BACKGROUND AND PURPOSE
According to the World Health Organization, 15 million people worldwide have a stroke each year. One of the primary concerns for individuals who experience stroke is the ability to regain walking function.1 Consequently, significant effort is focused on gait retraining during rehabilitation following a stroke2 and efforts to develop and improve locomotor retraining programs are a major focus of rehabilitation research. Despite these efforts, many individuals with stroke have residual gait deficits3–8 and never achieve community ambulation status.9,10 Spatiotemporal gait asymmetries are prevalent after stroke and are related to slow walking speed.6,11,12 Step length asymmetry also has consequences relative to other gait deviations. Specifically, a shorter nonparetic step length is related to a decreased propulsive force on the paretic leg,3 which limits forward propulsion of the body, is related to slow gait speed,3 and may also be related to reduced efficiency.13 Thus, recent poststroke gait retraining interventions have targeted step length asymmetry to promote greater recovery of walking.14
Many novel rehabilitation interventions for those with stroke have emerged in the past several years.14–16 Recently, a group of studies utilizing the principles of motor adaptation applied to walking have gained interest in the rehabilitation community because of their unique ability to target specific gait deviations.17–20 In these studies, motor adaptation has a specific definition as follows: it is the process of modifying or adjusting a movement from trial to trial on the basis of error feedback21 such that a new movement pattern is temporarily learned to respond to new task demands. Once the adaptation is complete, if the new demand is removed, movements are once again erroneous, this time in the opposite manner, because the adapted pattern remains. These initial, oppositely directed errors are termed aftereffects. With continued practice with the demands removed, the movement pattern returns to baseline, again by modifying or adjusting the movement from trial to trial on the basis of error feedback. Using this definition, then, motor adaptation is one specific component of true motor skill learning. To fully learn a novel motor skill (ie, retain permanently) requires much longer time periods; the process is influenced not only by adaptive mechanisms but also by offline learning, consolidation, and long-term storage.22,23
Recent studies in persons poststroke have shown that applying the principles of motor adaptation through a split-belt treadmill walking paradigm can lead to short-term improvements in step length asymmetry.19,20 To obtain these improvements, a person's step length asymmetry must be exaggerated while walking on the split-belt treadmill. Specifically, a person with stroke who takes a longer step with the paretic leg and a shorter step with the nonparetic leg during regular walking would need to walk on the split-belt treadmill with the paretic leg on the slow belt. Initially, this will cause the person to take an even longer step with the paretic leg and an even shorter step with the nonparetic leg. Over time (less than 15 minutes), the person will correct the exaggerated asymmetry by lengthening the nonparetic leg step and shortening the paretic leg step. When the belts are returned to the same speed, the person will continue this adjusted pattern, resulting in improved step length symmetry.19,20 The improvements in asymmetry are short-lived, and the person with stroke returns to the baseline asymmetry after several minutes of overground or treadmill walking. However, these results demonstrate that persons poststroke retain the capacity to produce a more symmetric walking pattern, which could be capitalized on during rehabilitation.
A critical component of the split-belt treadmill studies described previously is the strategy employed to achieve an aftereffect of improved symmetry. Specifically, participant's step length asymmetry is exaggerated with the split-belt treadmill, thereby augmenting her “error” (asymmetry) during split-belt walking. This error augmentation is critical because it provides the nervous system with a cue to correct the asymmetry.19,20 This suggests an interesting and important concept for rehabilitation—movement error augmentation may prompt the nervous system to make a movement correction. This could be especially useful for persons with chronic movement deviations, where the deviation may no longer be perceived by the nervous system as a movement error that requires correction.18 This would suggest that rather than providing interventions that correct movement errors, it may be useful to enhance error and allow the individual to correct the movement.
The temporary improvements in step length and double support asymmetry observed in persons with stroke following split-belt treadmill adaptation occur on the treadmill and also transfer to overground walking.19,20 Thus, repetitive practice of the improved walking pattern after split-belt treadmill adaptation can be undertaken over ground, providing for optimal locomotor task-specific training. This makes the utility of this type of locomotor adaptation training particularly appealing for rehabilitation. However, to determine the potential value of split-belt locomotor adaptation in rehabilitation, it is important to know whether the short-term improvements observed can be translated into longer-term improvements through repetitive training. Thus, the purpose of this case study was to provide repetitive split-belt treadmill training in a person with stroke to determine whether longer-term changes in step length asymmetry and gait function could be achieved.
The participant in this case study was a 36-year-old woman who sustained a single hemorrhagic stroke, of undetermined etiology, involving the right insular region 1 year and 7 months before training. Her other medical history was unremarkable. She gave informed consent to participate in training on the basis of procedures approved by the human subjects review board at the John Hopkins School of Medicine.
After surgery and acute management, the participant received inpatient and outpatient rehabilitation, which ended several months before the start of this training intervention. Before her stroke, the participant was a full-time doctoral student. At the time of the training, she was continuing part-time with her studies and was not currently undergoing formal therapy. Her exercise activity was inconsistent and included walking on the treadmill and over ground outside when the weather permitted. She was independent in all activities of daily living and reported no history of falls in the past year. Observational analysis revealed that the participant walked without orthotic or assistive device, but with a slow walking speed for someone of her age. On the paretic side, stance time was noticeably shortened and step length was longer. She had difficulty clearing the ground with her paretic foot and used compensatory patterns such as hip elevation and circumduction. She reported that fatigue limited her walking and the consistency of her exercise routine. The participant's goal from this intervention was to improve her walking quality, speed, and endurance.
A detailed baseline clinical assessment was performed before the start of training. The participant had no major cognitive deficits or symptoms of hemispatial neglect as determined by the star cancellation test.24 Fastest and self-selected walking speed was measured as an average of 3 trials of ecah along a 6-me walkway. The Timed Up and Go (TUG) test, lower extremity Fugl-Meyer, and Stroke Impact Scale (SIS) were administered using customary procedures.25–27 Self-selected and fast walking speed, TUG test, lower extremity Fugl-Meyer, and SIS were repeated immediately after the completion of training and then again 1 month later. The participant's scores on these clinical tests are shown in Table 1.
Baseline overground walking characteristics of the participant were measured with computerized gait analysis using OPTOTRAK (Northern Digital, Waterloo, Ontario, Canada) sensors that recorded 3-dimensional position data at 100 Hz from both sides of the body. Infrared emitting diodes were placed bilaterally on the foot (fifth metatarsal head), ankle (lateral malleolus), knee (lateral joint space), hip (greater trochanter), pelvis (iliac crest), and shoulder (acromion process). The participant walked over ground down a 9-m walkway at her self-selected gait speed. Data from 7 to 8 trials were recorded and the middle 2 strides from each trial were used for analysis. Step length was calculated as the anterior-posterior distance between the ankle markers at the time when each foot contacted the ground. Step length was labeled paretic or nonparetic on the basis of the leading leg. The percent time in double limb support was the time when both feet were in contact with the floor, expressed as a percentage of the stride time for each leg. The stance time (the time from foot contact to lift-off) was also expressed as a percentage of the stride time. Data from instrumented gait analysis in persons with chronic stroke have shown high day-to-day reliability (ICC's of 0.97–0.99) for spatiotemporal measurements during overground walking.28 Furthermore, step length data collected from 3 persons poststroke during overground walking with the motion capture system used in this study found day-to-day changes of no greater than 0.7 cm. As shown in Figure 1, the participant demonstrated a 10-cm step length asymmetry at baseline, with the paretic leg taking a longer step compared with the nonparetic leg. Given her substantial step length asymmetry, we configured the split-belt treadmill belt speeds during training to target step length asymmetry (see training protocol later).
The participant trained 3 d/wk for 4 weeks. Each session lasted approximately 1 hour, including a warm-up on the treadmill and rest periods between bouts. The training was designed so the participant would walk on the split-belt treadmill in six 5-minute bouts for a total of 30 minutes of split-belt treadmill walking each day. However, for the first session of training, the participant completed only 4 bouts and for the second and third sessions, she completed only 5 bouts because of fatigue. For all subsequent sessions, she was able to complete all 6 bouts. During each training block, heart rate and the rating of perceived exertion29 were recorded at 2 and 4 minutes. If the rating of perceived exertion exceeded 15 or heart rate exceeded 80% of age-predicted heart rate maximum, the participant was given a rest break. During the rest period, heart rate and blood pressure were monitored.
During split-belt treadmill training, the participant walked with the paretic leg on the slow belt and the nonparetic leg on the fast belt. This leg-belt speed configuration was chosen so that the participant's baseline step length asymmetry would be exaggerated by the split-belts (initially, the leg on the slow belt takes a longer step than the leg on the fast belt, thus exaggerating the participant's asymmetry). The speed of the fast belt was close to the participant's fast overground walking speed (1.0 m/s) and the slow belt speed was half of the fast belt speed (0.5 m/s). During all treadmill walking, the participant wore a ceiling-mounted harness for safety. The harness did not support body weight or interfere with the participant's walking. The participant was allowed to use the front handrail of the treadmill for safety but was encouraged not to use this support. By session 6, the participant could consistently walk on the treadmill without using the handrail. Each day, following completion of all treadmill walking bouts, the participant practiced walking overground for approximately 5 minutes with verbal cueing from the physical therapist to reinforce the improved step length symmetry.
All evaluations were completed by a physical therapist (D.S.R.) with more than 17 years of clinical experience and all intervention sessions were completed by a different physical therapist with 19 years of experience (HM).
The clinical evaluation and gait analysis performed at baseline were repeated within 1 week of the end of training and then again 1 month after the end of training.
The outcomes from the clinical assessment are presented in Table 1. Self-selected walking speed increased from 0.71 to 0.81 m/s after training and continued to improve slightly to 0.86 m/s 1 month later. Fast walking speed increased from 1.13 m/s to 1.2 m/s following training and this was maintained at the 1-month follow-up. The time taken to complete the TUG test decreased from 11.62 to 10.21 seconds after training and decreased further to 8.85 seconds 1 month later. On the participation domain of the SIS, scores declined slightly posttraining but then increased at 1 month posttraining. Percent recovery as measured by the SIS increased by 10% at posttraining and increased an additional 10% 1 month later. The lower extremity portion of the Fugl-Meyer scale increased by 2 points at posttraining and this increase was maintained 1 month later.
The outcomes for step length are illustrated in Figure 1. The step length on both legs increased from baseline to posttraining and this gain was maintained at 1 month follow-up. Most importantly, however, step length asymmetry, which was the gait deficit targeted by the intervention, improved from 21% asymmetry at baseline to 9% asymmetry posttraining, and improved further to 7% asymmetry by 1 month after training. The actual step length difference decreased from a 9.3-cm difference at baseline to a 4.5-cm difference posttraining and then a 3.7-cm difference 1 month later. Stance and double support time asymmetries, which were not targeted by the intervention, remained essentially unchanged (Table 2).
This case study examined whether short-term improvements in step length asymmetry after split-belt treadmill walking can be translated into longer-term improvements through repetitive training in a person with stroke. Improvements in step length asymmetry were observed after training, and these improvements were maintained 1 month later. Concomitant changes in clinical measures were also observed, although in some cases these changes were relatively small. Nonetheless, the outcomes for this participant are encouraging, especially given the relatively small dose of training utilized.
Step length asymmetry is a pervasive gait deviation observed after stroke.8,11,12 It is related to other gait deviations, such as decreased paretic leg propulsive force,11 and to slow self-selected walking speed.11 The participant in this case study demonstrated an improvement of more than 50% in her step length asymmetry after split-belt treadmill training. Her actual step length difference decreased from almost 10 cm to less than 5 cm after training. This means that her step length asymmetry as a percentage of her paretic step length decreased from 21% to only 9%. Data from our laboratory has consistently shown that the average ± 1 SD step length asymmetry in persons who are neurologically intact is around 5 cm,19,20,30 and that step length asymmetry as a percentage of step length is approximately 2%. Thus, this participant with stroke now demonstrates a step length asymmetry that is closer to the normal range observed for persons who are neurologically intact. In addition, the improvement in step length asymmetry was achieved by an increase in step length on both legs, but with a relatively greater increase on the nonparetic leg. This is important because an improvement in asymmetry could also be achieved by a decrease in paretic leg step length. That type of change in asymmetry would not be as functionally desirable given that increased step length has been associated with increased walking speed following a treadmill and overground walking program in persons poststroke.31
Step length asymmetry is relatively resistant to change with gait interventions after stroke15,32 (although see Kahn and Hornby14). One of the differences between the intervention in this case study and previous studies is the incorporation of error augmentation. During split-belt treadmill walking, the enhancement of the participant's asymmetry leads to trial-and-error adjustment of step length and to the symmetric after-effect observed. Trial-and-error practice has been shown to be important for human motor learning33 and thus may have been the mechanism underlying the improvements observed here.
Small improvements in the participant's walking speed were also observed after split-belt treadmill training. However, this change did not exceed the minimal detectable change in self-selected walking speed for persons with chronic stroke.34
The time required by the participant to complete the TUG improved immediately after split-belt treadmill training and showed continued improvement when tested 1 month later. The change of 2.77 seconds on the TUG exceeds the average change in TUG scores after overground gait training in persons poststroke (1.81 seconds 95% CI, −2.29 to −1.33])35 but does not exceed the minimal detectable change previously reported for persons with chronic stroke.34
The participant also reported an improvement in her recovery from stroke and an increase in participation (both measured by the SIS). The 10-point change in participation from baseline to 1-month follow-up for our participant is much larger than the approximately 2-point change observed in a previous study.36 A 10- to 15-point change in a single domain of the SIS has been suggested to represent real and meaningful change.37 Also, important for the participant is that her perception of recovery from the stroke increased from 40% at baseline to 50% after the intervention and then to 60% 1 month later.
It is noteworthy that the participant's perception of her recovery, her self-selected walking speed, and her time on the TUG all improved steadily from baseline to posttraining to 1 month follow-up. Why did these measures continue to improve 1 month after the end of training? It is possible that the improvements in step length symmetry and walking speed observed after training allowed for greater ease of walking and greater walking practice, ultimately resulting in the continued improvement observed 1 month after training. Previous studies have shown that better step length symmetry is associated with faster walking speed11 and that increases in walking speed are accompanied by decreased energy expenditure and increased daily step activity in persons poststroke.38,39 Unfortunately, we did not measure energy expenditure or daily step activity, which would have been useful information.
There are several limitations to this case study. First, the participant experienced the testing protocol on multiple occasions and, therefore, changes could have been due to experience and/or practice. Second, the changes observed could have been due to natural recovery, although this seems unlikely given that she was more than 1.5 years poststroke at the time of testing. Third, the physical therapist performing the evaluations was not blinded to the intervention. Finally, it is possible that the improvement in step length asymmetry was solely due to the overground walking training and had nothing to do with the split-belt treadmill training. However, 33% of community-dwelling persons living with chronic stroke (including this participant) continue to demonstrate persistent asymmetries following participation in conventional physical therapy, of which overground locomotor training is a common component.8 Furthermore, other more conventional treadmill training studies that have also included an overground walking component have not found changes in step length asymmetry in persons poststroke.40 Thus, it seems unlikely that the overground walking component of the intervention alone (without the split-belt training prior to overground walking practice) accounted for the changes observed. However, a case study design does not allow us to rule out this possibility.
Previous single-session studies have suggested that rehabilitation interventions that utilize motor adaptation may be effective at targeting specific movement deficits after stroke.19,20,41 This case study is the first report demonstrating that, through repetitive practice, it is possible to capitalize on the short-term adaptations observed in previous studies and obtain longer-term improvements. Specifically, improvements were observed in the participant's step length asymmetry (the gait deviation targeted by the intervention), and these improvements were maintained 1 month later. Changes in walking speed, time on the Timed Up and Go test, social participation, and her perception of recovery from the stroke all showed more modest improvements; the impact of the intervention on these measures is not clear. Current studies are under way to determine whether similar improvements are observed across a larger group of individuals with stroke, and to determine baseline characteristics that influence a person's response to this intervention after stroke.
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