clinical study comparison of the effectiveness of four

Clinical StudyComparison of the Effectiveness of Four BariatricSurgery Procedures in Obese Patients with Type 2 DiabetesA Retrospective Study

Sylvie Pham1 Antoine Gancel1 Michel Scotte2 Estelle Houivet3 Emmanuel Huet2

Herveacute Lefebvre14 Jean-Marc Kuhn14 and Gaetan Prevost14

1 Department of Endocrinology Diabetes and Metabolic Diseases University Hospital of Rouen 76031 Rouen France2Department of Digestive Surgery University Hospital of Rouen 76031 Rouen France3 Department of Biostatistics University Hospital of Rouen Institut de Recherche et drsquoInnovation BiomedicaleNormandie University 76031 Rouen France

4 INSERM U982 Neuronal and Neuroendocrine Differentiation and CommunicationInstitut de Recherche et drsquoInnovation Biomedicale Normandie University University of Rouen 76821 Mont Saint Aignan France

Correspondence should be addressed to Gaetan Prevost gaetanprevostchu-rouenfr

Received 25 November 2013 Accepted 23 April 2014 Published 22 May 2014

Academic Editor Francesco Saverio Papadia

Copyright copy 2014 Sylvie Pham et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Aim The aim of the present retrospective study was to evaluate the efficacy of four bariatric surgical procedures to induce diabetesremission and lower cardiovascular risk factors in diabetic obese patients Moreover the influence of surgery onweight evolution inthe diabetic population was compared with that observed in a nondiabetic matched populationMethods Among 970 patients whowere operated on in our center since 2001 81 patients were identified as type 2 diabetes Laparoscopic adjustable gastric banding(GB) intervention type Mason (MA) gastric bypass (RYGB) and sleeve gastrectomy (SG) were performed respectively in 2517 28 and 30 of this diabetic population ResultsThe resolution rate of diabetes one year after surgery was significantly higherafter SG than GB (625 versus 20 119875 lt 001) but not significantly different between SG and RYGB In terms of LDL-cholesterolreduction RYGB was equivalent to SG and superior to CGMA or GB Considering the other cardiovascular risk factors therewas no significant difference according to surgical procedures The weight loss was not statistically different between diabetic andnondiabetic matched patients regardless of the surgical procedures used Conclusion Our data confirm that the efficacy of surgeryto treat diabetes is variable among the diverse procedures and SG might be an interesting option in this context

1 Introduction

Bariatric surgery has proven to be a treatment of choicefor morbid obesity [1 2] It is recommended for patientswith body mass index (BMI) above 40 kgm2 or higher than35 kgm2 when associated with comorbidities which includethe different components of metabolic syndrome and type 2diabetes [3 4] Weight loss obtained after bariatric surgeryis associated with a highly significant reduction in cardio-vascular risk factors [5ndash7] More recently improvement orremission of diabetes has been observed following bariatricsurgery in obese patients with type 2 diabetes and mortalityrate linked to diabetes was consequently significantly reduced

[1 2 8ndash12]Weight loss induced by bariatric surgery is amajorfactor of diabetes improvement [11 13] However in severalstudies the resolution of diabetes has often been observedbefore a significant weight loss has been obtained [14ndash17]Theearly postsurgical improvement of diabetes suggested amajorphysiopathological role for changes in gut hormone secretion[18] As amatter of fact a decrease in plasma levels of ghrelinan orexigenic peptide has been described following gastricbypass for morbid obesity [19ndash22] The involvement of otherintestinal peptides like GLP-1 (hindgut hypothesis) [23ndash26]and neuropeptide YY [22 27ndash30] or a decreased secretionof anti-incretin hormones (foregut hypothesis) [31 32] hasbeen proposed to explain the rapid remission of diabetes

Hindawi Publishing CorporationJournal of ObesityVolume 2014 Article ID 638203 7 pageshttpdxdoiorg1011552014638203

2 Journal of Obesity

after bariatric surgery Otherwise Roux-en-Y bypass (RYGB)that excludes the duodenum from the nutrimentsrsquo route andprofoundly modifies the gut microbial metabolic cross-talk[33] has been shown to improve insulin resistance morerapidly than sleeve gastrectomy [15]

These observations raised the question of the choiceof chirurgical procedure for treating diabetes Most studieshave compared two by two procedures Using this approachRYGB and sleeve gastrectomy (SG) seem to be more efficientfor treating diabetes than gastric banding (GB) Howeverthese studies failed to provide clear conclusions owing to thegreat heterogeneity of the results For instance dependingon the mode of surgery used (restrictive malabsorptive orcombined) and study design the diabetes remission ratevaried from 45 to 97 of patients [5 9 12 34ndash39] In ourcenter four surgical procedures have been used for the last15 years to treat obesity GB SG calibrated gastrectomytype Mason (CGMa) and RYGB The aim of the presentretrospective study was to evaluate the efficacy of thesefour procedures to induce diabetes remission and lowercardiovascular risk factorsMoreover the influence of surgeryon weight evolution in the diabetic population was comparedwith that observed in a nondiabetic population matched forsex age BMI and surgical procedure

2 Patients and Methods

We have conducted a retrospective case-control comparativestudy aimed at evaluating the impact of bariatric surgery ontype 2 diabetes Among 970 patients who underwent bariatricsurgery in our center since 2001 81 patients were identifiedas type 2 diabetic (ICD coding) All patients had undergonea medical supervised therapy for weight loss for at least 12months before bariatric surgery

Preoperatively they were evaluated for medical or surgi-cal history and treatment usedwas recordedA clinical exam-ination was performed and risk factors and comorbiditiesincluding arterial hypertension and sleep apnoea syndromewere collectedThe serum levels of biologicalmarkers (fastingglycemia glycosylated hemoglobin total cholesterol HDL-and LDL-cholesterol and triglycerides) were measured

Then one of the four following surgical procedures wasused GB (20 patients) CGMa (14 patients) SG (24 patients)and RYGB (23 patients)

After surgery the weight change could be followed for 24months and biological parameters for 12 months 23 of thepatients were lost for follow-up

The weight changes in patients with diabetes were alsocompared to those observed in obese patients without dia-betes and matched for age sex BMI and type of surgery

3 Statistical Analysis

The evolution of diabetes has been chosen as the primary endpoint of the study It was evaluated on the basis of a score ofeffectiveness Remission of diabetes (score 1) was defined asHbA1c level lower than 65 and interruption of antidiabetictreatment Improvement (score 2) was defined as either a

Months

Wei

ght (

kg)

80

90

100

110

120

130

140

Base 3 6 12 24

Figure 1 Overall changes in weight (mean plusmn SEM) in patientstreated with bariatric surgery (Δ) obese patients without diabetes(◼) obese patients with type 2 diabetes

decrease in HbA1c level or a reduction in the antidiabetictreatment Score 3 corresponded to a stabilisation of diabetesand score 4 to a degradation of the glycaemic pattern As thelatter is a qualitative parameter statistical analysis of the dataused a 1205942 test Similar scores and statistical procedures wereused to evaluate the changes in the following comorbiditiesarterial hypertension sleep apnoea syndrome and serumlipid pattern

The serum HbA1c levels measured respectively beforeand 6 to 12 months after surgery were compared with theWilcoxon test The nonparametric test of Kruskal Wallis wasused to evaluate this biological parameter as a function of thetype of surgery employed

Theweight changes were initially analysed using ANOVAfor two factors time and type of surgery Depending on theresults of this first analysis a second statistical evaluationusing an ANOVA for one factor (type of surgery) wasperformed Complementary tests of comparison two by two(Newman and Keuls) were done for the different time pointswhere ANOVA (one factor) was statistically significant

Statistical analyses were performed with Statview soft-ware (5th version SAS Institute North Carolina) Statisticalsignificance was considered for a 120572 risk of 5

4 Results

Themain characteristics of diabetic patients are summarizedin Table 1 The mean diabetes duration was 8 plusmn 8 yearsAccording to WHO criteria 67 patients (827) harboureda profile of metabolic syndrome The number of patientswith cardiovascular risk factors was similar whatever thetype of surgery performed 38 of the patients suffered frommicro- andor macrovascular complications of diabetes and24 (296) complained of signs of depression 10 patientsweretreated by diet alone 44 patients (54) by oral antidiabeticdrugs (OAD) 7 by insulin and 25 by OAD plus insulin

Bariatric surgery induced a significant (119875 lt 0001) weightloss in both groups of obese patients (Figure 1) One yearafter surgery weight was reduced by 307 plusmn 21 and 372 plusmn26 kg in patients with and without diabetes respectively

Journal of Obesity 3

Table 1 Baseline characteristics of the obese patients with type 2 diabetes

GB CGMa SG RYGBNumber of patients 20 14 24 23Mean age (years) 44 46 48 45Mean BMI (kgm2) 46 52 52 46Arterial hypertension119873 () 14 (70) 10 (71) 18 (75) 19 (83)Hypertriglyceridemia119873 () 13 (65) 7 (50) 10 (42) 13 (57)Hypercholesterolemia119873 () 14 (70) 10 (71) 14 (58) 10 (43)Metabolic syndrome119873 () 17 (85) 10 (71) 22 (92) 18 (78)Sleep apnoea syndrome119873 () 6 (30) 10 (71) 14 (58) 10 (43)

Wei

ght (

kg)

Months

800

900

1000

1100

1200

1300

1400

1500

Base 3 6 12 24

a b c d

Figure 2 Changes in weight (mean plusmn SEM) induced by the differenttypes of bariatric surgery procedures in obese diabetic patients(Δ) gastric banding (GB) (o) calibrated gastrectomy type Mason(CGMa) (998771) sleeve gastrectomy (SG) (◼) Roux-en-Y gastric bypass(RYGB) a

119875 lt 005 CGMa versus GB b119875 lt 005 SG versus GB

c119875 lt 005 CGMa versus RYGB d

119875 lt 005 SG versus RYGB

(Figure 1) Basal weight before surgery was significantlydifferent according to the surgical procedure (119875 = 0002)(Figure 2) so further ANOVA analysis has been performedon the weight difference A significant weight loss (119875 lt001) was obtained after each surgical procedure reaching260 plusmn 20 (minus67 plusmn 46 kg GB) 280 plusmn 16 (minus278 plusmn 54 kgCGMa) 410 plusmn 33 (minus322 plusmn 50 kg SG) and 430 plusmn 29(minus282 plusmn 45 kg RYGB) of the initial weight on month sixafter surgery Repeated measure ANOVA analysis (time timessurgical procedure) revealed significant differences betweenthe weight loss and the surgery procedure in the diabeticgroup (119875 = 0007)Theweight loss in theGB group comparedto the three other procedures was statistically lower at 3 6and 12 months after the surgery

The weight loss was not statistically different betweendiabetic and nondiabetic matched patients regardless of thesurgical procedures performed (Figure 3)

In the whole group of obese patients with diabetes astatistically significant decrease in serum HbA1c level from

84 plusmn 02 to 68 plusmn 016 (119875 lt 0001) was observed oneyear following surgery As a function of type of surgeryserum HbA1c level dropped from 901 plusmn 044 to 733 plusmn 033(GB) 861 plusmn 047 to 721 plusmn 032 (CGMa) 794 plusmn 038 to681 plusmn 033 (SG) and 831 plusmn 043 to 634 plusmn 027 (RYGB 119875 lt0001) (Figure 4) In terms of decrease in HbA1c levels nostatistical difference was found between the different surgicalprocedures

Considering the overall surgical approach diabetes sig-nificantly (119875 = 0015) improved after surgery A remissionwas observed in respectively 20 of patients after GB 29after CGMa 625 after SG and 52 after RYGB Diabetesremission was clearly better after SG than following GB (119875 =00026) Conversely the superiority of RYGB on GB was onlyat the limit of statistical significance (119875 = 0051) (Figure 4)

Arterial hypertension resolved in 12 of the patients andwas improved in additional 7of them after bariatric surgeryHowever no statistically significant difference in eitherarterial blood pressure or antihypertensive drug need wasobserved between the four surgical proceduresThe intensityof sleep apnoea syndrome and the need of continuous positiveairway pressure were not modified on a statistical basis aftereach mode of surgery despite the weight loss In contrastin the group of diabetic patients considered as a wholesleep apnoea syndrome disappeared or was improved afterbariatric surgery in respectively 20 and 90 of casesThe serum levels of HDL-cholesterol did not significantlychange during the postsurgery follow-up In contrast serumtriglycerides fell in 76 of the patients but the comparisonbetween the four differentmodes of surgery did not reveal anysignificant difference among them Serum LDL-cholesterollevel was significantly (119875 = 00034) reduced after surgeryThe decrease in LDL-cholesterol was significantly (119875 =001) higher after CGMa than following GB and significantlyhigher (119875 = 003) after RYGB than following CGMa RYGBand SG induced similar decreases in serum LDL-cholesterollevel

5 Discussion

Bariatric surgery has been proven to be an effective approachfor the treatment of morbid obesity in adults with BMI gt40 kgm2 [2 5 17] An increasing body of evidence alsoemphasizes the bariatric surgery benefit for the treatmentof the type 2 diabetes in obese patients Moreover the


80

90

100

110

120

130

140

150

Base 3 6 12 2480

90

100

110

120

130

140

Base 3 6 12 24

80

90

100

110

120

130

140

150

Base 3 6 12 24

SG

60708090

100110120130140

Base 3 6 12 24

RYGB

MonthsMonths

MonthsMonths

Wei

ght (

kg)

Wei

ght (

kg)

Wei

ght (

kg)

Wei

ght (

kg)

GB CGMa

Figure 3 Changes in weight (mean plusmn SEM) induced by the four different types of bariatric surgery in nondiabetic and diabetic obese patientsGastric banding (GB) calibrated gastrectomy typeMason (CGMa) sleeve gastrectomy (SG) andRoux-en-Y gastric gypass (RYGB) (◻)Obesepatients without diabetes (◼) obese patients with type 2 diabetes

HbA

1c (

)

0

2

4

6

8

10

GB SG RYGBGCMa

(a)

Num

ber o

f pat

ient

s

0

10

20

30

GB SG RYGBGCMa

P = 0051

lowastlowast

(b)

Figure 4 Impact of bariatric surgery on the evolution of diabetes in diabetic obese patients (a) changes in serum HbA1c levels (mean plusmnSEM) observed in obese diabetic patients following each of the four different types of bariatric surgery White columns represent serumHbA1c levels measured before surgery and grey toned columns represent the value measured one year after surgery (b) Number of patientsin whom remission of the diabetes was observed after bariatric surgery White columns represent the total number of patients operated foreach type of surgery Grey toned zones show the number of patients in whom a remission of diabetes was observed Gastric banding (GB)calibrated gastrectomy type Mason (CGMa) sleeve gastrectomy (SG) and Roux-en-Y gastric bypass (RYGB) lowastlowast119875 lt 001

new therapeutic algorithms of type 2 diabetes suggest anearlier surgical intervention for increasing the likelihoodof remission of diabetes [4 40] However the question ofthe choice of surgical procedure to be used in this purposeremains yet largely debated and many variations in selectionof the surgical technique are observed among obesity carecentres Because randomized studies are scarce and verydifficult to realize until nowmost statements are issued from

observational studies and meta-analyses In this context thechoice for the surgical procedure remains open according toIDF recommendations [4]

Our study is the first one comparing four surgicalprocedures of bariatric surgery on the remission rate ofdiabetes weight loss and reduction of comorbidities in obesepatients with type 2 diabetes with similar effectiveness inthe diverse groups of patients Although weight loss was


similar following each type of bariatric surgery significantdifferences were observed in the remission rate of type 2diabetes depending on the surgical method used SG orRYBG gave no different results but were followed by betterremission rates than after GB The lack of standardizationfor the criteria of remission of diabetes between studiesintroduces a limit to the strength of the comparison withthose previously published on this topic However our resultsagree with those of Abbatini et al [37] and Campos et al [40]who showed a superiority of RYGB on GB on the remissionrate of type 2 diabetes and with the conclusions of the meta-analysis by Buchwald et al [11] It has been proposed thatdifferences in the secretion of gut hormones (ghrelin GLP-1 peptide YY) occurring after SG or RYGBmay play a pivotalrole in diabetes regression by acting on appetite [41 42]improving insulin sensitivity and restoring the first phase ofinsulin secretion [23 27 28] all effects which concomitantlyto weight loss participate to the improvement of diabetes

In our study the best rates of remission of diabeteswere observed after performing either SG (625) or RYGB(52) They seem to be quite lower than those previouslyreported but the results are variable from one study tothe other For instance Schauer et al [43] described aresolution of diabetes in 83 of the 240 patients operatedby laparoscopic RYGB and followed for a five-year periodHowever a recent randomised trial reported 42 remissionafter RYGB and 37 after SG 12 months after the surgerywith no difference between the 2 surgical groups in diabeticobese patients [44] This discrepancy of the efficacy could beexplained by the lack of standardisation for remission criteriaas well as phenotypic differences among patients Indeed ourpatients were quite older and one-third exhibited diabeticcomplications suggesting a more pronounced diabetic state

No significant difference in weight changes was observedin the group of nondiabetic obese patients by comparisonwith diabetic patients regardless of the type of surgeryperformed By comparisonwith nondiabetic patients a lowerdecrease in weight has been previously observed in obesediabetic patients treated with RYGB [45] in relation to themodalities of the treatment for diabetes In this study patientsrequiring a more powerful treatment of diabetes lost lessweight Conversely in the present study the proportion ofpatients who had the diverse modalities of treatment thatis diet alone oral hypoglycemic drugs andor insulin wassimilarly distributed between the four surgical procedures adirect incidence of the therapy for diabetes on the pattern ofweight loss appears unlikely

As frequently observed in retrospective studies the pre-operative characteristics of the patients were significantlydifferent between the groupsThis can be explained by the factthat the mode of surgery had been chosen according to thepatientrsquos profile In fact while GB or RYGBwere performed inpatients with lower BMI (40ndash45 kgm2) and in those sufferingfrom nibbling SG was preferentially proposed in patientswith BMI gt 50 kgm2 or with significant comorbidities

We observed a postsurgical improvement in arterialhypertension and sleep apnoea syndrome in the group ofdiabetic patients considered as a whole The higher number

of comorbidities found in our severely obese patients whosediabetes was imperfectly controlled as evidenced by highbasal HbA1c levels the long-lasting preoperative duration ofdiabetes which was frequently complicated (38 of cases)could explain the less pronounced improvement than thatreported in other studies [11] Considering each of the foursurgical procedures none appears to be significantly moreeffective than others to improve arterial hypertension orsleep apnoea syndrome Bariatric surgery was followed bya significant drop in serum triglycerides in agreement withpreviously published studies [6 15 46] However in contrastto reports of higher effectiveness of RYGB to reduce serumtriglyceride levels [15 46 47] we foundnodifference betweenthe four types of surgery used This observation likely resultsfrom the limited sizes of the patients groups Similarlyno significant change was noticed in HDL-cholesterol Incontrast RYGB appears as potent as SG to decrease LDL-cholesterol level both being more effective than CGMa

Like in the majority of retrospective investigations themain limitation of our study is the absence of randomisationHowever randomised trials are particularly difficult to realizein this field and even not conceivable for four differentsurgical procedures Another classical limitation in this typeof study is the high percentage of patients lost to follow-upHowever it is important to notice that 30 of these patientsdeclared that they had stopped the specialized follow-upbecause of diabetes regressionThis observation illustrates thedifficulties to follow these patients and emphasizes the needfor clinical investigators to develop collaborationwith generalpractitioners

To conclude the results of our study suggest that amongthe four surgical procedures available for the management ofobese patients with type 2 diabetes SG and RYGB might bemore efficient than CGMa and GB to improve DT2 one yearafter the intervention SG seems to be in our study at least asefficient as RYGB to treat diabetes and other comorbiditiesThis observation which needs to be confirmed in largerpopulations is interesting because SG offers several otheradvantages Especially SG which is a technically simplermethod of surgery than RYGB induces less vitamin defi-ciency and can be subsequently converted into RYGB if itseffects are considered unsatisfactory However its greatersafety and feasibility have not been clearly demonstrated [48]

Conflict of Interests

The authors declare no conflict of interests regarding thepublication of this paper

References

[1] T D Adams R E Gress S C Smith et al ldquoLong-termmortality after gastric bypass surgeryrdquoTheNew England Journalof Medicine vol 357 no 8 pp 753ndash761 2007

[2] L Sjostrom K Narbro C D Sjostrom K Karason B Larssonand H Wedel ldquoEffects of bariatric surgery on mortality inSwedish obese subjectsrdquoThe New England Journal of Medicinevol 357 pp 741ndash752 2007


[3] Haute Autorite de Sante ldquoObesite prise en charge chirurgicalede lrsquoadulterdquo in Recommandations de Bonnes Pratiques Janvier2009

[4] J B Dixon P Zimmet K G Alberti and F Rubino ldquoBariatricsurgery an IDF statement for obese type2 diabetesrdquo DiabeticMedicine vol 28 no 6 pp 628ndash642 2011

[5] L Sjostrom A K Lindroos M Peltonen et al ldquoLifestylediabetes and cardiovascular risk factors 10 years after bariatricsurgeryrdquo The New England Journal of Medicine vol 351 pp2683ndash2693 2004

[6] D Benaiges A Goday J M Ramon et al ldquoLaparoscopicsleeve gastrectomy and laparoscopic gastric bypass are equallyeffective for reduction of cardiovascular risk in severely obesepatients at one year of follow-uprdquo Surgery for Obesity andRelated Diseases vol 7 no 5 pp 575ndash580 2011

[7] M Shah V Simha and A Garg ldquoReview long-term impact ofbariatric surgery on bodyweight comorbidities and nutritionalstatusrdquo Journal of Clinical Endocrinology and Metabolism vol91 no 11 pp 4223ndash4231 2006

[8] W J Pories M S Swanson K G MacDonald et al ldquoWhowould have thought it An operation proves to be the mosteffective therapy for adult-onset diabetes mellitusrdquo Annals ofSurgery vol 222 no 3 pp 339ndash352 1995

[9] J B Dixon P E OrsquoBrien J Playfair et al ldquoAdjustable gas-tric banding and conventional therapy for type 2 diabetes arandomized controlled trialrdquo Journal of the American MedicalAssociation vol 299 no 3 pp 316ndash323 2008

[10] R S Gill D W Birch X Shi A M Sharma and S KarmalildquoSleeve gastrectomy and type 2 diabetes mellitus a systematicreviewrdquo Surgery for Obesity and Related Diseases vol 6 no 6pp 707ndash713 2010

[11] H Buchwald R Estok K Fahrbach et al ldquoWeight and type2 diabetes after bariatric surgery systematic review and meta-analysisrdquo The American Journal of Medicine vol 122 no 3 pp248ndash256 2009

[12] K G MacDonald Jr S D Long M S Swanson et alldquoThe gastric bypass operation reduces the progression andmortality of non-insulin-dependent diabetes mellitusrdquo Journalof Gastrointestinal Surgery vol 1 pp 213ndash220 1997

[13] B E Kadera K Lum J Grant A D Pryor D D Portenier andE J DeMaria ldquoRemission of type 2 diabetes after Roux-en-Ygastric bypass is associated with greater weight lossrdquo Surgery forObesity and Related Diseases vol 5 no 3 pp 305ndash309 2009

[14] K L Kiong R Ganesh A K S Cheng R Lekshiminarayananand S C Lim ldquoEarly improvement in type 2 diabetes mellituspost Roux-en-Y gastric bypass in Asian patientsrdquo SingaporeMedical Journal vol 51 no 12 pp 937ndash943 2010

[15] L Garrido-Sanchez M Murri J Rivas-Becerra et al ldquoBypassof the duodenum improves insulin resistance much morerapidly than sleeve gastrectomyrdquo Surgery for Obesity and RelatedDiseases vol 8 no 2 pp 145ndash150 2012

[16] F Rubino andM Gagner ldquoPotential of surgery for curing type 2diabetesmellitusrdquoAnnals of Surgery vol 236 no 5 pp 554ndash5592002

[17] P R Schauer S Ikramuddin W Gourash R Ramanathan andJ Luketich ldquoOutcomes after laparoscopic Roux-en-Y gastricbypass for morbid obesityrdquo Annals of Surgery vol 232 no 4pp 515ndash529 2000

[18] B Laferrere S Heshka KWang et al ldquoIncretin levels and effectare markedly enhanced 1 month after Roux-en-Y gastric bypasssurgery in obese patients with type 2 diabetesrdquo Diabetes Carevol 30 no 7 pp 1709ndash1716 2007

[19] D E Cummings D SWeigle R S Frayo et al ldquoPlasma ghrelinlevels after diet-induced weight loss or gastric bypass surgeryrdquoTheNew England Journal of Medicine vol 346 no 21 pp 1623ndash1630 2002

[20] J P Thaler and D E Cummings ldquoMinireview hormonal andmetabolicmechanisms of diabetes remission after gastrointesti-nal surgeryrdquo Endocrinology vol 150 no 6 pp 2518ndash2525 2009

[21] J Korner W Inabnet G Febres et al ldquoProspective study ofgut hormone and metabolic changes after adjustable gastricbanding and Roux-en-Y gastric bypassrdquo International Journalof Obesity vol 33 no 7 pp 786ndash795 2009

[22] C W Le Roux M Patterson R P Vincent C Hunt MA Ghatei and S R Bloom ldquoPostprandial plasma ghrelin issuppressed proportional to meal calorie content in normal-weight but not obese subjectsrdquo Journal of Clinical Endocrinologyand Metabolism vol 90 no 2 pp 1068ndash1071 2005

[23] N Basso D Capoccia M Rizzello et al ldquoFirst-phase insulinsecretion insulin sensitivity ghrelin GLP-1 and PYY changes72 h after sleeve gastrectomy in obese diabetic patients thegastric hypothesisrdquo Surgical Endoscopy andOther InterventionalTechniques vol 25 no 11 pp 3540ndash3550 2011

[24] C M Borg C W Le Roux M A Ghatei S R Bloom AG Patel and S J B Aylwin ldquoProgressive rise in gut hormonelevels after Roux-en-Y gastric bypass suggests gut adaptationand explains altered satietyrdquo British Journal of Surgery vol 93no 2 pp 210ndash215 2006

[25] L M Umeda E A Silva G Carneiro C H Arasaki BGeloneze and M T Zanella ldquoEarly improvement in glycemiccontrol after bariatric surgery and its relationships with insulinGLP-1 and glucagon secretion in type 2 diabetic patientsrdquoObesity Surgery vol 21 no 7 pp 896ndash901 2011

[26] D E Cummings J Overduin K E Foster-Schubert and M JCarlson ldquoRole of the bypassed proximal intestine in the anti-diabetic effects of bariatric surgeryrdquo Surgery for Obesity andRelated Diseases vol 3 no 2 pp 109ndash115 2007

[27] S N Karamanakos K Vagenas F Kalfarentzos and T KAlexandrides ldquoWeight loss appetite suppression and changesin fasting and postprandial ghrelin and peptide-YY levels afterRoux-en-Y gastric bypass and sleeve gastrectomy a prospec-tive double blind studyrdquo Annals of surgery vol 247 no 3 pp401ndash407 2008

[28] J KornerM Bessler L J Cirilo et al ldquoEffects of Roux-en-Y gas-tric bypass surgery on fasting and postprandial concentrationsof plasma ghrelin peptide YY and insulinrdquo Journal of ClinicalEndocrinology andMetabolism vol 90 no 1 pp 359ndash365 2005

[29] D J Drucker ldquoThe role of gut hormones in glucose homeosta-sisrdquo Journal of Clinical Investigation vol 117 no 1 pp 24ndash322007

[30] J L Chan E C Mun V Stoyneva C S Mantzoros and AB Goldfine ldquoPeptide YY levels are elevated after gastric bypasssurgeryrdquo Obesity vol 14 no 2 pp 194ndash198 2006

[31] F Rubino A Forgione D E Cummings et al ldquoThemechanismof diabetes control after gastrointestinal bypass surgery revealsa role of the proximal small intestine in the pathophysiology oftype 2 diabetesrdquo Annals of Surgery vol 244 no 5 pp 741ndash7492006

[32] M Bose B Olivan J Teixeira F X Pi-Sunyer and B LaferrereldquoDo incretins play a role in the remission of type 2 diabetes aftergastric bypass surgery what are the evidencerdquoObesity Surgeryvol 19 no 2 pp 217ndash229 2009


[33] J V Li H Ashrafian M Bueter et al ldquoMetabolic surgeryprofoundly influences gut microbialmdashhost metabolic cross-talkrdquo Gut vol 60 no 9 pp 1214ndash1223 2011

[34] A E Pontiroli F Folli M Paganelli et al ldquoLaparoscopic gastricbanding prevents type 2 diabetes and arterial hypertensionand induces their remission in morbid obesity a 4-year case-controlled studyrdquo Diabetes Care vol 28 no 11 pp 2703ndash27092005

[35] H J Sugerman L G Wolfe D A Sica et al ldquoDiabetes andhypertension in severe obesity and effects of gastric bypass-induced weight lossrdquo Annals of Surgery vol 237 no 6 pp 751ndash758 2003

[36] J Vidal A Ibarzabal F Romero et al ldquoType 2 diabetes mellitusand the metabolic syndrome following sleeve gastrectomy inseverely obese subjectsrdquoObesity Surgery vol 18 no 9 pp 1077ndash1082 2008

[37] F Abbatini M Rizzello G Casella et al ldquoLong-term effects oflaparoscopic sleeve gastrectomy gastric bypass and adjustablegastric banding on type 2 diabetesrdquo Surgical Endoscopy andOther Interventional Techniques vol 24 no 5 pp 1005ndash10102010

[38] E K Chouillard A Karaa M Elkhoury and V J GrecoldquoLaparoscopic Roux-en-Y gastric bypass versus laparoscopicsleeve gastrectomy for morbid obesity case-control studyrdquoSurgery for Obesity and Related Diseases vol 7 no 4 pp 500ndash505 2011

[39] J B Dixon and P E OrsquoBrien ldquoHealth outcomes of severelyobese type 2 diabetic subjects 1 year after laparoscopic adjustablegastric bandingrdquoDiabetes Care vol 25 no 2 pp 358ndash363 2002

[40] G M Campos C Rabl G R Roll et al ldquoBetter weight lossresolution of diabetes and quality of life for laparoscopic gastricbypass versus banding results of a 2-cohort pair-matched studyrdquoArchives of Surgery vol 146 no 2 pp 149ndash155 2011

[41] R Morınigo V Moize M Musri A M Lacy S Navarro andJ Marın ldquoGlucagon-like peptide-1 peptide YY hunger andsatiety after gastric bypass surgery in morbidly obese subjectsrdquoThe Journal of Clinical Endocrinology and Metabolism vol 91pp 1735ndash1740 2006

[42] A Jimenez R Casamitjana L Flores J Viaplana R Corcellesand A Lacy ldquoLong-term effects of sleeve gastrectomy andRoux-en-Y gastric bypass surgery on type 2 diabetes mellitus inmorbidly obese subjectsrdquo Annals of Surgery vol 256 pp 1023ndash1029 2012

[43] P R Schauer B Burguera S Ikramuddin et al ldquoEffect oflaparoscopic Roux-En Y gastric bypass on type 2 diabetesmellitusrdquo Annals of Surgery vol 238 no 4 pp 467ndash485 2003

[44] P R Schauer S R Kashyap K Wolski et al ldquoBariatricsurgery versus intensive medical therapy in obese patients withdiabetesrdquoThe New England Journal of Medicine vol 366 no 17pp 1567ndash1576 2012

[45] A M Carbonell L G Wolfe J G Meador H J Sugerman JM Kellum and J W Maher ldquoDoes diabetes affect weight lossafter gastric bypassrdquo Surgery for Obesity and Related Diseasesvol 4 no 3 pp 441ndash444 2008

[46] W K Karcz D Krawczykowski S Kuesters et al ldquoInfluenceof sleeve gastrectomy on NASH and type 2 diabetes mellitusrdquoJournal of Obesity vol 2011 Article ID 765473 7 pages 2011

[47] W J Lee K Chong K H Ser et al ldquoGastric bypass vssleeve gastrectomy for type 2 diabetes mellitus a randomizedcontrolled trialrdquo Archives of Surgery vol 146 no 2 pp 143ndash1482011

[48] P Topart G Becouarn and P Ritz ldquoComparative earlyoutcomes of three laparoscopic bariatric procedures sleevegastrectomy Roux-en-Y gastric bypass and biliopancreaticdiversionwith duodenal switchrdquo Surgery forObesity andRelatedDiseases vol 8 pp 250ndash254 2012

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014


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EndocrinologyInternational Journal of



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BioMed Research International

OncologyJournal of



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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

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Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom


after bariatric surgery Otherwise Roux-en-Y bypass (RYGB)that excludes the duodenum from the nutrimentsrsquo route andprofoundly modifies the gut microbial metabolic cross-talk[33] has been shown to improve insulin resistance morerapidly than sleeve gastrectomy [15]

These observations raised the question of the choiceof chirurgical procedure for treating diabetes Most studieshave compared two by two procedures Using this approachRYGB and sleeve gastrectomy (SG) seem to be more efficientfor treating diabetes than gastric banding (GB) Howeverthese studies failed to provide clear conclusions owing to thegreat heterogeneity of the results For instance dependingon the mode of surgery used (restrictive malabsorptive orcombined) and study design the diabetes remission ratevaried from 45 to 97 of patients [5 9 12 34ndash39] In ourcenter four surgical procedures have been used for the last15 years to treat obesity GB SG calibrated gastrectomytype Mason (CGMa) and RYGB The aim of the presentretrospective study was to evaluate the efficacy of thesefour procedures to induce diabetes remission and lowercardiovascular risk factorsMoreover the influence of surgeryon weight evolution in the diabetic population was comparedwith that observed in a nondiabetic population matched forsex age BMI and surgical procedure

2 Patients and Methods

We have conducted a retrospective case-control comparativestudy aimed at evaluating the impact of bariatric surgery ontype 2 diabetes Among 970 patients who underwent bariatricsurgery in our center since 2001 81 patients were identifiedas type 2 diabetic (ICD coding) All patients had undergonea medical supervised therapy for weight loss for at least 12months before bariatric surgery

Preoperatively they were evaluated for medical or surgi-cal history and treatment usedwas recordedA clinical exam-ination was performed and risk factors and comorbiditiesincluding arterial hypertension and sleep apnoea syndromewere collectedThe serum levels of biologicalmarkers (fastingglycemia glycosylated hemoglobin total cholesterol HDL-and LDL-cholesterol and triglycerides) were measured

Then one of the four following surgical procedures wasused GB (20 patients) CGMa (14 patients) SG (24 patients)and RYGB (23 patients)

After surgery the weight change could be followed for 24months and biological parameters for 12 months 23 of thepatients were lost for follow-up

The weight changes in patients with diabetes were alsocompared to those observed in obese patients without dia-betes and matched for age sex BMI and type of surgery

3 Statistical Analysis

The evolution of diabetes has been chosen as the primary endpoint of the study It was evaluated on the basis of a score ofeffectiveness Remission of diabetes (score 1) was defined asHbA1c level lower than 65 and interruption of antidiabetictreatment Improvement (score 2) was defined as either a

Months

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Figure 1 Overall changes in weight (mean plusmn SEM) in patientstreated with bariatric surgery (Δ) obese patients without diabetes(◼) obese patients with type 2 diabetes

decrease in HbA1c level or a reduction in the antidiabetictreatment Score 3 corresponded to a stabilisation of diabetesand score 4 to a degradation of the glycaemic pattern As thelatter is a qualitative parameter statistical analysis of the dataused a 1205942 test Similar scores and statistical procedures wereused to evaluate the changes in the following comorbiditiesarterial hypertension sleep apnoea syndrome and serumlipid pattern

The serum HbA1c levels measured respectively beforeand 6 to 12 months after surgery were compared with theWilcoxon test The nonparametric test of Kruskal Wallis wasused to evaluate this biological parameter as a function of thetype of surgery employed

Theweight changes were initially analysed using ANOVAfor two factors time and type of surgery Depending on theresults of this first analysis a second statistical evaluationusing an ANOVA for one factor (type of surgery) wasperformed Complementary tests of comparison two by two(Newman and Keuls) were done for the different time pointswhere ANOVA (one factor) was statistically significant

Statistical analyses were performed with Statview soft-ware (5th version SAS Institute North Carolina) Statisticalsignificance was considered for a 120572 risk of 5

4 Results

Themain characteristics of diabetic patients are summarizedin Table 1 The mean diabetes duration was 8 plusmn 8 yearsAccording to WHO criteria 67 patients (827) harboureda profile of metabolic syndrome The number of patientswith cardiovascular risk factors was similar whatever thetype of surgery performed 38 of the patients suffered frommicro- andor macrovascular complications of diabetes and24 (296) complained of signs of depression 10 patientsweretreated by diet alone 44 patients (54) by oral antidiabeticdrugs (OAD) 7 by insulin and 25 by OAD plus insulin

Bariatric surgery induced a significant (119875 lt 0001) weightloss in both groups of obese patients (Figure 1) One yearafter surgery weight was reduced by 307 plusmn 21 and 372 plusmn26 kg in patients with and without diabetes respectively




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5 Discussion



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References
























































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ObesityJournal of



















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5 Discussion



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References
























































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of

















80

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Base 3 6 12 2480

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Base 3 6 12 24

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SG

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RYGB

MonthsMonths

MonthsMonths

Wei

ght (

kg)

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ght (

kg)

Wei

ght (

kg)

Wei

ght (

kg)

GB CGMa


HbA

1c (

)

0

2

4

6

8

10

GB SG RYGBGCMa

(a)

Num

ber o

f pat

ient

s

0

10

20

30

GB SG RYGBGCMa

P = 0051

lowastlowast

(b)
















References
























































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of



























References
























































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of





































































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of
















clinical study comparison of the effectiveness of four

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