Chlorinated Pools and the Risk of Asthma

Referencing: Chlorinated Pool Attendance, Atopy, and the Risk of Asthma during Childhood

In a recent article, Bernard et al. (2006) presented data that led them to conclude that the use of chlorinated pools, especially by young children, interacts with atopic status to promote the development of childhood asthma. I question these conclusions for several reasons.

First, this finding is not consistent with the authors' recent publication from this same group of children (Nickmilder et al. 2005) concluding that children living in a home cleaned with chlorine bleach had a lower prevalence of asthma. It is difficult to understand how occasional exposure to chlorinated compounds at indoor swimming pools could cause asthma if more frequent and longer exposures at home were actually protective.

Second, the data presented by Bernard et al. (2006) do not fully support their conclusion. For example, the exposure metric they used to describe the children's exposure to chlorinated pools is the lifetime cumulative swimming pool attendance (CPA) given in hours. The CPA data are based on lifetime exposure derived from questionnaires that the parents of these 11- to 12-year-old children completed at home [American Thoracic Society, European Respiratory Society (ATS/ERS) 2005] and is thus subject to their understanding and interpreting the question, as well as to recall bias. In addition, systematic bias is introduced by using a lifetime cumulative measure like CPA to relate exposure to asthma prevalence. Lifetime cumulative exposure is obviously dependent on the age of the child; because asthma prevalence also increases during this same time, the child's age becomes a confounder that cannot be dealt with adequately in the analysis used by Bernard et al. (2006).

Third, the data presented to relate the dose response between CPA and asthma prevalence are confusing. In Table 2 of Bernard et al. (2006), the relationship is not significant, while in Figure 1 it is significant in a subgroup. In their Figure 1A, a dose response is suggested between CPA and the prevalence of doctor-diagnosed and total asthma, but only in those children whose total IgE is > 100 IU/mL. The subgroups in this figure are small; from data in Table 1 and the text, it appears that only 14 children had both IgE > 100 IU/mL and doctor-diagnosed asthma, and only 20 had total asthma with a high IgE concentration. Because Figure 1 (Bernard et al. 2006) divides all 341 children into approximately equal quartiles of CPA, it seems impossible to allocate the 14–20 children with asthma in such a way that would result in an asthma prevalence of 12–35% within each quartile. I suggest that the figure is drawn incorrectly and that the correct relationship is shown in their Table 2.

Fourth, insufficient information is available to address the uncertainties in the outcome measures of Bernard et al. (2006). The data in their Table 2 demonstrate that swimming pool attendance was associated with the prevalence of an elevated exhaled nitric oxide (eNO); neither doctor-diagnosed asthma nor total asthma was significantly related to swimming pool attendance unless combined with eNO measures. Although eNO is associated with asthma, it has been used primarily to measure the state of airway inflammation in asthma; the use of eNO is less certain as a diagnostic tool (ATS/ERS 2005). In fact, elevated eNO levels have been associated with viral respiratory tract infections, allergic rhinitis, and sinusitis (ATS/ERS 2005). These conditions were not included in the health questionnaire described by Bernard et al. (2006) in their "Materials and Methods." Indeed, only 20 of the 29 children with an elevated eNO (> 30 ppb) had doctor-diagnosed asthma. In addition, the study was conducted during winter months when viral respiratory infections are common; therefore, the presence of these infections could have produced outcome misclassification. Finally, inhaled steroid medications markedly reduce eNO, and use by these children could have introduced yet another reason for outcome misclassification.

To summarize, the uncertainty in both the exposure estimates and the outcome measures, coupled with the conflicting outcomes with home exposure to chlorine bleach, make it difficult to accept the strong conclusions reached by Bernard et al. (2006) in their article.

The author received an honorarium when attending a workshop sponsored by the Chlorine Chemistry Council.

References

ATS/ERS (American Thoracic Society, European Respiratory Society). 2005. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med 171: 912–930.

Bernard A, Carbonnelle S, de Burbure C, Michel O, Nickmilder M. 2006. Chlorinated pool attendance, atopy, and the risk of asthma during childhood. Environ Health Perspect 114:1567–1573.

Nickmilder M, Carbonnelle S, Bernard A. 2006. House cleaning with chlorine bleach and the risks of allergic and respiratory diseases in children. Pediatr Allergy Immunol 18:27–35.

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Chlorinated Pools: Bernard et al. Respond

We are pleased to respond to Eggleston because this offers us the opportunity to respond to some of the criticisms that have been formulated since we originally proposed the pool chlorine hypothesis (Bernard et al. 2003).

First, the divergent effects of chlorine [described in our recent study (Bernard et al. 2006)]—when this chemical is used to clean surfaces or to sanitize recreational water—are not inconsistent. Chlorine is a nonspecific biocide, and there are clearly situations in which the beneficial effects of this agent need to be balanced against its possible adverse effects. As we explained in the "Discussion" of our recent articles (Bernard et al. 2006; Nickmilder et al. 2007), exposure conditions are radically different when children live in a house cleaned with bleach compared with when they attend an indoor chlorinated pool. When a house is cleaned with bleach, children are not likely to be exposed to high concentrations of chlorine gas or trichloramine because they are not directly involved in the cleaning tasks. In that situation, the balance for children—but not necessarily for people doing the cleaning—is clearly in favor of the beneficial effects of chlorine from a decreased risk of asthma and respiratory allergy (Bernard et al. 2006; Martyny et al. 2005; Nickmilder et al. 2007). In contrast, when attending an indoor pool, children are directly in contact with the chlorination products that they actively inhale as gases, aerosols, or even water. It can be argued that the time children spend in a swimming pool is limited, but we should not forget that chlorine-based chemicals are rapidly acting oxidants, a property essential to their efficacy.

Eggleston raises the issue of a possible confounding between age and lifetime cumulative pool attendance (CPA). However, because our study (Bernard et al. 2006) focused on children in 5th and 6th grades, there is little variation in age (range 10–13 years), explaining why age did not emerge as a predictor of the outcomes (Table 1) and also why it did not vary across CPA categories (analysis of variance, p = 0.35). Eggleston states that cases of asthma cannot be allocated to the CPA categories of our Figure 1, but this is because he has misinterpreted the way these categories were constructed. Subjects were not divided into quartiles but into predefined categories of increasing CPA. If numbers of subjects included in each category approximate those of quartiles, this is no more the case when each category is further divided according to the total serum IgE. The reason for this is given in Figure 3, which shows that the proportion of children with higher serum IgE gradually decreases as CPA increases.

We agree with Eggleston that the exhaled nitric oxide (eNO) test is not a specific measure of airways inflammation in asthma. Rhinitis is a potential confounder that we took into account by adjusting the odds ratios (ORs) for the sensitization to aeroallergens, including house dust mites, the most frequent allergen in allergic rhinitis. We did not retain medication for asthma or allergy in the final analysis because of the strong collinearity of this factor with some outcomes, such as doctor-diagnosed asthma. However, adding medication to the list of possible predictors did not abolish the association between eNO and CPA (OR, 1.32; 95% confidence interval, 1.09–1.60). We also found no confounding by viral infections, which is not surprising because children seriously affected by a respiratory illness were absent from schools at the time of examination.

We used objective measures whenever possible in our study (Bernard et al. 2006), but in order to derive predictors such as CPA, we had no choice but to use the information provided by parents and school directors (for compulsory pool attendance at school). We believe that the strong associations found in our study should not be dismissed as having arisen by bias or insufficient adjustment. However, what makes us increasingly confident in our observations is their reproducibility. The findings reported in our study (Bernard et al. 2006) confirm earlier observations (Bernard et al. 2003), and a new larger study on adolescents, just completed, again brings to light quite strong associations between different indicators of asthma and CPA, especially among atopic children (Bernard et al., unpublished data).

The authors declare they have no competing financial interests.

References

Bernard A, Carbonnelle S, Michel O, Higuet S, De Burbure C, Buchet JP, et al. 2003. Lung hyperpermeability and asthma prevalence in schoolchildren: unexpected associations with the attendance at indoor chlorinated swimming pools. Occup Environ Med 60:385–394.

Bernard A, Carbonnelle S, de Burbure C, Michel O, Nickmilder M. 2006. Chlorinated pool attendance, atopy and the risk of asthma during childhood. Environ Health Perspect 114:1567–1573.

Martyny JW, Harbeck RJ, Pacheco K, Barker EA, Sills M, Silveira L. 2005. Aerosolized sodium hypochlorite inhibits viability and allergenicity of mold on building materials. J Allergy Clin Immunol 116:630–635.

Nickmilder M, Carbonnelle S, Bernard A. 2007. House cleaning with bleach and the risks of allergic and respiratory diseases in children. Pediatr Allergy Immunol 1:27–35.