The walking speed-dependency of gait variability in bilateral vestibulopathy and its association with clinical tests of vestibular function

Understanding balance and gait deficits in vestibulopathy may help improve clinical care and our knowledge of the vestibular contributions to balance. Here, we examined walking speed effects on gait variability in healthy adults and in adults with bilateral vestibulopathy (BVP). Forty-four people with BVP, 12 healthy young adults and 12 healthy older adults walked at 0.4 m/s to 1.6 m/s in 0.2 m/s increments on a dual belt, instrumented treadmill. Using motion capture and kinematic data, the means and coefficients of variation for step length, time, width and double support time were calculated. The BVP group also completed a video head impulse test and examinations of ocular and cervical vestibular evoked myogenic potentials and dynamic visual acuity. Walking speed significantly affected all gait parameters. Step length variability at slower speeds and step width variability at faster speeds were the most distinguishing parameters between the healthy participants and people with BVP, and among people with BVP with different locomotor capacities. Step width variability, specifically, indicated an apparent persistent importance of vestibular function at increasing speeds. Gait variability was not associated with the clinical vestibular tests. Our results indicate that gait variability at multiple walking speeds has potential as an assessment tool for vestibular interventions.

[1]  L L SLOAN,et al.  New test charts for the measurement of visual acuity at far and near distances. , 1959, American journal of ophthalmology.

[2]  I L Bailey,et al.  New Design Principles for Visual Acuity Letter Charts* , 1976, American journal of optometry and physiological optics.

[3]  T. Brandt,et al.  You are better off running than walking with acute vestibulopathy , 1999, The Lancet.

[4]  R. Fitzpatrick,et al.  Effects of galvanic vestibular stimulation during human walking , 1999, The Journal of physiology.

[5]  Thomas Brandt,et al.  Differential effects of vestibular stimulation on walking and running , 2000, Neuroreport.

[6]  A. Kuo,et al.  Active control of lateral balance in human walking. , 2000, Journal of biomechanics.

[7]  D. Sternad,et al.  Local dynamic stability versus kinematic variability of continuous overground and treadmill walking. , 2001, Journal of biomechanical engineering.

[8]  Thomas Brandt,et al.  Visually induced gait deviations during different locomotion speeds , 2001, Experimental Brain Research.

[9]  T. M. Owings,et al.  Measuring step kinematic variability on an instrumented treadmill: how many steps are enough? , 2003, Journal of biomechanics.

[10]  J. Donelan,et al.  Mechanical and metabolic requirements for active lateral stabilization in human walking. , 2004, Journal of biomechanics.

[11]  Kenton R Kaufman,et al.  Spatiotemporal gait deviations in a virtual reality environment. , 2006, Gait & posture.

[12]  K. Brantberg,et al.  Preserved vestibular evoked myogenic potentials (VEMP) in some patients with walking-induced oscillopsia due to bilateral vestibulopathy. , 2007, Journal of vestibular research : equilibrium & orientation.

[13]  Jesse C. Dean,et al.  The Effect of Lateral Stabilization on Walking in Young and Old Adults , 2007, IEEE Transactions on Biomedical Engineering.

[14]  J S Higginson,et al.  Two simple methods for determining gait events during treadmill and overground walking using kinematic data. , 2008, Gait & posture.

[15]  S. Iwasaki,et al.  Novel subtype of idiopathic bilateral vestibulopathy: bilateral absence of vestibular evoked myogenic potentials in the presence of normal caloric responses , 2009, Journal of Neurology.

[16]  John H Hollman,et al.  Number of strides required for reliable measurements of pace, rhythm and variability parameters of gait during normal and dual task walking in older individuals. , 2010, Gait & posture.

[17]  Mukul Mukherjee,et al.  The effect of virtual reality on gait variability. , 2010, Nonlinear dynamics, psychology, and life sciences.

[18]  Nicholas Stergiou,et al.  Wearing a safety harness during treadmill walking influences lower extremity kinematics mainly through changes in ankle regularity and local stability , 2012, Journal of NeuroEngineering and Rehabilitation.

[19]  J. Colebatch,et al.  Vestibular neuritis has selective effects on air- and bone-conducted cervical and ocular vestibular evoked myogenic potentials , 2011, Clinical Neurophysiology.

[20]  Jonathan B Dingwell,et al.  Comparison of walking overground and in a Computer Assisted Rehabilitation Environment (CAREN) in individuals with and without transtibial amputation , 2012, Journal of NeuroEngineering and Rehabilitation.

[21]  Ronald C Petersen,et al.  Normative spatiotemporal gait parameters in older adults. , 2011, Gait & posture.

[22]  A. Kuo,et al.  Energetic cost of walking with increased step variability. , 2012, Gait & posture.

[23]  T. Brandt,et al.  Differential effects of absent visual feedback control on gait variability during different locomotion speeds , 2012, Experimental Brain Research.

[24]  Nils Guinand,et al.  Visual acuity while walking and oscillopsia severity in healthy subjects and patients with unilateral and bilateral vestibular function loss. , 2012, Archives of otolaryngology--head & neck surgery.

[25]  Nils Guinand,et al.  Quality of Life of Patients with Bilateral Vestibulopathy , 2012, The Annals of otology, rhinology, and laryngology.

[26]  T. Brandt,et al.  Locomotion speed determines gait variability in cerebellar ataxia and vestibular failure , 2012, Movement disorders : official journal of the Movement Disorder Society.

[27]  Romeo Chua,et al.  Muscle-specific modulation of vestibular reflexes with increased locomotor velocity and cadence. , 2013, Journal of neurophysiology.

[28]  P. Beek,et al.  Assessing the stability of human locomotion: a review of current measures , 2013, Journal of The Royal Society Interface.

[29]  G. Jacobson,et al.  Effects of Age on the Tuning of the cVEMP and oVEMP , 2013, Ear and hearing.

[30]  Maria Cristina Bisi,et al.  Gait variability and stability measures: Minimum number of strides and within-session reliability , 2014, Comput. Biol. Medicine.

[31]  N König,et al.  Is gait variability reliable? An assessment of spatio-temporal parameters of gait variability during continuous overground walking. , 2014, Gait & posture.

[32]  Gaspar Epro,et al.  Deficient recovery response and adaptive feedback potential in dynamic gait stability in unilateral peripheral vestibular disorder patients , 2014, Physiological reports.

[33]  M M van der Krogt,et al.  Effects of adding a virtual reality environment to different modes of treadmill walking. , 2014, Gait & posture.

[34]  H. Kingma,et al.  Bilateral Vestibular Hypofunction: Challenges in Establishing the Diagnosis in Adults , 2015, ORL.

[35]  H. Kingma,et al.  Vestibular assistance systems: promises and challenges , 2016, Journal of Neurology.

[36]  Emmanuel C. Alozie,et al.  Promises and Challenges , 2015 .

[37]  Hamish G. MacDougall,et al.  The Video Head Impulse Test (vHIT) of Semicircular Canal Function – Age-Dependent Normative Values of VOR Gain in Healthy Subjects , 2015, Front. Neurol..

[38]  J. Guinan,et al.  Increasing the Stimulation Rate Reduces cVEMP Testing Time by More Than Half With No Significant Difference in Threshold , 2016, Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology.

[39]  Thomas Brandt,et al.  Noisy vestibular stimulation improves dynamic walking stability in bilateral vestibulopathy , 2016, Neurology.

[40]  T. Brandt,et al.  Clinical and neurophysiological risk factors for falls in patients with bilateral vestibulopathy , 2016, Journal of Neurology.

[41]  W. Zijlstra,et al.  Preliminary observations of the acute effects of vestibular nerve stimulation on stride length and time in two patients with bilateral vestibular hypofunction , 2016 .

[42]  Hans H. Jung,et al.  Ocular vestibular evoked myogenic potentials as a test for myasthenia gravis , 2016, Neurology.

[43]  K. Jahn,et al.  Falls and fear of falling in vertigo and balance disorders: A controlled cross-sectional study. , 2016, Journal of vestibular research : equilibrium & orientation.

[44]  M. Strupp,et al.  Comparison of the Bedside Head-Impulse Test with the Video Head-Impulse Test in a Clinical Practice Setting: A Prospective Study of 500 Outpatients , 2016, Front. Neurol..

[45]  Richard F. Lewis Vestibular implants studied in animal models: clinical and scientific implications. , 2016, Journal of neurophysiology.

[46]  H. Kingma,et al.  Bilateral Vestibular Hypofunction: Insights in Etiologies, Clinical Subtypes, and Diagnostics , 2016, Front. Neurol..

[47]  F. Horak,et al.  Velocity dependence of vestibular information for postural control on tilting surfaces. , 2016, Journal of neurophysiology.

[48]  Roman Schniepp,et al.  Noisy galvanic vestibular stimulation: an emerging treatment option for bilateral vestibulopathy , 2017, Journal of Neurology.

[49]  A. Sprenger,et al.  Postural Control in Bilateral Vestibular Failure: Its Relation to Visual, Proprioceptive, Vestibular, and Cognitive Input , 2017, Front. Neurol..

[50]  Stefan Glasauer,et al.  Quantification of Head Movement Predictability and Implications for Suppression of Vestibular Input during Locomotion , 2017, Front. Comput. Neurosci..

[51]  H. Kingma,et al.  The vestibular implant: A probe in orbit around the human balance system. , 2017, Journal of vestibular research : equilibrium & orientation.

[52]  M. Srinivasan,et al.  Walking with wider steps changes foot placement control, increases kinematic variability and does not improve linear stability , 2017, Royal Society Open Science.

[53]  H. Kingma,et al.  Bilateral vestibulopathy: Diagnostic criteria Consensus document of the Classification Committee of the Bárány Society , 2017, Journal of vestibular research : equilibrium & orientation.

[54]  Mark Vlutters,et al.  Rapid limb‐specific modulation of vestibular contributions to ankle muscle activity during locomotion , 2017, The Journal of physiology.

[55]  H. Kingma,et al.  The Video Head Impulse Test and the Influence of Daily Use of Spectacles to Correct a Refractive Error , 2018, Front. Neurol..

[56]  Wim Saeys,et al.  Do spatiotemporal parameters and gait variability differ across the lifespan of healthy adults? A systematic review. , 2018, Gait & posture.

[57]  H. Kingma,et al.  Is faster always better? The walking speed-dependency of gait variability in bilateral vestibulopathy , 2018 .

[58]  Christopher McCrum,et al.  Stimulating balance: recent advances in vestibular stimulation for balance and gait. , 2019, Journal of neurophysiology.

[59]  J. Golding,et al.  Motion sickness diagnostic criteria: Consensus Document of the Classification Committee of the Bárány Society , 2021, Journal of vestibular research : equilibrium & orientation.