Abstract
Metabolic surgery (MS) is a surgery that focuses on improving obesity-related comorbidities. It is often referred to as “diabetic surgery” because of its focus on treating type 2 diabetes. MS is distinguished from bariatric surgery (BS), in which weight loss is the primary goal. However, from a broader perspective, all surgeries for obese patients with diabetes can be considered MS. In Korea, metabolic and bariatric surgery (MBS) has been covered by the national health insurance since 2019. Patients with a body mass index (BMI) ≥35 or those with a BMI ≥30 and obesity-related comorbidities were eligible for MBS. Simultaneously, MS for patients with BMI values between 27.5 and 30 was partly reimbursed. The two major metabolic surgeries are Roux-en-Y gastric bypass (RYGB) and sleeve gastrectomy (SG). According to the registry of the Korean Society of Metabolic and Bariatric Surgery, 1,560 metabolic surgeries for obese patients with diabetes were performed between 2019 and 2021 in Korea, which was approximately 35.6% of all bariatric surgeries. SG was the most common, followed by RYGB and duodenal switch surgery. When dividing the patients with diabetes who underwent MBS into two groups, specifically those with BMI <35 and ≥35, we found that SG was performed most common procedure in both groups. However, there was a higher proportion of RYGB and duodenal switch operation in the former, indicating a difference in surgical methods between the two groups. MS is a promising tool for the management of poorly controlled diabetes. More data are needed to establish proper patient selection and choice of surgical type.
Keywords: Metabolic surgery; Diabetes mellitus; Gastrectomy; Gastric bypass; Obesity, morbid
INTRODUCTION
Bariatric surgery (BS) is considered the gold standard of treatment for morbid obesity [1,2]. In Korea, BS has been covered by national health insurance since 2019. The indication is a body mass index (BMI) same or higher than 35 kg/m2 or a BMI same or higher than 30 kg/m2 with obesity-related comorbidities, such as type 2 diabetes mellitus (T2DM), hypertension, or fatty liver disease.
Metabolic surgery (MS) is a surgery that focuses on improving obesity-related comorbidities, of which T2DM is the most common and important [3]. The type of MS does not differ from that of BS. In Korea and many other countries, the most common procedures nowadays are sleeve gastrectomy (SG) and Roux-en-Y gastric bypass (RYGB) [4,5]. The mechanisms by which diabetes improves after MS can be divided into 2 main categories: 1) weight loss effects and 2) non-weight loss effects. Recently, there has been growing interest in the latter category, primarily driven by the question of the source of significant diabetes improvement that occurs immediately after MS, specifically the improvement that starts before any weight loss. This question is currently the subject of active research, and some of the proposed mechanisms of action include changes in the gut hormones such as glucagon-like peptide-1, changes in bile secretion and absorption, changes in the gut microbiome, and decreased toxicity of fat cells [6,7].
Pure MS refers to MS performed in non-obese patients with diabetes. Although not yet clearly defined, it can be referred to as surgery for patients with a BMI less than 30 kg/m2 in East Asian countries, including Korea. Because the effect of MS is mainly related to body weight reduction after surgery, pure MS is generally considered less effective than MS in morbidly obese patients [8]. Therefore, several surgeons hesitate to perform pure MS, and data on pure MS remain very limited.
However, in Korea, pure MS can be performed as it is partly covered by the national health insurance. In 2018, one year before starting national insurance coverage for BS, patients with a BMI between 27.5 kg/m2 and 30 kg/m2 are indicated for MS. Herein, we aim to define MS and discuss the current status of MS in Korea, as well as the expected benefits for patients with T2DM.
DEFINITION OF MS: FOCUSING ON DIFFERENCES FROM BS
BS is progressively emerging as the standard treatment for morbid obesity unresponsive to medical treatment. However, following BS, not only does significant weight loss occurs, but several comorbidities related to obesity, such as T2DM, often show concurrent improvement. Recently, there has been an increasing number of cases in which the primary goal is to control T2DM through surgery, rather than focusing on weight loss. This is referred to as “metabolic surgery,” which is distinguished from BS. It is sometimes referred to as “diabetic surgery” because of its focus on the treatment of diabetes.
Calculating the proportion of MS among all BS is not straightforward, because a considerable number of morbidly obese patients also have diabetes, and determining whether the purpose of surgery in these patients is weight loss, diabetes treatment, or a combination of both can be more challenging than expected. From the patient’s perspective, they may experience a sense of guilt or shame regarding their morbid obesity. However, they do not typically experience the same feeling toward their diabetes; therefore, they desire the surgery they undergo to be MS. On the other hand, the perspective of a surgeon is somewhat diverse. however, it appears that they prefer to use the term ‘bariatric surgery,’ which has almost certain postoperative treatment effects, rather than the term ‘metabolic surgery,’ which has various postoperative treatment effects. Nevertheless, some surgeons with a strong academic interest in MS prefer to refer to their work as “metabolic surgery” whenever possible. From a broad perspective, surgery for all obese patients with diabetes can be considered as MS.
CURRENT EVIDENCES OF MS
MS is an effective procedure that combines the characteristics of adequate and sustainable weight loss, which is the hallmark of bariatric surgery, with improvement of diabetes through a variety of mechanisms that may or may not be related to weight loss. Although concrete guidelines have not yet been established, data on comparable glycemic control continue to be published, and the traditional notion of indications for MS for those above a certain BMI is rapidly evolving.
After the publication of the first guidelines on the surgical treatment for T2DM in 2007 by the first Diabetes Surgery Summit (DSS-I), a revised set of guidelines was announced in 2015 by the second DSS (DSS-II). After the predominantly observational study-based DSS-I guidelines [9], the American Diabetes Association (ADA) and the International Diabetes Federation (IDF) gradually advanced the evidence [10,11], and in the DSS-II [12], meaningful conclusions were drawn based on important randomized controlled trial results (Table 1). The DSS-II guideline stated that MS: 1) should be a recommended option to treat T2DM in appropriate surgical candidates with class III obesity (BMI ≥40 kg/m2), regardless of the level of glycemic control, as well as in patients with class II obesity (BMI 35.0–39.9 kg/m2) with inadequately controlled hyperglycemia despite lifestyle and optimal medical therapy; 2) should also be considered to be an option to treat T2DM in patients with class I obesity (BMI 30.0–34.9 kg/m2) and inadequately controlled hyperglycemia; and 3) all BMI thresholds should be reduced by 2.5 kg/m2 for Asian patients.
Table 1. Randomized controlled trials on MS for patients with T2DM.
| Authors | Type of surgery | No. of patients | BMI indication (% of patients with < or ≤35) | Overall remission rate (P<0.05) | Remission criteria* | Follow-up (period, rate) |
|---|---|---|---|---|---|---|
| Dixon et al. [13] | LAGB vs. control | 30 vs. 30 | >30 and <40 (<35, 22%) | 73% vs. 13% | HbA1c <6.2% | 24 months, 92% |
| Schauer et al. [14,15] | RYGB vs. SG vs. control | 50 vs. 50 vs. 50 | ≥27 and ≤43 (<35, 36%) | 35% vs. 20% vs. 0 | HbA1c ≤6.2% | 36 months, 91% |
| Mingrone et al. [16,17] | RYGB vs. BPD vs. control | 20 vs. 20 vs. 20 | ≥35 | 42% vs. 68% vs. 0 | HbA1c ≤6.5% | 60 months, 88% |
| Ikramuddin et al. [18,19] | RYGB vs. control | 60 vs. 60 | ≥30 and <40 (<35, 59%) | 25% vs. 0% | HbA1c ≤6.0% | 24 months, 92% |
| Liang et al. [20] | RYGB vs. control vs. Exenatide | 31 vs. 36 vs. 34 | >28 and <35 | 90% vs. 0 vs. 0 | No description | 12 months, 100% |
| Halperin et al. [21] | RYGB vs. control | 19 vs. 19 | ≥30 and ≤42 (<35, 34%) | 58% vs. 16% | HbA1c <6.5% | 12 months, 100% |
| Courcoulas et al. [22,23] | RYGB vs. LAGB vs. control | 20 vs. 21 vs. 20 | ≥30 and ≤40 (<35, 43%) | 40% vs. 29% vs. 0 | HbA1c <6.5% | 36 months, 85% |
| Wentworth et al. [24] | LAGB vs. control | 25 vs. 26 | ≥25 and ≤30 (≤30, 100%) | 52% vs. 8% | FBS <7.0 mmol/L | 24 months, 92% |
| Parikh et al. [25] | Bariatric surgery (RYGB, LAGB, SG) vs. control | 29 vs. 28 | ≥30 and ≤35 (≤35, 100%) | 65% vs. 0 | HbA1c <6.5% | 6 months, 100% |
| Cummings et al. [26] | RYGB vs. control | 23 vs. 20 | ≥30 and ≤45 (<35, 25%) | 60% vs. 5.9% | HbA1c <6.0% | 12 months, 74% |
| Mingrone et al. [27] | RYGB vs. BPD vs. control | 20 vs. 20 vs. 20 | ≥35 | 25% vs. 50% vs. 0 | HbA1c <6.5% | 120 months, 95% |
MS = metabolic surgery; T2DM = type 2 diabetes mellitus; BMI = body mass index; LAGB = laparoscopic adjustable gastric banding; HbA1c = glycated hemoglobin; RYGB = Roux-en-Y gastric bypass; sleeve gastrectomy; BPD = biliopancreatic diversion.
*Reaching HbA1c value without diabetes medication, unless otherwise specified.
Most importantly, the glycemic benefits of MS have been observed in patients with an initial BMI<35 kg/m2. In the STAMPEDE trial, the antidiabetic effects of MS were the same in patients with preoperative BMIs higher or lower than 35 kg/m2 [14,15,28]. The outcomes of pure MS in patients with BMI ≤30 have been reported in Taiwan and China. Lee et al. [8] in Taiwan reported a 25% complete remission rate and 60% diabetes improvement in 80 patients with type 2 diabetic and a BMI ≤30. Liang et al. [29] in China reported a 50% complete and partial remission rate in the same patient population. RYGB was reported to be effective in Indian patients with a baseline BMI of less than 35 kg/m2 [30], and meta-analyses have also demonstrated similar BMI-independent benefits of MS [31,32]. As a result, the current guidelines support the use of MS in patients with class I obesity and poorly controlled T2DM [12], particularly, the 2022 American Society for Metabolic and Bariatric Surgery/International Federation for the Surgery of Obesity and Metabolic Disorders guideline suggested that MS should be considered for patients with a BMI of 30–34.9 kg/m2 and for Asian patients with a BMI ≥27.5 kg/m2, indicating a downward revision of the BMI criteria [33].
CURRENT STATUS OF MS IN KOREA
1. MS in a broad definition (metabolic bariatric surgery [MBS] performed in morbidly obese patients with diabetes)
According to a national survey conducted by the Korean Society for Metabolic and Bariatric Surgery (KSMBS), the first MBS was performed in Korea in 2003 [5]. Since then, fewer than 100 procedures have been performed each year, and the number of cases has increased dramatically to approximately 1,700 in 2013, with the rise in gastric banding since 2009. However, along with the international decline in gastric banding, the number of domestic MBS procedures has gradually decreased to approximately 500–600 cases annually. However, since the National Health Insurance began covering MBS in 2019, the number of cases has sharply increased to almost 3,000 cases annually.
Since 2019, the KSMBS has conducted a registration program for MBS, targeting certified surgeons accredited by the KSMBS. From 2019 to 2021, 4,382 cases were registered in the registration program data, corresponding to 72% of the 6,714 MBS cases reported to the Health Insurance Review and Assessment Service during the same period. Of these, 1,560 cases were accompanied by T2DM, accounting for 35.6% of all the total number of MBS cases (Fig. 1). Based on this calculation, a maximum of 2,167 cases of MS in Korea were performed over 3 years, with an average of approximately 722 cases per year. In general, it can be predicted that the prevalence of diabetes will increase as BMI increases. However, as shown in Fig. 1, a lower rate of diabetes above BMI 35 kg/m2 can be interpreted as a stronger trend for BS for BMI ≥35 kg/m2 and a stronger trend for MS for BMI <35 kg/m2.
Fig. 1. Proportion of diabetes according to the body mass index (2019–2021).
DM = diabetes mellitus.
When comparing patients enrolled in the KSMBS registry through 2021 and categorizing them into diabetic and non-diabetic groups, the diabetic group had a mean age of 41.1 years, a relatively higher proportion of male patients, and a slightly lower mean weight by 1.4 kg. In terms of the operation type, the diabetic group had a lower proportion of SG (57.7% vs. 83.6%), a higher proportion of RYGB (24.8% vs. 10.6%), and a higher sleeve-duodenojejunal bypass (DJB) (6.8% vs. 0.6%; P<0.01) (Table 2).
Table 2. Comparison of demographics of DM vs. non-DM (2019–2021).
| Characteristics | DM group | Non-DM group | P value | |
|---|---|---|---|---|
| Cases | 1,560 (35.6%) | 2,822 (64.4%) | ||
| Mean age (year) | 41.1 | 35.7 | <0.05 | |
| Sex (M:F) | 1:2.0 | 1:2.8 | ||
| Mean body weight (kg) | 105.9 | 107.3 | <0.05 | |
| Mean BMI (kg/m2) | 38.3 | 39.0 | <0.05 | |
| Operation method | <0.01 | |||
| Sleeve gastrectomy | 900 (57.7%) | 2,360 (83.6%) | ||
| Gastric bypass | 387 (24.8%) | 298 (10.6%) | ||
| Sleeve-DJB | 106 (6.8%) | 17 (0.6%) | ||
| Gastric banding | 20 (1.3%) | 32 (1.1%) | ||
| Others (ex. Resectional bypass, Sleeve-PJB) | 147 (9.4%) | 115 (4.1%) | ||
The data in this table is for patients who had surgery in 2019-2021, and the data was collected in October 2022.
DM = diabetes mellitus; BMI = body mass index; DJB = duodenojejunal bypass; PJB = proximal jejunal bypass.
2. MS with BMI less than 35 kg/m2
Although the term “pure MS” was used to refer to surgeries performed on patients with diabetes who had a BMI less than 30 kg/m2, the number of cases was not sufficiently large; therefore, we expanded the scope to compare MS cases in patients with diabetes who had a BMI <35 and cases with a BMI ≥35 kg/m2. Similar to MS with a broad definition, SG was the most commonly performed procedure. However, its proportion was lower than that in the BMI ≥35 kg/m2 group (49.1% vs. 60.1%; P<0.001). Conversely, the proportion of RYGB and sleeve-DJB was significantly higher in the BMI<35 kg/m2 group (27.6% vs. 24.4%, 7.6% vs. 5.6%; P<0.05) (Table 3).
Table 3. Metabolic surgery for BMI 35 kg/m2 or less (2019–2020).
| Operation method | All cases | DM cases | ||||
|---|---|---|---|---|---|---|
| BMI <35 | BMI ≥35 | P value | BMI <35 | BMI ≥35 | P value | |
| Sleeve gastrectomy | 661 (65.9%) | 1,879 (77.4%) | <0.001 | 219 (49.1%) | 460 (60.1%) | <0.05 |
| Gastric bypass | 178 (17.8%) | 350 (14.4%) | 123 (27.6%) | 187 (24.4%) | ||
| Gastric banding | 18 (1.8%) | 27 (1.1%) | 8 (1.8%) | 9 (1.2%) | ||
| Sleeve-DJB | 38 (3.8%) | 48 (2.0%) | 34 (7.6%) | 43 (5.6%) | ||
| Others | 108 (10.8%) | 125 (5.1%) | 62 (13.9%) | 66 (8.6%) | ||
| Total | 1,003 | 2,429 | 446 | 765 | ||
The data in this table is for patients who had surgery in 2019-2020, and the data was collected in September 2021.
BMI = body mass index; DM = diabetes mellitus; DJB = duodenojejunal bypass.
It is widely accepted that obese patients with diabetes respond well to MS. The surgeons use several prediction models to calculate the possibility of diabetes improvement after MS. The most widely used ABCD system predicts the degree of diabetes remission based on four factors: age, BMI, C-peptide level, and duration of diabetes [8]. However, the aforementioned non-weight-loss effects cannot be ignored. One factor that many physicians and surgeons have highlighted as an outcome of diabetes improvement, in addition to weight loss, is the ability of the pancreatic beta cells to secrete insulin. This indicates that, as long as there is some insulin secretion, peripheral insulin resistance can be lowered by performing MS, which can lead to diabetes control, regardless of weight loss. In clinical practice, MS may be considered in patients who are not morbidly obese, such as those with intractable diabetes irresponsive to medical therapy, those with ongoing diabetic complications, or those who continue to gain weight with insulin use. In these patients, remission is uncommon, and improvement in the glycated hemoglobin (HbA1c) level is the most important therapeutic target, rather than discontinuing diabetes medication. Therefore, not only bariatric surgeons but also physicians are increasingly interested in the effects of MS in non-obese patients with diabetes. Because the surgical outcomes in non-obese patients with diabetes are somewhat inferior to those in obese patients with diabetes, it is crucial to make proper patient selection and provide the most appropriate surgery to the patient at the right time.
3. MS with BMI less than 30 kg/m2
Recognizing the clinical importance of MS for these non-obese patients with diabetes, the Korean government first recognized “pure MS” for T2DM with a BMI of 27.5 kg/m2 or more who are refractory to medical treatment as a new medical technology in 2018, and since January 2019, MS for patients with a BMI between 27.5 kg/m2 and 30 kg/m2 has been covered by partial national health insurance (80% patient contribution). According to the KSMBS registry data, among 1,398 registered cases of MBS in 2019, 475 were accompanied by diabetes, indicating that approximately 34% of MBS cases in Korea have an MS component, which is similar to the previously reported ratio of 35.6%. SG was performed in 74% of all MBS cases and RYGB in 15.4%. In contrast, in the MS group, SG and RYGB accounted for 59% and 29.9%, respectively, indicating that RYGB was performed more frequently. Among the patients with diabetes and a BMI of less than 30, a total of 23 patients, accounting for 4.8% of MS, were identified. The patients were relatively older, with an average age of 47.3 years, with a higher proportion of RYGB (34.8%), no banding procedure, and a relatively higher proportion of sleeve-DJB (8.7%) (Fig. 2).
Fig. 2. Comparison of the characteristics and operation types of patients who underwent bariatric, metabolic, and pure metabolic surgery (2019).
The data in this figure is for patients who had surgery in 2019, and the data was collected in August 2020.
DM = diabetes mellitus; BMI = body mass index.
In 2019, 23 pure MS were registered with the KSMBS in Korea, representing approximately 5% of the 475 registered MS. Of the 19 cases for which more detailed clinical outcomes were available, all but four cases had preoperative ABCD scores of 4 or less, indicating a very low likelihood of diabetes remission. The postoperative outcomes of these patients up to one year, showed that in all but five cases, the number of diabetes medications could be reduced, and in all but two cases, the HbA1c level could be lowered to 7.0% or less. Several multicenter long-term follow-up studies are underway in Korea, and the conclusions of the analysis of MS outcomes in patients with T2DM and obesity conducted by the National Evidence-based Healthcare Collaborating Agency will be particularly noteworthy.
CONCLUSION
MS is no longer a surgery that only surgeons claim to be superior. The IDF, an organization of endocrinologists, also recommends MS as a treatment for patients with T2DM who are morbidly obese with BMI ≥30 or 35. The mechanism by which MS cures diabetes is thought to be primarily a secondary effect of weight loss; however, there appear to be several other mechanisms.
More recently, the value of MS has been recognized in patients with T2DM who have a BMI <30 and are unresponsive to medical therapy. However, in these non-obese patients with diabetes, the improvement in diabetes is generally lower than that in obese patients with diabetes; therefore, it is expected that the effectiveness of treatment can be improved by actively engaging in multidisciplinary collaboration between physicians and surgeons before surgery to determine the indications, timing, and types of surgery.
ACKNOWLEDGMENTS
The data in this review were based on cases registered in the Korean Society for Metabolic and Bariatric Surgery registry program. The registry-based data can change over time owing to late registration and updates, potentially affecting the number of surgeries in future registry-related articles.
Footnotes
Funding: This study was supported by grants from the National Evidence-Based Healthcare Collaborating Agency (grant number: HC21C0099) funded by the Ministry of Health & Welfare, Republic of Korea. The funder played no role in the study design, data collection, analysis, interpretation, or manuscript preparation.
Conflict of Interest: None of the authors have any conflict of interest.
References
- 1.Sjöström L, Narbro K, Sjöström CD, Karason K, Larsson B, Wedel H, et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med. 2007;357:741–752. doi: 10.1056/NEJMoa066254. [DOI] [PubMed] [Google Scholar]
- 2.Heo Y, Lee HJ, editors. Indication of bariatric surgery. Textbook of Bariatric and Metabolic Surgery. Seoul: Koonja Publishing Inc.; 2018. Korean Society of Metabolic and Bariatric Surgery; pp. 71–76. [Google Scholar]
- 3.Gentileschi P, Bianciardi E, Benavoli D, Campanelli M. Metabolic surgery for type II diabetes: an update. Acta Diabetol. 2021;58:1153–1159. doi: 10.1007/s00592-021-01722-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Angrisani L, Santonicola A, Iovino P, Ramos A, Shikora S, Kow L. Bariatric surgery survey 2018: similarities and disparities among the 5 IFSO chapters. Obes Surg. 2021;31:1937–1948. doi: 10.1007/s11695-020-05207-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Lee HJ, Ahn HS, Choi YB, Han SM, Han SU, Heo YS, et al. Nationwide survey on bariatric and metabolic surgery in Korea: 2003-2013 results. Obes Surg. 2016;26:691–695. doi: 10.1007/s11695-015-2030-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Batterham RL, Cummings DE. Mechanisms of diabetes improvement following bariatric/metabolic surgery. Diabetes Care. 2016;39:893–901. doi: 10.2337/dc16-0145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Pok EH, Lee WJ. Gastrointestinal metabolic surgery for the treatment of type 2 diabetes mellitus. World J Gastroenterol. 2014;20:14315–14328. doi: 10.3748/wjg.v20.i39.14315. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Lee WJ, Almulaifi A, Chong K, Chen SC, Tsou JJ, Ser KH, 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;25:1772–1778. doi: 10.1007/s11695-015-1603-0. [DOI] [PubMed] [Google Scholar]
- 9.Rubino F, Kaplan LM, Schauer PR, Cummings DE Diabetes Surgery Summit Delegates. The Diabetes Surgery Summit consensus conference: recommendations for the evaluation and use of gastrointestinal surgery to treat type 2 diabetes mellitus. Ann Surg. 2010;251:399–405. doi: 10.1097/SLA.0b013e3181be34e7. [DOI] [PubMed] [Google Scholar]
- 10.American Diabetes Association. Standards of medical care in diabetes--2009. Diabetes Care. 2009;32(Suppl 1):S13–S61. doi: 10.2337/dc09-S013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Dixon JB, Zimmet P, Alberti KG, Rubino F International Diabetes Federation Taskforce on Epidemiology and Prevention. Bariatric surgery: an IDF statement for obese Type 2 diabetes. Diabet Med. 2011;28:628–642. doi: 10.1111/j.1464-5491.2011.03306.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Rubino F, Nathan DM, Eckel RH, Schauer PR, Alberti KG, Zimmet PZ, 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. doi: 10.2337/dc16-0236. [DOI] [PubMed] [Google Scholar]
- 13.Dixon JB, O’Brien PE, Playfair J, Chapman L, Schachter LM, Skinner S, et al. Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial. JAMA. 2008;299:316–323. doi: 10.1001/jama.299.3.316. [DOI] [PubMed] [Google Scholar]
- 14.Schauer PR, Kashyap SR, Wolski K, Brethauer SA, Kirwan JP, Pothier CE, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med. 2012;366:1567–1576. doi: 10.1056/NEJMoa1200225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Brethauer SA, Navaneethan SD, et al. Bariatric surgery versus intensive medical therapy for diabetes--3-year outcomes. N Engl J Med. 2014;370:2002–2013. doi: 10.1056/NEJMoa1401329. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, Leccesi L, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med. 2012;366:1577–1585. doi: 10.1056/NEJMoa1200111. [DOI] [PubMed] [Google Scholar]
- 17.Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, Nanni G, 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;386:964–973. doi: 10.1016/S0140-6736(15)00075-6. [DOI] [PubMed] [Google Scholar]
- 18.Ikramuddin S, Korner J, Lee WJ, Connett JE, Inabnet WB, Billington CJ, et al. Roux-en-Y gastric bypass vs intensive medical management for the control of type 2 diabetes, hypertension, and hyperlipidemia: the Diabetes Surgery Study randomized clinical trial. JAMA. 2013;309:2240–2249. doi: 10.1001/jama.2013.5835. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Ikramuddin S, Billington CJ, Lee WJ, Bantle JP, Thomas AJ, Connett JE, et al. Roux-en-Y gastric bypass for diabetes (the Diabetes Surgery Study): 2-year outcomes of a 5-year, randomised, controlled trial. Lancet Diabetes Endocrinol. 2015;3:413–422. doi: 10.1016/S2213-8587(15)00089-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Liang Z, Wu Q, Chen B, Yu P, Zhao H, Ouyang X. Effect of laparoscopic Roux-en-Y gastric bypass surgery on type 2 diabetes mellitus with hypertension: a randomized controlled trial. Diabetes Res Clin Pract. 2013;101:50–56. doi: 10.1016/j.diabres.2013.04.005. [DOI] [PubMed] [Google Scholar]
- 21.Halperin F, Ding SA, Simonson DC, Panosian J, Goebel-Fabbri A, Wewalka M, et al. Roux-en-Y gastric bypass surgery or lifestyle with intensive medical management in patients with type 2 diabetes: feasibility and 1-year results of a randomized clinical trial. JAMA Surg. 2014;149:716–726. doi: 10.1001/jamasurg.2014.514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Courcoulas AP, Goodpaster BH, Eagleton JK, Belle SH, Kalarchian MA, Lang W, et al. Surgical vs medical treatments for type 2 diabetes mellitus: a randomized clinical trial. JAMA Surg. 2014;149:707–715. doi: 10.1001/jamasurg.2014.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Courcoulas AP, Belle SH, Neiberg RH, Pierson SK, Eagleton JK, Kalarchian MA, 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. doi: 10.1001/jamasurg.2015.1534. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Wentworth JM, Playfair J, Laurie C, Ritchie ME, Brown WA, Burton P, et al. Multidisciplinary diabetes care with and without bariatric surgery in overweight people: a randomised controlled trial. Lancet Diabetes Endocrinol. 2014;2:545–552. doi: 10.1016/S2213-8587(14)70066-X. [DOI] [PubMed] [Google Scholar]
- 25.Parikh M, Chung M, Sheth S, McMacken M, Zahra T, Saunders JK, et al. Randomized pilot trial of bariatric surgery versus intensive medical weight management on diabetes remission in type 2 diabetic patients who do NOT meet NIH criteria for surgery and the role of soluble RAGE as a novel biomarker of success. Ann Surg. 2014;260:617–622. doi: 10.1097/SLA.0000000000000919. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Cummings DE, Arterburn DE, Westbrook EO, Kuzma JN, Stewart SD, Chan CP, et al. Gastric bypass surgery vs intensive lifestyle and medical intervention for type 2 diabetes: the CROSSROADS randomised controlled trial. Diabetologia. 2016;59:945–953. doi: 10.1007/s00125-016-3903-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, Capristo E, 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. doi: 10.1016/S0140-6736(20)32649-0. [DOI] [PubMed] [Google Scholar]
- 28.Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Aminian A, Brethauer SA, et al. Bariatric surgery versus intensive medical therapy for diabetes: 5-year outcomes. N Engl J Med. 2017;376:641–651. doi: 10.1056/NEJMoa1600869. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Liang H, Cao Q, Liu H, Guan W, Wong C, Tong D. The predictive factors for diabetic remission in Chinese patients with BMI >30 kg/m2 and BMI <30 kg/m2 are different. Obes Surg. 2018;28:1943–1949. doi: 10.1007/s11695-017-3106-7. [DOI] [PubMed] [Google Scholar]
- 30.Shah SS, Todkar JS, Shah PS, Cummings DE. Diabetes remission and reduced cardiovascular risk after gastric bypass in Asian Indians with body mass index <35 kg/m2. Surg Obes Relat Dis. 2010;6:332–338. doi: 10.1016/j.soard.2009.08.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.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. doi: 10.1097/SLA.0000000000000863. [DOI] [PubMed] [Google Scholar]
- 32.Cummings DE, Cohen RV. Bariatric/metabolic surgery to treat type 2 diabetes in patients with a BMI 35 kg/m2 . Diabetes Care. 2016;39:924–933. doi: 10.2337/dc16-0350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Eisenberg D, Shikora SA, Aarts E, Aminian A, Angrisani L, Cohen RV, et al. 2022 American Society for Metabolic and Bariatric Surgery (ASMBS) and International Federation for the Surgery of Obesity and Metabolic Disorders (IFSO): indications for metabolic and bariatric surgery. Surg Obes Relat Dis. 2022;18:1345–1356. doi: 10.1016/j.soard.2022.08.013. [DOI] [PubMed] [Google Scholar]