Surgery for Obesity and Related Diseases ] (2015) 00–00
Original article
Laparoscopic sleeve gastrectomy for type 2 diabetes mellitus: predicting the success by ABCD score Wei-Jei Lee, M.D., Ph.D.a,*, Abdullah Almulaifi, M.D.a, Ju Juin Tsou, R.N.a, Kong-Han Ser, M.D.a, Yi-Chih Lee, Ph.D.b, Shu-Chun Chen, R.N.a b
a Department of Surgery, Min-Sheng General Hospital, Taoyuan, Taiwan, Republic of China Department of International Business, Chien Hsin University of Science and Technology, Taoyuan, Taiwan, Republic of China Received October 31, 2014; accepted December 23, 2014
Abstract
Background: Laparoscopic sleeve gastrectomy (LSG) is becoming a primary bariatric surgery for obesity and related diseases. This study presents the outcome of LSG with regard to the remission of type 2 diabetes mellitus (T2 DM) and the usefulness of a grading system to categorize and predict outcome of T2 DM remission. Methods: A total of 157 patients with T2 DM (82 women and 75 men) with morbid obesity (mean body mass index 39.0 ⫾ 7.4 kg/m2) who underwent LSG from 2006 to 2013 were selected for the present study. The ABCD score is composed of the patient’s age, body mass index, C-peptide level, and duration of T2 DM (yr). The remission of T2 DM after LSG was evaluated using the ABCD score. Results: At 12 months after surgery, 85 of the patients had complete follow-up data. The weight loss was 26.5% and the mean HbA1c decreased from 8.1% to 6.1%. A significant number of patients had improvement in their glycemic control, including 45 (52.9%) patients who had complete remission (HbA1c o6.0%), another 18 (21.2%) who had partial remission (HbA1c o6.5%), and 9 (10.6%) who improved (HbA1c o7%). Patients who had T2 DM remission after surgery had a higher ABCD score than those who did not (7.3 ⫾ 1.7 versus 5.2 ⫾ 2.1, P o .05). Patients with a higher ABCD score were also at a higher rate of success in T2 DM remission (from 0% in score 0 to 100% in score 10). Conclusion: LSG is an effective and well-tolerated procedure for achieving weight loss and T2 DM remission. The ABCD score, a simple multidimensional grading system, can predict the success of T2 DM treatment by LSG. (Surg Obes Relat Dis 2015;]:00–00.) r 2015 American Society for Metabolic and Bariatric Surgery. All rights reserved.
Keywords:
Type 2 diabetes mellitus; Sleeve gastrectomy; ABCD score
Type 2 diabetes mellitus (T2 DM) affects more than 300 million people worldwide, and more than 60% of them are in Asia [1,2]. Bariatric surgery has been proven to be very successful in treating not only morbid obesity but also obesity-associated T2 DM [3–5]. Among all the bariatric * Correspondence: Wei-Jei Lee, M.D., Ph.D., Department of Surgery, Min-Sheng General Hospital, No. 168, Ching-Kuo Road, Taoyuan, Taiwan, Republic of China. E-mail: [email protected]
procedures, laparoscopic sleeve gastrectomy (LSG) has been gaining popularity as a stand-alone bariatric surgery worldwide despite the paucity of long-term outcome data [6,7]. However, the data about T2 DM remission after LSG is controversial. Some studies have reported very good results [8,9], and other studies have reported limited efficacy [10–12]. A possible explanation for this is that the patient characteristics might be different between these studies. It is also uncertain if the widely varied remission rates between the studies of LSG are related to patient
http://dx.doi.org/10.1016/j.soard.2014.12.027 1550-7289/r 2015 American Society for Metabolic and Bariatric Surgery. All rights reserved.
W. -J. Lee et al. / Surgery for Obesity and Related Diseases ] (2015) 00–00
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Table 1 Variables and point values used for the computation of the ABCD score* Variable
Age BMI (kg/m2) C-peptide (mmol/L) Duration of DM (yr)
Points on ABCD index 0
1
2
3
Z40 o27 o2 48
o40 27–34.9 2–2.9 4–8
35–41.9 3–4.9 1–3.9
Z42 Z5 o1
Abbreviations: ABCD ¼ age, body mass index, C-peptide level, and duration of diabetes; BMI ¼ body mass index; DM ¼ diabetes mellitus. * The cut-off values for the assignment of points are shown for each variable. The total possible value ranges from 0 to 10.
characteristics or other mechanisms. The authors previously reported the short-term results of LSG on nonobese T2 DM patients [12]. The study disclosed a 50% T2 DM remission rate, and patients with high C-peptide had a better remission rate. However, long-term data and a clinically useful predicting system are still lacking. To address these issues, this study reports the results of a retrospective analysis of the long-term effects of LSG on T2 DM patients and evaluates the possibility of using a specific diabetes surgery score (ABCD score) to help with patient selection [13]. Materials and methods Between January 2006 and July 2013, a total of 157 patients who had undergone laparoscopic sleeve gastrectomy (LSG) for poorly controlled T2 DM were recruited from Min-Sheng General Hospital in Taiwan. The study was approved by the human-research review board of the hospital, and all patients provided written informed consent. Diagnosis and classification of T2 DM was based on the criteria established by the American Diabetes Association [14]. The diabetic patients were eligible for the study if they had a body mass index (BMI) 425 kg/m2, with poorly controlled T2 DM after 6 months of medical treatment (HbA1c 47%), and had an acceptable operative risk. Patients were aged 18–67 years. The exclusion criteria were the presence of end-organ damage, pregnancy, and previous bariatric surgery. Participants were excluded if their C-peptide was o.9 ng/mL. Surgical technique The surgical technique of LSG has evolved over the years, with reinforcement suture and invagination of the stapler line, which was introduced in 2010 [15]. The authors have used the transumbilical 2-site modified single incision laparoscopic surgery technique for all LSG since 2012 [16]. Important surgical techniques were briefly described. All procedures were completed laparoscopically. Three skin incisions were placed at 2 sites of the abdomen, including 2 incisions along the fold of umbilicus and 1 incision at left lateral abdominal wall. A liver retractor was inserted
through a subxiphoid puncture to expose the angle of His. The greater omentum and short gastric arteries were devascularized starting 4 cm from pylorus to the angle of His. Large fat pads of Belsey at angle of His were dissected to provide a clean field for fundus resection. Vertical transection of the stomach was accomplished with 5–6 firings of a 60-mm linear staple using the orogastric tube size 36 Fr as calibrator. After gastric resection, the long gastric remnant stapler line was invaginated with 3–0 Vicryl suture to prevent leakage and hemorrhage. The gastric tube is then fixed to the posterior peritoneal tissue to prevent gastric volvulus. No intraoperative leak test was used. Drain was not routinely used. The resected stomach was extracted thorough the umbilical incision after dilation without using an endobag. The fascial defect was closed with Vicryl suture or plugged with absorbable gauze [17]. Age, BMI, C-peptide, and duration of T2 DM (ABCD) score The ABCD Diabetes Surgery Score was previously reported [13]. The score system consisted of 4 variables of independent predictors of T2 DM remission: patient age, BMI, C-peptide level, and duration of diabetes. A 4-point score, ranging from 0 (lowest value) to 3 (maximal value), was given to BMI, C-peptide, and duration of diabetes according to analysis. For age, only a 1-point score was given. The cut-off value for each point was slightly modified from the original one after further analysis Table 2 Comparison of clinical data before and after LSG
BMI (kg/m2) Waist (cm) Weight loss (%) SBP (mm Hg) DBP (mm Hg) Glucose (mg/dL) Total cholesterol (mg/dL) Triglyceride (mg/dL) LDL (mg /dL) HbA1c % C-peptide (ng/ mL) HOMA ALT, U/L Hemoglobin, g/dL Iron, ug/dL Calcium, mg/dL Serum albumin, g/dL
Before (n ¼ 85) Mean (SD) RYG
After (n ¼ 85) Mean (SD)
P
39.0 (7.4) 117.4 (16.9)
28.5 (5.4) 90.4 (11.0) 26.5% 122.9 (16.0) 76.7 (13.2) 102.4 (34) 102.4 (34)
o.001* o.001* o.001* o.001* o.001* o.001*
214.7 (116.1)
103.1 (39.2)
o.001*
127.8 (34.5) 8.1 (1.7) 4.9 (2.6)
126.5 (34.7) 6.1 (1.1) 2.2 (1.2)
.394 o.001* o.001*
139.8 87.5 154.6 200.0
8.9 57.5 14.5 89.2 9.1 4.4
(16.1) (12.4) (76.2) (45.3)
(10.0) (42.1) (1.8) (47.8) (.9) (.3)
1.5 19.4 13.6 86.9 9.1 4.2
(1.3) (2.2) (2.2) (40.4) (.4) (.5)
o.001* o.001* .002* .497 .372 .003*
Abbreviations: LSG ¼ laparoscopic sleeve gastrectomy; BMI ¼ body mass index; SBP ¼ systolic blood pressure; DBP ¼ diastolic blood pressure; LDL ¼ low density lipoprotein cholesterol, HOMA ¼ homeostasis model assessment; ALT ¼ alanine aminotransferase. * P o .05.
Sleev Gastrectomy and ABCD Score / Surgery for Obesity and Related Diseases ] (2015) 00–00
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[18,19]. The modified score cut-off values are defined in Table 1. The cut-off value for BMI was lowered from 30 to 27 kg/m2. The duration of T2 DM cut-off value was lowered to 1 year, and the C-peptide level was elevated to 2 ng/mL. The points for each variable were added, so that the total ABCD score ranged from 0 to 10 points.
the use of t test for independent samples. To evaluate the capacity of the ABCD score to predict success, the remission rate was evaluated according to separate score of the ABCD index. A 2-sided P value of .05 was considered statistically significant.
Study protocol
Results
In the cohort, T2 DM patients were evaluated by the multidisciplinary team before surgery after enrollment and were seen every 3–6 months for at least 1 year, then annually. The patient and family were contacted for the medical records if the patient failed to return for appointments. Complete remission of T2 DM was defined as an HbA1c value o6% without the use of oral hypoglycemic or insulin, and partial remission was defined as an HbA1c value o6.5% [20]. Patients with HbA1c o7% after surgery were considered to be improved. The remission rate was evaluated using the ABCD score. Statistical analysis All statistical analyses were performed using SPSS version 12.01 (SPSS Inc, Chicago, IL), with baseline comparison made using χ2 tests and 2-sample t tests. Continuous variables were expressed as mean (standard deviation). The differences between remission and nonremission in pertinent characteristics were established with
The mean age of the patients was 41.9 ⫾ 10.9 years, and the mean BMI was 39.0 ⫾ 7.4 (range, 25–67) kg/m2. The mean HbA1c at baseline was 8.1% ⫾ 1.7%, and the duration of T2 DM was 2.7 ⫾ 3.1 years. All the operations were performed successfully with laparoscopic surgery. The mean operation time was 128.2 ⫾ 38.6 minutes, and the hospital stay was 3.3 ⫾ 2.4 days. Major complication happened in 3 (1.9%) patients, but no patient died. Of all the patients, 85 had 1-year follow-up and with complete data. Significant reductions had occurred in weight (weight loss 26.5% ⫾ 10.1%) at 12 months after LSG, and BMI decreased to 28.3 ⫾ 5.4 kg/m2. The mean HbA1c decreased from 8.1% ⫾ 1.7% to 6.1% ⫾ 1.1%. Complete T2 DM remission (HbA1c o6%) was achieved in 45 (52.9%) patients; another 18 (21.2%) had partial remission (HbA1c o6.5%), and 9 (10.6%) had improved (HbA1c o7%). Significant improvements were also found in the blood lipid profile, insulin resistance, and blood pressure after LSG (Table 2). The weight loss and HbA1c reduction through the 5 years is displayed in Fig. 1. The
Fig. 1. Five-year outcome. Abbreviations: BMI ¼ body mass index; WL ¼ weight loss; Preop ¼ preoperative.
W. -J. Lee et al. / Surgery for Obesity and Related Diseases ] (2015) 00–00
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Table 3 Characteristics of the 85 patients, according to whether their diabetes had complete remission (HbA1c o6%) after surgery
Age, yr Gender, female, n (%) BMI (kg/m2) Waist (cm) C-peptide (ng/mL) Duration of T2 DM (yr) HOMA-IR SBP (mm Hg) DBP (mm Hg) Glucose (mg/dL) Total cholesterol (mg/ dL) Triglyceride (mg/dL) Uric acid (mg/dL) AST (IU/L) ALT (IU/L) Albumin (gm/dL) Hb (gm/dL) Insulin (uIU/mL) HDL-C (mg/dL) HbA1c, % LDL (mg/dL) hsCRP WBC (/μL) ABCD score Weight loss, %
Remission (n ¼ 45) Mean (SD)
Nonremission (n ¼ 40) Mean (SD)
P
38.5 20 41.4 122.9 5.7 1.9 11.6 142.2 89.4 160.4 206.8
(9.0) (41.7) (7.9) (15.9) (3.2) (2.5) (14.3) (16.2) (13.7) (92.1) (51.1)
45.4 21 34.6 106.7 3.8 3.9 6.7 135.4 85.4 169.5 195.4
(10.0) (56.8) (5.4) (14.5) (1.6) (3.9) (6.6) (14.8) (8.9) (76.0) (45.4)
.001* .187 o.001* o.001* o.001* o.001* .028* .025* .062 .312 .143
226.1 7.5 42.2 69.1 4.3 14.9 28.5 40.7 7.8 133.3 1.6 8.8 7.3 31.7
(124.1) (1.9) (24.1) (49.6) (.4) (1.8) (24.7) (8.7) (1.5) (33.9) (.32) (2.1) (1.7) (7.6)
209.8 6.2 29.8 40 4.4 14.3 16.3 42.1 8.8 126.6 .9 7.6 5.2 20.0
(107.0) (1.7) (15.7) (23.0) (.4) (1.9) (11.4) (7.9) (1.9) (38.4) (.7) (2.2) (2.1) (7.9)
.262 .020* .004* .001* .132 .062 .004* .222 .008* .208 .005* .006* o.001* o.001*
Abbreviations: BMI ¼ body mass index; T2 DM ¼ type 2 diabetes mellitus; HOMA-IR ¼ homeostasis model assessment–insulin resistance; SBP ¼ systolic blood pressure; DBP ¼ diastolic blood pressure; AST ¼ aspartate aminotransferase; ALT ¼ alanine transaminase; HDL-C ¼ high-density lipoprotein cholesterol; LDL ¼ low-density lipoprotein; hsCRP ¼ high-sensitive C-reactive protein; WBC ¼ white blood cell; ABCD ¼ age, body mass index, C-peptide level, and duration of diabetes. * P o .05.
weight loss and HbA1c reduction decreased rapidly at first 6 months and remained stable up to 5 years. Table 3 shows the comparison of clinical parameters between those with completely remission of T2 DM and those without. Patients with complete remission were significantly younger, with higher BMI, wider waist, higher C-peptide, shorter duration of T2 DM, higher liver enzyme, higher insulin resistance, higher white blood cell count, and greater weight loss. Patients with complete T2 DM remission after surgery had a higher ABCD score than those without (7.3 ⫾ 1.7 versus 5.2 ⫾ 2.1, P o .05). T2 DM remission rate in subgroups of different clinical parameters are shown in Table 4. There was no remission in patients with BMI o27 and in patients with C-peptide o2 ng/mL. Table 5 shows the ABCD score as a predictor of remission after bariatric surgery. The remission rate of gastric bypass, previously reported by the authors [13], was added to Table 5 for comparison. Patients with a higher
ABCD score were also at a higher rate of success in T2 DM remission (from 0% in score 0 to 100% in score 10). There was no complete remissions of T2 DM in those receiving LSG with an ABCD score o4. Patients with ABCD scores 48 had nearly 100% remission rate. Patients receiving gastric bypass had a higher complete remission rate (66.3% versus 53.9%). The remission rate was also higher in the gastric bypass group at each different score.
Discussion This study confirmed LSG is a well-tolerated and effective weight reduction surgery. In this study, primary LSG resulted in an average of 26.5% weight loss at 1 year and stabilized up to 5 years. The nutritional change after LSG is also minimal. This result concurs with recent publications, which reported 425% weight loss in longterm results [9,10,21]. However, remission of T2 DM after LSG varied. The 52.9% complete T2 DM remission rate at 1 year after LSG is lower than the 80% remission rate after gastric bypass [12,22,23] but compatible with some previous reports [10–12,23]. This study has found that a simple grading system, the ABCD score, can be used for patient selection in considering using LSG as a surgical therapy for T2 DM patients. The authors devised the Diabetes Surgery Score, or ABCD score, and validated its use by showing that it is a good predictor of the success after gastric bypass surgery for T2 DM treatment [13]. The ABCD score is useful Table 4 T2 DM remission rate according to different clinical factors No. of patients
Remission (HbA1c o6%) rate
P
o27 27– 34.9 35–42 Z42 o40 Z40 Female Male o1 1–3.9 4–8 48 o2
2 27
0% 29.6%
o.001*
34 22 40 45 41 44 21 42 13 8 5
64.7% 81.8% 75.0% 42.4% 48.8% 70.0% 85.7% 47.6% 53.8% 25.0% 0%
2–2.9 3–4.9 Z5 o.9 .9–1.0 41.0
13 33 34 13 46 26
61.5% 45.5% 94.1% 46.2% 52.2% 69.2%
Factors BMI (kg/m2)
Age (yr) Gender Duration (yr)
C-peptide (ng/ mL)
Waist/hip ratio
.016* .011* .044*
.115
.432
Abbreviations: T2 DM ¼ type 2 diabetes mellitus; BMI ¼ body mass index. * P o .05.
Sleev Gastrectomy and ABCD Score / Surgery for Obesity and Related Diseases ] (2015) 00–00
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Table 5 T2 DM remission rate for each ABCD score ABCD score
Patient no.
Complete remission (HbA1c o6.0%)
Partial remission (HbA1c o6.5%)
Improved (HbA1c o7%)
Complete remission (HbA1c o6.0%) in gastric bypass (n ¼ 63) [13]
0 1 2 3 4 5 6 7 8 9 10 Overall
0 3 1 3 10 7 20 11 14 10 5 85
0 0 0 0 3 (30%) 5 (71.4%) 9 (45%) 5 (45.4%) 11 (78.6%) 9 (90%) 45 (100%) 45 (52.9%)
0 0 0 1 (33.3%) 5 (50%) 6 (85.7%) 16 (80%) 7 (63.6%) 13 (92.8%) 10 (100%) 5 (100%) 63 (74.1%)
0 0 0 1 (33.3%) 9 (90%) 6 (85.7%) 19 (95%) 8 (72.7%) 14 (100%) 10 (100%) 5 (100%) 72 (84.7%)
33% 33% 43% 46% 41% 57% 83% 87% 100% 100% 100% 65.3%
Abbreviations: T2 DM ¼ type 2 diabetes mellitus; ABCD ¼ age, body mass index, C-peptide level, and duration of diabetes; HOMA ¼ homeostasis model assessment.
because it includes 1 domain that quantifies the degree of obesity (BMI), 1 that captures the insulin secretion capacity (C-peptide), 1 that reflects the nature course and deterioration of the pancreatic B-cell function (duration), and 1 that is a general reserve of the physiologic function (age). In Tables 3 and 4, each variable had good prediction power on T2 DM remission. Taken together, the ABCD score can be a very useful tool for patient selection. Although the original score system was developed in patients receiving gastric bypass surgery, this study has confirmed that this system is also applicable in patients receiving LSG. However, the remission rate after LSG was lower than after gastric bypass at each ABCD score. The authors would only recommend LSG for T2 DM for patients with an ABCD 44. The ABCD score can help in clinical practice for the choice of surgical procedure for T2 DM treatment. Studies have reported that some patients who had T2 DM remission after surgery experienced a recurrence of their disease over time [4,24,25]. DiGiorgi et al. have reported that beyond 3 years after gastric bypass, 24% of patients with initial remission of their T2 DM had reemergence of diabetes [24]. The recurrence of T2 DM was usually associated with weight regain and longer duration of T2 DM [25]. Therefore, the patients receiving metabolic surgery for their T2 DM required long-term follow-up and education for lifestyle modification to prevent weight regain. In patients with T2 DM recurrence due to weight regain, a revision surgery with duodenum exclusion may be required [26]. The mechanism of T2 DM remission after LSG is intrigue and complex [27]. Although LSG did not bypass the hormonally active foregut, LSG was still regarded as a metabolic surgery because LSG had the food stimulation of the hind-gut effect, including the rapid serge of glucagon-like peptide-1 (GLP-1) and peptide YY (PYY) after meal [28,29]. However, durable weight loss with associated decrease of insulin resistance is still the cornerstone of T2 DM remission after surgery [4,18,19]. In the present study, a dramatic
reduction of insulin resistance measured by HOMA was found and associated with a significant weight loss after LSG. The present study had some limitations. First, the case number in this study was relative small and precluded a more complicated statistical analysis. When applying this score in lower BMI patients, one must carefully consider small numbers in a particular group. However, this study has found that the ABCD score is still a practical tool for predicting the success of T2 DM remission after LSG. Second, the followup time is not long enough in this study. Without long-term follow-up, the predictive power of the ABCD score on prolonged T2 DM remission after LSG metabolic surgery is uncertain. Data for up to 10 years are needed to confirm the predictive power of this scoring system. Conclusions LSG is an effective surgical therapy for obese T2 DM patients. ABCD score, a simple multidimensional grading system, can predict the success of T2 DM treatment by LSG. Disclosures The authors have no commercial associations that might be a conflict of interest in relation to this article. References [1] Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004;27:1047–53. [2] Xu Y, Wang L, He J, et al. Prevalence and control of diabetes in Chinese adults. JAMA 2013;310:948–59. [3] Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg 2003;238:467–85. [4] Sjöström L, Lindroos AK, Peltonen M, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. New Engl J Med 2004;351:2683–93.
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[5] Buchwald H, Avidor Y, Braunwald E, et al. Bariatric surgery: a systematic review and meta-analysis. JAMA 2004;292:1724–37. [6] Lomanto D, Lee WJ, Goel R, et al. Bariatric surgery in Asia in the last 5 years (2005–2009). Obes Surg 2012;22:502–6. [7] Buchwald H, Oien DM. Metabolic/bariatric surgery worldwide 2011. Obes Surg 2013;23:427–36. [8] Todkar JS, Shah SS, Shah PS, Gangwani J. Long-term effects of laparoscopic sleeve gastrectomy in morbidly obese subjects with type 2 diabetes mellitus. Surg Obes Relat Dis 2010;6:142–5. [9] Peterli R, Borbély Y, Kern B, et al. Early results of the Swiss Multicenter Bypass or Sleeve Study (SM-BOSS): a prospective randomized trial comparing laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass 2013;258:690–5. [10] Rosenthal R, Li X, Samuel S, Martinez P, Zheng C. Effects of sleeve gastrectomy on patients with diabetes mellitus. Surg Obes Relat Dis 2009;5:429–34. [11] Lee WJ, Ser KH, Chong K, et al. Laparoscopic sleeve gastrectomy for diabetes treatment in nonmorbidly obese patients: efficacy and change of insulin secretion. Surgery 2010;147:664–9. [12] Schauer PR, Bhatt DL, Kirwan JP, et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N Engl J Med 2014;370:2002–13. [13] 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. [14] American Diabetes Association. Screening for type 2 diabetes. Diabetes Care 2004;27(Suppl 1):S11–4. [15] Ser KH, Lee WJ, Lee YC, Chen JC, Su YH, Chen SC. Experience in laparoscopic sleeve gastrectomy for morbidly obese Taiwanese: staple-line reinforcement is important for preventing leakage. Surg Endosc 2010;24:2253–9. [16] Lee WJ, Chen JC, Yao WC, Taou JJ, Lee YC, Ser KH. Transumbilical 2-site laparoscopic Roux-en-Y gastric bypass: initial results of 100 cases and comparison with traditional laparoscopic technique. Surg Obes Relat Dis 2012;8:208–13. [17] Chiu CC, Lee WJ, Wang W, Wei PL, Huang MT. Prevention of trocar-wound hernia in laparoscopic bariatric operations. Obes Surg 2006;16:913–8.
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Original article
Laparoscopic sleeve gastrectomy for type 2 diabetes mellitus: predicting the success by ABCD score Wei-Jei Lee, M.D., Ph.D.a,*, Abdullah Almulaifi, M.D.a, Ju Juin Tsou, R.N.a, Kong-Han Ser, M.D.a, Yi-Chih Lee, Ph.D.b, Shu-Chun Chen, R.N.a b
a Department of Surgery, Min-Sheng General Hospital, Taoyuan, Taiwan, Republic of China Department of International Business, Chien Hsin University of Science and Technology, Taoyuan, Taiwan, Republic of China Received October 31, 2014; accepted December 23, 2014
Abstract
Background: Laparoscopic sleeve gastrectomy (LSG) is becoming a primary bariatric surgery for obesity and related diseases. This study presents the outcome of LSG with regard to the remission of type 2 diabetes mellitus (T2 DM) and the usefulness of a grading system to categorize and predict outcome of T2 DM remission. Methods: A total of 157 patients with T2 DM (82 women and 75 men) with morbid obesity (mean body mass index 39.0 ⫾ 7.4 kg/m2) who underwent LSG from 2006 to 2013 were selected for the present study. The ABCD score is composed of the patient’s age, body mass index, C-peptide level, and duration of T2 DM (yr). The remission of T2 DM after LSG was evaluated using the ABCD score. Results: At 12 months after surgery, 85 of the patients had complete follow-up data. The weight loss was 26.5% and the mean HbA1c decreased from 8.1% to 6.1%. A significant number of patients had improvement in their glycemic control, including 45 (52.9%) patients who had complete remission (HbA1c o6.0%), another 18 (21.2%) who had partial remission (HbA1c o6.5%), and 9 (10.6%) who improved (HbA1c o7%). Patients who had T2 DM remission after surgery had a higher ABCD score than those who did not (7.3 ⫾ 1.7 versus 5.2 ⫾ 2.1, P o .05). Patients with a higher ABCD score were also at a higher rate of success in T2 DM remission (from 0% in score 0 to 100% in score 10). Conclusion: LSG is an effective and well-tolerated procedure for achieving weight loss and T2 DM remission. The ABCD score, a simple multidimensional grading system, can predict the success of T2 DM treatment by LSG. (Surg Obes Relat Dis 2015;]:00–00.) r 2015 American Society for Metabolic and Bariatric Surgery. All rights reserved.
Keywords:
Type 2 diabetes mellitus; Sleeve gastrectomy; ABCD score
Type 2 diabetes mellitus (T2 DM) affects more than 300 million people worldwide, and more than 60% of them are in Asia [1,2]. Bariatric surgery has been proven to be very successful in treating not only morbid obesity but also obesity-associated T2 DM [3–5]. Among all the bariatric * Correspondence: Wei-Jei Lee, M.D., Ph.D., Department of Surgery, Min-Sheng General Hospital, No. 168, Ching-Kuo Road, Taoyuan, Taiwan, Republic of China. E-mail: [email protected]
procedures, laparoscopic sleeve gastrectomy (LSG) has been gaining popularity as a stand-alone bariatric surgery worldwide despite the paucity of long-term outcome data [6,7]. However, the data about T2 DM remission after LSG is controversial. Some studies have reported very good results [8,9], and other studies have reported limited efficacy [10–12]. A possible explanation for this is that the patient characteristics might be different between these studies. It is also uncertain if the widely varied remission rates between the studies of LSG are related to patient
http://dx.doi.org/10.1016/j.soard.2014.12.027 1550-7289/r 2015 American Society for Metabolic and Bariatric Surgery. All rights reserved.
W. -J. Lee et al. / Surgery for Obesity and Related Diseases ] (2015) 00–00
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Table 1 Variables and point values used for the computation of the ABCD score* Variable
Age BMI (kg/m2) C-peptide (mmol/L) Duration of DM (yr)
Points on ABCD index 0
1
2
3
Z40 o27 o2 48
o40 27–34.9 2–2.9 4–8
35–41.9 3–4.9 1–3.9
Z42 Z5 o1
Abbreviations: ABCD ¼ age, body mass index, C-peptide level, and duration of diabetes; BMI ¼ body mass index; DM ¼ diabetes mellitus. * The cut-off values for the assignment of points are shown for each variable. The total possible value ranges from 0 to 10.
characteristics or other mechanisms. The authors previously reported the short-term results of LSG on nonobese T2 DM patients [12]. The study disclosed a 50% T2 DM remission rate, and patients with high C-peptide had a better remission rate. However, long-term data and a clinically useful predicting system are still lacking. To address these issues, this study reports the results of a retrospective analysis of the long-term effects of LSG on T2 DM patients and evaluates the possibility of using a specific diabetes surgery score (ABCD score) to help with patient selection [13]. Materials and methods Between January 2006 and July 2013, a total of 157 patients who had undergone laparoscopic sleeve gastrectomy (LSG) for poorly controlled T2 DM were recruited from Min-Sheng General Hospital in Taiwan. The study was approved by the human-research review board of the hospital, and all patients provided written informed consent. Diagnosis and classification of T2 DM was based on the criteria established by the American Diabetes Association [14]. The diabetic patients were eligible for the study if they had a body mass index (BMI) 425 kg/m2, with poorly controlled T2 DM after 6 months of medical treatment (HbA1c 47%), and had an acceptable operative risk. Patients were aged 18–67 years. The exclusion criteria were the presence of end-organ damage, pregnancy, and previous bariatric surgery. Participants were excluded if their C-peptide was o.9 ng/mL. Surgical technique The surgical technique of LSG has evolved over the years, with reinforcement suture and invagination of the stapler line, which was introduced in 2010 [15]. The authors have used the transumbilical 2-site modified single incision laparoscopic surgery technique for all LSG since 2012 [16]. Important surgical techniques were briefly described. All procedures were completed laparoscopically. Three skin incisions were placed at 2 sites of the abdomen, including 2 incisions along the fold of umbilicus and 1 incision at left lateral abdominal wall. A liver retractor was inserted
through a subxiphoid puncture to expose the angle of His. The greater omentum and short gastric arteries were devascularized starting 4 cm from pylorus to the angle of His. Large fat pads of Belsey at angle of His were dissected to provide a clean field for fundus resection. Vertical transection of the stomach was accomplished with 5–6 firings of a 60-mm linear staple using the orogastric tube size 36 Fr as calibrator. After gastric resection, the long gastric remnant stapler line was invaginated with 3–0 Vicryl suture to prevent leakage and hemorrhage. The gastric tube is then fixed to the posterior peritoneal tissue to prevent gastric volvulus. No intraoperative leak test was used. Drain was not routinely used. The resected stomach was extracted thorough the umbilical incision after dilation without using an endobag. The fascial defect was closed with Vicryl suture or plugged with absorbable gauze [17]. Age, BMI, C-peptide, and duration of T2 DM (ABCD) score The ABCD Diabetes Surgery Score was previously reported [13]. The score system consisted of 4 variables of independent predictors of T2 DM remission: patient age, BMI, C-peptide level, and duration of diabetes. A 4-point score, ranging from 0 (lowest value) to 3 (maximal value), was given to BMI, C-peptide, and duration of diabetes according to analysis. For age, only a 1-point score was given. The cut-off value for each point was slightly modified from the original one after further analysis Table 2 Comparison of clinical data before and after LSG
BMI (kg/m2) Waist (cm) Weight loss (%) SBP (mm Hg) DBP (mm Hg) Glucose (mg/dL) Total cholesterol (mg/dL) Triglyceride (mg/dL) LDL (mg /dL) HbA1c % C-peptide (ng/ mL) HOMA ALT, U/L Hemoglobin, g/dL Iron, ug/dL Calcium, mg/dL Serum albumin, g/dL
Before (n ¼ 85) Mean (SD) RYG
After (n ¼ 85) Mean (SD)
P
39.0 (7.4) 117.4 (16.9)
28.5 (5.4) 90.4 (11.0) 26.5% 122.9 (16.0) 76.7 (13.2) 102.4 (34) 102.4 (34)
o.001* o.001* o.001* o.001* o.001* o.001*
214.7 (116.1)
103.1 (39.2)
o.001*
127.8 (34.5) 8.1 (1.7) 4.9 (2.6)
126.5 (34.7) 6.1 (1.1) 2.2 (1.2)
.394 o.001* o.001*
139.8 87.5 154.6 200.0
8.9 57.5 14.5 89.2 9.1 4.4
(16.1) (12.4) (76.2) (45.3)
(10.0) (42.1) (1.8) (47.8) (.9) (.3)
1.5 19.4 13.6 86.9 9.1 4.2
(1.3) (2.2) (2.2) (40.4) (.4) (.5)
o.001* o.001* .002* .497 .372 .003*
Abbreviations: LSG ¼ laparoscopic sleeve gastrectomy; BMI ¼ body mass index; SBP ¼ systolic blood pressure; DBP ¼ diastolic blood pressure; LDL ¼ low density lipoprotein cholesterol, HOMA ¼ homeostasis model assessment; ALT ¼ alanine aminotransferase. * P o .05.
Sleev Gastrectomy and ABCD Score / Surgery for Obesity and Related Diseases ] (2015) 00–00
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[18,19]. The modified score cut-off values are defined in Table 1. The cut-off value for BMI was lowered from 30 to 27 kg/m2. The duration of T2 DM cut-off value was lowered to 1 year, and the C-peptide level was elevated to 2 ng/mL. The points for each variable were added, so that the total ABCD score ranged from 0 to 10 points.
the use of t test for independent samples. To evaluate the capacity of the ABCD score to predict success, the remission rate was evaluated according to separate score of the ABCD index. A 2-sided P value of .05 was considered statistically significant.
Study protocol
Results
In the cohort, T2 DM patients were evaluated by the multidisciplinary team before surgery after enrollment and were seen every 3–6 months for at least 1 year, then annually. The patient and family were contacted for the medical records if the patient failed to return for appointments. Complete remission of T2 DM was defined as an HbA1c value o6% without the use of oral hypoglycemic or insulin, and partial remission was defined as an HbA1c value o6.5% [20]. Patients with HbA1c o7% after surgery were considered to be improved. The remission rate was evaluated using the ABCD score. Statistical analysis All statistical analyses were performed using SPSS version 12.01 (SPSS Inc, Chicago, IL), with baseline comparison made using χ2 tests and 2-sample t tests. Continuous variables were expressed as mean (standard deviation). The differences between remission and nonremission in pertinent characteristics were established with
The mean age of the patients was 41.9 ⫾ 10.9 years, and the mean BMI was 39.0 ⫾ 7.4 (range, 25–67) kg/m2. The mean HbA1c at baseline was 8.1% ⫾ 1.7%, and the duration of T2 DM was 2.7 ⫾ 3.1 years. All the operations were performed successfully with laparoscopic surgery. The mean operation time was 128.2 ⫾ 38.6 minutes, and the hospital stay was 3.3 ⫾ 2.4 days. Major complication happened in 3 (1.9%) patients, but no patient died. Of all the patients, 85 had 1-year follow-up and with complete data. Significant reductions had occurred in weight (weight loss 26.5% ⫾ 10.1%) at 12 months after LSG, and BMI decreased to 28.3 ⫾ 5.4 kg/m2. The mean HbA1c decreased from 8.1% ⫾ 1.7% to 6.1% ⫾ 1.1%. Complete T2 DM remission (HbA1c o6%) was achieved in 45 (52.9%) patients; another 18 (21.2%) had partial remission (HbA1c o6.5%), and 9 (10.6%) had improved (HbA1c o7%). Significant improvements were also found in the blood lipid profile, insulin resistance, and blood pressure after LSG (Table 2). The weight loss and HbA1c reduction through the 5 years is displayed in Fig. 1. The
Fig. 1. Five-year outcome. Abbreviations: BMI ¼ body mass index; WL ¼ weight loss; Preop ¼ preoperative.
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Table 3 Characteristics of the 85 patients, according to whether their diabetes had complete remission (HbA1c o6%) after surgery
Age, yr Gender, female, n (%) BMI (kg/m2) Waist (cm) C-peptide (ng/mL) Duration of T2 DM (yr) HOMA-IR SBP (mm Hg) DBP (mm Hg) Glucose (mg/dL) Total cholesterol (mg/ dL) Triglyceride (mg/dL) Uric acid (mg/dL) AST (IU/L) ALT (IU/L) Albumin (gm/dL) Hb (gm/dL) Insulin (uIU/mL) HDL-C (mg/dL) HbA1c, % LDL (mg/dL) hsCRP WBC (/μL) ABCD score Weight loss, %
Remission (n ¼ 45) Mean (SD)
Nonremission (n ¼ 40) Mean (SD)
P
38.5 20 41.4 122.9 5.7 1.9 11.6 142.2 89.4 160.4 206.8
(9.0) (41.7) (7.9) (15.9) (3.2) (2.5) (14.3) (16.2) (13.7) (92.1) (51.1)
45.4 21 34.6 106.7 3.8 3.9 6.7 135.4 85.4 169.5 195.4
(10.0) (56.8) (5.4) (14.5) (1.6) (3.9) (6.6) (14.8) (8.9) (76.0) (45.4)
.001* .187 o.001* o.001* o.001* o.001* .028* .025* .062 .312 .143
226.1 7.5 42.2 69.1 4.3 14.9 28.5 40.7 7.8 133.3 1.6 8.8 7.3 31.7
(124.1) (1.9) (24.1) (49.6) (.4) (1.8) (24.7) (8.7) (1.5) (33.9) (.32) (2.1) (1.7) (7.6)
209.8 6.2 29.8 40 4.4 14.3 16.3 42.1 8.8 126.6 .9 7.6 5.2 20.0
(107.0) (1.7) (15.7) (23.0) (.4) (1.9) (11.4) (7.9) (1.9) (38.4) (.7) (2.2) (2.1) (7.9)
.262 .020* .004* .001* .132 .062 .004* .222 .008* .208 .005* .006* o.001* o.001*
Abbreviations: BMI ¼ body mass index; T2 DM ¼ type 2 diabetes mellitus; HOMA-IR ¼ homeostasis model assessment–insulin resistance; SBP ¼ systolic blood pressure; DBP ¼ diastolic blood pressure; AST ¼ aspartate aminotransferase; ALT ¼ alanine transaminase; HDL-C ¼ high-density lipoprotein cholesterol; LDL ¼ low-density lipoprotein; hsCRP ¼ high-sensitive C-reactive protein; WBC ¼ white blood cell; ABCD ¼ age, body mass index, C-peptide level, and duration of diabetes. * P o .05.
weight loss and HbA1c reduction decreased rapidly at first 6 months and remained stable up to 5 years. Table 3 shows the comparison of clinical parameters between those with completely remission of T2 DM and those without. Patients with complete remission were significantly younger, with higher BMI, wider waist, higher C-peptide, shorter duration of T2 DM, higher liver enzyme, higher insulin resistance, higher white blood cell count, and greater weight loss. Patients with complete T2 DM remission after surgery had a higher ABCD score than those without (7.3 ⫾ 1.7 versus 5.2 ⫾ 2.1, P o .05). T2 DM remission rate in subgroups of different clinical parameters are shown in Table 4. There was no remission in patients with BMI o27 and in patients with C-peptide o2 ng/mL. Table 5 shows the ABCD score as a predictor of remission after bariatric surgery. The remission rate of gastric bypass, previously reported by the authors [13], was added to Table 5 for comparison. Patients with a higher
ABCD score were also at a higher rate of success in T2 DM remission (from 0% in score 0 to 100% in score 10). There was no complete remissions of T2 DM in those receiving LSG with an ABCD score o4. Patients with ABCD scores 48 had nearly 100% remission rate. Patients receiving gastric bypass had a higher complete remission rate (66.3% versus 53.9%). The remission rate was also higher in the gastric bypass group at each different score.
Discussion This study confirmed LSG is a well-tolerated and effective weight reduction surgery. In this study, primary LSG resulted in an average of 26.5% weight loss at 1 year and stabilized up to 5 years. The nutritional change after LSG is also minimal. This result concurs with recent publications, which reported 425% weight loss in longterm results [9,10,21]. However, remission of T2 DM after LSG varied. The 52.9% complete T2 DM remission rate at 1 year after LSG is lower than the 80% remission rate after gastric bypass [12,22,23] but compatible with some previous reports [10–12,23]. This study has found that a simple grading system, the ABCD score, can be used for patient selection in considering using LSG as a surgical therapy for T2 DM patients. The authors devised the Diabetes Surgery Score, or ABCD score, and validated its use by showing that it is a good predictor of the success after gastric bypass surgery for T2 DM treatment [13]. The ABCD score is useful Table 4 T2 DM remission rate according to different clinical factors No. of patients
Remission (HbA1c o6%) rate
P
o27 27– 34.9 35–42 Z42 o40 Z40 Female Male o1 1–3.9 4–8 48 o2
2 27
0% 29.6%
o.001*
34 22 40 45 41 44 21 42 13 8 5
64.7% 81.8% 75.0% 42.4% 48.8% 70.0% 85.7% 47.6% 53.8% 25.0% 0%
2–2.9 3–4.9 Z5 o.9 .9–1.0 41.0
13 33 34 13 46 26
61.5% 45.5% 94.1% 46.2% 52.2% 69.2%
Factors BMI (kg/m2)
Age (yr) Gender Duration (yr)
C-peptide (ng/ mL)
Waist/hip ratio
.016* .011* .044*
.115
.432
Abbreviations: T2 DM ¼ type 2 diabetes mellitus; BMI ¼ body mass index. * P o .05.
Sleev Gastrectomy and ABCD Score / Surgery for Obesity and Related Diseases ] (2015) 00–00
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Table 5 T2 DM remission rate for each ABCD score ABCD score
Patient no.
Complete remission (HbA1c o6.0%)
Partial remission (HbA1c o6.5%)
Improved (HbA1c o7%)
Complete remission (HbA1c o6.0%) in gastric bypass (n ¼ 63) [13]
0 1 2 3 4 5 6 7 8 9 10 Overall
0 3 1 3 10 7 20 11 14 10 5 85
0 0 0 0 3 (30%) 5 (71.4%) 9 (45%) 5 (45.4%) 11 (78.6%) 9 (90%) 45 (100%) 45 (52.9%)
0 0 0 1 (33.3%) 5 (50%) 6 (85.7%) 16 (80%) 7 (63.6%) 13 (92.8%) 10 (100%) 5 (100%) 63 (74.1%)
0 0 0 1 (33.3%) 9 (90%) 6 (85.7%) 19 (95%) 8 (72.7%) 14 (100%) 10 (100%) 5 (100%) 72 (84.7%)
33% 33% 43% 46% 41% 57% 83% 87% 100% 100% 100% 65.3%
Abbreviations: T2 DM ¼ type 2 diabetes mellitus; ABCD ¼ age, body mass index, C-peptide level, and duration of diabetes; HOMA ¼ homeostasis model assessment.
because it includes 1 domain that quantifies the degree of obesity (BMI), 1 that captures the insulin secretion capacity (C-peptide), 1 that reflects the nature course and deterioration of the pancreatic B-cell function (duration), and 1 that is a general reserve of the physiologic function (age). In Tables 3 and 4, each variable had good prediction power on T2 DM remission. Taken together, the ABCD score can be a very useful tool for patient selection. Although the original score system was developed in patients receiving gastric bypass surgery, this study has confirmed that this system is also applicable in patients receiving LSG. However, the remission rate after LSG was lower than after gastric bypass at each ABCD score. The authors would only recommend LSG for T2 DM for patients with an ABCD 44. The ABCD score can help in clinical practice for the choice of surgical procedure for T2 DM treatment. Studies have reported that some patients who had T2 DM remission after surgery experienced a recurrence of their disease over time [4,24,25]. DiGiorgi et al. have reported that beyond 3 years after gastric bypass, 24% of patients with initial remission of their T2 DM had reemergence of diabetes [24]. The recurrence of T2 DM was usually associated with weight regain and longer duration of T2 DM [25]. Therefore, the patients receiving metabolic surgery for their T2 DM required long-term follow-up and education for lifestyle modification to prevent weight regain. In patients with T2 DM recurrence due to weight regain, a revision surgery with duodenum exclusion may be required [26]. The mechanism of T2 DM remission after LSG is intrigue and complex [27]. Although LSG did not bypass the hormonally active foregut, LSG was still regarded as a metabolic surgery because LSG had the food stimulation of the hind-gut effect, including the rapid serge of glucagon-like peptide-1 (GLP-1) and peptide YY (PYY) after meal [28,29]. However, durable weight loss with associated decrease of insulin resistance is still the cornerstone of T2 DM remission after surgery [4,18,19]. In the present study, a dramatic
reduction of insulin resistance measured by HOMA was found and associated with a significant weight loss after LSG. The present study had some limitations. First, the case number in this study was relative small and precluded a more complicated statistical analysis. When applying this score in lower BMI patients, one must carefully consider small numbers in a particular group. However, this study has found that the ABCD score is still a practical tool for predicting the success of T2 DM remission after LSG. Second, the followup time is not long enough in this study. Without long-term follow-up, the predictive power of the ABCD score on prolonged T2 DM remission after LSG metabolic surgery is uncertain. Data for up to 10 years are needed to confirm the predictive power of this scoring system. Conclusions LSG is an effective surgical therapy for obese T2 DM patients. ABCD score, a simple multidimensional grading system, can predict the success of T2 DM treatment by LSG. Disclosures The authors have no commercial associations that might be a conflict of interest in relation to this article. References [1] Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004;27:1047–53. [2] Xu Y, Wang L, He J, et al. Prevalence and control of diabetes in Chinese adults. JAMA 2013;310:948–59. [3] Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg 2003;238:467–85. [4] Sjöström L, Lindroos AK, Peltonen M, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. New Engl J Med 2004;351:2683–93.
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