OBJECTIVE: The goal was to estimate the burden of allergic diseases associated with chlorinated pool exposure among adolescents.
METHODS: We examined 847 students, 13 to 18 years of age, who had attended outdoor or indoor chlorinated pools at various rates. Of them, 114 had attended mainly a copper-silver pool and served as a reference group. We measured total and aeroallergen-specific immunoglobulin E (IgE) levels in serum and screened for exercise-induced bronchoconstriction. Outcomes were respiratory symptoms, hay fever, allergic rhinitis, and asthma that had been diagnosed at any time (ever asthma) or was being treated with medication and/or was associated with exercise-induced bronchoconstriction (current asthma).
RESULTS: Among adolescents with atopy with serum IgE levels of >30 kIU/L or aeroallergen-specific IgE, the odds ratios (ORs) for asthma symptoms and for ever or current asthma increased with the lifetime number of hours spent in chlorinated pools, reaching values of 7.1 to 14.9 when chlorinated pool attendance exceeded 1000 hours. Adolescents with atopy with chlorinated pool attendance of >100 hours had greater risk of hay fever (OR: 3.3-6.6), and those with attendance of >1000 hours had greater risk of allergic rhinitis (OR: 2.2-3.5). Such associations were not found among adolescents without atopy or with copper-silver pool attendance. The population attributable risks for chlorinated pool-related ever-diagnosed asthma, hay fever, and allergic rhinitis were 63.4%, 62.1%, and 35.0%, respectively.
CONCLUSION: Chlorinated pool exposure exerts an adjuvant effect on atopy that seems to contribute significantly to the burden of asthma and respiratory allergies among adolescents.
Swimming pools commonly are disinfected through water chlorination with hypochlorite, chlorine gas, or chloroisocyanurates. These chlorine-based disinfectants, loosely referred to as chlorine, release in water hypochlorous acid, a nonselective biocide that oxidizes all forms of organic matter in pool water, which has advantages but also some disadvantages. Because of its strong oxidizing potential, chlorine can inactivate a wide spectrum of waterborne pathogens, but it also reacts with organs of swimmers in contact with pool water or air, causing irritation of the skin, eyes, and upper respiratory tract. In addition, when oxidizing organic matter from swimmers or other sources, chlorine releases a mixture of harmful byproducts, including irritants such as chloramines and haloacetic acids.1–4
Regulatory bodies and health authorities long have regarded these irritating effects of pool chlorine as a mere source of discomfort for swimmers, arguing that the dangers of chlorine, if any, must be weighed against the risks of inadequate disinfection and the health benefits of swimming.1, 5 This way of reasoning, which has dominated swimming pool management for several decades, is being increasingly challenged by reports of health problems among swimmers.4 For several years, it has been known that elite swimmers have a higher prevalence of respiratory symptoms, asthma, and airway inflammation than do other athletes.4 It was assumed that this poorer respiratory health of swimmers was the consequence of a selection bias attributable to the lower asthmagenicity of indoor swimming, compared with other sports. Researchers increasingly acknowledge that these respiratory problems may be attributable, at least in part, to chlorine used to disinfect pool water.6–8 Public concern about the dangers of pool chlorine, however, was particularly aroused when it was found that indoor chlorinated pools may be detrimental to the airways of children, causing epithelial damage and increasing asthma risk.9–12 Studies by other investigators confirmed these respiratory effects of pool chlorine13–15 and provided additional evidence that chlorinated pools may contribute to the development of allergic diseases.16
Initially, the respiratory problems of swimmers were attributed to the irritating effects of trichloramine, the gas that gives indoor pools their typical smell and can cause asthma in lifeguards.17,18 However, the recent finding that asthma risk is increased similarly with attendance at outdoor pools demonstrates that trichloramine cannot be the main cause of respiratory effects in swimmers, because this highly volatile gas is quickly dispersed into the atmosphere when it is released outdoors.19 Substances causing asthma and breathing difficulties in swimmers must be sought among the chlorination products present in pool water or floating at the surface of the pool as aerosols or vapors. If this reasoning is correct, then it means that the respiratory impact of chlorinated pools can be assessed correctly only by taking into account total exposure to chlorinated pools, regardless of the type of pool and the conditions of attendance.
The aim of the present study was to assess for the first time the overall impact of chlorinated pool exposure on the respiratory health of adolescents, by considering the total time spent in indoor or outdoor chlorinated pools. The study took advantage of the existence in Belgium of copper-silver pools, which enabled us to identify a reference population of swimmers with no or minimal exposure to chlorination products.
The ethics committee of the Faculty of Medicine of the Catholic University of Louvain approved the study protocol. We recruited adolescents in 3 secondary schools in the southern part of Belgium, in the cities of Louvain-la-Neuve, Bastogne, and Lessines. Participation rates were similar among the 3 schools, as well as between girls and boys (between 70.6% and 72.1%).
Students in Louvain-la-Neuve had access to an indoor pool sanitized through the copper-silver method, whereas students at the other 2 schools could visit only indoor pools disinfected with chlorine. According to the Belgian legislation, each swimming pool is required to check the microbial and chemical qualities of water regularly by measuring several parameters, including active (0.5–1.5 ppm) and combined (<2 ppm) chlorine. In 2003, the legislation was enforced through a lowering of the standard for combined chlorine (<0.8 ppm) and the setting of a standard for trichloramine levels in pool air (<500 μg/m3 in air sampled 1.5 m above the pool surface). The concentrations of trichloramine in air ranged from 300 to 500 μg/m3. There were occasional exceedances of active or combined chlorine levels but without attaining levels that might pose a risk to swimmers, according to international guidelines (concentrations of active and combined chlorine never exceeded 4 ppm). The water of the copper-silver pool was sanitized with concentrations of copper (0.6–1.2 mg/L) and silver (2–10 μg/L) that were lower than drinking water guidelines.20
The protocol for examining students was described in detail elsewhere.19 Briefly, parents completed a questionnaire inquiring about the health of their child and risk factors for asthma and allergic diseases. The questions about respiratory symptoms and allergic diseases were those of the International Study of Asthma and Allergy in Childhood.21 The questionnaire also included questions intended to estimate the total time the child had spent in indoor or outdoor chlorinated pools. Students were asked not to visit a chlorinated pool during the 48 hours preceding the study. The examination of students, which was performed in schools, included measurements of height and body weight, an interview with the adolescent about respiratory symptoms, collection of a blood sample, and screening for exercise-induced bronchoconstriction (EIB). The EIB test consisted of measuring the decrease in forced expiratory volume in 1 second (FEV1) after 6 minutes of indoor running with submaximal effort, and results were considered positive when the exercise caused a decrease in FEV1 of ≥10%.22 Asthma medication use was not discontinued before the test. Asthma was defined either as “ever asthma,” corresponding to asthma diagnosed at any time by a physician, or as “current asthma,” corresponding to physician-diagnosed asthma that, at the time of the study, was being treated with medication (bronchodilators and/or inhaled corticosteroids) and/or was associated with positive EIB test results. Because the examination of adolescents in schools precluded any allergic provocation test, we screened for allergies by measuring total and aeroallergen-specific immunoglobulin E (IgE) concentrations in serum, using the Immulite IgE kit (Diagnostic Products, Los Angeles, CA). Sensitization against specific aeroallergens was defined as serum concentrations of specific IgE of >0.35 kIU/L.
We assessed associations between outcomes and cumulative chlorinated pool attendance (CPA) stratified into 4 categories, that is, <100 hours, 100 to 500 hours, 500 to 1000 hours, or >1000 hours. Adjusted odds ratios (ORs) for the outcomes in these categories were calculated with backward logistic regression models, using as the reference level the occurrence of the outcome among adolescents with CPA of <100 hours. Backward selection started with a model including all potential control variables and each step was performed by deleting the least-significant predictor, until the model contained only variables with P < .20. We tested a total of 26 potential predictors, including CPA, gender, total and aeroallergen-specific IgE levels, parental asthma or allergy, and maternal smoking during pregnancy. Population attributable risks (PARs) were calculated by using the formula P(OR − 1)/[P(OR − 1) + 1], where P is the prevalence of the exposure and OR is the adjusted OR attributable to the exposure. The level of statistical significance was set at P < .05.
Table 1 shows the characteristics of participants. The 2 genders were similarly represented in the 3 schools except for the school in Bastogne, which included more girls. There were no or little differences between the 3 schools with respect to age (15 years, on average), ethnicity, and indicators of respiratory health except for the prevalence of hay fever and FEV1 values, which were higher in Bastogne and Lessines, respectively. Students in Louvain-la-Neuve had higher socioeconomic status than their peers, as reflected by parental education levels and several lifestyle factors, such as breastfeeding, exposure to tobacco smoke, and access to a backyard pool. Because they had access to an indoor copper-silver pool, students in Louvain- la-Neuve had much lower CPA levels than did those in Bastogne and Lessines. Among them, 118 had a lifetime CPA value of <100 hours. Those students were selected to constitute the reference group.
We first assessed associations between chlorinated pools and outcomes through stratification of data into categories of increasing CPA (Table 2). The rate of sensitization to major aeroallergens did not vary with CPA, whereas the total serum IgE concentrations showed, if anything, a tendency to decrease. There also was little variation in FEV1 values, which showed only a very modest increase (2%, on average) between the lowest and highest CPA categories. Prevalences of wheezing and EIB, although increased in all groups with CPA values of >100 hours, did not show any significant exposure-related trend. In contrast, the prevalences and odds of ever asthma, current asthma, cough, and shortness of breath increased almost linearly with the time spent in chlorinated pools. These exposure-related increases persisted when students in Bastogne and Lessines, who visited only chlorinated pools, and those in Louvain-la-Neuve, who also had access to the copper-silver pool, were examined separately (eg, P values for trend were .02 and .07 for ever asthma and .02 and .04 for current asthma, respectively).
For cough and shortness of breath, these associations even persisted when adolescents with a diagnosis of asthma were excluded (P for trend of .004 and .05, respectively). The risk of hay fever was increased in all groups with CPA values of >100 hours, whereas the risk of allergic rhinitis was increased only in the group with the highest CPA value (>1000 hours).
Risks of respiratory symptoms (Table 3) and asthma (Table 4) associated with CPA were strongly influenced by atopic status. CPA increased the risks of wheezing, cough, shortness of breath, ever asthma, and current asthma only among adolescents with higher total serum IgE levels and had no influence on these outcomes among the other adolescents. For the risks of ever or current asthma, the same patterns of interactions between CPA and atopy, defined as sensitization to any aeroallergen, emerged. An interaction with the risk of EIB also emerged and was significantly increased only among sensitized adolescents. For respiratory symptoms, however, the interaction between CPA and aeroallergen sensitization was less clear cut, with CPA increasing the risk of cough for adolescents without and with atopy and the risk of shortness of breath only for adolescents without atopy (Table 4).
CPA also interacted with aeroallergen sensitization, and specifically pollen and dust mite sensitization, to increase the risks of hay fever and allergic rhinitis (Table 5). The exposure-response relationships for hay fever and allergic rhinitis were noticeably different, and they also were different from the relationships observed for asthma. Although the odds for allergic rhinitis were increased only among sensitized adolescents with the highest CPA values (>1000 hours), the odds for hay fever were increased significantly among sensitized adolescents with CPA values of >100 hours and above this threshold tended to plateau. This nonlinear relationship suggests an early increase of hay fever risk toward a plateau that seems to be reached when CPA exceeds 500 hours. To test this hypothesis, we further assessed the dose-response relationships by stratifying data for adolescents with CPA values of <500 hours. As shown in Fig 1, the prevalence of hay fever among these adolescents increased linearly with CPA, whether all subjects were considered or boys and girls were considered separately, and even when only adolescents without parental hay fever were considered. Quite remarkably, this early increase was found only among subjects who were sensitized to aeroallergens or pollen.
The PARs for atopic diseases associated with CPA were calculated by considering as exposed the students with atopy who had spent >100 hours in chlorinated swimming pools. When atopy was defined on the basis of total serum IgE levels, these calculations yielded PARs of 63.4% for ever asthma, 79.2% for current asthma, 62.1% for hay fever, and 35.0% for allergic rhinitis. We obtained similar PAR estimates when atopy was defined as sensitization to any aeroallergen (ever asthma: 46.2%; current asthma: 67.3%; hay fever: 49.8%; allergic rhinitis: 29.6%). By comparison, the PARs for ever and current asthma attributable to maternal smoking during pregnancy, the only other lifestyle risk factor remaining in the model with P values of <.20 (P = .09 and P = .11, respectively), were 8.3% and 10.1%, respectively.
Our findings show that CPA during childhood interacts with atopic status to increase the risk of asthma, hay fever, and allergic rhinitis. Although one could evoke the possibility of reverse causation to explain the associations between asthma and indoor pool attendance on the basis that indoor swimming is recommended frequently for individuals with asthma, this explanation does not hold for associations with hay fever and allergic rhinitis or for associations with respiratory symptoms (cough and shortness of breath) observed in the absence of a diagnosis of asthma. The hypothesis of reverse causation seems even more unlikely because it implies that only individuals with atopy would be encouraged to swim, a possibility refuted by the fact that the proportion of individuals with atopy showed a tendency to decrease with lifetime pool attendance. These associations cannot be ascribed to swimming itself, because none of the studied outcomes was influenced by attendance at the copper-silver pool. The only plausible explanation is that the chlorine-based oxidants in water or air floating at the pool surface cause some airway changes and promote the development of allergic diseases.
The present study confirms the pool chlorine-atopy interaction in asthma development that we found previously among schoolchildren who attended indoor chlorinated pools.11 Although they were based on different populations of swimmers, 2 Scandinavian studies reported observations that also suggest the existence of interactive effects of atopy and exposure to chlorinated pools. Among competitive swimmers, Helenius et al6 found that asthma risk was >10 times greater among elite swimmers who had atopy than among those who did not. Investigating the effects of infant swimming on the respiratory health of children, Nystad et al23 reported that infant swimming increased the risk of wheezing among children whose parents had atopy but not among those whose parents did not. Because children of parents with atopy are more likely to have atopy themselves, this study points indirectly to an interaction between atopic status and CPA in the development of childhood asthma.
Probably the most important finding of our study is that the pool chlorine-atopy interaction described initially for asthma may extend to other common allergic diseases, such as hay fever and allergic rhinitis. Exposure-response relationships seemed to differ according to the type of respiratory allergy, which is not surprising, given the variable deposition of inhalants along the respiratory tract. In particular, the interaction between chlorine and atopy in the risk of hay fever was triggered by much lower CPA levels, compared with asthma and allergic rhinitis. These differences in exposure-response relationships, as well as probably some differences in chlorine levels in swimming pools, might explain some conflicting results from other studies. In a retrospective analysis of data on medical history and swimming pool attendance of a cohort of adults in Germany, Kohlhammer et al16 found that early school pool attendance was associated with increased risk of hay fever but no association with asthma emerged, in contrast to our findings. We think that the explanation for this discrepancy might lie in the fact that the German cohort was composed of adults who, during their childhood, had been much less exposed to chlorinated pools than are present-day children. It is possible that, when they were children, these adults had attended chlorinated pools enough to exceed the CPA threshold for inducing hay fever but not enough to attain the CPA threshold for inducing asthma. More recently, the same German team further explored the relationship between swimming during infancy and the development of allergies by analyzing 6-year follow-up data for a prospective birth cohort study.24 The authors could not detect clear associations between swimming and the development of allergic diseases. The authors explained the findings on the basis of the fact that the German chlorine standards at the time those children attended pools had already been decreased to levels that were much lower (by factors of 2 and 10, respectively) than the standards in effect in the former German study24 and our studies.10–12 Another possible explanation would be that the population studied by Schoefer et al24 was still too young for detection of associations with asthma and other atopic diseases, conditions that usually are diagnosed correctly later in childhood.25
Disruption of epithelial barriers increasingly seems to be a basic mechanism in allergic sensitization.26 Most potent allergens, such as dust mites, cat dander, and pollen, display a proteolytic activity that allows then to open tight junctions, to cross epithelial barriers more easily, and from there to interact with immune cells.27–29 Chlorination products such as hypochlorous acid and chloramines are membrane-permeant oxidants that also can breach tight junctions and can facilitate the transepithelial delivery of allergens. These chemicals might thus promote allergic diseases through a mechanism similar to allergens displaying proteolytic activity. Because there is no reason to think that chlorine-based oxidants would react differently with the epithelia of the upper and lower airways, we think that differences in exposure-response relationships between hay fever and asthma might reflect primarily differences in the doses of chlorination products deposited along the respiratory tract. If the risk of hay fever increases significantly with much lower CPA levels than asthma, then it might be simply because the upper airways receive most of the burden of chlorine that swimmers inhale actively at the surface of the pool.30
Our study shows that CPA exerts a strong adjuvant effect on the development of asthma, hay fever, and allergic rhinitis. These findings reinforce the need to pursue research in this area and to enforce regulations concerning the levels of these chemicals in water and air of swimming pools.
This work was supported by the National Fund for Scientific Research in Belgium, the Agency for Environmental and Occupational Health Safety in France, the governments of the Walloon Region and the French Community of Belgium, and the European Union (project INTARESE; coordinator: David Briggs).
- Accepted May 28, 2009.
- Address correspondence to Alfred Bernard, PhD, Department of Public Health, Catholic University of Louvain, Avenue E. Mounier 53.02, B-1200 Brussels, Belgium. E-mail:
Financial Disclosure: The authors have indicated they have no financial relationships relevant to this article to disclose.
What's Known on This Subject:
Outdoor or indoor swimming pools can increase asthma risks, but their overall influence on allergic diseases has not been evaluated.
What This Study Adds:
This study shows that attendance at chlorinated swimming pools exerts a strong adjuvant effect that contributes significantly to the burden of asthma, hay fever, and allergic rhinitis during adolescence.
- ↵World Health Organization. Guidelines for Safe Recreational Waters, Vol 2: Swimming Pools and Similar Recreational-Water Environments. Geneva, Switzerland: World Health Organization; 2006
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- ↵Helenius I, Rytilä P, Sarna S, et al. Effect of continuing or finishing high-level sports on airway inflammation, bronchial hyperresponsiveness, and asthma: a 5-year prospective follow-up study of 42 highly trained swimmers. J Allergy Clin Immunol.2002;109 (6):962– 968
- ↵Bernard A, Carbonnelle S, Michel O, et al. Lung hyperpermeability and asthma prevalence in schoolchildren: unexpected associations with the attendance of indoor chlorinated pools. Occup Environ Med.2003;60 (6):385– 394
- ↵Bernard A, Carbonnelle S, Dumont X, Nickmilder M, Nickmilder M. Infant swimming, pulmonary epithelium integrity and the risk of allergic and respiratory diseases later in childhood. Pediatrics.2007;119 (6):1095– 1103
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- ↵Jacobs JH, Spaan S, van Rooy GB, et al. Exposure to trichloramine and respiratory symptoms in indoor swimming pool workers. Eur Respir J.2007;29 (4):690– 698
- ↵Bernard A, Nickmilder M, Voisin C. Outdoor swimming pools and the risks of asthma and allergies during adolescence. Eur Respir J.2008;32 (4):979– 988
- ↵World Health Organization. Guidelines for Drinking-Water Quality, Vol 2: Health Criteria and Supporting Information. 2nd ed. Geneva, Switzerland: World Health Organization; 1996
- ↵Dickinson JW, Whyte GP, McConnell AK, Nevill AM, Harries MG. Mid-expiratory flow versus FEV1 measurements in the diagnosis of exercise induced asthma in elite athletes. Thorax.2006;61 (2):111– 121
- Copyright © 2009 by the American Academy of Pediatrics