Athletes active in endurance sports are at an increased risk of acquiring asthma through their sports activities, especially so for cross-country skiers, biathlon skiers, swimmers and athletes of other endurance sports. Asthma may be present from early childhood or develop while in active sports. This article focuses on the physical activity and sports activities in children and adolescents. Exercise-induced asthma (EIA) is found in 8–10% of a normal child population of school age and in about 35% of children with current asthma.
EIA is caused by the markedly increased ventilation during exercise, with increased heat and water loss through respiration, leading to bronchial constriction. The risk of developing asthma in the young athlete is related to the repeated daily training activity with increased epithelial damage of the airways, delayed repair due to the daily repetition of the training and increased airway mucosal inflammation. The increased environmental exposure through the sports activity to environmental agents, such as cold, dry air in skiers and chlorine compounds in swimmers, increases symptoms and signs of asthma and bronchial hyper-responsiveness, either worsening an existing asthma or leading to a novel disease in a previously healthy athlete.
Several specific aspects of daily training life, environmental exposure, diagnostic procedures and aspects of treatment related to the regulations of medication use in sports need particular attention when addressing the adolescent athlete with respiratory symptoms.
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Asthma is among the most frequent chronic diseases in childhood and adolescence; prevalence of asthma ever is reported among 20.1% of 10-year-old children in Oslo from a birth cohort, and current asthma was found in 10.2%.1 Exercise-induced bronchoconstriction (EIB) occurred in 8.6% of a normal population of 10-year-old children,1 and was reported in 12% of non-asthmatic children of 7–17 years of age2 and among 36.7% of 10 year-olds with current asthma.1 Many children participating in sports and physical activity will thus have asthma and EIB.
A task force report defined exercise-induced symptoms and signs of asthma occurring after intensive physical exercise as exercise-induced asthma (EIA). The reduction in lung function (FEV1) occurring after a standardised exercise test is called EIB, denoted as a reduction of at least 10% in FEV1 after exercise.3
It is recognised that it is important for the child with asthma and adolescent to master physical exercise. Physical fitness has been reported to be related to the psychological function in children with asthma,4 and active physical activity to have an impact upon the development and growth.5 In all international guidelines of treatment of asthma in childhood, one of the major objectives of treating asthma is to treat EIA and to master physical activities of all kinds.6,–,9
Children continuously vary their activity between vigorous and low-intensive activity. Children were reported to have high-intensity activity 3.1% of the time as compared with low-intensity activity 77.1% of the time.10 For the child with asthma, it becomes important to master EIA without depending upon a planned premedication before a planned physical exercise. Thus, the control of asthma by anti-inflammatory treatment is important for daily life activities including play and participation in sports activities and competitions.
Participation in physical activity, training and sports in the growing child with asthma and adolescent
Asthma limits participation in physical activity, especially on a vigorous level.11 Therefore, optimal asthma treatment is a prerequisite for the child with asthma and adolescent's participation in physical activity, sports activities and competitions on the level of their peers.12 Children with asthma and adolescents' participation in sport activities and training improves their physical fitness and quality of life,12 whereas asthma activity, bronchial responsiveness and lung function are not influenced.13 A life more active and happy was reached after their participation in training groups with children having asthma.14
In the Oslo birth cohort study, an environmental childhood asthma study, 13-year-old children with asthma were as fit and physically active as their healthy peers,15 thus being able to participate in sports activities on an equal level with their healthy peers.
Physical training improves fitness, quality of life and also activity levels in children with asthma.12 14 A Cochrane-based meta-analysis of eight training studies including 226 with asthma from 6 years age group confirmed this,13 concluding that physical training improved fitness as measured by an increased maximum oxygen uptake. However, no change in lung function and bronchial responsiveness accompanied the increased physical fitness. Later on, more recent studies confirmed this.16 17
On the other hand, newly diagnosed adolescents with asthma were less fit with lower levels of high vigorous physical activity as compared with healthy controls.18 With 1 year of anti-inflammatory asthma treatment, adolescents obtained better asthma control and increased the fitness and level of vigorous activity.19
Mechanisms of EIA and the development of asthma in young, previously healthy athletes
Physical activity increases minute ventilation. The inhaled air is warmed up to 37°C and is fully saturated with vapour. This causes increased water and heat loss through respiration. The airways are cooled resulting in reflex parasympathetic nerve stimulation causing bronchoconstriction and initially reflex vasoconstriction of bronchial venules to conserve heat. When stopping exercise, the increased ventilation ceases, and so the cooling stimulus, thus giving a rebound vasodilatation. This results in smooth muscle constriction and mucosal oedema in susceptible individuals,20 reducing the size of the bronchial lumen with increased airways resistance.21
On the other hand, the increased water loss also caused by the increased minute ventilation is considered more important by increasing the osmolality in the extracellular fluid of the bronchial mucosal membranes. The water loss from the bronchial mucosa induces movement of water from inside the cell to the extracellular space22 causing an intracellular increase in ion concentration.23 This process may lead to mediators release; newly formed eicosanoids and preformed mediators such as histamine from intracellular granules are released and cause bronchoconstriction. It is suggested that cold air exerts its effect through its low content of water, thus participating in the drying of the respiratory mucosa.22
The first reports on increased prevalence of asthma and bronchial hyper-responsiveness (BHR) among elite athletes came more than 20 years ago, first reported among swimmers24 and then among cross-country skiers.25 26 Later, similar findings were reported in Olympic athletes with regard to the use of asthma drugs.27 The prevalence of asthma and BHR increased with increasing age in Norwegian national team cross-country skiers, being higher according to the length of their competitive period.26 28 Among adolescent swimmers, however, we found a high prevalence of BHR already at a younger age, between 16 and 22 years, as measured by metacholine bronchial provocation and by eucapnic voluntary hyperpnoea.29
The first report that BHR increased after heavy exercise was made on adolescent swimmers (12–18 years of age) swimming 3000 m. The increase in bronchial responsiveness correlated with the increase in exercise load (increase in blood lactate) in asthmatic and healthy swimmers.24 Later, Sue Chu et al showed that adolescent cross-country skiers (ski-gymnasts) during one competitive winter season developed signs of inflammation (lymphoid follicles and deposition of tenascin) in their bronchial biopsies independent of being asthmatics or not.30
Also, experiments with exercising animals show inflammatory changes in the airways. In addition, the epithelial damage is a repeated finding. Mice, exercised by running, developed inflammation and epithelial damage in their airways as compared with sedentary mice.31 This was also found in the Alaskan sledge dogs examined by bronchoscopy and bronchoalveolar lavage before and after a sledge race across Alaska.32
Positive metacholine bronchial challenges were found more often in competitive swimmers and winter sport athletes compared with healthy controls,33 also including positive tests for eucapnic voluntary hyperpnoea.34 Inflammatory markers in induced sputum with increased neutrophil counts in induced sputum from swimmers and winter sport athletes, and the neutrophil counts correlated to the number of training hours per week in both groups.33 Eosinophil counts were increased in swimmers in particular, as also was the number of bronchial epithelial cells.33
Moreover, amateur endurance runners had increased number of bronchial epithelial cells and apoptosis of bronchial cells in induced sputum from before to after repeated half-marathon races, in addition to the increased serum levels of clara cell protein 16 and increased supernatant interleukin 8 levels in induced sputum.35
Extracellular water movement across cell membranes is an important mechanistic part of the pathogenesis of EIA.22 Aquaporin is a channel for aqueous water transport driven by osmotic forces generated by sodium and chlorine ions and expressed in the respiratory subepithelial glandular cells and alveolar type 1 cells of the lungs.36 Mice lacking the gene for the aqueous water channel aquaporin (Aqp) 5 exhibit methacholine-induced BHR in comparison with normal mice.37 Park et al found a relationship between metacholine bronchial responsiveness and diminished pilocarpine-induced sweat secretion, tearing rate and salivary flow rate in healthy athletes36 indicating an autonomic dysfunction.
Intensive and regularly repeated training has been shown to influence autonomic regulation. Filipe et al demonstrated increased parasympathetic activity in athletes, especially in endurance runners by pupillometry.38 Also, Knopfli et al in two studies reported higher parasympathetic nervous activity in top cross-country skiers and in training children.39 40
The training environment is important for the adolescent athlete. Due to regular exercise up to twice daily with increased minute ventilation especially when training endurance, the athlete has a higher exposure to environmental air and possible pollutants and chemicals in the surrounding air (table 1).
As stated, young competitive swimmers develop BHR at an earlier age, earlier than competitive cross-country skiers.28 29 Exposure for swimming pools has been reported to increase asthma prevalence and EIA in Belgian children,41 even though a large English birth cohort study contradicted this finding and found cumulative swimming to be associated with increased lung function and decreased risk of asthma symptoms, especially in children with pre-existing respiratory illness.42 Several studies have reported increased neutrophils and eosinophils in induced sputum from competitive swimmers43 44 and frequently BHR.29 43 44 Increased LTB4 levels in exhaled breath condensate were reported in Italian elite swimmers.45 The environmental agent active in swimming pools is organic chlorine products, thought to cause airways inflammation and BHR46
Different types of sport will have different environmental exposures (table 1). Cross-country skiers are repeatedly exposed to cold air,26 athletes training and competing in ice rinks may be exposed to NOx from the freezing machinery as well as to ultrafine particles from the resurfacing machines47 in agreement with reports of high asthma prevalence among ice-hockey players48 and figure skaters.49
A study from South California including 3535 children living in six areas with a high level of pollution (ozone) and six with low pollution levels reported after a 5-year follow-up that children actively participating in more than three types of sports in areas with high ozone levels had an increased risk of asthma. Participating in sports in areas with low ozone levels gave no increased risk of asthma.50
It is thus clear that the environmental conditions in which sports and training are practised are important for the respiratory health of the adolescent athlete (table 1). Pollution and harmful chemicals in the environmental air increase the risk for asthma development and BHR in the competing athlete. The effective ventilation of swimming pools is important, and effort should be made to develop no harmful methods of disinfection of the water in swimming pools. Cross-country skiing competitions should not be carried out in too cold environments, and endurance sports should not be carried out in areas with high air pollution. For the athletes who are allergic, exposure to aeroallergens may worsen asthma symptoms, and the presence of concomitant allergic rhinitis may reduce the quality of life and sports performance.51
There are two main phenotypes of asthma in athletes. First, there are athletes who have had asthma from early childhood, often accompanied by allergic sensitisation. Second, there are those athletes who contract their asthmatic symptoms through the repeated heavy training, and competitions because of their sport.52 53 The latter may not have the obvious asthmatic symptoms caused by acute episodes of bronchoconstriction, but rather cough and phlegm over prolonged periods of time, and often provoked by repeated competitions and viral infections. The latter phenotype is not unlike chronic-persistent asthma.
It should also be noted that asthma occurring during competitive sports might occasionally have fatal outcome. A nationwide American study over a 7-year period reported that of 263 sports-related deaths, 61 deaths were asthma-related provoked by competitive sports. Among these 61 deaths most occurred in boys younger than 20 years, and only three of the athletes who died used controller medication, one inhaled steroids and two used disodium cromoglycate. The remainder used no controller asthma medication, thus underlining the necessity of an optimal asthma care in athletes with asthma54
Diagnosis and differential diagnosis
Symptoms of asthma including phlegm, cough and wheeze, especially occurring after exercise, should raise the suspicion of asthma. In athletes it is important that this suspicion should be confirmed by objective tests of two reasons: first, due to recent-time doping regulations objective measures have been required to obtain approval for the use of asthma drugs in sports; second, intensive physical activity may produce increased amounts of respiratory secretions which may be confused with asthmatic symptoms. The objective tests, which may confirm an asthma diagnosis, are standardised exercise tests, exercise field tests, tests for BHR, such as metacholine bronchial challenge, or indirect tests such as eucapnic voluntary hyperpnoea and mannitol test, as well as the reversibility test; FEV1 increase from before to after bronchodilator inhalation can be an indicative of asthma with a 12% increase in FEV1 from before to after inhaled bronchodilator.
The diagnosis of EIA can be made by a standardised exercise test. The test should be standardised with regard to environmental temperature and humidity,55 and with a high exercise load, up to 95% of maximum exercise load measured by heart rate.56 The exercise test has high specificity for asthma, but lower sensitivity, especially when the adolescents are treated with inhaled steroids. Testing for direct bronchial responsiveness, through bronchial challenge with metacholine, has higher sensitivity, but lower specificity for asthma.28 57 58 The metacholine test represents a useful measure of the respiratory problems of the athlete.
Eucapnic voluntary hyperpnoea,59 also an indirect test of bronchial responsiveness, is a sensitive test of bronchial responsiveness in athletes, but physically demanding to perform.29 Sports-specific field exercise tests have been maintained to be much more sensitive in athletes as compared with other tests,60 but this could not be verified by another study.28 Inhalation of mannitol has also been suggested as a substitute measure of EIA.61
EIA usually occurs shortly after a heavy exercise. The dyspnoea is expiratory with audible rhonchi and sibilating rhonchi on lung auscultation, and the bronchial constriction usually reaches its maximum 6–10 min after stopping exercise. Often confused with EIA is the respiratory stridor occurring during maximum exercise load, inspiratory of character and representing exercise-induced vocal cord dysfunction (VCD). First described by Refsum,62 and later in adolescents by Landwehr et al,63 this condition is frequently confused with EIA. It occurs often among well-trained young girls, active in sports and should be borne in mind as a frequent differential diagnosis to EIA. EIA and VCD may co-exist.64 Exercise-induced VCD should be suspected when the respiratory stridor occurs during maximum exercise intensity and is inspiratory. A maximal inspiratory flow at 50% of forced vital capacity (MIF50)/maximal expiratory flow at 50% of forced vital capacity (MEF50) ratio <1 after a metacholine bronchial provocation has been said to be typical of VCD.65 Running on a treadmill with maximum intensity with inspiratory stridor occurring during maximum intensity can confirm the diagnosis. The diagnosis is further verified by continuous laryngoscopic exercise test.66 67 There are different treatment modalities for exercise-induced VCD not including asthma drugs; even endoscopic surgery has been found useful in selected patients.68
There are also other differential diagnoses, which may be confused with EIA in young athletes, including other chronic respiratory or cardiac conditions, whereas poor physical fitness and obesity representing possible differential diagnosis in the not physically active child rarely are problematic in the well-trained adolescent athlete (table 2).
Measures to prevent asthma development in adolescent athletes and treatment of EIA and BHR in the aspiring young athlete
In a child with asthma and adolescent with an asthma already started earlier during childhood, one main objective of all international asthma guidelines is to treat EIA and help the patient master physical activity. The aim of the treatment is to help the growing child fulfil their potentials for development. This includes sports activities and may require a close follow-up of the patient with weight on giving optimal asthma treatment.
The treatment should in principle follow the common asthma treatment guidelines, but also take into account special considerations related to the sports activity. This includes modifying treatment options related to the regulations for the use of asthma drugs in sports. These regulations are usually changed once a year by the World Anti-Doping Agency (WADA), and the physician caring for adolescents active in sports should keep updated on these regulations. During the later years, these restrictions have become less restrictive, and after 1 January 2011, both inhaled corticosteroids and some short- and long-acting inhaled β2-agonists were allowed for use in sports. From 1 January 2012, the inhaled corticosteroids and the inhaled β2-agonists salbutamol, salmeterol and formoterol will be allowed. Thus, athletes with asthma can more easily be treated according to common asthma treatment guidelines.
The treatment should be followed up by regular control visits. The follow-up can be seen as part of the diagnostic process. Early recognition of exacerbations with early stepping up of medication is important to shorten time out of competition for the athlete. With present-day treatment options, physicians are usually able to treat asthma and help the patient to optimise his asthma control and master his EIA in such a way that the adolescent athlete with asthma may compete at the international top level.
Environmental control is another important part of caring for these athletes. Optimal ventilation of swimming pools to reduce the amount of inhaled chlorine products during periods of training and competitions, environmental control of indoor skating arenas and sports arenas, and the selection of locations for outdoor sports events without environmental pollution are important. During winter sports activities, endurance competitions like cross-country skiing competitions should not take place at temperatures below −15°C. During training outdoor, protective equipment for reducing the cold-air inhalation can be used, although some of these may be cumbersome to use during competitions. Also, environmental allergens are important for symptoms in the athletes who are allergic.
These environmental measures should be the same for healthy adolescent athletes, in order to reduce the risk for developing asthma.
Asthma in adolescent athletes should be treated in the same way and according to similar guidelines as asthma in other adolescents. Mild asthma should be treated with inhaled β2-agonists when needed (prn). Inhaled salbutamol can now be freely used with a maximum daily dosage of less than 1600 μg. Also, inhaled salmeterol may be used without restrictions.
When bronchodilation is needed, inhaled ipratropium bromide may also be tried as a premedication before exercise or competition. This drug has no restrictions related to sports, but is often found useful, especially in endurance sports athletes possibly because of the increased parasympathetic activity found in many endurance athletes. Also, Montelukast can be tried, due to its bronchodilating and its partly anti-inflammatory effect. With the presence of BHR and respiratory symptoms, inhaled steroids are the drugs of choice. Inhaled steroids have become without restrictions from 1 January 2011, leaving the decision of use to the physician. Inhaled steroids represent the fundamental asthma treatment option also for the athletes. The common guidelines for controller and reliever medications should be followed.
Also, immunotherapy against environmental allergens can be considered for the athletes in whom allergic exposure plays an important role for nasal and bronchial symptoms.51 Subcutaneous immunotherapy with regular injections may represent a problem for the athlete who travels much; in such a case, sublingual immunotherapy may be a solution.
In conclusion, new information about the pathogenesis of asthma among athletes have appeared during the past few years, focusing upon the epithelial damage of the airways with airways inflammation and increased parasympathetic activity. In the young athletes, early diagnosis of BHR and asthma enabling the early start of anti-inflammatory therapy is important to reduce the effect of ongoing airway inflammation and to reduce the harmful effects of the possible environmental pollutant agents in the sports environment.
Competing interests None.
Provenance and peer review Not commissioned; externally peer reviewed.
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