Objective biomarkers of balance and gait for Parkinson's disease using body‐worn sensors

Balance and gait impairments characterize the progression of Parkinson's disease (PD), predict the risk of falling, and are important contributors to reduced quality of life. Advances in technology of small, body‐worn, inertial sensors have made it possible to develop quick, objective measures of balance and gait impairments in the clinic for research trials and clinical practice. Objective balance and gait metrics may eventually provide useful biomarkers for PD. In fact, objective balance and gait measures are already being used as surrogate endpoints for demonstrating clinical efficacy of new treatments, in place of counting falls from diaries, using stop‐watch measures of gait speed, or clinical balance rating scales. This review summarizes the types of objective measures available from body‐worn sensors. The metrics are organized based on the neural control system for mobility affected by PD: postural stability in stance, postural responses, gait initiation, gait (temporal‐spatial lower and upper body coordination and dynamic equilibrium), postural transitions, and freezing of gait. However, the explosion of metrics derived by wearable sensors during prescribed balance and gait tasks, which are abnormal in individuals with PD, do not yet qualify as behavioral biomarkers, because many balance and gait impairments observed in PD are not specific to the disease, nor have they been related to specific pathophysiologic biomarkers. In the future, the most useful balance and gait biomarkers for PD will be those that are sensitive and specific for early PD and are related to the underlying disease process. © 2013 International Parkinson and Movement Disorder Society

[1]  F. Horak,et al.  Milestones in gait, balance, and falling , 2011, Movement disorders : official journal of the Movement Disorder Society.

[2]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[3]  L. Chiari,et al.  Anticipatory postural adjustments prior to step initiation are hypometric in untreated Parkinson’s disease: an accelerometer‐based approach , 2009, European journal of neurology.

[4]  F. Horak,et al.  Preparation for compensatory forward stepping in Parkinson's disease. , 2010, Archives of physical medicine and rehabilitation.

[5]  Laura Rocchi,et al.  Effects of deep brain stimulation in the subthalamic nucleus or globus pallidus internus on step initiation in Parkinson disease , 2012 .

[6]  R. Peterka,et al.  A new interpretation of spontaneous sway measures based on a simple model of human postural control. , 2005, Journal of neurophysiology.

[7]  Itshak Melzer,et al.  A retrospective analysis of balance control parameters in elderly fallers and non-fallers. , 2010, Clinical biomechanics.

[8]  Catherine Dehollain,et al.  Gait assessment in Parkinson's disease: toward an ambulatory system for long-term monitoring , 2004, IEEE Transactions on Biomedical Engineering.

[9]  Jeffrey M. Hausdorff,et al.  Gait variability and fall risk in community-living older adults: a 1-year prospective study. , 2001, Archives of physical medicine and rehabilitation.

[10]  Jeffrey M. Hausdorff,et al.  Time series analysis of leg movements during freezing of gait in Parkinson's disease: akinesia, rhyme or reason? , 2003 .

[11]  T. Mergner,et al.  Multisensory control of human upright stance , 2006, Experimental Brain Research.

[12]  Jeffrey M. Hausdorff,et al.  Increased gait unsteadiness in community-dwelling elderly fallers. , 1997, Archives of physical medicine and rehabilitation.

[13]  L. Rocchi,et al.  Dependence of anticipatory postural adjustments for step initiation on task movement features: a study based on dynamometric and accelerometric data , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[14]  Patricia Carlson-Kuhta,et al.  The effects of subthalamic and pallidal deep brain stimulation on postural responses in patients with Parkinson disease. , 2012, Journal of Neurosurgery.

[15]  Y Brenière,et al.  Are dynamic phenomena prior to stepping essential to walking? , 1987, Journal of motor behavior.

[16]  James A. Norris,et al.  Ability of static and statistical mechanics posturographic measures to distinguish between age and fall risk. , 2005, Journal of biomechanics.

[17]  R. Peterka,et al.  Role of somatosensory and vestibular cues in attenuating visually induced human postural sway , 2004, Experimental Brain Research.

[18]  Lynn Rochester,et al.  Understanding the impact of deep brain stimulation on ambulatory activity in advanced Parkinson’s disease , 2012, Journal of Neurology.

[19]  M S Redfern,et al.  A comparison of accelerometry and center of pressure measures during computerized dynamic posturography: a measure of balance. , 2011, Gait & posture.

[20]  F. Horak,et al.  Effects of deep brain stimulation and levodopa on postural sway in Parkinson's disease , 2002, Journal of neurology, neurosurgery, and psychiatry.

[21]  Laurie A. King,et al.  Do Clinical Scales of Balance Reflect Turning Abnormalities in People With Parkinson's Disease? , 2012, Journal of neurologic physical therapy : JNPT.

[22]  M. Hallett,et al.  Freezing of gait: moving forward on a mysterious clinical phenomenon , 2011, The Lancet Neurology.

[23]  M. Morris,et al.  Concurrent related validity of the GAITRite walkway system for quantification of the spatial and temporal parameters of gait. , 2003, Gait & posture.

[24]  V. Srikanth,et al.  Gait, gait variability and the risk of multiple incident falls in older people: a population-based study. , 2011, Age and ageing.

[25]  F. Horak,et al.  An alternative clinical postural stability test for patients with Parkinson’s disease , 2006, Journal of Neurology.

[26]  John R. Rebula,et al.  Measurement of foot placement and its variability with inertial sensors. , 2013, Gait & posture.

[27]  H. Hampel,et al.  Biomarker candidates of neurodegeneration in Parkinson’s disease for the evaluation of disease-modifying therapeutics , 2011, Journal of Neural Transmission.

[28]  Fay B. Horak,et al.  Quantifying freezing of gait in Parkinson's disease during the instrumented timed up and go test , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[29]  Andrea Merlo,et al.  Postural stability and history of falls in cognitively able older adults: the Canton Ticino study. , 2012, Gait & posture.

[30]  M. Do,et al.  Control of gait initiation. , 1991, Journal of motor behavior.

[31]  Lynn Rochester,et al.  Gait variability in Parkinson’s disease: an indicator of non-dopaminergic contributors to gait dysfunction? , 2011, Journal of Neurology.

[32]  L. Chiari,et al.  Quantification of Motor Impairment in Parkinson's Disease Using an Instrumented Timed Up and Go Test , 2013, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[33]  Emer P. Doheny,et al.  Evaluation of Falls Risk in Community-Dwelling Older Adults Using Body-Worn Sensors , 2012, Gerontology.

[34]  Kamiar Aminian,et al.  The instrumented timed up and go test: potential outcome measure for disease modifying therapies in Parkinson's disease , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[35]  R. Collins,et al.  Gait variability in Parkinson’s disease: influence of walking speed and dopaminergic treatment , 2011, Neurological research.

[36]  Jeffrey M. Hausdorff,et al.  Gait alterations in healthy carriers of the LRRK2 G2019S mutation , 2011, Annals of neurology.

[37]  Jeffrey M. Hausdorff,et al.  Gait variability and basal ganglia disorders: Stride‐to‐stride variations of gait cycle timing in parkinson's disease and Huntington's disease , 1998, Movement disorders : official journal of the Movement Disorder Society.

[38]  Luca Palmerini,et al.  Feature Selection for Accelerometer-Based Posture Analysis in Parkinson's Disease , 2011, IEEE Transactions on Information Technology in Biomedicine.

[39]  Brett W Fling,et al.  Asymmetric pedunculopontine network connectivity in parkinsonian patients with freezing of gait. , 2013, Brain : a journal of neurology.

[40]  Martin Wiesmann,et al.  Imaging human supraspinal locomotor centers in brainstem and cerebellum , 2008, NeuroImage.

[41]  M. Mancini,et al.  Impaired Trunk Stability in Individuals at High Risk for Parkinson's Disease , 2012, PloS one.

[42]  M. R. Adame,et al.  TUG Test Instrumentation for Parkinson’s disease patients using Inertial Sensors and Dynamic Time Warping , 2012 .

[43]  L. Reichertz,et al.  Assessing fall risk using wearable sensors: a practical discussion , 2012, Zeitschrift für Gerontologie und Geriatrie.

[44]  R. Iansek,et al.  Gait freezing in Parkinson's disease and the stride length sequence effect interaction. , 2009, Brain : a journal of neurology.

[45]  F. Horak,et al.  Trunk accelerometry reveals postural instability in untreated Parkinson's disease. , 2011, Parkinsonism & related disorders.

[46]  D. DeMets,et al.  Biomarkers and surrogate endpoints: Preferred definitions and conceptual framework , 2001, Clinical pharmacology and therapeutics.

[47]  Martina Mancini,et al.  Framework for understanding balance dysfunction in Parkinson's disease , 2013, Movement disorders : official journal of the Movement Disorder Society.

[48]  Jeffrey M. Hausdorff,et al.  An instrumented timed up and go: the added value of an accelerometer for identifying fall risk in idiopathic fallers , 2011, Physiological measurement.

[49]  F. B. Horak,et al.  Exploring Outcome Measures for Exercise Intervention in People with Parkinson's Disease , 2013, Parkinson's disease.

[50]  Lorenzo Chiari,et al.  ISway: a sensitive, valid and reliable measure of postural control , 2012, Journal of NeuroEngineering and Rehabilitation.

[51]  Jeffrey M. Hausdorff,et al.  Toward Automated, At-Home Assessment of Mobility Among Patients With Parkinson Disease, Using a Body-Worn Accelerometer , 2011, Neurorehabilitation and neural repair.

[52]  Gerard Boyle,et al.  Correlation of accelerometry with clinical balance tests in older fallers and non-fallers. , 2008, Age and ageing.

[53]  Fay B. Horak,et al.  Time-dependent influence of sensorimotor set on automatic responses in perturbed stance , 1999, Experimental Brain Research.

[54]  A. Kuo,et al.  Direction-dependent control of balance during walking and standing. , 2009, Journal of neurophysiology.

[55]  F. Horak,et al.  Step initiation in Parkinson's disease: Influence of levodopa and external sensory triggers , 1997, Movement disorders : official journal of the Movement Disorder Society.

[56]  F. Horak,et al.  The relevance of clinical balance assessment tools to differentiate balance deficits. , 2010, European journal of physical and rehabilitation medicine.

[57]  F. Horak,et al.  Postural sway as a marker of progression in Parkinson's disease: a pilot longitudinal study. , 2012, Gait & posture.

[58]  Rumpa Boonsinsukh,et al.  A Cane Improves Postural Recovery From an Unpracticed Slip During Walking in People With Parkinson Disease , 2012, Physical Therapy.

[59]  Jeffrey M. Hausdorff.  Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking. , 2007, Human movement science.

[60]  Jeffrey M. Hausdorff,et al.  Marked alterations in the gait timing and rhythmicity of patients with de novo Parkinson's disease , 2006, The European journal of neuroscience.

[61]  Jeffrey M. Hausdorff.  Gait dynamics in Parkinson's disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. , 2009, Chaos.

[62]  F. Horak,et al.  Effects of dopamine on postural control in parkinsonian subjects: scaling, set, and tone. , 1996, Journal of neurophysiology.

[63]  W. Ondo,et al.  Ambulatory monitoring of freezing of gait in Parkinson's disease , 2008, Journal of Neuroscience Methods.

[64]  S. Studenski,et al.  Too much or too little step width variability is associated with a fall history in older persons who walk at or near normal gait speed , 2005, Journal of NeuroEngineering and Rehabilitation.

[65]  A. Cappello,et al.  Feature selection of stabilometric parameters based on principal component analysis , 2006, Medical and Biological Engineering and Computing.

[66]  Age and Ageing.  Correlation of accelerometry with clinical balance tests in older fallers and non-fallers , 2009 .

[67]  James McNames,et al.  Mobility Lab to Assess Balance and Gait with Synchronized Body-worn Sensors. , 2011, Journal of bioengineering & biomedical science.

[68]  Terry D Ellis,et al.  Capturing Ambulatory Activity Decline in Parkinson's Disease , 2012, Journal of neurologic physical therapy : JNPT.

[69]  I. Melzer,et al.  Postural stability in the elderly: a comparison between fallers and non-fallers. , 2004, Age and ageing.

[70]  Jeffrey M. Hausdorff,et al.  Can an accelerometer enhance the utility of the Timed Up & Go Test when evaluating patients with Parkinson's disease? , 2010, Medical engineering & physics.

[71]  J. Summers,et al.  The pathogenesis of gait hypokinesia in Parkinson's disease. , 1994, Brain : a journal of neurology.

[72]  F. Horak,et al.  Postural inflexibility in parkinsonian subjects , 1992, Journal of the Neurological Sciences.

[73]  Toshiyo Tamura,et al.  Detection of anticipatory postural adjustments prior to gait initiation using inertial wearable sensors , 2011, Journal of NeuroEngineering and Rehabilitation.