Services on Demand
Print version ISSN 1413-3555
On-line version ISSN 1809-9246
Rev. bras. fisioter. vol.12 no.2 São Carlos Mar./Apr. 2008
Gonçalves RCI; Nunes MPTII; Cukier AIII; Stelmach RIII; Martins MAII; Carvalho CRFI
IPhysical Therapy Department, School
of Medicine, Universidade de São Paulo-USP São Paulo (SP), Brazil
IIMedical Clinics Department, USP
IIIPneumology Department, USP
OBJECTIVE: To evaluate the role of an
aerobic physical training program on psychosocial characteristics, quality of
life, symptoms and exhaled nitric oxide of adults with moderate or severe persistent
METHODS: Twenty patients were randomly assigned to a Control Group (CG, n= 10, education program and respiratory exercises) and a Trained Group (TG, n= 10, education program and respiratory exercises plus aerobic training at 70% of the maximum power obtained). The intervention took place twice a week for three months. Maximum aerobic capacity, pulmonary function, effort dyspnea, anxiety levels, depression levels and quality of life were assessed before and after the treatment. Exhaled nitric oxide at rest and the number of days without asthma symptoms were evaluated every month.
RESULTS: The TG presented increased numbers of symptom-free days (TG 24.8 days [95%CI= 23-27] versus CG 15.7 days [95%CI= 9-21]; p< 0.05), decreased exhaled nitric oxide levels (TG 25.8 ppb [95%CI= 15.3-44.0] versus CG 44.3 ppb [95%CI= 24-60]; p< 0.05), decreased anxiety scores (TG 39.3 [95%CI= 37-50] versus CG 40.9 [95%CI= 37-50]; p< 0.001), decreased depression scores (TG 6.6 [95%CI= 1-21] versus CG 9 [95%CI= 1-20]; p< 0.001), improved quality of life (TG 42.8% [95%CI= 34.3-71.7] versus CG 69.6% [95%CI= 45.1-87.9]; p< 0.001) and improved aerobic aptitude (TG 25.7 mL/kg/min [95%CI= 6.2-31.3] versus CG 20.5 mL/kg/min [95%CI= 17.3-24.1]; p< 0.001).
CONCLUSIONS: Our results suggest that physical training reduces exhaled nitric oxide and symptoms and improves the quality of life and psychosocial characteristics of adults with moderate or severe persistent asthma.
Key words: asthma; psychosocial characteristics; exhaled nitric oxide; quality of life; asthma symptoms; physical training.
Although there are a great number of stimuli which cause acute asthma attack, physical activity is one of the most common precipitating factors1. The dyspnea experienced by the asthmatic patients during exercise, or the fear of experiencing it, is responsible for distancing them from sports practice and group physical activities2. Therefore, asthmatic subjects tend to be less active and in poorer physical condition than healthy subjects3,4 and, hence, they remain physically inactive5,6. Physical, emotional and social restrictions imposed by asthma are capable of profoundly modifying patients lives, leading to depression, social isolation, low self-esteem, and loss of motivation7.
Physical conditioning has been considered an important part of rehabilitation programs for asthma patients8, however, a recent systematic review of the literature showed that the only proven effects are improvement of cardiovascular capacity, resistance to exercise, reduction of dyspnea related to exercise9, exercise-induced bronchospasm incidence and corticoid administration10. On the other hand, physical conditioning effects on factors related to quality of life, symptoms and psychosocial morbidity of asthma patients are still not well understood.
The fact that physical training reduces corticoid administration necessity and asthma symptoms, suggests a modulator role in pulmonary inflammation. However, the role of physical training on clinical management and pulmonary inflammation of asthmatic patients has never been analyzed. Reduction of the number of days free of symptoms, level of exhaled nitric oxide (NOe) and number of eosinophils in the induced sputum have been the main targets of inflammation management in asthmatic patients11,12.
Acute and unexpected shortness of breath episodes are constant threats to asthmatic patients and are associated with anxiety13. The benefits of physical conditioning for reduction of anxiety and depression levels in healthy adults and the elderly are widely recognized14 and, thus, it is possible that the regular practice of physical exercise can benefit asthmatic patients15. However, there are three studies which evaluated the effects of physical conditioning on quality of life of asthmatic subjects. The first one investigated adults with asthma and COPD16 and the other two evaluated the effects on children10,17.
The objective of the present study was to assess the effectiveness of an aerobic conditioning program on psychosocial aspects, quality of life and symptoms of adult patients with moderate or severe persistent asthma.
Twenty adults were studied (14F), men and women, with moderate or severe persistent asthma, aged between 20 and 50 years and with a body mass index (BMI) ranging between 20 and 30 Kg/m2. They had a score of 50% or inferior in the domain of physical limitation of the quality of life questionnaire - Escola Paulista de Medicina (EPM)18. The patients had to be under outpatient medical treatment for at least six months and demonstrate clinical stability (without hospitalization episodes or need for emergency care for, at least, 30 days). The diagnosis and treatments were conducted according to the Global Initiative for Asthma (GINA)19. The exclusion criteria included presence of another pulmonary associated disease, clinical diagnosis of cardiopathy and/or pulmonary hypertension, and osteomuscular diseases which could interfere in the evaluations. The patients were selected after a medical consultation and there were no medication changes during the whole program. Subjects with other diseases were excluded. The study was approved by the Ethics in Research Committee of Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo (HCFMUSP) with protocol number 0297/07 and the patients signed an informed consent form. Costs of transport and medication were paid by the researchers.
The subjects were randomly assigned to two groups: a control group (CG) and a training group (TG). The patients in the CG were submitted to an educational program and to a respiratory exercise program. Patients of the TG were submitted to all procedures of CG and to an additional program of physical aerobic conditioning. The training intensity was 70% of the maximal power obtained in the cardiopulmonary effort test carried out before the beginning of training. In the initiation and end of treatment period, all patients performed the pulmonary function test, cardiopulmonary effort test and answered questionnaires which assessed factors related to quality of life and levels of anxiety and depression. NOe and days free of symptoms were recorded and registered monthly, by means of a symptoms diary.
- Education program: The program had a duration of four hours and was comprised of two interactive classes which aimed at explaining disease physiopathology, correct use of medications, and an action plan in case of worsening of symptoms19.
- Respiratory exercise program: The program started the week after the education program. Patients of both groups were submitted to the respiratory exercise program which was carried out for 30 minutes, twice a week, over three months. The respiratory exercise program was conducted as previously described20.
- Aerobic Conditioning Program: The program started the week after the education program and each session had a duration of 30 minutes and was carried out after the CG performed the respiratory exercises. Patients were submitted to aerobic training on a treadmill (Imbramed Export Plus, RS, Brazil). The heart rate (HR) and level of respiratory discomfort of the subjects were monitored. The training intensity was 70% of maximum power obtained in the cardiopulmonary effort test, which was carried out before the beginning of the training and monitored by patients HR. During the first two weeks, the patients adapted to a program intensity level of 60% of the maximum power obtained10. There were no modifications in training intensity during the 12 weeks of treatment.
- Pulmonary function: Spirometric evaluations were conducted before and after the administration of 200ug of inhaled salbutamol (Kokko spirometer, Pulmonary Data System, USA). Technical procedures and criteria of acceptability and reproducibility were the ones recommended by ATS21 and previewed normality curves were the ones proposed by Knudson22. Increases of 12% or 200ml in the forced expiratory volume (FEV1) were defined as a positive response to bronchodilator21.
- Cardiopulmonary test: The test was performed on a treadmill linked to a digital computer which included a system of exercise evaluation (Sensormedics, Vmax 229, CA, USA). This system carried out analyses of metabolic, ventilatory and cardiovascular parameters of breathing patterns. The modified protocol of Balke-Ware23 was used and according to this protocol, the subject walked at the speed of 1.5 km/h on a non-inclined treadmill during a warm-up period and, after three minutes, an increase of 2.5 degrees occurred every two minutes. Values of VO2 peak were determined according to Cooper et al.24 and the lack of aerobic physical conditioning was classified as mild (over 70% of previewed), moderate (70-50% of previewed), or severe (lower than 50% of previewed)24. The values of VO2 at the anaerobic threshold (VO2AT) were determined by the gas exchange method through visualization of the point of inflexion of VCO2 versus VO2 (modified V slope)25. The values of VO2 at the point of respiratory compensation (VO2PCR) were detected through the exponential increases in CO2.
- Quality of life: This was evaluated through the EPM questionnaire of quality of life for asthmatic subjects. This questionnaire was translated and validated into the Portuguese language and consists of four domains18: i) patients physical limitations due to asthma symptoms; ii) symptom frequency; iii) socioeconomic limitations; and iv) psychosocial limitations. Questionnaire scores were expressed in percentages, with a maximum value of 100%. Low scores indicated better quality of life whereas high scores indicate poorer quality of life.
- Evaluation of the levels of anxiety and depression: The validated28,29 questionnaire of depression26 and State-trait Anxiety Inventory (IDATE)27 were used. IDATE is a questionnaire which examines the levels of state-anxiety and trait-anxiety symptoms.
- Asthma symptoms: These symptoms were analyzed through a previously described diary30. The diaries were filled out daily by patients and included questions about episodes of crises and symptoms (coughing, wheezing, shortness of breath, "waking up at night", and the use of inhalers. The days which were free of any of symptoms were summed and considered monthly. The 20 days before the beginning of treatment of both groups were considered for the first evaluation.
- Evaluation of exhaled nitric oxide levels: The fraction of NOe was measured over four occasions: before treatment and 30, 60 and 90 days after the termination of treatment. Patients were oriented to blow into a Mylar bag maintaining an expiratory pressure of 10 cmH2O, in order to avoid contamination of nasal cavity air. All collected samples were examined up to 24 hours after collection and analyzed by chemoluminescence (Sievers 280)31,32.
Sample size was calculated for an analysis of variance (ANOVA) with four groups (control and training, before and after training), and improvements of 40% for the domains related to quality of life (main variable), an expected within-group standard deviation of 30% and a statistical power of 80%. Normality of data was assessed through the Kolmogorov-Smirnov test. The variables obtained before training were compared with the Student t-test. Comparisons of the initial and final data on quality of life, anxiety, depression and aerobic capacity were analyzed using ANOVA. NOe and symptoms data were compared using repeated measures ANOVA. The level of significance was set at 5% (p< 0.05).
Three patients (2CG/1TG) dropped out of the study during the first month of treatment (two patients due to work schedule changes and one due to moving to another city). Twenty patients completed the study; 10 in the control group (6F) and 10 in the training group (7F). Before the beginning of the study, patients from the CG and TG were similar in relation to gender, age, body mass index, pulmonary functions and corticosteroid dose (Table 1). There were no differences related to aerobic capacity, factors related to quality of life and levels of anxiety and depression, number of days free of symptoms, and levels of NOe between subjects of CG and TG, before training.
After three months of treatment, individuals in the TG showed increases in the physiological effort parameters in comparison to theCG (Table 2). Trained adults reported increases in VO2peak, predicted VO2 and oxygen pulse at exercise peak (p< 0.05). Patients in the TG also showed increases in VO2peak, and in submaximal parameters, such as anaerobic threshold and point of respiratory compensation (p< 0.05). Trained subjects (TG) showed a reduction of effort perception at exercise peak in comparison to the values obtained before the physical training period (p< 0.05); however, effort perceptions of TG and CG were not different at the end of treatment (p> 0.05). None of the training programs resulted in pulmonary function improvement (data not presented).
The physical conditioning program improved the following domains: physical limitations, frequency of symptoms, psychosocial limitation, and the total score of quality of life questionnaire (p< 0.001) and there were no alterations in the socioeconomic domain (Table 3). Subjects who were not submitted to physical training showed equal or worse values in the domains of the reported quality of life questionnaire.
At the beginning of the study, patients of both groups (10/10; 100%) showed moderate trait-anxiety scores (Table 3). Physical conditioning reduced trait-anxiety levels of the TG in comparison to the initial levels (p< 0.05), although there were no differences in comparisons to the CG. On the other hand, there was no difference between initial and final levels of state-anxiety of the CG and TG.
It was observed that 50% of the patients in the CG (5/10) and in TG (5/10) had low scores of depression before the beginning of the study (Table 3). At the end of the study, the trained subjects demonstrated a reduction in their depression levels when compared to non-trained subjects (p<0.05). There was a significant reduction in the number of individuals with low levels of depression only in the TG (1/10).
The frequency of symptoms of patients was assessed by means of the monthly sum of days free of symptoms, reported and registered in their diary. Subjects in the CG and TG showed a mean of 12.9 days free of symptoms during the month before training (respectively, 12.10 [95%CI 8.0-18.0] and 13.7 [95%CI 10.0-18.0] days free of symptoms) (Figure 1). There was an increase in the number of days free of symptoms of TG, 30 days after the beginning of physical training (22.8 [95%CI 20.0-25.0]) which remained after 60 (24.0 [95%CI 22.0-26.0]) and 90 (24.8 [95%CI 23.0-27.0]) days of training (p<0.05) (Figure 2). In contrast, there was no alteration in the number of days free of symptoms of CG after 30, 60 and 90 days of training (respectively, 14.6 [95%CI 10 to 18], 14.7 [95%CI 10-18] and 15.7 [95%CI 9-21]) (p<0.05).
NOe measurements were conducted before the beginning of treatment and repeated every 30 days. There were no differences in NOe levels of TG and CG before the beginning of treatment (respectively, 35.03 [95%CI 22.4-59.2] vs 44.62 [95%CI 24.0-67.1] ppb). In contrast, NOe levels of CG patients were lower than the levels of TG patients at the evaluation carried out after 30 days (respectively, 31.5 [95%CI 14.0-62.0] vs 47.3 [95%CI 29.0-75.2] ppb) (p<0.05), 60 days (respectively, 28.7 [95%CI 18.0-50.0] vs 42.8 [95%CI 22.5-57.7] ppb) (p<0.05), and 90 days (respectively, 25.6 [95%CI 15.3-44.0] vs 44.35 [95%CI 24.0-60.0] ppb) (p<0.05) after the beginning of training (Figure 2).
The results of the present study showed that patients with moderate or severe persistent asthma demonstrated improvements of aerobic capacity and quality of life and reduction of symptoms, anxiety and depression and in levels of exhaled NOe after 12 weeks of moderate physical conditioning. Consequently, these data suggested that a physical conditioning program may have played a key role as an adjunct intervention in the treatment of asthmatic patients who were clinically stable and under appropriate drug therapy.
It has been demonstrated that the prescription of physical exercises for asthmatic patients produces an increase in aerobic capacity, leading these patients to achieve levels of physical activity which are within the normal range8. Generally, most patients (15/20, 75%) in the present study showed a maximal aerobic capacity (VO2peak) <70% of the predicted and, thus, a moderate physical limitation24. This decreased physical conditioning was related to an enhancement of the maximal and sub-maximal cardiovascular conditioning parameters (Table 2). Trained asthmatic patients showed an enhancement of VO2peak, anaerobic threshold and point of respiratory compensation. In fact, after training, all patients of TG, except one, showed an increase greater than 10% of their aerobic capacity. In contrast, all patients in the CG had an unaltered or reduced VO2peak at the second evaluation. There are only five randomized controlled studies which investigated the effects of physical training on VO2max. The improvements found were 5.5mLO2/kg/min (from 3.9 to 7.1 mLO2/kg/min)9. The results obtained in the present study are in accordance with those previously described, since our patients demonstrated a mean VO2peak increase of 5.1 mLO2/kg/min (from 0.1 to 10.7 mLO2/kg/min) (Table 2).
Quality of life is an individual perception which is inserted in the cultural context and value systems in which the subjects live. The context and values are related to the objectives, expectations, criteria and interests of these subjects33. Asthma causes negative effects on the quality of life to the extent that it causes anxiety related to the expectation of experiencing new crises. It also impairs sleep and makes participation in group and daily-living activities impossible34-36. The reduction in physical activity of asthmatic patients also contributes to obesity and low self-steam37. Studies which investigated the role of physical conditioning in the quality of life of adult asthmatic patients are still scarce. Cambach16 demonstrated that physical exercise, practiced regularly, is responsible for improving the quality of life of patients with respiratory diseases, including asthma and COPD patients. The results of the present study showed that physical conditioning lead to improvements of quality of life of asthmatic patients. Trained subjects showed reductions in their physical limitation scores, frequency of symptoms and psychosocial limitations, whereas none of these changes were observed in the untrained group.
Asthma can decrease quality of life and is consequently associated with psychosocial complications, such as high levels of depression and anxiety38. With asthmatic patients, psychosocial morbidity is associated with low adherence to drug treatment and to the worsening of the clinical disease picture39. Physical conditioning programs improve humor and reduce levels of anxiety and depression in healthy adults and the elderly11. However, the effects of regular physical activity practice on the psychosocial aspects of asthmatic patients are unknown. The present results demonstrated that 50% of the subjects (10/20) showed low levels of depression before the beginning of treatment in comparison to Brazilian data for a healthy population measured with the Beck inventory26. It is noteworthy that, after the physical conditioning period, patients in the TG showed improvements of the depression levels, suggesting that aerobic training programs can reduce depression in asthmatic subjects.
Anxiety levels were assessed using the Spielberger inventory which classifies anxiety as: trait-anxiety and state-anxiety27. State-anxiety refers to the fear of a subject facing a situation or a specific stimulus, such as an acute asthma crisis. Trait-anxiety refers to subjects perception of a situation in its totality, that is, asthma as a chronic disease. Before the beginning of the study, our patients showed anxiety levels greater than those described for healthy Brazilian individuals38. The reduction of trait-anxiety without modification in state-anxiety, observed in trained subjects, suggests that physical conditioning enhancement improved the perception of asthma as a chronic disease; however, it did not modify the fears of the patient facing acute asthma attacks (bronchoconstriction).
The role of physical training in reducing asthma symptoms is controversial9. Non-controlled and non-randomized studies suggest that, after a patient has submitted to an aerobic physical training program, there is a reduction in the number of hospitalizations and in the demand for medical emergency services2,8. In addition, the effects of physical exercise practice on exercise-induced bronchospasm, the necessity of control medication and symptoms of asthmatic patients remain controversial9. The present study demonstrated that the subjects who were submitted to a physical conditioning program demonstrated a reduction of asthma symptoms (coughing, wheezing, dyspnea, night awakening and need for relief medication).
Measurement of the levels of NOe is a simple and non-invasive means of evaluating pulmonary inflammation and this measure is used to assess patients improvements in response to treatment with inhaled corticosteroids40. The results presented in this study suggest that moderate aerobic physical training for asthmatic patients lead to a reduction in the values of NOe, as well as in the presence of disease symptoms, suggesting an adjunctive role of exercise in the reduction of chronic allergic pulmonary inflammation (Figure 2). It is important to stress that the decreases in NOe levels cannot be attributed to changes in medication, since the study was carried out during the period between two medical consultations, the two groups (control and training) received the same drug therapy, with inhaled corticosteroids, and the medication doses remained unaltered during the study.
Research involving asthmatic subjects and physical training relate cardiovascular capacity increases, quality of life improvement and symptom reduction in these patients, and hypothesize that their results are due to the reduction in pulmonary inflammation5. Recent studies show that ovalbumin-sensitive mice (experimental model of chronic allergic pulmonary inflammation) which were submitted to physical conditioning, demonstrated reductions in mucus production and pulmonary inflammations41 suggesting that aerobic training may cause pulmonary inflammation reductions.
NOe has been suggested as an inflammatory marker in asthma, which responds to treatment with corticoid40; however, this is still controversial42. In the present study, quantification of NOe levels had the objective of verifying if there would be any variations in this parameter over the physical training period. However, the fact that NOe levels were reduced in conjunction with reduced reported symptoms in the trained group suggest to us that it could be a marker of patients clinical improvements due to physical training. These data were even more relevant when it is verified that there were no alterations in NOe levels for the CG and that both groups maintained corticoid doses over the study.
Limitations of the study
A possible criticism to our study is the evaluation of pulmonary inflammation using NOe levels. Although these techniques are widely used in clinical practice to monitor pulmonary inflammation, some authors suggest that they have limitations and, thus, do not appropriately express pulmonary inflammatory processes42. However, NOe levels and asthma symptoms are used to measure the treatment effectiveness of corticoids in patients with moderate persistent asthma43. One possible interference in the evaluation of the behavior of NOe values of the subjects in this study could be modifications, made by the physician in charge of the patients, in corticoid doses. This limitation, however, was bypassed by conducting treatment during the period between two medical consultations, which made it impossible to change medication doses.
The reduced number of patients evaluated is a relevant limitation of our study. The authors, are aware of the importance of this issue and of the necessity of increasing the studied sample size, and are currently conducting a new study.
The results of the present study suggest that physical training reduced the values of exhaled NOe, the number of days with asthmatic symptoms and psychosocial morbidity in patients with moderate or severe persistent asthma. These results reinforce the importance of improving physical conditioning during clinical management of asthmatic patients.
1. V Diretrizes brasileiras para o manejo da asma. J Bras Pneumol. 2006;32 Supl 7:S447-74. [ Links ]
2. Disabella V, Sherman C. Exercise for asthma patients. Phys Sports Med. 1998;26:75-85. [ Links ]
3. Ludwick S, Jones T. Normalization of cardiorespiratory endurance in severely asthmatic children with asthma. J Pediat. 1986:106:556-80. [ Links ]
4. Clark C, Cochrane L. Assessment of work performance in asthma for determination of cardiorespiratory fitness and training capacity. Thorax. 1988;43:745-9. [ Links ]
5. Emtner M, Herala M, Stålenheim G. High-intensity physical training in adults with asthma. Chest. 1996;109:323-30. [ Links ]
6. 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;54:202-6. [ Links ]
7. Gift AG, Plaut SM, Jacox A. Psychologic and physiologic factors related to dyspnea in subjects with chronic obstructive pulmonary disease. Heart Lung. 1996;15:595-601. [ Links ]
8. Welsh L, Kemp JG, Roberts RGD. Effects of physical conditioning on children and adolescents with asthma. Sports Med. 2005;35(2):127-41. [ Links ]
9. Ram FS, Robinson SM, Black PN. Physical training for asthma. Cochrane Database Syst Rev (internet). 2005 Oct [date last accessed: 6 out 2006];19;(4):116. Available: http://medicine.plosjournals.org. [ Links ]
10. Fanelli A, Cabral ALB, Neder JA, Martins MA, Carvalho CRF. Exercise training on disease control and quality of life in asthmatic children. Med Sci Sports Exerc. 2007;39(9):1474-80. [ Links ]
11. Pijnenburg MW, Bakker EM, Hop WC, De Jongste JC. Titrating steroids on exhaled nitric oxide in children with asthma: a randomized controlled trial. Am J Respir Crit Care Med. 2005;172:831-6. [ Links ]
12. Zacharasiewicz A, Wilson N, Lex C, Erin EM, Li AM, Hansel T, et al. Clinical use of non-invasive measurements of airway inflammation in steroid reduction in children. Am J Respir Crit Care Med. 2005;171:1077-82. [ Links ]
13. ten Thoren C, Petermann F. Reviewing asthma and anxiety. Resp Med. 2000;94:409-15. [ Links ]
14. Cox RH, Thomas TR, Hinton PS, Donahue OM. Effect of acute bout of aerobic exercise on anxiety of women of different ages. Med Sci Sports Exerc. 2002;34 Suppl 1:S239. [ Links ]
15. Bingöl Karakoç G, Yilmaz M, Sur S, Ufuk Altintas D, Sarpel T, Güneter Kendirli S. The effects of daily pulmonary rehabilitation program at home on childhood asthma. Allergol et Immunopathol. 2000;28:12-4. [ Links ]
16. Cambach W, Chadwick-Straver RVM, Wagenaar RC. The effects of a community-based pulmonary rehabilitation programme on exercise tolerance and quality of life: a randomized controlled trial. Eur Respir J. 1997;10:104-13. [ Links ]
17. Basaran S, Guler-Uysal F, Ergen N, Seydaoglu G, Bingöl 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;38:130-5. [ Links ]
18. Oliveira MA, Barbieri A, Santos LA, Faresin SM, Fernandes ALG. Validation of a simplified quality of life questionnaire for a socioeconomic deprived asthma patients. J Asthma. 2005;42:41-4. [ Links ]
19. Global Initiative for Asthma - GINA. GINA Workshop Report (Updated 2006) Global Strategy for Asthma Management and prevention [text on the Internet]. Ontario, Canadá; 2000. [updated 2006 Oct; cited 2007]. Available from: http://www.ginasthma.org/ Guidelineitem.asp??l1=2&l2=1&intId=60- Med Res Methodol. [ Links ]2004;4:15. [ Links ]
20. Manocha R, Marks GB, Kenchington P, Peters D, Salome CM. Sahaja yoga in the management of moderate to severe asthma: a randomised controlled trial. Thorax. 2002;57:110. [ Links ]
21. American Thoracic Society. Lung function testing: selection of reference values and interpretative strategies. American Thoracic Society. Am J Respir Crit Care Med. 1991;144:1202-18. [ Links ]
22. Knudson RJ, Lebowitz MD, Holberg CJ, Burrows, B. Changes in the normal expiratory flow-volume curve with growth and aging. Am Rev Respir Dis. 1983;127:725-34. [ Links ]
23. Heyward VH. Advanced fitness assessment and exercise prescription. 5th ed. Champaign: Humans kinetics; 1997. [ Links ]
24. Cooper DM, Weiler-Ravell D, Whipp BJ, Wasserman K. Aerobic parameters of exercise as a function of body size during growth in children. J Appl Physiol. 1984;56:628-34. [ Links ]
25. Beaver WL, Wasserman K, Whipp BJ. A new method for detecting the anaerobic threshold by gas exchange. J Appl Physiol. 1986;60:2020-7. [ Links ]
26. Beck AT, Ward CH, Mendelson MD, Mocck J, Erbaugh J. An inventory for measuring depression. Arch Gen Psych. 1961;4:53-63. [ Links ]
27. Spilberger CD, Goursuch RL, Lushene RE. Inventário de ansiedade traço-ansiedade IDATE. In: Biaggio AM, Natalício L (ed). Psicologia aplicada. RJ: 1970. p. 60. [ Links ]
28. Biaggio A, Natalício L, Spielberger CD. Desenvolvimento da forma experimental em português do inventário de ansiedade traço-estado de Spielberger. Arq Bras Psicol Apl. 1977;29:31-44. [ Links ]
29. Gorenstein C, Pompéia S, Andrade L. Scores of a portuguese version of the Beck depression inventory ans state-trait anxiety inventory in Brazilian subjects. Braz J Med Biol Res. 1996;29:453-7. [ Links ]
30. Robles PG. Efeito da fisioterapia na condição clínica, na qualidade de vida, nos aspectos psicológicos e no desempenho físico de pacientes asmáticos persistentes [dissertação]. São Paulo (SP): USP; 2003. [ Links ]
31. Mehta S, Lilly CM, Rollenhagen JE, Haley KJ, Asano K, Drazen JM. Acute and chronic effects of allergic airway inflammation on pulmonary nitric oxide production. Am J Physiol. 1997;272:124-31. [ Links ]
32. Hadjikoumi I, Hassan A, Milner AD. Exhaled nitric oxide measurements in childhood asthma: comparison of two sampling techniques. Ped Res. 2002;52(5):745-9. [ Links ]
33. World Health Organization. Constitution of the World Health Organization. Geneva: WHO; 1947. [ Links ]
34. Gibson PG, HenrYGV, Vimpani JH. Asthma knowledge, attitudes, and quality of live in adolescents. Arch Dis Child. 1995;73;321-6. [ Links ]
35. Adams RJ, Wilson DH, Taylor AW, Daly A, Tursan dEspaignet E, Dal Grande E, et al. Psychological factors and asthma quality of life: a population based study. Thorax. 2004;59:930-5. [ Links ]
36. Fitch KD, Morton AR, Blanksby BA. Effects of swimming training on children with asthma. Arch Dis Child. 1976;51:190-4. [ Links ]
37. Ford ES, Health GW, Mannino DM, Redd SC. Leisure-time physical activity patterns among US adults with asthma. Chest. 2003;124:431-7. [ Links ]
38. Goldney RD, Ruffin R, Fisher LJ, Wilson DH. Asthma symptoms associated with depression and lower quality of life: a population survey. Med J Aust. 2003;178:437-41. [ Links ]
39. Bochner BS, Busse WW. Allergy and asthma. J Allergy Clin Immunol. 2005;115:953-9. [ Links ]
40. Pastva A, Estell K, Scoeb TR, Atkinson TP, Schwiehert LM. Aerobic Exercise Attenuates Airway Inflammatory: Responses in a mouse model of atopic asthma. J Immunol. 2004;172:4520-6. [ Links ]
41. Scollo M, Zaconato S, Ongaro R, Zaramella C, Zacchello F, Baraldi E. Exhaled nitric oxide and exercise induced bronchoconstriction in asthmatic children. Am J Respir Crit Care Med. 2000;161:1047-50. [ Links ]
42. Buchvald F, Eiberg H, Bisgaard H. Heterogeneity of FeNO response to inhaled steroid in asthmatic children. Clin Exp Allergy. 2003;33:1735-40. [ Links ]
43. Kharitonov SA, Donnelly LE, Montuschi P, Corradi M, Collins JV, Barnes PJ. Dose-dependent onset and cessation of action of inhaled budesonide on exhaled nitric oxide and symptoms in mild asthma. Thorax. 2002;57:889-96. [ Links ]
Correspondence to: Received: 12/07/2007
Raquel Calvo Gonçalves
Rua Vigário João Alvares, 157, apto. 44
CEP 01551-040, São Paulo(SP), Brasil
Financial support: Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Pesquisa (CNPq).