Predictors for type 2 diabetes mellitus remission after metabolic/bariatric surgery
Review Article

Predictors for type 2 diabetes mellitus remission after metabolic/bariatric surgery

Yue-Lin Fang1, Wei-Jei Lee2

1Division of General Surgery, Department of Surgery, Shin Kong Wu Ho-Su Memorial Hospital, Taiwan; 2Department of Surgery, Min-Sheng General Hospital, National Taiwan University, Taiwan

Contributions: (I) Conception and design: WJ Lee; (II) Administrative support: WJ Lee; (III) Provision of study materials or patients: All authors; (IV) Collection and assembly of data: All authors; (V) Data analysis and interpretation: All authors; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Dr. Wei-Jei Lee, MD, PhD. Min-Sheng General Hospital, No 168, Chin Kuo Road, Taoyuan, Taiwan. Email: wjlee_obessurg_tw@yahoo.com.tw.

Abstract: Type 2 diabetes mellitus (T2DM), fueled by an obesity epidemic, have emerged as a major health problem worldwide. Metabolic surgery, derived from bariatric surgery, is now proposed for the treatment of obese T2DM patients. Several randomized trials aimed at T2DM treatment have been performed and universally showed that metabolic surgery is more effective than medical treatment in glycemic control. However, not every T2DM patient benefit from metabolic surgery. An article review disclosed that pre-operative β-cell function, and its surrogates, including duration of diabetes and C-peptide, was the most important predictor of T2DM remission. Other factors were insulin use, HbA1c level, BMI, age, type of operation and miscellaneous ones. Some scoring systems, such as “ABCD” in the Diabetes surgery score (age, BMI, C-peptide and duration of T2DM), may help evaluate effectiveness of T2DM remission after surgery. In conclusion, metabolic surgery is a novel treatment option for obese T2DM patients but not all the patients are indicated. Pre-operative β-cell function (including duration of diabetes and C-peptide) are important predictor of the success of metabolic surgery. A scoring system is helpful for counseling patients and referring physicians, and may help to guide their expectations.

Keywords: Type 2 diabetes; metabolic surgery; predictor; remission


Received: 06 July 2017; Accepted: 17 July 2017; Published: 25 July 2017.

doi: 10.21037/ales.2017.07.08


Introduction

Type 2 diabetes mellitus (T2DM), booster by obesity epidemic, poses a major threat to health and represents an economic burden worldwide now (1). Bariatric/metabolic surgery is becoming a potential cure for T2DM in an unexpected way. Strong evidences have shown that this kind of surgery provides significant and durable weight loss and remission of associated T2DM in morbidly obese patients (2-4). A 78.1% complete remission (so-called “cure”) rate of T2DM was reported by Buchwald et al. in a meta-analysis study (2). Meijer et al. reported a similar 62–83% of T2DM remission rate at a 2- to 4-year follow-up in a systemic review (3). Pories et al. than reported a long-term T2DM remission rate of 82.9% at a 10- to 14-year follow-up in a case series. However, these studies were aimed at obesity treatment in morbid obese patients and using relatively loose criteria for T2DM remission. On the other hand, bariatric/metabolic surgery, sometimes irreversible, may cause considerable short- and long-term risks or co-morbidities (5). Therefore, for patients with T2DM, to achieve the most benefit from bariatric/metabolic surgery, strict and cautious preoperative evaluations are required. Optimal outcomes for the surgical treatment of T2DM depend on the way that distinguish patients suitable for surgery from patients not likely to respond well to surgery. Understanding the criteria for the latter group is critical in patients counseling and referring physicians and help guide their expectations with regard to the outcomes of various weight-relate disease. Although weight loss plays a key role in diabetes remission, other pre-operative predictors for diabetes remission are also important and should be considered in counseling patients for surgery. There were some review articles but lack an adequate number of relevant articles for review, resulting in controversial or inconsistent conclusions (5,6). In this review, we will focus on reported pre-operative predictors and predicting system for T2DM remission after metabolic surgery.


β -cell preserve

Because β cell is progressively deteriorating in the natural course of T2DM, the most important predicting factor for the success of metabolic surgery is related to the β-cell preserve and function of the T2DM patients. However, at present there is no good way to direct evaluate the beta cell mass or function of insulin secretion. There are several surrogates of β-cell function, such as C-peptide, duration and some challenge tests. We will discuss in the following.

C-peptide

C-peptide is a connecting peptide to insulin and was secreted at the same time when insulin was secreted. Although insulin levels have a similar indication as C-peptide levels, directly measuring insulin levels may be difficult because of the hepatic clearance or in patients receiving insulin therapy. Therefore, C-peptide becomes a surrogate of insulin and represents the capacity of insulin secretion, and can be used as an important predictor of patients who may benefit from bariatric surgery. As β cells are progressively destroyed in late stage T2DM, C-peptide levels may progressively decrease to very low levels in late stage patients. Therefore, levels of C-peptide levels reflect the pancreas preservation of T2DM patients. Measuring C-peptide levels help us to understand the β-cell preserve of T2DM patients. Although some controversies remained (7), many studies reported that fasting C-peptide is an important predictor of T2DM remission because C-peptide may represent the residual β-cell function of T2DM patients (8-19). Lee found that elevated C-peptide is very important in predicting the success of T2DM remission after LSG in low BMI patients for the first time (8). C-peptide was found to be linear correlated with the BMI and measurement of C-peptide is indicated in low BMI T2DM patients before considering metabolic surgery for the treatment of T2DM (9). High C-peptide levels equate to a good reserve of beta-cell function with sufficient mass, especially in the low BMI and Asian groups. Elevated C-peptide levels usually implicated the existence of insulin resistance and a compensated secretion of insulin by well-preserved pancreatic β-cell. Therefore, a greater C-peptide level usually associates with a higher T2DM remission rate after metabolic surgery (8,10). Some studies found that stimulated C-peptide level or total secretion amount of C-peptide (measured by area under curve during glucose tolerate test) was also predictor of T2DM remission (20,21).

Duration of T2DM

The importance of disease duration as predictor of T2DM was first reported by Pories et al. in his historical landmark article (4). Since then, many studies consistently confirmed that disease duration is an important predictor and the most commonly reported predictor of T2DM remission (10,12,13,17-19,22-40). Duration has also been confirmed by a multivariate analysis to be the only pre-operative predictor of T2DM remission after adjustable banding in a randomized trial (23). In sleeve gastrectomy patients, Rosenthal et al. found that the T2DM remission rate become very low once the patient’s T2DM duration greater than 5 years (25). Lee et al. also reported that the duration of T2DM was the most important predictor of success after metabolic using a decision tree analysis (28). Arteburn et al. in a big cohort study of 4,434 gastric bypass patients identified that longer diabetes duration is a significant predictor of complete remission and relapse (35). Because T2DM is a disease with progressive decrease of both of β-cell mass and function, the duration of disease usually can reflect the residual β-cell preserve. The long duration of T2DM indicates a smaller chance of T2DM remission. The cut-off point was calculated in some articles as 1.6, 2, 4, 5, 8 and 10 years. Therefore, earlier surgical intervention, equates to better outcomes, should be encouraged. Although some may argue that disease duration is subjective and estimated, this study shows the importance of disease duration in predicting the success of metabolic surgery. Therefore, earlier intervention is not only important to increase the rate of T2DM remission but can also prevent the development of T2DM (41).

Pre-operative β-cell function

Although C-peptide levels may partially reflect residual β-cell function, fasting levels of C-peptide have some limitations, such as their suppression in hyperglycemic status. Thus, the interpretation of low C-peptide levels must be made with caution (7). Various preoperative assessments of beta-cell function, including glucose sensitivity β-cell glucose sensitivity (BCGS) (42,43), lower insulin sensitivity (ISR) (44), glucagon like peptide-1 (GLP-1) response (45), area under the curve (AUC) of glucose, insulinogenic index derived from a standard meal test (IGIstm), acute insulin response to glucose (AIRg), disposition index derived from an intravenous glucose tolerance test (DIfsivgtt) (46), disproportion index (DI) (47), HOMA-%B (48), ISSI (49) and so on, have been proven to be useful in evaluating the degree of the beta-cell function reserve and predicting T2DM remission rates. However, these studies are too complex for routine clinical practice. C-peptide and duration are simple and good surrogates of β-cell preserve and should be adopted in pre-operative evaluation of T2DM patients for metabolic surgery.


Disease severity of T2DM

Good glycemic control is the principle goal of diabetes treatment. The severity of T2DM is interpreted by glycemic control represented by hemoglobin A1c (HbA1c) or using insulin therapy.

Pre-operative HbA1c or fasting glucose

HbA1c generally reflects the range of glucose fluctuation in the past two weeks and may indicate the severity of T2DM. Greater HbA1c levels indicate high blood glucose levels which usually result from poor higher insulin resistance or lower β-cell function. Many studies reported that lower HbA1c levels (HbA1c cut-off point was <7–8%) equate to a higher T2DM remission rate after surgery (24,26,30,34,35,37,50-52). High HbA1c correlates to a poorer baseline and lower probability of remission. However, many studies also found HbA1c is not a independent predictor when duration and C-peptide are consider because newly diagnosed T2DM patients might present with very high HbA1c but will response to surgery well. In addition, very T2DM patients with high HbA1c should not be denied for the metabolic surgery because high HbA1c means very high risk of diabetic related complication and those are the best to benefit from metabolic surgery (53). In some studies without HbA1c data, fasting glucose level was shown to be an independent predictor of T2DM remission (34,50).

Pre-operative Insulin use

Insulin usage is the second most reported preoperative predictor. Many studies reported that patients who did not receive insulin therapy are more likely to have T2DM remission after surgery than the patients who underwent insulin treatment after surgery (24,27,29,30,34,35,50,52,54-56). Insulin was usually prescribed when the residual β-cell reserve could not provide enough insulin for glycemic control. In another words, insulin usage implied a more severe disease stage, thus decreasing the DM remission rate. However, some of the studies which reported use of insulin is an independent predictor didn’t have the information of duration of T2DM (50,52,54,56). Because the longer the disease, the higher of the rate of insulin usage, insulin usage might not be a important predictor if duration was analyzed at the same time. Other important confounding factors of insulin usage are regional guideline, drug license, local practice and the compliance of patients (57). For example, UK had a higher rate of insulin usage than in the USA (23.3% vs. 8.1%) (58,59). In another randomized trial of surgical versus medical treatment of diabetes patients, more than 70% of the USA patients used insulin, while only 30% of Taiwanese patients used insulin (20). This study found that insulin usage is not a predictor of T2DM remission in the low BMI and Asian groups.


General physical status

Many general physical statuses had been reported to be independent predictors. These factors included age, sex, BMI, waist and some miscellaneous factors.

Age

Some studies found that young age predict a higher T2DM remission rate than old age (4,9,18,27,31,52,56,60-62). Age not only represents the general reserve of physiological function but also β-cell preserve. Increase of the age implied the decline of β-cell mass and functional reserve. It was found that each additional 12 years of age reduced 20% the chance of T2DM remission by metabolic surgery (62). Although young-onset T2DM patients had a worse glycemic control than adult-onset, young-onset patients had a better T2DM remission rates after metabolic surgery (63). Therefore, metabolic surgery is highly recommended not only in the early stage of T2DM but also in young-onset T2DM patients.

Pre-operative BMI (body mass index)

The predictive power of morbid obesity (BMI >35 Kg/m2) on T2DM remission after surgery is controversial. Lee et al. was the first to found that T2DM remission rate was lower in low BMI patients than in high BMI patients (64). Hayes et al. reported five independent predictors including BMI (50), whereas Mingrone et al. found negative results with BMI (65). Both studies had similar pre-operative mean baseline BMIs of 48 Kg/m2. Other studies support the role of BMI (10,18,31-33,61) where others didn’t (9,11,30,33,36,66). However, super-morbid obesity (BMI >50 Kg/m2) was found to be a negative predictor of T2DM remission (34), possibly as a result of the correlation between super obesity and severe insulin resistance or destroyed β-cells. Although BMI as a preoperative factor remains controversial, high BMI usually associated with greater weight loss and may provide a greater effect on T2DM remission. In randomized trials, the reported T2DM remission rate was progressively lower with decreasing of BMI (16,40,65,67). The T2DM remission rate after Roux-en-Y gastric bypass was 80% in a study with mean BMI of 48 Kg/m2 (65) and 50% in a study with mean BMI of 36 Kg/m2 (67), and less than 30% in those with a mean BMI <30 Kg/m2 (16,40,67). Other studies of patients with BMIs < 35 Kg/m2 also reported that BMI was an independent predictor (12,18,31,36). Therefore, the T2DM remission rate is probably higher in patients with BMIs >35 but <50 Kg/m2 than in patients with BMIs <35 Kg/m2. Although BMI as a predictor of T2DM remission after metabolic surgery remained controversial, it was important in evaluating the low BMI or Asian groups.

Waist

Data on waist is controversy, one study found waist is an independent predictor of T2DM remission after metabolic surgery (13) but another study found that waist is a negatively predict (54). One study found that visceral-to-subcutaneous fat ratio is an important predictor of T2DM remission (51). Cohen et al. found that reduction of 7% waist is the only predictor of T2DM remission after gastric bypass (68).

Sex

One study found that female was a favor predictor of T2DM remission (62) but controversy existed (56). Another study found that male was a negative predictor of T2DM remission (61).


Miscellaneous factors

Some miscellaneous factors reported to be predictors of T2DM remission after metabolic surgery was listed below.

Oral medication

One study found that oral medication (usage of sulfaurea) was a predictor of T2DM remission and put this factor into a predictive score, DiaRem score (52).

Meal stimulated GLP-1 response

Two studies found that strong response of meal stimulated GLP-1 response was a predictor of T2DM remission after surgery (43,45).

sRAGE

One study reported that soluble RAGE is a predictor of T2DM remission after surgery (69).

Rapid response to low calories diet (LCD)

One study reported that a rapid response to LCD is a predictor of success of metabolic surgery (66).

Robust incretin response

One study found that a robust incretin response was a predictor of success of metabolic surgery on T2DM treatment (49).


Weight loss

Since obesity is the most important risk for the development of T2DM, body weight reduction of course is important for T2DM remission. Many studies reported weight loss was important predictor of T2DM remission after surgery (12,22,30,39,55,60,62). A review article showed that decrease of HbA1c was linear correlated with weight loss even in BMI <35 Kg/m2 T2DM patients (70). One study found that weight loss was the most important predictor for success of metabolic surgery in patients with BMI <30 Kg/m2 (71). Because weight loss itself can’t be predicted before surgery but might be predicted by procedure, the role of weight loss as a pre-operative predictor was usually replaced by operation type.

Operative type

Gastric bypass procedure was found to have a higher T2DM remission rates than various restrictive procedures, such as laparoscopic adjustable gastric banding or laparoscopic sleeve gastrectomy (13,32,33,65,67,72-74). The superiority of different bypass procedures can be attributed to a greater weight loss rather than different anatomical changes and physiologic mechanisms (BPD > RYGB/MGB > SG > ABG) (70). However, recent studies found that duodenum exclusion plays an important role on T2D treatment (75-77). Duodenum jejunal bypass (DJB) tube was a concept pioneered by Rubino for the treatment of T2DM in animal model (78). A recent developed new device, duodenum jejuna sleeve tube or liner, was demonstrated having a similar glycemic control effect in human (79). Therefore, metabolic surgery with duodenum exclusion is more favor than other procedure for the treatment of T2DM (40,67,76).


Scoring system

If we can select T2DM patients who are best suited for metabolic surgery and exclude those who are predicted to have poor results, we shall have optimal outcomes for metabolic surgery. This requires an understanding of the predictor of T2DM remission after surgery and designing specific scoring system to counsel patients and referring physicians. Several scoring systems had been proposed (11,18,19,29,50,52). Table 1 showed the consisted components of different scoring systems. A model for predicting the resolution of type 2 diabetes in severely obese subjects following Roux-en Y gastric bypass surgery was first proposed by Hayes et al. (50). Another statistical model to predict type 2 diabetes remission after bariatric surgery was then designed by Ramos-Levi et al. (19). Dixon et al. using a simple score of duration, BMI and C-peptide can predict a 92% success rate of remission (11). Recently, a “Diabetes Surgical Score (ABCD score)” included age, BMI, c-peptide and duration of disease using prospectively collected data was proposed by Lee et al. (13). Still et al. proposed another probability score, DiaRem score, using age, use of insulin, HbA1c and type of anti-diabetic medication (52). The DiaRem score has been validated in different area but was found to be limited in high score patients (80,81). The ABCD score has a better differentiate power than DiaRem score, especially in patients with high DiaRem score (82,83). The ABCD score, system has also been validated in different population (84-87). One study demonstrated that ABCD score is the only important predictor of durable T2DM remission after metabolic surgery other than weight loss (88). Therefore, this ABCD score is recommended to identify the best candidates for metabolic surgery.

Table 1
Table 1 Predictors in different scoring system for T2DM remission of metabolic surgery
Full table

Conclusions

Bariatric/metabolic surgery significantly improves glycemic control in T2DM patients and may result in complete remission of T2DM in some patients. This review suggests that some pre-operative factors may be useful in clinical application. The most important factor is the pre-operative beta-cell preserve, represented by duration of disease and C-peptide level, which highlights the importance of early surgical intervention to treat T2DM. A simplified diabetes surgery scoring system, ABCD score, has been developed. This score system can help the physician in clinical practice. The endocrinologist may use this system to set the priority for referring T2DM patients for metabolic surgery. The surgeon can use this system to counsel the patients for outcome and choice of surgical procedure.


Acknowledgements

Funding: This work was partly supported by a grant from Ming-Shen General Hospital 2014-A01.


Footnote

Conflict of Interest: The authors have no conflicts of interest to declare.


References

  1. Chan JC, Cho NH, Tajima N, Shaw J. Diabetes in the Western Pacific Region--past, present and future. Diabetes Res Clin Pract 2014;103:244-55. [Crossref] [PubMed]
  2. Buchwald H, Estok R, Fahrbach K, et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 2009;122:248-56.e5. [Crossref] [PubMed]
  3. Meijer RI, van Wagensveld BA, Siegert CE, et al. Bariatric surgery as a novel treatment for type 2 diabetes mellitus: a systematic review. Arch Surg. 2011;146:744-50. [Crossref] [PubMed]
  4. Pories WJ, Swanson MS, MacDonald KG, et al. Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg. 1995;222:339-50; discussion 50-2. [Crossref] [PubMed]
  5. Wang GF, Yan YX, Xu N, et al. Predictive Factors of Type 2 Diabetes Mellitus Remission Following Bariatric Surgery: a Meta-analysis. Obes Surg. 2015;25:199-208. [Crossref] [PubMed]
  6. Adams ST, Salhab M, Hussain ZI, et al. Preoperatively determinable factors predictive of diabetes mellitus remission following Roux-en-Y gastric bypass: a review of the literature. Acta Diabetol. 2013;50:475-8. [Crossref] [PubMed]
  7. Cohen RV, Petry TZ, Caravatto PP. Low levels of C-peptide may not be a sign of pancreatic β-cell death or apotosis: New insight into pancreatic endocrine function and indications for metabolic surgery. Surg Obes Relat Dis 2013;9:1022-4. [Crossref] [PubMed]
  8. Lee WJ, Ser KH, Chong K, Lee YC, Chen SC, Tsou JJ, et al. Laparoscopic sleeve gastrectomy for diabetes treatment in nonmorbidly obese patients: efficacy and change of insulin secretion. Surgery 2010;147:664-9. [Crossref] [PubMed]
  9. Lee WJ, Chong K, Ser KH, et al. C-peptide predicts the remission of type 2 diabetes after bariatric surgery. Obes Surg 2012;22:293-8. [Crossref] [PubMed]
  10. Yan H, Tang L, Chen T, et al. Defining and predicting complete remission of type 2 diabetes: a short-term efficacy study of open gastric bypass. Obesity Facts 2013;6:176-84. [Crossref] [PubMed]
  11. Aarts EO, Janssen J, Janssen IM. Preoperative fasting plasma C-peptide level may help to predict diabetes outcome after gastric bypass surgery. Obes Surg 2013;23:867-73. [Crossref] [PubMed]
  12. Dixon JB, Chuang LM, Chong K, et al. Predicting the glycemic response to gastric bypass surgery in patients with type 2 diabetes. Diabetes Care 2013;36:20-6. [Crossref] [PubMed]
  13. 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/m(2)) Indian patients with type 2 diabetes mellitus. Surg Obes Relat Dis 2013;9:370-8. [Crossref] [PubMed]
  14. Lee YC, Lee WJ, Liew PL. Predictors of remission of type 2 diabetes mellitus in obese patients after gastrointestinal surgery. Obes Res Clin Pract 2013;7:e494-500. [Crossref] [PubMed]
  15. Ramos-Leví AM, Matía P, Cabrerizo L, et al. C-peptide levels predict type 2 diabetes remission after bariatric surgery. Nutr Hosp 2013;28:1599-603. [PubMed]
  16. Ikramuddin S, Koner J, Lee WJ, et al. Durability of addition of Roux-en-Y gastric bypass to lifestyle intervention and medical management in achieving primary treatment goals for uncontrolled type 2 diabetes in mild-to-moderate obesity: a randomized control trial. Diabetes Care 2016;39:1510-8. [Crossref] [PubMed]
  17. Park JY, Kim YJ. Prediction of diabetes remission in morbidly obese patients after Roux-en-Y gastric bypass. Obes Surg 2016;26:749-56. [Crossref] [PubMed]
  18. Lee WJ, Hur KY, Lakadawala M, et al. Predicting success of metabolic surgery: age, body mass index, C-peptide, and duration score. Surg Obes Relat Dis 2013;9:379-84. [Crossref] [PubMed]
  19. Ramos-Levi AM, Matia P, Cabrerizo L, et al. Statistical models to predict type 2 diabetes remission after bariatric surgery. J Diabetes 2014;6:472-7. [Crossref] [PubMed]
  20. Chong K, Ikramuddin S, Lee WJ, et al. National Differences in Remission of Type 2 Diabetes Mellitus After Roux-en-Y Gastric Bypass Surgery-Subgroup Analysis of 2-Year Results of the Diabetes Surgery Study Comparing Taiwanese with Americans with Mild Obesity (BMI 30-35 kg/m2). Obes Surg 2017;27:1189-95. [Crossref] [PubMed]
  21. Souteiro P, Belo S, Neves JS, et al. Preoperative beta dell function is predictive of diabetes remission after bariatric surgery. Obes Surg 2017;27:288-94. [Crossref] [PubMed]
  22. Dixon JB, O'Brien PE. Health outcomes of severely obese type 2 diabetic subjects 1 year after laparoscopic adjustable gastric banding. Diabetes Care 2002;25:358-63. [Crossref] [PubMed]
  23. Dixon JB, O’Brien PE, Playfair J, et al. Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial. JAMA 2008;299:316-23. [Crossref] [PubMed]
  24. Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg. 2003;238:467-84; discussion 484-5. [PubMed]
  25. Rosenthal R, Li X, Samuel S, et al. Effect of sleeve gastrectomy on patients with diabetes mellitus. Surg Obes Relat Dis 2009;5:429-34. [Crossref] [PubMed]
  26. Hall TC, Pellen MG, Sedman PC, Jain PK. Preoperative factors predicting remission of type 2 diabetes mellitus after Roux-en-Y gastric bypass surgery for obesity. Obes Surg 2010;20:1245-50. [Crossref] [PubMed]
  27. Kim S, Richards WO. Long-term follow-up of the metabolic profiles in obese patients with type 2 diabetes mellitus after Roux-en-Y gastric bypass. Ann Surg 2010;251:1049-55. [Crossref] [PubMed]
  28. Lee WJ, Hur KY, Lakadawala M, et al. Gastrointestinal metabolic surgery for the treatment of diabetic patients: a multi-institutional international study. J Gastrointest Surg 2012;16:45-51; discussion 51-2. [Crossref] [PubMed]
  29. Blackstone R, Bunt JC, Cortes MC, Sugerman HJ. Type 2 diabetes after gastric bypass: remission in five models using HbA1c, fasting blood glucose, and medication status. Surg Obes Relat Dis 2012;8:548-55. [Crossref] [PubMed]
  30. 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;256:1023-9. [Crossref] [PubMed]
  31. Huang CK, Shabbir A, Lo CH, et al. Laparoscopic Roux-en-Y gastric bypass for the treatment of type II diabetes mellitus in Chinese patients with body mass index of 25-35. Obes Surg 2011;21:1344-9. [Crossref] [PubMed]
  32. Wong SK, Kong AP, So WY, et al. Use of laparoscopic sleeve gastrectomy and adjustable gastric banding for suboptimally controlled diabetes in Hong Kong. Diabetes Obes Metab 2012;14:372-4. [Crossref] [PubMed]
  33. Lee WJ, Chong K, Chen JC, et al. Predictors of diabetes remission after bariatric surgery in Asia. Asian J Surg 2012;35:67-73. [Crossref] [PubMed]
  34. Robert M, Ferrand-Gaillard C, Disse E, et al. Predictive factors of type 2 diabetes remission 1 year after bariatric surgery: impact of surgical techniques. Obes Surg 2013;23:770-5. [Crossref] [PubMed]
  35. Arterburn DE, Bogart A, Sherwood NE, Sidney S, Coleman KJ, Haneuse S, et al. A multisite study of long-term remission and relapse of type 2 diabetes mellitus following gastric bypass. Obes Surg 2013;23:93-102. [Crossref] [PubMed]
  36. Våge V, Nilsen RM, Berstad A, et al. Predictors for remission of major components of the metabolic syndrome after biliopancreatic diversion with duodenal switch (BPDDS). Obes Surg. 2013;23:80-6. [Crossref] [PubMed]
  37. Dogan K, Betzel B, Homan J, et al. Long-Term Effects of Laparoscopic Roux-en-Y Gastric Bypass on Diabetes Mellitus, Hypertension and Dyslipidaemia in Morbidly Obese Patients. Obes Surg. 2014;24:1835-42. [Crossref] [PubMed]
  38. Wentworth JM, Playfair J, Lavrie C, et al. Multidisciplinary diabetes care with and without bariatric surgery in overweight people: a randomized controlled trial. Lancet Diabetes Endocrinol 2014;2:545-52. [Crossref] [PubMed]
  39. Panunzi S, Carlsson L, De Gaetano A, et al. Determinates of diabetes remission and glycemic control after bariatric surgery. Diabetes Care 2016;39:166-74. [Crossref] [PubMed]
  40. Schauer PR, Bhatt DL, Kirwan JP, et al. Bariatric surgery versus intensive medical therapy for diabetes – 5-year outcomes. N Engl J Med 2017;376:641-51. [Crossref] [PubMed]
  41. Carlsson LMS, Peltonen M, Ahlin S, et al. Bariatric surgery and prevention of type 2 diabetes in Swedish obese subjects. N Engl J Med 2012;367:695-704. [Crossref] [PubMed]
  42. Nannipieri M, Mari A, Anselmino M, et al. The role of beta-cell function and insulin sensitivity in the remission of type 2 diabetes after gastric bypass surgery. J Clin Endocrinol Metab 2011;96:E1372-9. [Crossref] [PubMed]
  43. Dutia R, Brakoniecki K, Bunker P, et al. Limited recovery of beta-cell function after gastric bypass despite clinical diabetes remission. Diabetes 2014;63:1214-23. [Crossref] [PubMed]
  44. De Paula AL, Stival AR, Halpern A, et al. Improvement in insulin sensitivity and beta-cell function following ileal interposition with sleeve gastrectomy in type 2 diabetic patients: potential mechanisms. J Gastrointest Surg 2011;15:1344-53. [Crossref] [PubMed]
  45. Nannipieri M, Baldi S, Mari A, et al. Roux-en-Y gastric bypass and sleeve gastrectomy: mechanisms of diabetes remission and role of gut hormones. J Clin Endocrinol Metab 2013;98:4391-9. [Crossref] [PubMed]
  46. Jiménez A, Casamitjana R, Flores L, et al. GLP-1 and the long-term outcome of type 2 diabetes mellitus after Roux-en-Y gastric bypass surgery in morbidly obese subjects. Ann Surg 2013;257:894-9. [Crossref] [PubMed]
  47. 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. [Crossref] [PubMed]
  48. 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. [Crossref] [PubMed]
  49. Hirsch FF, Pareja JC, Geloneze SR, et al. Comparison of metabolic effects of surgical-induced massive weight loss in patients with long-term remission versus non-remission of type 2 diabetes. Obes Surg 2012;22:910-7. [Crossref] [PubMed]
  50. Hayes MT, Hunt LA, Foo J, et al. A model for predicting the resolution of type 2 diabetes in severely obese subjects following Roux-en Y gastric bypass surgery. Obes Surg 2011;21:910-6. [Crossref] [PubMed]
  51. Kim MK, Lee HC, Kwon HS, et al. Visceral obesity is a negative predictor of remission of diabetes 1 year after bariatric surgery. Obesity (Silver Spring) 2011;19:1835-9. [Crossref] [PubMed]
  52. Still CD, Wood GC, 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. [Crossref] [PubMed]
  53. Yokoyama H, Okudaira M, Otani T, et al. High incidence of diabetic nephropathy in early onset Japanese NIDDM patients.Risk analysis. Diabetes Care 1998;21:1080-5. [Crossref] [PubMed]
  54. Torquati A, Lutfi R, Abumrad N, Richards WO. Is Roux-en-Y gastric bypass surgery the most effective treatment for type 2 diabetes mellitus in morbidly obese patients? J Gastrointest Surg 2005;9:1112-6; discussion 1117-8. [Crossref] [PubMed]
  55. Kadera BE, Lum K, Grant J, et al. Remission of type 2 diabetes after Roux-en-Y gastric bypass is associated with greater weight loss. Surg Obes Relat Dis 2009;5:305-9. [Crossref] [PubMed]
  56. Jurowich C, Thalheimer A, Hartmann D, et al. Improvement of type 2 diabetes mellitus (T2DM) after bariatric surgery--who fails in the early postoperative course? Obes Surg 2012;22:1521-6. [Crossref] [PubMed]
  57. Tharakan G, Scott R, Szepietowski O, et al. Limitation of the DiaRem score in predicting remission of diabetes following Roux-en-Y gastric bypass (RYGB) in an ethnically diverse population from a single institution in the UK. Obes Surg 2017;27:782-6. [Crossref] [PubMed]
  58. Sharma M, Nazareth J, Petersen I. Trends in incidence, prevalence and prescribing in type 2 diabetes mellitus between 2000 and 2013 in primary care: a retrospective cohort study. BMJ Open 2016;6:e010210. [Crossref] [PubMed]
  59. Pantalone KM, Hobbs TM, Wells BJ, et al. Changes in characteristics and treatment patterns of patients with newly diagnosed type 2 diabetes integrated health system between 2008 and 2013. Clin Med Insights Endocrinol Diabetes 2016;9:23-30. [Crossref] [PubMed]
  60. Sugerman HJ, Wolfe LG, Sica DA, Clore JN. Diabetes and hypertension in severe obesity and effects of gastric bypass-induced weight loss. Ann Surg. 2003;237:751-6; discussion 757-8. [Crossref] [PubMed]
  61. Chikunguwo SM, Wolfe LG, Dodson P, et al. Analysis of factors associated with durable remission of diabetes after Roux-en-Y gastric bypass. Surg Obes Relat Dis 2010;6:254-9. [Crossref] [PubMed]
  62. Hamza N, Abbas MH, Darwish A, et al. Predictors of remission of type 2 diabetes mellitus after laparoscopic gastric banding and bypass. Surg Obes Relat Dis 2011;7:691-6. [Crossref] [PubMed]
  63. Aung L, Lee WJ, Chen SC, et al. Bariatric surgery for patients with early-onset vs late-onset type 2 diabetes mellitus. JAMA Surg 2016;151:798-805. [Crossref] [PubMed]
  64. Lee WJ, Wang W, Lee YC, et al. Effect of laparoscopic mini-gastric bypass for type 2 diabetes mellitus: comparison of BMI>35 and <35 kg/m2. J Gastrointest Surg 2008;12:945-52. [Crossref] [PubMed]
  65. Mingrone G, Panunz S, De Gaetamo A, et al. Bariatric-metabolic surgery versus conventional medical treatment in obese patients with type 2 diabetes: 5 year follow-up of an open-label, single-center, randomized controlled trials. Lancet 2015;386:964-73. [Crossref] [PubMed]
  66. Biro SM, Olson DL, Garren MJ, Gould JC. Diabetes remission and glycemic response to pre-bariatric surgery diet. J Surg Res 2013;185:1-5. [Crossref] [PubMed]
  67. Lee WJ, Chong K, Ser KH, et al. Gastric bypass vs sleeve gastrectomy for type 2 diabetes mellitus: a randomized controlled trial. Arch Surg 2011;146:143-8. [Crossref] [PubMed]
  68. Cohen R, Caravatto PP, Correa JL, et al. Glycemic control after stomach-sparing duodenal-jejunal bypass surgery in diabetic patients with low body mass index. Surg Obes Relat Dis 2012;8:375-80. [Crossref] [PubMed]
  69. Parikh M, Chung M, Sheth S, 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;260:617-22; discussion 622-4. [Crossref] [PubMed]
  70. Ngiam KY, Lee WJ, Lee YC, Cheng A. Efficacy of metabolic surgery on HbA1c decrease in type 2 diabetes mellitus patients with BMI < 35 Kg/m2 – e review. Obes Surg 2014;24:148-58. [Crossref] [PubMed]
  71. 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. [Crossref] [PubMed]
  72. Lee WJ, Chong K, Lin YH, et al. Laparoscopic sleeve gastrectomy versus single anastomosis (mini-) gastric bypass for the treatment of type 2 diabetes mellitus: 5-year results of a randomized trial and study of incretin effect. Obes Surg 2014;24:1552-62. [Crossref] [PubMed]
  73. Dicker D, Yahalom R, Comaneshter DS, Vinker S. Long-term outcomes of three types of bariatric surgery on obesity and type 2 diabetes control and remission. Obes Surg 2016;26:1814-20. [Crossref] [PubMed]
  74. Melissas J, Stavroulakis K, Tzikoulis V, et al. Sleeve gastrectomy vs Roux-en-Y bypass. Data from IFSO-European chapter of excellence program. Obes Surg 2017;27:847-55. [Crossref] [PubMed]
  75. Rubino F, Marescaux J. Effect of duodenal-jejunal exclusion in a non-obese animal model of type 2 diabetes: a new perspective for an old disease. Ann Surg 2004;239:1-11. [Crossref] [PubMed]
  76. Lee WJ, Almulaifi AM, Tsou JJ, et al. Duodenal–jejunal bypass with sleeve gastrectomy versus the sleeve gastrectomy procedure alone: the role of duodenal exclusion. Surg Obes Relat Dis 2015;11:765-70. [Crossref] [PubMed]
  77. Zachariah PJ, Chen CY, Lee WJ, et al. Compared to Sleeve Gastrectomy, Duodenal-Jejunal Bypass with Sleeve Gastrectomy gives Better Glycemic Control in T2DM Patients, with a Lower β-Cell Response and Similar Appetite Sensations: Mixed Meal Study. Obesity Surgery 2016;26:2862-72. [Crossref] [PubMed]
  78. Rubino F, Forgione A, Cummings DE, et al. The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small in the pathophysiology of type 2 diabetes. Ann Surg 2006;244:741-9. [Crossref] [PubMed]
  79. Escalona A, Pimentel F, Sharp A, et al. Weight loss and metabolic improvement in morbidly obese subjects implanted for 1 year with endoscopic duodenal-jejunal bypass liner. Ann Surg 2012;255:1080-5. [Crossref] [PubMed]
  80. Aminian A, Brethauer SA, Kashyap SR, et al. DiaRem score: external validation. Lancet Diabetes Endocrinol 2014;2:12-3. [Crossref] [PubMed]
  81. Tharakan G, Scott R, Olivia S, et al. Limitation of the DiaRem in predicting remission of diabetes following Roux-en-Y gastric bypass (RYGB) in an ethnically diverse population from a single institution in the UK. Obes Surg 2017;27:782-6. [Crossref] [PubMed]
  82. Lee WJ, Chong K, Chen SC, et al. Pre-operative prediction of type 2 diabetes remission after gastric bypass surgery: a comparison of DiaRem scores and ABCD scores. Obes Surg 2016;26:2418-24. [Crossref] [PubMed]
  83. Park JY, Kim YJ. Reply to the comment on:”Prediction of diabetes remission in morbidly obese patients after Roux-en-Y gastric bypass. Obes Surg 2016;26:3011-3. [Crossref] [PubMed]
  84. Haruta H, Kasama K, Ohta M, et al. Long-term outcome of bariatric and metabolic surgery in Japan: Results of a multi-institutional surgery. Obes Surg 2017;27:754-62. [Crossref] [PubMed]
  85. Lee WJ, Almulaifi AM, Tsou JJ, et al. Laparoscopic Sleeve Gastrectomy for Type 2 Diabetes Mellitus: Predicting the Success by ABCD Score. Surg Obes Relat Dis 2015;11:991-6. [Crossref] [PubMed]
  86. Lee WJ, Chong K, Aung L, et al. Metabolic surgery for diabetes treatment: sleeve gastrectomy or gastric bypass? World J Surg 2017;41:216-23. [Crossref] [PubMed]
  87. Lee WJ, Almulaifi AM, 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. Obesity Surgery 2015;25:1772-8. [Crossref] [PubMed]
  88. Lee MH, Lee WJ, Chong K, et al. Predictors of long-term diabetes remission after metabolic surgery. J Gastrointest Surg 2015;19:1015-21. [Crossref] [PubMed]
doi: 10.21037/ales.2017.07.08
Cite this article as: Fang YL, Lee WJ. Predictors for type 2 diabetes mellitus remission after metabolic/bariatric surgery. Ann Laparosc Endosc Surg 2017;2:114.

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