Rev. bras. ortop. vol.49 número6

w w w . r b o . o r g . b r

Original

Article

Proprioceptive

deficit

in

patients

with

complete

tearing

of

the

anterior

cruciate

ligament

夽

,

夽夽

Pedro

Godinho

_,

_Eduardo

_Nicoliche

_,

_Victor

_Cossich

_,

_Eduardo

_Branco

_de

_Sousa

_,

Bruna

Velasques

,

José

Inácio

Salles

a_{MotorControlandExercisePhysiologyLaboratory,NationalInstituteofTraumatologyandOrthopedics(INTO),RiodeJaneiro,RJ,Brazil}

b_{AttentionNeuropsychologyandNeurophysiologyLaboratory,InstituteofPsychiatry,FederalUniversityofRiodeJaneiro(IPUB/UFRJ),}

RiodeJaneiro,RJ,Brazil

c_{InstituteofAppliedNeurosciences(INA),RiodeJaneiro,RJ,Brazil}

d_{DepartmentofBiosciences,SchoolofPhysicalEducationandSports(EEFD),FederalUniversityofRiodeJaneiro(UFRJ),}

RiodeJaneiro,RJ,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received2July2013 Accepted5August2013 Availableonline22October2014

Keywords:

Anteriorcruciateligament Proprioception

Knee

a

b

s

t

r

a

c

t

Objective:Toinvestigatetheexistenceofproprioceptivedeficitsbetweentheinjuredlimb andtheuninjured(i.e.contralateralnormal)limb,inindividualswhosufferedcomplete tearingoftheanteriorcruciateligament(ACL),usingastrengthreproductiontest.

Methods:SixteenpatientswithcompletetearingoftheACLparticipatedinthestudy.A voluntarymaximumisometricstrengthtestwasperformed,withreproductionofthemuscle strengthinthelimbwithcompletetearingoftheACLandthehealthycontralaterallimb, withthekneeflexedat60◦_{.Themeta-intensitywasusedfortheprocedureof20%ofthe}

voluntarymaximumisometricstrength.Theproprioceptiveperformancewasdetermined bymeansofabsoluteerror,variableerrorandconstanterrorvalues.

Results:SignificantdifferenceswerefoundbetweenthecontrolgroupandACLgroupforthe variablesofabsoluteerror(p=0.05)andconstanterror(p=0.01).Nodifferencewasfoundin relationtovariableerror(p=0.83).

Conclusion: Ourdatacorroboratethehypothesisthatthereisaproprioceptivedeficitin sub-jectswithcompletetearingoftheACLinaninjuredlimb,incomparisonwiththeuninjured limb,duringevaluationofthesenseofstrength.Thisdeficitcanbeexplainedintermsof partialortotallossofthemechanoreceptorsoftheACL.

©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublishedbyElsevierEditora Ltda.Allrightsreserved.

夽

Pleasecitethisarticleas:GodinhoP,NicolicheE,CossichV,deSousaEB,VelasquesB,SallesJI.Déficitproprioceptivoempacientes comrupturatotaldoligamentocruzadoanterior.RevBrasOrtop.2014;49:613–618.

夽夽

WorkdevelopedintheResearchDivisionoftheNeuromuscularResearchLaboratory,NationalInstituteofTraumatologyand Ortho-pedics(INTO),RiodeJaneiro,RJ,Brazil.

∗ _{Correspondingauthor.}

E-mail:[email protected](B.Velasques).

http://dx.doi.org/10.1016/j.rboe.2014.10.007

Déficit

proprioceptivo

em

pacientes

com

ruptura

total

do

ligamento

cruzado

anterior

Palavras-chave:

Ligamentocruzadoanterior Propriocepc¸ão

Joelho

r

e

s

u

m

o

Objetivo: Investigar,pormeiodotestedereproduc¸ãodaforc¸a,aexistênciadedéficits pro-prioceptivosentreomembrolesionadoeonãolesionado(i.e.,contralateralnormal)em indivíduosquetenhamsofridorupturatotaldeLCA.

Métodos: Participaramdoestudo16pacientescomrupturatotaldoLCA.Foifeitooteste deforc¸avoluntáriamáximaisométrica(FVIM)ereproduc¸ãodaforc¸amuscularnomembro comrupturatotaldoLCAecontralateralsaudável,comjoelhoa60◦_{deflexão.Foiusadaa}

intensidade-metaparaoprocedimentode20%daFVMI.Odesempenhoproprioceptivofoi determinadopormeiodosvaloresdeerroabsoluto(EA),errovariável(EV)eerroconstante (EC).

Resultados: Diferenc¸assignificativasforamencontradasentreosgruposcontroleeLCApara asvariáveiserroabsoluto(p=0,05)eerroconstante(p=0,01).Nãofoiencontradadiferenc¸a paraoerrovariável(p=0,83).

Conclusão: Nossosdadoscorroboramahipótesedeexistênciadedéficitproprioceptivoem sujeitoscomrupturatotaldeLCAemummembrolesionadoquandocomparadocomonão lesionadoduranteaavaliac¸ãodosensodaforc¸a.Essedéficitpodeserexplicadoporuma perdatotalouparcialdosmecanorreceptoresdoLCA.

©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublicadoporElsevier EditoraLtda.Todososdireitosreservados.

Introduction

Proprioceptionisdefinedastheconsciouscapacitytoperceive position,movementandtheforcesimposedonandproduced bybodysegments.1_{Ithasacrucialroleinjointstabilityand}

posturalandmotorcontrol.2,3_{Therefore,itisessentialfor}

ade-quate functioningofthe jointstructuresduringday-to-day activitiesandsportspractice.4_{Themainwaysofevaluating}

proprioceptionarethroughtestingjointpositionsense(JPS),5

the perceptionthreshold forpassive movement5–7 _{and the}

senseofstrength.8,9

Withregardtothekneejoint,tearingoftheanterior cruci-ateligament(ACL)isthecommonestinjury,anditsincidence hasbeenincreasingovertheyears.10 _{Ithasbeenestimated}

thatintheUnitedStates,95,000peoplesufferinjuriestothis ligamenteveryyear.11

TheACLfunctionstogetherwithotheranatomical struc-tures surrounding the knee so as to maintain static and dynamicbalance.Ithasanimportantroleinproprioceptive monitoringofmechanicalreceptorssuchasPacinicorpuscles andRuffiniendings.12–15

Many studies have indicated that subjects with partial tearingoftheACLpresentproprioceptivedeficits.16–18_These

deficitscanbeconsideredtobefactorspredisposingtoward kneeinstability17_{:theyadverselyaffecttheactivity,balance}

andstrengthofthequadricepsandincreasetheriskofnew injuriestotheknee.19

Thefunctional and proprioceptivelevels of the knee in subjectswithpartialtearingoftheACLhavebeenmeasured previouslyandmoststudieshaveusedtestsonJPSoronthe thresholdofdetectionofpassivemovement.13,20_Allofthese

studieshavefounddeficits intheinjuredlimbin compari-sonwiththeuninjuredlimb.14,21,22_{Thesenseofstrengthhas}

receivedmoreattentionintheliteraturerecently,butfewdata areavailableinrelationtothisparadigmforevaluating propri-oceptioninthekneejoint,giventhattherearenostudiesthat haveevaluatedpatientswithtotaltearingoftheACL.

Thus, the objective of the present study was to use a strength reproduction test to investigate the existence of proprioceptivedeficitsbetweentheinjuredlimbandthe unin-juredlimb(i.e.thenormalcontralaterallimb),inindividuals whohavesufferedtotaltearingoftheACL.Inthisregard,our studyhypothesiswasthatindividualswithtotaltearingofthe ACLwouldpresentproprioceptivedeficitsintheinjuredlimb, incomparisonwiththeuninjuredlimb.

Materials

and

methods

Subjects

Fig.1–Photoofanindividualpositionedinthe dynamometer.

Experimentalprocedureandtask

Anisokineticdynamometer(CSMI,HumacNorm)wasused, andbeforeeachtest,theequipmentwasproperlycalibrated. Thesubjectswerepositionedtositcomfortably,withthe lat-eralcondyleofthefemuralignedwiththerotationaxisofthe apparatusandtheanklefixedtotherodoftheknee assess-mentaccessorybymeansofaVelcrostrip(Fig.1).

Thefollowingtestswereperformed:

(1) Muscle strength andforce reproduction testswere per-formedwiththekneeextendedat60◦_{.Inordertoperform}

amaximumvoluntaryisometricstrength(MVIS)test,the subjectswarmed up and became familiarized withthe equipment by means offive repetitions, without resis-tance imposed by the apparatus, performed over their entirerangeofjointmotion.Afterthisfamiliarization,the subjectsperformedspecificwarm-upswiththree submax-imalisometriccontractions(withsubjectiveeffortof20%, 40%and60%ofthemaximumforce),withaone-minute interval between them.The MVISwas conducted after athree-minuteinterval,andthreeattemptsweremade withthree-minuteintervalsbetweenthem.Thegreatest instantaneoustorquefoundwastakentobe100%ofthe MVIS.Eachisometriccontraction lastedforsixseconds. Theuninjuredlimbwasevaluatedfirst.

(2) Areproductiontestontheipsilateralstrengthoftheknee extensorswasperformedafterleavinga10-mininterval followingtheMVIStest.Thetargetintensityforthe pro-cedurewas 20% ofthe MVIS. Theprocedure consisted

of performing a reference contraction, in which visual feedbackofthetorquelevelwasused.Thesubjectswere instructedtomaintainthedesiredforcelevel.Immediately afterthereferencecontraction,thesubjectsattemptedto reproducetheforceproducedpreviously,aspreciselyas possible, withoutvisual feedback.Three attemptswere made, withthree-minuteintervals betweenthem.Each isometriccontractionlastedforsixseconds.

Dependentvariables

Theindividualerrorvalueforeachattemptwasdetermined as the difference between the reproduced force and the forceexperienced.Theproprioceptiveperformancewas deter-mined bymeans ofthe values forthe absolute error(AE), variableerror(VE)andconstanterror(CE).SchmidtandLee23

describedthecalculationsforeachvariable,indetail.Briefly, theAEisobtainedfromthearithmeticmeanoftheindividual errorsinthemodulusanddeterminestheindividual’s accu-racyinreproducingforce;theVEisthestandarddeviationof theindividualerrorsanddeterminestheconsistencyofthe reproductionsperformed;andtheCEisthearithmeticmean oftheindividualerrorswiththesignsanddeterminesthe ten-dencytoreproducetheforceaboveorbelowthetarget(bias). Onlytheperiodofthetorquecurvesfromtwotosixseconds wasusedfordeterminingtheAE,CEandVE.Pilottests demon-stratedthatthiswouldbetheperiodneededforthesubjectsto stabilizetheintensityofcontraction,andwithinwhichthere would betheleasteffectfrom fatiguewhilesustaining the force.

Statisticalanalysis

Descriptive statistics(mean±standard deviation(SD))were used to describe the data. The dependent variables were the AE, VE and CE. The data were subjected to the Shapiro–Wilk test of normality. Comparisons were made betweentheinjuredanduninjuredlimbs.Thevalues deter-minedfor20% ofMVISwere comparedusingthettestfor paired measurements. The calculations were made using the Statistical Package for the Social Sciences (SPSS Inc. Chicago, IL, USA). The significance level established was

p≤0.05.

Results

Timeandcauseoftheinjuryandassociatedlesions

The mean length of time from the injury until the data gathering was 3.2±1.6years.In the majority ofthe cases, theinjuriesoccurredduringrecreationalsoccerpractice,all without contact (68.75%). Other cases occurred in relation to surfing (6.25%), falling (6.25%), playing handball (6.25%), playingbasketball(6.25%)andsufferingmotorcycleaccidents (6.25%).

Clinicalexaminations

Table1–Clinicalexaminations.

Lachmanandanteriordrawer

− +/+++ ++/+++ +++/+++

Lachman 3 13 0 0

Anteriordrawer 0 16 0 0

McMurrayandPivot

− +

Bocejo 8 8

Pivot 3 13

Table2–AE,VEandCEdeterminedfor20%MVIS (mean±SD).

AE VE CE

ACL 4.3±2.2%a _{1.6±1.2% 4.1±2.3%}a

Control 3.0±1.3% 1.7±1.1% 1.9±2.1%

a _{Significantlydifferentfromthecontrollimb.}

Valuesforabsoluteerror(AE),variableerror(VE)and constanterror(CE)

Afterthedata-gathering,thestrengthvalueswere standard-ized inrelation tobody weight. This wasdone to makeit possible to make comparisons between our subjects. The MVIScalculatedfortheuninjuredlimbwas3.2±1.0N/kgand fortheinjuredlimb,3.0±1.1N/kg.Nostatisticallysignificant differencewasfoundfortheMVIS(p=0.059).Thettest demon-stratedasignificantdifferencebetweenthelimbsregarding thevariablesAE(p=0.05)andCE(p=0.01)(Fig.2).Therewas nodifferenceregardingVE(p=0.83).Themeansandstandard deviationsforthe individualerrorsrelating tostrength are giveninTable2.

Discussion

Thepresentstudyhadtheobjectiveofdeterminingwhether patientswithtotaltearingoftheACLpresentedproprioceptive deficitsintheinjuredlimbduringassessmentoftheirsense

ofstrength.Forthis,musclestrengthandforcereproduction testswereperformedontheinjuredanduninjuredlimbs.In thisregard,weworkedwiththehypothesisthatindividuals with totaltearingofthe ACLwould present proprioceptive deficitsintheinjuredlimb,incomparisonwiththeuninjured limb.OurhypothesiswasinlinewiththestudybyHérouxand Tremblay,18_{whoidentifiedproprioceptiondeficitsinthissame}

populationusingaweightdiscriminationtest.

In particular, thesense ofstrength was evaluatedin 16 patientswithunilateraltotaltearingoftheACL,using20% oftheirMVIS.Significantdifferenceswerefoundintheforce reproductiontestbetweentheinjuredanduninjuredlimbs. TheAEresultsdemonstratedthattheinjuredlimbwasless capableofaccuratelyreproducingtheforce,giventhattheCE resultsdemonstratedthatalthoughbothlimbstendedto over-estimatethetarget,theinjuredlimboverestimatedthismuch more.WithregardtotheVE,wedidnotfindanystatistical difference,whichshowsthattheindividualswereconsistent regardingtheerrors.

Using the JPStest, Leeet al.16 _{and Carteret al.}17 _found

significantlydifferentAEvaluesbetweentheinjuredand unin-juredlimbs.HérouxandTremblay18_{conductedastudyonthe}

senseofstrengthusingtheweightdiscriminationtestandalso obtainedresultsthatindicatedloweracuityintheinjuredside. Theresultsfromourinvestigationcorroboratetheresultsfrom thesethreeexperiments.Fewstudiesonthesenseofstrength haveusedtheforcereproductiontest,whichmakesitdifficult tocomparetheresults.

Thus,onelikelyexplanationforthelowaccuracyofforce reproductionontheinjuredsidemaybepartialfailureofthe processofcalibratingthedescendingmotorcommandsdueto impairedassessmentoftheforcesignalsresultingfrom mus-clecontraction.Thispossibilityraisesthequestionofwhich afferentinformationsourcesaresusceptibletobeingaffected byACLinjuries.

Among the receptors, the Golgi tendon organ (GTO) is considered to bethe mainsource of afferentinputs com-ingfromperipheralregionsrelatingtomusclestrengthand tension.24–26 _{However, because the GTO is located in the}

muscle-tendonarea,itshouldnotbeaffectedbyACLinjuries.

Proprioceptive performance – absolute error

A

Control ACL 4

3

2

1

5

4

3

2

1

B

Absolute error (%) Constant error (%)

Control ACL

Thus,involvementoftheGTOinthelowacuityofoursubjects seemsveryunlikely.

ThereisevidencethatafferentstimulationoftheACLmay influencekneeflexorandextensoractivityduringvoluntary contractions27_{andthatthesensoryinnervationofthejoints}

israrelyrecovered afterinjury.28 _{Our subjects’ difficulty in}

forcereproductioncanbeattributedtolossofinnervationof themechanicalreceptorsoftheACL,whichthusreducesthe quantityofsensoryinformationrelatingtotensionandforce duringthetest.

Itisalsopossiblethatsomemechanicalreceptorslocated inthejointcapsulethatweresparedfrominjurymay nonethe-lesshavebeen altered.KhalsaandGrigg29 _{investigatedthis}

possibilityinananimalmodelandconcludedthatthe affer-entresponsecapacityofthejointcapsulewasnotsignificantly affected after complete transection of the ACL. Thus, we believethattherewassomeresidualinnervationintheinjured knee,togetherwiththeinputsfromtheGTO,whichremained intactinthequadriceps. Thiswouldexplainthevariability betweenindividualsthatwasobserved.Itmightalsoexplain whythecapacitytoreproduceforce,albeitreducedin compar-isonwiththeuninjuredleg,wasstillrelativelywellconserved inoursubjects.

In relationto the MVIS, our results didnot find signif-icantlydifferent values: 3.2±1.0N/kg forthe uninjured leg and3.0±1.1N/kgfortheinjuredleg.Thisdifferedfromwhat wasfoundbyHérouxandTremblay.18 _{Weattributethis}

dif-ferenceinresultstothe factthatoursubjectsweremostly practitionersofphysicalactivity.However,ourMVISvalues weremuchhigherthanthosefoundinthestudybyHéroux and Tremblay.18 _{This was probably because although they}

alsoused anisokinetic dynamometer,it was doneat with thekneeextendedat45◦_{.Weusedakneeextensionof60}◦_,

whichproducedgreatermechanicalefficiencyofthe quadri-ceps,withthecapacitytoreachhigherpeaktorque,according tothe database of ourlaboratory (unpublished data). This makesitimpossibletodirectlycomparetheresults,because we used force values that were standardizedaccording to weight.

Thus,ourdatacorroboratethehypothesisthatthereisa proprioceptivedeficitamongsubjectswithtotaltearingofthe ACLinoneinjured limb,incomparisonwiththeuninjured limbduringassessmentofthesenseofstrength.This propri-oceptivedeficitseemstobebetterexplainedinthestudyby HogesvorstandBrand,28_{alongwiththatofKhalsaandGrigg,}29

whoattributedthecapacityforforcereproductiontolosses, ortothecontinuingexistenceofsomeresidualinnervationof themechanicalreceptorsoftheACL,alongwithinputsfrom theGTO,whichremainedintactinthequadricepsandreduced thequantityofsensoryinformation.

Inthisregard,becauseoftheabsenceofstudiesrelating tothisproblem,wesuggestthatnewstudiesshouldbe con-ducted withthe aimsofexpandingthe knowledgeon this subjectandenablingcomparisonofresults.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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