ORIGINAL CONTRIBUTIONS

Resolution of Diabetes After Bariatric SurgeryAmong Predominantly African-American PatientsRace has no Effect in Remission of Diabetes After Bariatric Surgery

Mereb Araia & Michael Wood & Joshua Kroll &Abdul Abou-Samra & Berhane Seyoum

# Springer Science+Business Media New York 2014

AbstractBackground The aim of this study was to assess the relativeefficacy in diabetes remission among predominantly African-American patients who have undergone one of the threedifferent types of bariatric surgical procedures.Methods A total of 597 morbidly obese patients underwentone of the three bariatric surgical procedures at Harper Uni-versity Hospital, Detroit, Michigan from 2008 to 2011. Of thethree procedures, 203 (34 %) patients had laparoscopic sleevegastrectomy, 264 (44.2 %) patients had laparoscopic gastricbypass, and 130 (21.8 %) had laparoscopic adjustable gastricbanding. The prevalence of diabetes prior to surgery was 20.7,17.4, and 24 %, respectively. There was no statistical differ-ence in the prevalence of diabetes among the three surgicalgroups.Results Of the 119 patients with diabetes, 46 (38.7 %) weremales and 73 (61.3 %) were females. The majority of patientswere African-Americans (65 %). The average age of patientswas 42.2±8.3 years for sleeve gastrectomy, 44.8±7.9 yearsfor gastric banding, and 41.5±7.7 years for gastric bypasssurgery. Of all the study patients with a preoperative diagnosisof type 2 diabetes, 86 patients (72.3 %) had resolution ofdiabetes 1 year after surgery. The resolution of diabetes wasreported in 89.1, 66.7, and 54.8 % of patients who underwent

laparoscopic gastric bypass, sleeve gastrectomy, and gastricbanding, respectively.Conclusions This study, which was conducted among pre-dominantly African-Americans, showed consistent resultswith other studies. Patients who underwent laparoscopic gas-tric bypass appeared to benefit the most in terms of achievingbetter remission of diabetes.

Keywords Diabetes . African-Americans . Bariatric surgery

Introduction

Obesity is a major risk factor in the development of type 2diabetes mellitus (T2DM). The risk is proportional to thedegree of body mass index (BMI) and the duration of obesity.Because of the strong link with obesity, the term “diabesity”has been coined to describe these two disease processes [1].Several studies report that obesity and T2DM are highlyassociated [2]. Over 80 % of the patients with T2DM in theUSA are overweight or obese [3].

Effective lifestyle changes that result in significant weightloss is essential to the long-term treatment of T2DM. It hasbeen shown that weight loss as little as 5–10 % improvesglycemic control and reduces the requirements for antidiabeticmedication. In addition to hyperglycemia, diabetes is charac-terized by specific (microvascular) or nonspecific(cardiovascular) complications. To prevent such complica-tions, blood sugar control alone is not enough. It needs anextensive management plan that includes treating the othercomponents of metabolic syndrome such as hypertension anddyslipidemia to having more stringent goals than those with-out diabetes [4]. Besides the remission and improvement ofdiabetes, weight loss has other numerous benefits. Modestweight loss lowers blood pressure, improves dyslipidemia,and is associated with reduced T2DM-related morbidity and

M. Araia :M. Wood : J. KrollHarper Bariatric Medicine Institute, Harper University Hospital,Wayne State University School of Medicine, 4201 St. Antoine,UHC-4H, Detroit, MI 48201, USA

A. Abou-SamraHamad Medical Corporation, Doha, Qatar

B. Seyoum (*)Division of Endocrinology, Wayne State University School ofMedicine, 4201 St. Antoine, UHC-4H, Detroit, MI 48201, USAe-mail: bseyoum@med.wayne.edu

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mortality. The most significant challenge however is how toachieve and maintain weight loss in obese patients with dia-betes. Compliance and maintenance of lifestyle modificationshave been disappointing [1].

Bariatric surgery, or as some people call it metabolic sur-gery, has emerged as one of the most effective treatment forobesity. This surgery not only reduces body weight but alsoproduces sustained weight loss and improvement in manyobesity-related conditions, including diabetes and other com-ponents of metabolic syndrome. Bariatric surgery has beenshown to produce a loss of 48–70 % excess body weight inmost patients [5]. This surgery has become a beacon of hopeamong morbidly obese patents in achieving and maintainingweight loss.

Diabetes remission observed among patients who had bar-iatric surgery does not directly correlate with the amount ofweight loss. While weight loss is the recommended first-linemanagement of metabolic syndrome, it cannot account fullyfor the rapid results seen after bariatric surgery. In somepatients, glucose levels have been seen to drop to normallevels in the first 2–3 days post surgery, which clearly suggestthe presence of other factors that play a major role in changingthe metabolic milieu [6, 7].

The rate of remission of T2DM is higher after gastricbypass than after banding or other procedures. Many considerit as the gold standard bariatric procedure for achieving dia-betes remission. The remission rate after this type of bariatricsurgery ranges from 67 to 90 % [8–10]. Remission rates inpurely restrictive procedures are directly proportional to thedegree of weight loss. However, in procedures with an addi-tional malabsorptive component such as the bypass of theduodenum and jejunum, the reduction of blood sugar levelsand the improvement in glucose tolerance and insulin actionare remarkable. As a result of this concept, some authorssuggest that the proximal gut might play a major role in thepathogenesis of T2DM [11].

The most common surgical procedure for treating obesityin the USA is the laparoscopic Roux-en-Y gastric bypass(RYGB) with an estimated 180,000 operations performedeach year. As with any surgical procedure, gastric surgeryinvolves risks such as bleeding, infection, and reactions toanesthesia. The reported risk of death from bariatric surgery is0.1 to 2 % [12].

According to the 2009 consensus document, partial remis-sion of diabetes is defined as a subdiabetic hyperglycemia(HbA1c not diagnostic of diabetes (<6.5 %), fasting glucose100–125 mg/dl for at least 1-year duration in the absence ofactive pharmacologic therapy). We used this definition todetermine the remission of diabetes among predominantlyAfrican-American patients who have undergone the threecommonly performed bariatric surgical procedures [4]. Thisretrospective study with some prospective data gathering wasconducted to assess the relative efficacy of the three main

bariatric surgical procedures that were performedlaparoscopically: sleeve gastrectomy, Roux-en-Y gastric by-pass, and gastric banding, in the remission and treatment ofT2DM among predominantly African-American patients.

Patients and Methods

Patient Selection

We reviewed the medical records of all patients who haveundergone bariatric surgery during a 3-year period (2008 to2011) at Harper Bariatric Medicine Institute, Harper Univer-sity Hospital, Detroit, Michigan, USA. The inclusion criteriawe used was that set by the NIH for bariatric surgery (age>16years, BMI>35 kg/m2 with ≥1 existing comorbidity or BMI≥40 kg/m2 and a history of prolonged previous attempts ofweight loss by other means [13]).

A total of 597 patients who fulfilled the inclusion criteriawere included in this analysis. Of these, 119 patients haddiabetes prior to surgery. Patients were followed for 2–3weekspostoperatively, then every 3 months for the first year.

In order to reduce potential variations in surgical methods,we only included all surgical procedures that were performedby a single surgeon (MW). A thorough assessment was per-formed on each patient’s general condition and mental status,complications of diabetes, risk factors, and motivations forsurgery. The surgeon clinically evaluated all patients, and amedical practitioner conducted a preoperative assessment. Ateam that included a nutritionist, a psychologist, and an exer-cise consultant followed all patients before and after surgery.Baseline demographic data were collected on each patientincluded in the study. Those patients who failed to presentfor follow-up appointments following surgery were consid-ered dropouts and were removed from the study. There were atotal of eight patients who were excluded because they did nothave follow-up after surgery. The study was approved by theWayne State University School of Medicine institutional re-view board.

Types of Bariatric Surgery

Roux-en-Y Gastric Bypass

The Roux-en-Y gastric bypass (RYGBP) is a combined bar-iatric procedure, already being accepted as a standard in theUSA and seeing expanded use in Europe as well [14, 15]. Thefirst step in the procedure uses staples to divide the stomachinto a small pouch with an approximate volume of 20–30 ml.The second step is the bypass where the jejunum is connectedto the pouch. Bowel continuity is restored by an entero-enteroanastomosis, between the excluded biliary limb and the

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alimentary limb, performed at about 100 cm from thegastrojejunostomy.

Sleeve Gastrectomy

This is a restrictive procedure that reduces the volume of thestomach to approximately 10 % of its original size, leaving onaverage a sleeve remnant with a volume of 100 ml. The largestomach curve is separated from the omentum majus [16].During the procedure, a gastric tube (32–34 F) is placed intothe stomach to allow safe and exact formation of the sleeve.The resection is performed using staples. The resected part ofthe stomach is removed from the abdominal cavity.

Gastric Banding

This is one of the least invasive restrictive bariatric proceduresas no staples/incisions are placed in the stomach. The band isplaced around the fundus of the stomach immediately belowthe esophagogastric junction to create a small pouch, whichlimits the amount of food eaten at one time. The band isconnected to an access port that is under the skin of theabdomen [16, 17] and can be tightened by placing a needleinto the port and filling the balloon (band) with saline.

Statistical Analysis

SPSS software (SPSS Institute Inc, Chicago, IL, USA) wasused for all statistical analyses. Data were analyzed as mean±standard deviation (SD) for continuous variables and as fre-quency and percentage of study population for categoricalvariables. Chi-square tests were used to explore the univariaterelationships among categorical variables. Statistical signifi-cance was set at P<0.05 for all tests. Logistic regressionanalysis was conducted to determine the effect of age, race,duration of diabetes, and presurgical BMI on the outcome ofsurgery.

Results

Of the 119 patients with diabetes prior to surgery, 72.3 % hadresolution of their diabetes at the 1-year post-surgery mark.The prevalence of T2DM prior to surgery was 20.7 % forsleeve gastrectomy, 17.4 % for gastric bypass, and 24 % forgastric banding. Those who underwent the gastric bypassprocedure had the highest rate of diabetes resolution.

Of those patients with diabetes who underwent gastricbypass, sleeve gastrectomy, and gastric banding, 89.1, 66.7,and 54.8 % of patients respectively had resolution of theirdiabetes in the 1-year period (Fig. 1). A dramatic remission ofdiabetes was noted during the first few days immediately aftersurgery before patients were discharged from the hospital.

During these early days post surgery, all patients irrespectiveof the type of surgical procedure shared remarkable remissionof diabetes in the range of 20–35 %. However, subsequently,patients who had RYGBP surgery continued to show moreremission of diabetes than those of the other two groups(Fig. 2).

There was a larger percentage of female than male patientsdiagnosed with diabetes prior to surgery; 48 (38.7 %) patientswere males, and 73 (61.3 %) patients were females. Addition-ally, more females underwent surgery for obesity: of thosewho underwent sleeve gastrectomy, 64.3 % were females and35.7 % were males; of those who underwent gastric bypass,60.9 % were females and 39.1 % were males; and of thosewho had gastric banding, 58.1 % were females and 41.9 %were males. The average ages at the time of surgery for thethree procedures, 42.2±8.3 years for sleeve gastrectomy, 44.8±7.9 years for gastric banding, and 41.5±7.7 years for gastricbypass, were not significantly different.

The highest average HbA1c value before surgery wasfound among patients who have undergone gastric banding

*P<0.001

*P<0.01

*P>0.05

Fig. 1 Resolution of diabetes in the 1-year duration

p<0.001

Fig. 2 Remission of diabetes

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procedure, but the difference was not statistically significantfrom the others. The overall mean HbA1c prior to surgery was8.3±1.8 % and 1 year post surgery was 6.3±0.7 %. Forpatients who underwent gastric bypass, the presurgical HbA1cwas 7.6±1.2 % and 1 year post surgery was 5.9±0.7 %. Forpatients who have undergone sleeve gastrectomy, thepresurgical HbA1c was 8.2±1.8 % and 1 year post surgerywas 6.2±0.7 %.

Patients who had undergone gastric bypass surgery had thehighest average BMI prior to surgery, 56.4±6.8 kg/m2 versus53.2±7.2 kg/m2 for sleeve gastrectomy and 51.8±7.3 kg/m2

for gastric banding; however, these values are not statisticallydifferent. One year after surgery, all patients lost weight. Theaverage BMI dropped to 44.6±5.9, 41.9±7.3, and 40.8±6.9 kg/m2 in patients who have undergone gastric bypass,sleeve gastrectomy, and gastric banding, respectively (allvalues are SD; Table 1).

Logistic regression analysis done to determine the effect ofage, race, duration of diabetes, and presurgical BMI showedno effect in the outcome of surgery. Similar to other reports,patients who have undergone bypass surgery irrespective oftheir age, gender, BMI, duration of diabetes, or race were ableto have significant remission of diabetes [6, 18].

Discussion

Our study, which was conducted among a predominantlyAfrican-American population, showed similar results of dia-betes remission after bariatric surgery to what has been report-ed in the literature [18–20]. Moreover, our study furtherconfirmed that RYGB surgery which diverts ingested nutri-ents from passage through the upper gastrointestinal tractshowed a much higher remission of diabetes than the othersurgical procedures that restrict the size of the stomach such asgastric banding or sleeve gastrectomy. According to the meta-analysis done byGloy et al. [21], bariatric surgery achieved 22

times higher (relative risk 22.1 (3.2 to 154.3), P=0.002)diabetes remission compared to nonsurgical treatment.Among the surgical interventions, bypass surgery has beenshown to exceed the other surgical procedures. It is the mosteffective, safe, and reliable method for combating morbidobesity. Besides achieving 60–80 % of excess body weightloss [22, 23], over 80 % of the patients with diabetes who hadundergone gastric bypass have gone into remission, achievingnormal HbA1c without any treatment [20, 24]. Our resultsconcur with these findings.

Our study also confirmed that diabetes remission reportedduring the first few days immediately after surgery is indepen-dent of weight loss. Interestingly, all patients irrespective of thetype of surgical procedures shared dramatic remission of dia-betes in the range of 20–35 %, which is similar to the otherstudies [25]. However, after discharge in the subsequent weeksand months, patients who have undergone RYGB continued toshow more and significant improvements in diabetes remissioncompared to patients of other surgery types (Fig. 2).

Bariatric surgery is markedly more efficient than the usualcare in the management of obese patients with T2DM. Whileweight loss by any modality leads to improved glucose me-tabolism and decreased insulin resistance, bariatric surgery isan established means to achieve marked and persistent weightloss, leading to reversal of diabetes inmany cases [26, 27]. It isknown that shortly after bariatric surgical procedures, patientscan only consume 575±146 kcal/day. This “fasting” effectcan cause a rapid decline in weight and an upregulation ofinsulin receptors located on cell membranes in the muscleand adipose tissue that lead to significant improvement ininsulin resistance. However, the dramatic improvement indiabetes control seen in the early postoperative periods isbeyond the effects of weight reduction specially as is seenin the patients who have undergone RYGB surgery. Subse-quently however, the improved glucose metabolism andresolution of T2DM can be associated with the weight loss(~62 % of their excess weight).

Table 1 Patient characteristic before and after surgery

Characteristics Gastric bypass(n=264)

Sleeve gastrectomy(n=203)

Gastric banding(n=130)

All patients(n=597)

P value

Prevalence of DM, n (%) 46 (17.4) 42 (20.7) 31 (23.8) 119 >0.05

DM resolution, n (%) 41 (89.1) 28 (66.7) 17 (54.8) 86 <0.001

Mean age, years 41.5±7.7 42.2±8.3 44.8±7.9 42.6±8.0 >0.05

Gender, M/F 18/28 15/27 13/18 46/73 >0.05

Duration of diabetes before surgery (years±SE) 4.9±0.4 6.2±0.9 3.6±0.3 4.8±0.3 <0.05

HbA1c before surgery 7.6±1.2 8.2±1.8 8.3±1.8 8.0±1.5 >0.05

HbA1c 1 year after surgery 5.9±0.7 6.2±0.7 6.3±0.7 6.1±0.7 >0.05

BMI (kg/m2) before surgery 56.4±6.8 53.2±7.2 51.8±7.3 54.1±7.3 >0.05

BMI (kg/m2) 1 year after surgery 44.6±5.9 41.9±7.3 40.8±6.9 42.6±6.8 >0.05

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There are two prevailing theories that could possibly ex-plain the dramatic remission of diabetes after surgery. Theseare the foregut and hindgut theories. The foregut theory statesthat it is the overstimulation of the foregut (stomach, duode-num, and jejunum) that is the important causative factor inT2DM. Therefore, operations that bypass this area will resultin decreased stimulation of the foregut, resulting in improvedglycemic control. The current study of diabetes remissionrates secondary to various bariatric surgeries provides anadditional impetus to the prevailing understanding of themechanisms that the various surgical procedures exert theirbeneficial effects separately. The hindgut theory postulatesthat the increased stimulation of the distal small bowel is theresponsible factor. By facilitating the presentation of intestinalcontents to the ileum, incretin release, including GLP-1 andother peptide mediators, is enhanced, resulting in T2DMimprovement [13, 28].

Several studies attribute the early metabolic effects ofRYGB to alterations that resulted from bypass of the foregutand greater improvement in glucose tolerance and insulinresponses as compared to the effects of gastric banding [6,29]. In the sleeve gastrectomy procedure, a similar rapidimprovement in insulin resistance and diabetes remission bypartial stomach resection occurs with the absence of foregutbypass, leaning towards the hindgut theory [29].

Studies have shown that with improved glycemic control,each 1 % decrease in HbA1c decreases T2DM-related deathsby 21 % [26]. Furthermore, the improvement in glycemiccontrol results in an overall reduction of dollar amount spenton diabetes-related complications. Other reports have sug-gested that individuals with obesity-related complicationshave medical costs that are 42 % greater than normal-weightindividuals. Extreme obesity (BMI>40 kg/m2) engenderseven greater costs [30]. The overall cost of diabetes is alsosubstantially high. The estimated total economic cost of dia-betes in the USA in 2012 was US$245 billion, of whichUS$176 billion represents direct health care expenditure andUS$69 billion represents loss of productivity [31]. Cost effec-tiveness of bariatric surgery tends to increase over the yearsbecause the direct costs related to the procedure will be dilutedover time, whereas the cost savings related to reduction ofantidiabetic medications tend to accumulate [32]. Other stud-ies have shown that bariatric surgery provides cost-effectivemethods of reducing mortality and diabetes complications inseverely obese adults with diabetes [1, 33]. Such understand-ing is important because it will allow the identification of thepersons who are the most appropriate candidates for surgery.

Our study has significant limitations. We were not able toinclude socioeconomic impacts in the overall remission ofdiabetes after bariatric surgery. Moreover, as this is mainlyretrospective data, it has its own inherent limitations. However,the study has shown consistent results, in line with the reportsin the literature. The causes of T2DM are multifactorial, and

the mechanisms by which it can be treated or prevented are aswell complex. Bariatric surgery has the potential to be aneffective treatment option in all populations includingAfrican-Americans. In conclusion, in this study, we showedthat bariatric surgery is effective in reversing diabetes. More-over, it looks that race has no effect in the remission of diabetesafter bariatric surgery. However, this has to be confirmed in alarger prospective study. We recognize that the number ofsubjects included in this study is very low, which is a substan-tial shortcoming by itself.

Conflict of Interest All authors have no conflict of interest, and therewas no external funding for the study.

References

1. Arroyo K, Kini SU, Harvey JE, et al. Surgical therapy for diabesity.Mt Sinai J Med. 2010;77(5):418–30.

2. Mokdad AH, Ford ES, Bowman BA, et al. Prevalence of obesity,diabetes, and obesity-related health risk factors, 2001. JAMA.2003;289(1):76–9.

3. Mokdad AH, Ford ES, Bowman BA, et al. Diabetes trends in theU.S.: 1990-1998. Diabetes Care. 2000;23(9):1278–83.

4. Buse JB, Caprio S, Cefalu WT, et al. How do we define cure ofdiabetes? Diabetes Care. 2009;32(11):2133–5.

5. Gumbs AA, Modlin IM, Ballantyne GH. Changes in insulin resis-tance following bariatric surgery: role of caloric restriction andweight loss. Obes Surg. 2005;15(4):462–73.

6. Lee WJ, Huang MT, WangW, et al. Effects of obesity surgery on themetabolic syndrome. Arch Surg. 2004;139(10):1088–92.

7. Pournaras DJ, Aasheim ET, Sovik TT, et al. Effect of the definition oftype II diabetes remission in the evaluation of bariatric surgery formetabolic disorders. Br J Surg. 2012;99(1):100–3.

8. Milone M, Di Minno MN, Leongito M, et al. Bariatric surgery anddiabetes remission: sleeve gastrectomy ormini-gastric bypass?WorldJ Gastroenterol. 2013;19(39):6590–7.

9. Albeladi B, Bourbao-Tournois C, Huten N. Short- and midtermresults between laparoscopic Roux-en-Y gastric bypass and laparo-scopic sleeve gastrectomy for the treatment of morbid obesity. JObes. 2013;2013:934653.

10. Yip S, Plank LD, Murphy R. Gastric bypass and sleeve gastrectomyfor type 2 diabetes: a systematic review and meta-analysis of out-comes. Obes Surg. 2013;23(12):1994–2003.

11. Mingrone G. Role of the incretin system in the remission of type 2diabetes following bariatric surgery. Nutr Metab Cardiovasc Dis.2008;18(8):574–9.

12. Franco JV, Ruiz PA, PalermoM, et al. A review of studies comparingthree laparoscopic procedures in bariatric surgery: sleeve gastrecto-my, Roux-en-Y gastric bypass and adjustable gastric banding. ObesSurg. 2011;21(9):1458–68.

13. Mingrone G, Castagneto-Gissey L. Mechanisms of earlyimprovement/resolution of type 2 diabetes after bariatric surgery.Diabetes Metab. 2009;35(6 Pt 2):518–23.

14. Campos GM, Rabl C, Roll GR, et al. Better weight loss, resolution ofdiabetes, and quality of life for laparoscopic gastric bypass vsbanding: results of a 2-cohort pair-matched study. Arch Surg.2011;146(2):149–55.

15. Suter M, Giusti V, Heraief E, et al. Laparoscopic Roux-en-Y gastricbypass: initial 2-year experience. Surg Endosc. 2003;17(4):603–9.

OBES SURG

16. Ponce J, Haynes B, Paynter S, et al. Effect of lap-band-inducedweight loss on type 2 diabetes mellitus and hypertension. ObesSurg. 2004;14(10):1335–42.

17. Dixon JB, O'Brien PE, Playfair J, et al. Adjustable gastric bandingand conventional therapy for type 2 diabetes: a randomized con-trolled trial. JAMA. 2008;299(3):316–23.

18. Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopicRoux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg.2003;238(4):467–84. discussion 484-465.

19. Buchwald H, Estok R, Fahrbach K, et al. Weight and type 2 diabetesafter bariatric surgery: systematic review and meta-analysis. Am JMed. 2009;122(3):248–56. e245.

20. Pories WJ, Swanson MS, MacDonald KG, et al. Who would havethought it? An operation proves to be the most effective therapy foradult-onset diabetes mellitus. Ann Surg. 1995;222(3):339–50. dis-cussion 350-332.

21. Gloy VL, Briel M, Bhatt DL, et al. Bariatric surgery versus non-surgical treatment for obesity: a systematic review and meta-analysisof randomised controlled trials. BMJ. 2013;347:f5934.

22. DeMaria EJ, Sugerman HJ, Kellum JM, et al. Results of 281 consec-utive total laparoscopic Roux-en-Y gastric bypasses to treat morbidobesity. Ann Surg. 2002;235(5):640–5. discussion 645-647.

23. Schauer PR, Ikramuddin S, Gourash W, et al. Outcomes after lapa-roscopic Roux-en-Y gastric bypass for morbid obesity. Ann Surg.2000;232(4):515–29.

24. Buchwald H, Avidor Y, Braunwald E, et al. Bariatric surgery: asystematic review and meta-analysis. JAMA. 2004;292(14):1724–37.

25. Bradley D, Conte C, Mittendorfer B, et al. Gastric bypass andbanding equally improve insulin sensitivity and beta cell function. JClin Invest. 2012;122(12):4667–74.

26. de la Cruz-Munoz N, Messiah SE, Arheart KL, et al. Bariatricsurgery significantly decreases the prevalence of type 2 dia-betes mellitus and pre-diabetes among morbidly obese multi-ethnic adults: long-term results. J Am Coll Surg. 2011;212(4):505–11. discussion 512-503.

27. Smith Jr SC. Multiple risk factors for cardiovascular disease anddiabetes mellitus. Am J Med. 2007;120(3 Suppl 1):S3–11.

28. Gu YC, Yu JC. Mechanisms of gastrointestinal surgery in treatmentof type 2 diabetes. Zhongguo Yi Xue Ke Xue Yuan Xue Bao.2011;33(3):262–4.

29. Rizzello M, Abbatini F, Casella G, et al. Early postoperative insulin-resistance changes after sleeve gastrectomy. Obes Surg. 2010;20(1):50–5.

30. Myers VH, McVay MA, Adams CE, et al. Actual medical andpharmacy costs for bariatric surgery: 6-year follow-up. South MedJ. 2012;105(10):530–7.

31. Herman WH. The economic costs of diabetes: is it time for a newtreatment paradigm? Diabetes Care. 2013;36(4):775–6.

32. Terranova L, Busetto L, Vestri A, et al. Bariatric surgery:cost-effectiveness and budget impact. Obes Surg. 2012;22(4):646–53.

33. Hoerger TJ, Zhang P, Segel JE, et al. Cost-effectiveness of bariatricsurgery for severely obese adults with diabetes. Diabetes Care.2010;33(9):1933–9.

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