Archives of Physical Medicine and Rehabilitation journal homepage: www.archives-pmr.org Archives of Physical Medicine and Rehabilitation 2015;96:1098-102
ORIGINAL RESEARCH
Preliminary Investigation of Gait Initiation and Falls in Multiple Sclerosis Douglas A. Wajda, MSc, Yaejin Moon, MSc, Robert W. Motl, PhD, Jacob J. Sosnoff, PhD From the Department of Kinesiology and Community Health, University of Illinois at Urbana-Champaign, Urbana, IL.
Abstract Objective: To examine the relationship between gait initiation, fall history, and physiological fall risk in individuals with multiple sclerosis (MS) during both cognitive distracting and nondistracting conditions. Design: Single time point cross-sectional analysis. Setting: University research laboratory. Participants: Ambulatory individuals (NZ20) with MS ranging in age from 28 to 76 years. Intervention: Not applicable. Main Outcome Measures: Gait initiation time was quantified as the time to toe-off of the first step after an auditory cue. Gait initiation was performed with and without a concurrent cognitive challenge of reciting alternating letters of the alphabet. Additionally, participants underwent a test of fall risk using the Physiological Profile Assessment (PPA) and provided a self-report of the number of falls in the previous 3 months. Results: Gait initiation times ranged from .67 to 1.12 seconds during the single-task condition and .73 to 1.84 seconds during the cognitive challenge condition. PPA scores ranged from .80 to 3.87. Participants reported a median of 0.0 falls (interquartile range, 0.0e2.75) in the previous 3 months. There was a significant correlation between PPA score and gait initiation times only in the cognitive distraction condition (rZ.50). There was also a correlation between cognitive distraction gait initiation times and fall history (rZ.60). Conclusions: The observations provide preliminary evidence that gait initiation during cognitive challenge may represent a target for fall prevention strategies in MS. Archives of Physical Medicine and Rehabilitation 2015;96:1098-102 ª 2015 by the American Congress of Rehabilitation Medicine
Multiple sclerosis (MS) is a chronic disease of the central nervous system affecting approximately 2.2 million individuals worldwide.1 Individuals with MS commonly report decrements in balance2 and gait.3 Perhaps not surprising given these impairments, individuals with MS have a high risk of falling, with more than 50% reporting at least 1 fall over a 3- to 6-month period.4,5 Commonly, these falls occur during dynamic events such as transferring and transitions between positions6; however, most research has focused on the relationship between steady-state gait parameters and/or quiet stance with past or future falls.7 Gait initiationdthat is, taking a step from a quiet stance (eg, standing still)drepresents the complex transition between upright stance and steady-state gait. This process creates an intrinsically unstable condition as the individual shifts toward Supported by the National Multiple Sclerosis Society (grant no. IL Lot NMSS 006), which took no role in experimental design or manuscript preparation. Disclosures: none.
single-leg stance while concurrently generating the necessary momentum to take a step with the swing leg.8 The ability to effectively initiate gait or stepping is imperative for both the maintenance of upright posture and fall avoidance.9 Indeed, recent evidence demonstrates that choice stepping reaction time is significantly correlated to future falls in individuals with MS.10 Previous studies have examined the changes in gait initiation for individuals with MS compared with healthy controls. One such study11 consisting of 12 women with MS and 12 age- and sexmatched controls observed that the MS group had slower center of pressure (COP) movements and reduced COP shifts when initiating gait compared with controls. Similarly, a second study12 using a sample of 13 individuals with MS and matched controls investigated differences in single-step initiation between the groups during both standard and concurrent cognitive challenge conditions. The main observations were that individuals with MS had delayed step onset times compared with controls and that step initiation times increased during cognitive challenge conditions.
0003-9993/15/$36 - see front matter ª 2015 by the American Congress of Rehabilitation Medicine http://dx.doi.org/10.1016/j.apmr.2014.12.011
Gait initiation and falls in multiple sclerosis Individuals with a history of falling have been found to have an altered gait initiation compared with those who do not have a history of falling. For instance, Mbourou et al13 observed that elderly fallers exhibited smaller initial steps and increased initial step length variability compared with both elderly nonfallers and young adults. There is also recent evidence that choice stepping reaction time is impaired in frequent (>2 falls) fallers with MS compared with infrequent (1 fall) fallers.10 However, the choice stepping protocol does not inform whether the relationship with fall risk is associated with deficits in stepping or cognitive processes. The purpose of this pilot investigation was to further examine the relationship between gait initiation, fall history, and physiological fall risk in individuals with MS. Given the association between cognitive-motor interference (CMI) and fall risk in MS,14 gait initiation performance was examined during normal and concurrent cognitive challenge conditions. We hypothesized that gait initiation would be associated with fall history and physiological fall risk in individuals with MS and that this association would be strongest in the cognitive challenge condition.
Methods Participants The cross-sectional study consisted of a convenience sample of 20 individuals with MS who represented a subsample of participants in ongoing walking and balance exercise investigations. All data for the current protocol were collected within a single assessment. To be included, participants had to have a neurologistconfirmed diagnosis of MS and been relapse free for 30 days. Additionally, participants had to be able to stand and walk independently with or without the use of an assistive device.
Procedures The procedures for this investigation were approved by the local institutional review board. On arrival at the testing facility, participants were provided with a verbal explanation of the study procedures and presented with the informed consent document. Participants were given the opportunity to ask questions and then provided written informed consent. Subjects then provided demographic information and completed multiple trials of gait initiation. Additionally, a test of physiological fall risk was also performed. Demographic information including age, sex, assistive device use, MS subtype, and years since diagnosis was self-reported by the participants. The self-administered Kurtzke questionnaire was used to identify self-reported Expanded Disability Status Scale (EDSS) level.15 Self-reported disability level has demonstrated a high correlation (rZ.90) to the neurologist-administered EDSS.15 Fall history was operationalized as the total number of falls in the previous 3 months. Falls in the previous 3 months were reported using a standardized questionnaire that asked whether the participants had fallen, and if so, how many times in the previous
List of abbreviations: CMI COP EDSS MS PPA
cognitive-motor interference center of pressure Expanded Disability Status Scale multiple sclerosis Physiological Profile Assessment
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1099 3 months. This method for recording falls in the previous 3 months has previously been used in individuals with MS.16 Four trials of gait initiation were performed including 2 baseline trials and 2 trials with added cognitive challenge. Cognitive challenge tasks have been used previously during stepping tasks in this population and further highlighted gait initiation alterations.12 Additionally, cognitive challenge during voluntary stepping revealed significant differences between elderly fallers and nonfallers where baseline tests did not.17 In MS, measures of dual tasking have been shown to relate to physiological fall risk when standard spatiotemporal gait parameters did not.14 The kinematic parameters of gait initiation were quantified using a 6.1-m electronic Zeno walkway.a The Zeno walkway uses pressure sensors to calculate COP trajectories as well as the spatial and temporal parameters of gait based on individual footfalls. Participants were instructed to stand in place and then begin walking in response to an auditory cue. During the cognitive challenge condition, the participants simultaneously recited alternating letters of the alphabet (eg, A, C, E) aloud while performing the gait initiation task. Specifically, the participants recited letters during both phases (ie, standing and walking) of the cognitive distraction gait initiation trials. Participants practiced the letter task while seated before performing the cognitive challenge trials. This task has previously been used as a cognitive challenge during walking in MS.18 The main outcome measure for gait initiation was time to toe-off (step initiation time) of the first foot. The auditory signaling device was synced with the gait mat, and the time elapsed from signal presentation until toe-off of the first foot was recorded for each trial. Gait initiation times were averaged across trials within the specific conditions. An examination of physiological fall risk was performed using the short-form Physiological Profile Assessment (PPA).19 The PPA was originally developed for use in older adults and later validated for individuals with MS.20 The PPA consists of 5 tests examining visual contrast sensitivity (Melbourne Edge Test), simple reaction time, lower limb proprioception, isometric knee extensor strength, and standing balance on a compliant surface. The specifics of these tests are described in detail elsewhere.19 All 5 tests are administered with standardized instructions based on published guidelines.19 The results on these assessments are then entered into a database and compared with age-matched norms. Individual z scores are calculated for each subsection of the PPA, and an overall physiological fall risk score is presented as an overall z score, with larger values representing a higher risk.
Statistical analysis All statistical analyses were performed in SPSS version 20.b Descriptive statistics were calculated for all the outcome measures. Normality of the outcome measures was determined using the Shapiro-Wilk test. A repeated-measures analysis of variance was used to determine differences in gait initiation times between baseline and added cognitive challenge conditions. Spearman rank order correlations were performed to determine the relationships between the gait initiation times, fall history, and fall risk scores. Spearman correlations were selected because of the small sample size and nonnormality of the falls history outcome measure. All analyses used 2-sided tests, and P values .05 were considered statistically significant.
Results The ages of the participants ranged from 28 to 76 years (mean SD, 58.610.9y). The sample consisted of 15 women and 5 men.
1100 Sixteen of the individuals had relapse-remitting MS, 2 had secondary progressive MS, 1 had primary progressive MS, and 1 individual did not report MS type. The time since diagnosis ranged from 3 to 41 years (mean SD, 16.59.6y). Eleven of the individuals walked with no assistive devices, while 5 used unilateral support and 4 used bilateral support. The median selfreported EDSS score for the sample was 4.75 (interquartile range, 2.6e6.0), with a minimum of 3.0 and maximum of 7.0. The median number of falls in the previous 3 months was 0.0 (interquartile range, 0.0e2.75) and ranged from 0.0 to 6.0. The sample overall displayed an elevated fall risk, with a mean PPA score SD of 1.21.2. PPA fall risk scores ranged from a minimum of .80 to a maximum of 3.9. Table 1 provides descriptive statistics for the individual tests that comprise the PPA. These fall risk values are consistent with previous observations in MS.14,20 Gait initiation times during the baseline and cognitive challenge conditions took, on average (SD), .87.13 and 1.03.28 seconds, respectively. Results of the analysis of variance showed that gait initiation was significantly delayed during the cognitive challenge condition compared with baseline values (FZ8.9, PZ.008). Figure 1 displays scatterplots for single-task and cognitive challenge gait initiation times as a function of PPA fall risk score and falls in the previous 3 months. Spearman correlation analyses confirmed that PPA score had a positive correlation with cognitive challenge gait initiation time (rZ.50, PZ.03). Further analysis revealed that cognitive challenge gait initiation time was primarily related to deficiencies in the leg strength (rZ .47, PZ.04) and postural sway (rZ.46, PZ.04) components of the PPA. Moreover, a strong positive correlation was observed between cognitive challenge gait initiation time and fall history in the previous 3 months (rZ.60, PZ.01). No significant correlations were observed between single-task gait initiation times and either PPA score or past falls.
Discussion The aim of this pilot study was to investigate the relationship between gait initiation, fall history, and physiological fall risk in individuals with MS. We hypothesized that gait initiation would be related to both the number of falls in the previous 3 months and physiological fall risk, with the strongest relationships occurring during the cognitively challenging condition. Overall, this hypothesis was confirmed, as cognitive challenge gait initiation time was strongly correlated to fall history and physiological fall risk. The novel aspect of this observation is that gait initiation during cognitive distraction conditions but not single-task conditions was related to falls and fall risk in this sample. The observations further highlight the role of CMI in falls in persons with MS. The results add to the understanding of fall risk in MS and highlight that gait initiation during distracting conditions could possibly be a target of future fall prevention interventions. The hypothesis that gait initiation would be associated with physiological fall risk and fall history was based in part on previous research. First, falls are most common during movement transitions, such as standing to walking.6 Additionally, recent evidence demonstrates that choice stepping reaction time is significantly correlated to future falls in individuals with MS.10 The primary difference of the current observation with results from the choice stepping paradigm is that stepping was not confined to a single step toward target areas but was instead the first step to initiate walking. Additionally, the choice stepping task
D.A. Wajda et al Table 1
PPA component test descriptive statistics
Test Visual contrast sensitivity Simple reaction time Proprioception Knee extensor strength Postural sway
Mean SD 0.570.59 0.631.01 1.241.09 0.120.90 0.191.37
Minimum 1.37 2.80 2.94 1.74 2.36
Maximum 1.35 0.55 1.21 1.76 2.02
NOTE. All values are z scores. A negative sign indicates test performance below that of normative data.
did not delineate between stepping in isolation and stepping when engaged in a simultaneous cognitive task. Stepping represents one of the main compensatory strategies for avoiding a fall.9,21 Extending the results of the current study suggests that the effectiveness of the stepping strategy may be diminished in individuals with MS, particularly when cognitively engaged. That is, the individuals in this study who were at the greatest risk of falling took longer to initiate a step during cognitively challenging conditions compared with those at a lesser fall risk. Potentially this delayed stepping response indicates a reduced capacity to successfully implement a stepping strategy to recover from a balance perturbation (eg, trip), especially when distracted. Indeed, individuals in the present study who had the greatest number of falls in the previous 3 months demonstrated slower gait initiation times during cognitive challenge conditions. A caveat to this conclusion is that gait initiation was in response to an auditory cue, and this type of response may be distinct from initiation in response to an external perturbation. Cued gait initiation tasks inherently draw on various fall risk factors such as processing speed (ie, simple reaction time) and postural control. Consequently, it is possible that the association between gait initiation and falls is driven by declines in reaction time, declines in postural control, or both. There are copious amounts of evidence of deficits in processing speed22 and postural control2 in individuals with MS compared with controls. These factors are also subcomponents of the utilized fall risk assessment tool; thus the relationship between the gait initiation and fall risk is logical. To further investigate this explanation we analyzed correlations between stepping times and results from the individual tests of the PPA. We determined that higher cognitive challenge stepping times were indeed correlated to greater deficits in postural sway on a compliant surface, as well as to knee extensor strength. The lack of correlation between PPA simple reaction time and cognitive challenge gait initiation times challenges the contribution of cognitive processing speed in mediating the relationship between gait initiation and fall risk. Gait initiation performance during the current investigation was comparable to that in previous studies of individuals with MS who had mild to mild-moderate disability (median EDSS, 2.5; range, 0e4.5).12 Despite the current sample having an overall greater disability, we observed a similar slowing of gait initiation during cognitive challenge conditions compared with baseline. These alterations suggest the influence of interactions between cognitive performance and motor performance, typically termed cognitive-motor interference. During the cognitive challenge condition, both the motor and cognitive task compete for available attentional resources, which can lead to a decline in performance.23 CMI has been suggested to be related to falls in individuals with MS and other populations,14,24 and the current results further bolster this possibility. Given the adverse www.archives-pmr.org
Gait initiation and falls in multiple sclerosis
1101
Fig 1 Scatterplots of analyzed relationships. (A) Single-task gait initiation time versus PPA score. (B) Cognitive challenge gait initiation time versus PPA score. (C) Single-task gait time initiation versus past falls. (D) Cognitive challenge gait initiation time versus past falls.
consequences of CMI, it is logical that it become a focus of rehabilitation. Although there is some evidence that CMI can be impacted with targeted training in various clinical populations,25,26 there is no evidence that it can be altered in MS. The association between CMI and past falls and fall risk in individuals with MS further highlights the importance of including cognition and CMI in fall prevention rehabilitation programs.27 The results of this investigation suggest that gait initiation, especially during cognitive challenge, may represent a future target for falls prevention protocols. Although there is growing evidence that fall prevention is possible in individuals with MS,16,28 no interventions have focused on gait initiation in isolation or with a cognitive challenge. A small number of interventions have successfully focused on gait initiation in other clinical populations. For instance, tai chi training in older adults has been shown to improve gait initiation.29 Additionally, taskspecific stepping response training resulted in a decrease of fall risk in a sample of middle-aged and older women.30
limitations. First, the results come from a small convenience sample. Second, the study did not include a matched control group to consider the extension of these results beyond the current sample. Finally, retrospective recall of falls was used in a population in which memory deficits are common, necessitating caution when interpreting results.22 However, it is important to note that one of the best predictors of future falls and a commonly used clinical query is retrospectively reported falls.31
Conclusions Overall, the results of this pilot study serve to add to the understanding of falls and fall risk in individuals with MS. Additionally, the results suggest the pertinence of using dynamic tasks such as gait initiation as well as concurrent cognitive challenges for the analysis of fall risk in MS. Further study of gait initiation and its role in fall prevention strategies is warranted.
Study limitations
Suppliers
Despite the finding of correlations between gait initiation, fall history, and PPA fall risk scores, the current study has multiple
a. Zeno walkway; ProtoKinetics Inc. b. SPSS version 20; IBM Corp.
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Keywords Accidental falls; Rehabilitation
Gait;
Locomotion;
Multiple
sclerosis;
Corresponding author Douglas A. Wajda, MSc, University of Illinois at UrbanaChampaign, Department of Kinesiology and Community Health, 301 Freer Hall, 906 S Goodwin Ave, Urbana, IL 61801. E-mail address: [email protected].
References 1. Kalb R, Reitman N. Overview of multiple sclerosis. New York: National Multiple Sclerosis Society; 2012. 2. Frzovic D, Morris ME, Vowels L. Clinical tests of standing balance: performance of persons with multiple sclerosis. Arch Phys Med Rehabil 2000;81:215-21. 3. LaRocca NG. Impact of walking impairment in multiple sclerosis: perspectives of patients and care partners. Patient 2011;4:189-201. 4. Matsuda PN, Shumway-Cook A, Bamer AM, Johnson SL, Amtmann D, Kraft GH. Falls in multiple sclerosis. PM R 2011;3:624-32. 5. Nilsaga˚rd Y, Gunn H, Freeman J, et al. Falls in people with MSdan individual data meta-analysis from studies from Australia, Sweden, United Kingdom and the United States. Mult Scler. 2014 Jun 16. [Epub ahead of print] 6. Matsuda PN, Shumway-Cook A, Ciol MA, Bombardier CH, Kartin DA. Understanding falls in multiple sclerosis: association of mobility status, concerns about falling, and accumulated impairments. Phys Ther 2012;92:407-15. 7. Gianni C, Prosperini L, Jonsdottir J, Cattaneo D. A systematic review of factors associated with accidental falls in people with multiple sclerosis: a meta-analytic approach. Clin Rehabil 2014;28:704-16. 8. Polcyn AF, Lipsitz LA, Kerrigan DC, Collins JJ. Age-related changes in the initiation of gait: degradation of central mechanisms for momentum generation. Arch Phys Med Rehabil 1998;79:1582-9. 9. Lord SR, Fitzpatrick RC. Choice stepping reaction time: a composite measure of falls risk in older people. J Gerontol A Biol Sci Med Sci 2001;56:M627-32. 10. Hoang PD, Cameron MH, Gandevia SC, Lord SR. Neuropsychological, balance, and mobility risk factors for falls in people with multiple sclerosis: a prospective cohort study. Arch Phys Med Rehabil 2014;95: 480-6. 11. Remelius JG, Hamill J, Kent-Braun J, Van Emmerik RE. Gait initiation in multiple sclerosis. Motor Control 2008;12:93-108. 12. Jacobs J, Kasser S. Effects of dual tasking on the postural performance of people with and without multiple sclerosis: a pilot study. J Neurol 2012;259:1166-76. 13. Mbourou GA, Lajoie Y, Teasdale N. Step length variability at gait initiation in elderly fallers and non-fallers, and young adults. Gerontology 2003;49:21-6.
14. Wajda DA, Motl RW, Sosnoff JJ. Dual task cost of walking is related to fall risk in persons with multiple sclerosis. J Neurol Sci 2013;335: 160-3. 15. Ratzker PK, Feldman JM, Scheinberg LC, et al. Self-assessment of neurologic impairment in multiple sclerosis. Neurorehabil Neural Repair 1997;11:207-11. 16. Sosnoff JJ, Finlayson M, McAuley E, Morrison S, Motl RW. Homebased exercise program and fall-risk reduction in older adults with multiple sclerosis: phase 1 randomized controlled trial. Clin Rehabil 2014;28:254-63. 17. Melzer I, Kurz I, Shahar D, Levi M, Oddsson L. Application of the voluntary step execution test to identify elderly fallers. Age Ageing 2007;36:532-7. 18. Learmonth YC, Sandroff BM, Pilutti LA, et al. Cognitive motor interference during walking in multiple sclerosis using an alternate letter alphabet task. Arch Phys Med Rehabil 2014;95:1498-503. 19. Lord SR, Menz HB, Tiedemann A. A physiological profile approach to falls risk assessment and prevention. Phys Ther 2003;83:237-52. 20. Gunn H, Creanor S, Haas B, Marsden J, Freeman J. Risk factors for falls in multiple sclerosis: an observational study. Mult Scler 2013;19: 1913-22. 21. Melzer I, Oddsson LIE. The effect of a cognitive task on voluntary step execution in healthy elderly and young individuals. J Am Geriatr Soc 2004;52:1255-62. 22. Chiaravalloti ND, DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol 2008;7:1139-51. 23. Woollacott M, Shumway-Cook A. Attention and the control of posture and gait: a review of an emerging area of research. Gait Posture 2002; 16:1-14. 24. Hausdorff JM, Balash J, Giladi N. Effects of cognitive challenge on gait variability in patients with Parkinson’s disease. J Geriatr Psychiatry Neurol 2003;16:53-8. 25. Schwenk M, Zieschang T, Oster P, Hauer K. Dual-task performances can be improved in patients with dementia: a randomized controlled trial. Neurology 2010;74:1961-8. 26. Canning CG, Ada L, Woodhouse E. Multiple-task walking training in people with mild to moderate Parkinson’s disease: a pilot study. Clin Rehabil 2008;22:226-33. 27. Segev-Jacubovski O, Herman T, Yogev-Seligmann G, Mirelman A, Giladi N, Hausdorff JM. The interplay between gait, falls and cognition: can cognitive therapy reduce fall risk? Expert Rev Neurother 2011;11:1057-75. 28. Coote S, Hogan N, Franklin S. Falls in people with multiple sclerosis who use a walking aid: prevalence, factors, and effect of strength and balance interventions. Arch Phys Med Rehabil 2013; 94:616-21. 29. Hass CJ, Gregor RJ, Waddell DE, et al. The influence of Tai Chi training on the center of pressure trajectory during gait initiation in older adults. Arch Phys Med Rehabil 2004;85:1593-8. 30. Grabiner MD, Bareither ML, Gatts S, Marone J, Troy KL. Task-specific training reduces trip-related fall risk in women. Med Sci Sports Exerc 2012;44:2410-4. 31. Cameron MH, Thielman E, Mazumder R, Bourdette D. Predicting falls in people with multiple sclerosis: fall history is as accurate as more complex measures. Mult Scler Int 2013;2013: 496325.
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ORIGINAL RESEARCH
Preliminary Investigation of Gait Initiation and Falls in Multiple Sclerosis Douglas A. Wajda, MSc, Yaejin Moon, MSc, Robert W. Motl, PhD, Jacob J. Sosnoff, PhD From the Department of Kinesiology and Community Health, University of Illinois at Urbana-Champaign, Urbana, IL.
Abstract Objective: To examine the relationship between gait initiation, fall history, and physiological fall risk in individuals with multiple sclerosis (MS) during both cognitive distracting and nondistracting conditions. Design: Single time point cross-sectional analysis. Setting: University research laboratory. Participants: Ambulatory individuals (NZ20) with MS ranging in age from 28 to 76 years. Intervention: Not applicable. Main Outcome Measures: Gait initiation time was quantified as the time to toe-off of the first step after an auditory cue. Gait initiation was performed with and without a concurrent cognitive challenge of reciting alternating letters of the alphabet. Additionally, participants underwent a test of fall risk using the Physiological Profile Assessment (PPA) and provided a self-report of the number of falls in the previous 3 months. Results: Gait initiation times ranged from .67 to 1.12 seconds during the single-task condition and .73 to 1.84 seconds during the cognitive challenge condition. PPA scores ranged from .80 to 3.87. Participants reported a median of 0.0 falls (interquartile range, 0.0e2.75) in the previous 3 months. There was a significant correlation between PPA score and gait initiation times only in the cognitive distraction condition (rZ.50). There was also a correlation between cognitive distraction gait initiation times and fall history (rZ.60). Conclusions: The observations provide preliminary evidence that gait initiation during cognitive challenge may represent a target for fall prevention strategies in MS. Archives of Physical Medicine and Rehabilitation 2015;96:1098-102 ª 2015 by the American Congress of Rehabilitation Medicine
Multiple sclerosis (MS) is a chronic disease of the central nervous system affecting approximately 2.2 million individuals worldwide.1 Individuals with MS commonly report decrements in balance2 and gait.3 Perhaps not surprising given these impairments, individuals with MS have a high risk of falling, with more than 50% reporting at least 1 fall over a 3- to 6-month period.4,5 Commonly, these falls occur during dynamic events such as transferring and transitions between positions6; however, most research has focused on the relationship between steady-state gait parameters and/or quiet stance with past or future falls.7 Gait initiationdthat is, taking a step from a quiet stance (eg, standing still)drepresents the complex transition between upright stance and steady-state gait. This process creates an intrinsically unstable condition as the individual shifts toward Supported by the National Multiple Sclerosis Society (grant no. IL Lot NMSS 006), which took no role in experimental design or manuscript preparation. Disclosures: none.
single-leg stance while concurrently generating the necessary momentum to take a step with the swing leg.8 The ability to effectively initiate gait or stepping is imperative for both the maintenance of upright posture and fall avoidance.9 Indeed, recent evidence demonstrates that choice stepping reaction time is significantly correlated to future falls in individuals with MS.10 Previous studies have examined the changes in gait initiation for individuals with MS compared with healthy controls. One such study11 consisting of 12 women with MS and 12 age- and sexmatched controls observed that the MS group had slower center of pressure (COP) movements and reduced COP shifts when initiating gait compared with controls. Similarly, a second study12 using a sample of 13 individuals with MS and matched controls investigated differences in single-step initiation between the groups during both standard and concurrent cognitive challenge conditions. The main observations were that individuals with MS had delayed step onset times compared with controls and that step initiation times increased during cognitive challenge conditions.
0003-9993/15/$36 - see front matter ª 2015 by the American Congress of Rehabilitation Medicine http://dx.doi.org/10.1016/j.apmr.2014.12.011
Gait initiation and falls in multiple sclerosis Individuals with a history of falling have been found to have an altered gait initiation compared with those who do not have a history of falling. For instance, Mbourou et al13 observed that elderly fallers exhibited smaller initial steps and increased initial step length variability compared with both elderly nonfallers and young adults. There is also recent evidence that choice stepping reaction time is impaired in frequent (>2 falls) fallers with MS compared with infrequent (1 fall) fallers.10 However, the choice stepping protocol does not inform whether the relationship with fall risk is associated with deficits in stepping or cognitive processes. The purpose of this pilot investigation was to further examine the relationship between gait initiation, fall history, and physiological fall risk in individuals with MS. Given the association between cognitive-motor interference (CMI) and fall risk in MS,14 gait initiation performance was examined during normal and concurrent cognitive challenge conditions. We hypothesized that gait initiation would be associated with fall history and physiological fall risk in individuals with MS and that this association would be strongest in the cognitive challenge condition.
Methods Participants The cross-sectional study consisted of a convenience sample of 20 individuals with MS who represented a subsample of participants in ongoing walking and balance exercise investigations. All data for the current protocol were collected within a single assessment. To be included, participants had to have a neurologistconfirmed diagnosis of MS and been relapse free for 30 days. Additionally, participants had to be able to stand and walk independently with or without the use of an assistive device.
Procedures The procedures for this investigation were approved by the local institutional review board. On arrival at the testing facility, participants were provided with a verbal explanation of the study procedures and presented with the informed consent document. Participants were given the opportunity to ask questions and then provided written informed consent. Subjects then provided demographic information and completed multiple trials of gait initiation. Additionally, a test of physiological fall risk was also performed. Demographic information including age, sex, assistive device use, MS subtype, and years since diagnosis was self-reported by the participants. The self-administered Kurtzke questionnaire was used to identify self-reported Expanded Disability Status Scale (EDSS) level.15 Self-reported disability level has demonstrated a high correlation (rZ.90) to the neurologist-administered EDSS.15 Fall history was operationalized as the total number of falls in the previous 3 months. Falls in the previous 3 months were reported using a standardized questionnaire that asked whether the participants had fallen, and if so, how many times in the previous
List of abbreviations: CMI COP EDSS MS PPA
cognitive-motor interference center of pressure Expanded Disability Status Scale multiple sclerosis Physiological Profile Assessment
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1099 3 months. This method for recording falls in the previous 3 months has previously been used in individuals with MS.16 Four trials of gait initiation were performed including 2 baseline trials and 2 trials with added cognitive challenge. Cognitive challenge tasks have been used previously during stepping tasks in this population and further highlighted gait initiation alterations.12 Additionally, cognitive challenge during voluntary stepping revealed significant differences between elderly fallers and nonfallers where baseline tests did not.17 In MS, measures of dual tasking have been shown to relate to physiological fall risk when standard spatiotemporal gait parameters did not.14 The kinematic parameters of gait initiation were quantified using a 6.1-m electronic Zeno walkway.a The Zeno walkway uses pressure sensors to calculate COP trajectories as well as the spatial and temporal parameters of gait based on individual footfalls. Participants were instructed to stand in place and then begin walking in response to an auditory cue. During the cognitive challenge condition, the participants simultaneously recited alternating letters of the alphabet (eg, A, C, E) aloud while performing the gait initiation task. Specifically, the participants recited letters during both phases (ie, standing and walking) of the cognitive distraction gait initiation trials. Participants practiced the letter task while seated before performing the cognitive challenge trials. This task has previously been used as a cognitive challenge during walking in MS.18 The main outcome measure for gait initiation was time to toe-off (step initiation time) of the first foot. The auditory signaling device was synced with the gait mat, and the time elapsed from signal presentation until toe-off of the first foot was recorded for each trial. Gait initiation times were averaged across trials within the specific conditions. An examination of physiological fall risk was performed using the short-form Physiological Profile Assessment (PPA).19 The PPA was originally developed for use in older adults and later validated for individuals with MS.20 The PPA consists of 5 tests examining visual contrast sensitivity (Melbourne Edge Test), simple reaction time, lower limb proprioception, isometric knee extensor strength, and standing balance on a compliant surface. The specifics of these tests are described in detail elsewhere.19 All 5 tests are administered with standardized instructions based on published guidelines.19 The results on these assessments are then entered into a database and compared with age-matched norms. Individual z scores are calculated for each subsection of the PPA, and an overall physiological fall risk score is presented as an overall z score, with larger values representing a higher risk.
Statistical analysis All statistical analyses were performed in SPSS version 20.b Descriptive statistics were calculated for all the outcome measures. Normality of the outcome measures was determined using the Shapiro-Wilk test. A repeated-measures analysis of variance was used to determine differences in gait initiation times between baseline and added cognitive challenge conditions. Spearman rank order correlations were performed to determine the relationships between the gait initiation times, fall history, and fall risk scores. Spearman correlations were selected because of the small sample size and nonnormality of the falls history outcome measure. All analyses used 2-sided tests, and P values .05 were considered statistically significant.
Results The ages of the participants ranged from 28 to 76 years (mean SD, 58.610.9y). The sample consisted of 15 women and 5 men.
1100 Sixteen of the individuals had relapse-remitting MS, 2 had secondary progressive MS, 1 had primary progressive MS, and 1 individual did not report MS type. The time since diagnosis ranged from 3 to 41 years (mean SD, 16.59.6y). Eleven of the individuals walked with no assistive devices, while 5 used unilateral support and 4 used bilateral support. The median selfreported EDSS score for the sample was 4.75 (interquartile range, 2.6e6.0), with a minimum of 3.0 and maximum of 7.0. The median number of falls in the previous 3 months was 0.0 (interquartile range, 0.0e2.75) and ranged from 0.0 to 6.0. The sample overall displayed an elevated fall risk, with a mean PPA score SD of 1.21.2. PPA fall risk scores ranged from a minimum of .80 to a maximum of 3.9. Table 1 provides descriptive statistics for the individual tests that comprise the PPA. These fall risk values are consistent with previous observations in MS.14,20 Gait initiation times during the baseline and cognitive challenge conditions took, on average (SD), .87.13 and 1.03.28 seconds, respectively. Results of the analysis of variance showed that gait initiation was significantly delayed during the cognitive challenge condition compared with baseline values (FZ8.9, PZ.008). Figure 1 displays scatterplots for single-task and cognitive challenge gait initiation times as a function of PPA fall risk score and falls in the previous 3 months. Spearman correlation analyses confirmed that PPA score had a positive correlation with cognitive challenge gait initiation time (rZ.50, PZ.03). Further analysis revealed that cognitive challenge gait initiation time was primarily related to deficiencies in the leg strength (rZ .47, PZ.04) and postural sway (rZ.46, PZ.04) components of the PPA. Moreover, a strong positive correlation was observed between cognitive challenge gait initiation time and fall history in the previous 3 months (rZ.60, PZ.01). No significant correlations were observed between single-task gait initiation times and either PPA score or past falls.
Discussion The aim of this pilot study was to investigate the relationship between gait initiation, fall history, and physiological fall risk in individuals with MS. We hypothesized that gait initiation would be related to both the number of falls in the previous 3 months and physiological fall risk, with the strongest relationships occurring during the cognitively challenging condition. Overall, this hypothesis was confirmed, as cognitive challenge gait initiation time was strongly correlated to fall history and physiological fall risk. The novel aspect of this observation is that gait initiation during cognitive distraction conditions but not single-task conditions was related to falls and fall risk in this sample. The observations further highlight the role of CMI in falls in persons with MS. The results add to the understanding of fall risk in MS and highlight that gait initiation during distracting conditions could possibly be a target of future fall prevention interventions. The hypothesis that gait initiation would be associated with physiological fall risk and fall history was based in part on previous research. First, falls are most common during movement transitions, such as standing to walking.6 Additionally, recent evidence demonstrates that choice stepping reaction time is significantly correlated to future falls in individuals with MS.10 The primary difference of the current observation with results from the choice stepping paradigm is that stepping was not confined to a single step toward target areas but was instead the first step to initiate walking. Additionally, the choice stepping task
D.A. Wajda et al Table 1
PPA component test descriptive statistics
Test Visual contrast sensitivity Simple reaction time Proprioception Knee extensor strength Postural sway
Mean SD 0.570.59 0.631.01 1.241.09 0.120.90 0.191.37
Minimum 1.37 2.80 2.94 1.74 2.36
Maximum 1.35 0.55 1.21 1.76 2.02
NOTE. All values are z scores. A negative sign indicates test performance below that of normative data.
did not delineate between stepping in isolation and stepping when engaged in a simultaneous cognitive task. Stepping represents one of the main compensatory strategies for avoiding a fall.9,21 Extending the results of the current study suggests that the effectiveness of the stepping strategy may be diminished in individuals with MS, particularly when cognitively engaged. That is, the individuals in this study who were at the greatest risk of falling took longer to initiate a step during cognitively challenging conditions compared with those at a lesser fall risk. Potentially this delayed stepping response indicates a reduced capacity to successfully implement a stepping strategy to recover from a balance perturbation (eg, trip), especially when distracted. Indeed, individuals in the present study who had the greatest number of falls in the previous 3 months demonstrated slower gait initiation times during cognitive challenge conditions. A caveat to this conclusion is that gait initiation was in response to an auditory cue, and this type of response may be distinct from initiation in response to an external perturbation. Cued gait initiation tasks inherently draw on various fall risk factors such as processing speed (ie, simple reaction time) and postural control. Consequently, it is possible that the association between gait initiation and falls is driven by declines in reaction time, declines in postural control, or both. There are copious amounts of evidence of deficits in processing speed22 and postural control2 in individuals with MS compared with controls. These factors are also subcomponents of the utilized fall risk assessment tool; thus the relationship between the gait initiation and fall risk is logical. To further investigate this explanation we analyzed correlations between stepping times and results from the individual tests of the PPA. We determined that higher cognitive challenge stepping times were indeed correlated to greater deficits in postural sway on a compliant surface, as well as to knee extensor strength. The lack of correlation between PPA simple reaction time and cognitive challenge gait initiation times challenges the contribution of cognitive processing speed in mediating the relationship between gait initiation and fall risk. Gait initiation performance during the current investigation was comparable to that in previous studies of individuals with MS who had mild to mild-moderate disability (median EDSS, 2.5; range, 0e4.5).12 Despite the current sample having an overall greater disability, we observed a similar slowing of gait initiation during cognitive challenge conditions compared with baseline. These alterations suggest the influence of interactions between cognitive performance and motor performance, typically termed cognitive-motor interference. During the cognitive challenge condition, both the motor and cognitive task compete for available attentional resources, which can lead to a decline in performance.23 CMI has been suggested to be related to falls in individuals with MS and other populations,14,24 and the current results further bolster this possibility. Given the adverse www.archives-pmr.org
Gait initiation and falls in multiple sclerosis
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Fig 1 Scatterplots of analyzed relationships. (A) Single-task gait initiation time versus PPA score. (B) Cognitive challenge gait initiation time versus PPA score. (C) Single-task gait time initiation versus past falls. (D) Cognitive challenge gait initiation time versus past falls.
consequences of CMI, it is logical that it become a focus of rehabilitation. Although there is some evidence that CMI can be impacted with targeted training in various clinical populations,25,26 there is no evidence that it can be altered in MS. The association between CMI and past falls and fall risk in individuals with MS further highlights the importance of including cognition and CMI in fall prevention rehabilitation programs.27 The results of this investigation suggest that gait initiation, especially during cognitive challenge, may represent a future target for falls prevention protocols. Although there is growing evidence that fall prevention is possible in individuals with MS,16,28 no interventions have focused on gait initiation in isolation or with a cognitive challenge. A small number of interventions have successfully focused on gait initiation in other clinical populations. For instance, tai chi training in older adults has been shown to improve gait initiation.29 Additionally, taskspecific stepping response training resulted in a decrease of fall risk in a sample of middle-aged and older women.30
limitations. First, the results come from a small convenience sample. Second, the study did not include a matched control group to consider the extension of these results beyond the current sample. Finally, retrospective recall of falls was used in a population in which memory deficits are common, necessitating caution when interpreting results.22 However, it is important to note that one of the best predictors of future falls and a commonly used clinical query is retrospectively reported falls.31
Conclusions Overall, the results of this pilot study serve to add to the understanding of falls and fall risk in individuals with MS. Additionally, the results suggest the pertinence of using dynamic tasks such as gait initiation as well as concurrent cognitive challenges for the analysis of fall risk in MS. Further study of gait initiation and its role in fall prevention strategies is warranted.
Study limitations
Suppliers
Despite the finding of correlations between gait initiation, fall history, and PPA fall risk scores, the current study has multiple
a. Zeno walkway; ProtoKinetics Inc. b. SPSS version 20; IBM Corp.
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D.A. Wajda et al
Keywords Accidental falls; Rehabilitation
Gait;
Locomotion;
Multiple
sclerosis;
Corresponding author Douglas A. Wajda, MSc, University of Illinois at UrbanaChampaign, Department of Kinesiology and Community Health, 301 Freer Hall, 906 S Goodwin Ave, Urbana, IL 61801. E-mail address: [email protected].
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