w w w . r b o . o r g . b r
Original
Article
Neuromuscular
efficiency
of
the
vastus
lateralis
and
biceps
femoris
muscles
in
individuals
with
anterior
cruciate
ligament
injuries
夽
Fernando
Amâncio
Aragão
a,b,∗,
Gabriel
Santo
Schäfer
c,
Carlos
Eduardo
de
Albuquerque
a,
Rogério
Fonseca
Vituri
a,
Fábio
Mícolis
de
Azevedo
d,
Gladson
Ricardo
Flor
Bertolini
aaUniversidadeEstadualdoOestedoParaná,Cascavel,PR,Brazil
bLaboratóriodePesquisadoMovimentoHumano(LAPEMH),CascavelPRBrazil
cHospitaldeClínicas,UniversidadeFederaldoParaná(UFPR),Curitiba,PR,Brazil
dLaboratoryofBiomechanicsandMotorControl,SchoolofSciencesandTechnology(FCT),UniversidadeEstadualPaulista“Júliode
MesquitaFilho”(UNESP),PresidentePrudente,SP,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory: Received20May2013 Accepted11March2014 Availableonline7April2015
Keywords:
Anteriorcruciateligament Musclefatigue
Biomechanics
a
b
s
t
r
a
c
t
Objective:Toanalyzestrengthandintegratedelectromyography(IEMG)datainorderto deter-minetheneuromuscularefficiency(NME)ofthevastuslateralis(VL)andbicepsfemoris(BF) musclesinpatientswithanteriorcruciateligament(ACL)injuries,duringthepreoperative andpostoperativeperiods;andtocomparetheinjuredlimbatthesetwotimes,usingthe non-operatedlimbasacontrol.
Methods:EMGdataandBFandVLstrength datawerecollected duringthreemaximum isometriccontractionsinkneeflexionandextensionmovements.Theassessmentprotocol wasappliedbeforetheoperationandtwomonthsaftertheoperation,andtheNMEofthe BFandVLmuscleswasobtained.
Results:TherewasnodifferenceintheNMEoftheVLmusclefrombeforetoafterthe oper-ation.Ontheotherhand,theNMEoftheBFinthenon-operatedlimbwasfoundtohave increased,twomonthsafterthesurgery.
Conclusions:TheNMEprovidesagoodestimateofmusclefunctionbecauseitisdirectly relatedtomusclestrengthandcapacityforactivation.However,theresultsindicatedthat twomonthsaftertheACLreconstructionprocedure,atthetimewhenloadingintheopen kineticchainwithinrehabilitationprotocolsisusuallystarted,theneuromuscularefficiency oftheVLandBFhadstillnotbeenreestablished.
©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublishedbyElsevierEditora Ltda.Allrightsreserved.
夽
WorkdevelopedjointlybytheHospitalUniversitáriodoOestedoParaná(HUOP),LaboratóriodePesquisadoMovimentoHumano (LAPEMH)andUniversidadeEstadualdoOestedoParaná(UNIOESTE),CascavelCampus,Cascavel,PR,Brazil.
∗ Correspondingauthor.
E-mail:feraaragao@gmail.com(F.A.Aragão). http://dx.doi.org/10.1016/j.rboe.2015.03.010
Eficiência
neuromuscular
dos
músculos
vasto
lateral
e
bíceps
femoral
em
indivíduos
com
lesão
de
ligamento
cruzado
anterior
Palavraschave:
Ligamentocruzadoanterior Fadigamuscular
Biomecânica
r
e
s
u
m
o
Objetivo:Analisaraforc¸aeaintegraldaeletromiografia(IEMG)paraobteraeficiência neuro-muscular(ENM)dosmúsculosvastolateral(VL)ebícepsfemoral(BF)empacientescomlesão deligamentocruzadoanterior(LCA)nasfasespré-operatóriaepós-operatória,compararo membrolesionadonosdoismomentoseusaromembronãocirúrgicocomocontrole. Métodos: FoifeitaacoletadedadosdaEMGedaforc¸adeBFeVLdurantetrêscontrac¸ões isométricasmáximas nosmovimentos de flexãoe extensãodo joelho.Oprotocolo de avaliac¸ãofoiaplicadonosmomentospréepós-operatório(doismesesapósacirurgia)e obteve-seaENMdosmúsculosVLeBF.
Resultados: Nãofoiencontradadiferenc¸anaENMdomúsculoVLentreosmomentosprée pós-cirúrgico.Poroutrolado,houveaumentodaENMdoBFnomembronãocirúrgicodois mesesapósacirurgia.
Conclusões: AENMforneceboaestimativadafunc¸ãomuscularporestardiretamente rela-cionadaàforc¸aeàcapacidadedeativac¸ãodosmúsculos.Entretanto,osresultadosapontam quedoismesesapósoprocedimentodereconstruc¸ãodoLCA,quandonormalmentesão iniciadascargasemcadeiacinéticaabertanosprotocolosdereabilitac¸ão,aeficiência neu-romusculardoVLeBFaindanãoestárestabelecida.
©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublicadoporElsevier EditoraLtda.Todososdireitosreservados.
Introduction
Theanteriorcruciateligament(ACL)isoneofthemost impor-tantstructuresforstabilizingthekneejointandisoneofthe mostfrequently injuredligamentsduringsportsactivities.1
ACLinjurycausesgreatincapacityforthelimbandalsosome long-termproblemssuchasosteoarthritis.2Evenafter
surgi-calreconstructionandrehabilitation,significantdeficitsmay remain,forexampleinrelationtothekneeextensorandflexor musclestrength.3
Muscle weakness subsequent to ACL injury generates imbalancesbetweenagonistandantagonistmusclesduring knee flexion and extension movements.These imbalances oftencausedifficultyinrehabilitationforindividuals undergo-ingACLreconstructionprocedures.Thepersistentasymmetry inthetorqueratiobetweenkneeextensorsandflexorsthat isobserved in this situation has shown that it is of great importancetoattempttoidentifyandreversethecausesof persistentmuscle weakness subsequent toACL injury and reconstruction.4
Several factors need to be taken into consideration in relationtorecoveryofknee flexionand extensionstrength subsequenttoACLinjury.Themostimportantofthesefactors relatetomusclearchitectureandtheintegrityoftheoriginand insertionofthemuscles,alongwiththeefficacyoftheneural activitythatarrivesatthemotorplate.5,6
Neuralfactorsrelateparticularlytotheefficacyof activa-tionofthemotorunitsduringmusclecontraction.Itisknown thatthegreaterthenumberofmotorunitsrecruitedthrough astimulusis,thegreatertheresultantmusclegeneratedwill alsobe.7Biomechanically,neuromuscularefficiencyis
calcu-latedthroughtherelationshipbetweentheamountofneural
stimulus and the capacity to generateforce that a muscle has.8
Thus,therelationshipbetweenthemuscleforcemoment andtheintegratedelectromyographicsignal(IEMG),whichis considered tobethebestvariable fordescribingthe inten-sity of the neuromuscular effect during sustained muscle activity,hasbeenusedtoestimateneuromuscularefficiency (NME).9–11Thiscanbeinterpretedasanindividual’scapacity
togenerateaforcemomentinrelationtohislevelofmuscle activation.8 Nonetheless,studiesinvolvingmuscle
architec-tureandelectromyographicanalysishavedemonstratedthat results from the vastus lateralis (VL) and biceps femoris (BF) muscles are easier to measure and, especially, more reproducibleinrelation totheiragonists,12,13 whichmakes
these muscles appropriate representatives of the behavior of the knee extensor and flexor muscle groups, respec-tively.
The return to normal or to sports activities after ACL reconstructionusuallytakesplaceafterthesixth postopera-tivemonth.14However,patientsstarttobearweightinopen
kinetic chain exercises and to subject the ACL to greater tensiongenerallyafterthesixthpostoperativeweekin accel-eratedprotocolsandafterthetwelfthpostoperativeweekin conservativeprotocols.14,15Despitethis,notmuchdataexists
regardingthestateofneuromuscularefficiencyatthisstage oftherehabilitation.
Materials
and
methods
Thesamplewascomposedof12maleindividualsofmeanage 29.27±6.90year whopresentedunilateralACLinjuriesand who,afterthepreoperativeevaluation,underwentasurgical proceduretoreconstructtheACL,followedbyphysiotherapy. Thesurgicalprocedureswereperformedbythesame orthope-dists,usingthetendonsfromthesemitendinosusandgracilis musclesasgrafts,fixedinthefemurbymeansoftheRigidfix® systemandinthetibiausingabsorbableinterferencescrews, foralltheindividuals.Thisstudywasapprovedbeforehand bythelocalethicscommittee,inaccordancewithreportno. 155/2012-CEP(CAAE06519712.4.0000.0107).
Aftertheoperation,thepatientswerefollowedupby spe-cialistphysiotherapists,withperiodic60-minsessionstwicea week,fromthetimeofhospitaldischargeuntilthetwo-month reassessment.
Assessmentprotocol
The assessment protocol was carried out just before the operationandtwomonthsafterthesurgicalprocedure.The data-gatheringinrelationtomusclestrengthand electromyo-graphy(EMG)wasdonebilaterally.
Thestrength evaluationswereperformedatthe Labora-toryofHumanMovementResearch(LAPEMH)ofthePhysical RehabilitationCenter(CRF)oftheStateUniversityoftheWest ofParaná (UNIOESTE).Astructureappropriateforthis pur-posewasused. Thesubjectwasseated onahighextensor tablewiththehipflexedat90◦,withoutcontactbetweenthe poplitealfossaandthetableand/orcontactbetweenthelower limbsandthefloor.Afterthepatienthadbeenproperly pos-itioned,aloadcellof200kgfcoupledtothelaboratorywall wasfittedtothepatient’sanklebymeansofanon-extendable ankleband,insuchawaythattheforcevectorwasalways exertedat0◦ inrelationtotheaxisoftheloadcell.Inthis position,inwhichtherewasrestrictionofkneemovement, thepatientwasinstructedtoperformaseriesofmaximum voluntaryisometriccontractions(MVICs).
WhileperformingtheMVICs,withkneeflexionand exten-sion,thejointwaspositionedflexedat60◦(0◦=totalextension oftheknee).Thepositionofthekneewasdeterminedwith theaidofafleximeterandallthetestswererecordedusinga conventionalvideocamera(Panasonic,NV-GS180),positioned perpendicularlyatadistanceof1.5m,inalignmentwiththe intercondylarfossaoftheknee,inordertoobtainimagesof thelowerlimbsinthesagittalplaneduringtheMVICs.
Todeterminethekneejointangleontherecordedimages, three markers of diameter 5mm were fixed to the lower limbsbeforethecontractionswereperformed:onthegreater trochanterofthefemur,kneejointinterlineandlateral malle-olusoftheankle.Thevideodataweregatheredat30Hzusing theVirtualDubsoftware(v.0.9.11).Inordertopreciselyassess the real joint position, the Kinovea software(v.0.8.15) was used.
Three repetitions ofthe MVICswere performed ineach openkineticchainexercise.Thecontractionwasmaintained for 5s, with resting periods of 120s, in each direction of movement(extensionandflexion).Inalltheevaluations,the
researchersgaveverbalencouragementcommandsinorder tostimulatethepatientsduringtheisometriccontraction.
The analog data relating to EMG and strength were obtainedusinga12-channelbiologicaldata-gatheringsystem (BioEMG1100,Lynx,Brazil),bymeansoftheAqDadossoftware (Lynx AqDadosv.7.2),whichalsohadachannelcontaining datafromalightsynchronizationsystemthatwasalso gath-eredbythevideocamera,inordertoidentifythetimeatwhich thepeakforcewasattained.InpreparationforgatheringEMG data,thepatient’s skinwasshavedandthen cleanedusing 70% alcohol.TheEMGdataweregatheredusingdisposable surfaceelectrodespositionedonthebelliesofthevastus lat-eralis(VL)andbicepsfemoris(BF)muscles,inabipolarlayout.
Dataanalysis
ToobtaintheEMGdata,theintervalwaslimitedto0.25sbefore andafterthepeakforce.Followingthis,thesignalswere recti-fiedandfiltered(third-orderButterworthbandpassfilterfrom 10to500Hz)inordertoobtainedtheintegratedEMG(IEMG) signalvaluesfortheVLandBFmusclesinthetimedomain overthe0.5sinterval,onlyfortheMVICinwhichthe great-est peakofisometricforceoccurred inknee extensionand flexion.ThesignalsgatheredwereprocessedintheMatLab® environment(Mathworks,USA).
Thedataobtainedinrelationtomusclestrengthwere nor-malizedsoastoobtainamathematicalprojectionofgreater reliabilityfortheforceexertedindividuallybytheVLandBF muscles.Forthis,thecriterionoftheequivalentpercentage contributionofthesemusclesinrelationtothetotal physi-ologicalcross-sectionalareaoftherespectivemusclegroups wasused.Thus,theproportionsof36%fortheVLand40%for theBFwereusedasthebasisfortheentirekneeextensorand flexormusclegroup(100%),respectively.Thesepercentages followed thepatterndescribed inaninvivostudyinwhich the individuals inthe samplepresented mean age, height and weightsimilartothoseofthepatientsselectedforthe presentsample.16Subsequently,themuscleforcewasdivided
toobtain50%oftheMVICandtheNMEoftheVLandBF mus-cleswascalculatedusingtheratioofstrength/IEMG,at50% oftheMVIC.Thisconceptstartedfromtheassumptionthat atsubmaximalcontractionsofupto50%,therelationshipof forceversusEMGwasconstant.17
Statisticalanalysis
Forthestatisticalanalysis,theShapiro–Wilktestwasusedto identifythenormalityofthevariables.Theindependent Stu-dent’sttestwasusedtoidentifydifferencesinforce,IEMG andNME betweentheinjuredand uninjuredlimbsandthe pairedStudent’sttestwasusedtocomparevariablesbetween beforeandaftertheoperation(twomonthspostoperatively). Thesignificancelimitwasestablishedasp=0.05.
Results
Table1–Meansandstandarddeviationsofthekneejointangle,recordedduringtheMVICsatthepreoperativeand postoperativestages.Nosignificantdifferenceswerefound.
Limb Preoperative Postoperative
Extension Flexion Extension Flexion
Operated 52.44±5.6 65.9±8.8 53.1±7.9 64.9±6.7
Non-operated 52.49±5.0 65.2±7.3 51.6±6.8 62.8±8.4
Source:Thepresentauthors.
relationtothepositioningduringtheMVICsinextensionand flexion(Table1).
Takingkneeflexionmovementsasthereference,in com-paringfrom beforetoafterthe operation,it was seenthat thelimbthatunderwentsurgicalrepairpresentedsignificant decreasesinIEMGandinBFmusclestrength(Table2a,b).On the other hand,in the non-operatedlimb, whilethe IEMG decreased,themagnitudeoftheBFstrengthwasmaintained (Table2c).
FortheVLmuscle,comparingthetwotimes,althoughthe operatedlimbpresenteddiminishedmusclestrengthafterthe ACLreconstruction(Table2d),themagnitudeoftheIEMGdid notchange. Inrelationtothenon-operatedlimb,no differ-enceswerefoundincomparingthesituationsbeforeandafter thesurgery.
Bothbeforeand afterthe operation,thestrength ofthe BFandVLmuscleswasdiminishedintheoperatedlimb,in comparisonwiththeotherlimb(Table2e–h).
ItwasfoundthattheNMEoftheBFinthenon-operated limb increased from before to after the operation (Fig. 1). Moreover,itcouldbeseenthattheNMEoftheBFinthe non-operatedlimbhadincreasedinrelationtotheoperatedlimb, attheevaluationtwomonthsaftertheoperation.However,no differenceinrelationtotheNMEoftheVLwasfound.
Discussion
Neuromuscularefficiencyisrelatedtomusclefiberactivation andproductionofforcebyagivenmuscle.Thus,individuals whoarecapableofproducinggreatermuscleforcewithlower magnitudeof muscle fiber activation are considered to be moreefficient.18Inthepresentstudy,itwassoughttomeasure
musclestrengthandIEMG,inordertodeterminethe neuro-muscularefficiencyoftheVLandBFmusclesinpatientswith ACLinjuries,bothbeforeandaftertheoperation.
0 0.005 0.01 0.015 0.02 0.025 0.03
Operated Non-operated Operated Non-operated
Biceps femoris Vastus lateralis
NME (kg/mV.10
3)
Neuromuscular efficiency
Before
After
* *
The asterisks denote the significant differences that were found (*P<0.05)
Fig.1–Meansandstandarddeviationsofthe
neuromuscularefficiency(NME)oftheBFandVLmusclesat thetwotimesevaluated.Theasterisksdenotethe
significantdifferencesthatwerefound(*p<0.05).
Afterthe surgicalprocedure, these patientsmay havea tendencytoprotecttheoperatedlimb,throughlimitingtheir movementofitandtheweightbornebyit.Thismayleadto atrophyandweaknessoftheanteriorandposterior muscula-tureofthethigh.Gerberetal.,19observedatrophyandthatthe
quadricepsand bicepsfemorismusclestrength had dimin-ishedby20%and30%,respectively,threemonthsafterACL reconstruction,eventhoughthepatientswereundergoinga rehabilitationprocess.Theirdatacorroboratethefindingsof the present study,in relationto the strength and IEMGof the BFmuscle oftheoperated limb,giventhatdiminished strengthandneuralrecruitmentwereobservedafterthe surgi-calprocedure.Thiswaspossiblybecauseatthepostoperative
Table2–Meansandstandarddeviationsoftheintegratedelectromyography(IEMG)valuesinmV/secandestimated forceinkgf,exertedbytheBFandVLduringkneeflexionandextension,respectively.
Limb Operated Non-operated
Variable IEMG Forcea IEMG Force
BF Preoperative 1077.56±1004.64a 5.66±1.77b,e 977.84±531.23c 6.23±1.56e
Postoperative 588.78±246.79a 4.00±1.06b,f 708.40±354.84c 6.87±1.57h,f
VL Preoperative 912.61±714.11 10.41±4.27d,g 1028.77±734.34 11.50±2.15g
Postoperative 749.63±430.92 8.70±3.29d,h 840.59±415.51 11.23±2.35h
Source:Thepresentauthors.
evaluationperformedtwomonthsafterthe surgical recon-struction of the ligament, the joint was still healing and presentedweaknessandmuscleinhibition.
Forthenon-operatedlimb,comparingthepreand post-operativedata,itwasseenthattheelectricalactivity(IEMG) ofthe BFmuscle alsodecreased, althoughwithout change tothemusclestrength.Eventhoughthemethodologyused didnotallowdirectmeasurement, itcanbesupposedthat thisresultwasduetothelearnedeffectcausedbythetests performed and alsodue to the greatuse ofthe limb con-tralateraltotheinjuryafterthesurgicalprocedure,giventhat patientsaregenerallyafraidofapplyingforce,thus offload-ing weightfrom the operatedlimband avoiding movingit aftertheprocedure.20Moreover,thedecreaseinIEMG
with-outchangetothestrengthoftheBFwasresponsibleforthe increaseinitsNME.Thiseffectwasprobablyrelatedtothe muscledemandonthecontralaterallimbgeneratedthrough excessiveuse.
However,thiswasnotshowntobevalidfortheVLmuscle, giventhatnodifferencesinthevariablesstudiedwerefound. Thisfinding,inacertainmanner,denotesthattheVLmuscle onthenon-operatedsidewasnotgreatlyinfluencedbythe surgicalprocedureorbythephysiotherapeuticrehabilitation process.
Itisimportanttoemphasizethatthegraftused(fromthe semitendinosusandgracilis)istheonemostcommonlyused inBrazil.However,the functional resultspresented donot seemtodifferfromthosefromthemiddleportionofthe patel-lartendon.21
Themuscleforceproducedisdependentonthejointangle, accordingtotheforce–lengthrelationship.Specificallyin rela-tiontotheknee,ithasbeenwellestablishedthattheoptimum angleforforceproductioniscloseto60◦.22Fromtheimages
recordedwhiletheMVICswerebeingperformed,itwas cer-tainthat therewerenosignificant differencesbetweenthe jointangles,eitherinrelationtomovementorinrelationto theassessmenttime(beforeoraftertheoperation).
Neuromuscular alterations subsequent to an injury are representative of a complex clinical state, which may be manifestedthroughthepresenceofmuscleinhibitioninthe uninjuredmusculaturearoundthecompromisedjoint.23This
neuralresponsehastwomajorphysiologicalpurposes:(1)to diminishtheloadaroundtheinjuredjoint,soastopromote protectionagainstnewinjuries;24and(2)toprovide
compen-satorymotorstrategies,soastomaintainthefunctionsofthe limbinthepresenceofmuscleinhibition.25
These arguments might explain the data found in the presentstudy,withregardtothecomparisonmadebetween thepreandpostoperativestagesoftheVLmuscleinthe oper-atedlimb,inwhichtherewasadecreaseinmusclestrength withoutanysignificantchangetotheIEMG.Thisresultwas possiblyduetothepresenceofmuscleinhibition,withthe aimofsparingthejointandavoidingearlyrecurrenceofthe injury.26
Likewise,itiswellknownthatACLinjuriesareassociated withpoorneuromuscularcontrol,whichleadstodiminution oftheproprioceptive informationasafunctionofchanges to the efficiency of the mechanical receptors responsible forneuromuscularcontrol,27disturbancesofthe
somatosen-sorysystem28anddecreasedmuscleactivationandforce.29
According to Hewett et al.,30 coordinated coactivation of
the hamstrings and quadriceps has an important role in decreasingtheriskofprimaryinjury.Thisagonist–antagonist balance may protect the knee against recurrent injury to thereconstructedACL.Thesephysiopathologicalindications wouldexplainthefindingsofthepresentstudywithregardto comparisonsbetweenthelimbwithACLinjuryandthesound limb.
Since the postoperativeevaluation ofthe present study wasmadeonlytwomonthsafterthesurgicalprocedure,the limbwasstillundergoingrecovery.Thiscouldbeseenfrom thelowermusclestrengthfoundincomparingthelimbs ana-lyzed.Itwasdecidedtomakeevaluationstwomonthsafter the surgicalprocedureinordertoobtain indicationsofthe stateofneuromuscularefficiencyofthesemusclegroupsat theaveragetimewhenopenkineticchainexerciseprocedures arestartedinmostrehabilitationprotocols.14,15Nonetheless,
onelimitationofthepresentstudyispreciselythelackof eval-uationofthesubjectsaftersixmonths,causedbythelarge lossofsubjectsthatoccurredbeyondthesecondpostoperative month.Hence,itisrecommendedthatfuturestudiesshould evaluateNMEconditionsafterthistime.
Lastly,theresultsreportedhereemphasizethe complex-ity oftheprocessoffunctionalrecoveryofknee jointsthat undergoACLreconstructionandrehabilitation,andtheneed to beattentive towardrecovery ofthe neuromuscular effi-ciencyofthemusclesinvolvedinthejoint,beforeactivities atmorevigorouslevelsthatmightleadtorecurrenceofthe ligamentlesionareresumed.
Conclusion
AnincreaseintheNMEoftheBFmuscleinthenon-operated limbwasobservedtwomonthsaftertheoperation.In com-paringthelimbs,theBFonthenon-operatedsidewasmore efficientatthepostoperativestage.NodifferencesintheNME oftheVLmusclewereseen.
Theforce,electromyographicactivityandneuromuscular activity data showed asymmetries between the limbs two monthsafterthe ACLreconstruction surgery.Thus,atthat time, the operated knee was not fit for normal or sports activities. Furthermore, it is worth emphasizing that spe-cialattentionisneededaroundthesecondmonthafterthe surgery,duringtherehabilitationprocess,withregardto start-ing the stage of open kinetic chain weight-bearing, given that thelimbstillpresents diminishedneuromuscular effi-ciency.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgments
r
e
f
e
r
e
n
c
e
s
1. ThieleE,BittencourtL,OsieckiR,FornazieroAM,Hernadez SG,NassifPAM,etal.Protocolodereabilitac¸ãoaceleradaapós reconstruc¸ãodeligamentocruzadoanterior–Dados
normativos.RevColBrasCir.2009;36(6):504–8.
2. SmithHC,VacekP,JohnsonRJ,SlauterbeckJR,HashemiJ, ShultzS,etal.Riskfactorsforanteriorcruciateligament injury:areviewoftheliterature–Part1:neuromuscularand anatomicrisk.SportsHealth.2012;4(1):69–78.
3. KonishiY,FukubavashiT,TakeshitaD.Possiblemechanismof quadricepsfemorisweaknessinpatientswithruptured anteriorcruciateligament.MedSciSportsExerc. 2002;34(9):1414–8.
4. VasconcelosRA,Bevilaqua-GrossiD,ShimanoAC,Paccola CAJ,SalviniTF,PradoCL,etal.Análisedacorrelac¸ãoentre picodetorque,desempenhofuncionalefrouxidão ligamentaremindivíduosnormaisecomreconstruc¸ãodo ligamentocruzadoanterior.RevBrasOrtop.2009;44(2):134–42. 5. BrasileiroJS,PintoOM,ÁvilaMA,SalviniTF.Functionaland
morphologicalchangesinthequadricepsmuscleinducedby eccentrictrainingafterACLreconstruction.RevBrasFisioter. 2011;15(4):284–90.
6. LeeD,RavichandiranK,JacksonK,FiumeE,AgurA.Robust estimationofphysiologicalcross-sectionalareaand geometricreconstructionforhumanskeletalmuscle.J Biomech.2012;45(8):1507–13.
7. LieberRL.Skeletalmusclestructure,functionandplasticity. Baltimore:LippincottWilliams&Wilkins;2002.
8. TeschPA,DudleyGA,DuvoisinMR,HatherBM,ForceHarris RT.EMGsignalpatternsduringrepeatedboutsofconcentric oreccentricmuscleactions.ActaPhysiolScand.
1990;138(3):263–71.
9. DevriesAH.Efficiencyofelectricalactivityasaphysiological measureofthefunctionalstateofmuscletissue.AmJPhys Med.1968;47(1):10–22.
10.HäkkinenK,AlenM,KallinenM,NewtonRU,KraemerWJ. Neuromuscularadaptationduringprolongedstrength training,detrainingandre-strength-traininginmiddle-aged andelderlypeople.EurJApplPhysiol.2000;83(1):51–62. 11.HortobágyiT,BarrierJ,BeardD,BraspennincxJ,KoensP,
DevitaP,etal.Greaterinitialadaptationstosubmaximal musclelengtheningthanmaximalshortening.JApplPhysiol. 1996;81(4):1677–82.
12.BaroniBM,GeremiaJM,RodriguesR,DeAzevedoFrankeR, KaramanidisK,VazMA.Musclearchitectureadaptationsto kneeextensoreccentrictraining:rectusfemorisvs.vastus lateralis.MuscleNerve.2013;48(4):498–506.
13.BlazevichAJ,GillND,ZhouS.Intra-andintermuscular variationinhumanquadricepsfemorisarchitectureassessed invivo.JAnat.2006;209(3):289–310.
14.FukudaTY,FingerhutD,MoreiraVC,CamariniPMF,Scodeller NF,DuarteA,etal.Openkineticchainexercisesina restrictedrangeofmotionafteranteriorcruciateligament reconstruction:arandomizedcontrolledclinicaltrial.AmJ SportsMed.2013;41(4):788–94.
15.HeijneA,WernerS.Earlyversuslatestartofopenkinetic chainquadricepsexercisesafterACLreconstructionwith patellartendonorhamstringgrafts:aprospective
randomizedoutcomestudy.KneeSurgerySportsTraumatol Arthrosc.2007;15(4):402–14.
16.CuttsA,SeedhomB.Validityofcadavericdataformuscle physiologicalcross-sectionalarearatios:acomparativestudy ofcadavericandin-vivodatainhumanthighmuscles.Clin Biomech.1993;8(3):156–62.
17.DeLucaGC.Theuseofsurfaceelectromyographyin biomechanics.JApplBiomech.1997;13(2):135–63. 18.DeschenesMR,GilesJA,McCoyRW,VolekJS,GomezAL,
KraemerWJ.Neuralfactorsaccountforstrengthdecrements observedaftershort-termmuscleunloading.AmJPhysiol RegulIntegrCompPhysiol.2002;28(2):R578–83.
19.GerberJP,MarcusRL,DibbleLE,GreisPE,BurksRT,LaStayo PC.Effectsofearlyprogressiveeccentricexerciseonmuscle structureafteranteriorcruciateligamentreconstruction.J BoneJointSurgAm.2007;89(3):559–70.
20.ChmielewskiTL,JonesD,DayT,TillmanSM,LentzTA,George SZ.Theassociationofpainandfearofmovement/reinjury withfunctionduringanteriorcruciateligament
reconstructionrehabilitation.JOrthopSportsPhysTher. 2008;38(12):746–53.
21.ArlianiGG,AsturDC,KanasM,KalekaCC,CohenM.Lesãodo ligamentocruzadoanterior:tratamentoereabilitac¸ão. Perspectivasetendênciasatuais.RevBrasOrtop. 2012;47(2):191–6.
22.DuffellLD,DharniH,StruttonPH,McGregorAH.
Electromyographicactivityofthequadricepscomponents duringthefinaldegreesofkneeextension.JBack MusculoskeletRehabil.2011;24(4):215–23.
23.PalmieriRM,IngersollCD,HoffmanMA,CordovaML,Porter DA,EdwardsJE,etal.Arthrogenicmuscleresponsetoa simulatedanklejointeffusion.BrJSportsMed. 2004;38(1):26–30.
24.HurleyMV.Theeffectsofjointdamageonmusclefunction, proprioception,andrehabilitation.ManTher.1997;2(1):11–7. 25.HopkinsJT,IngersollCD,KrauseBA,EdwardsJE,CordovaML.
Effectofkneejointeffusiononquadricepsandsoleus motoneuronpoolexcitability.MedSciSportsExerc. 2001;33(1):123–6.
26.RiceDA,McNairPJ.Quadricepsarthrogenicmuscleinhibition: neuralmechanismsandtreatmentperspectives.Semin ArthritisRheum.2010;40(3):250–66.
27.BonsfillsN,Gómez-BarrenaE,RaygozaJJ,Nú ˜nezA.Lossof neuromuscularcontrolrelatedtomotionintheacutely ACL-injuredknee:anexperimentalstudy.EurJApplPhysiol. 2008;104(3):567–77.
28.CourtneyC,RineRM,KrollP.Centralsomatosensorychanges andalteredmusclesenergiesinsubjectswithanterior cruciateligamentdeficiency.GaitPosture.2005;22(1):69–74. 29.IngersollCD,GrindstaffTL,PietrosimoneBG,HartJM.
Neuromuscularconsequencesofanteriorcruciateligament injury.ClinSportsMed.2008;27(3):383–404.
