Current evidence for a role of GLP-1 in Roux-en-Y gastric bypass-induced remission of type 2 diabetes

Diabetes, Obesity and Metabolism

Volumn 14, Issue 4, 2012, Pages 291-298

  Rhee, N A ^a   Vilsboll T ^a   Knop, F K ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Glucagon; Glucagon like peptide 1; Glucose dependent insulinotropic polypeptide; Incretin hormones; Remission; Type 2 diabetes; Weight loss

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; GLUCOSE;

ANTIDIABETIC ACTIVITY; DIET THERAPY; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HORMONE ACTION; HORMONE RELEASE; HUMAN; INSULIN SENSITIVITY; NON INSULIN DEPENDENT DIABETES MELLITUS; ORAL GLUCOSE TOLERANCE TEST; OUTCOME ASSESSMENT; POSTOPERATIVE PERIOD; POSTPRANDIAL STATE; REMISSION; REVIEW; ROUX Y ANASTOMOSIS; WEIGHT REDUCTION;

EID: 84858004978     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/j.1463-1326.2011.01505.x     Document Type: Review

References (75)

1. IDF. Diabetes and impaired glucose tolerance, International Diabetes Federation. 2009. Available from URL:. Accessed 5 September 2011.
2. Dixon JB, O'Brien PE, Playfair J et al. Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial. JAMA 2008; 299: 316-323.
3. Kahan S. ACP Journal Club. Bariatric surgery was dominant over conventional therapy for lifetime management of type 2 diabetes in obese patients. Ann Intern Med 2009; 151: JC2-15.
4. Schauer PR, Burguera B, Ikramuddin S et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg 2003; 238: 467-484; discussion 84-85.
5. Chang C-Y, Huang C-K, Chang Y-Y, Tai C-M, Lin J-T, Wang J-D. Prospective study of health-related quality of life after Roux-en-Y bypass surgery for morbid obesity. Br J Surg 2010; 97: 1541-1546.
6. Suter M, Calmes J-M, Paroz A, Romy S, Giusti V. Results of Roux-en-Y gastric bypass in morbidly obese vs superobese patients: similar body weight loss, correction of comorbidities, and improvement of quality of life. Arch Surg 2009; 144: 312-318; discussion 318.
7. Hager C. Quality of life after Roux-en-Y gastric bypass surgery. AORN J 2007; 768: 770-775, 777-778.
8. Rea JD, Yarbrough DE, Leeth RR, Leath TD, Clements RH. Influence of complications and extent of weight loss on quality of life after laparoscopic Roux-en-Y gastric bypass. Surg Endosc 2007; 21: 1095-1100.
9. MacDonald KG, Long SD, Swanson MS et al. The gastric bypass operation reduces the progression and mortality of non-insulin-dependent diabetes mellitus. J Gastrointest Surg 1997; 1: 213-220; discussion 220.
10. Adams TD, Gress RE, Smith SC et al. Long-term mortality after gastric bypass surgery. N Engl J Med 2007; 357: 753-761.
11. Buchwald H, Avidor Y, Braunwald E et al. Bariatric surgery: a systematic review and meta-analysis. JAMA 2004; 292: 1724-1737.
12. Wickremesekera K, Miller G, Naotunne TD, Knowles G, Stubbs RS. Loss of insulin resistance after Roux-en-Y gastric bypass surgery: a time course study. Obes Surg 2005; 15: 474-481.
13. Kreymann B, Williams G, Ghatei MA, Bloom SR. Glucagon-like peptide-1 7-36: a physiological incretin in man. Lancet 1987; 2: 1300-1304.
14. Holst JJ. On the physiology of GIP and GLP-1. Horm Metab Res 2004; 36: 747-754.
15. Meier JJ, Gallwitz B, Salmen S et al. Normalization of glucose concentrations and deceleration of gastric emptying after solid meals during intravenous glucagon-like peptide 1 in patients with type 2 diabetes. J Clin Endocrinol Metab 2003; 88: 2719-2725.
16. Näslund E, Barkeling B, King N et al. Energy intake and appetite are suppressed by glucagon-like peptide-1 (GLP-1) in obese men. Int J Obes Relat Metab Disord 1999; 23: 304-311.
17. Zander M, Madsbad S, Madsen JL, Holst JJ. Effect of 6-week course of glucagon-like peptide 1 on glycaemic control, insulin sensitivity, and β-cell function in type 2 diabetes: a parallel-group study. Lancet 2002; 359: 824-830.
18. Larsen PJ, Fledelius C, Knudsen LB, Tang-Christensen M. Systemic administration of the long-acting GLP-1 derivative NN2211 induces lasting and reversible weight loss in both normal and obese rats. Diabetes 2001; 50: 2530-2539.
19. Gleysteen JJ. Five-year outcome with gastric bypass: Roux limb length makes a difference. Surg Obes Relat Dis 2009; 5: 242-247; discussion 247-249.
20. Dillemans B, Sakran N, Van Cauwenberge S et al. Standardization of the fully stapled laparoscopic Roux-en-Y gastric bypass for obesity reduces early immediate postoperative morbidity and mortality: a single center study on 2606 patients. Obes Surg 2009; 19: 1355-1364.
21. Pories WJ, Swanson MS, MacDonald KG 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: 339-350; discussion 350-352.
22. Whitson BA, Leslie DB, Kellogg TA et al. Entero-endocrine changes after gastric bypass in diabetic and nondiabetic patients: a preliminary study. J Surg Res 2007; 141: 31-39.
23. Smith BR, Hinojosa MW, Reavis KM, Nguyen NT. Remission of diabetes after laparoscopic gastric bypass. Am Surg 2008; 74: 948-952.
24. 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: 751-756; discussion 757-758.
25. Hall TC, Pellen MGC, Sedman PC, Jain PK. Preoperative factors predicting remission of type 2 diabetes mellitus after Roux-en-Y gastric bypass surgery for obesity. Obes Surg 2010; 20: 1245-1250.
26. Hayes MT, Hunt LA, Foo J, Tychinskaya Y, Stubbs RS. A model for predicting the resolution of type 2 diabetes in severely obese subjects following Roux-en Y gastric bypass surgery. Obes Surg 2011; 21: 910-916.
27. Cohen R, Pinheiro JS, Correa JL, Schiavon CA. Laparoscopic Roux-en-Y gastric bypass for BMI <35 kg/m(2): a tailored approach. Surg Obes Relat Dis 2006; 2: 401-404; discussion 404.
28. Carlin AM, O'Connor EA, Genaw JA, Kawar S. Preoperative weight loss is not a predictor of postoperative weight loss after laparoscopic Roux-en-Y gastric bypass. Surg Obes Relat Dis 2008; 4: 481-485.
29. Laferrère B, Teixeira J, McGinty J 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: 2479-2485.
30. Pattou F, Bearud G, Arnalsteen LL et al. Restoration of β cell function after bariatric surgery in type 2 diabetic patients: a prospective controlled study comparing gastric banding and gastric bypass. Obes surg 2007; 17: 1023-1068.
31. le Roux CW, Aylwin SJB, Batterham RL et al. Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg 2006; 243: 108-114.
32. 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.
33. 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.
34. Laferrère B, Heshka S, Wang K 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: 1709-1716.
35. Pournaras DJ, Osborne A, Hawkins SC et al. Remission of type 2 diabetes after gastric bypass and banding: mechanisms and 2 year outcomes. Ann Surg 2010; 252: 966-971.
36. Cummings DE, Weigle DS, Frayo RS et al. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med 2002; 346: 1623-1630.
37. Eissele R, Göke R, Willemer S et al. Glucagon-like peptide-1 cells in the gastrointestinal tract and pancreas of rat, pig and man. Eur J Clin Invest 1992; 22: 283-291.
38. Herrmann C, Göke R, Richter G, Fehmann HC, Arnold R, Göke B. Glucagon-like peptide-1 and glucose-dependent insulin-releasing polypeptide plasma levels in response to nutrients. Digestion 1995; 56: 117-126.
39. Gutniak MK, Linde B, Holst JJ, Efendić S. Subcutaneous injection of the incretin hormone glucagon-like peptide 1 abolishes postprandial glycemia in NIDDM. Diabetes Care 1994; 17: 1039-1044.
40. Deacon CF, Nauck MA, Toft-Nielsen M, Pridal L, Willms B, Holst JJ. Both subcutaneously and intravenously administered glucagon-like peptide I are rapidly degraded from the NH2-terminus in type II diabetic patients and in healthy subjects. Diabetes 1995; 44: 1126-1131.
41. Mason EE. The mechanisms of surgical treatment of type 2 diabetes. Obes Surg 2005; 15: 459-461.
42. Umeda LM, Silva EA, Carneiro G, Arasaki CH, Geloneze B, Zanella MT. Early improvement in glycemic control after bariatric surgery and its relationships with insulin, GLP-1, and glucagon secretion in type 2 diabetic patients. Obes Surg 2011; 21: 896-901.
43. de Carvalho CP, Marin DM, de Souza AL et al. GLP-1 and adiponectin: effect of weight loss after dietary restriction and gastric bypass in morbidly obese patients with normal and abnormal glucose metabolism. Obes Surg 2009; 19: 313-320.
44. Isbell JM, Tamboli RA, Hansen EN et al. The importance of caloric restriction in the early improvements in insulin sensitivity after Roux-en-Y gastric bypass surgery. Diabetes Care 2010; 33: 1438-1442.
45. Alam ML, Van der Schueren BJ, Ahren B et al. Gastric bypass surgery, but not caloric restriction, decreases dipeptidyl peptidase-4 activity in obese patients with type 2 diabetes. Diabetes Obes Metab 2011; 13: 378-381.
46. Dirksen C, Hansen DL, Madsbad S et al. Postprandial diabetic glucose tolerance is normalized by gastric bypass feeding as opposed to gastric feeding and is associated with exaggerated GLP-1 secretion: a case report. Diabetes Care 2010; 33: 375-377.
47. Hansen EN, Tamboli RA, Isbell JM et al. Role of the foregut in the early improvement in glucose tolerance and insulin sensitivity following Roux-en-Y gastric bypass surgery. Am J Physiol Gastrointest Liver Physiol 2011; 300: G795-802.
48. Shin AC, Zheng H, Townsend RL, Sigalet DL, Berthoud H-R. Meal-induced hormone responses in a rat model of Roux-en-Y gastric bypass surgery. Endocrinology 2010; 151: 1588-1597.
49. le Roux CW, Borg C, Wallis K et al. Gut hypertrophy after gastric bypass is associated with increased glucagon-like peptide 2 and intestinal crypt cell proliferation. Ann Surg 2010; 252: 50-56.
50. Suzuki S, Ramos EJB, Goncalves CG, Chen C, Meguid MM. Changes in GI hormones and their effect on gastric emptying and transit times after Roux-en-Y gastric bypass in rat model. Surgery 2005; 138: 283-290.
51. Meirelles K, Ahmed T, Culnan DM, Lynch CJ, Lang CH, Cooney RN. Mechanisms of glucose homeostasis after Roux-en-Y gastric bypass surgery in the obese, insulin-resistant Zucker rat. Ann Surg 2009; 249: 277-285.
52. Suter M, Donadini A, Romy S, Demartines N, Giusti V. Laparoscopic roux-en-y gastric bypass: significant long-term weight loss, improvement of obesity-related comorbidities and quality of life. Ann Surg 2011; 254: 267-273.
53. Rubino F, Gagner M, Gentileschi P 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: 236-242.
54. le Roux CW, Welbourn R, Werling M et al. Gut hormones as mediators of appetite and weight loss after Roux-en-Y gastric bypass. Ann Surg 2007; 246: 780-785.
55. Morínigo R, Moizé V, Musri M 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: 1735-1740.
56. Vidal J, Nicolau J, Romero F et al. Long-term effects of Roux-en-Y gastric bypass surgery on plasma glucagon-like peptide-1 and islet function in morbidly obese subjects. J Clin Endocrinol Metab 2009; 94: 884-891.
57. Borg CM, Roux CW le, Ghatei MA, Bloom SR, Patel AG, Aylwin SJB. Progressive rise in gut hormone levels after Roux-en-Y gastric bypass suggests gut adaptation and explains altered satiety. Br J Surg 2006; 93: 210-215.
58. Hamza N, Abbas MH, Darwish A, Shafeek Z, New J, Ammori BJ. Predictors of remission of type 2 diabetes mellitus after laparoscopic gastric banding and bypass. Surg Obes Relat Dis 2010 [Epub ahead of print].
59. Reimann F, Ward PS, Gribble FM. Signaling mechanisms underlying the release of glucagon-like peptide 1. 2006; 55: 78-85.
60. Ritzel U, Fromme A, Ottleben M, Leonhardt U, Ramadori G. Release of glucagon-like peptide-1 (GLP-1) by carbohydrates in the perfused rat ileum. Acta Diabetol 1997; 34: 18-21.
61. Beysen C, Karpe F, Fielding BA, Clark A, Levy JC, Frayn KN. Interaction between specific fatty acids, GLP-1 and insulin secretion in humans. Diabetologia 2002; 45: 1533-1541.
62. Gameiro A, Reimann F, Habib AM et al. The neurotransmitters glycine and GABA stimulate glucagon-like peptide-1 release from the GLUTag cell line. J Physiol (Lond). 2005; 569(Pt 3): 761-772.
63. Reimann F, Williams L, da Silva Xavier G, Rutter GA, Gribble FM. Glutamine potently stimulates glucagon-like peptide-1 secretion from GLUTag cells. Diabetologia 2004; 47: 1592-1601.
64. Carr RD, Larsen MO, Winzell MS et al. Incretin and islet hormonal responses to fat and protein ingestion in healthy men. Am J Physiol Endocrinol Metab 2008; 295: E779-784.
65. Cummings BP, Strader AD, Stanhope KL et al. Ileal interposition surgery improves glucose and lipid metabolism and delays diabetes onset in the UCD-T2DM rat. Gastroenterology 2010; 138: 2437-2446; 2446.e1.
66. Thomas C, Gioiello A, Noriega L et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab 2009; 10: 167-177.
67. Patti M-E, Houten SM, Bianco AC et al. Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity (Silver Spring) 2009; 17: 1671-1677.
68. Jia X, Brown JC, Kwok YN, Pederson RA, McIntosh CH. Gastric inhibitory polypeptide and glucagon-like peptide-1(7-36) amide exert similar effects on somatostatin secretion but opposite effects on gastrin secretion from the rat stomach. Can J Physiol Pharmacol 1994; 72: 1215-1219.
69. Hansen L, Deacon CF, Orskov C, Holst JJ. Glucagon-like peptide-1-(7-36)amide is transformed to glucagon-like peptide-1-(9-36)amide by dipeptidyl peptidase IV in the capillaries supplying the L cells of the porcine intestine. Endocrinology 1999; 140: 5356-5363.
70. Vilsbøll T, Krarup T, Deacon CF, Madsbad S, Holst JJ. Reduced postprandial concentrations of intact biologically active glucagon-like peptide 1 in type 2 diabetic patients. Diabetes 2001; 50: 609-613.
71. Nakagawa A, Satake H, Nakabayashi H et al. Receptor gene expression of glucagon-like peptide-1, but not glucose-dependent insulinotropic polypeptide, in rat nodose ganglion cells. Auton Neurosci 2004; 110: 36-43.
72. Balkan B, Li X. Portal GLP-1 administration in rats augments the insulin response to glucose via neuronal mechanisms. Am J Physiol Regul Integr Comp Physiol 2000; 279: R1449-1454.
73. Ahrén B. Sensory nerves contribute to insulin secretion by glucagon-like peptide-1 in mice. Am J Physiol Regul Integr Comp Physiol 2004; 286: R269-272.
74. Meier JJ, Gallwitz B, Siepmann N et al. Gastric inhibitory polypeptide (GIP) dose-dependently stimulates glucagon secretion in healthy human subjects at euglycaemia. Diabetologia 2003; 46: 798-801.
75. Knop FK. Resolution of type 2 diabetes following gastric bypass surgery: involvement of gut-derived glucagon and glucagonotropic signalling? Diabetologia 2009; 52: 2270-2276.