Sports Medicine

, Volume 39, Issue 4, pp 295–312

The Respiratory Health of Swimmers

Authors

  • Valérie Bougault
    • Centre de Recherche de l’Institut Universitaire de Cardiologie et de Pneumologie de Québec
  • Julie Turmel
    • Centre de Recherche de l’Institut Universitaire de Cardiologie et de Pneumologie de Québec
  • Benoît Levesque
    • Institut National de Santé Publique du Québec, Direction des Risques Biologiques, Environnementaux et Occupationnels
    • Centre de Recherche de l’Institut Universitaire de Cardiologie et de Pneumologie de Québec
Review Article

DOI: 10.2165/00007256-200939040-00003

Cite this article as:
Bougault, V., Turmel, J., Levesque, B. et al. Sports Med (2009) 39: 295. doi:10.2165/00007256-200939040-00003

Abstract

Regular physical activity is recognized as an effective health promotion measure. Among various activities, swimming is preferred by a large portion of the population. Although swimming is generally beneficial to a person’s overall health, recent data suggest that it may also sometimes have detrimental effects on the respiratory system. Chemicals resulting from the interaction between chlorine and organic matter may be irritating to the respiratory tract and induce upper and lower respiratory symptoms, particularly in children, lifeguards and high-level swimmers. The prevalence of atopy, rhinitis, asthma and airway hyper-responsiveness is increased in elite swimmers compared with the general population. This may be related to the airway epithelial damage and increased nasal and lung permeability caused by the exposure to chlorine subproducts in indoor swimming pools, in association with airway inflammatory and remodelling processes. Currently, the recommended management of swimmers’ respiratory disorders is similar to that of the general population, apart from the specific rules for the use of medications in elite athletes. Further studies are needed to better understand the mechanisms related to the development or worsening of respiratory disorders in recreational or competitive swimmers, to determine how we can optimize treatment and possibly help prevent the development of asthma.

In the general population, swimming is ranked among the preferred physical activities, after walking and cycling,[1,2] and is also now frequently being introduced in some schools’ sports curriculae, especially for young children. This activity is considered beneficial for health and particularly suitable for asthma patients since a humid and warm environment is less ‘asthmogenic’.[35] The limitations imposed by bodyweight on physical activity are lessened in water, so this sport is often suggested for obese subjects, pregnant women, the elderly and those with injuries or handicap. Finally, swimming lessons may also be motivated by the wish to help prevent drowning.

Although swimming is considered to contribute to general health, potential respiratory problems associated with this sport have been described, mostly with respect to the effects of environmental conditions in which swimming is performed. Indeed, swimming pools are mostly disinfected with chlorine or its derivatives, known to be highly efficient to control viruses and bacterial growth, but not without adverse effects.[6] Chemical by-products are released in swimming pools resulting from interactions between chlorine and organic matter. They include trihalomethanes, mostly represented by chloroform, and halocetic acids. Chlorine reacts with ammonia, brought to the pool water by users and originating from sweat, urine, soap residues, cosmetics and suntan oil.[6] Halocetic acids may produce eye and skin irritation, whereas chlorine gas and chloramines, particularly nitrogen trichloride, are mainly irritants to the respiratory system.

Therefore, whilst the warm and humid air of indoor swimming pools theoretically constitutes a beneficial environment for asthmatic subjects, research has shown that athletes who regularly use chlorinated swimming pools for prolonged periods of time may have a higher risk of developing respiratory health problems than the general population.[710] After reviewing the prevalence of respiratory symptoms and disorders among swimmers compared with the general population and other athletes, this article will discuss the determinants and mechanisms by which an indoor pool environment may induce respiratory problems. Finally, this article concludes with a review of the diagnosis and management of respiratory disorders in swimmers and provides perspectives for future research and prevention.

For this review, publications available until April 2008 in the peer-reviewed literature (mostly PubMed) using keywords such as ‘chlorine’, ‘airway hyperresponsiveness’, ‘asthma’ or ‘rhinitis’ in combination with ‘athletes’ or ‘swimmers’ were analyzed. Various governmental and sport organization reports were also analyzed.

1. Respiratory Symptoms

A high incidence of upper and lower airway respiratory symptoms has been reported in competitive athletes and schoolchildren attending swimming pools.[8,11] These are summarized in table I. Upper respiratory symptoms may be quite troublesome for athletes, particularly during periods of increased allergen exposure (e.g. during the pollen season). Several studies have shown that nasal symptoms were highly prevalent in swimmers regularly attending pools, with 25–74% of swimmers complaining of chronic rhinitis symptoms.[7,15] The main upper respiratory symptoms reported are sneezing, itching, rhinorrhoea, nasal obstruction and symptoms associated with sinusitis.[7,9,15] Swimmers also frequently report headache, ocular symptoms and throat pain.[9,14]
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Table I

Prevalence of respiratory tract symptoms obtained by questionnaire

Both upper and lower airway respiratory symptoms may have a deleterious effect on swimmers’ performance, unless minimal.[16] Zwick et al.[8] reported that 79% of the swimmers training 27–37 hours per week presented various upper and lower respiratory symptoms compared with 21% of controls. Helenius et al.[12] observed swimming-induced lower airway respiratory symptoms in 57% of the 42 Finnish National Team swimmers. The most frequently reported symptoms were cough and asthma-like symptoms such as breathlessness, wheezing and chest tightness.[9,10,14,13] Respiratory symptoms are not only frequently reported by elite swimmers, but also by children regularly attending swimming pools with their school.[11]

2. Prevalence of Respiratory Disorders in Swimmers

2.1 Prevalence of Atopy and Rhinitis

Although nasal symptoms such as sneezing are the most common complaints in swimmers, there is still a paucity of data available with regard to rhinitis in swimmers.[9] In this respect, swimmers seem to be a specific population of athletes associated with a high prevalence of upper respiratory illnesses.[17,18] Indeed, elite swimmers are more susceptible to rhinitis, whether seasonal or not.[8,18] Moreover, a large number of competitive swimmers (50–65%) are sensitized to various allergens, among which are seasonal allergens, as documented by allergy skin-prick tests, compared with a control group (29–36%).[8,12,19,20] However, despite a significantly higher prevalence of allergy in swimmers, Gelardi et al.[15] showed in a recent study of 40 swimmers training 90–240 minutes three to five times a week that rhinitis was mostly non-allergic. In their study, only 16 swimmers had a typical allergic rhinitis.[15] The remaining 24 swimmers presented with non-allergic rhinitis, including infectious rhinosinusitis, non-allergic rhinitis with eosinophilia and, more frequently, neutrophilic rhinitis, suggesting that chlorine may play a role in the development of this nasal disorder and not only seasonal allergen exposure. In addition, Passali et al.[17] observed an altered nasal mucociliary transport in 35 elite swimmers compared with other athletes, which may be due to the effect of chlorine sub-products and may not only contribute to nasal problems such as rhinosinusitis and otitis but also to asthma.

Rhinitis in athletes seems under-treated. In this regard, during the summer Sydney 2000 Olympic Games only half of all athletes with allergic rhinitis reported taking an antiallergic drug.[18] Finally, not only can untreated rhinitis interfere with current activities, but this condition, highly prevalent in swimmers, may also contribute to lower airway respiratory symptoms and dysfunction.[21]

2.2 Asthma and Airway Hyper-Responsiveness (AHR)

Symptoms compatible with exercise-induced bronchoconstriction (EIB), describing a transient airway narrowing following intense exercise, are commonly reported by athletes, many of whom have no physician-diagnosed asthma. The key characteristics of bronchial asthma include variable airway obstruction, inflammation, remodelling and airway hyper-responsiveness (AHR). AHR is defined as an abnormal susceptibility to airway narrowing following exposure to a wide range of bronchoconstrictor stimuli.[22] Interestingly, Potts[9] reported an increased prevalence of AHR in swimmers compared with other athletes, without any difference in exercise-induced bronchoconstriction compared with the general population. The increased airway responsiveness to histamine observed in athletes was frequently associated with atopy, as in non-athletes.[23]

Asthma is generally diagnosed clinically on the basis of symptoms of wheezing, dyspnoea, phlegm production and cough, associated with objective evidence of variable airway obstruction[24] or of AHR to a pharmacological agent such as methacholine. However, most studies have reported either respiratory symptoms or mostly AHR separately with only a few showing their comparative prevalence in a given athletes’ population. Helenius et al.[12,20] reported that 23–31% of competitive swimmers had asthma, as defined by the presence of an AHR (histamine provocative dose of inhaled drug producing a 15% decrease in forced expiratory volume in 1 second [PD15FEV1] ≤1.6 mg) associated with at least one exercise-induced bronchial symptom monthly during the last year. In the studies available, swimmers had a previous physician’s diagnosis of asthma in up to 21% of athletes compared with up to 9% in healthy non-swimmer controls.[9,10,12,14,19,20,25] An asthma diagnosis should always be confirmed by objective means,[26] and in this regard Dickinson et al.[27] observed that 21% of athletes with a previous physician-diagnosed asthma failed to produce a positive test for asthma according to the International Olympic Committee (IOC) criteria.

The prevalence of AHR in the general population varies from 4% to 35%.[28] It has been found in 36–79% of indoor competitive swimmers and in 14% of outdoor or sea swimmers.[810,12,19,20,29] Langdeau et al.[10] found a mean methacholine provocative concentration of inhaled drug producing a 20% decrease in FEV1 (PC20) of 7.3 ± 5.5 mg/mL in 25 swimmers versus 35.4 ± 56.9 mg/mL in 50 control subjects. In a population of 22 swimmers, Boulet et al.[30] found AHR (defined as PC20 ≪16 mg/mL) in 12, with a mean PC20 of 2.26 mg/mL compared with 36.5 mg/mL in swimmers without AHR and with a measurable PC20. The prevalence of asthma and AHR in swimmers is summarized in table II.
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Table II

Prevalence of asthma and bronchial hyper-responsiveness in swimmers

A discrepancy has often been observed between the prevalence of asthma symptoms and AHR in swimmers. In a population of 25 swimmers, Langdeau et al.[10] observed a prevalence of 20% of symptomatic asthma while it was surprisingly 76% for AHR (PC20 ≤16 mg/mL). This report may suggest that symptom recognition is impaired in swimmers; it may not inevitably reflect the exact prevalence of asthma or AHR in the population, as assessed by a physician.[9,10,26,32] Athletes may consider that exercise-related symptoms are a normal effect of high-intensity training and not the consequence of airway dysfunction, and thus may not report or deny these symptoms.[9,18,33] Perception of sensitory stimuli may possibly be altered in the airways of athletes (damaged sensitory receptors?) following chlorine exposure, although this remains to be investigated. Moreover, coughing may be explained by an increased cough reflex to environmental stimuli possibly mediated through neurogenic mechanisms, in the presence or absence of airway narrowing.[34]

3. Respiratory Health in Swimmers versus Other Athletes

Elite endurance athletes are more commonly affected by respiratory symptoms,[35] rhinitis,[17] asthma[9] and AHR[10] than other athletes or recreational competitive athletes.[21,3537] The increased airway ailments seem to be partly related to the duration and intensity of exercise.[36] Among elite summer athletes, swimmers seem to develop rhinitis and allergies more frequently.[17,38]

Despite conflicting results, swimmers seem more at risk to develop asthma than control subjects.[9,10,20,37] This may also be true for other sports.[39] Helenius et al.[20] reported a 25-fold increase in the relative risk of asthma (defined as increased AHR together with at least one exercise-induced symptom) in atopic speed and power athletes, a 42-fold increase in atopic long-distance runners, and as much as a 97-fold increase in atopic swimmers compared with nonatopic controls. In 2004, swimmers had the highest prevalence of exercise-induced asthma at the summer Olympics, 44% of swimmers of the Great Britain team responding to the criteria for asthma diagnosis according to the IOC guidelines.[27] Winter cold air athletes are also frequently affected by respiratory symptoms, mainly cough, in association with a prevalence rate of AHR of up to 75% in elite cross-country skiers.[40] However, Langdeau et al.,[10] who classified a cohort of 100 athletes into four groups according to their sport environment (dry air, cold air, mixed air and swimmers) and 50 control subjects, found that swimmers had more frequent or more marked AHR than cold-air athletes. The 25 swimmers had the lowest mean methacholine PC20 (7.3 ± 5.5 mg/mL) [controls mean PC20 = 35.4 ± 56.9 mg/mL, mean of all athletes: 16.9 ± 16 mg/mL], including cold-air athletes (15.8 ± 16 mg/mL). The proportion of swimmers with methacholine ≪8 mg/mL was 60% compared with 20% in cold- and dry-air athletes and 32% in triathletes.[10] As previously described, swimmers seem to report less cough than cold-air athletes,[10] but more than soccer players.[14]

If athletes, other than swimmers, frequently practise swimming as a recreational activity or for training, this may have been misleading. This may have caused an underestimation of the exposure to chlorinated products in certain previous studies. However, in previous studies conducted in our team, cold-air athletes were not attending swimming pools (unpublished observations), suggesting minimal influence on airway function and symptoms.

4. Determinants and Mechanisms of Development of Respiratory Disorders in Swimmers

Chlorine derivatives present in the ambient air of indoor pool environments may irritate the airway, and are increasingly blamed for the occurrence of respiratory symptoms in pool attendees. Among recreational swimmers, infants and young children are especially exposed to chlorine derivatives and thus may be more subject to the harmful effects of these substances.[4143] Occupational asthma to indoor pool contaminants contained in the pool atmosphere has been reported in lifeguards.[4447] As athletes spend many hours per week training while sustaining high levels of ventilation, they can be markedly affected by the constituents and characteristics of inhaled air.[19,20,48] Hence, swimmers training for 30 hours per week are 20 times more exposed to chlorine compounds than lifeguards and about 100 times more than recreational swimmers.[20,49] The marked penetration of ambient air pollutants from indoor or outdoor environments in proximal, but also possibly peripheral, airways may contribute to the development of respiratory tract disorders, and reduce exercise performance.[5053]

Chlorine is currently the main product used to disinfect the water of indoor swimming pools worldwide.[43,54] When added to water in its liquid form, at the pH found in swimming pools (7.2–7.8), chlorine reacts to form hypochlorous (HOCl) and hydrochloric acids (HCl), which are non-volatile, potentially harmful compounds.[6,9,55,56] Chlorine gas may provoke acute damage to the respiratory tract through the generation of free oxygen radicals in the upper as well as the lower respiratory tract.[56,57] HCl and HOCl may also cause cellular injury, particularly to epithelial mucosa of the ocular conjunctivae and the upper respiratory tract.[6,56] When reacting with nitrogenous and carbon contaminants brought by swimmers, chlorine generates a number of volatile chemical sub-products that are known irritants, sensitizing agents and possible carcinogens.[6,44,55,5860] Exposure to these chlorinated compounds may cause an oxidative stress in swimmers that could partly explain their toxicity on the respiratory tract.[61] Among chloramines, nitrogen trichloride is highly volatile and responsible for the chlorine smell in pools[43,60] and for the ocular and respiratory symptoms felt by swimming-pool attendees.[44,58]

4.1 Nasal Disorders

The mechanisms involved in nasal disorders in response to chlorine derivative inhalation remain unclear. The response to these products seems different according to the atopic history of the swimmers. Indeed, Shusterman et al.[62,63] have shown that subjects with seasonal allergic rhinitis had more marked nasal congestion after chlorine gas inhalation than non-rhinitic subjects, with increased nasal resistance. In healthy subjects without AHR or allergic rhinitis, short-term laboratory exposure to chlorine concentrations of 0.1–0.5 ppm did not induce an inflammatory response in the nasal epithelium.[64] Neither mast cell degranulation nor central or peripheral neurogenic reflexes seem to be responsible for chlorine-induced nasal airflow obstruction.[63] Because chlorine gas is not often used as a disinfectant in swimming pools, except in the case of chlorine accidents, these observations remain to be confirmed in the presence of chlorine sub-products used in swimming pools.

Gelardi et al.[15] showed that the majority of cases of rhinitis in competitive swimmers were non-allergic, with prevalent nasal obstruction and neutrophilia. Exercise itself is recognized as a potential cause of rhinitis,[65] causing a rhinorrhoea more than nasal congestion; the combination of chlorine by-product exposure and exercise may thus act in synergy to induce rhinitis in swimmers. Further studies are required to characterize populations at risk of developing rhinitis and to clarify the mechanisms of action of chlorine on the nasal function.

Regarding swimmers and allergy, lung permeability may increase in subjects who use swimming pools, in response to chlorinated products, probably reflecting airway epithelial damage. This may also occur in the nasal mucosa and facilitate the penetration of aeroallergens, increasing the risk of allergic manifestations as observed in swimmers.[43,66] In a recent excellent review, this relationship between atopy and swimming pool attendance was highlighted.[43] The author suggested that atopic subjects could be more at risk to develop atopic manifestations, as chlorine-related irritants in swimming pools could act as adjuvants not only in regard to sensitization to allergens, but may also contribute to the clinical expression.

4.2 Mechanisms of AHR and Asthma in Swimmers

Asthmatic individuals may have chosen swimming as a sport based upon a suggestion from their physician or peers, as it is frequently considered less ‘asthmogenic’ than others. However, in almost 80% of swimmers with a diagnosis of asthma, this condition likely appeared after the beginning of the swimming career, suggesting that they did not start swimming because of their asthma condition.[12] This seems to indicate that the indoor swimming environment may be involved in the development of airway dysfunction.[23,43,48,67] It has then been suggested that the increasing rate of asthma among children in the European population over a few years was partly due to the introduction of swimming in the school programmes in industrialized countries.[43,68]

The ‘united airways disease’ hypothesis, suggesting that upper and lower airway diseases are both manifestations of a single inflammatory process within the respiratory tract,[69,70] may partly explain the high prevalence of asthma and AHR in swimmers with regard to the high prevalence of rhinitis in this population.

4.2.1 Airway Inflammation and Epithelial Damage

Carbonnelle et al.[71] and Bernard et al.[41] studied the acute effects of a swimming session on the lung epithelium in recreational swimmers. They observed transient epithelium damage due to chlorinated swimming pool attendance in recreational swimmers. They compared serum levels of lung proteins such as CC16 released in the airways and alveolar surfactant-associated serum proteins (SP-A and SP-B) before and after 2 hours spent in a chlorinated swimming pool.[72] These proteins are used as markers of lung epithelial barrier integrity in a variety of acute or chronic lung disorders. The serum concentration of CC16 and surfactant proteins reflects an increase in the permeability of the alveolar-capillary barrier.[72] Indeed, surfactant proteins are normally secreted by airway or epithelial cells and their release in the blood can only be explained by assuming that they leak from the lung into the bloodstream.[72] After a 2-hour exposure to a chlorinated pool environment, an increase of blood SP-A and SP-B levels was reported, even after an hour without exercising, excluding a major role of exercise on the loss of pulmonary epithelium integrity. No significant variation of CC16 was noted in children or adults at the end of the second hour. These data indicate firstly that 2 hours spent in a swimming pool environment is sufficient to significantly alter lung permeability. Secondly, deep lung seems preferentially affected by such exposure with regard to changes in CC16 compared with SP-A and SP-B. This evidence of epithelial damage may be attributed to the presence of chlorine sub-products, as no such SP-A and SP-B changes have been observed after an exercise in swimming pools disinfected by a copper/silver process.[71] We should, however, note that the subjects developed neither respiratory symptoms nor a reduced pulmonary function in that last study.

Cumulated school pool attendance was positively correlated to the serum concentration of pneumoproteins, airway inflammation and asthma indicators (SP-A, SP-B and CC16).[41,42,71] The clinical significance of these effects on the lung epithelium of recreational swimmers exposed long term to chlorination products in indoor swimming pools are uncertain, but deserve further investigation, as they seem to persist and increase with the number of hours spent in the swimming-pool environment. That is also true for very young children attending pools as baby swimmers or with the highest pool attendance, who present epithelial damage, similar to that observed in current smokers.[41] Therefore, as a result of a prolonged exposure to chlorine, a reduction in the level of CC16 in blood serum similar to the one observed in smokers or in subjects exposed to chemical smoke was observed at rest in children who attended chlorinated swimming pools as infants compared with other children.[43,7375]

Levesque et al.[14] reported a positive correlation between the chloramine levels in the air or water of the swimming pools and upper and lower respiratory symptoms in 72 competitive swimmers to whom a questionnaire on respiratory symptoms was administered. Neutrophils were also more abundant in the induced sputum of elite swimmers at rest compared with healthy controls.[19,25] Helenius et al.[19] studied induced sputum in 29 elite swimmers who competed for a mean of 9.1 years versus 19 healthy controls. Contrary to the observation made by previous authors on recreational swimmers, they found a significantly increased eosinophil cell count in swimmers. Moreover, 21% of them had an eosinophilia, with a sputum differential eosinophil count over 4% compared with none in controls. During a 5-year follow-up, the eosinophilia increased in active swimmers.[12] Swimmers with EIB symptoms presented higher eosinophil counts (7.6%) compared with swimmers without symptoms (0.7%).[12,19] Neutrophils and eosinophils were more activated in swimmers than in control subjects, as indicated by eosinophil peroxidase and human neutrophil lipocalin levels.[19] These results suggest that exposure to chlorine derivatives, when repeated for many years, may contribute to the persistence of airway inflammation at rest and probably AHR in swimmers.

Chloramine-induced changes to the lung epithelium may become permanent in the case of a long-term exposure, for example in elite swimmers. Eosinophilic airway inflammation has been reported after long-term exposure to the pool environment in elite swimmers, but not in recreational swimming-pool attendees. However, other inflammatory cells (table III) remain to be studied in recreational and elite swimmers to better understand the inflammatory mechanisms involved, although epithelial damage seems to precede this process as suggested by our recent study.[81] Further studies are required to investigate whether epithelial damage is reversible as well as the time-course of recovery of pneumoproteins (SP-A and SP-B) and alveolo-capillary barrier permeability.
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Table III

Airway inflammatory cells in athletes and markers of activation of inflammatory cells in swimmers’ airways

4.2.2 Airway Remodelling

Inflammatory cell recruitment in the respiratory tract may be consecutive to airway epithelial damage, and especially bronchial epithelial cell (BEC) changes.[82] The high ventilation sustained during exercise itself may affect airway epithelium in changing the viscosity and tonicity of airway surface liquid.[53] BEC numbers and apoptosis seem to be increased after intense exercise, and a correlation was found between this change and ventilation rate sustained during exercise.[78,83] Moreover, after 45 days of a low- to moderate-intensity physical programme in mice training 5 days a week on a motorized rotor, Chimenti et al.[82] found a 2-fold increase in BEC apoptosis, a 4-fold reduction in ciliated epithelial cell counts, a 5-fold increase in proliferating cell counts and a 56% increase of epithelial thickness in bronchiolar epithelium compared with sedentary mice. Therefore, epithelial damage may appear consecutively to the intense hyperventilation through the dehydration of the mucosa and an induced shear stress on the airway wall, followed by a repair process.[78,82] However, as other authors found no change in the BEC level in sputum at rest and after a running or swimming race,[25,76] further studies are needed.

Basic mechanisms of chlorinated product toxicity are related to the high solubility of chlorine in water and, at the physiological pH found in the bronchi, to the formation of hydrochloric and hypochlorous acids within epithelial tissues. These acid compounds are known to be highly irritating to the mucosa. Moreover, repeated cleavage of chlorinated products in contact with respiratory tract water provokes a release of oxygen free radicals. Functional and pathological changes in the airways resulting from chlorine by-product exposure are often considered to be mainly caused by such resulting oxidative stress.[84]

The effects of long-term chlorine by-product exposure on a swimmer’s airways structure in the context of an indoor swimming pool are currently unknown. However, high-level acute exposure to chlorine has been described in experimental studies[8486] or in the case of accidental exposure.[8794] Airway epithelial damage and desquamation are the main consequences of an acute chlorine exposure, with an alteration in the morphology of the cells and replacement of cuboidal epithelial with flat cells.[8486] Increased subepithelial fibrosis has been observed, following subepithelial haemorrhage and inflammatory infiltrates, after accidental high-level short-term chlorine exposure.[85,90] Repeated low- to moderate-level exposure to chlorine may therefore induce an airway remodelling process though the activation of fibrogenic cytokines in elite swimmers. To our knowledge, Karjalainen et al.[40] and Sue-Chu et al.[95] are the sole authors who examined bronchial biopsies of athletes. They observed in elite cross-country skiers an inflammatory infiltrate and an increased subepithelial tenascin, as well as lymphoid aggregates.[40,95] These changes could be due to the combination of endurance training and repeated cold dry air exposure, but the time-course and mechanisms by which these changes occur are unknown.

4.2.3 Accidental Exposure to Chlorine: Reactive Airway Dysfunction Syndrome

Two main types of occupational asthma have been described, the ‘classic form’ with a latency period (months to years) between initiation of exposure and the development of symptoms, and another without such a latency period called ‘irritant-induced asthma’, initially described as the reactive airway dysfunction syndrome (RADS) after a single exposure to high levels of toxic irritant substances, or also after repeated subacute exposures.[96] Indeed, RADS has been described as resulting from exposure to high levels of toxic substances such as chlorine, sulphur dioxide, ammonia or other substances with highly irritant properties inducing acute and often persistent airway damage.[8794] Acute accidental release of high concentrations of chlorine in swimming pools may cause respiratory injuries, although very rarely death of the victims.[59,8893] In general, cough, breathlessness and wheezing are the main respiratory symptoms in patients exposed to an accidental high-level exposure to chlorine. In contrast to a low level exposure to common irritants in non-asthmatic workers, in the case of RADS, expiratory flows may sometimes be reduced by >50%,[93] and patients develop transient AHR of variable intensity according to the inhaled dose.[59,9294] Subjects with rhinitis, atopy, AHR or a chronic respiratory disease and those engaged in a physical exercise at the time of the accident report more severe respiratory distress than others, especially over a concentration of 1 ppm.[59,92,94,97] Reduced lung function generally recovers within approximately 15 days depending on the inhaled dose of chlorine.[59,91,94,97] However, the restitution of functional integrity does not necessarily mean histological integrity, as many days after expiratory flows and partly AHR have recovered, patients may still show epithelial desquamation and an inflammatory infiltrate, mainly neutrophilic.[87,89,91] Deschamps et al.[89] reported the case of an atopic patient without a diagnosis of asthma before the accidental inhalation of chlorine in the industry, but still with asthma 2 years after exposure; bronchial biopsies revealed in this patient a marked epithelial damage with a slight inflammatory lymphocytic process. The authors suggested that epithelial destruction could impair the epithelial release of bronchodilator substances and contribute to persistent asthma.[89]

The model of acute intense exposure may help to better understand what happens in the case of repetitive lower-dose chlorine by-products exposure, as in regular swimmers. Epithelial cell damage is evidenced by an increase in CC16 in the blood serum, as reported in a group of 18 children, victims of an accidental high-chlorine exposure during their swimming lesson.[91] It is, however, conceivable that low-level long-term exposures could cause a process of the same nature as RADS in some individuals, especially in those regularly attending swimming pools, although at a much lower grade.[98] However, this remains to be confirmed.

5. Diagnosis and Management of Respiratory Disorders in Swimmers

The diagnosis of rhinitis and asthma is initially based on the clinical features of these diseases. For asthma, the demonstration of a variable airway obstruction from measurements of expiratory flow response to a bronchodilator, spontaneous variations of airway obstruction, or measurement of airway responsiveness (e.g. methacholine, isocapnic hyperventilation) is essential to distinguish this entity from non-specific symptoms attributable to another condition. Currently, the management of asthma in swimmers is similar to asthma in other populations.[99] It is mostly based on the use of rapid-acting bronchodilators for intercurrent symptoms or prevention of EIB, associated with an inhaled corticosteroid if asthma symptoms are regularly experienced, and with added long-acting inhaled bronchodilators if asthma control is not achieved by a low dose of inhaled corticosteroid and, in some cases, additional medications such as leukotriene antagonists.[99]

The specific response to the various asthma medications in swimmers needs to be studied and reports in various sports have demonstrated a reduced response to some of these agents in high-level athletes,[100,101] possibly in relation to the different (neutrophilic) type of airway inflammation or other changes in the asthma phenotype. Asthma medications in competitive athletes are regulated and the IOC and World Anti-Doping Agency (WADA) regulations should be reviewed before using these medications.[102]

In this population, long-term intermittent chlorine exposure may possibly impair the respiratory function and affect athletic performance, as observed in the presence of other strong pollutants.[5053,103] As they may be particularly affected by the adverse effects of untreated rhinitis, elite swimmers should take the necessary precautions to minimize the impact of upper respiratory conditions on their ability to perform.[18,104] This holds especially true during spring and summer for pollen-sensitive swimmers. Allergy testing allows identification of sensitization to common airborne allergens and should be performed in athletes presenting upper or lower respiratory symptoms. Rhinitis should be recognized in order to reduce its impact on their daily life and performance.[104] Medications used to treat rhinitis have been summarized in a review from the Allergic Rhinitis and its Impact on Asthma (ARIA) group.[38,105] It has been shown that the symptoms, the quality of life, and the performance of athletes with allergic rhinoconjunctivitis were improved with appropriate medication and environmental measures.[104]

Current guidelines emphasize that an asthma diagnosis should be confirmed by objective means, in the presence of suggestive symptoms, to identify alternative aetiologies of the symptoms, assess the severity of the condition, and offer appropriate interventions to reduce the untoward effects of asthma and help prevent its worsening. It may be important to regularly assess swimmers’ respiratory health to identify such problems at an early stage. However, the increasing proportion of athletes taking asthma medication, particularly β2-agonists, led the IOC and WADA to institute guidelines to confirm asthma and document AHR.[106] The sole report of exercise-induced respiratory symptoms cannot justify asthma medication anymore, for previously described reasons (see section 2.2). Therefore, athletes using asthma medications must now be authorized beforehand by the proper sport authorities after a formal report by a physician. According to IOC and WADA, at least one authorized bronchial provocation testing must be positive to allow the use of regulated drugs for asthma, and the results must be provided if the swimmer performs at an international level. Different bronchial challenges are presently available to confirm the presence of variable airway obstruction such as eucapnic voluntary hyperpnoea, exercise test, hypertonic saline, methacholine and, recently, a mannitol challenge.[103] Guidelines for these challenges have previously been described,[107,108] as well as the positivity threshold for each test, which allows international athletes to use approved asthma medications, as summarized in table IV. For the Turin Olympic Games in 2006, the IOC recommended the following: a methacholine challenge was considered as positive in non-steroid-treated athletes if the PD20 was as low as 2 μmol or 400 μg or less (PC20 ≤ mg/mL).108] The criteria remained similar for the 2008 Beijing Olympic Games. In the general population, AHR has often been defined as a methacholine PC20 ≤16 mg/mL,[107] although there is a ‘grey zone’ of AHR between 4 and 16 mg/mL. However, if negative to methacholine, they may show a positive response to the other tests.[32] Respiratory symptoms in subjects with a PC20 between 4 and 16 mg/mL may be due to asthma as previously suggested.[109] The IOC and WADA guidelines are regularly updated.[102,106]
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Table IV

International Olympic Committee and World Anti-Doping Agency positivity criteria according to the test used

According to the WADA guidelines, recurrent symptoms of bronchial obstruction are a diagnostic prerequisite for asthma or EIA in athletes, and laboratory tests alone are not sufficient for the diagnosis.[102,106] However, athletes, and especially swimmers, may not recognize, may ignore or may not feel symptoms associated with bronchoconstriction and accordingly not consult a physician for a diagnosis or intervention.[10,13,26,33,110] Therefore, in elite swimmers, in addition to confirming the presence of AHR, particular attention should be paid to documenting relevant symptoms.

To prevent the consequences of exposure to chlorine derivates, it would be preferable to ensure that ambient levels of these components are kept at a minimum. In a review on chlorination products, Bernard[43] reported mean levels of nitrogen trichloride in the atmosphere of public indoor pools between 0.3 and 0.5 mg/m3, sometimes reaching 2 mg/m3. In the study of Levesque et al.,[14] the mean concentrations of chloramines in the air of seven swimming pools varied from 0.26 to 0.41 mg/m3. Using the same technique, Hery et al.[61] documented chloramine concentrations varying from ≪0.5 to 1.25 mg/m3 in 13 swimming pools. Massin et al.[44] also reported mean chloramine concentrations in the air of 46 swimming pools between 0.24 mg/m3 and 0.46 mg/m3 in 17 community centres. Elite swimmers, often training 2 hours twice daily and sometimes >30 hours per week, sustaining a high level of ventilation and inhaling immediately above the water surface, are a highly exposed population to chlorine derivatives. Because chloramine levels in the air above swimming-pool water is influenced by ventilation and the pool water chemistry, a proper aeration and reduction of human protein load in the water may reduce respiratory health problems of swimmers. Chloramine accumulations in the air above the water may be removed by efficient ventilation, which would increase turnover and remove concentrated chloramines. An efficient measure to reduce chloramine production would also be a modification of swimmers’ behaviour; for example, encouraging showering before entering any pool, wearing a swim cap and facilitating frequent bathroom breaks for swimmers, particularly children, since this could significantly reduce the amount of urine and other nitrogenous waste contaminating the water, which leads to the accumulation of chloramines in the swimming pool’s ambient air. Certain preventative measures are easy to implement and may contribute to a better respiratory health of swimmers and bathers. Alternative disinfection processes such as chlorine dioxide, bromine-based disinfectants, ozone or UV use may also replace chlorine, but further studies on their effects on the respiratory health should be performed. Bromine-based disinfectants are volatile liquids with toxic fumes that irritate the skin, eyes and respiratory tract, while ozone use, the most powerful oxidizing and disinfecting agent available, is often followed by a deozonation process necessitating chlorine or bromine use and is more expensive.[55] Ozone is also a strong respiratory irritant.[55] The risks posed by brominated by-products and the use of a disinfectant as an oxidizing agent have yet to be elucidated. Other disinfectant systems may be used and limit the production of chlorinated disinfection by-products, especially in smaller and domestic pools, as hydrogen peroxide is associated with copper/silver ions or iodine.[55] Logically, the air of a copper/silver pool has been shown to contain no detectable trichloramines. Epithelial damage observed in swimmers attending chlorinated pools was not found when copper/silver disinfection was used.[71] However, copper/silver disinfection cannot remove organic matter and does not seem to ensure the total elimination of viral pathogens from water, even if its use is combined with low levels of chlorine.[111] Little is known on the possible effects on the respiratory health of copper/silver ionization.

Because oxidative stress has been shown to be strongly involved in airway damage caused by chlorine,[58,84] an antioxidant supplementation has been suggested to have a protective role in swimmers,[58,112] and especially on AHR.[113,114] However, further studies are needed to support this recommendation.

6. Areas for Future Research

Further research is necessary to better understand the mechanisms involved in the development of rhinitis, asthma and AHR in swimmers, particularly on how inflammation and remodelling, especially those induced by environmental exposures, can lead to these changes.

Asthma and AHR may develop through the swimming career, but their prevalence seems to decrease in swimmers who stop high-level training, suggesting a reversibility of alterations in airways function.[12] Indeed, in a study of Helenius et al.[12] the prevalence of AHR went from 31% during swimming activity to 12% in former swimmers. This is in agreement with Potts,[9] who found a reduction in respiratory symptoms in swimmers who did not exercise in a swimming pool for several days, although the mechanism of improvement may be different. Similarly, Simon-Rigaud et al.[67] reported a significant reduction of AHR in eight competitive swimmers after the annual swimming-pool cleaning compared with before. This observation should be confirmed, but could help with understanding to what extent AHR is reversible and what the mechanisms involved in swimmers are. The reversibility of epithelial damage in the case of long-term chlorine exposure also remains to be studied.

Eventually, airway protective measures will be developed for competitive swimmers either in the form of medications or modifications of the pool environment. The efficacy and safety of different disinfection processes should be tested as well as the effects of better ventilation that could remove the contaminants present in the air above the water. It should be determined if some medications can prevent the effects of chlorine sub-products on airway function, and possibly inflammation or remodelling.

7. Conclusions

Swimming is an enjoyable sport that could help maintain physical fitness and therefore should be promoted. However, evidence has shown that chlorine derivatives may create irritant effects to the upper and lower airways. Although low level or infrequent exposure to these agents may not be detrimental, alterations in airway function are common in swimmers and various factors may promote the development of airway dysfunction in susceptible populations such as competitive athletes. Chlorine sub-products seem to be the main agents responsible for swimming pool-induced rhinitis, asthma and AHR. The clinical significance, time-course and reversibility of the observed airways changes are not well documented. However, the potential risks from exposure to chlorination by-products in well managed swimming pools should be set against the benefits of physical activity and the risks of microbial disease in the absence of disinfection. More information is needed to better understand the optimal management of respiratory problems in swimmers, particularly high-level athletes, and how to prevent changes in airway function and asthma.

Acknowledgements

Valérie Bougault was supported by Université Laval (GESER), Quebec, Canada. The authors have no conflicts of interest that are directly relevant to the content of this review.

Copyright information

© Springer International Publishing AG 2009