BRUSSELS—Chlorination is commonly used throughout the world to disinfect swimming pools. However, when chlorine compounds come into contact with organic material, they generate a mixture of potentially harmful byproducts—including nitrogen trichloride, a powerful irritant—that is then inhaled by swimmers. A new study has shown that regular indoor pool use by children is associated with a marked increase in lung epithelial permeability and an elevated risk of asthma.[1]

“This study raises the question of whether, in young children frequently attending poorly ventilated indoor pools, chlorine exposure is a possible cause for the unexplained increase in asthma,” commented Alfred Bernard, PhD, Professor of Toxicology at the Catholic University of Louvain in Brussels. This hypothesis is supported, he added, by findings from previous studies of bronchial hyperreactivity in elite swimmers.

Dr. Bernard and colleagues used a novel method of screening for subclinical changes in the respiratory epithelium that are caused by inhaled pollutants or irritants. Their method measures blood levels of lung-specific proteins that reflect the permeability or cellular integrity of the lung epithelial barrier. Three blood markers of lung epithelial hyperpermeability were identified: 16-kD Clara cell protein (CC16) and the alveolar surfactant-associated proteins A and B (SP-A and SP-B). To gauge the clinical significance of epithelial changes, they also assessed the prevalence of asthma among the children who swam regularly.

THREE STUDIES

The acute and chronic effects of indoor pool exposure on the lung epithelium were examined separately. In the chronic effects study, 226 children (mean age, 10 years) were recruited from seven primary schools—two in urban areas and five in rural areas. Blood samples were taken, and levels of SP-A, SP-B, and CC16 were measured. In all of the schools, pool attendance was compulsory.

The acute effects of indoor pool exposure were studied in 16 children (ages 5 to 14) and 13 adults (ages 26 to 47). The concentration of nitrogen trichloride was measured at a height of 1.5 m above the water surface. Blood samples were taken from all participants before they entered the pool and again after two hours of pool use for the children and after one to two hours for adults.

The third arm of the study was a retrospective analysis of data from a survey of asthma prevalence. This arm of the study included 1,881 children (ages 7 to 14) who had been recruited from 15 urban primary schools. At baseline, parents completed a questionnaire about their children’s health status, respiratory symptoms, and environmental/lifestyle variables. The schools provided information on pool attendance. Peak expiratory flow (PEF) was measured after six minutes of exercise. A decrease in PEF of 10% or more five to 10 minutes after exertion indicated significant exercise-induced bronchoconstriction (EIB).

CHRONIC EFFECTS STUDY

The children’s cumulative pool exposure varied widely, depending on the amount of time they spent in the water per week (30 to 60 minutes) and the age at which they began swimming. The one independent variable that consistently influenced serum concentrations of CC16, SP-A, and SP-B was pool exposure—the more time a child spent in the water, the greater the likelihood of increased endothelial permeability. The results did not differ between urban and rural areas.

The association was particularly strong for SP-B; in statistical analyses, pool exposure alone explained as much of the variance in levels of this protein as did all other factors combined. In these analyses, pool use had less of an effect on CC16 and SP-A concentrations, but its influence was stronger than that of environmental factors such as exposure to pets or tobacco smoke.

The children were grouped into quartiles based on their cumulative pool exposure. The serum levels of SP-A and SP-B rose significantly as pool use increased—from the second quartile upward for SP-B and from the third quartile upward for SP-A. In the present analysis, the effect of pool exposure on serum CC16 concentrations was inconsistent.

Serum immunoglobulin E (IgE) levels correlated positively with SP-B levels but negatively with CC16 levels. The data revealed no correlation between IgE and SP-A concentrations.

ACUTE EFFECTS STUDY

Most of the participants in this study were regular swimmers, and many of them already had increased levels of SP-A and SP-B. In fact, the two highest levels of SP-B were found in children who had been regular swimmers since infancy.

Exposure to chlorination byproducts caused acute changes in serum levels of SP-A and SP-B that were almost identical to those seen in the study of chronic effects. CC16 levels did not show an exposure-response relation, however. The correlations between IgE and SP-B and CC16 concentrations were identical to those in the study of chronic effects.

POOL EXPOSURE AND ASTHMA

Total asthma prevalence ranged from 5.5% to 30.5%, depending on the school. There was no correlation between the prevalence of EIB or asthma and age, sex, ethnicity, or exposure to pets or tobacco smoke.

Once again, the only variable that significantly correlated with asthma indicators (eg, prevalence of wheezing or other respiratory symptoms) was cumulative pool exposure. The association between pool use and asthma prevalence was strongest in the youngest children, who were presumed to have the highest exposure to chlorination byproducts. When exposure to pets and tobacco smoke was factored in, this association only became stronger.

CHLORINE EXPOSURE AND ITS EFFECT ON THE LUNGS

This study is one of the first to report an association between exposure to chlorination byproducts and adverse effects on the lung epithelium of swimmers. The authors noted that the increase in SP-B levels seen in the children with the highest pool attendance was of the same magnitude as that seen in smokers, indicating the severity of the lung epithelial changes, as well as the dose-dependent nature of variations in SP-B levels.

Swimmers are exposed to chlorination byproducts in indoor pools mainly when they are actively inhaling air just above the water’s surface. Levels of oxidants in the air or water of indoor pools may be high enough to affect the integrity of the lung epithelium.

“According to our observations, short-term effects on the lung epithelium seem to occur when nitrogen trichloride in the air exceeds a concentration of 300 mg/m3, a level at which the irritating effects of this gas were reported in lifeguards,” said Dr. Bernard, the study’s primary author.

These short-term effects of exposure to nitrogen trichloride are completely reversible, Dr. Bernard continued. “But the possibility of irreversible alterations in lung epithelium is suggested … since in the chronic study children had not attended the school pool the day before blood sampling.”

The authors noted that their findings appear paradoxical because swimming in the heated, humid air of an indoor pool is thought to carry a low risk of asthma development. However, Dr. Bernard observed, “there is complete lack of exposure data in [most] countries. The claim that there is no risk in indoor pools does not rely on actual measurement of [nitrogen trichloride] and is purely speculative.”

So, what can be done to minimize the potentially harmful effects of chlorination? The first step would be to measure nitrogen trichloride levels in pool air to see if they are too high and implement measures to keep these levels below 300 µg/m3, said Dr. Bernard. “Levels can be drastically reduced by improving bathers’ hygiene to reduce ’. nitrogen-containing substances (eg, urine and sweat), controlling the level of soluble chloramines in pool water by [installing] a regular water renewal or treatment system, and ventilating the pool hall.”

For now, however, noted the authors in the study’s introduction, most countries still focus on the microbiological quality of the water and largely ignore the quality of the air above.

—Gale Jurasek