Characterization of Compensatory Stepping in People With Multiple Sclerosis

Published:November 18, 2015DOI:



      To characterize postural responses to forward and backward external perturbations in people with multiple sclerosis (PwMS), and to relate performance to commonly used clinical outcomes.


      Cross-sectional study. Postural responses were tested during large stepping and smaller feet-in-place perturbations in forward and backward directions.


      University research laboratory.


      PwMS (n=54) and age-matched controls (n=21) (N=75).


      Not applicable.

      Main Outcome Measures

      Center of mass displacement and step latency after external perturbations.


      PwMS exhibited larger center of mass displacements and step latencies than control participants in response to stepping perturbations (P=.003 and P=.028, respectively). Stepping deficits were more pronounced during backward stepping and were significantly correlated to increased severity on clinical measures (European Database for Multiple Sclerosis disability score and Timed 25-Foot Walk).


      Compensatory stepping is impaired in PwMS and correlates with clinical disability. Measurement of backward compensatory stepping may be more effective at identifying postural dysfunction in PwMS than forward compensatory steps. Prolonged step latencies, large anticipatory postural adjustments, and multiple compensatory steps are especially altered in PwMS, suggesting possible targets for neurorehabilitation.


      List of abbreviations:

      APA (anticipatory postural adjustment), COM (center of mass), COP (center of pressure), MS (multiple sclerosis), PwMS (people with multiple sclerosis), T25FW (Timed 25-Foot Walk)
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        • Peterson E.W.
        • Ben Ari E.
        • Asano M.
        • Finlayson M.L.
        Fall attributions among middle-aged and older adults with multiple sclerosis.
        Arch Phys Med Rehabil. 2013; 94: 890-895
        • Cowan J.M.
        • Rothwell J.C.
        • Dick J.P.
        • Thompson P.D.
        • Day B.L.
        • Marsden C.D.
        Abnormalities in central motor pathway conduction in multiple sclerosis.
        Lancet. 1984; 2: 304-307
        • Cameron M.H.
        • Horak F.B.
        • Herndon R.R.
        • Bourdette D.
        Imbalance in multiple sclerosis: a result of slowed spinal somatosensory conduction.
        Somatosens Mot Res. 2008; 25: 113-122
        • Huisinga J.M.
        • St George R.J.
        • Spain R.
        • Overs S.
        • Horak F.B.
        Postural response latencies are related to balance control during standing and walking in patients with multiple sclerosis.
        Arch Phys Med Rehabil. 2014; 95: 1390-1397
        • Jacobs J.V.
        • Horak F.B.
        Cortical control of postural responses.
        J Neural Transm. 2007; 114: 1339-1348
        • Maki B.E.
        • McIlroy W.E.
        Control of rapid limb movements for balance recovery: age-related changes and implications for fall prevention.
        Age Ageing. 2006; 35: ii12-ii18
        • de Kam D.
        • Nonnekes J.
        • Oude Nijhuis L.B.
        • Geurts A.C.
        • Bloem B.R.
        • Weerdesteyn V.
        Dopaminergic medication does not improve stepping responses following backward and forward balance perturbations in patients with Parkinson's disease.
        J Neurol. 2014; 261: 2330-2337
        • King L.A.
        • Horak F.B.
        Lateral stepping for postural correction in Parkinson's disease.
        Arch Phys Med Rehabil. 2008; 89: 492-499
        • King L.A.
        • St George R.J.
        • Carlson-Kuhta P.
        • Nutt J.G.
        • Horak F.B.
        Preparation for compensatory forward stepping in Parkinson's disease.
        Arch Phys Med Rehabil. 2010; 91: 1332-1338
        • Nonnekes J.
        • Scotti A.
        • Oude Nijhuis L.B.
        • et al.
        Are postural responses to backward and forward perturbations processed by different neural circuits?.
        Neuroscience. 2013; 245: 109-120
        • Lu Z.
        • Zhang B.
        • Qiu W.
        • et al.
        Comparative brain stem lesions on MRI of acute disseminated encephalomyelitis, neuromyelitis optica, and multiple sclerosis.
        PLoS One. 2011; 6: e22766
        • Bowen J.
        • Gibbons L.
        • Gianas A.
        • Kraft G.H.
        Self-administered Expanded Disability Status Scale with functional system scores correlates well with a physician-administered test.
        Mult Scler. 2001; 7: 201-206
        • Fischer J.S.
        • Rudick R.A.
        • Cutter G.R.
        • Reingold S.C.
        The Multiple Sclerosis Functional Composite Measure (MSFC): an integrated approach to MS clinical outcome assessment. National MS Society Clinical Outcomes Assessment Task Force.
        Mult Scler. 1999; 5: 244-250
        • Dimitrova D.
        • Horak F.B.
        • Nutt J.G.
        Postural muscle responses to multidirectional translations in patients with Parkinson's disease.
        J Neurophysiol. 2004; 91: 489-501
        • Kamen G.
        • Gabriel D.
        Essentials of electromyography.
        Human Kinetics, Champaign2010
        • Lee P.Y.
        • Gadareh K.
        • Naushahi M.J.
        • Gresty M.
        • Bronstein A.M.
        Protective stepping response in Parkinsonian patients and the effect of vibrotactile feedback.
        Mov Disord. 2013; 28: 482-489
        • Welch T.D.
        • Ting L.H.
        Mechanisms of motor adaptation in reactive balance control.
        PLoS One. 2014; 9: e96440
        • Jacobs J.V.
        • Nutt J.G.
        • Carlson-Kuhta P.
        • Stephens M.
        • Horak F.B.
        Knee trembling during freezing of gait represents multiple anticipatory postural adjustments.
        Exp Neurol. 2009; 215: 334-341
        • Horak F.B.
        • Diener H.C.
        • Nashner L.M.
        Influence of central set on human postural responses.
        J Neurophysiol. 1989; 62: 841-853
        • Cohen J.
        Statistical power analysis for the behavioral sciences.
        in: 2nd ed. Lawrence Erlbaum Associates, New Jersey1988
        • Cabib C.
        • Llufriu S.
        • Casanova-Molla J.
        • Saiz A.
        • Valls-Sole J.
        Defective sensorimotor integration in preparation for reaction time tasks in patients with multiple sclerosis.
        J Neurophysiol. 2015; 113: 1462-1469
        • Van Emmerik R.E.
        • Remelius J.G.
        • Johnson M.B.
        • Chung L.H.
        • Kent-Braun J.A.
        Postural control in women with multiple sclerosis: effects of task, vision and symptomatic fatigue.
        Gait Posture. 2010; 32: 608-614
        • Enoka R.
        Neuromechanics of Human Movement.
        5th ed. Human Kinetics, Champaign2015
        • Mansfield A.
        • Peters A.L.
        • Liu B.A.
        • Maki B.E.
        Effect of a perturbation-based balance training program on compensatory stepping and grasping reactions in older adults: a randomized controlled trial.
        Phys Ther. 2010; 90: 476-491
        • Jobges M.
        • Heuschkel G.
        • Pretzel C.
        • Illhardt C.
        • Renner C.
        • Hummelsheim H.
        Repetitive training of compensatory steps: a therapeutic approach for postural instability in Parkinson's disease.
        J Neurol Neurosurg Psychiatry. 2004; 75: 1682-1687
        • Mansfield A.
        • Wong J.S.
        • Bryce J.
        • Knorr S.
        • Patterson K.K.
        Does perturbation-based balance training prevent falls? Systematic review and meta-analysis of preliminary randomized controlled trials.
        Phys Ther. 2015; 95: 700-709
        • McIlroy W.E.
        • Maki B.E.
        Do anticipatory postural adjustments precede compensatory stepping reactions evoked by perturbation?.
        Neurosci Lett. 1993; 164: 199-202