Narrative review: Effect of bariatric surgery on type 2 diabetes mellitus

Annals of Internal Medicine

Volumn 150, Issue 2, 2009, Pages 94-103

  Vetter, Marion L ^a   Cardillo, Serena ^a   Rickels, Michael R ^a   Iqbal, Nayyar ^a  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL BENZOATE PLUS PROGESTERONE; GASTRIC INHIBITORY POLYPEPTIDE; GASTROINTESTINAL HORMONE; GHRELIN; GLUCAGON LIKE PEPTIDE 1; GLYCOPEPTIDASE; INCRETIN; PEPTIDE YY;

BARIATRIC SURGERY; CALORIC RESTRICTION; GLYCEMIC CONTROL; HUMAN; HYPOGLYCEMIA; INSULIN RELEASE; INTESTINE SECRETION; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; REVIEW; STOMACH BYPASS; SURGICAL TECHNIQUE; WEIGHT REDUCTION;

EID: 58749090731     PISSN: 00034819     EISSN: 15393704     Source Type: Journal    
DOI: 10.7326/0003-4819-150-2-200901200-00007     Document Type: Review

References (87)

1. Rubino F. Bariatric surgery: effects on glucose homeostasis. Curr Opin Clin Nutr Metab Care. 2006;9:497-507. [PMID: 16778583]
2. Fetner R, McGinty J, Russell C, Pi-Sunyer FX, Laferrère B. Incretins, diabetes, and bariatric surgery: a review. Surg Obes Relat Dis. 2005;1:589-97; discussion 597-8. [PMID: 16925299]
3. Higgins JP, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions, Version 5.0.0 [updated February 2008]. The Cochrane Collaboration; 2008. Accessed at www.cochrane-handbook.org on 2 September 2008.
4. Pories WJ, Swanson MS, MacDonald KG, Long SB, Morris PG, Brown BM, et al. Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg. 1995;222:339-50; discussion 350-2. [PMID: 7677463]
5. Murphy KG, Bloom SR. Gut hormones and the regulation of energy homeostasis. Nature. 2006;444:854-9. [PMID: 17167473]
6. Maggard MA, Shugarman LR, Suttorp M, Maglione M, Sugerman HJ, Sugarman HJ, et al. Meta-analysis: surgical treatment of obesity. Ann Intern Med. 2005;142:547-59. [PMID: 15809466]
7. Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, et al. Bariatric surgery: a systematic review and meta-analysis. JAMA. 2004;292:1724-37. [PMID: 15479938]
8. Schneider BE, Mun EC. Surgical management of morbid obesity. Diabetes Care. 2005;28:475-80. [PMID: 15677820]
9. Ferchak CV, Meneghini LF. Obesity, bariatric surgery and type 2 diabetes - systematic review. Diabetes Metab Res Rev. 2004;20:438-45. [PMID: 15386803]
10. Shah M, Simha V, Garg A. Review: long-term impact of bariatric surgery on body weight, comorbidities, and nutritional status. J Clin Endocrinol Metab. 2006;91:4223-31. [PMID: 16954156]
11. Bult MJ, van Dalen T, Muller AF. Surgical treatment of obesity. Eur J Endocrinol. 2008;158:135-45. [PMID: 18230819]
12. Colquitt J, Clegg A, Loveman E, Royle P, Sidhu MK. Surgery for morbid obesity. Cochrane Database Syst Rev. 2005:CD003641. [PMID: 16235331]
13. Sjöström L, Narbro K, Sjöström CD, Karason K, Larsson B, Wedel H, et al. Swedish Obese Subjects Study. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med. 2007;357:741-52. [PMID: 17715408]
14. Dixon JB, O'Brien PE, Playfair J, Chapman L, Schachter LM, Skinner S, et al. Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial. JAMA. 2008;299:316-23. [PMID: 18212316]
15. Scopinaro N, Marinari GM, Camerini GB, Papadia FS, Adami GF. Specific effects of biliopancreatic diversion on the major components of metabolic syndrome: a long-term follow-up study. Diabetes Care. 2005;28:2406-11. [PMID: 16186271]
16. Marceau P, Hould FS, Simard S, Lebel S, Bourque RA, Potvin M, et al. Biliopancreatic diversion with duodenal switch. World J Surg. 1998;22:947-54. [PMID: 9717420]
17. MacDonald KG Jr, Long SD, Swanson MS, Brown BM, Morris P, Dohm GL, et al. The gastric bypass operation reduces the progression and mortality of non-insulin-dependent diabetes mellitus. J Gastrointest Surg. 1997;1:213-20; discussion 220. [PMID: 9834350]
18. Schauer PR, Burguera B, Ikramuddin S, Cottam D, Gourash W, Hamad G, et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg. 2003;238:467-84; discussion 84-5. [PMID: 14530719]
19. Sugerman HJ, Wolfe LG, Sica DA, Clore JN. Diabetes and hypertension in severe obesity and effects of gastric bypass-induced weight loss. Ann Surg. 2003;237:751-6; discussion 757-8. [PMID: 12796570]
20. Pontiroli AE, Pizzocri P, Librenti MC, Vedani P, Marchi M, Cucchi E, et al. Laparoscopic adjustable gastric banding for the treatment of morbid (grade 3) obesity and its metabolic complications: a three-year study. J Clin Endocrinol Metab. 2002;87:3555-61. [PMID: 12161474]
21. Sjöström L, Lindroos AK, Peltonen M, Torgerson J, Bouchard C, Carlsson B, et al. Swedish Obese Subjects Study Scientific Group. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med. 2004;351:2683-93. [PMID: 15616203]
22. Ponce J, Haynes B, Paynter S, Fromm R, Lindsey B, Shafer A, et al. Effect of Lap-Band-induced weight loss on type 2 diabetes mellitus and hypertension. Obes Surg. 2004;14:1335-42. [PMID: 15603648]
23. Levy P, Fried M, Santini F, Finer N. The comparative effects of bariatric surgery on weight and type 2 diabetes. Obes Surg. 2007;17:1248-56. [PMID: 18074502]
24. Torquati A, Lutfi R, Abumrad N, Richards WO. Is Roux-en-Y gastric bypass surgery the most effective treatment for type 2 diabetes mellitus in morbidly obese patients? J Gastrointest Surg. 2005;9:1112-6; discussion 1117-8. [PMID: 16269382]
25. Dixon JB, Dixon AF, O'Brien PE. Improvements in insulin sensitivity and β-cell function (HOMA) with weight loss in the severely obese. Homeostatic model assessment. Diabet Med. 2003;20:127-34. [PMID: 12581264]
26. Creutzfeldt W. The [pre-] history of the incretin concept. Regul Pept. 2005;128:87-91. [PMID: 15780427]
27. Perley MJ, Kipnis DM. Plasma insulin responses to oral and intravenous glucose: studies in normal and diabetic sujbjects. J Clin Invest. 1967;46:1954-62. [PMID: 6074000]
28. Creutzfeldt W. The incretin concept today. Diabetologia. 1979;16:75-85. [PMID: 32119]
29. Unger RH, Eisentraut AM. Entero-insular axis. Arch Intern Med. 1969;123:261-6. [PMID: 4885674]
30. Hansotia T, Drucker DJ. GIP and GLP-1 as incretin hormones: lessons from single and double incretin receptor knockout mice. Regul Pept. 2005;128:125-34. [PMID: 15780432]
31. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev. 2007;87:1409-39. [PMID: 17928588]
32. Flint A, Raben A, Ersbøll AK, Holst JJ, Astrup A. The effect of physiological levels of glucagon-like peptide-1 on appetite, gastric emptying, energy and substrate metabolism in obesity. Int J Obes Relat Metab Disord. 2001;25:781-92. [PMID: 11439290]
33. Gutzwiller JP, Göke B, Drewe J, Hildebrand P, Ketterer S, Handschin D, et al. Glucagon-like peptide-1: a potent regulator of food intake in humans. Gut. 1999;44:81-6. [PMID: 9862830]
34. Toft-Nielsen MB, Madsbad S, Holst JJ. Continuous subcutaneous infusion of glucagon-like peptide 1 lowers plasma glucose and reduces appetite in type 2 diabetic patients. Diabetes Care. 1999;22:1137-43. [PMID: 10388979]
35. Luque MA, González N, Márquez L, Acitores A, Redondo A, Morales M, et al. Glucagon-like peptide-1 (GLP-1) and glucose metabolism in human myocytes. J Endocrinol. 2002;173:465-73. [PMID: 12065236]
36. Meier JJ, Nauck MA, Schmidt WE, Gallwitz B. Gastric inhibitory polypeptide: the neglected incretin revisited. Regul Pept. 2002;107:1-13. [PMID: 12137960]
37. 3-36): Part I. Distribution, release and actions. Obes Surg. 2006;16:651-8. [PMID: 16687037]
38. Cummings DE, Overduin J. Gastrointestinal regulation of food intake. J Clin Invest. 2007;117:13-23. [PMID: 17200702]
39. Kageyama H, Funahashi H, Hirayama M, Takenoya F, Kita T, Kato S, et al. Morphological analysis of ghrelin and its receptor distribution in the rat pancreas. Regul Pept. 2005;126:67-71. [PMID: 15620416]
40. Cummings DE, Shannon MH. Ghrelin and gastric bypass: is there a hormonal contribution to surgical weight loss? J Clin Endocrinol Metab. 2003;88:2999-3002. [PMID: 12843132]
41. Vollmer K, Holst JJ, Baller B, Ellrichmann M, Nauck MA, Schmidt WE, et al. Predictors of incretin concentrations in subjects with normal, impaired, and diabetic glucose tolerance. Diabetes. 2008;57:678-87. [PMID: 18057091]
42. Holst JJ, Gromada J, Nauck MA. The pathogenesis of NIDDM involves a defective expression of the GIP receptor. Diabetologia. 1997;40:984-6. [PMID: 9267997]
43. Tseng CC, Boylan MO, Jarboe LA, Usdin TB, Wolfe MM. Chronic desensitization of the glucose-dependent insulinotropic polypeptide receptor in diabetic rats. Am J Physiol. 1996;270:E661-6. [PMID: 8928774]
44. Crockett SE, Mazzaferri EL, Cataland S. Gastric inhibitory polypeptide (GIP) in maturity-onset diabetes mellitus. Diabetes. 1976;25:931-5. [PMID: 976601]
45. Ross SA, Brown JC, Dupré J. Hypersecretion of gastric inhibitory polypeptide following oral glucose in diabetes mellitus. Diabetes. 1977;26:525-9. [PMID: 324834]
46. Nauck MA, Kleine N, Orskov C, Holst JJ, Willms B, Creutzfeldt W. Normalization of fasting hyperglycaemia by exogenous glucagon-like peptide 1 (7-36 amide) in type 2 (non-insulin-dependent) diabetic patients. Diabetologia. 1993;36:741-4. [PMID: 8405741]
47. Batterham RL, Cohen MA, Ellis SM, Le Roux CW, Withers DJ, Frost GS, et al. Inhibition of food intake in obese subjects by peptide YY3-36. N Engl J Med. 2003;349:941-8. [PMID: 12954742]
48. Tschöp M, Weyer C, Tataranni PA, Devanarayan V, Ravussin E, Heiman ML. Circulating ghrelin levels are decreased in human obesity. Diabetes. 2001;50:707-9. [PMID: 11289032]
49. Pöykkö SM, Kellokoski E, Hörkkö S, Kauma H, Kesäniemi YA, Ukkola O. Low plasma ghrelin is associated with insulin resistance, hypertension, and the prevalence of type 2 diabetes. Diabetes. 2003;52:2546-53. [PMID: 14514639]
50. Grey N, Kipnis DM. Effect of diet composition on the hyperinsulinemia of obesity. N Engl J Med. 1971;285:827-31. [PMID: 5570845]
51. Kelley DE, Wing R, Buonocore C, Sturis J, Polonsky K, Fitzsimmons M. Relative effects of calorie restriction and weight loss in noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab. 1993;77:1287-93. [PMID: 8077323]
52. Gumbs AA, Modlin IM, Ballantyne GH. Changes in insulin resistance following bariatric surgery: role of caloric restriction and weight loss. Obes Surg. 2005;15:462-73. [PMID: 15946423]
53. Rubino F, Gagner M, Gentileschi P, Kini S, Fukuyama S, Feng J, et al. The early effect of the Roux-en-Y gastric bypass on hormones involved in body weight regulation and glucose metabolism. Ann Surg. 2004;240:236-42. [PMID: 15273546]
54. Cummings DE, Overduin J, Foster-Schubert KE, Carlson MJ. Role of the bypassed proximal intestine in the anti-diabetic effects of bariatric surgery [Editorial]. Surg Obes Relat Dis. 2007;3:109-15. [PMID: 17386391]
55. Patriti A, Aisa MC, Annetti C, Sidoni A, Galli F, Ferri I, et al. How the hindgut can cure type 2 diabetes. Ileal transposition improves glucose metabolism and beta-cell function in Goto-kakizaki rats through an enhanced Proglucagon gene expression and L-cell number. Surgery. 2007;142:74-85. [PMID: 17630003]
56. Rubino F. Is type 2 diabetes an operable intestinal disease? A provocative yet reasonable hypothesis. Diabetes Care. 2008;31 Suppl 2:S290-6. [PMID: 18227499]
57. Rubino F, Forgione A, Cummings DE, Vix M, Gnuli D, Mingrone G, 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. 2006;244:741-9. [PMID: 17060767]
58. Cohen RV, Schiavon CA, Pinheiro JS, Correa JL, Rubino F. Duodenal-jejunal bypass for the treatment of type 2 diabetes in patients with body mass index of 22-34 kg/m2: a report of 2 cases. Surg Obes Relat Dis. 2007;3:195-7. [PMID: 17386401]
59. Deacon CF. What do we know about the secretion and degradation of incretin hormones? Regul Pept. 2005;128:117-24. [PMID: 15780431]
60. Clements RH, Gonzalez QH, Long CI, Wittert G, Laws HL. Hormonal changes after Roux-en Y gastric bypass for morbid obesity and the control of type-II diabetes mellitus. Am Surg. 2004;70:1-4; discussion 4-5. [PMID: 14964537]
61. Laferrère B, Teixeira J, McGinty J, Tran H, Egger JR, Colarusso A, 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. 2008;93:2479-85. [PMID: 18430778]
62. Laferrère B, Tran H, Egger JR, Yap K, Bawa B, Teixeira J, et al. The increase in GLP-1 levels and incretin effect after Roux-en-Y gastric bypass surgery (RYGBP) persists up to 1 year in patients with type 2 diabetes mellitus (T2DM) [Abstract]. Obesity 2007;15:7
63. Näslund E, Grybäck P, Backman L, Jacobsson H, Holst JJ, Theodorsson E, et al. Distal small bowel hormones: correlation with fasting antroduodenal motility and gastric emptying. Dig Dis Sci. 1998;43:945-52. [PMID: 9590405]
64. Folli F, Pontiroli AE, Schwesinger WH. Metabolic aspects of bariatric surgery. Med Clin North Am. 2007;91:393-414, x. [PMID: 17509385]
65. Shak JR, Roper J, Perez-Perez GI, Tseng CH, Francois F, Gamagaris Z, et al. The effect of laparoscopic gastric banding surgery on plasma levels of appetite-control, insulinotropic, and digestive hormones. Obes Surg. 2008;18:1089-96. [PMID: 18408980]
66. le Roux CW, Aylwin SJ, Batterham RL, Borg CM, Coyle F, Prasad V, et al. Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg. 2006;243:108-14. [PMID: 16371744]
67. Rodieux F, Giusti V, D'Alessio DA, Suter M, Tappy L. Effects of gastric bypass and gastric banding on glucose kinetics and gut hormone release. Obesity (Silver Spring). 2008;16:298-305. [PMID: 18239636]
68. Horowitz M, Collins PJ, Chatterton BE, Harding PE, Watts JM, Shearman DJ. Gastric emptying after gastroplasty for morbid obesity. Br J Surg. 1984;71:435-7. [PMID: 6722479]
69. Korner J, Bessler M, Inabnet W, Taveras C, Holst JJ. Exaggerated glucagon-like peptide-1 and blunted glucose-dependent insulinotropic peptide secretion are associated with Roux-en-Y gastric bypass but not adjustable gastric banding. Surg Obes Relat Dis. 2007;3:597-601. [PMID: 17936091]
70. le Roux CW, Welbourn R, Werling M, Osborne A, Kokkinos A, Laurenius A, et al. Gut hormones as mediators of appetite and weight loss after Roux-en-Y gastric bypass. Ann Surg. 2007;246:780-5. [PMID: 17968169]
71. Morínigo R, Moizé V, Musri M, Lacy AM, Navarro S, Marín JL, et al. Glucagon-like peptide-1, peptide YY, hunger, and satiety after gastric bypass surgery in morbidly obese subjects. J Clin Endocrinol Metab. 2006;91:1735-40. [PMID: 16478824]
72. Korner J, Bessler M, Cirilo LJ, Conwell IM, Daud A, Restuccia NL, et al. Effects of Roux-en-Y gastric bypass surgery on fasting and postprandial concentrations of plasma ghrelin, peptide YY, and insulin. J Clin Endocrinol Metab. 2005;90:359-65. [PMID: 15483088]
73. Morínigo R, Vidal J, Lacy AM, Delgado S, Casamitjana R, Gomis R. Circulating peptide YY, weight loss, and glucose homeostasis after gastric bypass surgery in morbidly obese subjects. Ann Surg. 2008;247:270-5. [PMID: 18216532]
74. Korner J, Inabnet W, Conwell IM, Taveras C, Daud A, Olivero-Rivera L, et al. Differential effects of gastric bypass and banding on circulating gut hormone and leptin levels. Obesity (Silver Spring). 2006;14:1553-61. [PMID: 17030966]
75. Laferrère B, Heshka S, Wang K, Khan Y, McGinty J, Teixeira J, 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. 2007;30:1709-16. [PMID: 17416796]
76. Whitson BA, Leslie DB, Kellogg TA, Maddaus MA, Buchwald H, Billington CJ, et al. Entero-endocrine changes after gastric bypass in diabetic and nondiabetic patients: a preliminary study. J Surg Res. 2007;141:31-9. [PMID: 17574036]
77. Patriti A, Facchiano E, Sanna A, Gullà N, Donini A. The enteroinsular axis and the recovery from type 2 diabetes after bariatric surgery. Obes Surg. 2004;14:840-8. [PMID: 15318993]
78. Cummings DE, Weigle DS, Frayo RS, Breen PA, Ma MK, Dellinger EP, et al. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med. 2002;346:1623-30. [PMID: 12023994]
79. Geloneze B, Tambascia MA, Pilla VF, Geloneze SR, Repetto EM, Pareja JC. Ghrelin: a gut-brain hormone: effect of gastric bypass surgery. Obes Surg. 2003;13:17-22. [PMID: 12630608]
80. Faraj M, Havel PJ, Phélis S, Blank D, Sniderman AD, Cianflone K. Plasma acylation-stimulating protein, adiponectin, leptin, and ghrelin before and after weight loss induced by gastric bypass surgery in morbidly obese subjects. J Clin Endocrinol Metab. 2003;88:1594-602. [PMID: 12679444]
81. Holdstock C, Engström BE, Ohrvall M, Lind L, Sundbom M, Karlsson FA. Ghrelin and adipose tissue regulatory peptides: effect of gastric bypass surgery in obese humans. J Clin Endocrinol Metab. 2003;88:3177-83. [PMID: 12843162]
82. Frühbeck G, Diez-Caballero A, Gil MJ, Montero I, Gómez-Ambrosi J, Salvador J, et al. The decrease in plasma ghrelin concentrations following bariatric surgery depends on the functional integrity of the fundus. Obes Surg. 2004;14:606-12. [PMID: 15186626]
83. Nijhuis J, van Dielen FM, Buurman WA, Greve JW. Ghrelin, leptin and insulin levels after restrictive surgery: a 2-year follow-up study. Obes Surg. 2004;14:783-7. [PMID: 15318982]
84. Kahn SE, Prigeon RL, McCulloch DK, Boyko EJ, Bergman RN, Schwartz MW, et al. Quantification of the relationship between insulin sensitivity and beta-cell function in human subjects. Evidence for a hyperbolic function. Diabetes. 1993;42:1663-72. [PMID: 8405710]
85. Dunn JP, Jagasia SM. Case study: management of type 2 diabetes after bariatric surgery. Clin Diabetes 2007;25:112-4.
86. Patti ME, McMahon G, Mun EC, Bitton A, Holst JJ, Goldsmith J, et al. Severe hypoglycaemia post-gastric bypass requiring partial pancreatectomy: evidence for inappropriate insulin secretion and pancreatic islet hyperplasia. Diabetologia. 2005;48:2236-40. [PMID: 16195867]
87. Goldfine AB, Mun EC, Devine E, Bernier R, Baz-Hecht M, Jones DB, et al. Patients with neuroglycopenia after gastric bypass surgery have exaggerated incretin and insulin secretory responses to a mixed meal. J Clin Endocrinol Metab. 2007;92:4678-85. [PMID: 17895322]