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Validation of the individualized metabolic surgery score for bariatric procedure selection in the merged data of two randomized clinical trials (SLEEVEPASS and SM-BOSS)

Open AccessPublished:November 08, 2022DOI:https://doi.org/10.1016/j.soard.2022.10.036

      Highlights

      • Remission rates of type 2 diabetes (T2D) were not statistically different after sleeve gastrectomy (SG) and Roux-en-Y gastric bypass (RYGB) among all included patients.
      • Remission rates of T2D were not statistically different after SG and RYGB among patients with mild, moderate, and severe diabetes stratified by the IMS score.
      • IMS score seemed to be useful in predicting long-term T2D remission after bariatric surgery.

      Abstract

      Background

      LSG and LRYGB are globally the most common bariatric procedures. IMS score categorizes T2D severity (mild, moderate, and severe) based on 4 independent preoperative predictors of long-term remission as follows: T2D duration, number of diabetes medications, insulin use, and glycemic control. IMS score has not been validated in a randomized patient cohort.

      Objectives

      To assess the feasibility of individualized metabolic surgery (IMS) score in facilitating procedure selection between laparoscopic sleeve gastrectomy (LSG) and laparoscopic Roux-en-Y gastric bypass (LRYGB) for patients with severe obesity and type 2 diabetes (T2D).

      Setting

      Merged individual patient-level 5-year data of 2 large randomized clinical trials (SLEEVEPASS and SM-BOSS [Swiss Multicenter Bypass or Sleeve Study]).

      Methods

      IMS score was calculated for study patients and its performance was analyzed.

      Results

      One hundred thirty-nine out of 155 patients with T2D had available preoperative data to calculate IMS score as follows: mild stage (n = 41/139), moderate stage (n = 77/139), severe stage (n = 21/139). At 5 years, 135 (87.1%, 67 LSG/68 LRYGB) were available for follow-up and 121 patients had both pre- and postoperative data. Diabetes remission rates according to preoperative IMS score were as follows: mild stage 87.5% (n = 14/16) after LSG and 85.7% (n = 18/21) after LRYGB (P = .999), moderate stage 42.9% (n = 15/35) and 45.2% (n = 14/31) (P = .999), and severe stage 18.2% (n = 2/11) and 0% (n = 0/7) (P = .497), respectively. The T2D remission rate varied significantly between the stages as follows: mild versus moderate odds ratio (OR) 8.3 (95% CI, 2.8–24.0; P < .001), mild versus severe OR 52.2 (95% CI 9.0–302.3; P < .001), and moderate versus severe OR 6.3 (95% CI, 1.3–29.8; P = .020).

      Conclusions

      In our study, remission rates of T2D were not statistically different after LSG and LRYGB among all patients and among patients with mild, moderate, and severe diabetes stratified by the IMS score. However, the study may be underpowered to detect differences due to small number of patients in each subgroup. IMS score seemed to be useful in predicting long-term T2D remission after bariatric surgery.

      Keywords

      The global obesity epidemic is ever increasing, resulting in concurrent increase of obesity associated diseases with type 2 diabetes (T2D) as one of the most important comorbidities driving towards an increased rate of cardiovascular morbidity and mortality [
      • Afshin A.
      • Forouzanfar M.H.
      • et al.
      Collaborators GBDO
      Health effects of overweight and obesity in 195 Countries over 25 years.
      ,
      • Flegal K.M.
      • Kruszon-Moran D.
      • Carroll M.D.
      • Fryar C.D.
      • Ogden C.L.
      Trends in obesity among Adults in the United States, 2005 to 2014.
      ,
      • La Sala L.
      • Pontiroli A.E.
      Prevention of diabetes and cardiovascular disease in obesity.
      ]. To date, bariatric surgery is the most effective treatment of severe obesity with good and sustainable weight loss and remission or alleviation of associated diseases at long-term follow-up [
      • Courcoulas A.P.
      • Belle S.H.
      • Neiberg R.H.
      • et al.
      Three-year outcomes of bariatric surgery vs lifestyle intervention for type 2 diabetes mellitus treatment: a randomized clinical trial.
      ,
      • Ikramuddin S.
      • Korner J.
      • Lee W.J.
      • et al.
      Lifestyle intervention and medical management with vs without Roux-en-Y gastric bypass and control of hemoglobin A1c, LDL cholesterol, and systolic blood pressure at 5 years in the diabetes surgery study.
      ,
      • Rubino F.
      • Nathan D.M.
      • Eckel R.H.
      • et al.
      Metabolic surgery in the treatment Algorithm for type 2 diabetes: a joint statement by international diabetes organizations.
      ,
      • Schauer P.R.
      • Bhatt D.L.
      • Kirwan J.P.
      • et al.
      Bariatric surgery versus intensive medical therapy for diabetes - 5-year outcomes.
      ,
      • Adams T.D.
      • Davidson L.E.
      • Litwin S.E.
      • et al.
      Weight and metabolic outcomes 12 Years after gastric bypass.
      ,
      • Mingrone G.
      • Panunzi S.
      • De Gaetano A.
      • et al.
      Metabolic surgery versus conventional medical therapy in patients with type 2 diabetes: 10-year follow-up of an open-label, single-centre, randomised controlled trial.
      ]. Currently, the annual number of bariatric procedures worldwide is around 750,000 and since 2014, laparoscopic sleeve gastrectomy (LSG) has been the most frequently performed bariatric procedure, while laparoscopic Roux-en-Y gastric bypass (LRYGB) represents the second most common procedure [
      • Angrisani L.
      • Santonicola A.
      • Iovino P.
      • et al.
      IFSO worldwide survey 2016: primary, endoluminal, and revisional procedures.
      ].
      Tailoring the surgical treatment of severe obesity for all bariatric surgery patients aiming to optimize outcomes is under active research and the optimal treatment choice is naturally a multifactorial issue. The severity of T2D and its predicted remission play an important role in this decision. Recent meta-analyses have shown no difference in either weight loss or T2D remission between LSG and LRYGB [
      • Han Y.
      • Jia Y.
      • Wang H.
      • Cao L.
      • Zhao Y.
      Comparative analysis of weight loss and resolution of comorbidities between laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass: a systematic review and meta-analysis based on 18 studies.
      ,
      • Lee Y.
      • Doumouras A.G.
      • Yu J.
      • et al.
      Laparoscopic sleeve gastrectomy versus laparoscopic Roux-en-Y gastric bypass: a systematic review and meta-analysis of weight loss, comorbidities, and biochemical outcomes from randomized controlled trials.
      ], but as stated by Lee et al. [
      • Lee Y.
      • Doumouras A.G.
      • Yu J.
      • et al.
      Laparoscopic sleeve gastrectomy versus laparoscopic Roux-en-Y gastric bypass: a systematic review and meta-analysis of weight loss, comorbidities, and biochemical outcomes from randomized controlled trials.
      ], long-term data from randomized controlled trials (RCTs) are lacking and firm conclusions cannot be drawn. In addition, even the most recent meta-analysis [
      • Lee Y.
      • Doumouras A.G.
      • Yu J.
      • et al.
      Laparoscopic sleeve gastrectomy versus laparoscopic Roux-en-Y gastric bypass: a systematic review and meta-analysis of weight loss, comorbidities, and biochemical outcomes from randomized controlled trials.
      ] still includes the RCT by Ruiz-Tovar et al., which was retracted in March 2021 for scientific inconsistencies further reducing the number of available RCT patients. In a large retrospective cohort study, LRYGB was associated with greater weight loss, a slightly higher T2D remission rate, less T2D relapses, and better long-term glycemic control compared to LSG [
      • McTigue K.M.
      • Wellman R.
      • Nauman E.
      • et al.
      Comparing the 5-year diabetes outcomes of sleeve gastrectomy and gastric bypass: the national patient-centered clinical research network (PCORNet) bariatric study.
      ].
      In order to increase statistical precision, the 5-year individual patient data of 2 large RCTs (SLEEVEPASS and SM-BOSS) were merged and additional patient-level data for T2D were retrieved. In this merged data, although LRYGB induced greater weight loss and better amelioration of hypertension than LSG, there was no difference in T2D remission and there were more complications after LRYGB [
      • Wölnerhanssen B.K.
      • Peterli R.
      • Hurme S.
      • et al.
      Laparoscopic Roux-en-Y gastric bypass versus laparoscopic sleeve gastrectomy: 5-year outcomes of merged data from two randomized clinical trials (SLEEVEPASS and SM-BOSS).
      ].
      While the probability of T2D relapse increases with follow-up, it should not be considered a failure as the trajectory of the disease and the associated cardiometabolic risk factors change favorably after bariatric surgery [
      • Schauer P.R.
      • Bhatt D.L.
      • Kirwan J.P.
      • et al.
      Bariatric surgery versus intensive medical therapy for diabetes - 5-year outcomes.
      ,
      • Aminian A.
      • Vidal J.
      • Salminen P.
      • et al.
      Late relapse of diabetes after bariatric surgery: not rare, but not a failure.
      ]. Longer preoperative duration of T2D, patient age, preoperative insulin use, poor glycemic control, and the number of T2D medications at baseline are all associated with greater likelihood of T2D relapse [
      • Wölnerhanssen B.K.
      • Peterli R.
      • Hurme S.
      • et al.
      Laparoscopic Roux-en-Y gastric bypass versus laparoscopic sleeve gastrectomy: 5-year outcomes of merged data from two randomized clinical trials (SLEEVEPASS and SM-BOSS).
      ,
      • 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.
      ,
      • Brethauer S.A.
      • 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.
      ,
      • Aminian A.
      • Brethauer S.A.
      • Andalib A.
      • et al.
      Can sleeve gastrectomy "cure" diabetes? Long-term metabolic effects of sleeve gastrectomy in patients with type 2 diabetes.
      ,
      • 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.
      ].
      Several scoring systems have been assessed as tools to facilitate optimal metabolic procedure choice for patients with severe obesity and T2D, and many of these scores have been validated and compared within a variety of patient cohorts [
      • Lee W.J.
      • Hur K.Y.
      • Lakadawala M.
      • et al.
      Predicting success of metabolic surgery: age, body mass index, C-peptide, and duration score.
      ,
      • Lee W.J.
      • Almulaifi A.
      • Tsou J.J.
      • Ser K.H.
      • Lee Y.C.
      • Chen S.C.
      Laparoscopic sleeve gastrectomy for type 2 diabetes mellitus: predicting the success by ABCD score.
      ,
      • Still C.D.
      • Wood G.C.
      • Benotti P.
      • et al.
      Preoperative prediction of type 2 diabetes remission after Roux-en-Y gastric bypass surgery: a retrospective cohort study.
      ,
      • Aminian A.
      • Brethauer S.A.
      • Andalib A.
      • et al.
      Individualized metabolic surgery score: procedure selection based on diabetes severity.
      ,
      • Aron-Wisnewsky J.
      • Sokolovska N.
      • Liu Y.
      • et al.
      The advanced-DiaRem score improves prediction of diabetes remission 1 year post-Roux-en-Y gastric bypass.
      ,
      • Pucci A.
      • Tymoszuk U.
      • Cheung W.H.
      • et al.
      Type 2 diabetes remission 2 years post Roux-en-Y gastric bypass and sleeve gastrectomy: the role of the weight loss and comparison of DiaRem and DiaBetter scores.
      ,
      • Fatima F.
      • Hjelmesæth J.
      • Hertel J.K.
      • et al.
      Validation of ad-DiaRem and ABCD diabetes remission prediction scores at 1-year after Roux-en-Y gastric bypass and sleeve gastrectomy in the randomized controlled Oseberg trial.
      ,
      • Debédat J.
      • Sokolovska N.
      • Coupaye M.
      • et al.
      Long-term relapse of type 2 diabetes after Roux-en-Y gastric bypass: prediction and clinical relevance.
      ]. The individualized metabolic surgery (IMS) score [
      • Aminian A.
      • Brethauer S.A.
      • Andalib A.
      • et al.
      Individualized metabolic surgery score: procedure selection based on diabetes severity.
      ] categorizes patients into 3 stages of T2D severity (mild, moderate, and severe) based on the following 4 independent preoperative predictors of long-term remission: T2D duration, number of diabetes medications, insulin use, and glycemic control. The IMS score suggested SG as the procedure of choice for patients with severe T2D based on the better risk-benefit ratio and LRYGB for patients with moderate stage T2D [
      • Aminian A.
      • Brethauer S.A.
      • Andalib A.
      • et al.
      Individualized metabolic surgery score: procedure selection based on diabetes severity.
      ]. To our knowledge, the IMS score has only been validated in retrospective cohorts and at short- or mid-term follow-up [
      • Chen J.C.
      • Hsu N.Y.
      • Lee W.J.
      • Chen S.C.
      • Ser K.H.
      • Lee Y.C.
      Prediction of type 2 diabetes remission after metabolic surgery: a comparison of the individualized metabolic surgery score and the ABCD score.
      ,
      • Ohta M.
      • Seki Y.
      • Ohyama T.
      • et al.
      Prediction of long-term diabetes remission after metabolic surgery in obese East Asian patients: a comparison between ABCD and IMS scores.
      ].
      Using the unique merged individual patient data of the so far 2 largest RCTs (SLEEVEPASS [
      • Salminen P.
      • Helmio M.
      • Ovaska J.
      • et al.
      Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss at 5 years among patients with morbid obesity: the SLEEVEPASS randomized clinical trial.
      ] and SM-BOSS [
      • Peterli R.
      • Wolnerhanssen B.K.
      • Peters T.
      • et al.
      Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss in patients with morbid obesity: the SM-BOSS randomized clinical trial.
      ]) comparing LSG and LRYGB with 5-year follow-up data [
      • Wölnerhanssen B.K.
      • Peterli R.
      • Hurme S.
      • et al.
      Laparoscopic Roux-en-Y gastric bypass versus laparoscopic sleeve gastrectomy: 5-year outcomes of merged data from two randomized clinical trials (SLEEVEPASS and SM-BOSS).
      ], the aim of this study is to validate the IMS score in a large prospective cohort assessing the feasibility of the IMS score in both tailoring the metabolic surgery procedure choice for patients with T2D and predicting the sustainability of T2D remission.

      Methods

      The study design, rationale, and methods of both RCTs have been previously reported [
      • Salminen P.
      • Helmio M.
      • Ovaska J.
      • et al.
      Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss at 5 years among patients with morbid obesity: the SLEEVEPASS randomized clinical trial.
      ,
      • Peterli R.
      • Wolnerhanssen B.K.
      • Peters T.
      • et al.
      Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss in patients with morbid obesity: the SM-BOSS randomized clinical trial.
      ]. The study protocols were approved by the local ethics committees of each participating hospital, the trials were conducted in accordance with the principles of the Declaration of Helsinki and registered at the clinical trials registry of the National Institutes of Health (ClinicalTrials.gov NCT00356213, NCT00793143). All patients gave written informed consent.
      The methods and analyses of the merged individual patient data have been previously described in detail [
      • Wölnerhanssen B.K.
      • Peterli R.
      • Hurme S.
      • et al.
      Laparoscopic Roux-en-Y gastric bypass versus laparoscopic sleeve gastrectomy: 5-year outcomes of merged data from two randomized clinical trials (SLEEVEPASS and SM-BOSS).
      ]. Briefly, both trials were randomized, controlled, multicenter, and multisurgeon trials comparing LSG and LRYGB involving a total of 240 patients with severe obesity from Finland and 225 patients from Switzerland, and similar inclusion and exclusion criteria and similar operative techniques [
      • Salminen P.
      • Helmio M.
      • Ovaska J.
      • et al.
      Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss at 5 years among patients with morbid obesity: the SLEEVEPASS randomized clinical trial.
      ,
      • Peterli R.
      • Wolnerhanssen B.K.
      • Peters T.
      • et al.
      Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss in patients with morbid obesity: the SM-BOSS randomized clinical trial.
      ]. For LSG, a 33-Fr to 35-Fr calibration bougie was used, and the resection was initiated from 3–6 cm proximal to the pylorus. For LRYGB, in both trials the standardized surgical technique for LRYGB entailed creating a small gastric pouch and constructing an antecolic end-to-side gastrojejunostomy, as either a circular or a linear anastomosis according to the preference of the surgeon. The alimentary limb was measured to 150 cm and the biliopancreatic limb was 50–cm in the SLEEVEPASS trial and 50 cm in the SM-BOSS trial.
      Raw patient level data from the 2 original RCTs were combined, and outcomes were standardized. Additional 5-year data were retrieved on T2D (preoperative T2D duration and number of T2D medications). Out of the 398 patients (398/465, 85.6%) available for follow-up in this merged data, 155 patients had T2D at baseline and were included in this study.
      The IMS score [
      • Aminian A.
      • Brethauer S.A.
      • Andalib A.
      • et al.
      Individualized metabolic surgery score: procedure selection based on diabetes severity.
      ] was calculated based on 4 different independent preoperative variables predicting long-term remission of T2D as follows: duration of T2D in years, the number of diabetes medications, insulin use, and glycemic control (glycated hemoglobin level, A1c <7%). Based on the calculated scores, patients were categorized into the following 3 different groups according to IMS score T2D severity stage: mild (IMS score ≤25), moderate (IMS score >25 to ≤95), and severe (IMS score >95), and the T2D remission rates were assessed according to these groups. Long-term T2D remission was defined according to ADA consensus statement as A1c<6.5%, fasting blood glucose 126 mg/dl, and off T2D medications at 5 years or more after surgery [
      • Buse J.B.
      • Caprio S.
      • Cefalu W.T.
      • et al.
      How do we define cure of diabetes?.
      ]. Furthermore, the changes in BMI were calculated according to T2D severity. Weight loss was defined as percentage total weight loss (%TWL [preoperative weight – postoperative weight/preoperative weight × 100]), as it is the recommended metric of choice when reporting weight loss.

      Statistical analyses

      Continuous variables were described using as means with standard deviations (SD) or, if the data were skewed, as medians with 25th (Q1) and 75th (Q3) percentiles. Non-parametric Kruskal-Wallis test was used to test differences in continuous baseline variables between the IMS T2D severity stages. Categorical variables were characterized using frequencies and percentages and tested using Pearson’s Chi Squared test or Fisher's exact test when appropriate. In order to be able to compare the results to the original publication, Pearson’s Chi Squared test was used to compare the remission rates of T2D between the operations separately in 3 severity stages, and one-way analysis of variance (ANOVA) was used to evaluate the differences in body mass index (BMI) between the severity stages separately in 2 operations. In addition, logistic regression analysis was used to evaluate the effect of T2D severity stage, operation, and percentage total weight loss (%TWL) on T2D remission. In contrast to the original article, we used %TWL in the model to represent the weight loss instead of change in BMI used in the original article. In the severe T2D stage, there was no remission after LRYGB operation and thus, we combined the severe stage with the moderate stage and this modified variable was used in the first reported model. First model included T2D severity stage (severe and moderate stages combined), operation, %TWL, and interaction of severity stage and operation. The final model included only the main effects of T2D severity stage (original variable with 3 categories) and operation because using this simple model enabled the use of severity stage with original categories. The results of logistic regression models were quantified using odds ratios (OR) with 95% confidence intervals (95% CIs).
      Two-sided tests were used and P values <.05 were considered statistically significant. Missing observations were excluded from the analyses. Statistical analyses were performed using SAS System for Windows (Version 9.4, SAS Institute Inc., Cary, NC, USA).

      Results

      The patient flow is presented in Figure 1 and the patient baseline characteristics are displayed in Table 1. Out of the 155 patients with T2D at baseline, 139 (89.7%) had the preoperative data for IMS calculations, and 135 (87.1%) were available for follow-up at 5 years. The T2D remission rate 5 years after LSG was 49.3% (n = 33/67) and 55.8% (n = 38/68) after LRYGB (P = .418). Baseline characteristics of the patients according to T2D severity stage and operation are shown in Table 2.
      Figure thumbnail gr1
      Figure 1Flow diagram. LSG = laparoscopic sleeve gastrectomy; LRYGB = laparoscopic Roux-en-Y gastric bypass; T2D = type 2 diabetes; IMS = individualized metabolic surgery.
      Table 1Baseline patient characteristics
      SM-BOSS (N = 54)SLEEVEPASS (N = 101)LSG (N = 78)LRYGB (N = 77)
      Age (yr), mean (SD)47.9 (10.3)51.6 (8.1)50.4 (8.9)50.2 (9.2)
      Sex: female/male, frequency (%)30/24 (55.6%)62/39 (61.4%)43/35 (55.1%)49/28 (63.6%)
      Body Mass Index, BMI (kg/m2), mean (SD)44.7 (10.3)46.9 (6.2)46.1 (6.2)46.1 (6.0)
      Preoperative duration of T2D (yr), median (Q1–Q3)1.0 (0.5–7.0)5.0 (2.0–8.0)5.0 (1.1–7.5)4.0 (1.0–7.0)
      No T2D medication, frequency (%)17/44 (38.6%)0/100 (0.0%)9/75 (12.0%)8/69 (11.6%)
      1 T2D medication, frequency (%)22/44 (50.0%)51/100 (51.0%)32/75 (42.7%)41/69 (59.4%)
      2 T2D medications, frequency (%)5/44 (11.1%)40/100 (40.0%)31/75 (41.3%)14/69 (20.3%)
      3 T2D medications, frequency (%)0/44 (0.0%)8/100 (8.0%)3/75 (4.0%)5/75 (7.3%)
      4 T2D medications, frequency (%)0/44 (0.0%)1/100 (1.0%)0/75 (0.0%)1/69 (1.5%)
      Insulin use, frequency (%)10/54 (18.5%)32/101 (31.7%)24/78 (30.7%)18/77 (23.4%)
      Glycated hemoglobin, A1c (%), median (Q1–Q3)6.8 (6.1–7.9)6.6 (6.3–7.2)6.7 (6.3–7.5)6.6 (6.1–7.7)
      Glycemic control, frequency (%)
      Glycated hemoglobin level (A1c) < 7%.
      31/51 (60.8%)67/101 (66.3%)51/77 (66.2%)47/75 (62.7%)
      LSG = Laparoscopic sleeve gastrectomy; LRYGB = Laparoscopic Roux-en-Y gastric bypass; T2D = Type 2 Diabetes mellitus; A1c = Glycated hemoglobin level; SD = Standard deviation.
      Glycated hemoglobin level (A1c) < 7%.
      Table 2Baseline patient characteristics by type 2 diabetes severity according to calculated individualized metabolic surgery score
      Mild stage (N = 41)Moderate stage (N = 77)Severe stage (N = 21)
      LSG (N = 19)LRYGB (N = 22)LSG (N = 41)LRYGB (N = 36)LSG (N = 12)LRYGB (N = 9)
      Age (yr), mean (SD)46.4 (9.2)50.6 (11.0)52.2 (8.0)49.2 (8.0)51.8 (8.0)52.5 (9.7)
      Sex: female/male, frequency (%)12/7 (63.2%)15/7 (68.2%)24/17 (58.5%)22/14 (61.1%)5/7 (41.7%)7/2 (77.8%)
      Body Mass Index, BMI (kg/m2), mean (SD)47.6 (6.4)47.8 (5.7)46.1 (6.4)46.8 (6.4)42.9 (6.0)43.8 (6.2)
      Glycated hemoglobin, A1c (%), median (Q1-Q3)6.2 (5.8–6.7)6.1 (5.7–6.5)6.7 (6.4–7.0)6.8 (6.2–7.7)8.6 (7.4–9.7)8.7 (8.2–9.7)
      Preoperative duration of T2D (yr), median (Q1-Q3)1.0 (0.5–1.5)1.0 (0.5–1.0)5.0 (4.0–7.0)5.0 (4.0–7.0)11.0 (8.0–20.5)15.0 (13.0–26.0)
      No T2D medication, frequency (%)7/19 (36.8%)8/22 (36.4%)1/41 (2.4%)0/36 (0.0%)0/12 (0.0%)0/9 (0.0%)
      1 T2D medication, frequency (%)12/19 (63.2%)14/22 (63.6%)19/41 (46.3%)22/36 (61.1%)0/12 (0.0%)4/9 (44.4%)
      2 T2D medications, frequency (%)0/19 (0.0%)0/22 (0.0%)20/41 (48.8%)10/36 (27.8%)10/12 (83.3%)3/9 (33.3%)
      3 T2D medications, frequency (%)0/19 (0.0%)0/22 (0.0%)1/41 (2.4%)4/36 (11.1%)2/12 (16.67%)1/9 (11.1%)
      4 T2D medications, frequency (%)0/19 (0.0%)0/22 (0.0%)0/41 (0.0%)0/36 (0.0%)0/12 (0.0%)1/9 (11.1%)
      Insulin use, frequency (%)0/19 (0.0%)0/22 (0.0%)10/41 (24.4%)7/36 (19.4%)12/12 (100.0%)9/9 (100.0%)
      Glycemic control, frequency (%)
      Glycated hemoglobin level (A1c) < 7%.
      18/19 (94.7%)22/22 (100.0%)28/41 (68.3%)19/36 (52.8%)1/12 (8.3%)1/9 (11.1%)
      LSG, Laparoscopic sleeve gastrectomy; LRYGB, Laparoscopic Roux-en-Y gastric bypass; T2D, Type 2 Diabetes mellitus; A1c = Glycated hemoglobin level; SD = Standard deviation.
      Glycated hemoglobin level (A1c) < 7%.
      There were altogether 121 patients with available data for both IMS score calculation and T2D remission analysis at 5 years. In total, 52.6% (n = 63/121) of these patients had complete remission of T2D at 5 years. Within the severity stages, the rates in achieving long-term remission at 5-year follow-up were 86.5% (n = 32/37) in the mild stage, 43.9% (n = 29/66) in the moderate stage, and 11.1% (n = 2/18) in the severe stage (P < .001). The remission rates after LSG and LRYGB according to T2D severity are presented in Table 3. The remission rates did not differ statistically and significantly between the operations in any of the severity stages.
      Table 3T2D remission rates by severity stage and operation
      Severity stageRemission after surgeryMerged dataRemission after LRYGBP value
      Remission after LSG
      Mild [frequency (%)]32/37 (86.5%)14/16 (87.5%)18/21 (85.7%).999
      Fisher’s exact test.
      Moderate [frequency (%)]29/66 (43.9%)15/35 (42.9%)14/31 (45.2%).999
      Fisher’s exact test.
      Severe [frequency (%)]2/18 (11.1%)2/11 (18.2%)0/7 (0.0%).497
      Fisher’s exact test.
      SLEEVEPASS
      Mild [frequency (%)]15/18 (83.3%)5/7 (71.4%)10/11 (90.9%).528
      Fisher’s exact test.
      Moderate [frequency (%)]18/48 (37.5%)10/26 (38.5%)8/22 (36.4%).999
      Fisher’s exact test.
      Severe [frequency (%)]0/13 (0.0%)0/7 (0.0%)0/6 (0.0%)NA
      SM-BOSS
      Mild [frequency (%)]17/19 (89.5%)9/9 (100.0%)8/10 (80.0%).474
      Fisher’s exact test.
      Moderate [frequency (%)]11/18 (61.1%)5/9 (55.6%)6/9 (66.7%).999
      Fisher’s exact test.
      Severe [frequency (%)]2/5 (40.0%)2/4 (50.0%)0/1 (0.0%).999
      Fisher’s exact test.
      LSG = Laparoscopic sleeve gastrectomy; LRYGB = Laparoscopic Roux-en-Y gastric bypass.
      Fisher’s exact test.
      The change in BMI at 5 years after LSG or LRYGB according to T2D severity is shown in Table 4. The change in BMI differed significantly (P = .043) between the severity stages in patients who underwent LRYGB with the highest BMI loss associated with T2D mild stage. In patients who underwent LSG, there were no significant differences (P = .454) in BMI change between the T2D severity stages.
      Table 4Change of body mass index by severity stage and operation
      Body Mass Index, BMI (kg/m2), mean (SD)LRYGBLSG
      MildModerateSevereP value
      One-way analysis of variance.
      MildModerateSevereP value
      One-way analysis of variance.
      Baseline47.8 (5.7)46.8 (6.4)43.8 (6.2).27547.6 (6.4)46.1 (6.4)42.9 (6.0).137
      5 yr33.25 (5.5)34.8 (6.1)35.1 (5.0).58636.6 (6.4)37.6 (5.9)33.3 (6.7).172
      Change from baseline−14.6 (6.1)−11.6 (4.2)−10.0 (3.5).043−11.0 (5.6)−9.3 (4.1)−10.4 (4.5).454
      LSG = Laparoscopic sleeve gastrectomy; LRYGB = Laparoscopic Roux-en-Y gastric bypass.
      One-way analysis of variance.
      In the logistic regression analyses for T2D remission, interaction of IMS severity (severe and moderate stages combined) and operation was not statistically significant (P = .524) and thus no further analyses were needed to test the difference between the operations separately in IMS severity stages. The effect of %TWL on T2D remission was statistically significant (P = .001) and the odds for remission increased with greater %TWL (OR, 1.1; 95% CI, 1.0–1.2). In the final model there was no statistically significant difference in T2D remission between LSG and LRYGB (OR, 1.1; 95% CI, 0.5–2.6; P = .812). Difference in T2D remission between the IMS score T2D severity stages was statistically significant (P < .001). The odds for T2D remission were the highest in the mild stage (mild versus moderate OR, 8.3; 95% CI, 2.8–24.0; P < .001 and mild versus severe OR, 52.2; 95% CI, 9.0–302.3; P < .001). There was also a statistically significant difference between the moderate and the severe stages in the odds for T2D remission (OR, 6.3, 95% CI, 1.3–29.8; P = .020).

      Discussion

      In this large merged randomized patient cohort, T2D remission rates between LSG and LRYGB were similar in all 3 IMS score T2D severity groups. However, the T2D severity stage was strongly associated with T2D remission with patients in the mild stage group being more likely to achieve remission compared to patients in the moderate or severe stage groups. Our results, therefore, suggest that IMS score does not facilitate the procedure selection between LSG and LRYGB, but IMS could be used as a general predictive model for T2D remission in patients with severe obesity.
      Our findings are in contrast to the original IMS score article [
      • Aminian A.
      • Brethauer S.A.
      • Andalib A.
      • et al.
      Individualized metabolic surgery score: procedure selection based on diabetes severity.
      ] by Aminian et al., who suggested LRYGB for patients with moderate stage T2D due to their retrospective results of LRYGB resulting in superior T2D remission rates in this group, but are in line with Chen et al., [
      • Chen J.C.
      • Hsu N.Y.
      • Lee W.J.
      • Chen S.C.
      • Ser K.H.
      • Lee Y.C.
      Prediction of type 2 diabetes remission after metabolic surgery: a comparison of the individualized metabolic surgery score and the ABCD score.
      ] who also found no difference in 5-year remission rates between LSG and LRYGB in the moderate stage. However, the latter study may have been influenced by the Asian ethnicity and lower preoperative BMI of the study population, while in our merged data set, both these factors are likely more similar to the dataset of the original IMS score article.
      A recent study by Ohta et al. [
      • Ohta M.
      • Seki Y.
      • Ohyama T.
      • et al.
      Prediction of long-term diabetes remission after metabolic surgery in obese East Asian patients: a comparison between ABCD and IMS scores.
      ] found LSG superior to LRYGB regarding T2D remission in patients with moderate T2D, although patients undergoing LSG had higher BMI compared to LRYGB in their study population. Their results showed sleeve gastrectomy with duodenojejunal bypass to be the most effective procedure in treatment of T2D in the moderate stage [
      • Ohta M.
      • Seki Y.
      • Ohyama T.
      • et al.
      Prediction of long-term diabetes remission after metabolic surgery in obese East Asian patients: a comparison between ABCD and IMS scores.
      ] in line with results showing that biliopancreatic diversion with duodenal switch is superior for T2D remission [
      • Mingrone G.
      • Panunzi S.
      • De Gaetano A.
      • et al.
      Metabolic surgery versus conventional medical therapy in patients with type 2 diabetes: 10-year follow-up of an open-label, single-centre, randomised controlled trial.
      ].
      To our knowledge, this is the first validation of the IMS score using randomized data comparing LSG and LRYGB with the randomization mitigating the selection bias. The IMS score is based on a large retrospective patient cohort (n = 900) with severe obesity and T2D with long-term glycemic follow-up after metabolic surgery (LSG or LRYGB). In the original IMS score training cohort only a quarter of the patients underwent LSG, which could potentially have led to a false-positive effect of LSG in the severe stage group [
      • Aminian A.
      • Brethauer S.A.
      • Andalib A.
      • et al.
      Individualized metabolic surgery score: procedure selection based on diabetes severity.
      ].
      The present study showed no significant difference in T2D remission rates between LSG and LRYGB. This result is in line with a recent meta-analysis by Lee et al. [
      • Lee Y.
      • Doumouras A.G.
      • Yu J.
      • et al.
      Laparoscopic sleeve gastrectomy versus laparoscopic Roux-en-Y gastric bypass: a systematic review and meta-analysis of weight loss, comorbidities, and biochemical outcomes from randomized controlled trials.
      ], which included 33 RCTs and 2475 patients comparing these 2 procedures. The Oseberg trial [
      • Hofsø D.
      • Fatima F.
      • Borgeraas H.
      • et al.
      Gastric bypass versus sleeve gastrectomy in patients with type 2 diabetes (Oseberg): a single-centre, triple-blind, randomised controlled trial.
      ] comparing LRYGB and LSG in the treatment of patients with T2D, and severe obesity with 2 endpoints of 1-year T2D remission and β-cell function was not included to this meta-analysis showing superior T2D remission after LRYGB with no difference in β-cell function. However, to detect a 10-percentage point difference in T2D remission rate between the operations, about 700 patients with T2D would need to be enrolled underlining the need for international scientific collaboration for an individual patient data meta-analysis.
      Previous studies have reported the ability of the IMS score in predicting overall T2D remission [
      • Plaeke P.
      • Beunis A.
      • Ruppert M.
      • De Man J.G.
      • De Winter B.Y.
      • Hubens G.
      Review, performance comparison, and validation of models predicting type 2 diabetes remission after bariatric surgery in a Western European population.
      ,
      • Shen S.C.
      • Wang W.
      • Tam K.W.
      • et al.
      Validating risk prediction models of diabetes remission after sleeve gastrectomy.
      ]. Plaeke et al. [
      • Plaeke P.
      • Beunis A.
      • Ruppert M.
      • De Man J.G.
      • De Winter B.Y.
      • Hubens G.
      Review, performance comparison, and validation of models predicting type 2 diabetes remission after bariatric surgery in a Western European population.
      ] compared the performance of 11 different predictive scores and found the IMS score to be the most accurate. In patients undergoing LSG, IMS score was able to discriminate T2D remissions [
      • Shen S.C.
      • Wang W.
      • Tam K.W.
      • et al.
      Validating risk prediction models of diabetes remission after sleeve gastrectomy.
      ]. Many scoring systems have been developed to predict T2D remission after bariatric surgery such as DiaRem [
      • Still C.D.
      • Wood G.C.
      • Benotti P.
      • et al.
      Preoperative prediction of type 2 diabetes remission after Roux-en-Y gastric bypass surgery: a retrospective cohort study.
      ], advanced-DiaRem (ad-DiaRem) [
      • Aron-Wisnewsky J.
      • Sokolovska N.
      • Liu Y.
      • et al.
      The advanced-DiaRem score improves prediction of diabetes remission 1 year post-Roux-en-Y gastric bypass.
      ], DiaBetter [
      • Pucci A.
      • Tymoszuk U.
      • Cheung W.H.
      • et al.
      Type 2 diabetes remission 2 years post Roux-en-Y gastric bypass and sleeve gastrectomy: the role of the weight loss and comparison of DiaRem and DiaBetter scores.
      ] and ABCD scores [
      • Lee W.J.
      • Hur K.Y.
      • Lakadawala M.
      • et al.
      Predicting success of metabolic surgery: age, body mass index, C-peptide, and duration score.
      ]. Chen et al. [
      • Chen J.C.
      • Hsu N.Y.
      • Lee W.J.
      • Chen S.C.
      • Ser K.H.
      • Lee Y.C.
      Prediction of type 2 diabetes remission after metabolic surgery: a comparison of the individualized metabolic surgery score and the ABCD score.
      ] reported that the ABCD scores have better discriminative ability between the procedures compared with the IMS score. This was suggested to derive from the lack of C-peptide value in the IMS score as it has been shown to predict T2D remissions [
      • Dixon J.B.
      • Chuang L.M.
      • Chong K.
      • et al.
      Predicting the glycemic response to gastric bypass surgery in patients with type 2 diabetes.
      ,
      • Lee W.J.
      • Chong K.
      • Ser K.H.
      • et al.
      C-peptide predicts the remission of type 2 diabetes after bariatric surgery.
      ,
      • Park J.Y.
      • Kim Y.J.
      Prediction of diabetes remission in morbidly obese patients after Roux-en-Y gastric bypass.
      ]. However, there are contradicting results of the role of C-peptide in predicting T2D remissions showing comparable prediction results of the IMS score to the ABCD score in an Asian population [
      • Ohta M.
      • Seki Y.
      • Ohyama T.
      • et al.
      Prediction of long-term diabetes remission after metabolic surgery in obese East Asian patients: a comparison between ABCD and IMS scores.
      ].
      DiaRem, ad-DiaRem, DiaBetter, and IMS score all include similar parameters; preoperative A1c along with the use of diabetes medications and insulin use all associated with T2D remission prediction [
      • Still C.D.
      • Wood G.C.
      • Benotti P.
      • et al.
      Preoperative prediction of type 2 diabetes remission after Roux-en-Y gastric bypass surgery: a retrospective cohort study.
      ,
      • Aron-Wisnewsky J.
      • Sokolovska N.
      • Liu Y.
      • et al.
      The advanced-DiaRem score improves prediction of diabetes remission 1 year post-Roux-en-Y gastric bypass.
      ,
      • Pucci A.
      • Tymoszuk U.
      • Cheung W.H.
      • et al.
      Type 2 diabetes remission 2 years post Roux-en-Y gastric bypass and sleeve gastrectomy: the role of the weight loss and comparison of DiaRem and DiaBetter scores.
      ,
      • Park J.Y.
      • Kim Y.J.
      Prediction of diabetes remission in morbidly obese patients after Roux-en-Y gastric bypass.
      ,
      • Schauer P.R.
      • Burguera B.
      • Ikramuddin S.
      • et al.
      Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus.
      ,
      • Panunzi S.
      • Carlsson L.
      • De Gaetano A.
      • et al.
      Determinants of diabetes remission and glycemic control after bariatric surgery.
      ]. Ad-Diarem, DiaBetter, and IMS score all include preoperative duration of T2D, which is strongly associated with remission rate [
      • Schauer P.R.
      • Bhatt D.L.
      • Kirwan J.P.
      • et al.
      Bariatric surgery versus intensive medical therapy for diabetes - 5-year outcomes.
      ,
      • Aron-Wisnewsky J.
      • Sokolovska N.
      • Liu Y.
      • et al.
      The advanced-DiaRem score improves prediction of diabetes remission 1 year post-Roux-en-Y gastric bypass.
      ,
      • Dixon J.B.
      • Chuang L.M.
      • Chong K.
      • et al.
      Predicting the glycemic response to gastric bypass surgery in patients with type 2 diabetes.
      ,
      • Schauer P.R.
      • Burguera B.
      • Ikramuddin S.
      • et al.
      Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus.
      ], and these 3 scores performed best in the comparison of the 11 predictive scores by Plaeke et al. [
      • Plaeke P.
      • Beunis A.
      • Ruppert M.
      • De Man J.G.
      • De Winter B.Y.
      • Hubens G.
      Review, performance comparison, and validation of models predicting type 2 diabetes remission after bariatric surgery in a Western European population.
      ]. With the progressing nature of T2D pathophysiology, worse A1c, number of diabetes medications, and insulin use are basically by-products of T2D duration and signs of progression of disease severity [
      • Turner R.
      • Cull C.
      • Holman R.
      United Kingdom Prospective Diabetes Study 17: a 9-year update of a randomized, controlled trial on the effect of improved metabolic control on complications in non-insulin-dependent diabetes mellitus.
      ,
      • Turner R.C.
      • Cull C.A.
      • Frighi V.
      • Holman R.R.
      Glycemic control with diet, sulfonylurea, metformin, or insulin in patients with type 2 diabetes mellitus: progressive requirement for multiple therapies (UKPDS 49). UK Prospective Diabetes Study (UKPDS) Group.
      ].
      In our study, we used both change in BMI and %TWL as weight loss variables, and change in BMI was used to facilitate the comparison with the original IMS score [
      • Aminian A.
      • Brethauer S.A.
      • Andalib A.
      • et al.
      Individualized metabolic surgery score: procedure selection based on diabetes severity.
      ]. Currently %TWL is considered to be the variable of choice in reporting weight loss outcomes after bariatric surgery [
      • Corcelles R.
      • Boules M.
      • Froylich D.
      • et al.
      Total weight loss as the outcome measure of choice after Roux-en-Y gastric bypass.
      ], and therefore, we used %TWL in our advanced model. The effect of preoperative BMI on T2D remission remains somewhat controversial [
      • Aron-Wisnewsky J.
      • Sokolovska N.
      • Liu Y.
      • et al.
      The advanced-DiaRem score improves prediction of diabetes remission 1 year post-Roux-en-Y gastric bypass.
      ,
      • Dixon J.B.
      • Chuang L.M.
      • Chong K.
      • et al.
      Predicting the glycemic response to gastric bypass surgery in patients with type 2 diabetes.
      ,
      • Schauer P.R.
      • Burguera B.
      • Ikramuddin S.
      • et al.
      Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus.
      ]. A meta-analysis of 4944 patients showed preoperative BMI not to be a significant predictor of T2D remission [
      • Panunzi S.
      • De Gaetano A.
      • Carnicelli A.
      • Mingrone G.
      Predictors of remission of diabetes mellitus in severely obese individuals undergoing bariatric surgery: do BMI or procedure choice matter? A meta-analysis.
      ].
      This study has limitations. First, the present study is limited by the number of patients and underpowered to detect differences in T2D remission between LSG and LRYGB. However, to our knowledge, this is so far the largest randomized cohort with the longest follow-up and high follow-up rate comparing LSG and LRYGB of patients with severe obesity and T2D. Second, the patients in our study population had somewhat better glycemic control (hemoglobin [Hb] A1C<7%) and shorter T2D duration (5 years in SLEEVEPASS but 1 year in SM-BOSS) at baseline compared to the training and validating cohort of the original IMS score study (HbA1C, 7.3%–7.4% and T2D duration, 5–6 years), which may partly contribute to the differences in our results. Third, the LRYGB surgical technique used in the original IMS training and validating cohorts was not reported limiting the assessment on the potential differences of the procedure details (e.g., limb lengths). Fourth, the study population consisted mostly of patients with Caucasian ethnic background limiting the generalizability of the results in patients of other ethnicities.

      Conclusions

      In our study, remission rates of T2D were not statistically different after LSG, and LRYGB among all patients and among patients with mild, moderate, and severe diabetes were stratified by the IMS score. However, the study may be underpowered to detect differences due to small number of patients in each subgroup. IMS score seemed to be useful in predicting long-term T2D remission after bariatric surgery.

      Acknowledgments

      The authors give their thanks to all trial patients. We thank all the collaborators in original trials: A. Juuti, A.C. Meyer-Gerspach, M. Slawik, P. Peromaa-Haavisto, T. Peters, D. Vetter, D. Kröll, Y. Borbely, B. Schultes, C. Beglinger, J. Drewe, M. Schiesser, P. Nett, J. Ovaska, M. Leivonen and M. Soinio. They also express thanks to M. Victorzon (Department of Surgery, University of Turku, and Vaasa Central Hospital, Vaasa, Finland) who was involved in this trial, but passed away before this work was submitted.

      Disclosures

      All authors have completed and submitted the ICMJE (International Committee of Medical Journal Editors) form for disclosure of potential conflicts of interest. No other authors reported disclosures.

      Author Contributions

      Drs Saarinen, Grönroos and Salminen had full access to all the data in the study and take full responsibility for the integrity of the data and the accuracy of the data analyses. Dr. Salminen had the final responsibility for the decision to submit the manuscript for publication. Concept and design: Saarinen, Grönroos, Hurme, Strandberg, Peterli, Bueter, Wölnerhanssen, and Salminen. Acquisition, analysis, or interpretation of data: Saarinen, Grönroos, Hurme, Helmiö, Peterli, Bueter, Strandberg, Wölnerhanssen, and Salminen. Drafting of the manuscript: Saarinen, Grönroos, Hurme, Strandberg, and Salminen. Critical revision of the manuscript: Helmiö, Peterli, Wölnerhanssen, Bueter, Saarinen, Grönroos, Hurme, Strandberg, and Salminen. Statistical analyses: Saarinen, Grönroos, Hurme, and Salminen. Administrative, technical, or material support: Saarinen, Grönroos, Hurme, Helmiö, Peterli, Bueter, Strandberg, Wölnerhanssen and Salminen. Supervision: Salminen.

      References

        • Afshin A.
        • Forouzanfar M.H.
        • et al.
        • Collaborators GBDO
        Health effects of overweight and obesity in 195 Countries over 25 years.
        N Engl J Med. 2017; 377: 13-27
        • Flegal K.M.
        • Kruszon-Moran D.
        • Carroll M.D.
        • Fryar C.D.
        • Ogden C.L.
        Trends in obesity among Adults in the United States, 2005 to 2014.
        JAMA. 2016; 315: 2284-2291
        • La Sala L.
        • Pontiroli A.E.
        Prevention of diabetes and cardiovascular disease in obesity.
        Int J Mol Sci. 2020; 21: 8178
        • Courcoulas A.P.
        • Belle S.H.
        • Neiberg R.H.
        • et al.
        Three-year outcomes of bariatric surgery vs lifestyle intervention for type 2 diabetes mellitus treatment: a randomized clinical trial.
        JAMA Surg. 2015; 150: 931-940
        • Ikramuddin S.
        • Korner J.
        • Lee W.J.
        • et al.
        Lifestyle intervention and medical management with vs without Roux-en-Y gastric bypass and control of hemoglobin A1c, LDL cholesterol, and systolic blood pressure at 5 years in the diabetes surgery study.
        JAMA. 2018; 319: 266-278
        • Rubino F.
        • Nathan D.M.
        • Eckel R.H.
        • et al.
        Metabolic surgery in the treatment Algorithm for type 2 diabetes: a joint statement by international diabetes organizations.
        Diabetes Care. 2016; 39: 861-877
        • Schauer P.R.
        • Bhatt D.L.
        • Kirwan J.P.
        • et al.
        Bariatric surgery versus intensive medical therapy for diabetes - 5-year outcomes.
        N Engl J Med. 2017; 376: 641-651
        • Adams T.D.
        • Davidson L.E.
        • Litwin S.E.
        • et al.
        Weight and metabolic outcomes 12 Years after gastric bypass.
        N Engl J Med. 2017; 377: 1143-1155
        • Mingrone G.
        • Panunzi S.
        • De Gaetano A.
        • et al.
        Metabolic surgery versus conventional medical therapy in patients with type 2 diabetes: 10-year follow-up of an open-label, single-centre, randomised controlled trial.
        Lancet. 2021; 397: 293-304
        • Angrisani L.
        • Santonicola A.
        • Iovino P.
        • et al.
        IFSO worldwide survey 2016: primary, endoluminal, and revisional procedures.
        Obes Surg. 2018; 28: 3783-3794
        • Han Y.
        • Jia Y.
        • Wang H.
        • Cao L.
        • Zhao Y.
        Comparative analysis of weight loss and resolution of comorbidities between laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass: a systematic review and meta-analysis based on 18 studies.
        Int J Surg. 2020; 76: 101-110
        • Lee Y.
        • Doumouras A.G.
        • Yu J.
        • et al.
        Laparoscopic sleeve gastrectomy versus laparoscopic Roux-en-Y gastric bypass: a systematic review and meta-analysis of weight loss, comorbidities, and biochemical outcomes from randomized controlled trials.
        Ann Surg. 2021; 273: 66-74
        • McTigue K.M.
        • Wellman R.
        • Nauman E.
        • et al.
        Comparing the 5-year diabetes outcomes of sleeve gastrectomy and gastric bypass: the national patient-centered clinical research network (PCORNet) bariatric study.
        JAMA Surg. 2020; 155: e200087
        • Wölnerhanssen B.K.
        • Peterli R.
        • Hurme S.
        • et al.
        Laparoscopic Roux-en-Y gastric bypass versus laparoscopic sleeve gastrectomy: 5-year outcomes of merged data from two randomized clinical trials (SLEEVEPASS and SM-BOSS).
        Br J Surg. 2021; 108: 49-57
        • Aminian A.
        • Vidal J.
        • Salminen P.
        • et al.
        Late relapse of diabetes after bariatric surgery: not rare, but not a failure.
        Diabetes Care. 2020; 43: 534-540
        • 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: 1023-1029
        • Brethauer S.A.
        • 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 (discussion 636-7): 628-636
        • Aminian A.
        • Brethauer S.A.
        • Andalib A.
        • et al.
        Can sleeve gastrectomy "cure" diabetes? Long-term metabolic effects of sleeve gastrectomy in patients with type 2 diabetes.
        Ann Surg. 2016; 264: 674-681
        • 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: 2297-2304
        • Lee W.J.
        • Hur K.Y.
        • Lakadawala M.
        • et al.
        Predicting success of metabolic surgery: age, body mass index, C-peptide, and duration score.
        Surg Obes Relat Dis. 2013; 9: 379-384
        • Lee W.J.
        • Almulaifi A.
        • Tsou J.J.
        • Ser K.H.
        • Lee Y.C.
        • Chen S.C.
        Laparoscopic sleeve gastrectomy for type 2 diabetes mellitus: predicting the success by ABCD score.
        Surg Obes Relat Dis. 2015; 11: 991-996
        • Still C.D.
        • Wood G.C.
        • Benotti P.
        • et al.
        Preoperative prediction of type 2 diabetes remission after Roux-en-Y gastric bypass surgery: a retrospective cohort study.
        Lancet Diabetes Endocrinol. 2014; 2: 38-45
        • Aminian A.
        • Brethauer S.A.
        • Andalib A.
        • et al.
        Individualized metabolic surgery score: procedure selection based on diabetes severity.
        Ann Surg. 2017; 266: 650-657
        • Aron-Wisnewsky J.
        • Sokolovska N.
        • Liu Y.
        • et al.
        The advanced-DiaRem score improves prediction of diabetes remission 1 year post-Roux-en-Y gastric bypass.
        Diabetologia. 2017; 60: 1892-1902
        • Pucci A.
        • Tymoszuk U.
        • Cheung W.H.
        • et al.
        Type 2 diabetes remission 2 years post Roux-en-Y gastric bypass and sleeve gastrectomy: the role of the weight loss and comparison of DiaRem and DiaBetter scores.
        Diabet Med. 2018; 35: 360-367
        • Fatima F.
        • Hjelmesæth J.
        • Hertel J.K.
        • et al.
        Validation of ad-DiaRem and ABCD diabetes remission prediction scores at 1-year after Roux-en-Y gastric bypass and sleeve gastrectomy in the randomized controlled Oseberg trial.
        Obes Surg. 2022; 32: 801-809
        • Debédat J.
        • Sokolovska N.
        • Coupaye M.
        • et al.
        Long-term relapse of type 2 diabetes after Roux-en-Y gastric bypass: prediction and clinical relevance.
        Diabetes Care. 2018; 41: 2086-2095
        • Chen J.C.
        • Hsu N.Y.
        • Lee W.J.
        • Chen S.C.
        • Ser K.H.
        • Lee Y.C.
        Prediction of type 2 diabetes remission after metabolic surgery: a comparison of the individualized metabolic surgery score and the ABCD score.
        Surg Obes Relat Dis. 2018; 14: 640-645
        • Ohta M.
        • Seki Y.
        • Ohyama T.
        • et al.
        Prediction of long-term diabetes remission after metabolic surgery in obese East Asian patients: a comparison between ABCD and IMS scores.
        Obes Surg. 2021; 31: 1485-1495
        • Salminen P.
        • Helmio M.
        • Ovaska J.
        • et al.
        Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss at 5 years among patients with morbid obesity: the SLEEVEPASS randomized clinical trial.
        JAMA. 2018; 319: 241-254
        • Peterli R.
        • Wolnerhanssen B.K.
        • Peters T.
        • et al.
        Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss in patients with morbid obesity: the SM-BOSS randomized clinical trial.
        JAMA. 2018; 319: 255-265
        • Buse J.B.
        • Caprio S.
        • Cefalu W.T.
        • et al.
        How do we define cure of diabetes?.
        Diabetes Care. 2009; 32: 2133-2135
        • Hofsø D.
        • Fatima F.
        • Borgeraas H.
        • et al.
        Gastric bypass versus sleeve gastrectomy in patients with type 2 diabetes (Oseberg): a single-centre, triple-blind, randomised controlled trial.
        Lancet Diabetes Endocrinol. 2019; 7: 912-924
        • Plaeke P.
        • Beunis A.
        • Ruppert M.
        • De Man J.G.
        • De Winter B.Y.
        • Hubens G.
        Review, performance comparison, and validation of models predicting type 2 diabetes remission after bariatric surgery in a Western European population.
        Obes Surg. 2021; 31: 1549-1560
        • Shen S.C.
        • Wang W.
        • Tam K.W.
        • et al.
        Validating risk prediction models of diabetes remission after sleeve gastrectomy.
        Obes Surg. Jan 2019; 29: 221-229
        • Dixon J.B.
        • 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: 20-26
        • Lee W.J.
        • Chong K.
        • Ser K.H.
        • et al.
        C-peptide predicts the remission of type 2 diabetes after bariatric surgery.
        Obes Surg. 2012; 22: 293-298
        • Park J.Y.
        • Kim Y.J.
        Prediction of diabetes remission in morbidly obese patients after Roux-en-Y gastric bypass.
        Obes Surg. 2016; 26: 749-756
        • Schauer P.R.
        • Burguera B.
        • Ikramuddin S.
        • et al.
        Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus.
        Ann Surg. 2003; 238 (discussion 84-5): 467-484
        • Panunzi S.
        • Carlsson L.
        • De Gaetano A.
        • et al.
        Determinants of diabetes remission and glycemic control after bariatric surgery.
        Diabetes Care. Jan 2016; 39: 166-174
        • Turner R.
        • Cull C.
        • Holman R.
        United Kingdom Prospective Diabetes Study 17: a 9-year update of a randomized, controlled trial on the effect of improved metabolic control on complications in non-insulin-dependent diabetes mellitus.
        Ann Intern Med. 1996; 124: 136-145
        • Turner R.C.
        • Cull C.A.
        • Frighi V.
        • Holman R.R.
        Glycemic control with diet, sulfonylurea, metformin, or insulin in patients with type 2 diabetes mellitus: progressive requirement for multiple therapies (UKPDS 49). UK Prospective Diabetes Study (UKPDS) Group.
        JAMA. 1999; 281: 2005-2012
        • Corcelles R.
        • Boules M.
        • Froylich D.
        • et al.
        Total weight loss as the outcome measure of choice after Roux-en-Y gastric bypass.
        Obes Surg. 2016; 26: 1794-1798
        • Panunzi S.
        • De Gaetano A.
        • Carnicelli A.
        • Mingrone G.
        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: 459-467