ORIGINAL CONTRIBUTIONS

Visceral Fat and Body Composition Changes in a FemalePopulation After RYGBP: a Two-Year Follow-Up by DXA

Alberto Bazzocchi & Federico Ponti & Stefano Cariani & Danila Diano &

Luca Leuratti & Ugo Albisinni & Giulio Marchesini & Giuseppe Battista

# Springer Science+Business Media New York 2014

AbstractBackground Our aim was to monitor the impact of Roux-en-Y gastric bypass (RYGBP) on body composition over a 24-month period by dual-energy X-ray absorptiometry (DXA).Methods Forty-one women (40.6±10.0 years old; 42.6±6.6 kg/m2) entering a bariatric surgery programme were sub-mitted to whole-body DXA (Lunar iDXA) before treatmentand after 3, 6, 12 and 24 months. Fat mass (FM), non-bonelean mass (LM), bone mineral content (BMC) and density(BMD) were measured at whole body and regionally. Androidvisceral adipose tissue (VAT) was estimated by a recentlyvalidated software.Results Twenty-nine patients (44.3±11.8 years old; BMI, 45.4±8.9 kg/m2) concluded the study. Following surgery, the pro-gressive decrease of BMI was associated with reduced whole-body and regional FM. LM showed a moderate decrease at3 months and stabilized thereafter. A progressive decrease oftotal FM/LM and android FM/LM ratios were observed in the

3- to 6-month (−19.1±8.4 % and −26.5±10.9 %, respectively;p<0.0001) and 6- to 12-month periods (−23.5±16.8 % and−29.4±23.9 %, respectively; p<0.0001). VAT was the param-eter showing the largest decrease (−65.6±17.5 % at 12 months;p<0.0001). Two years after the surgery, a slight but significantdecrease of total and regional LM was observed, without anysignificant change in BMI.Conclusions Body composition significantly changes afterRYGBP with a metabolically healthier redistribution of totaland regional FM and a positive balance of FM/LM variation.DXA should be considered as a valid supplementary tool forthe clinical assessment and follow-up in patients undergoingbariatric surgery.

Keywords Body composition . Absorptiometry, photon .

Obesity . Bariatric Surgery . Diseasemanagement .

Intra-abdominal fat

Introduction

The World Health Organization (WHO) defines overweightand obesity as “abnormal or excessive fat accumulation thatmay impair health”. At least 2.8 million adults die each year asa result of being overweight or obese. In addition, 44 % of thediabetes, 23 % of the ischemic heart disease and between 7and 41 % of certain cancer are attributable to overweight andobesity [1]. The combined medical costs associated withtreatment of these preventable diseases are estimated to in-crease by US$48–66 billion/year in the USA and by £1.9–2billion/year in the UK by 2030 [2].

It has been suggested that cardiometabolic risks associatedwith adipose tissue are strictly related to the visceral adiposetissue (VAT) compartment, while subcutaneous adipose tissue(SAT) plays a controversial role [3, 4]. The ratio between VATand SAT is crucial in predicting an unfavourable metabolic

A. Bazzocchi :U. AlbisinniDiagnostic and Interventional Radiology, The “Rizzoli” Institute,Via G. C. Pupilli 1, 40136 Bologna, Italy

F. Ponti (*) :D. Diano :G. BattistaDepartment of Specialized, Diagnostic, and Experimental Medicine,University of Bologna Sant’Orsola-Malpighi Hospital,Via G. Massarenti 9, 40138 Bologna, Italye-mail: pontifederico@libero.it

S. Cariani : L. LeurattiObesity Surgery Center, Department of Emergency-Urgency,General Surgery and Transplantation, University of BolognaSant’Orsola-Malpighi Hospital, Via G. Massarenti 9,40138 Bologna, Italy

G. MarchesiniUnit of Metabolic Diseases and Clinical Dietetics,University of Bologna Sant’Orsola-Malpighi Hospital,Via G. Massarenti 9, 40138 Bologna, Italy

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profile [5]. Inadequate subcutaneous fat might result in lipidoverflow into the visceral depot and non-adipose tissues,thereby modulating insulin sensitivity [5, 6]. Moreover, inobesity, type 2 diabetes and lipodystrophy, insulin resistancemight depend on alterations in the partitioning of fat betweenadipocytes and muscle, liver and pancreatic insulin-secretingbeta cell, with an ectopic excess fat storage in the last threetissues [6].

Bariatric surgery is an effective treatment producing long-term weight loss in randomized controlled trials [7]. Roux-en-Y gastric bypass (RYGBP) is considered the surgical proce-dure of choice for treating morbid obesity in the USA; how-ever, it is less commonly performed in several countriesbecause it precludes the traditional diagnostic evaluation ofthe distal stomach and duodenum [8, 9].

Body composition, i.e. the relative amounts of muscle, fat,bone and other vital parts of the body, is a “health-relatedcomponent of physical fitness” [10]. Evidence of the impor-tance of the body composition has grown rapidly in the lastfew years [11]. Body composition assessment may help de-termine the extent of the physiopathological processes occur-ring after bariatric surgery. In particular, the densitometricstudy of body composition is important for the quantitativeassessment and the redistribution of the soft tissue masses atwhole-body and regional level with diagnostic/prognosticaims [12–15].

The aim of the study was to monitor body compositionchanges by dual-energy X-ray absorptiometry (DXA) in acohort of women during the first 2 years after RYGBP bariat-ric surgery.

Materials and Methods

Study Design and Population

Forty-one women entering a bariatric surgery programme inour hospital between May 2009 and October 2012 wereincluded in the study. Mean age of the population was 40.6±10.0 years old (range 19.1–60.0), with BMI of 42.6±6.6 kg/m2 (35.1–68.3); out of 41 patients, 25.6 % were super-obese(BMI≥50). All patients underwent RYGBP. They were sub-mitted to clinical and surgical examination and were moni-tored bywhole-bodyDXA scan before and 3, 6 and 12monthsafter surgery. The baseline measurements were obtained from1 to 7 days prior to surgical intervention. Follow-up was laterextended to 24 months, for patients completing the interimcontrols during the first year.

Patients satisfying both surgical (NIH criteria) and densi-tometric criteria were considered eligible for the participationin the study [16]. In addition to surgical contraindications,exclusion criteria were related to densitometric issues: allsubjects with implantable devices, foreign bodies or those

who had recently undergone diagnostic tests using nuclidesor barium or radio-opaque substance were also excluded.

The study was conducted in respect of the Declaration ofHelsinki. The research was approved by the local ethicalcommittee, and all patients signed an informed consent.

DXA Analysis and Markers

Whole-body scan was performed using a narrow fan-beamdensitometer (Lunar iDXA 2005, Madison, WI, USA;enCORETM 2011, software version 13.6) for the total andregional assessment of fat mass (FM), non-bone lean mass(LM) and bone mineral content (BMC—and density [BMD]),according to a three-compartment molecular model of bodycomposition. In particular, the dual X-rays measure only twocomponents (bone and soft tissue or fat mass and non-bonelean mass). In order to determine the amount of each compo-nent, DXA primarily separates masses into those containingonly soft tissue and soft tissue plus bone mineral mass; sec-ondly, fat mass, non-bone lean mass and bone mineral contentcan be discriminated by mathematical algorithms.

DXA was performed by a skilled technician in a standardmanner following manufacturer recommendations and guide-lines [17]. The scanner was calibrated daily using a standardcalibration block supplied by the manufacturer. The measure-ments were carried out in subjects with underwear and a whitecoat in a supine position with arms at sides slightly separatedfrom the trunk and correctly centred on the scanning field.

The DXA software allows for adjustment of regions ofinterests (ROIs) including the sagittal line, which controlsthe left-right body distribution of tissue. In addition, the soft-ware uses an automatic routine detection to determine whetherthe subject is within the scan space. If the subject’s body is notcontained within the scan space, a half-scan analysis is auto-matically performed. “Half-body scan analysis” is a softwareoption allowing for an automatic estimate of total body com-position from a half-body scan by assuming the symmetry ofthe body (on its sagittal plane) [18].

ROIs were defined by the analytical programme includingtotal body assessment and five different corporeal districts:trunk, upper limb, lower limb, android region (a portion of theabdomen included between the line joining the two superioriliac crests and extended cranially up to the 20 % of thedistance between this line and the chin) and gynoid region (aportion of the legs leaving from the femoral great trochanter,directed caudally up to a distance double of the androidregion). The operator analysed all scans to manually reposi-tion line points that were not correctly placed by software. Forthe total body and each region, DXA scanned the weight (in g)of total mass, FM, LM and BMC (Fig. 1).

Visceral fat analysis was performed by CoreScan™, a soft-ware option for the assessment of visceral fat (mass in g andvolume in cm3) in the android region. The detection of the

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layer thickness of the SAT at sides of the android regionallowed the software to map the total SAT compartment. Theamount of VATwas derived by subtracting SAT from the totalandroid FM [19].

The analysis of total body and regional (trunk, legs andarms) values of BMD was also performed (Fig. 1).

In our study, we considered four DXA indexes as pivotalmarkers of body composition in terms of general balance ofmasses (total body FM/LM—TFM/TLM), central/peripheraldistribution of FM (android/gynoid FM—AFM/GFM) andcentral or VAT compartment (android FM/LM—AFM/ALMand VAT/SAT).

Statistical Analysis

The normal distribution of data in our population was testedby skewness and excess Kurtosis test; normal ranges wereconsidered for values between −2 and +2. Results are reportedas mean and standard deviation (±SD) and integrated withdelta percentage (Δ%). Student paired t test was used toanalyse the statistical significance of changes during the

follow-up period; two-tailed p was considered significant forvalues less than 0.05. Statview statistical package (version5.0.1 for Windows—SAS Inc., IL, USA) was used for theanalysis.

Results

Twelve patients missed at least one or more follow-up visitsand were excluded from the analysis. The reasons of drop-outwere mainly due to perceived treatment ineffectiveness or topersonal motivations, such as job constraints and/or distancefrom the study centre. The population concluding the entirefollow-up programme included 29 females, aged 44.3±11.8 years (range 26.0–65.5), with basal BMI of 45.4±8.9 kg/m2 (35.4–61.0). Fourteenwomen also reached the extrafollow-up point at 24 months. The normal distribution of thefinal population was proved for all parameters.

In this group, only one patient was within the normal widthof the whole-body DXA field of view at baseline, and “half-body” analysis was mandatory in 28/29 patients (96.6 %).

% fat mass

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Android region

Visceral fat

Subcutaneous fat

Fig. 1 Left, coloured soft tissue map of whole-body scan by DXAhighlights the regional assessment of body composition (T trunk,U upperlimbs, L lower limbs, A android, G gynoid). The histogram showing therelationship among colours on the whole-body scan and the fat percent-age is visualized on the upper-middle part of the figure: yellow, high fatpercentage—conventionally >60 %; orange, medium fat percentage—

between 25 and 60 %; red, low fat percentage— <25 %. In the lower-middle part of the figure, the box magnifies the android region with therepresentation of the subcutaneous and visceral fat. Right, skeletal map ofwhole-body scan with the region of interests (S spine, U upper limbs, Llower limbs, R ribs, P pelvis)

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Body composition values in the 12-month period of follow-up are listed in Tables 1 and 2. BMI and total weight significantlydecreased in all cases at 12 months with a parallel decrease ofTFM. On the other hand, TLM showed a moderate decrease at3 months and remained stable thereafter (Δ 6 vs. 3months: 1.0±4.0 %; p=0.351; Δ 12 vs. 6 months: −0.9±4.4 %; p=0.593).The regional analysis showed a similar trend for central andperipheral FM and LM compartments (android, gynoid, upperand lower limbs), with amore remarkable reduction of FM in theandroid region related to total body. As a consequence, a pro-gressive decrease of TFM/TLM and AFM/ALM ratios wasobserved during the whole follow-up period with a pronouncedreduction in the period between 3 and 6 months (−19.1±8.4 %

and −26.5±10.9 %, respectively; p<0.0001) and between 6 and12 months (−23.5±16.8 % and −29.4±23.9 %, respectively;p<0.0001) (Fig. 2). Furthermore, there was a significant reduc-tion of AFM/GFM at 12 months with a similar decrease in allintermediate controls (Δ 3 months vs. baseline: −8.2±7.2 %,Δ6 vs. 3 months: −10.7±9.6 % and Δ 12 vs. 6 months: −15.6±18.7 %; p<0.05) (Fig. 3).

The specific analysis of visceral and subcutaneous adiposetissues showed a marked decrease during the entire follow-upperiod; in particular, VAT showed the most pronounced re-duction among all densitometric parameters at 12 months. Nosignificant changes of VAT/SAT ratio were measured through-out the entire period (Fig. 3).

Table 1 Body composition, bone density parameters and derived indexes in obese women at baseline, 3-, 6- and 12-month follow-up

Baseline 3 months 6 months 12 months

Anthropometry Weight (kg) 117.75±28.22 97.66±20.29 89.56±19.87 79.81±18.28

BMI 45.4±8.9 37.7±6.3 34.6±6.3 30.8±5.8

Total FM (kg) 61.79±17.22 47.20±12.24 38.68±11.43 29.33±10.73

LM (kg) 53.37±11.15 47.89±8.53 48.36±8.91 48.02±9.74

BMC (kg) 2.60±0.41 2.57±0.44 2.51±0.41 2.45±0.43

Android FM (kg) 6.26±2.17 4.33±1.40 3.33±1.20 2.35±1.23

LM (kg) 4.23±1.41 3.61±0.78 3.79±0.89 3.76±0.90

VAT (dm3) 2.82±1.66 1.73±0.67 1.40±0.86 0.94±0.77

VAT (kg) 2.66±1.56 1.63±0.63 1.32±0.81 0.88±0.73

SAT (kg) 3.60±1.24 2.70±1.02 2.01±0.80 1.47±0.92

Gynoid FM (kg) 11.20±3.58 8.44±2.32 7.31±2.43 5.91±2.12

LM (kg) 7.60±2.11 6.73±1.42 6.81±1.55 6.56±1.50

Trunk FM (kg) 32.23±9.56 23.99±7.06 18.77±6.13 13.60±5.87

LM (kg) 24.23±5.35 22.09±4.11 22.73±3.94 23.07±4.36

BMC (kg) 0.85±0.18 0.83±0.20 0.76±0.17 0.73±0.18

Arms FM (kg) 7.36±1.85 5.80±1.54 4.86±1.35 3.65±1.35

LM (kg) 6.13±1.18 5.32±0.98 5.38±1.03 5.34±1.11

BMC (kg) 0.33±0.05 0.33±0.05 0.33±0.05 0.33±0.06

Legs FM (kg) 21.33±8.25 16.59±5.85 14.26±5.25 11.32±4.54

LM (kg) 20.10±5.43 17.64±3.91 17.40±4.06 16.84±4.57

BMC (kg) 0.94±0.16 0.94±0.16 0.94±0.16 0.91±0.16

Total BMD (g/cm2) 1.234±0.142 1.218±0.146 1.197±0.148 1.188±0.141

Arms BMD (g/cm2) 1.053±0.163 1.062±0.157 1.018±0.148 0.999±0.159

Legs BMD (g/cm2) 0.908±0.101 0.907±0.115 0.858±0.093 0.825±0.096

Pelvis BMD (g/cm2) 1.180±0.172 1.182±0.199 1.129±0.182 1.093±0.182

Ribs BMD (g/cm2) 0.773±0.091 0.762±0.097 0.752±0.093 0.735±0.093

Spine BMD (g/cm2) 1.263±0.178 1.265±0.171 1.247±0.157 1.208±0.155

Indexes TFM/TLM 1.15±0.14 0.98±0.15 0.79±0.14 0.61±0.21

AFM/ALM 1.49±0.29 1.19±0.25 0.87±0.22 0.63±0.32

AFM/GFM 0.57±0.17 0.52±0.15 0.47±0.13 0.39±0.15

VAT/SAT 0.77±0.47 0.64±0.27 0.72±0.59 0.86±0.88

Data are presented as mean±SD

BMI body mass index, FM fat mass, LM non-bone lean mass, BMC bone mineral content, VAT visceral adipose tissue, SAT subcutaneous adipose tissue,TFM/TLM total body FM/LM, AFM/ALM android FM/LM, AFM/GFM android/gynoid FM

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A slight, but significant reduction was observed in BMDparameters at 12 months with the maximum value for the ribsand minimum for the legs and whole body.

In the 14 females who extended their follow-up to24 months, only minor modifications of anthropometric anddensitometric parameters were observed. The average BMIdecreased slightly (from 29.9 to 29.5 kg/m2; p=0.678); itdecreased further only in 57.1 % of cases. Also, densitometricsoft tissue parameters did not change, with the exception ofTLM (−2.9±2.6 %, p=0.011), and LM at arms (−9.9±8.0 %,p=0.005), android (−5.9±6.5 %, p=0.029) and gynoid re-gions (−5.4±5.5 %, p=0.022). A significant reduction ofBMD was also observed (maximum for the arms: −3.5±2.9 %; p=0.005).

Conclusion

This study analyses body composition changes after RYGBP,focusing on the abdominal redistribution of FM anddistinguishing SAT and VAT compartments by DXA.

Although BMI remains the classical outcome mea-sure, it is considered inadequate for the assessment ofobese patients, particularly in the management of weightloss, since the benefits of weight loss treatments, includingbariatric surgery, are not only related to total body weight loss,but also to the cardiometabolic effects of local fat accumula-tion and distribution [20].

In the last few years, DXA technology improved the accu-racy in the assessment of body composition, especially in the

Table 2 Modification of body composition, bone density parameters and derived indexes in female participants expressed as Δ (%) afterRYGBP

Δ 3-month B Δ 6-month B Δ 12-month B

Weight—BMI −16.4±5.0*** −23.2±8.1*** −31.2±11.7***Total FM −23.0±6.0*** −36.8±10.4*** −50.9±18.0***

LM −9.7±5.1*** −8.8±6.9** −9.6±6.6***BMC −0.9±2.3NS −3.3±1.8*** −5.8±2.7***

Android FM −29.7±8.7*** −46.0±11.2*** −60.4±20.8***LM −12.1±10.5* −8.0±11.8* −8.7±12.2*VAT −32.9±13.5** −48.1±14.3*** −65.6±17.5***SAT −25.4±10.0*** −43.8±12.8*** −57.9±24.5***

Gynoid FM −23.4±8.0*** −33.9±12.4*** −45.4±18.5***LM −9.7±9.1* −8.9±9.0* −12.4±7.9***

Trunk FM −25.0±7.0*** −41.4±10.7*** −56.2±18.8***LM −8.1±6.9* −5.1±8.2* −3.9±8.3NSBMC −2.7±7.3NS −10.3±6.1*** −14.2±6.8***

Arms FM −20.7±10.9*** −32.7±15.4*** −48.2±20.9***LM −12.8±7.9*** −11.5±11.6** −12.6±9.0***BMC −0.6±7.0NS −0.5±7.8NS −1.0±7.2NS

Legs FM −21.3±5.5*** −32.1±10.8*** −45.0±17.4***LM −11.1±7.5*** −12.4±9.0** −15.6±8.4***BMC −0.2±2.3NS −0.3±1.7NS −3.1±2.3***

Total BMD 0.1±2.0NS −1.8±1.2*** −4.2±1.7***Arms BMD −1.5±3.4NS −2.7±3.7* −4.9±4.1*Legs BMD 0.3±2.3NS −1.1±2.3NS −4.2±2.8***Pelvis BMD 1.3±8.4NS −3.1±4.3* −5.1±4.7**Ribs BMD −0.2±4.3NS −5.4±3.2*** −8.9±6.0***Spine BMD 0.1±6.9NS −4.5±3.7*** −7.4±5.1***Indexes TFM/TLM −14.6±5.5*** −30.9±8.5*** −46.1±17.7***

AFM/ALM −19.7±7.8*** −41.0±11.1*** −56.7±20.8***AFM/GFM −8.2±7.2* −18.2±9.1*** −31.2±16.1***VAT/SAT −8.5±21.1NS −5.9±22.8NS 5.6±70.6NS

Data are presented as mean±SD

BMI body mass index, FM fat mass, LM non-bone lean mass, BMC bone mineral content, VAT visceral adipose tissue, SAT subcutaneous adipose tissue,TFM/TLM total body FM/LM, AFM/ALM android FM/LM, AFM/GFM android/gynoid FM, B baseline, NS not statistically significant

*p<0.05; **p<0.001; ***p<0.0001

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field of obesity. Developments of DXA equipments and soft-ware allow a differential estimate of VAT and SAT (in spite ofprojective limitations of DXA imaging acquisition) and toscan obese and heavier patients (even over 200 kg) withprecise half-body evaluations and very few technical limita-tions [18, 21].

Accuracy of DXA assessment of VAT and body composi-tion is superior to other methods, actually used in clinicalpractice. 2013 ISCD official guidelines recommend the useof total body DXA with regional analysis in obese patientsundergoing bariatric surgery to assess fat and lean masschanges when the weight loss exceeds about 10 % [22].Otherwise, the impact on clinical outcomes is uncertain.

Evidences showed that bariatric surgery leads to a higherlean mass loss than non-surgical methods of weight loss [23,24]. Other longitudinal studies, conducted in patients whoundergone bariatric surgery, observed a decrease in fat massand lean mass of about 30–50 % and 10–15 %, respectively.And the decrease was primarily documented within the first3–6 months after surgery [25, 26].

According to these results, early detection of lean massloss, especially in the first 3–6 months after bariatric surgery,might suggest clinical indications for exercise and dietarymodifications to prevent further decline in lean mass andphysical function. In these conditions, serial DXA measure-ments of body composition could be useful to identify those

patients who might benefit from additional interventions(physical exercise, diet etc.) to mitigate loss of lean mass.

Our analysis also revealed a modest reduction of total bodyLM at 3 months followed by maintenance of LM thereafter;this observation is in accordance with the study of Carrascoet al. [27], where a decrease of LM up to 6 months and aplateau in the period between 6 months and 1 year wasobserved. In contrast, Zalesin et al. [28] concluded that onlyfew patients were able to stop the decrease of total LM afterRYGBP, despite their self-reported participation in conven-tional exercise programmes. These conflicting data suggestthat a strict monitoring and a more aggressive postoperativeintervention in individual patients may be important to preventundesired effects.

Also, gastric bypass (GB) surgery was reported to lead to aprogressive decrease in LM [29–31], showing a predominantloss during the first year post-operatively [29]. As reported byGarrapa et al. [31], although both FM and LM were reduced,the decrease of FM was more pronounced leading to a reduc-tion of total FM/LM ratio. In addition to the substantial weightloss and improved cardiometabolic parameters, the treatmentoutcome of bariatric surgery might also consider the effects onbody FM redistribution. GB seems to produce a positive effectin terms of reduced total and regional (trunk) adiposity. In ourexperience, the beneficial effects of RYGBP apparently sumup and the relative preservation of LM may be an

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Fig. 2 Two examples of the different body composition trend over12 months. a Significant decrease of total fat mass (TFM), visceral andsubcutaneous adipose tissue (VATand SAT) and slight increase of total lean

mass (TLM), despite of a modest BMI reduction at 12months (−17.4%). bLarge reduction of BMI (−34.0 %) at 12 months with a marked decrease ofTFM, VAT, SAT and a less pronounced TLM loss

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additional value. Finally, the changes in VAT afterRYGBP were very large (−65.6 % at 12 months), al-though no statistical significant variation could be appreciatedin the VAT/SAT ratio between the pre-surgical and the 12-month analysis.

We measured a modest significant decrease (−4.2 %) intotal BMD after RYGBP during the whole follow-up period.Dixon et al. [24] found no changes in whole-bodyBMC inGBpatients, otherwise as reported in other RYGBP interventions[32]. Carrasco et al. [27] examining BMD at whole body,femur and lumbar spine level observed a significant decreaseat 6 and 12 months after RYGBP. This issue remains to bedefined, considering the limited diagnostic power of whole-body scan on BMD analysis and the other limitations of thepresent study.

The range of changes in DXA parameters during thefollow-up period was extremely wide. This was probably theexpression of the high degree of heterogeneity of the studiedpopulation in terms of age, degree of obesity and menopausalstatus. As an example, the changes of total FM at 12 monthsranged from −16.0 to −78.1 %, total LM from 5.3 to −22.3 %,

android FM from −17.7 to −89.5 % and VAT from −26.7 to−84.6 %. Thus, the importance of body composition assess-ment largely outweighs its role in describing the effects ofspecific bariatric surgery, but extends to provide useful infor-mation for the management of single patients [33], to pro-gramme interventions to facilitate the beneficial effects or tolimit untoward effects (e.g. to facilitate LM sparing by in-creased physical activity).

No study has so far reported DXA analysis at 2 years insubjects submitted to bariatric surgery.

In our study, only minor modifications of anthropometric(BMI) and densitometric parameters were observed in the 14women who completed the 2-year follow-up. Otherwise, itshould be taken very carefully both the data and the statisticalanalysis on the second year after bariatric surgery consideringthe slight but significant decrease of total and regional LM incomparison to insignificant change of BMI. In addition to theabove-mentioned heterogeneity of the population, anotherimportant limitation is the relatively high drop-out rate andthe consequent reduced number of subjects considered for thestatistical analysis. The reasons of drop-out could also

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Fig. 3 On the upper part, changes of total fat mass (TFM), total lean mass (TLM) and their ratio (on the left) during the follow-up period. On the lowerpart, visceral adipose tissue (VAT), subcutaneous adipose tissue (SAT) and their ratios (on the left)

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influence the interpretation of results, considering that non-compliant patients or those with an unsatisfying surgical out-come were probably preferentially missed to follow-up.

Besides, there is a lack of analysis in conjunction with othermajor factors that affect body composition such as physicalactivity, nutritional behaviour and supplements, menopausalstatus and TRH, smoking, use of medications that affect fatdeposition, etc.

Finally, the limited number of males entering our bariatricsurgery programme during the same period (not reported inthis analysis), as in the vast majority of obesity studies, doesnot allow any conclusion regarding possible gender-relateddifferences in body composition response to surgery.

In conclusion, this study demonstrates that RYGBP pro-duces a significant loss of FM, particularly in the androidregion and VAT, and a maintenance of LM after the criticalperiod of the first 3 months post-surgery, when the mainte-nance of nitrogen balance is at risk. Three DXA indexeschange favourably in the course of follow-up: TFM/TLMand AFM/ALM showed a progressive decrease, whereasAFM/GFM shows a redistribution of FM in favour of thegynoid region, in keeping with decreased cardiovascular risk.These changes may be easily monitored by DXA, whichqualifies as a valid supplementary tool for the clinical assess-ment and follow-up of patients undergoing bariatric surgery.

Conflict of Interest All the authors have no conflict of interest todeclare.

Statement of Informed Consent Informed consent was obtained fromall individual participants included in the study.

Statement of Human and Animal Rights All procedures performedin studies involving human participants were in accordance with theethical standards of the institutional and/or national research committeeand with the 1964 Helsinki declaration and its later amendments orcomparable ethical standards.

References

1. World Health Organization. Fact Sheet No 311 Obesity andOverweight. Geneva Ahwwimffe.

2. Wang YC, McPherson K, Marsh T, et al. Health and economicburden of the projected obesity trends in the USA and the UK.Lancet. 2011;378(9793):815–25.

3. Despres JP, Lemieux S, Lamarche B, et al. The insulin resistance-dyslipidemic syndrome: contribution of visceral obesity and thera-peutic implications. Int J Obes Relat Metab Disord. 1995;19 Suppl 1:S76–86.

4. Tran TT, Yamamoto Y, Gesta S, et al. Beneficial effects of subcuta-neous fat transplantation onmetabolism. Cell Metab. 2008;7(5):410–20.

5. Taksali SE, Caprio S, Dziura J, et al. High visceral and low abdom-inal subcutaneous fat stores in the obese adolescent: a determinant ofan adverse metabolic phenotype. Diabetes. 2008;57(2):367–71.

6. Ravussin E, Smith SR. Increased fat intake, impaired fat oxidation,and failure of fat cell proliferation result in ectopic fat storage, insulinresistance, and type 2 diabetes mellitus. Ann N Y Acad Sci.2002;967:363–78.

7. Leff DR, Heath D. Surgery for obesity in adulthood. BMJ. 2009;339:b3402.

8. Cariani S, Amenta E. Three-year results of Roux-en-Y gastricbypass-on-vertical banded gastroplasty: an effective and safe proce-dure which enables endoscopy and X-ray study of the stomach andbiliary tract. Obes Surg. 2007;17(10):1312–8.

9. Leuratti L, Di Simone MP, Cariani S. Unexpected changes in thegastric remnant in asymptomatic patients after Roux-en-Y gastricbypass on vertical banded gastroplasty. Obes Surg. 2013;23(1):131–9.

10. U.S. Department of Health and Human Services. Physical activityand health: a report of the surgeon general. Atlanta GUSDoHaHS.

11. De Lorenzo A, Bianchi A, Maroni P, et al. Adiposity rather than BMIdetermines metabolic risk. Int J Cardiol. 2013;166(1):111–7.

12. Bazzocchi A, Diano D, Ponti F, et al. Health and ageing: a cross-sectional study of body composition. Clin Nutr. 2013;32(4):569–78.

13. Verdich C, Barbe P, Petersen M, et al. Changes in body compositionduring weight loss in obese subjects in the NUGENOB study: com-parison of bioelectrical impedance vs. dual-energy X-ray absorpti-ometry. Diabetes Metab. 2011;37(3):222–9.

14. Malina RM. Body composition in athletes: assessment and estimatedfatness. Clin Sports Med. 2007;26(1):37–68.

15. St-Onge MP. Relationship between body composition changes andchanges in physical function and metabolic risk factors in aging. CurrOpin Clin Nutr Metab Care. 2005;8(5):523–8.

16. Gastrointestinal surgery for severe obesity: National Institutes ofHealth Consensus Development Conference Statement. Am J ClinNutr. 1992;55(2 Suppl):615S–9S.

17. Libber J, Binkley N, Krueger D. Clinical observations in total bodyDXA: technical aspects of positioning and analysis. J Clin Densitom.2012;15(3):282–9.

18. Rothney MP, Brychta RJ, Schaefer EV, et al. Body compositionmeasured by dual-energy X-ray absorptiometry half-body scans inobese adults. Obesity (Silver Spring). 2009;17(6):1281–6.

19. Micklesfield LK, Goedecke JH, Punyanitya M, et al. Dual-energy X-ray performs as well as clinical computed tomography for the mea-surement of visceral fat. Obesity (Silver Spring). 2012;20(5):1109–14.

20. Sjostrom L, PeltonenM, Jacobson P, et al. Bariatric surgery and long-term cardiovascular events. JAMA. 2012;307(1):56–65.

21. Bazzocchi A, Diano D. Dual-energy x-ray absorptiometry in obesity.CMAJ. 2013;186(1):48.

22. Kendler DL, Borges JL, Fielding RA, et al. The Official Positions ofthe International Society for Clinical Densitometry: indications of useand reporting of DXA for body composition. J Clin Densitom.2013;16(4):496–507.

23. Chaston TB, Dixon JB, O’Brien PE. Changes in fat-free mass duringsignificant weight loss: a systematic review. Int J Obes (Lond).2007;31(5):743–50.

24. Dixon JB, Strauss BJ, Laurie C, et al. Changes in bodycomposition with weight loss: obese subjects randomized tosurgical and medical programs. Obesity (Silver Spring). 2007;15(5):1187–98.

25. Vatier C, Henegar C, Ciangura C, et al. Dynamic relations betweensedentary behavior, physical activity, and body composition afterbariatric surgery. Obes Surg. 2012;22(8):1251–6.

26. Tamboli RA, Hossain HA, Marks PA, et al. Body composition andenergy metabolism following Roux-en-Y gastric bypass surgery.Obesity (Silver Spring). 2010;18(9):1718–24.

27. Carrasco F, Ruz M, Rojas P, et al. Changes in bone mineral density,body composition and adiponectin levels in morbidly obese patientsafter bariatric surgery. Obes Surg. 2009;19(1):41–6.

OBES SURG

28. Zalesin KC, Franklin BA, LillystoneMA, et al. Differential loss of fatand lean mass in the morbidly obese after bariatric surgery. MetabSyndr Relat Disord. 2010;8(1):15–20.

29. Gasteyger C, Suter M, Calmes JM, et al. Changes in body composi-tion, metabolic profile and nutritional status 24 months after gastricbanding. Obes Surg. 2006;16(3):243–50.

30. Giusti V, Suter M, Heraief E, et al. Effects of laparoscopicgastric banding on body composition, metabolic profile andnutritional status of obese women: 12-months follow-up. Obes Surg.2004;14(2):239–45.

31. Garrapa GG, Canibus P, Gatti C, et al. Changes in body compositionand insulin sensitivity in severely obese subjects after laparoscopicadjustable silicone gastric banding (LASGB). Med Sci Monit.2005;11(11):CR522–8.

32. von Mach MA, Stoeckli R, Bilz S, et al. Changes in bone mineralcontent after surgical treatment of morbid obesity. Metabolism.2004;53(7):918–21.

33. Rojas P, Carrasco F, Codoceo J, et al. Trace element status andinflammation parameters after 6 months of Roux-en-Y gastric by-pass. Obes Surg. 2011;21(5):561–8.

OBES SURG