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Published in: Surgical Endoscopy 8/2012

01-08-2012

Comparable early changes in gastrointestinal hormones after sleeve gastrectomy and Roux-En-Y gastric bypass surgery for morbidly obese type 2 diabetic subjects

Authors: Fabiola Romero, Joana Nicolau, Lílliam Flores, Roser Casamitjana, Ainitze Ibarzabal, Antonio Lacy, Josep Vidal

Published in: Surgical Endoscopy | Issue 8/2012

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Abstract

Background

Sleeve gastrectomy (SG) and Roux-en-Y gastric bypass (RYGBP) are associated with similar type 2 diabetes mellitus (T2DM) resolution rates for morbidly obese subjects. However, the mechanisms underlying the resolution of T2DM after SG have not been clarified to date. This study aimed to compare the early changes in gastrointestinal hormones involved in insulin and glucagon secretion in morbidly obese T2DM subjects undergoing SG or RYGBP.

Methods

This prospective study investigated 12 subjects with T2DM who had undergone SG (n = 6) or RYGBP (n = 6). Five body mass index (BMI)-matched obese non-diabetic subjects and five BMI-matched obese diabetic subjects served as control subjects. Glucose, insulin, glucagon, glucagon-like peptide 1 (GLP-1), glucose-dependent insulinotropic polypeptide (GIP), and GLP-2 were determined after a standardized mixed liquid meal before surgery and 6 weeks afterward.

Results

After 6 weeks, five of the six subjects in each surgical group presented with T2DM remission, although the area under the curve (AUC)0–120 of glucose was greater than that of the non-diabetic control subjects (P < 0.01). Postsurgically, the indices of insulin and glucagon secretion were comparable between the two surgical groups. The AUC0–120 of GLP-1 (P < 0.05) and GLP-2 (P < 0.05) was significantly and comparably enlarged after SG and RYGB. The postsurgical GIP response was significantly associated with the glucagon response throughout the meal test (ρ = 0.747; P < 0.01).

Conclusions

The data show that in a cohort of morbidly obese T2DM subjects, SG and RYGBP are associated with an early improvement in glucose tolerance, similar changes in insulin and glucagon secretion, and a similar GLP-1, GIP, and GLP-2 response to a standardized mixed liquid meal.
Literature
1.
go back to reference Gill RS, Karmali S, Sharma AM (2011) Treating type 2 diabetes mellitus with sleeve gastrectomy in obese patients. Obes Silver Spring 19:701–702CrossRef Gill RS, Karmali S, Sharma AM (2011) Treating type 2 diabetes mellitus with sleeve gastrectomy in obese patients. Obes Silver Spring 19:701–702CrossRef
2.
go back to reference Abbatini F, Rizzello M, Casella G, Alessandri G, Capoccia D, Leonetti F, Basso N (2010) Long-term effects of laparoscopic sleeve gastrectomy, gastric bypass, and adjustable gastric banding on type 2 diabetes. Surg Endosc 24:1005–1010PubMedCrossRef Abbatini F, Rizzello M, Casella G, Alessandri G, Capoccia D, Leonetti F, Basso N (2010) Long-term effects of laparoscopic sleeve gastrectomy, gastric bypass, and adjustable gastric banding on type 2 diabetes. Surg Endosc 24:1005–1010PubMedCrossRef
3.
go back to reference Omana J, Nguyen S, Herron D, Kini S (2010) Comparison of comorbidity resolution and improvement between laparoscopic sleeve gastrectomy and laparoscopic adjustable gastric banding. Surg Endosc 24:2513–2517PubMedCrossRef Omana J, Nguyen S, Herron D, Kini S (2010) Comparison of comorbidity resolution and improvement between laparoscopic sleeve gastrectomy and laparoscopic adjustable gastric banding. Surg Endosc 24:2513–2517PubMedCrossRef
4.
go back to reference Vidal J, Ibarzabal A, Romero F, Delgado S, Momblán D, Flores L, Lacy A (2008) Type 2 diabetes mellitus and the metabolic syndrome following sleeve gastrectomy in severely obese subjects. Obes Surg 18:1077–1082PubMedCrossRef Vidal J, Ibarzabal A, Romero F, Delgado S, Momblán D, Flores L, Lacy A (2008) Type 2 diabetes mellitus and the metabolic syndrome following sleeve gastrectomy in severely obese subjects. Obes Surg 18:1077–1082PubMedCrossRef
5.
6.
go back to reference Peterli R, Wölnerhanssen B, Peters T, Devaux N, Kern B, Christoffel-Courtin C, Drewe J, von Flüe M, Beglinger C (2009) Improvement in glucose metabolism after bariatric surgery: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy. Ann Surg 250:234–241PubMedCrossRef Peterli R, Wölnerhanssen B, Peters T, Devaux N, Kern B, Christoffel-Courtin C, Drewe J, von Flüe M, Beglinger C (2009) Improvement in glucose metabolism after bariatric surgery: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy. Ann Surg 250:234–241PubMedCrossRef
7.
go back to reference Karamanakos SN, Vagenas K, Kalfarentzos F, Alexandrides TK (2008) Weight loss, appetite suppression, and changes in fasting and postprandial ghrelin and peptide-YY levels after Roux-en-Y gastric bypass and sleeve gastrectomy. Ann Surg 247:401–407PubMedCrossRef Karamanakos SN, Vagenas K, Kalfarentzos F, Alexandrides TK (2008) Weight loss, appetite suppression, and changes in fasting and postprandial ghrelin and peptide-YY levels after Roux-en-Y gastric bypass and sleeve gastrectomy. Ann Surg 247:401–407PubMedCrossRef
8.
go back to reference Castañeda TR, Tong J, Datta R, Culler M, Tschöp MH (2010) Ghrelin in the regulation of body weight and metabolism. Front Neuroendocrinol 31:44–60PubMedCrossRef Castañeda TR, Tong J, Datta R, Culler M, Tschöp MH (2010) Ghrelin in the regulation of body weight and metabolism. Front Neuroendocrinol 31:44–60PubMedCrossRef
9.
go back to reference Valderas JP, Irribarra V, Rubio L, Boza C, Escalona M, Liberona Y, Matamala A, Maiz A (2011) Effects of sleeve gastrectomy and medical treatment for obesity on glucagon-like peptide 1 levels and glucose homeostasis in non-diabetic subjects. Obes Surg (Epub ahead of print 24 Feb) Valderas JP, Irribarra V, Rubio L, Boza C, Escalona M, Liberona Y, Matamala A, Maiz A (2011) Effects of sleeve gastrectomy and medical treatment for obesity on glucagon-like peptide 1 levels and glucose homeostasis in non-diabetic subjects. Obes Surg (Epub ahead of print 24 Feb)
10.
go back to reference Kahn SE, Hull RL, Utzschneider KM (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444:840–846PubMedCrossRef Kahn SE, Hull RL, Utzschneider KM (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444:840–846PubMedCrossRef
11.
go back to reference Shah P, Vella A, Basu A, Basu R, Schwenk WF, Rizza RA (2000) Lack of suppression of glucagon contributes to postprandial hyperglycemia in subjects with type 2 diabetes mellitus. J Clin Endocrinol Metab 85:4053–4059PubMedCrossRef Shah P, Vella A, Basu A, Basu R, Schwenk WF, Rizza RA (2000) Lack of suppression of glucagon contributes to postprandial hyperglycemia in subjects with type 2 diabetes mellitus. J Clin Endocrinol Metab 85:4053–4059PubMedCrossRef
12.
go back to reference Laferrere B, Teixeira J, McGinty J, Tran H, Egger JR, Colarusso A, Kovack B, Bawa B, Koshy N, Lee H, Yapp K, Olivan B (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 Metabo 93:2479–2485CrossRef Laferrere B, Teixeira J, McGinty J, Tran H, Egger JR, Colarusso A, Kovack B, Bawa B, Koshy N, Lee H, Yapp K, Olivan B (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 Metabo 93:2479–2485CrossRef
13.
go back to reference Laferrère B, Heshka S, Wang K, Khan Y, McGinty J, Teixeira J, Hart AB, Olivan B (2007) Incretin levels and effect are markedly enhanced 1 month after Roux-en-Y gastric bypass surgery in obese patients with type 2 diabetes. Diabetes Care 30:1709–1716PubMedCrossRef Laferrère B, Heshka S, Wang K, Khan Y, McGinty J, Teixeira J, Hart AB, Olivan B (2007) Incretin levels and effect are markedly enhanced 1 month after Roux-en-Y gastric bypass surgery in obese patients with type 2 diabetes. Diabetes Care 30:1709–1716PubMedCrossRef
14.
go back to reference Rubino F, Schauer PR, Kaplan LM, Cummings DE (2010) Metabolic surgery to treat type 2 diabetes: clinical outcomes and mechanisms of action. Annu Rev Med 61:393–411PubMedCrossRef Rubino F, Schauer PR, Kaplan LM, Cummings DE (2010) Metabolic surgery to treat type 2 diabetes: clinical outcomes and mechanisms of action. Annu Rev Med 61:393–411PubMedCrossRef
16.
go back to reference Kashyap SR, Daud S, Kelly KR, Gastaldelli A, Win H, Brethauer S, Kirwan JP, Schauer PR (2010) Acute effects of gastric bypass versus gastric restrictive surgery on beta-cell function and insulinotropic hormones in severely obese patients with type 2 diabetes. Int J Obes Lond 34:462–471PubMedCrossRef Kashyap SR, Daud S, Kelly KR, Gastaldelli A, Win H, Brethauer S, Kirwan JP, Schauer PR (2010) Acute effects of gastric bypass versus gastric restrictive surgery on beta-cell function and insulinotropic hormones in severely obese patients with type 2 diabetes. Int J Obes Lond 34:462–471PubMedCrossRef
17.
go back to reference Bose M, Teixeira J, Olivan B, Bawa B, Arias S, Machineni S, Pi-Sunyer FX, Scherer PE, Laferrère B (2010) Weight loss and incretin responsiveness improve glucose control independently after gastric bypass surgery. J Diabetes 2:47–55PubMedCrossRef Bose M, Teixeira J, Olivan B, Bawa B, Arias S, Machineni S, Pi-Sunyer FX, Scherer PE, Laferrère B (2010) Weight loss and incretin responsiveness improve glucose control independently after gastric bypass surgery. J Diabetes 2:47–55PubMedCrossRef
18.
go back to reference Hansen EN, Tamboli RA, Isbell JM, Saliba J, Dunn JP, Marks-Shulman PA, Abumrad NN (2011) 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 (Epub ahead of print 3 March) Hansen EN, Tamboli RA, Isbell JM, Saliba J, Dunn JP, Marks-Shulman PA, Abumrad NN (2011) 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 (Epub ahead of print 3 March)
19.
go back to reference Meier JJ, Gallwitz B, Siepmann N, Holst JJ, Deacon CF, Schmidt WE, Nauck MA (2003) Gastric inhibitory polypeptide (GIP) dose-dependently stimulates glucagon secretion in healthy human subjects at euglycaemia. Diabetologia 46:798–801PubMedCrossRef Meier JJ, Gallwitz B, Siepmann N, Holst JJ, Deacon CF, Schmidt WE, Nauck MA (2003) Gastric inhibitory polypeptide (GIP) dose-dependently stimulates glucagon secretion in healthy human subjects at euglycaemia. Diabetologia 46:798–801PubMedCrossRef
20.
go back to reference Meier JJ, Nauck MA, Pott A, Heinze K, Goetze O, Bulut K, Schmidt WE, Gallwitz B, Holst JJ (2006) Glucagon-like peptide 2 stimulates glucagon secretion, enhances lipid absorption, and inhibits gastric acid secretion in humans. Gastroenterology 130:44–54PubMedCrossRef Meier JJ, Nauck MA, Pott A, Heinze K, Goetze O, Bulut K, Schmidt WE, Gallwitz B, Holst JJ (2006) Glucagon-like peptide 2 stimulates glucagon secretion, enhances lipid absorption, and inhibits gastric acid secretion in humans. Gastroenterology 130:44–54PubMedCrossRef
21.
go back to reference le Roux CW, Borg C, Wallis K, Vincent RP, Bueter M, Goodlad R, Ghatei MA, Patel A, Bloom SR, Aylwin SJ (2010) Gut hypertrophy after gastric bypass is associated with increased glucagon-like peptide 2 and intestinal crypt cell proliferation. Ann Surg 252:50–56PubMedCrossRef le Roux CW, Borg C, Wallis K, Vincent RP, Bueter M, Goodlad R, Ghatei MA, Patel A, Bloom SR, Aylwin SJ (2010) Gut hypertrophy after gastric bypass is associated with increased glucagon-like peptide 2 and intestinal crypt cell proliferation. Ann Surg 252:50–56PubMedCrossRef
22.
go back to reference Morínigo R, Vidal J, Lacy AM, Delgado S, Casamitjana R, Gomis R (2008) Circulating peptide YY, weight loss, and glucose homeostasis after gastric bypass surgery in morbidly obese subjects. Ann Surg 247:270–275PubMedCrossRef Morínigo R, Vidal J, Lacy AM, Delgado S, Casamitjana R, Gomis R (2008) Circulating peptide YY, weight loss, and glucose homeostasis after gastric bypass surgery in morbidly obese subjects. Ann Surg 247:270–275PubMedCrossRef
23.
go back to reference Maki KC, Rains TM, Dicklin MR, Bell M (2010) Repeatability of indices of insulin sensitivity and secretion from standard liquid meal tests in subjects with type 2 diabetes mellitus or normal or impaired fasting glucose. Diabetes Technol Ther 12:895–900PubMedCrossRef Maki KC, Rains TM, Dicklin MR, Bell M (2010) Repeatability of indices of insulin sensitivity and secretion from standard liquid meal tests in subjects with type 2 diabetes mellitus or normal or impaired fasting glucose. Diabetes Technol Ther 12:895–900PubMedCrossRef
24.
go back to reference Hofso D, Jenssen T, Bollerslev J, Ueland T, Godang K, Stumvoll M, Sandbu R, Roislinen J, Hjelmesaeth J (2011) Beta cell function after weight loss: a clinical trial comparing gastric bypass surgery and intensive lifestyle intervention. Eur J Endocrinol 164:231–238PubMedCrossRef Hofso D, Jenssen T, Bollerslev J, Ueland T, Godang K, Stumvoll M, Sandbu R, Roislinen J, Hjelmesaeth J (2011) Beta cell function after weight loss: a clinical trial comparing gastric bypass surgery and intensive lifestyle intervention. Eur J Endocrinol 164:231–238PubMedCrossRef
25.
go back to reference Isbell JM, Tamboli RA, Hansen EN, Saliba J, Dunn JP, Phillips SE, Marks-Shulman PA, Abumrad NN (2010) The importance of caloric restriction in the early improvements in insulin sensitivity after Roux-en-Y gastric bypass surgery. Diabetes Care 33:1438–1442PubMedCrossRef Isbell JM, Tamboli RA, Hansen EN, Saliba J, Dunn JP, Phillips SE, Marks-Shulman PA, Abumrad NN (2010) The importance of caloric restriction in the early improvements in insulin sensitivity after Roux-en-Y gastric bypass surgery. Diabetes Care 33:1438–1442PubMedCrossRef
26.
go back to reference Vidal J, Nicolau J, Romero F, Casamitjana R, Momblan D, Conget I, Morínigo R, Lacy AM (2009) 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 94:884–891PubMedCrossRef Vidal J, Nicolau J, Romero F, Casamitjana R, Momblan D, Conget I, Morínigo R, Lacy AM (2009) 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 94:884–891PubMedCrossRef
27.
go back to reference Goldfine AB, Mun EC, Devine E, Bernier R, Baz-Hecht M, Jones DB, Schneider BE, Holst JJ, Patti ME (2007) Patients with neuroglycopenia after gastric bypass surgery have exaggerated incretin and insulin secretory responses to a mixed meal. J Clin Endocrinol Metab 92:4678–4685PubMedCrossRef Goldfine AB, Mun EC, Devine E, Bernier R, Baz-Hecht M, Jones DB, Schneider BE, Holst JJ, Patti ME (2007) Patients with neuroglycopenia after gastric bypass surgery have exaggerated incretin and insulin secretory responses to a mixed meal. J Clin Endocrinol Metab 92:4678–4685PubMedCrossRef
28.
go back to reference Pocai A, Carrington PE, Adams JR, Wright M, Eiermann G, Zhu L, Du X, Petrov A, Lassman ME, Jiang G, Liu F, Miller C, Tota LM, Zhou G, Zhang X, Sountis MM, Santoprete A, Capito’ E, Chicchi GG, Thornberry N, Bianchi E, Pessi A, Marsh DJ, SinhaRoy R (2009) Glucagon-like peptide 1/glucagon receptor dual agonism reverses obesity in mice. Diabetes 58:2258–2266PubMedCrossRef Pocai A, Carrington PE, Adams JR, Wright M, Eiermann G, Zhu L, Du X, Petrov A, Lassman ME, Jiang G, Liu F, Miller C, Tota LM, Zhou G, Zhang X, Sountis MM, Santoprete A, Capito’ E, Chicchi GG, Thornberry N, Bianchi E, Pessi A, Marsh DJ, SinhaRoy R (2009) Glucagon-like peptide 1/glucagon receptor dual agonism reverses obesity in mice. Diabetes 58:2258–2266PubMedCrossRef
29.
go back to reference Korner J, Bessler M, Inabnet W, Taveras C, Holst JJ (2007) 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 3:597–601PubMedCrossRef Korner J, Bessler M, Inabnet W, Taveras C, Holst JJ (2007) 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 3:597–601PubMedCrossRef
30.
go back to reference Rodieux f, Giusti V, D’Alessio DA, Suter M, Tappy L (2008) Effects of gastric bypass and gastric banding on glucose kinetics and gut hormone release. Obes Silver Spring 16:298–305CrossRef Rodieux f, Giusti V, D’Alessio DA, Suter M, Tappy L (2008) Effects of gastric bypass and gastric banding on glucose kinetics and gut hormone release. Obes Silver Spring 16:298–305CrossRef
31.
go back to reference Shah S, Shah P, Todkar J, Gagner M, Sonar S, Solav S (2010) Prospective controlled study of effect of laparoscopic sleeve gastrectomy on small bowel transit time and gastric emptying half-time in morbidly obese patients with type 2 diabetes mellitus. Surg Obes Relat Dis 6:152–157PubMedCrossRef Shah S, Shah P, Todkar J, Gagner M, Sonar S, Solav S (2010) Prospective controlled study of effect of laparoscopic sleeve gastrectomy on small bowel transit time and gastric emptying half-time in morbidly obese patients with type 2 diabetes mellitus. Surg Obes Relat Dis 6:152–157PubMedCrossRef
32.
go back to reference Meier JJ, Deacon CF, Schmidt WE, Holst JJ, Nauck MA (2007) Suppression of glucagon secretion is lower after oral glucose administration than during intravenous glucose administration in human subjects. Diabetologia 50:806–813PubMedCrossRef Meier JJ, Deacon CF, Schmidt WE, Holst JJ, Nauck MA (2007) Suppression of glucagon secretion is lower after oral glucose administration than during intravenous glucose administration in human subjects. Diabetologia 50:806–813PubMedCrossRef
33.
go back to reference Lund A, Vilsboll T, Bagger JI, Holst JJ, Knop FK (2011) The separate and combined impact of the intestinal hormones, GIP, GLP-1, and GLP-2 on glucagon secretion in type 2 diabetes. Am J Physiol Endocrinol Metab 300:E1038–E1046PubMedCrossRef Lund A, Vilsboll T, Bagger JI, Holst JJ, Knop FK (2011) The separate and combined impact of the intestinal hormones, GIP, GLP-1, and GLP-2 on glucagon secretion in type 2 diabetes. Am J Physiol Endocrinol Metab 300:E1038–E1046PubMedCrossRef
34.
go back to reference Lee WJ, Chong K, Ser KH, Lee YC, Chen SC, Chen JC, Tsai MH, Chuang LM (2011) Gastric bypass vs. sleeve gastrectomy for type 2 diabetes mellitus: a randomized controlled trial. Arch Surg 146:143–148PubMedCrossRef Lee WJ, Chong K, Ser KH, Lee YC, Chen SC, Chen JC, Tsai MH, Chuang LM (2011) Gastric bypass vs. sleeve gastrectomy for type 2 diabetes mellitus: a randomized controlled trial. Arch Surg 146:143–148PubMedCrossRef
Metadata
Title
Comparable early changes in gastrointestinal hormones after sleeve gastrectomy and Roux-En-Y gastric bypass surgery for morbidly obese type 2 diabetic subjects
Authors
Fabiola Romero
Joana Nicolau
Lílliam Flores
Roser Casamitjana
Ainitze Ibarzabal
Antonio Lacy
Josep Vidal
Publication date
01-08-2012
Publisher
Springer-Verlag
Published in
Surgical Endoscopy / Issue 8/2012
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-012-2166-y

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