1932

Abstract

Bariatric surgeries, such as Roux-en-Y gastric bypass and vertical sleeve gastrectomy, produce significant and durable weight loss in both humans and rodents. Recently, these surgical interventions have also been termed metabolic surgery because they result in profound metabolic improvements that often surpass the expected improvement due to body weight loss alone. In this review we focus on the weight-loss independent effects of bariatric surgery, which encompass energy expenditure and macronutrient preference, the luminal composition of the gut (i.e., the microbiota and bile acids), the transformation of the gastrointestinal lining, increases in postprandial gut hormone secretions, glycemic control, pancreas morphology, and micronutrient and mineral absorption. Taken together, these data point to several important physiological changes that contribute to the profound benefits of these surgical procedures. Identifying the underlying molecular mechanisms for these physiological effects will allow better utilization of these existing procedures to help patients and develop new treatments that harness these surgical effects with less invasive interventions.

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2017-02-10
2024-06-17
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Literature Cited

  1. Bray GA, Fruhbeck G, Ryan DH, Wilding JP. 1.  2016. Management of obesity. Lancet 387:1947–56 [Google Scholar]
  2. Schauer PR, Kashyap SR, Wolski K, Brethauer SA, Kirwan JP. 2.  et al. 2012. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N. Engl. J. Med. 366:1567–76 [Google Scholar]
  3. Odstrcil EA, Martinez JG, Santa Ana CA, Xue B, Schneider RE. 3.  et al. 2010. The contribution of malabsorption to the reduction in net energy absorption after long-limb Roux-en-Y gastric bypass. Am. J. Clin. Nutr. 92:704–13 [Google Scholar]
  4. Carswell KA, Vincent RP, Belgaumkar AP, Sherwood RA, Amiel SA. 4.  et al. 2014. The effect of bariatric surgery on intestinal absorption and transit time. Obes. Surg. 24:796–805 [Google Scholar]
  5. Shin AC, Zheng H, Townsend RL, Patterson LM, Holmes GM, Berthoud HR. 5.  2013. Longitudinal assessment of food intake, fecal energy loss, and energy expenditure after Roux-en-Y gastric bypass surgery in high-fat-fed obese rats. Obes. Surg. 23:531–40 [Google Scholar]
  6. Nosso G, Griffo E, Cotugno M, Saldalamacchia G, Lupoli R. 6.  et al. 2016. Comparative effects of Roux-en-Y gastric bypass and sleeve gastrectomy on glucose homeostasis and incretin hormones in obese type 2 diabetic patients: a one-year prospective study. Horm. Metab. Res. 48:312–17 [Google Scholar]
  7. Franco JV, Ruiz PA, Palermo M, Gagner M. 7.  2011. A review of studies comparing three laparoscopic procedures in bariatric surgery: sleeve gastrectomy, Roux-en-Y gastric bypass and adjustable gastric banding. Obes. Surg. 21:1458–68 [Google Scholar]
  8. Lang T, Hauser R, Buddeberg C, Klaghofer R. 8.  2002. Impact of gastric banding on eating behavior and weight. Obes. Surg. 12:100–7 [Google Scholar]
  9. Ullrich J, Ernst B, Wilms B, Thurnheer M, Schultes B. 9.  2013. Roux-en Y gastric bypass surgery reduces hedonic hunger and improves dietary habits in severely obese subjects. Obes. Surg. 23:50–55 [Google Scholar]
  10. Cushing CC, Benoit SC, Peugh JL, Reiter-Purtill J, Inge TH, Zeller MH. 10.  2014. Longitudinal trends in hedonic hunger after Roux-en-Y gastric bypass in adolescents. Surg. Obes. Relat. Dis. 10:125–30 [Google Scholar]
  11. Roberts K, Duffy A, Kaufman J, Burrell M, Dziura J, Bell R. 11.  2007. Size matters: gastric pouch size correlates with weight loss after laparoscopic Roux-en-Y gastric bypass. Surg. Endosc. 21:1397–402 [Google Scholar]
  12. Nishie A, Brown B, Barloon T, Kuehn D, Samuel I. 12.  2007. Comparison of size of proximal gastric pouch and short-term weight loss following routine upper gastrointestinal contrast study after laparoscopic Roux-en-Y gastric bypass. Obes. Surg. 17:1183–88 [Google Scholar]
  13. O'Connor EA, Carlin AM. 13.  2008. Lack of correlation between variation in small-volume gastric pouch size and weight loss after laparoscopic Roux-en-Y gastric bypass. Surg. Obes. Relat. Dis. 4:399–403 [Google Scholar]
  14. Higa KD, Boone KB, Ho T. 14.  2000. Complications of the laparoscopic Roux-en-Y gastric bypass: 1,040 patients—what have we learned?. Obes. Surg. 10:509–13 [Google Scholar]
  15. Stefater MA, Sandoval DA, Chambers AP, Wilson-Pérez HE, Hofmann SM. 15.  et al. 2011. Sleeve gastrectomy in rats improves postprandial lipid clearance by reducing intestinal triglyceride secretion. Gastroenterology 141:939–49.e4 [Google Scholar]
  16. Grayson BE, Schneider KM, Woods SC, Seeley RJ. 16.  2013. Improved rodent maternal metabolism but reduced intrauterine growth after vertical sleeve gastrectomy. Sci. Transl. Med. 5:199ra112 [Google Scholar]
  17. Stefater MA, Pérez-Tilve D, Chambers AP, Wilson-Pérez HE, Sandoval DA. 17.  et al. 2010. Sleeve gastrectomy induces loss of weight and fat mass in obese rats, but does not affect leptin sensitivity. Gastroenterology 138:2426–36.e3 [Google Scholar]
  18. Hao Z, Mumphrey MB, Townsend RL, Morrison CD, Münzberg H. 18.  et al. 2016. Reprogramming of defended body weight after Roux-en-Y gastric bypass surgery in diet-induced obese mice. Obesity 24:654–60 [Google Scholar]
  19. Furnes MW, Tommeras K, Arum CJ, Zhao CM, Chen D. 19.  2008. Gastric bypass surgery causes body weight loss without reducing food intake in rats. Obes. Surg. 18:415–22 [Google Scholar]
  20. Chambers AP, Wilson-Pérez HE, McGrath S, Grayson BE, Ryan KK. 20.  et al. 2012. Effect of vertical sleeve gastrectomy on food selection and satiation in rats. Am. J. Physiol. Endocrinol. Metab. 303:E1076–84 [Google Scholar]
  21. Bueter M, Lowenstein C, Olbers T, Wang M, Cluny NL. 21.  et al. 2010. Gastric bypass increases energy expenditure in rats. Gastroenterology 138:1845–53 [Google Scholar]
  22. Nestoridi E, Kvas S, Kucharczyk J, Stylopoulos N. 22.  2012. Resting energy expenditure and energetic cost of feeding are augmented after Roux-en-Y gastric bypass in obese mice. Endocrinology 153:2234–44 [Google Scholar]
  23. Abegg K, Corteville C, Bueter M, Lutz TA. 23.  2016. Alterations in energy expenditure in Roux-en-Y gastric bypass rats persist at thermoneutrality. Int. J. Obes. 40:1215–21 [Google Scholar]
  24. McGavigan AK, Garibay D, Henseler ZM, Chen J, Bettaieb A. 24.  et al. 2015. TGR5 contributes to glucoregulatory improvements after vertical sleeve gastrectomy in mice. Gut In press. doi: 10.1136/gutjnl-2015-309871 [Google Scholar]
  25. Das SK, Roberts SB, McCrory MA, Hsu LK, Shikora SA. 25.  et al. 2003. Long-term changes in energy expenditure and body composition after massive weight loss induced by gastric bypass surgery. Am. J. Clin. Nutr. 78:22–30 [Google Scholar]
  26. Schmidt JB, Pedersen SD, Gregersen NT, Vestergaard L, Nielsen MS. 26.  et al. 2016. Effects of RYGB on energy expenditure, appetite and glycaemic control: a randomized controlled clinical trial. Int. J. Obes. 40:281–90 [Google Scholar]
  27. de Castro Cesar M, de Lima Montebelo MI, Rasera I Jr., de Oliveira AV Jr., Gomes Gonelli PR, Aparecida Cardoso G. 27.  2008. Effects of Roux-en-Y gastric bypass on resting energy expenditure in women. Obes. Surg. 18:1376–80 [Google Scholar]
  28. Dirksen C, Jørgensen NB, Bojsen-Møller KN, Kielgast U, Jacobsen SH. 28.  et al. 2013. Gut hormones, early dumping and resting energy expenditure in patients with good and poor weight loss response after Roux-en-Y gastric bypass. Int. J. Obes. 37:1452–59 [Google Scholar]
  29. Flancbaum L, Choban PS, Bradley LR, Burge JC. 29.  1997. Changes in measured resting energy expenditure after Roux-en-Y gastric bypass for clinically severe obesity. Surgery 122:943–49 [Google Scholar]
  30. Faria SL, Faria OP, Buffington C, de Almeida Cardeal M, Rodrigues de Gouvêa H. 30.  2012. Energy expenditure before and after Roux-en-Y gastric bypass. Obes. Surg. 22:1450–55 [Google Scholar]
  31. Werling M, Olbers T, Fändriks L, Bueter M, Länroth H. 31.  et al. 2013. Increased postprandial energy expenditure may explain superior long term weight loss after Roux-en-Y gastric bypass compared to vertical banded gastroplasty. PLOS ONE 8:e60280 [Google Scholar]
  32. van Gemert WG, Westerterp KR, van Acker BA, Wagenmakers AJ, Halliday D. 32.  et al. 2000. Energy, substrate and protein metabolism in morbid obesity before, during and after massive weight loss. Int. J. Obes. Relat. Metab. Disord. 24:711–18 [Google Scholar]
  33. Faria SL, Kelly E, Faria OP. 33.  2009. Energy expenditure and weight regain in patients submitted to Roux-en-Y gastric bypass. Obes. Surg. 19:856–59 [Google Scholar]
  34. Fothergill E, Guo J, Howard L, Kerns JC, Knuth ND. 34.  et al. 2016. Persistent metabolic adaptation 6 years after “The Biggest Loser” competition. Obesity 24:1612–19 [Google Scholar]
  35. Wilson-Pérez HE, Chambers AP, Sandoval DA, Stefater MA, Woods SC. 35.  et al. 2013. The effect of vertical sleeve gastrectomy on food choice in rats. Int. J. Obes. 37:288–95 [Google Scholar]
  36. Saeidi N, Nestoridi E, Kucharczyk J, Uygun MK, Yarmush ML, Stylopoulos N. 36.  2012. Sleeve gastrectomy and Roux-en-Y gastric bypass exhibit differential effects on food preferences, nutrient absorption and energy expenditure in obese rats. Int. J. Obes. 36:1396–402 [Google Scholar]
  37. Sallet PC, Sallet JA, Dixon JB, Collis E, Pisani CE. 37.  et al. 2007. Eating behavior as a prognostic factor for weight loss after gastric bypass. Obes. Surg. 17:445–51 [Google Scholar]
  38. Engström M, Forsberg A, Søvik TT, Olbers T, Lönroth H, Karlsson J. 38.  2015. Perception of control over eating after bariatric surgery for super-obesity—a 2-year follow-up study. Obes. Surg. 25:1086–93 [Google Scholar]
  39. Scholtz S, Goldstone AP, le Roux CW. 39.  2015. Changes in reward after gastric bypass: the advantages and disadvantages. Curr. Atheroscler. Rep. 17:61 [Google Scholar]
  40. Ochner CN, Kwok Y, Conceição E, Pantazatos SP, Puma LM. 40.  et al. 2011. Selective reduction in neural responses to high calorie foods following gastric bypass surgery. Ann. Surg. 253:502–7 [Google Scholar]
  41. Faulconbridge LF, Ruparel K, Loughead J, Allison KC, Hesson LA. 41.  et al. 2016. Changes in neural responsivity to highly palatable foods following Roux-en-Y gastric bypass, sleeve gastrectomy, or weight stability: an fMRI study. Obesity 24:1054–60 [Google Scholar]
  42. Khoo CM, Muehlbauer MJ, Stevens RD, Pamuklar Z, Chen J. 42.  et al. 2014. Postprandial metabolite profiles reveal differential nutrient handling after bariatric surgery compared with matched caloric restriction. Ann. Surg. 259:687–93 [Google Scholar]
  43. Sommer F, Backhed F. 43.  2013. The gut microbiota—masters of host development and physiology. Nat. Rev. Microbiol. 11:227–38 [Google Scholar]
  44. Boulangé CL, Neves AL, Chilloux J, Nicholson JK, Dumas ME. 44.  2016. Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome Med 8:42 [Google Scholar]
  45. Aron-Wisnewsky J, Clement K. 45.  2014. The effects of gastrointestinal surgery on gut microbiota: potential contribution to improved insulin sensitivity. Curr. Atheroscler. Rep. 16:454 [Google Scholar]
  46. Furet JP, Kong LC, Tap J, Poitou C, Basdevant A. 46.  et al. 2010. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59:3049–57 [Google Scholar]
  47. Li JV, Ashrafian H, Bueter M, Kinross J, Sands C. 47.  et al. 2011. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut 60:1214–23 [Google Scholar]
  48. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M. 48.  et al. 2009. Human gut microbiota in obesity and after gastric bypass. PNAS 106:2365–70 [Google Scholar]
  49. Sweeney TE, Morton JM. 49.  2013. The human gut microbiome: a review of the effect of obesity and surgically induced weight loss. JAMA Surg 148:563–69 [Google Scholar]
  50. Li JV, Reshat R, Wu Q, Ashrafian H, Bueter M. 50.  et al. 2011. Experimental bariatric surgery in rats generates a cytotoxic chemical environment in the gut contents. Front. Microbiol. 2:183 [Google Scholar]
  51. Liou AP, Paziuk M, Luevano JM Jr., Machineni S, Turnbaugh PJ, Kaplan LM. 51.  2013. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci. Transl. Med. 5:178ra41 [Google Scholar]
  52. Tremaroli V, Karlsson F, Werling M, Stahlman M, Kovatcheva-Datchary P. 52.  et al. 2015. 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. 22:228–38 [Google Scholar]
  53. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA. 53.  et al. 2016. Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation. Nature 533:543–46 [Google Scholar]
  54. Li-Hawkins J, Gåfvels M, Olin M, Lund EG, Andersson U. 54.  et al. 2002. Cholic acid mediates negative feedback regulation of bile acid synthesis in mice. J. Clin. Investig. 110:1191–200 [Google Scholar]
  55. Mataki C, Magnier BC, Houten SM, Annicotte JS, Argmann C. 55.  et al. 2007. Compromised intestinal lipid absorption in mice with a liver-specific deficiency of liver receptor homolog 1. Mol. Cell. Biol. 27:8330–39 [Google Scholar]
  56. Chiang JY. 56.  2009. Bile acids: regulation of synthesis. J. Lipid Res. 50:1955–66 [Google Scholar]
  57. Kohli R, Setchell KD, Kirby M, Myronovych A, Ryan KK. 57.  et al. 2013. A surgical model in male obese rats uncovers protective effects of bile acids post-bariatric surgery. Endocrinology 154:2341–51 [Google Scholar]
  58. Flynn CR, Albaugh VL, Cai S, Cheung-Flynn J, Williams PE. 58.  et al. 2015. Bile diversion to the distal small intestine has comparable metabolic benefits to bariatric surgery. Nat. Commun. 6:7715 [Google Scholar]
  59. Noel OF, Still CD, Argyropoulos G, Edwards M, Gerhard GS. 59.  2016. Bile acids, FXR, and metabolic effects of bariatric surgery. J. Obes. 2016:4390254 [Google Scholar]
  60. Sayin SI, Wahlström A, Felin J, Jantti S, Marschall HU. 60.  et al. 2013. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell. Metab. 17:225–35 [Google Scholar]
  61. Myronovych A, Kirby M, Ryan KK, Zhang W, Jha P. 61.  et al. 2014. Vertical sleeve gastrectomy reduces hepatic steatosis while increasing serum bile acids in a weight-loss-independent manner. Obesity 22:390–400 [Google Scholar]
  62. Kohli R, Myronovych A, Tan BK, Salazar-Gonzalez RM, Miles L. 62.  et al. 2015. Bile acid signaling: mechanism for bariatric surgery, cure for NASH?. Dig. Dis. 33:440–46 [Google Scholar]
  63. Spinelli V, Lalloyer F, Baud G, Osto E, Kouach M. 63.  et al. 2016. Influence of Roux-en-Y gastric bypass on plasma bile acid profiles: a comparative study between rats, pigs and humans. Int. J. Obes. 40:1260–67 [Google Scholar]
  64. Thomas C, Auwerx J, Schoonjans K. 64.  2008. Bile acids and the membrane bile acid receptor TGR5—connecting nutrition and metabolism. Thyroid 18:167–74 [Google Scholar]
  65. Hylemon PB, Zhou H, Pandak WM, Ren S, Gil G, Dent P. 65.  2009. Bile acids as regulatory molecules. J. Lipid Res. 50:1509–20 [Google Scholar]
  66. Ryan KK, Tremaroli V, Clemmensen C, Kovatcheva-Datchary P, Myronovych A. 66.  et al. 2014. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature 509:183–88 [Google Scholar]
  67. Morton GJ, Matsen ME, Bracy DP, Meek TH, Nguyen HT. 67.  et al. 2013. FGF19 action in the brain induces insulin-independent glucose lowering. J. Clin. Investig. 123:4799–808 [Google Scholar]
  68. Ryan KK, Kohli R, Gutierrez-Aguilar R, Gaitonde SG, Woods SC, Seeley RJ. 68.  2013. Fibroblast growth factor-19 action in the brain reduces food intake and body weight and improves glucose tolerance in male rats. Endocrinology 154:9–15 [Google Scholar]
  69. Gerhard GS, Styer AM, Wood GC, Roesch SL, Petrick AT. 69.  et al. 2013. A role for fibroblast growth factor 19 and bile acids in diabetes remission after Roux-en-Y gastric bypass. Diabetes Care 36:1859–64 [Google Scholar]
  70. Jørgensen NB, Dirksen C, Bojsen-Møller KN, Kristiansen VB, Wulff BS. 70.  et al. 2015. Improvements in glucose metabolism early after gastric bypass surgery are not explained by increases in total bile acids and fibroblast growth factor 19 concentrations. J. Clin. Endocrinol. Metab. 100:E396–406 [Google Scholar]
  71. Peat CM, Kleiman SC, Bulik CM, Carroll IM. 71.  2015. The intestinal microbiome in bariatric surgery patients. Eur. Eat. Disord. Rev. 23:496–503 [Google Scholar]
  72. Arora T, Bäckhed F. 72.  2016. The gut microbiota and metabolic disease: current understanding and future perspectives. J. Intern. Med. 280:339–49 [Google Scholar]
  73. Fernandes R, Beserra BT, Mocellin MC, Kuntz MG, da Rosa JS. 73.  et al. 2016. Effects of prebiotic and synbiotic supplementation on inflammatory markers and anthropometric indices after Roux-en-Y gastric bypass: a randomized, triple-blind, placebo-controlled pilot study. J. Clin. Gastroenterol. 50:208–17 [Google Scholar]
  74. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 74.  2005. Host-bacterial mutualism in the human intestine. Science 307:1915–20 [Google Scholar]
  75. Korner J, Inabnet W, Febres G, Conwell IM, McMahon DJ. 75.  et al. 2009. Prospective study of gut hormone and metabolic changes after adjustable gastric banding and Roux-en-Y gastric bypass. Int. J. Obes. 33:786–95 [Google Scholar]
  76. Le Roux CW, Borg C, Wallis K, Vincent RP, Bueter M. 76.  et al. 2010. Gut hypertrophy after gastric bypass is associated with increased glucagon-like peptide 2 and intestinal crypt cell proliferation. Ann. Surg. 252:50–6 [Google Scholar]
  77. Mumphrey MB, Patterson LM, Zheng H, Berthoud HR. 77.  2013. Roux-en-Y gastric bypass surgery increases number but not density of CCK-, GLP-1-, 5-HT-, and neurotensin-expressing enteroendocrine cells in rats. Neurogastroenterol. Motil. 25:e70–79 [Google Scholar]
  78. Mumphrey MB, Hao Z, Townsend RL, Patterson LM, Berthoud HR. 78.  2015. Sleeve gastrectomy does not cause hypertrophy and reprogramming of intestinal glucose metabolism in rats. Obes. Surg. 25:1468–73 [Google Scholar]
  79. Li B, Lu Y, Srikant CB, Gao ZH, Liu JL. 79.  2013. Intestinal adaptation and Reg gene expression induced by antidiabetic duodenal-jejunal bypass surgery in Zucker fatty rats. Am. J. Physiol. Gastrointest. Liver Physiol. 304:G635–45 [Google Scholar]
  80. Habegger KM, Al-Massadi O, Heppner KM, Myronovych A, Holland J. 80.  et al. 2014. Duodenal nutrient exclusion improves metabolic syndrome and stimulates villus hyperplasia. Gut 63:1238–46 [Google Scholar]
  81. Kohli R, Kirby M, Setchell KD, Jha P, Klustaitis K. 81.  et al. 2010. Intestinal adaptation after ileal interposition surgery increases bile acid recycling and protects against obesity-related comorbidities. Am. J. Physiol. Gastrointest. Liver Physiol. 299:G652–60 [Google Scholar]
  82. Le Roux CW, Borg C, Wallis K, Vincent RP, Bueter M. 82.  et al. 2010. Gut hypertrophy after gastric bypass is associated with increased glucagon-like peptide 2 and intestinal crypt cell proliferation. Ann. Surg. 252:50–56 [Google Scholar]
  83. Taqi E, Wallace LE, de Heuvel E, Chelikani PK, Zheng H. 83.  et al. 2010. The influence of nutrients, biliary-pancreatic secretions, and systemic trophic hormones on intestinal adaptation in a Roux-en-Y bypass model. J. Pediatr. Surg. 45:987–95 [Google Scholar]
  84. Potten CS, Owen G, Hewitt D, Chadwick CA, Hendry H. 84.  et al. 1995. Stimulation and inhibition of proliferation in the small intestinal crypts of the mouse after in vivo administration of growth factors. Gut 36:864–73 [Google Scholar]
  85. Brubaker PL, Izzo A, Hill M, Drucker DJ. 85.  1997. Intestinal function in mice with small bowel growth induced by glucagon-like peptide-2. Am. J. Physiol. 272:E1050–58 [Google Scholar]
  86. Seeley RJ, Chambers AP, Sandoval DA. 86.  2015. The role of gut adaptation in the potent effects of multiple bariatric surgeries on obesity and diabetes. Cell. Metab. 21:369–78 [Google Scholar]
  87. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C. 87.  et al. 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761–72 [Google Scholar]
  88. Peterli R, Steinert RE, Woelnerhanssen B, Peters T, Christoffel-Courtin C. 88.  et al. 2012. Metabolic and hormonal changes after laparoscopic roux-en-Y gastric bypass and sleeve gastrectomy: a randomized, prospective trial. Obes. Surg. 22:740–48 [Google Scholar]
  89. Chambers AP, Smith EP, Begg DP, Grayson BE, Sisley S. 89.  et al. 2014. Regulation of gastric emptying rate and its role in nutrient-induced GLP-1 secretion in rats after vertical sleeve gastrectomy. Am. J. Physiol. Endocrinol. Metab. 306:E424–32 [Google Scholar]
  90. Cavin JB, Couvelard A, Lebtahi R, Ducroc R, Arapis K. 90.  et al. 2016. Differences in alimentary glucose absorption and intestinal disposal of blood glucose after Roux-en-Y gastric bypass versus sleeve gastrectomy. Gastroenterology 150:454–64.e9 [Google Scholar]
  91. Manning S, Pucci A, Batterham RL. 91.  2015. GLP-1: a mediator of the beneficial metabolic effects of bariatric surgery?. Physiology 30:50–62 [Google Scholar]
  92. Jørgensen NB, Dirksen C, Bojsen-Møller KN, Jacobsen SH, Worm D. 92.  et al. 2013. Exaggerated glucagon-like peptide 1 response is important for improved beta-cell function and glucose tolerance after Roux-en-Y gastric bypass in patients with type 2 diabetes. Diabetes 62:3044–52 [Google Scholar]
  93. Holst JJ. 93.  2011. Postprandial insulin secretion after gastric bypass surgery: the role of glucagon-like peptide 1. Diabetes 60:2203–5 [Google Scholar]
  94. Ye J, Hao Z, Mumphrey MB, Townsend RL, Patterson LM. 94.  et al. 2014. GLP-1 receptor signaling is not required for reduced body weight after RYGB in rodents. Am. J. Physiol. Regul. Integr. Comp. Physiol. 306:R352–62 [Google Scholar]
  95. Wilson-Pérez HE, Chambers AP, Ryan KK, Li B, Sandoval DA. 95.  et al. 2013. Vertical sleeve gastrectomy is effective in two genetic mouse models of glucagon-like peptide 1 receptor deficiency. Diabetes 62:2380–85 [Google Scholar]
  96. Zhou J, Hao Z, Irwin N, Berthoud HR, Ye J. 96.  2015. Gastric inhibitory polypeptide (GIP) is selectively decreased in the Roux-limb of dietary obese mice after RYGB surgery. PLOS ONE 10:e0134728 [Google Scholar]
  97. Laferrere B, Teixeira J, McGinty J, Tran H, Egger JR. 97.  et al. 2008. 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. 93:2479–85 [Google Scholar]
  98. Lee CJ, Brown T, Magnuson TH, Egan JM, Carlson O, Elahi D. 98.  2013. Hormonal response to a mixed-meal challenge after reversal of gastric bypass for hypoglycemia. J. Clin. Endocrinol. Metab. 98:E1208–12 [Google Scholar]
  99. Nguyen NQ, Debreceni TL, Bambrick JE, Bellon M, Wishart J. 99.  et al. 2014. Rapid gastric and intestinal transit is a major determinant of changes in blood glucose, intestinal hormones, glucose absorption and postprandial symptoms after gastric bypass. Obesity 22:2003–9 [Google Scholar]
  100. Svane MS, Bojsen-Møller KN, Nielsen S, Jørgensen NB, Dirksen C. 100.  et al. 2016. Effects of endogenous GLP-1 and GIP on glucose tolerance after Roux-en-Y gastric bypass surgery. Am. J. Physiol. Endocrinol. Metab. 310:E505–14 [Google Scholar]
  101. Gault VA, Kerr BD, Harriott P, Flatt PR. 101.  2011. Administration of an acylated GLP-1 and GIP preparation provides added beneficial glucose-lowering and insulinotropic actions over single incretins in mice with type 2 diabetes and obesity. Clin. Sci. 121:107–17 [Google Scholar]
  102. Bhat VK, Kerr BD, Vasu S, Flatt PR, Gault VA. 102.  2013. A DPP-IV-resistant triple-acting agonist of GIP, GLP-1 and glucagon receptors with potent glucose-lowering and insulinotropic actions in high-fat-fed mice. Diabetologia 56:1417–24 [Google Scholar]
  103. Gault VA, Bhat VK, Irwin N, Flatt PR. 103.  2013. A novel glucagon-like peptide-1 (GLP-1)/glucagon hybrid peptide with triple-acting agonist activity at glucose-dependent insulinotropic polypeptide, GLP-1, and glucagon receptors and therapeutic potential in high fat-fed mice. J. Biol. Chem. 288:35581–91 [Google Scholar]
  104. Le Roux CW, Welbourn R, Werling M, Osborne A, Kokkinos A. 104.  et al. 2007. Gut hormones as mediators of appetite and weight loss after roux-en-Y gastric bypass. Ann. Surg. 246:780–85 [Google Scholar]
  105. Zhou J, Hegsted M, McCutcheon KL, Keenan MJ, Xi X. 105.  et al. 2006. Peptide YY and proglucagon mRNA expression patterns and regulation in the gut. Obesity 14:683–89 [Google Scholar]
  106. Tsoli M, Chronaiou A, Kehagias I, Kalfarentzos F, Alexandrides TK. 106.  2013. Hormone changes and diabetes resolution after biliopancreatic diversion and laparoscopic sleeve gastrectomy: a comparative prospective study. Surg. Obes. Relat. Dis. 9:667–77 [Google Scholar]
  107. Pucci A, Cheung WH, Jones J, Manning S, Kingett H. 107.  et al. 2015. A case of severe anorexia, excessive weight loss and high peptide YY levels after sleeve gastrectomy. Endocrinol. Diabetes Metab. Case Rep. 2015:150020 [Google Scholar]
  108. Witte AB, Grybäck P, Holst JJ, Hilsted L, Hellsträm PM. 108.  et al. 2009. Differential effect of PYY1-36 and PYY3–36 on gastric emptying in man. Regul. Pept. 158:57–62 [Google Scholar]
  109. Challis BG, Pinnock SB, Coll AP, Carter RN, Dickson SL, O'Rahilly S. 109.  2003. Acute effects of PYY3–36 on food intake and hypothalamic neuropeptide expression in the mouse. Biochem. Biophys. Res. Commun. 311:915–19 [Google Scholar]
  110. Valderas JP, Irribarra V, Boza C, de la Cruz R, Liberona Y. 110.  et al. 2010. Medical and surgical treatments for obesity have opposite effects on peptide YY and appetite: a prospective study controlled for weight loss. J. Clin. Endocrinol. Metab. 95:1069–75 [Google Scholar]
  111. Chandarana K, Gelegen C, Karra E, Choudhury AI, Drew ME. 111.  et al. 2011. Diet and gastrointestinal bypass-induced weight loss: the roles of ghrelin and peptide YY. Diabetes 60:810–18 [Google Scholar]
  112. Boey D, Lin S, Enriquez RF, Lee NJ, Slack K. 112.  et al. 2008. PYY transgenic mice are protected against diet-induced and genetic obesity. Neuropeptides 42:19–30 [Google Scholar]
  113. Boey D, Lin S, Karl T, Baldock P, Lee N. 113.  et al. 2006. Peptide YY ablation in mice leads to the development of hyperinsulinaemia and obesity. Diabetologia 49:1360–70 [Google Scholar]
  114. Boey D, Heilbronn L, Sainsbury A, Laybutt R, Kriketos A. 114.  et al. 2006. Low serum PYY is linked to insulin resistance in first-degree relatives of subjects with type 2 diabetes. Neuropeptides 40:317–24 [Google Scholar]
  115. Zhu W, Zhang W, Gong J, Huang Q, Shi Y. 115.  et al. 2009. Peptide YY induces intestinal proliferation in peptide YY knockout mice with total enteral nutrition after massive small bowel resection. J. Pediatr. Gastroenterol. Nutr. 48:517–25 [Google Scholar]
  116. Estall JL, Drucker DJ. 116.  2003. Dual regulation of cell proliferation and survival via activation of glucagon-like peptide-2 receptor signaling. J. Nutr. 133:3708–11 [Google Scholar]
  117. Meek CL, Lewis HB, Reimann F, Gribble FM, Park AJ. 117.  2016. The effect of bariatric surgery on gastrointestinal and pancreatic peptide hormones. Peptides 77:28–37 [Google Scholar]
  118. Teixeira TF, Collado MC, Ferreira CL, Bressan J, Peluzio Mdo C. 118.  2012. Potential mechanisms for the emerging link between obesity and increased intestinal permeability. Nutr. Res. 32:637–47 [Google Scholar]
  119. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A. 119.  et al. 2009. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58:1091–103 [Google Scholar]
  120. Dong CX, Zhao W, Solomon C, Rowland KJ, Ackerley C. 120.  et al. 2014. The intestinal epithelial insulin-like growth factor-1 receptor links glucagon-like peptide-2 action to gut barrier function. Endocrinology 155:370–79 [Google Scholar]
  121. Laferrere B, Swerdlow N, Bawa B, Arias S, Bose M. 121.  et al. 2010. Rise of oxyntomodulin in response to oral glucose after gastric bypass surgery in patients with type 2 diabetes. J. Clin. Endocrinol. Metab. 95:4072–76 [Google Scholar]
  122. Day JW, Ottaway N, Patterson JT, Gelfanov V, Smiley D. 122.  et al. 2009. A new glucagon and GLP-1 co-agonist eliminates obesity in rodents. Nat. Chem. Biol. 5:749–57 [Google Scholar]
  123. Pocai A, Carrington PE, Adams JR, Wright M, Eiermann G. 123.  et al. 2009. Glucagon-like peptide 1/glucagon receptor dual agonism reverses obesity in mice. Diabetes 58:2258–66 [Google Scholar]
  124. Wynne K, Park AJ, Small CJ, Patterson M, Ellis SM. 124.  et al. 2005. Subcutaneous oxyntomodulin reduces body weight in overweight and obese subjects: a double-blind, randomized, controlled trial. Diabetes 54:2390–95 [Google Scholar]
  125. Wynne K, Park AJ, Small CJ, Meeran K, Ghatei MA. 125.  et al. 2006. Oxyntomodulin increases energy expenditure in addition to decreasing energy intake in overweight and obese humans: a randomised controlled trial. Int. J. Obes. 30:1729–36 [Google Scholar]
  126. Bhutta HY, Deelman TE, le Roux CW, Ashley SW, Rhoads DB, Tavakkoli A. 126.  2014. Intestinal sweet-sensing pathways and metabolic changes after Roux-en-Y gastric bypass surgery. Am. J. Physiol. Gastrointest. Liver Physiol. 307:G588–93 [Google Scholar]
  127. Mokadem M, Zechner JF, Margolskee RF, Drucker DJ, Aguirre V. 127.  2013. Effects of Roux-en-Y gastric bypass on energy and glucose homeostasis are preserved in two mouse models of functional glucagon-like peptide-1 deficiency. Mol. Metab. 3:191–201 [Google Scholar]
  128. Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ. 128.  et al. 2007. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. PNAS 104:15069–74 [Google Scholar]
  129. Margolskee RF, Dyer J, Kokrashvili Z, Salmon KS, Ilegems E. 129.  et al. 2007. T1R3 and gustducin in gut sense sugars to regulate expression of Na+-glucose cotransporter 1. PNAS 104:15075–80 [Google Scholar]
  130. Chambers AP, Stefater MA, Wilson-Pérez HE, Jessen L, Sisley S. 130.  et al. 2011. Similar effects of Roux-en-Y gastric bypass and vertical sleeve gastrectomy on glucose regulation in rats. Physiol. Behav. 105:120–23 [Google Scholar]
  131. Chambers AP, Jessen L, Ryan KK, Sisley S, Wilson-Pérez HE. 131.  et al. 2011. Weight-independent changes in blood glucose homeostasis after gastric bypass or vertical sleeve gastrectomy in rats. Gastroenterology 141:950–58 [Google Scholar]
  132. Bojsen-Møller KN, Dirksen C, Jörgensen NB, Jacobsen SH, Hansen DL. 132.  et al. 2013. Increased hepatic insulin clearance after Roux-en-Y gastric bypass. J. Clin. Endocrinol. Metab. 98:E1066–71 [Google Scholar]
  133. Bojsen-Møller KN, Dirksen C, Jörgensen NB, Jacobsen SH, Serup AK. 133.  et al. 2014. 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 63:1725–37 [Google Scholar]
  134. Dirksen C, Jörgensen NB, Bojsen-Møller KN, Jacobsen SH, Hansen DL. 134.  et al. 2012. Mechanisms of improved glycaemic control after Roux-en-Y gastric bypass. Diabetologia 55:1890–901 [Google Scholar]
  135. Xu G, Stoffers DA, Habener JF, Bonner-Weir S. 135.  1999. Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats. Diabetes 48:2270–76 [Google Scholar]
  136. Zhou X, Qian B, Ji N, Lui C, Liu Z. 136.  et al. 2016. Pancreatic hyperplasia after gastric bypass surgery in a GK rat model of non-obese type 2 diabetes. J. Endocrinol. 228:13–23 [Google Scholar]
  137. Fujita Y, Wideman RD, Asadi A, Yang GK, Baker R. 137.  et al. 2010. Glucose-dependent insulinotropic polypeptide is expressed in pancreatic islet alpha-cells and promotes insulin secretion. Gastroenterology 138:1966–75 [Google Scholar]
  138. Seyfried F, Miras AD, Rotzinger L, Nordbeck A, Corteville C. 138.  et al. 2016. Gastric bypass-related effects on glucose control, β cell function and morphology in the obese Zucker rat. Obes. Surg. 26:1228–36 [Google Scholar]
  139. von Drygalski A, Andris DA. 139.  2009. Anemia after bariatric surgery: more than just iron deficiency. Nutr. Clin. Pract. 24:217–26 [Google Scholar]
  140. Concors SJ, Ecker BL, Maduka R, Furukawa A, Raper SE. 140.  et al. 2016. Complications and surveillance after bariatric surgery. Curr. Treat. Options Neurol. 18:5 [Google Scholar]
  141. Kwon Y, Kim HJ, Lo Menzo E, Park S, Szomstein S, Rosenthal RJ. 141.  2014. Anemia, iron and vitamin B12 deficiencies after sleeve gastrectomy compared to Roux-en-Y gastric bypass: a meta-analysis. Surg. Obes. Relat. Dis. 10:589–97 [Google Scholar]
  142. Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan SL. 142.  2004. Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. J. Clin. Endocrinol. Metab. 89:1061–65 [Google Scholar]
  143. Shah M, Simha V, Garg A. 143.  2006. Review: long-term impact of bariatric surgery on body weight, comorbidities, and nutritional status. J. Clin. Endocrinol. Metab. 91:4223–31 [Google Scholar]
  144. Uebelhart B. 144.  2016. Effects of bariatric surgery on bone. Joint Bone Spine 83:271–75 [Google Scholar]
  145. Abegg K, Gehring N, Wagner CA, Liesegang A, Schiesser M. 145.  et al. 2013. Roux-en-Y gastric bypass surgery reduces bone mineral density and induces metabolic acidosis in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 305:R999–1009 [Google Scholar]
  146. Abdeen G, le Roux CW. 146.  2016. Mechanism underlying the weight loss and complications of Roux-en-Y gastric bypass. review. Obes. Surg. 26:410–21 [Google Scholar]
  147. Schafer AL, Weaver CM, Black DM, Wheeler AL, Chang H. 147.  et al. 2015. Intestinal calcium absorption decreases dramatically after gastric bypass surgery despite optimization of vitamin D status. J. Bone Miner. Res. 30:1377–85 [Google Scholar]
  148. Sakhaee K, Poindexter J, Aguirre C. 148.  2016. The effects of bariatric surgery on bone and nephrolithiasis. Bone 84:1–8 [Google Scholar]
  149. Stemmer K, Bielohuby M, Grayson BE, Begg DP, Chambers AP. 149.  et al. 2013. Roux-en-Y gastric bypass surgery but not vertical sleeve gastrectomy decreases bone mass in male rats. Endocrinology 154:2015–24 [Google Scholar]
  150. Stein EM, Silverberg SJ. 150.  2014. Bone loss after bariatric surgery: causes, consequences, and management. Lancet Diabetes Endocrinol 2:165–74 [Google Scholar]
  151. Cheng Q, Boucher BJ, Leung PS. 151.  2013. Modulation of hypovitaminosis D-induced islet dysfunction and insulin resistance through direct suppression of the pancreatic islet renin-angiotensin system in mice. Diabetologia 56:553–62 [Google Scholar]
  152. Leung PS. 152.  2016. The potential protective action of vitamin D in hepatic insulin resistance and pancreatic islet dysfunction in type 2 diabetes mellitus. Nutrients 8:147 [Google Scholar]
  153. Wortley KE, Garcia K, Okamoto H, Thabet K, Anderson KD. 153.  et al. 2007. Peptide YY regulates bone turnover in rodents. Gastroenterology 133:1534–43 [Google Scholar]
  154. Wong IP, Driessler F, Khor EC, Shi YC, Hormer B. 154.  et al. 2012. Peptide YY regulates bone remodeling in mice: a link between gut and skeletal biology. PLOS ONE 7:e40038 [Google Scholar]
  155. Sainsbury A, Baldock PA, Schwarzer C, Ueno N, Enriquez RF. 155.  et al. 2003. Synergistic effects of Y2 and Y4 receptors on adiposity and bone mass revealed in double knockout mice. Mol. Cell. Biol. 23:5225–33 [Google Scholar]
  156. Utz AL, Lawson EA, Misra M, Mickley D, Gleysteen S. 156.  et al. 2008. Peptide YY (PYY) levels and bone mineral density (BMD) in women with anorexia nervosa. Bone 43:135–39 [Google Scholar]
  157. Meng J, Ma X, Wang N, Jia M, Bi L. 157.  et al. 2016. Activation of GLP-1 receptor promotes bone marrow stromal cell osteogenic differentiation through β-catenin. Stem Cell. Rep. 6:579–91 [Google Scholar]
  158. Luger M, Kruschitz R, Marculescu R, Haslacher H, Hoppichler F. 158.  et al. 2015. The link between obesity and vitamin D in bariatric patients with omega-loop gastric bypass surgery—a vitamin D supplementation trial to compare the efficacy of postoperative cholecalciferol loading (LOAD): study protocol for a randomized controlled trial. Trials 16:328 [Google Scholar]
  159. O'Kane M, Barth JH. 159.  2016. Nutritional follow-up of patients after obesity surgery: best practice. Clin. Endocrinol. 84:658–61 [Google Scholar]
  160. Fernández-Real JM, López-Bermejo A, Ricart W. 160.  2005. Iron stores, blood donation, and insulin sensitivity and secretion. Clin. Chem. 51:1201–5 [Google Scholar]
  161. Lao TT, Ho LF. 161.  2004. Impact of iron deficiency anemia on prevalence of gestational diabetes mellitus. Diabetes Care 27:650–56 [Google Scholar]
  162. Cooksey RC, Jones D, Gabrielsen S, Huang J, Simcox JA. 162.  et al. 2010. Dietary iron restriction or iron chelation protects from diabetes and loss of β-cell function in the obese (ob/ob lep/) mouse. Am. J. Physiol. Endocrinol. Metab. 298:E1236–43 [Google Scholar]
  163. Vari IS, Balkau B, Kettaneh A, André P, Tichet J. 163.  et al. 2007. Ferritin and transferrin are associated with metabolic syndrome abnormalities and their change over time in a general population: data from an epidemiological study on the insulin resistance syndrome (DESIR). Diabetes Care 30:1795–801 [Google Scholar]
  164. Cooksey RC, Jouihan HA, Ajioka RS, Hazel MW, Jones DL. 164.  et al. 2004. Oxidative stress, β-cell apoptosis, and decreased insulin secretory capacity in mouse models of hemochromatosis. Endocrinology 145:5305–12 [Google Scholar]
  165. Swaminathan S, Fonseca VA, Alam MG, Shah SV. 165.  2007. The role of iron in diabetes and its complications. Diabetes Care 30:1926–33 [Google Scholar]
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