Verschuren, Olaf PhD; Maltais, Désirée B. PhD; Douma-van Riet, Danielle MPPT; Kruitwagen, Cas MSc; Ketelaar, Marjolijn PhD
Brain Center Rudolf Magnus and Center of Excellence for Rehabilitation Medicine (Drs Verschuren and Ketelaar), University Medical Center Utrecht and De Hoogstraat Rehabilitation, Utrecht, the Netherlands; Partner of NetChild (Drs Verschuren and Ketelaar), Network for Childhood Disability Research, Utrecht, the Netherlands; Department of Rehabilitation (Dr Maltais), Laval University, Quebec City, Quebec, Canada; Practice for Pediatric Physical Therapy (Ms Douma-van Reit), Zuidwest Koudum, the Netherlands; Julius Centre for Health Sciences and Primary Care (Ms Kruitwagen), Utrecht, the Netherlands.
Correspondence: Olaf Verschuren, PhD, Rehabilitation Centre De Hoogstraat, Rembrandtkade 10, 3583 TM, Utrecht, the Netherlands ( email@example.com).
Grant Support: This research was supported by the Dr Phelps Foundation, the Netherlands. The funding body did not participate in the design and execution of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the manuscript.
The authors declare no conflicts of interest.
Many of the daily activities of childhood consist of short bursts of high-intensity physical activity alternating with brief periods of rest.1 Performing these brief, high-intensity activities requires sufficient levels of anaerobic performance, making it a physiologic function that is critical to the ability of children to participate in daily activities.2 Children with milder forms of cerebral palsy (CP) (ie, those who walk without support) are often integrated into their community schools and recreational facilities, and thus are required to perform these same brief, high-intensity activities alongside their peers with typical development (TD). Furthermore, reports of studies of children with TD indicate that anaerobic performance increases as children age or mature,3–6 with a plateau reached around late adolescence.7 Thus, to understand the effect of anaerobic performance on participation in physical activities in CP, it is important to understand how the anaerobic performance of children with CP compares with that of their peers with TD.
To date, only 1 study, completed almost 20 years ago, has concluded that the anaerobic performance of children and adolescents with CP is reduced compared with that of children with TD.8 These conclusions are, however, limited for several reasons. First, the test protocol used for the children with CP was not the same as that used for the children with TD. Second, the normative values were derived from a test with a standardized braking force on the basis of body height.9 Third, the comparison between the CP group and the children with TD did not consider how growth (height) or maturation (age) might affect any differences between the 2 groups. Fourth, only 46 children with CP were tested and the sample was very diverse. Fifth, the test itself (cycling or arm cranking) was not necessarily representative of children's everyday physical activity, because children with CP are more likely to engage in walking and running-based activities than cycling or arm cranking.
Because level-ground walking and running are natural physical activities for children and thus easy for them to perform, the most functional, appropriate, and externally valid way to assess anaerobic performance in children may be a walking- or running-based test.10 For children with CP who are able to walk independently, and for children with TD, a valid and reliable running-based test, the Muscle Power Sprint Test (MPST), is available.10,11 The purpose of this study was therefore to compare the anaerobic performance of a large group of children with CP who walk without support with that of their peers with TD, using the running-based MPST.
MATERIAL AND METHODS
A secondary analysis of previously published anaerobic performance data for children with TD, 6 to 12 years old, and for children with CP, 6 to 12 years old, was conducted.11,12
Boys and girls between the ages of 6 and 12 years with TD were asked to participate in a previous study.12 For that study, children were considered eligible to participate if they met the specified age range, did not use any medications that might affect exercise capacity, and were not treated for a medical condition. Specific exclusion criteria included impairment of motor development or a diagnosis of pulmonary and/or cardiovascular disease.
The data set for children with CP between the ages of 6 and 12 years used for this analysis was a subset of the data from another previous study because the original study included participants up to 18 years of age.12 Because of the characteristics of the MPST, only children with CP who were classified at Gross Motor Function Classification System (GMFCS)13 level I (able to run and walk indoors and outdoors and climb stairs without limitations) or level II (able to walk indoors and outdoors and climb stairs holding onto a railing but experiencing limitations in walking on uneven or inclined surfaces and in walking in crowds or confined spaces) were included. Cognitive ability was required to be such that the children were able to follow simple commands. Children were excluded if they had undergone orthopedic surgery or neurosurgery within the 6 months before study entry or if they had cardiac or respiratory conditions that could be negatively affected by exercise.
The total data set from the previous study with children with TD (175 boys and 201 girls) and a subset of the data from the study with children with CP (102 boys and 57 girls) were used. In total, 3 groups were analyzed for boys and 3 groups for girls (those with TD and those with CP classified at GMFCS level I and those with CP classified at GMFCS level II).
Participants' body mass and height were measured using standardized methods. Before testing, each child was weighed in underwear to the nearest 100 g on digital scales (Seca, Hamburg, Germany; Soehnle, Nassau/Lahn, Germany; or Salter, Illinois) in the participating clinics. Height measurements were taken on the same day while the child was standing against a wall. Height was measured to the nearest 0.5 cm using a stadiometer or wall-mounted measuring stick. Body mass index was calculated as weight in kilograms divided by height in meters squared.
The GMFCS was used to classify the children with CP into groups on the basis of their functional mobility. The original GMFCS has been reported to yield reliable and valid data for children aged 6 to 12 years.13
Physical characteristics of the CP group (according to the GMFCS level) and the reference group have been summarized in Table 1.
Anaerobic performance was measured using the mean power (measured in watts) derived from the MPST.10 This test has been shown to be reliable and valid for children with CP (intraclass correlation [ICC] = 0.99)10,14 as well as for children with TD (ICC = 0.98).11 To perform the MPST, the participants were instructed to complete 6, 15-m walks/runs at maximum pace. The 15-m distance was marked by 2 lines taped on the floor. Cones were placed at both ends of the lines. The participant had to walk/run as fast as possible from one line to the other, and was instructed to cross the line. Between each run, each subject was allowed a 10-second rest before turning around to prepare for the following sprint.
The participants were given the cues “ready,” “3,” “2,” “1,” and “go” for the first run. For the second through sixth runs, the assessors counted backwards from “10” to “1” and then gave the cue “go.” An estimate of power output (watts) (force × velocity) for each sprint was calculated on the basis of the sprint velocity and body mass, where velocity (m/s) = distance/time, acceleration (m/s2) = velocity/time, force (kg·m/s2) = body mass × acceleration. Mean power was defined as average power output during the 6 runs.
To compare the anaerobic performance of a large group of children with CP who walk without support with that of their peers with TD, cross-sectional data analyses were performed using SPSS 18.0 (SPSS Inc, Chicago, Illinois) and R statistical program (R foundation for Statistical Computing, Vienna, Austria). Data from all participants (children with TD and children with CP, classified at GMFCS levels I and II) were analyzed through Generalized Additive Models for Location, Scale and Shape.15 Preliminary analyses demonstrated that height was the variable that best correlated with MPST performance. Age, height, sex, and their interactions were all included as possible predictors. Height was the most discriminative variable and demonstrated the highest explained variance (R2 > 0.7) with anaerobic performance. Model building was then performed to determine the significant predictor variables and their effect sizes, and formulas were constructed from these models. The increase in muscle power in the observed height range was exponential. To cope with this, we modeled the data using a logarithmic link function, meaning that the resulting estimates indicate a multiplicative effect on the original scale—the differences between groups are given relatively instead of absolutely.
As a consequence, we used ratios instead of differences to compare groups, so changes are relative rather than absolute. Separate graphs of the resulting models were made according to sex.
As can be seen in Figure 1, (1) those with CP showed lower mean power values than peers with TD of the same height, and (2) taller children in all groups (TD, GMFCS level I, and GMFCS level II) showed higher mean power values than shorter children in the same group. Figure 1 also shows that for children with CP classified at GMFCS level I, the rate of increase with increasing height was significantly higher than for children with TD (P = .002). Thus, although anaerobic power was impaired in the GMFCS level I group regardless of the height of the child, this impairment was less marked in taller than in shorter children. For the GMFCS level II group, on the other hand, Figure 1 shows that the rate of increase in power for the taller versus shorter children was lower than for children with TD (although not significant, P = .057). In other words, the anaerobic performance of the children classified at GMFCS level II was impaired regardless of their height, but the impairment was greater for the taller than for the shorter children.
The purpose of this study was to compare the walking- and running-related anaerobic performance of children with CP who walk without support with that of their peers with TD. The children with CP had impaired anaerobic performance as it was lower than that of their peers. Moreover, this impairment increased with height, especially in children with CP classified at GMFCS level II.
Although anaerobic performance increases with height in the children with CP, those classified at GMFCS level II appear to become less and less fit with increasing height. Although the focus in physical rehabilitation is often young (and therefore smaller) children, it may be prudent to follow them and intervene as necessary over time as it is possible that impairments in short-term muscle power are not static. Children with CP have deficits in the production of higher velocity movements (ie, muscle power).16 Muscle power is an important component of muscle performance that is often neglected in rehabilitative interventions. The results of a recent study by Moreau et al17 in children with CP that are ambulatory suggest that the ability to rapidly generate torque may be of great importance during certain tasks, such as sports and higher level functional activities. Anaerobic performance is modifiable with training in CP, as noted by Verschuren et al18 who have shown that a fitness training program predominantly of anaerobic nature is able to improve the anaerobic performance in children with CP. The results of a randomized controlled trial published by Moreau et al16 show that strengthening interventions involving higher velocity movements, such as velocity training or power training, are effective in improving muscle power and functional walking performance in youth with CP. This suggests that emphasizing rehabilitation programs that include anaerobic power-producing activities (such as running and jumping) with young children at GMFCS levels I and II may be a way to potentially mitigate the difference in anaerobic performance that is present with increasing height.
Height is a more robust parameter than age because individuals of the same age can differ substantially in height. An individual with a greater stride length is generally thought to have an advantage in sprint performance by being able to produce greater forward propulsion. The literature suggests that with growth, power output will increase further as will the differences between males and females.4 Therefore, it is not surprising that children who are taller can produce more power in the MPST. As shown in this study, this does not apply to children with CP. There are several reasons why children with CP may have lower anaerobic performance than their peers with TD. First, Young et al19 showed that muscle strength was closely related to maximal sprint velocity in children with TD. Children with CP have lower-limb muscle strength below normative values.20,21 Thus, this weakness may explain in part their lower anaerobic performance. Second, it has been shown that muscle power production is decreased in children with CP compared with control groups,22,23 possibly related to their impairments in motor control. Indeed, muscle contraction in children with CP is characterized by incomplete recruitment or decreased motor unit discharge rates during maximal voluntary contraction22,23 and greater coactivation of antagonist muscles. Third, upper motor lesions (such as occurs with CP) are associated with atrophy of the higher force-producing type II (fast) muscle fibers, resulting in a greater proportion of the force of contraction being generated by the lower force-producing type I (slow) muscle fibers.24 The lower anaerobic performance observed in this study may thus also reflect a change in the muscle fiber characteristics toward a higher percentage of slow fibers, compared with that seen in children with TD.
One important limitation of this study is its cross-sectional design. Given the difficulty of recruiting special populations, it would be quite difficult to conduct a similar study with a longitudinal design. Certainly, this is an area for future research—a future longitudinal study with a smaller cohort is required to conclusively determine the effect of growth on anaerobic performance impairments in CP. The study included only children and adolescents with spastic CP. Whether our results are generalizable to other clinical types of CP requires further investigation. Moreover, the participants in this study represented an “open-source” convenience sample of children and adolescents with CP who were receiving physical therapy. This selection procedure may have led to some degree of selection bias, as it is unknown whether or not these participants differ from children and adolescents who are not receiving treatment in a rehabilitation center or special education school. Another limitation is the relatively low number of girls with CP who are classified at GMFCS level II that were included in this study. In future studies, the number of girls should be increased.
In conclusion, the walking- and running-related anaerobic performance of children with CP who walk without support is impaired. This impairment increases with height.
1. Bailey RC, Olsen J, Pepper SL, Porszasz J, Bartsow TJ, Cooper DM. The level and tempo of children's physical activities: an observational study. Med Sci Sports Exerc. 1995; 27:1033–1041.
2. Verschuren O, Ketelaar M, Gorter JW, Helders PJ, Takken T. Relation between physical fitness and gross motor capacity in children and adolescents with cerebral palsy. Dev Med Child Neurol. 2009; 51:(11):866–871.
3. Dore E, Diallo O, Franca NM, Bedu M, Van Praagh E. Dimensional changes cannot account for all differences in short-term cycling power during growth. Int J Sports Med. 2000; 21:(5):360–365.
4. Armstrong N, Welsman JR, Chia MY. Short term power output in relation to growth and maturation. Br J Sports Med. 2001; 35:(2):118–124.
5. Martin RJ, Dore E, Twisk J, van Praagh E, Hautier CA, Bedu M. Longitudinal changes of maximal short-term peak power in girls and boys during growth. Med Sci Sports Exerc. 2004; 36:(3):498–503.
6. Van Praagh E. Testing of anaerobic performance. In: Bar-Or O., ed. The Encyclopedia of Sports Medicine: The Child and Adolescent Athlete (IOC). London, UK: Blackwell Science; 1996; :602–616.
7. Van Praagh E, Dore E. Short-term muscle power during growth and maturation. Sports Med. 2002; 32:(11):701–728.
8. Parker DF, Carriere L, Hebestreit H, Bar-Or O. Anaerobic endurance and peak muscle power in children with spastic cerebral palsy. Am J Dis Child. 1992; 146:1069–1073.
9. Bar-Or O. Pediatric Sports Medicine for the Practicioner. From Physiologic Principles to Clinical Applications. New York, NY: Springer-Verlag; 1983; .
10. Verschuren O, Takken T, Ketelaar M, Gorter JW, Helders PJ. Reliability for running tests for measuring agility and anaerobic muscle power in children and adolescents with cerebral palsy. Pediatr Phys Ther. 2007; 19:(2):108–115.
11. Douma-van Riet D, Verschuren O, Jelsma D, Kruitwagen C, Smits-Engelsman B, Takken T. Reference values for the muscle power sprint test in 6- to 12-year-old children. Pediatr Phys Ther. 2012; 24:(4):327–332.
12. Verschuren O, Bloemen M, Kruitwagen C, Takken T. Reference values for anaerobic performance and agility in ambulatory children and adolescents with cerebral palsy. Dev Med Child Neurol. 2010; 52:(10):e222–e228.
13. Palisano RJ, Rosenbaum P, Walter S. The development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997; 39:214–223.
14. Verschuren O, Bongers BC, Obeid J, Ruyten T, Takken T. Validity of the muscle power sprint test in ambulatory youth with cerebral palsy. Pediatr Phys Ther. 2013; 25:(1):25–28.
15. Stasinopoulos MRR. Generalized additive models for location, scale, and shape (GAMLSS). http://www.gamlss.com
. Accessed July 2009.
16. Moreau NG, Holthaus K, Marlow N. Differential adaptations of muscle architecture to high-velocity versus traditional strength training in cerebral palsy. Neurorehabil Neural Repair. 2013; 27:(4):325–334.
17. Moreau NG, Falvo MJ, Damiano DL. Rapid force generation is impaired in cerebral palsy and is related to decreased muscle size and functional mobility. Gait Posture. 2012; 35:(1):154–158.
18. Verschuren O, Ketelaar M, Gorter JW, Helders PJ, Uiterwaal CS, Takken T. Exercise training program in children and adolescents with cerebral palsy: a randomized controlled trial. Arch Pediatr Adolesc Med. 2007; 161:(11):1075–1081.
19. Young W, McLean B, Ardagna J. Relationship between strength qualities and sprinting performance. J Sports Med Phys Fitness. 1995; 35:(1):13–19.
20. Eek MN, Beckung E. Walking ability is related to muscle strength in children with cerebral palsy. Gait Posture. 2008; 28:(3):366–371.
21. Wiley ME, Damiano DL. Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol. 1998; 40:100–107.
22. Elder GC, Kirk J, Stewart G, et al. Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol. 2003; 45:(8):542–550.
23. Stackhouse SK, Binder-Macleod SA, Lee SC. Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve. 2005; 31:(5):594–601.
24. Marbini A, Ferrari A, Cioni G, Bellanova MF, Fusco C, Gemignani F. Immunohistochemical study of muscle biopsy in children with cerebral palsy. Brain Dev. 2002; 24:(2):63–66.
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