Cerebral palsy (CP) refers to a group of disorders in the development of posture and motor control resulting from a nonprogressive lesion of the developing central nervous system.1 Functional abilities and limitations of children with CP have been described in the 5-level classification system of the Gross Motor Function Classification System (GMFCS) and in the expanded and revised GMFCS (GMFCS-E&R), which includes an age band for youth 12 to 18 years of age, and emphasizes concepts of the World Health Organization's International Classification of Functioning, Disability and Health (ICF) reflecting the potential effect of environmental and personal factors.2
Youth with CP classified at GMFCS level I possess motor skills necessary for successful function within their homes, schools, and communities.2 They are able to ambulate independently without assistive devices, albeit with a limited movement repertoire resulting in restricted variation of movement strategies within a given environment or activity. Important factors leading to participation limitations include difficulties walking on uneven surfaces and inclines or walking in crowds or confined spaces, lack of endurance, reduced speed, balance, and coordination.2 Adolescents with CP have been reported to be less physically active and walk less than peers without CP.3
Adolescence and early adulthood has been recognized as an important time of transition particularly for individuals with CP. However, physiotherapy services for youth with CP classified at GMFCS level I are usually more limited as these youth are thought to have reached a plateau in their gross motor skills. The authors of a prospective longitudinal study in adolescence and early adulthood reported that the gross motor development curve for GMFCS level I follows a stable limit model on the basis of the Gross Motor Function Measure–66 (GMFM-66) and showed no evidence of functional decline or improvement in adolescence.4 In contrast, deterioration was shown in adults classified at GMFCS level I, where functional assessment revealed that walking ability decreased from GMFCS levels I to II.5
Although limited, there are data supporting the effectiveness of interventions aimed specifically at improving functional balance and mobility of youth classified at GMFCS level I. Woollacott et al6 reported on the effect of massed practice in recovery of postural control following perturbations with children with CP classified at GMFCS levels I and II and demonstrated significant improvement in their ability to recover stability with changes still present 1 month later. The intensive training resulted specifically in improvements in directional specificity and spatial-temporal characteristics of muscle responses.6 A clinical approach used for improving functional mobility in CP, bodyweight–supported treadmill training, has also shown significant improvements in walking velocity and energy expenditure following an intensive 2-week program in children with CP classified at GMFCS level I.7
Novel interventions using virtual reality (VR) are increasingly being used to optimize motor rehabilitation through task-oriented practice. Virtual environments (VEs) provide unique multidimensional media involving multimodal sensory processes where the individual interacts with virtual scenarios consistent with real life situations. The level of task difficulty may be modified to provide optimal, motivating challenges. In the VE, intensive repetition can be automated to deliver specific stimuli under very controlled conditions.8 Studies in adults have demonstrated the effectiveness of training using VEs when compared to physical world–based interventions on community-level functional mobility and improved confidence and independence.9 In pediatric motor rehabilitation, the literature supporting the use and effectiveness of VR-based interventions for children with CP is scarce. Among those studies, results showed improvements in motor learning with skill transfer and integration into real life situations,10 improved reaching kinematics,10 increased upper extremity control,11 and improved ankle selective motor control and participant motivation.12
This study examined the effect of an intensive VR training program on functional balance and mobility in 13- to 18-year-old adolescents with CP classified at GMFCS level I. We hypothesized that (1) a 5-day 90-minute per day intervention program would result in improvements on the Community Balance and Mobility Scale (CB&M), the 6-Minute Walk Test (6MWT), the Timed Up and Down Stairs (TUDS), and the GMFM Dimension E and (2) improvements would be maintained 1 week and 1 month after the intervention.
This study was approved by the University of Ottawa Research Ethics Board and the Ottawa Children's Treatment Center Research Review Committee. Participants met the following inclusion criteria: (1) between the ages of 13 and 18 years, (2) GMFCS level I, and (3) able to follow directions on standardized testing. Exclusion criteria were the following: (1) orthopedic surgery within the past 12 months and (2) botulinum toxin type A injections within the past 6 months. Four male adolescents were recruited (mean age = 16 y, SD = 2.25 y). Participant 1 (P1) was 17 years 8 months old and had spastic diplegia (L > R). Participant 2 (P2) was 13 years 9 months old and had choreoathetosis. Participant 3 (P3) was 18 years 9 months old with spastic diplegia. Participant 4 (P4) was 14 years old with spastic diplegia (R > L). Written informed consent or assent was obtained as appropriate from the participant and/or parent(s) of each participant.
A single-subject repeated measures multiple-baseline design (MBD) using A-B-A with 1-month follow-up was used. One trained physiotherapist, independent from the research team, completed all assessments during the 3 study phases: (1) baseline phase (BP)—between 3 and 6 assessments the week prior to intervention; (2) intervention phase (IP)—prior to training on days 2 through 5 to avoid possible fatigue due to training; and (3) follow-up phase (FUP)—3 times in the week following the intervention and at 1 month postintervention. The assessment session timeline for each participant is shown in the Table 1. The study design and method guidelines for single-subject research design (SSRD) levels of evidence developed by a subcommittee of the AACPDM (American Academy for Cerebral Palsy and Developmental Medicine) Treatment Outcomes Committee were used.13 On the basis of these guidelines, the present study provides level III evidence, defined as a nonrandomized, nonconcurrent, controlled MBD with clear-cut results that provides generalizability if the design consists of a minimum of 3 subjects, behaviors, or settings. The baseline, intervention, and FUPs were arranged to support a decision of causality and generalizability. Standardized measurement conditions were ensured for repeated participants testing with consistency in both location and time of day. Separate data collection forms were used for each session and each clinical measure to eliminate scoring bias from knowledge of prior results. There was no participant attrition or loss of data points during the study. The outcome measures were administered consecutively in the following order: CB&M, GMFM Dimension E, TUDS, and 6MWT. Participants had approximately 5 minutes of rest between outcome measures. The assessment period took 45 minutes and was followed by a 15-minute rest before the first VR intervention session.
Clinical Outcome Measures
The CB&M, the 6MWT, the TUDS, and the GMFM Dimension E were used to determine change in different aspects of functional balance and mobility emphasized during intervention. The CB&M, a clinically meaningful 13-item performance-based measure evaluates high-level balance abilities and addresses coordination, accuracy, and speed components required for everyday function in the community. Test items include lateral dodging, 180° tandem pivot, hopping forward, walking, and looking. The CB&M's 6-point rating scale uses precise response option descriptors for each item with a highest possible score of 96 points.14 Test content, construct validity, and high test-retest reliability have been reported in adults post–acquired brain injuries with high level balance abilities.14 The CB&M has shown excellent interrater reliability in youth with acquired brain injuries.15 The CB&M was chosen as the scale would not demonstrate a ceiling effect in youth with CP classified at GMFCS level I providing room for change to be detected.
The 6MWT, a submaximal test performed at a self-selected speed, assesses functional capacity for walking a prolonged distance. It has demonstrated excellent test-retest reliability with children who are ambulatory16 and adolescents with CP.17 Guidelines recommended by the American Thoracic Society18 were followed but without a practice trial.16 The 6MWT was expected to change as a function of exposure to an intense exercise program aimed at functional balance skills and endurance in standing.
The TUDS test assesses functional mobility by requiring participants to quickly walk up and down an 11-step flight of stairs. Children who are typically developing and 13 to 14 years old have been shown to average 0.52 sec/step on the TUDS.19 The TUDS is associated with the ability to be active in the community with higher demands on dynamic standing balance, coordination, strength, and anticipatory postural control. The TUDS has excellent reliability in school-aged children with CP and has been shown to be moderately correlated with the Timed Up and Go test.19 Each data point reflects the mean of 2 trials. The TUDS was expected to show change as the youth trained dynamic balance in single leg stance and control of postural sway while displacing their center of mass vertically.
Finally, the GMFM, a valid and reliable clinical measure of gross motor function in children with CP, has been shown to measure change over time.20 The GMFM Dimension E (walking, running, and jumping) has a minimum subset of 24 items for assessment of functional outcome in children with CP who are ambulatory.21 It has a possible total point score of 72, and allows a dimension percentage to be calculated.
The IP consisted of 90 minutes of VR-based balance training on 5 consecutive days. Daily interventions were delivered in two 45-minute sessions with a 30-minute rest break during which the participants engaged in a seated quiet activity of their choice. The VR-based balance training program was delivered using a commercially available system consisting of a 32-in widescreen LCD display, a high-performance computer, a video camera, and a green screen as background for computer-generated imaging (GestureTek Health, Toronto, Canada). Participants stood approximately 2.7 m from the screen display and had the ability to move within a space 2.2 m in width.
GestureTek's Interactive Rehabilitation and Exercise System software (IREX, version 1.4) immersed real-time video images of the participant into a 2D virtual world. The participants interacted with virtual objects to achieve tasks that had difficulty levels adjusted to the individual. Study participants were trained using 4 consecutive sets of 5 IREX applications in each of the two 45-minute daily training sessions. Applications lasted 2 minutes and were separated by a 10-second rest interval. Sets consisted of different combinations of applications of similar difficulty levels. The primary applications used were Soccer, Snowboard, Sharkbait, Zebra Crossing, and Gravball. Verbal guidance was provided if necessary to help participants understand task goals. As participants showed moderate degrees of success in movement abilities and game scores, the difficulty levels of the applications were progressively increased. The chosen IREX applications challenged dynamic standing balance, coordination and timing requiring participants to perform weight shifting in standing, single-leg stance, reaching away from the center of gravity, squats and jumps, side-lunges, side-steps, and gallops. Repeated, at times sustained, and unpredictable patterns of movement were elicited from the participant at increasing speed. The VR applications task descriptions and complex movements elicited are provided in the Appendix.
Guidelines recommended for rigorous analysis of SSRD were used.13 Before visual and statistical analyses can be analyzed, it is essential that baseline data from each participant in a single-subject design be analyzed for the presence of serial dependency. Serial dependency or autocorrelation refers to the fact that sequential measures or responses from the same individual are correlated with previous measures allowing for prediction of subsequent performance. Thus, serial dependency in a data set would suggest that change is due to repetition of the measure rather than implementation of an intervention. Serial dependency was determined on each outcome measure for each participant using a lag-1 autocorrelation.22 The autocorrelation coefficient was computed across the entire data series as 5 or fewer data points were present in each phase. Serial dependency was found for the TUDS for P1, P3, and P4 and for GMFM Dimension E for P2. For these data sets, the first difference transformation procedure was applied thus removing one data point22 and the autocorrelation coefficient was recalculated confirming elimination of the serial dependency. No serial dependency was found in the data for any of the participants for the CB&M or for the 6MWT.
Raw or, where appropriate, transformed data points for the CB&M, 6MWT, TUDS, and GMFM Dimension E were plotted for visual inspection using the same scale across participants. To allow for graphing of the transformed variables on the same scale, constants of 8 and 93 were added to the TUDS and GMFM-Dimension E data, respectively.22 Visual analysis of graphed data from adjacent phases was achieved by summarizing patterns of data on the basis of trend, level, and variability.23
Statistical analyses using the 2-SD band method complemented the visual analysis. Statistical significance was determined when 2 consecutive data points occurred outside the 2-SD band.23 If the values for the test scores at follow-up remained outside of the baseline 2-SD band, significant change was considered to be maintained.
Lastly, evidence of true change from the mean of the baseline was determined for the CB&M and 6MWT by computing the differences between the mean scores at baseline and the mean scores at intervention and follow-up. For the CB&M, a minimum change score of 5 points was used and is considered to correspond to true change in community integration and confidence in community mobility (JA Howe, personal communication, 2010). For the 6MWT, differences from the mean baseline scores were analyzed with respect to the minimum detectable change (MDC) value for GMFCS level I at an 80% confidence interval and used a standard error of measurement of 22.35, where MDC80 = 1.28 × √2 × SEM, for an MDC80 of 40.45 m.17
All adolescents completed all study phases and fully complied with the intervention. Baseline data stability was achieved for all outcome measures for each participant allowing for clear comparisons across the various phases. Data are graphed for each participant (Figures 1, 2, 3, and 4) for the CB&M, the 6MWT, the TUDS, and GMFM Dimension E.
Community Balance and Mobility Scale
Visual analysis revealed 2 patterns in the CB&M scores in response to the intervention. P1, P2, and P4 showed a gradual, consistent change evidenced by the accelerating trend throughout the IP. A more rapid response was seen in P3 with an immediate change in level and trend early in the intervention followed by small improvements throughout the IP. The CB&M gains maintained a stable level in the FUP. All participants showed statistically significant changes from the BP at both the IP and the FUP (Figure 1).
For the CB&M, true change from the mean of the baseline was achieved in the IP in 3 participants (P1: mean = 7.5, SD = 5.9; P2: mean = 5.5, SD = 3.4; P3: mean = 9.1, SD = 2.2), whereas P4 scores approached significance (mean = 4.6, SD = 1.7). In the FUP, improvements were maintained and true change was seen in all participants (P1: mean = 12, SD = 0.8; P2: mean = 10, SD = 0.8; P3: mean = 8.6, SD = 2.2; P4: mean = 7.1, SD = 2.5).
Six-Minute Walk Test
In P3, the 6MWT was characterized by a change in level identified as a change in the mean value from the baseline to the IP. In the remaining participants (P1, P2, and P4), an accelerating trend was seen in the IP that was most evident in the first few days and that leveled off in the last 2 days of intervention (Figure 2). In the FUP, the scores leveled off in P1 and P2 whereas P3 and P4 continued to improve. All participants showed statistically significant changes on the 6MWT in the IP, and these changes were maintained at follow-up. On the basis of the 6MWT MDC80 of 40.45 m, P3 (mean = 46.55 m, SD = 23.48 m) showed clinically significant change from baseline to the IP and the changes recorded for P2 (mean = 40.22 m, SD = 23.49 m) approached significance. Continued 6MWT improvements in the FUP led to achievement of clinically significant change in 3 participants (P2: mean = 46.58 m, SD = 13.60 m; P3; mean = 46.55 m, SD = 23.48 m, P4: mean = 43.46 m, SD = 14.31 m) and in P1 (mean = 39.96 m, SD = 8.44 m) the change approached significance.
Timed Up and Down Stairs
While the TUDS initially showed significant improvements, serial dependency was found in P1, P3, and P4. Once the data were transformed, these improvements disappeared and there were no changes in level and trend of the data for P1, P3, and P4 (Figure 3). However, P2, whose data were not autocorrelated, showed a change in level and slope on visual analysis and demonstrated significant improvements on the TUDS during IP (mean change = 1.3 s, SD = 1.23 s) as well as in the FUP (mean change = 2.61 s, SD = 0.36 s).
GMFM Dimension E
On GMFM Dimension E, participants scored a mean of 90% or higher in the BP and most, as expected, did not show significant changes (Figure 4). No change in level from the baseline to either the intervention or FUP was seen in any participant. An accelerating trend was demonstrated in P1 and P2 in the IP when compared to BP. Compared to the BP, P3 and P4 showed stable data in both IP and FUP. Only P1 demonstrated a small yet significant increase at the mid-point of the IP, which was maintained at follow-up.
We examined the effect of an intensive 5-day VR intervention on functional balance and mobility of adolescents with CP GMFCS level I. We hypothesized that complex balance and coordination skills in walking performance, walking speed and endurance, and stair climbing and descent would be improved in these children and that these improvements would be maintained at 1 week and 1 month following the end of training. Results from our study support 2 major findings. First, our data suggest that functional balance and mobility of 13- to 18-year-old adolescents with CP can improve with an intense, short duration VR intervention. Second, improvements in outcome measures are maintained for at least 1 month following the VR training. For all participants, a relationship was established between the VR intervention and the significant improvements on the CB&M and the 6MWT that was maintained in the FUP.
The true change found in the CB&M demonstrates that improvements in complex motor skills, specifically coordination, timing, and speed components required for ambulatory performance in community setting, were acquired and maintained for at least 1 month. The CB&M identified impairments in complex, coordinated responses and adaptable balance control and was responsive to change in these adolescents classified at GMFCS level I. Furthermore, the improvements in CB&M and 6MWT maintained in the FUP may indicate that high level balance, functional mobility skills and walking endurance acquired in training were integrated into everyday life.
The TUDS may not have shown the changes initially anticipated, as the complex movements elicited by the VR program applications did not specifically target forward translation combined with concentric and eccentric muscle control required for stair climbing and descent. Our VR program provided task-oriented training aimed at overground balance and ambulatory skills. Dimention E of the GMFM does not identify change in high-level walking coordination, speed, or timing components and demonstrates a ceiling effect for most youth classified at GMFCS level I. A Challenge Module is being developed as an adjunct to the GMFM to evaluate change in high level ambulatory skills in youth with CP classified at GMFCS level I.24 The piloted 20-item challenge module proposes to provide a comprehensive evaluative tool intended to address extent and accuracy of task completion as well as performance speed and will provide an opportunity to track improvements in abilities that contribute to youths' participation in school and community activities. Children classified at GMFCS level I are reported to have achieved 90% of their expected limit of gross motor skill acquisition by 4.8 years of age (50% range 4.0-5.8 y)25 and follow a stable limit model into adolescence based on the GMFM-66.4 However, our findings demonstrate that it is possible to alter the natural history of CP in adolescents classified at GMFCS level I. Our study builds on findings from Woollacott et al,6 who showed significant improvements in recovery of stability in children with CP classified at GMFCS levels I and II following a 5-day intervention of massed practice on a moveable platform. However, it is unknown to what extent the specificity of training on moveable force plate system in response to an external threat to stability can generalize to other types of training or to functional balance challenges. Our data clearly demonstrate that the training experienced using our program of GestureTek's IREX applications results in changes on outcome measures that relate to changes in community integration and mobility. In a clinical setting, this model of intervention lends itself well to training programs during youths' summer holidays or school breaks. The participants did not express fatigue and remained motivated for the entire intervention period. Further studies will be required to determine whether a longer intervention period would demonstrate greater changes.
Burtner et al26 has reported that, both in laboratory and in clinical settings, it is essential to fully challenge the balance abilities of children with CP to optimize their level of motor capacity for recovery. Our overground VR balance training program using IREX allowed the clinician to set the movement challenge to meet the individual's capacity. This was clearly a benefit for our participants whose mean CB&M baseline scores ranged from 44.0 to 66.3, indicating the need for distinct challenge levels. Our VR program required the participants to practice different movement sequences repeatedly with unexpected changes in direction, speed, and contexts within the VE. Our individualized intensive protocol progressively increased the frequency, the magnitude, and the speed of balance demands. Repetition has been shown to be an important aspect of a task and is crucial in improving performance; the repetitive practice provided by VR program thus enabled the nervous system to build on previous attempts and coordinate new muscular synergies to accomplish the task goal.
Task-oriented training strategies with greater intensity and complexity of practice show the strongest level of evidence for functional change and now constitute major trends in physical therapy treatment.27 Body weight–supported treadmill training, high intensity practice of a lower extremity task, has resulted in improvements in short distance walking speed as shown by the 10-Meter Walking Velocity test in children with CP classified at GMFCS level I.7 However, in contrast to our study, only half of the children studied showed improvements in performance on the 6MWT. Whereas treadmill training facilitates a limited motor behavior of forward progression, our intensive VR program focused on the multiple contributing factors of motor performance by addressing balance, coordination, strength, endurance, and perceptual-motor skill to produce the best functional outcomes.28 The VR program addressed the critical factors for motor training: the intensity, repetition, task-focused, and multisensory environments. Enriched environments are known to promote neuronal plasticity and functional recovery following traumatic brain injury8 and changes documented using functional magnetic resonance imaging have shown that training in a VE offers potential for long-term learning as evidenced by adaptive cerebral plasticity consistent with significant functional motor improvements in CP.29
A multiple-baseline, single-subject research design (A-B-A) was chosen to best inform and guide clinical practice by showing individual differences and demonstrating treatment effectiveness with a small group of adolescents with CP while ensuring rigorous guidelines for this quasi-experimental study. We used a single-subject MBD to strengthen internal validity, as participants were exposed to standardized experimental conditions in every phase of the design. Romeiser Logan et al13 developed 14 quality questions to evaluate the rigor of SSRD. It was determined that a methodologically strong SSRD required a total of 11 to 14 points. The evaluation of the current study study using this method generated a score of 12 points suggesting a strong methodology. The VR program involved a replicable protocol with defined sequences of IREX applications with progressive increases in levels of difficulty. None of the participants received concurrent interventions, and external factors were limited due to the short intensive nature of this study. Data were rigorously analyzed using visual analysis, statistical analysis, and determination of clinical significance where possible. Finally, the effects of the intervention were replicated across all participants. Concurrency in the MBD was not possible because of the intensive nature of this study and the availability of the VR system. Finally, we chose to observe changes following a 5-day intervention, while subsequent work may examine the effect of longer periods of treatment and longer-term retention of improvements in functional balance and mobility. The primary limitation of our study was that the outcome assessor was aware of the phase of the study in which the participant was involved.
Functional balance and mobility are necessary for safe performance of everyday tasks, yet are significant problems contributing to participation restrictions in adolescents with CP. Intervention programs in youth with CP need to address impaired balance as a contributor to functional limitations in order to improve motor performance and participation in sports and physical activity with peers. The changes recorded on the CB&M and 6MWT suggest refinement of coordination, timing, and speed of high-level balance skills as well as improvements in walking endurance needed for community participation.
This study has important clinical implications for therapists, as it contributes to the evidence that high-level balance skills and functional mobility are modifiable in ambulatory adolescents with CP classified at GMFCS level I and that these adolescents respond to short duration, high intensity VR training and have the ability to enhance their repertoire of movement strategies. This new intervention tool improves motor performance and may promote the adaptive changes, which facilitate neuroplasticity in these adolescents.
Further investigation is necessary to examine the effectiveness of different training protocols for intense VR interventions with children in younger age groups, with distinct types of CP and in different GMFCS levels. Moreover, additional research is needed to determine the intensity, frequency, and duration of the VR intervention required to best affect functional balance and mobility in children and adolescents with CP.
The Ottawa Children's Treatment Center provided the facilities and equipment for this study. The authors thank Veronica Patterson, physiotherapist, who provided the data collection and Shannon Thériault, physiotherapy assistant, who participated in the delivery of the intervention program. The authors thank the adolescents and their families for their participation in this study.
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