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.



Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Gill RS, Karmali S, Sharma AM (2011) Treating type 2 diabetes mellitus with sleeve gastrectomy in obese patients. Obes Silver Spring 19:701–702
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 24:1005–1010
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 24:2513–2517
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 18:1077–1082
Buchwald H (2004) Bariatric surgery: a systematic review and meta-analysis. JAMA 292:1724–1737
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 250:234–241
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 247:401–407
Castañeda TR, Tong J, Datta R, Culler M, Tschöp MH (2010) Ghrelin in the regulation of body weight and metabolism. Front Neuroendocrinol 31:44–60
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)
Kahn SE, Hull RL, Utzschneider KM (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444:840–846
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 85:4053–4059
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 93:2479–2485
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 30:1709–1716
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 61:393–411
Holst JJ (2007) The physiology of glucagon-like peptide 1. Physiol Rev 87:1409–1439
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 34:462–471
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 2:47–55
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)
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 46:798–801
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 130:44–54
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 252:50–56
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 247:270–275
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 12:895–900
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 164:231–238
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 33:1438–1442
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 94:884–891
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 92:4678–4685
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 58:2258–2266
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 3:597–601
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 16:298–305
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 6:152–157
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 50:806–813
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–E1046
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 146:143–148
Acknowledgments
The authors were grateful to Judith Viaplana for technical support. This work was supported by Grant PI 06/0157 from the Fondo de Investigaciones Sanitarias, Insituto de Salud Carlos III, Madrid, Spain.
Disclosures
Fabiola Romero, Joana Nicolau, Lílliam Flores, Ph.D, Roser Casamitjana, Ainitze Ibarzabal, Antonio Lacy, and Josep Vidal have no conflicts of interest or financial ties to disclose.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Romero, F., Nicolau, J., Flores, L. et al. Comparable early changes in gastrointestinal hormones after sleeve gastrectomy and Roux-En-Y gastric bypass surgery for morbidly obese type 2 diabetic subjects. Surg Endosc 26, 2231–2239 (2012). https://doi.org/10.1007/s00464-012-2166-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-012-2166-y