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An outbreak of swimming-pool related respiratory symptoms: An elusive source of trichloramine in a municipal indoor swimming pool
International Journal of Hygiene and Environmental Health 218 (2015) 386–391
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International Journal of Hygiene and Environmental Health journal homepage: www.elsevier.com/locate/ijheh
An outbreak of swimming-pool related respiratory symptoms: An elusive source of trichloramine in a municipal indoor swimming pool Sven F. Seys a , Ludo Feyen b , Stephan Keirsbilck c , Els Adams c , Lieven J. Dupont d , Benoit Nemery c,e,∗ a
KU Leuven, Clinical Immunology, Leuven, Belgium Laboratory Derva, Heusden-Zolder, Belgium c UZ Leuven, Clinic of Occupational and Environmental Health, Leuven, Belgium d UZ Leuven, Pulmonology, Leuven, Belgium e KU Leuven, Department of Public Health and Primary Care, Centre for Environment and Health, Leuven, Belgium b
a r t i c l e
i n f o
Article history: Received 17 October 2014 Received in revised form 27 February 2015 Accepted 3 March 2015 Keywords: Trichloramine Indoor swimming pool Airway hyper reactivity Competitive swimmer Asthma
a b s t r a c t Background: Several members of a swimming club complained of respiratory symptoms associated with attending a municipal indoor swimming pool. Trichloramine, a volatile chlorination by-product and a potent respiratory irritant, was the most probable culprit, but the exact cause for its presence in excessive concentrations remained elusive. Methods: Twenty-two competitive swimmers and six coaches were evaluated during the outbreak and nine swimmers and four coaches were re-evaluated one year later. Symptoms were recorded by nonstandardized history taking; pulmonary function testing included spirometry, measurement of fraction of exhaled nitric oxide (FE NO) and histamine provocation. Concentrations of trichloramine in air were measured repeatedly by the method of Héry. Results: The most commonly reported symptoms consisted of cough (n = 16), dyspnoea (n = 13), tearing eyes (n = 10) and blocked or runny nose (n = 6). Mean FEV1 % predicted was 109.1%. Mean FE NO level was 19.7 ppb (higher than 25 ppb in 3 subjects). Airway hyperreactivity to histamine (PC20 ≤ 8 mg/ml) was detected in 22/26 subjects. Measured trichloramine concentrations in air exceeded the maximal concentration (WHO) of 0.5 mg/m3 four times between May and October 2011 and four times between January and March 2012. Polyamine compounds, present in glue used for repairing pipework, were identified as a probable external source of nitrogen resulting in increasing trichloramine concentrations. After the removal of the presumed cause of the excessive trichloramine concentrations, most subjects improved clinically, but several subjects remained symptomatic and had bronchial hyperreactivity. Discussion: A high prevalence of airway hyperreactivity, accompanied by symptoms of upper and lower airways, was detected in swimmers who had been repeatedly exposed to high trichloramine concentrations. A glue containing polyamines, used to repair a pipework, was suspected to be the source of this excessive production of trichloramine. © 2015 Elsevier GmbH. All rights reserved.
Introduction Swimming is considered to be a healthy activity and in the past, pulmonologists used to recommend regular swimming for patients with respiratory complaints given the beneficial effect of a warm, humidified environment in swimming pools (Bar-Or and Inbar, 1992). However, concerns have been expressed about the
∗ Corresponding author at: KU Leuven, Centre for Environment and Health, Herestraat 49/706, 3000 Leuven, Belgium. Tel.: +32 16 330801. E-mail address: [email protected] (B. Nemery). http://dx.doi.org/10.1016/j.ijheh.2015.03.001 1438-4639/© 2015 Elsevier GmbH. All rights reserved.
irritant nature of the environment of indoor swimming pools as a result of unwanted volatile chlorine-containing compounds resulting from the use of chlorine to disinfect swimming pool water (Weisel et al., 2009). Chlorination is the most commonly used disinfection method to avoid water-borne infections (Florentin et al., 2011; Catto et al., 2012). The disinfectant and its disinfection byproducts (DBPs) can have detrimental effects on the health status of swimmers and swimming pool staff (Nemery et al., 2002; Massin et al., 1998; Jacobs et al., 2007). When chlorine (Cl2 ) is added to water, it reacts to form hypochlorite (ClO− ) and hypochlorous acid (HClO) depending on the pH. Hypochlorite and hypochlorous acid can in turn react
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with several substances in the water, especially nitrogen compounds produced by swimmers (saliva, sweat, urine, etc.), resulting in the formation of chloramines. Monochloramine (NH2 Cl) and dichloramine (NHCl2 ) are soluble in water and they remain in the swimming pool water. Trichloramine (NCl3 ) dissolves as a gas in water and appears as a free gas in the surrounding air, a process that is enhanced by water turbulences. Trichloramine is a strong respiratory irritant that is easily inhaled by swimmers (Catto et al., 2012). Several factors may influence the concentration of disinfection by-product (DBPs) in the air of indoor swimming pools: degree of chlorination in the water, number and hygiene of the bathers, water temperature and ventilation of the indoor swimming pool, as well as the presence of some undesired products used for maintenance and/or cleaning purposes (Bessonneau et al., 2011). Significant ocular and respiratory symptoms have been reported to occur in swimming pool workers when airborne trichloramine levels exceed 0.5 mg/m3 (Fantuzzi et al., 2013). The World Health Organisation (WHO) recommends a maximal concentration of trichloramine of 0.5 mg/m3 in the air of indoor pools (World Health Organisation, 2006). Health hazards related to chlorination in swimming pools depend on the pattern of exposure (Uyan et al., 2009). Acute health hazards require high levels of chlorine compounds and occur after explosions, leaks or malfunctioning of chlorine-disinfection installations. Chronic health effects have been less recognized compared to acute health hazards and affect mainly swimming pool workers but also competitive swimmers (as a result of their high exposure, both in terms of duration and intensity). General respiratory symptoms are more common among swimming pool workers than in a control population (Jacobs et al., 2007). Furthermore, the prevalence of bronchial hyperreactivity and usage of short-acting bronchodilators is higher in competitive swimmers than in control individuals (Fitch, 2012). This study was initiated upon referral of a young member of a swimming club who reported asthmatic complaints when attending the municipal swimming pool where she trained. Since other members of the club experienced similar symptoms, an evaluation of the swimmers and teachers of the club was performed as well as an investigation into the cause of the outbreak.
Methods Study population In September 2011, a 14-year old competitive swimmer was evaluated at the outpatient clinic for occupational and environmental disorders of the University Hospital of Leuven (UZ Leuven). She had no history of respiratory disease, until a few months earlier when she started to experience respiratory symptoms, which had worsened over the course of a few months and were clearly associated with exposure to the irritant environment of the municipal swimming pool of Leopoldsburg (Flanders, Belgium), where she trained with her swimming club. Several other swimmers of her club reported having experienced similar de novo respiratory symptoms. Therefore, all competitive swimmers (n = 39) and coaches (n = 10) of the local swimming club were invited for a voluntary medical evaluation. Thus, 22 competitive swimmers and 6 coaches were investigated in the university hospital of Leuven between September 2011 and January 2012. All coaches were current or past swimmers. Therefore, swimmers and coaches were named swimmers through the manuscript. Some subjects were subsequently seen at follow-up outpatient clinic visits (to adjust their asthma treatment) and all subjects were given the opportunity to attend a follow-up evaluation a year later.
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Because this medical evaluation was done for diagnostic and clinical purposes and not for research purposes, no prior ethical clearance was requested from the hospital’s ethical review board. All subjects came out of their free will; their medical costs were paid by themselves (with partial reimbursements by their personal social security insurance). Clinical assessment Symptoms were recorded by non-standardized history taking at time of medical evaluation. Swimmers and coaches rated multiple times a week the conditions in the swimming pool (subjective assessment: low-moderate-severe). Pulmonary function tests were performed in the pulmonary function laboratory according to standard procedures. Forced Vital capacity (FVC) and Forced Expiratory Volume in 1 Second (FEV1 ), and their ratio (FEV1 /FVC) were measured using a Jaeger spirometer following ATS/ERS guidelines (Miller et al., 2005). The Fraction of exhaled nitric oxide (FE NO) was evaluated by means of chemiluminescence (CLD 88 sp, Eco Medics, Switzerland). Airway hyperreactivity was measured by histamine provocation using the method of Cockcroft et al. (1977), which involves the inhalation during successive periods of 2 min tidal breathing of increasing concentrations of histamine (from 0.03 mg/ml up to 8 mg/ml), thus allowing the determination of the PC20 , i.e. the concentration of histamine causing a 20% decrease in FEV1 compared to baseline. Total serum Immunoglobulin (Ig)E and specific IgEs for common aeroallergens (house dust mite, pets, grass and tree pollen, fungi) were determined by ImmunoCap (Phadia, Uppsala, Sweden). Trichloramine measurements Trichloramine in the air was analysed according to the reference method developed by Héry et al. (1995). Sampling cassettes were prepared and analysed by the ISO 17025 certified (Belac) laboratory Derva. In brief, air (at 1.50 m above the water surface) was sampled for about 120 min using a calibrated air pump (2 l/min) connected to a series of filters in a filter holder. The first filter was a Teflon filter to avoid chlorides present in the air from reaching the final filter; the final filter used for the quantitative analysis of the trichloramine was treated with a solution of sodium carbonate and diarsenic trioxide to convert the trichloramine to chloride. The chlorides on the final filter were analysed by ion chromatography and recalculated to the concentration of trichloramine per m3 air. The LOD (limit of detection) was 0.05 mg/m3 . Statistics Statistical analyses were performed with Graphpad Prism V for Macintosh (Graphpad Software Inc., San Diego, USA) by use of Student’s paired t-test. Normality was analyzed prior to between group analysis by the Kolmogorov Smirnov test. A difference was considered to be significant when p < 0.05. Results Clinical and functional evaluation at presentation Among the 39 club members and 10 coaches, 22 swimmers (9 to 17 years, 10 boys, 12 girls) and 6 coaches (18 to 60 years, 3 men, 3 women) were evaluated between September 2011 and February 2012 (Table 1). Most patients (22/28, 78.5%) gave a consistent history of complaints of respiratory irritation that had begun in February 2011. Over the following months, these symptoms had been variable in intensity and they were generally associated with the report of a strong “chlorine” smell in the swimming pool.
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Table 1 Subject characteristics. Age is expressed as median with interquartile range. Exposure to the swimming pool environment and lung function parameters are expressed as mean with standard deviation. Number of subjects (n)
28
Gender (male/female) Age (years) Exposure (h/week)
13/15 15.0 (12.0–18.0) 5.2 ± 1.9
Spirometry FEV1 (% predicted) FVC (% predicted) FEV1 /FVC (%)
109.1 ± 14.5 112.0 ± 15.7 82.6 ± 6.7
Histamine provocation PC20 > 8 mg/ml (n) 1 ≤ PC20 ≤ 8 mg/ml (n) 0.1 ≤ PC20 ≤ 1 mg/ml (n)
4 17 5
FE NO (ppb)
19.7 ± 16.4
Atopy Total IgE (>126 kU/l, n) Specific IgE (number of positive individuals)
5 11
Environmental assessment
Based on the information retrieved from the patient notes, the mean time spent in the swimming pool by the swimmers and coaches was 5.2 ± 1.9 h/week. The symptoms had generally been less pronounced during the summer months, but they had reappeared in the early fall, together with a feeling of a worsening of the swimming pool’s air quality. At the time of the examinations, many subjects were symptomatic (Table 2): 16 subjects complained of cough; 13 subjects complained of dyspnoea (often affecting their swimming performance); 10 subjects had ocular complaints (red and tearing eyes); 6 subjects reported upper respiratory symptoms (blocked or runny nose); 4 subjects had both upper and lower respiratory symptoms; 5 swimmers reported nausea during or after swimming. Mean (± standard deviation, SD) of FEV1 and FVC % predicted was 109.1% ± 14.5 and 112.0% ± 15.7, respectively (Table 1). FE NO was elevated (exceeding the cut off value of 25 ppb) in only 3 subjects (mean (±SD) FE NO levels: 19.7 ± 16.4; Table 1). Eleven swimmers were atopic based on a positive ImmunoCap test. Two of the 22 swimmers had a prior diagnosis of asthma and both were taking inhaled corticosteroids daily. Airway hyperreactivity (PC20 ≤ 8 mg/ml) was detected in 22 swimmers (PC20 ≤ 1 mg/ml: n = 5, 1 ≤ PC20 ≤ 8 mg/ml: n = 17). Four swimmers had a PC20 value higher than 8 mg/ml. Hyperreactivity was not assessed in 2 individuals because of symptoms of acute infection or chest pain at the time of evaluation. Atopic swimmers had significantly lower PC20 values compared to non-atopic swimmers (p = 0.007). Airway hyperreactivity did not correlate with
Table 2 Upper and lower respiratory symptoms. Upper and lower respiratory symptoms were recorded by non-standardized history taking. End 2011
End 2012
Number of subjects
28
13
Symptoms caused by irritation
Red, tearing eyes10 (37%) 5 (13%) Nausea
1 (8%) 0 (0%)
Symptoms of Upper airways Lower airways Upper and lower airways Symptom free
Runny nose Blocked nose Dyspnoea Cough
2 (7%) 3 (11%) 13 (46%) 16 (57%) 4 (14%) 6 (21%)
exposure (hours swimming/week) (Spearman r = −0.15; p = 0.25) or age (Spearman r = 0.1; p = 0.63).
1 (8%) 0 (0%) 7 (54%) 3 (23%) 1 (8%) 4 (31%)
Several measurements of airborne trichloramine levels were performed in 2011–2012. Three measurements were made between March and May 2011 and these samples revealed concentrations of 0.42, 1.28, and 0.53 mg/m3 (Fig. 1). Additional measurements of trichloramine were made at the time of medical evaluation of the swimmers (Fig. 1) and some of these levels also exceeded the WHO recommendation (0.5 mg/m3 ). The swimming pool was closed by the Flemish Government’s Department of Public Health on 14th of April 2012, pending improvements in air quality. Investigation of the possible sources for the high concentrations of trichloramine initially focused on the usual causes. These include excessive chlorination, too many swimmers and/or poor hygiene (leading to high water concentrations of nitrogen-containing compounds such as urea), and/or insufficient ventilation (for instance to conserve energy in winter). However, none of these causes could convincingly explain why the complaints had started in February 2011, although some improvements in air quality had been obtained by reducing the numbers of swimmers allowed in the pool at any time and by insisting on hygiene improvements. It emerged that the respiratory complaints and eye irritation had started shortly after repair works had been done (in January 2011) to pipework connecting the pool to an overflow reservoir (Fig. 2). A leaking pipe was repaired using a synthetic glue (T primer) containing polyamines. This type of glue was not supposed to be used in the presence of water or acid. The presence of nitrogen in high abundance was hypothesized to have allowed the generation of trichloramine upon reaction with hypochlorite in the water. After removal (on 28th of March 2012) of the glue from the pipework, the trichloramine concentration of the air decreased to a concentration below 0.5 mg/m3 (Fig. 1). The pool was re-opened on 8th of June 2012.
Follow-up after one year Thirteen individuals (46% of the initial study population) presented for re-evaluation after one year in order to assess symptoms and bronchial hyperreactivity. Although most swimmers considered that the air quality and their symptoms had improved following the reopening of the pool, several individuals reported a recent recurrence of their airway symptoms at the time of this second series of evaluations. This was attributed to a reduction of outside air intake in the swimming pool because of the low outside temperature. High trichloramine levels (0.66 mg/m3 ) were again measured during that period (March 2013). On average, bronchial reactivity to histamine did not differ between the initial value and the value one year later: PC20 was increased (i.e. bronchial reactivity had become less pronounced) in 6 out of 12, decreased in 5 out of 12 individuals and was unchanged in 1 individual (Fig. 3A). One individual did not complete the histamine test because of a vasovagal syncope during the test. Of those whose PC20 increased, three had no longer been exposed to high trichloramine in the period prior to the second evaluation. Overall, FE NO did not significantly change after 1 year (Fig. 3B). From the four individuals with elevated FE NO levels (>25 ppb), only two had a second FE NO measurement one year later. Both individuals had decreased FE NO levels, which can be explained by their therapy with inhaled steroids. All other individuals with a measured FE NO value after one year showed increased or stable FE NO levels.
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Fig. 1. Time line representing periods with severe complaints, medical evaluation and airborne trichloramine measurements (between Jan 2011 and Dec 2012). Maximal tolerated value of trichloramine (according to WHO) is indicated with a dotted line. Interventions at the swimming pool environment are marked with a cross (repair of pipework using glue containing polyamines) or an arrow (from left to right: restriction of the number of bathers, removal of the contaminated pipework and closing of the swimming pool). Respiratory complaints were reported several times a week by swimmers and coaches (low-moderate-severe).
Discussion In this study we report high airborne trichloramine levels (>0.5 mg/m3 ) on several occasions in a municipal swimming pool in Flanders (Belgium). Almost 80% of the evaluated swimmers and coaches reported symptoms of eye irritation or complaints of the airways, as a result of attending the pool. Other studies have shown that exposure to trichloramine in lifeguards can give rise to irritant eye, nasal and throat symptoms (Massin et al., 1998), and that respiratory symptoms are elevated in employees with high exposure to trichloramine (Jacobs et al., 2007). We found airway hyperreactivity (AHR) in 85% of our subjects. This is the highest prevalence of AHR among competitive swimmers reported in literature until now (Bougault and Boulet, 2012;
Fig. 2. Schematic overview of the overflow pipework of the swimming pool towards the water reservoir. Application of glue containing polyamines is indicated with a black arrow. Water from the reservoir is recirculated to the swimming pool.
Bougault et al., 2009a,b). However, the study subjects included here were relatively young compared to other studies of competitive swimmers. Whether children are more prone to develop airway hyperreactivity upon exposure to by-products of chlorination has
Fig. 3. Airway hyperreactivity (A) at the end of 2011 (n = 26) and at the end of 2012 (n = 12). Airway hyperreactivity was measured by histamine provocation test (up to 8 mg/ml). PC20 values between the two time points were compared by Student’s paired t-test. Fraction of Exhaled Nitric Oxid (B) at the end of 2011 (n = 23) and at the end of 2012 (n = 12). FE NO levels between the two time points were compared by Wilcoxon matched-pairs signed rank test.
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not been investigated to our knowledge. Airway hyperreactivity and exercise-induced bronchoconstriction in adolescents not performing competitive sports and without asthma were found in 27.3% and 7.7% of individuals, respectively (Pedersen et al., 2008). Elite athletes on the other hand, especially swimmers and athletes exposed to cold air, have an increased prevalence of AHR (Kippelen et al., 2012; Bonini et al., 2006). One study reported up to 69% of elite swimmers with AHR (Bougault et al., 2009a,b). In that particular study, however, 16 mg/ml of methacholine was used as a cut-off value to define a normal response. Therefore, in our study, the prevalence of AHR was possibly even higher, since we considered a stricter cut-off value of 8 mg/ml of histamine. Admittedly, our subjects were not a random sample of competitive swimmers, but a self-selected group of symptomatic individuals who were concerned about their health after having been exposed for some months to an environment with clearly irritant properties. Moreover, we do not know the subjects’ values of PC20 prior to the outbreak, but most of them were previously healthy and asymptomatic. So, despite the obvious limitations of this crosssectional observation of a self-selected group, it is reasonable to conclude that the proportion of subjects with bronchial hyperreactivity, some with really low values of PC20 , was high by any standard. In other words, within the context of this outbreak of de novo upper and lower respiratory disease, it is reasonable to presume that the bronchial hyperreactivity was newly acquired. A relationship between allergic sensitization and the development of airway damage/hyperreactivity has been suggested. In our study population, atopic individuals showed a higher degree of airway hyperreactivity compared to non-atopics. Whether atopics were more susceptible to develop AHR due to exposure to byproducts of chlorination or whether they had lower baseline PC20 values cannot be established from the cross-sectional study. Bougault et al. (2011) showed that airway hyperreactivity is reversible in many elite swimmers after 2 weeks of swimming cessation. It was also shown that both AHR and sputum eosinophils decreased after 5 years in past swimmers but not in active swimmers (Helenius et al., 2002). In our study, we found bronchial hyperreactivity in all subjects that were seen again after one year. However, we do not know whether this is indicative of a persistent effect – i.e. “irritant-induced asthma” – or reflective of recent high chloramine exposure, since the values of chloramine had risen again at the time of re-evaluation. Interestingly, three subjects who had stopped attending the affected swimming pool, showed reduced bronchial reactivity compared to the initial values. Further follow-up should help to determine the prognosis. Remarkably, only 3/23 swimmers had FE NO levels >25 ppb. This, however, does not rule out the presence of airway inflammation in the other swimmers. High FE NO is considered a marker of eosinophilic airway inflammation in asthma. Bonetto and colleagues showed that acute chlorine exposure leads to decreased FE NO levels (Bonetto et al., 2006), however further studies are required to elucidate the effect of swimming on FE NO levels. Alternatively, neutrophilic airway inflammation might have been induced, which cannot be detected by measurement of FE NO levels. Indeed, we found in another study that elite swimmers had higher sputum neutrophil levels compared to age-matched controls (Seys et al., 2015). Whether this may be attributed to the chronic exposure to by-products of chlorination or to intensive exercise needs to be elucidated. Several factors have been identified to lead to elevated concentrations of trichloramine in swimming pool air (Weisel et al., 2009; Catto et al., 2012). High trichloramine levels in the air may be caused by increased free chlorine in the water, increased water/air temperature ratio, increased activity in the swimming pool or decreased circulation of the surrounding air. Bodily substances like sweat or urine are known to interact with hypochlorous acid resulting
in trichloramine formation. In the present outbreak, these wellestablished causes were all considered and water quality was found to be in compliance with prevailing regulations, but despite efforts to optimize the swimming pool environment, the trichloramine levels in the air – and the accompanying complaints – remained too high. Only by removing the suspected source of additional trichloramine contamination, did the airborne trichloramine levels consistently decrease to values well below 0.5 mg/m3 . Whether this is sufficient to eliminate all ocular and respiratory symptoms is not clear. A Swiss study showed that irritative symptoms might occur at trichloramine levels of even 0.3 mg/m3 (Parrat et al., 2012). Polyamine-containing glue providing nitrogen to react with hypochlorite and generate high amounts of trichloramine has, to our knowledge, not been previously reported as a mechanism for causing swimming pool related respiratory complaints. Although this hypothesis is plausible, it remains to be verified experimentally. The outbreak caused considerable commotion in the local community, and beyond. Some parents felt that the authorities (and some local doctors) did not take the situation seriously; the authorities argued that all technical conditions for the operation of the municipal swimming pool were being met. The situation was complicated by the absence of legally binding standards for trichloramine concentrations in the air of swimming pools in the Flemish Region and, hence, no air monitoring programme was in place. The outbreak led to interpellations in the Flemish Parliament. Partly as a result of this incident, a limit of 0.5 mg/m3 for trichloramine has been recently introduced for public indoor swimming pools in the Flemish Region.
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International Journal of Hygiene and Environmental Health journal homepage: www.elsevier.com/locate/ijheh
An outbreak of swimming-pool related respiratory symptoms: An elusive source of trichloramine in a municipal indoor swimming pool Sven F. Seys a , Ludo Feyen b , Stephan Keirsbilck c , Els Adams c , Lieven J. Dupont d , Benoit Nemery c,e,∗ a
KU Leuven, Clinical Immunology, Leuven, Belgium Laboratory Derva, Heusden-Zolder, Belgium c UZ Leuven, Clinic of Occupational and Environmental Health, Leuven, Belgium d UZ Leuven, Pulmonology, Leuven, Belgium e KU Leuven, Department of Public Health and Primary Care, Centre for Environment and Health, Leuven, Belgium b
a r t i c l e
i n f o
Article history: Received 17 October 2014 Received in revised form 27 February 2015 Accepted 3 March 2015 Keywords: Trichloramine Indoor swimming pool Airway hyper reactivity Competitive swimmer Asthma
a b s t r a c t Background: Several members of a swimming club complained of respiratory symptoms associated with attending a municipal indoor swimming pool. Trichloramine, a volatile chlorination by-product and a potent respiratory irritant, was the most probable culprit, but the exact cause for its presence in excessive concentrations remained elusive. Methods: Twenty-two competitive swimmers and six coaches were evaluated during the outbreak and nine swimmers and four coaches were re-evaluated one year later. Symptoms were recorded by nonstandardized history taking; pulmonary function testing included spirometry, measurement of fraction of exhaled nitric oxide (FE NO) and histamine provocation. Concentrations of trichloramine in air were measured repeatedly by the method of Héry. Results: The most commonly reported symptoms consisted of cough (n = 16), dyspnoea (n = 13), tearing eyes (n = 10) and blocked or runny nose (n = 6). Mean FEV1 % predicted was 109.1%. Mean FE NO level was 19.7 ppb (higher than 25 ppb in 3 subjects). Airway hyperreactivity to histamine (PC20 ≤ 8 mg/ml) was detected in 22/26 subjects. Measured trichloramine concentrations in air exceeded the maximal concentration (WHO) of 0.5 mg/m3 four times between May and October 2011 and four times between January and March 2012. Polyamine compounds, present in glue used for repairing pipework, were identified as a probable external source of nitrogen resulting in increasing trichloramine concentrations. After the removal of the presumed cause of the excessive trichloramine concentrations, most subjects improved clinically, but several subjects remained symptomatic and had bronchial hyperreactivity. Discussion: A high prevalence of airway hyperreactivity, accompanied by symptoms of upper and lower airways, was detected in swimmers who had been repeatedly exposed to high trichloramine concentrations. A glue containing polyamines, used to repair a pipework, was suspected to be the source of this excessive production of trichloramine. © 2015 Elsevier GmbH. All rights reserved.
Introduction Swimming is considered to be a healthy activity and in the past, pulmonologists used to recommend regular swimming for patients with respiratory complaints given the beneficial effect of a warm, humidified environment in swimming pools (Bar-Or and Inbar, 1992). However, concerns have been expressed about the
∗ Corresponding author at: KU Leuven, Centre for Environment and Health, Herestraat 49/706, 3000 Leuven, Belgium. Tel.: +32 16 330801. E-mail address: [email protected] (B. Nemery). http://dx.doi.org/10.1016/j.ijheh.2015.03.001 1438-4639/© 2015 Elsevier GmbH. All rights reserved.
irritant nature of the environment of indoor swimming pools as a result of unwanted volatile chlorine-containing compounds resulting from the use of chlorine to disinfect swimming pool water (Weisel et al., 2009). Chlorination is the most commonly used disinfection method to avoid water-borne infections (Florentin et al., 2011; Catto et al., 2012). The disinfectant and its disinfection byproducts (DBPs) can have detrimental effects on the health status of swimmers and swimming pool staff (Nemery et al., 2002; Massin et al., 1998; Jacobs et al., 2007). When chlorine (Cl2 ) is added to water, it reacts to form hypochlorite (ClO− ) and hypochlorous acid (HClO) depending on the pH. Hypochlorite and hypochlorous acid can in turn react
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with several substances in the water, especially nitrogen compounds produced by swimmers (saliva, sweat, urine, etc.), resulting in the formation of chloramines. Monochloramine (NH2 Cl) and dichloramine (NHCl2 ) are soluble in water and they remain in the swimming pool water. Trichloramine (NCl3 ) dissolves as a gas in water and appears as a free gas in the surrounding air, a process that is enhanced by water turbulences. Trichloramine is a strong respiratory irritant that is easily inhaled by swimmers (Catto et al., 2012). Several factors may influence the concentration of disinfection by-product (DBPs) in the air of indoor swimming pools: degree of chlorination in the water, number and hygiene of the bathers, water temperature and ventilation of the indoor swimming pool, as well as the presence of some undesired products used for maintenance and/or cleaning purposes (Bessonneau et al., 2011). Significant ocular and respiratory symptoms have been reported to occur in swimming pool workers when airborne trichloramine levels exceed 0.5 mg/m3 (Fantuzzi et al., 2013). The World Health Organisation (WHO) recommends a maximal concentration of trichloramine of 0.5 mg/m3 in the air of indoor pools (World Health Organisation, 2006). Health hazards related to chlorination in swimming pools depend on the pattern of exposure (Uyan et al., 2009). Acute health hazards require high levels of chlorine compounds and occur after explosions, leaks or malfunctioning of chlorine-disinfection installations. Chronic health effects have been less recognized compared to acute health hazards and affect mainly swimming pool workers but also competitive swimmers (as a result of their high exposure, both in terms of duration and intensity). General respiratory symptoms are more common among swimming pool workers than in a control population (Jacobs et al., 2007). Furthermore, the prevalence of bronchial hyperreactivity and usage of short-acting bronchodilators is higher in competitive swimmers than in control individuals (Fitch, 2012). This study was initiated upon referral of a young member of a swimming club who reported asthmatic complaints when attending the municipal swimming pool where she trained. Since other members of the club experienced similar symptoms, an evaluation of the swimmers and teachers of the club was performed as well as an investigation into the cause of the outbreak.
Methods Study population In September 2011, a 14-year old competitive swimmer was evaluated at the outpatient clinic for occupational and environmental disorders of the University Hospital of Leuven (UZ Leuven). She had no history of respiratory disease, until a few months earlier when she started to experience respiratory symptoms, which had worsened over the course of a few months and were clearly associated with exposure to the irritant environment of the municipal swimming pool of Leopoldsburg (Flanders, Belgium), where she trained with her swimming club. Several other swimmers of her club reported having experienced similar de novo respiratory symptoms. Therefore, all competitive swimmers (n = 39) and coaches (n = 10) of the local swimming club were invited for a voluntary medical evaluation. Thus, 22 competitive swimmers and 6 coaches were investigated in the university hospital of Leuven between September 2011 and January 2012. All coaches were current or past swimmers. Therefore, swimmers and coaches were named swimmers through the manuscript. Some subjects were subsequently seen at follow-up outpatient clinic visits (to adjust their asthma treatment) and all subjects were given the opportunity to attend a follow-up evaluation a year later.
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Because this medical evaluation was done for diagnostic and clinical purposes and not for research purposes, no prior ethical clearance was requested from the hospital’s ethical review board. All subjects came out of their free will; their medical costs were paid by themselves (with partial reimbursements by their personal social security insurance). Clinical assessment Symptoms were recorded by non-standardized history taking at time of medical evaluation. Swimmers and coaches rated multiple times a week the conditions in the swimming pool (subjective assessment: low-moderate-severe). Pulmonary function tests were performed in the pulmonary function laboratory according to standard procedures. Forced Vital capacity (FVC) and Forced Expiratory Volume in 1 Second (FEV1 ), and their ratio (FEV1 /FVC) were measured using a Jaeger spirometer following ATS/ERS guidelines (Miller et al., 2005). The Fraction of exhaled nitric oxide (FE NO) was evaluated by means of chemiluminescence (CLD 88 sp, Eco Medics, Switzerland). Airway hyperreactivity was measured by histamine provocation using the method of Cockcroft et al. (1977), which involves the inhalation during successive periods of 2 min tidal breathing of increasing concentrations of histamine (from 0.03 mg/ml up to 8 mg/ml), thus allowing the determination of the PC20 , i.e. the concentration of histamine causing a 20% decrease in FEV1 compared to baseline. Total serum Immunoglobulin (Ig)E and specific IgEs for common aeroallergens (house dust mite, pets, grass and tree pollen, fungi) were determined by ImmunoCap (Phadia, Uppsala, Sweden). Trichloramine measurements Trichloramine in the air was analysed according to the reference method developed by Héry et al. (1995). Sampling cassettes were prepared and analysed by the ISO 17025 certified (Belac) laboratory Derva. In brief, air (at 1.50 m above the water surface) was sampled for about 120 min using a calibrated air pump (2 l/min) connected to a series of filters in a filter holder. The first filter was a Teflon filter to avoid chlorides present in the air from reaching the final filter; the final filter used for the quantitative analysis of the trichloramine was treated with a solution of sodium carbonate and diarsenic trioxide to convert the trichloramine to chloride. The chlorides on the final filter were analysed by ion chromatography and recalculated to the concentration of trichloramine per m3 air. The LOD (limit of detection) was 0.05 mg/m3 . Statistics Statistical analyses were performed with Graphpad Prism V for Macintosh (Graphpad Software Inc., San Diego, USA) by use of Student’s paired t-test. Normality was analyzed prior to between group analysis by the Kolmogorov Smirnov test. A difference was considered to be significant when p < 0.05. Results Clinical and functional evaluation at presentation Among the 39 club members and 10 coaches, 22 swimmers (9 to 17 years, 10 boys, 12 girls) and 6 coaches (18 to 60 years, 3 men, 3 women) were evaluated between September 2011 and February 2012 (Table 1). Most patients (22/28, 78.5%) gave a consistent history of complaints of respiratory irritation that had begun in February 2011. Over the following months, these symptoms had been variable in intensity and they were generally associated with the report of a strong “chlorine” smell in the swimming pool.
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Table 1 Subject characteristics. Age is expressed as median with interquartile range. Exposure to the swimming pool environment and lung function parameters are expressed as mean with standard deviation. Number of subjects (n)
28
Gender (male/female) Age (years) Exposure (h/week)
13/15 15.0 (12.0–18.0) 5.2 ± 1.9
Spirometry FEV1 (% predicted) FVC (% predicted) FEV1 /FVC (%)
109.1 ± 14.5 112.0 ± 15.7 82.6 ± 6.7
Histamine provocation PC20 > 8 mg/ml (n) 1 ≤ PC20 ≤ 8 mg/ml (n) 0.1 ≤ PC20 ≤ 1 mg/ml (n)
4 17 5
FE NO (ppb)
19.7 ± 16.4
Atopy Total IgE (>126 kU/l, n) Specific IgE (number of positive individuals)
5 11
Environmental assessment
Based on the information retrieved from the patient notes, the mean time spent in the swimming pool by the swimmers and coaches was 5.2 ± 1.9 h/week. The symptoms had generally been less pronounced during the summer months, but they had reappeared in the early fall, together with a feeling of a worsening of the swimming pool’s air quality. At the time of the examinations, many subjects were symptomatic (Table 2): 16 subjects complained of cough; 13 subjects complained of dyspnoea (often affecting their swimming performance); 10 subjects had ocular complaints (red and tearing eyes); 6 subjects reported upper respiratory symptoms (blocked or runny nose); 4 subjects had both upper and lower respiratory symptoms; 5 swimmers reported nausea during or after swimming. Mean (± standard deviation, SD) of FEV1 and FVC % predicted was 109.1% ± 14.5 and 112.0% ± 15.7, respectively (Table 1). FE NO was elevated (exceeding the cut off value of 25 ppb) in only 3 subjects (mean (±SD) FE NO levels: 19.7 ± 16.4; Table 1). Eleven swimmers were atopic based on a positive ImmunoCap test. Two of the 22 swimmers had a prior diagnosis of asthma and both were taking inhaled corticosteroids daily. Airway hyperreactivity (PC20 ≤ 8 mg/ml) was detected in 22 swimmers (PC20 ≤ 1 mg/ml: n = 5, 1 ≤ PC20 ≤ 8 mg/ml: n = 17). Four swimmers had a PC20 value higher than 8 mg/ml. Hyperreactivity was not assessed in 2 individuals because of symptoms of acute infection or chest pain at the time of evaluation. Atopic swimmers had significantly lower PC20 values compared to non-atopic swimmers (p = 0.007). Airway hyperreactivity did not correlate with
Table 2 Upper and lower respiratory symptoms. Upper and lower respiratory symptoms were recorded by non-standardized history taking. End 2011
End 2012
Number of subjects
28
13
Symptoms caused by irritation
Red, tearing eyes10 (37%) 5 (13%) Nausea
1 (8%) 0 (0%)
Symptoms of Upper airways Lower airways Upper and lower airways Symptom free
Runny nose Blocked nose Dyspnoea Cough
2 (7%) 3 (11%) 13 (46%) 16 (57%) 4 (14%) 6 (21%)
exposure (hours swimming/week) (Spearman r = −0.15; p = 0.25) or age (Spearman r = 0.1; p = 0.63).
1 (8%) 0 (0%) 7 (54%) 3 (23%) 1 (8%) 4 (31%)
Several measurements of airborne trichloramine levels were performed in 2011–2012. Three measurements were made between March and May 2011 and these samples revealed concentrations of 0.42, 1.28, and 0.53 mg/m3 (Fig. 1). Additional measurements of trichloramine were made at the time of medical evaluation of the swimmers (Fig. 1) and some of these levels also exceeded the WHO recommendation (0.5 mg/m3 ). The swimming pool was closed by the Flemish Government’s Department of Public Health on 14th of April 2012, pending improvements in air quality. Investigation of the possible sources for the high concentrations of trichloramine initially focused on the usual causes. These include excessive chlorination, too many swimmers and/or poor hygiene (leading to high water concentrations of nitrogen-containing compounds such as urea), and/or insufficient ventilation (for instance to conserve energy in winter). However, none of these causes could convincingly explain why the complaints had started in February 2011, although some improvements in air quality had been obtained by reducing the numbers of swimmers allowed in the pool at any time and by insisting on hygiene improvements. It emerged that the respiratory complaints and eye irritation had started shortly after repair works had been done (in January 2011) to pipework connecting the pool to an overflow reservoir (Fig. 2). A leaking pipe was repaired using a synthetic glue (T primer) containing polyamines. This type of glue was not supposed to be used in the presence of water or acid. The presence of nitrogen in high abundance was hypothesized to have allowed the generation of trichloramine upon reaction with hypochlorite in the water. After removal (on 28th of March 2012) of the glue from the pipework, the trichloramine concentration of the air decreased to a concentration below 0.5 mg/m3 (Fig. 1). The pool was re-opened on 8th of June 2012.
Follow-up after one year Thirteen individuals (46% of the initial study population) presented for re-evaluation after one year in order to assess symptoms and bronchial hyperreactivity. Although most swimmers considered that the air quality and their symptoms had improved following the reopening of the pool, several individuals reported a recent recurrence of their airway symptoms at the time of this second series of evaluations. This was attributed to a reduction of outside air intake in the swimming pool because of the low outside temperature. High trichloramine levels (0.66 mg/m3 ) were again measured during that period (March 2013). On average, bronchial reactivity to histamine did not differ between the initial value and the value one year later: PC20 was increased (i.e. bronchial reactivity had become less pronounced) in 6 out of 12, decreased in 5 out of 12 individuals and was unchanged in 1 individual (Fig. 3A). One individual did not complete the histamine test because of a vasovagal syncope during the test. Of those whose PC20 increased, three had no longer been exposed to high trichloramine in the period prior to the second evaluation. Overall, FE NO did not significantly change after 1 year (Fig. 3B). From the four individuals with elevated FE NO levels (>25 ppb), only two had a second FE NO measurement one year later. Both individuals had decreased FE NO levels, which can be explained by their therapy with inhaled steroids. All other individuals with a measured FE NO value after one year showed increased or stable FE NO levels.
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Fig. 1. Time line representing periods with severe complaints, medical evaluation and airborne trichloramine measurements (between Jan 2011 and Dec 2012). Maximal tolerated value of trichloramine (according to WHO) is indicated with a dotted line. Interventions at the swimming pool environment are marked with a cross (repair of pipework using glue containing polyamines) or an arrow (from left to right: restriction of the number of bathers, removal of the contaminated pipework and closing of the swimming pool). Respiratory complaints were reported several times a week by swimmers and coaches (low-moderate-severe).
Discussion In this study we report high airborne trichloramine levels (>0.5 mg/m3 ) on several occasions in a municipal swimming pool in Flanders (Belgium). Almost 80% of the evaluated swimmers and coaches reported symptoms of eye irritation or complaints of the airways, as a result of attending the pool. Other studies have shown that exposure to trichloramine in lifeguards can give rise to irritant eye, nasal and throat symptoms (Massin et al., 1998), and that respiratory symptoms are elevated in employees with high exposure to trichloramine (Jacobs et al., 2007). We found airway hyperreactivity (AHR) in 85% of our subjects. This is the highest prevalence of AHR among competitive swimmers reported in literature until now (Bougault and Boulet, 2012;
Fig. 2. Schematic overview of the overflow pipework of the swimming pool towards the water reservoir. Application of glue containing polyamines is indicated with a black arrow. Water from the reservoir is recirculated to the swimming pool.
Bougault et al., 2009a,b). However, the study subjects included here were relatively young compared to other studies of competitive swimmers. Whether children are more prone to develop airway hyperreactivity upon exposure to by-products of chlorination has
Fig. 3. Airway hyperreactivity (A) at the end of 2011 (n = 26) and at the end of 2012 (n = 12). Airway hyperreactivity was measured by histamine provocation test (up to 8 mg/ml). PC20 values between the two time points were compared by Student’s paired t-test. Fraction of Exhaled Nitric Oxid (B) at the end of 2011 (n = 23) and at the end of 2012 (n = 12). FE NO levels between the two time points were compared by Wilcoxon matched-pairs signed rank test.
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not been investigated to our knowledge. Airway hyperreactivity and exercise-induced bronchoconstriction in adolescents not performing competitive sports and without asthma were found in 27.3% and 7.7% of individuals, respectively (Pedersen et al., 2008). Elite athletes on the other hand, especially swimmers and athletes exposed to cold air, have an increased prevalence of AHR (Kippelen et al., 2012; Bonini et al., 2006). One study reported up to 69% of elite swimmers with AHR (Bougault et al., 2009a,b). In that particular study, however, 16 mg/ml of methacholine was used as a cut-off value to define a normal response. Therefore, in our study, the prevalence of AHR was possibly even higher, since we considered a stricter cut-off value of 8 mg/ml of histamine. Admittedly, our subjects were not a random sample of competitive swimmers, but a self-selected group of symptomatic individuals who were concerned about their health after having been exposed for some months to an environment with clearly irritant properties. Moreover, we do not know the subjects’ values of PC20 prior to the outbreak, but most of them were previously healthy and asymptomatic. So, despite the obvious limitations of this crosssectional observation of a self-selected group, it is reasonable to conclude that the proportion of subjects with bronchial hyperreactivity, some with really low values of PC20 , was high by any standard. In other words, within the context of this outbreak of de novo upper and lower respiratory disease, it is reasonable to presume that the bronchial hyperreactivity was newly acquired. A relationship between allergic sensitization and the development of airway damage/hyperreactivity has been suggested. In our study population, atopic individuals showed a higher degree of airway hyperreactivity compared to non-atopics. Whether atopics were more susceptible to develop AHR due to exposure to byproducts of chlorination or whether they had lower baseline PC20 values cannot be established from the cross-sectional study. Bougault et al. (2011) showed that airway hyperreactivity is reversible in many elite swimmers after 2 weeks of swimming cessation. It was also shown that both AHR and sputum eosinophils decreased after 5 years in past swimmers but not in active swimmers (Helenius et al., 2002). In our study, we found bronchial hyperreactivity in all subjects that were seen again after one year. However, we do not know whether this is indicative of a persistent effect – i.e. “irritant-induced asthma” – or reflective of recent high chloramine exposure, since the values of chloramine had risen again at the time of re-evaluation. Interestingly, three subjects who had stopped attending the affected swimming pool, showed reduced bronchial reactivity compared to the initial values. Further follow-up should help to determine the prognosis. Remarkably, only 3/23 swimmers had FE NO levels >25 ppb. This, however, does not rule out the presence of airway inflammation in the other swimmers. High FE NO is considered a marker of eosinophilic airway inflammation in asthma. Bonetto and colleagues showed that acute chlorine exposure leads to decreased FE NO levels (Bonetto et al., 2006), however further studies are required to elucidate the effect of swimming on FE NO levels. Alternatively, neutrophilic airway inflammation might have been induced, which cannot be detected by measurement of FE NO levels. Indeed, we found in another study that elite swimmers had higher sputum neutrophil levels compared to age-matched controls (Seys et al., 2015). Whether this may be attributed to the chronic exposure to by-products of chlorination or to intensive exercise needs to be elucidated. Several factors have been identified to lead to elevated concentrations of trichloramine in swimming pool air (Weisel et al., 2009; Catto et al., 2012). High trichloramine levels in the air may be caused by increased free chlorine in the water, increased water/air temperature ratio, increased activity in the swimming pool or decreased circulation of the surrounding air. Bodily substances like sweat or urine are known to interact with hypochlorous acid resulting
in trichloramine formation. In the present outbreak, these wellestablished causes were all considered and water quality was found to be in compliance with prevailing regulations, but despite efforts to optimize the swimming pool environment, the trichloramine levels in the air – and the accompanying complaints – remained too high. Only by removing the suspected source of additional trichloramine contamination, did the airborne trichloramine levels consistently decrease to values well below 0.5 mg/m3 . Whether this is sufficient to eliminate all ocular and respiratory symptoms is not clear. A Swiss study showed that irritative symptoms might occur at trichloramine levels of even 0.3 mg/m3 (Parrat et al., 2012). Polyamine-containing glue providing nitrogen to react with hypochlorite and generate high amounts of trichloramine has, to our knowledge, not been previously reported as a mechanism for causing swimming pool related respiratory complaints. Although this hypothesis is plausible, it remains to be verified experimentally. The outbreak caused considerable commotion in the local community, and beyond. Some parents felt that the authorities (and some local doctors) did not take the situation seriously; the authorities argued that all technical conditions for the operation of the municipal swimming pool were being met. The situation was complicated by the absence of legally binding standards for trichloramine concentrations in the air of swimming pools in the Flemish Region and, hence, no air monitoring programme was in place. The outbreak led to interpellations in the Flemish Parliament. Partly as a result of this incident, a limit of 0.5 mg/m3 for trichloramine has been recently introduced for public indoor swimming pools in the Flemish Region.
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