Infant swimming in chlorinated pools and the risks of bronchiolitis, asthma and allergy

Bronchiolitis is an acute infection of the small airways that primarily affects young infants, most often those aged 2–24 months. The main causative agent is respiratory syncytial virus (RSV), although other viruses may sometimes be involved. The disease occurs with a seasonal pattern, peaking during winter in temperate climates and the rainy season in tropical climates 1, 2. The disease burden of bronchiolitis is substantial and seems to have increased in most developed countries since the 1960s–1970s 3. In the USA and Europe, the annual incidence of bronchiolitis during the first year of life is estimated to be 10–20%, but incidences as high as 30% have been reported in some urban areas 3, 4. Since bronchiolitis increases the risk of childhood asthma 5, 6, it also contributes to the rising incidence of chronic respiratory diseases in children.

Factors that may increase the frequency or severity of bronchiolitis are male sex, low gestational age, young or unmarried mothers, infant condition at birth (Apgar score), lack of breastfeeding, early weaning, congenital heart or lung diseases, and a family history of atopic diseases. The risk of bronchiolitis is also higher for infants living with older siblings, attending a day-care centre or exposed to environmental tobacco smoke 2, 7. Since ambient air pollution appears to play, if any, a marginal role 8, factors driving the rise of the disease in industrialised countries remain largely unknown.

Infant swimming is a practice that has been greatly popularised in most industrialised countries. Nystad and co-workers 9, 10 were among the first to draw attention to the risks that this practice may pose to the airways of infants. These authors noted that infants of atopic parents were more likely to develop wheezing or lower respiratory tract infections when they were attending swimming pools. In a cross-sectional study of schoolchildren aged 10–13 yrs, it was also found that infant swimmers were more likely to develop asthma and recurrent bronchitis than their peers who had never attended a chlorinated pool before the age of 2 yrs 11, 12. Interestingly, this poorer respiratory health of infant swimmers was associated with lower serum levels of Clara cell protein (CC16), a protein protecting from inflammation in acute RSV infection 13. These findings led to the postulate that the chlorine used to disinfect swimming pools can cause airway changes making the lungs more sensitive to infection- and asthma-inducing agents 12. A Swedish study also described decreased levels of serum CC16 in children who swam during infancy compared to those who did not 14, providing further evidence that terminal airways and, in particular, Clara cells may be damaged during infant swimming.

Given these associations between infant swimming, serum CC16 and RSV infection, it was hypothesised that the infant swimming practice should be associated with a higher risk of bronchiolitis. In order to test this hypothesis, the associations between infant swimming, bronchiolitis and its sequelae were explored in a cross-sectional study focused on young schoolchildren. Since both outdoor and indoor pools may affect the airways of swimmers 15, the present study was not limited to baby swimming lessons in indoor pools, but considered all kinds of swimming activity during infancy, regardless of the type of chlorinated pool and the conditions of attendance.

RESULTS

Table 1 compares the characteristics of infant swimmers in indoor or outdoor chlorinated pools (n = 195) and children who never swam before the age of 2 yrs (n = 235). On average, infant swimmers had spent 6 h in indoor and 8 h in outdoor chlorinated pools before the age of 2 yrs. These infant swimmers also showed a greater lifetime CPA at indoor or outdoor chlorinated swimming pools (total indoor and outdoor CPA 132 versus 35 h in other children) (table 1). There were no significant differences between the two groups regarding most risk factors of respiratory disease, including sex, age, body mass index, birthweight, exposure to tobacco smoke and parental allergies. The social class or socioeconomic status, as evaluated on the basis of parental education, and the proportions of children with parental asthma, who had been breastfed or attended a day-care centre were higher in the group of swimmers than in non-swimmers. The two groups did not differ with respect to the prevalences of wheezing and ever-diagnosed asthma, respiratory allergies, bronchitis, sinusitis and pneumonia. The prevalence of bronchiolitis was, however, significantly greater in infant swimmers than in their controls (36.4 versus 23.8%; p = 0.004).

The logistic regression analysis confirmed the association between infant swimming and the risk of bronchiolitis (OR 1.68; 95% CI 1.08–2.68; p = 0.03). Other risk factors of bronchiolitis identified included male sex (OR 1.65; 95% CI 1.05–2.59; p = 0.03), parental asthma and/or respiratory allergies (OR 1.73; 95% CI 1.20–2.74; p = 0.02), number of older siblings (OR 1.69; 95% CI 1.07–2.67; p = 0.02), maternal smoking during pregnancy (OR 1.80; 95% CI 1.01–3.37; p = 0.05) and day-care centre attendance (OR 1.87; 95% CI 1.17–3.00; p = 0.009). Breastfeeding, by contrast, was associated with a protective effect towards bronchiolitis (OR 0.58; 95% CI 0.34–0.97; p = 0.04). The parental educational level, a surrogate of socioeconomic status, the use of bleach for house cleaning or parental smoking at home did not emerge as significant predictors of bronchiolitis (p>0.20 for all).

The analysis was pursued by examining whether or not the risk of bronchiolitis was different when attending indoor or outdoor chlorinated pools. As shown in table 2, the OR for bronchiolitis increased dose-dependently with CPA at both types of swimming pool considered separately (p-value for trend <0.05 for both). Stratification of infant swimmers into tertiles of CPA at indoor or outdoor chlorinated pools led to similar patterns of significant increases (p-value for trend 0.009 for indoor and 0.03 for outdoor pools; data not shown). The same pattern of exposure-related increases was found when the analysis was based on children attending only indoor or only outdoor pools to the exclusion of the other type of pool.

It was also ascertained that these associations were not confounded by differences in participation rate between schools or by other risk factors for bronchiolitis, especially those linked to the socioeconomic status of the children, which, indeed, was higher in infant swimmers than in controls. This analysis was conducted by combining the CPA at indoor and outdoor pools in order to obtain sufficient subjects in the different pool attendance categories. As shown in table 3, associations between bronchiolitis and infant swimming persisted, and were very consistent (OR for CPA of >20 h was 2.2–2.7, p≤0.03) across categories created by excluding children from schools with a low participation rate (<50%), children from parents with a lower educational level, children who had not been breastfed, children who had been exposed to tobacco smoke or else who had lived with older siblings or in a house cleaned with bleach. Quite interestingly, exclusion of children of parents with asthma or respiratory allergies, or of children having attended a day-care centre, two well-known risk factors for bronchiolitis, noticeably strengthened the associations between bronchiolitis and infant swimming (OR for CPA of >20 h 4.45 and 4.44; p = 0.001 and 0.007, respectively), which emerged through a particularly remarkable dose–response relationship among children who had never attended a day-care centre (p<0.001).

Lastly, the temporal coherence of these associations was checked by comparing the age of bronchiolitis occurrence with the age at which the child started to attend swimming pools. Of the 71 infant swimmers who had bronchiolitis, there were 54 cases for which the parents provided the exact dates when their child started swimming and developed bronchiolitis. On average, these infant swimmers developed bronchiolitis at the age of 9.6±5.9 months and were diagnosed with asthma at the age of 21.8±18.6 months. Among these, bronchiolitis occurred after the start of infant swimming in 35 (65%) cases, a number consistent with the excess of bronchiolitis cases observed in the infant swimming group. Children who never swam during infancy had bronchiolitis at about the same age as infant swimmers (9.3±5.5 months), but were diagnosed with asthma later, at the age 30.6±10.0 months.

Since bronchiolitis is known to increase the risk of wheezing, asthma or allergic sensitisation in subsequent years, the late consequences of bronchiolitis were also compared between infant swimmers and nonswimmers. This comparison was made by adjusting the ORs for CPA at indoor or outdoor pools after the age of 2 yrs, which, indeed, was very different between the two groups. Table 4 clearly shows that bronchiolitis was associated with an increased risk of wheezing, doctor-diagnosed asthma and hay fever only among children who had attended chlorinated pools during their infancy. Interestingly, bronchiolitis and infant swimming also interacted to increase the risk of sensitisation to house dust mite (p = 0.04) and pollen (p = 0.05). There were no differences in the ORs for cat allergy and allergic rhinitis between the two groups. When considering children who never developed bronchiolitis, there were no significant differences in the prevalences of respiratory diseases and sensitisation to aeroallergens between children who swam during infancy and those who did not (p>0.07 for all; Chi-squared test) (table 4).

DISCUSSION

The present study shows that swimming in indoor and outdoor pools during infancy is associated with an exposure-related increase in the risk of bronchiolitis. This effect is independent of other known risk factors for bronchiolitis, such as day-care attendance, exposure to tobacco smoke or parental antecedents of atopic diseases. The present study also shows that, among children who had bronchiolitis, only those who were infant swimmers were at greater risk of asthma and respiratory allergies in subsequent years.

These results are in concordance with the observation of Nystad and co-workers 9, 10 that swimming before the age of 2 yrs increases the prevalence of lower respiratory tract infection. They are also consistent with a prior study on schoolchildren 11, 12, suggesting that infant swimming may cause airway changes predisposing to asthma and recurrent bronchitis. In the present study focusing on younger children, no significant differences were found between infant swimmers and other children regarding the risk of asthma and allergies. This lack of association between infant swimming and asthma, reported by other authors for children of the same age 18–20, does not necessarily argue against the hypothesis of a causal link between infant swimming and poorer respiratory health later during childhood. Children aged 5–6 yrs are probably too young to detect associations with chronic respiratory diseases that develop and are correctly diagnosed later during childhood. This might explain why studies linking swimming pool attendance to childhood asthma were all based on children with a mean age of >9 yrs 21–23. The follow-up of the present cohort of infant swimmers should provide more conclusive data regarding the long-term consequences of infant swimming.

The swimming pool factor responsible for the risk of bronchiolitis is hard to identify with certainty given the multiplicity of potentially harmful agents in the swimming pool environment 20, 24. Currently, one of the most plausible explanations is that the airways of infant swimmers are made more sensitive to infections because of the irritating effects of the chlorine used to disinfect swimming pools. The fact that bronchiolitis is increased by outdoor, as well as by indoor, pools means that chloramines are not the sole and probably not the main irritants that might be implicated in the risk of bronchiolitis. The first reason for this is that the outdoor pools attended by infant swimmers in the present study were mainly residential pools. Compared to public pools, residential pools are, indeed, much less polluted by organic matter from bathers, in particular by urine, which is the main source of nitrogen leading to the formation of chloramines. The second reason is that trichloramine, the ultimate chlorination by-product, is a highly volatile gas that is very quickly dispersed into the atmosphere once released at the surface of open-air pools, which, therefore, do not have the characteristic chlorine smell of indoor pools. As for the risks of asthma and respiratory allergies associated with outdoor pools 15, we suspect that the major burden of oxidants irritating the airways of infant swimmers comes from the microaerosols or small volumes of water that they inhale while actively playing and having their head under water 12. The risk of inhaling small volumes during submersion exercise is especially important since infants cannot control their breathing. If the infant swimming practice is considered to be safe, it is because of the laryngeal or gag reflex (closure of the larynx with the epiglottis) that is triggered when water gets into the infant’s mouth. This gag reflex disappears, however, when the infant gets older (>6 months), and, anyway, this reflex cannot prevent small amounts of chlorinated water deposited or trapped in the upper respiratory tract being conducted more deeply into the lungs when the infant surfaces to breathe 12.

The most reactive and concentrated chlorine compound present in the water and microaerosols of both outdoor and indoor pools is hypochlorite/hypochlorous acid, i.e. the active chlorine itself (concentrations ranging 1–2 ppm). Depending on the level of organic pollution of pool water, infant swimmers have also been exposed to chlorination by-products, among which the most irritating and concentrated are mono-, dichlor- and trichloramine, as well as dichloromethylamine 19, 20, 24, 25. Since public pools are usually more polluted by nitrogenous substances from bathers (urine, sweat and saliva) than residential pools, irritating effects caused by the chloramines might explain why the ORs for bronchiolitis are higher with indoor than with outdoor pools.

Chlorine-based oxidants, such as hypochlorous acid or chloramines, are known to be potent oxidants capable of damaging the endothelial and epithelial barriers 26, 27. Studies based on lung injury markers have shown that, at concentrations commonly found in indoor pools, these chemicals can affect the permeability or the cellular integrity of the deep lung epithelium. Regular attendance at chlorinated pools by schoolchildren has been associated with an exposure-dependent increase in lung epithelium permeability (lung hyperpermeability), resulting in intravascular leakage of surfactant-associated proteins A and B 28. A decrease in serum CC16 has also been described in children who use indoor pools during their infancy or later in childhood, which is a reflection of a decrease in Clara cell numbers and an ensuing decrease in CC16 production 11, 12, 14. The latter observation is particularly relevant to the present study given the experimental evidence that CC16 downregulates inflammation during acute RSV infection 13.

Even though airways irritation by chlorine-based oxidants appears to be a very likely explanation for the increased risk of bronchiolitis associated with infant swimming, other causative factors might also play a role. As a result of inadequate disinfection with chlorine, the swimming pool environment can be contaminated by viruses (adeno-, noro- and echovirus), which may cause outbreaks of water-borne illnesses, such as gastroenteritis, dermatitis and respiratory infections 29. Respiratory illnesses in these incidents are rather uncommon, and, in most cases, limited to the upper airways. Nevertheless, we have no evidence permitting us to exclude the possibility that the swimming pool environment may increase the risks of cross-infection with RSV 30, 31. Another possibility that should be considered is the inhalation of swimming pool water when infants perform submersion activities. Owing to its hypotonicity, swimming pool water deposited in airways might, perhaps, cause some airway alterations, aggravating the toxic effects of chlorination products 32.

The present study has certain limitations. The most important one concerns exposure assessment, since it was obviously not possible to retrieve exposure data regarding the levels of chlorine in the indoor or outdoor swimming pools that the children attended during infancy. There was no choice but to use the information provided by the parents. The existence of exposure–response relationships for both outdoor and indoor pools suggests that the lack of data regarding the precise levels of chlorine in swimming pools has not been critical to the point of distorting the present analysis. Another limitation concerns the participation rate, which only reached 51% overall and varied greatly between schools. The young age of the children combined with the fact that the medical examination, though based on noninvasive tests, was performed in schools probably deterred a significant proportion of parents from participating in the study. This low participation rate does not seem to have biased the study since there were no significant correlations between participation rate and the prevalences of the main outcomes and risk factors. The response rate, tested along with other potential confounders, did not emerge as a significant predictor of bronchiolitis either. This lack of confounding by the participation rate probably stems from the fact that parents were blinded to the tested hypothesis. Since the study was conducted in the framework of a prospective study on environmental factors affecting the respiratory health of children, infant swimming was only one of the many items addressed by the questionnaire.

In summary, the present study shows that infant swimming is associated with a dose-dependent increase in the risk of bronchiolitis. Exposure to chlorinated pools during infancy also interacts with bronchiolitis to increase the risks of asthma and respiratory allergies later during childhood, which suggests that the infant swimming practice may have a more long-standing impact on the respiratory health of children.