Muscle Activity Adaptations to Spinal Tissue Creep in the Presence of Muscle Fatigue

14 Pages·2016·0.39 MB·French

RESEARCHARTICLE
Muscle Activity Adaptations to Spinal Tissue
Creep in the Presence of Muscle Fatigue
JacquesAbboud1☯*,FrançoisNougarou2,MartinDescarreaux3☯
1 Départementd’Anatomie,UniversitéduQuébecàTrois-Rivières,Québec,Canada,2 Départementde
GénieÉlectrique,UniversitéduQuébecàTrois-Rivières,Québec,Canada,3 DépartementdesSciencesde
l’ActivitéPhysique,UniversitéduQuébecàTrois-Rivières,Québec,Canada
☯Theseauthorscontributedequallytothiswork.
*[email protected]
Abstract
Aim
Theaimofthisstudywastoidentifyadaptationsinmuscleactivitydistributiontospinaltis-
suecreepinpresenceofmusclefatigue.
OPENACCESS Methods
Citation:AbboudJ,NougarouF,DescarreauxM Twenty-threehealthyparticipantsperformedafatiguetaskbeforeandafter30minutesof
(2016)MuscleActivityAdaptationstoSpinalTissue passivespinaltissuedeformationinflexion.Rightandlefterectorspinaeactivitywas
CreepinthePresenceofMuscleFatigue.PLoSONE
recordedusinglarge-arrayssurfaceelectromyography(EMG).Tocharacterizemuscle
11(2):e0149076.doi:10.1371/journal.pone.0149076
activitydistribution,dispersionwasused.Duringthefatiguetask,EMGamplituderoot
Editor:FrancescoCappello,UniversityofPalermo,
meansquare(RMS),medianfrequencyanddispersioninx-andy-axiswerecompared
ITALY
beforeandafterspinalcreep.
Received:October9,2015
Accepted:January26,2016 Results
Published:February11,2016 Importantfatigue-relatedchangesinEMGmedianfrequencywereobservedduringmuscle
Copyright:©2016Abboudetal.Thisisanopen fatigue.Medianfrequencyvaluesshowedasignificantmaincreepeffect,withlowermedian
accessarticledistributedunderthetermsofthe frequencyvaluesontheleftsideunderthecreepcondition(p(cid:1)0.0001).Asignificantmain
CreativeCommonsAttributionLicense,whichpermits
creepeffectonRMSvalueswasalsoobservedasRMSvalueswerehigheraftercreep
unrestricteduse,distribution,andreproductioninany
deformationontherightside(p=0.014);asimilartendency,althoughnotsignificant,was
medium,providedtheoriginalauthorandsourceare
credited. observedontheleftside(p=0.06).Asignificantcreepeffectsforx-axisdispersionvalues
wasobserved,withhigherdispersionvaluesfollowingthedeformationprotocolontheleft
DataAvailabilityStatement:Allrelevantdataare
withinthepaper. side(p(cid:1)0.001).Regardingy-axisdispersionvalues,asignificantcreepxfatigueinteraction
effectwasobservedontheleftside(p=0.016);asimilartendency,althoughnotsignificant,
Funding:UniversitéduQuébecàTrois-Rivières
ExcellenceFundandtheNaturalSciencesand wasobservedontherightside(p=0.08).
EngineeringResearchCouncilofCanada.The
fundershadnoroleinstudydesign,datacollection
Conclusion
andanalysis,decisiontopublish,orpreparationof
themanuscript. Combinedmusclefatigueandcreepdeformationofspinaltissuesledtochangesinmuscle
activityamplitude,frequencydomainanddistribution.
CompetingInterests:Theauthorshavedeclared
thatnocompetinginterestsexist.
PLOSONE|DOI:10.1371/journal.pone.0149076 February11,2016 1/14
CreepDeformationandTrunkNeuromuscularControl
Introduction
Spinestabilityisoftendescribedasacomplexmechanisminvolvingthreeessentialcompo-
nents:spinalmuscles,passivespinaltissuesandneuromuscularcontrol[1].Undernormalcon-
ditions,thesesubsystemsarehighlycoordinatedandoptimizedtoprovideadequatestabilityof
thespine.However,intheabsenceofmusclestoprovidespinalstability,compressiveloadsas
lowas100Ncanleadtobucklingoftheentirelumbarspine[2].Conversely,whenspinalmus-
clesareactivated,individualscanwithholdspinalloadsof4000Nwithoutreportinganypain
orundesirableeffects[3].Moreover,ithasbeenhypothesizedthatchangesinmusclerecruit-
mentpatterns,suchasmuscleco-contraction,actascompensationforspinalinstabilityresult-
ingfrompassiveelementslaxityorreducedneuromuscularcontrol[1,4].
Suchadaptationsinmusclerecruitementpatternscanalsobeobservedwiththeuseof
large-arrayssurfaceelectromyography(EMG)undertheinfluenceofmusclefatigue[5].
Indeed,amigrationofmuscleactivityhasbeendescribedduringalowbackmusclefatiguetask
[5,6].Moreover,large-arrayssurfaceEMGhasbeenshowntobearelevanttoolintheidentifi-
cationofdistinctivemusclerecruitmentstrategiesbetweensympatomaticvsasymptomatic
individualsindifferentlowbackregionsthroughdifferentmotortasks[7,8].Zwartsshowed
thatlarge-arrayssurfaceEMGoffersuniquespatialinformationtoourknowledgeregarding
thedistributionofmuscleactivity,suchasmotorunitactivation.[9].
Ontheotherhand,spinalinstabilityassociatedwithadeformationofpassivespinaltissues,
asitoccursinrepetitiveexposuretoprolongeddeeptrunkflexion,hasbeenassociatedwiththe
developmentoroccurrenceoflowbackpain(LBP)anddisorders[10–12].Thisassociation
couldpartlybeexplainedbythecombinationofgraduallyincreasingcreepintheviscoelastic
tissuesanddecreasesinreflexivemuscularactivationthatleavethespinewithdiminishedpro-
tectionfrominstability[13].Experimentallyinducedlowbackmusclecreephasbeenusedin
severalstudiestofurtherourunderstandingofthepassiveandactivestructurecontributionto
spinalstability[14–21].Inthesestudies,active(dynamic)orpassive(static)flexion-extensions
ofthetrunkarethemostcommonlyusedprotocolstoinducespinalcreep.Thesesustainedor
repeatedmovementsusuallyleadtoanincreaseinthetrunkflexionrangeofmotion[15–18,
22].Indeed,thecreepinthespineligamentsisthoughttoincreasetheintervertebraljointslax-
ity,allowingincreasedrelativemotion.
Thelaxitydevelopedinthespinefromthecreepintheviscoelastictissuesofligaments,
discsandjointcapsulesisrelativelysmall,andcaneasilybecompensatedbymoderateadjust-
mentsintheco-contractionlevelsofagonistandantagonistmuscles[23].However,theeffects
ofactiveorpassiveprolongeddeepflexionsofthetrunkonlowbackmuscleactivityarenot
wellunderstood.Indeed,nochangehasbeenobservedinthetimingofmuscleactivationonset
forthelowererectorspinaemusclesfollowingastaticpassivelumbarflexionperiodof10[19]
or15minutes[14],whereasonsetlatencyofthesamemusclesincreasedafteronehourofstatic
passivelumbarflexion[20].Olsonetal.showedthatnodifferenceexistsregardingonset
latencyofthelowererectorspinaemusclesfollowingeitheractiveorpassivetrunkflexion-
extensionrepetitions[21].Furthermore,humaninvivostudiesindicatethataprolongedtrunk
flexionresultsinahigherparaspinalmusclereflexgain[14],whilerepeatedlyappliedshort-
durationcreepreducesspinalreflexresponses[15].Decreasedprotectivemuscularreflexwas
showntobethedirectmanifestationofmechanoreceptordesensitizationcausedbylaxityin
theviscoelastictissuesofthespine[23].Lastly,thespinalstabilizingsystemactsbyaltering
muscleactivationpatternsviathenervoussysteminresponsetotheligamentoustissuemecha-
noreceptorafferentsignals.Spinalmuscularactivityisthengeneratedinordertocompensate
thedecreasedcontributionofviscoelastictissuesbyimplementingalternativerecruitment
strategiessuchastheco-contractionoftrunkmuscles[4,24].
PLOSONE|DOI:10.1371/journal.pone.0149076 February11,2016 2/14
CreepDeformationandTrunkNeuromuscularControl
Undertheinfluenceofbackmusclefatigue,asimilarreorganizationofmotorstrategiesis
implementedtoperformthefatiguetask.Indeed,manystudieshaveshownadaptationsin
recruitmentpatternsduringmusclefatigue[6,8,25].Moreover,lowbackmusclefatigueseems
tobeassociatedwithchangesinmotorreflexactivityfollowingunexpectedposturalperturba-
tion[26–28].Additionnally,creepdeformationhasbeenshowntoalterpassivestructures,
whichareknowntoplayacrucialroleinlowerbackspinalstability[1].
ArjmandandShirazisuggestedthatstaticflexionofthetrunk,whichinducescreepdefor-
mationofthepassivestructures,maybeasignificantriskfactorforlowbackdisordersor
developmentofmusclefatigue[29]andcanpossiblyincreasethedemandonothertrunkstabi-
lizingstructures.
Theaimofthisstudywastodescribetheeffectofspinaltissuecreeponmuscleactivitydistri-
butioninpresenceofmusclefatigue.BasedonpreviousstudiesshowingthatincreasesinEMG
amplitudesignalsareobservedundertheinfluenceoflowbackcreepdeformation,itwashypoth-
esizedthatbackmusclerecruitmentstrategies,whicharebelievedtoplayanimportantrolein
redistributingstabilizationefforts,willbemodifiedfollowingasofttissuecreepinthespine.
MaterialsandMethods
Participants
Twenty-threehealthyadultparticipantswithouthistoryofLBPwererecruited.Thisgroupwas
composedof12womenand11men(mean(SD):age=26.7years(5.1);height=1.70m(0.1);
weight=67.7kg(14.2);BMI=23.2kg/m2(3.9)).Exclusioncriteriawere:anyhistoryofacute/
chronicthoracicorlowbackpaininthepast6months,ankylosingspondylitis,trunkneuro-
musculardisease,inflammatoryarthritis,scoliosis((cid:3)15°),andpreviousspinalsurgery.The
projectreceivedapprovalfromtheUniversity’sethicscommitteeforresearchwithhumans
(Comitéd'éthiquedelarechercheavecdesêtreshumains)andallparticipantsgavetheirwrit-
teninformedconsentpriortotheirparticipationinthestudy.
Experimentalprotocol
Eachsubjectparticipatedinoneinitialexperimentationduringwhichtheyperformedamaxi-
malvoluntaryisometrictrunkextensioncontraction(MVC),rangeofmotion(ROM)assess-
mentanda1-minutefatiguetaskbeforebeingsubmittedtothe30-minutepassivetissue
deformationcondition.Aftercreepdeformationwasobtained,theROMassessmentandthe
fatiguetaskwereconductedagain.Alltogether,thetwoROMtestswererepeated3timeseach.
First,thetrunkanglewasmeasuredbyplacingthedigitalinclinometer(DualerIQPro™Digital
Inclinometer,JTECHMedical;USA)ontheL3vertebra.Theparticipantsstooduprightand
thentiltedthetrunkforwardasmuchaspossible,withoutbendingtheknees.TheROMwas
alsomeasuredbyaskingtheparticipanttositonthefloorandcompletelyrestthesolesoftheir
feetagainstthestandardFlex-Tester(BaselineSitn’ReachBox,FabricationEnterprisesInc.,
USA).Withtheirarmsandfingersinfullextensioninfrontofthem,participantswereaskedto
pushthemetalplatethefarthesttheycould,withoutbendingthekneessothatthetrunkleaned
forwardasmuchaspossible.Theflexionpositionwasmaintainedfor2secondsbeforepartici-
pantswereallowedtosituprightagain.
TheMVCprotocolwasperformedpriortothefatigueprotocol.Participantswereaskedto
layinapronepositionona45°Romanchair,withtheiliaccrestsalignedwiththechaircush-
ionedge.Abeltfixedtothegroundandinstalledoverparticipantsshouldersresistedtheforce.
ThefatigueprotocolconsistedofamodifiedversionoftheSorensenendurancetest[30],exe-
cutedinthesamepositionastheMVCprotocol.Inordertoquicklyinducemuscularfatigue,
participantshadtolifta12.5-kilogramweightplateduringthetask.Theplatewasheldasclose
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CreepDeformationandTrunkNeuromuscularControl
Fig1.Illustrationofthelowbackcreepdeformationprotocol.
doi:10.1371/journal.pone.0149076.g001
aspossibletothechestbytheparticipants.Theparticipants’trunkwasmaintainedunsup-
portedinahorizontalpositionrelativetothegroundforoneminute.Immediatelyafterthe
fatigueprotocol,participantswereaskedtoperformthedeformationprotocol.Perceivedeffort
scale(6–20)[31],measuringtheintensityofthefatiguetask,wasratedbyeachparticipantat
theendofthefatiguetest.
Thelowbackcreepdeformationprotocolstartedwiththeparticipantssittingonabench
andthenbendingforward,sothattheirtrunkwassupportedbyatable(Fig1).Participants’
trunkswereflexedbyapproximately75%oftheirrangeoffulltrunkflexion.Theirlegswere
alsoflexedby90degreestolimittheoccurrenceofharmstringmusclesstretching.Theymain-
tainedthispositionfor30minutes.Immediatelyafter,theROMwasmeasuredagainbythe2
previouslymentionedtests,andthefatiguetaskswereperformedasecondtimeafterwards.
Lumbarmuscles’activation(EMG)wasobtainedonlyduringthefatiguetaskandconsequently
assessedbeforeandafterthedeformationprotocol.
DataAcquisition
Rightandlefterectorspinae’activitywasrecordedusingtwolarge-arrayssurfaceEMGmatrices
(modelELSCH064;LISiN-OTBioelettronica;Torino,Italy).Thearraygridconsistedof64elec-
trodesplacedinan8x8matrix(10mminter-electrodedistance).Thecenterofeachgridwas
locatedatL3level(Fig2),andonegroundelectrodewasplacedontheleftulnarprocess.Skin
impedancewasreducedbyshavingbodyhair,gentlyexfoliatingtheskinwithfine-gradesandpa-
per(RedDotTracePrep,3M;St.Paul,MN,USA)andwipingtheskinwithalcoholswabs.The
bipolarEMGsignalswereamplified(64-channelsurfaceEMGamplifier,SEA64,LISiN-OT
Bioelettronica;Torino,Italy;–3dBbandwidth10–500Hz)byafactorof2000,sampledat2048
Hzandconvertedtodigitalformbya12bitA/Dconverter.Thedatawerecollectedusingthe
OTBioelettronicacustomsoftwareandprocessedbyMatlab(MathWorks;Natick,MA,USA).
DataAnalysis
TheROMmeasuredinastandingpositionusinganinclinometerwasassessedfollowingthe
AmericanMedicalAssociationrecommendations[32].Toestablishtheinitialposition,the
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CreepDeformationandTrunkNeuromuscularControl
Fig2.Representationoftwo64-electrodematricesusedintherecordingoferectorspinaemuscle
activity(modelELSCH064;LISiN-OTBioelettronica,Torino,Italy).
doi:10.1371/journal.pone.0149076.g002
individualswerestandingwiththeirkneesextendedandtheirweightbalancedonbothfeet
(spinewasinaneutralposition).Thepositionofeachparticipantwasverifiedbythesame
experimentertolimitmeasurementerrors.TheSitn’Reachtestwasperformedusingthepro-
ceduresoutlinedintheAmericanCollegeofSportsMedecine(ACSM)manual[33].Forboth
ROMtests,thehighestvaluefromthe3trialswasconsideredforallanalyses.
EachbipolarEMGsignalobtainedfrombothmatriceswasdigitallyband-passfilteredinthe
frequencybandwidth20-450Hz(2ndorderButterworthfilter).Notchfilterswerealsoapplied
toeliminatethe60Hzpowerlineinterferenceanditsharmonics.Asdescribedinaprevious
study,dispersionwasobtainedbycalculatingthecenterofgravitydispersionduringtheSoren-
sentestofagivensubject[8].Inshort,myoelectricsignalsfromeachelectrodewerenormal-
izedwiththebaselineEMGsignalobtainedfromMVCtrials.Eachelectrode-filteredsignalwas
thendividedinLwindowsof0.5sforwhichanindividualrootmeansquare(RMS)valuewas
computed.Foreachwindow,themeanofallelectrodesRMSwascalculatedandcorrespond
thecentroidposition.Tocharacterizemuscleactivitydistribution,thedispersionvariableinx-
andy-axis,representingthemuscleactivityrangeofdisplacement(centroid),wasextracted
fromthebipolarEMGsignals.Thex-axiscorrespondstothemediolateraldirection,whilethe
y-axiscorrespondstothecephalic-caudaldirection.Inordertoconfirmthepresenceofmuscle
fatigueinbothconditions(nocreepandcreep),themeannormalizedslopeofthemedianfre-
quency(MDF)(meanofthe64electrodesofeachmatrix)wascalculatedusingthesamemeth-
odsastheoneusedforRMS.TheFouriertransformfunctionfromMatlabsoftware
(MathWorks;Natick,MA,USA)wasusedtocalculatetheMDFvalues.TheMDFwasdefined
asthefrequencythatdividedthespectrumintotwoequalareas.Eachsignalswasthendivided
in0.5swindowswithoutoverlapforwhichanMDFvaluewascomputed[34].Morespecifi-
cally,MDFvalueswereobtainedthrougheachelectrodesignal.TheslopeofMDFwasthencal-
culatedforeachelectrode.Finally,avaluerepresentingthemeanslopeofMDFwasobtained.
Statisticalanalyses
NormalityofdistributionforeverydependentvariablewasassessedusingtheKolmogorov–
Smirnovtest,inadditiontovisualinspectionofthedata.Thet-testfordependentsampleswas
usedtocompareratesofperceivedeffortattheendofthefatiguetestbeforeandafterthe
deformationprotocol.Rangesofmotionmeasuredbythedigitalinclinometerandthe“Sitn’
ReachBox”werealsocomparedbeforeandafterthedeformationprotocolusingthet-testfor
dependentsamples.Thet-testfordependentsampleswasalsousedtocomparenormalized
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CreepDeformationandTrunkNeuromuscularControl
MDFslopesbeforeandafterthedeformationprotocol.EMGmusclevariables(meanMDF,
meanRMS,dispersioninx-andy-axis)datawerecomparedbetweenthetwoconditions(no
creepandcreep)usingatwo-wayrepeated-measureanalysisofvariance(ANOVA)toassess
themaineffectsofcreepandfatigue(earlyfatigue:10firstsecondsandlatefatigue:10lastsec-
ondsoftheSorensentest).Whennecessary,theTukeyposthoctestwasperformedasthepost
hocanalysesforpair-wisecomparisons.Forallstatisticalanalyses,p<0.05wasconsideredto
bestatisticallysignificant.
Results
Fromthe23originalparticipants,threewereexcludedfromEMGanalysesduetohighlevelsof
EMGnoiseinrecordings.
Impactsofmusclefatigue
Importantfatigue-relatedchangesinsEMGtime-frequencywereobservedduringthefatigue
protocol.Dependentt-testsrevealednosignificantdifferencebetweenthebefore-deformation
condition(ontheleftside:mean=–0.30;SD=0.09andontherightside:mean=–0.29;
SD=0.12)andafter-deformationcondition(ontheleftside:mean=–0.29;SD=0.10andon
therightside:mean=–0.27;SD=0.19)regardingthenormalizedMDFslopes(p(cid:3)0.05).There
wasalsonodifferenceregardingtheratedperceivedeffort(beforedeformation,mean=13.2/
20;SD=2.9andafterdeformation,mean=13.6/20;SD=3.2)(p>0.05).
Creepdeformationeffects
Rangeofmotion. RegardingtheROMcomparisonbeforeandaftercreepdeformation,
resultsshowedasignificantincreaseinROMafterthedeformationprotocolmeasuredbythe
Sitn’ReachBoxtest(p=0.02).However,nodifferencewasfoundregardingROMmeasured
bytheinclinometer(p=0.42).
MDF. TheANOVArevealedmainsignificantfatigueeffectsonMDFforbothconditions.
Asexpected,MDFwaslowerattheendofthefatiguetaskincomparisontoitsbeginningon
therightside[F(1,19)=80.73,p(cid:1)0.0001]andtheleftside[F(1,19)=178.51,p(cid:1)0.0001].
Moreover,resultsofMDFvaluesshowedasignificantmaincreepeffect,withlowerMDFval-
uesontheleftside[F(1,19)=38.73,p(cid:1)0.0001]underthecreepcondition,butnodifference
wasobservedontherightside[F(1,19)=2.37,p=0.14](Fig3B).
Fig3. MeanRMS(A)andMDF(B)valuesovertimeontherightandleftsides(RMS:RootMeanSquare;
MDF:MedianFrequency).Errorbarsindicatestandarddeviations.$representsamaineffectoffatigue.✦
representsamaineffectofcreep.Posthocresultsareillustratedby*=p<0.01and**=p<0.001.
doi:10.1371/journal.pone.0149076.g003
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CreepDeformationandTrunkNeuromuscularControl
Fig4. Meandispersionvaluesinx-axis(A)andy-axis(B)valuesovertimeontherightandleftsides
(DispX:Dispersioninx-axis;DispY:Dispersioniny-axis).Errorbarsindicatestandarddeviations.$
representsamaineffectoffatigue.✦representsamaineffectofcreep.Posthocresultsareillustratedby
*=p<0.01.
doi:10.1371/journal.pone.0149076.g004
RMS. TheANOVArevealedasignificantmaincreepeffectonmeanRMSvalues,asRMS
washigheraftercreepdeformationontherightside[F(1,19)=7.31,p=0.014]andasimilar
tendendy,althoughnotsignificant,wasobservedontheleftside[F(1,19)=3.92,p=0.06].The
ANOVAalsorevealedasignificantmainfatigueeffectonmeanRMSvalues.RMSvalueswere
higherattheendofthefatiguetaskontherightside[F(1,19)=25.70,p(cid:1)0.0001]andtheleft
side[F(1,19)=32.20,p(cid:1)0.0001].Finally,theanalysesalsorevealedasignificantinteraction
effect(creepxfatigue)ontheright[F(1,19)=7.26,p=0.014]andleftside[F(1,19)=8.93,
p=0.008].AsillustratedinFig3A,posthocanalysesrevealedsignificantdifferencesduringthe
first10seconds,withhigherRMSvaluesunderthecreepcondition.
X-axisdispersion. TheANOVArevealedmainsignificantcreepeffectsforx-axisdisper-
sionvalues,withhigherdispersionvaluesfollowingthedeformationprotocolontheleftside[F
(1,19)=5.92,p(cid:1)0.001],butnotontherightside[F(1,19)=0.86,p=0.36].Moreover,the
ANOVAshowedasignificantmainfatigueeffectonx-axisdispersionvalueswheredispersion
wassignificantlyhigherbytheendofthefatigueprotocolontheleftside[F(1,19)=17.0,
p(cid:1)0.001],butnotontherightside[F(1,19)=1.43,p=0.25](Fig4A).Reprensatativedataof
thedispersionarepresentedinFig5.
Y-axisdispersion. TheANOVArevealedmainsignificantfatigueeffectsony-axisdisper-
sionvalueswheredispersionwassignificantlyhigherbytheendofthefatigueprotocolonthe
rightside[F(1,19)=7.49,p=0.013]andontheleftside[F(1,19)=5.77,p=0.027].Theanaly-
sesalsoshowedasignificantcreepxfatigueinteractioneffectontheleftside[F(1,19)=6.95,
p=0.016];asimilartendency,althoughnotsignificant,wasobservedontherightside[F(1,19)
=3.44,p=0.08](Fig3B).AsillustratedinFig4B,posthocanalysesrevealedhigherdispersion
valuesonthey-axisunderthecreepconditionduringthefirst10secondsofthefatiguetask.
ReprensatativedataofthedispersionarepresentedinFig5.
Discussion
Thestudy’smainobjectivewastoidentifymuscleactivityadaptationstospinaltissuecreepin
thepresenceofmusclefatigue.Theresultsshowedthatprolongedflexionofthetrunkledto
adaptationsinmuscleactivitydistribution.Indeed,highervaluesofamplitudefromlumbar
erectorspinaemyoelectricsignals,aswellashigherdispersionvalues,wereobservedinthe
presenceofspinaltissuecreep.
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CreepDeformationandTrunkNeuromuscularControl
Fig5.Typicalrepresentationofdispersiondatafromaparticipantontherighterectorspinae.The
large-arrayEMGwasenlargedtobetterobserveddispersiondata.Boldblacklinesillustratethemigrationof
thecentroidduringtheearly(upperpartofthefigure)andlate(lowerpartofthefigure)musclefatigue.Note
theshiftinthedistributionofEMGamplitudetowardthecaudalregionofthelumbarerectorspinae(grey
lines).
doi:10.1371/journal.pone.0149076.g005
Toconfirmthepresenceofspinaltissuecreep,ROMvalueswerecalculatedbeforeandafter
thedeformationprotocol.Althoughlimited,anincreaseinROMwasobservedfollowingspinal
tissuecreep.Overall,theincreaseinfullflexionanglemightresultfromthecombinedvisco-
elasticelongationofhamstringanderectorspinaemuscles.Despitetheoveralltendency
observed,thetwoROMtestsyieldeddifferentresults.Suchdisparitycouldbeexplainedbythe
differencesbetweenthetasksandinstruments.Thestandingposition,aspreviouslydescribed,
isassociatedtoaco-contractionphenomenonofposteriorandanteriortrunkmuscleswhich
couldpossiblyexplainedadecreasedROMinfullflexionofthetrunk.Indeed,anincreasein
trunkmuscleactivityhasbeenshowninstandingposturewhencomparedtosittingposture
[35].Itisalsopossiblethattheactivationoftheanteriormuscles(rectusabdominis)contrib-
utestoanincreasedabilityofthetrunktotravelthroughagreaterrangeoftrunkflexion.Using
aninclinometer,insteadofadualinclinometer,providesaglobalevaluationofthelowerlimb
andbackantigravitymuscles,whereasadualinclinometershouldbeconsideredtoassessthe
specificlumbarspinechangesfollowingcreepdeformation[36].
Inthepresentstudy,participantswereaskedtoperformatrunkextensormusclefatigue
taskforoneminute.Thepresenceofanacutelowerbackmusclefatiguephenomenonwas
indicatedbyamarkeddecreaseinthemeanMDFslope,whichisconsideredareliableindica-
torofmusclefatigue[37],aswellasascoreoftheratedperceivedeffortscalecategorized
between“somewhathard”and“hard”.Moreover,similarnegativeslopeswerefoundbefore
andafterthedeformationprotocol,andparticipantsratedsimilarperceptionofeffortscoresat
theendofthefatiguetask.Theseresults,asawhole,indicatethatparticipantsseemedtobein
asimilarstateoffatigueinbothconditions(nocreepandcreep).Ontheotherhand,differ-
encesappearedwhenthemeanMDFwasconsidered.Indeed,lowervaluesofmeanMDFwere
observedinthepresenceofspinaltissuecreep.Duringearlyfatigue,MDFvaluesaredeter-
minedbymusclefibertypedistribution[38].ThefrequencyshifttowardslowerMDF,inthe
presenceofmusclefatigue,hasbeenassociatedtochangesinmotorunitrecruitementandsyn-
chronisationaswellaschangesinconductionvelocityandmusclefibertypes[39,40].These
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CreepDeformationandTrunkNeuromuscularControl
resultsareinaccordancewiththoseofShinandal.,whoobservedareductioninmedianpower
frequencyduringsubmaximalextensioncontractionof15and30%ofparticipants’5-seconds
maximalvoluntarycontractions,followingastatictrunkflexion[41].Theseobservationstaken
together,couldsuggestthatfollowingspinaltissuecreep,fatigue-relatedphenomenomsare
facilitated.Itcanbehypothesizedthatprolongedtrunkflexionleadstopassivetissuedeformar-
tionwhichmayincreasetrunkmusclecontributiontospinalstabilizationmechanismsduring
fatigue.AnotherstudyconductedbyHowarthetal.foundareductioninmedianpowerfre-
quencyafterrepetitiveactivespineflexions;however,thisdifferencewasnotstatisticallysignif-
icant[18].Inthisstudy,themedianpowerfrequencywasassessedduringaSorensentest
lasting5seconds,whereasrecordingslastedoneminuteinthepresentstudy.Methodological
considerationsmightthereforeexplainthedifferencesobservedbetweentheresultsofboth
studies.
Withregardtomuscleactivationamplitude(RMSvalues),highervalueswereobserved
immediatelyfollowingthedeformationprotocol.Itisimportanttonotethatthesecondfatigue
taskwasconducted30minutesafterthefirstone,anditisunlikelythattheincreaseinRMS
wasassociatedtoaresidualeffectofthefirstfatiguetask.Indeed,Larivièreetal.showedthata
restperiodof10to15minutesfollowingabackmusclefatiguetaskisenoughtoallowcomplete
backmusclerecovery[42].
RMSvaluesweresimilarinbothconditionsattheendofthefatigueprotocol,withaten-
dencytowardshighervaluesafterthedeformationprotocol.Inthepresenceofmusclefatigue,
anincreaseofEMGamplitudesignalswasalsoobservedinthepreviousstudy5or10minutes
afterperformingliftingtrialsinstaticlumbarfullflexion[16,41].Indeed,theincreasedactivity
ofextensormusclessuggeststhatincreasedmuscleactivationisrequiredtogeneratemore
activeforcestocompensateforthelossofcontributionofpassivetissuestospinalstability[43].
Moreover,Toosizadehetal.showedthattrunkmuscleactivitymeasuredbyRMSincreasedby
5%followingcreepdeformationinducedbyrepetitiveliftingtasks[44].Giventhatthemoment
armsofparaspinalmusclesarerelativelysmall[45],onlysmallincreasesinmuscleforcesare
neededtoincreasespinalloadsandcompensateforreducedspinalstability.
Itiswellknownthatneurophysiologicalperturbations,suchasmusclefatigueormusculo-
skeletalpain,areassociatedwithalteredmusclesrecruitmentdistribution[7,8,46].Thepres-
entstudyisthefirstoneinvestigatingmuscleactivitydistributioninthepresenceofspinal
tissuecreep.Dispersionofmuscleactivity,representingthemuscleactivityrangeofdisplace-
ment,wasusedtoidentifyrecruitmentstrategiesadaptationsduringthefatiguetaskbeforeand
afterthedeformationprotocol.Anincreaseindispersionvalueswasobservedthroughoutthe
fatiguetask,whichisinaccordancewithpreviousstudies[5,8].Indeed,acaudalandlateral
shiftofthemuscleactivitywasobservedinthecurrentstudy.Thisfindingssupportotherstud-
iesthatspecificallyreportedacaudalshiftofbackmuscleactivitycentroidduringmuscle
fatigueinasymptomaticparticipants[5,6].Thisobservationsuggestsvariationsinthedistribu-
tionofmusclefibertypesthroughoutsegmentsoflumbarerectorspinae.Indeed,alarger
decreaseinEMGpowerspectralfrequency,aswellasasimultaneousincreaseinEMGampli-
tudehavealsobeenshowedtothelowerpartoflumbarmusclesincomparisontoupperpart
undertheinfluenceofmusclefatigue[47,48].Moreover,higherdispersionvalueswere
observedatthebeginningofthefatiguetaskunderthespinaltissuecreepcondition.Asdis-
cussedearlier,adaptationsinrecruitmentstrategies,suchasco-contractionoftrunkmuscles,
havebeendescribedaspotentialstrategiestocompensatethedecreasedcontributionofvisco-
elastictissues[4,24].Thepresentstudyshowsthatmuscleactivityadaptationscouldalso
occurwithinthesamemusclethroughanincreaseinmuscleactivitydistributioninresponse
tospinaltissuecreep.Itcanbehypothesizedthatlong-lastingcreepdeformationwillincrease
spinalpassivetissuemechanoreceptorsthreshold,leadingtoincreasedmuscleactivityduring
PLOSONE|DOI:10.1371/journal.pone.0149076 February11,2016 9/14
CreepDeformationandTrunkNeuromuscularControl
staticlumbarextension.Ligamentscontainmechanoreceptorsactingastransducers,sending
posturalinformationtothecentralnervoussystem.Therefore,followingaspinaltissuecreep
andunderposturalinstability,thecentralnervoussystemrepliesviaanappropriateandcoor-
dinatedfeedbackmuscularaction[1,49].Thissuggeststhatspinaltissuecreepyieldsneuro-
muscularadaptations(redistributionofmuscleactivity)similartothoseobservedunder
musclefatigueormuscularpainconditions.Furthermore,prolongedpassivestretchingofthe
musclesmightcauseviscoelasticdeformationandsubsequentfatigue-likechangesofthelum-
barerectorspinaemuscles[50,51],whichisconsistentwithourobservationoflowervaluesof
MDFinthepresenceofspinaltissuecreep.Reductioninmotorunitactivationandaverage
conductionvelocityfollowingpassivestretchinghaveindeedbeendescribed[52,53].Despite
theoveralltendencytoobservecreepeffectsinmuscleactivitydistribution,asignificantx-axis
dispersiondifferencewasonlyobservedontheleftside.Infact,x-axisdispersionsaremodest
withhigherlevelsofvariabilitythany-axisdispersion,andthesignificanteffectobservedon
theleftsidemaybeduetoaslightmisalignmentofthearrayswithrespecttothefiberorienta-
tionand/ortochangesinlocationoftheinnervationzoneovertimeaspreviouslysuggestedin
otherstudies[54].
Dispersionvalues,however,weresimilarattheendofthefatiguetask,whethertherewas
spinaltissuecreepornot.Dispersioninx-axisremainedhighafterthedeformationprotocol,
whereasdispersioniny-axisdecreasedinpresenceofspinaltissuecreep.Thephysiological
mechanismsunderlyingthisphenomenonremainunclear.Itcouldbehypothesizedthatthe
centralnervoussystem,whenmusclefatigueandspinaltissuecreeparecombined,strivesto
maintainvertebralstabilityusingincreasedmuscleactivation,butlessvariableneuromuscular
recruitmentpatterns.
Recommendationsforfuturestudies
Lowbackmusclemotorunitrecruitmentandadaptationunderspinaltissuecreepconditions
shouldbeinvestigatedtodocumentthephysiologicalphenomenonunderlyingchangesin
musclerecruitmentstrategies.Additionally,sincetheeffectofcreepdeformationonmuscular
stabilizingactivitypartiallyrecoversupto25%followinga10-minuterest[23]orupto50%
followinga25-minuterest[22],futurestudiesshouldfocusondocumentingcreepdeformation
effectsduringprolongedfatiguingexercises.
Limitations
Thestudy’slimitationsincludetheparticipants’status(younghealthyadults),whichmaylimit
thegeneralizationofresults.ThreeparticipantswerealsoexcludedfromEMGanalysesdueto
highlevelsofEMGnoiseinrecordings.Specifically,EMGsignalsfrom2participantscouldnot
beusedasthegroundelectrodedisconnectedduringthesecondSorensentest.Theotherpar-
ticipantwasnotincludedintheanalysesbecauseEMGarraysfailedtoproperlyrecordEMG
signalsduringthefirstSorensentest.
ROMresultsshouldbeinterpretedwithcautionsincedifferencesbetweensittingandstand-
ingROMassessmentshavebeendescribed.Thiscouldbeexplainedbyvaryingtrunkmuscle
recruitmentstrategiesbetweenpositions.
TheeffectofcreeponRMSandMDFvariables,andtheinteractionbetweenfatigueand
creeponthey-axisdispersiononlyreachedstatisticalsignificanceononesideofthetrunk.
Thissuggeststhatthestudymayhavebeenunderpowered.Inthisstudy,thepresenceoflow
backmusclefatiguewascharacterizedbyamarkeddecreaseinthemeanMDFslope.Itisalso
knownthatMDFchangescanbetriggeredbychangesinintramusculartemperature[55].
IntramusculartemperaturecanalsoinduceanincreaseinthespectralcontentofthesEMG
PLOSONE|DOI:10.1371/journal.pone.0149076 February11,2016 10/14