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Effects of Combined Exercise Training on Functional Performance in Children With Cerebral Palsy

A Randomized-Controlled Study

Peungsuwan, Punnee PhD; Parasin, Pattamavadee MSc; Siritaratiwat, Wantana PhD; Prasertnu, Jilada BSc; Yamauchi, Junichiro PhD

doi: 10.1097/PEP.0000000000000338
RESEARCH REPORTS
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Purpose: The purpose of this study was to investigate the effects of combined exercise training on functional performance in participants with cerebral palsy.

Methods: Fifteen participants with spastic cerebral palsy were randomly allocated into either exercise or control groups. Participants in the exercise group participated in a combined strength and endurance training program for 70 minutes per day, 3 days per week, for 8 weeks, whereas those in the control group did not participate in an exercise program. Study participants in both groups continued with their regular physical therapy during the study.

Results: After the 8-week training, a 6-minute walk, 30-second sit-to-stand, 10-m walk, and Functional Reach Tests, participants in the exercise group had significant improvement over their baseline values and were significantly higher than those in the control group.

Conclusions: Combined exercise training improved walking ability, functional lower limb strength, and balance in participants with cerebral palsy.

The purpose of this study was to investigate the effects of combined exercise training on functional performance in children with cerebral palsy.

Research Center in Back, Neck, Other Joint Pain and Human Performance (BNOJPH), Khon Kaen University, Thailand (Drs Peungsuwan, Siritaratiwat, and Yamauchi); School of Physical Therapy, Faculty of Associated Medical Sciences, Khon Kaen University, Thailand (Drs Peungsuwan and Siritaratiwat); Physical Therapy Department, Faculty of Allied Health Sciences, University of Phayao, Thailand (Ms Parasin); Srisangwan Khon Kaen Special School, Thailand (Ms Prasertnu); Graduate School of Human Health Sciences, Tokyo Metropolitan University, Japan (Dr Yamauchi); Future Institute for Sport Sciences, Tokyo, Japan (Dr Yamauchi).

Correspondence: Punnee Peungsuwan, PhD, School of Physical Therapy, Faculty of Associated Medical Sciences, Khon Kaen University, 123 Mittraphap Highway, Muang District, Khon Kaen Province 40002, Thailand (ppunne@kku.ac.th).

The authors declare no conflicts of interest.

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INTRODUCTION

Participants with cerebral palsy (CP) have a group of disorders affecting the development of movement and posture, causing activity limitation, that are attributed to nonprogressive disturbances in the developing fetal or infant brain.1 Regardless of the type of CP, participants with CP have lowered physical fitness levels because their motor impairments restrict their participation in daily physical activities.2,3 This inactivity in participants with CP further causes a loss of neuromuscular function in physical performance, which includes decreases in muscular strength.4 These losses of neuromuscular functions in participants with CP can be prevented and improved through exercise training. Strength training can increase muscular strength in association with improvements of functional activities,5–9 whereas endurance training improves aerobic fitness in participants with CP.10,11 Both strength and endurance exercise training become increasingly demanding in participants with CP. The adaptive responses in skeletal muscle to endurance training are different and sometimes opposite from those of strength training. For example, strength training may cause muscle fiber hypertrophy and a decrease in both capillary density and mitochondrial volume density, whereas endurance training may cause an increase in capillary density, mitochondrial volume density, and oxidative enzyme activity. Concurrent endurance and strength training may result in an antagonism of the training response.12 This antagonism of concurrent strength and endurance training may rely on training design variables and the interaction of these variables, including the training status of the trainees and the training modes.13–15 Accordingly, appropriate training programs play a role in developing specific motor abilities. Exercise training programs should be closely related to the functional activities of daily living such as a knee-hip extension exercise (squat).16 Because many of our daily living activities require muscle strength and aerobic endurance, a functional exercise program with combined strength and endurance training should be a better way to improve physical function for participants with CP. The literature supports including both strength and endurance training exercises for participants and with cerebral palsy.17 Therefore, a concurrent lower-body strength and endurance training may be an effective way to enhance both lower-body strength in neuromuscular learning and cardiorespiratory functions, consequently improving motor function and health-related quality of life (HRQOL) scores. It is important to understand how exercise training combined with strength and endurance exercises in participants with CP affects muscle functions that relate to daily activity; however, no studies have shown the effects of a functionally related combined strength and endurance exercise program on functional performance in participants with CP. The aim of this study was to investigate the effect of a functionally related combined strength and endurance exercise program on walking ability, lower limb strength, balance, and flexibility in participants with CP. We hypothesized that a combined strength and endurance exercise program would have a positive effect on muscle functions that are related to daily activities for participants with CP.

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METHODS

Study Design

A randomized controlled trial was conducted at a special education school for participants with disabilities. The local ethics committee for human research approved the study. Participants with CP were randomly allocated into an exercise group (EX) or a control group (CON) by computer. They were stratified according to sex, age, and the Gross Motor Function Classification System (GMFCS) levels (I to III). The 2 examiners were masked to the groups when performing assessments and data analysis. Assessments were performed at baseline and after the 8-week training program.

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Participants

Thirty participants and, who could walk with either hemiplegic or diplegic CP, with GMFCS levels from I to III, were enrolled in and screened for this study. Eighteen participants with CP aged 7 to 16 years met the inclusion criteria. The inclusion criteria were the ability to perform the exercise training program and outcome tests and to understand verbal instructions. The exclusion criteria included receiving botulinum toxin injections or surgical procedures for spasticity treatment within the 3 months prior to the intervention, including serious medical conditions in which a physician suggested that exercise was contraindicated; performing other exercise programs within the previous 4 months; and having muscle contractures that limited movements of the lower limbs. Participants were screened for these criteria using passive movements and pretesting of each test criterion. Three participants were excluded from the study. One participant refused to enter the program because he had to go home after school, and 2 participants could not perform the exercises because they were unwilling or unable. Fifteen participants with hemiplegic or diplegic CP completed the study, which included CON (n = 7) and EX (n = 8) groups. Most of the participants resided at the boarding school. Demographics and classification of participants, baseline age (CON, 13 ± 4.16; EX, 13.5 ± 3.3 years), height (CON, 1.39 ± 0.15; EX, 1.38 ± 0.16 m), and body mass (CON, 36.29 ± 12.99; EX, 37.63 ± 11.07 kg), which were not significantly different between groups (P > .05), are shown in Table 1. There were 2 participants with hemiplegia in each group, and 5 and 6 participants with diplegia in the CON and EX groups, respectively. There were 2, 4, and 1 participants at GMFCS levels I, II, and III, respectively, included in the CON group, and 2, 4, and 2 participants in the EX group, respectively. Most of the participants had spastic diplegia and were classified as GMFCS-E&R level II and III. Three participants were without aids in each group and 4 and 5 participants with aids in the CON and EX groups, respectively. Figure 1 is a flow chart of participants through the trial and data analysis. One participant was lost to follow-up at the final testing of outcomes. Data were analyzed using the principle of intention to treat. Missing data were replaced using the last observation carried forward method.18 Details of the testing procedure and parental consent forms were explained to the parents or guardians prior to the onset of the study, and informed consent was obtained from all participants and their parents or guardians.

Fig. 1

Fig. 1

TABLE 1

TABLE 1

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Procedures

The EX group received a functional exercise program that included a combined strength and endurance training program for 8 weeks, whereas the CON group did not receive this exercise program. EX participants trained after school classes. The exercise training program consisted of functional strength and endurance training, which was designed by pediatric physical therapists as a group circuit. A functionally based exercise program was performed using simple equipment including leg stationary bicycles and elliptical machines (Figure 2). Prior to exercise, the participants had warm-up and cool-down periods with self-muscle stretching of the hip external rotator and abductor muscles, knee extensor and flexor muscles, and calf muscles. The total 70-minute exercise program consisted of a 5-minute warm-up period, 60 minutes of circuit exercises, and a 5-minute cool-down period. This 3 days per week training program was supervised by a physical therapist. Music was used to motivate participants. Both the EX and CON groups continued their physical therapy (PT) program for 1 session per week. A physical therapist from a special school determined the appropriate PT program for the participants. The PT program consisted of passive leg muscle stretching, upper limb activity in groups, sitting or standing ball throwing, handiwork, and a leisurely walk or playing for 1 hour during school hours. This physical therapist was also masked to each group. After school, the CON group had leisure time while we monitored their varied activities. They often had physical inactivity such as talking and playing with each other.

Fig. 2

Fig. 2

Functional strength training consisted of a sit-to-stand (STS) and a step up-down (SUD) activity. Each participant performed the standard protocols of the STS.19 For STS, each participant sat with hip flexion at 90°, knee flexion at 105°, ankle dorsiflexion at 15°, and feet flat on the floor. Most participants folded their arms over the chest, but participants who used assistive devices were permitted to use a stall bar. They were instructed to stand up at a comfortable speed without swinging their arms or moving their feet. Repetitions were counted each time their legs and hips were within 15° of the extended position. For SUD, participants stood in front of a step 17 cm in height for the starting position and moved up and down at a self-paced speed. During practice, the participants were allowed to hold the handrail if they felt unstable. Repetitions were counted when their legs returned to the starting position. In the first week of exercise training, the participants performed STS and SUD with free load for 8 to 10 repetitions per set, 3 to 5 sets per day, with 3 minutes' rest between sets. They were subsequently asked to wear a weighted vest. These weights were initially added in the second week as 30% of body weight, and afterward the progressive resistance was adjusted from 50% to 60% to 60% to 70% of 1-repetition maximum STS every 2 weeks.

Endurance training was performed on cycling and stepping machines in a circuit. The 3 stations for endurance training included (1) leg stationary bicycles, (2) elliptical machines, and (3) recreational fast walking or running. For leg cycling, participants initially sat on the saddle with a knee flexion of 30° to 35° and performed cycling with a self-selected speed and load. For the elliptical machine, the participants stood on the pedals, grabbed the handlebars, and pedaled their feet while pushing the handlebars alternately forward while stepping. For walking or running, each participant was asked to walk as fast as possible, or run in a race by picking up a ball from a basket and putting the ball in another basket placed 20 m away. Each participant continuously exercised on the leg stationary bicycles and elliptical machines for 15 minutes per session, and recreational fast walking or running was performed for 10 minutes, with a 5-minute rest between stations. Total exercise time was 40 minutes for the 3 exercise stations. Each participant was encouraged to perform the program to the end of the period. If the participants wanted to rest, they could stop. During the endurance exercises, the participants' heart rates were maintained at 65% to 85% of their maximum heart rate as determined with a heart rate monitor (FT4, Polar, Kempele, Finland). Maximum heart rate was defined as equal to 220 minus age of each participant.

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Outcome Measures

Physical performance was evaluated using the 6-minute walk test (6MWT), 30-second sit-to-stand test (30sSTST), 10-m walk test (10mWT), Timed Up and Go test (TUGT), and a Functional Reach Test (FRT). All outcome measures have been shown to have high to very high levels of test-retest reliability.17–21 To determine the consistency of each measure, assessors evaluated the intratester reliability of variables. Outcomes were measured 1 week before the start of the program and within a week after the conclusion of the exercise program. All participants wore shoes and could use walking assistive devices during the tests if needed, and they were allowed to rest between testing for 3 to 10 minutes, or as required. All participants completed all outcomes.

6MWT is a measure used to assess functional cardiorespiratory capacity.16 The test-retest reliability is very high.20 A 40-m square course was replicated indoors. A 1-m wide walkway was designated with traffic cones and ropes between the 4 inside and outside corners of the course. Masking tape was placed at 2-m intervals along the route. The patients were instructed to walk as far as they could within 6 minutes. They were allowed to slow down or stop as necessary, and when they had to stop for rest, the duration of the rest period was recorded. The participants were given encouragement to do the test when examiners found that they did not try to walk continuously. The distance walked was recorded after the test.

30sSTST is a measurement of functional lower limb muscle strength and performance with a high test-retest reliability.21 30sSTST measured the number of repetitions for a sit-to-stand task within a 30-second period. Each participant sat on a chair without a backrest or armrest with feet flat on the ground, and hips and knees flexed at 90° and 105°, respectively. The examiner instructed the participant to repetitively move from the sitting to standing position as many times as they could within a 30-second period without using arms for support. Two participants who used walkers were allowed to use their support tool when their hips were extended at the end range. Repetitions of a sit-to-stand task were counted when their hips extended beyond 75°from sitting to standing.

10mWT is a measure to assess walking speed. 10mWT has a high test-retest reliability,21 and this test is correlated with gross motor functions for participants with CP.22,23 The test was conducted on a 14-m walkway that included 2 m at the start and end points to allow for acceleration and deceleration. Before the test, the examiner instructed, “Please walk towards the end, at your usual speed.” When the participant was given the cue “ready and go,” they walked toward the end of the walkway. The examiner started a timer when the participant's first foot crossed the plane of the 2-m line and stopped the timer when the first foot crossed the plane of the 12-m line. During the test, an examiner walked beside the participant and encouraged him/her to continue walking. The time to reach the middle of the 10-m walk was recorded for walking speed calculations.23,24

TUGT is a measure used to assess functional dynamic balance that has good test-retest reliability.24,25 Participants sat in an adjustable-height chair with no backrest or armrest. The height of the seat was adjusted such that both knee and hip flexion were 90° while sitting with the feet resting on the floor. None of participants wore shoes or orthoses, and participants with level III were allowed to use walking devices for the test. During the test, the participant stood up from an adjustable-height chair, walked a distance of 3 m, turned around a mark, walked back to the chair, and sat down again. Time was recorded from the “go” until the participant sat down in the chair. Each participant performed the test 3 times. The best time was recorded in seconds.25

FRT is a clinical measure of balance developed by Duncan et al26 that has excellent reliability.27 This study followed standard protocol.26 FRT measures the distance between the length of the arm and a maximal forward reach in the standing position. Participants were instructed to stand close to a wall (not wearing shoes or socks), but not touching the wall, with the dominant side arm position set at the zero mark of the stick, which was placed on a measuring stick against the wall at the height of the participants' acromion. The participants were asked to extend their arms to 90° of shoulder flexion. The assessor recorded the starting position at the third metacarpal head on the yardstick and instructed the participants to “reach as far as you can forward without taking a step.” The location of the third metacarpal was then recorded. The difference between the start and end positions was the reach distance. The test was repeated 3 times with 5-second rest intervals between each test, and the results were recorded and averaged for data analysis.

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Data Analysis

All data are presented as a mean (standard deviation). The distribution of the data was examined with the Shapiro-Wilk test for the assumption of normality. All data for 6MWT, 30sSTST, 10mWT, TUGT, and FRT were normally distributed. The difference between pre- and posttest for each outcome was analyzed with a paired t test. An analysis of covariance compared differences between adjusted posttest means between the 2 groups; the pretest means were used as covariates. The baseline differences of each outcome were analyzed using an independent t test. The individual training effect was further analyzed for the relationships of magnitude of change between 6MWT and other variables after the training using Pearson's correlation coefficient test. The power of the test was 0.8 and the level of significance was set at P < .05. The reliability of each tool was tested by 2 assessors using the test-retest intraclass correlation coefficient and Bland-Altman analyses.

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RESULTS

Table 2 has the comparison outcomes within and between EX and CON. The intraclass correlation coefficients of the intrareliability of 6MWT, 30sSTST, 10mWT, TUGT, and FRT were 0.99, 0.97, 0.93, 0.99, and 0.75, respectively. The baseline scores of outcome variables were not significantly different between the groups. After the 8-week intervention, outcomes significantly improved in EX, except TUGT, but outcomes did not change in CON compared with the baseline scores. The adjusted postmean of EX and CON for each outcome was compared; the 6MWT, 30sSTST, 10mWT, and FRT in EX were significantly different in comparison with the CON means. TUGT was not significantly different between groups. Changes in 6MWT were positively correlated with 10mWT (r = 0.8, P < .001) but not with 30sSTST or FRT.

TABLE 2

TABLE 2

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DISCUSSION

This study supported positive effects of a combined exercise training program on walking endurance (6MWT), walking speed (10mWT), leg muscle strength (30sSTST), and physical balance (FRT) for participants with CP. The task-specific exercise program designed to imitate functional mobility, such as sitting-to-standing with extra load, progressive step-up and step-down, walking and running, resulted in improved physical performance tests. Stationary cycling exercise improved respiratory and cardiovascular capacity and elliptical machine exercise reduced muscle tightness and increased range of motion of joints, which increases step length and speed and leg muscle strength and physical balance. The importance of muscle strength for participants with CP can be seen in the direct relation between strength and motor function. Participants with stronger knee extensors can walk faster.8 These results support previous research supporting improvement of muscle strength and physical fitness and HRQOL scores in participants with CP after exercise training.28,29

Our combined functional strength and endurance exercise program supported an increase in muscle strength associated with improvements of functional activities similar to the results of strength training alone.5,6,7–9 Despite the antagonism of concurrent training previously described in healthy people,30 it may be possible to integrate resistance and endurance training regimens for positive effects on physical performance.31,32 Increased muscle strength after the exercise training had a positive influence on activities of daily living in participants with CP. Many participants with CP experience difficulty when moving their bodies quickly or standing up from a chair. These disabilities are predictive of falls and subsequent disability. Increases in leg muscle strength support bodyweight during those movements.

Appropriate exercise and regular participation in activities are important goals for therapeutic interventions in participants with CP, and feasibility and reproducibility of the program are important factors in a clinical setting and after the school day. This study had 70-min/session durations and a frequencies of 3 sessions per week for 8 weeks, with a total of 3.5 hours per week of exercise. The exercise sessions were supervised by a physical therapist. Although the frequency, intensity, time, and type of exercise for health and fitness benefits in participants with CP are unknown, the design of an exercise training program could be based on the same principles as those for the general population. The findings of this study suggest that because a combined functional strength and endurance exercise program with supervision by a physical therapist elicits beneficial effects for physical functional ability in participants with CP, this program could be an alternative treatment in both clinical and school settings.

Our results did not show improvement in the TUGT because our exercise program did not include specific balance training. During the TUGT measurements, participants with CP had difficulty turning around while walking quickly because of limited balance or agility. Participants with CP have less ability to maintain their postural control during physical performance.25,29 Moreover, participants with spastic CP often have cocontractions of the distal and proximal muscles and do not have a smooth distal-to-proximal patterns of muscle activity.33

A limitation of the study was the lack of outcome measures across the World Health Organization International Classification of Functioning, Disability and Health. Because HRQOL is an important outcome of treatment for participant with CP, a long-term exercise training program is needed to maintain their fitness levels and HRQOL. Because it seems to be difficult for participants with CP to maintain their fitness level after an exercise program, future studies are needed to determine the clinical efficacy of a combined functional strength and endurance exercise program over the long term in participants with CP. Another limitation was the small sample of participants with CP. The study might be underpowered for some results, and thus a replication study with a larger sample is necessary before the results could be considered more than preliminary. Despite these limitations, our findings may contribute to the advancement of the general understanding of a combined functional strength and endurance exercise program for participants with CP.

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CONCLUSIONS

This study provides evidence that an 8-week combined functional strength and endurance exercise program carried out as a group circuit can be an effective and feasible strategy for improving motor function, such as walking performance and leg muscle strength, in participants with CP. This study suggests that a concurrent lower body strength and endurance training program may provide positive adaptations in cardiorespiratory and motor function for physical activities of daily living and may lead to improvement of HRQOL in participants with CP.

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ACKNOWLEDGMENTS

The authors would like to thank all who participated in this study. The study was supported by the Research Center of the Back, Neck, Other Joint Pain and Human Performance, Faculty of Associated Medical Sciences, Khon Kaen University, Thailand. Additional thanks to Srisangwan, Khon Kaen Special School, for the location and equipment that was used in this study.

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Keywords:

combined strength and endurance training; exercise training intervention; flexibility; leg strength; walking ability

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