Original article
A temporal analysis of bilateral gait coordination in people with multiple sclerosis

https://doi.org/10.1016/j.msard.2020.102445Get rights and content

Highlights

  • PwMS walk with slower gait speeds, independent of the selected walking speed.

  • Regardless of the walking speed, PwMS exhibit poor bilateral coordination.

  • PCI provides a valuable assessment tool for evaluating gait performance of PwMS.

Abstract

Background

: Gait performance often dictates an individual's ability to navigate the dynamic environments of everyday living. With each stride, the lower extremities move through phases of stance, swing, and double support. Coordinating these motions with high accuracy and consistency is imperative to constraining the center of mass within the base of support, thereby maintaining balance. Gait abnormalities accompany neurodegeneration, impeding stride to stride cohesion and increasing the likelihood of a fall. This study sought to identify the temporal actions underlying bilateral coordination in people with multiple sclerosis (PwMS) and furthermore, how bilateral coordination is affected by gait speed augmentation in these individuals.

Methods

: The Phase Coordination Index (PCI), a temporal analysis of left-right step pattern generations throughout the gait cycle was used to quantify bilateral coordination in twenty-nine neurotypical (21 females and 8 males) and twenty-seven PwMS (20 females and 7 males). PCI was acquired with inertial monitoring units while performing two-minute over ground gait trials while walking at a self-selected pace and at a fast pace.

Results

: PwMS displayed significantly worse bilateral coordination compared to neurotypical adults regardless of gait speed. The poorer left-right stepping patterns generated by PwMS were derived from significant decreases in both phase (step) generation accuracy and consistency. In addition to demonstrating poorer bilateral coordination, PwMS walked more slowly than their neurotypical peers during each walking condition.

Conclusion

: PwMS exhibited poorer left-right coordinated stepping patterns during gait compared to neurotypical peers across walking conditions. Beyond the novelty of this examination, this assessment highlights PCI as a potential target for future rehabilitative interventions for PwMS and individualized rehabilitation strategies aimed at improving the health span and overall quality of life for PwMS.

Introduction

Mobility is a reflection of an individual's ability to control their center of mass (CoM) during bipedal locomotion (Cruz-Jimenez, 2017). During bipedal locomotion, the summation of specific spatial and temporal movement parameters creates ambulatory patterns to effectively constrain the CoM within a continually changing base of support. Taken as a whole, these movement parameters describe an individual's gait performance. Gait performance has been deemed a “global health marker” and a putative predictor of survival, declines in cognitive function, falls status, and overall quality of life (Lord et al., 2013). Multiple sclerosis is a disease that results in gait performance deficits in 93.7% of affected individuals (E. W. Peterson et al., 2008). The majority (63%) of people with multiple sclerosis (PwMS) incur a fall within any twelve-month span and 45% of those individuals will develop into recurring fallers (Gianni et al., 2014). Given that there are nearly one million adults living with multiple sclerosis (MS) in the United States (Wallin et al., 2019) substantially more research is necessary to understand the specifics of mobility disability in PwMS.

During ambulation, each leg works independently through successive phases of stance and swing to establish gait patterns. A gait cycle is defined as two steps or the heel strike of one foot to the heel strike of the same foot and is broadly comprised of a stance and a swing phase. Prior work demonstrates that PwMS walk at slower velocities during both self-selected and fast pace gait. Further, PwMS exhibit significantly reduced stride length, increased time in double support, and reduced time spent in swing phase compared to age- and sex-matched neurotypical adults (Comber et al., 2017). In addition to these more traditional spatiotemporal measures of mobility, effective gait requires left-right coordination between bilateral stance and swing phases to effectively constrain the CoM and regulate velocity at the moment of foot placement (i.e. stepping) (Townsend, 1985; Winter and Rogers, 1992). The accuracy and consistency of the steps generated during locomotion may provide insight into how successful an individual is at maintaining their CoM within their dynamic base of support during gait, thereby preventing a fall.

The degree of accuracy and consistency of left-right step coordination can be quantified with the Phase Coordination Index (PCI) (Plotnik et al, 2007). Previous research has demonstrated that neurodegeneration stemming from the aging process or a neurological disease (i.e. Parkinson's disease) are known contributors to reduced bilateral coordination, reflected by a higher PCI value (Plotnik et al., 2008, 2009; Swanson and Fling, 2018; Williams et al., 2013). Furthermore, gait coordination measured via PCI has significant condition effects across slow, normal, and fast walking, as well as during dual-task walking in people with Parkinson's disease (Plotnik et al., 2009). To date, the majority of studies have evaluated PCI in advancing age and neurologically diseased populations, with an emphasis on Parkinson's disease or implemented this analysis with a gait mat (Gianfrancesco et al., 2011); however, gait coordination with this novel and comprehensive metric has only been reported in one additional study with portable instrumentation in PwMS. This investigation (Plotnik et al., 2020) showed that PCI became worse with increasing disease severity. However, they did not directly compare these results with a matched neurotypical population and only examined one gait speed.

The impact of neurodegeneration stemming from MS on bilateral coordination in gait during over-ground walking remains unclear, this study provides novel insights into the mechanisms underlying bilateral coordination deficits during gait in PwMS. The current manuscript compares bilateral coordination in PwMS and neurotypical, age-matched adults while walking at both a self-selected and a fast pace. Reflecting literature in other neurologic populations with mobility impairment, we hypothesized that PwMS would demonstrate poorer bilateral coordination compared to their neurotypical counterparts regardless of gait speed. In addition, similar to previous studies investigating neurotypical individuals (Plotnik et al., 2013), we hypothesized that augmenting gait speed would coincide with reduced bilateral coordination deficits (i.e. lower PCI values) regardless of the presence of neurodegeneration.

Section snippets

Participants

Twenty-nine neurotypical adults were sex- and age-matched on an individual participant basis to twenty-seven adults enrolled in the study with a confirmed diagnosis of relapse-remitting MS (Table 1). Participants were excluded if they were unable to safely walk unassisted (an Expanded Disability Systems Scale < 4.0; PwMS median [3.5] and range [0 - 4.0]) or if they had a joint replacement, musculoskeletal or vestibular disorder, or any additional neurological impairment outside of their MS

Phase coordination index

A significant main effect of group was found (F1,54 = 6.056, p = 0.017), demonstrating that across both walking conditions, PwMS displayed significantly higher PCI values (Tables 2) compared to their neurotypical counterparts, indicative of poorer phase coordination during walking in PwMS. No main effect of condition was observed for PCI (F1,54 = 0.913, p = 0.343). Additionally, PwMS generated bilateral coordination phases with significantly lower accuracy (F1,54 = 5.816, p = 0.019) and

Discussion

To our knowledge, this is one of the first studies to utilize wireless inertial sensors to investigate bilateral coordination in PwMS and to describe how bilateral coordination during gait is affected by speed augmentation. Regardless of walking at a self-selected or fast pace, PwMS exhibited poorer gait coordination and walked significantly slower with shorter strides than their neurotypical counterparts. These outcomes derived from portable instrumentation indicate that mobility deficits in

Conclusions

PwMS exhibit poorer accuracy and consistency in left-right stepping compared to neurotypical adults irrespective of the augmentation of speed. Further, poorer bilateral coordinated stepping was directly related with reduced gait speed in PwMS. Together, the concepts established within the current manuscript prompts the need to explore the underlying neural mechanisms of bilateral coordination and address the neural functional performance of these mechanisms.

Funding

This work was supported by the Dana Foundation and the National Multiple Sclerosis Society [PP-1708-29077] that facilitated the research presented in this manuscript.

CRediT authorship contribution statement

Sutton B. Richmond: Conceptualization, Methodology, Software, Formal analysis, Investigation, Data curation, Writing - original draft, Visualization, Project administration. Clayton W. Swanson: Methodology, Software, Investigation, Writing - review & editing. Daniel S. Peterson: Conceptualization, Writing - review & editing, Supervision. Brett W. Fling: Conceptualization, Writing - review & editing, Supervision, Funding acquisition.

Declaration of Competing Interest

None of the authors have any conflicts of interest to declare.

Acknowledgements

This work was supported by the Dana Foundation and the National Multiple Sclerosis Society [PP-1708-29077] that facilitated the research presented in this manuscript. The authors would like to thank, Moriah R. Hanson, Patrick G. Monaghan, Arianna D. Odom, and Tyler T. Whittier for their assistance in the acquisition of data for this project.

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