Airborne trichloramine (NCl 3 ) levels and self-reported health symptoms in indoor swimming pool workers: dose-response relationships

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1 Joural of Exposure Sciece ad Evirometal Epidemiology (2013) 23, & 2013 Nature America, Ic. All rights reserved /13 ORIGINAL ARTICLE Airbore trichloramie (NCl 3 ) levels ad self-reported health symptoms i idoor swimmig pool workers: dose-respose relatioships Guglielmia Fatuzzi 1, Elea Righi 1, Guerrio Predieri 1, Pierluigi Giacobazzi 1, Berchotd Petra 1 ad Gabriella Aggazzotti 1 The hypothesis that attedace at idoor chloriated swimmig pool is a risk factor for irritative ocular ad respiratory symptoms ad brochial asthma is well kow i literature, although epidemiological evidece is still icoclusive. The aim of this study was to evaluate the associatio betwee airbore trichloramie (NCl 3 ) levels ad irritative symptoms i swimmig pool employees i order to obtai detailed data regardig dose-respose relatioships ad to idetify the airbore NCl 3 exposure level, if ay, without health effects. A total of 20 idoor swimmig pools i the Emilia Romaga regio of Italy were icluded i the study. Iformatio about the health status of 128 employees was collected usig a self-admiistered questioaire. Exposure to airbore NCl 3 was evaluated i idoor swimmig pools by a modified DPD/KI method. The results of the study evideced a mea value of airbore NCl 3 of 0.65±0.20 mg/m 3 (ragig from 0.20 to 1.02 mg/m 3 ). Both ocular ad upper respiratory symptoms, i particular red eyes, ruy ose, voice loss ad cold symptoms, were declared more frequetly by lifeguards ad traiers whe compared with employees workig i other areas of the facility (office, cafe, ad so o). Pool attedats exposed to airbore NCl 3 levels of 40.5 mg/m 3 experieced higher risks for ruy ose (OR: 2.91; 95% CI: ) red eyes (OR: 3.16; 95% CI: ), voice loss (OR: 3.56; 95% CI: ) ad itchy eyes (OR: 2.23; 95% CI: ) tha other employees. Moreover, red eyes, itchy eyes, ruy ose ad voice loss are related to airbore NCl 3 levels, with strog dose-respose relatioships. I coclusio, this study shows that lifeguards ad traiers experiece ocular ad respiratory irritative symptoms more frequetly tha employees ot exposed. Irritative symptoms become sigificat startig from airbore NCl 3 levels of 40.5 mg/m 3, cofirmig that the WHO-recommeded value ca be cosidered protective i occupatioal exposure to airbore NCl 3 i idoor swimmig pools. Joural of Exposure Sciece ad Evirometal Epidemiology (2013) 23, ; doi: /jes ; published olie 27 Jue 2012 Keywords: swimmig pools; trichloramie i ambiet air; ocular ad respiratory irritative symptoms; lifeguards ad pool attedats INTRODUCTION The hypothesis that attedace at idoor chloriated swimmig pool is a risk factor for irritative ocular ad respiratory symptoms ad brochial asthma is well kow i literature, although epidemiological evidece is still icoclusive, especially with regard to the oset of brochial asthma. 1 The presece of respiratory symptoms ad brochial asthma i people attedig idoor swimmig pools is geerally liked to the evirometal exposure to chloramies, N by-products of pool water chloriatio treatmets, ad i particular to trichloramie (NCl 3 ), which is the most irritat ad volatile compoud amog chloramies Epidemiological studies have bee performed to ivestigate the associatio betwee huma exposure to chemical derivatives of pool water chloriatio ad health complaits, both i swimmers, maily i childre, ad i swimmig pool workers. 1,2,5--13 Regardig occupatioal exposure, acute respiratory symptoms i swimmig pool istructors were foud to be associated with airbore NCl 3 levels, for the first time, by Héry et al. 2 i I the study, swimmig pool istructors declared to have complaits of ocular ad respiratory irritatio startig from a airbore NCl 3 value 40.5 mg/m 3 ; as a cosequece, this value has bee suggested as a comfort limit value. 2 Sice the, ocular ad respiratory symptoms i swimmig pool employees were reported i literature, both i accidetal coditios with acute exposure to chlorie derivatives ad i ormal workig coditios i idoor swimmig pools. 5,9, Studies i Frace, ad more recetly i The Netherlads ad i Italy, clearly evideced that swimmig pool workers, ad i particular lifeguards ad traiers, are at icreased risk of developig ocular ad respiratory irritative symptoms. 5,9,13 The oset of brochial asthma iduced by airbore NCl 3 exposure i pool workers is a more cotroversial aspect. I the Frech study, o associatio betwee a cumulative airbore NCl 3 exposure idex ad occupatioal asthma was foud. 5 Istead, occupatioal asthma attributed to NCl 3 exposure was reported i two lifeguards ad oe swimmig teacher by Thickett et al. 16 i 2001, although the mechaisms of iduced asthma were ot completely explaied. More recetly, a excess risk for respiratory symptoms idicative of asthma was observed i swimmig pool employees i the Netherlads. 9 I the study, asthma-related symptoms such 1 Departmet of Public Health Scieces, Uiversity of Modea ad Reggio Emilia, Via G. Campi, 287, Modea, Italy. Correspodece to: Professor Guglielmia Fatuzzi, Dipartimeto di Scieze di Saità pubblica, Via G. Campi, 287, Modea, Italy. Tel.: þ Fax: þ guglielmia.fatuzzi@uimore.it Received 16 Jauary 2012; accepted 1 May 2012; published olie 27 Jue 2012

2 as cough, phlegm, shortess of breath ad tightess were associated with self-reported evirometal coditios of the employees, but ot with the estimated average airbore NCl 3 levels observed i six idoor swimmig pools. I a previous study o the prevalece of ocular, respiratory ad cutaeous symptoms i idoor swimmig pool workers, we observed a excess risk of asthma oly i employees exposed to high levels of trihalomethaes (THMs) i alveolar air (421 mg/m 3 ); however, the low umber of asthmatic workers ivolved i the study (oly 10 subjects) leads to cautio. 13 Overall, the evaluatio of airbore NCl 3 levels i epidemiological studies is ot frequet ad very few studies have liked respiratory symptoms with actual levels of airbore NCl 3 i swimmig pool atmospheres. The majority of the relevat studies o asthma icidece ad other health effects cosider the pool attedace or the time spet i idoor swimmig pool facilities, the swimmig activities (yes/ot) ad the time of swimmig as airbore NCl 3 exposure idicators, without ay aalytical determiatio of airbore NCl 3 i idoor swimmig pool atmosphere. As a cosequece, few data exist regardig the associatio betwee the airbore NCl 3 levels ad health complaits. The presece of a possible dose-respose relatioship betwee exposure to airbore NCl 3 i idoor swimmig pool atmospheres ad the oset of symptoms must be ivestigated i more detail i order to defie which NCl 3 evirometal levels are resposible for irritative effects i people attedig idoor swimmig pools ad, i particular, i subjects spedig a lot of time ear the pool waters, like lifeguards ad traiers. Studies coducted so far have rarely delved ito this aspect. The aim of this study was to evaluate the associatio betwee airbore NCl 3 levels ad irritative symptoms i swimmig pool employees i order to obtai more detailed data about doserespose relatioships ad to idetify the airbore NCl 3 exposure levels, if ay, without health effects. Aother purpose of this study was to ivestigate about evirometal factors, such as physical ad chemical characteristics of pool water ad ambiet air, which ca ifluece the occurrece of NCl 3 i idoor swimmig pool atmosphere, as iformatio is scarce ad eeds to be more ivestigated. MATERIALS AND METHODS Study Desig As described i a previous study, 20 public idoor swimmig pools located i the Emilia-Romaga regio (Norther Italy) were ivestigated i Iformatio about pool water treatmets ad disifectio procedures was collected durig each samplig sessio ad the umber of swimmers iside the pools was take ito accout. Samplig sessios were carried out durig the witer period whe the exchage idoor/outdoor was ot frequet, usually o Tuesday or Wedesday morig i order to obtai very similar evirometal coditios amog swimmig pools. Subjects workig i idoor swimmig pools ad preset the day of the samplig sessios were asked to participate i the study ad, o a volutary basis, 133 subjects were erolled. All the cotacted employees durig our visit to each swimmig pool agreed to participate i the study ad each participat provided iformed coset: as a cosequece of the o-ivasive character of the study, o ethical approval was required. Questioaires A self-admiistrated questioaire was draw up to record iformatio about health status as well as persoal data ad specific workig activities iside the swimmig pool. The frequecy of self-reported ocular symptoms (red eyes, itchy eyes, eye ifectios, watery eyes), upper respiratory symptoms (asal itch, seezig, cold, ruy ose, blocked ose, voice loss, pharygitis/brochitis, coughig) ad asthma-related symptoms (wheezig, shortess of breath ad dyspea/asthma) was recorded. Possible aswers to questios about symptoms were ever, sometimes ad ofte. Swimmig pool trichloramie ad health i workers Fatuzzi et al Five subjects had filled the questioaire partially ad hece they were excluded from the study. Evirometal Exposure Pool water temperature ad ph, free ad combied chlorie ad evirometal microclimatic parameters (temperature, relative humidity ad vetilatio rate) were evaluated. Temperature, ph, free ad combied chlorie i pool water samples were aalyzed at three differet poits ear the edge of the pool; the mea value was cosidered represetative of the pool water durig the samplig sessio. Microclimate parameters were collected withi few meters at the edge of the pool durig a 2-h samplig period. Airbore NCl 3 levels were evaluated at a height of 100 cm, 3 m from the edge of the pool by a active air samplig, at a flow rate of 1000 ml/mi for 100 mi. Oly oe samplig sessio was performed i each ivestigated swimmig pool. Aalytical Methods Water temperature ad ph were detected o site with a thermometer ad a portable ph meter; free ad combied chlorie were evaluated by the colorimetric DPD/KI method, accordig to EN ISO :2000, usig a photometer (PC Compact--Aqualytic). 17 Air temperature, relative humidity ad vetilatio were measured by a multi-data logger (BABUC A-LSI, Lastem) equipped with a software (IfoGAP) aimed to calculate microclimate idices for moderate eviromets. Airbore NCl 3 levels were ivestigated accordig to the aalytical method recetly suggested by Predieri ad Giacobazzi. 18 Briefly, the method is based o the etrapmet of airbore NCl 3 i two impigers through a active ambiet air samplig. The impigers (oe for aalysis ad oe as a blak) are filled with a water solutio of diethylp-pheyleediamie ad potassium iodide. The solutio is the aalyzed as combied chlorie, accordig to the DPD/KI colorimetric method. Airbore NCl 3 value was the differece betwee the readig values from the two impiger solutios ad, after stoichiometric coversio, the observed value is expressed as mg/m Statistical Methods Statistical aalyses were performed usig SPSS (Statistical Package for Social Scieces; 1986; Chicago, IL, USA) versio 16.0 for Widows. Evirometal data were preseted as arithmetic mea±sd. Correlatio coefficiets ad ANOVA test were calculated. The characteristics of exposed ad ot exposed workers were compared accordig to the X 2 test, with probabilities of o0.05 cosidered statistically sigificat. Associatios betwee self-reported health symptoms ad occupatioal airbore NCl 3 exposure were evaluated usig a multivariate logistic regressio, adjusted for cofoudig variables such as sex, age ad smokig habits. The odds ratios (ORs) ad their 95% cofidece itervals (95% CIs) were computed. RESULTS The descriptive characteristics of evirometal data of the 20 ivestigated idoor swimmig pools are show i Table 1. Physical ad chemical parameters i pool water ad ambiet air samples are also reported, takig ito accout the differet ature of chlorie compouds used for the disifectio treatmets. Chloriatio was the oly disifectio procedure adopted i all the ivestigated swimmig pools. Pool water temperature ad ph values raged from 26 1C to 30 1C ad from 6.8 to 7.6, respectively, with very low variability. Free chlorie i pool waters evideced a mea value of 1.31±0.32 mg/l, ad i 5 swimmig pools free chlorie levels were higher tha the Italia limit value (1.7 mg/l). Also, combied chlorie showed a high mea value (0.51±0.21 mg/l): i 15 swimmig pools (75%), a combied chlorie value higher tha the 89 & 2013 Nature America, Ic. Joural of Exposure Sciece ad Evirometal Epidemiology (2013),

3 90 Table 1. Swimmig pool trichloramie ad health i workers Fatuzzi et al Descriptive characteristics of 20 idoor swimmig pools. Total idoor swimmig pools ( ¼ 20) Disifectio treatmets Sodium hypochlorite ( ¼ 7) Trichloroisocyauric acid ( ¼ 8) Sodium hypochlorite ad trichloroisocyauric acid ( ¼ 5) Mea±SD Mi--Max Mea±SD Mi--Max Mea±SD Mi--Max Mea±SD Mi--Max Pool water Temperature (1C) 28.4± ± ± ± ph 7.3± ± ± ± Free chlorie (mg/l Cl 2 ) 1.3± ± ± ± Combied chlorie (mg/l Cl 2 ) 0.5± ± ± ± Ambiet air Temperature (1C) 26.8 ± ± ± ± Relative humidity (%) 63.7± ± ± ± Vetilatio rate (m/s) 0.10± ± ± ± Trichloramie (mg/m 3 ) 0.65± ± ± ± Data are show as arithmetic mea±sd, miimum ad maximum. Italia limit values (r0.4 mg/l) was detected. Whe chloriatio treatmets were take ito accout, o sigificat differece i physical ad chemical parameter (water temperature, ph, free ad combied chlorie levels) mea values was observed. Ambiet air temperature, relative humidity ad vetilatio values agreed to the Italia limit values, although air temperature values were sometimes lower tha the recommeded oes. Airbore NCl 3 levels showed a mea value of 0.65±0.20 mg/m 3, ragig from 0.20 to 1.02 mg/m 3 ad the highest value of NCl 3 i ambiet air was observed i a idoor swimmig pool that used both sodium hypochlorite ad trichloroisocyauric acid i the disifectio treatmet. More tha 75% of the idoor swimmig pools showed NCl 3 levels 40.5 mg/m 3 (the recommeded provisioal value, suggested by WHO guidelies) ad o sigificat differece was evideced i airbore NCl 3 levels due to chloriatio procedure. Airbore NCl 3 levels r0.5 mg/m 3 were observed i four swimmig pools, whereas airbore NCl 3 levels ragig from 0.5 to 0.6 mg/m 3 were evideced i four swimmig pools, with values ragig from 0.6 to 0.7 mg/m 3 i three swimmig pools, from 0.7 to 0.8 mg/m 3 i three swimmig pools ad, fially, airbore NCl 3 levels 40.8 mg/m 3 were observed i six swimmig pools. Airbore NCl 3 levels were sigificatly correlated with combied chlorie i pool water (r ¼ 0.46; P ¼ 0.037) ad with the umber of swimmers iside the pool durig the samplig sessios (r ¼ 0.265; P ¼ 0.002). Temperature ad ph i pool waters ad microclimate parameters (temperature, relative humidity ad vetilatio rates) were ot associated with airbore NCl 3 cocetratios i swimmig pool atmospheres. Descriptive characteristics of the employees, accordig to their workig activity, are show i Table 2. Amog subjects ivolved i the study ( ¼ 128), 81 were lifeguards or traiers ad 47 subjects were occupied as receptioists, maager ad office workers, techicias ad barteders; lifeguards ad traiers were slightly youger ad more frequetly o-smokers. Approximately 30% of the employees (both lifeguards ad traiers ad referet group) had a duratio of occupatioal activity at idoor swimmig pools of more tha 10 years, ad more tha 50% of the subjects had atteded idoor swimmig pools for more tha 20 years, maily as swimmers. Regardig the frequecy of exposure, employees had mea weekly work total of 25.2±14.1 h, correspodig to 4.7±2.4 h/day, showig a wide but similar variability i both groups. Table 2. Descriptive characteristics of swimmig pool workers ( ¼ 128) by sex, age, smokig habits ad duratio of employmet. Variables Lifeguards ad traiers ( ¼ 81) Other employees ( ¼ 47) % % P-value Geder Male Female NS Age (years) a o Z NS Smokig habits Smoker Ex-smoker Never smoked NS Duratio of occupatioal activity at idoor swimmig pools (years) NS a Data available for oly 126 subjects. The prevalece of ocular ad respiratory symptoms was calculated i subgroups of employees, accordig to their airbore NCl 3 exposure: six levels of exposure have bee cosidered. Subjects workig as receptioists, maager ad office workers, techicias ad barteders were cosidered as the referet group, as they spet their workig activities geerally outside the water pool eviromets, although withi the swimmig pool facilities. Five levels of exposure to airbore NCl 3 were defied for traiers ad lifeguards: level 1 (airbore NCl 3 values r0.5 mg/m 3 ), level 2 (airbore NCl 3 values 40.5 mg/m 3 ), level 3 (airbore NCl 3 values 40.6 mg/m 3 ), level 4 (airbore NCl 3 values 40.7 mg/m 3 ) ad, fially, level 5 (airbore NCl 3 values 40.8 mg/m 3 ). These levels were idetified i order to evidece the lowest value of airbore NCl 3 without referred symptoms. Joural of Exposure Sciece ad Evirometal Epidemiology (2013), & 2013 Nature America, Ic.

4 Regardig ocular symptoms (Table 3), i referet group the prevalece of both red ad itchy eyes was 34%, whereas the prevalece of watery eyes ad eye ifectio was 19% ad 4%, respectively. Whe differet levels of NCl 3 exposure were cosidered, a geeral icrease i the prevalece of ocular symptoms was observed. The prevalece of red eyes raged from 30% i level 1 to 62% (level 2), 68% (level 3), 72% (level 4) ad 67% (level 5): the risk of excess of red eyes became sigificat from level 2 of exposure (40.5 mg/m 3 ) ad icreased accordig to the icreased levels of exposure. Also, itchy eye prevalece was frequet i lifeguards ad traiers: whe airbore NCl 3 exposure was 40.5 mg/m 3 (level 2), the prevalece of itchy eyes raged from 54% to 57% ad the risk icreased ad was statistically sigificat. O the cotrary, o sigificat icreased risks of eye ifectios ad watery eyes were observed i high levels of airbore NCl 3 exposure. I Tables 4 ad 5, the associatios betwee respiratory symptoms ad airbore NCl 3 levels were reported. Ruy ose, blocked ose, cold ad voice loss showed, i referet subjects, prevalece values of 19%, 38%, 57% ad 25%, respectively. Sigificat icreased risks of ruy ose were observed i lifeguard ad traiers startig from level 2 (OR: 2.91; CI: ); i level 5, the risk was 4.22 ( ) ad the ruy ose prevalece reached 50%. A sigificat risk of blocked ose was observed oly i subjects exposed to level 5 (airbore NCl 3 levels 40.8 mg/m 3 ); the prevalece of blocked ose i level 5 was 63% vs 38% i cotrol subjects. Similar results were observed for cold that showed a sigificat icreased risk oly i high exposure coditios (levels 4 ad 5), showig high prevalece value (480% i both levels) compared with referece group (57%). Pool attedats ad traiers startig from airbore NCl 3 levels of 40.5 mg/m 3 (level 2) also experieced higher risks of voice loss (OR: 3.6; 95% CI: ) tha other employees. Other irritat symptoms such as seezig, asal itch ad brochitis were cosidered but they did ot show evidece of ay associatios with airbore NCl 3 levels (data ot show). Regardig asthma ad other related symptoms such as coughig, wheezig ad shortess of breath, oly 10 subjects (7.8%) had brochial asthma, whereas coughig (37.5%), wheezig (9.4%) ad shortess of breath (17.2%) were more frequetly reported. No sigificat risks of asthma ad other respiratory symptoms were observed i lifeguards ad traiers compared with the other employees. Swimmig pool trichloramie ad health i workers Fatuzzi et al Moreover, other exposure categories were take ito accout i statistical aalyses such as referece, low (o0.50 mg/m 3 ), itermediate (Z0.50--o0.7 mg/m 3 ) ad high exposure (Z0.70 mg/m 3 ); however, the results showed evidece of the same previously described tred. DISCUSSION I this study, the prevalece of self-declared ocular ad respiratory symptoms i swimmig pool employees was evaluated accordig to airbore NCl 3 exposure i swimmig pools. I geeral, lifeguards ad traiers experieced irritative ocular ad respiratory symptoms, ad these results cofirm other epidemiological studies. 2,5,9,13,19 Moreover, the prevalece of irritative symptoms i lifeguards ad traiers was higher tha the prevalece observed i employees workig as receptioists, office workers, techicias ad barteders, cosidered as referet group. These subjects, who spet their activity out of the pool eviromet, although i idoor swimmig pool facilities, ca be cosidered ot exposed to disifectio by products as reported i our previous study. 13 Ocular ad upper respiratory symptoms were foud closely associated with the levels of airbore NCl 3 i swimmig pools: sigificat dose-depedet icreases i the prevalece of red eyes, itchy eyes, ruy ose ad voice loss were observed i lifeguards ad traiers exposed to airbore NCl 3 levels of 40.5 mg/m 3. I these subjects, whe exposure was particularly high (NCl 3 levels 40.7 mg/m 3 ), the risks of developig irritative ocular ad upper respiratory symptoms were 3--5 times higher tha i the referet group. Our results are i cocordace with the study of Héry et al., 2 ad cofirm that a airbore NCl 3 level of o0.5 mg/m 3, as suggested by Héry et al. 2 i 1995 ad actually recommeded i WHO guidelies, ca be cosidered protective for occupatioally exposed subjects. 2,20 Of course, efforts should be made to obtai the lowest NCl 3 evirometal cocetratios i order to protect susceptible subjects ad pool workers, ad i particular atopic subjects who ca also experiece irritative symptoms i low levels of airbore NCl 3 exposure. Moreover, childre ad elite swimmers are cosidered at a icreased risk of developig a atopic or asthmatic coditio as they atted these eviromets for log periods of time. For these reasos, a airbore NCl 3 value of o0.5 mg/m 3 is to be adopted as exposure limit i EU coutries. 91 Table 3. Risks of ocular symptoms (odds ratios ad 95% CI) i referet group (ot exposed) ad i lifeguards ad traiers exposed to differet levels of airbore NCl 3 i 20 swimmig pool facilities. Airbore NCl 3 levels Total subjects Ocular symptoms Red eyes Itchy eyes Watery eyes Eye ifectios Referet group Level ( ) ( ) ( ) (r0.5 mg/m 3 ) Level ( ) ( ) ( ) ( ) (40.5 mg/m 3 ) Level ( ) ( ) ( ) ( ) (40.6 mg/m 3 ) Level ( ) ( ) ( ) ( ) (40.7 mg/m 3 ) Level 5 (40.8 mg/m 3 ) ( ) ( ) ( ) ( ) Data are preseted as odds ratios (95% cofidece iterval) ad are adjusted for age, sex ad smokig habits. & 2013 Nature America, Ic. Joural of Exposure Sciece ad Evirometal Epidemiology (2013),

5 Swimmig pool trichloramie ad health i workers Fatuzzi et al 92 Table 4. Risks of upper respiratory symptoms (odds ratios ad 95% CI) i referet group (ot exposed) ad i lifeguards ad traiers exposed to differet levels of airbore NCl 3 i 20 swimmig pool facilities. NCl 3 levels Total subjects Upper respiratory symptoms Ruy ose Blocked ose Cold Voice loss Referet group Level ( ) ( ) ( ) ( ) (r0.5 mg/m 3 ) Level ( ) ( ) ( ) ( ) (40.5 mg/m 3 ) Level ( ) ( ) ( ) ( ) (40.6 mg/m 3 ) Level ( ) ( ) ( ) ( ) (40.7 mg/m 3 ) Level 5 (40.8 mg/m 3 ) ( ) ( ) ( ) ( ) Data are preseted as odds ratios (95% cofidece iterval) ad are adjusted for age, sex ad smokig habits. Table 5. Risks of respiratory ad asthma-related symptoms (odds ratios ad 95% CI) i referet group (ot exposed) ad i lifeguards ad traiers exposed to differet levels of airbore NCl 3 i 20 swimmig pool facilities. NCl 3 levels Total subjects Asthma-related symptoms Cough Wheeze Shortess of breath Dyspea/asthma Referet group Level ( ) ( ) (r0.5 mg/m 3 ) Level ( ) ( ) ( ) ( ) (40.5 mg/m 3 ) Level ( ) ( ) ( ) ( ) (40.6 mg/m 3 ) Level ( ) ( ) ( ) ( ) (40.7 mg/m 3 ) Level 5 (40.8 mg/m 3 ) ( ) ( ) ( ) ( ) Data are preseted as odds ratios (95% cofidece iterval) ad are adjusted for age, sex ad smokig habits. Recetly, a icreased risk of irritative symptoms has bee observed i up to a level of mg/m 3 of airbore NCl 3 ad the authors strogly suggest fixig the NCl 3 occupatioal exposure limit at 0.3 mg/m I the preset study, we did ot show evidece of ay associatio betwee self-declared brochial asthma ad airbore NCl 3 levels; the icreased risk of a asthmatic coditio i lifeguards ad traiers that we foud related to THM exposure i a previous study was ot cofirmed i the preset study, whe airbore NCl 3 levels were take ito accout. A possible explaatio for these coflictual fidigs could be both the low umber of asthmatic subjects erolled i the study ad the differet exposure assessmet procedures adopted i the two differet studies. The THM determiatio i alveolar air samples, adopted i the previous oe, provides iformatio about the absorbed dose at idividual level, whereas the airbore NCl 3 evirometal moitorig refers to oly a overall coditio of exposure. Other studies have to be performed i a large umber of occupatioally exposed subjects i order to deepe our uderstadig of this aspect. Regardig evirometal characteristics, high levels of both free ad combied chlorie i pool waters were observed; oly 25% of the ivestigated swimmig pools showed combied chlorie levels of r0.4 mg/l, which is the Italia limit value. The overuse of chlorie i pool water maagemet may be the resposible factor for the high levels of airbore NCl 3 evideced i the swimmig pool atmospheres; i our study, more tha 50% of the idoor swimmig pools showed airbore NCl 3 levels higher tha the recommeded provisioal value of 0.5 mg/m 3, as suggested i WHO guidelies. The observed airbore NCl 3 mea value is slightly higher tha values reported elsewhere. 2,5,9,14 I this study, physical ad microclimate parameters did ot seem to ifluece airbore NCl 3 levels i idoor swimmig pool atmospheres. The oly evirometally sigificat correlatio was Joural of Exposure Sciece ad Evirometal Epidemiology (2013), & 2013 Nature America, Ic.

6 observed betwee combie chlorie i pool waters ad the umber of swimmers iside the pools, as also reported by other authors. 5,9 As iformatio about health status was collected usig a selfadmiistered questioaire, with o medical cotrol, the recall bias may affect the quality of our data; thus, misclassificatios may have occurred. Regardig asthma-related symptoms, aother limitatio could be the low umber of employees erolled i the study with cosequet low umber of employees with asthma; this fact probably plays a role i the statistical aalysis. Moreover, o questio about the oset of asthma symptoms (before or after the begiig of the work activity) was icluded i the questioaire ad the reverse causatio or the healthy worker effect caot be excluded. However, i our sample, 7 lifeguards ad traiers ad 3 subjects of the referet group had asthma, ad the prevalece values were 8.5% ad 6.4%, respectively. The prevalece of asthma i pool workers was slightly higher tha the prevalece value (6.6%) reported for the Italia geeral populatio. 21 As more tha 50% of the workers declared to atted idoor swimmig pools sice their childhood as swimmers, maily as competitive swimmers, we could ot exclude that some asthmatic subjects became lifeguards or traiers. Prospective studies are eeded i order to approach this problem. A positive aspect of the study is that o selectio bias is preset as all the cotacted employees durig our visit to each swimmig pool agreed to participate i the study. CONCLUSION I coclusio, this study cofirms that idoor swimmig pool lifeguards ad traiers experiece irritative symptoms i ocular ad upper respiratory systems more frequetly tha employees who are ot exposed. Red eyes, itchy eyes, ruy ose ad voice loss are related to airbore NCl 3 levels, with strog dose-respose relatioships. Health symptoms become sigificat startig from airbore NCl 3 levels of 40.5 mg/m 3. Hece, the WHO-recommeded value i idoor swimmig pools ca be cosidered protective i occupatioal exposure. No sigificat associatio betwee asthma ad airbore NCl 3 levels was observed; however, these results eed to be ivestigated i detail i a large umber of occupatioally exposed subjects. CONFLICT OF INTEREST The authors declare o coflict of iterest. ACKNOWLEDGEMENTS This study was supported by a grat from the Italia Miistry of Work (o. 1299, 2006). We are also grateful to the tow coucilors ad all of the staff at the participatig swimmig pools for their support ad collaboratio. REFERENCES 1 Weisel C.P., Richardso S.D., Nemery B., Aggazzotti G., Baraldi E., ad Blatchley III E.R., et al. Childhood asthma ad evirometal exposures at swimmig pools: state of the sciece ad research recommedatios. Eviro Health Perspect 2009: 117: Swimmig pool trichloramie ad health i workers Fatuzzi et al 2 Héry M., Hecht G., Gedre J.C., Hubert G., ad Rebuffaud I. Exposure to chloramies i the atmosphere of idoor swimmig pools. A Occup Hyg 1995: 39: Li J., ad Blatchley III E.R. Volatile disifectio by-product formatio resultig from chloriatio of orgaic-itroge precursors i swimmig pools. Eviro Sci Techol 2007: 41: Weaver W.A., Li J., We Y., Johsto J., Blatchley M.R., ad Blatchley III E.R. Volatile disifectio by-product aalysis from chloriated idoor swimmig pools. Water Res 2009: 43: Massi N., Bohadaa A.B., Wild P., Hery M., Toamai J.P., ad Hubert G. Respiratory symptoms ad brochial resposiveess i lifeguards exposed to itroge trichloride i idoor swimmig pools. Occup Eviro Med 1998: 5: Lèvesque B., Duchese J.F., Gigras S., Lavoie R., Prud Homme D., Berard E., Boulet J.F., ad Erst P. The determiats of prevalece of health complaits amog youg competitive swimmers. It Arch Occup Eviro Health 2006: 80: Berard A., Carboelle S., Michel O., Higuet S., De Burbure C., Buchet J., Hermas C., Dumot X., ad Doyle I. Lug hyperpermeability ad asthma prevalece i schoolchildre: uexpected associatios with the attedace at idoor chloriated swimmig pools. Occup Eviro Med 2003: 60: Berard A., Carboelle S., de Burbure C., Michel O., ad Nickmilder M. Chloriated pool attedace, atopy, ad the risk of asthma durig childhood. Eviro Health Perspect 2006: 114: Jacobs J.H., Spaa S., va Rooy G.B., Meliefste C., Zaat V.A., Rooyackers J.M., ad Heederik D. Exposure to trichloramie ad respiratory symptoms i idoor swimmig pool workers. Eur Respir J 2007: 29: Goodma M., ad Hays S. Asthma ad swimmig: a meta-aalysis. J Asthma 2008: 45: Fot-Ribera L., Kogevias M., Zock J.P., Nieuwehuijse M.J., Heederik D., ad Villaueva C.M. Swimmig pool attedace ad risk of asthma ad allergic symptoms i childre. Eur Respir J 2009: 34: Fot-Ribera L., Villaueva C.M., Nieuwehuijse M.J., Zock J.P., Kogevias M., ad Hederso J. Swimmig pool attedace, asthma, allergies ad lug fuctio i the ALSPAC cohort. Am J Respir Crit Care Med 2011: 183: Fatuzzi G., Righi E., Predieri G., Giacobazzi P., Mastroiai K., ad Aggazzotti G. Prevalece of ocular, respiratory ad cutaeous symptoms i idoor swimmig pool workers ad exposure to disifectio by-products (DBPs). It J Eviro Res Public Health 2010: 7(4): Che L., Dag B., ad Mueller C., et al. Health Hazard Evaluatio Report: Ivestigatio of Employee Symptoms at a Idoor Waterpark. US Departmet of Health ad Huma Services, CDC, Natioal Istitute for Occupatioal Safety ad Health, Ciciati, OH, Report o. HETA Ceters for Disease Cotrol ad Prevetio (CDC). Respiratory ad ocular symptoms amog employees of a hotel idoor waterpark resort---ohio, MMWR Morb Mortal Weekly Rep 2009: 58(4): Thickett K.M., McCoach J.S., Gerber J.M., Sadhra S., ad Burge P.S. Occupatioal asthma caused by chloramies i idoor swimmig-pool air. Eur Respir J 2002: 19: Europea stadard EN ISO Water quality - Determiatio of free chlorie ad total chlorie - Part 2: Colorimetric method usig N, N-diethyl-1,4- pheyleediamie for routie cotrol purposes, Predieri G., ad Giacobazzi P. Determiatio of itroge trichloride (NCl 3 ) levels i the air of idoor chloriated swimmig pools: a impiger method proposal. It J Ev Aal Chem 2012: 92: Parrat J., Dozé G., Iseli C., Perret D., Tomicic C., ad Schek O. Assessmet of occupatioal ad public exposure to trichloramie i Swiss idoor swimmig pools: a proposal for a occupatioal exposure limit. A Occup Hyg 2012: 56(3): World Health Orgaizatio. Guidelies for Safe Recreatioal-Water Eviromets, Vol. 2, Swimmig Pools, Spas ad Similar Recreatioal-Water Eviromets. World Health Orgaizatio, Geeva, de Marco R., Cappa V., Accordii S., Rava M., Atoicelli L., Bortolami O., Braggio M., Bugiai M., Casali L., Cazzoletti L., Cerveri I., Fois A.G., Girardi P., Locatelli F., Marco A., Marioi A., Paico M.G., Piria P., Villai S., Zaoli M.E., ad Verlato G. for the GEIRD study group. Treds i the prevalece of asthma ad allergic rhiitis i Italy betwee 1991 ad Eur Respir J 2012: 39(4): & 2013 Nature America, Ic. Joural of Exposure Sciece ad Evirometal Epidemiology (2013),

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