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www.rpped.com.br

REVISTA

PAULISTA

DE

PEDIATRIA

ORIGINAL

ARTICLE

Respiratory

muscle

strength

test:

is

it

realistic

in

young

children?

João

Paulo

Heinzmann-Filho,

Márcio

Vinícius

Fagundes

Donadio

CentroInfant,InstitutodePesquisasBiomédicas,PontifíciaUniversidadeCatólicadoRioGrandedoSul(PUCRS),PortoAlegre, RS,Brazil

Received1September2014;accepted18January2015 Availableonline27June2015

KEYWORDS Respiratoryfunction tests;

Musclestrength; Respiratorymuscles; Feasibilitystudies

Abstract

Objective: Todeterminethesuccessrateofthemanovacuometrytestinchildrenbetween4

and12yearsofage.

Methods: Cross-sectionalstudyinvolvingchildrenandadolescentsfrom4to12yearsofage,

enrolledinthreebasiceducationschools.Allsubjectshadtheanthropometricandrespiratory

musclestrength(maximuminspiratorypressureandmaximumexpiratorypressure)data

mea-sured.Studentswhoseparentsdidnotauthorizeparticipationorwhodidnotwanttoundergo

thetestwereexcluded.Thetestwasconsideredsuccessfulwhenthesubjectreached

accept-ability(noairleaks)andreproducibility(variation<10%betweenthetwo majormaneuvers)

criteriaestablishedbyguidelines.Failurewasdefinedwhensubjectsdidnotmeettheabove

criteria.Datawereexpressedasmeanandstandarddeviationandthecategoricalvariablesin

absoluteandrelativefrequency.Thecomparisonbetweenproportionswasperformedusingthe

chi-squaretest.

Results: Weincluded196childrenandadolescents,meanageof8.4±2.5years,53.1%female.

Thesuccessrateofthemanovacuometrytestinchildrenandadolescentsevaluatedwas92.3%.

Whencomparingthedifferencesbetweenthesuccessratesofpreschoolchildrenwiththose

childrenandadolescentsofschoolage,therewasasignificantlylowersuccessrateinthe

pre-school(85.1%)groupcomparedtotheschoolgroup(94.6%)(p=0.032).However,nosignificant

differences(p=0.575)werefoundwhengendercomparisonswereperformed.

Conclusions: Themanovacuometrytestshowedahighsuccessrateinbothpreschoolandschool

populationassessed.Furthermore,therateofsuccessappearstoberelatedtoaging.

© 2015Sociedadede Pediatria de S˜ao Paulo. Published by Elsevier Editora Ltda.All rights

reserved.

DOIoforiginalarticle:http://dx.doi.org/10.1016/j.rpped.2015.01.008

Correspondingauthor.

E-mail:mdonadio@pucrs.br(M.V.F.Donadio).

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PALAVRAS-CHAVE Testesdefunc¸ão pulmonar; Forc¸amuscular; Músculos respiratórios; Estudosde viabilidade

Testedeforc¸amuscularventilatória:éviávelemcrianc¸asjovens?

Resumo

Objetivo: Determinarataxadesucessodotestedemanovacuometriaemcrianc¸asdequatro

a12anos.

Métodos: Estudotransversalqueincluiucrianc¸aseadolescentesdequatroa12anos,

matricu-ladasemtrêsescolasdaredebásicadeensino.Todososparticipantesfizeramamensurac¸ãodas

medidasantropométricas,seguidasdotestedemanovacuometria(pressãoinspiratóriamáxima

epressãoexpiratóriamáxima).Escolares cujosresponsáveisnão autorizaramaparticipac¸ão

e aquelesque nãoquiseram fazeroteste foramexcluídos.Oteste foiconsiderado sucesso

quandoo sujeitoavaliado atingia oscritérios de aceitabilidade(ausênciade escapeaéreo)

ereprodutibilidade(variac¸ão<10%entreasduasmaioresmanobras)estabelecidospelas

dire-trizes.Oinsucessofoidefinidocomonãopreenchimentodoscritériosdescritosacima.Osdados

foramexpressosemmédiaedesviopadrãoeemfrequênciaabsolutaerelativa.Acomparac¸ão

entreasproporc¸õesfoifeitapormeiodotestedequi-quadrado.

Resultados: Foramincluídas196crianc¸aseadolescentes,comidademédiade8,4±2,5anos,

53,1%dosexofeminino.Ataxadesucessodotestedemanovacuometriaem crianc¸ase

ado-lescentesavaliadosfoide92,3%.Quandocomparadasasdiferenc¸asentreastaxasdesucesso

de crianc¸asnafaixa etáriapré-escolarcomcrianc¸as eadolescentesnafaixaetáriaescolar,

observou-seumataxadesucesso significativamentemenornogrupopré-escolar(85,1%),em

comparac¸ãocomogrupoescolar(94,6%)(p=0,032).Noentanto,nãohouvediferenc¸a

significa-tiva(p=0,575)quandoanalisadasdiferenc¸asentresexos.

Conclusões: Otestedemanovacuometriaapresentouumaelevadataxadesucessonapopulac¸ão

pré-escolareescolaravaliada.Alémdisso,ataxadesucessopareceestarrelacionadacomo

aumentodaidade.

© 2015Sociedadede Pediatriade S˜ao Paulo. Publicado porElsevier Editora Ltda.Todosos

direitosreservados.

Introduction

Althoughrespiratorydiseases andotherclinical conditions inthepediatricpopulationaresomeofthemaincausesof morbidityandmortalityinchildhood,1,2manyofthemhave

not often been evaluatedby objectivemeasures in clini-calpractice.Thereareseveralreasonsforthisinchildren, mainlythefactthatmanytestsarenotstandardized.3Itis

difficultforthesubjectstounderstandandcooperate,there islowreproducibility,andalsolackofinformationon cer-tainmethodsamonghealthcareprofessionals,aspartofthe evaluationofmanylungconditionsanddiseases.3

In this sense, lung function tests are important tools usedtoevaluatetherespiratorysystem.Theysupply objec-tivemeasurestohelpdiagnoseandmanagevariousclinical conditions.3Among these,therespiratory musclestrength

testisasimple,non-invasiveresource,easytoapply,andis usedtoevaluatethemaximumstaticrespiratorypressures, which reflect respiratory muscle strength.4 It consists of

twomeasures:onedirectedatevaluatinginspiratory mus-cle strength throughmaximum inspiratorypressure (MIP), the other to investigate the expiratory muscle strength throughmaximum expiratory pressure (MEP).4,5 It is

com-monlyusedtodeterminerespiratorymuscleweaknessand toquantifytheseverityofcertaindiseases.4,6Inthe

pedi-atricagerange,itcanhelpinthemanagementandfollow-up of neuromusculardiseases, lung disorderssuch asasthma and cystic fibrosis, and it is also used in rehabilitation programs.4,7

In clinical practice, respiratory muscle weakness can beassociatedwithhypercapnia, withrecurrent infections and inefficient coughing, predisposing to the develop-ment of respiratory failure and the onset of more severemorbidities.8,9 Therefore, inthe lasttwodecades,

studies10---12havebeenperformedtogeneratereference

val-ues for maximum static respiratory pressures in healthy childrenandadolescents,inordertomakegreater useof theminclinicalpractice,duetothepossibilityof normal-izingandinterpreting theserespiratoryfindings.Recently, normalityvalues were published for healthy preschoolers andschoolchildren,10 showing that this evaluationcan be

performedeveninyoungindividuals.Theabsenceof normal-ityvaluesinsmallerchildrenhasbeenascribedmainlytothe technicaldifficultyandthechildren’slackofunderstanding whilethe test isbeingperformed,13,14 demonstratingthat

theagefactormaybethemainlimitationtoevaluatingand usingrespiratorymusclestrengthinthispopulationgroup. However,thereisasyetnoevidenceshowinghowthe suc-cessratesoftherespiratorymusclestrengthtestbehavein differentagegroups.

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patientsunderdifferentsituationsandconditionsinclinical practice.

Method

This is a cross-sectional, observational study with chil-drenandadolescentsaged4---12yearswhowereregularly enrolledat threebasic educationschools (two publicand oneprivate) in Porto Alegre, state of Rio Grande do Sul, during 2011 and 2012. First, all the children and adoles-cents were invited to participate in the study, and they receiveda letterofinvitation,togetherwiththefreeand informedconsentform.Aftertheparentsand/orguardians hadsignedandauthorizedit,theywereinvitedfor anthro-pometricmeasurements,followedbytherespiratorymuscle strengthtest (manovacuometry) at their ownschool. Stu-dentswhoseparentsand/orguardiansdidnotauthorizethe subjects’participationinthestudy,andschoolchildrenwho did not want toundergo the test on the day when eval-uation was performed were not included. The study was approvedby theResearchEthicsCommitteeofthe Pontif-ícia Universidade Católica doRio Grande doSul (PUCRS), underregistration number 11/05503. The anthropometric evaluationwasperformedbymeasuringweightandheight intriplicate, or until twoidenticalvalues wereobtained. Weight was obtained with the individuals in the ortho-staticposition,wearingaminimumamountofclothesand noshoes,usingdigital scales (G-Tech, Glass1 FW, Riode Janeiro,Brazil)previouslycalibratedwitha100gprecision. Then,heightwasobtained,withtheparticipantsbarefoot andfeetinaparallelposition,anklesjoinedtogether,arms extended along thebody, andthe head ina neutral posi-tion.Theheightwasobtainedusingaportablestadiometer (AlturaExata,TBW,SãoPaulo,Brazil)witha1mmprecision. Respiratorymusclestrengthwasevaluatedalwaysbythe sameevaluator(physiotherapist),whopresentedoverayear ofpreviousexperienceperformingthetestandwhowasalso trainedandsupervisedbytheprincipalinvestigatorofthe study.Thetestwasevaluatedusingapreviouslycalibrated digital manovacuometer(MVD300, Globalmed, Porto Ale-gre, Brazil) witha variationof −300 to+300cmH2O. The instrument wasconnected to a silicone tube, coupled to an isolatingfilterand toaconnector withan inner diam-eter of approximately 2.5cm, which was connected to a mouthpiece.Theflattish,semi-rigidmouthpiecehadan ori-fice,withadiameterofapproximately2mmtopreventan increaseinintra-oralpressuregeneratedbythecontraction oftheoralcavitymuscles.4Beforemeasuringtherespiratory

pressures,thetechniciandemonstratedandgavedetailed guidanceregardingthemaneuverstobeperformed.

First, MIP was measured from the residual volume, followedbyMEP fromthetotallungcapacity.4 While

per-formingthelattermeasurement,theindividualsweretold topositiontheirhandsonthecheekstokeepairfrom accu-mulatingonthesidesoftheoralcavity.15Themeasurements

were performed with a nasal clip, in a seated position, withthetorso erect at a positionof 90◦ tothe hip.Both

measurementswere performed withmaximum efforts, at approximately1-min intervalsbetweenthemeasures,and sustainedforatleastonesecond.16Aminimumofthreeand

amaximumofninemeasureswereusedforeachtest.13The

Table1 Characterizationofthestudysample.

Variables n=196

Demographiccharacteristics

Age(years) 8.4±2.5

Female,n(%) 104(53.1)

Anthropometry

Weight(kg) 32.0±12.5

Height(cm) 130.0±15.2

BMI(absolute) 18.2±3.5

BMI(percentile) 66.6±26.8

Manovacuometry(cmH2O)

MIP 83.5±21.9

MEP 96.8±26.8

Resultspresentedasmeanandstandarddeviation.

n,totalnumberofsubjects evaluated;BMI,bodymassindex; MIP, maximal inspiratory pressure; MEP,maximum expiratory pressure.

testwasconsideredsuccessfulwhenthesubjectperformed technicallycorrectmaneuvers,includingthreeacceptable measures(withoutairescaping)andtworeproducibleones (variationoflessthan10%betweenthetwolarger maneu-vers). The last value recorded could not be larger than the previous ones,4 and the final result was the highest

value obtained.The test wasconsidered inadequate (fail-ure)whenthesubjectevaluateddidnotreachthecriteria ofacceptabilityandreproducibilitydescribedabove.

Thesample sizewasestimated todetect afailurerate of approximately10%,witha confidencelevel of95% and amaximumacceptabledifferenceof5%.Forthat,itwould benecessarytoincludeatleast140individuals.Thus,the sampleincludedinthisstudysurpassesthisestimate.Data normalitywastestedusingtheKolmogorov---Smirnovtestand presentedanormaldistribution,sothedatawereexpressed asmeanandstandarddeviationofthemean.Thecategorical variableswerepresentedinabsoluteandrelativefrequency. Thecomparisonbetweenproportions(agegroupsand gen-derinrelationtothetestsuccessrate)wasperformedusing the Chi-square test. All analyses and the data processing wereperformedusingtheSPSSsoftware,version18.0(SPSS Inc., EUA). In all cases, the differences were considered significantwhenp<0.05.

Results

In thestudy,196children andadolescentswereincluded, withameanageof8.4±2.5years,weightof32.0±12.5kg, and130.0±15.2cmofheight;theywerepredominantly Cau-casian(69.4%),and53.1%werefemale.Thecharacterization ofthesamplewiththeanthropometricdataandinformation onrespiratorymusclestrengthareshowninTable1.

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Table2 Success rateoftherespiratory musclestrength

testaccordingtotheagestudied.

Agegroup(years) n(N) Successrate(%)

4 16(19) 84.2

5 24(28) 85.7

6 16(18) 88.9

7 20(21) 95.2

8 25(27) 92.6

9 22(23) 95.7

10 19(20) 95.0

11 18(19) 94.7

12 21(21) 100

n,subjectswithasuccessfultest;N,totalsubjectsevaluated.

from84.2%at4yearsofageto100%at12years.Thesuccess valuesforeachagegroupareshowninTable2.

Whenthedifferencesbetweensuccessratesofchildren inthepre-schoolagerange(4and5years)andchildrenand adolescentsintheschoolagerange(6---12)werecompared, asignificantlylowersuccessratewasseen(p=0.032)inthe pre-school group (85.1%), compared to the school group (94.6%)(Fig.1).Differencesinthesuccessrateswerealso analyzedaccordingtogender.However,therewasno signif-icantdifference(p=0.575)whenthesuccessratesbetween boysandgirlswerecompared(Fig.2).

Discussion

In this study, the success rate observed in children and adolescentsevaluatedwas92.3%.Thisshowsthatthe respi-ratory muscle strength test is a simple resource,easy to apply and highly feasible in this age group. Further, it is a non-invasive method that supplies important infor-mation about the function of the respiratory muscles implicatedinthebreathingprocess,thatareofteninvolved inand/oratamechanicaldisadvantageunderseveral con-ditionsor clinicalsituations,asinlungandneuromuscular diseases.4,5

100

*

Preschool

School 80

60

40

20

Total rate observed

0

Failure Success Failure Success

Figure1 Comparisonbetweenthesuccessandfailurerates

observedinbothagegroups(preschoolandschool).*Chi-square

test:p=0.032.

100

Girls

Boys 80

60

40

20

Total rate observed

0

Failure Success Failure Success

Figure2 Comparisonbetweenthesuccessandfailurerates

observedinrelationtosex.

Tothebestofourknowledge,thisisthefirststudy aim-ingtodeterminethesuccessrateoftherespiratorymuscle strengthtestindifferentagegroupsofthepre-schooland schoolpopulation,whichmakesitdifficulttocomparethe valuesfoundinthoseofotherstudies.Inanycase, consid-eringotherlungfunctiontests,webelievethatthesuccess ratefound in thisstudy ishigh. Possiblecontributing fac-tors includea higher level of explanationtothe subjects evaluated,alongermeasurementtimeandpatienceofthe evaluatorresponsibleforperformingthetests.10Differently

fromspirometry,inwhichspecificstandardsandguidelines weredeveloped to allow itsuse in younger age groups,17

toevaluatetherespiratorymusclestrengthinthisstudyit wasnotnecessary touse anymethodologydifferent from thatpublishedbytheguideline,4,13 suggestingthatitisnot

difficult to perform the test in these age groups in the clinicalpractice.Whenwecomparedourresultstothe suc-cess rates of the spirometry test, the respiratory muscle strength test is also easy and simple, since the spirom-etry success rates are close to the results shown here, around85%.18---21 Additionally,areviewofrecentliterature

hasshownthatalthoughthepreschoolagegroupis charac-terizedasanextremelyyoung sample,withitsdifficulties andmotor limitations, thesuccess rate of thespirometry (regardless of previous experience) ranged between 71% and92%,demonstratingthefeasibilityofpulmonary evalu-ationinthisagegroup.22Althoughbothtestshavedifferent

methodologies,objectives andfunctionality, the compari-sonwithawell-knownandextensivelystudiedlungfunction testmayindicateaparameteruntilfurthersuccessratesare generatedfortheevaluationofpediatricrespiratorymuscle strength.

As expected,the successrates of the respiratory mus-cle strength test appear to increase with the age of the childrenevaluated.Inaddition,whencomparedtothe vari-ablesex,nosignificantdifferencewasfound.Thesefindings aresimilartothosefoundinvariousstudiesthatevaluated thelungfunctionsuccessratesinthepediatricpopulation, showingthat asthe children grow older, thesuccess rate alsorises.21,23,24Previousstudies thataimedat generating

normality values for the respiratory muscle strength test ascribethefailureofthetechniquetothedifficultyin under-standing,lowreproducibilityandlackofcooperationbythe childreninthisagegroup.13,14However,thesestudieshave

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hinderingabetterknowledgeandunderstandingoftheage asaninfluencingfactoronthisoutcome.Inthissense, sev-eralstudiesthatevaluatedthefrequencyofsuccessofthe spirometrytesthave shownthat,in preschoolers,the dif-ficultyofobtaining anadequate test maybeexplainedas beingduetoreducedattention,easydistraction,difficulty inunderstanding,motorcoordination,andlowtolerancefor frustrationduringmaneuvers.Besides,thechild’semotional stage and stage of development are important factors in determiningthesuccessofthetest.18,25

Although the present study does not show informa-tionabout theprevious respiratoryhistoryofthesubjects included,itis believedthatthosefactorswouldnot influ-encetheabilityofanindividualtoperformthetest,which wasthemainoutcomeofthestudy.Also,itisunlikelythat severerespiratory conditionsthatcouldpossiblyalterthe performanceofthetestwouldbepresentinsuchayoung, healthysample,recruitedataschoolenvironment,andwith normalnutritionalstatus.Ontheotherhand,evenifthatis possible,previousstudies26,27haveshownthatmildto

mod-erateasthmaticsubjectsdonotpresentrespiratorymuscle strengthreduction, whichis usually associatedwithmore severelungdisease,includingthepresenceofhyperinflation andpoornutritionalstatus.28,29

One of the limitations of this study is that the test is performedby anexperienced evaluator,whoisinterested inachievingasmuchsuccessaspossibleinthetests,which mayhavecontributedtothehighsuccessratefoundinthis sample. However,these findings only strengthen the idea thatitispossibletoperformthistestinthepediatricage range,andthatatleastinpart,achievingsuccessdepends notonlyonthechildrenand/oradolescentsevaluated,but also on the effort and stimulus supplied by the evalua-tor.Inthissense,apreviousstudy30 recentlydemonstrated

thatthequalityofspirometrytestsincreasedfrom57%to 83%aftertheinclusionofatrainingprogramconductedby telemedicinein15participatingcenters.Newstudies con-cerningthefrequencyofsuccessinthepre-schoolagegroup shouldbeencouragedtoobtainnewinformationaboutthe behaviorofsuccessrates inthisagegroup,enabling com-parisonsamongstudiesandhelpingtoachievegreateruse ofthisresourceamongthechildpopulation.

Inbrief, therespiratorystrength test presented ahigh rate of success amongthe pre-school and school popula-tionevaluated.Besides,thesuccessrateappearstoincrease withage.Thefindingsofthisstudyshowthattherespiratory musclestrengthtestisasimpleandeasytoapplyresource. Thus, obtaining an adequate test may ensure the quality ofthemeasurementsandconsequently,successinthe con-trolandfollow-upoftheoutcome ofdifferentrespiratory involvements.

Funding

Thisstudydidnotreceivefunding.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

TheauthorsthankFAPERGSforthescholarship(JPHF).

References

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8.SimõesRP,DeusAP,AuadMA,DionísioJ,MazzonettoM, Borghi-SilvaA.Maximalrespiratorypressureinhealthy20to89 year-oldsedentaryindividualsofcentralSãoPauloState.RevBras Fisioter.2010;14:60---7.

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12.Mendes RE, Campos TF, Macêdo TM, Borja RO, Parreira VF, Mendonc¸a KM. Prediction equations for maximal respi-ratory pressures of Brazilian adolescents. Braz J Phys Ther. 2013;17:218---26.

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19.Pesant C, Santschi M, Praud JP, Geoffroy M, Niyon-senga T, Vlachos-Mayer H. Spirometric pulmonary function in 3- to 5-year-old children. Pediatr Pulmonol. 2007;42: 263---71.

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25.StocksJ.Clinicalimplicationsofpulmonaryfunctiontestingin preschoolchildren.PaediatrRespirRev.2006;7:S26---9. 26.OliveiraCM,LanzaF,SoléD.Respiratorymusclestrengthin

chil-drenand adolescentswithasthma:similartothatofhealthy subjects?JBrasPneumol.2012;38:308---14.

27.MarcelinoAM,CunhaDA,CunhaRA, daSilvaHJ.Respiratory musclestrengthinasthmaticchildren.IntArch Otorhinolaryn-gol.2012;16:492---6.

28.LaghiF,Tobin MJ.Disordersoftherespiratorymuscles. AmJ RespirCritCareMed.2003;168:10---48.

29.Weiner P, Suo J, FernandezE, Cherniack RM. The effectof hyperinflationonrespiratorymusclestrengthandefficiencyin healthysubjectsandpatientswithasthma.AmRevRespirDis. 1990;141:1501---5.

Imagem

Table 1 Characterization of the study sample.
Figure 1 Comparison between the success and failure rates observed in both age groups (preschool and school)

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