REVISTA
PAULISTA
DE
PEDIATRIA
www.rpped.com.br
ORIGINAL
ARTICLE
Waist
circumference
as
a
mediator
of
biological
maturation
effect
on
the
motor
coordination
in
children
Leonardo
G.O.
Luz
a,d,
André
Seabra
b,
Cristina
Padez
c,
João
P.
Duarte
d,
Ricardo
Rebelo-Gonc
¸alves
d,
João
Valente-dos-Santos
d,e,
Tatiana
D.D.
Luz
a,
Bruno
C.M.
Carmo
a,
Manuel
Coelho-e-Silva
d,∗aLaboratóriodeCineantropometria,AtividadeFísicaePromoc¸ãodaSaúde(Lacaps),UniversidadeFederaldeAlagoas(Ufal),
Arapiraca,AL,Brazil
bCentrodeInvestigac¸ãoemAtividadeFísica,SaúdeeLazer(CIAFEL),UniversidadedoPorto,Porto,Portugal cCentrodeInvestigac¸ãoemAntropologiaeSaúde(CIAS),UniversidadedeCoimbra,Coimbra,Portugal dUniversidadedeCoimbra,Coimbra,Portugal
eUniversidadeLusofonadeHumanidadeseTecnologias,Lisboa,Portugal
Received4August2015;accepted17January2016 Availableonline15June2016
KEYWORDS
Biological maturation; Physicalfitness; Anthropometrics; Children
Abstract
Objective: Thepresentstudy aimedto:1) examinetheassociationofbiologicalmaturation effectonperformanceatamotorcoordinationbatteryand2)toassesswhethertheassociation betweenbiologicalmaturationandscoresobtainedinmotorcoordinationtestsismediatedby someanthropometricmeasurement.
Methods: Theconvenience sampleconsisted of73 malechildren aged 8yearsold. Anthro-pometric data consideredtheheight, body mass, sittingheight, waistcircumference, body massindex,fatmassandfat-freemassestimates.Biologicalmaturationwasassessedbythe percentageofthepredictedmaturestature.Motorcoordinationwastestedbythe Körperkoor-dinationstestf¨urKinder.Apartialcorrelationbetweenanthropometricmeasurements,z-score ofmaturationandthemotorcoordinationtestswereperformed,controllingforchronological age.Finally,causalmediationanalysiswasperformed.
Results: Height,bodymass,waistcircumference andfatmassshowedaslighttomoderate inversecorrelationwithmotorcoordination.Biologicalmaturationwassignificantlyassociated withthebalancetestwithbackwardwalking(r=−0.34).Totalmediationofthewaist circum-ferencewasidentifiedintheassociationbetweenbiologicalmaturationandbalancetestwith backwardwalking(77%).
∗Correspondingauthor.
E-mail:mjcesilva@hotmail.com(M.Coelho-e-Silva). http://dx.doi.org/10.1016/j.rppede.2016.02.004
Conclusions: We identifiedan associationbetween biological maturation andKTK test per-formanceinmalechildren andalsoverifiedthatthereismediationofwaistcircumference. It is recommended that studies be carried out with female individuals and at other age ranges.
©2016SociedadedePediatriadeS˜aoPaulo.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).
PALAVRAS-CHAVE
Maturac¸ãobiológica; Aptidãofísica; Antropometria; Crianc¸as
Perímetrodecinturacomomediadordainfluênciadamaturac¸ãobiológica nodesempenhodecoordenac¸ãomotoraemcrianc¸as
Resumo
Objetivo: Opresenteestudotevecomoobjetivos:1)analisaraassociac¸ãodoestado matura-cionalcomodesempenhonasprovasdecoordenac¸ãomotoraemcrianc¸ase2)examinarsea relac¸ãoentreoestadomaturacionaleodesempenhonoKTKémediadaporalgumamedida antropométrica.
Métodos: Aamostradeconveniênciafoicompostapor73crianc¸as dosexo masculinocom8 anos.Aantropometriaconsiderouaestatura,massacorporal,alturasentado,operímetrode cintura,índicedemassacorporal,asestimativasdemassagordaemassalivredegordura.A maturac¸ãobiológicafoiavaliadapelopercentualdaestaturamaturapredita.Acoordenac¸ão motorafoitestadapelabateriaKörperkoordinationstestf¨urKinder.Foifeitaacorrelac¸ão par-cial entreas medidasantropométricas, z-escoredamaturac¸ãoe asprovas decoordenac¸ão motora, comcontrolepara idadecronológica. Porúltimo, aanálisedemediac¸ãocausal foi feita.
Resultados: Estatura, massa corporal, perímetro de cintura e massa gorda apresentaram correlac¸ãoinversademagnitudepequenaamoderadacomasprovasdecoordenac¸ãomotora. Amaturac¸ãobiológicaassociou-sesignificativamenteàprovadeequilíbrioemmarchaà reta-guarda(r=−0,34).Foiidentificadamediac¸ãototaldoperímetrodecinturanarelac¸ãodoestado maturacionalcomoequilíbrioemmarchaàretaguarda(77%).
Conclusões: Foipossívelidentificaraassociac¸ãoentreoestadofísicomaturacionaleo desem-penhoemumaprovadabateriadecoordenac¸ãomotoraemcrianc¸asdosexomasculinoe,ainda, afirmarquehámediac¸ãodoperímetrodecintura.Recomenda-sequeestudossejamfeitoscom indivíduosdeoutrasidadesedosexofeminino.
©2016SociedadedePediatriadeS˜aoPaulo. PublicadoporElsevier EditoraLtda.Este ´eum artigoOpenAccesssobumalicenc¸aCCBY(http://creativecommons.org/licenses/by/4.0/).
Introduction
The motor coordination of children seems to be associ-atedwithhealth-relatedphysicalfitness,1physicalactivity,2
bodycomposition,3sociodemographiccharacteristics,4and
consequently the overall health of this population. How-ever, motor development in prepubertal ages appears to influencedecisively themotivation5andeventhe
involve-mentinmotorpracticesinadolescence,suchasgamesand sports.6
The Körperkoordinationstest für Kinder (KTK) test has been usedtoevaluatemotor coordinationinchildren and adolescents.7,8However,thereisalackofstudiesinthe
lit-eraturedescribingthemultiplefactorsthatmayberelated to motor development of children, including the biologi-cal maturation.The studies performed with the KTK test battery aimed primarily at the association of the anthro-pometric characteristics of children andyouth, especially bodymassindex(BMI),withtestperformance.7,8However,
in arecent systematic review withmeta-analysisof stud-iesonthesubject,noselectedstudytookintoaccountthe
relationshipbetweenmaturationalstatusandBMIvaluesof individuals,aswell asperformanceonmotorcoordination tests.7
The maturational status has been related to physical activity9andphysicalfitnessofyoungsubjects.10 However,
themostpopularmeasuresofbiological maturationresult fromsexualmaturationstagesthatareuniquetothe puber-talyearsanddonotcorrespondtoacontinuousscale,likely tobeusedinacorrelational design.11 Katzmarzyketal.10
usedtheskeletalmaturationmethodandtheresultsshowed thecomplexityoftheinterrelationsbetweenbodysize, sex-ualmaturation,andphysicalfitness.Still,theauthorsstated that the effects of biological maturation in children are mainlyexpressedthroughbodysizeandthatmaturational statuswasthe strongestinfluence onthe physical perfor-manceofchildren.
Method
Thisisadescriptivestudyinwhichdatawerecollectedata singletimepointandrepresentacross-sectionofthe char-acteristicsof individuals in the study.The fourschools in ArapiracaandAlagoas, Brazil,wereselectedthrough non-probability sampling accessibility. The selection criterion wasonly theschools’ stratification according toitspublic (n=2)andprivate(n=2)nature.Informedconsentwasgiven toallmalechildrenintheagegroupofinterestforthestudy, aswell astotheir guardians.The sample consisted of 73 malestudents,agedbetween8and8.99years, represent-ing90%oftheeligiblechildrennumber.Notgivinginformed consent,absenceonthedayofdatacollection,orphysical disabilitytoperformthetestbatterywereexclusion crite-ria.The studywasdesigned andconductedin compliance withinternational standardsof experimentation involving humansubjects(HelsinkiDeclarationof1975)andwasduly approvedbytheInstitutionalReview Boardof theFederal University of Alagoas, registered under the Opinion CAAE 09200413.5.0000.5013.
The anthropometric measurements were: height,body mass(BM), sittingheight (SH),waistcircumference (WC), andskinfolds,allmeasuredatschoolinthesameperiodof theday.Height(0.1cm)andSH(0.1cm)weremeasuredwith aportablestadiometer(SannyCaprice,SãoPaulo,Brazil). BM(0.1kg) wasmeasured onadigital scale(Techline, São Paulo, Brazil). The students wore only light clothing and were barefoot, remained with the arms relaxed at their sides.WC(0.1cm)wasmeasuredat midpointbetweenthe last rib and iliac crest, at the time of minimum breath-ing, withan anthropometric steel measuring tape (Sanny MedicalStarrett,SãoPaulo,Brazil).Subscapularis,triceps, and leg skinfolds(1mm) were measured with Lange skin-foldcaliper(BetaTechnology,SantaCruz,California,USA), fromanaverage ofthreemeasurementscollectedateach presetanatomicalpoint,inarotationalorder,ontheright side of the subjects. The procedures used were based on the instructions described by Lohman et al.12 Body
massindex(BMI)andfatpercentage13werecalculatedand
used for BM fragmentation in fat mass (FM) and fat-free mass (FFM). Technical error of measurement and reliabil-itycoefficient of anthropometricvariables were obtained by test---retest, with one week interval in a group of 19 children.Therespectivevalueswere:height(0.6cm;0.98) bodymass(0.6kg,0.99),waistcircumference(1.6cm;0.93), sitting height (0.5cm; 0.96), and skinfolds (1.0---1.4mm; 0.94---0.98).
Biological maturation evaluation was performed using thepercentageofmatureheightachievedatagiventime. The percentage of the predicted mature height (%PMH) obtained at a certain age with the Khamis and Roche method14 is considered as anoninvasive method and
pro-vides data in a continuous format. The measurement, as acontinuousvariable,ismoderatelyassociatedwithbone age,considered a benchmark of biologicalmaturation.9,15
To assess the biological maturation, %PMH wasexpressed as Z-score on the mean and standard deviation for age and sex for the sample of the Berkeley Guidance Study, University of California.16 Maturation Z-scores are often
usedtoassessbiologicalmaturation:average-maturing(z
-scorebetween−1.0and1.0);late-maturing(Z-score<−1.0); early-maturing(Z-score>1.0.17,18).Inthepresentstudy,the
parents’heightswereself-reportedandmaturationz-score wasthevariableusedtorepresentthebiologicalmaturation ofindividuals.
Motorcoordination wasevaluatedwith the body coor-dination test for children (Körperkoordinationstest für Kinder---KTK).19Thechoicewasbasedonthepositiveaspects
highlighted by Cools et al.20 Psychometric characteristics
of KTK19 indicate a test---retest reliability coefficient for
each test separately, ranging between 0.80 and 0.96. Its application requires aspace withan areaof 4×5 meters. KTKhasinitsfinalformfourtests:balanceinwalking back-ward(WB),lateraljumps(LJ),lateraltransposition(LT)and monopedaljumps(MJ).Thesubjectswerenotfamiliarwith the tests prior to testing. In the present study, we con-sidered the isolatedperformance in each KTK test. Thus, thevaluesstandardizedbytheoriginalauthors19 werenot
used nor the motor ratio was calculated, as the original study wasintended toobtain a categorical assessment of children and young people withmotor deficits. The same procedurewasadoptedinanotherstudy.21Thisdecisionwas
basedon:1)lackofstudyshowingthecross-cultural valid-ity of the score suggested by the original authors of the resultsofeachtestinBrazilianchildren;2)absenceofsolid informationonthevalidityofmotorratiocutoffvaluesin Brazilian children; 3) having noknowledge of theclinical andpedagogicalsignificanceoftheproposedclassification bythe Germanauthors;4)thefact thatourstudysample comprised onlyindividuals of the samesex andsame age group;and5)thefactthatthemainobjectiveofthestudy is to examine the association of anthropometricand bio-logical maturationvariableswiththeperformance onKTK tests.
The evaluations were conducted at the premises of schools. Evaluations in each school lasted four weeks. Each week, an average quantity of 10 individuals was evaluated. Regarding evaluationtimes, first anthropomet-ric measurementswere taken, andin another week, KTK wasappliedindividually withchildren wearingshoes.The sequence of KTK’s evidence was uniformly applied to subjects in the following order: balance in walking back-ward,lateraljumps, lateraltransposition,and monopedal jumps.
Descriptivestatisticsofcentraltendencyanddispersion weredeterminedandthenormalityofthedistributionwas furthertestedwiththeKolmogorov---Smirnovtest.Variables that did notmeet the assumptions of normal distribution weresubjectedtologarithmictransformationforthe infer-entialanalysis.However,we chosetopresentthe original values in the tables of results. Subsequently, the partial correlation test was performed, controlled by chronolog-icalage, between anthropometric variables(height, body mass, BMI, sitting height, waist circumference, fat mass, andfat-freemass),maturationZscore,andresultsforeach KTKtest.Correlationcoefficientswereinterpreted accord-ingtoHopkinsetal.22Aftercorrelations,inordertoexamine
howmuchoftheassociationbetweenbiologicalmaturation and performance in KTK was mediated by anthropomet-riccharacteristics,linearregressionmodelswereadjusted based in the procedures described by Baron andKenny.23
the independentvariable (biological maturation Z score). The second equation uses the dependent variable (KTK score) and the independent variable (biological matura-tionZ score). The third equation assessedthe dependent variable(KTKscore)withtheindependentvariable (biolog-icalmaturationZscore)andthemediator(anthropometry). The following criteria were used to establish a media-tion: 1) the independent variable should be significantly relatedtothemediator;2)theindependentvariableshould besignificantly related tothe dependent variable;3) the mediatorshouldbesignificantly relatedtothedependent variable; and 4) the association between the indepen-dentvariableanddependentvariableshouldbeattenuated when the mediator is included in the regression model. Finally, mediation is tested with the steps described by Sobel24:first, an estimated attenuation or indirect effect
(i.e., the effect of independent variables on the media-tor,equation 1, multipliedby the mediatoreffecton the dependent variable, equation 3); and, second, the indi-recteffectis dividedbythe effectcalculatedin equation 2. A significance of p<0.05 was considered in the analy-sis. The SPSS 22.0 software (SPSS, Inc., Chicago, IL) was used.
Results
DescriptiveresultsareshowninTable1.Regardingbiological maturation,thesubjectsareintheaveragepercentageof thepredictedmatureheightof74.7%,withasmallstandard deviationmagnitude(±1.6).ThesamewasnottrueinKTK tests.Thelateraltranspositiontestistheonewithless vari-ationinthestandarddeviationvalues.
Table 2 shows the partial correlation coefficients
between anthropometric variables, biological maturation (maturation Z score), and performance in each KTK test, controlled for the spurious effect of chronological age. Biological maturation did not correlate significantly with mostKTKtests,notablylateraljumps,lateraltransposition,
andmonopedal jumps.Incontrast,therewasasignificant inversecorrelationofmoderatemagnitudewiththebalance in walking backward (r=−0.34). Height, body mass, BMI, waistcircumference,andfat masswereinverselyand sig-nificantlyassociatedwithmaturation Z scoreandbalance inwalkingbackwardKTK test, rangingbetween weakand moderatemagnitudes.
Ofallanthropometricvariablesshowingsignificant asso-ciation with the balance in walking backward KTK test, waistcircumferencewasthe onlyonetopresent itself as amediatoroftherelationshipbetweenthebiological mat-urationandtestperformance(Fig.1).Theresultsshowthat theeffectofbiologicalmaturation onperformance inthe balanceinwalkingbackwardKTKtestactedasfullmediator ofwaistcircumference(77%;Z=−2.523,p<0.05).
Discussion
Thepresentstudyfoundaninverseassociationbetween bio-logical maturation and balance in walking backward KTK test,whosecorrelationcoefficient showedmoderate mag-nitude.Waist circumference wasthe onlyanthropometric variableactingasmediatorintherelationshipbetween bio-logicalmaturationandKTKtestperformance,notablyinthe balanceinwalkingbackwardtest.
Biological maturation has been taken into account in studies involving the pediatric population. Currently, the relationship between biological maturation and level of physical activity9 and motor performance10 are issues
reportedintheliterature.However,itisnoteworthythat, normally,thestudiesconsider‘‘motorperformance’’as per-formance in physical fitness tests related to health, and not necessarily in motor coordination tests. Few studies withchildren have considered both biological maturation andperformanceontests ofmotor coordinationor motor skills.25,26 Recently, Freitas et al.25 assessed the
contribu-tionofskeletalmaturationintheperformanceofKTKtests inchildrenaged7---10years.Theauthorsstatedthat,inmost
Table1 Generalcharacteristicsoftotalsample(n=73).
Variables Range Mean Standarddeviation
Minimum Maximum Value (95%CI)
Chronologicalage(years) 8.00 8.99 8.52 (8.45---8.59) 0.30
Predictmatureheight(cm) 161.6 188.7 175.4 (173.9---176.9) 6.4
Predictmatureheight(%) 72.2 78.6 74.7 (74.4---75.1) 1.6
Height(cm) 119.2 146.2 131.1 (129.8---32.5) 5.8
Bodymass(kg) 18.1 61.7 31.4 (29.6---33.3) 7.9
Bodymassindex(kg·m−2) 12.0 30.8 18.1 (17.3---18.9) 3.4
Sittingheight(cm) 41.8 79.0 68.3 (67.3---69.4) 4.5
Waistcircumference(cm) 48.0 92.8 61.6 (59.7---63.4) 7.9
Fatmass(kg) 1.5 40.1 8.4 (7.0---9.9) 6.2
Fat-freemass(kg) 16.6 30.3 23.0 (22.3---23.6) 2.9
Backwardbalancea 3 68 37.8 (34.4---41.2) 14.4
Lateraljumpsa 11 57 33.2 (31.0---35.5) 9.7
Lateraltranspositiona 18 60 32.4 (30.8---34.0) 6.8
Monopedaljumpsa 9 65 36.6 (33.8---39.4) 12.1
Table2 Partialcorrelationcoefficientsbetweenanthropometricvariablesandperformanceonmotorcoordinationtests(KTK), controlledbychronologicalage.
Anthropometric variables
MaturationZscore KTK
Backwardbalance Lateraljumps Lateraltransposition Monopedaljumps
Height 0.52a −0.25a −0.42a −0.26a −0.24a
Bodymass 0.68a −0.36a −0.41a −0.27a −0.30a
Bodymassindex 0.60a −0.35a −0.30a −0.22 −0.29a
Sittingheight 0.42a
−0.16 −0.18 −0.24a
−0.23
Waistcircumference 0.67a −0.44a −0.43a −0.27a −0.36a
Fatmass 0.68a
−0.37a
−0.37a
−0.27a
−0.33a
Fat-freemass 0.40a −0.13 −0.34a −0.27a −0.14
MaturationZscore --- −0.34a −0.17 −0.10 −0.15
ap<0.05.
Maturation Z score Backward balance
Waist circumference
Maturation Z score Backward balance
Equation 2
β= –0.384∗
Equation 1
β=0.780∗
Equation 3
β= –0.383∗
Sobel test: –2.523∗ Equation 3
β= –0.085∗
Figure1 Measurementmodelofwaistcircumferenceonthe relationshipbetweenbiologicalmaturationandperformanceon backwardbalanceofmotorcoordinationbattery,controlledby chronologicalage(*p<0.05).
cases,thecorrelationcoefficientsarenegative,suggesting thatalaterbiologicalmaturationisassociatedwithbetter results in test trials. Also,they concludedthat biological maturation alone, or combinedwith body size, has little influenceonKTKresults.
In alongitudinal study,Deus etal.27 followed the
per-formanceofchildrenaged6---10yearsinKTKtestsandthe results showed that the coordinative competency of KTK testsshoweddistinct trajectories.The balancein walking backwardtestwastheonlyonethatshowedalinear trajec-tory,whichdidnotoccurinothertests,anddemonstrated initsresultsthat thehigherthestarting value,thelower theannualgains (r=−0.55).Moreover,thefindingsofDeus etal.27 alsoshowedthatBMIisanessentialfactor forthe
goodperformanceofthistest.Infact,thistestrequiresthe displacementofthecenterofgravityinabalancedmanner, whichmaypenalize childrenwithhigherbody fat,mainly located in the trunk area. D’Hondt et al.28 also reported
thatthereisaninverserelationshipbetweenbodyfatand performanceonKTKtests,which seemsmore pronounced inthosewithmoreadvancedage.Apossibleexplanationfor thesefindingsintheliteraturemaybethatmotor develop-mentof children increasesasthey becomemore mature. However,themoreadvanced thebiological maturationof an individual tends to be, this advancement tends tobe slowerandstabilize.11Ontheotherhand,weightgainthat
isalsorelatedtobiologicalmaturation,tendstoincrease, which would contribute toa greater chance of havingan inverselyproportionalassociation betweenbodymass and performance on KTK in children with advanced biological maturation.
Inrecentstudywithchildrenofbothsexes,Lopesetal.8
reported that, in addition to BMI, waist circumference, height-waistratio,andbodyfatpercentagealsowere asso-ciatedwithperformanceonKTK.However,fatpercentage (ˇ=2.395,95%CI1.234---4.646;p=0.010)showedhigher sen-sitivity to predict low motor coordination in girls. For males, increased value of waist circumference (ˇ=3.296, 95%CI 1.784---6.090; p<0.001) was more prevalent in the association with low performance on KTK. Such findings are in line withthe results of ourstudy, as it wasfound inverserelationshipbetweenbiologicalmaturationand per-formanceonthebalanceinwalkingbackwardtestmediated by central fat, characterized by the waist circumference values.
Giventheabove,ourfindingsshowevidencethat biolog-icalmaturation,althoughinsmallproportion,iscorrelated withtheperformanceonKTKinprepubertalmalechildren, especiallybytheinversecorrelationofmoderatemagnitude obtainedonthebalanceinwalkingbackwardtest.However, onecannot concludethe samefor other KTKtests. These findingssupportthoseintheliteratureandraiseevidence that thedevelopmentof childrencoordination isnot only relatedtotheinfluenceof biologicalmaturation,butalso to the behavioral and environmental influences and their interactions.25,29,30
factthat parentalheights werenotdirectly measured for %PMH calculation. However, the results contribute to the knowledge of the coordination performance of children. Furthermore, it denotes the possibilityof interference of biological maturationin the relationship of bodysize and the results of motor coordination,especially on KTK test battery.
In conclusion,taking intoconsideration thatthemotor coordination development is of paramount importance in childhood,foritscharacteristicofpredictingphysical activ-ityinsubsequentstagesoflife,6itisevidentthattheresults
reinforce not only the need for attention to the knowl-edge of biological maturation of individuals, but mainly highlightstheconceptthatgrowth,maturation,andmotor developmentare biocultural phenomena.11 Futurestudies
with individuals of other age groups are recommended, withlargersampleand assessingtheeffectof maturation onperformancewithothermethodsofmotorcoordination assessmentinthepediatricpopulation.
Funding
ThefirstauthorisaPhDstudentattheFaculdadede Ciên-cias do Desporto e Educac¸ão Física da Universidade de Coimbra (registration uid/dtp/04213/2013), Portugal and is fundedby full PhD scholarshipabroad, Coordenac¸ão de Aperfeic¸oamentodePessoaldeNívelSuperior(Capes), Pro-cessNo.BEX1617/13-3.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
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