Asthma is a common chronic inflammatory pulmonary disorder resulting in a detrimental impact on the physical, emotional, and social daily life activity of patients (1). Asthmatics should have a reliever or controller medications. However, a variety of adverse events can occur, especially in children with asthma (2-4). To date, considerable research has been devoted to asthma’s characteristics and non-pharmacologic interventions. Pulmonary rehabilitation, a reputed feasible method of exercise training, education, and behavioral change, is designed to improve the physical and psychological condition of those with chronic respiratory disease and promote long-term adherence to health-enhancing behaviors (5,6). As an essential component of pulmonary rehabilitation, physical exercise demonstrated improvement in cardiovascular function, physical activity levels, and sociological benefits in previous studies (7-9).
Reports of physical exercise interventions vary methodologically in terms of the mode, intensity, frequency, and duration (10). The Centers for Disease Control and Prevention and American College of Sports Medicine recommend at least 30 minutes of moderately intense physical activity five days per week or vigorously intense activity for a minimum of 20 minutes three days per week (11). Prior studies (12,13) reported that the best method of increasing activity levels was spending more time on moderate-intensity exercise and less time on high-intensity activity. Aerobic exercise is considered any form of physical activity that produces an increased heart rate and respiratory volume to meet the oxygen requirements of the activated muscles. Oxygen inhalation and demand are equal in the human body to achieve physiological equilibrium during training. In a mouse model of allergic asthma, moderately intense aerobic exercise attenuated lung inflammatory responses (14). Neder et al. (15) reported aerobic improvement and significant medication reduction with aerobic training in patients with moderate to severe asthma.
Systematic reviews have verified that physical training improved cardiopulmonary fitness, maximum oxygen uptake, asthma symptoms, and quality of life in asthmatic patients, with no adverse effects on lung function (16-19). Conversely, several emerging studies demonstrated improved asthma symptoms and lung function (20,21) after aerobic exercise. Despite obvious benefits of aerobic exercise for asthmatic patients, controversies persist. We performed a meta-analysis for an exhaustive review of the available evidence on pulmonary function and quality of life between asthma and continuous aerobic exercise.
We present the following article in accordance with the PRISMA reporting checklist (available at http://dx.doi.org/10.21037/jtd-19-2813).
A comprehensive electronic search for aerobic exercise training trials in asthmatic patients was conducted in PubMed, EMBASE, and the Cochrane Central Register of Controlled Trials (CINAHL) containing the following retrieval strategies: “asthma AND (train* OR exercise* OR physical activity* OR aerobic exercise* OR pulmonary rehabilitation*)”. There were no age, language, or date of publication restrictions.
The inclusion criteria are as follows: The clinical diagnosis of asthma according to the Global Initiative for Asthma (GINA) recommendations or made by a physician and/or using objective criteria such as bronchodilator reversibility or both; any type of whole aerobic exercise lasting at least 20 minutes and two times per week for a minimum duration of 4 weeks; original trials in which continuous aerobic training and asthma were involved and a control group consisting of no intervention or receiving the same level of education or medication; and outcomes of trials for quantitative synthesis including pulmonary function and quality of life (QoL). We excluded studies that did not conform to whole body continuous aerobic physical training in asthma patients and did not contain randomized controlled trial designs or valid data. Two reviewers independently assessed the rationality of the included articles. In cases of dispute, agreement was reached through consultation.
The primary endpoints were pulmonary function (FEV1, FEV1%pred, FVC, FVC%pred, PEF, FEF25–75%, and FEV1/FVC%) and the secondary outcome was quality of life (QoL).
Quality assessment and data extraction
Two investigators evaluated the quality of the trials and the risk of bias using the Jadad Scale score (22) and the Cochrane Handbook for Systematic Reviews of Intervention Criteria (23), respectively. The characteristics of eligible articles were stated with the first author, publication, year, country, age, interventions, patients, and outcomes (Tables 1,2). Two pursuers independently extracted the sample size, mean value, and standard deviation of the outcome indicators. In cases of inconsistency, the results were discussed with a third researcher.
For the continuous variables, the standardized mean difference (SMD) or weighted mean difference (WMD) were calculated according to the uniformity of the measuring unit. The pooled effect size was described using forest plots, and a P value <0.05 was statistically significant. The heterogeneity of the studies was assessed via I2-and Chi-squared (χ2) statistics, and a fixed-effects model was used to amalgamate the effect size when I2≤50% or P>0.1 in the χ2 statistics. We also attempted to find potential sources of heterogeneity through subgroup analysis or sensitivity analysis if significant heterogeneity (I2>50%) emerged or incorporated heterogeneity using a random-effects model (23). Funnel plots were quantified to detect any publication bias (P value <0.05) if there were sufficient articles (10 or more studies). All of the data analyses were completed using Stata 14.0 software.
We identified 2,379 manuscripts from an initial search of the databases, and 1,517 citations remained after duplicates were removed. Of these, 1,359 were excluded after appraising the titles/abstracts. Based on full-text screening, we agreed on 25 articles for qualitative synthesis. Finally, 22 studies were incorporated into the meta-analysis due to insufficient data in 3 articles (Figure 1).
Characteristics of eligible studies
Twenty-two trials (24-45) involving the randomization of 874 participants assessing the effect of aerobic exercise on lung function or quality of life in asthmatic patients were published between 1990 and 2019. Of these, the patients in 12 articles (25-27,29-32,34,36,41,44,45) were children. Six studies involved individuals with moderate or severe persistent asthma, and others had mild to moderate persistent asthma. The measurements of outcomes were recorded after a 6- to 16-week training run, and spirometric variables and quality of life of post-exercise intervention were compared between the exercise group and control group. In most of the studies, the training modes were cycling, treadmill walking, and swimming. One involved submaximal basketball, two included multiple aerobic exercises, and four trials did not refer to a specific form of exercise. The frequency of aerobic exercise training in 12 studies involved two sessions per week, while others studies mandated exercise 3 times a week. The exercise training sessions ranged from 20 to 90 minutes, and moderate exercise intensity was controlled by maintaining the heart rate between 50% and 80% of the maximum heart rate (46,47) (HRmax) during exercise in the majority of the included trials (Tables 1,2).
Methodologic quality assessment of the included trials
All of the trials mentioned randomization, but many did not provide detailed information. In the Jadad Scale score, six studies were marked by four scores, eight studies were given three marks, and others scored two (Tables 1,2). The risk of bias is summarized in Figure 2. Low means that there was a plausible bias unlikely to seriously alter the results. High means that plausible bias occurred that can seriously weaken confidence in the results. Uncertain was stated if there were unclear risks of bias or if plausible bias could raise some doubts about the results (23). However, blinding of the participants and personnel was not regarded as a possible bias because the design of the study itself (exercise vs. no exercise) precluded blinding.
Results of the meta-analysis
We excluded several studies by Mendes et al. (in 2010, 2011) (35,39) and Gonçalves et al. (33) from the current meta-analysis because of the presentation of medians and interquartile ranges in the relevant parameters. We were unable to clarify whether the participants enrolled in three studies would overlap because the subjects were recruited by the same researchers. A study by Farid et al. (28) could not be pooled due to the imprecise description of the variables. A study by Wicher et al. (36) was excluded due to obvious differences in the pre-study FEV1% and FVC%pred parameters between the exercise and control groups. A study by Andrade et al. (41) was removed because no valid data could be pooled.
Twelve studies (24-27,29,32,36,37,41-43) with 455 patients reporting forced expiratory volume in one second at the endpoint of exercise were meta-analyzed. No heterogeneity existed among trials (I2=10.2%, P=0.345), and a fixed-effects model of the pooled effect showed adequate efficiency (WMD: 0.12, 95% CI: 0.05–0.20, P=0.011) (Figure 3) in adults and children trained with aerobic exercise. The forest plot diagrammed in Figure 3 and Egger’s test demonstrated no evidence of publication bias (P=0.663).
We assessed the pooled fixed-effect model of 11 studies (24,26,27,29,30,32,33,38,42,44,45) with 439 participants. There was no difference between two groups after aerobic training (I2=36.0%, WMD: 0.68, 95% CI: −0.64 to 2.01, P=0.312) whether in adults (P=0.808) or children (P=0.325) as participants. Egger’s test displayed no publication bias (P=0.413) from the forest plot (Figure 3). We conducted a subgroup analysis with different modes of training. Swimming (P=0.015) and indoor treadmill (P=0.006) improved significantly (Table 3).
Ten trials (25-27,32,34,36,37,41-43) involving 373 subjects provided data on the forced vital capacity index that could be pooled with a fixed model (I2=0.0%, P=0.817). The meta-analysis demonstrated a significant difference in favor of aerobic exercise compared with the controls (WMD: 0.18, 95% CI: 0.09–0.27, P=0.0001) in swimming (P=0.003) and indoor treadmill (P=0.005) exercise programs (Table 3) and no publication bias using Egger’s test (P=0.546) (Figure 3).
In six studies (26,27,34,37,41,43) with 113 patients in exercise groups and 111 in control groups focused on peak expiratory flow levels of the subjects during follow up. A random-effects model (I2=87.30%, P=0.001) indicated that aerobic exercise improved predominantly more than the control groups (WMD: 0.66, 95% CI: 0.24–1.09, P=0.002) (Figure 4), and a subgroup analysis proved the same advantage in swimming (P=0.001) and indoor treadmill (P=0.001) groups (Table 3).
We used a fixed-effects model for the pooled effect of FVC as a percentage of the predicted value in 6 studies (27,28,31,34,42,44) including 207 participators. Aerobic exercise increased FVC%pred compared with control groups (I2=3.9%, WMD: 4.30, 95% CI: 0.88–7.72, P=0.014) (Figure 4).
FEV1/FVC% was included in 7 articles (26,30,34,36,37,42,45) at the end of training programs, and a fixed-effects model revealed no effectiveness of aerobic exercise (I2=0.0%, WMD: 0.27, 95% CI: −0.43 to 0.98, P=0.443) (Figure 4).
Five studies (27,32,34,36,42) referred to forced expiratory flow between 25% and 75% of vital capacity at the end of exercise. A pooled fixed-effects model demonstrated a significant improvement in aerobic exercise groups (I2=0.0%, WMD: 9.65, 95% CI: 2.84–16.46, P=0.005) (Figure 4).
Four of seven studies incorporated the Pediatric Asthma Quality of Life Questionnaire (PAQLQ) (30-32,41,44) with children and the others reported the Asthma Quality of Life Questionnaire (AQLQ) (42,43) with adults. They demonstrated that aerobic exercise groups had significantly improved quality of life among children (I2=72.1%, WMD: 0.81, 95% CI: 0.32–1.30, P<0.001) and adults (I2=0.0%, WMD: 0.20, 95% CI: 0.07–0.32, P=0.002) (Figure 5).
This meta-analysis confirmed the effectiveness of aerobic exercise training for ameliorating partial spirometry parameters (PEF, FEV1, FVC, FVC%pred, and FEF25–75%) and quality of life associated with asthma. Asthmatic patients should participate in mild to moderate continuous aerobic exercise programs.
The BTS Guideline on Pulmonary Rehabilitation in Adults (48) proposed that those with chronic respiratory disease should be referred to pulmonary rehabilitation, and the routine referral of patients with asthma to pulmonary rehabilitation is not recommended based on inadequate clinical evidence. Asthmatics can be anxious about exercise-induced bronchoconstriction (EIB) (49-52), which is why some prefer a sedentary lifestyle and avoid physical activity to deter asthmatic exacerbation (53,54). Nevertheless, the increasing amount of published research proved that asthmatic patients could benefit from regular exercise training (18); the same effectiveness emerged in patients with exercise-induced asthma (55-57).
However, viewpoints concerning which exercise programs are the most beneficial did not achieve a consensus. Regarding the training modality, aerobic training is exercise that can be performed for at least 20 minutes with mild or moderate fatigue (58,59). Most clinical trials designed to research chronic respiratory disease with exercise usually focus on regular aerobic training programs rather than high-intensity anaerobic exercise that can trigger exercise-induced asthma (EIA) (51,60). A review by Crosbie et al. (57) reported that training intensity was the most prominent factor for increasing aerobic capacity. A third session of prescribed exercise for 30 minutes each time was recommended by the American Thoracic Society/European Respiratory Society Official Policy (61). Hence, asthmatics should participate in appropriate whole-body aerobic exercise with a moderate intensity to provide evidence-based support for clinical practice.
Spirometry parameters play an essential role in the diagnosis, severity, and prognosis of asthma and are relevant to cardiorespiratory fitness (62,63). Previous studies of exercise training rarely considered lung function as the main outcome indicator and thus were insufficient to assess the effectiveness of interventions for chronic respiratory diseases (such as asthma and COPD). Accordingly, our research concentrated on lung function. In contrast to the Cochrane meta-analysis of Carson et al. (18), we included five additional recent studies from our search strategy and eliminated the literature with overlapping trials, unclear outcome indicators, and interventions of high-intensity volume or frequency, resulting in differences in literature inclusion. In addition, Carson et al. analyzed limited indicators of lung function (FEVI, FVC), on the basis of which we added other variables and obtained valuable results.
Forced expiratory volume in one second (FEV1) and peak expiratory flow (PEF) are the two most common indicators of the objective evaluation of asthma. The Global Initiative for Asthma (GINA) guidelines recommend spirometry to manage exacerbations of asthma that require emergency treatment or hospitalization, including specific FEV1 and PEF values as indications for admission and response to treatment (64,65). Both parameters reflect airway patency and are used to measure airway function and respiratory muscle strength to indicate the degrees of airway obstructions and lesions (63,66). Our meta-analysis showed noteworthy improvements in FEV1 and PEF in contrast with a review by Philipp et al. (67) that reported amelioration of FEV1 rather than PEF. This discrepancy may be due to the cooptation of newly published reports (41,43) and normative difference with intervention. However, there were unexplained sources of heterogeneity with PEF, even if age, exercise patterns, follow-up time, and asthma severity were taken into account, which may be related to the time variability of the PEF measurement (66,68).
Our meta-analysis observed amelioration of FVC, FVC%pred, and FEF25–75% after aerobic training programs, and no significant heterogeneity or selective was reported.
Both FVC and FVC%pred are indicators of force dependence and are considerably affected by respiratory muscle function, lung compliance airway resistance, and the patient’s overall health. These conditions significantly improve after using bronchodilators (63,65,66). Improved in FVC, FVC%pred and FEV1, no significantly change was observed in FEV1/FVC% and FEV1%pred, which are mainly affected by airway resistance. This confirms that the FEV1/FVC ratio is not a reliable index of reversibility as FVC can increase more than FEV1, causing FEV1/FVC to decrease in the presence of a useful degree of bronchodilation (65). FEF25–75%, a non-force dependent part of FVC that’s flow value is mainly affected by a small airway diameter with less variability, may be useful for pediatric patients as it has greater elasticity and empties more rapidly (69,70). Of the five studies included in the meta-analysis, four involved patients with children, and credible improvement was demonstrated by the pooled effect.
For further insight into the involvement of aerobic exercise in the qualified articles, age and mode of exercise were considered. There was credible improvement in FEV1, PEF, and FVC in swimming or indoor treadmill training groups. Moreover, most eligible patients had mild to moderate asthma, so regular sustained aerobic exercise for both adults and children with mild to moderate asthma is recommended, and swimming or treadmill training is a suitable choice.
The current mechanisms pertaining to improving lung function of asthmatic patients participating in aerobic exercise remain unclear. One pathophysiological study verified an increase in residual air flow and a decrease in reinforced bronchial expansion ventilation in asthmatic patients during physical exercise (71). Bronchial hyperresponsiveness (BHR) is a basic characteristic of asthma. Asthmatic animal models have systematically demonstrated that aerobic exercise reduced BHR (72,73). Three studies in our meta-analysis compared BHR with the control group post-intervention and shown a trend for lower, respectively. Moreover, a literatures review of Eichelberger et al. (67). reported the same argument. Additional research observed that regular moderate aerobic training prior to allergic asthma reduced airway inflammation and remodeling (74), similar to Qin et al., who reported that low-intensity aerobic exercise training attenuated airway hyperresponsiveness, inflammation, and remodeling in a rat model of steroid-resistant asthma (75). Recent research confirmed the various molecular biological mechanisms of this effect (76). A randomized controlled trial demonstrated that supervised aerobic physical exercise for 8 weeks (2 times per week) could reduce asthma’s pulmonary inflammation (77). According to those mechanism studies, aerobic exercise ameliorates airway inflammation, airflow obstruction, airway hyperresponsiveness, and remodeling in asthma. However, whether these effects improve lung function has not yet been determined considering that not all parameters of airway obstruction improved from our meta-analysis. Welsh et al. reported that physical activity increased expiratory reserve capacity (78). Shaw et al. (37) observed a reduction in airway obstruction and an increase in inspiratory force after aerobic training in asthmatics. Alberta et al. reported that aerobic exercise training alone increased abdominal muscular endurance (79).
The inconsistent conclusions of pulmonary function parameters may not only be related to the duration of aerobic training and airway variability, but also to amelioration of general health conditions, respiratory motivation, and lung compliance caused by continuous aerobic training.
Ten studies in the literature assessed quality of life associated with asthma. One (40) reported no overall scores, and another (33) presented median and quartile intervals that could not be pooled together. Routine activity, asthma symptoms, emotion, and the total quality of life score improved overall in eight trials (30,31,33,35,39,41,43,44). Because different types of questionnaires were utilized, we conducted a subgroup analysis according to the PAQLQ (children) and AQLQ (adults), and higher scores indicated better quality of life. Conversely, one study that evaluated quality of life (QoL) (45) using PADQLQ scores found that higher scores indicated worse quality of life. Our meta-analysis indicated that aerobic training improved asthma-related quality of life in both adults and children. The same conclusions were summarized in three studies (33,35,39) that could not be meta-analyzed, which is consistent with other research (67,80). Basaran et al. (30) indicated that changes in symptom scores significantly correlated with changes in total QoL scores, which was also reported by França-Pintoet al. (42). Zhang et al. (45) observed that asthmatics’ wheezing, coughing, and sleep improved significantly in an exercise group. These reports found that regular aerobic exercise promotes the overall quality of life of asthmatic patients as demonstrated by physical fitness, asthma symptoms, and psychosocial factors (18,19). This advantageous effect may also ameliorate airway hyperreactivity and pulmonary function (67).
Aerobic exercise benefits many factors related to asthma. A recent longitudinal and multi-country study reported that the advantages of physical activity may differ according to body mass index (BMI) (81). A prospective trial by Torii et al. compared morning, afternoon, and evening exercise times over a 4-week period suggested that aerobic training was most effective in the afternoon (82). van Veldhoven et al. (26) conducted a multivariate analysis of variance (MANOVA) on sex factors and confirmed that boys in an experimental group benefited more from aerobic exercise than girls. Our meta-analysis found that some parameters improved more notably in children with asthma. Relatively few studies reported the effects of aerobic exercise on adult asthma. Different responses to aerobic exercise between adults and children must be further confirmed.
None of the qualified research articles reported adverse events during aerobic exercise training except two trials. Mendes et al. (35) observed that five patients (control group: 4; training group: 1) visited the emergency department, and eight (control group: 7; training group: 1) had asthma exacerbations. Turner et al. found that four patients (control group: 2; training group: 2) had asthma exacerbation during exercise (40). These studies also reported that severe asthma was associated with a higher risk of acute attacks (83). However, there was no increased risk of acute episodes due to exercise training, and aerobic exercise was well tolerated, as reported by Russell et al. (81), who found no association between physical activity and asthma incidents over 10 years, and lighter physical activity reduced asthma in middle-aged adults over time. Medication may be an important protective mechanism; the usage of prophylactic bronchodilators before each training session was mentioned in many of the eligible studies.
There are limitations to this study that merit mention. First, some relevant trials were excluded due to lack of outcomes of lung function and quality of life, or insufficient data were analyzed that could have potentially been a source of risk of bias. Second, most of the included articles had a small number of participants and evaluated only the short-term benefits of physical training, and some studies were low quality. Finally, there was indecipherable heterogeneity among some studies although the random-effects model was used.
Overall, our research demonstrated that regular continuous moderate intensity aerobic exercise at least 20 minutes two or three times per week over at least four weeks improved lung function and quality of life and would be a non-pharmacological benefit for asthmatic patients. Regarding the mode of exercise, swimming or treadmill training are appropriate options.
Reporting Checklist: The authors have completed the PRISMA Checklist reporting checklist. Available at http://dx.doi.org/10.21037/jtd-19-2813
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at http://dx.doi.org/10.21037/jtd-19-2813). The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The ethical committee approval was not required at our institution because our research is a systematic review and meta-analysis, and all analyses were based on previous published studies.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
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