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Jornal Brasileiro de Pneumologia

Print version ISSN 1806-3713On-line version ISSN 1806-3756

J. bras. pneumol. vol.30 no.2 São Paulo Mar./Apr. 2004 



Exercise-induced bronchospasm in children and adolescents with a diagnosis of asthma*



Vitor E. Cassol; Maria E. Trevisan; Eliane Z. C. de Moraes; Luiz O. C. Portela; Sérgio Saldanha Menna Barreto(TE SBPT)





INTRODUCTION: In asthmatic children and adolescents a high incidence of temporary bronchospasm is perceived after physical exertion.
OBJECTIVE: To investigate incidence and severity of exercise-induced bronchospasm in children and adolescents with a clinical diagnosis of mild, moderate or severe asthma.
METHOD: A descriptive, cross-sectional, not controlled study was carried out. The sample encompassed follow-up of 40 asthmatic patients of both genders, between 7 and 18 years of age who were not regularly using anti-inflammatory medication. A standardized exercise provocation test that consisted of steady running on a treadmill with a 10% inclination was administered Pulmonary function was tested with forced spirometry using six expiratory maneuvers repeated at approximately 1, 5 ,10,15, 20 and 30 minutes after the exercise. The highest of six FEV1 readings was used for analysis. The FEV1 was employed to evaluate the presence and to classify the severity of positive exercise induced bronchospasm (EIB). The asthmatic patients presented adequate clinical and spirometric conditions for testing (FEV1 at least 70 % of the predicted value). A drop of > 10% in relation to FEV1 before exercise was adopted as a criterion for (EIB).
RESULTS: 26 (65 %) patients developed EIB. The proportion by category was: mild asthma 44%, moderate and severe asthma 100%. There was a significant association between proportion of EIB and severity of asthma (p<0.05), and a significant difference between severity of EIB (confirmed by a recorded decrease in the 1 second forced expiratory volume) and asthma severity (p<0.05).
CONCLUSION: The proportion and severity of EIB were clearly related to the clinical severity of asthma.

Key words: Asthma, exercise-induced/diagnosis. Children. Adolescent. Spirometry/methods.



Abbreviations used in this paper:
EIB – Exercise-induced bronchospasm
FEV1 – Forced expiratory volume in one second
FEF25-75% – Forced expiratory flow between 25% and 75% of forced vital capacity
PEF – Peak expiratory flow
FVC – Forced vital capacity
HR – Heart rate



Many centuries ago, Aretaeus of Cappadocia stated, “If from running, gymnastic exercise, or any other work, the breathing becomes difficult, it is called asthma.” However, the empirical establishment of a relationship between physical exertion and asthma came only recently.(1) Studies on exercise-induced bronchospasm (EIB) were first conducted in the 1960s by Jones et al. and later by others.(2,3,4,5) These various authors clearly showed that EIB is a characteristic of asthmatic children and young people and established a relationship between EIB pattern changes and clinical severity of the disease.(2-5)

Asthma manifests most commonly as airway hyperreactivity to various physical, chemical, pharmacological, or immunological stimuli, resulting in bronchoconstriction.(6) Temporary bronchoconstriction that occurs after a relatively short period of physical exertion is called exercise-induced asthma or EIB.(7) When patients are submitted to bronchial provocation tests, changes in pulmonary function generally appear within 2 to 4 minutes, peak within 4 to 8 minutes, and spontaneously return to the pre-exercise level within 20 to 40 minutes.(8) Many children and teenagers have difficulty breathing during physical activities, games, training sessions, and competitions and are unaware of the source of the problem.(9) In many cases, EIB may be the cause. This is especially problematic for children, preventing them from participating in a variety of activities compatible with their age, since many of these activities involve physical exertion.(10) A study conducted in the USA showed that 30% of asthmatic children are limited in their capacity for physical activity, whereas only 4.5% of the overall pediatric population is similarly limited.(11)

The prevalence of EIB in asthmatic patients ranges from 13% to 90%, according to various authors.(12,13,14) Bar-Or stated that, when challenged in laboratory tests, 40% to 95% of asthmatic patients have an EIB response.(8) The discrepancies among the results from these studies is attributable to disparities among the protocols employed, lack of standardization of ambient temperature and humidity, inconsistencies in standards for pre-testing discontinuation of medication, variations in disease severity and lack of a consensus regarding positive EIB test criteria.

In Brazil, the first EIB studies were carried out in the 1980s.(15,16,17,18) These studies have allowed for better understanding of this problem in our country. However, the lack of testing standards, together with the adoption of disparate protocols, still casts doubt on the incidence and degree of EIB in asthmatic children and adolescents.

The objective of this study was to increase knowledge of EIB and to determine its incidence and degree in a group of children and adolescents diagnosed with mild, moderate or severe asthma, based on a standardized treadmill test.



The present study was carried out from 1995 to 2001 in the Pediatric Pulmonology Clinic of the Hospital Universitário de Santa Maria and in the Exercise Physiology and Human Performance Laboratory of the Universidade Federal de Santa Maria (UFSM).

The convenience sample comprised 40 children and adolescents clinically diagnosed with mild, moderate or severe asthma, according to the classification system described in the Guidelines for the Diagnosis and Management of Asthma published by the (American) National Heart, Lung and Blood Institute.(19) Patients were selected without regard for disease severity or previous history of EIB. Patients were of both genders, from 7 to 18 years of age, and were being treated as outpatients.

In selecting the sample, we sought patients who had been clinically diagnosed with asthma, defined as having had 3 or more episodes (involving dyspnea or wheezing and sudden cough) that responded positively to bronchodilators. We employed the following exclusion criteria: presence of other chronic lung diseases, tobacco use and regular use of oral or inhaled anti-inflammatory medication (corticoids, cromoglicate, nedocromil or antileukotriene).

In addition, patients suffering from acute asthma attacks during the study period, or exhibiting symptoms compatible with viral infection (cold, influenza) in the last 6 weeks prior to the exam, were excluded. All patients underwent at-rest pulmonary function testing (spirometry) prior to the exam, and patients presenting forced expiratory volume in one second (FEV1) less than 70% of the predicted value according to gender, height, and age were also excluded.

The children and adolescents that comprised our study sample had discontinued regularly use of maintenance medication at least 4 weeks prior to the study, as attested to by their parents or by the subjects themselves. More than 4 weeks prior to the study, two patients diagnosed with moderate asthma had used inhaled cromoglicate, and other 3 patients diagnosed with severe asthma had used inhaled beclomethasone.

Patients were instructed to discontinue use of asthma medications for a certain period prior to the test. This period was 8 hours for those using oral or inhaled short-acting bronchodilator, short-acting theophylline or anticholinergic drugs, 12 hours for those using long-acting bronchodilators or long-acting theophylline, 24 hours for those using short-acting antihistamines, and 72 hours for those using long-acting antihistamines.

The provocation test (running) was carried out on a treadmill (model ESD-01, FUNBEC, São Paulo, Brazil) with automatic mode control, as well as speed (km/hour), and inclination (percentage) indicators.

Patients reached maximal exertion after running for 6 to 8 minutes on the treadmill at 10% inclination, with the speed controlled by the examiner. The speed was regulated in such a way that patients attained 75% to 85% of their age-predicted maximum heart rate (HR) within the first 2 minutes and maintained that rate between 85% and 90% until the end of the test.

Heart rate was monitored with a model Vantage XL heart rate monitor (Polar Electro, Kempele, Finland).

A computer-assisted spirometer (model 1.91, Circardian, California, USA) was used for pulmonary function tests. Six FEV1 maneuvers were executed, and the highest reading was recorded. Pulmonary function tests were performed prior to the provocation test and then again at 1, 5, 10, 15, 20, and 30 minutes after the test.

Recorded FEV1 values were used to evaluate the presence and severity of EIB. Patients were considered positive for EIB when there was a 10% or greater increase in FEV1 within the first 30 minutes after the test in relation to the at-rest FEV1 value obtained prior to the test. The classification system developed by Anderson20 was used to determine the severity of EIB. That system is based on FEV1 values and defines drops of 10% to 20% as mild EIB, 25% to 35% as moderate EIB, 35% to 50% as moderate to severe EIB, and greater than 50% as severe EIB. Tests were performed in the mornings, in a climate-controlled environment in which room temperature was maintained between 20°C and 25°C and relative humidity between 55% and 65%.

The database was compiled using Epi-Info software, version 6.04, and statistical analysis was made using SAS (Statistical Analysis System) software. In order to compare differences between asthmatic patients who did or did not present EIB and to determine the relationship between asthma severity and severity of EIB, data were submitted to chi-square test with a 5% significance level, analysis of variance (ANOVA) and Duncan’s test.

The Research Ethics Committee of the Centro de Ciências da Saúde of the UFSM approved the study. Data collection did not begin until after the parents or legal guardians of all patients had given written informed consent.



In the study group of 40 asthmatic children and adolescents, results were analyzed to determine presence or absence of EIB and, in those presenting EIB, the relationship of EIB incidence to the clinical diagnosis of mild, moderate and severe asthma. In the group of 26 who presented EIB, the results were analyzed to determine the relationship between EIB and the severity of asthma.

Demographic data (age, weight, and height) for the 40 children and adolescents diagnosed with mild, moderate or severe asthma are shown in Table 1. Table 2 shows EIB incidence within the study group. Table 3 relates EIB severity to asthma severity. Baseline FEV1 values for the 26 children and adolescent who presented EIB are listed in Table 4, and Table 5 shows the Duncan’s test results of the percentage of FEV1 decrease within the same group of patients.












Godfrey,(21) using studies on the physiopathology of EIB conducted within the past few years, developed a model for EIB that allows modifications to be made according to the evolution of knowledge regarding the condition. The design of the model makes it clear that EIB is variable (since there are various factors that interact to cause bronchoconstriction) and that the severity of the response to exercise is unpredictable (since some variables can not be quantified). In addition, the author emphasizes that standardization of the test and test environment, as well as control of allergic factors, is imperative when bronchial provocation tests are administered to a patient or group of patients.

Within this group of 40 patients, all of whom underwent standardized provocation testing, there was a 65% rate of EIB positivity. This rate is comparable to those ranging from 45% to 100% reported by various other authors(22,23,24) if we consider only studies involving the same type of exercise (running on a treadmill). This finding is also in agreement with that of Bar-Or,(8) who reviewed the literature and reported that positive EIB values ranging from 40% to 95% are obtained with asthmatic patients undergoing provocation tests under controlled variables in laboratory. The author states that, although there are various factors that determine the high variability in EIB incidence, a decrease in FEV1 of at least 10% to 15% is expected in approximately 70% of children diagnosed with perennial asthma if bronchodilator medication is discontinued 6 to 8 hours prior to the bronchial provocation test. In the present study, 100% of patients diagnosed with moderate or severe asthma presented EIB. This value is significantly higher than that reported by Bar-Or.(8)

In comparing the present study to other studies testing patients under similar conditions and analyzing variables such as type of exercise, workload, test duration and age, we found some similarities, Our result of 65% positivity for EIB is similar to that obtained by Silverman & Anderson,(25) who used a 10% decrease in peak expiratory flow (PEF) as a diagnostic criterion and reported EIB in 70% of cases. However, other findings are contradictory. Shapiro et al.(26) used a 10% decrease in FEV1 as their diagnostic standard and reported only a 56% incidence of EIB, and Godfrey(21) found that 79% of patients exhibited EIB. The differences between results in these studies might be due to, among other variables, differences in degree of asthma severity among the study subjects.

Nascimento et al.(15) studied prevalence of EIB in 40 young patients clinically diagnosed with asthma. The authors employed a cycloergometer as the provocation test and, when a 20% decrease in FEV1 was used as the diagnostic standard, obtained results of only 35% EIB (14 patients). However, the overall EIB prevalence was 47.5% when forced expiratory flow between 25% and 75% of forced vital capacity (FEF25-75%; 15 patients), PEF (8 patients) and forced vital capacity (FVC; 6 patients) were also considered. The higher incidence in our study is likely due to the less stringent diagnostic standard adopted (a 10% or greater drop in FEV1) and to the fact that the provocation test was performed on a treadmill, which creates greater bronchial provocation.(9)

Sano et al.,(17) studying EIB in 45 asthmatic children submitted to a cycloergometer provocation test, adopted a 20% decrease in PEF as a measure of EIB positivity and reported a 14% prevalence, considerably lower than that found in our study. This is undoubtedly due to the diagnostic standard set and to the fact that provocation tests on a cycloergometer have a lower asthma-inducing effect than those performed on a treadmill. Rosov,(16) in a study of children and adolescents with asthma (25% mild, 7% moderate and 68% severe), used a cycloergometer (at submaximal effort) and defined EIB positivity as a 10% decrease in FEV1 or PEF.(3) The author found a 66.5% incidence of EIB, similar to that found in our study, although most of the patients in that study had severe asthma. However, in the Rosov study, tests were performed on a cycloergometer, whereas, in our study (in which most of the patients had mild or moderate asthma) tests were performed on a treadmill. In a subsequent study, Sano et al.,(18) testing 30 asthmatic children on a cycloergometer and using a 20% decrease in FEV1 as the diagnostic definition of EIB, reported an incidence of 33%, also considerably lower than that found in our study. This discrepancy may be explained by the diagnostic criterion, the type of provocation test and the slightly higher relative ambient humidity (55% to 75%) employed by the authors.

The present study demonstrated an increase in the incidence and severity of EIB in patients with severe asthma, which is in agreement with various studies in which the level of bronchial responsiveness was correlated with the severity of asthmatic symptoms.(27,28,29,30,31,32,33) Lee et al.(34) and Mahler(35) consider asthma severity one of the most critical factors affecting the incidence and degree of EIB.

More recently, Cabral et al.(36) studied the effect of asthma severity on the incidence of EIB in asthmatic children in Brazil. The children studied were not treated with inhaled corticoids, and the prevalence of EIB was found to be 45.7%. Significantly, children with more severe asthma responded (presented EIB) more frequently. This study also revealed differences in the intensity of bronchial responsiveness between patients diagnosed with intermittent asthma and those diagnosed with persistent asthma. However, there were no differences found among the different degrees of persistent asthma severity. These results are in accordance with ours, although the authors reported a lower EIB prevalence, possibly due to the fact that the bronchial provocation test was performed on a cycloergometer with lower level of exertion (80% of maximum heart rate). However, our study also revealed differences in the incidence and severity of EIB between the moderate and severe forms of persistent asthma.

Based on our results, we can conclude that the incidence and severity of EIB is related to the clinical severity of asthma. This is in accordance with various other studies, although the present study also revealed differences among studies in relation to the incidence and severity of the EIB reported. These differences can be explained by the type of provocation testing employed, since treadmill testing, such as that used in our study, is considered to be more effective at inducing asthma than are other means of provocation testing.



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Vitor Emanuel Cassol
Pinheiro Machado 2350, CEP: 97050-600
Phone: (55)222-3033 Fax: (55)263-2208

Submitted: 4 February 2003.
Accepted, after revision: 3 December 2003.
Financial support from and equipment supplied by: the Universidade Federal de Santa Maria



* Study carried out at the Universidade Federal de Santa Maria, RS.

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