Original
article
/
Article
original
Contribution
of
new
techniques
to
study
the
gait
in
old
populations
Contribution
des
nouvelles
techniques
a` l’e´tude
de
la
marche
chez
la
personne
aˆge´e
S.
Gillain
Q1
*
,
J.
Petermans
Geriatricdepartment,CHULie`ge,Lie`ge,Belgium Received28June2012;accepted25May2013
Abstract
Objectives.– Forseveralyears,theconceptof‘‘physiologicalsenilegait’’hasbeenstronglycontestedandseemstobeassociatedwithabnormal gait.Indeed,somechangescharacteristicofsenilegaitappearearlyoninsubjectswithneurodegenerativepathologies.Theaimofthisarticlewas todeterminehowrecentcontributionscanimprovethestudyofgaitinoldpopulations.Thispaperisathematicreviewofrecentcontributionsfrom medicalimagingtechniquesaswellasinstrumentalgaitanalysistechniquesinolderadults.ThisarticledidnotfocusonParkinson’sdiseaseor otherspecificdiseasesbearingcertaingaitdisturbances,sincetheybelongtoliteraturefocusingontheseparticulardisorders.
Materialandmethods.– Thisworkwasnotintendedasasystematicreviewbutonlyasathematiconeconductedbygeriatriciansinorderreview therecentliteratureinordertobetterapprehendhownewtechnicscouldbeimplementedwithintheirclinicalpractice.Articleswereselectedin onlineMedlineandCochraneLibrarydatabases,andsomewerepreviouslyidentifiedbytheauthors.
Results.– Thispaperhighlightsthemostrecentcontributionsinmagneticresonanceimaging,functionalmagneticresonanceimagery,positron emissiontomographyandinstrumentalgaitanalyzingdevicesbetterunderstandingtheunderlyinggaitmechanismsinelderlypopulations. Conclusions.– Thisthematicreview suggeststhat gaitcouldbeconsidered asamarkerof ‘‘successfulaging’’.Its evaluationassociatedto longitudinalfollow-upcouldbeusefultopredictcognitiveandfunctionalchangesinfrailolderadults.
#2013PublishedbyElsevierMassonSAS. Keywords:Gait;Aging;Imagery;Cognitive;Instrumental Re´sume´
Objectif.– Depuisquelquesanne´es,leconceptde«de´marchese´nilephysiologique»estfortementconteste´.Certainesmodificationsdelamarche pre´senteschezle sujetaˆge´ semblent leplussouvent eˆtreassocie´es a` desprocessus pathologiquesde´butants.Cetarticleproposeune revue the´matiquedesapportsre´centsobtenusparlestechniquesd’imagerieme´dicaleetlestechniquesinstrumentalesd’analysedelamarcheapplique´es auxpersonnes aˆge´es.La maladiedeParkinsonainsique d’autres pathologiesincluantdesmodifications delamarchede´ja` de´criteslorsde publicationsspe´cifiques,nesontpasspe´cifiquemente´voque´esdanscetarticle.
Mate´rieletme´thodes.– Lesre´fe´rencescite´esdanscetarticleonte´te´ enpartiese´lectionne´esenrecherchantdanslaCochraneLibraryetdans Medline.Certainsarticlesutilise´se´taientde´ja` connusdesauteurs.Cetarticlenepre´tendpaseˆtreunerevuesyste´matiquemaisunerevuethe´matique faitere´cemmentpardesge´riatrescliniciensafinderassemblerlesdonne´esre´centesdelalitte´ratureetenvisagerleurinte´gration lorsdeleur pratiquequotidienne.
Re´sultats.– Cetarticlere´sumelescontributionsre´centesdel’imagerieparre´sonancemagne´tiquestructurelleetfonctionnelle,delatomographie pare´missiondepositonsetdesinstrumentsd’analysedesparame`tresdemarchepermettantunemeilleureconnaissancedesme´canismes sous-jacentsdelade´marchechezlespersonnesaˆge´es.
Conclusion.– Laqualite´ delamarchepourraiteˆtreconside´re´ecommeunmarqueurde«vieillissementre´ussi»etl’analysedesade´te´rioration pourraitaidera` pre´voirleschangementscognitifsetfonctionnelsyaffe´rant.
#2013Publie´ parElsevierMassonSAS.
Motscle´s: Marche;Vieillissement;Imagerie;Cognition;Instrumentale Availableonlineat
www.sciencedirect.com
AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 49 *Correspondingauthor.
E-mailaddress:sgillain@chu.ulg.ac.be,s.gillain@gmail.com(S.Gillain). 1877-0657/$–seefrontmatter#2013PublishedbyElsevierMassonSAS.
1. Englishversion 1.1. Introduction
Over thelast fewyears,studyinggait inolderadultshas raisedagreatdealofinterest.Indeed,gaitchangescanleadto falls increasing the risk of institutionalization, functional decline and onset of comorbidities [34]. Therefore, gait changesinolderadultscanbeconsideredasafrailtymarker. Recentstudies have underlined that changes in certain gait parameterscouldbeconsidered asasign ofcognitivefrailty [11,38]. Therefore, the concept of a ‘‘physiological senile gait’’ has been strongly argued and the question in fact remains:Isthe‘‘physiologicalsenilegait’’truly physiologi-callynormorcoulditreflect theonset ofsomepathological disorders,such as cognitiveones, leading to falls? Further-more, could there be a cut-off discriminatinghealthy older adultsfromfrailones?
It iswell known thatgait results from amotor command stemmingfromthecentralnervoussystemandisexecutedby the peripheral nervous system. The execution of this motor command involves not only the vestibular and peripheral nervous systems but also good quality osteoarticular and musclefeatures,withoutforgettingthecardiovascularsystem. Clinicalfeatures are the first step to evaluategait, including thoroughmedicalhistory(surgeries,treatments,and preexist-ing diseases), physical examination and other clinical tests, these elements are essential to understand the locomotor abilitiesinelderlypopulations.Nevertheless,nowadays there aretwocorecomponentsforanalyzingin-depthgaitfeatures: anatomical and functional analysis of the central nervous systeminchargeofmanagingmotorcommandsandmeasures of gait spatiotemporal parameters. In fact, motor command organizationcanbestudiedthroughimagingtechniquessuchas magnetic resonance imaging (MRI), functional MRI (fMRI) andpositronemissiontomography (PET).Thetestsandtools forgaitanalysisusedindailyclinicalpracticehaveshowntheir limitscomparedtoinstrumentalgaitanalysis[11,42].Walkway and accelerometric methods allow analyzing spatiotemporal gaitparametersandthesetechniqueshaverecentlybeenusedin oldpopulations.Thepurposeofthisarticleistocommentnew, useful and promising techniques for gait analysis in elderly subjects.ThisarticledidnotspecificallyfocusonParkinson’s diseaseor otherpathologieswheregaitchanges havealready beendefinedinspecificdomainswithin theliterature. 1.2. Method
The aim of this article was not to conduct a systematic review of the literature with precise inclusion or exclusion criteria,butinsteadtoproposeathematicreviewbasedthemost recentarticles andthose already known by the authors. The literatureselectionwas basedon:
theircontributiontothecoveralargeoverviewinputwithina largereviewofgaitanalysis;
experienceoftheworkingteam ingaitstudies;
practical aspect of the knowledge contained within the article.Inasecondtime,thereferencesofeacharticlewere studied andsomearticleswere selectedbythisway.
Toselectthemostrecentarticles,wecarriedoutasearchin theCochraneLibraryusingthe keywords‘‘gait ANDolder’’. Thisresultedineightarticlesbutinfact,onlytwowerefocused ongait(specificallygaitrehabilitation)inolderadults.Inthe samedatabase,usingthekeywords‘‘gaitANDelderly’’,only one article was found and this article only concerned gait rehabilitation.Noarticleswerefoundontheinputofmedical imagingandinstrumentalgaitanalysis.
We searched for articles in MEDLINE with the same keywordsand limitedoursearch to‘‘items withlinks tofull text, Human, English, French and Age>65years published withinthelast10years’’.Wefoundmorethan900references. The most interesting references were selected based on the previouslyreportedcriteria.Forty-sevenabstractwereinitially consideredtoamounttoafinalof12articles.
1.3. Results
1.3.1. Medical imagingcontribution
1.3.1.1. Magnetic resonance imaging. Table 1 lists the following commented studies. Zimmerman [45] highlighted a correlation between the anatomical structures of the hippocampus and changes in gaitparameters. In a group of 48 cognitively healthy older adults, mean age of 81years, hippocampusvolumewasmeasuredusingvolumetricMRIand itsmetabolismevaluatedbyprotonnuclearmagneticresonance spectrometry. A correlation between step length and hippo-campalvolumewasunveiled,aswellasarelationshipbetween step length variability and hippocampal metabolism. Some studiesreportedarelationshipbetweenvascularlesionsandgait changes[24,25].Arecentstudyevaluatedmobilityin331adults with no history of strokes and not affected by dementia or Parkinson’sdisease.Inthisgroupofhealthy olderadults,the vascularlesionsinthewhitematterandsubclinicalstrokeswere associated with slower gait speed, shorter stride length and longerdoublesupporttime[29].Furthermore,thesamestudy indicated a relationship between a greater step length variability andhigher prevalence of infarcts, including basal gangliainfarcts[30].
Morphological MRI has also promoted the ‘‘vascular’’ theorytoexplaingaitchangesinrelationstocognitivedisorders linkedwithaging.Ageitselfhasbeenrelatedto microangiopa-thy.Intwosimilarpublications,theroleofarterioscleroticbrain lesionsinthe developmentof dementiainpatientswithmild cognitiveimpairment(MCI)hasbeendemonstrated[14,27].
Inpreviousstudies,vascularlesionshavebeenidentifiedasa significant risk factor for developing gait changes and/or cognitivedecline. The risk of fallsdepends on how vascular lesions are distributed in the frontal region in charge of executive functions and organization of motor commands. Another study highlights the relevanceof subcortical lesions notonlyinfrontal regionsbutalsoinsevenspecificregions: frontal,temporal, parietal, andoccipitallobes, basal ganglia,
49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 99 100 100 101 104 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 S.Gillain,J.Petermans/AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx
internal capsule, external capsule and cerebellum. A multi-variateanalysisreportedthatsubcorticalvascularlesionswere the sole significant predictor for the risk of falls in elderly populations.Accordingtotheauthors,thiscouldberelatedto the subcortical hypoperfusioninterrupting long loopreflexes critical for gait andbalance mediated by deep white matter sensoryandmotortractsaswellsas descending motorfibers arisingfrommedialcorticalareas[12].
To sum up, it would seem that morphological MRI has unveiled a correlation between presence of vascular lesions, atrophyand hippocampalmetabolism tochanges ingait and subsequentrelationstothecognitiveevolutionofolderadults withMCI.
1.3.1.2. Functional imaging. Table 2 lists the studies dis-cussed. Structures involvedin gait control can be evaluated withtechniquessuchassinglephoton emission tomography with technetium (HMPAO-SPECT), near-infrared spectros-copy (NRIS), transcranial magnetic stimulation (TMS),
electro-encephalography (EEG),fMRI andPET. Depending ontechnicallimitations,fMRIandPET arethetechniquesmost oftenused[4]andthisiswhywechosetoonlyfocusonthese techniques. Furthermore, some studies reported in this paragraph concern young subjectsbecause evaluations have yettobeconductedinolderadults.FunctionalMRIdoesnot usearadioactivetracer,butinsteaditistheconcentrationof desoxyhemoglobinewhichreflectsariseintheactivationlevel. Thistechniquedistinguishesthecorticalorsubcorticalregions activatedduringthetaskrequestedbytheexaminerhowever, fMRI(requiringforthepatienttoremainstill)isnotableto studybrainactivationdirectlyduringtherealtask,butrather thesecondaryactivationobtainedwhenimaginingthistask.In 2006,Bakkeretal.[3]demonstratedthatcharacteristics(time needed)involvedinthemotorimageryofwalkingcomparedto realwalkingunderthesameconditions(pathlengthandpath width)inyoung people.Theyconcluded toahightemporal correspondence between real and imagined walking and unveiledthepossibilityofstudyingthecentralcomponentsof
160 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 Table1
Summaryofnewknowledgefrommagneticresonanceimaging(MRI).
Firstauthorsandreferences Observations
Zimmermanetal.,BrainRes,2009 Correlationbetweenstepslengthandthehippocampalvolumeandbetweenthevariability ofthestepslengthandthehippocampalmetabolism
Onenetal.,NeurosciLett355,2004 Onenetal.,BrainRes,2008
RelationshipvascularlesionsinspecificregionsandgaitdisordersinMCI
Onen,JNeuroradiol,2005 RoleofmicroangiopathyandcirculationofcerebralspinalfluidandgaitdisordersinMCI Q4 Rosanoetal.,Neuroepidemiology,2006 Vascularlesioninwhitematterandsubclinicalstrokesareassociatedwithslowergaitspeed,
shorterstridelengthandlongerdoublesupporttime
Rosanoetal.,Neuroepidemiology,2007 Infarctsinbasalgangliaareassociatedwithvariabilityofsteplength PughandLipsitz,NeurobiolAging,2002 Ageitselfisassociatedwithmicroangiopathy
Henry-Feugeasetal.,ClinIntervenAging,2008 RoleofarterioscleroticbrainlesionsinthedevelopmentofdementiainpatientswithMCI Guerinietal.,ArchPhysMedRehabil,2008 Subcorticalhypoperfusioninterruptinglongloopsreflexesofdeepwhite-mattermotor
tractsanddescendingmotorfibersarisingfrommedialcorticalareas MCI:mildcognitiveimpairment.
Table2
Summaryofnewknowledgefromfunctionalimagery.
Firstauthor,technicsandreferences Observations
Bakkeretal.,JNeuralTransm,2007 fMRIandPETscanaremostoftenusedtostudygait
Bakkeretal.,fMRI,ExpBrainRes,2007 Hightemporalcorrespondencebetweenrealandimaginedwalkinyoungpeople Personnieretal.,NeurosciLett,2010 Oldpeopleareatriskofoverestimatingthedurationofimaginedmovements Beauchetetal.,JNeurolSci,2010 Oldpeopleareatriskofunderestimatingthedurationofimaginedmovements
Malouinetal.,PETscan,HumBrainMapp,2003 Roleofthepre-supplementarymotorarea,legareaofthemotorcortexandbasalganglia involuntarylocomotormovements
Jahnetal.,fMRI,Neuroimage,2004 Standing:activationinthalami,leftputamen,leftfrontalgyriandvermis
Walking:activationinSMA,parahippocampalandfusiformgyri,occipitalvisualareas, inferiorfrontalgyri,leftputamenandvermis
JahnK,fMRI,BrainRes,2008 Importanceofactivityinparahippocampicandfusiformgyriwhenprecisedgaitisneeded DeshpandeandPatla,Galvanicvestibular
stimulations,BrainRes,2007
Decreasingdownregulationcapacityofvestibularinformationwithage
Zwergaletal.,fMRI,NeurobiolAging,2012 Corticalinhibitionandinteractionbetweensensorysystemsduringlocomotionandstance declineswithage
LaFouche`re,fMRIandPET,Neuroimage,2010 Roleofbasalgangliaintheinitiationofgait
Vidonietal.,fMRI,JNeurolPhysTher,2012 Decreasedactivationinaccessorymotorregions,supplementarymotorareaandcerebellum inearlystagesofAlzheimer’sdiseaseandincreasedcoactivationinprimarymotorcortex ofbilateralmotorandvisualregionsinADsubjects
AD:Alzheimer’sdisease;SMA:supplementarymotorarea.
gaitwiththistechnique.Toourknowledge,onlytwostudies comparingyoungandolderpeoplehavebeenconducted.One study demonstrated that older subjects overestimated the durationofimaginedmovements[26],whiletheotherstudy showedthattheimaginedperformancewasfasterthanthereal physicalperformances[7].Inthesestudies,thefirststepcould havebeentosystematicallyconsiderthecomparisonbetween time needed to perform the real task and time required for imagining that same task. Furthermore, considering the available scientific literature, the population studied by functional imaging must be completely defined and the conclusionsmaynotbeextrapolatedtootherpopulations.In 2003,Malouinetal.[21],inaPETstudyassessingsixhealthy adults (mean age: 55.9years) compared brain activation duringmotorimageryoflocomotor-relatedtasksandreported the involvement of the pre-supplementary motor area (pre-SMA)aswellasthelegareaofthemotorcortexinconditions requiringlocomotormovements(walking,initiatinggaitand walkingoveranobstacle).Thisstudyalsosuggestedthatthe basalgangliaplayedaroleinlocomotormovements,whichare automatic by nature. In 2004, Jahn et al. [17], in a study focusingon13healthyyoungsubjects(meanage:27.3years), compared cerebral activation during standing, walking and running. Standing was associated with activation in both thalami(moretotheright),theleftputamen,leftfrontalgyrus andcerebellar vermis andtherewere nodeactivation areas. Walkingdemonstratedactivationinadditionalmotorareaslike SMA,parahippocampalgyrusandfusiformgyrusaswellas occipitalvisualareas,inferiorfrontalgyrus,leftputamenand the vermis as well as the anterior lobe hemisphere of the cerebellum. When subjects imagined themselves walking, therewasanactivationinthevermis,(nexttotheareaactivated duringwalking)andinthepontomedullaryarea,furthermorea decreased activation of the fusiform gyrus and parahippo-campalgyrus washighlighted(just likeduring walking).In 2008, in a study evaluating nineteen healthy young adults (meanage:33.5years),thesameauthorsaskedthesubjectsto representthemselveswalking alongacurvedline,usingthe same method published in their previous study, and they validatedtheimportance oftheactivation in the parahippo-campal and fusiform gyrus when visual navigation was required to perform a precise walking task. However, deactivationswerenotedinthesuperiorandmedialtemporal gyrus. Jahn et al. suggested that this deactivation could decreasethe importance ofvestibular afferents and avoida possible conflict between visual and vestibular inputs [40]. Thismodulationoftheinformationcomingfromthevestibular systemwasconfirmedinastudybyDeshpandeandPatlausing galvanicvestibularstimulation(GVS)tothemastoidbone,the authors noted the effect of vestibular disruptions in the locomotorperformanceofyoung(ninehealthysubjectsaged 20–35years) andhealthyolderadults(age65–85years)[9]. Thisstudy showedthat inyoungpopulations, thevestibular stimulicanbedown-regulatedinfavorofbettervisualstimuli. However,thisdown regulationdoesdecline withinageand thus older adultsare more prone toimpaired balancewhen vestibular and visual stimuli differ. Similarly, it has been
demonstrated that the mechanism of cortical inhibitory reciprocalinteractionbetweenthesensorysystemsasobserved during locomotionand stance phasesdoes decline withage [46].These dataseem relevant when studyinggait in older adultswithsensoryimpairments.
Finally,theauthorcomparedtheresultsfromtwofunctional imaging techniques:fMRI and,18F-FDGPET, andvalidated theroleofbasalgangliaingaitinitiation(GI)inapopulation thatincludedsixteenhealthyadults (agerange: 51–73,mean age:61.37.8years)[18].
Briefly andaccording to the author’s research, the stance phase seemsmodulated by thebrainstem andthe cerebellum whilespecificareahavevariouswell-definedrolesduringgait: thebrainstemseemstoinvolvedingatinitiationandending,the corticalareas,basalgangliaandthalamiareimplicatedinGI andchangesindirection.
Thebasalgangliaandcorticalareasareresponsibleforgait changesforfollowingspecificdirectionoravoidingobstacles. Thecerebellumseemstocommandgaitrhythm andvelocity. CorticalareaslikeSMA areinvolvedthe cognitivecontrolof gaitanditsimportanceincreaseswithage.Infact,whileolder adults are less able to down-regulate vestibular inputs, the corticalcomponentseemsmoreimportantduringdirectedgait andchangesofdirection.Accordingtotherecentliterature,the activity of the cortical network increases with age and thus could explain difficulties in performing dual tasks. A recent study has reported that the network organizing gait evolves along a person’s lifetime and according to certain specific disorders[39].Then,intheearlystagesofAlzheimer’sdisease (AD),patientsexhibitadecreasedactivationintheaccessory motorareas,thesupplementarymotorareaandthecerebellum incomparisontosubjectswithoutdementia.Atthesametime ADsubjectsshowanincreasedcoactivationofbilateralmotor andvisualregionswiththe primarymotorcortex.
Considering the actual literature, available studies most oftenconcern younger people.Very fewhave focuson older adults and especially elderly populations with cognitive disorders. This lack of data could be explained by the difficultiesinconvincing olderadultstotrythesetechnics,as theyarenoteasytoreachandthetechniquesarecomplicatedto implement.Anotherdifficultyseemstolieintheinterpretation of the results as these cannot be extrapolated to other populations, furthermorecarrying out a comparison between ‘‘healthy’’ older adults and adults with specific disorders is quitedifficultandmost oftenincludesbias.
1.3.2. Contribution ofthe spatio-temporalparametersof gait
TheTable 3liststhe studiesdiscussed below.
Today,toconductaprecisestudy onspatiotemporalgait’s parameters there is a choice between treadmills (i.e., GaitRite1) or accelerometer devices (i.e., Locome´trix1 or Dynaport1). Many teams have used the GaitRite1 system (howeverothertypesoftreadmillsareavailable).Thistreadmill comes in different distances and is equipped with pressure sensorstomeasurespatiotemporalparameters.Collecteddata consistinspeed,numberofgaitcycles,steplengthandwidthas
197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 S.Gillain,J.Petermans/AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx
well as duration of the double stance period. Then, by calculating the variables’ coefficient of variation (CV) and comparingeachgaitcycletotheother,itispossibletoexpress gait‘‘variability’’.
Aswell-detailedinarecentreviewregardingtherelevance ofgaitanalysis,thesetechnicshelptoimprovetheprecisionof gaitprofiles, much better than clinical testsalone could [8]. Then, in the last ten years, studies which have used these techniqueshavereportedthatwithagewalkingrequiresmore attention[41].
Someauthorshaveshownthatgaitspeedandvariabilityare two predictors for the risk of falls in older adults [36]; a variationof0.017minsteplengthwithinagaitcycleactually increasesthisrisktwofold[13].Afewyearsago, BrianMaki usingfootswitches,reportedthatdecreasedspeed,reducedstep lengthandincreaseddurationofthedoublestanceperiodwere independent fall predictors. However in the same study the authorhighlightedthatstep-to-stepvariabilitywasnotrelated totheriskoffallsbutratherassociatedwiththefearoffalling [20].Unfortunately,acomparisonbetweenthesethreestudies remainsdifficultwithoutacompleteanddetaileddescriptionof the three different populations and the patients’ potential historyof fallsprior tothe evaluation.
UsingGaitRite1,numerousauthorshavedemonstratedthe relevance of analyzing gait during dual task, i.e. asking the subject towalk while simultaneouslycompleting acognitive task.Threeparameters,gaitspeedsteplengthandvariabilityof gaitparameters,seemgoodpredictorsfortheriskoffallsinthis condition[6,10].
Other teams have studied older adults at the onset of cognitivedisordersor Alzheimer’sdisease andhavereported theinfluenceof memoryandexecutivefunctions[1]butalso the importance of divided attention capacities [31] on the variability of gait parameters, mainly gait speed [15]. Most recently, a significant relationship was reported between an increasedCVforsteptime(i.e.,timeneededtocompleteagait cycle)inolderadultswithfrontotemporaldementia,compared toolderadultssufferingfromAD andtohealthysubjects[2].
In asurvey of 400 subjects withoutcognitivedisorders,a cognitive assessment and instrumental study of their gait parameterswereperformedatthebeginningofthe studyand after 5years. At the 5-year visit, the authors described a significantcorrelation(P=0.02)betweentheevolutionofgait speed,steplengthandglobaldeclineincognitiveandexecutive functions, oncevariables hadbeen adjusted for age, sexand levelof education[37].
Arecentstudyreportedthereliabilityoftheresultsobtained using a triaxial accelerometer device (Dynaport1) based on two 18- meter walking courses. Furthermore, the results obtainedwerecorrelatedwithfallsandfunctionalstatus[5]in olderadults.Inthiscontext,ourteamanalyzedgaitparameters withatriaxialportableaccelerometer,theLocome´trix1.This device, fitted around the patient’s waist with an elastic belt, recordedtheaccelerationsintheantero-posterior,medio-lateral and cranio-caudal axes. Gait parameters were analyzed in a populationofhealthyolderadults,adultswithMCIandadults withAlzheimer’sdisease(AD).Inallthreegroups,thesubjects hadtowalkalongastraight,40-meterlongcorridor,inasimple task (walking) and dual task (walking while counting backwards).Inbothconditions,theLocome´trix1differentiated thethreepopulationsbasedontheirgaitprofilerelatedtotheir cognitivestatus[11].
The instrumental gait analysis seems quite relevant for discriminating one or several spatiotemporal variables that couldincreasetheriskoffallingandhelpidentifysubjectswith cognitivedisordersbasedontheirgaitprofileandthusdiscern thoseatriskof developingdementia.
Thesemethodsforstudyinggaitparametershaveshownthat agewasnottheonlyelementtoexplaingaitvariability.Infact, factors such as cognitivedisorders, histories historyof falls, givenwalkingspeedandgaitconditions(singleordualtask)do haveanimpactongaitinolderpopulationsandremainuseful indicators to evaluate the risk of falls or predict cognitive evolution.Then,consideringtheseparametersandinorderto assess gaitit isessential torefinegaitconditions, population characteristics(not onlyagebuthistoryoffalls,medications,
310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 Table3
Contributionofthespatio-temporalparametersofgait.
Author,references Observations
BridenbaughandKressig,Gerontology,2011 Instrumentalmethodmoreprecisethanclinicaltests Wangetal.,JNeuralTransm,2009 Attentionalcomponentofgaitincreasewithage
Vergheseetal.,JGerontolABiolSciMedSci,2009 Gaitspeedandvariabilityofgaitaretwomarkerofrisktofall
Hausdorffetal.,ArchPhysMedRehabil,2001 Anincreaseof0.017minthelengthofthestepinacycleofstepdoublestherisktofall Maki,JAmGeriatrSoc,1997 Variabilityofgaitisamarkeroffearoffallingnotamarkeroffallrisk
Beauchetetal.,JAGS,2008 Dubostetal.,HumMovSci,2006
Interestofstudythespeedandthelengthofthestepandthevariabilityofgaitduring dualtaskconsideringtheriskoffalls
Allalietal.,DementGeriatrCognDisord,2008 Importanceofexecutivefunctionsconsideringthevariabilityofthegait Sheridanetal.,JAGS,2003 Importanceofdividedattentioncapacitiesconsideringthevariabilityofthegait Holtzeretal.,Neuropsychology,2007 Importanceofcognitivefunctionsconsideringthevariabilityofgaitspeed Allalietal.,MovDisord,2010 Specificgait’sprofileconsideringpeoplewithADorfronto-temporaldementia Vergheseetal.,JNeurolNeurosurgPsychiatry,2007 Modificationsofgait’sprofilecouldhelptopredictthecognitiveevolutionofMCI Bautmansetal.,GaitPosture,2011 ReliabilitybetweentheresultsobtainedbyDynaport1
andGaitRite1
whenbasedon twowalksover18mandcorrelationwithfallsandfunctionalstatusinoldersubjects Gillainetal.,AnnPhysRehabilMed,2009 Anaccelerometricdeviceallowstohighlightspecificgait’sprofilesaccordingto
thecognitivestatusofoldersubjects MCI:mildcognitiveimpairment;AD:Alzheimer’sdisease.
comorbidities,sensoryimpairments,neurologicdisorders...), requiredwalkingspeedandevaluationtechnicused.It seems important to note that results from a study with a specific technicconductedonaspecificpopulationandusingaspecific protocolcannotbeextrapolatedtoothersituations.Inlightof the above, teams who are studying gait do encounter some generaldifficultiesingeriatricpopulations:designofthestudy and finding a balance between the need to highlight some results with a strong statistical power and the relevance of underlingthisresultina‘‘real-life’’population.
1.3.3. Gaitinitiation
More recently, several teams have tried with various techniques to study the precise onset of GI. Indeed, this moment seems particularly dangerous for older adults presenting arisk of falls.GIisa voluntarytransition froma stabledoublestancepositiontoacontinuouslyunstableposture when walking, which requires anticipatory postural adjust-mentstoshiftthecenterofmasstowardsthesupportingsideto lift-upthe leg [32]. As showed bysingle-photon or positron emissiontomography[21]or repetitivetranscranialmagnetic stimulation [16] GI requires the activation of the SMA and basal ganglia also seem to be playing a crucial role as demonstrated in subjects with in Parkinson’s disease (PD) subject[43].GIisoftenevaluatedusingforceplatforms.Inthe pastyears, severalteams have studied GI ina population of healthyolderadults[22],in olderpeoplewithfearof falling [33],fallers[23],subjectswithPD[28]andAD[44].GIseems to vary according to the population studied. Further studies shouldbeconductedtovalidateandrefinetheseobservations. 1.4. Discussionand conclusion
Several studies have reported the relevance of gait assessment in older populations. New imaging techniques andinstrumentalanalysesenabletounderlinetherelationship betweenanatomyandmetabolismofthecentralstructuresand spatiotemporalgaitparameters.Gaitseemstobeanindicatorof ‘‘successful aging’’ by predicting cognitive and functional changes. Unfortunately, and despite very useful elements provided by these new techniques, they remain quite confidential, restrained to an experimental setting and are notwidelyavailableinclinicalpractice.Steplength,gaitspeed and variability seem essential indicators of gait quality. Moreover, studying gait in dual task condition could bring informationontheriskoffalls,andcognitivereserveallocated forgaitorganization.Furthermore,inthiselderlypopulationit seemsquiterelevanttoconductsystematicgaitevaluationsin single and dual task conditions associated with a long-term follow-up.
Finally, GI seems a crucial element to evaluate safety in olderadults.Studyingthisspecificmoment,couldbetterrefine theunderlying mechanisms involvedingaitandbalanceand worktowardsimproving them.
Inouropinion,clinicaltestsremainessentialforevaluating quickly and efficiently the gait and balance of older adults, available testsinclude the 10-meter walking test to evaluate
speed, the Timed-up-and-go test, the short physical perfor-mance battery including the Sit-to-Stand test, the Berg or Tinettibalanceteststestshouldremainthebestwaytoperform a quick useful study of the balance of older subjects. Concerningdualtaskcondition,theStopwalkingwhentalking test represent a very good predictor of risk [19]. Indeed, comparing gait speed in single and dual task is a relevant screening tool to evaluate the risk of falls; with a low 40% sensitivitybut ahigh96%specificity[35].
In choosing asystematic method for gait assessment, the mostimportantthingwouldbetoselectsomeeasytoperform test,reproducibleunderthesameconditionsandwellknownby theexaminerinordertobesystematicallyrepeated.Finally,a hand grip test or Martin’s vigorimeter could be relevant to evaluate muscle mass inelderly populations and predict the evolutionoftheirandfuturefunctionalstatus.Inthefuture,the useofthesenewtechnics,enhancing‘‘central’’or‘‘peripheral’’ markers with a predictivevalue for functionaland cognitive decline,mightimprovethedetectionofpeopleatriskoffalling and enable teams to propose multidisciplinary screening evaluation and monitoring follow-ups. These studies might permitthedesignofadaptedandspecificgaitbutalsocognitive rehabilitationprotocols,inapopulationof frailolderadults.
Disclosureofinterest
Theauthorshavenotsuppliedtheirdeclarationofconflictof
interest. Q2
2. Versionfranc¸aise 2.1. Introduction
Aucoursdecesdernie`resanne´es,l’e´tudedelamarchechez le sujet aˆge´ a suscite´ beaucoup d’attention. En effet, une alte´rationdelamarchepeutentraıˆnerdeschutesetaugmenter le risque de placement, de de´clin cognitif et la survenue de comorbidite´s [34]. C’est pourquoi les changements de la marche peuvent eˆtre conside´re´s comme un indicateur de fragilite´. Des travauxre´centsmontrent que lesalte´rationsde certains parame`tres de la marche peuvent eˆtre conside´re´es commeunsignedefragilite´ cognitive[11,38].Leconceptde « de´marche se´nile physiologique » est donc conteste´. Le questionnementactuelduclinicienest:–La«de´marchese´nile physiologique » estvraiment physiologiquement normale ou est-ellelerefletd’unprocessuspathologiquede´butant,comme untroublecognitif,pouvantentraıˆnerdeschutes?–Etqu’en est-ild’une´ventuelseuilpermettantdediffe´rencierlapersonne aˆge´eenbonnesante´ de lapersonne aˆge´efragile?
Ilestadmisquelamarcheestlere´sultatd’unecommande motrice e´manant du syste`me nerveux central et exe´cute´e au niveau du syste`me nerveux pe´riphe´rique. L’exe´cution de la commande motrice est possible graˆce a` l’implication du syste`me vestibulaire, dusyste`me nerveux pe´riphe´rique et du syste`mecardiovasculairemaise´galementparunebonnequalite´ musculaireetoste´oarticulaire. 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 S.Gillain,J.Petermans/AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx
Poure´tudierlamarche,ilestne´cessaired’e´tudierlesaspects cliniques. Une liste exhaustive des ante´ce´dents (chirurgies, traitements me´dicaux, conditions pre´existantes), examen physiqueettestscliniquessontessentielsa` la compre´hension delamobilite´ delapersonneaˆge´e.Deplus,ilexistedeuxvoies d’analysedel’organisationspe´cifiquedelamarche:l’analyse anatomique et fonctionnelle du syste`me nerveux central qui organise la commande motrice et la mesure des parame`tres spatiotemporelsdelamarche.L’organisationdelacommande motricepeutactuellement eˆtrepre´cise´egraˆceauxtechniques d’imagerie par re´sonance magne´tique (IRM), IRM fonction-nelle(IRMf),ettomographiepare´missiondepositons(PET). Quant a` l’e´tude pre´cise des parame`tres de marche, les tests cliniques utilise´s en pratique quotidienne ont rapidement montre´ leurslimitescompare´ auxanalysesinstrumentalesdes parame`tresdemarche[11,42].Eneffet,lestapisdemarcheet les acce´le´rome`tres permettant l’analyse des parame`tres spatiotemporelsdelamarche,onte´te´ re´cemmentutilise´schez lesujetaˆge´.
L’objectif de cet article est de discuter des nouvelles techniquesd’analysedelamarchechezlesujetaˆge´.Lamaladie de Parkinson ainsi que d’autres pathologies incluant des modificationsde lamarche de´ja` de´criteslors de publications spe´cifiques,nesontpasaborde´es.
2.2. Me´thode
Le but de cet article n’est pas de mener une revue syste´matique de la litte´rature. Lesauteurs proposent ici une revue the´matique base´e sur les articles re´cents et d’autres pre´ce´demment connus des auteurs. Les articles ont e´te´ se´lectionne´sselon:
leurcontribution a` unelargerevuethe´matique;
l’expertise des principaux auteurs concernant l’e´tudede la marche;
l’aspect pratique des connaissances et de´couvertes cite´es dans l’article.
Ensuite,lesauteursontanalyse´ labibliographiedechaque article afin de se´lectionner d’autres re´fe´rences contributives. Lesrecherches bibliographiquesont e´te´ mene´esauseindela Cochrane Library avec les mots cle´s « gait AND older » (marcheETaˆge´).Nous avonsidentifie´ ainsihuitarticlesdont deux de´crivaient spe´cifiquementla re´e´ducation dela marche chezlapersonne aˆge´e.Dansla meˆmebasededonne´es eten utilisantlesmots«gaitANDelderly»(marcheETpersonnes aˆge´es),nousn’avonsretrouve´ qu’unseulearticleportantsurla re´e´ducation fonctionnelle uniquement. Aucun article n’a e´te´ retrouve´ sur la contribution de l’imagerie et des techniques d’analyseinstrumentaledelamarche.Lesauteursontensuite cherche´ viaMEDLINE aveclesmeˆmesmotscle´senlimitant avec « articles complets uniquement, Humains, Anglais, Franc¸ais, Aˆ ge : +65ans, publie´s au cours des dix dernie`res anne´es».
Nous avons retrouve´ plus de 900 re´fe´rences. Les plus inte´ressantes e´taient se´lectionne´es en fonction des crite`res
de´critsplushaut.Initialement,47re´sume´sfurentconside´re´set seulement12articlesfinalementretenus.
2.3. Re´sultats
2.3.1. Apportdel’imagerie
2.3.1.1. L’imagerie a` re´sonance magne´tique. Le Tableau 1 re´sume lesdiffe´rentese´tudes de´crites.
Dansungroupede48patientsaˆge´setcognitivementsains (aˆgemoyende81ans),levolumedel’hippocampeae´te´ mesure´ parIRMvolume´triqueetsonme´tabolismepartomographiepar e´mission de positons [45]. Les auteurs ont montre´ une corre´lation entre la longueur dupas et levolume hippocam-piqueainsiqu’unerelationentrelavariabilite´ delalongueurdu pasetleme´tabolismehippocampique.
Concernant l’influence des le´sions vasculaires, une e´tude re´cente vient confirmer les re´sultats pre´ce´demment obtenus [24,25]. Lesauteurs ont e´value´ la mobilite´ chez 331 adultes sans ante´ce´dents d’AVC, de´mence ou maladiede Parkinson. Danscegroupedepersonnesaˆge´esenbonnesante´,lesle´sions vasculaires de la substance blanche et les AVC silencieux e´taientrelie´sa` unevitessedemarchepluslente,unelongueur de pas plus courte et unedure´e de phase de double support augmente´e[29].Deplus,lameˆmee´tudemontraitunlienentre augmentation de la variabilite´ de la longueur du pas et augmentationdelapre´valencedesinfarctusycomprispourles noyauxgriscentraux[30].
L’IRM morphologique soutient e´galement la the´orie « vasculaire» pour expliquerlesmodifications dela marche etcertainstroublescognitifsapparaissantavecl’aˆge.Eneffet, dans deux publications similaires, le roˆle des le´sions athe´roscle´rotiquesdanslede´veloppementdelade´mencechez lespatientsMCIae´te´ misene´vidence[14,27].
Enconside´rantlese´tudespre´ce´dentes,lesle´sions vasculai-ressemblentunfacteurderisquesignificatifdude´veloppement d’alte´rationsdelamarcheet/oud’unde´clincognitif.Lerisque de chutes de´pend de la topographie des le´sions vasculaires pre´sentes dans la re´gion frontale, responsable des fonctions exe´cutivesetdel’organisationdelacommandemotrice.Une autre e´tude souligne l’importancedes le´sions sous-corticales nonseulementdanslare´gionfrontalemaise´galementdanssept re´gions spe´cifiques : frontale, temporale, lobes parie´taux et occipitaux, noyaux gris centraux, capsule interne, capsule externeetlecervelet.L’analysestatistiquemultivarie´emontre queseuleslesle´sionsvasculairessous-corticalesconstituentun facteurderisquepre´dictifdechutesdansunepopulationaˆge´e de´termine´e[12].
Selonlesauteurs,leme´canismesous-jacentpourraiteˆtreune hypoperfusionsous-corticaleinterrompantlesre´flexesa` longue boucledesvoiesmotricesdelasubstanceblancheprofondeet desfibresmotricesissuesdesairescorticalesme´dianes.
En re´sume´, il semble que l’IRM morphologique souligne unecorre´lationentrepre´sencedele´sionsvasculaires,atrophie de l’hippocampe, changements de la marche et leurs implications dansl’e´volutioncognitivedessujetsaˆge´sMCI.
491 492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510 511 512 513 514 515 516 517 518 519 520 521 522 522 523 523 524 524 525 525 526 527 527 528 528 529 522 522 523 524 524 525 526 527 527 528 529 530 531 532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 S.Gillain,J.Petermans/AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx 7
2.3.1.2. Imagerie fonctionnelle. Le Tableau 2 re´sume les principalese´tudes.
Les structures implique´es dans le controˆle de la marche peuventeˆtreanalyse´esa` l’aidedenouvellestechniquescomme la TEMP/SPECT-HMPAO, une tomographie d’e´mission monophotonique avec techne´tium, la spectroscopie proche infrarouge NIRS), la stimulation magne´tique transcranienne (SMT), l’e´lectroence´phalographie (EEG), l’IRMf et le PET-scan.Enfonctiondeslimitestechniques,l’IRMfonctionnelleet le PET-scan sont les me´thodes d’imagerie les plus souvent utilise´es[4]etc’estpourcelaquenousavonschoisideparler uniquementdecesdeuxtechniques.Deplus,certainese´tudes de´critesdans ceparagrapheconcernent unepopulation jeune car aucune e´tude similaire n’est retrouve´e au sein d’une populationaˆge´e.
L’IRMfn’utilisepasdetraceurradioactif,maisde´tecteles changements de concentration de la de´soxyhe´moglobine qui refle`tentlesdiffe´rencesd’activationsentreplusieursconditions. Cette technique diffe´rentie les zones corticales et sous-corticalesactive´esparlestaˆchesdemande´esparl’examinateur. L’IRMf (ne´cessitant que le patient reste immobile) ne peut e´tudier l’activation ce´re´brale lie´e directement a` la ve´ritable actionmaiselleanalysel’activationsecondaireobtenuequand le sujet se repre´sente mentalement cette action. En 2006, Bakker et al. [3] ont montre´ que le temps ne´cessaire a` la repre´sentation mentaledelamarche e´tait comparablea` celle d’une marche re´elle dans lesmeˆmes conditions (longueur et largeur du pas) chez le sujet jeune. Ils ont conclu a` une concordance temporelle forte entre la marche re´elle et la marche imagine´e et la possibilite´ d’e´tudier les me´canismes
602 603 604 605 606 607 608 609 610 611 612 613 614 615 616 617 617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 Tableau1
Re´sume´ desnouvellesconnaissancesgraˆcea` l’imagerie.
Premierauteuretre´fe´rencesbibliographiques Observations
Zimmermanetal.,BrainRes,2009 Corre´lationentrelalongueurdupasetlevolumehippocampiqueainsiqu’entrelavariabilite´ delalongueurdupasetleme´tabolismehippocampique
Onenetal.,NeurosciLett355,2004 Onenetal.,BrainRes,2008
Lienentrele´sionsvasculairesdansdeszonesspe´cifiquesettroublesdelamarchechez lapersonneMCI
OnenF.,JNeuroradiol,2005 Roˆledelamicroangiopathieetcirculationduliquidece´phalorachidiendanslestroubles delamarchechezlapersonneMCI
Rosanoetal.,Neuroepidemiology,2006 Le´sionvasculairedelasubstanceblancheetAVCsilencieuxsontassocie´savecunemarcheralentie, unpasraccourcietuneaugmentationdeladure´edelaphasededoublesupport
Rosanoetal.,Neuroepidemiology,2007 Infarctusdesnoyauxgriscentrauxsontassocie´sa` lavariabilite´ delalongueurdupas PughetLipsitz,NeurobiolAging,2002 L’aˆgelui-meˆmeestassocie´ a` lamicroangiopathie
Henry-Feugeasetal.,ClinIntervenAging,2008 Roˆledesle´sionsce´re´bralesathe´roscle´rotiquesdanslede´veloppementdelade´mence chezlapersonneMCI
Guerinietal.,ArchPhysMedRehabil,2008 Hypoperfusionsous-corticaleinterrompantlesre´flexesa` longueboucledesvoiesmotrices delasubstanceblancheprofondeetdesfibresmotricesissuesdesairescorticalesme´diane MCI:mildcognitiveimpairment.
Tableau2
Re´sume´ desnouvellesconnaissancesgraˆcea` l’imageriefonctionnelle. Premierauteuretre´fe´rencesbibliographiques Observations
Bakkeretal.,JNeuralTransm,2007 IRMfetPET-Scansontlestechniqueslesplussouventutilise´esdansl’analysedelamarche Bakkeretal.,fMRI,ExpBrainRes,2007 Concordancetemporelleforteentremarchere´elleetmarcheimagine´echezlesujetjeune Personnieretal.,NeurosciLett,2010 Tendancedusujetaˆge´ a` surestimerladure´edesmouvementsimagine´s
Beauchetetal.,JNeurolSci,2010 Tendancedusujetaˆge´ a` sous-estimerladure´edesmouvementsimagine´s
Malouinetal.,PETscan,HumBrainMapp,2003 Roˆledel’airemotricepre´-supple´mentaire(pre´-AMS),delare´gionjambeducortexmoteuret desnoyauxgriscentrauxdanslesmouvementslocomoteursvolontaires
Jahnetal.,fMRI,Neuroimage,2004 Stationdebout:activationdesthalamus,putamengauche,gyrusfrontalgaucheetvermis Marche:activationdel’AMS,gyrusparahippocampiqueetfusiforme,airesvisuelles occipitales,gyrusfrontalinfe´rieur,putamengaucheetvermis
JahnK.,fMRI,BrainRes,2008 Importancedel’activite´ danslegyrusparahippocampiqueetlegyrusfusiformequand lamarchedoiteˆtrepre´cise
DeshpandeetPatla,Galvanicvestibularstimulations, BrainRes,2007
Diminutiondelacapacite´ d’atte´nuationdel’informationvestibulaireavecl’aˆge
Zwergaletal.,fMRI,Neurobiologyofaging,2012 Inhibitioncorticaleetinteractionentrelessyste`messensorielsdurantlamarcheetlaphase desupportde´clinentavecl’aˆge
LaFouche`re,fMRIandPET,Neuroimage,2010 Roˆledesnoyauxgriscentrauxdansl’initiationdelamarche
Vidonietal.,fMRI,JNeurolPhysTher.2012 Activationdiminue´edanslesre´gionsmotricesaccessoires,airemotricesupple´mentaires etlecerveletchezlespatientsauxstadespre´cocesdelamaladied’Alzheimeretaugmentationde lacoactivationdanslecortexmoteurprimairedesre´gionsmotricesetvisuelleschezlessujets atteintsdeMA
MA:maladied’Alzheimer;pre´-AMS:airemotricepre´-supple´mentaire.
S.Gillain,J.Petermans/AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx 8
sous-jacents de la marche de cette manie`re. A` notre connaissance, il existe seulement deux e´tudes comparant les sujetsjeunesetlessujetsaˆge´s.Unee´tudemontraitquelesujet aˆge´ surestimait la dure´e des mouvements imagine´s [26]. Et l’autree´tudemontraitquel’action imagine´ee´tait plusrapide quel’actionphysiqueelle-meˆme[7].Lorsdelare´alisationde cetyped’e´tudeilsembledoncne´cessairedecomparerletemps ne´cessaire pour accomplir la taˆche et le temps passe´ a` se repre´senterlataˆche.Deplus,lapopulatione´tudie´eenimagerie fonctionnelle doit eˆtrepre´cise´mentde´finie etles conclusions obtenuesdans ungroupeetselonunprotocolebiende´finine peuventeˆtreextrapole´esa` d’autresgroupesnicompare´esaux re´sultatsobtenusavec d’autresprotocoles.
En2003,Malouinetal.[21],dans leure´tudesurPETscan avec six sujets sains (aˆge moyen de 59ans) comparaient l’activation ce´re´brale durant l’imagerie motrice d’une taˆche locomotriceetmontraient l’implicationde l’airemotrice pre´-supple´mentaire (pre´-AMS), et la re´gion jambes du cortex moteur dans des conditions ne´cessitant des mouvements locomoteurs (marche, initiation de la marche (IM) et franchissementd’unobstacle).Cettee´tudemontraite´galement leroˆlejoue´ parlesnoyauxgriscentrauxdanslesmouvements locomoteurs,automatiquesparnature.
En 2004,Jahn et al. [17], dans unee´tude chez 13 sujets jeunes en bonne sante´ (aˆge moyen 27,3ans), comparaient l’activationce´re´braleenpositiondebout,durantlamarcheetla course.Lapositiondeboute´taitassocie´eavecuneactivationau seindesthalamus(plusversladroite),duputamengauche,du gyrusfrontalgaucheetduvermis,deplusiln’existaitpasde de´sactivationdesautresre´gions.Lamarche,quanta` elle,e´tait lie´ea` uneactivationauseindesairesmotricessupple´mentaires comme l’AMS, du gyrus parahippocampique et du gyrus fusiforme ainsi qu’au sein desaires visuellesoccipitales, du gyrusfrontalinfe´rieur,duputamengauche,duvermisetdulobe ante´rieurducervelet.
En2008,ce meˆmeauteuramene´ unee´tudesur19jeunes adultes en bonne sante´ (aˆge moyen 33,5ans), en leur demandant de s’imaginer marchant le long d’une ligne incurve´e, il a utilise´ la meˆme me´thode de´crite lors de son e´tudepre´ce´dente,etilavalide´ l’importancedel’activationdu gyrus parahippocampique et du gyrus fusiforme quand la navigation visuelle est indispensable pour mener a` bien un sche´mapre´cisdemarche.Cependant,deszonesde de´sactiva-tion e´taientidentifie´esdans legyrus temporal supe´rieuretle gyrustemporelmoyen.Jahnasugge´re´ quecettede´sactivation diminuait l’importance des affe´rences vestibulaires et ainsi e´vitaitunconflite´ventuelentrelesinformationsprovenantdes syste`mes visuel et vestibulaire [40]. Cette modulation de l’information du syste`me vestibulaire semble avoir e´te´ confirme´e dans l’e´tude de Deshpande et Patla, utilisant une stimulationvestibulairegalvaniqueauniveaudel’osmastoı¨de pour souligner l’effet de la perturbation vestibulaire sur la performancelocomotricechezlesujet jeuneetsain (de20 a` 35ans)etlapersonneaˆge´eenbonnesante´ (de65a` 85ans)[9]. Cette e´tudesoulignait que chez le sujet jeune, l’information vestibulairepouvaiteˆtreatte´nue´epourfavoriserl’information visuelle.Cependant,cettecapacite´ d’atte´nuationdiminueavec
l’aˆgeetlesujetaˆge´ estplussensibleaude´se´quilibrequandles informations vestibulaire et visuelle diffe`rent. De la meˆme fac¸on, il a e´te´ de´montre´ que le me´canisme d’interaction inhibitricere´ciproqueentrelessyste`messensorielspendantla marcheetlapositionde´boutde´clinechezlesujetaˆge´[46].Ces donne´essemblentimportantespour e´tudierlamarchechezla personne aˆge´e atteinte de de´ficits sensoriels. Enfin, en comparant les re´sultats de deux techniques d’imagerie fonctionnelle, l’IRMf et le 18F-FDG PET scan, l’auteur a valide´ leroˆledesnoyauxgriscentrauxdansl’IMauseind’une populationde16adultesenbonnesante´ (entre51et73ans,aˆge moyen:61,3ans7,8ans)[18].
SelonJahnetal.,durantlamarche,lesre´gionsce´re´bralesont des roˆles spe´cifiques: le tronc ce´re´bralestimplique´ dans le de´butetlafindelamarchealorsquel’airecorticale,lesnoyaux gris centraux et les thalamus s’activent pendant l’IM et les changements de direction. Lesnoyaux griscentraux etl’aire corticalesontresponsablesdelamodulationdelamarchepour suivre des directions spe´cifiques ou dans le but d’e´viter un obstacle.Lecerveletsemblecommanderlerythmeetlavitesse de marche. Certaines aires corticales, comme l’AMS, sont implique´es dans le controˆle cognitif de la marche et leur importanceaugmenteavecl’aˆge.Eneffet,alorsque l’atte´nua-tion de l’information provenant du syste`me vestibulaire est moinsefficaceavecl’aˆge,lacomposantecorticalesembleplus importantequandlamarchetendversunbutpre´cisetdurantles changementsdedirection.Selondese´tudesre´centes,l’activite´ du re´seau cortical augmente avec l’aˆge, expliquant ainsi les difficulte´s a` accomplir plusieurs taˆches. Une e´tude re´cente confirmequelere´seaucoordonnantlamarchesemodifieavec l’aˆge et lors de certaines pathologies [39]. Dans les stades pre´cocesdelamaladied’Alzheimer(MA),lessujetssemblent pre´senter une diminution de l’activation dans les re´gions motricesducortex,l’airemotricesupple´mentaireetlecervelet compare´ auxsujetssains.Deplus,cesmeˆmessujetsatteintsde laMAmontrentuneaugmentationdelacoactivationauseindu cortex moteur primaire des aires motrices et visuelles bilate´rales.
Les re´centes e´tudes disponibles se focalisent sur des populations jeunes. Tre`s peu de travaux sont mene´s sur des populations aˆge´es et surtout des sujets aˆge´s souffrant de troublescognitifs.Cemanquededonne´espeuteˆtreexplique´ par diffe´rents e´le´ments. D’abord, le nombre restreint de centres disposantdecetypedetechniquesetladifficulte´ d’amenerune population de personnes aˆge´es a` se mobiliser pour de telles e´tudes. Un autre facteur limitant e´tant la difficulte´ d’inter-pre´tation desre´sultatsobtenusau seindepetitsgroupes etla difficulte´ d’extrapolercesre´sultatsa` depluslargespopulations. 2.3.2. Contribution desparame`tresspatiotemporelsde la marche
LeTableau3 re´sumelesdiffe´rentese´tudes.
A` l’heure actuelle, l’e´tude pre´cise des parame`tres spatio-temporels de la marche ne´cessite l’utilisation de tapis de marche (comme le GaitRite1) ou de me´thodes acce´le´rome´-triques(Locome´trix1ouDynaport1).Denombreusese´quipes utilisent le syste`me GaitRite1 (bien que d’autres syste`mes
632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730 731 732 733 734 735 736 737 738 739 740 741 742 743 744 S.Gillain,J.Petermans/AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx 9
existent).Cetapisdemarcheexisteenplusieurslongueursetil est e´quipe´ de capteurs de pression mesurant les parame`tres spatiotemporelsdelamarche.Lesdonne´esenregistre´essontla vitesse,ladure´educycledemarche,longueuretlargeurdepas etdure´e delaphasedesimplesupport.Enfin,encalculantle coefficient de variation du temps du cycle de marche et en comparant entreeux chaque cyclede marche, il estpossible d’exprimerla« variabilite´ »delamarche.
Comme re´cemment rapporte´ dans une revue sur la pertinencedel’analysedelamarche,cestechniquespermettent d’affinerleprofildemarchebienpluspre´cise´mentquelesseuls testscliniques[8].Deplus,aucoursdesdixdernie`resanne´es, l’utilisation de ces techniques a montre´ qu’avec l’aˆge, la personne doit se concentrer sur l’action de marcher [41]. Certainsauteursontsouligne´ quelavitesseetlavariabilite´ dela marche sont deux indicateurs du risque de chutes chez la personneaˆge´e[36];unevariationde0,017mdelalongueurdu pasdansuncycledepasdoublecerisque[13].Quelquesanne´es auparavant,BrianMakia` l’aidedecapteurssouschaquepied, rapportequ’unevitessere´duite,unediminutiondelalongueur dupasetl’augmentationdutempsdephasedesupporte´taient desfacteursinde´pendants de risquede chutes. Mais,dans la meˆme e´tude l’auteur souligne qu’une augmentation de la variabilite´ entre les cycles de marche n’est pas associe´e au risquede chutes mais uniquement a` la peurde tomber [20]. Malheureusement,ilestdifficiledecomparercestroise´tudes sansdisposer desdescriptions et caracte´ristiques exactes des populations e´tudie´es et de leurs ante´ce´dents de chutes avant l’e´valuation.
En utilisant le GaitRite1 plusieurs auteurs ont releve´ l’importancedel’e´tude delamarche en conditiondedouble taˆche, consistant a` demander au sujet de marcher tout en exe´cutantunetaˆchecognitive.Troisparame`tres:lavitesse,la longueurdupasetlavariabilite´ delamarchesemblentpre´dire
avecacuite´ lerisquedechutesdanscetteconditiondedouble taˆche[6,10].
D’autrese´quipesayantmene´ dese´tudessurdespatientsaˆge´s aude´butd’unde´veloppementdetroublescognitifsoudeMA, ont souligne´ l’influence de la me´moire, des fonctions exe´cutives [1] mais e´galement de la capacite´ a` diviser l’attention[31]surlavariabilite´ desparame`tresdelamarche et notamment la vitesse [15]. Plus re´cemment, un lien significatif a e´te´ valide´ entre l’augmentation du coefficient de variation du temps de cycle de marche chezle sujet aˆge´ atteintdede´mence fronto-temporaleencomparaisonausujet sain[2].Dansunee´tudesur400sujetssainsd’esprit,lesauteurs ontmisenplaceunee´valuationcognitiveetinstrumentaledes parame`tresde marchea` l’inclusion eta` cinqans.Apre`scinq ans, les auteurs rapportent une corre´lation significative (p=0,02) entre l’e´volution de la vitesse et de la longueur dupasetlede´clindesfonctionscognitivesetexe´cutives,apre`s ajustementpour l’aˆge,lesexe etleniveaud’e´ducation[37].
Utilisantunacce´le´rome`tretriaxial(Dynaport1),fixe´ autour de la taille du patient a` l’aide d’une ceinture e´lastique et enregistrantles acce´le´rationsdans les axesante´ro-poste´rieur, me´dio-late´raletrostro-caudal,unee´quipeamontre´ lafiabilite´ etlareproductibilite´ desparame`tresdemarcheobtenuslorsde deuxaller-retoursurunparcoursde18mdelongdanscorridor rectiligne.Enfin,lesperformancesobtenuesparlesvolontaires aˆge´sparticipantontmontre´ unecorre´lationavecleschutesetle statutfonctionnel[5]dessujets.Danscecontexte,notree´quipe a souhaite´ analyser les parame`tres de marche a` l’aide d’un acce´le´rome`tre triaxialportable leLocome´trix1auseind’une population de sujets aˆge´s sains, de sujets MCI et de sujets atteintsdeMA.Lessujetsdestroisgroupesdevaientmarcher aumilieud’uncorridordroitetsansobstaclede40mdelong, lors d’une taˆche simple (marche) et d’une taˆche double (marchertoutencomptanta` l’envers).Danslesdeuxtests,le
745 746 747 748 749 750 751 752 753 754 755 756 757 758 759 760 761 762 763 764 765 766 767 768 769 770 771 772 773 774 775 776 777 778 779 780 781 782 783 784 785 786 787 788 789 790 791 792 793 794 795 796 797 798 799 800 801 802 803 804 805 806 807 808 809 810 811 812 Tableau3
Contributiondesparame`tresspatiotemporelsdelamarche.
Auteuretre´fe´rencesbibliographiques Observations
BridenbaughetKressig,Gerontology,2011 Me´thodeinstrumentalepluspre´cisequelestestscliniques Wangetal.,JNeuralTransm,2009 Lacomposanteattentionnelledelamarcheaugmenteavecl’aˆge
Vergheseetal.,JGerontolABiolSciMedSci,2009 Vitesseetvariabilite´ delamarchesontdeuxindicateursdurisquedechutes Hausdorffetal.,ArchPhysMedRehabil,2001 Uneaugmentationdelalongueurdupasaucoursd’uncycledepasdouble
lerisquedechutes
Maki,JAmGeriatrSoc,1997 Lavariabilite´ delamarcheestunindicateurdelapeurdetomberetpasun indicateurdurisquedechutes
Beauchetetal.,JAGS,2008 Dubostetal.,HumMovSci,2006
Lapertinencedel’e´tudedelavitesse,delalongueurdupasainsiquelavariabilite´ delamarcheenconditiondedoubletaˆcheenrelationaveclerisquedechutes Allalietal.,DementGeriatrCognDisord,2008 L’importancedesfonctionsexe´cutivesenrelationdelavariabilite´ delamarche
Sheridanetal.,JAGS,2003 L’importancedelacapacite´ a` diviserl’attentionenrelationaveclavariabilite´ delamarche Holtzeretal.,Neuropsychology,2007 Importancedesfonctionscognitivesenrelationaveclavariabilite´ delavitessedelamarche Allalietal.,MovDisord,2010 ProfildemarcheparticulierchezlessujetsatteintsdeMAoude´mencefronto-temporale Vergheseetal.,JNeurolNeurosurgPsychiatry,2007 Leschangementsduprofildemarchepourraientaidera` pre´direl’e´volutioncognitive
dessujetsMCI
Bautmansetal.,GaitPosture,2011 Fiabilite´ entrelesre´sultatsobtenusavecleDynaport1etleGaitRite1aucours dedeuxparcoursdemarchede18metenrelationavecleschutesetlestatut fonctionnelchezlapersonneaˆge´e
Gillainetal.,AnnPhysRehabilMed,2009 Unacce´le´rome`trepermetdesoulignerlesprofilsdemarchespe´cifiquesselonlestatut cognitifchezlapersonneaˆge´e
S.Gillain,J.Petermans/AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx 10
Locome´trix1e´taitcapabledediffe´rentierlestroispopulations a` partirdeleur profildemarchelie´ au statutcognitif[11].
L’e´tudeinstrumentalise´edelamarchesembleutilecarelle permetd’identifieruneouplusieursvariablesspatiotemporelles augmentantlerisquedechutesetainsiaidera` discriminerles patients avec troubles cognitifs en fonctionde leur profil de marcheetainsiidentifierlespersonnesa` risquedede´velopper unede´mence.
Cesme´thodes instrumentalesd’e´tudedesparame`tresdela marchemontrent quel’aˆge n’estpasleseule´le´mentpouvant expliquer la variabilite´ de la marche. En effet, les troubles cognitifs,ante´ce´dentsdechutesainsiquevitesseetconditions de marche demande´es (simple ou double taˆche) sont des facteursessentielsayantunimpactsurlamarchedelapersonne aˆge´eet peuventaidera` estimerlerisquedechutes etpre´dire l’e´volution cognitive. Ainsi, en prenant en compte les parame`tresdelamarcheilconvientdepre´ciserlesconditions ne´cessairesa` l’e´valuationdelamarche,lescaracte´ristiquesde lapopulation(nonseulementl’aˆgemaise´galementante´ce´dents de chutes, traitements, comorbidite´s, de´ficits sensoriels, troubles neurologiques...), vitesse de marche demande´e, technique utilise´.Dans ce contexte,lesre´sultats d’une e´tude re´alise´ea` l’aided’unetechniquespe´cifiqueetserapportanta` unepopulationde´termine´enepeuvent s’extrapolera` d’autres situations. Dans ce contexte, les e´quipes e´tudiant la marche rencontrentdesdifficulte´sdansunepopulationge´riatrique,tout d’abordaveclaconceptiondel’e´tudeetensuitepourtrouverun e´quilibre(oupas)entrelane´cessite´ desoulignerdesre´sultatsa` forte puissance statistique et l’inte´reˆt de montrer cetimpact dansunepopulation« plusre´aliste».
2.3.3. Initiationdelamarche
Plus re´cemment, plusieurs e´quipes ont tente´, a` l’aide de diffe´rentes techniques,d’e´tudier le moment spe´cifique d’IM. Eneffet,cemomentsembleparticulie`rementdangereuxchezla personneaˆge´eayantunrisquee´leve´ de chutes.L’IM estune transition volontaire entre un e´tat statique stable (phase de support) et une posture continuellement instable durant la marchequi ne´cessitedes ajustementsposturauxanticipateurs pour glisser le centre de masse vers le coˆte´ d’appui afin de pouvoirlever la jambe[32]. Comme souligne´ a` l’aidede la TEMP ou PET-scan [21] et la stimulation magne´tique transcranienne re´pe´titive (rTMS), l’IM ne´cessite l’activation de l’AMS mais e´galement des noyaux gris centraux qui semblente´galementimplique´s,comme rapporte´ chezlesujet parkinsonien[16,43].
L’IM est souvent analyse´e a` l’aide d’une plateforme de force. Au cours des dernie`res anne´es, plusieurs e´quipes ont e´tudie´ l’IM dans une population ge´ne´rale aˆge´e[22], chezla personneaˆge´eayantpeurdetomber[33],chezlapersonneaˆge´e avecante´ce´dentsdechutes[23]ainsiquechezdespatientsavec maladie de Parkinson [28] et MA [44]. L’IM montre des modifications spe´cifiques lie´es a` la population e´tudie´e. Des e´tudescomple´mentairesseraientpertinentespourconfirmeret affinercesobservations,bienquel’IMsoitl’objetd’ungrand inte´reˆtscientifique.
2.4. Discussionetconclusion
Plusieurse´tudesmontrentlapertinencedel’e´valuationdela marche chez la personne aˆge´e. Les nouvelles techniques d’imagerieetd’analysesinstrumentalespermettentd’objectiver lelienentrel’anatomiedesstructurescentrales,leurme´tabolisme et les parame`tres spatiotemporels de la marche. La marche sembleeˆtre unindicateur«devieillissementre´ussi »pouvant pre´dire leschangementscognitifsetfonctionnels. Malheureu-sement etmalgre´ les informations essentielles recueillies,ces techniquesrestentconfine´esauniveauexpe´rimentaletsontpeu utilise´esenpratiqueclinique.Lavitesse,lalongueurdupasetla variabilite´ delamarchesemblentdesindicateursimportantsdela qualite´ demarche.Deplus,l’e´tudedelamarcheenconditionde doubletaˆchepourraitfournirdese´le´mentssurlerisquedechutes etlare´servecognitiveattribue´epourl’organisationdelamarche. Ainsi, il semble pertinent de proce´der a` une e´valuation syste´matique de la marche en simple et double taˆche ainsi qu’un suivichez la personneaˆge´e. Enfin,l’IM repre´sente un e´le´mentcrucialpourde´terminerlase´curite´ delapersonneaˆge´e, c’est pourquoi l’e´tude de ce moment pourrait identifier les me´canismessous-jacentsa` l’e´quilibredynamiqueetlamarche afind’essayerdelesame´liorer.
Selonnous,lestestscliniquesdelamarcherestentessentiels commelavitessedemarchesur10mle«TimedUpandGo test ». Le Short Physical Performance Battery Test qui comprendle test«Sit-to-stand», lestestdeBergouTinetti, reste le meilleur moyen d’e´tudier de fac¸on rapide et utile l’e´quilibredusujetaˆge´.Encequiconcerneladoubletaˆche,le « stop walking when talking » test semble un pre´dicteur importantdurisquedechuteschezlesujetaˆge´[19].Eneffet,la comparaisondelamarcheensimpleetdoubletaˆcheavecune taˆchedeparole,estunoutilpre´dictifdurisquedechuteavec unesensibilite´ assezbassede40%maisunespe´cificite´ de96% [35].Pourlechoixd’uneme´thoded’e´valuationdelamarche, l’importantestdese´lectionneruntestfacilea` reproduiredans lesmeˆmesconditionsetbienmaitrise´ parl’examinateur.Enfin, un test de force de pre´hension ou vigorime`tre de Martin, pourraienteˆtredebonsindicateursdemassemusculairepour mesurer lestatutfonctionnelpre´sent eta` venirdusujetaˆge´.
A` l’avenir, l’utilisation de ces nouvelles techniques et l’ame´lioration des indicateurs des syste`mes centraux et pe´riphe´riques pourrait ame´liorer l’identification du sujet a` risque de chutes afin de leur proposer un suivi multidisci-plinaire. Ces travaux permettront de mettre en place des protocoles de re´e´ducation spe´cifique, de la marche et de la fonctioncognitive, adapte´sausujetaˆge´ fragile.
De´claration d’inte´reˆts
Les auteurs n’ont pas transmis de de´claration de conflits d’inte´reˆts.
References
[1] AllaliG,AssalF,KressigRW,DubostV,HerrmannFR,BeauchetO.Impact ofimpairedexecutivefunctionongaitstability.DementGeriatrCognDisord 2008;8626:364–9. 813 814 815 816 817 818 819 820 821 822 823 824 825 826 827 828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843 844 845 846 847 848 849 850 851 852 853 854 855 856 857 858 859 860 861 862 863 864 865 866 867 868 868 869 870 871 872 873 874 875 876 877 878 879 880 881 882 883 884 885 886 887 888 889 890 891 892 893 894 895 896 897 898 899 900 901 902 903 904 905 906 907 908 909 910 911 912 913 914 915 916 917 918 919 920 S.Gillain,J.Petermans/AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx 11
[2]
Q3 AllaliG,DuboisB,AssalF,LallartE,deSouzaLC,BertouxM,etal. Frontotemporaldementia:pathologyofgait?MovDisord2010;731–7.
[3]BakkerM,deLangeFP,StevensJA,ToniI,BloemBR.Motorimageryof gait:aquantitativeapproach.ExpBrainRes2007;179:497–504.
[4]Bakker M, Verstappen CC, Bloem BR, Toni I. Recent advances in functionalneuroimagingofgait.JNeuralTransm2007;114:1323–31.
[5]BautmansI,JansenB,VanKeymolenB,MetsT.Reliabilityandclinical correlatesof3D-accelerometrybasedgaitanalysisoutcomesaccordingto ageandfall-risk.GaitPosture2011;366–72.
[6]BeauchetO,AnnweilerC,AllaliG,BerrutG,HerrmannFR,DubostV. Recurrentfallsanddualtask-relateddecreaseinwalkingspeed:istherea relationship?JAGS2008;56:1265–9.
[7]BeauchetO,AnnweilerC,AssalF,BridenbaughS,HermannFR,Kressig RW,etal.ImaginedTimedUp&Gotest:anewtooltoassesshigher-level gaitandbalancedisordersinolderadults?JNeurolSci2010;294:102–6.
[8]BridenbaughSA,KressigRW.Laboratoryreview:theroleofgaitanalysis inseniors’mobilityandfallprevention.Gerontology2011;57:256–64.
[9]DeshpandeN,PatlaAE.Visual-vestibularinteractionduringgoaldirected locomotion: effects of aging and blurring vision. Exp Brain Res 2007;176:43–53.
[10]DubostV,KressigRW,GonthierR,HermannFR,AminianK,NajafiB,etal. Relationshipbetweendual-taskrelatedchangesinstridevelocityandstride timevariabilityinhealthyolderadults.HumMovSci2006;25:372–82.
[11]GillainS,WarzeeE,LekeuF,WojtasikV,MaquetD,CroisierJL,etal. The value of instrumental gait analysis in elderly healthy, MCI or Alzheimer’sdiseasesubjectsona comparisonwithotherclinicaltests used in single and dual-task conditions. Ann Phys Rehabil Med 2009;52:453–74.
[12]Guerini F, Frisoni G, Marre` A, Turco R, Bellelli G, Trabucchi M. Subcorticalvascularlesionspredictfallsat12monthsinelderlypatients discharged from rehabilitation ward. Arch Phys Med Rehabil 2008;89:1522–7.
[13]HausdorffJM,RiosDA,EdelbergHK.Gaitvariabilityandfallsriskin community-livingolderadults:a1-yearprospectivestudy.ArchPhysMed Rehabil2001;82:1050–6.
[14]Henry-FeugeasMC,OnenF,Schouman-ClaeysE.Classifyinglate-onset dementiawithMRI:isarterioscleroticbraindegenerationthemostcommon causeofAlzheimer’ssyndrome?ClinIntervAging2008;3:189–99.
[15]HoltzerR,FriedmanR,LiptonRB,KatzM,XueX,VergheseJ.The relationship between specific cognitive functions and falls in aging. Neuropsychology2007;540–8.
[16]JacobsJV,LouJS,KraakevikJA,HorakFB.Thesupplementarymotor area contributesto thetiming of theanticipatory posturaladjustment duringstepinitiationinparticipantswithandwithoutParkinson’sdisease. Neuroscience2009;164(2):877–85.
[17]JahnK,Deutschla¨nderA,StephanT,StruppM,WiesmannM,BrandtT. Brainactivationpatternsduringimagingstanceetlocomotionin func-tionalmagneticresonanceimaging.Neuroimage2004;22:1722–31.
[18]LaFouge`reC,ZwergalA,RomingerA,Fo¨rsterS,FeslG,DieterichM, etal.Realversusimaginedlocomotion:a[18F]-FDGPET-fMRI compar-aison.Neuroimage2010;50:1589–98.
[19]Lundin-OlssonL,NybergL,GustafsonY.‘‘Stopwalkingwhentalking’’ asapredictoroffallsinelderlypeople.Lancet1997;349:617.
[20]MakiBE.Gaitchangesinolderadults:predictorsoffallsorindicatorsof fear.JAmGeriatrSoc1997;45:313–20.
[21]MalouinF,RichardsCL,JacksonPL,DumasF,DoyonJ.Brainactivations during motorimagery oflocomotors-relatedtasks:a PETstudy.Hum BrainMapp2003;19:47–62.
[22]MartinK,BlizzardL,GarryM,ThomsonR,McGinleyJ,SrikanthV.Gait initiationinolderpeople–Timetofirstlateralmovementmaybethe measureofchoice.GaitPosture2011;374–8.
[23]Mbourou GA, Lajoie Y, Teasdale N. Step length variability at gait initiationinelderlyfallersandnon-fallers,andyoungadults.Gerontology 2003;49:21–6.
[24]OnenF,Henry-FeugeasMC,BaronG,DeMarcoG,Godon-HardyS, Peretti I, etal.Leukoaraiosisand mobilitydecline: a highresolution
magneticresonanceimagingstudyinolderpeoplewithmildcognitive impairment.NeurosciLett2004;355:185–8.
[25] OnenF,Henry-FeugeasMC,RoyC,BaronG,RavaudP.Mobilitydecline ofunknoworigininmildcognitiveimpairment:a MRI-basedclinical studyofthepathogenesis.BrainRes2008;1222:79–85.
[26] PersonnierP,KubickiA,LarocheD,PapaxanthisC.Temporalfeaturesof imaginedlocomotioninnormalaging.NeurosciLett2010;476:146–9.
[27] PughKG,LipsitzLA.Themicrovascularfrontalsubcorticalsyndromesof aging.NeurobiolAging2002;23:421–31.
[28] Roemmich RT,NoceraJR,VallabhajosulaS, AmanoS,Naugle KM, Stegemo¨llerEL,etal.Spatiotemporalvariabilityduringgaitinitiationin Parkinson’sdisease.GaitPosture2012;36:340–3.
[29] RosanoC,BrachJ,LongstrethJrWT,NewmanAB.Quantitative mea-suresofgaitcharacteristicsindicateprevalenceofunderlyingsubclinical structuralbrainabnormalitiesinhighfunctioningolderadults. Neuroe-pidemiology2006;26:52–60.
[30] RosanoC,BrachJ,StudenskiS,LongstrethJrWT,NewmanAB.Gait variabilityisassociatedwithsubclinicalbrainvascularabnormalitiesin high-functioningolderadults.Neuroepidemiology2007;29:193–200.
[31] SheridanPL,SolomontJ,KowallN,HausdorffJM.Influenceofexecutive functiononlocomotorfunction:dividedattentionincreasesgaitvariability inAlzheimer’sdisease.JAGS2003;51:1633–7.
[32] TateuchiH,IchihashiN,ShinyaM,OdaS.Anticipatorypostural adjust-mentsduringlateralstepmotioninpatientwithhiposteoarthritis.JAppl Biomech2011;27:32–9.
[33] UemuraK,YamadaM,NagaiK,TanakaB,MoriS,IchihashiN.Fearof falling is associated with prolonged anticipatory postural adjustment during gaitinitiation under dual-task conditionsin older adults.Gait Posture2012;35:282–6.
[34] VergheseJ,AmbroseAF,LiptonRB,WangC.Neurologicalgait abnor-malitiesandriskoffallsinolderadults.JNeurol2010;257:392–8.
[35] VergheseJ,BuschkeH,ViolaL,KatzM,HallC,KuslanskyG,etal. Validityofdividedattentiontaskinpredictingfallsinolderindividiuals:a preliminarystudy.JAGS2002;50:1572–6.
[36] VergheseJ,HoltzerR,LiptonRB,WangC.Quantitativegaitmarkersand incident fall risk in older adults. J Gerontol A Biol Sci Med Sci 2009;8:896–901.
[37] VergheseJ,WangC,LiptonRB,HoltzerR,XueX.Quantitativegait dysfunctionandriskofcognitivedeclineanddementia.JNeurol Neu-rosurgPsychiatry2007;929–35.
[38] VergheseJ,RobbinsM,HoltzerR,ZimmermanM,WangC,XueX,etal. Gait dysfunction in mild cognitive impairment syndromes. JAGS 2008;56:1244–51.
[39] VidoniED,ThomasGP,HoneaRA,LoskutovaN,BurnsJM.Evidenceof alteredcorticomotorsystemconnectivityinearly-stagealzheimer’s dis-ease.JNeurolPhysTher2012;36:8–16.
[40] WagnerJ,StephanT,KallaR,Bru¨ckmannH,StruppM,BrandtT,etal. Mindthebend:cerebralactivationassociatedwith mentalimagery of walkingalongacurvedpad.ExpBrainRes2008;191:247–55.
[41] WangJ,WaiY,WengY,NgK,HuangYZ,YingL,etal.FunctionalMRI. intheassessmentofcorticalactivationduringgaitrelatedimaginarytasks. JNeuralTransm2009;116:1087–92.
[42] Warzee E, Elbouz L, Seidel L, Petermans J. Evaluation of gait by 115 inpatientsin geriatric department of CHU Lie`ge. AnnGerontol 2010;3:1–9.
[43] Wichmann T, Delong MR. Deep-brain stimulation for basal ganglia disorders.BasalGanglia2011;1:65–77.
[44] WittwerJE, AndrewsPT,Webster KE,Menz HB.Timing variability during gaitinitiation is increasedin peoplewith Alzheimer’s disease comparedtocontrols.DementGeriatrCognDisord2008;26:215–25.
[45] ZimmermanME,LiptonRB,PanJW,HetheringtonHP,VergheseJ. MRI-and MRS- derived hippocampal correlates of quantitative locomotor functioninolderadults.BrainRes2009;1291:73–81.
[46] ZwergalA,LinnJ,XiongG,BrandtT,StruppM,JahnK.Agingofhuman supraspinallocomotor andposturalcontrolin fMRI.NeurobiolAging 2012;33:1073–84. 921 922 923 924 925 926 927 928 929 930 931 932 933 934 935 936 937 938 939 940 941 942 943 944 945 946 947 948 949 950 951 952 953 954 955 956 957 958 959 960 961 962 963 964 965 966 967 968 969 970 971 972 973 974 975 976 977 978 979 980 981 982 983 984 985 986 987 987 988 989 990 991 992 993 994 995 996 997 998 999 1000 1001 1002 1003 1004 1005 1006 1007 1008 1009 1010 1011 1012 1013 1014 1015 1016 1017 1018 1019 1020 1021 1022 1023 1024 1025 1026 1027 1028 1029 1030 1031 1032 1033 1034 1035 1036 1037 1038 1039 1040 1041 1042 1043 1044 1045 1046 1047 1048 1049 1050 1051 1052 1053 1053 S.Gillain,J.Petermans/AnnalsofPhysicalandRehabilitationMedicinexxx(2013)xxx–xxx
