Physiological Effects of a Physical Training Program in Children With Exercise-lnduced Asthma
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1 Pediatric Exercise Science, 1989, 1, Physiological Effects of a Physical Training Program in Children With Exercise-lnduced Asthma M. Jonathan King, Timothy David Noakes, and Eugene Godfrey Weinberg Twelve boys with atopic asthma, ages 9-14 years, were divided equally into exercise and control groups. Identical measurements were made before and after a 3-month trial period during which the exercise group was trained. The trained group, but not the control group, showed significant improvements.in parameters of physical fimess including maximum oxygen consumption (V02max) and peak running velocity during the maximal treadmill test (p<0.05). Treadmill velocity at the lactate turnpoint was greater and heart rate during submaximal exercise was lower in the trained subjects after the trial period. Subjective and objective findings (less use of medication, fewer asthmatic attacks, increased physical activity) suggested that clinical asthma improved with training. However exercise-induced asthma (EIA), measured by the airway's response to a standardized treadmill run, did not alter with training. There are conflicting reports concerning the efficacy of physical training programs for asthmatic children. Relatively few have demonstrated an increase in maximal oxygen consumption (V0,max) in asthmatic children in response to training (2,7, 1 1, 13). These studies have shown that the improvement in V0,max can be achieved only if premedication is used to prevent the development of exercise-induced asthma (EIA) at the exercise intensities required for a training effect. A number of studies have also investigated the effect of a physical training program on the severity of EIA. Although some have shown an attenuation of EIA after training (1, 5, 12), the majority have failed to show this effect (2, 4, 6, 7, 10, 14). Thus it appears that the achievement of the trained state is not invariably associated with an attenuation of EIA. Similarly, there are conflicting M. Jonathan King and Timothy David Noakes are with the MRCIUCT Bioenergetics of Exercise Research Unit, Department of Physiology, University of Cape Town Medical School, Observatory, 7925, South Africa. Eugene Godfrey Weinberg is with the Allergy Clinic, Red Cross War Memorial Children's Hospital, Rondebosch, South Africa.
2 138 - King, Noakes, and Weinberg reports concerning the course of clinical asthma during a training program. Clinical improvement measured as a reduced frequency of asthmatic attacks or lesser use of medications, or both, has been reported by some (2, 4, 9, 16) but not all investigators (7, 10, 11, 14). We therefore undertook a pilot study to clarify some of these controversies. Twelve boys from a local community were divided into control and exercising groups. The exercising group used premeditation in order to prevent their training being restricted by the development of EIA. The training program lasted for 12 weeks. Methods Twelve boys ages 9-14 years who attended the Allergy Clinic at the Red Cross War Memorial Children's Hospital, Cape Town, South Africa, volunteered to participate in the study. Both the approval of the protocol by the Ethics and Research Committee of the University of Cape Town and written consent from the subjects' parents were obtained before the program began. Subjects were accepted into the program only after they had demonstrated a fall in forced expiratory volume in 1 second (FEV,) of greater than 15% after a standardized asthmagenic exercise test performed on a treadmill at 85% of maximum heart rate (3, 15). Thereafter the boys were divided equally into exercising and control groups. Their selected physical characteristics are listed in Table 1. Subjects performed two exercise tests at the beginning and end of the 3-month trial period: the asthmagenic test and a test of maximum oxygen consumption according to methods described previously from this laboratory (8). All were required to abstain from all medications prescribed for their asthma, with the exception of corticosteroids, for 12 hours prior to the asthmagenic tread- Table 1 Physical Characteristics of Subjects Exercise group Control group 0 3 mos. 0 3 mos. Age (mo) SD Height (cm) SD Weight (kg) SD 010 Fat SD Note. Values are expressed as M * SD, N = 6 for each group. *p<0.05, time 0 vs. 3 mos.; * *p<0.005, time 0 vs. 3 mos.
3 Physiological Effects and Asthma mill test. Prescribed medication was used prior to the vozmax tests. No tests were performed until at least 1 week after a subject had recovered from an upper respiratory tract infection. Baseline lung function was measured prior to the asthmagenic treadmill test in all subjects. Peak expiratory flow rate (PEFR) was measured with a mini-wright peak flow meter (Airrned, Clement Clarke International Ltd, England), and FEV,, maximal midexpiratory flowrate (MMEF), and forced vital capacity (FVC) with a Type S Vitallograph spirometer (Buckingham, England). During exercise the heart rate was monitored with a 3-lead ECG Life Trace monitor (Albury Instruments, London, England). Inspiratory rates of ventilation were measured with a Morgan Ventilometer Mark 2 (PK Morgan Ltd, Kent, England). All subjects were acquainted with all apparatus before testing was begun. The ambient temperature varied from 2 1 to 26 "C and relative humidity from 50 to 60 % during these tests. For the asthmagenic treadmill test, the starting treadmill speed was chosen according to each subject's athletic ability. The treadmill speed was increased during the first 2 to 3 minutes until the heart rate reached 80% of the predicted maximum heart rate for age. The subjects continued to run on the horizontal treadmill at the target speed for a further 6 minutes or until they developed symptomatic EIA. Lung function was measured before and at 2,4, 6, 8, 10, 15, 20,25, and 30 minutes after cessation of running. Only one spirometer recording was performed unless a particularly poor effort was noticed. If the EIA was severe enough to prevent recording of FEV, or FVC, these values were recorded as zero. These tests were performed twice on separate days for each subject before and after the trial period. The subject completed the first test without premedication; prior to the second test appropriate premedication was provided. The maximal rate of oxygen consumption (VOzmax), the peak treadmill running velocity, and the lactate turnpoint were measured using a continuous horizontal treadmill protocol as previously described (8). Five minutes before the start of the test, subjects were required to take their prescribed medication and, in addition, two metered doses of fenoterol hydrobromide aerosol (2 X 200 mcg: Berotec, Boehringer Ingelheim) and 20 mg of sodium cromoglycate powder (Lomudal, Fisons). Thereafter a 22G Jelco teflon intravenous catheter placement unit (Critikon, Tampa, FL) was inserted into a forearm vein from which blood samples were drawn continuously for determination of blood lactate concentrations as previously described (8). During these tests, subjects ran with a nose clip to prevent nasal breathing; heart rate and ventilation were measured as previously described. Expired air was directed through clear-bore 35-mrn tubing into a 15-1 mixing chamber from where it was continuously sampled through Drierite anhydrous CaSO, (Vacumed Inc., Ventura, CA) to the inlet ports of an Ametek Oxygen Analyzer Model S3AI (Applied Electrochemistry, Ametek Inc., Pittsburgh, PA) and an Ametek Carbon Dioxide Analyzer, Model CD3A (Applied Electrochemistry, Ametek Inc., Pittsburgh). The ouputs of the analyzers were recorded on a Four Channel Chart Recorder model N (Mennen Medical Ltd., Rehovot, Israel). Rates of oxygen consumption, carbon dioxide production, and respiratory exchange ratio were calculated according to conventional equations (8). Blood samples were collected every 60 seconds during the test, mixed with ice-cold 10% perchloric
4 140 - King, Noakes, and Weinberg acid, and stored frozen for later analysis as previously described (8). The blood lactate turnpoint was determined visually (8). The exercise training sessions were held twice weekly and lasted for 90 minutes each. Each training session consisted of a short warm-up period, stretching exercises, calisthenics, strengthening exercises, breathing exercises, interval training, and team games such as soccer. Swim training was also included. The emphasis was on intense, intermittent activities alternating with periods of rest. If a subject developed bronchoconstriction, he stopped his activity, used a beta-2 stimulant aerosol, and rested. He returned to activity when he felt better, restarting at a low exercise intensity. Statistical Methods The paired Ttest was used for within-group comparisons of measurements made before and after the trial period. The two-sample T test was used to compare between-group differences before and after the trial period (Statpak, Northwest Analytical, Inc., Portland, OR). Physical Characteristics Results The boys in the exercise group were older and taller than those in the control group but the differences were not statistically significant. Boys in both groups grew significantly taller QK0.05) during the trial period and showed a significant decrease in percent body fat during the study QK0.05: control group; p<0.005: exercise group). Body mass did not change significantly in either group. Measurements of Maximal Treadmill Performance The trained subjects, but not the control group, achieved a significantly higher maximal treadmill velocity after see Table 2). The difference between the mean group changes in this variable was also statistically The V0,max also increased significantly with training only in the trained group w.05; see Table 2). Maximum rates of ventilation and heart rate did not -alter with training (data not shown). The blood lactate concentration at the maximal treadmill speed achieved during the initial treadmill test was compared to the blood lactate concentration at the corresponding speed during the final treadmill test. No significant changes occurred in blood lactate concentration in either group after the trial period (Table 2). Although the blood lactate turnpoint did not alter significantly with training, after the trial period the lactate turnpoint occurred at a higher treadmill velocity in the trained-than in the control group (Table 2). Measurements During the Asthmagenic Treadmill Run Without Premedication. Three subjects in the exercise group and two in the control group were able to complete the prescribed 8 minutes of treadmill running before and after the trial period without prernedication. One subject in the exercise group and two in the control group increased their run times during the final exercise test.
5 Table 2 Physiological Effects and Asthma Effect of Training on Physiological Parameters Measured During Maximal Exercise Exercise group Control group 0 3 mos. 0 3 mos. ~0,max (ml kg-l min-l) ~0,max (I min-') Maximum treadmill velocity (km h-') Peak blood lactate level (mmol I-') o Treadmill velocity at the lactate turn point (km h-') 1.9 Values are expressed as M * SD. 'W0.05 trained vs. control group. *p<0.05, time 0 vs. 3 mos.; *'p<0.005, time 0 vs. 3 mos. As the final run time was greater than or equal to the initial run time for most of the subjects, the heart and ventilation rates during the final minute of the initial test were compared to the corresponding minute in the final test. Ventilation rates did not change significantly after the trial period in either group, but the exercise group showed a significant reduction in mean heart rate after the trial period (190+6 vs. 182 f 7; pre vs. post; p<0.05). With Premeditation. Mean run times, ventilation, and heart rates increased with the use of premedication in both groups both before and after the trial period. However, only ventilation and treadmill run time increased significantly with premedication in the control group after the trial period. The mean postexercise values for lung function are not directly comparable because of the differing run times. However, mean values for PEFR, MMEF, FEV,, and FVC did not change significantly after the trial period in either group (Table 3). There were also no significant intergroup differences, although control subjects appeared to have less severe EIA both before and after the trial period. Status of Clinical Asthma The posttrial questionnaire revealed that more boys in the exercise group used aerosol and other medication less frequently, reported being more active physically, and experienced fewer asthmatic episodes compared to those in the control group (Table 4). These responses were confirmed by physicians who reported a reduction in the amount of medication prescribed for the boys in the exercise group.
6 142 - King, Noakes, and Weinberg Table 3 Mean Maximal Postexercise Percentage Falls in Parameters of Lung Function Exercise group Control group 0 3 mos. 0 3 mos. PEFR FEV, MMEF FVC Note. Values are expressed as M * SD. Table 4 Change in Behavioral Variables Relating to Severity of Clinical Asthma Less frequent Less frequent phys. prescrip. of: use of: More Fewer Oral Meds Inhaler active attacks Inhaler steroids Exercise (n = 24) Control (n=5) Note. Meds = oral theophylline tablets; lnhaler = fenoterol hydrobromide aerosol inhaler. Thus, at the end of the study two trained subjects continued to use fenoterol aerosols compared to all six boys in the control group. Oral corticosteroid medication was discontinued in the one boy in the exercise group who had used this medication prior to the start of the study. In contrast, the two boys in the control group who used corticosteroids continued to do so. No additional asthma medication was started in either group during the trial period.
7 Discussion Physiological Effects and Asthma This study shows that children with exercise-induced asthma can improve their absolute and relative V02max values and increase their maximal treadmill running velocities following a period of specific training. There was also a reduction in heart rate during submaximal exercise in the trained group. Although the lactate turnpoint did not alter with training, it occurred at a significantly higher treadmill velocity in the trained than in the control subjects at the completion of the study. Despite these changes, all of which indicate enhanced physical fitness in the trained children, there was no objective evidence that the severity of EIA was influenced by training. Thus, the peak percentage falls in PEFR, FEV,, MMEF, and FVC after the asthmagenic exercise test were as great in the trained group at the end of the study as they had been at the start. Despite this, the severity of clinical asthma in the trained group would seem to have improved. This was shown by a reported reduction in the frequency of asthma attacks, the reduced use of medication for the control of asthma, and a general increase in physical activity. In summary, this study confirms that children with moderately severe asthma can be trained successfully to improve their aerobic fitness (2,7, 11, 13) without adverse effect on their EIA. In addition, the study suggests that exercise training may influence the course of clinical asthma without altering susceptibility to EIA. This possibility deserves further study. References 1. Arborelius, M., and E. Svenonius. Decrease of exercise-induced asthma after physical training. Europ. J. Respir. Dis. (Suppl. 136), 65:25-31, Bundgaard, A., T. Ingemann-Hansen, A. Schmidt, and J. Hallcjaer-Kristensen. Effect of physical training on peak oxygen consumption rate and exercise-induced asthma in adult asthmatics. Scand. J. Clin. Lab. Invest. 42:9-13, Eggleston, P.A. Section 11. Exercise challenge: Indications, techniques and data analysis. J. Allergy Clin. Zrnmunol. 64: , Fitch, K.D., A.R. Morton, and B.A. Blanksby. Effects of swimming training on children with asthma. Arch. Dis. Child. 51: , Henriksen, J.M., and T.T. Nielsen. Effect of physical training on exercise-induced bronchoconstriction. Acta. Paediat. Scand. 72:31-36, Hyde, J.S., and C.L. Swarts. Effect of an exercise program on the perennially asthmatic child. Am. J. Dis. Child. 116: , Itkin, I.H., and M. Nacman. The effect of exercise on the hospitalised asthmatic patient. J. Allergy 37: , Matter, M., T. Stittfall, J. Graves, K. Myburgh, B. Adams, P. Jacobs, and T.D. Noakes. The effect of iron and folate therapy on maximal exercise performance in female marathon runners with iron and folate deficiency. Clin. Sci. 72: , McElhenney, T.R., and K.H. Petersen. Physical fitness for asthmatic boys. J.A. M. A. 185: , Nickerson, B.G., D.B. Bautista, M.A. Namey, W. Richards, and T.G. Keens. Distance running improves fitness in asthmatic children without pulmonary complications or changes in exercise-induced bronchospasm. Pediatrics 7 1 : , 1983.
8 144 - King, Noakes, and Weinberg 11. Orenstein, D.M., M.E. Reed, F.T. Grogan, and L.V. Crawford. Exercise conditioning in children with asthma. J. Pediatr , Oseid, S., and K. Haaland. Exercise studies in asthmatic children before and after regular physical training. In Swimming Medicine N, B. Eriksson and B. Furberg (Eds.). Baltimore: University Park Press, 1978, pp Ramazanoglu, Y.M., and R. Kraemer. Cardiorespiratory response to physical conditioning in children with bronchial asthma. Pediatr. Pulmonol. 1 : , Schnall, R., P. Ford, I. Gillam, and L. Landau. Swimming and dry land exercises in children with asthma. Aust. Paediatr. J. 18:23-27, Silverman, M., and S.D. Anderson. Standardization of exercise tests in asthmatic children. Arch. Dis. Child. 47: , Sly, R.M., R.T. Harper, and I. Rosselot. The effect of physical conditioning upon asthmatic children. Ann. Allergy , Acknowledgments This work was funded by the Medical Research Council of South Africa, the Duncan Baxter, Nellie Atkinson, and Harry Crossley Research Funds of the University of Cape Town, and the South African Association for Sport Science, Physical Education and Recreation.
Keywords: asthma; swimming training; exercise training; children; lactate threshold; bronchial responsiveness
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