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REVISTA

PAULISTA

DE

PEDIATRIA

www.rpped.com.br

ORIGINAL

ARTICLE

Practice

of

martial

arts

and

bone

mineral

density

in

adolescents

of

both

sexes

Igor

Hideki

Ito

a,

,

Alessandra

Madia

Mantovani

a

,

Ricardo

Ribeiro

Agostinete

b

,

Paulo

Costa

Junior

b

,

Edner

Fernando

Zanuto

b

,

Diego

Giulliano

Destro

Christofaro

b

,

Luis

Pedro

Ribeiro

c

,

Rômulo

Araújo

Fernandes

b

aInstitutodeBiociências,UniversidadeEstadualPaulista‘‘JúliodeMesquitaFilho’’(Unesp),RioClaro,SP,Brazil bUniversidadeEstadualPaulista‘‘JúliodeMesquitaFilho’’(Unesp),PresidentePrudente,SP,Brazil

cUniversidadedoAlgarve,Faro,Portugal

Received29April2015;accepted13September2015 Availableonline2January2016

KEYWORDS

Martialarts;

Bonemineraldensity; Adolescents

Abstract

Objective: The purposeof thisstudy was to analyze therelationship between martial arts practice(judo,karateandkung-fu)andbonemineraldensityinadolescents.

Methods: The study was composed of 138 (48 martial arts practitioners and 90 non-practitioners) adolescentsofboth sexes, with anaverage age of12.6 years.Bone mineral densitywasmeasuredusingDual-EnergyX-rayAbsorptiometryinarms,legs,spine,trunk,pelvis andtotal.Weeklytrainingloadandprevioustimeofengagementinthesportmodalitywere reportedbythecoach.Partialcorrelationtestedtheassociationbetweenweeklytrainingload andbonemineraldensity,controlledbysex,chronologicalage,previouspracticeandsomatic maturation.Analysisofcovariancewasusedtocomparebonemineraldensityvaluesaccording tocontrolandmartialartsgroups,controlledbysex,chronologicalage,previouspracticeand somaticmaturation.Significantrelationshipsbetweenbonemineraldensityandmusclemass wereinsertedintoamultivariatemodelandtheslopesofthemodelswerecomparedusingthe Studentttest(controlversusmartialart).

Results: Adolescentsengagedinjudopracticepresentedhighervaluesofbonemineraldensity thanthecontrolindividuals(p-value=0.042;Medium Effect size[Eta-squared=0.063]),while the relationship between quantityofweeklytraining andbone mineral densitywas signifi-cantamongadolescentsengagedinjudo(arms[r=0.308]andlegs[r=0.223])andkung-fu(arms [r=0.248]andspine[r=0.228]).

Conclusions: Differentmodalitiesofmartialartsarerelatedtohigherbonemineraldensityin differentbodyregionsamongadolescents.

©2015SociedadedePediatriadeSãoPaulo.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBYlicense(https://creativecommons.org/licenses/by/4.0/).

Correspondingauthor.

E-mail:[email protected](I.H.Ito).

http://dx.doi.org/10.1016/j.rppede.2015.09.003

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PALAVRAS-CHAVE

Artesmarciais; Densidademineral óssea;

Adolescentes

Práticadeartesmarciaisedensidademineralósseaemadolescentesdeambosos sexos

Resumo

Objetivo: O objetivo desse estudo foi analisar a relac¸ão entre aprática de artes marciais (judô,karatêekung-fu)eadensidademineralósseaemadolescentes.

Métodos: Oestudofoicompostopor138adolescentes(48praticantesdeartesmarciaise90não praticantes)deambosossexos,comidademédiade12,6anos.Adensidademineralósseafoi medidausandoabsortometriaradiológicadeduplaenergiaembrac¸os,pernas,coluna,tronco, pelveetotal.Acargadetreinamentosemanaleotempoanteriordeenvolvimentona modal-idadeesportivaforamrelatadospelotreinador.Acorrelac¸ãoparcialtestouaassociac¸ãoentre a cargasemanalde treinamento eadensidade mineral óssea, controlada para sexo,idade cronológica,práticaanteriorematurac¸ãosomática.Aanálisedecovariânciafoiutilizadapara compararosvaloresdedensidademineralósseadeacordocomosgruposcontroleedeartes marciais, controlados parasexo, idadecronológica, práticaanterior ematurac¸ãosomática. Associac¸õessignificativasentreadensidademineralósseaeamassamuscularforaminseridas em ummodelomultivariadoeasinclinac¸ões dosmodelosforamcomparadasusandooteste

tdeStudent(controleversusartemarcial).

Resultados: Osadolescentesenvolvidosnapráticadejudôapresentaram valoresmaioresde densidademineralósseadoqueosindivíduosdogrupocontrole(p=0,042;tamanhodeefeito médio[eta-quadrado=0,063]),enquanto arelac¸ãoentreaquantidadedetreinos semanaise adensidademineralósseafoisignificativaentreosadolescentespraticantesdejudô(brac¸os [r=0,308]epernas[r=0,223])ekung-fu(brac¸os[r=0,248]ecoluna[r=0,228]).

Conclusões: Diferentesmodalidadesdeartesmarciaisestãorelacionadascommaiordensidade mineralósseaemdiferentesregiõesdocorpoemadolescentes.

©2015SociedadedePediatriadeSãoPaulo.PublicadoporElsevierEditoraLtda.Esteéumartigo OpenAccesssobalicençaCCBY(https://creativecommons.org/licenses/by/4.0/deed.pt).

Introduction

Duringadulthood,bonehealthisaffectedbyphysical inac-tivityandaging,sinceboth affectbone structureand can lead to osteoporosis and fractures.1 Therefore, physical

exerciseiswidelyadvocatedforthepreventionoffractures andosteoporosisthroughincreasesinbonemineraldensity (BMD)andreductioninage-relatedboneloss.2Inadulthood,

physical exercise produces low increments in bone mass2

and,thus,childhoodandadolescenceappeartobethemost significantperiodsinwhichtoimproveBMD2,3and,hence,

preventoutcomessuchasosteoporosisinadulthood. Duringchildhoodandadolescencegrowthhormone con-tributes to bone mass gain and the concentration of this hormone in the blood is increased by physical exercise.4

Furthermore, the strength and geometry of bone are substantially affected by the higher continuous muscle contractions observed in sport activities.5 Therefore, the

practiceofphysicalactivityisrecommendedandsome stud-ieshavereportedimprovementinBMDinmanymodalities6---8

suchassoccer,9volleyball10andbadminton;11butthisevent

islessreportedinmartialarts.12

Martialartsincludehigh-magnitudeforcesthrough mus-clepullingonthebone,ground reactionforcesintensified bytheabsenceoffootweartoattenuateimpactshocksand high-impactloading of theskeleton due torepeatedfalls ontheground.13TheAmericanCollegeofSportsMedicine14

recognizesthebeneficialeffectofsportspracticeonbone mass gain during human growth,but the same statement

identifiesthat,althoughmartialartshaveaspectsrelatedto BMDgain,thefindingsaremainlybasedoneliteathletes,6

anditisnotclearifthisrelationshipoccursinchildrenand adolescents.15 Moreover,the absenceof controlby

impor-tantvariablesrelated tobone mass gainduring childhood andadolescence(fat free mass[FFM] andbiological mat-uration) constitutes a limitation in studies analyzing the relationship between sport practice and BMD in Pediatric populations.16

Therefore,theaimsof thisstudywere(i)toverifythe relationshipbetweenwidelyperformedmartialarts(judo, karateandkung-fu)andBMDinadolescents,aswellas(ii) toidentifywhetherthisrelationshipisindependentof bio-logicalmaturationandFFM.Wehypothesizedthat martial artspracticewouldberelatedtohigherBMDinadolescents ofbothsexes.

Method

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conducted during 2013 and 2014 and the presented data formspartofthebaselinemeasures.

Sample size estimation was performed using an equa-tionbasedonanalysisofvariance(ANOVA),whichtookinto accountaminimumdifferencefor BMD of 0.255(g/cm2)13

between the control and martial arts groups, a standard deviationof0.180g/cm2,fourindependentgroups(Control,

Karate,Kung-fuandJudo),apowerof80%andalphaof5%. Finalsample sizewasestimatedasa minimumof12 ado-lescentsper groupand,therefore,atleast48 adolescents wererequired.Foradolescentsengagedinmartialarts,the followingcriteriawereincluded: (i)agedbetween11and 17;(ii) a minimumof 03 months of previous involvement inthecurrentmartialartand(iii) thecoach’spermission. Adolescentsofbothsexes,engagedinmartialarts(regional level),wererecruitedfromsportclubsindifferentregions ofthecityasfollows:Karate(9girlsand5boys[Shotokan

style]),Judo (8girls and10 boys)andKung-fu (1girland 15boys[sandastyle]).Thecontrolgroupwascomposedof adolescentsfromfiveschoolslocatedindifferentregionsof thecity.Inthesefiveschools,allstudentsagedbetween11 and17wereinvitedtoparticipateandafterconfirmingthat theymettheinclusioncriteria,([i]agedbetween11and17 and[ii]notengagedinregularphysical activity/sport out-sideschool),thecontrolgroupwascomposedof36girlsand 54boys.

Theparentsorguardianssignedawrittenconsentform andthestudyhadbeenpreviouslyapprovedbytheEthical BoardoftheSaoPauloStateUniversityCampusofPresidente Prudente,Brazil.

Body weight wasmeasured usinga digital scale (Filiz-zola,SaoPaulo,Brazil,tothenearest0.1kg)andheightwas measuredwithawall-mountedstadiometer(tothenearest 0.1cm) with a maximum length of 200cm. All anthropo-metricmeasurementswereperformedfollowingpreviously publishedstandard methods.17 The leglength and

sitting-heightwerealsoassessedusingstandardizedtechniques.17

Thesemeasurementswere usedtocalculate thematurity offset, which denotes the time (years) from/to peak of heightvelocity(PHV),18 an importantmaturationalevent.

PHVisanindicatorofsomaticmaturity(lineargrowth)and reflectstheageofmaximumrateofgrowthinstatureduring adolescence.

Weeklytrainingloadwasmeasuredbymeansofa ques-tionnaire filled in by the coach, in which the following questions about each athlete were asked: (i) the num-ber of days per week and (ii) number of hours per day spent training.Weekly training load was calculated using theequation:numberofdays×hoursperday(expressedin minutes/week).Timeofpreviousengagementinthemartial artwasalsoreportedbythecoach(inmonths),aswellas theuseofanysupplementation(weightlossormusclemass gain).

The bone mineraldensity (in g/cm2) in differentbody

regions([i]wholebodyBMD,[ii]BMDofthelowerlimbs,[iii] BMDoftheupperlimbs,[iv]BMDofthespineregion,[v]BMD ofthepelvisand[vi]BMDofthetrunk)wasanalyzedusing the Dual-Energy X-ray Absorptiometry (DEXA) technique. The device usedwasthe Lunarmodel --- DPX-NT(General Electric [GE]). The radiation dose that each participant receivedwaslessthan0.05mrem,inotherwords,equivalent to50timeslessthanaconventionalX-rayexamination.19All

participantsworelightclothingandwerebarefoot(nometal belongingsonthebody),andwereplacedontheequipment in the supine position, remaining motionless throughout the examination, approximately15min. The results were calculated by means of specific softwareprovided by the manufacturer.Moreover,measuresofbodyfatness(asa per-centage) and FFM (in kg) were also provided by the DXA software.

Chronologicalage,sex(maleorfemale),FFMandsomatic maturation were treated as potential confounders in this study and, thus, were used to adjust the multivariate models. Chronological age (in a decimal scale) was esti-matedbythedifferencebetweenbirthdateandassessment date.

The normality of data was analyzed using the Komogorov---Smirnov test (weekly training load pre-sented non-parametric distribution and, thus, was log transformed).Descriptivestatisticsconsisted ofmeanand standard-deviationvalues.Partialcorrelationanalyzedthe relationship between weekly training load and BMD con-trolledbysex,chronologicalage,timeofpreviouspractice and somatic maturation.Analysis of covariance (ANCOVA) was used to compare BMD values relating to the control and martial arts groups, controlled by sex, chronological age,timeofpreviouspracticeandsomaticmaturation(the Bonferroniposthocwasusedwhennecessary).Measuresof effect size were provided through values of Eta-squared. Finally,significantrelationshipsbetweenBMDandFFMwere insertedintoamultivariatemodel(adjustedsimultaneously byage,sexandsomaticmaturation)andtheslopesofthe models were compared using the Student t test (control versus martial art). All statistical procedures were per-formedusingthesoftwareBioEstat(version5.0[Mamirauá Institute,Tefé---Brazil])andthesignificancelevel(p-value) wassetatp<0.05.

Results

The sample of the present study was composed of 137 adolescents (47 engaged and 90 not engaged in martial arts).Significantdifferencesbetweengroupswereobserved for the variables of age (p-value=0.020), body weight (p-value=0.026) and somatic maturation (p-value=0.012). Adolescents engagedinmartialartspresentedhigherBMD intheirarms,legs,trunk,spineandtotalBMD(Table1).

TheANCOVAidentifiedthatonlyadolescentsengagedin judo practicepresentedhighervalues ofBMD in thearms thanthecontrolgroup(Eta-squared=0.063;mediumeffect size)aftercontrollingbysex,age,FFMandsomatic matu-ration(Table2).

Even aftercontrolling for potentialconfounders,there weresignificantrelationshipsbetweenFFMandBMDinthe control group (arms, legs, trunk, spine and whole body), Judogroup(trunk,pelvisandspine)andKarategroup(legs, trunk,pelvis,spine andwholebody)(Table 3).Therewas a strongerrelationshipbetween FFMandwholebodyBMD in the controland Karategroups thanthe Kung-fu group. Similarpatternswerealsoobservedforspine,trunkandleg BMD.

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Table1 Generalcharacteristicsoftheadolescentsstratifiedbypracticeofmartialarts(n=137).

Variables Controlgroup(n=90) Martialartsgroup(n=47) p-value Mean(SD) Mean(SD)

Age(years) 11.93(0.90) 12.36(1.01) 0.020 Weight(kg) 49.50(11.36) 54.78(15.52) 0.026 Stature(cm) 155.67(7.73) 158.43(11.31) 0.165 %bodyfatness 27.62(12.43) 27.59(12.56) 0.808 Fatfreemass(kg) 32.43(5.47) 35.35(9.70) 0.065 Maturityoffseta

−2.67(0.72) −2.26(0.94) 0.012

Bonemineraldensityg/cm2

Arms 0.68(0.06) 0.76(0.19) 0.007

Legs 1.08(0.10) 1.18(0.23) 0.015

Trunk 0.83(0.07) 0.88(0.09) 0.002

Pelvis 1.11(0.97) 1.07(0.13) 0.790

Spine 0.89(0.11) 0.95(0.12) 0.002

Wholebody 1.01(0.07) 1.04(0.09) 0.010

SD,Standarddeviation.

Fisher’sexacttestwithp-value=0.020.

a Ageatpeakheightvelocity.

Table2 Analysisofcovarianceestimatedmeansofbonemineraldensityinadolescentsaccordingtocontrolandmartialarts (n=137).

Variables Control(n=90) Judo(n=17) Karate(n=14) Kung-fu(n=16) ANCOVA

Mean(SE) p-value Eta-squared Effectsize Arms(g/cm2) 0.695(0.01) 0.771(0.02)a 0.695(0.03) 0.735(0.03) 0.042 0.063 Medium

Legs(g/cm2) 1.105(0.01) 1.173(0.03) 1.139(0.04) 1.150(0.04) 0.264 0.031 Small

Trunk(g/cm2) 0.845(0.01) 0.841(0.01) 0.863(0.02) 0.876(0.01) 0.243 0.032 Small

Pelvis(g/cm2) 1.122(0.08) 1.028(0.20) 1.098(0.24) 1.089(0.23) 0.979 0.001 Trivial

Spine(g/cm2) 0.904(0.01) 0.897(0.02) 0.944(0.02) 0.963(0.02) 0.083 0.051 Small

Wholebody(g/cm2) 1.021(0.01) 1.009(0.01) 1.033(0.02) 1.049(0.02) 0.292 0.029 Small

ANCOVA,analysisifcovariancecontrolledbysex,age,fatfreemassandsomaticmaturation;SE,Standarderror.

a p-value<0.05comparedtothecontrolgroup.

3.15±1.20hours/week for Kung-fu (p-value<0.001 among all martialarts). Even aftercontrolling for potential con-founders,BMD inthelegsandarmswasrelatedtoweekly trainingloadintheJudo group.Similarrelationshipswere identifiedintheKung-fugroupforarmsandspine(Table4). TherewerenosignificantrelationshipsfortheKarategroup.

Discussion

Thefindingsofthepresentstudyidentifiedthatadolescents engagedin martialartspresented higherBMDin different bodyregions;howeverBMDvaluesweresimilaramongthe martialartstested.Moreover,therelationshipbetweenFFM and BMD occurred at different magnitudes in the control groupanddifferentmartialartsgroupsanalyzed.

Inthepresentstudy,theweeklytrainingloadpresented asignificantrelationshipwithBMD,principallyforthearms andlegs.Regardingtheupperlimbs,Kung-fuandJudo pre-sented a significant relationship between weekly training load and BMD when compared to the control group. The upperlimbsarewidelyusedinJudopracticeandthus our findingswereexpected(highervaluesthanthecontrolgroup

andasignificantrelationshipwithweeklytrainingload).On theotherhand,ourfindingsalsosuggest thatthisspecific Kung-fufightingstyle(calledsanda)hasasignificantimpact ontrainingandfighting,asitencompassesalargenumberof techniqueswithphysicalimpacttotheupperlimbs,suchas awidevarietyofpunches.20Karatepresentedsimilarvalues

tothecontrolgroup,perhapsbecauseKarateshotokan(the stylestudied) is considered a formof semi contact (dur-ingcompetitions, the physical contactis prohibited)and, thus,physicalcontactisnotcommoninthetrainingofthis modality.

In this sample, no significant differences were found in the pelvis BMD of practitioners and non-practitioners, suggesting that these methods of combat do not include mechanisms for jumping or generating impactin the hip region in the way that volleyball and artistic gymnastics do.21 Inhighlytrainedathletes(between18and25 years)

karate and judo practice increases BMD more than the practiceof waterpolo.6 In addition,judo andtaekwondo

practitioners presented higher BMD than runners.22

How-ever,intheaforementionedstudies,6,22pelvisBMDwasnot

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Table3 Slopecomparisonsoftherelationshipbetweenfat freemassandbonemineral densityinadolescentsofdifferent martialarts(n=138).

Bonemineral density(g/cm2)

Control(n=90) Judo(n=17) Karate(n=14) Kung-fu(n=16) FFM(kg) FFM(kg) FFM(kg) FFM(kg)

␤(␤95%CI)a (␤95%CI)a (␤95%CI)a (␤95%CI)a

Arms(g/cm2) 0.006(0.004to0.009) 0.005(0.069

to0.080)

0.010(−0.001 to0.020)

0.004(−0.002 to0.010) Versuscontrol --- p-value=0.976 p-value=0.435 p-value=0.528 Legs(g/cm2) 0.013(0.010to0.017) 0.010(

−0.085 to0.105)

0.026(0.011 to0.042)

0.003(−0.003 to0.009) Versuscontrol --- p-value=0.945 p-value=0.077 p-value=0.006 Trunk(g/cm2) 0.010(0.007to0.012) 0.023(0.006

to0.040)

0.017(0.005 to0.028)

0.001(−0.003 to0.005) Versuscontrol --- p-value=0.110 p-value=0.173 p-value=0.001 Pelvis(g/cm2) 0.022(0.026to0.070) 0.035(0.007

to0.064)

0.024(0.007 to0.040)

0.001(−0.006 to0.005) Versuscontrol --- p-value=0.635 p-value=0.936 p-value=0.385 Spine(g/cm2) 0.012(0.008to0.015) 0.031(0.010

to0.052)

0.026(0.007 to0.045)

−0.001(-0.008 to0.007) Versuscontrol --- p-value=0.065 p-value=0.132 p-value=0.002 Wholebody(g/cm2) 0.007(0.005to0.010) 0.016(0.001

to0.032)

0.017(0.005 to0.029)

0.002(−0.003 to0.008) Versuscontrol --- p-value=0.206 p-value=0.053 p-value=0.027

FFM,fatfreemass.

aModeladjustedbysex,ageandsomaticmaturation.Boldindicatesp-valuesignificantandpositivecorrelationbetweenfatfreemass

andbonemineraldensity.

Table4 Partialcorrelationbetweenbonemineraldensityandweeklytrainingloadinadolescentsofdifferentmartialarts (n=138).

Bonemineral density(g/cm2)

Controlversus Judo

(n=108)

Controlversus Karate (n=104)

Controlversus Kung-Fu (n=106)

r(r95%CI) r(r95%CI) r(r95%CI)

Arms 0.308(0.126to0.470) 0.018(−0.175to0.210) 0.248(0.060to0.419)

Legs 0.223(0.036to0.395) 0.144(−0.050to0.328) 0.185(−0.006to0.363) Trunk 0.012(−0.177to0.201) 0.124(−0.070to0.309) 0.171(−0.020to0.350) Pelvis −0.018(−0.206to0.172) −0.008(−0.200to0.185) −0.013(−0.203to0.178) Spine −0.009(−0.198to0.180) 0.165(−0.028to0.347) 0.228(0.039to0.401)

Wholebody −0.071(−0.257to0.120) 0.065(−0.129to0.254) 0.149(−0.043to0.330)

Modeladjustedbysex,age,somaticmaturationandfatfreemass.BoldindicatesapositivecorrelationbetweenBMWandweeklytraining load.

Musclemassandbiologicalmaturationhavebeenpointed out as important determinants of the bone mass gain andgeometryrelatedtosportpractice,23,24 predominantly

becauseboth variablesarestrongly relatedtoeach other duringchildhoodandadolescence.Ontheotherhand,the absenceofmusclemassandbiologicalmaturationin stud-iesanalyzingBMDvaluesandsportpracticeinadolescents constitutesarelevantlimitationinthespecializedscientific literature.16Inourstudy,sportpracticeaffectedBMDvalues

independentofthesomaticmaturationstatusorvaluesof FFM,which agreeswithFerry,25 whoalsoidentifiedthat8

monthsofsoccerpracticeaffectedbonegeometryevenin post-pubertaladolescents.Apparently,thepathwayslinking

sportpractice(inthis case,martialarts) andbonehealth duringadolescenceareprobablyboostedbybiological mat-urationevents,butthesepathwaysseemtobeindependent ofbiologicalmaturation.

Althoughsome authors have found a positiveeffect of othersportmodalitiesonBMD,13,23,24,26 thereisno

consen-sus about the ideal training loadfor young athletes. The guidelineoftheAmericanCollegeofSportsMedicine14

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betweenexerciseintensityandquantityfortargetingBMD gainin adolescentsis stillunclear andfurtherresearchis necessary.

Itisimportanttopointoutsomelimitationsofthisstudy; thecross-sectional designin whichthereis anabsenceof causality should be considered. Moreover, the absenceof nutritionalfactors(e.g.calciumandvitaminD)andexposure tosunlightshouldbeconsideredinfuturestudies.Allbone variablesanalyzedinthepresentstudyarestronglyaffected bybiologicalmaturation,whichiscommonlyrepresentedby theTannermethod(sexualmaturation).Inthepresentstudy PHVwasadoptedasamaturationmarker,asPHVisa non-invasivemethod, whichdiscriminates maturationalevents (hormonalpatterns)aseffectivelyastheTannermethodin bothsexes.27Finally,DXAdoesnotprovidemeasuresofbone

geometry, which could be useful in studies analyzing this issue.25

In conclusion,despitethelimited understandingof the effectsofmartialartsonchildrenandadolescents,a pos-itive relationship between BMD and practice of martial artswasidentified,although thisrelationshipseemstobe dependentonthemartialartanalyzed.

Funding

Conselho Nacional de Desenvolvimento Científico e Tec-nológico(CNPq),Brazil.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

The authorswouldlike tothanktheCNPq(MasterDegree scholarship) andSao Paulo Research Foundation ---FAPESP (Process:2013/06963-5[Undergraduatescholarship]).

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Table 1 General characteristics of the adolescents stratified by practice of martial arts (n=137).
Table 3 Slope comparisons of the relationship between fat free mass and bone mineral density in adolescents of different martial arts (n=138).

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