Obesity Surgery

, Volume 28, Issue 1, pp 195–203 | Cite as

Predictors of Long-Term Remission and Relapse of Type 2 Diabetes Mellitus Following Gastric Bypass in Severely Obese Patients

  • Vanessa Lopes Preto de Oliveira
  • Gianluca P. Martins
  • Cláudio C. Mottin
  • Jacqueline Rizzolli
  • Rogério Friedman
Original Contributions



Diabetes remission is not observed in all obese patients with type 2 diabetes submitted to bariatric surgery. Relapses occur in patients in whom remission is achieved. We investigated the factors associated with long-term (≥3 years) remission and relapse of type 2 diabetes after Roux-en-Y gastric bypass (RYGB) in these patients.


By a retrospective review, we analyzed data from 254 patients with type 2 diabetes who had undergone RYGB from May 2000 to November 2011 and had at least 3 years of follow-up. The criteria for remission and relapse of type 2 diabetes followed the current American Diabetes Association recommendations.


Remission was achieved in almost 82% of participants (69.7% complete, and 12.2% partial remission). Of these, 12% relapsed within a mean follow-up of 5.1 ± 2.0 years after surgery. Predictors of complete remission were younger age, better preoperative glycemic control, and shorter diabetes duration. Preoperative insulin use was associated with a ninefold increase in the relapse hazard (HR = 9.1 (95% CI: 3.3–25.4)). Use of two or more oral anti-diabetic agents increased the relapse hazard sixfold (HR = 6.1 (95% CI: 1.8–20.6)). Eighteen point one percent of patients did not achieve any remission during follow-up. However, they exhibited significant improvements in glycemic control.


These data indicate that RYGB should not be delayed when remission of type 2 diabetes is a therapeutic goal, and also suggest that the best possible metabolic control should be sought in obese patients who may eventually be candidates for RYGB.


Diabetes Bypass Bariatric surgery Remission Relapse 


Compliance with Ethical Standards


This study received funding from the Brazilian National Research and Development Council (CNPq).

Conflict of Interest

Dr. Lopes Preto de Oliveira was the recipient of a grant from the Brazilian National Research and Development Council (CNPq); Gianluca Pioli Martins was the recipient of a grant from the Brazilian National Research and Development Council (CNPq); Dr. Rizzolli has nothing to disclose; Dr. Mottin has nothing to disclose; Dr. Friedman reports grants from this study. It received funding from the Brazilian National Research and Development Council (CNPq) during the conduct of the study.

Ethical Approval

All procedures were in accordance with the ethical standards of the institutional and/or national research committee and the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent

Does not apply

Supplementary material

11695_2017_2830_MOESM1_ESM.docx (24 kb)
ESM 1 (DOCX 24kb)


  1. 1.
    Aguiree F, Brown A, Cho N, et al. IDF Diabetes Atlas. 2013; doi: 10.1016/j.diabres.2009.10.007.
  2. 2.
    Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature. 2006;444:840–6. doi: 10.1038/nature05482.CrossRefPubMedGoogle Scholar
  3. 3.
    American Diabetes Association. Prevention or Delay of Type 2 Diebetes. Diabetes Care 2017;40(Suppl. 1):S44-S47. doi: 10.2337/dc17-S008.
  4. 4.
    Rubino F, Nathan DM, Eckel RH, et al. Metabolic surgery in the treatment algorithm for type 2 diabetes: a joint statement by international diabetes organizations. Diabetes Care. 2016;39:861–77. doi: 10.2337/dc16-0236.CrossRefPubMedGoogle Scholar
  5. 5.
    Mingrone G, Panunzi S, De Gaetano A, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med. 2012;366:1577–85. doi: 10.1056/NEJMoa1200111.CrossRefPubMedGoogle Scholar
  6. 6.
    Schauer PR, Mingrone G, Ikramuddin S, et al. Clinical outcomes of metabolic surgery: efficacy of glycemic control, weight loss, and remission of diabetes. Diabetes Care. 2016;39:902–11. doi: 10.2337/dc16-0382.CrossRefPubMedGoogle Scholar
  7. 7.
    Keating CL, Dixon JB, Moodie ML, et al. Cost-efficacy of surgically induced weight loss for the management of type 2. Diabetes Care. 2009;32:4580–4. doi: 10.2337/dc08-1748.Google Scholar
  8. 8.
    Hoerger TJ, Zhang P, Segel JE, et al. Cost-effectiveness of bariatric surgery for severely obese adults with diabetes. Diabetes Care. 2010;33:1933–9. doi: 10.2337/dc10-0554.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Courcoulas AP, Belle SH, Neiberg RH, et al. Three-year outcomes of bariatric surgery vs lifestyle intervention for type 2 diabetes mellitus treatment. JAMA Surg. 2015;15213:1–9. doi: 10.1001/jamasurg.2015.1534.Google Scholar
  10. 10.
    Sjöström L, Peltonen M, Jacobson P, et al. Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA. 2014;311:2297–304. doi: 10.1001/jama.2014.5988.CrossRefPubMedGoogle Scholar
  11. 11.
    Tice JA, Karliner L, Walsh J, et al. Gastric banding or bypass? A systematic review comparing the two most popular bariatric procedures. Am J Med. 2008;121:885–93. doi: 10.1016/j.amjmed.2008.05.036.CrossRefPubMedGoogle Scholar
  12. 12.
    Lee W-J, Chong K, Lin Y-H, et al. Laparoscopic sleeve gastrectomy versus single anastomosis (mini-) gastric bypass for the treatment of type 2 diabetes mellitus: 5-year results of a randomized trial and study of incretin effect. Obes Surg. 2014:1552–62. doi: 10.1007/s11695-014-1344-5.
  13. 13.
    Buse JB, Caprio S, Cefalu WT, et al. How do we define cure of diabetes? Diabetes Care. 2009;32:2133–5. doi: 10.2337/dc09-9036.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    DiGiorgi M, Rosen DJ, Choi JJ, et al. Re-emergence of diabetes after gastric bypass in patients with mid- to long-term follow-up. Surg Obes Relat Dis. 2010;6:249–53. doi: 10.1016/j.soard.2009.09.019.CrossRefPubMedGoogle Scholar
  15. 15.
    Hall TC, Pellen MGC, Sedman PC, et al. Preoperative factors predicting remission of type 2 diabetes mellitus after Roux-en-Y gastric bypass surgery for obesity. Obes Surg. 2010;20:1245–50. doi: 10.1007/s11695-010-0198-8.CrossRefPubMedGoogle Scholar
  16. 16.
    Hamza N, Abbas MH, Darwish A, et al. Predictors of remission of type 2 diabetes mellitus after laparoscopic gastric banding and bypass. Surg Obes Relat Dis. 2011;7:691–6. doi: 10.1016/j.soard.2010.03.292.CrossRefPubMedGoogle Scholar
  17. 17.
    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;252:966–71. doi: 10.1097/SLA.0b013e3181efc49a.CrossRefPubMedGoogle Scholar
  18. 18.
    Kim MK, Lee HC, Kwon H-S, et al. Visceral obesity is a negative predictor of remission of diabetes 1 year after bariatric surgery. Obesity (Silver Spring). 2011;19:1835–9. doi: 10.1038/oby.2011.205.CrossRefGoogle Scholar
  19. 19.
    Lee WJ, Chong K, Chen JC, et al. Predictors of diabetes remission after bariatric surgery in Asia. Asian J Surg. 2012;35:67–73. doi: 10.1016/j.asjsur.2012.04.010.CrossRefPubMedGoogle Scholar
  20. 20.
    Blackstone R, Bunt JC, Cortés MC, et al. Type 2 diabetes after gastric bypass: remission in five models using HbA1c, fasting blood glucose, and medication status. Surg Obes Relat Dis. 2012;8:548–55. doi: 10.1016/j.soard.2012.05.005.CrossRefPubMedGoogle Scholar
  21. 21.
    Dixon JB, Chuang L-M, Chong K, et al. Predicting the glycemic response to gastric bypass surgery in patients with type 2 diabetes. Diabetes Care. 2013;36:20–6. doi: 10.2337/dc12-0779.CrossRefPubMedGoogle Scholar
  22. 22.
    Robert M, Ferrand-Gaillard C, Disse E, et al. Predictive factors of type 2 diabetes remission 1 year after bariatric surgery: impact of surgical techniques. Obes Surg. 2013;23:770–5. doi: 10.1007/s11695-013-0868-4.CrossRefPubMedGoogle Scholar
  23. 23.
    Iacobellis G, Xu C, Campo RE, et al. Predictors of short-term diabetes remission after laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2014;25:782–7. doi: 10.1007/s11695-014-1477-6.CrossRefGoogle Scholar
  24. 24.
    Zenti MG, Rubbo I, Ceradini G, et al. Clinical factors that predict remission of diabetes after different bariatric surgical procedures: interdisciplinary group of bariatric surgery of Verona (G.I.C.O.V.). Acta Diabetol. 2015; doi: 10.1007/s00592-015-0738-8.
  25. 25.
    Kadera BE, Lum K, Grant J, et al. Remission of type 2 diabetes after Roux-en-Y gastric bypass is associated with greater weight loss. Surg Obes Relat Dis. 2009;5:305–9. doi: 10.1016/j.soard.2009.02.007.CrossRefPubMedGoogle Scholar
  26. 26.
    Chikunguwo SM, Wolfe LG, Dodson P, et al. Analysis of factors associated with durable remission of diabetes after Roux-en-Y gastric bypass. Surg Obes Relat Dis. 2010;6:254–9. doi: 10.1016/j.soard.2009.11.003.CrossRefPubMedGoogle Scholar
  27. 27.
    Jiménez A, Casamitjana R, Flores L, et al. Long-term effects of sleeve gastrectomy and Roux-en-Y gastric bypass surgery on type 2 diabetes mellitus in morbidly obese subjects. Ann Surg. 2012;256:1. doi: 10.1097/SLA.0b013e318262ee6b.CrossRefGoogle Scholar
  28. 28.
    Aarts EO, Janssen J, Janssen IMC, et al. Preoperative fasting plasma C-peptide level may help to predict diabetes outcome after gastric bypass surgery. Obes Surg. 2013;23:867–73. doi: 10.1007/s11695-013-0872-8.CrossRefPubMedGoogle Scholar
  29. 29.
    Ramos-Levi A, Sanchez-Pernaute A, Matia P, et al. Diagnosis of diabetes remission after bariatic surgery may be jeopardized by remission criteria and previous hypoglycemic treatment. Obes Surg. 2013;23:1520–6. doi: 10.1007/s11695-013-0995-y.CrossRefPubMedGoogle Scholar
  30. 30.
    Arterburn DE, Bogart A, Sherwood NE, et al. A multisite study of long-term remission and relapse of type 2 diabetes mellitus following gastric bypass. Obes Surg. 2013;23:93–102. doi: 10.1007/s11695-012-0802-1.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Brethauer SA, Aminian A, Romero-Talamás H, et al. Can diabetes be surgically cured? Long-term metabolic effects of bariatric surgery in obese patients with type 2 diabetes mellitus. Ann Surg. 2013;258:628–36–7. doi: 10.1097/SLA.0b013e3182a5034b.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Stone NJ, Robinson JG, Lichtenstein AH, et al. 2013 ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association Task Force on practice guidelines. Circulation. 2014;129:S1–45. doi: 10.1161/01.cir.0000437738.63853.7a.CrossRefPubMedGoogle Scholar
  33. 33.
    James PA, Oparil S, Carter BL, et al. Evidence-based guideline for the management of high blood pressure in adults: report from the panel members appointed to the Eighth Joint National Committee (JNC 8). JAMA. 2014;311:507–20. doi: 10.1001/jama.2013.284427.CrossRefPubMedGoogle Scholar
  34. 34.
    Inzucchi SE, Bergenstal RM, Buse JB, et al. Classification and diagnosis of diabetes. Diabetes Care. 2014;38:S8–16. doi: 10.2337/dc15-S005.Google Scholar
  35. 35.
    Dixon JB, McPhail T, O’Brien PE. Minimal reporting requirements for weight loss: current methods not ideal. Obes Surg. 2005;15:1034–9. doi: 10.1381/0960892054621053.CrossRefPubMedGoogle Scholar
  36. 36.
    Dogan K, Betzel B, Homan J, et al. Long-term effects of laparoscopic Roux-en-Y gastric bypass on diabetes mellitus, hypertension and dyslipidaemia in morbidly obese patients. Obes Surg. 2014:1835–42. doi: 10.1007/s11695-014-1310-2.
  37. 37.
    Mingrone G, Panunzi S, De Gaetano A, et al. Bariatric-metabolic surgery versus conventional medical treatment in obese patients with type 2 diabetes: 5 year follow-up of an open-label, single-centre, randomised controlled trial. Lancet. 2015;386:964–73. doi: 10.1016/S0140-6736(15)00075-6.CrossRefPubMedGoogle Scholar
  38. 38.
    Nannipieri M, Mari A, Anselmino M, et al. The role of β-cell function and insulin sensitivity in the remission of type 2 diabetes after gastric bypass surgery. J Clin Endocrinol Metab. 2011;96:E1372–9. doi: 10.1210/jc.2011-0446.CrossRefPubMedGoogle Scholar
  39. 39.
    Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg. 2003;238:467–84–5. doi: 10.1097/01.sla.0000089851.41115.1b.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Svane MS, Madsbad S. Bariatric surgery—effects on obesity and related co-morbidities. Curr Diabetes Rev. 2014;10:208–14.CrossRefPubMedGoogle Scholar
  41. 41.
    Arterburn D, Schauer DP, Wise RE, et al. Change in predicted 10-year cardiovascular risk following laparoscopic Roux-en-Y gastric bypass surgery. Obes Surg. 2009;19:184–9. doi: 10.1007/s11695-008-9534-7.CrossRefPubMedGoogle Scholar
  42. 42.
    The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993;329:977–86.CrossRefGoogle Scholar
  43. 43.
    Heller SR. A summary of the ADVANCE trial. Diabetes Care. 2009;32(Suppl 2):1–5. doi: 10.2337/dc09-S339.Google Scholar
  44. 44.
    Isbell JM, Tamboli RA, Hansen EN, et al. Early improvements in insulin sensitivity. Diabetes Care. 2010;33:1438–42. doi: 10.2337/dc09-2107.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Madsbad S, Holst JJ. GLP-1 as a mediator in the remission of type 2 diabetes after gastric bypass and sleeve gastrectomy surgery. Diabetes. 2014;63:3172–4. doi: 10.2337/db14-0935.CrossRefPubMedGoogle Scholar
  46. 46.
    Manning S, Pucci A, Batterham RL. GLP-1: a mediator of the beneficial metabolic effects of bariatric surgery? Physiology. 2015;30:50–62. doi: 10.1152/physiol.00027.2014.CrossRefPubMedGoogle Scholar
  47. 47.
    Holst JJ. Enteroendocrine secretion of gut hormones in diabetes, obesity and after bariatric surgery. Curr Opin Pharmacol. 2013;13:983–8. doi: 10.1016/j.coph.2013.09.014.CrossRefPubMedGoogle Scholar
  48. 48.
    Still CD, Wood GC, Benotti P, et al. Preoperative prediction of type 2 diabetes remission after Roux-en-y gastric bypass surgery: retrospective cohort study. Lancet Diabetes Endocrinol. 2014;2:38–45. doi: 10.1016/j.jsbmb.2011.07.002.Identification.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Post-Graduate Program in EndocrinologyUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  2. 2.Division of EndocrinologyHospital São Lucas da Pontifícia Universidade do Rio Grande do SulPorto AlegreBrazil
  3. 3.Department of Internal MedicineUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  4. 4.Obesity and Metabolic Syndrome CenterPontifícia Universidade Católica do Rio Grande do SulPorto AlegreBrazil
  5. 5.Division of EndocrinologyHospital de Clínicas de Porto AlegrePorto AlegreBrazil

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