Brazilian Journal of Pulmonology

ISSN (on-line): 1806-3756 | ISSN (printed): 1806-3713


Publication continuous and bimonthly

SCImago Journal & Country Rank
Advanced Search


Current Issue: 2012 - Volume 38 - Number 4 (July/August)


Children and adolescents with mild intermittent or mild persistent asthma: aerobic capacity between attacks

Capacidade aeróbica em crianças e adolescentes com asma intermitente e persistente leve no período intercrises


Eliane Zenir Corrêa de Moraes; Maria Elaine Trevisan; Sérgio de Vasconcellos Baldisserotto; Luiz Osório Cruz Portela



Objective: To assess children and adolescents diagnosed with mild intermittent or mild persistent asthma, in terms of their aerobic capacity between attacks. Methods: We included 33 children and adolescents recently diagnosed with asthma (mild intermittent or mild persistent) and 36 healthy children and adolescents. Those with asthma were evaluated between attacks. All participants underwent clinical evaluation; assessment of baseline physical activity level; pre- and post-bronchodilator spirometry; and a maximal exercise test, including determination of maximal voluntary ventilation, maximal oxygen uptake, respiratory quotient, maximal minute ventilation, ventilatory equivalent, ventilatory reserve, maximal HR, SpO2, and serum lactate. Results: No significant differences were found among the groups (intermittent asthma, persistent asthma, and control) regarding anthropometric or spirometric variables. There were no significant differences among the groups regarding the variables studied during the maximal exercise test. Conclusions: A diagnosis of mild intermittent/persistent asthma has no effect on the aerobic capacity of children and adolescents between asthma attacks.



Objetivo: Aferir a capacidade aeróbica de crianças e adolescentes com diagnóstico de asma brônquica intermitente leve ou persistente leve no período intercrises. Métodos: Foram estudadas 33 crianças e adolescentes com diagnóstico clínico recente de asma leve intermitente e asma leve persistente, no período intercrises, e 36 crianças e adolescentes saudáveis. Foram realizadas avaliação clínica, avaliação do nível basal do nível de atividade física, espirometria antes e após o uso de broncodilatador e determinação de ventilação voluntária máxima, consumo máximo de oxigênio, quociente respiratório, ventilação minuto máxima, equivalente ventilatório, reserva ventilatória, FC máxima, SpO2 e lactato. Resultados: Não foram encontradas diferenças significativas entre os grupos asma intermitente, asma persistente e controle em relação às variáveis antropométricas e espirométricas. Não houve diferenças significativas em relação às variáveis analisadas durante o teste de esforço máximo entre os grupos. Conclusões: O diagnóstico de asma intermitente ou persistente leve não influenciou a capacidade aeróbica em crianças e adolescentes no período intercrises.



Keywords: : Asthma; Exercise; Respiratory function tests.


Palavras-chave: Asma; Exercício; Testes de função respiratória.




Asthma is a chronic inflammatory disease characterized by lower airway hyperresponsiveness and variable airflow limitation that can resolve spontaneously or with treatment; the clinical manifestations of asthma include recurrent episodes of wheezing, dyspnea, chest tightness, and cough, particularly at night and upon waking in the morning.(1) Exercise capacity expresses the temporal state of acute and chronic physiological adaptations in individuals. The temporal component implies that those adaptations have transitory and lasting effects. There is a consensus that, during an attack, asthma patients experience a considerable reduction in exercise capacity, which can be recovered as soon as the attack is controlled. However, because asthma symptoms lead to impaired health-related quality of life, many asthma patients choose to adopt a sedentary lifestyle.(2-4) Although it is commonly believed that children with asthma have reduced aerobic capacity, there are conflicting data in the literature.(5) Although recent studies have suggested that reduced aerobic capacity is related to greater disease severity,(6) the impact of asthma on patients with less severe disease remains unclear.

Because asthma is the most prevalent chronic disease in children and adolescents, because most asthma patients have mild intermittent or mild persistent disease,(1) and because regular physical activity has been proven to have beneficial effects,(7-9) it is essential to determine whether asthma has negative effects on exercise capacity between attacks, the approach to physical training being based on the answer to this question. Therefore, the objective of the present study was to assess children and adolescents with mild intermittent or mild persistent asthma, in terms of their aerobic capacity between attacks.


We evaluated 33 children and adolescents recently diagnosed with mild intermittent or mild persistent asthma and 36 healthy children and adolescents (control group). All participants were in the 11-14 year age bracket, those with asthma having been evaluated between attacks. None of the asthma patients were receiving inhaled corticosteroid therapy at the time of enrollment. The asthma patients were recruited from among those being treated at the pediatric outpatient clinic of the Santa Maria University Hospital, located in the city of Santa Maria, Brazil. The diagnosis and severity of asthma were established in accordance with the Global Initiative for Asthma criteria.(1) Stable disease was defined as no attacks or medication changes in the last 90 days. We excluded children/adolescents with other respiratory diseases, those with symptoms of viral infection (cold and flu) in the last six weeks, and those with abnormal at-rest pulmonary function test (spirometry) results on the day of the test. We ruled out asthma and allergic rhinitis in the control group by administering the International Study of Asthma and Allergies in Childhood questionnaire,(10,11) a negative answer to question 2 and a total score < 6 indicating the absence of the two diseases. We determined the level of physical activity by administering the International Physical Activity Questionnaire (IPAQ), short version.(12,13) We used the Lohman equation to calculate the percentage of body fat.(14)

The present study was approved by the Research Ethics Committee of the Federal University of Santa Maria Health Sciences Center. The parents or legal guardians of all participants gave written informed consent.

Spirometry was performed with a Vmax Series 229 spirometer (SensorMedics, Yorba Linda, CA, USA) before and after the administration of 400 µg of inhaled albuterol, having been performed in accordance with the acceptability and reproducibility criteria established by the American Thoracic Society(15) and the reference values proposed by Knudson et al.(16) In addition to measuring the spirometric values, we measured maximal voluntary ventilation (MVV), and the volumes were corrected for body temperature, ambient pressure, and saturated air.

Exercise testing was performed on a 10200 ATL treadmill (Inbramed, Porto Alegre, Brazil), in accordance with the protocol proposed by Mader et al.,(17) until maximal voluntary effort was achieved. Twenty minutes before the exercise test, we administered 400 µg of inhaled albuterol with a spacer, in order to prevent exercise-induced bronchospasm. Maximal oxygen uptake (VO2max), respiratory quotient (RQ), minute ventilation (VE), and ventilatory equivalent for oxygen (VE/VO2) were measured with the abovementioned spirometer (SensorMedics), whereas serum lactate was measured with a glucose/lactate analyzer (model Biosen 5030; EKF Diagnostics, Cardiff, UK). Blood samples were collected at the end of each stage (5 min). We monitored HR with an Accurex PlusT HR monitor (Polar Electro Ou, Kempele, Finland). All variables were measured at rest, during exercise, and during recovery.

The pulmonary function test and the exercise test were performed in a climate-controlled environment, i.e., at a temperature of 18-26°C and a relative humidity of 55-60%.

The data collected were evaluated for normality by the Shapiro-Wilk test (n < 2,000), and descriptive statistical analysis was performed. The variables age, height, body mass, percentage of body fat, FVC, FEV1, FEV1/FVC, PEF, MVV, VO2max, ventilatory reserve, VE/VO2, RQ, and International Study of Asthma and Allergies in Childhood questionnaire score showed normal distribution, ANOVA being therefore used in order to compare the means. The variables that showed statistically significant differences, namely pre-bronchodilator FEV1 and FEV1/FVC (both in % of predicted), were analyzed by Duncan's post hoc test. The variables that showed non-normal distribution, namely IPAQ score, running speed, exercise duration, maximal HR, and serum lactate, were analyzed by the Kruskal-Wallis test. All statistical analyses were performed with the program Statistical Analysis System, version 8.2 (SAS Institute, Cary, NC, USA).


The anthropometric characteristics were similar among the three groups studied (mild intermittent asthma, mild persistent asthma, and control), as were the physical activity characteristics. As shown in Table 1, ANOVA showed no statistically significant differences among the groups regarding age, body mass, height, or percentage of body fat; in addition, the Kruskal-Wallis test showed no statistically significant differences among the groups regarding the level of physical activity, as measured by the IPAQ score.

As expected, there were no significant differences among the groups regarding pulmonary function test results (Table 2). Although we found a significant difference among the groups regarding pre-bronchodilator FEV1/FVC (% of predicted), the means were above 80%, which is considered normal for the age group under study. The results showed no airway obstruction, confirming that the children and adolescents were between attacks. As can be seen in Table 2, there were no significant differences among the groups regarding MVV (in absolute values or in % of predicted). There were no statistically significant differences among the groups regarding the variables analyzed during the maximal cardiopulmonary exercise test, namely maximal VE (VEmax), ventilatory reserve, VE/VO2, RQ, maximal HR, VO2max, serum lactate, maximum speed attained, and exercise duration (Table 3).


The objective of the present study was to assess children and adolescents with mild asthma, in terms of their aerobic capacity between attacks. We chose to study patients with mild intermittent or mild persistent asthma because these are the most prevalent forms of the disease.

Although different levels of baseline physical activity can influence the results of studies such as ours, we found no statistically significant differences among the groups in terms of baseline physical activity, as measured by the IPAQ score. The three groups studied were classified as being physically active.(12) The results of the tests performed showed that the physical performance of the individuals in the control group was better than was that of those in the asthma groups. We believe that this was due to higher routine physical activity in the control group, given that the possibility of experiencing attacks during exercise might prevent the asthma patients from engaging in physical activity more often. However, because the IPAQ is not appropriate to determine that and because this is outside the scope of the present study, we cannot draw definitive conclusions.

Obesity is another variable that affects the physical performance of individuals with or without asthma. According to the classification proposed by Lohman,(14) the percentage of body fat in the three groups studied was optimal. Therefore, the results of the present study should be analyzed from the perspective that the individuals studied were physically active and had an adequate percentage of body fat, which was similar among the three groups.

Group homogeneity is important when the objective is to compare individuals with asthma of varying severity and those without in terms of their aerobic capacity. Homogeneity reduces the variability in pulmonary evaluation results. As shown in Table 2, none of the patients studied had airflow obstruction at the time of the evaluation (exclusion criterion), all had normal pre- and post-bronchodilator spirometry, and the possibility of exercise-induced asthma, a potential confounding variable during a maximal cardiopulmonary exercise test, was controlled by administering albuterol (400 µg) 20 min before the test. In the present study, the difference, albeit small, between the asthma patients and the controls regarding at-rest spirometry results was suggestive of reduced aerobic capacity during exercise. However, this proved not to be the case.

Defined as the maximum volume of air that an individual can inhale and exhale in 1 min during maximal voluntary effort, MVV provides a nonspecific overview of respiratory function. Moderate and severe obstructive pulmonary disease can result in abnormal MVV values; this is due to excessive air trapping and respiratory muscle disadvantage, which is common in patients with such breathing patterns.(18) The MVV that individuals can achieve depends on the integrity of their respiratory physiology. In all three groups, MVV values remained within the reference range, indicating that the individuals with asthma and those without had similar ventilatory capacity.

We found that MVV was higher than the maximal levels of ventilation during exercise, a finding that is consistent with the literature. This is due to the fact that, during exercise, the respiratory system is not required to work to the utmost. Studies suggest that specific exercises for individuals with obstructive pulmonary disease are interesting because training can increase respiratory muscle strength, respiratory muscle endurance, and MVV.(19)

If any type of organ dysfunction or adaptation is expected to occur as a result of the severity of asthma, it will necessarily be expressed by VO2max, which is a measure that includes the performance of the various systems involved in the mechanism of oxygen consumption. It reflects cardiovascular, pulmonary, and muscular components, being considered the best single index of health-related physical fitness.(20) The VO2max values obtained in the present study were similar to those reported in several studies involving children and adolescents.(20-22)

In the present study, VO2max was found to be similar among the three groups, a finding that is consistent with those of a study evaluating exercise performance in 80 children with mild to moderate asthma and 80 healthy children. The two groups were found to be similar in terms of aerobic capacity, as assessed by maximal exercise testing (40.5 ± 8.4 mL  kg−1  min−1 vs. 42.6 ± 9.6 mL  kg−1  min−1).(23) Garfinkel et al.(2) reported similar findings, i.e., no significant differences between stable patients with mild to moderate asthma and controls in terms of VO2max (36.85 ± 10.80 mL  kg−1  min−1 vs. 38.48 ± 5.34 mL  kg−1  min−1; p = 0.32). Baraldi reported that VO2 and VE during submaximal and maximal exercise testing were similar between children with asthma and those without, the two groups of children being therefore similar in terms of aerobic capacity.(24)

The results of the present study are inconsistent with those of a study involving 8 children with asthma and 7 children without; VO2max was significantly lower in the former than in the latter (44 ± 5.4 mL  kg−1  min−1 vs. 55.6 ± 10.3 mL  kg−1  min−1), a finding that was negatively correlated with bronchial obstruction.(25) In another study,(26) a significant difference was found between boys with asthma and those without in terms of VO2max (31.6 ± 5.1 mL  kg−1  min−1 vs. 35.2 ± 6.1 mL  kg−1  min−1) but not between girls with asthma and those without (25.3 ± 2.8 mL  kg−1  min−1 vs. 23.9 ± 4.9 mL  kg−1  min−1). The variation in aerobic capacity across studies comparing individuals with asthma and those without can be explained, in part, by the differences in methods, types, intensities, duration of exercise, level of training, and, first and foremost, identification, characterization, and classification of asthma severity.

The mean VO2max values in the groups under study allow us to conclude that the severity of asthma had no impact on aerobic capacity between attacks. For instance, the mean VO2max in the mild persistent asthma group was nearly equal to that in the control group.

The fact that the three groups studied were similar in terms of VO2max indicates that the responses of the remaining VO2 components do not differ from one another or that possible deficiencies are fully compensated. This answers the question regarding respiratory failure, which has been reported in other studies.(24-26) On the basis of exercise tolerance variables such as VEmax, VEmax/MVV, VE/VO2, and VO2max, we can affirm that neither asthma severity nor ventilatory limitation during exercise influenced aerobic capacity (VO2max) in any of the three groups studied.

The behavior of VEmax in the present study was similar to that reported in other studies, which found no significant differences in VEmax between individuals with asthma and those without, as well as no ventilatory limitation to the work capacity of asthma patients.(27) Ventilatory limitation to exercise capacity can occur in cases of severe asthma, in which complex mechanisms are involved in the pathophysiology of the disease, being unlikely to occur in cases of controlled, mild to moderate asthma.(28) The VEmax values found in the present study confirm the findings of Lewis et al.(28)

Ventilatory reserve is the difference between the maximum ventilation rate that an individual can theoretically achieve (MVV) and the ventilation rate that is actually achieved at a given time point. The VEmax/MVV ratio has been used as an index of ventilatory reserve, or rather of its inverse, meaning that high VEmax/MVV values indicate low ventilatory reserve. Although VEmax/MVV varies widely in males and females, values above 85% for males and above 75% for females (i.e., a ventilatory reserve of 15% and a ventilatory reserve of 25%, respectively) are uncommon in healthy sedentary individuals.(29) Some studies have reported findings that are similar to ours, i.e., no significant differences in ventilatory reserve between children with mild to moderate asthma and those without.(27)

In order to assess breathing economy during exercise, we calculated VE/VO2, which is the ratio between the volume of air ventilated and the amount of oxygen consumed. A higher VE/VO2 translates to lower breathing economy. In the present study, VE/VO2max values ranged from 37 to 69, indicating breathing economy and being consistent with those reported in a study involving children and youths.(30)

Finally, judging from the final result obtained, the period between attacks was clinically well characterized and well selected in the present study. This allowed group homogeneity, which is required to compare individuals with asthma of varying severity and those without in terms of their aerobic capacity. As a result, there were no statistically significant differences between the patients with mild intermittent asthma and those with mild persistent asthma or between the asthma patients and the controls in terms of the spirometric values. This demonstrates that the classification of asthma severity is not supported by the functional variables investigated during the period between attacks. Therefore, the limitations imposed by the criteria for determining asthma severity(3) in the period between attacks do not allow functional differentiation between patients with mild intermittent asthma and those with mild persistent asthma. It could be argued that there are no differences, given that both groups of patients are clinically equal. However, this is not supported by the literature; the results of studies on this topic refer to study groups rather than populations and are discrepant.(5)

The limitations of the present study lie in the fact that our sample was a study group. Therefore, the results reflect the characteristics of the group and those of the methods employed. Because this was not a population-based study, the results obtained cannot be generalized. We conclude that a diagnosis of bronchial asthma (mild intermittent or mild persistent) has no effect on the aerobic capacity of children and adolescents between asthma attacks.


1. Bateman ED, Hurd SS, Barnes PJ, Bousquet J, Drazen JM, FitzGerald M, et al. Global strategy for asthma management and prevention: GINA executive summary. Eur Respir J. 2008;31(1):143-78.

2. Garfinkel SK, Kesten S, Chapman KR, Rebuck AS. Physiologic and nonphysiologic determinants of aerobic fitness in mild to moderate asthma. Am Rev Respir Dis. 1992;145(4 Pt 1):741-5. Erratum in: Am Rev Respir Dis 1992;146(1):269. PMid:1554194.

3. Sociedade Brasileira de Pneumologia e Tisiologia. III Consenso brasileiro no manejo da asma. J Pneumol. 28(Suppl 1):1-51.

4. Hallstrand TS, Curtis JR, Aitken ML, Sullivan SD. Quality of life in adolescents with mild asthma. Pediatr Pulmonol. 2003;36(6):536-43. 10.

5. Welsh L, Roberts RG, Kemp JG. Fitness and physical activity in children with asthma. Sports Med. 2004;34(13):861-70.

6. Villa F, Castro AP, Pastorino AC, Santarém JM, Martins MA, Jacob CM, et al. Aerobic capacity and skeletal muscle function in children with asthma. Arch Dis Child. 2011;96(6):554-9. PMid:21429976.

7. Neder JA, Nery LE, Silva AC, Cabral AL, Fernandes AL. Short-term effects of aerobic training in the clinical management of moderate to severe asthma in children. Thorax. 1999;54(3):202-6.

8. Morris PJ. Physical activity recommendations for children and adolescents with chronic disease. Curr Sports Med Rep. 2008;7(6):353-8. PMid:19005359.

9. Basaran S, Guler-Uysal F, Ergen N, Seydaoglu G, Bingol-Karakoç G, Ufuk Altintas D. Effects of physical exercise on quality of life, exercise capacity and pulmonary function in children with asthma. J Rehabil Med. 2006;38(2):130-5.

10. Solé D, Vanna AT, Yamada E, Rizzo MC, Naspitz CK. International Study of Asthma and Allergies in Childhood (ISAAC) written questionnaire: validation of the asthma component among Brazilian children. J Investig Allergol Clin Immunol. 1998;8(6):376-82. PMid:10028486.

11. Asher MI, Keil U, Anderson HR, Beasley R, Crane J, Martinez F, et al. International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J. 1995;8(3):483-91.

12. Matsudo S, Araújo T, Matsudo V, Andrade D, Andrade E, Oliveira L, et al. Questionário Internacional de Atividade Física (IPAQ): estudo de validade e reprodutibilidade no Brasil. RBAFS. 2001;6(2):5-18.

13. Hallal PC, Gomez LF, Parra DC, Lobelo F, Mosquera J, Florindo AA, et al. Lessons learned after 10 years of IPAQ use in Brazil and Colombia. J Phys Act Health. 2010;7 Suppl 2:S259-64.

14. Lohman TG. Research progress in validation of laboratory methods of assessing body composition. Med Sci Sports Exerc. 1984;16(6):596-605.

15. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005;26(2):319-38.

16. Knudson RJ, Lebowitz MD, Holberg CJ, Burrows B. Changes in the normal maximal expiratory flow-volume curve with growth and aging. Am Rev Respir Dis. 1983;127(6):725 34. PMid:6859656.

17. Mader A, Liesen H, Heck H, Philippi H, Schürch PM, Hollmann W. Zur beurteilung der sportartspezifischen Ausdauerleinstungsfähigkeit im Labor. Sportarzt Sportmed. 1976;26:109-12.

18. Pereira CA. Espirometria. J Pneumol. 2002;28(Suppl 3):1-83.

19. Akabas SR, Bazzy AR, DiMauro S, Haddad GG. Metabolic and functional adaptation of the diaphragm to training with resistive loads. J Appl Physiol. 1989;66(2):529-35.

20. Krahenbuhl GS, Skinner JS, Kohrt W. Developmental aspects of
maximal aerobic power in children. Exerc Sport Sci Rev. 1985;13:503-38.

21. Massicotte DR, Macnab RB. Cardiorespiratory adaptations to training at specified intensities in children. Med Sci Sports. 1974;6(4):242-6.

22. Anderson SD, Godfrey S. Cardio-respiratory response to treadmill exercise in normal children. Clin Sci. 1971;40(5):433-42.

23. Santuz P, Baraldi E, Filippone M, Zacchello F. Exercise performance in children with asthma: is it different from that of healthy controls? Eur Respir
J. 1997;10(6):1254-60.

24. Baraldi E. Chronic respiratory diseases and sport in children. Int J Sports Med. 2000;21 Suppl 2:S103-4; discussion S105.

25. Counil FP, Karila C, Varray A, Guillaumont S, Voisin M, Préfaut C. Anaerobic fitness in children with asthma: adaptation to maximal intermittent short exercise. Pediatr Pulmonol. 2001;31(3):198-204.

26. Clark CJ, Cochrane LM. Assessment of work performance in asthma for determination of cardiorespiratory fitness and training capacity. Thorax. 1988;43(10):745-9.

27. Santuz P, Baraldi E, Filippone M, Zacchello F. Exercise performance in children with asthma: is it different from that of healthy controls? Eur Respir J. 1997;10(6):1254-60.

28. Lewis MI, Belman MJ, Monn SA, Elashoff JD, Koerner SK. The relationship between oxygen consumption and work rate in patients with airflow obstruction. Chest. 1994;106(2):366-72.

29. Neder JA, Nery LE. Teste de exercício cardiopulmonar. J Pneumol. 2002;28(Suppl. 3):166-206.

30. Bar-Or O. Pediatric sports medicine for the practitioner - from physiologic principles to clinical applications. New York: Springer; 1983.

Study carried out at the Federal University of Santa Maria, Santa Maria, Brazil.
Correspondence to: Eliane Zenir Corrêa de Moraes. Rua Cezar Trevisan, 1333, Tomazetti, CEP 97065-060, Santa Maria, RS, Brasil.
Tel. 55 55 3211-4135 or 55 55 9963-8143. E-mail:
Financial support: None.
Submitted: 9 November 2011. Accepted, after review: 14 May 2012.

About the authors

Eliane Zenir Corrêa de Moraes
Professor. Federal University of Santa Maria, Santa Maria, Brazil.

Maria Elaine Trevisan
Assistant Professor, Department of Physical Therapy and Rehabilitation, Federal University of Santa Maria, Santa Maria, Brazil.

Sérgio de Vasconcellos Baldisserotto
Adjunct Professor of Clinical Medicine. Federal University of Santa Maria,

Santa Maria, Brazil.
Luiz Osório Cruz Portela
Associate Professor. Federal University of Santa Maria, Santa Maria, Brazil.



The Brazilian Journal of Pulmonology is indexed in:

Latindex Lilacs SciELO PubMed ISI Scopus Copernicus pmc


CNPq, Capes, Ministério da Educação, Ministério da Ciência e Tecnologia, Governo Federal, Brasil, País Rico é País sem Pobreza
Secretariat of the Brazilian Journal of Pulmonology
SCS Quadra 01, Bloco K, Salas 203/204 Ed. Denasa. CEP: 70.398-900 - Brasília - DF
Fone/fax: 0800 61 6218/ (55) (61) 3245 1030/ (55) (61) 3245 6218

Copyright 2019 - Brazilian Thoracic Association

Logo GN1