www.bjorl.org
Brazilian
Journal
of
OTORHINOLARYNGOLOGY
ORIGINAL
ARTICLE
Effects
of
distractors
on
upright
balance
performance
in
school-aged
children
with
attention
deficit
hyperactivity
disorder,
preliminary
study
夽,夽夽
Fatma
Esen
Aydinli
a,∗,
Tuna
C
¸ak
b,
Meltem
C
¸i˘
gdem
Kirazli
a,
Betül
C
¸ic
¸ek
C
¸inar
c,
Alev
Pektas
¸
d,
Ebru
Kültür
C
¸engel
b,
Songül
Aksoy
aaHacettepeUniversity,FacultyofHealthSciences,SpeechandLanguageDepartment,Ankara,Turkey bHacettepeUniversity,FacultyofMedicine,ChildandAdolescentMentalHealthDepartment,Ankara,Turkey cHacettepeUniversity,FacultyofHealthSciences,AudiologyDepartment,Ankara,Turkey
dHacettepeUniversityHospital,EarNoseandThroatDepartment,AudiologyandSpeechPathologyUnit,Ankara,Turkey
Received24May2016;accepted21October2016 Availableonline17November2016
KEYWORDS Attentiondeficit hyperactivity disorder; Balance; Distractor; Sensoryorganization test Abstract
Introduction:Attentiondeficithyperactivitydisorderisacommonimpairingneuropsychiatric disorderwithonsetinearlychildhood.Almosthalfofthechildrenwithattentiondeficit hyper-activitydisorderalsoexperienceavarietyofmotor-relateddysfunctionsrangingfromfine/gross motorcontrolproblemstodifficultiesinmaintainingbalance.
Objectives:The mainpurposeofthisstudywastoinvestigatetheeffectsofdistractorstwo differentauditorydistractorsnamely,relaxingmusicandwhitenoiseonuprightbalance per-formanceinchildrenwithattentiondeficithyperactivitydisorder.
Methods:Wecompareduprightbalanceperformanceandtheinvolvementofdifferentsensory systems inthe presence of auditory distractors between school-aged children with atten-tiondeficithyperactivitydisorder(n=26)andtypicallydevelopingcontrols(n=20).Neurocom SMARTBalance MasterDynamicPosturography devicewas usedfor thesensory organization test.Sensoryorganizationtestwasrepeatedthreetimesforeachparticipantinthreedifferent testenvironments.
夽 Pleasecitethisarticleas:AydinliFE,C¸akT,KirazliMC¸,¸inarC BC¸,Pektas¸A,C¸engelEK,etal.Effectsofdistractorsonuprightbalance performanceinschool-agedchildrenwithattentiondeficithyperactivitydisorder,preliminarystudy.BrazJOtorhinolaryngol.2018;84:280---9.
夽夽Preliminaryresultsofthisstudywerepresentedorallyin11thEFAScongressheldontheJune19---22nd2013,inBudapest,Hungary. ∗Correspondingauthor.
E-mails:fesen04@gmail.com,fesen04@hacettepe.edu.tr(F.E.Aydinli).
PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial. https://doi.org/10.1016/j.bjorl.2016.10.007
1808-8694/©2016Associac¸˜aoBrasileiradeOtorrinolaringologiaeCirurgiaC´ervico-Facial.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).
Results:The balance scores inthesilenceenvironment were lowerinthe attentiondeficit hyperactivitydisordergroupbutthedifferenceswerenotstatisticallysignificant.Inaddition tolowerbalancescoresthevisualandvestibularratioswerealsolower.Auditorydistractors affected thegeneralbalance performancepositively forbothgroups.Morechallenging con-ditions,usinganunstableplatformwithdistortedsomatosensorysignalsweremoreaffected. Relaxingmusicwasmoreeffectiveinthecontrolgroup,andwhitenoisewasmoreeffective intheattention deficithyperactivity disordergroup andthepositive effectsofwhitenoise becamemoreapparentinchallengingconditions.
Conclusion: Tothebest ofourknowledge,this isthefirst study evaluating balance perfor-mance inchildrenwithattentiondeficithyperactivitydisorderundertheeffectsofauditory distractors. Althoughmorestudiesareneeded,ourresultsindicatethatauditory distractors mayhaveenhancingeffectsonuprightbalanceperformanceinchildrenwithattentiondeficit hyperactivitydisorder.
© 2016 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Published by Elsevier Editora Ltda. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/4.0/). PALAVRAS-CHAVE Transtornodedéficit deatenc¸ãoe hiperatividade; Equilíbrio; Distrac¸ão;
Testedeorganizac¸ão sensorial
Efeitosdedistrac¸õessobreodesempenhodoequilíbrioverticalemcrianc¸asemidade escolarcomtranstornodedéficitdeatenc¸ãoehiperatividade-estudopreliminar Resumo
Introduc¸ão: O transtorno do déficit de atenc¸ão e hiperatividade é um distúrbio neurop-siquiátrico comum que causa comprometimentos, com início na primeira infância. Quase metade dascrianc¸ascomtranstornododéficitdeatenc¸ãoehiperatividadetambém experi-mentamumavariedadededistúrbiosrelacionadosàshabilidadesmotoras,desdeproblemasde controledehabilidadesmotorasfinas/grossasatédificuldadesnamanutenc¸ãodoequilíbrio.
Objetivos: Oprincipalobjetivo deste estudofoi investigaros efeitosde distrac¸ões, especi-ficamente duas distrac¸ões auditivas diferentes, música relaxante e ruído branco, sobre o desempenhodoequilíbrioverticalemcrianc¸ascomtranstornodedéficitdeatenc¸ãoe hipera-tividade.
Método: Comparamos o desempenho do equilíbrio vertical e oenvolvimento de diferentes sistemas sensoriais napresenc¸a dedistrac¸ãoauditiva entrecrianc¸as em idade escolarcom transtorno dodéficit de atenc¸ão ehiperatividade (n=26) econtrolescomdesenvolvimento típico(n=20).OdispositivoNeurocomSMARTBalanceMasterDynamicPosturographyfoi uti-lizadoparaotestedeorganizac¸ãosensorial.Otestedeorganizac¸ãosensorialfoirepetidotrês vezesparacadaparticipanteemtrêsambientesdetestediferentes.
Resultados: Osescoresdeequilíbrio noambienteem silêncioforammenoresnogrupo com transtorno dodéficit deatenc¸ão ehiperatividade,mas asdiferenc¸as não foram estatistica-mentesignificativas.Alémdosescoresdeequilíbriomaisbaixos,asrazõesvestibularesevisuais tambémforammenores.Asdistrac¸õesauditivasafetarampositivamenteodesempenhodo equi-líbriogeralparaambososgrupos.Condic¸õesmaisdesafiadoras,usandoumaplataformainstável comsinaissomatossensoriaisdistorcidosforammaisafetados.Músicarelaxantefoimaiseficaz nogrupodecontrole,eruídobrancofoimaiseficaznogrupodehiperatividadecomdéficit deatenc¸ãoeosefeitospositivosdoruído brancose tornarammaisevidentesemcondic¸ões desafiadoras.
Conclusão:Quesejadenossoconhecimento,esseéoprimeiroestudoqueavaliaodesempenho doequilíbrioemcrianc¸ascomtranstornododéficitdeatenc¸ãoehiperatividadesobosefeitos dedistrac¸õesauditivas.Emboramaisestudossejamnecessários,osnossosresultadosindicam queasdistrac¸õesauditivaspodemterefeitosdeaumentonodesempenhodoequilíbriovertical emcrianc¸ascomtranstornodedéficitdeatenc¸ãoehiperatividade.
© 2016 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Publicado por Elsevier Editora Ltda. Este ´e um artigo Open Access sob uma licenc¸a CC BY (http:// creativecommons.org/licenses/by/4.0/).
Introduction
Attention deficit hyperactivity disorder (ADHD) is a
com-monimpairingneuropsychiatricdisorderwithonsetinearly
childhood.ChildrenwithADHDshowdevelopmentally
inap-propriatelevelsofinattentiveand/orhyperactiveimpulsive
behaviorsinmultiplesettings.1Epidemiologicstudies
indi-catethat ADHDis prevalentthroughout theworld,witha
generalconsensusthat7---9%ofyouthshavethedisorder.2
Almost half of the children with ADHD also
expe-rience a variety of motor-related dysfunctions ranging
from fine/gross motor control problems to difficulties
in maintaining balance.3---10 Studies examining underlying
processesshow thatmotorimpairmentinADHD is
charac-terized by timing, coordination, and force deficits, all of
which areassociated withcerebellar dysfunction.11 ADHD
symptomatology is suggested to be related with
fronto-striato---cerebellarcircuitdysfunctionsandconvergingdata
has revealed volume reduction of the cerebellar vermis
in children with ADHD.12---15 Balance control requires the
integrationofsomatosensory,vestibular,andvisualsensory
informationandcerebellar integrityis believed tobethe
key process.16 What’s more balance control also requires
attention and central information processing and
there-foreisstronglyrelatedtothecognitiveprocess17---25 rather
than being a subcortical, pure reflex mechanism.17,18,21,22
Studies in ADHD populations may provide valuable
infor-mation regarding balance because of the accompanying
attention,inhibitionandexecutivefunctiondeficits.Afew
studiesexaminedbalanceinchildrenwithADHDandmostly
concluded disturbed balance performance.18,23,26---30 Most
studiesfocused onupright balanceperformance26,28,29and
a couple investigated the effects of different cognitive
tasksonbalance performance.18,23 In a study,researchers
found greater postural sway while participants were
per-formingauditory---memory-demandingcognitivetasks.23Ina
study,researchersexaminedtheeffectofmethylphenidate
on standing balance performance under three different
test conditions: standing upright; performing a memory
attention-demandingtask;andlisteningtorelaxingmusic.18
The results revealed that methylphenidate significantly
improved postural stability while performing a dual task
andlisteningtorelaxingmusic.However,thestudydidnot
includehealthycontrolsordifferentdistractors.
Therearetwomainwaystodetectbalanceperformance:
centerofpressuredisplacementmeasurementsandthe
Sen-soryOrganization Test (SOT).The SOT isusedtoevaluate
thecontributionsof differentsensorysystems tostanding
balancecontrol.Thetestisacommonresearchtoolinthe
evaluationof sensory organizationof balance controland
hasbeen previouslyusedby other researchersinstudying
balanceperformanceinchildren.28
In summary, motor and balance impairments can be
observedin children withADHDsharing a common
neuro-biologicalbasiswithcoreADHDsymptoms.Balancecontrol
requiresattention,anddistractorsthataffectattentionmay
alsoaffectbalanceperformance.Somestudieshaveshown
theeffectsofdistractorsoncognitiveskillsinchildrenwith
ADHD31,32;however, no study has investigatedthe effects
ofdistractors onbalanceperformance.To thebestofour
knowledge,nostudyhasevaluatedbalanceperformancein
children withADHD using distractors, suchas background
musicandwhitenoise.Theaimofthisstudyis(1)to
com-pare uprightbalance performancein school-aged children
withADHDandtypicallydeveloping controls,(2) to
inves-tigate the effects of relaxing music and white noise as
distractors and (3) evaluate the involvement of different
sensorysystemsduringperformanceinthepresenceof
dis-tractors.
Methods
Participants
IntheADHDgroup,children whohadundergonefirst-time
psychiatricadmissionandassessmentwererecruitedfrom
theChildandAdolescentPsychiatryOutpatientClinic.The
inclusioncriteriawereasfollows:(1)aformaldiagnosisof
ADHDconfirmedbytwodifferentchildandadolescent
psy-chiatristswithat leasttenyearsofexperiencewithADHD
accordingtotheDiagnosticandStatisticalManualof
Men-tal Disorders (DSM-IV-TR) and confirmed by the Schedule
for Affective Disorders and Schizophrenia for School-Age
Children-PresentandLifetimeVersion(K-SADS-PL),(2)age
between 7 and 12 years, (3) normal vision with or
with-out glasses, and(4) normal hearingstatus. Childrenwere
excluded fromthestudyiftheyhad anyofthe following:
(1) history of a chronic neurological condition or
move-mentdisorders,(2)totalIQscorebelow80ontheWechsler
IntelligenceScaleforChildren-Revised(WISC-R),(3)
signif-icant musculoskeletal or cardiopulmonary conditions that
mayinfluencebalanceperformance,(4)anykindofcurrent
psychotropic medication, and(5) diagnosis of a psychotic
disorder,autismspectrumdisorder,ordevelopmental
coor-dinationdisorder(DCD)accordingtotheDSM-IV-TRcriteria.
To warrant a diagnosis of DCD, the child had to
demon-stratemotorcoordinationsubstantiallybelowtheexpected
ofthechild’sage,whichinterferedwithactivitiesofdaily
livingandacademicperformance.Thechildreninthe
con-trolgroupwerematchedbyageandsexandwererecruited
fromthecommunity;theyhadtofulfillthesameinclusion
andexclusioncriteriasetabove,exceptthatthefirst
inclu-sioncriteriawassetasfollows:(1)noformaldiagnosisofany
psychiatricdisordermadeconfirmedbytwoexperienceda
childandadolescentpsychiatristsaccordingtothe
DSM-IV-TRcriteriaandconfirmedbytheK-SADS-PL.
Measures
Schedule for Affective Disorders and Schizophrenia for
School-AgeChildren-PresentandLifetimeVersion
(K-SADS-PL) is a semi-structured diagnostic interview designed to
assesscurrentandpastepisodesofpsychopathologyin
chil-drenandadolescentsaccordingtotheDSM-III-RandDSM-IV
criteria.33 K-SADS-PL is administered by interviewing the
parent(s) andthechild, afterwhich,summary ratingsare
providedthatalsoincludeallsourcesofinformation.
Gök-leretal.showedthevalidityandreliabilityofK-SADS-PLfor
Turkishchildrenandadolescents,andthekappavaluesfor
variousdisordersrangingbetween0.458and0.875.34
WechslerIntelligenceScale forChildren-Revised
(WISC-R), is an individually administered intelligence test that
Arithmetic, Judgment, Vocabulary, and Digit Span) and
six performance (Picture Completion, Picture
Arrange-ment, Block Design, Object Assembly, Digit Symbol, and
Labyrinths) subscales. Five verbal (General Information,
Similarities,Arithmetic,Judgment,andDigitSpan)andfive
nonverbal(PictureCompletion,PictureArrangement,Block
Design, Object Assembly, and Digit Symbol) subscales of
WISC-R wereusedin this study.Savas¸ırandS¸ahin showed
thevalidityandreliabilityofWISC-RforTurkishchildrenand
adolescents.35
TheConners’ParentRatingScale(CPRS-48)isoneofthe
mostusedbehavioralscalesinclinicalandresearchsettings
for childrensuffering fromneurodevelopmentaldisorders,
particularlyforchildrenwithADHD.CPRS-48consistsof48
itemsonafour-pointlikertscaleindicatingtheseverityofa
particularbehaviorandisusedintheevaluationofproblem
behaviorsrelated to ADHD by obtaining reports from
pri-marycaregivers.36TheCPRS-48Turkishversionisrecognized
asavalidandreliableinstrumentinscreeningADHD
symp-tomsinbothclinicalandcommunitysettingsintheTurkish
population.37
The SensoryOrganization Test(SOT)quantifiesthe
effi-cacies of three sensory systems (visual, vestibular, and
somatosensorial)inobtaininguprightbalancecontrol.SOT
evaluates balance performance under six conditions with
gradually increasing difficulty. Somatosensorial, visual, or
sensoryinformationaredistortedthroughcalibrated‘‘sway
referencing’’ of the support surface and/or visual
sur-round.TheseconditionsareconditionC1:eyesopen,stable
platform; C2:eyesclosed,stableplatform;C3:visual
dis-orientation (swayreferenced vision), stableplatform; C4:
eyes open, unstable platform; C5: eyes closed, unstable
platform;andC6:visualdisorientation,unstableplatform.
‘‘Stableplatform’’referstoconditionsinwhichthedynamic
platformismaintainedinastaticstableposition.‘‘Unstable
platform’’ referstoconditionsin whichtheEquitest
plat-formisreferencedtotheswayofthesubject.Theplatform
respondedtochangesinweighttransfersandshiftsin the
subject’scenterofgravitywhilethesubjectattemptedto
maintainhis/herbalance.38Theequilibriumscorequantifies
the posturalstability of thesix sensoryconditions.
Effec-tiveuseofindividualsensoryinputsisdeterminedfromthe
overallpatternofscoresonthesixconditions.The
compos-iteequilibriumscore,whichistheweightedaverageofthe
scores of all sensoryconditions, characterizesthe overall
levelofperformance.Sensoryanalysisratiosareusedin
con-junctionwiththe individualequilibriumscores toidentify
impairmentsofindividualsensorysystems.The
somatosen-soryratioistheratioofthebalancescoreofC2tothatof
C1.ThevisualratioistheratioofthebalancescoreofC4
tothatofC1.Thevestibularratioistheratioofthebalance
scoreofC5tothatofC1.Thepreferenceratioistheratio
ofthescoreofC3+C6tothatofC2+C5.39
Procedure
InstitutionalreviewandapprovalfromtheEthicsCommittee
wasobtained (Number:B.30.2HAC.0.20.05.04/321).
Chil-drenintheADHDandcontrolgroupswerefirstevaluatedby
twochildandadolescentpsychiatristsbyconductingclinical
interviewsandtheK-SADS-PLseparatelyforthechildrenand
theirparents.Allparentsgaveinformedconsentfor
partic-ipation,whichwasconsistentwiththeCodeofEthicsofthe
WorldMedicalAssociation (Declarationof Helsinki).
WISC-Rwasadministeredindividuallyondifferentdays,toavoid
thepossibility of differentcarryover effects between the
ADHDandthecontrolgroups,byaclinicalpsychologistina
quietroomatthepediatrichospital,andtheparentsfilled
CPRS-48.Childrenfulfillingtheinclusionandexclusion
crite-riaforthestudywerefurtherevaluatedbyperformingthe
experimentalbalancetasksonanotherdayintheVestibular
Laboratoryatthesamehospital.Atotalof55childrenwere
evaluated,but9children wereexcludedfor thefollowing
reasons:hearingloss(n=3),TotalIQscorebelow80(n=1),
learningdisorder(n=1),additionalhandicaps(n=2),
aphysi-ologicpatterninSOT(n=1),andproblemsinadaptingtothe
test(n=1).Finally,26childrenwereincludedintheADHD
groupand20 childrenwereincludedinthecontrolgroup.
These46childrencompletedallmeasurements.
SOTprotocol
Inthis study,a NeurocomSMART Balance MasterDynamic
PosturographydevicewasusedinSOT.Theexaminerswere
three licensed audiologists. The participants stood
bare-footon the platform withtheir feet placed 5.7cm apart
andthemedialmalleolusalignedwiththeaxisofthe
plat-formrotation.Foot position wasmarked on the platform
toensureconsistencybetweenthetrialsandsessions.The
participantsworeaharnessthatwasattachedoverheadand
prevented falls but did not limit sway; they were asked
to stand quietly with their arms across their chest and
their eyes open or closed (depending on the condition).
An examiner remained stationed behind each subject for
safetythroughout the test. Each test condition was
com-pletedthreetimesfor20sinthesameorder.Inadditionto
thestandardSOTprotocolinwhichtherewasno
accompa-nyingdistractor (silenceenvironment), all protocolswere
repeatedwhile the participantswerelistening torelaxing
musicandwhitenoisethroughearphones.TheMP3player
(Philips Model SA3115/02; Headphones: AY3809) was in a
caseandplacedneartheupperchestheldbyappropriate
lengthstrips.Disposableearphonecovers wereused,
but-tonswerelockedduringthetests,andthevolumelevelwas
stabilizedtopreventmanipulations.Theparticipantswere
asked to warnthe audiologist if the sound wasdistorted
or interrupted. Therefore, SOT wasrepeated threetimes
foreach participant inthreedifferent test environments:
(1) silence (no background distractor), (2) accompanying
backgroundmusic,and(3)accompanyingbackgroundnoise.
Musiccomposedof soothing naturesounds,such asforest
andwaterfallsounds, waschosen asthemusic distractor,
and‘‘whitenoise’’waschosenasthenoisedistractor.The
orderoftestenvironmentswasselectedrandomlyforevery
participant,and5minbreaksweregivenbetweenthetests
andchildren wereencouraged to walk aroundduring the
break.
Statisticalanalysis
SPSS18.0wasusedforall statisticalanalyses. Continuous
Table1 MaincharacteristicsoftheADHDandthecontrolgroups. ADHD (n=26) Control (n=20) Statistics p-Value Age(months) 109.50±21.38 116.45±15.02 1.236 0.223 Male/female 20/6 14/6 0.281 0.596 Height(cm) 136.76±10.21 138.90±12.77 0.625 0.535 WISC-RtotalIQ 104.68±12.67 102.75±11.17 −0.535 0.596 WISC-RverbalIQ 99.24±14.11 102.05±11.08 0.728 0.470 WISC-RperformanceIQ 109.44±13.93 103.10±12.68 −1.578 0.122 CPRS-48scores 21.89±10.54 10.82±7.26 −3.624 0.001a
ADHD,attentiondeficithyperactivitydisorder;WISC-R,WechslerIntelligenceScaleforChildren-Revised;CPRS-48,TheConners’Parent RatingScale.
aindicatesp<0.05.
Kolmogorov---SmirnovtestwithLillieforssignificance
correc-tion.Student’st-testandthechi-squaretestwereapplied
todetermine the differences in continuous and
categori-calvariablesbetweenthetwogroups,respectively. Effect
sizevalues,computedusingthedstatistics,werealsoused
toreflectthe differencebetween twomeans.40 Repeated
measuresanalysisofvariancewasappliedwithBonferroni
adjustment in pairwise comparisons to compare balance
performances in three different test environments in the
groups. For sensoryanalysis ratios, the Mann---Whitney
U-testwasusedtocomparebalanceperformancebetweenthe
groups,andFriedman’stwo-waytestwasusedtoreveal
dif-ferencesbetweenthegroups.Significantlevelwasaccepted
as0.05.
Results
Bydesigngenderandagewerenotsignificantlydifferentin
theADHD and thecontrol groups. In addition,heightand
totalIQscoreswerenotdifferentbetweenthetwogroups.
Children in the ADHD group had lowerscores onGeneral
Information,Similarities,Arithmetic,Judgment,DigitSpan
andDigitSymbolsubscalesoftheWISC---Rbutthedifferences
couldnotreachstatisticalsignificance(p=0.124,p=0.362,
p=0.216,p=0.193,p=0.095,p=0.144).Asexpected
chil-dren in theADHD grouphad significantlyhigherscores on
theCPRS-48(Table1).
Mean Equilibrium Scores (MES) of the control and the
ADHDgroupsinthethreetestenvironments,namelysilence,
relaxingmusicandwhitenoiseareshowninFig.1.Auditory
distractors affected the Composite Scores (CS) positively
for both groups. C4,C5 andC6 werethe conditionsmore
affected in both of the groups. When the changes are
tested for statisticalsignificance, MESdid notchange
sig-nificantly for C1, C2, C3, C4 and C5 in the three test
environmentsintheADHDgroup.However,childreninthe
ADHDgroupshowedsignificantlydifferentbalance
perform-ances for C6 and the CS in the three test environments
0.00
C1 C2 C3 C4 C5 C6 CS C1 C2 C3 C4
ADHD Test environment
Silence Music Noise
Control C5 C6 CS 20.00 40.00 60.00 80.00 100.00 MES
Figure1 MeanequilibriumscoresofthecontrolandtheADHDgroupsinthethreetestenvironments.MES,meanequilibrium scores;ADHD,AttentionDeficitHyperactivityDisorder;C1,eyesopen,stableplatform;C2,eyesclosed,stableplatform;C3,visual disorientation(swayreferencedvision),stableplatform;C4,eyesopen,unstableplatform;C5,eyesclosed,unstableplatform;and C6,visualdisorientation,unstableplatform;CS,compositescore.
Table2 MeanequilibriumscoresintheADHDandthecontrolgroupsinthethreetestenvironments.
SOTcondition ADHD(mean±SD) Control(mean±SD) Statistics p-Value d Silence C1 88.96±5.63 90.35±3.29 1.050 0.300 0.008 C2 85.43±6.17 85.79±3.18 0.253 0.802 0.001 C3 82.71±9.81 86.17±3.61 1.653 0.108 0.290 C4 71.53±15.64 75.54±9.84 1.063 0.294 0.004 C5 43.36±17.04 51.47±15.50 1.682 0.100 0.360 C6 38.52±20.46 49.29±21.22 1.732 0.091 0.440 Compositescore 63.30±12.42 69.15±8.54 1.886 0.066 0.042 Music C1 88.75±6.26 90.76±3.40 1.388 0.173 0.041 C2 84.53±9.07 86.72±4.90 1.049 0.300 0.022 C3 83.39±9.92 86.22±4.72 1.277 0.209 0.025 C4 72.88±13.28 82.34±6.67 3.149 0.003a 0.150 C5 50.12±20.17 57.52±16.34 1.373 0.177 0.020 C6 51.84±17.85 57.77±19.92 1.039 0.305 0.019 Compositescore 66.80±10.69 73.55±8.70 2.294 0.027a 0.080 Noise C1 90.54±3.56 90.39±3.23 −0.150 0.881 0.001 C2 85.96±5.38 85.64±3.85 −0.235 0.815 0.001 C3 86.72±4.77 86.87±3.96 0.118 0.907 0.002 C4 75.36±12.88 78.78±9.94 1.015 0.316 0.010 C5 52.56±17.36 58.98±15.60 1.318 0.195 0.022 C6 48.64±21.91 54.83±19.55 1.009 0.319 0.009 Compositescore 69.69±10.54 72.60±9.08 1.003 0.322 0.009
SOT,SensoryOrganizationTest;ADHD,attentiondeficithyperactivitydisorder;Effect sized,mean ofADHDgroup-meanofcontrol group/pooledstandarddeviationoftwogroups.
a indicatesp<0.05.
(p=0.015, p=0.009). For C6 children in the ADHD group
showedbetterbalanceperformanceinthelisteningtomusic
andthewhitenoiseenvironmentthaninthesilence
environ-ment(p=0.042,p=0.006).MESinthemusicandthenoise
environment were not significantly different (p=0.990).
For CS children in the ADHD group showed better
bal-ance performance in the white noise environment than
in the silence environment (p=0.001). MES in the music
and the noise environment were not significantly
differ-ent (p=0.438).In the controlgroup balance performance
didnotsignificantlychange forC1,C2, C3,C5,C6andCS
in the three test environments. Unlike the ADHD group,
childreninthecontrolgroupshowedsignificantlydifferent
balance performances for C4 in the three test
environ-ments (p=0.032). For C4, children in the control group
showedsignificantlybetterperformanceinthemusic
envi-ronment than in the silence environment (p=0.012). MES
in the silence and the noise and music and the noise
environment were not significantly different (p=0.829,
p=0.208).
Table2presentsMESforalltheSOTconditionsandthe
CSfor thebothgroups inthethreetestenvironments. All
MES for each SOT condition in all theenvironments were
lower in the ADHD group. However only MES for C4 and
theCSinthemusicenvironmentreachedstatistical
signifi-cancewithsmalleffectsizes(Table2).Theoverallbalance
performances oftheADHD andthecontrolgroups ineach
environment arepresented in Fig.2. The MES for all the
SOT conditions and CSwere higher in the control group,
buttheoverallbalanceperformancesofthetwogroupsin
eachenvironmentwerenotsignificantlydifferent(p=0.429,
p=0.084,p=0.833).
Thesensoryanalysistestresultsshowedthatchildrenin
theADHDandthecontrolgrouphadsimilarsomatosensory
andpreferenceratiosinthethreetestenvironments.
Chil-drenintheADHDgrouphadlowervisualandvestibularratios
butthedifferencereached significanceonlyfor thevisual
ratiointhemusic environment(Table3).WithintheADHD
groupthesomatosensory,visual,vestibularandpreference
ratiosdidnotsignificantlydifferinthethreetest
environ-ments(p=0.808,p=0.071, p=0.254,p=0.302). Whereas,
withinthe control group the visual ratios changed
signif-icantly between the three test environments (p=0.014).
The visual ratio in the silence environment was
signifi-cantlylowerthenonlythemusicenvironmentinthecontrol
group(p=0.034,p=0.144). The somatosensory, vestibular
andpreferenceratiosdidnotsignificantlydifferinthethree
testenvironmentsinthecontrolgroup(p=0.294,p=0.099,
p=0.709).
Discussion
Themain purposeof thecurrent study wastoinvestigate
theeffectsof distractors onupright balanceperformance
in children with ADHD. When there were no distractors,
thebalancescores underallSOT conditionsandthe
com-posite equilibrium score were lower in the ADHD group.
Althoughthedifferenceswere notstatisticallysignificant,
100.00 90.00 80.00 70.00 60.00 50.00 40.00 30.00 C1 C2 C3 C4 Silence Mean equilibr ium score C5 C6 CS C1 C2 C3 C4 Music C5 C6 CS C1 C2 C3 C4 White noise Control ADHD Group C5 C6 CS
Figure2 ComparisonofthemeanequilibriumscoresoftheADHDandthecontrolgroupsinthethreetestenvironments.ADHD, attentiondeficithyperactivitydisorder;C1,eyesopen,stableplatform;C2,eyesclosed,stableplatform;C3,visualdisorientation (swayreferencedvision),stableplatform;C4,eyesopen,unstableplatform;C5,eyesclosed,unstable platform;andC6,visual disorientation,unstableplatform;CS,compositescore.
C6,andthe compositescore.These findingsindicatethat
childrenwithADHDhadworseuprightbalanceperformance
when they had to rely on visual and vestibular signals
insteadofsomatosensorialsignals.Shumetal.foundworse
balancescores underall SOT conditionsexcept in C1and
lower somatosensorial, vestibular, and visual ratios in
childrenwithADHD.28Theirstudydesignwassimilartothat
ofours; however,theyincluded ahighernumber ofADHD
children(n=43)andcalculatedbalanceperformanceafter
correctingforthephysicalactivitylevel.Theyarguedthat
somatosensorialinformationin additiontovisual and
ves-tibular signalsaffects balancecontrol. The lowernumber
ofparticipantsinourstudy,andthecorrectionofbalance
scores according to physical activity level in theprevious
studymayexplainwhythedifferenceswerenotstatistically
significant in ourstudy. In another study,Buderath et al.
found increased sway area in C4 in children with ADHD
(n=10),and anincreasednumber offalls inC5 andC6 in
childrenwithchroniccerebellarlesions(n=7).26The
abnor-malitiesindynamicSOTweremoreapparentinC4,C5,and
C6;these resultswereconsistent withthoseofourstudy.
Itisknownthatvestibularandvisual signalsarecrucialin
maintainingposturalcontrol.Severalbrainmagnetic
reso-nanceimagingstudieshaveshownanatomicalabnormalities
in the cerebellar vermis, which is important in postural
and gait control.14,16,22 In addition to the cerebellum,
Table3 SensoryanalysisratiosintheADHDandthecontrolgroupsinthethreetestenvironments.
Sensoryanalysisratios ADHD(mean±SD) Control(mean±SD) Statistics p-Value Silence Somatosensory 0.96±0.04 0.95±0.04 282.50 0.608 Visual 0.84±0.19 0.86±0.10 202.50 0.199 Vestibular 0.53±0.30 0.64±0.18 195.50 0.152 Preference 0.94±0.12 0.96±0.14 226.50 0.449 Music Somatosensory 0.95±0.04 0.97±0.02 222.00 0.383 Visual 0.84±0.16 0.95±0.07 123.50 0.002a Vestibular 0.65±0.24 0.71±0.20 201.00 0.190 Preference 0.98±0.11 1.00±0.05 233.00 0.518 Noise Somatosensory 0.96±0.04 0.95±0.04 285.50 0.561 Visual 0.89±0.19 0.94±0.10 213.00 0.292 Vestibular 0.63±0.26 0.72±0.17 212.50 0.291 Preference 0.96±0.07 0.97±0.08 248.00 0.782
ADHD,attentiondeficithyperactivitydisorder. aindicatesp<0.05.
fronto-striatal-cerebellarsystemdysfunctionwasobserved
in childrenwithADHD.12,13,41 Inadditiontolower balance
scores in C4, C5, andC6, particularly the visual and
ves-tibular ratios were lower in sensory analysisin the ADHD
groupinthesilenceenvironment.Althoughnotstatistically
significant (p=0.199, p=0.152), this result may be
clini-cally important. Thus, it can be said that in the silence
environment,theADHDpatients’abilitiestouseinputfrom
thevisualandthevestibularsystemsareaffected.
It is known that quiet standing is not a pure reflex
mechanism and is strongly associated with cognitive
pro-cesses. In daily life, static or dynamic balance control is
performedsimultaneouslywithcognitivetasks,suchas
lis-teningtomusicwhile running.42 Theattentionalneedsfor
balancecontrolvarydependingontheposturaltask,ageof
theindividual,andtheirbalanceabilities.25 Toinvestigate
theroleofcognitioninpostural control,dual-taskstudies
havebeenconducted.21,43,44Ingeneral,ithasbeenthought
thatasecond taskmayadverselyaffectbalancecontrol.45
Shorer et al. included 24 children with ADHD and
mea-suredswayvelocityundersingle-taskandauditory---memory
attention-demandingdual-task conditions.23 Incontrastto
their hypothesis, concurrent auditory---memory cognitive
tasksdidnothaveanegativeeffectonposturalcontrolin
eithertheADHDgrouporthecontrolgroup.Jacobi-Polishook
etal. investigatedthe effectof methylphenidate on
pos-turalstabilityundersingle-anddual-taskconditions(n=24),
withlisteningtomusicasoneofthetasks.Methylphenidate
administrationresulted inbetter posturalstability
perfor-manceunderthedual-taskconditionandwhilelisteningto
music.18 The researchersconcluded that enhanced
atten-tionabilitiesimprovedbalanceperformance. InSöderlund
et al.’s study,although noise was perceived as adversely
affecting cognitive performance, white noise had a
posi-tiveeffectoncognitiveperformanceinchildrenwithADHD.
The researchersexplainedthisresultbyapossible
under-lying mechanism, termed moderate brain arousal model,
whichsupposesthatnoiseintheenvironmentcauses
inter-nal noise in the neural system through the perceptual
system and that this noise affects the neurotransmitter
systemsandimproves cognitiveperformance.32 The
possi-ble enhancing effects of distractors on cognitive process
have been discussed in several other reports.31,46---48 They
hypothesizedthatarousal,activation,andeffortmodulate
children’s information-processing abilities and distracting
information can enhance performance temporarily,
possi-blybyincreasingarousaltoanoptimallevel.48Similarlyour
resultsshowedthat,eventhoughnotreachingstatistical
sig-nificance levels,auditory distractors affected the general
balanceperformancepositivelyforbothgroups.More
chal-lengingconditions,usinganunstableplatform(C4,C5,C6)
withdistortedsomatosensory signals,weremoreaffected
by auditory distractorsin both groups. It can beassumed
thatmorechallengingconditionsneedmorecognitiveeffort
andmoreinformation-processing,thereforemoreaffected
by the possible enhancing effects of auditory distractors.
Basedontheabovesummarizedknowledgeandour
congru-entresultsitcanbehypothesizedthatauditorydistraction
suchasmusic andwhitenoise isnotalways distractingin
children with ADHD and can also have beneficial effects.
Thepositiveeffectofmusicandwhitenoisereached
signif-icancelevelinC6intheADHDgroup.C6isassumedtobe
themostchallengingconditionwithconflicting
somatosen-soryand visual signals and leaving only vestibularsignals
available.IntheADHDgroupthepositiveeffectsofthe
audi-torydistractorsbecamemoreapparentandsignificantasthe
conditiongotharder.Inthecontrolgroup,thepositiveeffect
reachedsignificance in onlyC4 while listening torelaxing
musiconly.Extendingtheprevioushypothesis,wethinkthat
intermsofbalancecontrol,childrenwithADHDbenefitmore
thantypicallydevelopingchildrenfromauditorydistractors
inchallengingconditionsneedingmorecognitiveprocesses.
Inaway,thepositiveeffectsofauditorydistractorsin
typ-icallydevelopingchildrenandtheirADHDcounterpartscan
becomparedtothoseofstimulants.Itisknownthat
stimu-lantsenhancecognitivefunctionsinhealthyindividualstoo
buttheenhancingeffectsaremuchmoresignificantin
peo-plewith ADHD.49 In the sensoryratio analysis children in
theADHDgrouphadlowervisualandvestibularratiosbut
thedifferencereachedsignificanceonlyforthevisualratio
inthemusicenvironment.Deficitsinvisualprocessingand
integrationhavebeenpreviouslyreportedinchildrenwith
ADHD.9,50SimilarlyShumetal.showedthegreatestbetween
groupdifferencesinthevisualratio.Inaddition,inourstudy
whentheADHDandthecontrolgroupswerecomparedMES
forC4andtheCSreachedstatisticalsignificance.28Infact
C4is the condition where the children areforced torely
moreonthevisualinformationwhensomatosensorysignals
aredisrupted.Wethinkitcanbespeculatedthatthevisual
systemmaybethemostinvolvedsystemincontributingto
thebalancedeficitsamongchildrenwithADHD.
Strengthsofthis currentstudy includea DSM-IV-based,
multi-method(interviewandratingscale)diagnostic
proce-dureforADHD,matchingofthechildrenintheADHDgroup
intermsofageandgender.Therearealsoseverallimitations
withthestudy.Wedidnothavetheopportunityto
admin-isterthe diagnosis according tothe DSM-Vbut the period
inwhichthestudywascarriedoutDSM-IV-TRwasthemost
reliablemethodcongruentwithasemi-structuredinterview
forperformingtheassessment.Eventhoughthegroupswere
matchedforageandgender,theremaybeothervariations
thatcannotbecontrolledinfluencingthechildren’s
perfor-mance.Duetosmallsamplesizethenumberofsignificant
findingsmaybesomewhatreduced.Moreimportantly,the
enhancing effect of white noise and relaxing music may
changewithsignalamplitude.32Therefore,differentsignal
amplitudesshouldhavebeentested.Inaddition,wedidnot
investigatetheeffectofbackgroundspeechsignalsasa
dis-tractor; examining this effectmay provide morerealistic
informationsimilartothatinaclassroomsetting.Moreover,
agerange may influence realbalance performance; thus,
maturationofsomatosensorialinformationcompletesbythe
ageof 3---4years,whereasmaturationof visualand
vesti-bularinformationinbalanceisstilldevelopingat15yearsof
age.38Thesecharacteristicsmayexplainthefindingof
bet-terscoresinC1,C2andC3andworsescoresinC4,C5andC6.
However,the resultsobtained inthe vestibularandvisual
ratioanalysispossiblyreflecttherealcapabilityinefficiency
ofvestibularandvisualsignalsinchildrenwithADHD.
Conclusion
Tothe bestof ourknowledge, this isthe firststudy
theeffects ofauditory distractors. Although morestudies
areneeded,ourresultsindicatethatdistractorsmayhave
enhancing effects on upright balance performance and it
may be advantageous to investigate the effects of early
vestibularrehabilitationinthispopulation.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
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