Maximal Treadmill Performance of Children With Cerebral Palsy
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1 Pediatric Exercise Science, 1995, 7, O 1995 Human Kinetics Publishers, Inc. Maximal Treadmill Performance of Children With Cerebral Palsy Martine Hoofwijk, Viswanath Unnithan, and Oded Bar-Or Nine children with spastic cerebral palsy (CP) and 9 controls (mean age 13.5 and 14.0, respectively) completed a maximal walking test on the treadmill. Initial gradient was set at 0% with a speed increase every 2 minutes until the "fastest walking speed" was achieved in the third stage. The gradient was then increased by 2.5-5% every 2 minutes. V0,max of the CP children was significantly lower (p =.001) than that of the controls (32.7 vs ml. kg-'. mid). There was no significant difference in maximal heart rate between the two groups (189 vs. 197). However, the CP subjects had significantly higher (p =.007) venti!atory equivalent for 9 compared to the controls (41.4 vs. 33.6). The lower VOzmax values of the CP children might reflect inefficient ventilation, compromised circulation, and local fatigue in the spastic limb muscles. Maximal aerobic power is the component of physical fitness that is often used to measure the effect of training in healthy children and those with physical disabilities (7, 9, 15, 18, 20). It has also been used in assessing the effects of rehabilitation (6). In addition, there has been an increase in the use of maximal aerobic power to describe special populations (1,5, 16). It is known that children and adolescents with cerebral palsy (CP) have a lower maximal oxygen uptake (V02max) compared to healthy peers (2, 3, 11, 12). This might be related to a low level of physical activity and a lower mechanical efficiency due to constantly high muscle tone, postural regulation, and involuntary movements (7, 8, 12, 14). Another possible reason may be poor posture and inefficient gait caused by genu valgum. Active muscle mass is an important determinant of ~0,rnax. Although a larger proportion of muscle mass is used for walking than for cycling or propelling a wheelchair, almost all researchers have reported VOlmax of children with.cp on the cycle or wheelchair ergometer. So far two studies have examined the V02 of CP children walking on a treadmill. Rieckert et al. (17) assessed the V02max of subjects with a diversity of handicaps; only 10 of the 16 subjects had a spastic type of CP. In addition, there was no indication in the methods section of Viswanath Unnithan is with the Department of Movement Science and Physical Education at the University of Liverpool, P.O. Box 147, Liverpool, L69 3BX, U.K. Oded Bar-Or is with the Children's Exercise on Nutrition Centre, Chedoke Hospital, Eve1 Building, P.O. Box 2000, Station A, Hamilton, ON Canada L8N 325. Martine Hoofwijk was with Chedoke Hospital at the time of this study.
2 306 - Hoofwijk, Unnithan, and Bar-Or standardization of treadmill arm support, which could have affected the VO~ values obtained. Rose et al. (19) collected only submaximal VOz data on a horizontal treadmill. Thus, there is very little information on treadmill-based vo2ma?: data for children with CP. Nor are there published protocols for administering V02max tests to such children. The objective of this study, therefore, was to see whether it would be possible for CP children to perform a V02max test walking on a treadmill and thereby to compare their V02max, ventilation, and maximum heart rate (HR) with those of able-bodied controls. Subjects Methods Thirteen children diagnosed with CP were recruited and classified according to published taxonomy (4). Three of them could not retain the mouthpiece, and one child was not able to walk on the treadmill without holding onto the bars. These 4 were mentally retarded and did not complete the test. This study therefore includes the remaining 9 CP children, one of whom was mentally retarded, (7 boys and 2 girls) plus 9 gender-matched able-bodied controls. The age of the controls ranged between 11 and 16 years (mean 14.0), that of the CP children between 10 and 16 years (mean 13.5). Prior to completion of written informed consent from the parents, verbal assent was given by all children. The study was approved by the McMaster University Ethics Committee. Procedures The subjects came to the Children's Exercise and Nutrition Centre in the afternoon at least 2 hours after their last meal. They completed two questionnaires, one regarding their daily physical activity over the last 6 months and a second detailing information about physical activity, medicine, and food intake on the day of the test. Height and weight were measured in light sports clothes without shoes, using a stadiometer (CMS Weighing Equipment, London, U.K.) and the Ancaster electroscale model UMC-600 bodyweight scale (20 g accuracy), respectively. To assess body composition, the RJL-BIA lola bioelectrical impedance was used. The subjects were then asked to walk 20 meters three times along a carpeted corridor at their "comfortable walking speed" (CWS). This was timed without the subject's knowledge. The mean of these three trials was used to calculate the comfortable walking speed. The treadmill (Quinton, 465) was modified to accommodate speeds as low as 1.68 km. hr-i. Each subject had only one 15- min treadmill practice, which consisted of three stages. This involved the subject walking (a) holding onto the treadmill support bars and being supported around the waist, (b) just being supported around the waist, and (c) walking totally unaided. Each of these periods was separated by 2-3 min of rest. During the V02max test subjects did not hold onto the bars; however, they were allowed to touch it momentarily to maintain their balance. HR was measured and stored during the test using a sport tester (PE3000, Polar Electro Fitness Technology). For gas collection, subjects used, depending on their age, a small, medium, or large two-way NRBV valve (Hans Rudolph 1410, 2600, or 2700, dead spaces: 20.1, 48.9, and ml). A 3-cm diameter hose was connected to
3 Treadmill Performance each subject's own biking helmet and was led backwards over his or her head to the expired air port of the metabolic cart (Beckman MMC Horizon). At the end of the visit subjects performed a self-assessment of the development of secondary sexual characteristics, pubic hair in boys and breast in girls, to determine developmental level. The classifications were based on Tanner's photographs of stages of maturity (23). The one boy who was mentally retarded was assisted by his mother in this rating. Exercise Protocol The average starting speed was 4.4 km. hr' for the able-bodied versus 3 km. hr-i for the CP subjects. Otherwise, exercise protocols were identical for both groups. The individual starting speed was determined according to the predetermined "comfortable walking speed" (CWS). When the CWS was between 2 and 3.5 km. hr-' the subject started on the treadmill at 2.4 km. hr-i, for a CWS of km. hr-' the subject started at 3.0 km h?, and for CWS higher than 5 km. hr-i at 4.0 km. hr-i. Every 2 min the speed was increased until the "fastest walking speed" (FWS) was achieved in the third step. This was the fastest speed the subject was able to sustain for 2 min without breaking into a run. It was determined by "negotiation" between the subject and the investigator, during the first 30 s of that stage. After these three submaximal stages the gradient was raised by 2.4-5% every 2 minutes while the walking speed was set km. hr-i below the fastest walking speed. This speed was kept constant during the rest of the test. The test was terminated when the subject was too exhausted to keep on walking, in spite of continuous encouragement by the investigators. During the test, mass-relative oxygen consumption, (VO~ ml. kg-'. mid), ventilation, (VE L. min-i), respiratory exchange ratio (RER), and heart rate (HR) were measured every 15 s. V02max was taken as the average of the two highest consecutive 15-s values within the same stage. The maximum heart rate (HRmax) was defined as the highest 15-s value. Statistical Analysis Descriptive data are presented as means + standard deviation. Significant differences between healthy and CP subjects were calculated by means of an unpaired t test. All statistical analyses were performed using Minitab statistical software package. Because there were only 2 girls in each group, these analyses were only performed for the entire groups and for the boys. Statistical significance was set at p <.05. Subject Characteristics Results Table 1 lists the physical characteristics of the two groups. Height and weight for all subjects were within the normal range. The range for the Tanner state pubic hair was 1-5 in the CP boys and 2-5 in the control boys. The range for breast development in the girls was 2-4 for both CP and control group. One of
4 308 - Hoofwijk, Unnithan, and Bar-Or Table 1 Physical Characteristics of the Groups CP Controls M SD M SD Age (years) Weight (kg) Height (cm) % fat Tanner stage Note. CP = subjects with cerebral palsy. n = 9 CP and 9 controls. Table 2 Clinical and Walking Characteristics of Individual Children With Cerebral Palsy Child Classification" CWS FWS Usual walking aids (kmhr) (km/hr) Spastic quadriplegia Spastic hemiplegia (mentally handicapped) None 5.0 None 5.5 None 4.0 Crutches 2.8 None 4.9 None 4.5 None 4.9 Crutches and orthotics 3.5 None 6.5 Note. CWS = comfortable walking speed; FWS = fastest walking speed. "According to published taxonomy (4). the CP subjects classified herself as "inactive," none as "occasionally active," 5 as "moderately active," 3 as "active," and none as "very active." The respective ratings by the control subjects were 1, 0, 2, 4, 2. As shown in Table 2, one CP boy was classified as hemiplegic, 7 as diplegic, and 1 as quadriplegic. The 2 children who habitually used crutches performed the max test without their crutches. Individual comfortable walking speed and fastest walking speed of all CP subjects are listed in Table 2. A significant (p =.001) difference was found between the means of the fastest walking speed in both groups (CP: 4.8 km. hr-'; controls: 7.5 krn. hr-i). Surprisingly, there was no difference between the
5 Table 3 Physiological Characteristics of the Subject Groups Treadmill Performance VO~ HR (ml.kg-i VO~ VE (beats1.min-') (L.min-I) (L.min-I) %T/7j0, RER min) M SD M SD M SD M SD M SD M SD CP F M Total Controls F M * * * Total ** * Note. RER = respiratory exchange ratio; HR = heart rate. CP = subjects with cerebral palsy. *Significantly <.05) from same sex CP. **Significantly different (p <.01). Physiological Responses During Peak Exercise As seen in Table 3, the average ~0,max (ml. kg-'. min-i) in the entire CP group was significantly =.001) than in the control group. Mean ~0,max per kilogram and absolute V0,max values for the CP boys were significantly lower compared to the control =.001 and p =.049, respectively). Table 3 also shows that VE/V02 of the total CP group and the CP boys was significantly higher than that of the total control =.007) and control =.028), respectively. As summarized in Figure 1, all CP boys had lower V0,max per kilogram than any of the control boys. Plateau Assessment Attainment of a VO, plateau was calculated using a criterion of a less than 2 ml kg-'. min-l increase from penultimate to final stage (22). The results illustrate that only 319 (33%) of the able-bodied subjects attained a plateau compared to 419 (44%) of the CP subjects. Discussion The major finding of this study is that, with a standardized practice and protocol, children with CP can perform a maximal walking test on a treadmill. As expected, ~0,max of the CP children was lower than in the controls; however, the CP children had a higher ventilatory equivalent for 0,. Few data are published about VO, of CP children during maximal exercise (Table 4). Only Rieckert et al. (17) reported ~0,max values of CP children during treadmill walking. Their values
6 Hoofwijk, Unnithan, and Bar-Or Controls Figure 1 - Individual $02max of CP and control boys and girls on a treadmill. The solid lines indicate the means, and the dotted lines are the standard deviations, p <.05. are comparable with ours. However, a lack of standardization of arm support for the CP subjects limits these findings. Bar-Or et al. (3) administered a maximal arm cycle test to adolescents with CP. Assuming that an all-out arm exercise yields 65% of the real maximal power (3), we recalculated their data and derived VO~ values between 32 and 33 (ml. kg-'. min-i), which is comparable with Rieckert et al.'s values (17) and the present study. Lundberg's V0,max values (12) using a cycle ergometer are considerably higher than any others reported. However insufficient methodological details and lack of subject description make the interpretation of his values difficult. Even when trained adult athletes with CP were tested on a cycle ergometer (5), their VOlmax values were lower (38.6 ml. kg-' - mid) than Lundberg's values (12). Several possible mechanisms have been suggested to account for the lower ~0,max of CP children. In part, this may be due to the higher ventilatory equivalent for 0, found for CP children in both Lundberg's study (13) and ours. This can be caused by a lower breathing efficiency due to chest wall distortion and possibly respiratory muscle spasticity. Another cause for a low V0,max may be the muscle spasticity of CP children. The constantly high muscle tone can cause a local obstruction of the venous return in the leg muscles (12), leading to an inhibition of muscle lactate clearance and thereby increase acidity and local muscular fatigue (10). It has been stated that the energy used for postural stabilization, high muscle tone, and involuntary movements cause an increase in
7 Treadmill Performance Table 4 Literature Survey of q0,rnax Tests With Children With Cerebral Patsy Age (ml-kg-' Study Ergometer N Diagnosis (yrs) min-') Comments v 0 2 Bar-Or (2) Arm 10 M+F di M+F di Lundberg (13) Cycle 4 F di M di Rieckert (17) Treadmill 8 M+F 3 t, 1 dia 7-19 Present study Treadmill 9 M+F 1 h, 7 di, q 21.3 Active 20.9 Inactive Walk usually with supports 34.7 Walk usually without supports 32.7 Note. h = spastic hemiplegia; di = spastic diplegia; t = spastic tetraplegia; q = spastic quadriplegia. "Remaining children had other handicaps such as ataxia, spina bifida, myelodysplasia. the O2 uptake during submaximal exercise (11, 12). However, it is not clear whether these factors also influence the maximal V02 of those children. There are other factors not yet investigated that may influence the performance of children with CP on a treadmill. For example, the pattem of habituation and accommodation to treadmill walking for CP children has yet to be investigated. If this mode of treadmill testing is to be used as a diagnostic, rehabilitative, or exercise prescription tool for children with CP, determining the optimal pattem for habituation is important. Within the context of the present study, the structured practice time of 15 min appeared to be satisfactory in preparing the children for the treadmill walking test. Of the 13 recruited CP children, only 9 were able to complete a maximal walking test on the treadmill. Five CP children were mentally retarded, of whom 4 did not complete the test. The one mentally retarded boy, who did complete the test, had the lowest V02max value of all subjects (22.2 ml. kg-'. mid). Femhall et al. (9) showed that children with a mental retardation score lower ~0~ values on a maximal walking Jest than do control subjects. However, the effect of mental retardation on the V0,max of CP children has not been studied to date. Two of the CP subjects had a maximal heart rate of only 164 and 170 beatslmin and did not seem exhausted when they stopped the test. Two other subjects found it hard to continuously seal their lips around the mouthpiece. It is therefore possible that our mean VOzmax for CP children is an underestimate of the "real" maximal aerobic power of this group.
8 Hoohuijk, Unnithan, and Bar-Or Examination of the attainment of plateau in VO, (less than 2 ml. kg-'. min-' increase from penultimate to final work load) in the two groups yielded some interesting results. Sixty-seven percent (619) of the able-bodied subjects did not attain a plateau compared to 55% (519) of the CP subjects. These results reflect the findings of Rowland and Cunningham (21) that able-bodied children are capable of exercising to exhaustion without demonstrating \jo2 plateau, and despite the small sample size, this trend appears to be reflected in our CP group too. In addition, these results indicate that our V02max protocol was suitable in achieving maximal effort and intensity in a CP population. However, we suggest on the basis of both maximal HR and maximal RER criteria, that maximal effort and intensity was achieved in both groups, independent of the attainment of a V02 plateau. The major limitation of this study was the inability of the majority of the mentally handicapped subjects to complete the testing. The small number of subjects in the study prevented any conclusive findings on the impact of anatomical distribution of CP on V0,max. Hence, further research is required into the development of appropriate equipment and protocols to cater for the specific needs of the mentally retarded spastic CP child. Two further areas are worthy of research: (a) the reproducibility of maximal data in the CP population, and (b) any possible gender differences with respect to the CP response to rnaximal exercise. In the present study the 2 CP girls did not differ with respect to VOzmax compared to the controls, despite having much lower maximal heart rates. In summary, this study has shown that it is possible for children with CP to perform a maximal walking test on a treadmill, using an almost identical protocol as able-bodied children. V02max and fastest walking speed of the CP children are significantly lower, whereas the ventilation equivalent for O2 is higher than that of the controls. References 1. Baraldi, E., S. Zanconato, C. Zorzi, P. Santuz, F. Benini, and F. Zacchello. Exercise performance in very low birth weight children at the age of 7-12 years. Eur. J. Pediatr. 150~ , Bar-Or, 0. Pediatric Sports Medicine for the Practitioner. New York: Springer- Verlag, Bar-Or, O., 0. Inbar, and R. Spira. Physiological effects of a sports rehabilitation program on cerebral palsied and post-poliomyelitic adolescents. Med. Sci. Sports 8: , Bax, M.C.O. Terminology and classification of cerebral palsy. Dev. Med. Child Neurol. 6: , Bhambhani, Y.N., L.J. Holland, and R.D. Steadward. Maximal aerobic power in cerebral palsied wheelchair athletes: Validity and reliability. Arch. Phys. Med. Rehabil. 73: , Dahlback, G.O., and R. Norlin. The effect of corrective surgery on energy expenditure during ambulation in children with cerebral palsy. Eur. J. Appl. Physiol. 54:67-70, Dresen, M.H.W., G. de Groot, J.R. Mesa Menor, and L.N. Bouman. Aerobic energy expenditure of handicapped children after training. Arch. Phys. Med. Rehabil. 66:302-
9 Treadmill Performance Ekblom, B., and A. Lundberg. Effect of physical training on adolescents with severe motor handicaps. Acta Paediatr. Scand. 57:17-23, Fernhall, B., A.L. Millar, G.T. Tymeson, and L.N. Burkett. Maximal exercise testing of mentally retarded adolescents and adults: Reliability study. Arch. Phys. Med. Rehabil. 71: , Jones, N.L., and G.J.F. Heigenhauser. Effects of hydrogen ions on metabolism during exercise. In: Perspectives in Exercise Science and Sports Medicine: Vol. 5. Energy Metabolism in Exercise and Sport, D.R. Lamb and C.V. Gisolfi (Eds.). Dubuque, IA: Brown and Benchmark, 1992, pp Lundberg, A. Oxygen consumption in relation to work load in students with cerebral palsy. J. Appl. Physiol , Lundberg, A. Maximal aerobic capacity of young people with spastic cerebral palsy. Dev. Med. Child Neurol. 20: , Lundberg, A. Longitudinal study of physical working capacity of young people with spastic cerebral palsy. Dev. Med. Child Neurol. 26: , Lundberg, A., C.O. Ovenfors, and B. Saltin. Effect of physical training on schoolchildren with cerebral palsy. Acta Paediatr. Scand. 56: , Mahon, A.D., and P. Vaccaro. Ventilatory threshold and V0,max changes in children following endurance training. Med. Sci. Sports Exerc. 2 1 : , Moura e Castro, J., 0. Costa, and F. defreitas. Evaluation of the aerobic capacity of blind people, but direct VO, maximal measurement. Rev. Port. Cardiol , Rieckert, H., L. Bruhn, U. Schwalm, and W. Schnitzer. Ein Ausdauertrainung im Rahmen des Schulsports bei vorwiegend spastisch gelahmten Kindern. [Endurance training within a program of physical education in children predominantly with cerebral palsy]. Med. Welt 28: , Rintala, P., H. Lyytinen, and J.M. Dunn. Influence of a physical activity program on children with cerebral palsy: A single subject design. Ped. Exer. Sci. 2:46-56, Rose, J., J.G. Gamble, J. Medeiros, A. Burgos, and W.L. Haskell. Energy cost of walking in normal children and in those with cerebral palsy: Comparison of heart rate and oxygen uptake. J. Pediatr. Orthop. 9: , Rowland, T.W. Aerobic response to endurance training in prepubescent children: A critical analysis. Med. Sci. Sports Exerc. 17: , Rowland, T.W., and L.N. Cunningham. Oxygen uptake plateau during maximal treadmill exercise in children. Chest 101: , Shephard, R.J. The working capacity of school children. In: Frontiers of Fitness, R.J. Shephard (Ed.). Springfield, IL: Thomas, 1971, pp Tanner, J.M. Growth and Adolescence (2nd ed.). Oxford: Blackwell, Acknowledgment We thank Camen Kirkness for her assistance with the data collection. This study was supported by a grant from the Hospital for Sick Children Foundation in Toronto.
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