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Review |

Bariatric Surgery for Weight Loss and Glycemic Control in Nonmorbidly Obese Adults With Diabetes:  A Systematic Review FREE

Melinda Maggard-Gibbons, MD, MSHS; Margaret Maglione, MPP; Masha Livhits, MD; Brett Ewing, MS; Alicia Ruelaz Maher, MD; Jianhui Hu, PhD; Zhaoping Li, MD, PhD; Paul G. Shekelle, MD, PhD
[+] Author Affiliations

Author Affiliations: Rand Health, Santa Monica, California (Drs Maggard-Gibbons, Maher, Hu, and Shekelle and Ms Maglione and Ms Ewing); Department of Surgery, David Geffen School of Medicine at the University of California, Los Angeles (Dr Maggard-Gibbons and Livhits); VA Greater Los Angeles Healthcare System, Los Angeles, California (Drs Maggard-Gibbons, Livhits, Li, and Shekelle); Department of Surgery, Olive View-University of California, Los Angeles Medical Center, Sylmar (Dr Maggard-Gibbons); and the Akasha Center for Integrative Medicine, Santa Monica, California (Dr Maher).


JAMA. 2013;309(21):2250-2261. doi:10.1001/jama.2013.4851.
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Published online

Importance Bariatric surgery is beneficial in persons with a body mass index (BMI) of 35 or greater with obesity-related comorbidities. There is interest in using these procedures in persons with lower BMI and diabetes.

Objective To assess the association between bariatric surgery vs nonsurgical treatments and weight loss and glycemic control among patients with diabetes or impaired glucose tolerance and BMI of 30 to 35.

Evidence Review PubMed, EMBASE, and Cochrane Library databases were searched from January 1985 through September 2012. Of 1291 screened articles, we included 32 surgical studies, 11 systematic reviews on nonsurgical treatments, and 11 large nonsurgical studies published after those reviews. Weight loss, metabolic outcomes, and adverse events were abstracted by 2 independent reviewers.

Findings Three randomized clinical trials (RCTs) (N = 290; including 1 trial of 150 patients with type 2 diabetes and mean BMI of 37, 1 trial of 80 patients without diabetes [38% with metabolic syndrome] and BMI of 30 to 35, and 1 trial of 60 patients with diabetes and BMI of 30 to 40 [13 patients with BMI <35]) found that surgery was associated with greater weight loss (range, 14.4-24 kg) and glycemic control (range, 0.9-1.43 point improvements in hemoglobin A1c levels) during 1 to 2 years of follow-up than nonsurgical treatment. Indirect comparisons of evidence from observational studies of bariatric procedures (n ≈ 600 patients) and meta-analyses of nonsurgical therapies (containing more than 300 RCTs) support this finding at 1 or 2 years of follow-up. However, there are no robust surgical data beyond 5 years of follow-up on outcomes of diabetes, glucose control, or macrovascular and microvascular outcomes. In contrast, some RCT data of nonsurgical therapies show benefits at 10 years of follow-up or more. Surgeon-reported adverse events were low (eg, hospital deaths of 0.3%-1.0%), but data were from select centers and surgeons. Long-term adverse events are unknown.

Conclusions and Relevance Current evidence suggests that, when compared with nonsurgical treatments, bariatric surgical procedures in patients with a BMI of 30 to 35 and diabetes are associated with greater short-term weight loss and better intermediate glucose outcomes. Evidence is insufficient to reach conclusions about the appropriate use of bariatric surgery in this population until more data are available about long-term outcomes and complications of surgery.

Bariatric surgery is often used to promote weight loss and manage obesity-related comorbidities in morbidly obese patients (body mass index [BMI; calculated as weight in kilograms divided by height in meters squared] ≥35). In this population, procedures such as laparoscopic adjustable gastric banding and Roux-en-Y gastric bypass have resulted in better glucose control and more weight loss at 1 or 2 years than nonsurgical therapy.1,2 Metabolic changes are often observed shortly after surgery suggesting that the mechanism may be partly independent of weight loss.35 There is precedent for weight-independent effects. In the Swedish Obese Subjects study, participants who underwent bariatric surgery had a 33% reduction in cardiovascular events compared with a matched group of patients without surgery, and this was unrelated to weight loss past 4 years of follow-up.6

Bariatric surgical procedures are being advocated as a treatment for diabetes in less-obese individuals (BMI, 30-35).7 However, this practice remains controversial. In 2006, the Centers for Medicare & Medicaid Services (CMS) would not approve coverage for patients with lower BMI and diabetes,8 whereas the US Food and Drug Administration has approved gastric banding for individuals with a BMI of 30 to 35 who have an obesity-related comorbidity.914 Given this lack of consistency—and uncertainties regarding the comparative effectiveness of different procedures—we conducted a systematic review of the relative benefits and risks associated with surgical and nonsurgical therapies for treating diabetes or impaired glucose tolerance in patients with a BMI of 30 to 35.

A protocol for this review was developed with input from stakeholders.15 Our literature search included PubMed, EMBASE, and 3 Cochrane Library databases from January 1985 through September 2012. We also searched for studies of nonsurgical treatments (diet, exercise, education, medications [not including insulin], and other interventions). Search terms included (diabetes or diabetic* or diabetes mellitus) and intervention and (follow-up studies or longitudinal studies or outcome assessment [health care] or randomized controlled trial [pt]). A complete description of the search strategy is included in our evidence report (available at http://www.effectivehealthcare.ahrq.gov/weight-loss-surgery.cfm).16

Our objective was to assess the association between bariatric surgery compared with nonsurgical therapy, and weight loss and glycemic control among patients with diabetes and a BMI of 30 to 35. Because preliminary searches identified few head-to-head randomized trials comparing surgical and nonsurgical therapies in this population, we specified a priori that we would attempt to draw conclusions using both direct and indirect methods. Direct comparisons of surgically treated and nonsurgically treated patients would come from randomized and nonrandomized studies that directly compared outcomes within the same study. Indirect comparisons would come from data of outcomes of surgically treated patients in a group of studies and data of outcomes of nonsurgically treated patients in a different group of studies. We initially included all studies reporting outcomes for surgically treated patients with the following exceptions: (1) studies not reporting clinical outcomes of effectiveness or adverse events; (2) surgical procedures not commonly performed in the United States or considered experimental (ie, sleeve gastrectomy with ileal interposition, and duodenal-jejunal bypass); and (3) studies with a sample size fewer than 3. In addition, recognizing that weight and glucose control are continuums, we used discretion when selecting or rejecting studies for inclusion based on these criteria. For example, we included studies that enrolled patients with a BMI of 29 to 37. Similarly, we included studies in which some patients had impaired glucose tolerance instead of clinical diabetes, because impaired glucose tolerance is a precursor to clinical diabetes. Because the literature about nonsurgical treatment of obesity and its comorbidities is voluminous, with dozens of systematic reviews, for our indirect comparison we searched for high-quality systematic reviews and supplemented these with reports of recent clinical trials not included in those reviews. New clinical trials with less than 1 year of follow-up were excluded.

Two independent reviewers extracted data, including metabolic outcomes (glucose, blood pressure, and lipids), weight loss, mortality, and adverse events. Other details included population characteristics, eligibility and exclusion criteria, cointerventions, comparisons, and other outcomes. Data for patients with a BMI less than 35 were obtained from the author of 1 of the included trials (John B. Dixon, MBBS, PhD, Centre for Obesity Research and Education, Monash University Medical School, November 2012, written communication). Discrepancies were resolved through discussion.

The quality of controlled trials of surgery was assessed using the Cochrane risk of bias tool.17 We used AMSTAR (Assessment of Multiple Systematic Reviews) to assess the quality of systematic reviews.18,19 Case series and cohort studies were evaluated in terms of the completeness of follow-up, the generalizability of the population, and whether patients were consecutively enrolled.

We summarized studies in the following order: clinical trials that directly compared surgical with nonsurgical therapy for patients with diabetes or the metabolic syndrome; observational studies that directly compared, within a study, patients who did or did not receive surgery; and an indirect comparison between the results of case series or cohort studies in which all patients received surgical therapy and the results of systematic reviews or recent clinical trials of nonsurgical therapies for diabetes. We quantitatively summarized the observational studies of patients receiving surgery by combining studies with similar surgical procedure, measured outcome, and follow-up time (0-3 months, 6-11 months, and ≥12 months). For each study that provided sufficient outcome data, we calculated the mean change from baseline to follow-up, in which a negative mean change indicates decrease in outcome measure (eg, BMI). We used the estimates to calculate a weighted mean change within surgery type, outcome, and follow-up time.

We also summarized the adverse event data from all studies of surgical therapies that reported adverse events, using meta-analysis to combine studies reporting similar outcomes for the same surgical procedures. The data analysis and output for this article were generated using SAS software (version 9.2).

Description of the Studies Identified by the Literature Search

We identified 7496 articles; 1291 studies were selected for full-text review after abstract screening. We included 32 surgical studies, 11 systematic reviews of nonsurgical studies and 6 surgical systematic reviews (that we used for reference mining), and 11 large nonsurgical studies published after those reviews (eFigure).2051 Of the 32 studies reporting bariatric surgery results in patients with metabolic conditions, there were 3 controlled trials with a nonsurgical comparison group, 2 head-to-head trials comparing surgical procedures, 1 small matched trial including a nonsurgical group, and 26 observational studies, including 1 cohort study that compared surgical procedures. A single study could include more than 1 surgical treatment group. The 32 surgery studies reported 40 individual surgical groups: 20 groups involving gastric bypass; 9 groups, gastric banding; 5 groups, biliopancreatic diversion, 6 groups, sleeve gastrectomy. Two observational studies47,49 grouped the results of gastric bypass, sleeve gastrectomy, and gastric banding together, preventing them from incorporation in our analyses.

The majority of the surgical studies reported data from a single institution (27 of 32). Of these, 3 studies reported that only 1 surgeon performed the cases, 5 studies had 2 surgeons, and 3 surgeons completed the operations in 1 study. There were 3 multi-institutional studies. The numbers of surgeons participating in the others was not reported. The authors of 26 studies had at least 1 academic affiliation. Three studies had sample sizes greater than 200 patients. Fourteen studies noted that patients were consecutively enrolled. The risk of bias was low for all 3 trials comparing surgery to nonsurgical treatment (eTable 1). The observational studies are all considered to have high risk of bias.

Data are presented in the following order: (1) direct surgical vs nonsurgical intervention comparisons; (2) direct comparisons and observational studies of procedure types; (3) observational studies of surgery with no comparison group; (4) summary of nonsurgical intervention systematic reviews; and (5) summary of surgical adverse events.

Direct Comparisons of Surgical vs Nonsurgical Interventions

Randomized Trials. We identified 3 randomized clinical trials that compared bariatric surgery with a nonsurgical intervention; they assessed different procedures with varied BMI range, percentage of patients with diabetes, severity of diabetes, and length of follow-up (Table 1). None of these trials enrolled patients exclusively in our target population: in 2 trials the mean BMI was 37 and in 1 trial not all patients had diabetes. Nevertheless, we decided all 3 trials provided randomized comparisons of surgical and nonsurgical treatment that were informative to our target population. We considered all 3 trials too clinically different in terms of procedures, degree of impaired glucose control, intensity of medical treatment, and duration of follow-up to justify statistical pooling.

Table Graphic Jump LocationTable 1. Direct Comparison of Surgical vs Nonsurgical Interventions, Randomized Clinical Trials

Schauer and colleagues44 randomized 150 patients with uncontrolled type 2 diabetes (hemoglobin A1c [HbA1c] >7.0%) and a BMI of 27 to 43 to either intensive medical therapy (nonsurgical) or medical treatment following gastric bypass or sleeve gastrectomy. The mean BMI was about 37, slightly higher than the upper limit of our target population. Ninety-three percent of patients completed 12-month follow-up. The surgical groups lost about 20 kg more weight at 12 months than the medical therapy group. More patients in the surgical groups achieved glycemic control (HbA1c ≤6.0%): 42% of patients receiving gastric bypass and 37% of patients receiving sleeve gastrectomy (P <.001) compared with 12% of patients receiving medical therapy (P = .008). The mean HbA1c at 1-year follow-up was lower among surgical patients—6.4% in patients receiving gastric bypass (P <.001) and 6.6% of patients receiving sleeve gastrectomy (P = .003)—than among patients (7.5%) receiving medical therapy. The surgical groups also had a lower mean serum cholesterol level and need for hypertension medications than the medical therapy group (P < .001). In a sensitivity analysis, the authors assessed whether the effectiveness of therapy varied in patients with lower BMI compared with those with higher BMI; no statistically significant interaction effect was found (P = .60), indicating that there was no evidence that the beneficial effect of surgery was dissimilar across patients with varying BMI. With small sample sizes, the power of this test to detect differences is limited.

O’Brien and colleagues21 randomized 80 patients with a BMI of 30 to 35 to gastric banding vs an intensive medical treatment intervention. About 38% of enrolled patients had the metabolic syndrome. Both groups lost a similar amount of weight (13.8%) by 6 months. The surgical group continued to lose weight to 24 months, but the medical treatment group regained much of the weight lost (mean BMI, 26.4 in the surgical group vs mean BMI, 31.5 in the medical group, P < .001), with a between-group difference of about 15 kg. Fasting blood glucose was lower in patients receiving gastric banding than those treated medically, which did not experience a decrease. The prevalence of the metabolic syndrome decreased from 38% to 2.7% in the patients receiving gastric banding and to 24% in the patients receiving medical treatment (P <.001 between-group comparison).

Dixon and colleagues22 randomized 60 patients with diabetes and a BMI between 30 to 40 to gastric banding vs usual diabetes care. The mean BMI of included patients was about 37, slightly higher than our target population. Similar to the study by Schauer et al,43 surgically treated patients lost a mean of about 20 kg more than nonsurgically treated patients at 2 years. Fasting blood glucose was lower in the patients treated with surgery than in the medical therapy group (mean difference, −32.8 mg/dL [95% CI, −53.1 to −12.3]). The HbA1c also decreased to a greater degree in the surgically treated patients (6.00 vs 7.21; mean difference, −1.43 [95% CI, −2.1 to −0.8]). A total of 13 patients in this trial had a BMI of less than 35 (6 treated surgically, 7 treated with conventional therapy). A test for interaction did not show any statistically significant difference in the effect of surgery in patients with a BMI less than 35 compared with patients with a BMI of 35 or more. Again, with small sample sizes there is limited power of this interaction test to detect differences. However, in the low BMI subgroup, there were statistically significant differences between groups in weight loss (14 kg loss vs 0.2 kg gain, P = .03) and the composite outcome of remission of diabetes (66% vs 0%, P = .02).

Observational Studies. We found 2 small cohort studies matching data from surgical patients with data from similar patients who did not have bariatric surgery. A small study involving 12 participants by Chiellini and colleagues32 had only a 1-month follow-up, which we judged too short to be clinically useful. Serrot and colleagues42 compared 17 patients with diabetes who underwent gastric bypass with 17 matched patients receiving routine medical management for diabetes and weight control. All patients had a BMI of 30 to 34.9.Similar to the randomized comparisons, at 1 year, the surgically treated patients had greater weight loss, a decrease in mean BMI to 25.8 vs 0.3 gain in the comparison group, and an improvement in HbA1c concentration of about 2 points (a decrease from 8.2% at baseline to 6.1% at 1 year in the gastric bypass group, but no significant change in the comparison group).

Comparisons Between Surgical Procedures. We identified 2 randomized clinical trials comparing surgical procedures in our target population. Lee and colleagues33 randomized 60 patients with diabetes in Taiwan to receive gastric bypass or sleeve gastrectomy (mean BMI, 30.3). At 12 months, the gastric bypass group had lost more weight: mean BMI forpatients receiving gastric bypass was 22.8 compared with 24.4 for patients receiving sleeve gastrectomy (P = .009). The HbA1c levels decreased by a mean of 4.2 percentage points in the gastric bypass group vs 3.0% in the sleeve gastrectomy group (P < .05). Fasting glucose was also lower in the gastric bypass group (99.3 mg/dL vs 140.1 mg/dL; P < .001; to convert glucose from mg/dL to mmol/L, multiply by 0.0555). Diabetes resolved (fasting plasma glucose < 126 mg/dL and HbA1c < 6.5% without medications) in 93% of patients receiving gastric bypass compared with 47% of patients receiving sleeve gastrectomy (P = .02). Total cholesterol level, triglycerides, low-density lipoprotein, and high-density lipoprotein improved in both groups but to a greater degree in the gastric bypass group.

As described above, Schauer et al43 randomized 150 US patients to receive gastric bypass, sleeve gastrectomy, or intensive medical therapy. At 12 months, patients receiving gastric bypass lost more weight than those who received sleeve gastrectomy (−29.4 kg vs −25.1 kg, P = .02). Changes in blood glucose were similar; however, all patients in the gastric bypass group who achieved a target HbAlc level of 6% did so without medications, whereas 28% in the sleeve gastrectomy group required medications. Changes in blood pressure and cholesterol did not differ by surgical group.

One cohort comparing results between surgical procedures found greater weight loss and better control of diabetes with gastric bypass than with laparoscopic gastric banding;28 and 1 small cohort of 16 participants found that diabetes control was better at 1 year in patients who received biliopancreatic diversion than in patients who received gastric bypass.35

Indirect Comparisons of Surgical and Nonsurgical Interventions

Observational Surgical Studies—Weight Loss and Diabetes Outcomes. Table 2 displays data from the observational studies in which all patients had diabetes at baseline.2325,2830,3242,4446,48,50,52 eTable 2 includes a descriptive table of the individual study characteristics.

Table Graphic Jump LocationTable 2. Observational Surgical Studies on Diabetes Outcomes by Surgery Typea

Body Mass Index. At 3 months or less, the mean decrease in BMI ranged from 2.3 in 1 study of gastric banding to 4.3 in 2 studies of sleeve gastrectomy. At 12 to 24 months, the mean BMI decrease was 5.6 for biliopancreatic diversion, 7.3 for sleeve gastrectomy, and 7.5 for gastric bypass. In long-term studies of weight loss following bariatric surgery in other populations, the maximal weight loss is usually seen about 2 years after surgery, with more variable results seen at longer periods.53

Blood Glucose. Glucose control following surgery was reported in various ways, including changes in HbA1c and plasma glucose concentration, percentage of patients who no longer required diabetes medication, and remission or resolution of diabetes. Ten surgery groups reported changes in HbA1c at 6 to 11 months. Baseline HbA1c values were higher than 9% in all but 1 study, and mean improvements were 2.9 percentage points for biliopancreatic diversion, 2.5 percentage points for sleeve gastrectomy, and 3.0 percentage points for gastric bypass. None of the observational studies of gastric banding reported HbA1c outcomes. Studies of gastric bypass, sleeve gastrectomy, and biliopancreatic diversion with longer-term follow-up (12-24 months) reported improvements in mean HbA1c values ranging from −2.4 to −3.1 percentage points. Consistent with these results are the reported improvements in blood glucose levels, with baseline values exceeding 150 to 200 mg/dL and decreases of 60 to 90 mg/dL at 1-year follow-up.

Remission/Resolution. Studies reported the variable outcome of remission or resolution of diabetes at 12 months or more in 12 surgery groups.33,34,3842,44,50,51 All studies reporting this outcome found large proportions of patients achieving remission or resolution. Of note, the definitions of diabetes improvements in these studies were variable. For example, resolution typically referred to patients who were not taking diabetes medications but without a predefined HbA1c level goal that needed to be achieved.

Effectiveness of Nonsurgical Therapy for Diabetes. Behavioral Therapies or Medications. We identified 11 representative fair- to excellent-quality systematic reviews about the effects of interventions such as exercise, diet, health education, and medications on weight loss and diabetes outcomes.5464 Six behavioral studies (2 reported only patients with impaired glucose tolerance) and 5 medication studies (1 study had a mix of patients with or without diabetes) were included (Table 3). Although the original studies included in the systematic reviews did not all necessarily focus on patients with a BMI of 30 to 35, the mean BMI of patients included across the randomized clinical trials was in this general range, and we therefore judged the conclusions of these reviews to be applicable to our target population.

Table Graphic Jump LocationTable 3. Systematic Reviews on Nonsurgical Interventions Including Diabetes Medications

One systematic review of behavioral interventions (such as physical activity, a low-calorie diet, and self-monitoring of blood glucose)54 and 3 systematic reviews of different types of diets5658 reported, in general, weight loss of a few kilograms (approximately 2-10 kg) compared with usual care and changes in HbA1c concentration ranging from 0 to about 2 points (<2-year follow-up). Two reviews of patients with impaired glucose tolerance found small amounts of modest weight loss and reduction or delay in onset of diabetes.55,59 Five systematic reviews that focused on the efficacy and safety of diabetes medications in patients with type 2 diabetes (Table 3)6064 found that most blood glucose control medications were effective in glycemic control, with decreases in HbA1c concentrations of between 0.5 and 1 point for each medication (up to 2 medications); a few medications also were associated with modest weight loss.

Evidence From Major Trials Published Since the Systematic Reviews

Since the systematic reviews discussed above were published, long-term follow-ups of several of the included studies have been conducted. These studies assessed the long-term (10-20 years follow-up) effects of nonsurgical interventions in China,65 Finland66 (behavioral intervention), the United States67 (behavioral and medications), and the United Kingdom68 (medications). Overall, weight loss effects observed during active intervention periods often did not persist in the long-term, whereas the reductions in diabetes incidence and other outcomes did persist. Behavioral interventions did not lead to significant reductions in some major clinical end points such as mortality. Pharmacological interventions were associated with reduced mortality in the long-term. A 10-year follow-up study of the United Kingdom Prospective Diabetes Study showed decreased diabetes-related mortality and all-cause mortality in patients who are overweight and treated with metformin compared with dietary therapy.68

Adverse Events in Lower-Weight Individuals Following Bariatric Surgery

The incidence of adverse events following bariatric surgery is displayed in eTable 3) for all studies, including case series, cohorts, and controlled trials. Follow-up times varied widely from the day of surgery to 2 years; the exceptions are 2 studies that reported events up to 3 and 5 years after surgery. Few studies were clear on exactly when the adverse events took place, and data were not always available for all patients. Adverse events were often identified and self-reported by the surgical team, with definitions of most complications varying from study to study. Few administrative data were available to diminish these biases. In addition, few studies compared adverse events among surgical procedures, making direct comparisons difficult.

Studies were included in our mortality analyses only if they reported or mentioned either the number of deaths or the lack of deaths. Thus, 14 studies were included, accounting for 5 gastric banding treatment groups, 1 sleeve gastrectomy group, 9 gastric bypass groups, and 1 biliopancreatic diversion group. Only 1 death was reported—a patient receiving gastric banding with complications of a gastric perforation. Cardiovascular, respiratory, and gastrointestinal complications were relatively rare. Other than 1 study that used self-reporting to measure hypoglycemia, metabolic adverse events were also uncommon in these studies with relatively short follow-up times. Infections or seroma were reported in 10 of 231 patients receiving gastric bypass (4.3%) and in 1 of 30 patients receiving gastric banding. Incisional hernias were reported in 3 of 67 patients receiving gastric bypass (4.5%). Five percent of 363 patients receiving gastric bypass experienced stricture. Four of 439 patients receiving gastric bypass, and 1 of 49 patients receiving sleeve gastrectomy experienced an anastomotic leak. An ulcer was reported in 5.3% of 133 patients receiving gastric bypass. One gastric bypass study reported an anastomotic hemorrhage in 1 of 22 patients. One occurrence of intra-abdominal hemorrhage was reported in both a study of 109 patients and a study of 30 patients receiving biliopancreatic diversion.

Several complications specific to gastric banding were reported. Band slippage was reported in 3.0% of 361 patients, port or tube problems were reported in about 1.9% of 462 patients, and 3.3% of 210 patients receiving gastric banding had the band removed. Of 240 patients receiving gastric banding, 5.4% experienced pouch dilation after surgery.

Current evidence suggests that bariatric surgery is associated with more short-term weight loss and better intermediate glucose outcomes than nonsurgical therapy in patients with diabetes and a BMI of 30 to 35. However, data on long-term benefits and risks are unknown.

There are limited data from randomized clinical trials to directly address the clinically important question of whether bariatric surgery is associated with greater weight loss and better glycemic control than nonsurgical therapy in patients with diabetes and a BMI of 30 to 35. Our review identified and included only 3 clinical trials, totaling 290 patients (170 treated surgically), that compared bariatric surgical procedures with nonsurgical procedures in patients with impaired glycemic control and elevated BMI. However, the populations enrolled in these studies did not exactly match the target patient population we sought to evaluate in our review. Subgroup analyses from 1 clinical trial of a small number of patients with a BMI less than 35 (6 treated surgically and 7 treated with conventional therapy) suggest that the findings may be applicable to patients with this BMI range. Although the test of interaction for treatment of patients in this trial with a BMI above or below 35 was not significant, the small sample size limits the power of this interaction test to detect differences. In addition, 2 trials that reported outcomes at 24 months were conducted in the same center.

However, in support of this modest clinical trial evidence are direct comparisons of surgery and nonsurgical therapy in more obese populations and indirect comparisons of the associations between surgical and nonsurgical therapies and the outcomes of weight loss and glycemic control. Although indirect comparisons are always potentially problematic due to confounding factors, the magnitude of the weight loss and the decrease in HbA1c levels observed in the surgical studies is 2- to 5-fold greater than in the studies of nonsurgical therapies, decreasing the likelihood that confounding alone can explain these differences. Overall, the direct, but limited, data from clinical trials in patients with a BMI of 30 to 35, the direct data from clinical trials of patients with higher BMI, and the indirect comparisons of surgical and nonsurgical therapies all consistently find that weight loss and short-term glucose control are better in patients treated with bariatric surgery. Data also indicate these improvements are greater in patients treated with gastric bypass than with gastric banding.

The mechanism of diabetes control following bariatric surgery is complex. Partly due to weight loss in some patient populations, improved glucose control is observed in the early postoperative period, before substantial weight loss, and is seen in patients who are not severely obese preoperatively.3,4,69,70 The degree of improvement does not always correlate with the amount of weight loss. It has been hypothesized that alterations to the foregut may mediate peptides (such as insulin level, insulin resistance, and glucagon-like peptide 1) and neural signaling. This field of study continues to evolve.7175

The evidence is insufficient to reach conclusions about the preferred treatment for diabetes in this target population due to the lack of long-term data on patients who have undergone bariatric surgery. Only 4 studies had follow-up longer than 2 years. In these studies, small sample sizes or poor follow-up preclude definitive conclusions. Additionally, many of the studies were from single surgeons at single academic institutions and may not be representative of results in a general population of patients and surgeons. Furthermore, data comparing bariatric surgery to nonsurgical therapy in more obese populations show that the maximal benefit favoring surgery in terms of weight loss and many other outcomes accrues at about 2 years after surgery.53 In some clinical situations, surgical procedures from academic institutions have been shown to have fewer complications than those reported from general clinical settings.76

Considering the academic settings and 2-year follow-up, the studies published to date are likely to represent a best case estimate of outcomes from current bariatric surgery. In contrast, behavior and medication interventions have been studied extensively in a wide variety of clinical settings; several large, long-term randomized clinical trials have found improved HbA1c levels for up to 10 years. Therefore, the evidence for longer-term control of glucose in patients with diabetes is stronger for behavioral and medication therapies than for surgery. The evidence that treatment reduces the microvascular and macrovascular outcomes of diabetes, although not robust for nonsurgical interventions, is still much stronger than the evidence available for surgical interventions. More data about the durability of benefit are needed. Recently, 2 studies have reported results regarding long-term effects in diabetes. Adams and colleagues77 reported that among 88 patients with diabetes at baseline, 66 (75%) were in remission 2 years after surgery. By 6 years, this had decreased to 62%, for an 18% relapse rate. By contrast, Arterburn and colleagues78 found that 68% of 4434 patients with diabetes had complete diabetes resolution at 5 years following surgery, but 35% of these patients redeveloped diabetes at 6 years after surgery.

As recently pointed out, 1 potential limitation of studies comparing surgical vs nonsurgical treatments is that the intensity of treatment in the surgical group may be inherently greater.79 Intensity of treatment in surgical therapy may improve weight loss and glucose outcomes. Caution is warranted when considering differences between surgical and nonsurgical therapy when the intensity of treatment is not balanced in the 2 groups. Future studies should pay careful attention to this potential confounding factor.

In the studies we reviewed, major surgical complications were uncommon (1.8%-7.4%), but these events often required a significant intervention. Reported mortality rates were very low (0.3%-0%). However, the published literature we reviewed represents a narrow segment of the patients undergoing bariatric surgery.

From the substantial body of literature about more obese populations, there are reports of numerous nutritional deficiencies and the development of renal stones.8082 Persons starting with lower BMI may be at increased risk of malnutrition as well. Most data are surgeon-reported outcomes from selected, experienced centers, and the studies are not designed to assess complication rates.

Lay media reports suggest serious adverse events happen more commonly than reported in medical literature. For example, the Los Angeles Times reported 5 deaths occurring shortly after patients received the gastric banding procedure.83,84 Additional clinical details are not reported sufficiently to characterize whether those deaths occurred in patients in the target population of this review. Nevertheless, the lay media reports heighten concern about the potential underestimation of adverse events of which the reporting relies solely on published studies from select surgery centers. We found no long-term studies of postsurgery adverse events in patients with diabetes within our target BMI range. Additional studies are needed before definitive conclusions can be reached about the choice of therapy.

In sum, current evidence suggests bariatric surgery is associated with greater improvements in weight loss, HbA1c and fasting blood glucose levels, blood pressure, and hyperlipidemia than nonsurgical interventions such as medications, diet, and behavioral changes for patients with a BMI of 30 to 35 and diabetes. However, there are limited data from clinical trials in this specific patient population, and it is unknown whether the benefits observed are durable long-term and if these findings might translate into reductions in the microvascular and macrovascular complications of diabetes. Until such data are available, the evidence is insufficient to reach conclusions about the appropriate use of bariatric surgery in this patient population, performance of these procedures in this target population should be under close scientific scrutiny, and additional studies comparing procedures are warranted.

Corresponding Author: Melinda A. Maggard-Gibbons, MD, MSHS, Department of Surgery, David Geffen School of Medicine at the University of California, Los Angeles, CHS 72-215, 10833 Le Conte Ave, Los Angeles, CA 90095 (mmaggard@mednet.ucla.edu).

Author Contributions: Dr Maggard-Gibbons had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. All data used for this study are accessible for review.

Study concept and design: Maggard-Gibbons, Maglione, Maher, Hu, Li, Shekelle.

Acquisition of data: Maggard-Gibbons, Livhits, Ewing, Maher, Hu.

Analysis and interpretation of data: Maggard-Gibbons, Maglione, Livhits, Ewing, Maher, Li, Shekelle.

Drafting of the manuscript: Maggard-Gibbons, Livhits, Ewing, Maher, Hu, Shekelle.

Critical revision of the manuscript for important intellectual content: Maglione, Maher, Li, Shekelle.

Statistical analysis: Maggard-Gibbons, Livhits, Ewing, Maher, Hu, Li.

Obtained funding: Maglione, Shekelle.

Administrative, technical, or material support: Maglione, Shekelle.

Study supervision: Maglione, Li, Shekelle.

Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Dr Maggard-Gibbons reports receiving grant support from the Agency for Healthcare Research and Quality (AHRQ). Ms Maglione reports receiving grant support from AHRQ. Dr Hu reports receiving grant support from AHRQ. Dr Li reports receiving grant support from AHRQ. Dr Shekelle reports consulting for Emergency Care Research Institute, being employed at VA Health Services, and receiving grant support from AHRQ, VA Health Services, Centers for Medicare & Medicaid Services, National Institutes of Health, and Office of the National Coordinator and royalties from UpToDate.

Funding/Support: This project was funded under the contract 290-2007-10062I from the AHRQ and US Department of Health and Human Services.

Role of the Sponsor: The AHRQ had input into the design and conduct of evidence reviews conducted by the Evidence-Based Practice Centers, but not this specific evidence review, and was not involved in the collection, management, or analyses of the data, nor the decision to submit the manuscript for publication, but did review and provide comments on the evidence report upon which this article is based.

Disclaimer: The authors of this report are responsible for its content. Statements in the report should not be construed as endorsement by the AHRQ, US Department of Health and Human Services, and the Department of Veterans Affairs.

Additional Contributions: We thank Dr Dixon for the data on his trial. We also thank Roberta Shanman, MLS (Reference Services, RAND Library), who conducted the literature searches and Tanja Perry, BHM (Southern California Evidence-Based Practice Center, RAND Health), who contributed to the manuscript. Dr Dixon received no compensation for his contribution. All other contributors are regular staff of the Southern California Evidence-Based Practice Center.

Buchwald HA, Avidor Y, Braunwald E,  et al.  Bariatric surgery: a systematic review and meta-analysis.  JAMA. 2004;292(14):1724-1737
PubMed   |  Link to Article
Sjöström CDL, Lissner L, Wedel H, Sjöström L. Reduction in incidence of diabetes, hypertension and lipid disturbances after intentional weight loss induced by bariatric surgery: the SOS Intervention Study.  Obes Res. 1999;7(5):477-484
PubMed   |  Link to Article
Mingrone G, Castagneto-Gissey L. Mechanisms of early improvement/resolution of type 2 diabetes after bariatric surgery.  Diabetes Metab. 2009;35(6 pt 2):518-523
PubMed   |  Link to Article
Gill RS, Birch DW, Shi X, Sharma AM, Karmali S. Sleeve gastrectomy and type 2 diabetes mellitus: a systematic review.  Surg Obes Relat Dis. 2010;6(6):707-713
PubMed   |  Link to Article
Maggard MA, Shugarman LR, Suttorp M,  et al.  Meta-analysis: surgical treatment of obesity.  Ann Intern Med. 2005;142(7):547-559
PubMed   |  Link to Article
Sjöström L, Peltonen M, Jacobson P,  et al.  Bariatric surgery and long-term cardiovascular events.  JAMA. 2012;307(1):56-65
PubMed   |  Link to Article
 Executive summary of the clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults.  Arch Intern Med. 1998;158(17):1855-1867
PubMed   |  Link to Article
Phurrough S, Salive ME, Brechner R, Meltzer A. Decision memo for surgery for diabetes (CAG-00497N). http://www.cms.gov/medicare-coverage-database/details/nca-decision-memo.aspx?NCAId=219. Published December 2, 2010. Accessed May 6, 2013
US Food and Drug Administration.  FDA expands use of banding system for weight loss. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm245617.htm. Published February 16, 2011. Updated March 3, 2011. Accessed April 15, 2013
Finks JF, Kole KL, Yenumula PR,  et al; Michigan Bariatric Surgery Collaborative, from the Center for Healthcare Outcomes and Policy.  Predicting risk for serious complications with bariatric surgery: results from the Michigan Bariatric Surgery Collaborative.  Ann Surg. 2011;254(4):633-640
PubMed   |  Link to Article
Padwal R, Klarenbach S, Wiebe N,  et al.  Bariatric surgery: a systematic review of the clinical and economic evidence.  J Gen Intern Med. 2011;26(10):1183-1194
PubMed   |  Link to Article
Colquitt JL, Picot J, Loveman E, Clegg AJ. Surgery for obesity.  Cochrane Database Syst Rev. 2009;(2):CD003641
PubMed
Lin VW, Wright A, Flum DR, Garrison LP Jr, Alfonso-Cristancho R, Sullivan SD. Patients' experience and outcomes after laparoscopic adjustable gastric banding in Washington state.  Surg Obes Relat Dis. 2012; April 14
PubMed
Kral JG, Christou NV, Flum DR,  et al.  Medicare and bariatric surgery.  Surg Obes Relat Dis. 2005;1(1):35-63
PubMed   |  Link to Article
Agency for Healthcare Research and Quality.  Research protocol—comparative effectiveness of bariatric surgery and nonsurgical therapy in adults with metabolic conditions and a body mass index of 30.0 to 34.9. http://effectivehealthcare.ahrq.gov/index.cfm/search-for-guides-reviews-and-reports/?pageaction=displayproduct&productid=595. Published December 14, 2010. Accessed January 11, 2013
Maglione M, Maggard Gibbons M, Livhits M,  et al.  Bariatric surgery and nonsurgical therapy in adults with metabolic conditions and a body mass index of 30.0 to 34.9 kg/m²: comparative effectiveness review no. 82.  Rockville, MD: Agency for Healthcare Research and Quality; September 2012. AHRQ Publication 12-EHC139-EF
Higgins JPT, Green S, edsCochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. The Cochrane Collaboration, 2011. http://www.cochrane-handbook.org. Updated March 2011. Accessed April 15, 2013
Shea BJ, Grimshaw JM, Wells GA,  et al.  Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews.  BMC Med Res Methodol. 2007;7:10
PubMed   |  Link to Article
Shea BJ, Hamel C, Wells GA,  et al.  AMSTAR is a reliable and valid measurement tool to assess the methodological quality of systematic reviews.  J Clin Epidemiol. 2009;62(10):1013-1020
PubMed   |  Link to Article
Angrisani LF, Favretti F, Furbetta F,  et al.  Italian Group for Lap-Band System: results of multicenter study on patients with BMI < or =35 kg/m2 Obes Surg. 2004;14(3):415-418
PubMed   |  Link to Article
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PubMed   |  Link to Article
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PubMed   |  Link to Article
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PubMed   |  Link to Article
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PubMed   |  Link to Article
Sultan SP, Parikh M, Youn H, Kurian M, Fielding G, Ren C. Early US outcomes after laparoscopic adjustable gastric banding in patients with a body mass index less than 35 kg/m2 Surg Endosc. 2009;23(7):1569-1573
PubMed   |  Link to Article
Parikh MD, Duncombe J, Fielding GA. Laparoscopic adjustable gastric banding for patients with body mass index of < or =35 kg/m2 Surg Obes Relat Dis. 2006;2(5):518-522
PubMed   |  Link to Article
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PubMed
Lee WJW, Wang W, Lee YC, Huang MT, Ser KH, Chen JC. Effect of laparoscopic mini-gastric bypass for type 2 diabetes mellitus: comparison of BMI>35 and <35 kg/m2 J Gastrointest Surg. 2008;12(5):945-952
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PubMed   |  Link to Article
Choi JD, Digiorgi M, Milone L,  et al.  Outcomes of laparoscopic adjustable gastric banding in patients with low body mass index.  Surg Obes Relat Dis. 2010;6(4):367-371
PubMed   |  Link to Article
Chiellini CR, Rubino F, Castagneto M, Nanni G, Mingrone G. The effect of bilio-pancreatic diversion on type 2 diabetes in patients with BMI <35 kg/m2 Diabetologia. 2009;52(6):1027-1030
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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(2):143-148
PubMed   |  Link to Article
Boza C, Gamboa C, Viscido G,  et al.  Laparoscopic Roux-en-Y gastric bypass for the treatment of type 2 diabetes in patients with BMI below 35.  Obes Surg. 2010;20(8):1011
Frenken M, Cho EY. Metabolic intestinal bypass surgery for type 2 diabetes in patients with a BMI <35 kg/m2: comparative analysis of 16 patients undergoing either BPD, BPD-DS, or RYGB.  Obes Facts. 2011;4:(suppl 1)  13-17
PubMed   |  Link to Article
Lee WJ, Chong K, Chen CY,  et al.  Diabetes remission and insulin secretion after gastric bypass in patients with body mass index <35 kg/m2 Obes Surg. 2011;21(7):889-895
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Lembach H, Lanzarini E, Csendes A, Carlos Molina J, Braghetto I, Gutierrez L. Metabolic outcomes of sleeve gastrectomy in patients with impaired glucose metabolism.  Obes Surg. 2010;20(8):988
Ramos A, Neto MPG, Galvao M,  et al.  Metabolic bypass: initial experience with Roux-and-Y gastric bypass on type 2 diabetes treatments for non-morbid obese patients.  Obes Surg. 2010;20(8):1011-1012
Scopinaro N, Adami GF, Papadia FS,  et al.  The effects of biliopancreatic diversion on type 2 diabetes mellitus in patients with mild obesity (BMI 30-35 kg/m2) and simple overweight (BMI 25-30 kg/m2): a prospective controlled study.  Obes Surg. 2011;21(7):880-888
PubMed   |  Link to Article
Huang CK, Shabbir A, Lo CH, Tai CM, Chen YS, Houng JY. 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(9):1344-1349
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Abbatini F, Capoccia D, Casella G, Coccia F, Leonetti F, Basso N. Type 2 diabetes in obese patients with body mass index of 30-35 kg/m2: sleeve gastrectomy versus medical treatment.  Surg Obes Relat Dis. 2012;8(1):20-24
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PubMed   |  Link to Article
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PubMed   |  Link to Article
Pontiroli AE. Bariatric surgery for obese type 2 diabetes: do we have enough information?  Nutr Metab Cardiovasc Dis. 2012;22(9):e24-e25
PubMed   |  Link to Article
Laferrère B, Heshka S, Wang K,  et al.  Incretin levels and effect are markedly enhanced 1 month after Roux-en-Y gastric bypass surgery in obese patients with type 2 diabetes.  Diabetes Care. 2007;30(7):1709-1716
PubMed   |  Link to Article
Cummings DE, Overduin J, Shannon MH, Foster-Schubert KE.2004 ABS Consensus Conference.  Hormonal mechanisms of weight loss and diabetes resolution after bariatric surgery.  Surg Obes Relat Dis. 2005;1(3):358-368
PubMed   |  Link to Article
Korner J, Bessler M, Inabnet W, Taveras C, Holst JJ. Exaggerated glucagon-like peptide-1 and blunted glucose-dependent insulinotropic peptide secretion are associated with Roux-en-Y gastric bypass but not adjustable gastric banding.  Surg Obes Relat Dis. 2007;3(6):597-601
PubMed   |  Link to Article
Kashyap SR, Daud S, Kelly KR,  et al.  Acute effects of gastric bypass versus gastric restrictive surgery on beta-cell function and insulinotropic hormones in severely obese patients with type 2 diabetes.  Int J Obes (Lond). 2010;34(3):462-471
PubMed   |  Link to Article
Castagneto M, Mingrone G. The effect of gastrointestinal surgery on insulin resistance and insulin secretion.  Curr Atheroscler Rep. 2012;14(6):624-630
PubMed   |  Link to Article
Mingrone G. Role of the incretin system in the remission of type 2 diabetes following bariatric surgery.  Nutr Metab Cardiovasc Dis. 2008;18(8):574-579
PubMed   |  Link to Article
Leape LL, Park RE, Solomon DH, Chassin MR, Kosecoff J, Brook RH. Relation between surgeons' practice volumes and geographic variation in the rate of carotid endarterectomy.  N Engl J Med. 1989;321(10):653-657
PubMed   |  Link to Article
Adams TD, Davidson LE, Litwin SE,  et al.  Health benefits of gastric bypass surgery after 6 years.  JAMA. 2012;308(11):1122-1131
PubMed   |  Link to Article
Arterburn DE, Bogart A, Sherwood NE,  et al.  A multisite study of long-term remission and relapse of type 2 diabetes mellitus following gastric bypass.  Obes Surg. 2013;23(1):93-102
PubMed   |  Link to Article
Ludwig DS, Ebbeling CB, Livingston EH. Surgical vs lifestyle treatment for type 2 diabetes.  JAMA. 2012;308(10):981-982
PubMed   |  Link to Article
Sinha MK, Collazo-Clavell ML, Rule A,  et al.  Hyperoxaluric nephrolithiasis is a complication of Roux-en-Y gastric bypass surgery.  Kidney Int. 2007;72(1):100-107
PubMed   |  Link to Article
Slater GH, Ren CJ, Siegel N,  et al.  Serum fat-soluble vitamin deficiency and abnormal calcium metabolism after malabsorptive bariatric surgery.  J Gastrointest Surg. 2004;8(1):48-55discussion 54-55
PubMed   |  Link to Article
Juhasz-Pocsine K, Rudnicki SA, Archer RL, Harik SI. Neurologic complications of gastric bypass surgery for morbid obesity.  Neurology. 2007;68(21):1843-1850
PubMed   |  Link to Article
Pfeifer S. Another patient dies after Lap-Band surgery. Los Angeles Times. September 23, 2011. http://articles.latimes.com/2011/sep/23/business/la-fi-lap-band-death-20110924. Accessed December 10, 2012
Pfeifer S, Blankstein A. LAPD probes Lap-Band death. Los Angeles Times. April 06, 2012. http://articles.latimes.com/2012/apr/06/business/la-fi-get-thin-lapd-20120407. Accessed December 10, 2012

Figures

Tables

Table Graphic Jump LocationTable 1. Direct Comparison of Surgical vs Nonsurgical Interventions, Randomized Clinical Trials
Table Graphic Jump LocationTable 2. Observational Surgical Studies on Diabetes Outcomes by Surgery Typea
Table Graphic Jump LocationTable 3. Systematic Reviews on Nonsurgical Interventions Including Diabetes Medications

References

Buchwald HA, Avidor Y, Braunwald E,  et al.  Bariatric surgery: a systematic review and meta-analysis.  JAMA. 2004;292(14):1724-1737
PubMed   |  Link to Article
Sjöström CDL, Lissner L, Wedel H, Sjöström L. Reduction in incidence of diabetes, hypertension and lipid disturbances after intentional weight loss induced by bariatric surgery: the SOS Intervention Study.  Obes Res. 1999;7(5):477-484
PubMed   |  Link to Article
Mingrone G, Castagneto-Gissey L. Mechanisms of early improvement/resolution of type 2 diabetes after bariatric surgery.  Diabetes Metab. 2009;35(6 pt 2):518-523
PubMed   |  Link to Article
Gill RS, Birch DW, Shi X, Sharma AM, Karmali S. Sleeve gastrectomy and type 2 diabetes mellitus: a systematic review.  Surg Obes Relat Dis. 2010;6(6):707-713
PubMed   |  Link to Article
Maggard MA, Shugarman LR, Suttorp M,  et al.  Meta-analysis: surgical treatment of obesity.  Ann Intern Med. 2005;142(7):547-559
PubMed   |  Link to Article
Sjöström L, Peltonen M, Jacobson P,  et al.  Bariatric surgery and long-term cardiovascular events.  JAMA. 2012;307(1):56-65
PubMed   |  Link to Article
 Executive summary of the clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults.  Arch Intern Med. 1998;158(17):1855-1867
PubMed   |  Link to Article
Phurrough S, Salive ME, Brechner R, Meltzer A. Decision memo for surgery for diabetes (CAG-00497N). http://www.cms.gov/medicare-coverage-database/details/nca-decision-memo.aspx?NCAId=219. Published December 2, 2010. Accessed May 6, 2013
US Food and Drug Administration.  FDA expands use of banding system for weight loss. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm245617.htm. Published February 16, 2011. Updated March 3, 2011. Accessed April 15, 2013
Finks JF, Kole KL, Yenumula PR,  et al; Michigan Bariatric Surgery Collaborative, from the Center for Healthcare Outcomes and Policy.  Predicting risk for serious complications with bariatric surgery: results from the Michigan Bariatric Surgery Collaborative.  Ann Surg. 2011;254(4):633-640
PubMed   |  Link to Article
Padwal R, Klarenbach S, Wiebe N,  et al.  Bariatric surgery: a systematic review of the clinical and economic evidence.  J Gen Intern Med. 2011;26(10):1183-1194
PubMed   |  Link to Article
Colquitt JL, Picot J, Loveman E, Clegg AJ. Surgery for obesity.  Cochrane Database Syst Rev. 2009;(2):CD003641
PubMed
Lin VW, Wright A, Flum DR, Garrison LP Jr, Alfonso-Cristancho R, Sullivan SD. Patients' experience and outcomes after laparoscopic adjustable gastric banding in Washington state.  Surg Obes Relat Dis. 2012; April 14
PubMed
Kral JG, Christou NV, Flum DR,  et al.  Medicare and bariatric surgery.  Surg Obes Relat Dis. 2005;1(1):35-63
PubMed   |  Link to Article
Agency for Healthcare Research and Quality.  Research protocol—comparative effectiveness of bariatric surgery and nonsurgical therapy in adults with metabolic conditions and a body mass index of 30.0 to 34.9. http://effectivehealthcare.ahrq.gov/index.cfm/search-for-guides-reviews-and-reports/?pageaction=displayproduct&productid=595. Published December 14, 2010. Accessed January 11, 2013
Maglione M, Maggard Gibbons M, Livhits M,  et al.  Bariatric surgery and nonsurgical therapy in adults with metabolic conditions and a body mass index of 30.0 to 34.9 kg/m²: comparative effectiveness review no. 82.  Rockville, MD: Agency for Healthcare Research and Quality; September 2012. AHRQ Publication 12-EHC139-EF
Higgins JPT, Green S, edsCochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. The Cochrane Collaboration, 2011. http://www.cochrane-handbook.org. Updated March 2011. Accessed April 15, 2013
Shea BJ, Grimshaw JM, Wells GA,  et al.  Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews.  BMC Med Res Methodol. 2007;7:10
PubMed   |  Link to Article
Shea BJ, Hamel C, Wells GA,  et al.  AMSTAR is a reliable and valid measurement tool to assess the methodological quality of systematic reviews.  J Clin Epidemiol. 2009;62(10):1013-1020
PubMed   |  Link to Article
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Maggard-Gibbons M, Maglione M, Livhits M, et al. Bariatric surgery for weight loss and glycemic control in nonmorbidly obese adults with diabetes: a systematic review. JAMA. doi:10.1001/jama.2013.4851

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eTable 1. Cochrane risk of bias of randomized clinical trials of bariatric surgery

eTable 2. Descriptive table for observational surgical data by study level

eTable 3. Adverse events following bariatric surgery in patients with BMI 30-35 kg/m2: by individual study level

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