UNNITHAN, VISWANATH B.1; KATSIMANIS, GEORGE2; EVANGELINOU, CHRISTINA2; KOSMAS, CHRISTOULAS2; KANDRALI, IFIGENIA2; KELLIS, ELEFTHERIOS2
Cerebral palsy (CP) is considered a nonprogressive, neurodevelopmental disorder (26) characterized by an increased latency of onset of movement, poor temporal and spatial organization of muscles and joints, inadequate muscle force production, hypertonus, and excessive agonist/antagonist cocontraction. Spastic diplegia is the most common subtype of CP and preferentially affects lower rather than the upper extremities (26).
It has been documented that children with CP have an oxygen cost of walking that is approximately three times that seen in able-bodied children (27). The underpinning physiological mechanisms that have been associated with this high oxygen cost (poor walking economy) have been high levels of both muscle coactivation (27) and total-body mechanical power (28). Poor walking economy in children with CP has been linked to the early onset of fatigue (5). The physiological basis for this early onset of fatigue has been hypothesized to be related to the higher relative exercise intensity during locomotion and the concomitant reduced metabolic reserve (27). The capacity to improve economy and potentially ameliorate fatigue through training in children with CP has yet to be fully investigated. There is, however, evidence from the adult literature to suggest that a combined strength and endurance training program will improve running economy in healthy adult runners (20,23).
Several studies have used strength training alone to try and reduce the submaximal energy cost of locomotion in children with CP. The findings from these training studies have demonstrated no impact on the submaximal energy cost of movement (7,8,15). The major limitation associated with these studies was the use of surrogate measures of oxygen uptake such as the energy expenditure index. There is a paucity of well-designed aerobic training studies in children with CP. Van Den Berg-Emons et al. (30) have demonstrated that a 9-month aerobic training program (4× wk−1) resulted in a 35% improvement in peak V˙O2. Furthermore, Bar-Or et al. (1) have demonstrated an 8% improvement in arm-cranking peak V˙O2 after a twice-weekly sports program for a period of 2 yr. In this latter study, however, there were no improvements in arm-cranking economy as a result of this training.
Two mechanisms have been postulated to be responsible for the improvements in running economy seen in the adult literature after strength training. For an equivalent level of muscle tension, type II motor units are preferentially recruited at lower gait cycle frequencies, when the force required at each cycle is higher. If stride frequency remains unaltered, evidence from the literature suggests that improvements in maximal strength can lead to a lower relative peak tension for a given stride frequency (lower percent maximal force) and, therefore, an increased contribution of type I compared with type II motor units with a concomitant increase in slow-twitch fiber recruitment. This altered motor unit recruitment strategy has been linked to improved running economy in the adult literature (11,20). Improvements in running economy as a result of strength training have also been linked to increased storage of elastic energy and, therefore, improved energy conservation; titin has also been postulated to influence the elastic characteristics of muscle fibers and has been implicated with enhanced running economy (9,20). The lack of improvement in economy as a result of single-specificity training (strength or aerobic) in children with CP, and the evidence from the adult literature (20), suggest that a combined strength and aerobic training protocol in children with CP could be effective in improving economy in children with CP.
Consequently, the aim of this study was to evaluate the effect of a 12-wk combined aerobic interval and strength training program on 1) arm-cranking economy, 2) peak V˙O2, and 3) gross motor function skills in a group of spastic diplegic children with CP.
All subjects attended a local rehabilitation center (Center of Education and Rehabilitation of Children with CP (CERCP)). The inclusion criteria were that each subject a) had been diagnosed as a spastic diplegic by a medical practitioner, using the traditional taxonomy; b) was able to walk, with or without walking aids; c) was aged between 14 and 18 yr; d) had not been subject to any orthopedic surgical operation and had not received any botulinum toxin injections for the treatment of spasticity in the year preceding the start of the study; and e) attended a similar physical therapy program that did not include any form of systematic exercise. There was no evidence of abduction and internal rotation of the shoulder in the individuals with CP who participated in this study.
Seventeen subjects were assessed for their eligibility to participate in the study. Four were excluded for failing to meet the inclusion criteria. The remaining 13 individuals fulfilled the above criteria and agreed to participate in the study. The subjects were recruited on a staggered basis during a 6-month period and, therefore, were randomly allocated into either the training group (N = 7) or control group (N = 6) on the basis of the timing of their recruitment into the study. The training group consisted of seven participants (five females, two males; mean age 15.9 yr, range 14-18 yr). The control group consisted of six participants (four females, two males; mean age 15.7 yr, range 14-17 yr). All participants (training and control) maintained their normal physical therapy regimen for the duration of the study; this consisted of an individualized physical therapy program, twice a week, of 45-min duration for each session. Each session was carried out by an experienced physical therapist and was based on the neurodevelopmental/Bobath treatment philosophy (3). Stature was measured while the child was in a supine position, stabilized by a researcher. Body mass was obtained from calibrated electronic scales (Seca, Hamburg, Germany).
All participants were ambulatory, but motor ability ranged from functional walkers (two in the training group and two in the control group) to individuals who always required walking aids (anterior walkers) and used a wheelchair regularly. The Gross Motor Function Classification System (24) levels of the subjects were classified as II (walks without assistive mobility devices) and III (walks with assistive mobility devices; limitation walking outdoors and in the community). Similar ambulatory function was present in both the training group and the control group. None of the children wore orthoses (Table 1). Verbal assent was obtained from the participant, and written informed consent was obtained from the parent/guardian before the start of the training program. Ethical approval was given by a local university ethics committee. Furthermore, permission was also obtained from the director of secondary education and the school headmaster at the CERCP. The CERCP psychologist was also consulted before the initiation of the project.
Two measurement sessions were performed on all subjects, before (baseline) and immediately after the 12-wk training period. All subjects were randomly allocated into either the training group or control group on the basis of their timing of recruitment into the study. The Gross Motor Function Measures (GMFM) measurements were conducted by a researcher (G.K.) familiar with the measurement procedure. This researcher was aware of which group each CP participant belonged to, and this assessment was conducted without walking aids. The same researcher evaluated the subjects before and after the training period. One week before the start of the study, all subjects underwent a thorough familiarization with the equipment. All participants were allowed to practice on the arm ergometer at the rehabilitation center for a period of 1 wk for 15 min·d−1. The duration of the practice time and the level of encouragement was standardized for all subjects. All subjects practiced at the submaximal power output that they would experience during the baseline testing session.
For the submaximal and peak exercise testing, an arm-crank ergometer was used (Monark, Rehab. Trainer 881 E, Stockholm, Sweden). The radius of the handles of the arm ergometer was 16 cm. The height of the seat was set to allow each subject to place his/her feet on the floor. Hips, knees, and ankles were flexed to 90°. The backrest was almost vertical. A chest strap held the subject in the seat. Subjects were given detailed instructions to use only the upper-body muscles. The center of the handles was adjusted at shoulder height for each subject when he or she was sitting straight. The distance and angle between the seat and the handle were adjusted for each subject, so that the subject could use the whole span of the arm from the shoulder to the palm to execute the arm-cranking test. When the handle was furthest from the subject, the shoulder and elbow were flexed approximately 90 and 0°, respectively. These distances and angles were registered during the first visit, and the same experimental set-up was used in the posttraining testing session.
The major reason that an arm ergometer was chosen as the primary aerobic exercise test can be linked to the data seen in Table 1. Five of the seven subjects used a wheelchair sometimes or quite often as part of their activities of daily living. Furthermore, five of the seven subjects used anterior walkers as their primary walking aid. Previous research by Unnithan et al. (29) calculated the approximate proportion of body weight that is supported by the upper body when using anterior or posterior walkers. This ranged from 8 to 52%. Consequently, a significant proportion of body weight can be supported by the upper-body musculature during their normal activities of daily living; a decision, therefore, was made to use an arm ergometer to assess submaximal and peak V˙O2 in the present study. A further rationale for the selection of the arm ergometer is that the high levels of coactivation noted in the upper and lower legs of children and adolescents with CP make a single independent leg revolution hard to execute for these individuals (16). The treadmill is very challenging, and the validity of the data can be compromised at times by the participant holding on to the treadmill support bars. Therefore, although the arm ergometer is still a difficult test for an individual with CP to accomplish, it was the only viable option for this group of subjects.
Submaximal and peak exercise testing.
After a 3-min warm-up (arm cranking without resistance at 50 rpm), the initial workload was applied. A 4-min submaximal workload (16) was selected to achieve cardiorespiratory steady state (power output of 2.5 W at 50 rpm). The cadence for arm cranking was maintained at 50 rpm using a metronome; while the subjects could also view the cadence on a liquid crystal display, the subjects were verbally prompted to maintain their cadence within ± 5 rpm of the stated cadence. A 4-min, submaximal exercise stage has previously been used in paraplegic subjects to achieve cardiorespiratory steady state without provoking undue fatigue (29). Fifteen-second V˙O2 measurements from minute 3 to 4 of the arm-cranking test were averaged and considered as an index of steady-state, submaximal cardiorespiratory measurements. After the initial load of 2.5 W for the first 4 min, the workload was increased at a rate of 2.5 W per min until volitional exhaustion, with the cadence maintained at 50 rpm. Five minutes after the cessation of exercise, blood samples were drawn from a fingertip. A single, 5-min, postexercise collection time was used as the optimal time needed to detect peak lactate levels. The determination was made by means of reflectance photometry (Accutrend Softclix, Boehringer Mannheim, Germany); the calibration took place according to the instructions of the manufacturer.
Oxygen uptake was determined during exercise using open-circuit spirometry (Jaeger EOS- Spring oxygen analyzer, Erich Jaeger GmbH and Co. KG, Wurzburg, Germany). For the calibration of the volume sensor in the analyzer, a 2-L syringe was used, and for the calibration of the gas analyzers, a gas of known concentration was used (O2: 15.39%; CO2: 6.19%). Because children with CP can have poor oral control, leading to excess saliva in the mouthpiece and valve used to collect the expired gases, a saliva pump was used to clear saliva from both (26). Heart rate (HR) was monitored continuously by means of an electrocardiograph (PPG-HELLIGE GMBH, Freiburg, Germany). All measurements took place at approximately the same time of the day before and after the 12-wk training period.
The main criterion for attainment of V˙O2max was considered a plateau in oxygen consumption (V˙O2plateau) at the end of the test. Secondary criteria for the attainment of V˙O2max included (i) HR values within 10 bpm of the age-predicted maximum, and (ii) a respiratory exchange ratio (RER) greater than 1.1. In the absence of the main or secondary criteria, this point of maximal exertion was termed V˙O2peak (18). Submaximal and peak oxygen uptake (V˙O2peak), ventilation (V˙E), HR, RER, and blood lactate (La) were measured. The ratio of submaximal V˙O2/V˙O2peak (fractional utilization) was subsequently calculated.
The GMFM test is a validated test instrument designed to assess motor status in CP (21). Interrater (0.88) and intrarater reliability (0.68) has been established (24). It consists of 88 items within five dimensions: (A) lying and rolling, (B) sitting, (C) crawling and kneeling, (D) standing, and (E) walking, running, and jumping. Each GMFM item was scored on a four-point Likert scale (0-3). Values of 0, 1, 2, and 3 were assigned to each of the four categories: 0 = could not initiate task; 1 = initiated task (< 10% of task); 2 = partially completed task (10 to < 100% of task); and 3 = completed task (100%). Participants were asked to attempt each of the items up to three times without using any assistive devices. Scores are presented as percentages. Separate scores were calculated for each of the five dimensions as well as for the total score. In this study, only dimensions D and E were assessed. These dimensions were chosen because a) they represent areas that many children and adolescents with spastic diplegic CP have difficulty with, and b) our objective was to evaluate changes in motor function while walking.
The training group trained three times a week for 12 wk. Each session lasted approximately 70 min and started with a warm-up (10 min) that included walking for 4 min (with or without an anterior walker). After this aerobic warm-up, a strength training warm-up (3 min) was initiated, using body weight as the primary resistance. Five sets of 10 repetitions that included elbow flexion and extension, shoulder abduction, flexion, extension, and internal and external rotation were conducted for the upper body. Lower-leg exercises focused on the hip flexors, knee extensors and flexors, and the ankle dorsi and plantar flexors. The warm-up concluded (3 min) with passive stretching of the arm, hip, knee, and trunk muscle groups; each stretch was held for 30 s.
A 20-min strength training protocol was then initiated. For strengthening of the upper extremities (elbow flexors and extensors, shoulder abductors, flexors, extensors and internal and external rotators, forearm pronators and supinators) hand weights of 2-3 kg were used to perform biceps curls, triceps extensions, and side arm lifts. Initially, three sets of 20 repetitions were conducted for all the upper-body exercises. Strengthening of the lower extremities focused on the quadriceps, hamstrings, and gastrocnemius muscle groups; ankle weights of between 0.5 and 1.0 kg were used to perform knee and hip extensions and heel rises, respectively. Four sets of 10 hip and knee extensions were performed, and three sets of 15 hip abductions were performed on each leg. Core strengthening of the abdominal muscles and the muscles of the trunk was achieved by using body weight as resistance for push-ups (three sets of eight repetitions) and sit-ups (five sets of 10 repetitions). A 30-s recovery period was used between all sets, and a 1-min recovery period was used between exercises. Intensity was increased progressively every 3 wk on an individualized basis by increasing the number of sets by one and repetitions by five, while the weight remained stable. All subjects were able to complete all the exercises within the strength training protocol.
After the strength training protocol, a game for general strengthening was initiated (10 min) using a light medicine ball (1 kg). All individuals in the training group performed lateral trunk rotations using the medicine ball and a variety of drills that involved passing the ball and both push-ups and sit-ups using the ball.
The second major component of the session was aerobic interval training (20-22 min). Initially, this involved three, 60-m, outdoor, uphill walking repetitions (gradient 5%, with or without an anterior walker). The recovery time between walks was three times the time taken to perform the walk (work:rest ratio of 1:3). The average time to cover this distance was 100 s (range = 90-112 s); therefore, the recovery time was approximately 300 s. The initial intensity of the aerobic training was approximately 65% of the age-predicted maximal HR, as measured by carotid palpation at the end of each repetition. Active recovery, in the form of walking, was used between each repetition of the aerobic interval training session. All subjects walked slowly back to the start position, with assistance, where necessary, from the researchers.
As the individuals improved their physical fitness (i.e., the subjects covered the 60 m in less time while maintaining the desired exercise intensity), the number of repetitions were increased, with the work:rest ratio maintained at 1:3.The intensity of the training sessions had increased to 75% of age-predicted maximal heart rate by the end of the 12wk. The training session concluded with breathing exercises and passive stretching (7 min). Each stretch was held for about 20-30 s.
A one-sample Kolmogorov-Smirnov test of equality of variances confirmed normally distributed data. A two-way analysis of variance (ANOVA) with repeated measures was applied to examine the effect of time (week 0-week 12) and group (control-training) on each dependent variable. If any significant interactions were identified, post hoc, Bonferroni-adjusted t-tests were performed. The level of significance was set at P < 0.05. SPSS version 13 was used for all statistical analyses.
Submaximal exercise intensity.
All subjects (training and control) participated in all the week 0 and week 12 tests, and none of the subject data were excluded from the subsequent data analyses. There were no intergroup differences for body mass at week 0 or week 12. Significant (P < 0.05) interactions were obtained for absolute, submaximal V˙O2 (L·min−1) and relative, submaximal V˙O2 (mL·kg−1·min−1) (Fig. 1). Post hoc, Bonferroni-adjusted t-tests demonstrated significant (P < 0.05) reductions in submaximal V˙O2 at week 12 for the training group compared with the control group (Table 2). Furthermore, a significant (P < 0.05) interaction for fractional utilization (%V˙O2peak) was also obtained, with a post hoc test identifying a significant reduction in fractional utilization in the training group compared with the control group at week 12 (Table 2, Fig. 2). Subsequent post hoc tests demonstrated a significant (P < 0.05) reduction in submaximal V˙O2 at week 12 for the training group compared with the control group. There were no significant interaction effects for submaximal RER, V˙E, and V˙E/V˙O2 at 2.5 W.
There were significant (P < 0.05) interaction effects (Table 3) for relative peak V˙O2, absolute peak V˙O2, and V˙E. Bonferroni-adjusted post hoc t-tests indicated that the training group generated significantly (P< 0.05) higher peak V˙O2 and V˙Epeak values compared with the control group at week 12. There were no significant interactions for peak HR, RER, or La. The duration of the peak V˙O2 tests increased from 338.6 ± 16.9 s during the pretraining phase to 415.7 ± 131.3 s during the posttraining phase in the training group.
A significant (P < 0.05) interaction effect for GMFM values was identified (Table 4). Post hoc comparisons indicated that the total score (dimensions D and E) significantly increased (P < 0.05) in the training group but not in the control group.
An effect size calculation was conducted for peak V˙O2, and a Cohen's d of 0.55 (medium) was determined. Moreover, a Cohen's d of 0.25 (low-medium) was also obtained for the change in submaximal V˙O2.
The major findings from this study were that a 12-wk strength and aerobic interval training program in a group of children with spastic CP resulted in 1) significant improvements in arm-cranking economy and a significant reduction in the fractional utilization for a given external workload, 2) a significant increase in V˙O2peak, and 3) improvements in the GMFM score.
The 12-wk strength and aerobic interval training program resulted in significant improvements (3.9%) in arm-cranking economy and a significant reduction in the fractional utilization for a given workload in the training group compared with the control group. There are, however, a lack of data in the CP literature against which to contextualize these findings. There are a few studies that have evaluated the effect of training on the submaximal oxygen cost of cycling, but the findings are equivocal (1,7,14). Of these studies, only one (7) has demonstrated a 10% reduction in the energy cost of cycling at 30 W after a 10-wk program of enhanced physical education. These authors speculate that the improved oxygen cost of cycling stemmed from enhanced coordination and integration of agonists and antagonists during movement. The other two studies (1,14) have demonstrated no effect of exercise training on the energy cost of cycling.
Evidence from the adult domain has indicated that a combined strength and endurance training program can elicit improvements in running economy (20,23). It is possible to speculate that some of the physiological changes that underpin the improvements in running economy could apply to the present study. The improved arm-cranking economy could be a product of a more efficient motor unit recruitment and synchronization pattern (20). As previously stated, improvements in maximal strength as a result of strength training can lead to a lower relative peak tension (lower percent maximal force) for a given cadence and, therefore, an increased contribution of type I compared with type II motor units, with a concomitant increase in slow-twitch fiber recruitment (20). Work from Bosco et al. (4) has demonstrated that a greater percentage of type II fibers has been directly linked to a greater energy expenditure during running at slow speeds. Therefore, by increasing slow-twitch fiber recruitment, there is the possibility that this could favor energy conservation. Unnithan and coworkers (27,28) have demonstrated that both high levels of coactivation and total body mechanical power were associated with a high oxygen cost of walking in children with CP. Consequently, the improved economy seen in the present study could also stem from a reduction in coactivation, thereby allowing greater activation in the agonist muscle and a greater net force production from the prime mover (19).
Quantifying aerobic capacity in children with CP is important because it is provides an indication of the functional capacity of the child. A 20% increase in peak V˙O2 was noted after the 12-wk training program in the present study; this increase lies within the range (8-35%) seen in other CP training studies (1,13,14). The lack of a control group acts as a major limitation with many of these training studies. Van Den Berg-Emons (30) and coworkers implemented an aerobic exercise training program of four 45-min sessions per week for 9 months in a group of children with CP. This training program incorporated a control group and resulted in a 35% increase in maximal aerobic power (cycle and arm ergometry) in the training group compared with the control group. In the only other comparable arm-cranking training study, Bar-Or and coworkers (1) have demonstrated an 8% improvement in peak V˙O2 after a twice-weekly, mild conditioning program for 12 months.
There was no change noted in the HRmax obtained during the posttraining peak V˙O2 tests in the present study; consequently, according to the Fick principle, any increase in peak V˙O2 noted could be attributed to training-induced increases in stroke volume and or arterial-venous oxygen difference. Evidence exists in the literature to support the contention that exercise training in patients with CP will result in an increase in blood flow to the exercising muscle during a submaximal task (14). Spastic muscles have reduced blood flow during exercise (10); thus, any posttraining increase in blood flow could reflect a decrease in spasticity with a concomitant reduction in coactivation. Therefore, the higher peak V˙O2 values noted after training could also reflect a reduction in coactivation levels. The improvement in aerobic capacity in the training group in the present study was also accompanied by a significant increase in V˙E at peak exercise; these findings are in agreement with previous studies (1,13,30). The significant upper-body strength component of the training may have led to a decrease in respiratory muscle spasticity with a concomitant in increase in respiratory frequency and or tidal volume at peak exercise intensities (12). Evidence exists in the literature to demonstrate that upper- and lower-body training can give rise to improvements in the maximal sustainable ventilatory capacity (V˙E), increases in maximal voluntary ventilation, and improvements in the oxidative capacity of the diaphragm (25). It is possible to speculate that one further mechanism could be responsible for the increase in peak V˙O2 noted in the present study: a reduction in muscle coactivation in the arms could result in the generation of greater propulsive power and the attainment of a higher peak V˙O2. Evidence from work by O'Connell and Barnhart (22) demonstrates that upper-body resistance training resulted in improvements in wheelchair propulsive power in children with CP.
The results demonstrate a significant improvement in gross motor function performance after training (Table 4). These results are in agreement with previous training studies that have used either the whole of the GMFM or just items D and E to evaluate the quantitative changes in the gross motor function of individuals with CP (6,8). The evidence from the literature is unequivocal: even very severely disabled individuals can gain functional improvements with training. The mechanisms behind these improvements could be attributed to the effect of strength training on changes in reciprocal inhibition of the knee flexors and extensors. Increases in muscle strength of the hip extensors and hip abductors would also contribute to the improved walking ability. Because of the short duration of the training program, the increase in GMFM score in the training group might be ascribed to an increase in muscle strength mediated through neural adaptations. As previously stated, these adaptations could stem from improved coordination between agonist and antagonist and increased activation of prime mover muscles. The low (30%) GMFM scores could have stemmed from the assessment being carried out without the use of walking aids; this identical assessment protocol, however, was carried out before and after training.
There were certain limitations associated with this study. The major limitation was the fact that the aerobic interval training sessions were conducted in a field setting. Despite the fact that no physiologic correlates of this field test were established, these types of tests have been recommended for their ease of administration and motivational benefits (2). Furthermore, the subject numbers in each group were low; however, a medium effect size was generated for peak V˙O2.
In summary, the findings from this study demonstrate that improvements in economy can be obtained from a combined strength and aerobic interval training program in children with CP. Previous research has demonstrated that low levels of physical activity have been linked to the high oxygen cost of walking in children with CP (17). Consequently, the application of a training stimulus that reduces the energy cost of arm cranking (as seen in the present study) may have implications for increasing the habitual physical activity levels in children with CP, and this research question warrants further investigation.
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