Changes in Achilles tendon stiffness and energy cost following a prolonged run in trained distance

17 Pages·2017·3.23 MB·English

RESEARCHARTICLE
Changes in Achilles tendon stiffness and
energy cost following a prolonged run in
trained distance runners
JaredR.Fletcher1,2*,BrianR.MacIntosh1
1 HumanPerformanceLaboratory,FacultyofKinesiology,UniversityofCalgary,Calgary,Canada,
2 DepartmentofHealthandPhysicalEducation,MountRoyalUniversity,Calgary,Canada
a1111111111 *[email protected]
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a1111111111 Abstract
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Duringprolongedrunning,themagnitudeofAchillestendon(AT)lengthchangemay
increase,resultinginincreasedtendonstrainenergyreturnwitheachstep.ATelongation
mightalsoaffectthemagnitudeoftricepssurae(TS)muscleshorteningandshortening
OPENACCESS velocity,requiringgreateractivationandincreasedmuscleenergycost.Therefore,we
aimedtoquantifythetendonstrainenergyreturnandmuscleenergycostnecessaryto
Citation:FletcherJR,MacIntoshBR(2018)
ChangesinAchillestendonstiffnessandenergy allowenergystoragetooccurpriortoandfollowingprolongedrunning.14trainedmale
costfollowingaprolongedrunintraineddistance (n=10)andfemale(n=4)distancerunners(24±4years,1.72±0.09m,61±10kg,V_O max
runners.PLoSONE13(8):e0202026.https://doi. 2
64.6±5.8ml•kg-1•min-1)ran90minutes(RUN)atapproximately85%oflactatethreshold
org/10.1371/journal.pone.0202026
speed(sLT).PriortoandfollowingRUN,ATstiffnessandrunningenergycost(E )at85%
run
Editor:HazelRCScreen,QueenMaryUniversityof
sLTweredetermined.ATenergyreturnwascalculatedfromATstiffness,measuredwith
London,UNITEDKINGDOM
dynamometryandultrasoundandestimatedTSforceduringstance.TSenergycostwas
Received:March18,2018
estimatedonthebasisofATforceandassumedcrossbridgemechanicsandenergetics.
Accepted:July26,2018 FollowingRUN,ATstiffnesswasreducedfrom328±172N•mm-1to299±148N•mm-1
Published:August8,2018 (p=0.022).E increasedfrom4.56±0.32J•kg-1•m-1to4.62±0.32J•kg-1•m-1(p=0.049).
run
EstimatedATenergyreturnwasnotdifferentfollowingRUN(p=0.99).EstimatedTSmus-
Copyright:©2018Fletcher,MacIntosh.Thisisan
openaccessarticledistributedunderthetermsof cleenergycostincreasedsignificantlyby11.8±12.3J•stride-1,(p=0.0034),accountingfor
theCreativeCommonsAttributionLicense,which muchofthepost-RUNincreaseinE (8.6±14.5J•stride-1,r2=0.31).Theseresultsdemon-
run
permitsunrestricteduse,distribution,and
stratethataprolonged,submaximalruncanreduceATstiffnessandincreaseE intrained
reproductioninanymedium,providedtheoriginal run
authorandsourcearecredited. runners,andthattheelevatedTSenergycostcontributessubstantiallytotheelevatedErun.
DataAvailabilityStatement:Allrelevantdataare
withinthepaperanditsSupportingInformation
file.
Funding:JRFwassupportedbyNaturalSciences
andEngineeringResearchCouncilofCanada Introduction
(NSERCPGSD2-391898-2010),andbyMitacsand
Theenergycostofrunning(E )isoneofthekeydeterminantsofdistancerunningperfor-
OwnthePodiumthroughtheMitacs-Accelerate run
mance[1].E isprimarilydeterminedbytheenergycostofgeneratingtheforceneededto
Program.Thefundershadnoroleinstudydesign, run
datacollectionandanalysis,decisiontopublish,or supportbodyweightforthedurationofthestride(2footstrikesperstride)[2–4]andthereis
preparationofthemanuscript. growingevidencetosuggestthatmechanicalpropertiesofthetendonsofthemajorforce-gen-
eratingmusclesthatareactiveduringrunninggreatlyinfluenceE [5–7].Ithasbeensug-
Competinginterests:Theauthorshavedeclared run
thatnocompetinginterestsexist. gestedthatthemechanicalpropertiesoftendonallowa‘decoupling’betweenthelength
PLOSONE|https://doi.org/10.1371/journal.pone.0202026 August8,2018 1/17
Achillestendonstiffnessandenergycost
Abbreviations:ANOVA,analysisofvariance;AT, changeofthemusclefasciclestothatofthewholemuscle-tendonunit,allowingthemusclefas-
Achillestendon;dL,tendonelongation;Erun,energy ciclestoshortenatamuchslowerspeedwhilehigh-velocityshorteningcanbeachievedbythe
costofrunning;F,force;F,verticalground
z recoilofthetendon[8,9].Thisminimizedshorteningmagnitudeandshorteningvelocitywill
reactionforce;MG,medialgastrocnemius;MVC,
minimizetherequiredlevelofmuscleactivationneededtogeneratethenecessaryforce,dueto
maximalvoluntarycontraction;RUN,prolonged90
themuscle’sforce-velocityrelationship[10,11].
minuterun;SD,standarddeviation;sLT,speedof
lactatethreshold;SWC,smallestworthwhile TheAchillestendon(AT)undergoesrapidlengtheningandshorteningduringthestance
change;TS,tricepssurae;V_O max,maximal phaseofrunning,takingupmuchofthelengthchangeofthewholemuscle-tendonunit,and
2
oxygenuptake. reducingtheneedformusclefibrelengtheningandshortening[8,9,11].Themuscleenergy
costshouldbelowestwhentheATismechanically‘tuned’toallowminimalmusclefascicle
shorteningduringthestancephaseandmuchofthelengthchangeofthemuscle-tendonunit
canbeaccommodatedbytheAT.
Whencyclicallyloaded,duringrunningofsufficientduration,theATmaydevelop
dynamiccreep[12],resultingingreaterlengthchangeforagivenload.Dynamiccreepcanbe
assessedbymeasuringchangesinATstiffnessfollowingarun.Ifsignificantdynamiccreep
doesoccurduring/followingaprolongedrun,thisimpliesthatforanymuscle-tendonunit
lengthandthesameforcerequirementsduringstance,ATelongationwouldbegreater,neces-
sitatinggreaterTSfascicleshortening.Thisadditionalfascicleshorteningwouldrequiremore
muscleenergy[10,13],whichwouldbeproportionaltotheadditionalshortening,duetoshort-
ening-inducedincreasesinATPturnover[14]andhighershorteningvelocity[15,16].The
additionalmuscleenergycostshouldcontributetoanelevatedE althoughthemeasurement
run
ofE and/orfascicleshorteningduringrunningmaylacksufficientsensitivitytodemon-
run
strateameaningfulcausation.Indeed,AlbrachtandArampatzis[17]havepreviouslydemon-
stratedthatE wassignificantlyreducedwhenATstiffnesswaselevatedfollowingaperiodof
run
resistancetrainingbutcouldnotshowasignificantdifferenceinMGfascicleshortening.No
studiestodatehaveevaluatedtheoppositeeffect.Thatis,doesareductioninATstiffness
resultinconcomitantincreasesinE ?
run
Boutsoflongdistancerunningof60–90minuteshavebeenshowntoacutelyelevateE in
run
moderately-trainedrunners[18–20].Repetitivecontractions,havebeenshowntodecreaseAT
stiffness[21,22];however,arecentreview[23]suggestsprolongedrunninghasonlyatrivial
effectonalteringtendonmaterialproperties.Specifically,Parketal.(2011)showednodiffer-
enceinATstiffnessfollowingashortwarm-upconsistingofa6-minjogat180m(cid:1)min-1anda
seriesofstaticstretches.Similarly,Farrisetal.[24]couldnotdemonstrateasignificantreduc-
tioninATstiffnessfollowinga30minrunat200m(cid:1)min-1andonlyinolderrunnersdidAT
stiffnessdecreasefollowinga“halfmarathon”run(20.5km)at186m(cid:1)min-1.ATstiffnesswas
unalteredbya20.5kmrunat216m(cid:1)min-1inyoungrunners[25],confirmingtheresultsof
Lichtwarketal.[26]followinga5kmrun.However,thelatterauthorsshowedasmallbutsig-
nificantincreaseintendonstrainfollowingtherun.Increasedtendonstrainwouldallow
greaterenergystorage,butalsolikelyresultsinanelevatedmuscleenergycost[27].Theinter-
actionbetweenelevatedtendonstrainenergystorage/returnandmuscleenergycosthasto
datenotbeeninvestigatedtheoretically.Thus,thepurposeofthisstudywastoinvestigatethe
impactofaprolonged,submaximalrunof90minutesonpotentialchangesinATstiffness,
estimatedstrainenergyreturnandmuscleenergycost.Wesetouttotestthenullhypothesis
thattherewouldbenochangeinATstiffness,strainenergyreturn,E ormuscleenergycost
run
followingaprolonged,submaximalrun.
Materialsandmethods
14trainedmale(n=10)andfemale(n=4)distancerunnersparticipatedinthisstudy.Itwas
anticipatedthatthemaleandfemalerunnerswoulddemonstratearangeofvaluesforE and
run
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Achillestendonstiffnessandenergycost
Table1. Subjectcharacteristics.
N Age Height Mass V_O2max sLT
(years) (m) (kg) (ml(cid:1)kg-1(cid:1)min-1) (m(cid:1)min-1)
Male 10 25.8±4.5 1.76±0.06 66.3±6.7 66.8±4.7 265.4±15.2
Female 4 21.0±0.8 1.61±0.05 47.8±2.6 59.0±4.3 234.8±18.6
Total 12 24.4±4.4 1.72±0.09 61.0±10.4 64.6±5.7 256.7±21.1
Valuesaremean±sd.
https://doi.org/10.1371/journal.pone.0202026.t001
ATstiffness.SubjectcharacteristicsareshowninTable1.Allrunnersweretrainingregularly
atleast6timesperweekandfollowingasimilar,periodizedtrainingplandesignedforpeak
5000mor10000mperformanceforthefemalesandmales,respectively.Averageweeklytrain-
ingvolumewas80±7km•wk-1and101±28km•wk-1forthefemaleandmalerunners,respec-
tively.Noneoftherunnershadanyneuromuscularormusculoskeletalinjuriesatthetimeof
thestudy.Therunnersgavetheirinformedwrittenconsentfortheexperimentalprocedures.,
TheUniversityofCalgaryConjointHealthResearchEthicsBoardreviewedandapprovedthis
study.
Thesubjectsvisitedthelabontwoseparateoccasions.Theexperimentalprotocolisshown
inFig1.Duringthefirstvisit,anincrementaltesttoexhaustionwasperformedonatreadmill
(WoodwayPro,WoodwayUSA,Waukeshka,WA)todeterminethesubject’smaximaloxygen
uptake(V_O max)andspeedassociatedwiththelactatethreshold(sLT).Themethodsusedto
2
determineV_O maxandsLTwerethesameasthosemethodsusedpreviouslyinourlaband
2
describedelsewhere[28–30].Briefly,subjectsbeganrunningatapproximately3km(cid:1)hr-1below
theirmostrecent10kmraceperformancefor2min.Thespeedwasincreasedby0.8km(cid:1)hr-1
everytwominutes.Attheendofeach2minstage,afingertipbloodsamplewastakenforlac-
tatedetermination(LactatePro).Oncebloodlactateconcentrationrosemorethan1mM
fromtheprevioussample,thetreadmillspeedwasdecreasedby0.8km(cid:1)hr-1andthegradewas
Fig1.Experimentalprotocol.Onthefirstvisittothelab(Visit1),thesubject’sVO2maxand85%sLTweredetermined.Thesubjectsreturnedtothelab
48–96hourslater(Visit2),whenATstiffnessandErunat85%sLTweredeterminedbeforeandaftera90minrunataprescribedheartrateassociated
with85%sLT.
https://doi.org/10.1371/journal.pone.0202026.g001
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Achillestendonstiffnessandenergycost
increased2%everyminuteuntilvolitionalexhaustion.ThisspeedwasconsideredthesLT.
V_O maxwasconsideredthehighest30saverageV_O duringtheincrementaltest.Allincre-
2 2
mentaltestswereterminatedduetovolitionalexhaustionandallsubjectsattainedV_O max
2
basedonprimaryorsecondarycriteria[28].
Between48and96hoursfollowingthefirstlaboratoryvisit,thesubjectsreturnedtothelab
fordeterminationofATstiffnessandE .Subjectsthencompletedaprolonged,90minute
run
run(RUN).RUNwasperformedoverlevelgroundonanoutdoorroadloopsurface(inthe
subject’sownrunningshoes)atapacecorrespondingtoapproximately85%ofsLT.Carewas
takentoensuresimilarrunningenvironmentalconditionsbetweensubjects(14–19˚C,38–
54%relativehumidity).Thespeedandheartrateassociatedwith85%sLTweredetermined
fromtheincrementaltesttoensureconsistentrelativepacingbetweensubjects.Eachsubject
woreaheartratemonitor(Suuntot6c,Oy,Finland)duringRUNandwasinstructedtomain-
taintheheartratecorrespondingto85%sLTthroughout.Sincethesewereexperiencedrun-
ners,theywerealsogiveninformationpriortoRUNregardingtheapproximatetargetspeed
(minutes•km-1andminutes•mile-1).FollowingRUN,heartratedataweredownloadedtoa
computerusingthemanufacturer’ssoftware(SuuntoTeamManager,Suunto,Oy,Finland).
Theaverage(±2SD)heartratewascalculatedandonlythoserunsforwhichtheaverageheart
ratewaswithin±3beats•min-1ofthetargetheartratethrough-outRUNwereusedforsubse-
quentanalysisforATstiffnessandE .Intotal,fiveRUNtrials(4menand1woman)hadto
run
berepeated7dayslaterbasedontheaboveexclusioncriterion.Averageheartrateduring
RUNwasusedtoestimateapproximaterunspeed,fromtheheartrate-speed(belowsLT)rela-
tionshipdeterminedduringtheincrementaltest.
MeasurementofE
run
ImmediatelyfollowingthemeasurementofATstiffnessandbeforeRUN,a5-minutewarmup
at133m•min-1forthefemalesand160m•min-1forthemaleswasperformedonamotorized
treadmill(WoodwayPro,WoodwayUSA,Waukesha,WI).ThemeasurementofE wasper-
run
formedfollowingthewarm-upbyhavingthesubjectsruninthesameshoeswornduring
RUNat85%sLTforfiveminutes.FollowingRUNandthemeasurementofpost-RUNAT
stiffness,E wasmeasuredonthesametreadmillatthesamerelativespeed.Nocool-down
run
wasperformedfollowingRUN.V_O wasmeasuredthroughoutthe5-minuterunusingameta-
2
bolicmeasurementcart(TrueMax2400,Parvomedics,SaltLakeCity,UT).Thecartwascali-
bratedbeforeandaftereachsessionwithatwo-pointcalibrationusingroomairandagas
mixtureofknowncomposition(4%CO ,16%O )andamanual3-Lsyringe.Accordingtothe
2 2
manufacturer,theaccuracyofthissystemis0.03%and0.1%forO andCO ,respectivelyand
2 2
±2%forvolume.
E wascalculatedfromthesteady-stateV_O andrespiratoryexchangeratio(RER)over
run 2
thefinal2minutesofthe5-minutestage.E wasexpressedinunitsofenergy(J•kg-1•m-1),as
run
describedpreviously[30,31].
DeterminationofATstiffness
PriortoandimmediatelyfollowingRUN(ie.within2minutes),ATstiffnesswasdetermined
onthesubject’srightlegusingmethodsdescribedpreviously[27–29]anddetailedhere.Three
isometricrampmaximalvoluntarycontractions(MVC)oftherightplantarflexorswereper-
formedonadynamometer(BiodexSystem3,BiodexMedicalSystemsInc.,Shirley,NY,USA).
TheshankandunshodfootwereaffixedtothedynamometerusingaseriesofVelcrostraps
ThehighestmeasuredMVCwasusedforsubsequentanalysis.ThefirstMVCwasperformed
lessthan2minutesfollowingthecompletionofRUNinallsubjects.DuringtheMVC,a12.5
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Achillestendonstiffnessandenergycost
MHzlineararrayultrasoundprobe(50mm,PhilipsEnvisor,PhilipsHealthcare,Eindhoven,
Netherlands)wasusedtovisualizethemedialgastrocnemiusmuscle(MG)fasciclesata
frequencyof49Hz.ContrarytothemethodsofFletcheretal.[29]whomeasuredtendon
translationclearlyonthemusclebelly,wechosetomeasuretendontranslationnearthemyo-
tendinousjunction.Thiswasdonetoreduceanyeffectofaponeurosiscomplianceonthemea-
surementoftendonelongation[32]whilestillbeingabletovisualizeaseriesofMGfascicles.
Theprobewassecuredusingacustom-builtapparatusandelasticstraps.ATtendonelonga-
tionwasestimatedbythedisplacementofaninsertionofafascicleintothedeepaponeurosis
ascloseaspossibletothemyotendinousjunction,measuredduringtheMVC,usingImageJ,
(NIH,Baltimore,MD,USA).MeasuredmomentsandATelongationsweresynchronized
usinganexternalfunctiongenerator(B-KPrecision3010,DynascanCorp,Chicago,ILUSA),
whichwasmanuallyinitiatedatthestartofeachcontraction.Anklejointrotationwasdetected
byvideoanalysis.Theapparenttendontranslationduetojointrotationwascorrected,know-
ingthepassivejointangle-tendontranslationrelationship[10,29].ATmomentarmlengthat
the90˚ankleanglewasestimatedusingthetendontravelmethod[33]bypassivelyrotating
thesubject’sanklejointfrommaximalplantarflexiontomaximaldorsiflexionat0.17rad(cid:1)s-1
andmeasuringtendondisplacement,correctedforpassiveforceusingultrasound[34].AT
forcewascalculatedbydividingtheanklejointmomentbytheestimatedATmomentarm.
ATForce(F)-elongation(d )datawerefittedtoaquadraticregressionequationusing:
L
F ¼Ad2þBd ð1Þ
L L
whereAandBareconstants.InordertoaccountforanydifferenceinMVCforcepriortoand
followingRUN,ATstiffnesswasdefinedastheslopeofthefittedF-d equationfrom50–100%
L
ofmaximumisometricplantarflexionforcepriortoRUN.
ATenergystorage/releaseandmuscleenergycost
ATenergystorageandrelease,aswellasmuscleenergycosttoallowATenergystorageto
occurwereestimatedaccordingtoFletcherandMacIntosh[27].Briefly,ATenergystorage
wascalculatedastheareaundertheF-d curve,whereFwasestimatedfromtheassumed
L
averagepeakverticalgroundreactionforcesandrunningspeed[35]andassumingthe
momentarmofF duringthestancephasewas1.5xgreaterthantheATmomentarm[36].
z
Weacknowledgethatthislengthisnotfixedduringthestancephaseandisdifferentbetween
rearandmidfootstrikers[37].However,wechoseafixedF :ATmomentarmratiosincein
z
somecases,aratiolargerthanthisresultedinanestimatedATforceduringrunningwhich
wasgreaterthanthemaximumisometricforce.ItseemsunlikelythattheATforceduring
runningattheprescribedspeedwouldbenearthemaximumisometricforce.Thisover-esti-
mationoftheATforcewouldresultinbothanover-estimationoftheATenergyreleaseas
wellasoftheestimatedmuscleenergycost.WefurtherassumedthatF wassimilarpriorto
z
andfollowingRUN[38–40].AreductioninF followingrun(forexample,withanincrease
z
instridefrequency),wouldresultinareducedATenergyreleaseaswellasareducedmuscle
energycost.
Thecorrespondingtendonlengthchange(d )duringrunningwasestimatedfromeach
L
subject’smeasuredF-d curve(seeEq1)andexpectedjointrotation,aconservativebutrea-
L
sonableestimateofanklejointrotationatthetimeofpeakverticalgroundreactionforce
[9,38].Theshorteningduetojointrotationwasaddedtotheshorteningduetoforce-depen-
dentstretchofthetendontocalculatetotalshorteningduringthestancephase.ATenergy
storagewascalculatedandATenergyrelease,wasestimatedassuminganAThysteresisof10%
[41].
PLOSONE|https://doi.org/10.1371/journal.pone.0202026 August8,2018 5/17
Achillestendonstiffnessandenergycost
TSmuscleenergycostforATstorage/releasetooccurwascalculatedfromtheestimated
ATforceandfascicleshorteningduringtwosequentialfootstrikes(onestride),describedelse-
where[27].Briefly,TSforcewasestimatedbycalculatingtheforceneededinthismuscledur-
ingtwostancephases(onestride).Thenumberofactivecrossbridgesneededtogeneratethe
requiredforceduringstancewasestimated,assumingacrossbridgeforceof3pNpercross-
bridge[42].Thenumberofactivecrossbridgeswasthenmultipliedbythenumberofcross-
bridgecycles,basedontheamountofshorteningexpectedineachsarcomere,thedifference
betweenrestingsarcomerelengthandthesarcomerelengthduringstance.Bothsarcomere
lengthswereextrapolatedfromtheestimatedfasciclelength-sarcomerelengthrelationship.
Weassumedthissarcomerelengthtobe2.6μmatMVCwhichisthesarcomerelength
expectedforhumanmuscleattheshortendoftheplateauoftheforce-lengthrelationship
[43].Alinearincreaseinforceasafunctionoffasciclelength,withnoevidenceofaplateau
[44]suggeststhatduringmaximalcontractions,theMGoperatesontheascendinglimbof
theforce-lengthrelationship.Thus,thelongestsarcomerelengthcouldbenolongerthanthe
shortendoftheplateauoftheforce-lengthrelationship.Thenumberofsarcomeresinseries
wasestimatedbydividingtheassumedsarcomerelengthintotheknownfasciclelength.We
furtherassumedeachsarcomereshortenedby10nmwitheachcrossbridgecycle[45]andthat
48kJofenergywereusedpercrossbridgecycle[46].Forgreaterdetail,seeFletcherandMac-
Intosh[27,47].
Statistics
Valuesarepresentedasmean±SDunlessotherwiseindicated.Two-tailedpairedt-testswere
usedtotestfordifferencesbetweenpreandpost-runvaluesforE ,MVCforce,ATstiffness,
run
ATenergyreleaseandmuscleenergycost.One-wayANOVAwasusedtotestfordifferences
ind acrossabsoluteforcelevels.Linearregressionanalysiswasusedtoexaminetherelation-
L
shipbetweenATstiffnessandE ,priortoandfollowingtherunaswellastoexaminethe
run
relationshipsbetweenthechangeinATstiffness,andthechangeinE ,andthechangein
run
ATenergyreleaseandmuscleenergycostfollowingRUN.Allanalyseswereperformedusing
GraphPadPrismversion6.04forWindows(GraphPadSoftware,LaJolla,CA,USA,www.
graphpad.com).TheapriorilevelofstatisticalsignificancewassetatP<0.05.
Results
MeanheartrateduringRUNwas139±9b•min-1,equivalenttotheheartrateat83.6±4.1%
sLT.Thiscorrespondstoanapproximaterunspeedof214.1±13.7m•min-1.Thisspeedwas
notdifferentthantheanticipatedspeedassociatedwith85%sLT(218.2±17.9m•min-1,
p=0.175).Theaveragerundistancewas19.3±1.2km.
E priortoandfollowingRUNisshowninFig2.FollowingRUN,E wassignificantly
run run
higher(p=0.049)comparedtoE measuredpriortoRUN.Thisrepresentsameanincrease
run
inE of0.06±0.10J•kg-1•m-1(1.3%)followingRUN.
run
MVCforcewasreducedby3.0±5.7%followingRUN,from4489±2013Nto4333±1917N.
The95%C.I.forthedifference(POST-PRE)was-312to1N.Thisdifferencewasnotsignifi-
cant(p=0.0512).TheF-d relationshippriortoandfollowingRUNisshowninFig3.AT
L
stiffnesspriortoandfollowingRUNareshowninFig4.ATstiffnesswasreducedfollowing
RUNby28.5±36.5N•mm-1.ThisreductioninATstiffnesswassignificant(p=0.009).
Consideringthemeasurementspriortoandaftertherun,therewasasignificantrelation-
ship(r2=0.430,p=0.011)betweenchangeinE andchangeinATstiffness.Adecreasein
run
stiffnesswasassociatedwithanincreaseinE (Fig5).
run
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Achillestendonstiffnessandenergycost
Fig2.E priorto(PRE)andfollowing(POST)90minrun.Blacklinesrepresentindividualsubjectresponses.E wassignificantlyelevated
run run
(p=0.044)following90minrun.
https://doi.org/10.1371/journal.pone.0202026.g002
Anychangeind and/orforceduringstanceduetoRUNwouldresultinachangeinthe
L
amountofATenergystorage/release.PriortoRUN,weestimatedthisamountofstrainenergy
releasetobe21.6±9.0J•stride-1.FollowingRUN,ATenergyrelease(21.6±7.5J•stride-1)was
notsignificantlydifferentfromPRE(p=0.996).
EstimatedTSmuscleenergycostwassignificantlyelevatedfollowingRUN,from164±61
J•stride-1to175±62J•stride-1(p=0.0034).ThechangeinestimatedTSmuscleenergycostwas
significantlyrelatedtothechangeinE followingRUN(r2=0.368,p=0.023),suggesting
run
thatnearly40%ofthevarianceinE canbeaccountedforbychangesinmuscleenergycost
run
followingRUN.ThisrelationshipisshowninFig6.
Discussion
Theresultsofthecurrentstudydemonstratethataprolonged,submaximalrunsimilartothat
regularlyperformedintrainingbydistancerunnerscanelicitasmallbutsignificantincrease
inE andareductioninATstiffness.ThechangesinE andATstiffnessasaresultofthis
run run
RUNweresignificantlyrelated,confirmingpreviousreportsthatachangeinATstiffnessis
associatedwithachangeinE inhighly-traineddistancerunners[17,29].Ourestimatesof
run
TSmuscleenergycostsuggestthechangeinATstiffnesswouldresultinanincreaseinmuscle
energycost,andthismightcontributetothemeasuredincreaseinE .However,wecannot
run
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Achillestendonstiffnessandenergycost
Fig3.ATforce-elongationcurvepriortoandfollowing90minrun.d isshownatthesameabsoluteforcelevel(shownat20%MVC-PREforce
L
increments).Atallabsoluteforces,assessed,d wassignificantlyhigherPOST-RUN(p<0.001).
L
https://doi.org/10.1371/journal.pone.0202026.g003
discountthatpotentialpost-RUNchangesinrunningkineticswouldalterthisrelationship.
WealsorecognizethatourdataindicatethatsomerunnersapparentlydecreasedtheirE
run
afterRUN.Thispossibilityrequiresfurtherresearch.Furthertestingtoconfirmthatany
changesinrunningkineticsdidnotaltermuscleforcesand/orlengthchangeduringthepost-
RUNperiodarealsorequired.
ChangesinE followingprolongedrunninghavebeendemonstratedinhighly-trained
run
runnerspreviously[48].Specifically,itisreportedthatrunnershada5.2%increaseinE
run
followingamarathonrunat273m•min-1[18].Here,weobservedasmallerchangeinE
run
(1.3%)followinga90minrunataslowerspeed(214m•min-1).Itseemslogicaltoconsider
thatthechangeinE shouldbedependentonspeedanddistancerun.Brueckneretal.[18]
run
havepreviouslyestimatedthatE increasesasafunctionofdistancerun,byapproximately
run
0.08%•km-1.Here,weshowasimilarchangeof0.07±0.12%•km-1.
Itcannotbeoverlooked,however,thattheobservedchangeinE issmall.Themagnitude
run
ofdifferencebetweenpreandpost-RUNvaluesforE (1.3%)issmallerthanthetypicalerror
run
inmeasurementofE ofhighly-trainedrunnersreportedinourlab[30]andothers[49].The
run
smallestworthwhilechange(SWC)inE inhighly-trainedrunnershasbeenreportedtobe
run
2.7%whenE isexpressedintermsofenergy[49].However,datafromourlaboratoryfor
run
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Achillestendonstiffnessandenergycost
Fig4.ATstiffnessmeasuredpriorto(PRE)andfollowing(POST)90minrun.Solidlinesrepresentindividualsubjectresponses.ATstiffnesswas
significantlylower(p=0.009)following90minrun.
https://doi.org/10.1371/journal.pone.0202026.g004
trainedandelitemaleandfemaledistancerunnerssuggesttheSWCinE isbetween0.8%
run
and1.1%[27,30];thisSWCissmallerthanthemagnitudeofchangewereportinE follow-
run
ingRUN.Althoughwemustbecautiousintheinterpretationthatthechangesseenpost-RUN
are‘real’and‘worthwhile’andnotsimplyrelatedtotestingerrorandtypicalvariationofE ,
run
thefactthatthedifferencedidreachsignificance,probablybecauseoftheconsistencyofmea-
surement,isevidencethatitisreal.Certainly,achangeof1%canimpactperformance,and
manyofoursubjectsshowedincreasesinE greaterthanthis.
run
ItisinterestingtoconsiderthecontextofaprogressiveincreaseinE anditsimpacton
run
performanceofarecord-breakingmarathonperformance.TherewasarecentViewpoint[50]
thatpresentedthequestion:“WhoandWhen”withreferencetobreakingthatrecord.Inthe
associatedCommentaries[51],therewasageneralconsensusthatcurrentphysiologicalmea-
suresofeliterunnersareconsistentwithperformanceofa2hourmarathon.However,previ-
ousstudiesandthisrecentCommentaryhaveignoredthepotentialthatE mayincrease
run
progressivelythroughouttherun.ThisprogressiveincreaseinE hasonlyrecentlybeenfully
run
acknowledged[52].IfthereisaprogressiveincreaseinE intheserunners,thenclearlya
run
slow-downwouldberequiredifaconstantenergycostwasnecessaryforeliteperformance.A
similarchangeinE of0.07%perkmoverthecourseofaworld-classmarathon(eg.2hours
run
5minutes)wouldequatetoanear4minute(3minuteand41seconds)increaseinracetime.It
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Achillestendonstiffnessandenergycost
Fig5.RelationshipbetweenthechangeinE andATstiffnessfollowing90minrun.ThesolidlinerepresentsthelinearrelationshipbetweenE
run run
andstiffness(r2=0.430,p=0.011).Dashedlinesrepresentthe95%confidenceintervalfortherelationship.Notethattherelationshipcrossesthe
abscissaat0%changeinstiffness.
https://doi.org/10.1371/journal.pone.0202026.g005
maybemoredifficultthanwethinktobreakthe2hourbarrier,despitetheargumentthata
2-hourmarathonispossiblewithcooperativedrafting,anidealcourseandweatherconditions
andlighter,morecompliantrunningshoes[53].
Wespecificallychosetoperformtherunswhentheoutdoorambienttemperatureandrela-
tivehumiditywererelativelylowinordertopreventanyheat-associatedincreasesinE .
run
Bodytemperaturewouldriseprimarilyfrommetabolicheatgeneration,forwhichweestimate
90±10kJ/kgbasedonourmeanE values.Assuming50%ofthisheatwaslostbyconduc-
run
tion/convection,theremainingheatwouldnecessitate1.1±0.3Lofsweatinordertoloseheat
byevaporation(forsubjectsranginginmassfrom45to73kg).Oursubjectsmayhavehada
reductionofbodymassoverthecourseoftherunsotheirE shouldhavebeendividedbya
run
smallerbodymass.Estimatesofmuscleenergycostandtendonenergyreturn(J•stride-1)
wouldalsobeaffectedbythispossiblechangeinbodymass;alowerbodymasswouldrequire
alowerF atagivenspeed[35]aswellasalowertendonenergystorage.Ifweassumeaweight
z
changeof1kgfollowingtherun,thenthepost-E is3.0%higherthantheE measured
run run
priortoRUN.Inordertotrytoconfirmthishypothesizedweightchange,welatermeasured
theweightsoftrainedmale(n=18)andfemale(n=7)runners(someofwhomhadalso
PLOSONE|https://doi.org/10.1371/journal.pone.0202026 August8,2018 10/17