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      Can Gait Signatures Provide Quantitative Measures for Aiding Clinical Decision-Making? A Systematic Meta-Analysis of Gait Variability Behavior in Patients with Parkinson's Disease

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          Abstract

          A disturbed, inconsistent walking pattern is a common feature of patients with Parkinson's disease (PwPD). Such extreme variability in both temporal and spatial parameters of gait has been associated with unstable walking and an elevated prevalence of falls. However, despite their ability to discretise healthy from pathological function, normative variability values for key gait parameters are still missing. Furthermore, an understanding of each parameter's response to pathology, as well as the inter-parameter relationships, has received little attention. The aim of this systematic literature review and meta-analysis was therefore to define threshold levels for pathological gait variability as well as to investigate whether all gait parameters are equally perturbed in PwPD. Based on a broader systematic literature search that included 13′195 titles, 34 studies addressed Parkinson's disease, presenting 800 PwPD and 854 healthy subjects. Eight gait parameters were compared, of which six showed increased levels of variability during walking in PwPD. The most commonly reported parameter, coefficient of variation of stride time, revealed an upper threshold of 2.4% to discriminate the two groups. Variability of step width, however, was consistently lower in PwPD compared to healthy subjects, and therefore suggests an explicit sensory motor system control mechanism to prioritize balance during walking. The results provide a clear functional threshold for monitoring treatment efficacy in patients with Parkinson's disease. More importantly, however, quantification of specific functional deficits could well provide a basis for locating the source and extent of the neurological damage, and therefore aid clinical decision-making for individualizing therapies.

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          Most cited references57

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          Temporal structure of motor variability is dynamically regulated and predicts motor learning ability.

          Individual differences in motor learning ability are widely acknowledged, yet little is known about the factors that underlie them. Here we explore whether movement-to-movement variability in motor output, a ubiquitous if often unwanted characteristic of motor performance, predicts motor learning ability. Surprisingly, we found that higher levels of task-relevant motor variability predicted faster learning both across individuals and across tasks in two different paradigms, one relying on reward-based learning to shape specific arm movement trajectories and the other relying on error-based learning to adapt movements in novel physical environments. We proceeded to show that training can reshape the temporal structure of motor variability, aligning it with the trained task to improve learning. These results provide experimental support for the importance of action exploration, a key idea from reinforcement learning theory, showing that motor variability facilitates motor learning in humans and that our nervous systems actively regulate it to improve learning.
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            Gait variability and basal ganglia disorders: stride-to-stride variations of gait cycle timing in Parkinson's disease and Huntington's disease.

            The basal ganglia are thought to play an important role in regulating motor programs involved in gait and in the fluidity and sequencing of movement. We postulated that the ability to maintain a steady gait, with low stride-to-stride variability of gait cycle timing and its subphases, would be diminished with both Parkinson's disease (PD) and Huntington's disease (HD). To test this hypothesis, we obtained quantitative measures of stride-to-stride variability of gait cycle timing in subjects with PD (n = 15), HD (n = 20), and disease-free controls (n = 16). All measures of gait variability were significantly increased in PD and HD. In subjects with PD and HD, gait variability measures were two and three times that observed in control subjects, respectively. The degree of gait variability correlated with disease severity. In contrast, gait speed was significantly lower in PD, but not in HD, and average gait cycle duration and the time spent in many subphases of the gait cycle were similar in control subjects, HD subjects, and PD subjects. These findings are consistent with a differential control of gait variability, speed, and average gait cycle timing that may have implications for understanding the role of the basal ganglia in locomotor control and for quantitatively assessing gait in clinical settings.
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              Assessing the stability of human locomotion: a review of current measures.

              Falling poses a major threat to the steadily growing population of the elderly in modern-day society. A major challenge in the prevention of falls is the identification of individuals who are at risk of falling owing to an unstable gait. At present, several methods are available for estimating gait stability, each with its own advantages and disadvantages. In this paper, we review the currently available measures: the maximum Lyapunov exponent (λS and λL), the maximum Floquet multiplier, variability measures, long-range correlations, extrapolated centre of mass, stabilizing and destabilizing forces, foot placement estimator, gait sensitivity norm and maximum allowable perturbation. We explain what these measures represent and how they are calculated, and we assess their validity, divided up into construct validity, predictive validity in simple models, convergent validity in experimental studies, and predictive validity in observational studies. We conclude that (i) the validity of variability measures and λS is best supported across all levels, (ii) the maximum Floquet multiplier and λL have good construct validity, but negative predictive validity in models, negative convergent validity and (for λL) negative predictive validity in observational studies, (iii) long-range correlations lack construct validity and predictive validity in models and have negative convergent validity, and (iv) measures derived from perturbation experiments have good construct validity, but data are lacking on convergent validity in experimental studies and predictive validity in observational studies. In closing, directions for future research on dynamic gait stability are discussed.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                30 June 2016
                2016
                : 10
                : 319
                Affiliations
                [1] 1Department of Health Sciences and Technology, Institute for Biomechanics, Swiss Federal Institute of Technology in Zurich (ETHZ) Zürich, Switzerland
                [2] 2Department of Neurology, University Hospital Zürich, University of Zürich Zürich, Switzerland
                Author notes

                Edited by: Olivier Darbin, University of South Alabama, USA

                Reviewed by: Annalisa Setti, University College Cork, Ireland; Sue Lord, Newcastle University, UK

                *Correspondence: William R. Taylor taylorb@ 123456ethz.ch
                Article
                10.3389/fnhum.2016.00319
                4927578
                27445759
                6e0cd5de-ba38-457a-a676-5dd1c1621316
                Copyright © 2016 König, Singh, Baumann and Taylor.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 12 April 2016
                : 13 June 2016
                Page count
                Figures: 1, Tables: 1, Equations: 1, References: 67, Pages: 7, Words: 5820
                Categories
                Neuroscience
                Mini Review

                Neurosciences
                gait variability,walking balance,dynamic stability,systematic review,meta-analysis,quality of movement,rhythmicity

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