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Gait termination in individuals with multiple sclerosis
Gait & Posture, In Press, Corrected Proof, Available online 7 July 2015
- Gait termination in individuals with MS and healthy controls was assessed.
- Normal and cognitively distracting conditions were used.
- Cognitive distracting conditions had highest failure rates in both groups.
- The MS group was more unstable compared to controls during gait termination.
Despite the ubiquitous nature of gait impairment in multiple sclerosis (MS), there is limited information concerning the control of gait termination in individuals with MS. The purpose of this investigation was to examine planned gait termination in individuals with MS and healthy controls with and without cognitive distractors. Individuals with MS and age matched controls completed a series of gait termination tasks over a pressure sensitive walkway under non-distracting and cognitively distracting conditions. As expected the MS group had a lower velocity (89.9 ± 33.3 cm/s) than controls (142.8 ± 22.4 cm/s) and there was a significant reduction in velocity in both groups under the cognitive distracting conditions (MS: 73.9 ± 30.7 cm/s; control: 120.0 ± 25.9 cm/s). Although individuals with MS walked slower, there was no difference between groups in the rate a participant failed to stop at the target (i.e. failure rate). Overall failure rate had a 10-fold increase in the cognitively distracting condition across groups. Individuals with MS were more unstable during termination. Future research examining the neuromuscular mechanisms contributing to gait termination is warranted.
Keywords: Multiple Sclerosis, Gait termination, Mobility, Gait.
Multiple sclerosis (MS) is a disease of the central nervous system impacting over 2.5 million people worldwide  . It results in a heterogeneous array of symptoms including impairments in sensorimotor functioning, cognition, balance and gait , , , and . Gait impairments in MS are often characterized by a decline in gait speed, reduced step length and cadence compared with controls  and . The majority of research on MS and gait impairment focuses on continuous gait tasks such as the six-min walk test and 25 foot walk test  and . Although these performance tasks provide information regarding gait in general, they provide minimal information regarding the control of subtasks of gait, such as starting and stopping, that are essential for effective locomotion.
Coming to a stop from walking (i.e. gait termination) is a fundamental component of locomotion  and . It is a necessary skill for avoiding obstacles and maintaining balance when transitioning from walking to standing  . From a motor control perspective, maintaining posture during gait termination is potentially more challenging than maintaining posture during continuous walking due to larger destabilizing forces that are incurred when transitioning from dynamic to static posture  and . This postural transition has the potential to lead to falls in populations at a high risk of falling, such as MS  . Indeed, in individuals with MS transfers and ambulated-related activities are the two most cited actions that are performed at the time of a fall  .
Gait termination is dependent on two distinct control strategies. First, a macro control strategy requires planning proper foot placement in order to terminate gait at a desired target  . Second, a micro control strategy involves continuous control of the body center of mass (COM) inside the stability boundary as the feet are placed in the desired location  . Deficits in gait termination can result from difficulties with either of these control strategies and have been observed in clinical populations including individuals with cerebellar ataxia and peripheral neuropathy  and . Given the similarity in gait impairment between these pathologies and individuals with MS , , and , it is logical to speculate that individuals with MS will have impairments in gait termination.
Furthermore, gait subtasks such as gait termination are rarely done in isolation but rather under more complex conditions of divided attention. Although there is evidence that continuous walking  , gait initiation  and  and static balance control  under attentional distracting conditions are impacted in persons with MS, there is no data related to gait termination in this context. It is logical to speculate that a cognitive distraction could impede an individual's ability to execute a complex motor task, such as gait termination.
The purpose of this study was to examine planned gait termination in individuals with MS compared to healthy age matched adults during normal conditions and cognitively distracting conditions. Based on the high prevalence of gait impairments in individuals with MS, we hypothesized that they would demonstrate greater impairments in gait termination compared to age matched adults. Specifically it was predicted that they would have higher task failure rates and be more unstable during stopping. Additionally, under cognitively distracting conditions, gait termination performance would decrease in both groups with greater deficits observed in individuals with MS compared to controls.
This cross-sectional analysis included a convenience sample of twenty-five individuals with MS who participated in a fall prevention trial (ClinicalTrials.org # NCT01956227 )  . Inclusion criteria included a neurologist-confirmed diagnosis of MS, relapse free for the previous three months, the ability to walk with or without an assistive device, and having experienced a fall in the previous year. Medication use was not collected and consequently did not impact inclusion or exclusion from the study. All measures for the current analysis were completed during a single assessment. Additionally, the study included a control group of thirty adults similar in age and gender composition to the MS group. Recruitment of participants happened through fliers posted in the community and email advertisements to the university community. Prior to enrollment in the study, control subjects were screened to confirm the absence of neurological and musculoskeletal conditions along with any medications that might interfere with gait or cognitive functioning.
All procedures for the investigation were approved by the University of Illinois at Urbana-Champaign's institutional review board. After arriving at the testing facility, all participants were given a verbal explanation of study procedures, an informed consent document, and the opportunity to ask questions about the study. After providing written informed consent, the participants completed demographic questionnaires and multiple walking trials.
All participants provided demographic information including age and gender. Participants with MS also provided self-reported MS subtype, disability level and years since diagnosis. Self-reported disability was assessed with the self-administered Kurtzke questionnaire  .
Participants completed four 5 m walking trials starting and stopping on a 6 m Zeno™ pressure sensitive walkway ( Fig. 1 ). Participants were instructed to stand in the starting zone and begin walking after hearing an auditory cue. Participants were instructed to stop walking when they reached the stop zone. Starting and stopping zones were indicated by cones. During the first two trials, participants walked normally, and during the last two trials, participants completed a simultaneous cognitive task (i.e. dual task). For the added cognitive task, participants listed alternating letters of the alphabet from a given starting point (e.g. M, O, Q), and this task has been applied in MS  . No explicit task prioritization instructions were given to participants.
2.3. Data analysis
Maximum walking velocity was determined for each trial and the average for each unique condition for each participant was calculated. Gait termination was quantified with two distinct measures. First, in order to evaluate the macro control strategy, a global measure of success or failure was determined. Gait termination was successful if the participant stopped with both feet inside the designated gait termination zone ( Fig. 1 ). The gait termination zone was 26.6 cm long by 61.0 cm wide and was identified in data analysis by exported pressure sensor data form the Zeno™ walkway. The active pressure sensors for each walking trial were examined to determine if the participant stopped within the gait termination zone.
Second, in order to evaluate the micro control strategy, the time needed for the center of mass estimate (COMe) to stabilize during the stopping phase of gait termination was determined  and . The COMe was determined by the ProtoKinetics™ Movement Analysis Software based on the shift patterns of footfalls and values of pressure sensor activations over time, described in the software's measurements manual. Two gait termination stabilization time measures were reported, a raw measure of gait termination stabilization time (GTST) reported in seconds and a gait termination stabilization time normalized to maximum gait velocity (GTSTnorm). GTST was measured from first heel contact in the gait termination zone until COMe velocity in the anterior-posterior (AP) plane returned to baseline value. Baseline AP COMe velocity was the average AP COMe velocity during 4 s of quiet stance prior to the initiation of each trial. Only successful gait termination trials were included in the stabilization time analysis. GTST was determined for forty-two trials (84%) for the MS group and 57 trials (95%) in the control group. Given that gait velocity was expected to be higher in controls compared to the MS group and that gait velocity impacts available response time to stabilize during gait termination , , and , GTST was normalized to the maximum walking velocity of the trial, reported as GTSTnorm. This was done by dividing the GTST by the maximum gait velocity for each trial.
All statistical analyses were performed in SPSS Statistics 22.0 (IBM Inc., Armonk, NY). Descriptive statistics were computed for all demographic and gait termination outcome measures. Independent samples t-tests and chi-squared tests were used to determine differences in age and gender respectively between groups. A Wald chi-squared test for independence was used to evaluate differences in failure rates with group (MS/control) as the between subject factor and task (single/dual) as the within subject factor. Continuous outcome measures (maximum gait velocity, GTST, and GTSTnorm), were placed into separate 2 × 2 repeated measures analysis of variance (ANOVA) with group (MS/control) as the between subject factor and task (single/dual condition) as the within subject factor. The significance level for statistical tests was set at p ≤. 05.
The MS group consisted of 16 females and 9 males with a mean age of 61.1 years (SD = 8.4). The average number of years since MS diagnosis was 17.4 (SD = 8.6) and the median SR-EDSS was 6.0 (IQR = 4.5–6.5). Fifteen individuals had relapse remitting, 5 had secondary progressive, 3 had primary progressive, and 2 did not report MS subtype. The control group consisted of 23 females and 7 males with a mean age of 64.3 years (SD = 5.3). There was no difference in mean age between the groups (t = 1.63, p = .112). Gender distribution between groups was similar (χ2 = 1.1, p = .303).
Descriptive statistics for maximum walking velocity as a function of group and task are reported in Table 1 . As expected, there was a significant effect of group [F(1,53) = 45.8; p < .01] with the MS group walking slower than the control group. There was also a significant effect of task [F(1,53) = 92.9; p < .01] with a slower maximum velocity being reached in the dual task condition compared to single task. The was no significant group by task interaction [F(1,53) = 2.83; p = .09].
|Single task condition||Dual task condition|
|Mean ± SD||Range||Mean ± SD||Range|
|Max velocity (cm/s)|
|MS||89.9 ± 33.1||10.2–140.3||73.9 ± 30.6||8.1–129.1|
|Control||142.8 ± 22.6||97.7–200.8||120.0 ± 26.1||73.9–206.5|
|MS||0.918 ± 0.370||0.308–1.900||0.782 ± 0.360||0.175–1.529|
|Control||0.735 ± 0.268||0.150–1.392||0.712 ± 0.230||0.375–1.450|
|MS||1.733 ± 2.273||0.468–7.863||2.144 ± 3.306||0.222–13.670|
|Control||0.532 ± 0.220||0.096–0.915||0.610 ± 0.196||0.249–1.174|
a Normalized to max gait velocity reported in s2/m.
Failure rates are reported in Table 1 . The MS group failed to stop appropriately in 8% (i.e. failure rate) of the single task conditions and 60% of the dual task conditions. The control group had a failure rate of 3.3% under single task conditions and a failure rate of 50% under dual task conditions. Failure rates were not different between groups (Wald χ2 = 0.94, p = .33) but were significantly different between task conditions (Wald χ2 = 20.57, p < .01). Higher failure rates were noted under dual task conditions. There was no group by task interaction (Wald χ2 = 0.14, p = .71).
GTST as a function of group and task are reported in Table 1 . There was a trend for the MS group to take longer to stabilize than controls, however this effect was not significant [F(1,43) = 2.6; p = .115]. Also, there was not a significant effect of task [F(1,43) = 2.640; p = .101] nor a group by task interaction [F(1,43) = 1.4; p = .237] on GTST.
GTSTnorm as a function of group and task are reported in Table 1 . There was a significant effect of group on GTSTnorm [F(1,42) = 6.8; p = .012] with the MS group being more unstable. There was no effect of task [F(1,42) = 2.640; p = .112] nor a group by task interaction [F(1,42) = .05; p = .83] on GTSTnorm.
In persons with MS, there is limited knowledge concerning impairments in specific subtasks of gait that are essential to community ambulation. This analysis is the first to evaluate gait termination characteristics under single task and cognitively distracting dual task conditions. Findings indicate impaired gait termination in individuals with MS as well as decreased task performance for both groups in gait termination under cognitively distracting conditions.
Planning to terminate gait at a designated location requires macro and micro control strategies  and . Macro control involves successfully stopping at the appropriate time and place while micro control involves the control of the center of mass to accomplish gait termination (e.g. transition from dynamic to static postural control). On the macro level, there were no observed differences between groups. That is, individuals with MS and controls failed to stop walking at the same rate under single task and dual task conditions. At first glance, this could be interpreted that individuals with MS did not have impairments in gait termination at this level of analysis. However, it is important to note that the MS group walked ∼40% slower than controls and still had a similar rate of failures. This indicates that persons with MS were not able to utilize the greater amount of time prior to reaching the target to successfully terminate their walking. These results are consistent with documented impairments in motor planning specifically in online control, that is the ability to utilize sensory feedback to modify ongoing movement  , in persons with MS  and .
As hypothesized, failure rates increased in both groups under the cognitively distracting dual task conditions. This is consistent with the phenomena of cognitive-motor interference which explains the interaction between simultaneously performed cognitive and motor tasks  . Often that interaction results in decreased performance in one or both of the tasks  and . Cognitive motor interference is theorized to result from a cognitive task and a motor task competing for limited attentional resources  and . Recently it has been reported that slowed gait initiation during cognitively challenging conditions is related to falls in persons with MS  . It remains to be seen if impairments in gait termination are related to falls or other adverse consequences in persons with MS.
While there were no observed group differences in the overall ability to successfully terminate gait, GTSTnorm (e.g. micro strategies) was significantly higher in the MS sample than the controls. While this observation was only observed in the normalized measure, it indicates that individuals with MS were more unstable during gait termination. The current observations are consistent with a recent report of decreased dynamic stability and slower approach speeds in individuals with MS compared to controls in a walking and turning task  . Collectively, this is consistent with other gait termination investigations that have demonstrated elevated stabilization times in populations with motor impairments such as cerebellar ataxia and peripheral neuropathy  and .
Although traditional levels of statistical significance were not reached, there was a trend for higher GTSTnorm under the cognitively distracting condition (p = 0.11). Indeed, GTSTnorm was nearly 25% higher in the cognitively distracting condition compared to baseline within the MS group. Previous literature has demonstrated increased impairment under cognitively distracting conditions on various gait tasks in persons with MS , , and . For instance, cognitive distractions have shown to delay anticipatory postural adjustments on a step initiation task in individuals with MS  as well as increase postural sway in persons with MS  .
This analysis presents preliminary data on gait termination impairments in individuals with MS, and due to its behavioral nature, the mechanisms underlying these deficits cannot be concluded. However, considering symptoms in MS, there are several logical mechanisms that can be proposed and examined in future research. Possible mechanisms include muscle weakness, balance impairment, impaired somatosensory processing, and delayed anticipatory postural adjustments. It is well established that individuals with MS have muscle weakness that is associated with walking function , , and . Although it has been shown that muscle weakness is related to deficits in gait termination in older adults  , there is no data specific to MS. Instabilities during stopping could also result from balance impairment, another common symptom in persons with MS  and . Impairments in anticipatory postural adjustments have also been found in individuals with MS  and  and could contribute to the instabilities observed here. Another viable mechanism is declines in somatosensory processing. Somatosensory processing impairments contribute to dynamic balance deficits in persons with MS  and  and deficits in somatosensory processing resulted in more variable foot placement and higher loading forces necessary to terminate gait in young adults  . It is also quite possible that there is not a single mechanism but rather a combination of underlying factors contributing to gait termination impairment in persons with MS.
Possible limitations of this study come from the relatively small sample size where gait termination trials were collected after the MS group completed a fall prevention intervention. The sample consisted of older adults with MS who generally had higher disability; therefore it is possible the current results are not generalizable across the whole MS population. Additionally, an estimate of center of mass calculated by the ProtoKinetics™ software was used for the stabilization time measure. It is not clear if results from traditional center of mass techniques would yield the same observations. It is also important to note that only planned gait termination was investigated. A future analysis of unplanned gait termination in MS might reveal novel observations.
Overall this investigation revealed evidence of deficits in gait termination in individuals with MS. Despite walking 40% slower than controls, they still failed to stop at the same rate, indicating impairments in online control. Differences between the MS and control group were observed in the fine control of body COMe during termination, with the MS group being more unstable. Overall, these findings suggest impaired gait termination characteristics in individuals with MS. Therefore, understanding gait termination characteristics and control mechanisms and their link to adverse outcomes such as falls in the MS population warrants further investigation.
This study was funded in part by the National Multiple Sclerosis Society [IL LOT 006], who had no influence on experimental design or manuscript preparation.
Conflict of interest
The authors declare they have no conflict of interest.
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Department of Kinesiology and Community Health, University of Illinois at Urbana–Champaign, United States
⁎ Corresponding author at: University of Illinois at Urbana–Champaign, Department of Kinesiology and Community Health, 906 South Goodwin Ave., Urbana, IL 61801, United States. Tel.: +1 217 333 9472; fax: +1 217 244 6086.
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