Physical activity and quality of life in children with well-controlled asthma

Abstract Background Asthma is the most common disease in childhood. Appropriate management and programs encouraging exercise enable children to enjoy a good quality of life (QoL). Objective To assess the association between lung function, physical activity (PA), and QoL in children with well-controlled asthma. Methods Fifty-four children aged 7–14 years attending a Pediatric Asthma Clinic were included. All children underwent spirometry and completed three self-administered validated questionnaires: The Godin Leisure-Time Exercise Questionnaire (GLTEQ), the ACT (Asthma Control Test), and the DISABKIDS for QoL. Results Mean age of the study population was 11.43(±2.1), BMI, kg/m2 (20.8 ± 3.9), FVCpp (97.1% ±12.4), and FEV1pp (99.7% ±12.43), ACT (23.4 ± 3). The GLTEQ revealed that only 3% of the studied population presented satisfactory activity, while 86% were sedentary. Both FEV1pp, and PA were significantly correlated to the children’s QoL ((r2: 0.55, p:0.0001), and (r2:0.45, p:0.003), respectively). Conclusions Despite reasonable asthma control, the children exhibited low physical activity levels, which negatively correlated to their QoL. Families of asthmatic children should be educated to highlight the benefits of exercise and increase the PA of their children.


Introduction
Asthma remains the most frequent disease of childhood (1,2). It is estimated that almost one out of five children aged 13-14 years has asthma in English-speaking countries of North America, Europe, and Australasia, while an estimated 8.6% of the population aged 18-45 years report asthma symptoms (attacks of wheezing or whistling breath) in the past 12 months (3). In Greece, asthma is a significant contributor to total childhood morbidity. Following the global trend, the prevalence of asthma in Greece has been rising during the last three decades (4,5). The degree to which asthma affects health-related quality of life (HRQoL) depends on various factors, the most critical being asthma control (3,6). Appropriate asthma management can enable children to enjoy a good quality of life. Therefore, asthma management through additional individual exercise programs may positively affect daily problems by enhancing lung function and encouraging participation in collective activities despite the disease (7). Studies have also demonstrated that through exercise, asthma exacerbations are both reduced and prevented (8). Therefore, physical activity (PA) can positively affect asthma control among asthmatic children by improving their physical fitness. This can reduce the threshold of triggers causing asthma symptoms, leading to decreased medication use and increased quality of life (9).
Current evidence shows that regular physical activity improves general health and can positively impact asthma outcomes, such as exercise capacity, asthma control, and quality of life (10,11). Despite this, many asthma patients do not engage in regular physical activity because they mistakenly believe they should restrict exercise participation. Children with well-controlled asthma should not refrain from physical activity (12,13).
The aim of the study was to assess PA and QoL among children with well-controlled asthma; the secondary aim was to evaluate the correlation between PA and lung function on the one hand, and QoL, on the other.

Methods
In the present prospective study, 54 children aged 7-14 years (59% male, 41% female) with well-controlled intermittent and mild persistent asthma without any other co-morbidities were included (14). Asthma control is defined as the degree to which disease manifestations are reduced or removed by therapy (15). Asthma control was evaluated with a detailed history of asthma symptoms, sleep disturbances, limitation of activity, and frequency of reliever use in the past four weeks (14,15). Demographics and patient characteristics were collected at the Pediatric Outpatient Asthma Clinic of a tertiary referral hospital over 12 months. All children underwent spirometry performed by experienced personnel and completed three self-administered questionnaires, as part of their evaluation, without knowing the purpose of the study, to ensure objective and blinded results. The Godin Leisure-Time Exercise Questionnaire (GLTEQ) is a simple, reliable, and effective tool for assessing physical activity among children and adolescents (Appendix 1) (16,17). It estimates physical activity over a typical week and is divided into three categories of intensity expressed as METs (Metabolic equivalent of task). GLTEQ is expressed in units (strenuous > 24, moderate 14-23, mild <14), ranking individuals from the highest to the lowest. The second questionnaire used was the ACT (Asthma Control Test), ranging from 5 to 25 (a score over 19 refers to reasonable asthma control) (Appendix 2) (18)(19)(20). The third questionnaire was the DISAKIDS questionnaire to assess the quality of life. The questionnaires used were the DISABKIDS chronic generic measurelong form (DCGM-37) and the DISABKIDS Condition-specific modules for asthma (Appendices 3 and 4). The DISABKIDS chronic generic module (DCGM37) consists of 37 rating-scaled items assigned to six dimensions: Independence, Emotion, Social inclusion, Social exclusion, Limitation, and Treatment. These scales have shown satisfactory internal consistencies, ranging from a ¼ 0.79 (Social inclusion) to a ¼ 0.90 (Emotion). Therefore, these six dimensions can be combined to produce a general score for HRQoL

Statistical analysis
The Student's t-test and the Mann-Whitney test were used to evaluate the association between normally distributed and skewed continuous variables, respectively, with a categorical variable consisting of two groups. The Pearson correlation coefficient was used to estimate the correlation between the different parameters. A probability value of 5% was considered statistically significant (p < 0.05). All calculations were conducted using SPSS for Windows (v19, SPSS Inc, Chicago, IL, USA). The patients' characteristics data were expressed as mean ± SD.
The results of the Quality-of-Life questionnaires are shown in Figure 2. The most restraining adversely affected parameters were the sense of social exclusion (stigma, feeling left out), social inclusion (acceptance of others, positive social relationships), the worry about the disease and medication burden. In addition, FEV1pp, as well as physical activity, showed a significantly but moderate correlation to the children's quality of life (r 2 : 0.55, p:0.0001) and (r 2 : 0.45, p:0.003), respectively (Figures 3 and 4). However, no significant correlation was found between the physical activity level and FEV1pp ( Figure 5).

Discussion
In the present study, we evaluated the level of physical activity among children with well-controlled asthma and assessed the correlation of PA with QoL and lung function. The results demonstrated that most children showed low physical activity levels despite their well-controlled asthma. The sense of social exclusion, social inclusion, the worry about asthma, and medication burden were the most significant affected parameters of their QoL. Furthermore, we showed a strong correlation between QoL, respiratory function, and PA. These findings highlight the need for appropriate education of asthmatic children and their families to encourage them to engage in physical activities by emphasizing the benefits of exercise and assuaging the family fears regarding exercise-induced dyspnea among asthmatic children with well-controlled asthma.     Physical activity plays an essential role in childhood growth. However, the rates of physical activity have significantly declined, and sedentary time has markedly increased over the last decades (22). Concerning physical exercise, almost half of Greek children stand below the recommended duration of at least one hour per day of physical activity (23). The sedentary level of the children with asthma in our study may reflect the current activity level in children without asthma. The lung function parameters and the ACT questionnaire scale demonstrated that asthma was well controlled among the children in our study, but their GLTEQ scale revealed that the majority had a sedentary lifestyle (Figure 1), as only 3% were active. Although our results regarding the level of physical activity of asthmatic children agree with other studies (24)(25)(26), there is also data showing no evidence that asthmatic children are involved in less physical activity compared to healthy peers (27). Several factors may contribute to the inactivity of asthmatic children. While exercise is a common trigger for bronchoconstriction in asthmatic children, the fear of an asthma attack emerged as the main barrier to exercise, as reported by Winn et al. (28). Additional factors contributing to the inactivity of asthmatic children include negative self-efficacy, child and parents health beliefs, and less frequent advice about exercise they receive from physicians and teachers than their healthy peers (22,24,25). Parents believe that physical activity can worsen their children's asthma symptoms is an essential factor associated with their restrictive attitudes toward physical activities (9). As this behavior may discourage children from having an active, healthy lifestyle, it is vital to appropriately evaluate, effectively treat, and counsel the asthmatic family that they do not need to avoid physical activities and can be stimulated to be fully active. An effective asthma self-management, education, and empowerment program can increase physical activity among children with well-controlled asthma (29).
Despite well-controlled asthma, the most affected parameters of our study population QOL were social exclusion (stigma, feeling left out), social inclusion (acceptance of others, positive social relationships), worry about their disease, and medication burden ( Figure 2). Stelmach et al. and Tibosch et al. showed that children, adolescents, and their caregivers reported few impairments in asthma-related QoL (30,31). On the other hand, Banjari et al. showed that significantly poorer quality of life was observed in children with uncontrolled asthma (32).
Although respiratory function values are usually within normal ranges in asthmatic children, the FEV1 decrease is associated with the disease's worsening, present or upcoming exacerbation, and exercise-induced bronchoconstriction (EIB) (25,33). Therefore, FEV1 is one of the most used clinical parameters for diagnosing and grading asthma severity (34). Also, as assessed by FEV1, asthma severity can predict the disease's progression, the patient's functional impairment, and QoL. Our study showed that respiratory function was significantly correlated to the children's QoL (Figure 3). Similar results were found by Levy et al., who used the PAQLQ (Pediatric Asthma Quality of Life Questionnaire) in a subgroup of children with well-controlled asthma (35).
As long as there is adequate asthma control, routine exercise has been proven safe in children with asthma (22). Regular PA by children and adolescents with asthma is associated with improving disease control and quality of life and reducing exacerbations, hospital admissions, school absenteeism, unscheduled medical visits, and the number of medications used to control asthma (9,36). Moreover, as the most common chronic disorder among top athletes, optimal diagnosis and treatment make it possible for athletes with asthma to compete equally with healthy athletes. When assessing the use of asthma drugs during the Olympic Games, it was even discovered that during the Winter and Summer Olympic Games from 2002 to 2010, the asthmatic athletes outperformed their healthy peers, taking more medals during the Olympics than their healthy peers (37).
Our data showed a significant correlation between physical activity and QoL ( Figure 4). In this domain, the recent literature is contradictory. Basso et al. (38) and Fanelli et al. (39) in children and adolescents reported that physical activity is related to a better QoL. On the other hand, Matsunaga et al. (10) found no correlation between physical activity, asthma control, spirometry, and QoL.
Another feature of our study was the poor correlation between respiratory function and physical activity, probably because most children (86%) were sedentary despite well-controlled asthma and good lung function. Contrarily, in a 10-week randomized controlled trial (RCT) of aerobic exercise in 38 children with asthma, Abdelbasset et al. reported significant improvements in pulmonary function, including FEV1pp, FVCp, VO2max, and all dimensions of QoL in the exercise group compared to control (40). In addition, Ram et al., in a meta-analysis reviewing eight studies with a total of 226 subjects, showed that physical training improves cardiopulmonary fitness without changing lung function (41).
Despite the effects of exercise on asthma outcomes, a particular form of exercise has not been proven more beneficial than others. An RCT of three different exercise interventions (swimming, football, and basketball) and a control group in children with asthma showed a significant improvement in lung function, their asthma symptoms, and general well-being in the swimming group compared to the others (42). Lahart and Metsios reported in a meta-analysis of the effects of swimming in non-elite or noncompetitive swimmers that children/adolescents with asthma presented substantial improvements in VO2max and PEF, significant reductions in bronchial hy p e r-r e s p o n s i v e n e s s , i mp r o v e m e nt s i n exercise-induced bronchoconstriction, methacholine challenge test performance compared to controls (43).

Limitations of the study
The small sample size and the fact that the majority (86%) of the children had a sedentary lifestyle are potential limitations of the study. Moreover, we used the GODIN physical activity questionnaire to assess physical activity. However, more accurate ways of assessing physical activity like telemonitoring using accelerometers, pedometers, or electronic dairy data have been developed. Although the physical activity questionnaires are less sensitive than physical activity assessed with accelerometry, it has been shown that the physical activity questionnaire might be used as a low-cost and easy-to-use PA screening tool for ruling out physical inactivity in a portion of the pediatric asthma population (20).

Conclusions
Our study showed that despite reasonable asthma control, the children presented low levels of physical activity, which negatively correlated to their quality of life. In children and adolescents with asthma, the disease may reduce the perceived capability to participate in physical activity contributing to an increase in the sedentary lifestyle. Therefore, families of asthmatic children should be educated on the benefits of exercise and the minimal risk of dyspnea among well-controlled asthmatic children in order to increase their physical activity.