VU Research Portal
Recovery of gait after quadriceps muscle fatigue.
van Dieen, J.H.; Barbieri, F.A.; Beretta, S.S.; Pereira, V.A.
published in
Gait and Posture
2016
DOI (link to publisher)
10.1016/j.gaitpost.2015.10.015
Link to publication in VU Research Portal
citation for published version (APA)
van Dieen, J. H., Barbieri, F. A., Beretta, S. S., & Pereira, V. A. (2016). Recovery of gait after quadriceps muscle
fatigue. Gait and Posture, 43, 270-274. https://doi.org/10.1016/j.gaitpost.2015.10.015
General rights
Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain
• You may freely distribute the URL identifying the publication in the public portal ?
Take down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim.
E-mail address:
vuresearchportal.ub@vu.nl
Recovery
of
gait
after
quadriceps
muscle
fatigue
Fabio
Augusto
Barbieri
a,b,*
,
Stephannie
Spiandor
Beretta
a,
Vinicius
A.I.
Pereira
a,b,
Lucas
Simieli
a,
Diego
Orcioli-Silva
a,
Paulo
Cezar
Rocha
dos
Santos
a,
Jaap
H.
van
Diee¨n
c,
Lilian
Teresa
Bucken
Gobbi
aaUnivEstadualPaulista,PostureandGaitStudiesLaboratory,RioClaro,Brazil b
UnivEstadualPaulista,LaboratoryofInformation,Vision,andAction,Bauru,Brazil
c
MOVEResearchInstituteAmsterdam,FacultyofHumanMovementSciences,VUUniversityAmsterdam,Amsterdam,TheNetherlands
1. Introduction
Musclefatiguehasbeendefinedasalossofcontractilecapacity
ofthemuscle asa consequenceof muscleactivity,reflected in
failure to maintain a required or expected force, in failure to
continue working at a given exerciseintensity, or in a loss of
performanceduringrepeatedorcontinuousactivation[1]Muscle
fatigue negatively affects aspects related to balance, such as
muscle contractile capacity, coordination and proprioception
[2,3]. Consequently, quadriceps muscle fatigue affects gait of
youngadultsirrespectiveoftheirphysicalactivitylevel[4]and
typeofgait,suchasobstaclecrossingandsteppingdownastep
[4–7]. It coincides with adjustments in the spatio-temporal
[3,4,6,8,9],kinetic[4,7]andmuscleactivity[5,8]parametersof
gait.Youngadultswereshowntoreduceactivityofthequadriceps
muscleduringgaitafterexhaustiveexercise[5,8,10],whichmay
impair weight acceptance [4] since the quadriceps muscle
dissipates most of the energy at contact of the foot with the
ground [7,11]. In addition, muscle fatigue coincides with
compensatorygaitadjustmentsthatenhancegaitstability,such
asanincreasedstepwidthanddecreasedstepduration[4,6].
After prolonged exercise and especially after eccentric
con-tractionsfatigueandpotentiallymuscledamagemayhave
long-lastingeffects[12,13].Consideringthenegativeeffectsofmuscle
fatigueon gait, it is importanttoknowtherecoveryof
spatio-temporal, kinetics and electromyographic parameters and to
determinehow muchtimeis neededforfullrecovery.Previous
studies indicated negative effects of fatigue after exhaustive
exercise on the force generating capacity of muscle [14] and
balance[15,16]arenegativelyaffectedbymusclefatigueandneed
10–20mintorecoverafterexhaustivemusclefatigue.However,
the time needed for recovery of gait parameters after muscle
fatiguehastoourknowledgenotbeenstudied.Theperiodofrest
ARTICLE INFO Articlehistory:
Received19March2015
Receivedinrevisedform5October2015 Accepted7October2015 Keywords: Walking Musclefatigue Recoverytime Humanmovement ABSTRACT
Theaimofthisstudywastoinvestigatetheeffectofrecoverytimeafterquadricepsmusclefatigueon gaitinyoungadults.Fortyyoungadults(20–40yearsold)performedthree8-mgaittrialsatpreferred velocitybeforeandaftermusclefatigue,andafter5,10and20minofpassiverest.Inaddition,ateach timepoint,twomaximalisometricvoluntarycontractionswerepreformed.Musclefatiguewasinduced by repeated sit-to-stand transfers until task failure. Spatio-temporal, kinetic and muscle activity parameters,measuredinthecentralstrideofeachtrial,wereanalyzed.Datawerecomparedbetween beforeand afterthemusclefatigue protocoland afterthe recoveryperiods byone-wayrepeated measuresANOVA.Thevoluntaryforcewasdecreasedafterthefatigueprotocol(p<0.001)andafter5, 10and20minofrecoverycomparedtobeforethefatigueprotocol.Stepwidth(p<0.001)andRMSof bicepsfemoris(p<0.05)wereincreasedimmediatelyafterthefatigueprotocolandremainedincreased aftertherecoveryperiods.Inaddition,stridedurationwasdecreasedimmediatelyafterthefatigue protocolcomparedtobeforeandtoafter10and20minofrest(p<0.001).Theanterior–posterior propulsiveimpulsewasalsodecreasedafterthefatigueprotocol(p<0.001)andremainedlowafter5, 10and20minofrest.Weconcludethat20minisnotenoughtoseefullrecoveryofgaitafterexhaustive quadricepsmusclefatigue.
ß2015ElsevierB.V.Allrightsreserved.
* Corresponding author at: Universidade Estadual Paulista-UNESP-FC-Bauru, LaboratoryofInformation,Vision,andAction,DepartmentofPhysicalEducation, Av.Eng.LuizEdmundoCarrijoCoube,14-01,VargemLimpa,CEP:17.033-360, Bauru,SP,Brazil.Tel.:+551431036082x7612.
E-mailaddress:barbieri@fc.unesp.br(F.A.Barbieri).
ContentslistsavailableatScienceDirect
Gait
&
Posture
j our na l ho me pa g e : w ww . e l se v i e r . com / l oca t e / ga i t po st
http://dx.doi.org/10.1016/j.gaitpost.2015.10.015
required to recover gait parameters after muscle fatigue is
important,since around23–30%of fallsinoccupational setting
occurbecauseoffatigue[17].Fatigueintheseincidentsmayrefer
tootherprocessesinadditiontomusclefatigue,e.g.mentalfatigue.
Nevertheless,thisstudyfocusesoneffectsofmusclefatigueonly.
Theaimofthisstudywastoinvestigatetheeffectofdifferent
recoveryperiods (5, 10 and 20min) after fatiguing quadriceps
muscleexerciseon gaitin youngadults.We hypothesizedthat
muscle fatigue would negatively affect gait, which would be
reflectedincompensatory adjustmentstoimprovestability(i.e.
greater step width, decreased step duration). Moreover, we
hypothesized that gait changes would return towards baseline
valuesover20minofrest.
2. Method
Forty individuals aged between 20 and 40 years (age:
28.95.0 years; body weight: 78.614.0kg; body height:
1.760.06m; bodymass index:24.84.0kg/m2) participatedin
thisstudy.Theexclusioncriteriaofthestudywerefactorsthatcould
interfere with gait and other experimental procedures, such as
medication use,presence ofosteomyoarticular, neuromuscular or
cardio-respiratorydiseasesandbalanceandvisiondisorders.During
thesampleselectionprocess,26initiallyrecruitedindividualsdidnot
fitthecriteriaofthestudy.ThestudywasapprovedbythelocalEthics
Committee(#2055/2008).
Participants were instructed not to perform any strenuous
physical activity 48h before evaluation. The participants
per-formedawarm-upperiodof5min,withwalkingandstretching.
Afterthisperiod,theparticipantsperformedaseriesof
familiari-zation trials in the leg press instrument (for the maximum
voluntary isometric contraction protocol). Subsequently, the
participants(Fig.1):
1)filledoutaquestionnaireonmedicalhistory;
2)performedtheunobstructedgaittask;
3)performed the maximum voluntary isometric contraction
protocol;
4)performedthefatigueprotocol(sit-to-standtask);
5)repeatedthesecondandthirditemsafterthefatigueprotocol
and after5, 10and 20min ofrest. Theperiodsof restwere
passivewiththeparticipantsseated.
Theparticipantswalkedoveran8mpathwayatself-selected
speed.Eachparticipantperformedthreetrialsbeforethefatigue
protocol,afterthefatigueprotocolandafter5,10and20minof
rest.Weanalyzedthestrideinthemiddleofthepathwayonthe
forceplates(AccuGait,AdvancedMechanicalTechnologies,Boston,
MA)–50cm50cm–withrateof200samples/s.Kineticdatawere
filteredwitha4thorderfilterwithacutofffrequencyof16Hzand
themagnitudeofthegroundreactionforcewasnormalizedbybody
weight. Kinematic data were collected by a three-dimensional
optoelectronicsystem(OPTOTRAKCertus),positionedorthogonalto
the plane of progression tothe right of the walkway, usinga
samplerateof100samples/s.Fourinfraredemitterswereplaced
overthefollowinganatomicalpoints:lateralfaceofcalcaneusand
headofthefifthmetatarsusoftherightlimb,andmedialfaceof
calcaneusandheadofthefirstmetatarsusoftheleftlimb.These
data werefiltered witha 5thorder low-pass filterwith cutoff
frequencyof6Hz.Muscleactivitywasassessedusingdisposable
Ag/AgClsurface-electrodes(lead-offarea1.0cm2,inter-electrode
distance 2.0cm) in combinationwith a signal amplifier (EMG
SystemdoBrasilLtda.).Afterabrasionandcleaningwithalcohol,
electrodes were attachedover the vastus lateralis and biceps
femoris in the right limb. ElectrodesandEMG data collection
followedtheSENIAMguidelines[18].EMGsignalswereamplified
(1000times,commonmoderejectionratio>120dB)andstored
on disc (12bits AD converted, resolution 5V, sample rate
1000samples/s). Off-line, EMG signals were band-pass filtered
between20and500Hzandrectifiedandlow-passfilteredat15Hz.
In addition, values were normalized to peak values of the
correspondingsignalsintheunfatiguedtrialsofeachparticipant.
Thedataacquisitionsystemswereelectronicallysynchronized.
Thestridelength,strideduration,stridevelocity,stepwidth,
double supporttime, brakingand propulsiveanterior–posterior
impulses and root mean square (over a stride—between two
consecutive left heel contacts) of vastus lateralis and biceps
femorisEMG wereanalyzedbeforeandafterthemusclefatigue
protocolandafter5,10and20minofpassiverestineachtrial.
Maximumvoluntaryisometriccontractionswereperformedin
acustom-builtlegpressdevice[4,6](Fig.2).Asourfatigueprotocol
causes fatiguein thewhole leg and does not isolate a specific
musclegroup,wechosethelegpressdevicetotestforchangesthe
maximalforceproducedwiththewholelegandnobyanisolated
musclegroup.A loadcellwithprecision of0.98Nwasused in
combinationwithasignalamplifier(EMGSystemdoBrasilLtd.).
Theparticipantswereseatedinabackwardinclinedchair,withthe
hipjointat908(1808isfullextension)andkneejointat1108(1808
is full extension). Total contraction duration was 5s. The
participantperformedthetestwithbothlegs,withtheinstruction
togenerateasmuchforceasfastaspossible.Twoattemptswere
made with 2min rest between attempts before the fatigue
protocol,afterthefatigueprotocolandafter5,10and20minof
rest.Themaximumforcegeneratingandmedianfrequencyofthe
powerspectrumvalueoftheEMGofthevastuslateralisandbiceps
femoris in each period were determined. Results of the two
attempts at each time point (before and after fatigue, after 5,
10and20minrest)wereaveraged.
Thefatigueprotocolwasarepeated sit-to-standtaskfroma
chairwitharmsacrossthechest[4,5].Thesubjectperformedthis
task until theparticipant wasunable tocontinue orwhen the
movementfrequencyfellbelowandremainedbelow0.5Hzafter
encouragement and theduration of theprotocolwasrecorded.
RatingofperceivedexertionwasmeasuredbytheBorgScale[19]
atthebeginningandtheendofthefatigueprotocol,andafter5,
10and20minofrest.
2.1. Dataanalysis
The spatiotemporal, kinetic and muscle activity parameters
werecalculatedinMatlab(Version2012—MathWorks,Inc.).The
dependentvariables ofinterestwerestatisticallyanalyzed with
SPSS18.0forWindows.The datawerenormallydistributed,as
verifiedbytheShapiro–Wilktest.Thedependentvariableswere
comparedusingrepeatedmeasuresANOVAs,withperiod(before
fatigueafterfatigue5minofrest10minofrest20minof
rest)asmainfactor(
a
<0.05).Polynomialcontrasttestswereusedtolocalizethedifferencesamongperiods(Bonferroniadjustments
to
a
<0.005).3. Results
Themeandurationofthefatigueprotocolwas12.43min(SD:
10.63min). The meansand standarddeviationsof theratingof
perceived exertion,maximal isometricvoluntarycontraction,
spa-tiotemporal,kinetic andelectromyographyparametersbeforeand
aftermusclefatigueandafter5,10and20minofrestarepresentedin
Table1.ANOVAindicatedthattheindividualshadahigherratingof
perceivedexertionaftermusclefatigueandaftertheperiodsofrest
(5,10and20min)thanbeforemusclefatigue(p<0.001).Inaddition,
theratingofperceivedexertionimmediatelyaftermusclefatiguewas
higherthanafter5,10and20minofrest(p<0.001)(Table1).Also
force generatingcapacity wasdecreasedafter musclefatigue and
remaineddecreasedaftertherestperiods(p<0.001).Withregardto
the EMG signals, vastus lateralis showed a decreased median
frequencyafterthefatigueprotocol(p<0.01),whichwasrecovered
after20minofrest(nodifferencesbetweenbeforemusclefatigueand
20min of rest). Median frequency of biceps femoris showed a
reductiononlydirectlyafterthefatigueprotocolcomparedtobefore
(p<0.05),withoutdifferencesbetweenbeforethefatigueprotocol
andafter5,10and20minofrest.
Afterthe fatigueprotocol, participantsshowedincreasedstep
width (p<0.001) and muscle activity of the biceps femoris
(p<0.005)anddecreasedstrideduration(p<0.005)andpropulsive
anterior–posteriorimpulse(p<0.001)(Table1).Twentyminutesof
restwerenotenoughforrecoveryofthesegaitparameters.Step
width (p<0.001), activityof the biceps femoris (p<0.005) and
propulsiveanterior–posteriorimpulse(p<0.001)hadnotreturned
tobaselinevaluesafter20minofrest.Onlystridedurationshowed
clearrecovery(after5minofrest).Noneoftheotherparameters
analyzeddidshoweffectsofquadricepsmusclefatigueorrest.
4. Discussion
Theaimofthisstudywastoinvestigatetheeffectofdifferent
recovery periods (5, 10 and 20min) after quadriceps muscle
fatigueongaitinyoungadults.Asweexpected,musclefatigue
coincidedwithchangesinsomegaitparameters.Afterthefatigue
protocolstepwidthwasincreasedandstridedurationdecreased.
In addition, gait propulsion (decreased propulsive anterior–
posteriorimpulse)andbicepsfemorisactivity(increasedRMSof
theEMG)weremodified afterthefatigueprotocol.Nochanges
were observedin stride length, stride velocity, double support
Fig.2.Pictureoftheequipment(custom-builtlegpressdevice)formaximum voluntaryisometriccontractionsduringkneeextension.
Table1
Meansandstandarddeviationsoftheratingofperceivedexertion,maximalisometricvoluntarycontraction,spatiotemporal,kineticsandelectromyographyparameters beforeandaftermusclefatigueandafter5,10and20minofrest.
Beforefatigue Afterfatigue 5minofrest 10minofrest 20minofrest Rateofperceivedexertion
Borgscale 7.101.39* 18.93
1.28& 8.95
2.66 9.032.81 8.732.84 Maximalisometricvoluntarycontraction
Muscleforce(kg/f) 375.6513.23*
318.3425.90 330.7912.02 326.6214.76 333.2546.11 Medianfrequencyofvastuslateralis 128.8437.52+
111.7840.30 110.8138.46 112.5240.02 118.1839.71 Medianfrequencyofbicepsfemoris 103.0635.66#
87.9428.27 91.8919.92 93.6426.03 95.3325.13 Spatial-temporalparameters Stridelength(cm) 134.9610.85 135.3811.98 134.7210.93 135.4511.83 135.6011.74 Stepwidth(cm) 11.452.31* 12.762.66 12.182.38 12.332.72 12.822.78 Strideduration(s) 1.070.08# 1.05 0.08 1.060.07 1.070.09 1.070.09 Stridevelocity(cm/s) 127.3115.16 129.3915.29 128.1514.05 127.9918.63 127.8317.97 Doublesupportduration(%) 26.792.99 26.693.29 27.843.93 26.432.93 26.432.84 Kineticsparameters
Brakinganterior–posteriorimpulse(BW) 0.040.04 0.050.04 0.050.04 0.050.04 0.050.04 Propulsiveanterior–posteriorimpulse(BW) 0.040.02*
0.030.01 0.030.01 0.030.01 0.030.01 Muscleactivity RMSvastuslateralis(%) 23.065.09 24.8913.18 24.6114.01 23.3815.55 21.89.89 RMSbicepsfemoris(%) 21.135.63* 23.63 9.77 24.8912.25 24.1211.21 25.0111.67 *
Beforefatigueissignificantlydifferentfromotherperiods.
#
Beforefatigueissignificantlydifferentfromafterfatigue.
&
Afterfatigueissignificantlydifferentfromafter5,10and20minofrest.
+
time,brakingimpulseandquadricepsmuscleactivity.
Unexpect-edly,forcegeneratingcapacity,stepwidth,propulsiveanterior–
posteriorimpulseandmuscleactivityofthebicepsfemoriswere
notrecoveredafter20minof rest,incontrast withoursecond
hypothesis.Therefore,inthefollowingparagraphs,wewilldiscuss
theapparentabsenceofrecoveryoftheeffectsofmusclefatigueon
gaitparametersafter20minofrestandofferinterpretationsofthe
consequencesofsuchsustainedeffectsongait.
Several possibly interrelated considerations are to be made
regardingtheeffectsofourfatigueprotocol.First,ingeneral,gait
appearstobequiteresistantagainstfatigue[2,4–7].Thefactthat
gait is a very sub-maximal task may explain that some gait
parametersarenotaffectedbymusclefatigue.Specificallychanges
inquadricepsmuscleactivityduringgaitwere,however,expected.
Previously,adecreaseinthequadricepsactivityduringastepof
the ipsilateral leg was found with muscle fatigue during the
approachofastepdown[5].Inaddition,andinlinewithalthough
notnecessarily coincidingwithdecreasedquadricepsactivity,a
decrease in knee moments withfatigue was found during the
stancephaseofthelegfirstlandingonthelowerlevelinstepping
down[7].Alsointheapproachofastepdownandincontrastwith
thepresentfindings,bicepsfemorisactivitywasdecreasedwith
fatigue[5].Allinall,thesedatasuggestthatmusclefatigueeffects
cannot be generalized across these different gait types. The
increasedbicepsfemorisactivityanddecreasedforcegenerating
capacity of thequadriceps muscles foundin the presentstudy
might affectin particular stancephase kinematicsof theknee,
whereakneeextensormomentisusedtogeneratebodyweight
support.However,increasedankleandhipextensormoments,to
whichtheincreasedbicepsfemorisactivitymightcontribute,can
potentiallycompensateforthis[20].
Second,theMVCdatashowednoevidenceofneuromuscular
recovery. The duration of the fatigue protocol was substantial
(13min) and consequently the fatigue induced may have
required longer recovery times than shorter, high-intensity
protocolswould[21].Inducingfatigueunderdynamicconditions,
suchas thesit-to-stand task, does not involvemaximum force
generating duringtheexercise.Thelonger recoverytimes after
contractions of lower force are reportedly due to greater
involvementofperipheralfactorsthaninrecoveryaftermaximum
contractions,whereamorecentralcomponentissuggested[22].
Third,theprotocolmostlikelyaffectedthewholelegsandnot
just the quadriceps muscles. We fatigued participants by a
repetitivesit-to-standtask,whichwe choseforitsecological
validityandrepresentativenessofdailylifeconditions[2].This
fatigueprotocolrequireshighactivityofthequadricepsmuscles,
butinvolvessubstantialactivityandpossiblyfatigueofankle[5]
andhipextensors.Inaddition,themovementtomusclefatigue
may also contains eccentric components, which may lead to
microfailureandpain[12,13]andmightberelatedtothelackof
recovery. Therefore, the fatigue protocol may have affected
variousmusclesofthe(whole)legandnotanisolatedmuscle
group. Fatigue of multiple muscles simultaneously requires
more time for recovery than fatigue of an isolated muscle
[17,23].Moreover,theneuromuscular systemmay beableto
compensatethe deficits causedby muscle fatigueof a single
musclegroupbyadaptingactivityofantagonisticand
synergis-ticmuscles,whereasthismay benotpossibleif thesemuscle
groups, suchas we found in our study, are fatigued as well
[15,16].
Fourthandfinal,ithasbeensuggestedthatwithmoremuscles
fatiguedtherearechangesinthesupraspinalactivityregulating
theactivityofothermuscles,butalsoofmusclespindles[24].The
effects of fatigue-related changes on proprioception may have
contributedtodestabilizingthegait.Toourknowledge,nodataon
recoveryofproprioceptionafterfatigueisavailable.
Thegaitchangesobservedsuggestthatwalkingbecamemore
challenging after the muscle fatigue protocol, as reflected in
adjustments of gait parameters todeal withthe loss of motor
controlandtomaintainstabilityandsafety,corroboratingprevious
studies [3–9]. Specifically, participants increased the base of
support and decreased stride duration, probably to deal with
reducedbalancecontrolinthemedio-lateraldirection[4–7,25].In
addition,thereducedstepfrequencyimpliesmoretimetoplanand
executemovementsandmovementadjustments[26].Highforce
generatingcapacityoflegmusclesisimportanttoperformfastgait
adjustments,forexampletochangedirection,avoidanobject,or
recoverfromanimbalance.Absenceofrecoveryofforcegenerating
capacityafter20minofrestmaythusimplyincreasedriskoffalls
duetoperturbations.Wethereforesuggest,thattopreservegait
stabilityinthepresenceofmusclefatigue,subjectschooseamore
stablegaitpattern,toavoidhavingtomakefastgaitadjustments
andrecoveryresponses.However,thegaitchangesobservedmay
haveanegativeeffect,intermsofanincreasedenergycost[27,28],
whichmight preventrecoveryorcausefurtherfatigue
develop-ment during longer walking episodes. Previous studies have
suggestedthatenergycostdeterminestheselectionofacertain
gaitpattern[29],butourresultssuggestthatoptimizingenergy
costisnotthesoleobjectivewhenwalking.Thechoiceforacertain
gaitpatternmayberelatedtoimprovinggaitstabilityandreducing
fallriskratherthanminimizingenergycost[30].
Participantsincreasedbicepsfemorismuscleactivity,whichis
in contrast to our previous study [5]. In addition, propulsive
impulseswerefoundtobereducedafterthefatigueprotocol.The
increasedbicepsfemorisactivitymayhavebeenusedtopartially
compensatea propulsiondeficitcausedbymusclefatigueorto
compensate reduced weight support, through increased hip
extensionmoments[5,31]orthroughimprovedkneemechanical
efficiency[8,32].Reducedabilitytogeneratepropulsiveanterior–
posterior impulse diminishes the possibility to increase stride
length[30]and,consequently,toimproveorcorrectthebalancein
theforwarddirection,whichcouldincreasetheriskoffallingafter
perturbationsuchastripping.
Thepresentstudywaslimitedtolevelgaitinhealthyyoung
adults. Futurestudiesshouldinvestigate theeffects ofrecovery
after muscle fatigue in populations that are more affected by
fatigueorhaveanincreasedfallrisk,indifferenttypesofgait,such
assteppingdownastepandobstaclecrossing,aswellasrecovery
overalongertimeperiodsafterdifferentfatigueprotocols.Asecond
limitationwasaquitelargestandarddeviationoftheendurance
timeinfatigueprotocol.Althoughlevelsoffatiguemayhavediffered
between participants, maximumforce andmedian frequencyof
both muscles were decreased after the fatigue protocol in all
participants,whiletheratingofperceivedexertionwasincreased.
Wethereforebelievethatthishasnotstronglyaffectedourresults,
althoughitwillhavelimitedthestatisticalpower.Finally,wedidnot
analyzethejointkinematicsandkinetics(ankle,kneeandhipjoint
anglesandmoments).Inourexperimentalprocedures,weusedonly
fourinfraredemittersplacedoverthefeet(seeSection2),which
prevents the calculation of joint kinematics and kinetics. We
recommendforfuturestudiestheanalysisofthesevariablestohave
fullgaitanalysisandtoassessthefatigueeffectsonthedifferent
jointlevelsduringwalking.
In conclusion, our hypotheses were partially confirmed.
Changesinstepwidthandstridedurationcoincidedwithmuscle
fatigue and appear to reflect compensations for impaired gait
stability. In addition, propulsive impulses were reduced while
bicepsfemorisactivitywasincreased.Twentyminutesofrestwas
not enoughfor recoveryof thegaitparameters. These findings
indicatethatthemodulationsofgait,caused bymusclefatigue,
werequitepersistentandmaybeaneffectofthepersistentdecline
offorcegeneratingcapacityofmuscle.
Acknowledgement
The authors thank FAPESP (#2013/12774-0) for financial
support. References
[1]Bigland-RitchieB,WoodsJJ.Changesinmusclecontractilepropertiesand neuralcontrolduringhumanmuscularfatigue.MuscleNerve1984;7:691–9.
[2]BarbieriFA,Santos PC,Lirani-SilvaE,Vito´rioR, GobbiLT,vanDie¨enJH. Systematicreviewoftheeffectsoffatigueonspatiotemporalgaitparameters. JBackMusculoskeletRehabil2013;26:125–31.
[3]ParijatP,LockhartTE.Effectsofquadricepsfatigueonthebiomechanicsofgait andslippropensity.GaitPosture2008;28:568–73.
[4]BarbieriFA,SantosPCR,Vito´rioR,vanDiee¨nJH,GobbiLTB.Effectofmuscle fatigueandphysicalactivitylevelinmotorcontrolofthegaitofyoungadults. GaitPosture2013;38:702–7.
[5]BarbieriFA,LeeYJ,GobbiLTB,PijnappelsM,vanDiee¨nJH.Theeffectofmuscle fatigue on the last stride before stepping down a curb. Gait Posture 2013;37:542–6.
[6]BarbieriFA,dosSantosPC,SimieliL,Orcioli-SilvaD,vanDiee¨nJH,GobbiLT. Interactionsofageandlegmusclefatigueonunobstructedwalkingand obstaclecrossing.GaitPosture2014;39:985–90.
[7]BarbieriFA,GobbiLT,LeeYJ,PijnappelsM,vanDiee¨nJH.Effectoftricepssurae andquadricepsmusclefatigueonthemechanicsoflandinginsteppingdown inongoinggait.Ergonomics2014;57:934–42.
[8]MurdockGH,Hubley-KozeyCL.Effectofahighintensityquadricepsfatigue protocolonkneejointmechanicsandmuscleactivationduringgaitinyoung adults.EurJApplPhysiol2012;112:439–49.
[9]GranacherU,WolfI,WehrleA,BridenbaughS,KressigRW.Effectsofmuscle fatigueongaitcharacteristicsundersingleanddual-taskconditionsinyoung andolderadults.JNeuroengRehabil2010;7:56.
[10]PaduaDA,ArnoldBL,PerrinDH,GansnederBM,CarciaCR,GranataKP.Fatigue, verticallegstiffness,andstiffnesscontrolstrategiesinmalesandfemales.J AthlTrain2006;41:294–304.
[11]vanDiee¨nJH,SpanjaardM,Ko¨nemannR,BronL,PijnappelsM.Mechanicsof toe and heel landing in stepping down in ongoing gait. J Biomech 2008;41:2417–21.
[12]ProskeU,MorganDL.Muscledamagefromeccentricexercise:mechanism, me-chanicalsigns,adaptationandclinicalapplications.JPhysiol2001;537:333–45.
[13]MilletGY,LepersR.Alterationsofneuromuscularfunctionafterprolonged running,cyclingandskiingexercises.SportsMed2004;34:105–16.
[14]OksaJ,Rintama¨kiH,TakataloK,Ma¨kinenT,LusaS,LindholmH,etal. Fire-fightersmuscularrecoveryafteraheavyworkboutintheheat.ApplPhysiol NutrMetab2013;38:292–9.
[15]BoyasS,RemaudA,BissonEJ,CadieuxS,MorelB,BilodeauM.Impairmentin posturalcontrolisgreaterwhenankleplantarflexorsanddorsiflexorsare fatigued simultaneously than when fatigued separately. Gait Posture 2011;34:254–9.
[16]DickinDC,DoanJB.Posturalstabilityinalteredandunalteredsensory envir-onmentsfollowingfatiguingexerciseoflowerextremityjoints.JMedSci Sports2008;18:765–72.
[17]SwaenGM,vanAmelsvoortLG,BultmannU,KantIJ.Fatigueasariskfactorfor beinginjuredinanoccupationalaccident:resultsfromtheMaastrichtCohort Study.OccupEnvironMed2003;60:88–92.
[18]HermensHJ,FreriksB,Disselhorst-KlugC,RauG.Developmentof recommen-dationsforSEMGsensorsandsensorplacementprocedures.JElectromyogr Kinesiol2000;10:361–74.
[19]BorgGAV.Psychophysicalbasesofperceivedexertion.MedSciSportsExerc 1982;14:377–81.
[20]WinterDA.Kinematicandkineticpatternsinhumangait:variabilityand compensatingeffects.HumMovSci1984;3:51–76.
[21]LattierG,MilletGY,MartinA,MartinV.Fatigueandrecoveryafter high-intensity exercise part I: neuromuscular fatigue. Int J Sports Med 2004;25:450–6.
[22]LinnamoV1,Ha¨kkinenK,KomiPV.Neuromuscularfatigueandrecoveryin maximalcomparedtoexplosivestrengthloading.EurJApplPhysiolOccup Physiol1998;77:176–81.
[23]YaggieJA,McGregorSJ.Effectsofisokineticanklefatigueonthemaintenance ofbalanceandposturallimits.ArchPhysMedRehabil2002;83:224–8.
[24]PearsonK,GordonJ.Spinalreflexes. In:KandelER,SchwartzJH,JessellTM, editors.Principlesofneuralscience.NewYork:McGrawHill;2000.p.713–36.
[25]HofAL,vanBockelRM,SchoppenT,PostemaK.Controloflateralbalancein walking.Experimentalfindingsinnormalsubjectsandabove-kneeamputees. GaitPosture2007;25:250–8.
[26]HakL,HoudijkH,BeekPJ,vanDiee¨nJH.Stepstotaketoenhancegaitstability: theeffect ofstride frequency,stridelength,and walkingspeedonlocal dynamicstabilityandmarginsofstability.PLoSOne2013;8.
[27]IjmkerT,HoudijkH,LamothCJ,BeekPJ,vanderWoudeLH.Energycostof balancecontrolduringwalkingdecreaseswithexternalstabilizerstiffness independentofwalkingspeed.JBiomech2013;46:2109–14.
[28]RibeiroF,MotaJ,OliveiraJ.Effectofexercise-inducedfatigueonpositionsense ofthekneeintheelderly.EurJApplPhysiol2007;99:379–85.
[29]BertramJE.Constrainedoptimizationinhumanwalking:costminimization andgaitplasticity.JExpBiol2005;208:979–91.
[30]BarelaAM,DuarteM.Biomechanicalcharacteristicsofelderlyindividuals walkingonlandandinwater.JElectromyogrKinesiol2008;18:446–54.
[31]Vila-Cha˜ C,RiisS,LundD,MøllerA,FarinaD,FallaD.Effectofunaccustomed eccentricexerciseonproprioceptionofthekneeinweightandnon-weight bearingtasks.JElectromyogrKinesiol2011;21:141–7.