Does Metabolic Surgery Lead to Diabetes Remission in Patients with BMI < 30 kg/m2?: a Meta-analysis

  • Matilde Rubio-AlmanzaEmail author
  • David Hervás-Marín
  • Rosa Cámara-Gómez
  • Jana Caudet-Esteban
  • Juan Francisco Merino-Torres
Original Contributions



Bariatric surgery has demonstrated to be effective in remission of type 2 diabetes in obese patients, but it is unclear in non-obese patients. The aim of this study is to investigate if metabolic surgery is effective in diabetes resolution in patients with BMI < 30 kg/m2.

Materials and Methods

A systematic review was performed and the content of the PubMed, Ovid, and the Cochrane Library databases covering the period January 2008 to April 2018 was searched. Studies with metabolic surgery performed in patients with type 2 diabetes, BMI < 30 kg/m2 and a follow-up ≥ 6 months were included. Type 2 diabetes remission rate and metabolic parameters changes were measured. A meta-analysis was conducted with the selected studies.


Twenty-six studies were included in the meta-analysis (1105 patients). The mixed-effects meta-analysis model for overall diabetes remission rate produced an estimate of 43% (95% IC 34–53%, p < 0.001). Moderator effects of the variables race, preoperative HbA1c, BMI, months of follow-up, duration of diabetes, and age on diabetes remission were also assessed, with no significant effects being found in any of them. A reduction in BMI (− 3.57 kg/m2), fasting blood glucose (− 55.93 mg/dL) and HbA1c (− 2.08%) was observed after surgery.


Metabolic surgery could be effective in remission of type 2 diabetes in BMI < 30 kg/m2 patients but randomized and long-term studies are necessary. The scientific community should agree in a single definition of type 2 diabetes remission, in order to know the real effect of metabolic surgery in this group of patients.


Metabolic surgery Type 2 diabetes BMI < 30 kg/m2 Systematic review Meta-analysis 


Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interests.

Ethical Approval Statement

For this type of study, formal consent is not required.

Informed Consent Statement

Informed consent statement does not apply.

Supplementary material

11695_2018_3654_MOESM1_ESM.docx (27 kb)
Supplementary table Newcastle-Otawa scale. Quality assessment of the included studies in the meta-analysis. S1: Representativeness of the exposed cohort; S2: Selection of the non-exposed cohort; S3: Ascertainment of exposure; S4: Demonstration that outcome of interest was not present at start of study. O1: Assessment of outcome; O2: Was follow-up long enough for outcomes to occur; O3: Adequacy of follow up of cohorts (DOCX 26 kb)


  1. 1.
    NCD Risk Factor Collaboration (NCD RisC). Worldwide trends in diabetes since 1980: a pooled analysis of 751 population-based studies with 4.4 million participants. Lancet. 2016;387:1513–30.CrossRefGoogle Scholar
  2. 2.
    Adams TD, Gress RE, Smith SC, et al. Long-term mortality after gastric bypass surgery. N Engl J Med. 2007;357:753–61.CrossRefGoogle Scholar
  3. 3.
    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.CrossRefGoogle Scholar
  4. 4.
    Cohen R, Le Roux CW, Junqueira S, et al. Roux-en-Y gastric bypass in type 2 diabetes patients with mild obesity: a systematic review and meta-analysis. Obes Surg. 2017;27:2733–9.CrossRefGoogle Scholar
  5. 5.
    Cummings DE, Cohen RV. Bariatric/metabolic surgery to treat type 2 diabetes in patients with BMI <35 kg/m2. Diabetes Care. 2016;39:924–33.CrossRefGoogle Scholar
  6. 6.
    Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 2009;6:e1000100.CrossRefGoogle Scholar
  7. 7.
    The Otawa Hospital Research Institute [Internet]. Canada, The Otawa Hospital; [Cited 2018, July 16]. Avaliable from:
  8. 8.
    DePaula AL, Stival AR, DePaula CC, et al. Impact on dyslipidemia of the laparoscopic ileal interposition associated to sleeve gastrectomy in type 2 diabetic patients. J Gastrointest Surg. 2010;14:1319–25.CrossRefGoogle Scholar
  9. 9.
    Navarrete SA, Leyba JL, Llopis SN. Laparoscopic sleeve gastrectomy with duodenojejunal bypass for the treatment of type 2 diabetes in non-obese patients. Obes Surg. 2011;21:663–7.CrossRefGoogle Scholar
  10. 10.
    Scopinaro N, Adami GF, Papadia FS, et al. The effects of biliopancreatic diversion on type 2 diabetes mellitus in patients with mild obesity (BMI 30-35 kg/m2) and simple overweight (BMI 25-30 kg/m2): a prospective controlled study. Obes Surg. 2011;21:880–8.CrossRefGoogle Scholar
  11. 11.
    Geloneze B, Geloneze SR, Chaim E, et al. Metabolic surgery for non-obese type 2 diabetes: incretins, adipocytokines, and insulin secretion/resistance changes in a 1-year interventional clinical controlled study. Ann Surg. 2012;256:72–8.CrossRefGoogle Scholar
  12. 12.
    García-Caballero M, Valle M, Martínez-Moreno JM, et al. Resolution of diabetes mellitus and metabolic syndrome in normal weight 24-29 BMI patients with one anastomosis gastric bypass. Nutr Hosp. 2012;27:623–31.Google Scholar
  13. 13.
    Heo Y, Ahn JH, Shin SH, et al. The effect of duodenojejunal bypass for type 2 diabetes mellitus patients below body mass index 25 kg/m2: one year follow-up. J Korean Surg Soc. 2013;85:109–15.CrossRefGoogle Scholar
  14. 14.
    Astiarraga B, Gastaldelli A, Muscelli E, et al. Biliopancreatic diversion in nonobese patients with type 2 diabetes: impact and mechanisms. J Clin Endocrinol Metab. 2013;98:2765–73.CrossRefGoogle Scholar
  15. 15.
    Dixon JB, Hur KY, Lee WJ, et al. Gastric bypass in type 2 diabetes with BMI < 30: weight and weight loss have a major influence on outcomes. Diabet Med. 2013;30:e127–34.CrossRefGoogle Scholar
  16. 16.
    Chen W, Yan Z, Liu S, et al. The better effect of Roux-en-Y gastrointestinal reconstruction on blood glucose of nonobese type 2 diabetes mellitus patients. Am J Surg. 2014;207:877–81.CrossRefGoogle Scholar
  17. 17.
    Kim MJ, Hur KY. Short-term outcomes of laparoscopic single anastomosis gastric bypass (LSAGB) for the treatment of type 2 diabetes in lower BMI (<30 kg/m2) patients. Obes Surg. 2014;24:1044–51.CrossRefGoogle Scholar
  18. 18.
    Malapan K, Goel R, Tai CM, et al. Laparoscopic Roux-en-Y gastric bypass for nonobese type II diabetes mellitus in Asian patients. Surg Obes Relat Dis. 2014;10:834–40.CrossRefGoogle Scholar
  19. 19.
    Ugale S, Gupta N, Modi KD, et al. Prediction of remission after metabolic surgery using a novel scoring system in type 2 diabetes - a retrospective cohort study. J Diabetes Metab Disord. 2014;13:89.CrossRefGoogle Scholar
  20. 20.
    Wentworth JM, Playfair J, Laurie C, et al. Multidisciplinary diabetes care with and without bariatric surgery in overweight people: a randomised controlled trial. Lancet Diabetes Endocrinol. 2014;2:545–52.CrossRefGoogle Scholar
  21. 21.
    Yin J, Xu L, Mao Z, et al. Laparoscopic Roux-en-Y gastric bypass for type 2 diabetes mellitus in nonobese Chinese patients. Surg Laparosc Endosc Percutan Tech. 2014;24:e200–6.Google Scholar
  22. 22.
    Cui JF, Chen T, Shi L, et al. Gastric bypass surgery in non-obese patients with type 2 diabetes mellitus: a 1-year follow-up of 58 cases in Chinese. Int J Clin Exp Med. 2015;8:4393–8.Google Scholar
  23. 23.
    Liang H, Guan W, Yang Y, et al. Roux-en-Y gastric bypass for Chinese type 2 diabetes mellitus patients with a BMI < 28 kg/m2: a multi-institutional study. J Biomed Res. 2015;29:112–7.Google Scholar
  24. 24.
    Lee WJ, Almulaifi A, Chong K, et al. The effect and predictive score of gastric bypass and sleeve gastrectomy on type 2 diabetes mellitus patients with BMI < 30 kg/m2. Obes Surg. 2015;25:1772–8.CrossRefGoogle Scholar
  25. 25.
    Kwon O, Lee YJ, Yu JH, et al. The recovery of beta-cell function is critical for antidiabetic outcomes of gastric bypass in Asian subjects with type 2 diabetes and a body mass index below 30. Obes Surg. 2017;27:541–4.CrossRefGoogle Scholar
  26. 26.
    Wang G, Zhu L, Li W, et al. Can low BMI Chinese patients with type 2 diabetes benefit from laparoscopic Roux-en-Y gastric bypass surgery? Surg Obes Relat Dis. 2016;12:1890–5.CrossRefGoogle Scholar
  27. 27.
    Celik A, Cagiltay E, Ugale S, et al. Diverted sleeve gastrectomy with ileal transposition in overweight, obese, and morbidly obese patients with type 2 diabetes: results of 1-year follow-up. Surg Obes Relat Dis. 2016;12:541–9.CrossRefGoogle Scholar
  28. 28.
    Di J, Zhang H, Yu H, et al. Effect of Roux-en-Y gastric bypass on the remission of type 2 diabetes: a 3-year study in Chinese patients with a BMI <30 kg/m2. Surg Obes Relat Dis. 2016;12:1357–63.CrossRefGoogle Scholar
  29. 29.
    Ramakrishnapillai P, Pai M, Shams F, et al. Effectiveness of minimally invasive hybrid surgery for ileal interposition (MIHSII) for the resolution of type 2 diabetes. Surg Innov. 2016;23:42–51.CrossRefGoogle Scholar
  30. 30.
    Zhang H, Han X, Yu H, et al. Effect of Roux-en-Y gastric bypass on remission of T2D: medium-term follow-up in Chinese patients with different BMI obesity class. Obes Surg. 2017;27:134–42.CrossRefGoogle Scholar
  31. 31.
    Kim DJ, Paik KY, Kim MK, et al. Three-year result of efficacy for type 2 diabetes mellitus control between laparoscopic duodenojejunal bypass compared with laparoscopic Roux-en-Y gastric bypass. Ann Surg Treat Res. 2017;93:260–5.CrossRefGoogle Scholar
  32. 32.
    Gong K, Li K, Zhang N, et al. Gastric bypass procedure for type 2 diabetes patients with BMI <28 kg/m2. Surg Endosc. 2017;31:1172–9.CrossRefGoogle Scholar
  33. 33.
    Ke Z, Li F, Chen J, et al. Effects of laparoscopic Roux-en-Y gastric bypass for type 2 diabetes mellitus: comparison of BMI > 30 and < 30 kg/m2. Obes Surg. 2017;27:3040–7.CrossRefGoogle Scholar
  34. 34.
    Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.CrossRefGoogle Scholar
  35. 35.
    American Diabetes Association. Obesity management for the treatment of type 2 diabetes: standards of medical care in diabetes-2018. Diabetes Care. 2018;41(Suppl 1):S65–72.CrossRefGoogle Scholar
  36. 36.
    Batterham RL, Cummings DE. Mechanisms of diabetes improvement following bariatric/metabolic surgery. Diabetes Care. 2016;39:893–901.CrossRefGoogle Scholar
  37. 37.
    Cummings DE, Rubino F. Metabolic surgery for treatment of type 2 diabetes in obese individuals. Diabetologia. 2018;61:257–64.CrossRefGoogle Scholar
  38. 38.
    Rao WS, Shan CX, Zhang W, et al. A meta-analysis of short-term outcomes of patients with type 2 diabetes mellitus and BMI ≤ 35 kg/m2 undergoing Roux-en-Y gastric bypass. World J Surg. 2015;39:223–30.CrossRefGoogle Scholar
  39. 39.
    Panunzi S, De Gaetano A, Carnicelli A, et al. Predictors of remission of diabetes mellitus in severely obese individuals undergoing bariatric surgery: do BMI or procedure choice matter? A meta-analysis. Ann Surg. 2015;261:459–67.CrossRefGoogle Scholar
  40. 40.
    Lakdawala M, Shaikh S, Bandukwala S, et al. Roux-en-Y gastric bypass stands the test of time: 5-year results in low body mass index (30-35 kg/m2) Indian patients with type 2 diabetes mellitus. Surg Obes Relat Dis. 2013;9:370–8.CrossRefGoogle Scholar
  41. 41.
    Hsu CC, Almulaifi A, Chen JC, et al. Effect of bariatric surgery vs medical treatment on type 2 diabetes in patients with body mass index lower than 35: five-year outcomes. JAMA Surg. 2015;150:1117–24.CrossRefGoogle Scholar
  42. 42.
    Huang ZP, Guo Y, Liu CQ, et al. The effect of metabolic surgery on nonobese patients (BMI<30 kg/m2) with type 2 diabetes: a systematic review. Surg Obes Relat Dis. 2018;14:810–20.CrossRefGoogle Scholar
  43. 43.
    Baskota A, Li S, Dhakal N, et al. Bariatric surgery for type 2 diabetes mellitus in patients with BMI <30 kg/m2: a systematic review and meta-analysis. PLoS One. 2015;10:e0132335.CrossRefGoogle Scholar
  44. 44.
    Kang JH, Le QA. Effectiveness of bariatric surgical procedures: a systematic review and network meta-analysis of randomized controlled trials. Medicine (Baltimore). 2017;96:e8632.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Endocrinology and Nutrition DepartmentHospital Universitario y Politécnico La FeValenciaSpain
  2. 2.Unidad Mixta de Investigación en Endocrinología, Nutrición y Dietética ClínicaInstituto de Investigación Sanitaria La Fe (Health Research Institute La Fe)ValenciaSpain
  3. 3.Biostatistics UnitInstituto de Investigación Sanitaria La Fe (Health Research Institute La Fe)ValenciaSpain

Personalised recommendations