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Abstract
Respiratory diseases such as asthma, chronic cough, recurrent respiratory infections and various upper airways conditions are common in elite athletes, but these conditions are often underdiagnosed and undertreated. Recurrent cough, often observed after exercise, is the most commonly reported symptom in athletes, particularly winter athletes, but it does not predict airway function; its intensity correlates with the dryness of inspired air but may not be associated with airway hyper-responsiveness. Rhinitis, either allergic or not, is highly prevalent in athletes, particularly non-allergic rhinitis in swimmers. Finally, dysfunctional breathing, including vocal cord dysfunction, may mimic or accompany asthma in a significant number of athletes. These conditions should be recognised and treated properly according to current guidelines, although how these last apply in the athlete is uncertain. Furthermore, regulatory agencies' restrictions on the type of drugs allowed for therapeutic use of these conditions in competitive athletes should be checked.
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Introduction
Elite athletes frequently report respiratory symptoms, particularly postexercise dyspnoea and cough.1 These symptoms can be related to one or more of the many respiratory ailments affecting athletes, such as asthma,2,–,9 rhinitis,10 11 vocal cord dysfunction (VCD)/dysfunctional breathing,12 13 recurrent respiratory infections or be related to environmental exposures.14 15 Allergy frequently contributes to the development and manifestations of airway diseases in the athlete but other factors, such as exposure to pollutants, respiratory irritants or ambient air properties,16 may play a role. Furthermore, psychological disorders and overtraining can mimic respiratory diseases.17 This report reviews the possible mechanisms responsible for chronic or exercise-induced cough in the athlete, and the main upper airway conditions which may induce cough or other respiratory symptoms in this population.
Respiratory symptoms in athletes
Elite athletes frequently report troublesome asthma-like respiratory symptoms, mostly after exercise, which can interfere with training and performance although such symptoms are not always associated with the presence of abnormal airway function.1 18,–,24 Therefore, respiratory symptoms are not very useful to predict pulmonary function or airway responsiveness in the athlete.18 25 Such symptoms can be related to exercise-induced bronchoconstriction (EIB), but they can also occur in the absence of airway narrowing.25 26 In many instances, they are caused or promoted by upper airway disorders but in some, they probably reflect a normal physiological response to intense exercise in elite athletes.
Cough in the athlete
Prevalence of cough in the athlete
Cough is a particularly predominant symptom in winter athletes, while swimmers rarely report respiratory symptoms despite a high prevalence of airway hyper-responsiveness (AHR) in this population.9 23 26 27 Rundell et al25 have reported that cough is the most common symptom among athletes with exercise-induced asthma. Heir et al found that 86% of skiers and 35% of control subjects had at least one respiratory symptom, and that cough was the most common symptom among skiers and controls.27 Furthermore, we have recently observed that winter athletes had an increase in respiratory symptoms in the winter compared with the summer, with a particularly troublesome cough following exercise in 44% of the athletes in summer and 71% of these athletes in the winter, while there was no change in control non-athletes.28
Mechanisms of cough
Cough is primarily a protective reflex, involved in the elimination of foreign bodies and bronchial secretions.29 It may also be due to an underlying disease or an airway response to environmental agents, often in association with irritation with or without inflammation of the airways. It can be associated with hypersensitivity of the cough reflex or with AHR. Potential causes of postexercise cough in athletes include asthma, upper airway cough syndrome (UACS) related to rhinitis, sinusitis, laryngitis or other upper airways conditions, gastro-oesophageal reflux disease (GERD), chronic eosinophilic bronchitis (CEB) or environmental exposures.29
With regard to the mechanisms of cough, there are two main types of vagal afferent pathways that could induce cough when activated: cough receptors and C-fibres. Rapidly adapting receptors are located in the larynx and trachea, and respond to mechanical simulation. Bronchopulmonary C-fibres are activated selectively by stimuli such as capsaicin, bradykinin and activators of the cation channel transient receptor potential ankyrin-1 (TRPA1).30 C-fibres end in the airways and lung parenchyma in addition to pulmonary vascular walls. These C-fibre terminals contain neuropeptides such as substance P, neurokinin A and calcitonin gene-related peptide.30
In subjects with asthma, cough may result from the release of bronchial mediators by airways mast cells, often in association with bronchoconstriction.31 Cough may be the only symptom reported by asthmatic patients (cough-variant asthma) particularly when its sole manifestation is exercise-induced asthma.32 The airway narrowing following exercise is considered to mainly result from airway water loss during the conditioning of inspired air, and this might also play a role in cough.31 Banner et al33 34 showed that hyperpnoea with poorly conditioned air resulted in coughing, with a frequency correlated with the rate of respiratory heat loss. Respiratory mucosal drying can induce a physical distortion of nerve endings and trigger cough receptors. Furthermore, water loss in the bronchial mucosa can make bronchial fluid more hyperosmolar and trigger sensitory nerve receptors. Factors that stimulate these receptors trigger an autonomic reflex which may cause airway constriction and mucosal secretion. Cough receptors can also respond to thermal stimuli or to mediators that are produced or released as a consequence of airway cooling. Lung distortion or stretching can cause the release of prostaglandins, which have been shown to provoke cough through their effects on airways C-fibres.30 Cold air inhalation can also possibly induce neurogenic inflammation, with the release of tachykinins.
Treatment of cough
The treatment of cough in the athlete is uncertain and before further studies on this topic, we should treat according to current guidelines.29 35 36 According to those last, we have to treat the underlying cause, but if there is no evidence of a specific underlying condition, we should use an empirical approach. Furthermore, in high-level athletes antidoping regulations will modulate those recommendations. For example, UACS is usually treated with first-generation antihistamines associated with pseudoephedrine or with an inhaled nasal anticholinergic agent. However, pseudoephedrine above a urinary concentration of 150 µg/ml is prohibited in competition only and therefore should not be taken within 24 h of any competition.37
In the presence of asthma or CEB, inhaled corticosteroids are the mainstay of cough treatment and in the presence of GERD, a proton pump inhibitor is usually prescribed. All these last conditions frequently affect the athlete. However, the optimal treatment of cough in athletes, and its effects on performance have not been formally studied.
Upper airways diseases in the athlete
Athletes often suffer from many upper airway diseases such as allergic or non-allergic rhinitis, sinusitis, dysfunctional breathing and glottic dysfunction/VCD. The prevalence of respiratory allergies is high in the athlete, in the order of 25–56%.9 16 21 38 39 It is predictive of a diagnosis of rhinitis, and is associated with an increased risk of asthma, mostly observed in endurance athletes.39 40
Upper respiratory infections
Symptoms suggestive of upper respiratory tract infection (URTI) are responsible for 30 to 40% of visits to sports medicine clinics by elite athletes.41,–,44 URTI are frequently of viral origin, rhinoviruses, adenovirus, coronavirus and respiratory syncytial virus being common causative agents.45 In a study looking at respiratory symptoms in athletes, an infectious cause was found in 31% of the episodes over a 5-month period.42 Physicians attributed 89% of episodes of upper airways symptoms in elite athletes to viral or bacterial URTI. However, a pathogen or another laboratory parameter indicative of infection was found in only 57% of episodes. Laboratory investigation identified allergy in a considerable proportion of the cohort (39%). The possibility that URTI-like symptoms could be due to a non-infectious cause is supported by the report of a beneficial effect of prophylactic use of a topical anti-inflammatory oral/nasal spray on the incidence of postrace upper respiratory symptoms in runners.44 46
It has been suggested that moderate physical activity could reduce the incidence of respiratory infections while prolonged high-intensity exercise could have the opposite effect.47 48 An impaired cell-mediated immunity and increased inflammatory response, via a decreased macrophage and Th-1 cell cytokine production have been proposed to explain this phenomenon.48,–,50
Rhinitis
Allergic and non-allergic rhinitis, and more specifically exercise-induced rhinitis, are common in the athlete, and they affect more than a third of the athletes.9 11 51 52 Globally, allergic diseases are estimated to affect about half of the athletic population and as atopy is strongly associated with rhinitis, it is not surprising to see so many athletes suffering from this condition.11 51 53 54 In a cohort of 133 athletes, we found that 73% of athletes were atopic, with at least one positive skin prick test response to airborne allergens. In a study from Katelaris et al on 214 athletes, 56% reported symptoms consistent with allergic rhinoconjunctivitis, 41% also having a positive skin test response to at least one allergen.54 In a survey of Australian Olympic and Paralympic athletes, 56% had a positive skin prick test to at least one allergen, 37% had allergic rhinoconjunctivitis and 24% seasonal allergic rhinoconjunctivitis. Swimmers were most likely to have asthma and positive skin tests to any allergen. Very few athletes with self-reported allergic rhinitis took any medication to relieve their symptoms.53 Furthermore, the prevalence of allergic rhinitis seems to have increased since the 1980s.5 10 11
During training, athletes are often markedly exposed to airborne allergens, cold air and various pollutants which could contribute to their rhinitis. Although some athletes experience an improvement of rhinitis symptoms during exercise, probably following an increase in nasal sympathetic tone, exposure to allergens or to irritants such as particulates, sulphur dioxide, ozone or chlorine derivatives from swimming pools, in addition to weather changes, can worsen this condition and cause troublesome symptoms. These exposures may also worsen underlying airway inflammation and epithelial damage.55,–,58 Nasal breathing has a protective effect against exercise-induced asthma,59 60 probably through its conditioning of inspired air.56 57 60 When athletes develop nasal obstruction however, they switch from nasal breathing to oral breathing, increasing penetration of air content in lower airways.
There is much evidence now that upper airway inflammation influences lower airway.61 62 Studies using nasal allergen challenges in allergic rhinitis subjects have shown that following local deposition of allergens in the nose, there was an increase in eosinophils and adhesion molecules in the lower airway of atopic subjects.63 We also previously found lower airway remodelling in rhinitic subjects without evidence of asthma.64 The mechanisms of interaction of upper and lower airways include aspiration of bronchial secretions from the upper airways, mouth-breathing, nasobronchial reflex or passage in the systemic circulation of cytokines and mediators acting on the lower airway.57 During regular training, athletes are repeatedly exposed to allergens, cold air and pollutants and these can have a significant impact on their allergic diseases and respiratory physiology through these mechanisms.38 40
With regard more specifically to competitive swimmers, up to 74% of swimmers report symptoms of rhinitis.52 65 Intense swimming training is associated with an increase in nasal symptoms and a reduction in rhinitis-related quality of life in most competitive swimmers.61 Most often, rhinitis symptoms probably result from chlorine derivatives exposure as they are more prevalent during training season in swimmers while they recover quickly after swimming training.52
Otherwise, runners often experience repeated episodes of rhinorrhoea, mucociliary clearance being reduced after running.56 In skiers, rhinorrhoea and nasal congestion are common after performing exercise in cold air. Cold air can trigger a parasympathetic reflex with associated rhinorrhoea while nasal vasculature congestion may explain nasal congestion. Mucociliary transport time and nasal resistance were reported to be abnormal but normalise after use of a nasal decongestant, in elite skiers.56
Evaluation of a subject with suspected rhinitis includes past/present medical history, nasal/thoracic examination and allergy skin tests. It has been suggested that pulmonary function testing including evaluation for EIB should be performed, as many athletes do not recognise and report symptoms of asthma.51 65 Allergic rhinitis can affect sport performance and should be treated according to current guidelines.61 66 The treatment of rhinitis in the athlete includes allergen avoidance, a reduction of irritant exposure, inhaled nasal corticosteroids, inhaled nasal anticholinergics, leukotriene receptor antagonists and immunotherapy.61 66
Intranasal corticosteroids are the first-line therapy for perennial allergic rhinitis.61 Athletes who are treated with intranasal steroids for their seasonal rhinitis show significant improvements in symptoms, quality of life and performance scores.67 Topical decongestants including eyedrops and nasal inhalers are permitted in sport, but if regularly used they cause a rhinitis medicamentosa. Oral decongestants are not allowed for high-level competitions as they may enhance performance and cause significant side-effects. Antihistamines are helpful in relieving symptoms of allergic rhinoconjunctivitis. First-generation antihistamines have sedative and anticholinergic effects but last-generationantihistamines do not have these effects.
Immunotherapy may be considered in athletes who cannot avoid allergens and may not control their symptoms with allergen avoidance and pharmacotherapy.
The high-level athlete should check regularly with and adhere to antidoping regulations.
Dysfunctional breathing: vocal cord dysfunction
Dysfunctional breathing is often observed in the athlete in the form of VCD or hyperventilation syndrome. These conditions can lead to long-term inappropriate treatment and be misinterpreted as difficult-to-control asthma.
VCD (or glottic dysfunction) can mimic exercise-induced asthma and is a common cause of upper airways obstruction during exercise, occurring in 5 to 27% of patients referred for exercise-induced dyspnoea.12 68,–,74 VCD is characterised by a paradoxical closure of the vocal cords during inspiration and can occur during exercise. VCD can occur at any level of exertion and frequently presents as noisy breathing, dyspnoea, wheezing and sensation of obstruction at the neck and upper chest level and cough. It has a sudden onset, usually lasts less than 5 min and is self-limited. In a study of 370 elite athletes assessed for the presence of VCD by evaluating the symptoms of inspiratory stridor, Rundell and Spiering13 found that 5% of the group exhibited signs of VCD.
Although its origin is unclear, VCD is more frequent in women and can be related to anxiety disorders, chronic rhinosinusitis and GERD. Various triggers such as inhalation of irritants, cold air, talking, laughing, deep breathing, exercise and others such as postnasal drainage and viral infections can trigger such paradoxical vocal cords movement. In a retrospective study of videolaryngoscopic tapes of 22 juvenile patients with VCD, Powell et al75 found that 95% of those studied exhibited signs and symptoms related to GERD, supporting an association between VCD and GERD. Otherwise, a relationship between psychological stress and VCD has also been suggested.75 76 Powell et al found that 55% of the 20 young patients with VCD reported considerable stressors, mostly from participation in competitive sports.75
The diagnosis of VCD is sometimes difficult, particularly as it may be intermittent. It can be suspected by an incomplete or truncated inspiratory loop of the flow-volume curve.71 73 Direct visualisation of the upper airway (fibreoptic laryngoscopy) is the gold standard for making a definitive diagnosis of VCD.77 78 Multiple manoeuvres can precipitate the abnormal closure of the cords during inspiration and thus help diagnose the condition.
With regard to treatment, reassurance of the patient is the first intervention to offer, mentioning that the condition is not life-threatening.79,–,81 Reassurance can be successful in resolving VCD, while benzodiazepines have also been used.80 81 Heliox, a combination gas of helium and oxygen, has been suggested, but it is not practical.82 Biofeedback, speech therapy, hypnosis, psychological therapy and even botulinum toxin have all been used with some variable success to treat chronic VCD.79 81,–,85 A consultation with a speech pathologist should be considered.
Conclusion
In conclusion, respiratory symptoms, including cough, are frequently experienced by athlete, and have many possible aetiologies. The possible impact of persistent or exercise-induced cough on performance and its optimal treatment remain to be further determined. A systematic investigation and treatment according to current guidelines are required to allow athletes to minimise this troublesome symptom. Upper airway diseases are common in elite athletes, particularly rhinitis, which may be allergic or not. VCD may mimic or accompany asthma in a significant number of athletes but is often undiagnosed. All these conditions should be recognised and treated properly to ensure that the athlete's performance and quality of life are not affected by these ailments.
References
Footnotes
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Competing interests Disclosure of potential conflicts of interest of L.-P. Boulet. Advisory Boards: AstraZeneca, GlaxoSmithKline, Merck Frosst and Novartis. Lecture fees: 3M, AstraZeneca, GlaxoSmithKline, Merck Frosst and Novartis. Sponsorship for investigator-generated research: AstraZeneca, GSK, Merck Frosst and Schering. Research funding for participating in multicentre studies: Altair, Asmacure, AstraZeneca, Boehringer-Ingelheim, Genentech, GlaxoSmithKline, Pharmaxis, Schering, Wyeth. Support for the production of educational materials: AstraZeneca, GlaxoSmithKline and Merck Frosst. Governmental: Adviser for the Conseil du Médicament du Québec, AETMIS. Organisational: Chair of the Canadian Thoracic Society Respiratory Guidelines Committee and chair of GINA Guidelines Dissemination and Implementation Committee. Holder of the Laval University Chair on Knowledge Transfer, Prevention and Education in Respiratory and Cardiovascular Health. Member of the Knowledge Translation (KT Canada) supported by the CIHR.
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Provenance and peer review Not commissioned; externally peer reviewed.