w w w . r b o . o r g . b r
Original
Article
Proprioceptive
deficit
in
individuals
with
unilateral
tearing
of
the
anterior
cruciate
ligament
after
active
evaluation
of
the
sense
of
joint
position
夽
,
夽夽
Victor
Cossich
a,
Frédéric
Mallrich
a,b,
Victor
Titonelli
a,
Eduardo
Branco
de
Sousa
a,
Bruna
Velasques
a,b,c,d,∗,
José
Inácio
Salles
a,eaNeuromuscularResearchLaboratory,NationalInstituteofTraumatologyandOrthopedics(INTO),RiodeJaneiro,RJ,Brazil
bDepartmentofBiosciences,SchoolofPhysicalEducationandSports(EEFD),FederalUniversityofRiodeJaneiro(UFRJ),RiodeJaneiro,
RJ,Brazil
cNeurophysiologyandAttentionNeuropsychologyLaboratory,InstituteofPsychiatry,FederalUniversityofRiodeJaneiro(IPUB/UFRJ),
RiodeJaneiro,RJ,Brazil
dInstituteofAppliedNeurosciences(INA),RiodeJaneiro,RJ,Brazil
eBrazilianVolleyballConfederation(BV),RiodeJaneiro,RJ,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory: Received12June2013 Accepted30July2013
Availableonline27October2014
Keywords:
Anteriorcruciateligament Somatosensorysystem Knee
a
b
s
t
r
a
c
t
Objective:Toascertainwhethertheproprioceptivedeficitinthesenseofjointposition con-tinues tobepresentwhenpatientswithalimbpresentingadeficientanteriorcruciate ligament(ACL)areassessedbytestingtheiractivereproductionofjointposition,in com-parisonwiththecontralaterallimb.
Methods:TwentypatientswithunilateralACLtearingparticipatedinthestudy.Theiractive reproductionofjointpositioninthelimbwiththedeficientACLandinthehealthy con-tralaterallimbwastested.Meta-positionsof20%and50%ofthemaximumjointrangeof motionwereused.Proprioceptiveperformancewasdeterminedthroughthevaluesofthe absoluteerror,variableerrorandconstanterror.
Results:Significantdifferencesinabsoluteerrorwerefoundatbothofthepositions evalu-ated,andinconstanterrorat50%ofthemaximumjointrangeofmotion.
Conclusion: Whenevaluated intermsofabsoluteerror,theproprioceptivedeficit contin-uestobepresentevenwhenanactiveevaluationofthesenseofjointpositionismade. Consequently,thissenseinvolvesactivityofbothintramuscularandtendonreceptors.
©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublishedbyElsevierEditora Ltda.Allrightsreserved.
夽
Pleasecitethisarticleas:CossichV,MallrichF,TitonelliV,deSousaEB,VelasquesB,SallesJI.Déficitproprioceptivoemindivíduoscom rupturaunilateraldoligamentocruzadoanteriorapósaavaliac¸ãoativadosensodeposic¸ãoarticular.RevBrasOrtop.2014;49:607–612. 夽夽
WorkdevelopedinNeuromuscularResearchLaboratory,NationalInstituteofTraumatologyandOrthopedics(INTO),RiodeJaneiro, RJ,Brazil.
∗ Correspondingauthor.
E-mail:[email protected](B.Velasques).
http://dx.doi.org/10.1016/j.rboe.2013.07.003
Déficit
proprioceptivo
em
indivíduos
com
ruptura
unilateral
do
ligamento
cruzado
anterior
após
a
avaliac¸ão
ativa
do
senso
de
posic¸ão
articular
Palavras-chave: LCA
Sistemasomatossensorial Joelho
r
e
s
u
m
o
Objetivo: VerificarseodéficitproprioceptivonoSPApermanecequandopacientescomum membroLCAdeficientesãoavaliadospormeiodotestedereproduc¸ãoativadaposic¸ão articular,emcomparac¸ãocomomembrocontralateral.
Métodos: Participaramdoestudo20pacientescomrupturaunilateraldoLCA.Foifeitoo testedereproduc¸ãoativadaposic¸ãoarticularnomembroLCAdeficienteecontralateral saudável.Foramusadasasposic¸õesmetade20%e50%daamplitudearticularmáxima. Odesempenhoproprioceptivofoideterminadopormeiodosvaloresdeerroabsoluto(EA), errovariável(EV)eerroconstante(EC).
Resultados: Diferenc¸assignificativasforamencontradasparaoEAemambasasposic¸ões avaliadaseparaoECem50%AAM.
Conclusão: OdéficitproprioceptivoquandoavaliadopeloEApermanecemesmoquandoa avaliac¸ãodosensodeposic¸ãoarticularéativae,consequentemente,envolveaatividadede receptoresintramuscularesetendíneos.
©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublicadoporElsevier EditoraLtda.Todososdireitosreservados.
Introduction
Appropriatekinematicsforthekneedependonthe mechan-icalstability of the joint that is providedby its static and dynamiccomponents.1,2 Theligaments furnishstatic
stabi-lization and their main function isto enable normaljoint kinematicsandpreventabnormalandrotationalmovements thatcoulddamagethejointsurfaces,2whiledynamic
stabi-lizationisgivenbycoordinatedmusclecontraction activity modulated by the neuromuscular system.3,4 This system
requiresproprioceptiveinformationfromthejoint kinesthe-sia and position5–7 and from the force developed by the
muscles.8–10
Thisinformationis obtainedthrough acquiringafferent signals from the peripheral mechanical receptors that are foundinthemuscles,tendons,ligaments,jointcapsulesand skin.11Mechanicalreceptorshavealsobeenidentifiedinthe
anteriorcruciateligament(ACL)12anditisbelievedthatthese
contributetowardproprioceptionofthejoint.13,14Thus,
tear-ingoftheACLwouldleadtojointinstabilitynotonlybecause oftheimpairmentduetothemechanicalrestrictionbutalso becauseproprioceptionisdisturbed14,15 andthecapacityof
themusclesactingonthekneetorespondadequatelytothe loadsappliedisdiminished.15,16
Proprioceptive deficits have been observed in patients with ACL tearing and have been correlated with reduced functionalcapacity.7,17Thesedeficitshavebeenidentifiedin
relationtothepassivemovementdetectionthreshold(PMDT) and joint positionsense (JPS),in comparison with normal individuals18,19 and withthehealthy contralaterallimb.19,20
Assessmentsof PMDT and passive JPShave been adopted preferentiallyforuseinstudies.18,21,22Thispracticeisbased
on the assumption that the low angular velocities used wouldspecificallystimulatethereceptorsofthecapsuleand ligament structures without stimulating the intramuscular andtendonreceptors.In theseprocedures,the individuals’
voluntary muscle activity is not involved. However, under normal conditions ofhumanmovement, voluntarymuscle activityisalwayspresent.
There islittle evidenceto demonstratethat propriocep-tivedeficits,inthe wayinwhichthey areassessed, would adverselyaffect patientswithinsufficiencyoftheACL ora surgicallyreconstructedACL.22Thus,proceduresthatinvolve
voluntary muscle action and consequently stimulation of the muscle-tendon receptors should receive greater atten-tion inevaluationson proprioception.JPSassessmentwith active positioning and reproduction may be an option for investigating proprioceptive capacity in a more functional manner. Thus,thepresent studyhad theaimof ascertain-ingwhethertheproprioceptivedeficitregardingJPScontinues whenpatientswithadeficientACLareevaluatedbymeansof atestonactivereproductionofjointposition,incomparison withthehealthycontralaterallimb.
Materials
and
methods
Subjects
Table1–Clinicalexaminations.
Lachmanandanteriordrawer
− +/+++ ++/+++ +++/+++
Lachman 5 13 2 0
Anteriordrawer 0 7 13 0
McMurrayandpivot
− +
Bocejo 1 19
Pivot 12 8
sameorthopedist(Table1).Thisstudywasapprovedbythe localethicscommitteeandthesubjectswereinformedabout theobjectivesand proceduresthroughafreeandinformed consentstatement,inaccordancewithResolution196/96of theNationalHealthCouncil.
Assessmentofjointpositionsense
Instrument
Anisokineticdynamometer(CSMI,HumacNorm)wasusedin alltheprocedures.
Positioning
Thesubjectswerepositionedseated,withthelateralcondyle ofthefemuralignedwiththeaxisofrotationoftheapparatus andtheanklefixedtoanaccessoryrodforkneeevaluation,by meansofaVelcrostrip(Fig.1).Carewastakentopositionthe poplitealfossaawayfromthelimitoftheseat,soastoenable completejointmovementandminimizeskinstimulationin thisregion.Theprecisionoftheanglemeasurementswas1◦.
Maximumjointamplitude
TheMJAoftheflexion–extensionmovementwasdetermined bymeasuringtheamplitudebetweenthemaximumextension (0◦)andthemaximumflexionoftheknee.
Jointpositionreproductiontest
Thesubjectswererequiredtoexperienceandthenreproduce jointpositions,inbothcasesthroughvoluntarymovements. Thecommandsforcarryingoutthetaskwereissuedverbally bytheevaluatorandthedirectionofmovementwasfrom flex-iontoextension.Twotargetpositionstobeexperiencedwere used:20%and50%oftheMJA(0%=maximumextension).Both limbswereevaluatedandtheorderofassessmentwas cho-senrandomly.Throughouttheprocedure,thepatientswere blindfolded.Variationsof±5◦aroundthetargetpositionwere allowed.Whenthesubjectviolatedthismargin,theattempt wasdiscarded.Fiveattemptsineachtargetpositionwere per-formed(10intotal).
Determinationoftheindividualerrorandcalculationof theproprioceptiveacuity
The individual error value for each attempt made was determined through the difference between the position reproducedandthepositionexperienced.Theproprioceptive performancewasdeterminedbymeansofthevaluesofthe absoluteerror(AE),variableerror(VE)andconstanterror(CE).
Fig.1–Subjectpositionedintheisokineticdynamometer toperformthejointpositionreproductiontest(sensingof position).
SchmidtandLee23describedthecalculationofeachvariable
indetail.Briefly,theAEisobtainedthroughthearithmetic meanoftheindividualerrorsinthemodulusanddetermines theindividual’saccuracyinreproducingtheposition;theVE isthestandarddeviationoftheindividualerrorsand deter-minestheconsistencyofthereproductionsmade;andtheCE isthearithmeticmeanoftheindividualerrorswiththeirsigns anddeterminesthetendencyforthepositiontobereproduced aboveorbelowthetarget(bias).
Statistical
analysis
Subjects
−16−14−12−10 −8 −6 −4 −2 0 2 4 6 8 10 12 14 16 0
2 4 6 8 10 12 14 16 18 20
Individual error (°)
Fig.2–Distributionoftheindividualerrorsinthejoint positionreproductiontest:20%MJA.Blackcirclesreferto thelimbwiththedeficientACLandwhitecirclestothe controllimb.Thecontinuouslinerepresentsthetarget positiongraphically.
Results
Timeofinjury,causeofinjuryandassociatedlesions
The mean time that elapsed until the data-gathering was 3.7±1.2years.Theinjuriesmostlyoccurredduetosprainsin situationsofday-to-daylife(45%),injuriesnotinvolving con-tactinrecreationalsoccer(35%),falls(15%)andcaraccidents (5%).Associatedlesionswereseen in14 patients:13inthe medialmeniscusandonlyoneinthelateralmeniscus.
MJA,20%MJA,50%MJAandpositionsexperienced
Themaximum joint amplitude determined forthe ACL of theaffectedlimbwas105.3◦±11.8◦andforthecontrollimb, 111.2◦±10.2◦.ThetargetpositionscalculatedfortheACLat 20%and 50%MJA were 21.1◦±2.4◦ and52.6◦±5.9◦, respec-tively.Thetargetpositionedcalculatedforthecontrolat20% and50% MJAwere 22.2◦
±2.0◦ and55.6◦
±5.1◦,respectively. Thepositionsexperiencedthatwereusedinthejointposition reproductiontestwere0.3◦±3.8◦and50.5◦±7.2◦fortheACL oftheaffectedlimb,whilethesepositionsinthecontrolwere 21.1◦
±3.0◦and52.4◦
±5.9◦.
Individualerrors
Thevaluesdeterminedfortheindividualerrorsare demon-stratedgraphicallyinFigs.2and3.
AE,VEandCE
ThevaluesdeterminedforAE,VEandCEarelistedinTable2. ThelimbwiththeaffectedACLgenerallydemonstratedhigher values(worsevalues).Significantdifferences werefoundin relationtotheAEinboththepositionsevaluatedandin rela-tiontoCEat50%MJA.
Individual error (°)
Subjects
−16−14−12−10 −8 −6 −4 −2 0 2 4 6 8 10 12 14 16 0
2 4 6 8 10 12 14 16 18 20
Fig.3–Distributionoftheindividualerrorsinthejoint positionreproductiontest:50%MJA.Blackcirclesreferto thelimbwiththedeficientACLandwhitecirclestothe controllimb.Thecontinuouslinerepresentsthetarget positiongraphically.
Discussion
Theligamentshavethefunctionofmechanicallyrestricting jointamplitudeandlimitingmovementbymeansofastable arc.1,2Inaddition,theysupplyproprioceptiveinformation24,25
and enabledynamicstabilizationofthejointmodulatedby the neuromuscularsystem.3,4 If thissystem iscomplete,it
allowsappropriatereflexmotorresponsesanddiminishesthe possibility ofoccurrenceofabnormaljointmovements and subluxation.2,16,26
Patients with ACL injuries present proprioceptive deficits18,20 and it has been proposed that these deficits
are responsibleforthefeelingsoffunctionalinstabilityand the falls reported by patients with anterior instability of the knee.27 Proprioception ofthe knee has been evaluated
through passive tests6,28 in which the subjects’ voluntary
muscle action has not been present. The equipment gen-erates passive movement through low angular velocities (approximately0.5◦/s)withtheaimofselectivelyevaluating the capsule and ligament receptors.29 Stimulation of the
intramuscular and tendon receptors occurs continuously duringvoluntarymotoractivities.Therefore,itisimportant
Table2–AE,VEandCEdeterminedfor20%and50% MJA(mean±SD).
AE VE CE
20%MJA
DeficientACL 4.3◦±2.0◦a 3.2◦±2.0◦ −2.2◦±3.3◦ Control 2.9◦±1.3◦ 3.0◦±1.4◦ −0.6◦±1.5◦
50%MJA
DeficientACL 4.2◦±2.1◦a 2.8◦±1.1◦ −3.3◦±3.1◦a
Control 3.5◦±1.3◦ 2.8◦±1.0◦ −1.6◦±2.8◦
toascertainwhetherdeficitsinjointpositionsensecontinue tobepresentwhenanactivemethodfortestingJPSisused.
Inthisstudy,weevaluatedJPSinpatientswithunilateral ACLinjuriesbyusinganisokineticdynamometerwithactive measurementsat20%and50%ofthemaximumjoint ampli-tude.Itwas decidedtouse percentages ofMJA,instead of absolutevalues, inorder to beable tomake relative com-parisonsbetweenthesubjects.30Significantdifferenceswere
foundatboththepositions,usingAEfortheevaluation,and thisdemonstratesthatlimbswithadeficientACLhavelower accuracyinreproducingjointpositions,incomparisonwith thehealthycontralaterallimb.Carteretal.20evaluatedJPSin
50patients withunilateralACLinjuriesusinganisokinetic dynamometerandfoundsignificantlydifferentAEbetween theinjured and controllimbs(9.42◦±3.14◦ and7.1◦±2.32◦, respectively),therebycorroboratingtheresultsofLeeetal.19
Nosignificantdifferences relatingtoVE were identified, whichdemonstratesthattheindividualspresentedthesame consistenciesinreproducingjointpositions,independentof theinjury.TheCEdeterminedforboththelimbwiththe defi-cient ACL and the healthy contralateral limb had negative values(repositioning ofthelimbbelowthetargetposition). Thisbehaviorhasalsobeenidentifiedbyourgroupin indi-vidualswhowerefreefromorthopedicinjuries(unpublished data).Inthepresentstudy,onlytheCEof50%MJAreacheda statisticaldifference.However,fromthemethodsapplied,it wasnotpossibletoobtainaphysiologicalresponseforthis behavior.VE and CEvaluesare notcommonly usedinthe literature,whichimpedescomparisonoftheresults.
Conclusion
Whentheproprioceptivedeficitisevaluatedbymeansofthe AE,itcontinuesevenwhentheassessmentofjointposition sense is active. Consequently, this involves activity of the intramuscularand tendonreceptors. Future studiesshould includecalculationofthevariableerrorandconstanterror,so astomakeitpossibletocomparetheresultsandthusexpand knowledgeofthebehaviorofthesevariables.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
r
e
f
e
r
e
n
c
e
s
1. BarrettDS.Proprioceptionfunctionafteranteriorcruciate
reconstruction.JBoneJointSurgBr.1991;73(5):833–7.
2. BeynnonBD,JohnsonRJ,CoughlinKM.Relevant
biomechanicsoftheknee.In:DeLeeJC,DrezD,MillerMD,
editors.Orthopaedicsportsmedicine.2003.p.577–1595.
3. RiemannBL,LephartSM.Thesensorimotorsystem,partI:
thephysiologicbasisoffunctionaljointstability.JAthlTrain.
2002;37(1):71–9.
4. RiemannBL,LephartSM.Thesensorimotorsystem,partII:
theroleofproprioceptioninmotorcontrolandfunctional
jointstability.JAthlTrain.2002;37(1):80–4.
5. SallesJI,CossichVRA,AmaralMV,MonteiroMT,CagyM,
MottaG,etal.Electrophysiologicalcorrelatesofthethreshold
todetectionofpassivemotion:aninvestigationin
professionalvolleyballathleteswithandwithoutatrophyof
theinfraspinatusmuscle.BioMedResInt.2013;2013:634891.
6.FremereyRW,LobenhofferP,ZeichenJ,SkutekM,BoschU,
TscherneH.Proprioceptionafterrehabilitationand
reconstructioninkneewithdeficiencyoftheanterior
cruciateligament.JBoneJointSurgBr.2000;82(6):
801–6.
7.PapG,MachnerA,NebelungW,AwiscusF.Detailedanalysis
ofproprioceptioninnormalandACL-deficientknees.JBone
JointSurgBr.1999;81(5):764–8.
8.HérouxME,TremblayF.Weightdiscriminationafteranterior
cruciateligamentinjury:apilotstudy.ArchPhysMed
Rehabil.2005;86(7):1362–8.
9.TremblayF,EstephanL,LegendreM,SulpherS.Influenceof
localcoolingonproprioceptiveacuityinthequadriceps.J
AthlTrain.2001;36(2):119–23.
10.TorresR,VasquesJ,DuarteJA,CabriJM.Kneeproprioception
afterexercise-inducedmuscledamage.IntJSportsMed.
2010;31(6):410–5.
11.MyersJB,WassingerCA,LephartSM.Sensoriomotor
contributiontoshoulderstability:effectofinjuryand
rehabilitation.ManTher.2006;11(3):197–201.
12.JohanssonH.Roleofkneeligamentsinproprioceptionand
regulationofmusclestiffness.JElectromyogrKinesiol.
1991;1(3):158–79.
13.CashRM,GonzalezMH,GarstJ,BarmadaR,SternSH.
Proprioceptionafterarthroplasty.ClinOrthopRelatRes.
1996:172–8.
14.DhillonMS,BaliK,VasisthaRK.Immunohistological
evaluationofproprioceptivepotentialoftheresidualstump
ofinjuredanteriorcruciateligaments.IntOrthop.
2010;34(5):737–41.
15.BeynnonBD,RyderSH,KonradsennL,JohnsonRJ,JohnsonK,
RenstromPA.Theeffectofanteriorcruciateligamenttrauma
andbracingonkneeproprioception.AmJSportsMed.
1999;27(2):150–5.
16.SolomonowM,KrogsgaardM.Sensorimotorcontrolofknee
stability.Areview.ScandJMedSciSports.2001;11(2):64–80.
17.ArockiarajJ,KorulaRJ,OommenAT,DecasahayamS,
WankharS,VelkumarS,etal.Proprioceptivechangesinthe
contralateralkneejointfollowinganteriorcruciateinjury.
BoneJointJ.2013;95-B(2):188–91.
18.CorriganJP,CashmanWF,BradyMP.Proprioceptioninthe
cruciatedeficientknee.JBoneJointSurgBr.1992;74(5):247–50.
19.LeeHM,ChengCK,LiauJJ.Correlationbetween
proprioception,musclestrength,kneelaxity,anddynamic
standingbalanceinpatientswithchronicanteriorcruciate
ligamentdeficiency.Knee.2009;16(5):387–91.
20.CarterND,JenkinsonTR,WilsonD,JonesDW,TorodeAS.Joint
positionsenseandrehabilitationintheanteriorcruciate
ligamentdeficientknee.BrJSportsMed.1997;31(3):209–12.
21.ReiderB,ArcandMA,DiehlLH,MroczeckK,AbulenciaA,
StroudCC,etal.Proprioceptionofthekneebeforeandafter
anteriorcruciateligamentreconstruction.Arthroscopy.
2003;19(1):2–12.
22.GokelerA,BenjaminseA,HewettTE,LephartSM,Engebretsen
L,AgebergE,etal.ProprioceptivedeficitsafterACLinjury:are
theyclinicallyrelevant?BrJSportsMed.2012;46(3):180–92.
23.SchmidtR,LeeT.Motorcontrolandlearning:abehavioral
emphasis.5thed.HumanKinetics;2011.
24.AdachiN,OchiM,UchioY,IwasaJ,RyokeK,KuriwakaM.
Mechanoreceptorsintheanteriorcruciateligament
contributetothejointpositionsense.ActaOrthopScand.
2002;73(3):330–4.
25.SchutteMJ,DabeziesEJ,ZimnyML,HappelLT.Neural
anatomyofthehumananteriorcruciateligament.JBone
26.IwasaJ,OchiM,UchioY,AdachiN,KawasakiK.Decreasein
anteriorkneelaxitybyelectricalstimulationofnormaland
reconstructedanteriorcruciateligaments.JBoneJointSurg.
2006;88(4):477–83.
27.IngersollD,GrindstaffTL,PietrosinomeBG,HartJM.
Neuromuscularconsequencesofanteriorcruciateligament
injury.ClinSportsMed.2008;27(3):383–404.
28.BorsaPA,LephartSM,IrrgangJJ,SafranMR,FuFH.Theeffects
ofjointpositionanddirectionofjointmotionon
proprioceptivesensibilityinanteriorcruciate
ligament-deficientathletes.AmJSportsMed.
1997;25(3):336–40.
29.RiemannBL,MyersJB,LephartSM.Sensorimotorsystem
measurementtechniques.JAthlTrain.2002;37(1):85–98.
30.JanwantanakulP,MagareyME,JonesMA,DaniseBR.Variation
inshoulderpositionsenseatmidandextremerangeof