Obese Patients with Type 2 Diabetes: Outcomes After Laparoscopic Sleeve Gastrectomy

Abstract

Background:

Bariatric surgery is superior to medical treatment for type 2 diabetes mellitus (T2DM) control in obese patients. Reports in the literature have been mainly based on Roux-en-Y gastric bypass (RYGB) or adjustable gastric band. The aim of this study was to analyze mid- and long-term metabolic results after laparoscopic sleeve gastrectomy (LSG).

Methods:

Obese patients with T2DM undergoing LSG were included in this study. Selection criteria for T2DM remission were: post-operatory fasting glucose (FG) level <100 mg/dL, and hemoglobin A1c (HbA1c) <6% without medication.

Results:

Between January 2009 and July 2016, 166 T2DM obese patients underwent LSG and completed ≥1 year follow-up. There were 101 women (60.8%; mean age 49.07 ± 12.8 years). Initial body mass index (BMI) was 46.44 ± 7.68 kg/m². Mean time since T2DM diagnosis was 5.95 years (1–28). Preoperative HbA1c was 7.53% ± 0.97%. Before LSG, 75.3% (n = 125) were receiving oral hypoglycemic agents, and 13.25% (n = 22) insulin. Mean follow-up was 65 ± 10 months. Complete T2DM remission was achieved in 78.3%, 76.2%, and 71.4% at 1, 3, and ≥5 years respectively; in the long term, 7.2% attained partial remission, 10% improved, and 11.4% experienced recurrence of the disease. Remission rate was significantly lower in patients under insulin therapy preoperatively, and in patients with T2DM diagnosed ≥5 years before consultation (P = .0004 and .0001, respectively).

Conclusions:

At mid- and long-term follow-up, T2DM control was satisfactory after LSG. Preoperative insulin therapy and T2DM duration ≥5 years were predictors of less favorable outcomes.

Introduction

Obesity and type 2 diabetes mellitus (T2DM) are severe chronic diseases, and they are usually associated with a complex metabolic disorder, increasing morbidity, and mortality risk. Lately, this situation has become a real problem for the public health worldwide. The International Diabetes Federation (IDF) informs that currently 1 in 11 adults has diabetes; this means that more than 425 million people are diagnosed with this disease. It has been estimated that this number will increase up to 693 million by 2045. Prevalence of T2DM and obesity in Argentina is between 9.8% and 20.8%, respectively, according to a recent Risks Factors National Survey.^1,2

Health care costs devoted to the treatment of this disease have exponentially increased during the last decade.³ Pharmacological treatment associated with lifestyle modification only changes discreetly glycemic control, but it does not achieve long-term treatment goals.^4–7

Since the last publications from Pories, bariatric surgery has been gaining field in the treatment of this disease.⁸ So far, the majority of publications addressing this issue reported encouraging results after Roux-en-Y gastric bypass (RYGB).^9–15

Laparoscopic sleeve gastrectomy (LSG) is a relatively novel surgery that has shown up now to good results in terms of weight loss and resolution/improvement of comorbidities with low postoperative complication rate.^16,17 Specifically, short- and mid-term results in regard to T2DM are promising, and they can be compared with those coming from other current techniques.^17–21

The goal of this study was to analyze the effect of LSG at 1, 3, and 5 years on obese patients with T2DM.

Materials and Methods

Obese patients with T2DM undergoing LSG at our institution were included in this study. Data were analyzed retrospectively from a prospectively collected database. Statistical analysis was performed using the SPSS 19.0 Statistics 2011 program.

The following parameters were evaluated: demographics, pre- and postoperative body mass index (BMI), percentage excess weight loss (%EWL), time since T2DM diagnosis, type of treatment received before surgery, outcomes after surgery (complete remission, partial remission, improvement, no change, and eventual recurrence of the disease), pre- and postoperative glycemia, and HbA1C.

For complete remission, the ASMBS, SOARD, and outcome reporting standards criteria were used.²²

(1)

Fasting glucose (FG) <100 mg/dL

(2)

HbA1c <6%

(3)

No pharmacologic treatment

Partial remission was considered when values of HbA1c were between 6% and 6.4% and FG between 100 and 125 mg/dL for at least 1 year, in the absence of pharmacologic treatment.²²

Improvement was defined as HbA1c and FG significantly reduced, although remission criteria were not reached or when medication requirements were reduced (discontinuation of insulin therapy or oral hypoglycemic drugs [OHD] or reduction to half dosage).²²

Recurrence was defined as HBA1c or glycemia within T2DM range (HbA1c ≥ 6.5% and FG ≥126 mg%) or need for medications after having reached complete or partial remission at any point after surgery.²²

Long-standing T2DM was considered when diagnosis had been done at least 5 years before consultation.²²

To homogenize follow-up length, short-term was defined as 1 year, mid-term as 3 years, and long term as ≥5 years.

Surgical technique

A 12-mm optical trocar was inserted (EXCEL^® Endopath, Ethicon Endosurgery, Cincinnati, OH) for the camera in the midline supraumbilical position under direct vision. Then, two 5-mm trocars were inserted, one on the left upper quadrant, and the other one on the right upper quadrant; a 10-mm trocar was introduced on the left flank. The Nathanson liver retractor was placed in the epigastrium. The short gastric vessels were all divided using the harmonic scalpel (Harmonic Ace^®, Ethicon Endosurgery). Dissection of the greater curvature of the stomach continued toward the left pillar of the crus. The gastric sleeve was calibrated with a 42 Fr bougie. Then, using between four and five linear staplers (Echelon 60, Ethicon Endosurgery) the stomach was divided vertically starting on the greater curvature about 4–6 cm above the pylorus parallel to the lesser curvature and from this position toward the angle of His. Black (4.2 mm), green (4.1 mm), gold (3.8 mm), or blue (3.5 mm) cartridges were chosen depending on the thickness of the stomach wall. Staple line was reinforced with running stitches of absorbable suture. The specimen was retrieved in a plastic bag. A multi-lumen drain was left along the staple line.

Results

Demographics and perioperative data

Between January 2009 and July 2016, 166 obese patients with T2DM underwent LSG at our institution. There were 101 women (61%; mean age 49 ± 12.8 years; range 26–69). Initial BMI was 46 ± 7.6 kg/m² (range 33–69). At 1, 3, and 5 years BMI was 31, 33, and 34 kg/m², while %EWL was 68%, 65%, and 53%. Changes in BMI and %EWL are shown in Figures 1 and 2.

FIG. 1.

BMI evolution at 1, 3, and 5 years. BMI, body mass index.

FIG. 2.

%EWL evolution at 1, 3, and 5 years. %EWL, percentage excess weight loss.

Time since T2DM diagnosis was 5.9 years (range 1–28). Operative time was 59 ± 11.5 minutes (range 38–130). Hospital stay was 2.1 days (range 2–5). Follow-up was 65 ± 10 months (range 12–84).

Medication usage

Before the operation, 75.3% (n = 125) of patients were only taking OHD; among them, 52.8% (n = 66) were receiving just one drug, 30.4% (n = 38) two drugs, 15.2% (n = 19) three drugs, and 1.6% (n = 2) four drugs. Of the remaining patients, 13.25% (n = 22) were on insulin therapy; within this last group, 31.8% (n = 7) were on insulin alone, and 68.2% (n = 15) on insulin and OHD. The remaining 11.45% (n = 19) did not receive any medication (Fig. 3).

FIG. 3.

Preoperative treatment. OHD, oral hypoglycemic agents.

Complications

Postoperative morbidity was 2.4% (n = 4). Three patients presented abdominal bleeding; they were managed conservatively, and they did not require blood transfusion. The remaining patient had an intra-abdominal collection, which was managed with percutaneous drainage and antibiotics. There were no conversions to open surgery, no reoperations, and no mortality in this series.

Postsurgical evolution of FG and HbA1c after LSG

Preoperative FG was 140.3 ± 29.3, and HbA1c 7.5% ± 0.9%. FG decreased significantly at 1, 3, and 5 years to 98, 108, and 108.5 mg/dL, respectively (P = .001). Similarly, HbA1c values dropped to 5.8%, 6.3%, and 6.3% at same periods of time (P = .001) (Figs. 4 and 5).

FIG. 4.

Evolution of glycemia after LSG. LSG, laparoscopic sleeve gastrectomy.

FIG. 5.

Evolution of HbA1c after LSG. HbA1C, glycated hemoglobin.

Short-term T2DM remission after LSG

Follow-up was achieved in all patients at 1 year. T2DM complete remission was observed in 78.3% (n = 130) of patients (Fig. 6). Then, the results were analyzed according to their preoperative treatment. Before the operation, 75.3% (n = 125) were on OHD. Complete remission was attained in 78.4% (n = 98) of these patients. In contrast, 13% (n = 22) were receiving insulin. Among those, 50% (n = 11) showed complete remission.

FIG. 6.

T2DM complete remission. T2DM, type 2 diabetes mellitus.

Outcomes were also compared according to time since T2DM diagnosis. At 1- year follow-up, all 166 patients were analyzed; 76 of them were diagnosed ≥5 years before consultation. Remission in this group was observed in 59% (n = 45) of them. The remaining 90 patients had shorter evolution (<5 years) of the disease. Remission was achieved in 81% (n = 73) of patients in the last group (P = .001).

Mid-term T2DM remission after LSG

Follow-up was completed in 59% (n = 98) of patients at 3 years; 75.5% (n = 74) showed complete remission (Fig. 6). Within this group, 86.7% (n = 85) were receiving OHD before the surgery. Remission was observed in 75% (n = 64) of them. We were able to contact all 13 patients who were under insulin therapy before LSG; 30.7% (n = 4) of them continued in complete remission, while 60.3% (n = 9) showed improvement.

T2DM remission at ≥5 years

Five-year follow-up was accomplished in 42% (n = 70) patients. Complete remission was attained in 71.4% (n = 50) of them. Partial remission was observed in 7.1% (n = 5), improvement in 10% (n = 7), while 11.4% (n = 8) experienced recurrence of the disease (Fig. 7).

FIG. 7.

T2DM status at 5-year follow-up after LSG. T2DM, type 2 diabetes mellitus.

Again, results were analyzed according to their preoperative treatment. Before the operation, 88.5% (n = 62) were on OHD. Complete remission was attained in 72.5% (n = 45) of these patients. In contrast, 11.5% (n = 8) were receiving insulin. Among those, only 37.5% (n = 3) showed complete remission (P = .004)

Also, outcomes were compared according to time since T2DM diagnosis at 5-year follow-up. Among the 70 patients available, 22 were diagnosed ≥5 years before consultation. Remission was seen in 40.9% (n = 9) of them. In the remaining 48 patients who had shorter evolution (<5 years) of the disease, a remission was observed in 70.8% (n = 34) (P = .001).

Recurrence

At ≥5 years, 11.4% (n = 8) of patients showed recurrence of the disease. Age was 49.7 ± 15.2 years (range 28–64), and disease duration was 8.1 ± 4.1 years (range 1–13). Preoperative BMI was 39.6 ± 5.82 kg/m², decreasing to 34.32 ± 4.17 kg/m² at 5-year follow-up; %EWL was 54.83 ± 15.2. Preoperative FG and HbA1c were 170 ± 56.9 mg/dL and 8.5% ± 2.1%, respectively. At 1 and 5 years, glycemia was 111 ± 18.2 and 129.4 ± 34 mg/dL, respectively. HbA1c at the same periods was 6.3% ± 0.6% and 6.7% ± 0.9%. Outcomes at 1, 3, and 5 years are shown in Table 1.

Table 1.

Evolution at 1, 3, and 5 Years in Patients Showing Recurrence

Variable	Patients with recurrence	Patients without recurrence	P
Age (years)	49.75 ± 15.2	48.53 ± 14.4	NS
Disease duration (years)	8.13 ± 4.1	5.75 ± 2.9	P = .0001
Preoperative BMI (kg/m²)	39.6 ± 5.82	43 ± 8.1 kg/m²	NS
Postoperative BMI at 5 years (kg/m²)	34.32 ± 4.17	32.55 ± 3.24	NS
%EWL at 5 years	54.83 ± 15.2	56.3 ± 14.98	NS
Fasting glucose before LSG (mg/dL)	170 ± 56.95	139.5 ± 25.4	P = .003
HbA1c before LSG (%)	8.56 ± 2.18	7.4 ± 0.85%	NS
Outcomes at 1-year follow-up (n = 166)	75% (n = 6) complete remission	79.5% (n = 124) complete remission
	25% (n = 2) improvement	9% (n = 16) partial remission
		9% (n = 14) improvement
		2.5 (n = 4) without changes
Outcomes at 3-year follow-up (n = 98)	25% (n = 2) complete remission	80% (n = 72) complete remission
	25% (n = 2) partial remission	8% (n = 7) partial remission
	25% (n = 2) improvement	8% (n = 7) improvement
	25% (n = 2) recurrence	4% (n = 4) without changes
Outcomes at 5-year follow-up (n = 70)	100% (n = 8) recurrence	81% (n = 50) complete remission
		8% (n = 5) partial remission
		11% (n = 7) improvement

BMI, body mass index; %EWL, percentage excess weight loss; HbA1c, glycated hemoglobin; LSG, laparoscopic sleeve gastrectomy.

At the time of recurrence, 87.5% (n = 7) were prescribed OHD, and only 1 patient (12.5%) went back on insulin therapy.

Outcomes on patients receiving insulin preoperatively

Out of all patients, 22 were on insulin therapy before LSG. Age was 53.5 ± 9.5 years (range 36–66), and T2DM duration was 10.68 ± 5.7 years (range 1–28). Pre- and postoperative BMI was 41.3 ± 5.12 kg/m² (range 38–54) and 34 ± 2.2 (range 28–40), respectively, and %EWL was 58.01% ± 3.5%. Preoperative glycemia and HbA1c were 124 ± 33.5 mg/dL and 7.1% ± 1.3%, respectively. At 1 and 5 years, glycemia was 114 ± 20.9 and 123 ± 30 mg/dL, respectively. HbA1c at the same periods was 6.3% ± 0.6% and 6.7% ± 0.9%. Outcomes of these patients at 1, 3, and 5 years are shown in Table 2.

Table 2.

Evolution at 1, 3, and 5 Years in Patients Receiving Insulin Preoperatively

Variable	Findings
Age (years)	53.5 ± 9.5
Disease duration (years)	10.68 ± 5.7
Preoperative BMI (kg/m²)	41.33 ± 5.12
Postoperative BMI (kg/m²)	34 ± 2.2
%EWL	58.01
Fasting glucose before LSG (mg/dL)	124 ± 33.5
HbA1c before LSG (%)	7.15 ± 1.3
Outcomes at 1-year follow-up	50% (n = 11) complete remission
Outcomes at 1-year follow-up	50% (n = 11) improvement
Outcomes at 3-year follow-up	30.7% (n = 4) complete remission
Outcomes at 3-year follow-up	60.3% (n = 9) improvement
Outcomes at 5-year follow-up	37.5% (n = 3) complete remission
	50% (n = 4) improvement
	12.5% (n = 1) recurrence

Discussion

Obesity and T2DM have shown a dramatic growth in prevalence. This problem demands immediate action from the governments, the health system, and the medical community.

Medical treatment including diet and lifestyle changes, plus pharmacologic treatment in some cases, could result in partial improvement in insulin resistance, T2DM, hypertension, and dyslipidemia, decreasing risk factors in this population.^4–6

In 2011, the IDF proposed surgery as an adequate treatment option for obese patients with T2DM who had poor metabolic control. They stated that surgical treatment would be a good option not only for obese patients with BMI ≥35 kg/m² and T2DM but also for those with BMI between 30 and 35 kg/m² when T2DM could not be controlled by medical treatment, especially in patients with a high risk of cardiovascular disease.⁹

The majority of publications that address long-term outcomes on obese patients and T2DM include mainly results after RYGB. So far, short- and mid-term T2DM remission reported was around 67–86%, while long-term remission was between 46% and 80%, RYGB being the standard of care for this group of patients.^10–15

In 2012, the American Society for Metabolic and Bariatric Surgery (ASMBS) accepted LSG as a primary surgery for the treatment of obesity. This technique has demonstrated several advantages over other current procedures. Lower morbidity and mortality rates, less invasiveness, lack of malabsorption, possibility of conversion to another procedure in case of failure, coupled with satisfactory mid-term results in terms of weight loss and resolution of comorbidities, represent contributing factors for choosing this technique over others.^16–21

Short-term T2DM remission after LSG

Regardless of the different definitions used for T2DM remission, short-term diabetes remission rates after LSG are high, being between 37% and 91%.^20,21,23,24 For instance, Gill et al. reported their results on 673 patients at 13.1 months, with an improvement/resolution rate of 93.1%.²³ In contrast, Schauer et al. reported 37% remission in 49 T2DM patients at 12 months. Preoperative HbA1C was 9.2 ± 1.5, duration of the disease 8.5 years, and 44% of them were on insulin therapy preoperatively.²⁴ The long-time standing of the disease, elevated HbA1C, and high percentage of patients on insulin therapy before the operation might explain the “relative” low remission rate if compared with other publications. In our series, 78.3% of patients achieved remission at 1-year follow-up.

Mid-term T2DM remission after LSG

According to literature, percentages vary from 24% to 94%.^25–28 Abbatini et al. observed a remission rate of 87.6% at 3 months, which was stable at around 84.6% at 36-month follow-up. The authors remarked that all 4 patients with no remission were either on high doses of insulin or had poor metabolic control before the operation or had been diabetic for ≥10 years.²⁵ Schauer et al. reported remission in 24% of patients at 3-year follow-up according to their primary goal, which was HbA1c ≤ 6.²⁸ In our group, complete remission at 3 years was observed in 76.2%.

Long-term T2DM remission after LSG

Long-term results were less frequently reported. The vast majority of publications exhibited decrease in LSG efficacy with time, although others showed remission rates above 50%, with variations between 11% and 85%.^25,29,30 Likewise, Schauer et al. found remission in 7 out of 47 patients (14.9%).²⁹ Duration of the disease (8.5 ± 4.8 years), high percentage of patients on insulin therapy before LSG (44%), and elevated preoperative HbA1c (9.5 ± 1.7) might serve as interpretation for the low remission rate at 5 years in this set of patients. Aminian et al. demonstrated a significant decrease in HbA1c, FG, and the usage of antidiabetic medication after LSG (P = <.001). Although long-term complete remission was seen in only 11%, partial remission in 15%, and improvement in 47%, this gave a number of 63% of patients with adequate diabetes control after LSG (HbA1c < 7%) versus 31% before the surgery. They concluded that LSG significantly improved glycemic control in T2DM although long-term remission and its maintenance for ≥5 years occurred infrequently.³⁰ Sieber et al. found 85% remission (normal FG, without antidiabetic medication for 1 year, and HbA1c < 6%) in 62 patients at 5-year follow-up.³¹ Other authors reported dissimilar results regarding complete remission.^32,33 Our results showed that complete remission was accomplished in 71.4% of patients, partial remission in 7.14%, and improvement in 10% at 5-year follow-up. Patients receiving insulin preoperatively, and with duration of disease ≥5 years, presented lower remission rates (P = .0004 and .0001, respectively).

Outcomes on patients receiving insulin preoperatively

Despite some interesting results coming from some publications, it is clear that remission rates in diabetic patients receiving insulin are lower than in patients treated only with OHD.^{30,31,33–38} In our study, 13% of patients were receiving insulin. At short-term follow-up, remission was observed in half of them, while the other half showed improvement. Efficacy started to drop at 3-year follow-up, shifting remission rate to 30% and improvement to 70%. At 5 years, 8 patients were available for evaluation; remission was 37.5% (n = 3), improvement 50% (n = 4), whereas 12.5% (n = 1) showed recurrence of the disease. While percentages were lower, >85% of patients were able to obtain either remission or improvement, decreasing the dosage of insulin or eventually receiving only OHD, with adequate metabolic control maintaining glucose values of 123 ± 30.02 mg/dL and HbA1c 6.75% ± 0.9% at ≥5-year follow-up. Golomb et al. demonstrated similar results at 3 years. In their series, 54.5% of patients were able to drop insulin therapy or were able to attain metabolic control just with OHD.³⁵ At 5-year follow-up, Sieber et al. found remission in 25% of patients who were under insulin therapy before LSG, versus 85% of those who were either on OHD or were not receiving any medication.³¹ Aminian et al. found a significant drop in insulin use after LSG, going from 42% to 25% at long-term follow-up (P = .004).³⁰

T2DM recurrence and associated risk factors after LSG

In our series, 11.4% (n = 8) of patients experienced recurrence of disease at ≥5 years. These patients had longer history of T2DM (P = .0001), FG, and HbA1c significantly higher than of patients who remained with their disease under control (P = .003 and .06, respectively). Only 25% of them were receiving insulin before LSG. It is worth mentioning that during the first year, 100% of them showed either complete remission or improvement. The evolution in this group was as follows: at 3 years, 75% showed complete/partial remission or improvement, and 25% already had recurrence; at 5 years, the total group presented recurrence of disease. Only few publications addressed T2DM recurrence after LSG, with rates between 0% and 44%.^{25,30,33,37,38} Aminian et al. reported 44% (n = 24) recurrence at long-term follow-up. All of these patients had shown remission initially. The only related factor they could identify was the need for two or more OHD for T2DM control before the surgery (P = .02). Despite the high recurrence rate, 67% of patients who belonged to this subgroup were able to achieve adequate control of their glycemia in the long run, decreasing their dosage of medications, even in patients who were on insulin.³⁰ Jimenez et al. described 16.2% recurrence after LSG, clearly related to patient's age, preoperative insulin therapy, and weight regain. Disease recurrence was observed approximately 25.2 ± 11.0 months after remission was achieved.³⁷

Summary

Our long-term results confirmed the benefit of LSG in the treatment of T2DM, showing remission rates of 78.3%, 75.5%, and 71.4% at 1, 3, and ≥5 years, respectively. A significant drop in HbA1c and FG was also observed. Although remission rate in patients under insulin therapy was inferior (37.5%), all of them were able to attain control with lower doses of insulin or even with OHD only. Our recurrence rate is similar to the one reported by others, and undoubtedly related to poor glycemic control before LSG. According to what have been previously discussed, we believe that LSG has a significant role in the treatment of obesity and T2DM, demonstrated by satisfactory long-term weight loss, low morbidity and reoperation rate, becoming a suitable alternative as a first step in the treatment of this disease. The tendency has shown a gradual decrease in efficacy with time; however, we believe that patients were still able to accomplish better metabolic control, even those who were on insulin and those who experienced recurrence of the disease.

Conclusion

Our results showed that at short, mid, and long term, T2DM control was satisfactory after LSG. Patients receiving insulin preoperatively and those with T2DM for ≥5 years revealed significantly lower remission rates.

Footnotes

Disclosure Statement

No competing financial interests exist.

References

International Diabetes Federation. IDF Diabetes Atlas, 8th Ed. Karuranga

, da Rocha Fernandes

, Huang

, Malanda

(eds). Brussels, Belgium: IDF, 2017.

Begué

Third national survey of risk factors for noncommunicable diseases. Buenos Aires, Argentina: Health National Ministery, 2015.

Yang

, Dall

, Halder

, Gallo

, Kowal

, Hogan

. Economic costs of diabetes in the U.S. in 2012. Diabetes Care, 2013; 36:1033–1045.

Torgeson

, Hauptman

, Boldrin

, Sjöström

. XENical in the prevention of diabetes in obese subjects (XENDOS) study: A randomized study of orlistat as an adjunct to lifestyle changes for the prevention of type 2 diabetes in obese patients. Diabetes Care, 2004; 27:155–161.

Stevens

, Obarzanek

, Cook

, Lee

, Appel

, Smith West

, et al. Long-term weight loss and changes in blood pressure: Results of the trials of hypertension prevention phase II. Ann Intern Med, 2001; 134:1–11.

The Look AHEAD Research Group. Cardiovascular Effects of Intensive Lifestylke Intervention In Type 2 Diabetes. N Engl J Med, 2013; 369:145–154.

Casagrande

, Fradkin

, Saydah

, Rust

, Cowie

. The prevalence of Meeting A1C, Blood Pressure, and LDL goals among people with diabetes, 1988–2010. Diabetes Care, 2013; 36:2271–2279.

Pories

, Swanson

, MacDonald

, Long

, Morris

, Brown

, et al. Who would have thought it?. An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg, 1995; 3:339–352.

Peterly

, Steinert

, Woelenerhanssen

, Peters

, Christoffel-Courtin

, Gass

, et al. Metabolic and hormonal changes after laparoscopic roux-en- Y gastric bypass and sleeve gastrectomy: A randomized, prospective trial. Obes Surg, 2012; 22:740–748.

10.

Kothari

, Borgert

, Kallies

, Baker

, Grover

. Long-term (>10-year) outcomes after laparoscopic Roux-en-Y gastric bypass. Surg Obes Relat Dis, 2017; 13:972–978.

11.

Ikramuddin

, Korner

, Lee

, Connett

, Inabnet

, Billington

, 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.

12.

Adams

, Davidson

, Litwin

, Kolotkin

, LaMonte

, Pendleton

, et al. Health benefits of gastric bypass surgery after 6 years. JAMA, 2012; 308:1122–1131.

13.

Himpens

, Verbrugghe

, Cadière

, Everaerts

, Greve

. Long term results of laparoscopic Roux-en-Y Gastric bypass: Evaluation after 9 years. Obes Surg, 2012; 22:1586–1593.

14.

Schauer

, Burguera

, Ikramuddin

, Cottam

, Gourash

, Hamad

, et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg, 2003; 238:467–484.

15.

Buchwald

, Estok

, Fahrbach

, Banel

, Jensen

, Pories

, et al. Weight and type 2 diabetes after bariatric surgery: Systematic review and meta-analysis. Am J Med, 2009; 122:248–256.

16.

ASMBS Clinical Issues Committee. Updated position statement on sleeve gastrectomy as a bariatric procedure. Surg Obes Relat Dis, 2012; 8:e21–e26.

17.

Boza

, Gamboa

, Salinas

, Achurra

, Vega

, Pérez

. Laparoscopic Roux-en-Y gastric bypass versus laparoscopic sleeve gastrectomy: A case-control study and 3 years of follow-up. Surg Obes Relat Dis, 2012; 8:243–249.

18.

Gumbs

, Gagner

, Dakin

, Pomp

. Sleeve gastrectomy for morbid obesity. Obes Surg, 2007; 17:962–969.

19.

Sakran

, Raziel

, Goitein

, Szold

, Goitein

. Laparoscopic sleeve gastrectomy for morbid obesity in 3003 patients: Results at a high-volume bariatric center. Obes Surg, 2016; 26:2045–2050.

20.

Hutter

, Schirmer

, Jones

, Ko

, Cohen

, Merkow

, et al. First report from the American College of Surgeons Bariatric Surgery Center Network: Laparoscopicsleeve gastrectomy has morbidity and effectiveness positioned between the band and the bypass. Ann Surg, 2011; 254:410–420.

21.

Boza

, Salinas

, Salgado

, Pérez

, Raddatz

, Funke

, et al. Laparoscopic sleeve gastrectomy as a stand-alone procedure for morbid obesity: Report of 1,000 cases and 3-year follow-up. Obes Surg, 2012; 22:866–871.

22.

Brethauer

, Kim

, El Chaar

, Papasavas

, Eisenberg

, Rogers

, et al. Standardized outcomes reporting in metabolic and bariatric surgery. Surg Obes Relat Dis, 2015; 11:489–506.

23.

Gill

, Birch

, Shi

, Sharma

, Karmaly

. Sleeve gastrectomy and type 2 diabetes mellitus: A systematic review. Surg Obes Relat Dis, 2010; 6:707–713.

24.

Schauer

, Kashyap

, Wolsky

, Brethauer

, Kirwan

, Pothier

, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med, 2012; 366:1567–1576.

25.

Abbatini

, Capoccia

, Casella

, Soricelli

, Leonetti

, Basso

. Long-term remission of type 2 diabetes in morbidly obese patients after sleeve gastrectomy. Surg Obes Relat Dis, 2013; 9:498–502.

26.

Albanopoulos

, Tsamis

, Natoudi

, Alevizos

, Zografos

, Leandros

. The impact of laparoscopic sleeve gastrectomy on weight loss and obesity-associated comorbidities: The results of 3 years of follow-up. Surg Endosc, 2016; 30:699–705.

27.

Abelson

, Afaneh

, Dolan

, Chartrand

, Dakin

, Pomp

. Laparoscopic Sleeve Gastrectomy: Co-morbidity Profiles and Intermediate-Term Outcomes. Obes Surg, 2016; 26:1788–1793.

28.

Schauer

, Bhatt

, Kirwan

, Wolski

, Brethauer

, Navaneethan

, et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N Engl J Med, 2014 22;370:2002–2013.

29.

Schauer

, Bhatt

, Kirwan

, Wolski

, Aminian

, Brethauer

, et al. Bariatric Surgery versus Intensive Medical Therapy for Diabetes - 5-Year Outcomes. N Engl J Med, 2017; 376:641–651

30.

Aminian

, Brethauer

, Andalib

, Punchai

, Mackey

, Rodriguez

, et al. Can sleeve gastrectomy “cure” diabetes? long-term metabolic effects of sleeve gastrectomyin patients with type 2 diabetes. Ann Surg, 2016; 264:674–681.

31.

Sieber

, Gass

, Kern

, Peters

, Slawik

, Peterli

. Five-year results of laparoscopic sleeve gastrectomy. Surg Obes Relat Dis, 2014; 10:243–249.

32.

Casella

, Soricelli

, Giannotti

, Collalti

, Maselli

, Genco

, et al. Long-term results after laparoscopic sleeve gastrectomy in a large monocentric series. Surg Obes Relat Dis, 2016; 12:757–762.

33.

Nedelcu

, Loureiro

, Skalli

, Galtier

, Jaussent

, Deloze

, et al. Laparoscopic sleeve gastrectomy: Effect on long term remission for morbidly obese patients with type 2 diabetes at 5-year follow up. Surgery, 2017; 162:857–862.

34.

Lemanu

, Singh

, Rahman

, Hill

, Babor

, MacCormick

. Five-year results after laparoscopic sleeve gastrectomy: A prospective study. Surg Obes Relat Dis, 2015; 11:518–524.

35.

Golomb

, Ben David

, Glass

, Kolitz

, Keidar

. Long-term metabolic effects of laparoscopic sleeve gastrectomy. JAMA Surg, 2015; 150:1051–1057.

36.

Peterli

, Wölnerhanssen

, Vetter

, Nett

, Gass

, Borbély

, et al. Laparoscopic sleeve gastrectomy versus roux-y-gastric bypass for morbid obesity-3-year outcomes of the prospective randomized swiss multicenter bypass or sleeve study (SM-BOSS). Ann Surg, 2017; 265:466–473.

37.

Jimenez

, Casamitjana

, Flores

, Viaplana

, Corcelles

, Lacy

, et al. Long-term effect of sleeve gastrectomy and Roux-en- Y gastric bypass surgery on type 2 diabetes mellitus in morbidly obese subjects. Ann Surg, 2012; 256: 1023–1029.

38.

Brethauer

, Aminian

, Romero Talamás

, Batayyah

, Mackey

, Kennedy

, et al. Can diabetes be surgically cured?. Long-term metabolic effects of bariatric surgery in obese patients with type 2 diabetes mellitus. Ann Surg, 2013; 258:628–637.