The Gut Microbiota as a Mediator of Metabolic Benefits after Bariatric Surgery

Canadian Journal of Diabetes

Volumn 41, Issue 4, 2017, Pages 439-447

  Anhê, Fernando F ^a,b   Varin, Thibault V ^b   Schertzer, Jonathan D ^c   Marette, André ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

gastric bypass; glycemic control and bile acids; Roux en Y; sleeve gastrectomy

Indexed keywords

SHORT CHAIN FATTY ACID;

ACTINOBACTERIA; AMINO ACID METABOLISM; ANAEROBIC CAPACITY; BACTEROIDETES; BARIATRIC SURGERY; BILE ACID METABOLISM; BILE ACID SYNTHESIS; BILIOPANCREATIC BYPASS; CECUM; CELL MOTILITY; CHLOROFLEXI; CONTROLLED STUDY; FATTY ACID METABOLISM; FECES MICROFLORA; FIBROBACTERES; FIRMICUTES; FUSOBACTERIA; GASTRIC BANDING; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLYCEMIC CONTROL; HUMAN; INTESTINE BYPASS; INTESTINE FLORA; LAPAROSCOPIC SLEEVE GASTRECTOMY; MICROBIAL COMMUNITY; MICROBIAL DEGRADATION; NONHUMAN; PROTEOBACTERIA; REVIEW; ROUX-EN-Y GASTRIC BYPASS; SPECIES RICHNESS; SPIROCHETE; SULFUR BACTERIUM; SYNTHESIS; VERRUCOMICROBIA; WEIGHT REDUCTION; GASTROINTESTINAL TRACT; METABOLISM; OBESITY; PHYSIOLOGY; TRENDS;

BARIATRIC SURGERY; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; OBESITY;

EID: 85019949133     PISSN: 14992671     EISSN: 23523840     Source Type: Journal    
DOI: 10.1016/j.jcjd.2017.02.002     Document Type: Review

References (116)

1. Jaacks, L.M., Siegel, K.R., Gujral, U.P., Narayan, K.M., Type 2 diabetes: A 21st century epidemic. Best Pract Res Clin Endocrinol Metab 30 (2016), 331–343.
2. Dyson, P.A., The therapeutics of lifestyle management on obesity. Diabetes Obes Metab 12 (2010), 941–946.
3. Phelan, S., Wing, R.R., Prevalence of successful weight loss. Arch Intern Med, 165, 2005, 2430.
4. Kang, J.G., Park, C.Y., Anti-obesity drugs: A review about their effects and safety. Diabetes Metab J 36 (2012), 13–25.
5. Sjostrom, L., Lindroos, A.K., Peltonen, M., et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 351 (2004), 2683–2693.
6. Sjostrom, L., Peltonen, M., Jacobson, P., et al. Bariatric surgery and long-term cardiovascular events. JAMA 307 (2012), 56–65.
7. Anhe, F.F., Varin, T.V., Le Barz, M., et al. Gut microbiota dysbiosis in obesity-linked metabolic diseases and prebiotic potential of polyphenol-rich extracts. Curr Obes Rep 4 (2015), 389–400.
8. Arora, T., Backhed, F., The gut microbiota and metabolic disease: Current understanding and future perspectives. J Intern Med 280 (2016), 339–349.
9. Samuel, I., Mason, E.E., Renquist, K.E., et al. Bariatric surgery trends: An 18-year report from the International Bariatric Surgery Registry. Am J Surg 192 (2006), 657–662.
10. Ochner, C.N., Kwok, Y., Conceicao, E., et al. Selective reduction in neural responses to high calorie foods following gastric bypass surgery. Ann Surg 253 (2011), 502–507.
11. Angrisani, L., Santonicola, A., Iovino, P., et al. Bariatric surgery worldwide 2013. Obes Surg 25 (2015), 1822–1832.
12. Sjostrom, L., Narbro, K., Sjostrom, C.D., et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med 357 (2007), 741–752.
13. Werling, M., Fandriks, L., Bjorklund, P., et al. Long-term results of a randomized clinical trial comparing Roux-en-Y gastric bypass with vertical banded gastroplasty. Br J Surg 100 (2013), 222–230.
14. Paluszkiewicz, R., Kalinowski, P., Wroblewski, T., et al. Prospective randomized clinical trial of laparoscopic sleeve gastrectomy versus open Roux-en-Y gastric bypass for the management of patients with morbid obesity. Wideochir Inne Tech Maloinwazyjne 7 (2012), 225–232.
15. Ashrafian, H., Bueter, M., Ahmed, K., et al. Metabolic surgery: An evolution through bariatric animal models. Obes Rev 11 (2010), 907–920.
16. Thirlby, R.C., Bahiraei, F., Randall, J., Drewnoski, A., Effect of Roux-en-Y gastric bypass on satiety and food likes: The role of genetics. J Gastrointest Surg 10 (2006), 270–277.
17. 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, 8, 2016, 67.
18. 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 22 (2015), 228–238.
19. 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 13 (2013), 514–522.
20. 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 98 (2013), 16–24.
21. Furet, J.P., Kong, L.C., 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 59 (2010), 3049–3057.
22. Zhang, H., DiBaise, J.K., Zuccolo, A., et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 106 (2009), 2365–2370.
23. Liou, A.P., Paziuk, M., Luevano, J.M. Jr, et al. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med, 5, 2013, 178 ra41.
24. Li, J.V., Ashrafian, H., Bueter, M., et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut 60 (2011), 1214–1223.
25. Mingrone, G., Panunzi, S., De Gaetano, A., et al. Bariatric-metabolic surgery versus conventional medical treatment in obese patients with type 2 diabetes: 5-year follow-up of an open-label, single-centre, randomised controlled trial. Lancet 386 (2015), 964–973.
26. Kashyap, S.R., Bhatt, D.L., Wolski, K., et al. Metabolic effects of bariatric surgery in patients with moderate obesity and type 2 diabetes: Analysis of a randomized control trial comparing surgery with intensive medical treatment. Diabetes Care 36 (2013), 2175–2182.
27. Le Chatelier, E., Nielsen, T., Qin, J., et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500 (2013), 541–546.
28. Denou, E., Marcinko, K., Surette, M.G., et al. High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity. Am J Physiol Endocrinol Metab 310 (2016), E982–93.
29. Plourde, C.E., Grenier-Larouche, T., Caron-Dorval, D., et al. Biliopancreatic diversion with duodenal switch improves insulin sensitivity and secretion through caloric restriction. Obesity (Silver Spring) 22 (2014), 1838–1846.
30. Isbell, J.M., Tamboli, R.A., Hansen, E.N., et al. The importance of caloric restriction in the early improvements in insulin sensitivity after Roux-en-Y gastric bypass surgery. Diabetes Care 33 (2010), 1438–1442.
31. Chen, P.J., Tseng, C.C., Chan, H.T., Chao, C.M., Acute otitis due to vibrio fluvialis after swimming. Case Rep Emerg Med 2012 (2012), 838–904.
32. 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 (2005), 4777–4783.
33. Osto, M., Abegg, K., Bueter, M., et al. Roux-en-Y gastric bypass surgery in rats alters gut microbiota profile along the intestine. Physiol Behav 119 (2013), 92–96.
34. Van den Abbeele, P., Gerard, P., Rabot, S., et al. Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats. Environ Microbiol 13 (2011), 2667–2680.
35. 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 54 (2004), 1469–1476.
36. Duncan, S.H., Louis, P., Thomson, J.M., Flint, H.J., The role of pH in determining the species composition of the human colonic microbiota. Environ Microbiol 11 (2009), 2112–2122.
37. Jackson, M.A., Goodrich, J.K., Maxan, M.E., et al. Proton pump inhibitors alter the composition of the gut microbiota. Gut 65 (2016), 749–756.
38. Imhann, F., Bonder, M.J., Vich Vila, A., et al. Proton pump inhibitors affect the gut microbiome. Gut 65 (2016), 740–748.
39. Wang, Z., Klipfell, E., Bennett, B.J., et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472 (2011), 57–63.
40. Koeth, R.A., Wang, Z., Levison, B.S., et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 19 (2013), 576–585.
41. Tang, W.H., Wang, Z., Levison, B.S., et al. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med 368 (2013), 1575–1584.
42. Spence, J.D., Jenkins, D.J., Davignon, J., Egg yolk consumption and carotid plaque. Atherosclerosis 224 (2012), 469–473.
43. Troseid, M., Hov, J.R., Nestvold, T.K., et al. Major increase in microbiota-dependent proatherogenic metabolite TMAO one year after bariatric surgery. Metab Syndr Relat Disord 14 (2016), 197–201.
44. Romeo, S., Maglio, C., Burza, M.A., et al. Cardiovascular events after bariatric surgery in obese subjects with type 2 diabetes. Diabetes Care 35 (2012), 2613–2617.
45. Ajouz, H., Mukherji, D., Shamseddine, A., Secondary bile acids: An underrecognized cause of colon cancer. World J Surg Oncol, 12, 2014, 164.
46. Forbes, J.D., Van Domselaar, G., Bernstein, C.N., The gut microbiota in immune-mediated inflammatory diseases. Front Microbiol, 7, 2016, 1081.
47. Sobhani, I., Amiot, A., Le Baleur, Y., et al. Microbial dysbiosis and colon carcinogenesis: Could colon cancer be considered a bacteria-related disease?. Therap Adv Gastroenterol 6 (2013), 215–229.
48. Derogar, M., Hull, M.A., Kant, P., et al. Increased risk of colorectal cancer after obesity surgery. Ann Surg 258 (2013), 983–988.
49. Ostlund, M.P., Lu, Y., Lagergren, J., Risk of obesity-related cancer after obesity surgery in a population-based cohort study. Ann Surg 252 (2010), 972–976.
50. Casselbrant, A., Elias, E., Fandriks, L., Wallenius, V., Expression of tight-junction proteins in human proximal small intestinal mucosa before and after Roux-en-Y gastric bypass surgery. Surg Obes Relat Dis 11 (2015), 45–53.
51. Aminian, A., Andalib, A., Ver, M.R., et al. Outcomes of bariatric surgery in patients with inflammatory bowel disease. Obes Surg 26 (2016), 1186–1190.
52. Colombo, F., Rizzi, A., Ferrari, C., et al. Bariatric surgery in patients with inflammatory bowel disease: An accessible path? Report of a case series and review of the literature. J Crohns Colitis 9 (2015), 185–190.
53. Kant, P., Hull, M.A., Excess body weight and obesity: The link with gastrointestinal and hepatobiliary cancer. Nat Rev Gastroenterol Hepatol 8 (2011), 224–238.
54. Gronbach, K., Eberle, U., Muller, M., et al. Safety of probiotic Escherichia coli strain Nissle 1917 depends on intestinal microbiota and adaptive immunity of the host. Infect Immun 78 (2010), 3036–3046.
55. Kruis, W., Fric, P., Pokrotnieks, J., et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53 (2004), 1617–1623.
56. Arribas, B., Rodriguez-Cabezas, M.E., Camuesco, D., et al. A probiotic strain of Escherichia coli, Nissle 1917, given orally exerts local and systemic anti-inflammatory effects in lipopolysaccharide-induced sepsis in mice. Br J Pharmacol 157 (2009), 1024–1033.
57. Buchwald, H., Estok, R., Fahrbach, K., et al. Weight and type 2 diabetes after bariatric surgery: Systematic review and meta-analysis. Am J Med 122 (2009), 248–256 e5.
58. Pories, W.J., Swanson, M.S., MacDonald, K.G., et al. Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg 222 (1995), 339–350 discussion 50-2.
59. Rubino, F., Forgione, A., Cummings, D.E., et al. The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg 244 (2006), 741–749.
60. Wickremesekera, K., Miller, G., Naotunne, T.D., et al. Loss of insulin resistance after Roux-en-Y gastric bypass surgery: A time course study. Obes Surg 15 (2005), 474–481.
61. Bojsen-Moller, K.N., Dirksen, C., Jorgensen, N.B., et al. Early enhancements of hepatic and later of peripheral insulin sensitivity combined with increased postprandial insulin secretion contribute to improved glycemic control after Roux-en-Y gastric bypass. Diabetes 63 (2014), 1725–1737.
62. Penney, N.C., Kinross, J., Newton, R.C., Purkayastha, S., The role of bile acids in reducing the metabolic complications of obesity after bariatric surgery: A systematic review. Int J Obes (Lond) 39 (2015), 1565–1574.
63. Clemente-Postigo, M., Roca-Rodriguez Mdel, M., Camargo, A., et al. Lipopolysaccharide and lipopolysaccharide-binding protein levels and their relationship to early metabolic improvement after bariatric surgery. Surg Obes Relat Dis 11 (2015), 933–939.
64. Monte, S.V., Caruana, J.A., Ghanim, H., et al. Reduction in endotoxemia, oxidative and inflammatory stress, and insulin resistance after Roux-en-Y gastric bypass surgery in patients with morbid obesity and type 2 diabetes mellitus. Surgery 151 (2012), 587–593.
65. Cani, P.D., Amar, J., Iglesias, M.A., et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56 (2007), 1761–1772.
66. Denou, E., Lolmede, K., Garidou, L., et al. Defective NOD2 peptidoglycan sensing promotes diet-induced inflammation, dysbiosis, and insulin resistance. EMBO Mol Med 7 (2015), 259–274.
67. Ryan, K.K., Tremaroli, V., Clemmensen, C., et al. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature 509 (2014), 183–188.
68. Bose, M., Teixeira, J., Olivan, B., et al. Weight loss and incretin responsiveness improve glucose control independently after gastric bypass surgery. J Diabetes 2 (2010), 47–55.
69. Peterli, R., Steinert, R.E., Woelnerhanssen, B., et al. Metabolic and hormonal changes after laparoscopic Roux-en-Y gastric bypass and sleeve gastrectomy: A randomized, prospective trial. Obes Surg 22 (2012), 740–748.
70. Miras, A.D., le Roux, C.W., Mechanisms underlying weight loss after bariatric surgery. Nat Rev Gastroenterol Hepatol 10 (2013), 575–584.
71. Wu, Q., Li, J.V., Seyfried, F., et al. Metabolic phenotype-microRNA data fusion analysis of the systemic consequences of Roux-en-Y gastric bypass surgery. Int J Obes (Lond) 39 (2015), 1126–1134.
72. Asmar, M., New physiological effects of the incretin hormones GLP-1 and GIP. Dan Med Bull, 58, 2011, B4248.
73. Yan, M., Song, M.M., Bai, R.X., et al. Effect of Roux-en-Y gastric bypass surgery on intestinal Akkermansia muciniphila. World J Gastrointest Surg 8 (2016), 301–307.
74. Evrard, S., Aprahamian, M., Hoeltzel, A., et al. Trophic and enzymatic adaptation of the intestine to biliopancreatic bypass in the rat. Int J Obes Relat Metab Disord 17 (1993), 541–547.
75. Nadreau, E., Baraboi, E.D., Samson, P., et al. Effects of the biliopancreatic diversion on energy balance in the rat. Int J Obes (Lond) 30 (2006), 419–429.
76. Saeidi, N., Meoli, L., Nestoridi, E., et al. Reprogramming of intestinal glucose metabolism and glycemic control in rats after gastric bypass. Science 341 (2013), 406–410.
77. Cavin, J.B., Couvelard, A., Lebtahi, R., et al. Differences in alimentary glucose absorption and intestinal disposal of blood glucose after Roux-en-Y gastric bypass vs sleeve gastrectomy. Gastroenterology 150 (2016), 454–464 e9.
78. Drucker, D.J., Erlich, P., Asa, S.L., Brubaker, P.L., Induction of intestinal epithelial proliferation by glucagon-like peptide 2. Proc Natl Acad Sci USA 93 (1996), 7911–7916.
79. Cani, P.D., Everard, A., Duparc, T., Gut microbiota, enteroendocrine functions and metabolism. Curr Opin Pharmacol 13 (2013), 935–940.
80. Wang, J., Jia, H., Metagenome-wide association studies: Fine-mining the microbiome. Nat Rev Microbiol 14 (2016), 508–522.
81. Anhe, F.F., Roy, D., Pilon, G., et al. A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice. Gut 64 (2015), 872–883.
82. Everard, A., Belzer, C., Geurts, L., et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110 (2013), 9066–9071.
83. 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 63 (2014), 727–735.
84. Everard, A., Lazarevic, V., Derrien, M., et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60 (2011), 2775–2786.
85. Karlsson, F.H., Tremaroli, V., Nookaew, I., et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498 (2013), 99–103.
86. Lefebvre, P., Cariou, B., Lien, F., et al. Role of bile acids and bile acid receptors in metabolic regulation. Physiol Rev 89 (2009), 147–191.
87. Benhamed, F., Filhoulaud, G., Caron, S., et al. O-GlcN acylation links ChREBP and FXR to glucose-sensing. Front Endocrinol (Lausanne), 5, 2014, 230.
88. Thomas, C., Gioiello, A., Noriega, L., et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab 10 (2009), 67–77.
89. Kumar, D.P., Rajagopal, S., Mahavadi, S., et al. Activation of transmembrane bile acid receptor TGR5 stimulates insulin secretion in pancreatic beta cells. Biochem Biophys Res Commun 427 (2012), 600–605.
90. Schittenhelm, B., Wagner, R., Kahny, V., et al. Role of FXR in beta-cells of lean and obese mice. Endocrinology 156 (2015), 1263–1271.
91. Watanabe, M., Houten, S.M., Mataki, C., et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439 (2006), 484–489.
92. Fang, S., Suh, J.M., Reilly, S.M., et al. Intestinal FXR agonism promotes adipose tissue browning and reduces obesity and insulin resistance. Nat Med 21 (2015), 159–165.
93. Kohli, R., Bradley, D., Setchell, K.D., et al. Weight loss induced by Roux-en-Y gastric bypass but not laparoscopic adjustable gastric banding increases circulating bile acids. J Clin Endocrinol Metab 98 (2013), E708–12.
94. Patti, M.E., Houten, S.M., Bianco, A.C., 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 (2009), 1671–1677.
95. Ahmad, N.N., Pfalzer, A., Kaplan, L.M., Roux-en-Y gastric bypass normalizes the blunted postprandial bile acid excursion associated with obesity. Int J Obes (Lond) 37 (2013), 1553–1559.
96. Kohli, R., Setchell, K.D., Kirby, M., et al. A surgical model in male obese rats uncovers protective effects of bile acids post-bariatric surgery. Endocrinology 154 (2013), 2341–2351.
97. Zhang, X., Wang, Y., Zhong, M., et al. Duodenal-jejunal bypass preferentially elevates serum taurine-conjugated bile acids and alters gut microbiota in a diabetic rat model. Obes Surg 26 (2016), 1890–1899.
98. Aron-Wisnewsky, J., Dore, J., Clement, K., The importance of the gut microbiota after bariatric surgery. Nat Rev Gastroenterol Hepatol 9 (2012), 590–598.
99. Islam, K.B., Fukiya, S., Hagio, M., et al. Bile acid is a host factor that regulates the composition of the cecal microbiota in rats. Gastroenterology 141 (2011), 1773–1781.
100. Van Eldere, J., Celis, P., De Pauw, G., et al. Tauroconjugation of cholic acid stimulates 7 alpha-dehydroxylation by fecal bacteria. Appl Environ Microbiol 62 (1996), 656–661.
101. Nakatani, H., Kasama, K., Oshiro, T., et al. Serum bile acid along with plasma incretins and serum high-molecular weight adiponectin levels are increased after bariatric surgery. Metabolism 58 (2009), 1400–1407.
102. Pournaras, D.J., Glicksman, C., Vincent, R.P., et al. The role of bile after Roux-en-Y gastric bypass in promoting weight loss and improving glycaemic control. Endocrinology 153 (2012), 3613–3619.
103. Simonen, M., Dali-Youcef, N., Kaminska, D., et al. Conjugated bile acids associate with altered rates of glucose and lipid oxidation after Roux-en-Y gastric bypass. Obes Surg 22 (2012), 1473–1480.
104. Chen, X., Lou, G., Meng, Z., Huang, W., TGR5: A novel target for weight maintenance and glucose metabolism. Exp Diabetes Res, 2011 853501.
105. Broeders, E.P., Nascimento, E.B., Havekes, B., et al. The bile acid chenodeoxycholic acid increases human brown adipose tissue activity. Cell Metab 22 (2015), 418–426.
106. McGavigan, A.K., Garibay, D., Henseler, Z.M., et al. TGR5 contributes to glucoregulatory improvements after vertical sleeve gastrectomy in mice. Gut 66:2 (2015), 226–234.
107. Trabelsi, M.S., Daoudi, M., Prawitt, J., et al. Farnesoid X receptor inhibits glucagon-like peptide-1 production by enteroendocrine L cells. Nat Commun, 6, 2015, 7629.
108. Flynn, C.R., Albaugh, V.L., Cai, S., et al. Bile diversion to the distal small intestine has comparable metabolic benefits to bariatric surgery. Nat Commun, 6, 2015, 7715.
109. Thomas, T., Gilbert, J., Meyer, F., Metagenomics: A guide from sampling to data analysis. Microb Inform Exp, 2, 2012, 3.
110. Wagner Mackenzie, B., Waite, D.W., Taylor, M.W., Evaluating variation in human gut microbiota profiles due to DNA extraction method and inter-subject differences. Front Microbiol, 6, 2015, 130.
111. Kuczynski, J., Lauber, C.L., Walters, W.A., et al. Experimental and analytical tools for studying the human microbiome. Nat Rev Genet 13 (2012), 47–58.
112. Kennedy, N.A., Walker, A.W., Berry, S.H., et al. The impact of different DNA extraction kits and laboratories upon the assessment of human gut microbiota composition by 16S rRNA gene sequencing. PLoS ONE, 9, 2014, e88982.
113. Larsen, A.M., Mohammed, H.H., Arias, C.R., Comparison of DNA extraction protocols for the analysis of gut microbiota in fishes. FEMS Microbiol Lett, 362, 2015.
114. Langille, M.G., Zaneveld, J., Caporaso, J.G., et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31 (2013), 814–821.
115. Poretsky, R., Rodriguez, R.L., Luo, C., et al. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS ONE, 9, 2014, e93827.
116. Qin, J., Li, R., Raes, J., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464 (2010), 59–65.