Rev. bras. ortop. vol.51 número5

SOCIEDADE BRASILEIRA DE ORTOPEDIA E TRAUMATOLOGIA

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

Original

Article

Index

of

fatigue

quadriceps

in

soccer

athletes

after

anterior

cruciate

ligament

reconstruction

夽

Maria

Luzete

Costa

Cavalcante

_,

_Paulo

_Renan

_Lima

_Teixeira

,

Tamara

Cristina

Silva

Sousa

_,

_Pedro

_Olavo

_de

_Paula

_Lima

_,

_Rodrigo

_Ribeiro

_Oliveira

a_{UniversidadeFederaldoCeará(UFC),HospitalUniversitárioWalterCantídio(HUWC),Fortaleza,CE,Brazil}

b_{UniversidadeUnichristu,Fortaleza,CE,Brazil}

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o

Articlehistory:

Received12March2015 Accepted14December2015 Availableonline17August2016

Keywords:

Fatigue

Anteriorcruciateligament Football

a

b

s

t

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c

t

Objective:Thepresentstudyaimedtoevaluatethemusclefatigueofthequadricepsmuscle inhigh-performancesoccerplayersundergoing(anteriorcruciateligament)ACL reconstruc-tion.

Methods:Weevaluated17high-performancesoccerplayersfromthreeprofessionalsoccer teamsofastateinBrazilfromAugust2011toJuly2012.Allsubjectswereevaluatedbetween 5.5and7monthsafterACLreconstructionwithaBiodex®isokineticdynamometer(System 4Pro)withtestprotocolCON/CONat60◦_/sand300◦_{/swith5and15repetitions,respectively.} Inthecalculationoflocalmusclefatigue,thefatigueindexwasused,whichiscalculated bydividingthelabordoneinthefirstone-thirdoftherepetitionsbythatdoneatthefinal one-thirdoftherepetitions,andmultiplyingby100toexpressaunitinpercentage(i.e.,as adiscretequantitativevariable).

Results:All subjects were male, with a mean age of 21.3±4.4 years and mean BMI 23.4±1.53cm;leftdominancewasobservedin47%(n=8)ofathletes,andrightdominance, in53%(n=9)ofathletes;andthelimbinvolvedinthelesionwasthedominantin29%(n=5) andthenon-dominantin71%(n=12).Fatiguerateswere19.6%intheinvolvedlimband 29.0%inthenon-involvedlimb.

Conclusion: Theresultsallowustoconcludethattherewasnosignificantdifferencebetween thelimbsinvolvedandnotinACLinjuriesregardinglocalmusclefatigue.Noassociation wasobservedbetweenthedominantsideandthelimbinvolvedintheACLinjury.

©2016SociedadeBrasileiradeOrtopediaeTraumatologia.PublishedbyElsevierEditora Ltda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

夽

StudyconductedattheOrthopedicsandTraumatologyService,HospitalUniversitárioWalterCantídio(HUWC),UniversidadeFederal doCeará(UFC),Fortaleza,CE,Brazil.

∗ _{Correspondingauthor.}

E-mails:renanteixeira.ortopedia@hotmail.com,prenanlt@yahoo.com.br(P.R.Teixeira). http://dx.doi.org/10.1016/j.rboe.2016.08.009

Índice

de

fadiga

do

músculo

quadríceps

femoral

em

atletas

de

futebol

após

reconstruc¸ão

do

ligamento

cruzado

anterior

Palavras-chave:

Fadiga

Ligamentocruzadoanterior Futebol

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e

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u

m

o

Objetivos: Opresenteestudopropõeavaliarafadigamusculardomúsculoquadrícepsem atletasdefuteboldealtorendimentosubmetidosàligamentoplastiadoligamentocruzado anterior(LCA).

Métodos: Foramavaliados17atletasdefutebolcomaltorendimentoquepertenciam con-juntamenteatrêstimesdefutebolprofissionaldeumdeterminadoestadobrasileiro,de agostode2011ajulhode2012.Todosforamavaliadosentre5,5e7mesesdepós-operatório deligamentoplastiadoLCAnodinamômetroisocinéticodamarcaBiodex®(System4Pro) comprotocolodetesteCON/CONnasvelocidadesde60◦_/se300◦_{/scom5e15repetic¸ões,} respectivamente.Nocálculodafadigamuscularlocal,usamosoíndicedefadigaqueé cal-culadocomadivisãodotrabalhofeitonoterc¸oinicialdasrepetic¸õespeloterc¸ofinaldas repetic¸õeseamultiplicac¸ãopor100paraexpressarumaunidadeemporcentagem(i.e., variávelquantitativadiscreta).

Resultados: Todoseramdosexomasculino,commédiade21,3±4,4anos;IMCmédiode 23,4±1,53cm;comdominânciaàesquerdaem47%(n=8)dosatletas;eadireitaem53% (n=9)dosatletas;omembroenvolvidonalesãofoiodominanteem29%(n=5)doscasoseo nãodominanteem71%(n=12).Osíndicesdefadigaforamde19,6%nomembroenvolvido ede29,0%nosmembrosnãoenvolvidos.

Conclusão: Osresultadosnospermitemconcluirquenãohádiferenc¸asignificativaentreos membrosenvolvidosenãoenvolvidosnalesãodeLCAnoquedizrespeitoàfadigamuscular local.Tambémnãofoiobservadaassociac¸ãoentreserdestrooucanhotocomomembro envolvidonalesãodeLCA.

©2016SociedadeBrasileiradeOrtopediaeTraumatologia.PublicadoporElsevier EditoraLtda.Este ´eumartigoOpenAccesssobumalicenc¸aCCBY-NC-ND(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Rupture ofthe anterior cruciate ligament (ACL)is a recur-ring andfunctionally limitinginjury amongsoccer players. TheliteratureindicatesthatinEuropeansoccer,ahigh per-formanceathletewillinjuretheACLforevery2000hoursof sportspractice,that14%ofkneesprainsinjurethisstructure, andthatevery seasoneach clubplays12.8matches under-strengthduetoACLrupture.1_{Thisinjuryiscommoninhigh} performancesoccerplayers,whomakesudden hyperexten-sion,valgustwist,and excessive knee rotationmovements withthefootplantedontheground.2

In addition to the large number of individuals exposed tosuchlesions,injuriesresulting fromsoccer practiceand thehigh riskfortheiroccurrencehavebeen the subjectof interestandconcernofhealthcareprofessionals.Afterall,in mostcasestheseinjuresareincapacitatingandpreventthe athletesfromparticipatingintrainingandcompetitionfor var-iousperiodsoftime,sothattheinjurycanbecorrectlyand consistentlytreated.3

In addition to the known biomechanical functions, anatomicalstudieshavealsoshownthattheACLhasa sen-sory function, due to the presence of mechanoreceptors.4 AftertotalorpartialACLrupture,individualsmaypresentjoint proprioception deficit,5 _{deficiency in perception of change} positionduring passive movement,6 _{andcontraction reflex} ofthe muscles posteriorto the tibiarelative tothe femur,

especiallythe hamstringgroupofthe affectedside.7 _These proprioceptivechanges,inturn,inhibittheactionofthemotor unitsofthekneeextensormusclegroup,thusreducingthe strength,power,andendurance,leadingtoapossiblelossof performance.2

ACL reconstructive surgeries are commonly performed inorthopedicpractice.Choosingthebest autograftforACL reconstructioninkneeswithinsufficiencyofthisligamenthas beenthesubjectofdebate.Graftsfromthecentralthirdofthe patellarligamentwerewidelyusedinthe1980sand1990s.In thelate1990s,theuseoftheflexortendonsofthe semitendi-nosusandgracilisincreased.Sofar,thereisdisagreementin thechoiceofgraftforACLreconstruction.8

The muscle dysfunction observed in patients after ACL reconstructionincludesweaknessofthequadricepsmuscle, promotedbyreductionoftheoverload,aswellasjointswelling andpain,whichcanevenpersistmorethansixmonthsafter surgerywithaggressiverehabilitation.Thisweaknessisdue to anincomplete voluntary muscle activation arising from arthrogenicmuscularinhibition,whichisareflectionofthe continuousinhibitionofthemusclesaroundthekneewhen thereisdamagetothisjoint;itslowsdownrehabilitationasit preventsmusclestrengthgaininthequadricepsfemorisand changesproprioception.9

electricalactivity,inwhichthereisadecreaseinthe excite-mentofmotorunitsandchangeintheimpulseconduction velocity.Althoughthisisanimportantissue,it isnotfully elucidated.10–12_{Accordingtothedefinitionofmusclefatigue} anditsaspects,it ispossibletohypothesizethatthereisa changeofthis variableinthe quadricepsmuscleafterACL rupture.

Two typesof muscle fatigueare traditionally described: thatresultingfromchangesinskeletalmusclehomeostasis, regardlessoftheneuralimpulseconductionvelocityand des-ignatedbyfatigueofperipheralorigin;andthatresultingfrom alterationsintheneuralinputthatreachesthemuscle, trans-latedbyaprogressivereductionoftheconductionvelocityand frequencyofthevoluntarypulsetothemotoneuronsduring theperiod,usuallycalledfatigueofcentralorigin.13

Onewaytoassessthemusclebalancebetweenthe quadri-cepsand hamstringsisatestperformedinadevice called isokineticdynamometer.Theevaluationofmusclestrength throughanisokineticdynamometerhasbeenusedinthe diag-nosisofneuromusculardisorders,rehabilitation,training,and research,asanindicatorofthefunctionandperformanceof certainmusclegroups.14

Studiesdifferon themuscular fatiguelevelsinsubjects undergoingligamentreconstructionsurgery;theideaof test-ingandassessingthetruebehavioroftheextensormusclesin themusclefatigueprocessarosefromthefactthattheresults intheliteratureareconflicting.Moreover,withtheincreased incidenceofligamentinjuriesinprofessionalsoccerplayers, the impact of surgery on the performance of these high-performanceathletescanbeobserveddirectlyandclearly;in thefuture,rehabilitationprotocolsthatenableimproved per-formanceandincreasedresistancetofatiguecanbeproposed. ThemainobjectivesofrehabilitationafterACL reconstruc-tionaretoregainnormaljointstability,restorefullrangeof motion,achieve good muscle strength in the injured limb, increaseneuromuscularcontrol, resume normalfunctional activity,andminimizetheriskofsecondarystructural dam-age to the knee, with the primary objective of achieving post-surgicalkneesymmetry.15_{Therefore,therehabilitation} protocolshouldbecarefullyplannedinordertofirstrestore rangeofmotionandthengraduallyincreaseenduranceand musclestrength.14

Thisstudyaimedtoassessthefatigueindexofthe quadri-ceps in high-performance soccer players undergoing ACL reconstruction,usingthecontralaterallimbasareference.

Methods

Thiswas a cross-sectionalstudy, developedat the Human MotionAnalysisLaboratory from August 2011toJuly2012, whichwasapprovedbytheResearchEthicsCommitteeunder protocolNo.230/2011.Afreeandinformedconsentformwas signedbytheparticipants,whoconfirmedtheirvoluntary par-ticipationintheresearch.

Thestudy included 17 high-performancesoccer players fromthreeprofessionalfootballteamsinastateinBrazil;all thosewhosufferedACLinjuryandunderwentligament recon-struction surgerywere included. Athletes were referred by themedicaldepartmentsoftheteamsforwhichtheyplayed.

Toparticipateinthestudy,athleteswererequiredtopresent nodecompensationsofthecardiorespiratorysystem,suchas uncontrolledhypertension,angina,orarrhythmia;inaddition, athleteswhohadacutepainbeforeorduringthetests(analog painscaleequaltoorabove70/100mm),untreatedinjury,or anyotherfactorthatwouldaffecttheirperformanceonthe testwereexcluded.

ABiodex®_{isokineticdynamometer(System4Pro)wasused}

toassessquadricepsmusclefatigue.Theathletesunderwent alightaerobicwarm-upsession,withoutstretchingexercises, forfiveminutesbeforetheisokinetictest.Thedynamometer chairwaspositionedsothatthehipwouldbeat85◦_flexion,

andthatthemotionaxisoftheequipmentwasalignedwith thelateralintercondylarspace.Then,subjectswereseatedin thedynamometerchairandthepositionwasstabilizedwith bracesplacedatthetrunk,abdomen,andnon-assessedthigh levels, in order to prevent compensatory movements. The leverarmoftheequipmentwasfixedat2cmabovethemedial malleolus.Thetestalwaysstartedinthedominantlimb.The established isokineticprotocol was that ofconcentric con-tractions (CON/CON)withtwo speeds:60◦ _{and 300}◦_/s,with

5:15 repetitions,respectively, withaninterval of30seconds ofrest.Theequipmentwascalibratedtotherangeofmotion from the maximumflexion tothe maximumextensionfor eachparticipant,inwhichthereferencepointwas90◦

flex-ion.Thelimbwasweighedbytheequipmentitselftoavoid biascausedbygravity.Afterthepositioningand alignment procedures,individualswereaskedtomakefivemovements offlexionandextensionatsubmaximalintensityinorderto completethewarm-upprocess,andtofamiliarizethemselves withtheequipmentandtestingprocedures.Theupperlimbs werefixedlaterallytothechairinanappropriateplace. Subse-quently,thetestwasinitiated,whereuponaverbalcommand wasgivenbythesameexaminerduringalltests.

To test the hypothesis that fatigue in the quadriceps femorismuscleismorelikelytooccurinthelimbinvolvedin ACLinjurymusclethaninthenon-involvedlimb,the inferen-tialStudent’st-testforpairedsampleswasused,asthehealthy limbwasadoptedascontroltotheinjuredlimb.Foranalysis andprocessingofthedata,SPSS(version15.0)wasused;a5% significancelevelwasadoptedforallcalculations.

Inthecalculationoflocalmusclefatigue,thefatigueindex wasused,whichisderivedbydividingtheworkdoneinthe firstthirdoftherepetitionsbythatdoneinthefinalthirdof repetitions,andmultiplyingthatby100toexpressthevalue asapercentage(i.e.,adiscretequantitativevariable).16

Thecharacteristicsofthesamplewereexpressedthrough descriptivemeasuressuchasmeasuresofcentraltendency (mean)anddispersion(standarddeviation).Todeterminethe distribution ofthe data, the Kolmogorov–Smirnovtest was used,whichindicatedthatthedatafollowedastandard nor-maldistribution.

Results

Samplecharacterization

Table1–Samplecharacterization.

Age(years) 21.3±4.4a

BMI(kg/cm2_{) 23.4±1.5}a

Sex 100%male

Dominantside 47%(n=8)Left 53%(n=9)

Right

Injuredlimb 29%(n=5)Dominant 71%(n=12)

Non-dominant

BMI,bodymassindex.

a _{Valuesexpressedasmean±standarddeviation.}

Fatigueindexofthenon-involvedlimb

Thefatigueindexofthequadricepsfemorismuscleinthelimb notinvolvedwithACLinjuryisshowninFig.1.

Fatigueindexoftheinvolvedlimb

Thefatigueindexofthequadricepsfemorismuscleinthelimb involvedwithACLinjuryisshowninFig.2.

Fig.3presentsthemeanfatigueindexforextensionofthe limbsinvolvedandnotinvolvedinreconstructivesurgery.

Discussion

Studiesthatcharacterizeisokineticperformancearefrequent inthesportsliterature,mainlyduetothehighprevalenceof

60

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20

10 30.5

47.7

26.9 34.7 35

25 38.3

29.8

23.9 37.8

20 30.5

24.7

7.5 29.7

22.7

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 29.1

0

Fatigue at extension in the non-involved limb

Fig.1–Fatigueatextensioninthelimbnotinvolvedin reconstructivesurgery.

50

33.9 44.1

33.1 33.1

33.8 39.6

35.4

27.4 32.6

10.6 20.6

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Fatigue at extension in the involved limb

Fig.2–Fatigueatextensioninthelimbinvolvedin reconstructivesurgery.

P=.246 60

%

40

20

0

Involved limb Non-involved limb

Fig.3–Meanfatigueindexforextensionofthelimbs involvedandnotinvolvedinreconstructivesurgery.

ligamentinjuriesinhigh-performancesoccerplayers,which are due in part to the changes in the sport observed in recentyears,inwhichthephysicalrequirementshavebecome higher,pushingtheseathletestoworkclosetotheir perfor-mancelimitandfavoringtheoccurrenceofinjuries.

Regarding theanthropometric datadescribedinTable1, themeanageofthepatientswas21.33±4.4years,which cor-roboratestheliterature,sinceACLlesionsoccurmoreoftenin youngindividualswhopracticesomekindofsport, particu-larlyinmalepatients.17

Inthepresentstudy,itwasobservedthat71%(n=12)of thepatientshadthenon-dominantlimbinvolvedintheACL injury,whichisjustifiable,asrotationaltraumaisthemost frequentmechanismofthisinjury. Insuchcases,the body rotatesexternallyonthelimbrestingontheground.18

TheclassicmechanismofACLinjuryistwistingwiththe foot fixed standingon the ground; inthis mechanism, the tibiamovesanteriorlyinrelationtothefemur.Othertypesof traumacanalsocauseACLcruciateinjuries,especiallyduring sportspractice,buttheanteriorprojectionofthetibia rela-tivetothefemurisundoubtedlythemaincauseofligament injury.18,19

Itwasobservedthat47%ofthepresentathleteshadthe leftsideasdominantandhence53%weredominantinthe rightlimb(OR:0.476,95%CI:0.057–3.990),showingthatthere wasnoassociationbetweenrightorleftdominancewiththe limbinvolvedinACLinjuries.

In the present study, of the 17 athletes studied, the meanfatigueindexinextensionofthelimbinvolvedinthe lesionwas19.6%±39.4andthemeanindexfatiguein exten-sionobservedinthelimbnotinvolvedwiththelesionwas 29.0%±11.1(p=0.246).Althoughthefatigueindexwashigher inthenon-injuredlimb,therewasnosignificantdifference betweenthelimbsinvolvedandnotinvolvedinACLinjuries regardingthevariableoflocalmusclefatigue.

withACLinjurieshavelessresistancetofatiguethanhealthy subjects, due to the weakness of the quadriceps femoris. However,McNairetal.22 _{believethat patientswithchronic} ACLlesionsdeveloptypeIImusclefiberhypertrophyasthese subjectsshowed greater resistancetofatigue than healthy individuals.

Theonsetoffatiguemayberelatedtotheincreased lac-ticacidconcentrationintheextracellularmediumofmuscle tissue.Theoretically,theincreaseoflacticacidconcentration leadstoadecreaseinextracellularpH,whichisrelatedtothe decreaseinpotentialoftheconductionvelocityoftheaction potentialthroughmusclefiber.23

Anatomicalstudiesofthehumankneehavedemonstrated thatnervefiberspenetratethecruciateligaments.InanACL injury, there is loss of proprioceptive information, thereby aggravatingtheinstabilityofthisjointbydecreasingthesense ofposition andthe absenceofthestimulus forreflex con-traction.Theremainingkneestructureshaveothersourcesof proprioceptiveinformation;throughspecifictrainingof neu-romuscularcoordinationrequiredtostabilizethe joint,this responseshouldoccurthroughdynamiccontrol,inorderto decreasetheresponsetimeofmusclereaction.24

Musclefatigueisafrequentphenomenonintrainingand competitionroutinesofsomeathletes;itcandegrade perfor-manceandpredisposethemtoanumberofmusculoskeletal injuries.Thisdamagecanbetemporary,lastingforminutes orhours afterexercise,or persistforlong periodsoftime, such as several days.25 _{The short-term losses result from} metabolicdisturbancesafterhighintensityexercise.26_Inturn, thelong-termdamagemayberelatedtotissueinjurycaused byexercise and the phenomenonknown as delayed onset musclesoreness.27

Several therapeutic strategies that are widely used in sportstoacceleratetheprocessofpost-exercisemuscle recov-eryhavebeenstudied,suchasactiverecovery,cryotherapy, massage, heat contrast therapy, hydrotherapy, stretching, hyperbaricoxygentherapy,non-steroidalanti-inflammatory drugs,andelectricalstimulation.28

Themaincausesforthereductionofproprioceptive reac-tions are joint injuries, namely the rupture or permanent distension of articular components constituting the liga-ments,tendons,and thecapsule,whichnotonlyresultsin a mechanical change, but alsoin loss of positional sense, duetoadysfunctionintheperipheralmechanoreceptors.The development or restoration of proprioception, kinesthesia, and neuromuscularcontrol ofthe injured individual mini-mizestheriskofinjuryrecurrenceandrestoresthekinesthetic awareness.24,29,30

Conclusion

Theresultsallowfortheconclusionthatthereisnosignificant differencebetweentheinvolvedoruninvolvedlimbsinACL injuriesregardinglocalmuscle fatigue.No associationwas observedbetweenthedominantsideandthelimbinvolved intheACLinjury.

Longitudinalstudiesevaluatingvariousisokinetic param-etersarestillscarceintheliterature;therefore,newstudies arerecommendedfortheanalysisoftheseparameters.These

studiesshouldincludealargernumberofindividuals,include othersports,andinvolvebothgenders.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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1.EkstrandJ,HägglundM,WaldénM.Epidemiologyofmuscle injuriesinprofessionalfootball(soccer).AmJSportsMed. 2011;39(6):1226–32.

2.AlvesPHM,SilvaDCO,LimaFC,PereiraML,SilvaZ.Lesãodo ligamentocruzadoanterioreatrofiadomúsculoquadríceps femoral.BiosciJ.2009;25(1):146–56.

3.GayardoA,MatanaSB,SilvaMR.Prevalênciadelesõesem atletasdofutsalfemininobrasileiro:umestudoretrospectivo. RevBrasMedEsporte.2012;18(3):186–9.

4.LeeBI,MinKD,ChoiHS,KwonSW,ChunDI,YunES,etal. Immunohistochemicalstudyofmechanoreceptorsinthe tibialremnantoftherupturedanteriorcruciateligamentin humanknees.KneeSurgSportsTraumatolArthrosc. 2009;17(9):1095–101.

5.KatayamaM,HiguchiH,KimuraM,KobayashiA,HatayamaK, TerauchiM,etal.Proprioceptionandperformanceafter anteriorcruciateligamentrupture.IntOrthop. 2004;28(5):278–81.

6.DhillonMS,BaliK,PrabhakarS.Proprioceptioninanterior cruciateligamentdeficientkneesanditsrelevanceinanterior cruciateligamentreconstruction.IndianJOrthop.

2011;45(4):294–300.

7.BeardDJ,KyberdPJ,FergussonCM,DoddCA.Proprioception afterruptureoftheanteriorcruciateligament.Anobjective indicationoftheneedforsurgery?JBoneJointSurgBr. 1993;75(2):311–5.

8.CohenM,FerrettiM,AmaroJT.Reconstruc¸ãodoligamento cruzadoanterior:escolhadoenxerto.SãoPaulo:Sociedade BrasileiradeOrtopediaeTraumatologia;2007.Projeto Diretrizes.

9.MacielNFB.Influênciadafadiganocomportamento neuromusculardoquadrícepsfemoralapósreconstruc¸ãodo ligamentocruzadoanterior.RioGrandedoNorte:

UniversidadeFederaldoRioGrandedoNorte,Natal;2010. Dissertac¸ão.

10.DimitrovaNA,DimitrovGV.InterpretationofEMGchanges withfatigue:facts,pitfalls,andfallacies.JElectromyogr Kinesiol.2003;13(1):13–36.

11.GarciaMAC,MagalhãesJ,ImbiribaLA.Comportamento temporaldavelocidadedeconduc¸ãodepotenciaisdeac¸ãode unidadesmotorassobcondic¸õesdefadigamuscular.RevBras MedEsporte.2004;10(4):299–303.

12.SantosMCA,SemeghuiniTA,AzevedoFM,ColugnatiDB, NegrãoFilhoRF,AlvesN,etal.Análisedafadigamuscular localizadaematletasesedentáriosatravésdeparâmetrosde frequênciadosinaleletromiográfico.RevBrasMedEsporte. 2008;14(6):509–12.

13.DavisM,BaileyS.Possiblemechanismsofcentralnervous systemfatigueduringexercise.MedSciSportsExerc. 1997;29(1):45–57.

14.WeberFS,SilvaBGC,CadoreLE,PintorSS,PintorRS. Avaliac¸ãoisocinéticadafadigaemjogadoresdefutebol profissional.RevBrasCiêncEsporte.2012;34(3):775–88. 15.MendesBMC.Prevenc¸ãoereabilitac¸ãofisiátricanalesãodo

deMedicinadaUniversidadedoPorto,Portugal;2012. Dissertac¸ão.

16.PinciveroDM,GearWS,SternerRL.Assessmentofthe reliabilityofhigh-intensityquadricepsfemorismuscle fatigue.MedSciSportsExerc.2001;33(2):334–8.

17.NicoliniAP,CarvalhoRT,MatsudaMM.Lesõescomunsno joelhodoatleta:experiênciadeumcentroespecializado.Acta OrtopBras.2014;22(3):127–31.

18.DaiB,MaoD,GarrettWE,YuB.Anteriorcruciateligament injuriesinsoccer:loadingmechanisms,riskfactors,and preventionprogram.JSportHealthSci.2014;3(4):299–306. 19.FaunøP,JakobsenBW.Mechanismofanteriorcruciate

ligamentinjuriesinsoccer.IntJSportsMed.2006;27(1): 75–9.

20.OliveiraMP.DesempenhoisocinéticodoJoelhoapósalesão primáriadoligamentocruzadoanteriorutilizandoenxertodo ligamentocontralateral.Brasília:UniversidadedeBrasília; 2008.Dissertac¸ão.

21.BonatoP,ChengMS,Gonzales-CuetoJ,LeardiniA,O’ConnorJ, RoySH.Basedmeasuresoffatigueduringarepetitivesquat exercises.Assessmentofdynamicconditionscanprovide informationaboutcompensatorymusclefunctioninACL patients.IEEEEngMedBiol.2011;20(6):133–43.

22.McNairPJ,WoodGA.FrequencyanalysisoftheEMGfromthe quadricepsofanteriorcruciateligamentdeficientindividuals. ElectromyogrClinNeurophysiol.1993;33(1):43–8.

23.MoritaniT.Neuromuscularadaptationsduringthe acquisitionofmusclestrength,powerandmotortasks.J Biomech.1993;26Suppl1:95–107.

24.PaizanteGO,KirkwoodRN.Reeducac¸ãoproprioceptivana lesãodoligamentocruzadoanterior.RevMeioAmbSaúde. 2007;2(1):123–35.

25.BarnettA.Usingrecoverymodalitiesbetweentraining sessionsineliteathletes.Doesithelp?SportsMed. 2006;36(9):781–96.

26.WesterbladDH,AllenDG,LannergrenJ.Musclefatigue:lactic acidorinorganicphosphatethemajorcause?NewsPhysiol Sci.2002;17(1):17–21.

27.CheungK,HumePA,MaxwellL.Delayedonsetmuscle soreness:treatmentstrategiesandperformancefactors. SportsMed.2003;33(2):145–64.

28.BaroniBM,LealJuniorECP,GenerosiRA,GrosselliG,CensiS, BertollaF.Efeitodacrioterapiadeimersãosobrearemoc¸ão dolactatosanguíneoapósexercício.RevBrasCineantropom DesempenhoHum.2010;12(3):179–85.

29.BonfimTR,GrossiDB,PaccolaCAJ.Effectofadditionalsensory informationintheproprioceptionandposturalcontrolof individualswithacllesion.ActaOrtopBras.2009;17(5):291–6. 30.CossichaV,MallrichaF,TitonelliV.Déficitproprioceptivoem