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Research Reports |
JH Kahn, PT, DPT, NCS, is Research Physical Therapist, Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, Illinois.
TG Hornby, PT, PhD, is Assistant Professor, Department of Physical Therapy, University of Illinois at Chicago, 1919 W Taylor St, Chicago, IL 60612 (USA), and Research Scientist, Sensory Motor Performance Program, Rehabilitation Institute of Chicago.
Address all correspondence to Dr Hornby at: tgh{at}uic.edu
Submitted August 6, 2008;
Accepted January 30, 2009
| Abstract |
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Subjects and Design: Eighteen individuals with chronic hemiparesis and substantial SLA during overground walking participated in a single-group, pretest-posttest study. The study consisted of 2 phases, with 10 subjects participating in each phase; 2 subjects participated in both phases.
Interventions and Measurements: To investigate rapid effects of UST, the participants completed a 20-minute session of UST on a treadmill with their unimpaired limb, with the impaired limb held stationary off the treadmill. Data for spatiotemporal gait parameters during overground walking at self-selected and fastest speeds were collected prior to and following UST, with follow-up measurements at 1 day and 1 week. To investigate the prolonged effects, the participants completed ten 20-minute sessions of UST. Data for spatiotemporal gait parameters were collected prior to training as well as after every third session, with follow-up measurements at 1 and 2 weeks.
Results: Immediately following UST, SLA tested during fast-paced overground walking improved by up to 13% (49% reduced to a 36% SLA), with changes retained for up to 24 hours. Following 10 sessions of UST, SLA improved significantly, with changes retained for up to 2 weeks.
Limitations: Despite repeated baseline measurements, the absence of a control group was a limitation. Furthermore, stepping characteristics during UST were not quantified.
Conclusion: Unilateral step training may improve spatiotemporal patterns in people with substantial gait asymmetry poststroke. Repeated training may be necessary for maintenance of adaptations.
| Introduction |
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Despite recent insight into potential factors underlying SLA poststroke, there is little evidence to indicate these behaviors can be modified with physical rehabilitation. For example, locomotor training using body-weight support (BWS) on a motorized treadmill has been shown to facilitate recovery of independent walking function poststroke,16 with improvements in postural control, gait speed, and endurance.17,18 There is, however, little emphasis on potential alterations in gait symmetry following such training,19,20 with recent data indicating little change in spatial symmetry.21 A previous investigation22 attempted to alter step timing symmetry using a standing biofeedback paradigm to augment paretic-limb weight bearing, although changes in gait symmetry were not different from those of a control group that did not receive such feedback training. No studies using conventional physical therapy approaches have shown substantial changes in SLA.
A long-standing body of literature has demonstrated the capacity of the locomotor system to adapt rapidly in response to experimental perturbations and, depending on the magnitude and duration of perturbing stimuli, retain such adaptations (ie, demonstrate aftereffects) following removal of the stimulus.23–25 To investigate adaptations in interlimb coordination during walking, Reisman and colleagues26 utilized a split-belt training paradigm in which a belt under each limb was controlled separately. In their paradigm, subjects walked on a split-belt treadmill with 2- to 4-fold differences in individual belt speeds while data for kinematic gait parameters were collected. During 10 minutes of split-belt walking, rapid changes in intralimb parameters (ie, stride length and percentage of stance time) were observed, but the changes were not maintained during normal treadmill walking when the belts were tied together. In contrast, interlimb parameters (ie, step length and percentage of double support time) changed gradually throughout the training paradigm, with significant adaptations following return to normal treadmill conditions. Such adaptations were characterized by longer step lengths on the perturbed (fast-trained) limb, with a gradual reversion to symmetrical walking patterns.
Recent data indicate that similar adaptations in spatiotemporal gait parameters are evident in people with hemiparesis poststroke following split-belt walking.26,27 More precisely, gait symmetry improved following split-belt walking when the limb with shorter step lengths was trained at the faster speed; however, changes returned to baseline within the 6-minute post-adaptation period. Evidence of rapid alterations in spatiotemporal gait parameters in individuals with gait asymmetry poststroke is appealing in that repeated exposure to such perturbations may induce lasting alterations in walking characteristics.28 Preliminary evidence indicates the transfer of locomotor adaptations during overground walking,29 although these adaptations persist for a brief duration. Unfortunately, minimal access to split-belt treadmills also may limit the clinical application of this training.
The purpose of this study was to investigate the potential adaptations in spatiotemporal gait parameters in individuals poststroke following unilateral step training (UST). Subjects with marked SLA were trained using a simple stepping paradigm in which they were required to step with their unimpaired limb on the treadmill while their impaired limb was held stationary off the treadmill. The study consisted of 2 phases: phase 1 assessed the rapid changes in gait symmetry following a single session of UST, and phase 2 determined long-term alterations in SLA with repeated UST. We hypothesized that UST would decrease SLA during overground walking in people with chronic hemiparesis poststroke on both rapid and prolonged time courses. Alterations in spatiotemporal gait patterns following UST may further demonstrate the adaptive capacity of locomotor behaviors in people with damage to supraspinal pathways and reveal a clinical strategy to enhance gait symmetry.
| Method |
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6 months duration following stroke and clinical presentation of hemiparesis completed both phase 1 and phase 2. Preliminary power analysis estimated effect sizes of changes in SLA to be greater than 1.0 using paired comparisons of pretraining versus posttraining data. Therefore, 10 subjects were recruited for each phase. Two subjects participated in both phases, for a total of 18 subjects. All subjects ambulated without physical assistance at speeds of less than 1.0 m/s, but they were permitted to use an assistive device or orthosis below the knee, as needed. Specific criteria included the presence of substantial SLA, defined as an unimpaired step length at least 20% less than that of the impaired limb during overground walking at a self-selected pace. Additional exclusion criteria included: presence of severe lower-extremity contractures or orthopedic injuries limiting range of motion or mobility; uncontrolled hypertension; cardiac arrhythmias; uncontrolled diabetes; bilateral, brain-stem, or cerebellar stroke; presence of unhealed decubiti; and significant cognitive impairments that would limit the subject's ability to understand the study procedures (Folstein Mini Mental Status Examination scores >22/30). All subjects provided written informed consent. The intent to investigate walking patterns following UST was explained to the subjects, but they were not given specific information on the primary hypothesis. Individual subject characteristics are provided in the Table.
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For both phases, data for spatiotemporal gait parameters were collected and averaged over 2 to 3 walking trials on the Gait Mat II at both self-selected and fastest speeds with specific instructions to "walk at your normal, comfortable pace" and "walk as fast as you safely can," respectively.
For UST, subjects were escorted to a motorized treadmill
and fitted with a safety harness attached to a counterweight system. Body-weight support was provided only as necessary to minimize buckling of the impaired limb (phase 1: mean=8 kg, 95% confidence interval [CI]=2 to 14; phase 2: mean=0 kg, 95% CI=0). Subjects were permitted to hold on to a support bar placed at waist height across the treadmill, but they were discouraged from substantial upper-extremity weight bearing and encouraged to ambulate without upper-extremity support whenever possible. Subjects were permitted to rest, as needed, with vital signs obtained prior to, during, and following training and maintained within American College of Sports Medicine guidelines for individuals with known cardiovascular disease.32 In both phases, UST was performed for 20 minutes (1 session for phase 1 and 10 sessions for phase 2) with the stepping (unimpaired) limb positioned on the treadmill belt and the nonstepping (impaired) limb off the belt at the same height. Subjects were instructed to step continuously with their unimpaired limb, while the impaired limb was to remain stationary (ie, in stance). Visual or verbal cues were provided only as necessary at initial training sessions to facilitate continuous stepping, maintain upright posture, and minimize upper-extremity support.
Phase 1.
Following the screening examination, subjects attended one 20-minute session of UST (Fig. 1A) and 2 follow-up testing sessions. Initial treadmill speed was determined by the average overground walking speed at subjects self-selected pace, recorded immediately prior to training, with walking speed gradually increased by 25% every 5 minutes. Following 20 minutes of UST, subjects were removed from the treadmill using a wheelchair and were not permitted to walk between testing intervals. Spatiotemporal data were collected over 2 to 3 trials at self-selected and fastest-possible speeds at 10, 20, and 30 minutes following UST, with similar instructions provided as in the initial evaluation. Follow-up evaluations for spatiotemporal gait patterns were performed approximately 24 hours following the single UST session and at 1 week posttraining.
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Outcomes and Statistical Analysis
Spatiotemporal data collected during self-selected and fast walking speeds were averaged within each testing period, with specific parameters (step and stride lengths and stance and swing durations) analyzed using the Gait Mat II software. The primary dependent variable was SLA, calculated by the following equation:
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Data across subjects were pooled, and spatiotemporal data were described as the mean (CI) unless stated otherwise. All statistical analysis was performed using StatView (version 5.0.1),
with
=.05. To assess for improvements in gait patterns due to familiarity of the testing apparatus, paired t tests were performed between data collected at the screening examination and data collected during testing immediately prior to unilateral stepping, indicating no significant differences in any gait parameter. Specifically, SLA at self-selected speed changed slightly (mean=43%, 95% CI=27% to 59%, to mean=46%, 95% CI=29% to 63%; P=.09) with repeated baseline testing. Pearson correlation coefficients were calculated to assess the strength of associations between baseline gait asymmetry (SLA and STA) measures during both self-selected and fastest walking conditions and gait speed to compare data with those previously published.8,13
Data were tested for normality using the Kolmogorov-Smirnov test, and, following determination of normality, parametric testing was done. The statistical analysis focused on the primary outcome of differences in SLA calculated immediately prior to UST and during subsequent testing sessions. For phases 1 and 2, separate one-way, repeated-measures analyses of variance were used to calculate differences in SLA during both overground walking speeds, with post hoc Tukey-Kramer tests as necessary, emphasizing changes in gait parameters prior to versus following UST. Conditions tested in phase 1 were: pretraining; 10, 20, and 30 minutes posttraining; 1-day follow-up; and 1-week follow-up. Conditions compared for phase 2 were: pr-training; SLA prior to sessions 4, 7, and 10; and follow-up assessments at 1 and 2 weeks posttraining. Additional analyses were directed toward secondary outcomes, including changes in individuals step lengths and changes in STA and gait speed. Pearson correlation analyses were completed to further describe potential relationships between changes in SLA and changes in STA and gait speed at each testing interval posttraining (ie, pretraining values compared with values in all subsequent testing conditions).
Role of the Funding Sources
This study was supported by the Taylor Fellowship, Rehabilitation Institute of Chicago, and the National Institutes of Disability Rehabilitation Research, Rehabilitation Research Training Center (grant #H133B031127). Funding sources had no role in study design or reporting.
| Results |
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Phase 1
Alterations in SLA.
Measurements for spatiotemporal gait parameters were collected prior to and following a single 20-minute session of UST with the unimpaired limb. Following UST, changes in SLA at self-selected and fast speeds were altered differentially. Changes in SLA during self-selected speed approached significance (improved by 9% at 10 minutes posttraining, P=.05). Differences were characterized by a nearly 20% (0.04-m) increase in step length in the unimpaired limb, but also an approximately 9% (0.04-m) increase in the impaired (untrained) limb (Fig. 2).
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Alterations in STA and gait speed.
Alterations in selected temporal aspects of gait also were assessed following UST to determine their potential association with SLA. At self-selected walking speed, there were no changes in STA from pretraining values. During fast walking, however, improvements in STA were observed following UST, with significant differences at 30 minutes (mean=20%, 95% CI=–2% to 42%; P<.05), although no significant differences were observed at other testing periods. Adaptations in STA were characterized by an improvement in single-limb stance time of the impaired limb (
12%), without alterations in stance time of the unaffected limb. There were no significant correlations between changes in SLA and STA at either overground walking speed.
Gait speed at self-selected walking speed tested following UST increased from pretraining values, with significant differences at 30 minutes posttraining (16% [0.05-m/s] increase, 95% CI=3% to 29%) and at 1 day posttraining (15% [0.03-m/s] increase, 95% CI=0% to 30%). There was no significant increase in fastest-possible speed. Increases in gait speed were not correlated with changes in SLA at either self-selected or fastest-possible walking speed.
Phase 2
Alterations in SLA.
Measurements for spatiotemporal gait parameters were collected prior to and intermittently throughout 10 sessions of UST with the unimpaired limb. Following training, SLA during both self-selected walking speed (P=.01) and fastest walking speed (P<.01) increased only slightly following the first 3 UST sessions (range=4%–5%), with significant differences of up to 12% observed at the follow-up sessions. Changes in SLA were characterized by increased step length of the unimpaired limb observed before session 7 and at 1 and 2 weeks posttraining, with the greatest change at 1 week posttraining for self-selected pace (32% [0.04-m] increase, 95% CI=24% to 40%) and at 2 weeks posttraining for fast walking (24% [0.04-m] increase, 95% CI=20% to 28%) (Fig. 3). Initial SLA was correlated with the amount of improvement in SLA (r=.64, P<.05).
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Changes in gait speed were analyzed to determine potential association with alterations in gait symmetry parameters. Overground gait speed at self-selected pace increased throughout testing, with the largest increase at 1 week posttraining (18% [0.06-m/s] increase, 95% CI=15% to 21%), with a moderate correlation with changes in SLA (r=.50, P<.001). There were no significant changes in gait speed for the fastest-possible walking condition, despite large changes in SLA.
| Discussion and Conclusions |
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In contrast to previous investigations of gait asymmetry poststroke,27,33 selected spatiotemporal characteristics of walking were observed over ground and maintained with repeated exposure to UST in the current study. Previous studies using bilateral locomotor training and a treadmill in individuals poststroke have demonstrated very little change in SLA.17,34 In addition, recalculation of our own previously published data21 for subjects with substantial SLA (ie, >20%, n=9) following locomotor training did not show significant improvements in SLA. Patterson and colleagues19 recently demonstrated increases in step length of the paretic and nonparetic limbs following 6 months of treadmill exercise, although no changes in interlimb symmetry were observed.
The present data are consistent with previous evidence demonstrating adaptations in stepping behaviors following locomotor perturbations in people who were neurologically intact and in people with impairments. For example, in subjects without impairments who were asked to jog either forward or backward on a treadmill, Anstis23 demonstrated inadvertent forward or backward motion, respectively, when the subjects were asked to jog in place without visual guidance immediately following the treadmill stimuli. Patients with Parkinson disease35 or spinal cord injury36 also demonstrated rapid increases in gait speed following brief bouts of fast treadmill walking. Alterations in locomotor trajectory were observed following stepping on a circular treadmill, in which subjects both with and without neurological injury demonstrated curved trajectories of stepping or walking in the opposite direction of the rotation of the treadmill.24,25,37 More pertinent to the present study, alterations in intralimb coordination38 and interlimb coordination26,27 have been observed following exposure to specific locomotor stimuli (ie, split-belt walking) as described previously. Such changes appear dependent on cerebellar structures,39,40 although patients with other neurological diagnoses, including stroke,27 can demonstrate such adaptations and aftereffects.
Consistent with these studies, the present investigation revealed significant locomotor adaptations consistent with the demands of the experimental task. Specifically, subjects were required to step only with their unimpaired limb at progressively faster speeds. Although gait kinematic data were not collected during the training period (also see Earhart et al,24 Hong et al,25 and Weber et al37), a likely reason for the observed changes in SLA may be that subjects were taking longer steps on the unimpaired limb to keep pace with the treadmill speed, consistent with the changes observed following single or repeated sessions of UST. These adaptations are consistent with previous data27 and indicate that positive changes in gait symmetry are possible in subjects with damage to supraspinal centers.
Of additional interest was the general lack of improvement in STA following repeated sessions of UST. Specifically, substantial loading of the impaired limb occurs during UST with the unimpaired limb, and intuitively we would expect STA to improve accordingly. The lack of significant findings may be due to the inclusion criteria used for this study, which focused only on SLA in our potential population, and resulted in substantial variability in our STA measurements.
Specific limitations of the present study warrant further discussion. Despite the perturbation applied to the subjects, they were initially given verbal instruction for continuous stepping, at least in the first session to facilitate accommodation to the novel stepping paradigm. Often, this was necessary only to ensure subjects continued to maintain their position on the treadmill. Despite data indicating a potential for auditory cueing to facilitate symmetry during treadmill walking in subjects with hemiparesis following stroke,41,42 verbal cueing was minimal, did not occur with all subjects, and was not directed for subjects to increase their step length on their impaired limb. It is unlikely, therefore, that minimal cueing contributed to the results.
In this protocol, we increased treadmill speed during UST to increase practice (ie, number of steps) during the allotted training paradigm. Changes in spatiotemporal patterns observed following training could potentially be due to increased speed, as indicated by a moderate correlation between changes in self-selected gait speed and changes in SLA in phase 213 (however, see Roth et al8). However, lack of significant differences in subjects pretest SLA at either speed may argue against this possibility. Specifically, subjects walked with similar asymmetrical patterns at baseline assessments at their self-selected or fastest-possible walking speed. Additionally, in the fastest overground walking conditions for phases 1 and 2, there were no changes in gait speed; however, there were significant changes in SLA, further indicating that the 2 variables may not be dependent on each other.
Finally, in this pilot study, we did not quantify the stepping characteristics during the intervention, but rather collected data only on the spatiotemporal gait characteristics during overground walking prior to and following training. Future studies should include quantification of kinetics13 and kinematics26,27 during and following the stepping perturbations to understand potential mechanisms underlying the observed changes in SLA, influenced primarily by changes in step length of the unimpaired limb. For example, other authors have indicated that paretic propulsion13 or spastic plantar-flexor activity10 may be related to stepping asymmetries in people with hemiparesis after stroke, although neither of these variables was assessed. Following bilateral locomotor training, however, changes in ankle spasticity (hypertonicity) are inconsistent, with either small changes43 or negligible changes44 observed. In contrast, the degree of SLA and gait speed are both correlated with paretic propulsive forces and may have been a contributing factor to our present results, although the contribution of propulsion to our current results is unknown and further investigation is needed.
Although targeting asymmetrical walking is certainly a goal of both patients1 and therapists18 in rehabilitation, the clinical and functional significance of the present results warrant further consideration. For example, Perera et al45 recently attempted to describe clinically significant changes in gait performance related to walking speed or distance, although there are no studies that identify what a clinically significant change is for gait symmetry. Following repeated training, our current data represent a relatively large (28%) reduction in asymmetry compared with baseline conditions (mean SLA change=12% versus mean baseline SLA=43%).
Whether such changes are functionally important is unclear. Specifically, although both SLA and gait speed increased following UST, the small potential relationship between changes in these variables brings into question whether gait symmetry may provide a functional benefit beyond improved gait cosmesis. One potential positive aspect of improved symmetry may be increased gait efficiency. Although the energetic costs of asymmetrical gait in people with hemiparesis has not been established, previous studies46,47 indicate that alterations in step length may increase the metabolic requirements of ambulation.
Despite the limitations described, the observed changes in spatiotemporal parameters indicate the potential capacity for immediate improvements in gait symmetry in people with hemiparesis following specific stimuli, with repeated exposure required for persistence of adaptations. Unilateral step training may have the potential to be used as an adjunct treatment to improve gait symmetry in people with chronic hemiparesis and can be applied readily in the clinical setting. Future studies to determine alterations in gait symmetry between UST and other physical interventions are warranted.
| Footnotes |
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The authors thank the following individuals for assistance with data collection: Donielle Campbell, PTA, Tobey DeMott, PT, Jennifer Moore, PT, NCS, and Heidi Roth, PT, NCS.
This study was approved by the Institutional Review Board of Northwestern University.
Poster presentations of this research were give at the Combined Sections Meetings of the American Physical Therapy Association; February 1–5, 2006; San Diego, California; and February 9–12, 2009; Las Vegas, Nevada.
This study was supported by the Taylor Fellowship, Rehabilitation Institute of Chicago, and the National Institutes of Disability Rehabilitation Research, Rehabilitation Research Training Center (grant #H133B031127).
* EQ Inc, PO Box 16, Chalfont, PA 18914-0016. ![]()
Woodway GmbH, Steinackerstrasse 20, D79576 Weil am Rhein, Germany. ![]()
SAS Institute Inc, PO Box 8000, Cary, NC 27513. ![]()
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