"SWIMMER'S ASTHMA": THE SERIOUS HEALTH PROBLEM WITH CHLORINATED POOLS

Brent S. Rushall, Ph.D.,R.Psy.
San Diego State University

and

Larry Weisenthal, M.D.,Ph.D.
Weisenthal Cancer Group
Huntington Beach, California

[First published in Select, the on-line journal of the National Sports Medicine Institute of the UK, in December, 2003: http://www.nsmi.org.uk/select/dec03/asthma.html.]

The vast majority of swimming pools use chlorination as the sanitizing method to maintain a "healthy" level of water hygiene. The understanding and control of chlorine concentrations is far from an exact or trained science for those individuals often in charge of heavily used recreational and competitive swimming pools. The sanitization of home and small recreation pools is not a focus of this discussion.

Chlorination is a dangerous but institutionalized and accepted method of pool sanitation. Chlorine concentrations in water decline very quickly under a variety of swimming pool and environmental conditions. To combat the decline in effectiveness problem, pool managers often over-chlorinate a pool (>3 ppm) to offset chlorine reduction and occasionally use even more as a "precautionary measure" to kill "missed" bacteria. A heightened concentration of chlorine often leads to excessive absorption through the skin and inspiration leading to breathing problems in many swimmers. There is considerable variation in chlorine concentrations in fresh and salt water pools with the latter usually being much higher (Beech et al., 1980).

The general rule-of-thumb about an over-chlorinated pool is: If you can smell the chlorine in the pool environment, it is dangerously high. When chlorination alone is the form of sanitization health threats exist.

There is considerable individual variation among swimmer in sensitivity to chlorine concentrations. A large majority can tolerate slight levels of over-chlorination. As the amount of over-chlorination increases, more individuals become noticeably affected.

Some of the substances released from chlorinated water include bromodichloromethane, chloroform, dibromochloromethane, and bromoform (collectively called trihalomethanes - THMs). Chlorine reacts with bodily proteins to form chloramines; the most volatile and prevalent in the air above swimming pools is nitrogen trichloride (NCl3).

Why would chlorine be a problem in pools when it has been used for so long? Once, the vast majority of swimming pools were outdoors or in high-ceilinged rooms with good ventilation. As the cost of such facilities rose, the room space shrunk in proportion to water volume. When chlorine escapes from pool water it is diluted in the available air space. The smaller the air volume, the greater the concentration of airborne chloramines (the nasty product of pool chlorination). The concentration of chlorine in the air is gradual, being highest at the water surface and least at the greatest distance from the surface. Chlorine concentration is also governed by the movement of air across the water surface (the greater the movement, the less the concentration of chloramines assuming that removed air is replaced by fresh air). Many modern pools are structured to not facilitate removal of escaping chlorine.

Some structural characteristics of pools increase chlorine concentrations near the water surface. Some examples are:

These three features result in accumulated concentrations of THMs just above the water surface, that is, in the air that swimmers continually breathe. Admittedly, one swim in such a pool might not produce any health problems in a swimmer, but frequent users such as competitive age-group, school, college, and master's swimmers suffer extended periods of exaggerated breathing in the hyper-chlorinated micro atmosphere.

With most outdoor pools, chlorine concentrations at the surface are usually low because environmental breezes whisk the contaminant away and replace it with "fresh" air. However, when outdoor pool sides are high, the atmosphere is heavy with moisture, and there is no breeze, dangerous atmospheric chlorine conditions can be produced. The atmosphere acts as a "blanket" that holds the escaping chlorine down at the surface where swimmers breathe. That results in hyper-chlorination in outdoor pools. This condition happens quite frequently, particularly early in the morning when "serious" swimmers are training.

The conditions of many pools are such that swimmers are subjected to breathing in a moderately toxic aeration, for chlorine is a poison.

Serious swimmers exacerbate the situation further. The intensity of their exercise is such that the volume of inspired air is increased by rises in frequency and volume of tidal air (Drobnic et al., 1996; Helenius & Haahtela, 2000). It is possible, that an exercising swimmer could be exposed to 30 or more times the volume of escaping chlorine byproducts than that experienced by a passive onlooker. Many swimmers agitate the water through vigorous exercise which accelerates the release of chlorine into the atmosphere. When chlorine concentrations in the air are measured as part of pool maintenance, it is usually done when no swimmers are present and water is minimally disturbed. Thus, when a pool is deemed "safe" it is because of an arbitrary measure in rare conditions. It bears no relationship to what exists in a pool busy with competitive swimmers when the atmosphere of a "safe" chlorinated pool becomes toxic. Exercising in a chlorinated pool increases the levels of assimilation of chlorine related gases. The greater the amount of exercise, the greater the concentrations of absorbed THMs. Thus, hard training swimmers are at greater risk than occasional recreational swimmers. It takes at least one night for absorbed substances to be removed from the body. If insufficient time exists between training sessions the possibility of toxic build-up is real (Cammann & Hubner, 1995).

The benefits of swimming as a form of exercise are frequently extolled (Bar-Or & Inbar, 1992) and demonstrated (Matsumoto, 1999). However, while the actions of the exercise in possibly non-threatening atmospheres are usually discussed, real threats of traditional environments are mostly ignored.

Swimmers and Chlorine

The existence of respiratory problems in competitive swimmers in chlorinated pools has been known for some time (Decker & Koch, 1978; Mustchin & Pickering, 1979). It has received little attention from the health or swimming communities. Testimonies and anecdotes about extreme respiratory problems have been illustrated (Rushall, 2003). Health problems of swimmers in indoor pools have traditionally been attributed to chlorine in the water. Chlorine reacts with bodily proteins to form chloramines; the most volatile and prevalent in the air above the pool surface being nitrogen trichloride (NCl3) (Thickett et al, 2002). The health of pool workers is also affected by these airborne toxins although they are relatively sedentary.

Bernard et al. (2003) studied exposure to nitrogen trichloride in indoor chlorinated pools and its affect on the respiratory epithelium of children. Increased risk of some lung diseases such as asthma was also assessed. Healthy children (N = 226), were measured for serum surfactant associated proteins. Lung specific proteins were measured in the serum of 16 children and 13 adults before and after exposure to NCl3 in an indoor chlorinated pool. The relation between pool attendance and asthma prevalence was studied in 1881 children. Asthma was screened with the exercise induced bronchoconstriction test (EIB).

Regular attendance at chlorinated pools by young children was associated with an exposure-dependent increase in lung epithelium permeability and increase in the risk of developing asthma, especially in association with other risk factors. It is postulated that increased exposure of children to chlorination products in indoor pools might be an important cause of the rising incidence of childhood asthma and allergic diseases in industrialized countries.

Aggazzotti et al. (1998) studied exposure to THMs in indoor chlorinated swimming pools. Environmental and biological monitoring of THMs was undertaken to assess the uptake of these substances after a defined period in competitive swimmers (N = 5), regularly attending an indoor swimming pool to train for competition during four sampling sessions. After one hour of swimming, the THM uptake was approximately seven times higher than at rest. The main implication of this study was that training for swimming in a poorly ventilated indoor swimming pool has the potential to cause illness through breathing undesirable concentrations of mainly chloroform.

Alveolar breath sampling was used to evaluate THM exposures encountered by collegiate swimmers during a typical 2-hr training period in an indoor natatorium (Lindstrom, Pleil, & Berkoff, 1997). The uptake of two THMs (chloroform and bromodichloromethane) was very rapid, with chloroform concentrations exceeding the natatorium air levels within eight minutes after the exposure began. Chloroform levels continued to rise steeply until they were more than two times the indoor levels. These findings suggest there may be appreciable transcutaneous absorption of THMs, in addition to absorption through the respiratory route.

Aiking et al. (1994) concluded that toxic effects of chlorine products in swimmers training in indoor pools are greater in younger than older swimmers. Young swimmers are therefore at a greater health risk. The hypersensitivity of young children to pool chlorination was also emphasized by Wood, Colombo, and Benson, (1987). They reported two cases of serious respiratory injury in two young children exposed to chlorinator tablets in backyard pools. Although this paper does not consider small self-monitored pools, the reactivity of young children to chlorine products does emphasize the threat that hyper-chlorination presents to younger people.

A different effect of chlorinated water on competitive swimmers was reported by Centerwall et al, (1986) and Geurtsen (2000). Erosion of dental enamel was reported in competitive swimmers from the same club. Symptoms compatible with dental enamel erosion were reported by 3% of non-swimmers (9/295), 12% of swimmers who were not members of the swim team (46/393), and 39% of swim team members (23/59). Four swimmers with clinically verified dental enamel erosion had trained regularly in the same pool. That pool was compared to one that had eight equivalent swimmers without enamel erosion. The implicated swimming pool revealed a gas-chlorinated pool with corrosion of metal fixtures and etching of cement and a pH of 2.7. Acid erosion of dental enamel ("swimmer's erosion") is a painful, costly, irreversible condition which can be caused by inadequately maintained gas-chlorinated swimming pools. Dentists who locate such erosion rarely link it to hyper-chlorine exposure but more to drinking of sodas and other acidic beverages. It should be remembered that over-chlorinated pools that produce excessively elevated levels of acidity can contribute to dental enamel erosion in competitive swimmers.

The extent of other health complications due to chlorination is not known. Nelemans et al. (1994) reported a positive association between a history of swimming and melanoma risk even after adjusting for sun exposure history. This suggests that carcinogenic agents in water, possibly chlorination by products, may play a role in melanoma etiology.

The most common adverse health effects related to pool chlorination are obstructive airway problems, particularly asthma. Dr. Stephen J. McGready, and colleagues measured the lung function of competitive swimmers (N = 28) before and after cycle ergometer testing in swimming pool and laboratory settings. The study was initiated after observations of university team swimmers displaying significant airway obstruction and many swimmers using beta-agonist inhalers. Lung function was significantly worse in the pool than in the laboratory. Swimmers (14%) not previously asthmatic displayed airway obstruction at baseline. Exercise-induced bronchospasm occurred in a further 11% of swimmers not known to have that problem or asthma. Swimmers known to have asthma seemed to do better than swimmers who had not previously been diagnosed with asthma. Exercise-induced bronchospasm negatively affected performance. It was concluded that swimming is worse with respect to bronchospasm than other endurance sports, a paradox since swimming is supposed to promote health. The facility/exercise setting is implicated as the cause of these respiratory afflictions (Reuters Health, 2001). Helenius & Haahtela (2000) reported the risk of asthma is especially increased among competitive swimmers, of which 36% to 79% show bronchial hyperresponsiveness to methacholine or histamine. Helenius et al. (1998) and Langdeau and Boulet (2001) also reported on asthma and hyper-responsiveness in athletes, particularly competitive swimmers. A greater prevalence of these problems occurred in swimmers than in the general population.

Fjellbirkeland, Gulsvik, and Walloe (1995) described the development of respiratory problems in four age-group swimmers who participated in heavy swimming. They were said to have symptoms of exercise-induced asthma (EIA). Three of them started to develop the symptoms after several years of training and had no former history of asthma. In the fourth, the asthma was diagnosed in childhood but the EIA-symptoms were exacerbated by swimming. All four experienced more symptoms when pool air was warm, or when there was a strong smell of chlorine. Two of the athletes reported having no symptoms when they swam in outdoor pools and had only minor symptoms or none at all, when they did other forms of exercise, including running. Swimming performance was hampered by the respiratory symptoms in all subjects.

Helenius et al. (2002) completed a 5-year study on eosinophil airway inflammation, bronchial hyper-responsiveness, and asthma in elite competitive swimmers. Initial and final rates of occurrence of these problems were measured in swimmers who ceased training (N = 26) and those who continued training (N = 16) over the period. All measures increased significantly in continuing swimmers but decreased significantly in those who left the sport. This important study directly contradicts the oft-quoted assertion that swimming has a salubrious or mitigating effect on asthma (e.g. Rusnak, 2003). In fact, the opposite appears to be the case. The demonstration of reversibility upon swimming cessation accounts for respiratory-problem abatement when some swimming environment factors are changed. The Helenius study also challenges the assertion that the higher incidence of asthma in swimmers is due to selection (asthmatics preferentially choosing swimming over other sports), as opposed to causation (swimming causing asthma).

It seems that the more extensive the investigation, the more extensive are the discovered effects of chlorinated pools. Zwick et al. (1990) compared competitive swimmers (N = 14) and matched control subjects (N = 14) for clinically manifest allergies, subclinical sensitization to aeroallergens, imbalance of the cellular immune system, and bronchial hyperresponsiveness. Conjunctival or respiratory symptoms were found in 11 swimmers and in 3 controls. Sensitization to aeroallergens was confirmed in 9 swimmers by a skin test and in 11 swimmers by a radioallergosorbent test. Control subjects recorded 4 and 5 respectively. An altered cellular immune system, (i.e., imbalance in T-cell system, B-cell system, or natural killer cells) was detected in 7 swimmers and 2 controls. Bronchial hyperresponsiveness to methacholine was seen in 11 swimmers and 5 controls. This higher incidence of allergic diseases and subclinical sensitization to aeroallergens, disorders of the cellular immune system, and bronchial hyperresponsiveness in competitive swimmers was attributed to repeated exposure to chlorine in swimming pools.

Consistent and frequent training in chlorinated swimming pools presents a serious risk to individuals who are susceptible to respiratory reactions as well as other illnesses. The intensity of the stimulus may be relatively low but with time, even years, health problems develop. Once respiration begins to be impaired, the problem most probably would be accelerated. When an obstructive airway disorder is established, swimmers are not as efficient in emptying their airways as are people who do not have airway obstruction. If airway/blood exchange of oxygen, nitrogen, and carbon dioxide are more efficient than that of THM, then THM would accumulate in the alveoli over time to above ambient air levels without absorption from any other route. The rate of absorption would consequently increase. This is an important point which should be researched.

The symptoms of respiratory difficulties due to the atmospheric toxins are similar to asthma, which leads to the common diagnosis and treatment of the condition as "swimmer's asthma." However, it is proposed that the designation as asthma is incorrect. The reactions and problems are environment specific and are better classified as toxic reactions. When "chlorine asthmatics" swim in pools that are not normally or heavily chlorinated, in pools that use different chemicals or systems to sanitize water, or in environments where escaping substances from the chlorinated water are ventilated away almost immediately to yield a very low concentration, the asthma problem often disappears. It is reasonable to assert that a substitute for the ancient method of pool chlorination could result in a reduction in the occurrence of swimmer's asthma and a more healthful response to competitive swimming.

Alternative Pool Sanitization Manipulations

The principal reason why chlorine has persisted as a sanitizer for swimming pools is that it is very effective in that role. Alternative water treatments (e.g., ozone, bromine, ultra-violet light) have usually relied on a single chemical treatment. That focus on using one agent could be a limitation for devising an adequate substitute for the hyperchlorination of heavily used pools. Some alternatives to sole chlorination that have been effective and some as improvements have been suggested.

Chlorine and ozone. A bacteriological study was conducted at the first Leisure Centre swimming pool in the United Kingdom to be disinfected with ozone/chlorine. Results suggested that a free chlorine concentration of approximately 0.8 mg/l was necessary to maintain a bacteriologically satisfactory condition. That amount of free chlorine is similar to that required when a pool is disinfected with chlorine alone. However, the associated amount of combined chlorine was much lower when disinfection was by ozone/chlorine. This produced more acceptable bathing conditions (Wyatt & Wilson, 1979). Ozonation allows markedly reduced levels of chlorine in pool water (Lindstrom, Pleil, & Berkoff, 1997).

Chlorine and ionization. As an alternative disinfectant to sole chlorination, electrolytically generated copper and silver ions (400 and 40 micrograms/L copper and silver, respectively) with and without free chlorine (0.3 mg/L) was evaluated over a period of 4 weeks in indoor and outdoor water systems (100 L tap water with natural body flora and urine). Numbers of total coliform, pseudomonas, and staphylococci were all less than drinking water standards in systems treated with copper:silver and free chlorine and systems treated with free chlorine alone (1.0 mg/L). It was concluded that the addition of electrolytic copper and silver to water systems may allow the concentration of free chlorine to be reduced while still providing comparable sanitary quality of the water (Yahya et al. 1990).

Chlorine and hydrogen peroxide. Jessen (1989) reported supplementing hyperchlorine with 20-30% hydrogen peroxide or potassium peroxide sulphate. The reaction between the chlorine and hydrogen peroxide resulted in the spontaneous formation of nascinating oxygen. Chloramines were reduced. This can be explained by the reaction of oxygen with chlorine. Because of its low expense, the forced decomposition of hydrogen peroxide could be an alternative to ozone for use in small baths. Potassium peroxide sulphate and chlorine did not result in a significant improvement in water quality.

Chlorine and ultraviolet light. Ultraviolet light alone does not effectively sanitize pool water (De Jonckheere, 1982). However, a combination of reduced amounts of chlorine and ultraviolet light has been reported as being successful (Carlile Swimming Organization, Australia, personal communication, October 1, 2003).

Chlorine, Oxone®, and ionization. The Carlile Swimming Organization (personal communication, October 1, 2003) has experimented with low levels of chlorine, ionization, and Oxone® (potassium monopersulfate) in combination as treatment for high-use teaching pools. Aquabrite® is a proprietary blend of oxidizers, one of which is Oxone®. The oxidizers are a non-chlorine shock treatment but not a chlorine substitute because they are not disinfectants. The Carlile Swimming Organization's pools were used to evaluate the combination of low levels of chlorine, Aquabrite®, and ionization with silver, zinc, and copper. The oxidizers reduce organic matter, particularly chloramines, and other nitrogenous compounds and also work in synergy with copper and silver as a disinfectant. This system has advantages over chlorine and bromine systems in that it does not rely on a halogen based disinfectant that produce odor and respiratory illnesses. Small amounts of chlorine are used to "burn out" some organic substances and to bring water back to a clear blue color. This treatment has been so successful that it has been accepted by the state government of New South Wales as a viable water treatment protocol.

These alternative water treatments are acceptable methods for reducing the amount of noxious chlorine-related substances in swimming pool environments while still providing excellent sanitization. In the interests of serious swimmers and young people, they are worthwhile adopting rather than persisting with singularly dangerous chlorine treatments.

Summary

There are a number of implications and conclusions that can be drawn from works associated with the evaluation of swimming in chlorinated pools. They are listed below in point form.

References

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  27. Yahya, M. T., Landeen, L. K., Messina, M. C., Kutz, S. M., Schulze, R., & Gerba, C. P. (1990). Disinfection of bacteria in water systems by using electrolytically generated copper:silver and reduced levels of free chlorine. Canadian Journal of Microbiology, 36, 109-116.
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