Multiple sclerosis (MS) is a progressive neurologic disease that causes debilitating motor, cognitive, and sensory impairments [
Dual-task walking assessments that require individuals to perform multiple tasks simultaneously often result in a decrement in performance of one or both tasks in persons with MS [
Recently, backward walking has been recognized as a sensitive clinical measure of mobility and fall risk in the elderly [
Therefore, our study compared spatiotemporal gait parameters of forward walking and backward walking in single- and dual-task conditions in persons with MS and age- and sex-matched healthy controls. Additionally, we compared the relationships between forward walking and backward walking spatiotemporal measures to measures of cognitive function, retrospective fall reports, and balance. We hypothesized that persons with MS would demonstrate greater deficits in backward walking single-task and dual-task walking performance compared to forward single-task and dual-task walking performance than healthy controls. Additionally, we hypothesized that backward walking would exhibit stronger correlations to cognitive function, retrospective fall reports, and balance in comparison to forward walking in persons with MS. Identification of relationships between single- and dual-task backward walking to cognitive function, falls, and balance would aid in the development of practical, cost-efficient, and clinically feasible tools that may sensitively detect critical underlying processes that are commonly impacted by MS and related to fall risk (i.e., motor and cognitive function), thereby improving upon the current forward walking methods.
Eighteen individuals with relapsing-remitting MS were recruited from a parent study exploring training effects of video-game exercise. Fourteen age- and sex-matched healthy controls were recruited through fliers, posts on the university research database, and by word-of-mouth. Inclusion criteria for individuals with MS included 30-59 years of age, a diagnosis of relapsing-remitting MS, and an Expanded Disability Status Scale (EDSS) score between 1.0 and 5.5. Age- and sex-matched healthy controls were included if they were within 2 years of the participant with MS and of the same sex. Both MS and healthy control participants were excluded if they reported an orthopedic, neurologic, or cognitive impairment that would limit participation in study assessments. All measures were collected in a single session. The Institutional Review Board at The Ohio State University approved this study. All participants signed consent forms before participating.
Spatiotemporal measures of gait were acquired with the GAITRite electronic walkway (V3.9, MAP/CIR Inc.; Franklin, NJ). The GAITRite is reliable and valid for use in individuals with MS (Givon, 2009). Individuals ambulated across the GAITRite at a self-selected, comfortable pace for three trials per each of the four conditions: (1) forward, (2) forward + cognitive task (serial 3 subtraction starting at 97), (3) backward, and (4) backward + cognitive task (serial 3 subtraction starting at 95). We
The number of past falls over six months was assessed by self-report. All participants were asked, “Have you fallen within the last six months? If yes, how many times?” Falls were operationally defined at the time of the retrospective fall data collection as an “unexpected event that resulted in an unintentional landing on the ground or a lower surface” [
Participants received a key with nine numbers each corresponding to a symbol and were asked to determine the number belonging with a series of symbols using this key. The score is the number of correct answers in 90 seconds. The SDMT is a validated and reliable test in MS to analyze attention and information processing speed [
The WLG is measure of verbal fluency and semantic retrieval, reliable, and validated for use in persons with MS [
A priori power analysis based on Wajda et al. indicates sample size of 8 per group needed for 80% power to detect a change in performance between groups [
Eighteen individuals with relapsing-remitting MS and fourteen age- and sex-matched healthy controls enrolled in this study. There was no significant difference in age (MS: 45.5(8.2); HC: 44.0 (8.8);
Figure
Walking velocity (a), stride length (b), and double support time (c) as a function of walking direction and group.
Main effects and interactions for spatiotemporal measures of gait.
Main effects | Velocity (m/s) | Stride length (cm) | Double support time (s) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Mean (SD) | Mean (SD) | Mean (SD) | ||||||||||
Group | ||||||||||||
MS | 0.50 (0.33) | 3.5 | 0.071 | 0.12 | ||||||||
Control | 0.37 (0.12) | |||||||||||
Direction | ||||||||||||
Forward | ||||||||||||
Backward | ||||||||||||
Condition | ||||||||||||
Single-task | 109.43 (27.23) | 2.1 | 0.160 | 0.07 | ||||||||
Dual-task | 107.54 (25.88) | |||||||||||
Group x direction | ||||||||||||
MS forward | 1.21 (0.33) | 3.6 | 0.068 | 0.11 | 122.49 (17.61) | 1.3 | 0.263 | 0.04 | 0.38 (0.12) | 3.9 | 0.059 | 0.12 |
MS backward | 0.72 (0.30) | 86.76 (20.82) | 0.63 (0.42) | |||||||||
Control forward | 1.37 (0.30) | 133.09 (14.00) | 0.34 (0.10) | |||||||||
Control backward | 0.98 (0.23) | 100.82 (12.54) | 0.40 (0.12) | |||||||||
Group x condition | ||||||||||||
MS single-task | 1.04 (0.40) | 0.87 | 0.359 | 0.03 | 106.09 (25.77) | 0.31 | 0.584 | 0.01 | 0.45 (0.27) | 1.7 | 0.199 | 0.06 |
MS dual-task | 0.91 (0.39) | 103.62 (27.06) | 0.55 (0.38) | |||||||||
Control single-task | 1.21 (0.29) | 117.64 (19.19) | 0.34 (0.08) | |||||||||
Control dual-task | 1.14 (0.37) | 116.28 (22.89) | 0.39 (0.14) | |||||||||
Direction x condition | ||||||||||||
Forward single-task | 1.33 (0.29) | 1.2 | 0.311 | 0.06 | 128.11 (15.33) | 0.94 | 0.341 | 0.03 | ||||
Forward dual-task | 1.23 (0.35) | 126.15 (18.47) | ||||||||||
Backward single-task | 0.90 (0.30) | 94.18 (17.59) | ||||||||||
Backward dual-task | 0.78 (0.28) | 91.80 (20.32) |
Bolded values represent significant effects.
There were significant differences in backward walking velocity between groups for both single- (
There was a significant difference in forward walking stride length between groups for the dual-task condition (
There was no difference in double support time between individuals with MS and healthy controls during single-task forward (
Better performance on the SDMT was significantly associated with longer stride length in both the forward walking condition (
Falls at six months were not associated with forward walking or forward dual-task performance; however, falls at six months were significantly associated with backward dual-task velocity (
Better performance on the BBS was significantly associated with increased forward walking velocity (
An exploratory analysis was performed to examine differences in performance between individuals with
Subanalysis to examine differences in walking performance among individuals with
This study compared spatiotemporal measures in forward walking and backward walking in single- and dual-task conditions between persons with MS and healthy controls. Further, we compared the relationships between forward and backward walking spatiotemporal measures to cognitive function (i.e., processing speed and verbal fluency), retrospective fall reports at six months, and balance. The critical finding of the current study was that backward walking measures, particularly in the dual-task condition, revealed greater decrements in walking performance compared to forward walking that better differentiate persons with MS from healthy controls. Additionally, backward walking measures were more strongly related to retrospective falls at six months whereas no forward walking measures were related. Though not adequately powered to comprehensively examine differences in walking performance among individuals with MS with higher (
Backward walking velocity revealed significant differences between groups for both single-task (
Persons with MS demonstrated significant differences in double support time when shifting from single- to dual-task conditions in both forward (
Given the high demand of cognitive resources during dual-task walking and backward walking [
Backward walking measures were more strongly related to retrospective falls at six months whereas no forward walking measures were related. These findings reflect the sensitivity of backward walking and its potential to supplement the current clinical dual-task and fall risk assessments. Additionally, these findings agree with previous studies in the elderly [
We examined the relationship between forward and backward walking performance under single- and dual-task performance and balance, using the BBS. Interestingly, BBS demonstrated stronger relationships with forward walking measures than with backward walking measures. This is perhaps because the BBS comprises primarily measures of static and anticipatory balance control but does not require adaptive or reactive control. Future studies should explore whether balance tests incorporating adaptive or reactive control are more strongly related to measures of backward walking and backward dual-task walking.
An exploratory analysis indicated that individuals with lower disability (
Our findings are the first to elucidate that persons with MS exhibit greater deficits in backward walking single-task and dual-task walking performance compared to forward single-task and dual-task walking performance when compared to age- and gender-matched healthy controls. Additionally, these findings are the first to demonstrate the potential for backward walking dual-task assessment to sensitively detect fall risk in persons with MS. Importantly, the backward walking dual-task measures described in this work are clinically feasible, easy to administer, and could be immediately scalable for clinical use as a sensitive clinical outcome tool to use in addition to current methods to detect underlying impairments in key domains relevant to MS (i.e., cognitive function, fall risk, balance). However, a larger sample size with comprehensive multidomain cognitive testing, prospective falls monitoring, and dynamic balance assessment is needed to further elucidate clinical utility and validity for backward walking dual-task assessment in MS.
Limitations of this study include its small sample size of 32 individuals (eighteen individuals with relapsing-remitting MS and fourteen age-matched healthy controls), which may not generalize to ambulatory persons with progressive subtype. However, these limited data satisfy prior gaps in knowledge regarding the relationship between backward walking dual-task assessment and falls, as well as successfully age- and sex-matching healthy controls while observing differences between forward and backward walking dual-task measures. This study relied on retrospectively collected data on falls at six months. Several studies in MS highlight the underestimation of falls with retrospective recall [
This study was limited to two discrete measures of cognition, namely, the SDMT to measure information processing speed and the WLG to measure verbal fluency and semantic memory, and therefore did not evaluate other domains of cognition that are known to be impacted by MS (i.e., attention, visuospatial memory, executive function) and have been related to motor measures and fall frequency in MS [
This study demonstrated that differences in MS and healthy controls are more pronounced during backward walking compared to forward walking. Importantly, we incorporated age- and sex-matched controls to better understand these differences. Future work with a larger sample size is needed to validate the clinical utility of backward walking and dual-task assessments and mitigate the limited sensitivity of the current dual-task assessments that primarily rely upon forward walking. Based on our data, larger scale studies could leverage identification of definitive variables that are easily measurable in the clinic setting (i.e., velocity) along with respective dual-task walking assessment cutoff scores for clinical use. Additionally, studies aimed at developing a comprehensive understanding of potential mechanisms (i.e., brain pathology and specific cognitive correlates) underlying the impairments observed in dual-task assessment and more specifically, backward walking dual-task assessment, would further enhance targeted rehabilitation interventions. Our findings suggest that backward walking and dual-task assessment may better differentiate persons with MS and healthy controls, providing additional tools to supplement the current standard of forward walking assessment and warrants further research.
Readers may contact the authors for access to the deidentified dataset.
The OSF Registration is dated 7/13/19 and is available for review at:
The authors declare that there are no conflicts of interest regarding publication of this article.
This project was supported by Award Number Grant 8TL1TR000091-05 to Dr. Fritz from the National Center for Advancing Translational Sciences. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Advancing Translational Sciences of the National Institutes of Health. In addition, Dr. Kloos received funding for this project from an Ohio State University Center for Clinical and Translational Sciences (CCTS) 2011 Collaborative Pilot Grant.
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