Seasonal dynamics of water and air chemistry in an indoor chlorinated swimming pool

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

Available online at www.sciencedirect.com

ScienceDirect journal homepage: www.elsevier.com/locate/watres

Seasonal dynamics of water and air chemistry in an indoor chlorinated swimming pool Mehrnaz Zare Afifi a, Ernest R. Blatchley IIIa,b,* a b

Lyles School of Civil Engineering, Purdue University, West Lafayette, IN 47907, USA Division of Environmental & Ecological Engineering, Purdue University, West Lafayette, IN 47907, USA

article info

abstract

Article history:

Although swimming is known to be beneficial in terms of cardiovascular health, as well as

Received 10 July 2014

for some forms of rehabilitation, swimming is also known to present risks to human

Received in revised form

health, largely in the form of exposure to microbial pathogens and disinfection byproducts

15 October 2014

(DBPs). Relatively little information is available in the literature to characterize the sea-

Accepted 20 October 2014

sonal dynamics of air and water chemistry in indoor chlorinated swimming pools. To

Available online 29 October 2014

address this issue, water samples were collected five days per week from an indoor chlorinated swimming pool facility at a high school during the academic year and once per

Keywords:

week during summer over a fourteen-month period. The samples were analyzed for free

Chlorination

and combined chlorine, urea, volatile DBPs, pH, temperature and total alkalinity. Mem-

Volatile disinfection by-products

brane Introduction Mass Spectrometry (MIMS) was used to identify and measure the

(DBPs)

concentrations of eleven aqueous-phase volatile DBPs. Variability in the concentrations of

Swimming

these DBPs was observed. Factors that influenced variability included bather loading and mixing by swimmers. These compounds have the ability to adversely affect water and air quality and human health. A large fraction of the existing literature regarding swimming pool air quality has focused on trichloramine (NCl3). For this work, gas-phase NCl3 was analyzed by an air sparging-DPD/KI method. The results showed that gas-phase NCl3 concentration is influenced by bather loading and liquid-phase NCl3 concentration. Urea is the dominant organic-N compound in human urine and sweat, and is known to be an important precursor for producing NCl3 in swimming pools. Results of daily measurements of urea indicated a link between bather load and urea concentration in the pool. © 2014 Elsevier Ltd. All rights reserved.

1.

Introduction

Swimming in pools is a common recreational activity worldwide and is believed to provide health and fitness benefits. Chlorination is the predominant disinfection method applied in swimming pools due to its cost-effectiveness, ease of application, and ability to inactivate a wide variety of pathogenic microorganisms. Chlorination also promotes oxidation

of some dissolved organic compounds (AWWA, 1999). However, it is also known to produce disinfection by-products (DBPs), mostly via reactions between free chlorine (defined as the sum of the concentrations HOCl, OCl
, and Cl2) and natural organic matter in source water, as well as inputs from bathers through sweat, urine, hair, skin particles, and personal care products (Kristensen et al., 2009; Judd and Black, 2000). Both sweat and urine contain important precursors to the formation of volatile DBPs that are introduced to

* Corresponding author. Lyles School of Civil Engineering, Purdue University, West Lafayette, IN 47907, USA. E-mail address: [email protected] (E.R. Blatchley). http://dx.doi.org/10.1016/j.watres.2014.10.037 0043-1354/© 2014 Elsevier Ltd. All rights reserved.

772

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

swimming pools by humans (Weaver et al., 2009; Li and Blatchley, 2007). Urine introduction to pools has been reported to be 25e77.5 mL of per bather (Gunkel and Jessen, 1986; Erdinger et al., 1997; Weng et al., 2011). The amount of sweat per bather is highly variable and depends on the individual level of physical activity and hygiene habits prior to entering the pool. In the United States, the recommended free available chlorine concentration range in pools is 1e5 mg/L as Cl2, with an ideal range between 2 and 4 mg/L as Cl2 (NSPF, 2010). The preferred pH range in swimming pools is 7.4e7.6 (NSPF, 2010). However, in European countries the recommended free chlorine range in the swimming pools is often lower. For example, in Germany the concentration of free chlorine must be kept in the range of 0.3e0.6 mg/L in pool water at a pH range between 6.5 and 7.6 (Zwiener et al., 2007). Most studies regarding health effects of DBPs have focused on drinking water exposure; however, in some respects swimming may present a greater risk of exposure to DBPs as uptake may occur through three different exposure paths: ingestion, inhalation, and dermal absorption. Moreover, the concentrations of DBPs in pool water often exceed those of drinking water. For some DBPs (e.g., CHCl3 and halophenols), the dominant pathway for uptake during swimming is dermal absorption due to contact of large surface area of skin with water (Lindstrom et al., 1997; Weisel and Shepard, 1994; Xiao et al., 2012). For other compounds (e.g., NCl3), inhalation has been identified as an important route of exposure (Zwiener et al., 2007). These pathways for human exposure are potentially problematic due to the toxic nature of some DBPs. Dermal uptake is particularly important because it provides direct access to the bloodstream, without going through the digestive system. Therefore, mutagenicity, genotoxicity, and cytotoxicity responses to swimming pool water can be greater than with tap water sources (Richardson et al., 2012). More than 600 DBPs have been identified in chlorinated waters, and many of them are mutagenic or carcinogenic (Richardson et al., 2012). To date, the DBPs identified in swimming pools include trihalomethanes (THMs), iodoTHMs, haloacetates, haloacetic acids, haloacids, halodiacids, haloaldehydes, halonitriles, haloketones, halopyrroles, halomethanes, halonitromethanes, bromate, haloamides, haloalcohols, nitrosamines, combined chlorine, halofuranones (Richardson et al., 2012), halophenols (Xiao et al., 2012) and halobenzoquinones (HBQs) (Wang et al., 2013). In indoor chlorinated swimming pool facilities, air and water qualities are both relevant issues with respect to human health. Li and Blatchley (2007) identified eleven volatile DBPs that are formed in chlorinated swimming pools including: three inorganic chloramines, four THMs, cyanogen chloride, cyanogen bromide, dichloroacetonitrile, and dichloromethylamine. Acute and chronic human health problems that have been associated with exposure to these DBPs in swimming pools include: promotion of asthma (Bernard et al., 2003, 2007); increased incidence of rhinitis and hay fever (Bougault et al., 2010; Bernard et al., 2009); as well as skin (contact dermatitis) and eye irritation (Fantuzzi et al., 2010; Safranek et al., 2007). DBP exposure in swimming pools has also been associated with an increased risk of bladder cancer (Villanueva et al., 2007).

Therefore, it is important to understand the chemistry and physics that govern the formation, transfer, and decay of DBPs in pools; however, their behavior is complicated by competing reactions and transport phenomena, as well as a general lack of research for some of these DBPs. THM formation in pools is believed to originate from reactions between free chlorine with organic precursors such as humic substances, skin particles, hair, lotions, and cosmetics (Kim et al., 2002). Aggazzotti et al. (1990, 1993, 1995, 1998) performed a series of studies in Italy and found correlations between chloroform concentrations in air and water and the number of swimmers, chloroform concentration in water, free and combined residual chlorine and water pH, but these were generally only weak to moderate correlations. Reported values of the concentration of chloroform have ranged from 33 to 140 mg/L. Measurements of the concentration of other THMs in water and in air in swimming pools have also been reported (see SI-1). In general, chloroform is the dominant THM (by mass) in swimming pools. Chloroform (CHCl3) is a highly volatile compound that can be inhaled and also readily absorbed via dermal uptake (Lindstrom et al., 1997). The presence of chloroform in the atmosphere of indoor swimming pools has been reported by several authors (WHO, 2006; Faust, 1993; Aggazzotti et al., 1998; Matthiessen and Jentsch, 1999; Lahl et al., 1981; L'evesque et al., 2000) with reported gas-phase concentrations ranging from 1.7 to 1630 mg/m3. Some of the factors that have been reported to influence the chloroform concentration in air in indoor swimming pool facilities include: ventilation rate, bather loading, and free chlorine concentration (Aggazzotti et al., 1998; Chu and Nieuwenhuijsen 2002). According to the International Agency for Research on Cancer, chloroform has been classified as a 2B (possible carcinogen); therefore, human exposure related to THMs in indoor swimming pools is an issue of concern (Aggazzotti et al., 1998). With respect to chloroform exposure, Lindstrom et al. (1997) estimated that 80% of uptake for swimmers is via dermal absorption. However, Erdinger et al. (2004) performed a study to clarify the uptake pathway of chloroform into the human body. Their data indicated that inhalation was the most important pathway, and that uptake over the skin is significantly less. According to the Erdinger et al. (2004) study, chloroform concentration in blood is correlated to air concentration of chloroform and is not linked directly to chloroform concentrations in water. However, the rate of inhalation depends on the intensity of the exercise Chu and Nieuwenhuijsen 2002; Aggazotti et al., 1995). Dichloracetonitrile (DCAN) and other halonitriles can be produced from the chlorination of free amino acids, heterocyclic nitrogen in nucleic acids, proteinaceous materials, and combined amino acids bound to humic structures (Lee et al., 2007; Li and Blatchley, 2007). Previous research has indicated that DCAN will undergo hydrolysis in aqueous solution; the rate of DCAN decay is enhanced in the presence of free chlorine and at high pH (Bieber and Trehy, 1983; Reckhow et al., 2001). DCAN toxicity was investigated after McKinney et al. (1976) identified this compound as the unique ingredient in tap water suspected of causing reduced fertility and decreases in litter size in a colony of laboratory rodents (Smith et al.,

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

1989). The concentration of DCAN is typically in the ppb range in drinking water (Periera et al., 1985; Osgood and Sterling, 1991). It is possible that over a lifetime of chronic exposure, the effects of exposure to these compounds on human health may be significant (Osgood and Sterling, 1991). Muellner et al. (2007) indicated that DCAN is almost 300 times more cytotoxic than its haloacetic acid analogue (dichloroacetic acid (DCAA)). The World Health Organization (1995), based on the additional cancer risk 10
5, has set qualitative target levels of 90 mg/L for DCAN in drinking water. Several organic-N compounds have been identified as cyanogen halide (CNX) precursors, including glycine, serine, threonine, and uric acid (Shang et al., 2000; Li and Blatchley, 2007; Lian et al., 2014). Among the amino acids, glycine appears to have the greatest potential to form cyanogen chloride (Na and Olson, 2006). Free chlorine participates in the formation of CNX compounds and in their decay (Na and Olson, 2004). As such, CNX compounds will exist as intermediates in most pool settings. In 1991, CNCl was included on the USEPA Drinking Water Priority list. The WHO (2004) has recommended that a maximum of 70 mg/L (as cyanide) be used as a guideline for total cyanogen compounds in drinking water. In indoor pools, CNCl appears to represent a compound that could adversely affect the health of swimmers or swimming pool employees. It has been reported that CNCl can cause irritation of skin, eyes, and nasal system (NIOSH, 2003). CNCl is harmful to several vital organs including the heart, lungs, and nervous system. To date, no measurements of gas-phase CNCl have been reported for chlorinated pools. However, as reported by the National Institute for Occupational Safety and Health (NIOSH), CNCl is highly toxic. NIOSH has suggested an occupational exposure limit of 0.6 mg/m3 for gas-phase CNCl (NIOSH, 2003). Gas-phase CNCl concentrations of 2.5 mg/m3 and 120 mg/m3 have been reported to cause irritation and death, respectively in humans (WHO, 2009). Weaver et al. (2009) measured liquid-phase CNCl concentration in several pools and found concentrations that ranged from 1 to 170 mg/L. The American Conference of Governmental Industrial Hygienists (ACGIH) aqueous Threshold Limit Value (TLV) for cyanogen chloride (CNCl) is 0.3 mg/L in the liquid phase and 0.75 mg/m3 in the gas phase (OSHA, 1992; NIOSH, 2003). Formation of inorganic chloramines (monochloramine, dichloramine, trichloramine) in chlorinated/chloraminated waters has been studied extensively. Jafvert and Valentine (1992) assembled a comprehensive summary of these reactions and their kinetics. Ammonia (NH3) will react with free available chlorine in swimming pools. These reactions are dependent on the initial chlorine to nitrogen (Cl:N) ratio, pH, temperature, and time. However, NH3 is generally present at low concentrations in most pools. Pathways for formation of NCl3 and the other inorganic chloramines in pools have been identified from urea, creatinine, and several amino acids (Li and Blatchley, 2007; Blatchley and Cheng, 2010). A large fraction of research regarding swimming pool air quality has focused on trichloramine (NCl3) exposure. NCl3 has a high Henry's law constant, so it has relatively high potential to escape from liquid to gas phase. NCl3 causes eye, skin, and respiratory tract irritation, has been associated with acute lung injuries, and has a suspected association to early-aged asthma (Hery et al., 1995; Massin et al., 1998; Bernard et al.,

773

2003; Jacobs et al., 2007; Dang et al., 2010). Hery et al. (1995) reported complaints of eye and throat irritation among swimmers at trichloramine concentrations higher than 0.5 mg/m3 in the pool air. Gas-phase NCl3 concentration is likely to be influenced by liquid-phase NCl3 concentration, temperature, air circulation (as governed by heating, ventilation, and air conditioning (HVAC) system design and operation), number of swimmers and transport behavior at the liquid:gas interface (Bessonneau et al., 2011; Schmalz et al., 2011; Weng et al., 2011). Previous studies have shown positive correlation between irritation symptoms among swimmers and patrons and high gas-phase NCl3 concentration at indoor pool facilities (Bowen et al., 2007; Kaydos-Daniels et al., 2008). Impaired respiratory system behavior has been observed among elite swimmers, which suggests the potential for adverse health effects resulting from frequent visit to swimming pool environments (Clearie et al., 2010; Bougault and Boulet, 2012). The aim of this research was to examine and characterize seasonal changes in water and air quality at an indoor pool facility. Measurements of air and water quality were conducted routinely over a 14-month period to define changes that were attributable to seasonal effects, including building operations and changes in use patterns for the pool.

2.

Methods and materials

Air and water chemistry were monitored at the chlorinated, high school indoor swimming facility 5 times per week during the academic year and once per week during summer. This facility houses an L-shaped pool that contains 770 m3 of water. One leg of the “L” is a six-lane, 22.86 m (25-yard) pool, while the other leg of the “L” is a six-lane, 25 m pool. The air space of this facility has a volume of approximately 3200 m3, and the HVAC system at the facility is operated at roughly nine air changes per hour. All of the air brought into this facility by the HVAC system was from the outside. The mean hydraulic detention time for water in the pool is approximately 5 h. Chlorine content in the pool is controlled using an on-line ORP controller. The signal from this device is used to allow introduction of chlorine from an erosion feeder, in which Ca(OCl)2 pellets are present. Tap water is added to the pool as needed to maintain water level. Water in the pool has not been replaced for many years. The recirculation system at the pool includes a heater for the water, followed by two sand filters operated in parallel, followed by chlorine addition as described above. Swimming pool water samples were collected in 125 mL Nalgene polyethylene bottles with polypropylene screw caps. Samples were collected from approximately 30 cm below the pool water surface without head-space and transported to the Environmental Engineering Laboratories at Purdue University. Samples were always collected at a fixed location to avoid complicating issues associated with spatial variability. The sampling program was conducted in a manner that did not interfere with use of the pool. As such, these tests did not include control of several parameters that are likely to influence water and air quality, including: operation and

774

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

maintenance of the pool, operation of the HVAC system, and use of the pool by swimmers. Sample collection was conducted five days per week from September through May of the following year; from May to the following September, sampling was conducted once per week because the pool was not open for use. The five day per week sampling regimen was resumed at the end of September and continued until the end of the 14-month sampling period. This high school pool is used for swimming lessons and physical education (PE) classes by students at the high school, as well as competitive swimmers on high school teams. Table 1 summarizes the pool usage pattern and bather loading of this pool during this research. The pool was closed during summer. The analytical procedures used in this experiment for quantification of volatile DBPs and some precursors that are known to be common to pool water and air are summarized in Table 2 (See SI-2 for additional information regarding the analytical methods that were applied for this study).

3.

Results and discussion

Summaries of measurements of fundamental water quality parameters (pH, free chlorine concentration, alkalinity, temperature) are included in SI-3, SI-4, and SI-5. These parameters will all influence the dynamic behavior of residual chlorine and DBPs in pools. Of particular interest was a slow but steady increase of pH from roughly 7e8 over period of 6e7 months, when the pool experienced consistently heavy use. This increase of pH will decrease the effectiveness of free chorine as an oxidant and disinfectant and increase the rate of oxidation of some compounds (e.g., CNCl and DCAN). The shift of free chlorine speciation that would accompany this pH change will also influence the rate of DBP formation. Many of the organic-N compounds that are common in human sweat and urine (e.g., urea, uric acid, amino acids, and creatinine) react with free chlorine to generate DBPs (Judd and Black, 2000; Weaver et al., 2009; Li and Blatchley, 2007; WHO, 2006; Weng et al., 2012; Blatchley and Cheng, 2010; Lian et al., 2014). Among the DBPs that are formed in pools, some are chemically stable (e.g. THMs), while others may undergo additional reactions with chlorine, or other compounds. All of the compounds that were measured by MIMS in this study are volatile. Their dynamic behavior will also be influenced by liquid / gas transfer, which has been shown previously to be influenced by mechanical mixing, such as by swimmers (Weng et al., 2011). Therefore, the compounds that were measured in this study will all exist as intermediates in chlorinated swimming pools. Time-course summaries of liquid-phase and gas-phase concentration measurements are presented in Fig. 1 through

7. These figures should be interpreted as follows: the dashed vertical lines in all figures indicate alternate Mondays (twoweek periods). As appropriate, the solid horizontal lines represent concentration limits or guidelines for each compound. The dashed horizontal lines in Figs. 2e5 indicate MIMS detection limits for each volatile compound.

3.1.

Free and combined chlorine

Free chlorine was quantified using the DPD spectrophotometric method and inorganic combined chlorine concentration was measured by MIMS. From Fig. 1, the free chlorine concentration at this pool ranged from 0.05 to 8 mg/L as Cl2, with mean concentration of 2.6 mg/L as Cl2. The combined chlorine concentration ranged from 0.026 to 3.053 mg/L, with mean concentration of 0.458 mg/L as Cl2. The variability of free and combined chlorine concentrations observed in this study were similar to those that have been reported in earlier work (Weaver et al., 2009; Weng and Blatchley, 2011). The National Swimming Pool Foundation (NSPF) (2010) established a lower-limit guideline of 1 mg/L (as Cl2) for free chlorine, and an upper-limit guideline of 5 mg/L (as Cl2) for swimming pools; an ideal free chlorine concentration range of 2e4 mg/L (as Cl2) was also defined. NSPF (2010) also suggested upper limits for combined chlorine (as measured by the DPD/ KI method) of 0.2 mg/L (as Cl2) and 0.5 mg/L (as Cl2) for pools and spas, respectively. As shown in Fig. 1, the free chorine concentration exceeded the NSPF recommended maximum value (5 mg/L (as Cl2)) eight times and fell below the recommended minimum value (1 mg/ L (as Cl2)) 15 times in this period. High concentrations of free chlorine will promote the formation of many DBPs (Weaver et al., 2009), and as such, these free chlorine excursions have the potential to influence air and water chemistry. Low concentrations of free chlorine have been associated with high concentrations of some DBPs, especially CNCl (Weaver et al., 2009). As discussed below, this is because CNCl oxidation is catalyzed by OCl
(Na and Olson, 2004). Based on the NSPF (2010) guideline, the combined chlorine in swimming pools should be below 0.2 mg/L as Cl2; however, from Fig. 1, it is evident that the combined chlorine concentration regularly exceeded the recommended limit. This behavior is common among chlorinated, indoor pools (Weaver et al., 2009). Compliance with this recommended upper limit is uncommon among indoor chlorinated swimming pools in the U.S. If compliance with this limit is viewed as a priority among the swimming community, this implies that the conditions of pool use and operation in the U.S. may need to change. Changes that could bring about reductions of combined chlorine concentration may include alterations of treatment processes (e.g. inclusion of UV-based treatment) and improvements of swimmer

Table 1 e Pool usage pattern and bather loading. Date Average total bather loading per day

Oct 17 - Dec 10, 2011

March 26-May 23, 2012

Sep 24 - Nov 26, 2012

161 (PE classes) þ 54 (swimming team)

between 110 and 140 (just PE classes)

112 (PE classes) þ 30 (swimming team)

Colorimetric DPD with portable photometer Antipyrine digestion/colorimetric method Air sparging- DPD/KI method Portable pH meter Alkaphot (Palintest) tablets with portable photometer

References for these methods Target analytes

Volatile DBPs including: NH2Cl, NHCl2, NCl3, CHCl3, CHBr3, CHBr2Cl, CHBrCl2, CNCl, CNBr, CNCHCl2, and CH3NCl2 Free chlorine Urea Gas-phase NCl3 pH and temperature (see SI-2 and SI-3) Total alkalinity (see SI-4) Membrane Introduction Mass Spectrometry (MIMS)

Methods

Table 2 e Analytical methods used for characterization water and air chemistry.

(Weaver et al., 2009); (Shang and Blatchley, 1999); (Li and Blatchley, 2007) APHA-AWWA-WEF, 1998 Prescott and Jones, 1969 (Aggazzotti et al., 2007); (Weng et al., 2011)

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

775

hygiene (i.e., showering before entering a pool and not urinating in a pool).

3.2.

Trihalomethanes (THMs)

In swimming pools, the THMs normally include the chlorinated and brominated forms: chloroform (SI-6), dichlorobromomethane, dibromochloromethane (SI-7) and bromoform (SI-8). Chloroform usually dominates the total THM signal, unless a substantial source of bromide exists in the pool. These DBPs tend to be chemically stable in pools, but are volatile halogenated hydrocarbons that can be transferred from water to air in swimming pools. The dominant THM by mass was chloroform. This observation is consistent with previous reports (Kim et al., 2002; Judd and Jeffrey, 1995). Therefore, chloroform is potentially a significant concern with respect to swimming pool exposure (Aggazzotti et al., 1998; Lindstrom et al., 1997). The US EPA has established a maximum contaminant level (MCL) for total THMs of 80 mg/L in drinking water; but in Europe this limit is fixed in 100 mg/L for
et al., 2011). The Fe
de
ration Internationale de NataTTHM (Sa tion Amateur (FINA), which is the international governing body for competitive swimming, established a recommended limit of 20 mg/L for total THMs in pools. There is no swimming pool regulation for THMs in the United States. The highest and lowest total trihalomethane (TTHM) concentrations at this pool were 282.7 and 32.70 mg/L, respectively, with a mean value of 77.00 mg/L. TTHM exceeded the FINA recommended limit in 98% of samples collected in this study; among 168 measurements of TTHMs by MIMS, 38% exceeded the EPA MCL. The peaks of THMs concentration in Fig. 2 generally coincided with the free chlorine excursions. Also evident in Fig. 2 is a weekly pattern of TTHM concentration. In most weeks the TTHM concentration was high on Mondays and it started to decrease during the following days until the following Friday. It is hypothesized that this weekly pattern was due to pool usage. During the weekend, particularly on Sundays, the swimming pool was not used; this would allow accumulation of volatile DBPs in the liquid phase during the weekend because of no activity in the pool and reduced liquid / gas transfer. The loss of TTHM compounds during the weekdays (while the pool was being used) was attributed to volatilization, which is known to be promoted by mechanical mixing associated with swimming activities. Kristensen et al. (2010) observed similar behavior of THMs due to pool usage, but on a much shorter time-scale. Specifically, they conducted online (real-time) monitoring of TTHMs, wherein the liquidphase THM concentration started to increase in the evening when the pool closed and kept increasing until the pool opened again the following morning, when THM concentrations began to decline during the period of swimming activity. The data from Fig. 2 indicate that this same trend is evident for THM concentration over longer periods of time as well.

3.3.

Halonitriles

Halonitriles that are known to be formed in chlorinated swimming pools include haloacetonitriles (HANs) (e.g. dichloroacetonitrile (DCAN)), cyanogen chloride (CNCl) and cyanogen bromide (CNBr) (see SI-9). Compared to THMs,

776

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

8

Concentration (mg/L as Cl2)

Free chlorine Conc. (by DPD/KI) Combined Chlorine Conc.(by MIMS) Free Chlorine NSPF min Free Chlorine NSPF Max Combined Chlorine NSPF max (0.2 mg/L)

6

4

2

0 1 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 /1 12 26 10 24 /7 21 /5 19 /2 16 30 13 27 12 26 /9 23 /7 21 /4 18 /2 16 30 13 27 10 24 /8 22 /5 19 9/ 9/ 10/ 10/ 11 11/ 12 12/ 1 1/ 1/ 2/ 2/ 3/ 3/ 4 4/ 5 5/ 6 6/ 7 7/ 7/ 8/ 8/ 9/ 9/ 10 10/ 11 11/

Fig. 1 e Free and combined chlorine concentration as a function of date.

halonitriles are generally less volatile and tend to be present at lower mass concentrations. Among the volatile DBPs that were measured in this study, halonitriles tend to be the most genotoxic toward mammalian cells, and they are also important contributors to cytotoxicity, similar to other N-DBPs, haloamides, and halonitromethanes (Richardson et al., 2012).

3.3.1.

Dichloroacetonitrile (CNCHCl2)-MIMS

DCAN has been identified as a skin and respiratory irritant and possible mutagenic and carcinogenic compound (Osgood and Sterling, 1991; Oliver, 1983). As indicated in Fig. 3, the DCAN concentration ranged from 0.67 to 30.5 mg/L, with a mean

value of 8.56 mg/L, which is much lower than the WHO (1995) target of 90 mg/L for DCAN in drinking water. As illustrated in Fig. 3, the free chlorine excursions led to rapid DCAN formation. A pattern of DCAN decline from Monday through Friday was often observed (see Section 3.2). Previous reports of the rates of DCAN formation and decay indicate that these two processes tend to be slow as compared to the analogous reaction rates for other DBPs examined in this work, with time-scales on the order of days to weeks (Li and Blatchley, 2007; Reckhow et al., 2001). Bieber and Trehy (1983) reported a half-life of 29 h for DCAN at pH 8.3 (25  C). DCAN is sufficiently volatile to be detected by MIMS; however the

Fig. 2 e TTHM concentration as a function of sampling date at high school pool.

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

777

Fig. 3 e Dichloroacetonitrile (CNCHCl2) concentration as a function of sampling date, as measured by MIMS.

Henry's law constant for DCAN is roughly 0.048% of that of NCl3 (Weng et al., 2011). As such, liquid / gas transfer of DCAN is expected to be slow. Given this behavior, and the fact that the known precursors to DCAN formation in pools are introduced by swimmers, it is evident that the DCAN concentration is related to pool usage. DCAN concentration tends to increase steadily during periods of heavy use, while periods of little or no use allow for DCAN decay. As shown in Fig. 3, the concentration of DCAN increased steadily from October 2011 until December 2011, when competitive swimmers and students from physical education classes were using the pool (heavy usage led to net production during this period), presumably

because the pool received inputs of the organic-N precursors that are responsible for formation of DCAN. In contrast, from February 2012 through March 2012 when the pool experienced low or zero bather loads, the concentration of DCAN showed a slow, steady decay (light usage led to net consumption during this period). This pattern was repeated in the period from the 3rd week of March 2012 when students from physical classes started to use pool until the 3rd week of May 2012. After the third week of May 2012, DCAN concentration decreased gradually because of no usage of pool (summer time) and again DCAN concentration began to gradually increase until the end of September 2012, when pool was opened.

Fig. 4 e Cyanogen chloride (CNCl) concentration as a function of sampling date, as measured by MIMS.

778

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

Fig. 5 e Liquid-phase trichloramine (NCl3) concentration as a function of sampling date, as measured by MIMS.

3.3.2.

Cyanogen chloride (CNCl)-MIMS

CNCl is highly toxic and volatile; it is quickly metabolized to cyanide in humans (Na and Olson, 2004). Cyanogen chloride is known to be produced and oxidized rapidly as a result of reactions involving amino acids and free chlorine (Na and Olson, 2004); the time-scale for these reactions is known to be on the order of minutes to hours (Na and Olson, 2004). In addition, the Henry's law constant for CNCl is roughly 500x greater than that of DCAN; however, the Henry's law constant of CNCl is roughly 24% of that of NCl3 (Weng et al., 2011). As such,

liquid/gas transfer of CNCl is likely to more important than with DCAN. Overall, these characteristics suggest that CNCl concentrations in pool water can be expected to change rapidly. In the absence of free chlorine at near neutral pH, the halflife of CNCl due to OH-assisted hydrolysis is greater than 19 h (Na and Olson, 2004). However, its half-life has been reported as approximately 60 min in water with a free chlorine concentration of 0.5 mg/L (as Cl2) at 25  C, pH ¼ 7 (Na and Olson, 2004). This explains why the highest CNCl concentrations in

Fig. 6 e Gas-phase trichloramine concentration as a function of sampling date, as measured by air sparging DPD/KI method (left vertical axis) and bather loading (right vertical axis). The vertical bars indicate the bather load (right vertical axis) in the pool at the time of gas-phase trichloramine measurements. For dates that do not show a bather loading bar, no swimmers were in the pool at the time of measurement.

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

779

Fig. 7 e Urea concentration as a function of sampling date at a high school. Data points represents mean of triplicate measurements, while error bars represent the standard deviation. The vertical solid lines indicate the periods based on the total daily bather use of high school pool per day.

pools tended to be associated with low or below detection limit free chlorine concentration. The highest and lowest cyanogen chloride concentration at this high school chlorinated indoor pool were 203 mg/L and 1.07 mg/L, respectively, with a mean value of 23.7 mg/L. The CNCl concentration in pool water appears to depend on several factors, including: free chlorine concentration, bather loading, type of swimmer activity, temperature, pH, and the hygiene habits of swimmers (Na and Olson, 2004, 2006; Lian et al., 2014). The toxicology of cyanogen chloride has not yet determined for swimming pool exposure, however the data represented in Fig. 4 indicate that the concentration of CNCl in this pool was consistently below the ACGIH Threshold Limit Value (300 mg/L). A pattern of concentration decrease from Monday through Friday was observed in some weeks (as explained in Section 3.2). On dates with free chorine excursions, the CNCl concentration tended to be low because as mentioned earlier, CNCl will undergo OCl
-catalyzed oxidation (Na and Olson, 2004). The concentration of CNCl in water showed a weak, negative correlation to free chlorine concentration (SI-10). This suggests that other factors will also influence the CNCl concentration in pools.

3.4.

Chloramines

Free chlorine reacts rapidly with ammonia and organic-N compounds to form other chlorine species such as inorganic chloramines (monochloramine (SI-11), dichloramine (SI-12), and trichloramine), and organic chloramines (e.g. dichloromethylamine) (SI-13) which have been reported to have less or no inactivation potential against microorganisms (Shang and Blatchley, 1999; Donnermair and Blatchley, 2003).

3.4.1.

Trichloramine (NCl3)-MIMS

Measurements of inorganic combined chlorine, particularly trichloramine, are often used as an indicator of swimming pool water and air quality. As cited by the IARC (2004), Kirk and Othmer (1993) identified that trichloramine aqueous concentrations of 0.02 mg/L (as Cl2) can cause strong and unpleasant odors. At this indoor swimming pool, the highest and lowest concentrations of trichloramine were 2.19 mg/L as Cl2 and undetectable, respectively, with a mean concentration of 0.42 mg/L as Cl2. As shown in Figs. 1 and 5, the peak NCl3 concentrations coincided with the free chlorine excursions. A weekly pattern of relatively high concentration on Monday, followed by steady decline during the week, was often observed for trichloramine during periods when the pool experienced heavy usage. Trichloramine is stable with presence of free chlorine (Kumar et al., 1987). The NCl3 concentration was consistently higher than the other inorganic chloramines (mono- and dichloramine) in this swimming pool, which it is consistent with its direct formation from urea and other organic-N compounds (Blatchley and Cheng, 2010; Li and Blatchley, 2007; Schmalz et al., 2011; Lian et al., 2014). On the other hand, NCl3 will also undergo hydrolysis to yield NHCl2 and NH2Cl, and it is quite volatile. Therefore, NCl3 exists as an intermediate in swimming pools. The high Cl:N molar ratio that characterizes this and (most) other chlorinated pools also favors preferential NCl3 formation, relative to the other inorganic chloramines (Blatchley and Cheng, 2010).

3.5. Gas-phase trichloramine concentration measurements Among swimming pool DBPs, NCl3 has been the focal point of many studies, and it is a sentinel compound for poor water

780

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

and air quality in pools, largely because of the characteristic “chlorine” odor that it carries. Trichloramine (NCl3) is the most volatile of the inorganic chloramines; it has been estimated that trichloramine is more than 1000 times as volatile as monochloramine (Holzwarth et al., 1984) and it is roughly 2.3 times more volatile than chloroform (Sander, 1999). Fig. 6 illustrates the relationships between bather load and gas-phase trichloramine concentration, as a function of sampling date at this high school pool facility. Because measurements were collected no more than once per day, sometimes the pool was used heavily before the NCl3 gas-phase measurement, and at other times no swimmers were present at the time of measuring. Mechanical mixing by swimmers has been demonstrated to have a strong influence of liquid / gas NCl3 transfer in pools (Weng et al., 2011). Therefore, the nature of the sampling regime contributed to variability in the relationship between gas-phase NCl3 concentration and bather loading (see SI-14). The highest and lowest gas-phase trichloramine concentration at this pool were 0.62 mg/m3 and undetectable, respectively, with the mean value of 0.15 mg/m3. The horizontal lines in Fig. 6 indicate the suggested gasphase limits of Bernard et al. (2006) and WHO (2006). These guidelines were established to limit irritation of the eyes and respiratory system. As shown in Fig. 6, the concentration of NCl3 in the gas-phase appeared to be influenced by increases in bather load and/or swimmer activity. The highest NCl3 concentration in the gas phase was measured when 54 competitive swimmers were using the pool; a similarly strong link between gas-phase NCl3 concentration and bather loading was reported previously by Weng et al. (2011). By increasing the bather load, liquid / gas transfer of NCl3 was promoted. In addition, a large number of swimmers would likely result in increases of the concentrations of NCl3 precursors (organic-N compounds) in the liquid phase, which are introduced to pools largely in the form of human sweat and urine. However, the changes in water chemistry in indoor pools that result from swimmer inputs have been shown to take place on a much longer time scale than the changes in NCl3 concentration in the gas-phase that result from swimmer activity (Li and Blatchley, 2007). Therefore, short term (i.e., time scale of less than hour) changes in gas-phase composition above a chlorinated, indoor pool are likely to be influenced by other factors (e.g., HVAC system behavior; swimmerinduced mixing of the liquid phase), rather than chemicals that are introduced to a pool by swimmers (Weng et al., 2011).

3.6.

Urea

By mass, urea is the dominant organic-N compound in human urine and sweat; urea is also a component of “natural moisturizing factor” in human skin, which is rapidly rinsed from the skin by exposure to water (Gunkel and Jessen, 1986; Erdinger et al., 1997; ISRM, 2009). Urea has been shown to function as an important precursor to NCl3 production in swimming pools, although the time scale for this reaction is on the order of days to weeks, depending on solution pH and Cl:N molar ratio (Blatchley and Cheng, 2010). For the conditions that exist in most chlorinated pools, urea reacts with chlorine quite slowly. Consequently, urea concentration may

be used as an index of reduced-N compounds introduced via human body fluids in pools. De Laat et al. (2011) reported urea concentrations in swimming pools ranging from 0.12 mg/L to 3.6 mg/L. Weng and Blatchley (2011) reported urea concentrations in a pool from 72.4 mg/L to 155 mg/L at indoor swimming pool under condition of heavy use. Fig. 7 illustrates measurements of urea concentration based on the timecourse pattern at a high school pool. According to Fig. 7, the urea concentrations during heavy usage were generally higher than during periods of light or no usage of the pool (SI-15). The highest concentration of urea appeared to coincide with period of greatest use. During the summer, the pool was closed, but during July and August the concentration of urea increased. It was subsequently discovered that a high school sports team used the pool after their practices during this period.

4.

Conclusions

The following conclusions were observed during the fourteen months of monitoring air and water chemistry at an indoor chlorinated high school swimming pool facility:  Free chlorine excursions had a direct and immediate effect on the concentrations of a number of volatile DBPs. The peak concentrations of all volatile DBPs (except CNCl) coincided with the free chlorine excursions. The CNCl concentration was low on dates with free chorine excursions, probably because CNCl will undergo OCl
- catalyzed oxidation.  A weekly pattern of volatile DBP concentrations was often observed, in which the concentrations of DBPs were typically high on Mondays and decreased gradually through the following Friday. This pattern was attributed to loss by volatilization when the pool experienced heavy use. Pool use on weekends was typically less than during the week. Therefore, it is hypothesized that this weekly pattern was due to pool usage.  DCAN showed slow, but steady increases and decreases during this sampling period. DCAN concentration increased during periods of heavy pool use, presumably because the pool received inputs of the organic-N precursors that are responsible for formation of DCAN, and other DBPs. In contrast, when the pool experienced low or zero bather loads, the DCAN concentration showed a slow, steady decay.  Among the inorganic chloramines, the NCl3 concentration was consistently higher than the other inorganic chloramines (also higher than other volatile DBPs). This is believed to be because in swimming pools, NCl3 will be formed directly from reactions between free chlorine and organic-N compounds (e.g., urea). On the other hand, NCl3 will also decay by hydrolysis to yield NHCl2 and NH2Cl, and it is quite volatile. Therefore NCl3 exists as an intermediate in swimming pools.  Gas-phase NCl3 concentration measurements indicated that NCl3 transfer to the gas phase was influenced by bather loading and swimmer activity, as well as NCl3 aqueous concentration.

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

 Urea concentration increased during periods of heavy usage. Urea concentration was generally higher during periods of heavy use than during periods of light or no usage of the pool.  The introduction of DBP precursors can likely be reduced through showering of swimmers prior to entering the pool, and by alteration of the hygiene habits of swimmers, particularly as related to urination.

Acknowledgements Support for this work was provided by grants from the National Swimming Pool Foundation (NSPF), the American Chemistry Council, and Engineered Treatment System, LLC (ETS). The cooperation and support of pool operators and facility managers involved in this study is also greatly appreciated. AP Chemistry class students at the high school were active participants in this work.

Appendix A. Supplementary data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.watres.2014.10.037.

references

Aggazzotti, G., Fantuzzi, G., Tartoni, P.L., Predieri, G., 1990. Plasma chloroform concentrations in swimmers using indoor swimming pools. Archives Environ. Health: An Int. J. 45 (3), 175e179. Aggazzotti, G., Fantuzzi, G., Righy, E., Tartoni, P., Cassinadri, T., Predieri, G., 1993. Chloroform in alveolar air of individuals attending indoor swimming pools. Archives Environ. Health: An Int. J. 48 (4), 250e254. Aggazzotti, G., Fantuzzi, G., Righi, E., Predieri, G., 1995. Environmental and biological monitoring of chloroform in indoor swimming pools. Chromatogr. A 710 (1), 181e190. Aggazzotti, G., Fantuzzi, G., Righi, E., Predieri, G., 1998. Blood and breath analyses as biological indicators of exposure to trihalomethanes in indoor swimming pools. Sci. Total Environ. 217 (1e2), 155e163. Aggazzotti, G., Giacobazzi, P., Predieri, G., 2007. In: P. E. R. B. III, (Ed.), Nitrogen Trichloride Detection in Indoor Swimming Pool Air. University of Modena and Reggio Emilia. APHA-AWWA-WEF, 1998. Standard Methods for the Examination of Water and Wastewater, twentieth ed. DC, Washington. AWWA, 1999. Water Quality and Treatment: a Handbook of Community Water Supplies, fifth ed. McGraw-Hill, New York. Bernard, A., Carbonnelle, S., Michel, O., Higuet, S., de Burbure, C., Buchet, J.-P., Hermans, C., Dumont, X., Doyle, I., 2003. Lung hyperpermeability and asthma prevalence in schoolchildren: unexpected associations with the attendance at indoor chlorinated swimming pools. Occup. Environ. Med. 60, 385e394. Bernard, A., Carbonnelle, S., Dumont, X., Nickmilder, M., 2007. Infant swimming practice, pulmonary epithelium integrity, and the risk of allergic and respiratory diseases later in childhood. Pediatrics 119 (6), 1095e1103.

781

Bernard, A., Nickmilder, M., Voisin, C., Sardella, A., 2009. Impact of chlorinated swimming pool attendance on the respiratory health of adolescents. Pediatrics 124, 1110e1118.
ment, M., Thomas, O., 2011. Bessonneau, V., Derbez, M., Cle Determinants of chlorination by-products in indoor swimming pools. Int. J. Hyg. Environ. Health 215 (1), 76e85. Bieber, T.I., Trehy, M.L., 1983. Dihaloacetonitriles in chlorinated natural waters. Environ. Impact Health Eff. 4, 85e96. Book 1, Chemistry and Water Treatment. Blatchley III, E.R., Cheng, M., 2010. Reaction mechanism for chlorination of urea. Environ. Sci. Technol. 44 (22), 8529e8534. Bougault, V., Boulet, L.P., 2012. Airway dysfunction in swimmers. Br. J. Sports Med. 46 (6), 402e406. Bougault, V., Turmel, J., Boulet, L.P., 2010. Effects of intense swimming training on rhinitis in high-level competitive swimmers. Clin. Exp. Allergy 40, 1238e1246. Bowen, A.B., Kile, J.C., Otto, C., Kazerouni, N., Austin, C., Blount, B.C., Wong, H.N., Beach, M.J., Fry, A.M., 2007. Outbreaks of short-incubation ocular and respiratory illness following exposure to indoor swimming pools. Environ. Health Perspect. 115 (2), 267e271. Chu, H., Nieuwenhuijsen, M.J., 2002. Distribution and determinants of trihalomethane concentrations in indoor swimming pools. Occup. Environ. Med. 59, 243e247. Clearie, K.L., Vaidyanathan, S., Williamson, P.A., Goudie, A., Short, P., Schembri, S., Lipworth, B.J., 2010. Effects of chlorine and exercise on the unified airway in adolescent elite Scottish swimmers. Allergy 65 (2), 269e273. Dang, B., Chen, L.L., Mueller, C., Dunn, K.H., Almaguer, D., Roberts, J.L., Otto, C.S., 2010. Ocular and respiratory symptoms among lifeguards at a hotel indoor Waterpark resort. Occup. Environ. Med. 52 (2), 207e213. De Laat, J., Feng, W., Freyfer, D.A., Dossier-Berne, F., 2011. Concentration levels of urea in swimming pool water and reactivity of chlorine with urea. Water Res. 45 (3), 1139e1146. Erdinger, L., Kirsch, F., Sonntag, H.G., 1997. Potassium as an indicator of anthropogenic contamination of swimming pool water. Zentralbl Hyg. Umweltmed 200 (5e6), 297e308. Erdinger, L., Ku¨hn, K.P., Kirsch, F., Feldhues, R., Frobel, T., Nohyek, B., Gabrio, T., 2004. Pathways of trihalomethane uptake in swimming pools. Int. J. Hyg. Environ. Health 571e575. Fantuzzi, G., Righi, E., Predieri, G., Giacobazzi, P., Mastroianni, K., Aggazzotti, G., 2010. Prevalence of ocular, respiratory and cutaneous symptoms in indoor swimming pool workers and exposure to disinfection by-products (DBPs). Int. J. Environ. Res. Public Health 7, 1379e1391. Faust, M., 1993. Determination of volatile brominated and chlorinated hydrocarbons in public indoor swimming-pool air (abstract only). LCGC Int. 6 (7), 432e435. Gunkel, K., Jessen, H.J., 1986. Untersuehungen u¨ber den Harnstoffeintrag in das Badewasser. Acta gydrochimica hydroblologica 14 (5), 451e461. Hery, M., Hecht, G., Gerber, J.M., Gender, J.C., Hubert, G., Rebuffaud, J., 1995. Exposure to chloramines in the atmosphere of indoor swimming pools. Annu. Occup. Hyg. 39 (4), 427e439. Holzwarth, G., Balmer, R.G., Soni, L., 1984. The fate of chlorine and chloramines in coolingtowerse Henrys law constants for flashoff. Water Res. 18 (11), 1421e1427. IARC, 2004. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, vol. 84. Retrieved July 2012, from. http:// monographs.iarc.fr/ENG/Monographs/vol84/mono84-8.pdf. Institute of Sport and Recreation Management (ISRM), 2009. Managing Trichloramine in Indoor Pools. Information Notes (Ref-349:01/09). Loughborough University, Loughborough, UK. Jacobs, J.H., Spaan, S., van Rooy, G.B.G.J., Meliefste, C., Zaat, V.A.C., Rooyackers, J.M., Heederik, D., 2007. Exposure to trichloramine and respiratory symptoms in indoor swimming pool workers. Eur. Respir. J. 29 (4), 690e698.

782

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

Jafvert, C.T., Valentine, R.L., 1992. Reaction scheme for the chlorination of ammoniacal water. Environ. Sci. Technol. 26 (3), 577e586. Judd, S.J., Black, S.H., 2000. Disinfection by-product formation in swimming pool waters: a simple mass balance. Water Res. 34 (5), 1611e1619. Judd, S.J., Jeffrey, J.A., 1995. Trihalomethane formation during swimming pool water disinfection using hypobromous and hypochlorous acids. Water Res. 29 (4), 1203e1206. Kaydos-Daniels, S.C., Beach, M.J., Shwe, T., Magri, J., Bixler, D., 2008. Health effects associated with indoor swimming pools: a suspected toxic chloramine exposure. Public Health 122 (2), 195e200. Kim, H., Shim, J., Lee, S., 2002. Formation of disinfection byproducts in chlorinated swimming pool water. Chemosphere 46 (1), 123e130. Kirk, R.E., Othmer, D.F., 1993. Dyes, Anthraquinones. fourth ed. In: Kroschwitz, J.I., Howe-Grant, M. (Eds.), Kirk-Othmer Encyclopedia of Chemical Technology, vol. 8. John Wiley & Sons, Inc., New York, USA, pp. 653e666. Kristensen, G.H., Kausen, M.M., Hansen, V.A., Lauritsen, F.R., 2010. Online monitoring of the dynamics of trihalomethane concentrations in a warm public swimming pool using an unsupervised membrane inlet mass spectrometry system with off-site real-time surveillance. Rapid Commun. Mass Spectrom. 24, 30e34. Kumar, K., Shinness, R.W., Margerum, D.W., 1987. Kinetics and mechanisms of the base decomposition of nitrogen trichloride in aqueous solution. Inorganic Chemistry 26 (21), 3430e3434. L'evesque, B., Ayotte, P., Tardif, R., Charest-Tardif, G., Dewailly, E., Prud’Homme, D., 2000. Evaluation of the health risk associated with exposure to chloroform in indoor swimming pools. Toxicol. Environ. Health part A 6 (4), 225e243. € tjer, K., Duszeln, J.V., Gabel, B., Stachel, B., Lahl, U., Ba Thiemann, W., 1981. Distribution and balance of volatile halogenated hydrocarbons in the water and air of covered swimming pools using chlorine for water disinfection. Water Res. 15 (7), 803e814. Lee, W., Westerhoff, P., Croue, J.P., 2007. Dissolved organic nitrogen as a precursor for chloroform, dichloroacetonitrile, N-nitrosodimethylamine and trichloronitromethane. Environ. Sci. Technol. 41, 5485e5490. Li, J., Blatchley III, E.R., 2007. Volatile disinfection by-product formation resulting from chlorination of organic-nitrogen precursors in swimming pools. Environ. Sci. Technol. 41, 6732e6739. Lian, L., E, Y., Li, J., Blatchley III, E.R., 2014. Volatile disinfection byproducts resulting from chlorination of uric acid: Implications for swimming pools. Environ. Sci. Technol. 48, 3210e3217. Lindstrom, A.B., Pleil, J.D., Berkoff, D.C., 1997. Alveolar breath sampling and analysis to assess trihalomethane exposures during competitive swimming training. Environ. Health Perspect. 105 (6), 636e642.
ry, M., Toamain, J.P., Massin, N., Bohadana, A.B., Wild, P., He Hubert, G., 1998. Respiratory symptoms and bronchial responsiveness in lifeguards exposed to nitrogen trichloride in indoor swimming pools. Occup. Environ. Med. 55 (4), 258e263. Matthiessen, A., Jentsch, F., 1999. Trihalomethanes in air of indoor swimming pools and uptake by swimmers. In: Proceedings of ISIAQ: Indoor Air 99 Conference, Edinburgh, Scotland, August 8e13. McKinney, J.D., Mauer, R.R., Hall, J.R., Thomas, R.O., 1976. Possible factors in the drinking water of laboratory animals causing reproductive failure. In: Keith, L.H. (Ed.), Identification & Analysis of Organic Pollutants in Water. Ann Arbor Science Pub., Ann Arbor, MI, pp. 417e432. Muellener, M.G., Wagner, E.D., Jazwierska, P., Richardson, S.D., Woo, Y.T., Plewa, M.J., 2007. Haloacetonitriles vs. regulated

haloacetic acids: are nitrogen-containing DBPs more toxic? Environ. Sci. Technol. 41 (2), 645e651. Na, C., Olson, T.M., 2004. Stability of cyanogen chloride in the presence of free chlorine and monochloramine. Environ. Sci. Technol. 38 (22), 6037e6043. Na, C., Olson, T.M., 2006. Mechanism and kinetics of cyanogen chloride formation from the chlorination of glycine. Environ. Sci. Technol. 40, 1469e1477. National Institute of Occupational Safety and Health (NIOSH), 2003. The Emergency Response Safety and Health Database: CYANOGEN CHLORIDE. NIOSH, CDC, Atlanta GA. Retrieved July 6, 2012, from. http://www.cdc.gov/NIOSH/ershdb/ EmergencyResponseCard_29750039.html. National Swimming Pool Foundation (NSPF), 2010. NSPF Certified Pool-spa Operator Handbook. National Swimming Pool Foundation, Colorado Springs, CO. Oliver, B.G., 1983. Dihaloacetonitriles in drinking water: algae and fulvic acid as precursors. Environ. Sci. Technol. 17 (2), 80e83. Osgood, C., Sterling, D., 1991. Dichloroacetonitrile, a by-product of water chlorination, induces aneuploidy in drosophila. Mutat. Res. Genetic Toxicol. 261 (2), 85e91. OSHA, 1992. Chemical Sampling Information - Cyanogen Chloride. Retrieved on July 6, 2012, from. http://www.osha. gov/dts/chemicalsampling/data/CH_230505.html. Periera, M.A., Daniel, F.B., Lin, E.L.C., 1985. Relationship between metabolism of haloacetonitriles and chloroform and their carcinogenic activity. Water Chlorination 5, 229e236. Chemistry, Environmental Impact and Health Effects, Lewis, Chelsea, MI. Prescott, L.M., Jones, M.E., 1969. Modified methods for the determination of carbamoyl aspartate. Anal. Biochem. 32 (3), 408e419. Reckhow, D.A., Platt, T.L., MacNeill, A.L., McClellan, J.N., 2001. Formation and degradation of dichloroacetonitrile in drinking waters. Aqua: Q. Bull. Int. Water Supply Assoc. 50 (1), 1e13.
, C.P.D. (Eds.), 2012. Richardson, S.D., Cristina, Postigo D., Barcelo Drinking Water Disinfection By-products: Emerging Organic Contaminants and Human Health. Handbook of Environmental Chemistry, vol. 20, pp. 93e138.
, C.S.A., Boaventura, R.A.R., Pereira, I.B., 2011. Analysis of Sa trihalomethanes in water and air from indoor swimming pools using HS-SPME/GC/ECD. Environ. Sci. Health Part A 46, 355e363. Safranek, T., Semerena, S., Huffman, T., Theis, M., Magri, J., € ro € k, T., Beach, M.J., Buss, B., 2007. Ocular and respiratory To illness associated with an indoor swimming pool - Nebraska, 2006. Morb. Mortal. Wkly. Rep. (MMWR) 56 (36), 929e932. Sander, R., 1999. Compilation of Henry's Law Constants for Inorganic and Organic Species of Potential Importance in Environmental Chemistry. Max-Planck Institute of Chemistry, Mainz, Germany. Schmalz, C., Frimmel, F.H., Zwiener, C., 2011. Trichloramine in swimming pools e formation and mass transfer. Water Res. 45 (8), 2681e2690. Shang, C., Blatchley III, E.R., 1999. Differentiation and quantification of free chlorine and inorganic chloramines in aqueous solution by MIMS. Environ. Sci. Technol. 33 (13), 2218e2223. Shang, C., Gong, W.-L., Blatchley, E.R., 2000. Breakpoint chemistry and volatile byproduct formation resulting from chlorination of model organic-N compounds. Environ. Sci. Technol. 34 (9), 1721e1728. Smith, M.K., Randall, J.L., Stober, J.A., Read, A.J., 1989. Developmental toxicity of dichloroacetonitrile: a by-product of drinking water disinfection. Fundam. Appl. Toxicol. 12, 765e772. Villanueva, C.M., Cantor, K.P., Grimalt, J.O., Malatas, N., Silverman, D., Tardon, A., Garcia-Closas, R., Serra, C., Carrato, A., Castano-Vinyals, G., Marcos, R., Rothman, N., Real, F.X., Dosemeci, M., Kogevinas, M., 2007. Bladder cancer and exposure to water disinfection by-products through

w a t e r r e s e a r c h 6 8 ( 2 0 1 5 ) 7 7 1 e7 8 3

ingestion, bathing, showering, and swimming in pools. Am. J. Epidemiol. 165 (2), 148e156. Wang, W., Qian, Y., Boyd, J.M., Wu, M., Hrudey, S.E., Li, X.F., 2013. Halobenzoquinones in swimming pool waters and their formation from personal care products. Environ. Sci. Technol. 47 (7), 3275e3282. Weaver, W.A., Li, J., Wen, Y., Johnston, J., Blatchley, M.R., Blatchley III, E.R., 2009. Volatile disinfection by-product analysis from chlorinated indoor swimming pools. Water Res. 43 (13), 3308e3318. Weisel, C.P., Shepard, T.A., 1994. Chloroform exposure and the body burden associated with swimming in chlorinated pools. In: Wang, R.G.M. (Ed.), Water Contamination and Health. Marcel Dekker, New York. Weng, S.C., Weaver, W.A., Zare Afifi, M., Blatchley, T.N., Carmer, J.S., Chen, J., Blatchley III, E.R., 2011. Dynamics of gasphase trichloramine in chlorinated, indoor swimming pool facilities. Indoor air 21, 391e399. Weng, S.C., Blatchley III, E.R., 2011. Disinfection by-product dynamics in a chlorinated, indoor swimming pool under conditions of heavy use: National swimming competition. Water Research 45 (16), 5241e5248. Weng, S.C., Li, J., Blatchley III, E.R., 2012. Effects of UV254 irradiation on residual chlorine and DBPs in chlorination of model organicN precursors in swimming pools. Water Res. 46 (8), 2674e2682.

783

World Health Organization (WHO), 1995. Health and Environmental Briefing PamPhlet Series. Disinfection de L' eau, local authorities, vol. 3. World Health Organization (WHO), 2004. Geneva, Switzerland Recommendations in Guidelines for Drinking Water Quality, third ed., vol. 1 Ch.8. World Health Organization (WHO), 2006. Guidelines for Safe Recreational-water Environments, Swimming Pools, Spas and Similar Recreational-water Environments, 2. World Health Organization Press, Geneva, p. 146. Retrieved November 24, 2010, from. http://www.who.int/water_sanitation_health/ bathing/srwe2chap4.pdf. World Health Organization (WHO), 2009. Cyanogen Chloride in Drinking-water, Background Document for Development of WHO Guidelines for Drinking-water Quality. WHO, Geneva. Xiao, F., Zhang, X., Zhai, H., Lo, I.M.C., Tipoe, G.L., Yang, M., Pan, Y., Chen, G., 2012. New halogenated disinfection byproducts in swimming pool water and their permeability across skin. Environ. Sci. Technol. 46 (13), 7112e7119. Zwiener, C., Richardson, S.D., De Marini, D.M., Grummt, T., Glauner, T., Frimmel, F.H., 2007. Drowning in disinfection byproducts? Assessing swimming pool water. Environ. Sci. Technol. 41 (2), 363e372.