal bacteria associated with weight loss in obese adolescents. Int. J. Obes. (Lond.) 33, 758–767 (2009).

    Article  CAS  Google Scholar 

  112. 112

    Walker, A. W. et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 5, 220–230 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. 113

    Di Marzo, V., Bifulco, M. & De Petrocellis, L. The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug Discov. 3, 771–784 (2004).

    Article  CAS  PubMed  Google Scholar 

  114. 114

    Laferrère, B. Do we really know why diabetes remits after gastric bypass surgery? Endocrine 40, 162–167 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. 115

    Thaler, J. P. & Cummings, D. E. Minireview: Hormonal and metabolic mechanisms of diabetes remission after gastrointestinal surgery. Endocrinology 150, 2518–2525 (2009).

    Article  CAS  PubMed  Google Scholar 

  116. 116

    Mathurin, P. et al. Prospective study of the long-term effects of bariatric surgery on liver injury in patients without advanced disease. Gastroenterology 137, 532–540 (2009).

    Article  CAS  Google Scholar 

  117. 117

    Everard, A. et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60, 2775–2786 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. 118

    Shi, H. et al. TRL4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015–3025 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. 119

    Musso, G., Gambino, R. & Cassader, M. Obesity, diabetes and gut microbiota: the hygiene hypothesis expanded. Diabetes Care 33, 2277–2284 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  120. 120

    Nie, B. et al. Specific bile acids inhibit hepatic fatty acid uptake. Hepatology http://dx.doi.org/10.1002/hep.25797.

  121. 121

    le Roux, C. W. et al. Gut hormones as mediators of appetite and weight loss after Roux-en-Y gastric bypass. Ann. Surg. 246, 780–785 (2007).

    Article  PubMed  Google Scholar 

  122. 122

    le Roux, C. W. et al. Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann. Surg. 243, 108–114 (2006).

    Article  Google Scholar 

  123. 123

    Asmar, M. New physiological effects of the incretin hormones GLP-1 and GIP. Dan. Med. Bull. 58, B4248 (2011).

    PubMed  Google Scholar 

  124. 124

    Vella, A. & Rizza, R. A. Extrapancreatic effects of GIP and GLP-1. Horm. Metab. Res. 36, 830–836 (2004).

    Article  CAS  PubMed  Google Scholar 

  125. 125

    Flint, H. J. Obesity and the gut microbiota. J. Clin. Gastroenterol. 45 (Suppl.), S128–S132 (2011).

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Contributions

J. Aron-Wisnewsky contributed to the research, discussion of content and writing of this manuscript. J. Doré and K. Clement contributed to the discussion of content, writing and reviewing/editing the manuscript before submission.

Corresponding author

Correspondence to Judith Aron-Wisnewsky.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Aron-Wisnewsky, J., Doré, J. & Clement, K. The importance of the gut microbiota after bariatric surgery. Nat Rev Gastroenterol Hepatol 9, 590–598 (2012). https://doi.org/10.1038/nrgastro.2012.161

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing