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Aortic compliance variation in long male distance
triathletes: A new insight into the athlete’s artery?
Anne-Charlotte Dupont, Mathias Poussel, Gabriela Hossu, Pierre-Yves Marie,
Bruno Chenuel, Jacques Felblinger, Damien Mandry
To cite this version:
Anne-Charlotte Dupont, Mathias Poussel, Gabriela Hossu, Pierre-Yves Marie, Bruno Chenuel, et
al..
Aortic compliance variation in long male distance triathletes: A new insight into the
ath-lete’s artery?.
Journal of Science and Medicine in Sport, Elsevier, 2016, 20 (6), pp.539-542.
ContentslistsavailableatScienceDirect
Journal
of
Science
and
Medicine
in
Sport
j o u r n a l ho me p a g e :w w w . e l s e v i e r . c o m / l o c a t e / j s a m s
Original
research
Aortic
compliance
variation
in
long
male
distance
triathletes:
A
new
insight
into
the
athlete’s
artery?
Anne-Charlotte
Dupont
a,
Mathias
Poussel
b,c,
Gabriela
Hossu
d,
Pierre-Yves
Marie
e,f,g,
Bruno
Chenuel
b,c,
Jacques
Felblinger
a,d,e,
Damien
Mandry
a,e,g,∗aINSERM,IADIU947,France
bCHRUNancy,DepartmentofPulmonaryFunctionTestingandExercisePhysiology,France
cUniversitedeLorraine,EA3450DevAH—Development,AdaptationandDisadvantage,CardiorespiratoryRegulationsandMotorControl,France dINSERM,CIC-IT1433,France
eCHRUNancy,DepartmentofMedicalImaging,France fINSERMUMR-1116,France
gUniversitedeLorraine,France
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:
Received21February2016 Receivedinrevisedform 21September2016 Accepted21October2016 Availableonline29October2016 Keywords:
Vascularstiffness(G09.330.940) Compliance(G01.374.590.210) Magneticresonanceimaging (EO1.370.350.825.500) Athletes(M01.072) Triathlon
a
b
s
t
r
a
c
t
Objectives:Toassesscardiacandvascularadaptationsinlong-distancemaletriathletesandtheinfluence ofanincreasedtrainingvolumeontheseparameters.
Design:Case-controlstudyusinglong-distancemaletriathletes(Tri)(n=12)andanage-matchedcohort ofsedentaryvolunteers(Ctrl).
Methods:AllparticipantsgaveaninformedconsentandunderwentaCardiovascularMagneticResonance imaging(CMR)examtomeasureleftandrightventriclefunctionalparameters,andaorticparameters (surface,strain,compliance,pulsewavevelocity).Thisexamwasrepeatedinthetriathletes’groupafter anincreasedtrainingvolumeofatleast2h/weekforsixweeks.
Results:Comparedtocontrolvolunteers,triathletespresentedatbaselineatypicalpatternofathlete’s heart(higherend-diastolic,end-systolicandstrokevolumesindex,p≤0.009,andlowercardiacrate, p=0.015)butsimilarvascularcharacteristicsexceptatrendtowardsanenlargedascendingaorta(surface 942±106vs812±127mm2,p=0.058).Betweenthetwovisits,thetriathletesincreasedtheirweekly
trainingtimefrom9.67±2.43(Tri1)to12.15±3.01h(Tri2):nomodificationswerefoundregarding cardiacparameters,butcomplianceanddistensibilityoftheascendingaortaincreased,from2.60to 3.34mm2/mmHg(p=0.028)andfrom3.36to4.40×10−3mmHg−1(p=0.048)respectively.
Conclusions:UsingCMR,weshowedthatvascularcharacteristicsoftheascendingaortamayvaryalongthe sportseasoninenduranceathletes.Thisremodellingcouldbeconsideredasaphysiologicaladaptation, butcouldeventuallyleadtoanadversevascularremodelling.
©2016SportsMedicineAustralia.PublishedbyElsevierLtd.Allrightsreserved.
1. Introduction
The health benefits of regular moderate intensity exercise are welldemonstrated,1 but the upperlimit of this relation is
regularlyquestioned,especiallyregardingpossiblesports-related cardiac injuries in endurance athletes.2 Dealing with this
spe-cificpopulation,moststudiesfocusedonthecardiacremodelling consecutivetoprolongedintenseenduranceexercise,andthe ath-lete’sheartcharacteristicsarenowwellestablished.3,4,5Intense
enduranceexerciseboutshavealsobeenshowntoinvolvemore acute functionaland biochemical cardiac dysfunctions, withan
∗ Correspondingauthor.
E-mailaddress:d.mandry@chu-nancy.fr(D.Mandry).
unclearsignificance.6 Overall,it appearsthat exerciseinexcess
maysometimesspecificallyharmtheheart.2Someevidencealso
suggesttheconceptofan“athlete’sartery”,evenifthesevascular adaptationsinathleteshavenotyetbeenfullycharacterized. Inter-estingly,studiesdealingwiththeeffectoflongtermandregular enduranceexercisetrainingoncentralbloodpressurereveal con-trastingfindings.Forinstance,someauthorsshowthat,compared tohealthycontrols,enduranceathleteshaveloweraorticpressure7
whereassomeothershowcomparableaorticfunction.8 Inthese
contrastingstudies,thelackofadjustmentforconfoundingfactors (amongthem,nodoubtthattheamountoftrainingvolumeplays animportantrole)isgenerallydiscussedasapossibleexplanation. CardiacMagneticResonanceimaging(CMR)hasnowbeenaccepted asthereferenceforcardiacassessmentintheathleticpopulation,9
butmoststudiesdealingwithvascularadaptationinathletesare http://dx.doi.org/10.1016/j.jsams.2016.10.009
540 A.-C.Dupontetal./JournalofScienceandMedicineinSport20(2017)539–542
basedonnon-invasivetonometrythereforeexcludingthedirect evaluationofcentrallargearteries.10,11
Therefore,usingCMR,ourstudywasdesignedtoassess car-diovascular characteristics in a long distance male triathlete populationtotestthehypothesisthatnotonlycardiacbutalso aor-ticadaptationsmayfurtherbemodifiedaccordingtotheamount oftrainingvolume.
2. Methods
Inthisprospectivesingle-centrepilotstudy,approvedbythe local ethics committee, conducted in a tertiary centre, twelve malenon-professionaltriathletes,practisinganendurance activ-ity for severalyears, were enrolled betweenJanuary and April 2014.Informedconsentwasobtainedfromallparticipants,who werescreenedforcontra-indicationstoCMR,includingnon-sinus rhythm.Inclusioncriteriawere:agebetween18to45yearsold atthetimeofinclusion,aregularworkoutofatleasteighthours perweekinpreparationeitherforalongdistancerace(1900-m swim/90-kmbike/21.1-kmrun)oranIronman(3800-m swim/180-km bike/42.2-kmrun). Alltriathletes underwent two CMR,the firstone(Tri1)withinonemonththebeginningoftheirtraining, consideredas theirbaseline,and the second(Tri2) six toeight weeksafterhavingincreasedtheirweeklyvolumeoftrainingby atleasttwohours.Twelvesedentarypeople(controlgroup=Ctrl), matchedonsexandage,wererecruitedbymeansofadvertising; sedentarylifestyle,asdefinedbytheWorldHealthOrganisation, wasalackofphysicalactivity.12Exclusioncriteriawere:chronic
diseases including cardiovascular, medical therapy susceptible toinfluencecardiovascularremodellingsuchasantihypertensive or lipid-lowering drugs, current tobacco smoking of at least 5 cigarettesperday.
Amedical examinationwasconducted prior toCMR:height andweightweremeasuredandbodysurfacearea(BSA)calculated usingtheMostellerstandardequation.13
CMRwasperformedona3-Tunit (SignaHDx,General Elec-tric Healthcare, Milwaukee, Wisconsin, USA) using a dedicated 8-channelcardiaccoil.Participantswereinsupineposition,arms alongthebody.Acuffwasplacedontheirleftarm,atthesame levelastheheart,toallowautomatedblood pressurerecording (MaglifeC;SchillerMedical, Wissembourg,France); three mea-surementswereobtainedthroughouttheCMRexaminationand medianvalues were stored for furtheranalysis.For left ventri-cle(LV)andrightventricle(RV)functionalassessment,avertical, ahorizontallongaxisandastackofcontiguousshort-axisslices wereobtainedduring10–15sbreath-holdusingabalancedSteady StateFreePrecession(bSSFP)sequence.Typicalparameterswere as follows: 30 reconstruction phases per cardiac cycle; 35 cm-fieldofview;224×224-mmmatrix;8mmthickness;1.5ms-echo time; 45◦-flip angle; 3.7–4.1ms-repetition time; parallel imag-ing with an acceleration factor of 2; 12 views per segment, yieldingatemporalresolutionof45–50ms.Imageanalysiswas per-formedusingadedicatedsoftware(Mass(MRAnalyticalSoftware System) v2013-EXP, Leiden University Medical Center, Depart-mentofRadiology,DivisionofImageProcessing,Leiden,NL);LV andRVend-diastolicvolumes(EDV),end-systolicvolumes(ESV) and LV mass were obtained after manual contouring, follow-ing theSociety for CardiovascularMagnetic Resonance(SCMR) recommendations.14PapillarymuscleswereincludedintoLV
cav-ity.Allvalueswereindexedtobodysurfaceareaandtheconcentric remodellingindex calculated as LV mass/LVEDV (Left Ventricle End-DiastolicVolume).15
Tomeasureascendingand descendingaorticsurfaces,aslice perpendicular tothe ascending aortain its middle part,at the leveloftherightpulmonaryartery,wasrecordedduringa breath-hold,withaSSFP sequencesimilartothatdescribed above,but
Table1
Physicalcharacteristicsoftriathletesandcontrolvolunteers.
Parameter Tri1(n=12) Ctrl(n=12) Pvalue
Age(year) 32.3±7.1 33.1±8.8 >0.99
Weight(kg) 74.2±6.1 80.5±13.3 >0.99
Height(m) 1.81±0.07 1.80±0.08 >0.99
BMI(kg/m2) 22.60±1.06 24.93±3.98 0.302
BSA(m2) 1.93±0.11 2.00±0.18 >0.99
BMI,bodymassindex;BSA,bodysurfacearea;Ctrl,controlvolunteers;Tri1, triath-letesatinclusion.
Dataaregivenasmeans±standarddeviations.Pvaluesareadjustedformultiple
comparisonsaccordingtoBonferroni–Holmcorrection.
withahighertemporal(20–25ms)andspatialresolution(26 cm-field of view). Ascending and descending aorta contours were automatically detected and propagated throughout the cardiac cycle; minimal and maximal surfaces were stored for further analysis,beingAominandAomaxrespectively.Aorticstrain(AS) wasdefinedas(Aomax−Aomin)/Aomin;distensibilitycalculated asAS/brachial pulsepressure,in mmHg−1 or cm2dyn−1×10−6, and complianceas (Aomax−Aomin)/brachialpulsepressure, in mm2mmHg−1.
Flowmeasurementswereperformedwithaphasecontrastcine sequence,withthefollowingparameters:electrocardiogram(ECG) gating;40cm-fieldofview;256×128mm-matrix;10mm thick-ness;3.3ms-echotime;20◦-flipangle;200cm/svelocityencoding; 6ms-repetition time; 4 views per segment; 30 cardiac phases reconstruction.Aorticstrokevolumewasobtainedatthemiddle partoftheascendingaorta,usingCVFlowsoftware(v2011-EXP, LeidenUniversityMedicalCentre,DepartmentofRadiology, Divi-sionofImageProcessing,Leiden,NL)foranalysis;velocitieswere correctedbyaregionofinterest-basedmethodincaseofevident offset error.16 Aorticpulsewave velocity was measuredasthe
ratioofthedistancebetweentwomeasurementssites,atthemid ascendingaortaandthedistaldescendingaorta,tothetransittime ofthevelocitycurves,obtainedwitha8ms-temporalresolution phasecontrastcinesequence,aspreviouslydescribed.3,17
Quantitativeresultswereexpressedasmean±standard devia-tion.Nonparametrictestswereusedasanormaldistributioncould notbeassumedowingtoaninsufficientlyhighnumberofcases. Differencesbetweenmeansoftriathletesandthesedentarygroup (i.e.Tri1vsCtrl)wereassessedbyusingthenon-parametrictest ofWilcoxonforindependentsamples.Meandifferencesbetween beforeandaftertrainingsessionfortriathletes(i.e.Tri1vsTri2) wereassessedbyusingpairedWilcoxontest.
Alltestswerealsoadjustedformultiplecomparisons accord-ing to Bonferroni–Holm correction. Throughout the analysis, a two-sidedpvalueoflessthan0.05wasconsideredstatistically sig-nificant.AllcomputationswereperformedwithsoftwareR(version 3.2.0,theRFoundationforStatisticalComputing,Vienna,Austria).
3. Results
The anthropometric characteristics of all participantsat the inclusionare presentedin (Table1).Thetwo groupswere well matched, without significant difference between Tri1 and Ctrl. Cardiac and vascular characteristics of control volunteers and triathletes,bothatinclusionandfollow-up,aredetailedin(Table2). As compared to Ctrl,Tri1 had greater left and right ventri-clesvolumes,withadaptedLVmass,increasedLVstrokevolume, and lower resting heart rate, typical of athlete’s heart, but no difference regarding vascular characteristics of the aorta were observed,exceptatrendtowardsanenlargedascendingaorta (sur-face942±106vs812±127mm2,p=0.058).
ThedelaybetweenTri1andTri2was66.25±11.13daysandthe amountofweeklytrainingvolumeincreasedfrom9.67±2.43hto
Table2
Comparisonofthecardiacandvascularcharacteristicsbetweenthetriathletesatbaselineandthecontrolvolunteers,andthetriathletesbeforeandafteranincreased workout.
Parameter Ctrl(n=12) Tri1(n=12) Tri2(n=12) Pvalue(Tri1/Ctrl) Pvalue(Tri1/Tri2)
Restingheartrate(bpm) 73±11 60±11 55±11 0.015* 0.098
Bloodpressure(mmHg)
Systolic 123±11 126±8 112±4 >0.99 0.001*
Mean 89±9 86±11 79±7 >0.99 0.122
Diastolic 70±10 66±12 61±5 >0.99 0.355
Medianpulsepressure(mmHg) 53±8 61±7 52±4 0.090 0.007*
Leftventricle
EDvolumeindex(mL/m2) 84.3±11.5 113.7±14.3 116.7±12.2 <0.001* 0.904
ESvolumeindex(mL/m2) 37.6±6.3 49.8±10.5 52.1±9.1 0.009* 0.611
Strokevolumeindex(mL/m2) 46.7±7.5 63.9±8.9 64.6±7.0 <0.001* >0.99
Massindexatenddiastole(g/m2) 55.7±5.8 73.2±8.0 74.1±7.3 <0.001* >0.99
Ejectionfraction(%) 55.3±4.5 56.4±6.0 55.5±4.6 >0.99 >0.99
Rightventricle
EDvolumeindex(mL/m2) 81.2±12.6 112.5±12.0 114.3±10.8 <0.001* 0.798
ESvolumeindex(mL/m2) 35.6±7.4 48.5±7.8 49.7±8.5 0.001* >0.99
Strokevolumeindex(mL/m2) 45.6±7.7 64.0±8.8 64.6±6.5 <0.001* >0.99
Ejectionfraction(%) 56.2±5.1 56.9±5.2 56.7±4.9 >0.99 >0.99
Cardiacindex(L/min/m2) 3.3±0.4 3.9±0.8 3.7±0.7 0.062 >0.99
Ascendingaorta Aomax(mm2) 812±127 942±106 957±98 0.058 >0.99 Aorticstrain(%) 18.5±5.4 20.2±7.3 22.9±9.2 >0.99 0.388 Distensibility(10−3mmHg−1) 3.44±0.67 3.36±1.17 4.40±1.58 >0.99 0.048* Compliance(mm2/mmHg) 2.36±0.59 2.60±0.71 3.34±0.90 >0.99 0.028* Descendingaorta Aomax(mm2) 497±67 576±86 591±90 0.113 0.816 Aorticstrain(%) 25.6±6.2 25.0±6.0 23.4±7.3 >0.99 0.611 Distensibility(10−3mmHg−1) 3.86±0.88 3.30±0.65 3.62±0.73 0.340 0.388 Compliance(mm2/mmHg) 1.92±0.54 1.89±0.38 2.1±0.48 >0.99 0.388 AortaPWV(m/s) 5.05±0.65 4.74±0.51 5.1±0.79 >0.99 >0.99
Aomax,maximalcross-sectionalareaatsystole;Ctrl,controlvolunteers;ED,end-diastolic;ES,end-systolic;PWV,pulsewavevelocity;Tri1andTri2,triathletesatbaseline andfollow-uprespectively.
Dataaregivenasmeans±standarddeviations;PvaluesareadjustedformultiplecomparisonsaccordingtoBonferroni–Holmcorrection.
*Statisticallysignificant.
12.15±3.01h(p=0.011).Systolicbloodpressureandmedianpulse pressuredecreased,butnofurtherdifferencewasfoundregarding leftand rightventricle parameters.Compliance and distensibil-ityoftheascendingaorta(respectively2.60vs3.34mm2/mmHg,
p=0.028;3.36vs4.40×10−3mmHg−1,p=0.048)wereincreased but not those of the descending aorta (respectively 1.89 vs 2.1mm2/mmHg,p=0.388;3.30vs3.62×10−3mmHg−1,p=0.388).
4. Discussion
The health benefits of regular moderate intensity exercise are wellestablished,both on cardiovascularand noncardiovas-cular morbi-mortality.1 However, repeated prolonged intense
endurance exercise can also induce significant cardiac remod-elling(termedthe“athlete’sheart”)sometimesleadingtorarebut remarkablesuddencardiacevents.18 Thetriathletesinvolved in
ourstudyundoubtedlypresentedthecharacteristiccardiac adap-tationsoftheathlete’sheart(Tables1and2).4Theathlete’sheart
isnowagenerallyacceptedtermwithnumerousstudiesfocusing onthestructural,functionalandelectricalremodellingthat accom-paniesregularexercise.4Someauthorsindeedhypothesizedthat
excessiveintenseexercisemayharmtheheart2;thishasbeen
par-ticularlysuggestedforexcessiveboutsofexercise(i.e.toointense orwithtooshortrecoveryperiod)possiblyleadingtocardiacinjury withproarrhythmicremodelling(predominantlyaffectingtheright ventricle).19
Incontrast,thevascular adaptationinathleteshasnotbeen fullycharacterized, evenifsomeevidencessuggesttheconcept of an “athlete’s artery”.10 The CMR imaging technique used in
ourstudyallowedustoassessthevascularcharacteristicsofthe aortawhereasmoststudiesdealingwithathlete’sartery20 only
consideredmore peripheralarteriesbasedonpulsewave
anal-ysismethod.11 Facingtheathlete’sheartand thehemodynamic
stressimposedduringexercise,theascendingaortaactsasthefirst (i.e.justbeyondtheheart)elasticbufferingchamberknownasthe Windkesselfunction.21TheWindkesselfunctionisdirectlyrelated
totheelasticproperties(i.e.compliance)oftheaorta,andhasa criticalinfluenceontheperipheralcirculationbutalsoontheheart function(reductionofleftventricularafterload,improvementin coronarybloodflowandleftventricularrelaxation).Theoriginal findingofthisstudywastheincreasedcomplianceand distensibil-ityoftheascendingaortabetweenTri1andTri2,i.e.afterincreasing thetrainingvolume,butnotofthedescendingaorta.Considering thecloserelationshipoftheheartandtheaorta,thiscouldbe con-sideredasanadaptiveremodellingofthevascularstructureofour triathletepopulation.Eveniffarlessattentionhasbeendevoted toathlete’sarteriesthanathlete’sheart,someevidencessupport that endurance athletes have enlarged arteries with decreased wallthicknessasaresult ofprolongedtraininginterventions.20
Thisspecificathlete’swallthicknesschanges shouldbe consid-ereda physiological adaptation onwallremodellingin healthy arteriesunderrepetitiveexercisestress,butthelong-termvascular consequencesarecurrentlyunknown.Furthermore,thisincreased complianceoftheascendingaortabetweenTri1andTri2associated withtheabsenceofanysignificantdifferencesinarterial compli-ancebetweenCtrlandTri1(Table2)mayalsohighlightsakindof dose-responserelationshipfortheexercise-relatedbenefitsin vas-cularadaptation,involvingaminimumamountoftimetraining tobeeffective(i.e.theminimalthresholdtotriggerthis vascu-laradaptation).Indeed,theincreasedcomplianceoftheascending aortawasobservedafterourtriathletepopulationhadincreased theirweeklytraininghoursfrom9.67±2.43to12.15±3.01hfor atleasttwomonths.Theseresultssupportthat,oncetheheartis alreadyadaptedinathletes(i.e.athlete’sheart),afurtherincreased
542 A.-C.Dupontetal./JournalofScienceandMedicineinSport20(2017)539–542
intraininghours(i.e.betweenTri1andTri2)maynotsignificantly impacttheheartbutmaypredominantlyaffectthevascular struc-turebeyondtheheart.Thus,byanalogywiththesuspectedadverse cardiacremodellingofexcessiveexercise,2wecouldspeculatethat
thevariationofaorticcomplianceaccordingtotheamountof train-inghoursduringatrainingseasonmayalsoleadtosomeadverse vascularremodelling.Indeed,availabledatanowshowthat aor-ticrootenlargementcanbefoundineliteathletesintheabsence of apparent aetiology.22 Initially, it was found that aortic root
diameterwasgreaterinstrength-trainedathletescomparedwith endurance-trainedonesand that theduration of high-intensity strengthtrainingappeared tobethestrongestpredictorof aor-ticdimensions.23,24MorerecentlyPelliciaetal.foundthataortic
dimensionswerelargerinenduranceathletesthaninstrength ath-letesbutthecauseof thisaortic enlargementina fewathletes remainstobeclarified.25Despitethelimitedsizeofthe
popula-tion,weindeedfoundatrendtowardalargerascendingaortaof Tri1thanCtrl(Aomax;p=0.058).Inthelightofourmajorresult,we couldspeculatethattherepeatedvariationsofcomplianceofthe ascendingaortaovertheyearsinenduranceathletesmaysometime leadtopathologicalvascularremodellingandpossibly “exercise-inducedaorticrootdilatation”.Astheseresultswereobtainedina limitedpopulationofmaletriathletes,furtherstudiesareneededto confirmtheminbothmaleandfemaleathletes,andtoinvestigate theimpactoflong-termenduranceexerciseonarterialstructure andremodelling.
Apartfromthelimitedsizeofthepopulation,weacknowledge thatwedidn’tobtaincentralpressuresbutreliedonbrachial arte-rialpressuretocalculateaorticcomplianceanddistensibility,as usualforMRI assessmentof theseparameters.17,26,27 Theother
limitationofthisstudyisthatnofollow-upstudywasobtained inthecontrolsubjects,asthisstudywasdesignedtoassessaortic adaptationsaccordingtotheathletes’trainingvolume.
5. Conclusion
Vascularremodellingintheathleticpopulationresultsinthe emergenceoftheconceptof“athlete’sartery”,butthelong-term consequencesofsucharemodellingarecurrentlyunknown.Using CMRinaspecificpopulationoftrainedlongdistancetriathletes,our studydemonstratedanincreasedcomplianceanddistensibilityof theascendingaortarelatedtotheamountoftrainingvolume.Thus, vascularcharacteristicsmayvaryduringthesportseason depend-ingonthetrainingandrecoveryperiodsinenduranceathletes.If thisremodellingcanbeconsideredasaphysiologicaladaptation, italsoquestionsthepotentialforsomepossibleadverse vascu-larremodelling,especiallyinthelightoftheincreasingreportsof aorticrootenlargementineliteathletes.Then,whetherrepeated prolongedintenseexercisemaynotonlyharmtheheartbutalso thearteriesneedstobeclarified.
Practicalimplications
• ThisstudyshowsthatlongdistancetriathletespresentwithLV andRVremodellingtypicalofanathlete’sheart.
• Italsodemonstratedthattheseventricularparameterswerenot furthermodifiedduring an8-week periodof increased train-ing,whereasaorticcomplianceanddistensibilityincreasedinthe meantime.
• Thesemodificationsofvascularcharacteristicsduringasport sea-son,alongwithatrendtowardsdilationoftheascendingaorta bringsnewevidenceofanathlete’sarterythatcouldleadto car-diovascularevents.
Funding
Nofinancialassistancewasobtainedforthisstudy.
Ethicalapproval
Thisstudywasapprovedbythelocalethicalcommitteeand informedconsentwasobtainedfromeachparticipant.
Acknowledgement
TheauthorswouldliketothankProf.MichelClaudonforcritical reviewofthisarticle.
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