comparison of total and regional body composition in adolescent patients with anorexia nervosa and...

ORIG I NALRESEARCH

PAPER

Comparison of total and regional bodycomposition in adolescent patientswith anorexia nervosa and pair-matched controls

P. Schneider*, J. Biko*, D. Schlamp***, G.-E. Trott**, F. Badura**, A.Warnke**, andChr. Reiners**Clinic for Nuclear Medicine, **Clinic for Child and Adolescent Psychiatry, University of Würzburg, Würzburgand ***Heckscher Clinic, Munich, Germany

ABSTRACT. Body composition in 31 adolescent girls suffering from anorexia nervosa (ANwas measured at the time of hospitalization in order to assess the muscle/bone relationshipas a potential source of the development of osteopenia. Differences in lean tissue, fat andbone mass in total body, weight bearing and non weight bearing limbs were estimated in ANand pair-matched controls aged 14.2±1.8 years (range: 9-17 years). Further, it was investigated if bone mineral density (BMD) better reflects the muscle/bone relationship than bone mineral content (BMC). At the distal radius parameters measured by peripheral quantitative computed tomography (pQCT) were used to estimate the association of volumetric bone densityto bone strength and lean body mass. The correspondence to the same and different bodyregions was assessed. Total lean mass in the controls was closely related to total body bonemineral content (TBBMC), as was lean tissue and bone mass of the limb subregions (r=0.82 to0.93). In contrast, the correlation was significantly lower in AN (r=0.33 to 0.77). In the controls, the pQCT-derived bone strength was correlated with muscle mass of the forearm(r=0.78, p<0.001), but only moderately in AN (r=0.47, n.s.). Regional lean tissue was 11-20%and fat mass was 56-66% lower in AN (p<0.01). After adjustment for height, TBBMC was different at p=0.01. Within the limbs subregions, BMC (but not BMD) was different in bothgroups only in the upper arm and the thigh. BMC reflected the bone/muscle relationship better than BMD. Intra- and between group regressions gave no significant differences betweenweight bearing and non weight bearing limbs. In conclusion, the assessment of musculoskeletal factors may be a useful tool to develop individual preventive measures for therapyafter recovery of our patients.(Eating Weight Disord. 3, 179-187, 1998). ©1998, Editrice Kurtis

INTRODUCTION

Reduced bone density is a recognized com-plication of anorexia nervosa (AN). Whetheror not bone density can be regained, is amajor question already concerning youngadolescent individuals. The onset of AN mayalready occur at prepuberal stage, proceed-ing in a chronic course, known to affectbody weight and menstrual status in adoles-cent females. Reduction in body weight andestrogen deficiency are recognized asimportant risk factors for osteoporosis inadults. Around the time of puberty, theoccurrence of illness and estrogen deficien-cy may prevent the attainment of peak bone

density. Lean individuals, markedly depletedof adipose tissue, have an increased fracturerisk, that can be diminished by estrogentherapy (1). The association between bodyweight and bone density can partly beattributed to a function of the adipose celmass (2, 3).

It was suggested that bone mass and muscle force are both associated with a feedback mechanism (4-6). Muscle force is considered an important determinant of totabody bone mineral mass. In contrast, leantissue mass (LTM) and muscle strength haverecently been shown to be associated withBMD, partly determined by a moderategenetic component (7). LTM has been shown

Key words:Anorexia nervosa, bodycomposition, bone mass,bone strength, DXA, leanmass, pQCT.Correspondence:PD Dr. Peter Schneider,Clinic for Nuclear Medicine,Josef-Schneider-Strasse 2,97080 Würzburg, Germany.

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Regional body composition and anorexia nervosa

to be highly linear to bone mineral content(BMC) and independent of age or ethnicclassification (8). The relationship of BMCand LTM in the early onset of AN, in com-parison to controls, has not yet beenassessed. BMC deficiency observed in sever-al studies regarding adult individuals wasmore likely due to bone loss or to a deficientpeak bone density. In contrast, intensive epi-physeal bone formation during adolescenseis more likely to be associated with bonegain rather than loss. Therefore, in ourdesign of a cross sectional study, a deficitshould be detectable in comparison to acontrol group which is precisely matchedregarding height and age.

A previous study revealed musclestrength to be related to LTM (9). DXA-derived limb muscle mass was found toaccurately predict the muscle mass derivedfrom other muscle-related parameters (10).In several previous studies of AN, the cor-relation between BMC or BMD parameters(11-13) and fat free tissue has not beenshown. Recently, however, interesting per-spectives of the relation between muscle-force and BMC in children were pointedout (14). In our study the following aimswere addressed:

a) to assess differences in lean tissue, fatand BMC in total body, weight bearing andnon weight bearing limbs using DXA,

b) to investigate if BMD better reflectsthe muscle/bone relationship than BMC,and,

c) to analyze the association of volumetricbone density to bone strength and LTM atthe distal radius and the upper limb usingpQCT.

MATERIALS AND METHODS

1. Sample studiedThirty-one children and adolescent girls ofan age group between 9 and 17 were stud-ied, shortly after clinically relevant occur-rence of AN based on DSM IV (15) criteria.Two children of age 9 and 2 children of age11 had not reached menarche. The controlgroup was randomly drawn from a largergroup of children to match age and heightof the AN patients. These children hadbeen submitted for screening tests includ-ing bone densitometry in order to rule outevidence for thyroid, blood, bone or otherdiseases after having been exposed to

radioactive fallout at the Gomel area(Belarus) during childhood. They had allmaintained a normal lifestyle and thescreening tests gave no evidence of anydisease. The serum Ca-level in both groupswas not significantly different. All studiedsubjects were Caucasians.

2. Bone and soft tissue variablesmeasured

Peripheral QCT (16-18) was used to mea-sure cross sectional bone mass, apparentdensity (e.g. a structural property) andbone strength parameters. The latter pro-vide information about mechanical compe-tence of the radius at the measurement sitein terms of the cross sectional moment ofinertia (CSMI) or the second moment ofinertia (CSMR). These parameters weredetermined with a XCT900 pQCT device(Stratec Medizintechnik, Germany). A scoutview of the distal forearm was first per-formed to locate the measurement site at4% of the length of the ulna from the distalradius endplate, followed by a CT-scan.After applying filter algorithms and imagesegmentation (19), volumetric total and tra-becular bone density (mg/cm3) and area(mm2) were automatically determined.Using the average slice thickness, the tra-becular and cortical mass were estimatedin mg, based on the calibration standard.The total bone area was used to calculatethe cross-sectional properties. The integralsum of pixels containing bone was multi-plied by their square distances from thehorizontal (x-) axis passing through thecenter of mass of the cross section, as anapproximation of the maximum or xCSMI.The second moment of inertia (xCSMR) asa measure of bending strength was thenderived by division of xCSMI through themaximum excentricity. Accuracy error inmass determination was 5% for corticaland total mass using the European forearmphantom (20). General precision of themeasurements was below 3%.

Whole body scans were performed using aDPX-L DXA device (Lunar Corp., Madison,WI). The typical scan duration was 15 min-utes. The scan evaluation included regionalanalysis of the upper and lower extremitiesusing the research options of software ver-sion 1.34. Total body scans were analysedusing the “Auto Analysis” option. The validi-ty of the automatically set total body regionsof interest (ROI) was cross-checked and cor-

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rected if necessary. The limbs were analysedusing the “Manual Analysis” and the“Extended Research Analysis” options. Thesub-ROI’s were defined for the left and rightupper arm and forearm, medially by the ver-tical line bisecting the glenoid fossa andthrough the middle of the elbow and carpo-radial joints. The leg ROI’s were defined bythe oblique line superomedially, a transverseline between femur and tibia and a trans-verse line dividing distal tibia and talus. Theanalysis retrieved fat mass, LTM, BMC andBMD within each ROI. Assessment of bone,fat and fat free mass is generally achievedwith high precision (21-25). The reproducibil-ity of the DXA derived parameters wasbelow 2%, and comparable to 1-2% asdescribed in literature. Although accuracyerrors of ±19.5% were reported for theabsolute determination of total body fatusing DXA, the estimated parameters werehighly correlated (r=0.98) with the directchemical reference method (21). In our studyit was assumed to be comparable to a clinicalerror range of a reported 6% regarding fatand muscle mass (22,23). The accuracy errorof total body BMC and BMD measurementswas reported to be smaller than 40 g(approx. 2%) in children (standard estimateof error).

The radiation exposure in both proce-dures (total body DXA and pQCT) is smallerthan 0.1μSv. The procedures were necessaryto determine the bone mineral status of theindividuals for clinical reasons, therefore noapproval of the local ethic committee wasneeded.

3. StatisticsStatistical analysis of the data comprisedregression analysis, Students t-test forindependent samples and 1-way MANCO-VA to compare both groups after adjust-ment for height. STATISTICATM was usedto perform these tests. Significance wasconsidered at a p-level smaller than 5%(p<0.05).

RESULTS

The group differences as the results of the t-test are summarized in Table 1A. The pairmatched structure of the groups resulted inan identical mean age and standard devia-tion. Based on this approach, the anthropo-metric data showed a highly significant dif-

ference in body weight as expected, where-as height distribution was nearly identical.Height was taken as covariate in order toadjust all dependent body composition vari-ables. The adjustment revealed very smallchanges of the mean values (Table 1A). Thedifference in body weight was mainly dueto an average difference in fat tissue of 59%.Only 12% accounted for the difference inLTM. The adjusted difference in TBBMCmass was 13% (or 290 g) in both groups(p<0.01), whereas the TBBMD showed nosignificant difference. However, the rangeof TBBMC and TBBMD appeared to be con-siderably restricted in AN patients at thehigher end. The subregions reflected thesame findings.

The right and left side intra group com-parison of upper and lower leg subregionsrevealed correlation coefficients, rangingfrom r= 0.95 to 0.98 for soft tissue, andr=0.91 to 0.95 for BMC; BMD ranged fromr=0.82 to 0.87, respectively. Because no sig-nificant differences between right and leftside in the upper and lower extremitieswithin the groups were observed, werestricted the analyses and tables to the leftlimbs.

All bone mineral related parameters,except for the upper arm and the thighBMC (p=0.01 and p=0.004), were not signif-

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TABLE 1AT-test of global group characteristics in pair-matched controls vs

anorexia nervosa patients (n=31 per group). (Unadjustedmean±standard deviation, and mean,

MANCOVA-adjusted to height).

Controls Anorexia nervosa p-level

Age [years] 14.2±1.8 14.2±1.8 1.0

Weight [kg] 56.8±12.8 40.7±7.5 <0.001

Height [cm] 160.2±9.3 160.7±8.7 0.8

Serum calcium [mmol/l] 2.45±0.12 2.44±0.11 0.9

Total BMC [kg] 2.21±0.48 1.96±0.33 0.05(adj.) 2.23 1.94 0.01

Total BMD [g/cm2] 1.09±0.08 1.07±0.08 0.2(adj.) 1.10 1.05 0.1

Total lean mass [kg] 37.2±6.1 32.8±4.3 0.002(adj.) 37.3 32.6 <0.001

Total fat mass [kg] 16.2±8.2 6.7±5.0 <0.001(adj.) 16.3 6.6 <0.001

1


icantly different (Table 1B). The lean tissuecomparison between the groups revealedsignificant differences at all sites. The fatpresented the biggest differences betweencontrols and AN patients in the four ROI’scompared, matching the results of the totalbody fat mass comparison.

Table 2A presents the results of the cor-relation analyses of the regional soft tissueversus the bone mineral parameters of theupper and lower limb subregions, includ-ing the pQCT-derived strength parametersat the left distal radius. The different tissuecompartments of the upper arms and theforearms were highly correlated in the con-trols, whereas they were considerablylower in the AN patients. The correlation oftotal bone with lean tissue parameters inboth groups was generally higher as com-pared to the analysis of the subregions.

The pQCT-derived xCSMR of the radiusvs lean mass of the upper arm and theneighboring forearm correlated low inAN (r=0.33 and 0.47) as compared to thecontrols (r=0.66 and 0.78). Trabeculardensity and mass were not significantlycorrelated with the upper limbs LTM.However, cortical mass in controlsshowed a moderate correlation comparedto none in AN.

A comparison of DXA-derived BMC

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TABLE 1BMean±standard deviation and significance level of

MANCOVA-adjusted differences (covariate=height) of regionalbone mineral and soft tissue parameters in pair matched controls

versus AN patients (n=31 per group, left side limbs)

Controls Anorexia nervosa p-level

DXA-derived parametersBMC [g] UA 58±14 50±11 0.01

FA 46±12 43±9 n.s.T 213±55 180±33 0.004LL 155±40 139±24 n.s.

Lean mass [g] UA 1166±219 854±166 <0.001FA 544±111 438±78 <.0001T 4227±776 3498±612 <0.001LL 1672±316 1494±221 0.01

Fat mass [kg] UA 421±267 143±111 <0.001FA 147±71 60±39 <0.001T 2531±1207 1003±797 <0.001LL 734±316 321±221 <0.001

pQCT-derived parameters trabec. density (mg/cm3) 151±36 167±89 n.s. trabecular mass (mg) 22±6 23±7 n.s.cortical density (mg/cm3) 381±64 389±115 n.s.cortical mass (mg) 65±18 65±23 n.s.xCSMR (mm3) 182±53 161±39 n.s.

UA= upper arm, FA= forearm, T= thigh, LL= lower leg

TABLE 2A Correlation coefficients of the regional and total lean tissue and the bone mineral parameters of the left side limbs.

Lean massUpper arm Forearm Thigh Lower leg Total body

DXA Controls AN Controls AN Controls AN Controls AN Controls AN

Total body BMC - - - - - - - - 0.91 0.75Upper arm BMC 0.92 0.48 0.91 0.54 - - - - 0.92 0.69Forearm BMC 0.80 0.50 0.86 0.63 - - - - 0.84 0.74Thigh BMC - - - - 0.93 0.68 0.69 0.81 0.92 0.81Lower leg BMC - - - - 0.92 0.56 0.85 0.77 0.94 0.71Total body BMD - - - - - - - - 0.85 0.54Upper arm BMD 0.78 0.28* 0.66 0.31* - - - - 0.66 0.44Forearm BMD 0.50 0.33* 0.59 0.36* - - - - 0.54 0.50Thigh BMD - - - - 0.81 0.47 0.76 0.63 0.85 0.68Lower leg BMD - - - - 0.70 0.37 0.54 0.53 0.70 0.50

PQCTRadius trabec. density 0.21* 0.17* 0.22* 0.05* - - - - - -Radius trabec. mass 0.23* 0.04* 0.30* 0.14* - - - - - -Radius corical mass 0.59 0.00* 0.69 0.19* - - - - - -Radius xCSMR 0.66 0.33* 0.78 0.47 - - - - - -

*Marked correlations are p>.05 and not significant; AN=anorexia nervosa.


(resp. BMD) and lean mass parametersbetween remote sites generally showed asomewhat lower correlation. In the follow-ing analyses and tables we also includedonly BMC, since the poorer correlationsinvolving BMD did not permit furtherinsight.

The correlation coefficients of the region-al and total BMC parameters of bothgroups are presented in Table 2B. Therewas a close interrelationship between BMC

in the upper and lower subregions and inthe total body in controls, which appearedto be somewhat lower in AN patients. Thetotal body BMC had the highest correlationwith the subregions, which might merelyreflect the lowest variation in the estima-tion of the parameters. Volumetric trabecu-lar mass and density, representing a mater-ial quality, were only modestly related toDXA-derived BMC. In contrast, cross sec-tional cortical mass and CSMR in the con-

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TABLE 2BCorrelation coefficients of the regional and total bone mineral content and the pQCT-derived parameters.

Upper arm Forearm Total bodyBMC BMC BMC

Controls AN Controls AN Controls AN

Upper arm BMC - - 0.90 0.82 0.94 0.88

Forearm BMC 0.90 0.82 - - 0.91 0.87

Thigh BMC 0.93 0.81 0.88 0.82 0.94 0.91

Lower leg BMC 0.91 0.58 0.85 0.80 0.95 0.88

Radius trabec. density 0.14* 0.21* 0.20* 0.13* 0.13* 0.03*

Radius trabec. mass 0.30* 0.46 0.23* 0.38 0.26* 0.21*

Radius cortical mass 0.73 0.60 0.69 0.59 0.70 0.49

Radius xCSMR 0.80 0.67 0.75 0.76 0.80 0.71

*Marked correlations are p>0.05 and not significant.

TABLE 3MANCOVA-adjusted (covariate=height) regression analysis of bone variables to lean mass in AN and controls. Significance of

the differences between the height-adjusted regressions in both groups.

Controls AN Significance

Region of interest r Slope (Y) Constant (Y) r Slope (Y) Constant (Y)

Total bodyBMC/lean mass 0.91 11.4 11.9 0.75 9.7 13.7 n.s.

ForearmxCSMR/lean mass 0.82 2.9 645 0.47 1.4 622 n.s.

Upper armBMC/lean mass 0.92 14.9 315 0.33 7.8 460 p<0.001

ForearmBMC/lean mass 0.90 9.9 95 0.63 6.3 179 p<0.01

ThighBMC/lean mass 0.93 13.1 1338 0.68 12.6 1228 p<0.01

Lower legBMC/lean mass 0.85 6.7 619 0.77 7.1 499 n.s.


trols showed a moderate correlation withtotal body BMC. The correlations betweenbone strength parameters at the distalradius and DXA-derived BMC at the fore-arm and the upper arm were surprisinglyhigh in controls, and somewhat but not sig-nificantly lower in AN patients. Table 3summarizes the differences in the slopes ofthe MANCOVA-adjusted regressions. Theadjustment with height as covariate result-ed in very small effects. Therefore, the cor-rection equations are not shown. Theregressions of forearm CSMR, lower legBMC and total BMC vs lean mass were notsignificantly different between bothgroups. Regional bone mineral parametersgenerally showed a close correlation withlean tissue mass in controls, whereas corre-lation was reduced in AN patients (Figs. 1-

4). Both lean mass and BMC in AN did notreach the high values of the controls.

DISCUSSION

This study particularly focuses on muscu-loskeletal differences of the so-called “weightbearing” compared to “non weight bearing”skeletal regions of interest, including someinformation of pQCT-assessed bone archi-tecture related to DXA-assessed lean tissue.The latter is assumed to represent predomi-nantly muscle as the functional counterpart.Intra group comparison of the study clearlyrevealed that the regression analysis of boneand lean tissue of the upper (non weightbearing) compared to the lower (weightbearing) limb was not substantially different

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FIGURE 1Cross-sectional second moment of inertia derived by pQCT of the leftdistal forearm (CSMR) versus forearm lean mass, derived by DXA,

after MANCOVA adjustment with body height as covariate.

FIGURE 2Bone mineral content (BMC) of the left upper arm versus lean mass,


FIGURE 3Bone mineral content (BMC) of the left lower leg versus lean mass,


FIGURE 4Total body bone mineral content (BMC) versus total lean mass, after

MANCOVA adjustment with body height as covariate.


in the controls and in AN patients. This find-ing is in line with newly discussed perspec-tives of functional adaptation of bones (4-6,26), in that each bone is specifically adaptedby modelling to its imposed loads, to handleweight and forces. Modelling correspond-ingly increases bone strength in limbs, andmuscle force appears to be adapted.

Furthermore, our results characterizesome differences in bone mineral, lean tissueand fat mass at the onset or the early stage ofAN. The pair-matched structure of our sam-ples allowed us to exclude height and age asimportant confounding factors. As predictedfrom new insights in bone biology (6), ourAN patients did not reach the bone and mus-cle mass level of the comparatively more“obese” controls. The difference betweenforearm CSMR and the associated musclemass was considerably smaller as comparedto the difference between bone and musclemass. This suggested a mechanism whichtried to achieve maximum strength, compen-sating for a limited (or reduced) amount ofbone. The finding was also suggested in anearlier study, where a strong correlationbetween (cross sectional-) bone mass andbone strength (27) in healthy and osteoporot-ic fractured individuals was found. This cor-relation was also confirmed by mechanicalex vivo testing (16, 17).

Heredity of muscle and bone parametersmight be an important factor (1). However,BMD at standard measurement sites (lum-bar spine, femoral neck, distal forearm) anddirectly measured muscle strength demon-strated a poor correlation. A reason for thiscould be the inadequate measurement sitesand lacking direct functional association.

Regional and total BMC, BMD and total tis-sue composition in a fairly large number ofboys and girls have been investigated by twodifferent groups (28, 29) in order to establishnormative data. In both studies the ratio ofBMC or BMD to lean tissue has not been pre-sented. A poor correlation of fat-free tissue toBMD was found, when standard regions ofinterest of the lumbar spine and hip were ana-lyzed (30), probably due to functionally notrelated lean tissue and BMD. In contrast, inboth groups of our study, the non muscularlean mass in total body estimation tended toenhance the correlation with total BMC. BMCwas also found to generally enhance the cor-relation with soft tissue parameters, com-pared to BMD. This complies with the obser-vation of Barondess et al. (31). Nutrition, exer-

cise, endocrine and other factors may haveaffected our AN patients, in that a higher vari-ation in soft tissue mass and bone variableswas observed. Apparently, due to these influ-ences, part of our patients obviously wasunable to improve the bone mass in compari-son to their age-matched controls. A possibleexplanation might be that reduced activationgenerally causes disuse atrophy to muscle, i.e.it decreases expression of protein isoformscomprising the contractile system resulting inbone mass reduction, as known from long-term space flight (32-34). Weight loss in ourAN patients occurred in a comparable shorttime, however, based on a pathophysiologi-cally different situation.

The results at the radius show that ANpatients have been at least able to optimizethe spatial distribution of the bone by model-ing or remodeling, in order to achieve opti-mal bone strength. This might explain whythe correlation between forearm LTM andpQCT-derived bone parameters increased inthe following order: bone density > mass >strength.

Analysis of the limbs does have theadvantage of a low percentage of non liquidand non muscular lean tissue, mainly con-sisting of muscle mass (35). It was conclud-ed that muscle mass is an important deter-minant of total body bone mineral mass andpeak bone mass in different regions of theskeleton (36). Our results clearly pointed outlean mass as a strong determinant of theassociated regional BMC. Although neigh-boring bone or muscle mass may directlyinteract and determine each other, this doesnot necessarily apply to remote sites.Comparison of remote sites should be inter-preted with caution.

Changes in LTM are associated withchanges in strength and force (r=0.72 to0.91) (37), and, as recently reported, theymay also be associated with genetic compo-nents (7). AN patients intending to looseweight, developed quite different levels ofphysical activity (12). Therefore, as the bene-fit from this study a differentiated treatmentregimen could be derived regarding nutri-tional aspects, hormone status, restriction oreven stimulation of exercise. These mea-sures should be appropriate to the specificsituation before or after recovery from thesevere phase of illness and hospitalization.

Between group comparison showed theinability of the AN patients to reach a nor-mal bone mass which was significant at the

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upper arm and the thigh. This observationwas also independent whether the limbwas weight bearing or not. The deficientbone mass coincided expectedly with a lackof muscle mass, supported by the abovediscussed biomechanical proposal (4-6).The proposed rules continuously governadaptation of any bone during skeletalgrowth and development (26), regardless ofsite. In addition, the reduced muscle massmight be considered as a determinant fac-tor to maintain osteopenia and developosteoporosis in future. Hospitalization withshort term bedrest periods was shown notto affect total bone mass very impressivelyas might be concluded from trabecularbone density changes (11, 38, 39).

Earlier cross-sectional studies supportedan optimistic outlook, as subgroups whohad gained weight had improved bone den-sities. The first report of a long term recov-ered adult AN group included no specificbaseline and/or follow-up information, com-parable to our results. Longitudinal studies,however, have been suggested (40). The dis-cussion regarding the value of estrogentherapy remains controversial, even sug-gesting adverse effects on epiphyseal pro-ductivity. This is based on evidence support-ing an important role of estrogen in growthplate closure in both males and females (41,42). Our approach may provide additionalparameters as a basis to follow up the influ-ence of therapy measures on muscle andbone mass.

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