Pt

Ja

b

a

ARRA

KTHHCTN

I

lpsmcedh(pG

dB

1d

International Journal of Hygiene and Environmental Health 213 (2010) 465–474

Contents lists available at ScienceDirect

International Journal of Hygiene andEnvironmental Health

journa l homepage: www.e lsev ier .de / i jheh

roduction of various disinfection byproducts in indoor swimming pool watersreated with different disinfection methods

in Leea,b, Myung-Jin Juna, Man-Ho Leea, Min-Hwan Leea, Seog-Won Eoma, Kyung-Duk Zohb,∗

Seoul Metropolitan Government Research Institute of Public Health and Environment, Gyeonggi Province 427-070, South KoreaInstitute of Health and Environment, School of Public Health, Seoul National University, Seoul 152-742, South Korea

r t i c l e i n f o

rticle history:eceived 13 April 2010eceived in revised form 27 August 2010ccepted 9 September 2010

eywords:rihalomethanes (THMs)aloacetic acids (HAAs)aloacetonitriles (HANs)hloral hydrate (CH)OCitrate

a b s t r a c t

In this study, the concentrations of disinfection byproducts (DBPs), including trihalomethanes (THMs;chloroform, bromodichloromethane, dibromochloromethane, and bromoform), haloacetic acids (HAAs;dichloroacetic acid and trichloroacetic acid), haloacetonitriles (HANs; dichloroacetonitrile, trichloroace-tonitrile, bromochloroacetonitrile, and dibromoacetonitrile), and chloral hydrate (CH) were measured in86 indoor swimming pools in Seoul, Korea, treated using different disinfection methods, such as chlo-rine, ozone and chlorine, and a technique that uses electrochemically generated mixed oxidants (EGMOs).The correlations between DBPs and other environmental factors such as with total organic carbon (TOC),KMnO4 consumption, free residual chlorine, pH, and nitrate (NO3

−) in the pools were examined. The geo-metric mean concentrations of total DBPs in swimming pool waters were 183.1 ± 2.5 �g/L, 32.6 ± 2.1 �g/L,and 139.9 ± 2.4 �g/L in pools disinfected with chlorine, ozone/chlorine, and EGMO, respectively. Themean concentrations of total THMs (TTHMs), total HAAs (THAAs), total HANs (THANs), and CH differed

significantly depending on the disinfection method used (P < 0.01). Interestingly, THAAs concentrationswere the highest, followed by TTHMs, CH, and THANs in all swimming pools regardless of disinfectionmethod. TOC showed a good correlation with the concentrations of DBPs in all swimming pools (chlo-rine; r = 0.82, P < 0.01; ozone/chlorine; r = 0.52, P < 0.01, EGMO; r = 0.39, P < 0.05). In addition, nitrate waspositively correlated with the concentrations of total DBPs in swimming pools disinfected with chlorineand ozone/chlorine (chlorine; r = 0.58; ozone/chlorine; r = 0.60, P < 0.01), whereas was negative correlated

f tota

with the concentrations o

ntroduction

Swimming provides health benefits and has advantages overand-based activities for people of all ages. To conserve theositive aspect of aquatic activities, it is necessary to disinfectwimming pool water to protect swimmers against infection byicrobiological pathogens. In many countries, chlorine is the most

ommon method for disinfection of swimming pool water. How-ver, when chlorine reacts with organic matter in water, a variety ofisinfection by-products (DBPs) can be formed. Among these, tri-alomethanes (THMs), haloacetic acids (HAAs), haloacetonitrilesHANs), and chloral hydrate (CH) were found to be the mostrevalent chlorinated byproducts (Nieuwenhuijsen et al., 2000a,b;

unten et al., 2001; Lee et al., 2001; Golfinopoulos et al., 2003).

THMs consist of chloroform, bromodichloromethane (BDCM),ibromochloromethane (DBCM), and bromoform. Chloroform,DCM, and bromoform are classified as probable carcinogens in

∗ Corresponding author. Tel.: +82 2 880 2737; fax: +82 2 762 2888.E-mail address: zohkd@snu.ac.kr (K.-D. Zoh).

438-4639/$ – see front matter © 2010 Elsevier GmbH. All rights reserved.oi:10.1016/j.ijheh.2010.09.005

l DBPs (r = −0.53, P < 0.01) in the EGMO-treated pools.© 2010 Elsevier GmbH. All rights reserved.

humans (Group B2), while DBCM is listed as a possible carcino-gen (Group C). Dichloroacetic acid (DCAA) and trichloroacetic acid(TCAA) are the most common of the nine HAA compounds, and arealso categorized as Groups C and B2 carcinogens, respectively (USEPA, 2008).

HANs consist of dichloroacetonitrile (DCAN), trichloroacetoni-trile (TCAN), bromochloroacetonitrile (BCAN), and dibromoace-tonitriles (DBAN). DCAN shows mutagenicity in bacterial assays(Oliver, 1983), and DBAN and BCAN show carcinogenic or muta-genic effects in mice (Bull et al., 1985). HANs produce DNA strandbreaks in cultured human lymphoblastic cells (CCRF-CEM), withTCAN showing the most potent effect (Daniel et al., 1986; Lin et al.,1986), and also induce acute genomic DNA damage in Chinese ham-ster ovary (CHO) cell assays (Muellner et al., 2007). Chloral hydrate(CH) is also classified as a possible human carcinogen (Group C) (USEPA, 2008).

THMs are the most frequently measured and best studied ofthese DBPs, and are therefore recognized as DBP surrogates. How-ever, other DBPs, such as HAAs, HANs, and CH, have not beenmeasured as extensively, and therefore relatively little informationis available regarding these DBPs in swimming pools.

4 e and

scd(sWhk(

fmiotdwr2adpgitdtV

(tmcitte

M

W

gfTesclcfi

D

atdi

ct(

66 J. Lee et al. / International Journal of Hygien

The formation and distribution of DBPs are dependent on waterource, contact time, chlorine dose and residual, total organicarbon (TOC), bromide concentration, and pH. A higher chlorineose and TOC concentration can enhance the formation of DBPsSinger, 1994; Nikolaou et al., 2004). The presence of bromide ionshifts DBP products into brominated species (Duong et al., 2003;

hitaker et al., 2003; Uyak and Toroz, 2007). Increased pH valuesave a positive effect on THM formation and HAA levels are alsonown to increase at low pH (American Water Works AssociationAWWA), 1999; Singer, 1994; Liang and Singer, 2003).

Although chlorination is still the major method used for disin-ection of swimming pool water in Korea (Lee et al., 2009), other

ethods such as ozone followed by chlorine as a secondary dis-nfectant (ozone/chlorine) and electrochemically generated mixedxidants (EGMOs) are increasingly being substituted for chlorineo minimize the formation of DBPs. Ozone is a high potential oxi-ant and disinfect but is usually followed by sequential disinfectionith chlorine (ozone/chlorine) because of its instability and the

elatively high doses required (Kleiser and Frimmel, 2000; Jo et al.,005). The technology of EGMOs is based on the principle of passingn electric current through a salt brine solution to produce oxi-ants. It has been suggested that oxidants other than chlorine areroduced by this technology such as ozone, chlorine dioxide, hydro-en peroxide, and hydroxyl radicals (USACHPPM, 2006). However,t has been clearly demonstrated in several studies that chlorine inhe form of hypochlorous acid (HOCl) is the primary oxidant pro-uced and other oxidants are typically very difficult to measure dueo very fast reaction rates. (Patermarakis and Fountoukidis, 1990;enczel et al., 1997; Drees et al., 2003; Kerwick et al., 2005).

With the exception of THM measurement in our recent studyLee et al., 2009), limited data are available regarding DBPs produc-ion in swimming pool waters treated with the three disinfection

ethods. Therefore, the aim of this study was to measure the con-entrations of THMs, and other DBPs such as HAAs, HANs, and CHn swimming pools in Seoul, Korea, treated with different disinfec-ion methods, including chlorine, ozone/chlorine, and EGMOs, ando assess the correlation between the concentrations of DBPs andnvironmental factors based on the disinfection method used.

aterials and methods

ater treatment system in the swimming pools

All of the swimming pools were made of concrete covered withlazed tiles, had rectangular shapes and different volumes rangingrom 150 m3 to 800 m3 and were filled with chlorinated tap water.he water treatment systems in swimming pools adopting differ-nt disinfection methods were similar. The typical water treatmentystems of swimming pools consist of balancing tank, hair catcher,oagulation, filtration, followed by disinfection process. Raw pol-utants such as hairs and plasters are removed from water by a hairatcher, and undissolved particles are removed by coagulation andltration system such as a sand filter or a cartridge filter.

isinfection method

The chlorine in the chlorine disinfected pools was supplied byutomated chlorine feeders. For the chlorine- and ozone/chlorine-reated pools, sodium hypochlorite (NaOCl) has been used as aisinfectant to produce hydrochloric acid (HOCl) and hypochlorite

on (OCl−).The use of ozone has become popular due to its high chemi-

al oxidation potential and the absence of THM formation. All ofhe circulating water is treated with sufficient amount of ozonebetween 1.0 and 1.2 g/m3) to satisfy the oxidant demand of the

Environmental Health 213 (2010) 465–474

water and attain a residual of dissolved ozone for several minutesin contact tank. However, it is unsuitable for use as a residual dis-infectant in the swimming pools, as it readily vaporizes, is toxicand is heavier than air, leading to discomfort and adverse healtheffect (World Health Organization (WHO), 2006). Due to the lack ofresiduals and the relatively high doses required, ozone disinfectionis usually followed by deozonation before water enters the pool,and the addition of a residual disinfectant such as chlorine-baseddisinfectants (over 0.2 mg/L for free chlorine residual) (Venczel etal., 1997; Kleiser and Frimmel, 2000; Jo et al., 2005).

The technology of EGMOs is accomplished by combining salt(3000–6000 mg/L), water, and electricity in electrolytic cells. A volt-age of 240–400 V was then applied to the electrolytic cells. Theprimary oxidant produced by EGMO disinfection is chlorine in theform of HOCl (USACHPPM, 2006), although oxidants other thanchlorine have been suggested to result, such as O3, chlorine dioxide,H2O2, and some short-lived species. Several studies have clearlydemonstrated that chlorine is the primary oxidant produced byEGMOs, and other oxidants have not been detected at measurablelevels (Patermarakis and Fountoukidis, 1990; Venczel et al., 1997;Drees et al., 2003; Kerwick et al., 2005). Therefore, the toxicity con-cerns of EGMO are similar to those in typical chlorine disinfection.The overall disinfectant dosage of EGMO technology is also quanti-fied in terms of free chlorine residual (FCR) (Nakajima et al., 2004;USACHPPM, 2006; Alvarez-Uriate et al., 2010).

Free chlorine residual and pH were checked automatically everyday in all swimming pool waters. The filter backwashing fre-quency was once per week (ozone/chlorine and EGMO), twice orthree times per week (chlorine). The fresh water replacement over20–25% (chlorine), 20% (ozone/chlorine), 10–20% (EGMO) of poolwater volume was conducted every week. The average number ofbathers was 50–300 (chlorine), 30–450 (ozone/chlorine), 80–500(EGMO) per day, respectively.

Sampling

In the study, total 86 public swimming pools located inSeoul, Korea, were monitored from June to November 2006. Ofthe pools sampled, 30 were disinfected with chlorine, 30 withozone/chlorine, and 26 with EGMOs.

For measuring THMs in the samples, a 40-mL brown glass bottlewas filled until overflowing with pool water and tightly sealed witha screw cap. Prior to sampling, 3 mg of sodium thiosulfate wereadded to each 40 mL bottle to quench any residual chlorine reaction.

To quantify HAAs, HANs, and CH compounds in the samples, anamber glass bottle (60 mL) was filled with pool water until over-flowing to remove head space, and tightly sealed with TFE-linedscrew caps. Before sampling, to the samples for HAAs measure-ment, 6 mg of ammonium chloride as a dechlorinating agent wereadded to each bottle, and to the samples for HANs and CH mea-surement, 0.8 g of the mixture of 1% sodium phosphate monobasic(Na2HPO4) and 99% potassium phosphate monobasic (KH2PO4) byweight was added to bottles to lower the sample pH to between 4.8and 5.5 in order to inhibit base catalyzed degradation of the HANs,and to standardize the pH of the samples. Then, 6 mg of ammoniumchloride was added to each 60 mL bottle to eliminate any remainingresidual chlorine.

Samples were also collected in 1-L plastic bottles for analysis ofTOC, KMnO4 consumption, and nitrate (NO3

−). Free residual chlo-rine and pH were measured concurrently with sample collection.All samples were refrigerated at 4 ◦C until analysis.

Analysis

The concentrations of THMs, HAAs, HANs, and CH were mea-sured using the US EPA 500 method series (US EPA Method

e and

51f

Hct1nr3rtmb

dgeftrd(tftitw

Te1wgf3(3D0

m

TC

a

(

J. Lee et al. / International Journal of Hygien

24.2, 1995; US EPA Method 552.2, 1995; US EPA Method 551.1,995). These measurement methods are briefly summarized asollows.

The THMs were measured with a gas chromatograph (HP 6890;ewlett Packard, Palo Alto, CA) with a purge and trap (3100 sampleoncentrator; Tekmar-Dohrmann, Mason, OH), and a mass selec-ive detector (Agilent 5976 Network; Hewlett Packard). The Agilent22-1334 DB-624 capillary column (30.0 m × 250 �m × 1.40 �mominal) was used for peak separation. The oven temperatureegime for gas chromatography was as follows; initial temperature,5 ◦C for 5 min; first ramp of 5 ◦C/min to 100 ◦C (1 min); secondamp of 2.8 ◦C/min to 110 ◦C (1 min); and third ramp of 3 ◦C/mino 130 ◦C (1 min). The detector temperature was 240 ◦C. With this

ethod, the limit of detection for chloroform, BDCM, DBCM, andromoform was 0.2 �g/L.

For the analysis of HAAs, a surrogate standard (100 ppm, 2,3-ibromopropionic acid in methyl-tert-butyl-ether, MTBE, HPLCrade) was added to each sample before extraction. The HAAsxtraction were performed with methyl-tert-butyl-ether (MTBE)ollowed by derivatization with 10% sulfuric acid in methanol,he HAAs in the extracts were measured by gas chromatog-aphy (HP 6890; Hewlett Packard) with an electron captureetector (ECD). The Agilent 19091J-433E HP-5 capillary column30.0 m × 250 �m × 0.25 �m nominal) was used for peak separa-ion. The oven temperature for the gas chromatograph was asollows; initial temperature of 35 ◦C for 1 min, first ramp of 5 ◦C/mino 75 ◦C (5 min), and second ramp of 5 ◦C/min to 110 ◦C (1 min). Thenjector and detector temperatures were 210 ◦C and 240 ◦C, respec-ively. With this method, the detection limits for DCAA and TCAAere 0.3 and 0.2 �g/L, respectively.

HANs and CH were measured by gas chromatography (Thermorace GC; Thermo Finnigan, Rockford, IL) with an ECD detector afterxtraction with methyl-tert-butyl-ether (MTBE). The Agilent 122-033E DB-1 capillary column (30.0 m × 250 �m × 1.0 �m nominal)as used for peak separation. The oven temperature regime for

as chromatography was as follows: initial temperature of 35 ◦Cor 10 min, first ramp of 8 ◦C/min to 62 ◦C (2 min), second ramp of◦C/min to 90 ◦C (1 min), and third ramp of 15 ◦C/min to 150 ◦C

10 min). The injector and detector temperatures were 200 ◦C and◦

50 C, respectively. With this method, the limits of detection for

CAN, TCAN, BCAN, DBAN, and CH were 0.1, 0.2, 0.2, 0.1, and.1 �g/L, respectively.

A sample dispenser (APG 64; Analytik Jena AG, Jena, Ger-any) and a TOC analyzer (multi N/C 3000; Analytik Jena AG)

able 1oncentrations of environmental parameters (mg/L) for swimming pool water samples tr

Arithmetric mean Arithmetric SD

ChlorineTOC 2.3 1.5KMnO4 consumption 4.6 3.7Free chlorine residual 0.7 0.2pH 7.9 0.1NO3

− 10.8 4.8Ozone/chlorine

TOC 1.7 0.5KMnO4 consumption 0.7 0.4Free chlorine residual 0.6 0.2pH 7.6 0.3NO3

− 12.5 6.3EGMO

TOC 3.2 1.0KMnO4 consumption 15.2 3.4Free chlorine residual 0.8 0.1pH 7.9 0.1NO3

− 23.0 11.1

The range of concentrations in filling tap water were known as 0.3–1.4 mg/L (TOC), 0.3pH), and 1.1–1.9 mg/L (NO3

−) (WRISMG, 2008).

Environmental Health 213 (2010) 465–474 467

were used to measure TOC in the filtered samples. The detectionlimit for TOC was 0.1 mg/L. The KMnO4 consumption was mea-sured using a Standard Method for Korean Drinking Water (DigitalInformation Center for Environment Research, 2004). Nitrate wasmeasured with ion chromatography (ICS-3000; DIONEX, USA) andED40 Electrochemical detector. The IonPac AS14 Analytical column(4 mm × 250 mm) Product No. 46124 was used for peak separationfor NO3

−. Since chloride ions are known to interfere with the analy-sis of TOC, KMnO4 consumption, and nitrate, silver sulfate (Ag2SO4)was added to the samples before analysis to precipitate as a silverchloride (AgCl), and the samples were then filtered with a 0.45 �mmixed cellulose ester (MCE) membrane filter (Advantec MFS Inc.,Dublin, CA) (American Public Health Association, 1998; NationalInstitute of Environmental Research, 2004).

Free residual chlorine was measured with the DPD (N,N-diethyl-p-phenylenediamine) method using a pocket colorimeter (model46700-00; HACH, Japan). The pH was measured using a pH meter(model 920A; Orion Research, Inc., Beverly, MA).

Statistical analysis

Statistical analyses were performed using the SAS v8 package(SAS Inst., Cary, NC). The Kruskal–Wallis test was used to evaluatedifferences in the mean concentrations of total THMs (TTHMs), totalHAAs (THAAs), total HANs (THANs), and CH among the differentdisinfection methods. Spearman’s rank correlation coefficient wasused to examine the correlations between concentrations of eachDBPs (TTHMs, THAAs, THANs, and CH) and other environmentalfactors.

Results and discussion

Environmental parameters of swimming pool water

The water quality parameters of swimming pool disinfectedwith chlorine, ozone/chlorine, and EGMO are summarizedin Table 1. Notes in Table 1 also show the reported concen-trations of TOC, KMnO4 consumption, free chlorine residual,pH, and NO3

− in filling tap water in Seoul as 0.3–1.4 mg/L,

0.3–2.2 mg/L, 0.03–0.57 mg/L, 6.8–7.8, and 1.1–1.9 mg/L, respec-tively (Waterworks Research Institute Seoul MetropolitanGovernment (WRISMG), 2008).

Regardless of disinfection method, the average concentrationsof free residual chlorine (0.7 mg/L, 0.6 mg/L, and 0.8 mg/L) in the

eated with three different disinfection methods.

Geometric mean Geometric SD Range

1.9 1.8 0.5–7.03.3 2.3 0.9–13.50.7 1.4 0.24–1.47.9 1.0 7.6–8.2

10.1 1.4 6.6–23.8

1.6 1.8 0.7–3.90.6 1.4 0.3–1.80.6 1.4 0.2–1.27.6 1.0 7.1–8.0

10.3 2.1 1.2–22.0

3.1 1.3 1.9–5.814.8 1.3 8.7–21.4

0.7 1.2 0.4–1.00.7 1.2 7.6–8.0

20.9 1.5 10.9–49.2

–2.2 mg/L (KMnO4 consumption), 0.03–0.57 mg/L (free chlorine residual), 6.8–7.8

468 J. Lee et al. / International Journal of Hygiene and Environmental Health 213 (2010) 465–474

Table 2DBPs concentrations (�g/L) for swimming pool water samples treated with three different disinfection methods.

Arithmetric mean Arithmetric SD Geometric mean Geometric SD Range

ChlorineChlorofom 20.9 13.2 20.3 1.4 N.D.–45.8BDCM 2.1 1.4 2.2 1.4 N.D.–7.0DBCM N.D. – N.D. – N.D.Bromoform N.D. – N.D. – N.D.DCAA 68.3 69.2 43.6 2.5 14.1–246TCAA 156.4 180.9 77.3 3.4 19.7–636DCAN 3.9 3.3 2.7 2.5 0.5–12.2TCAN N.D. – N.D. – N.D.BCAN 0.8 0.5 0.7 2.0 N.D.–1.9DBAN 0.5 0.3 0.4 2.1 N.D.–0.9CH 16.9 8.7 14.9 1.7 5.1–34.9

Ozone/chlorineChlorofom 7.4 5.9 9.3 1.5 N.D.–21.2BDCM 1.1 0.9 1.8 1.2 N.D.–2.5DBCM N.D. – N.D. – N.D.Bromoform N.D. – N.D. – N.D.DCAA 12.0 8.3 11.0 2.0 N.D.–31.9TCAA 17.4 24.6 9.1 3.0 1.3–85.8DCAN 1.3 0.9 1.0 2.1 0.2–3.2TCAN N.D. – N.D. – N.D.BCAN 0.4 0.2 0.4 2.1 N.D.–0.6DBAN 0.4 0.3 0.4 2.0 N.D.–0.8CH 3.6 3.0 2.6 7.3 N.D.–10.4

EGMOChlorofom 14.5 10.7 12.9 2.3 N.D.–40.1BDCM 10.1 8.7 7.5 3.2 N.D.–34.1DBCM 8.9 7.3 8.4 2.1 N.D.–32.3Bromoform 4.1 4.7 2.6 4.0 N.D.–18.0DCAA 33.7 26.4 21.0 3.4 1.5–98.5TCAA 97.2 96.9 49.9 4.5 1.0–413DCAN 3.8 2.5 3.2 2.0 N.D.–9.0TCAN N.D. – N.D. – N.D.

a N.D.–2

cisa2

05m(pmka(

t02lh(apuscs

f

BCAN 3.5 2.2DBAN 2.6 1.9CH 10.2 6.7

The tap water in Seoul contains 3.9–13.5 �g/L of TTHMs, N.D.–8.3 �g/L of THAAs,

hlorine-, ozone/chlorine-, and EGMO-disinfection pools were sim-lar, and found to be higher than the level (0.2 mg/L) for theufficient microbial inactivation (US EPA, 2006; Baytak et al., 2008),nd the typical level (0.03–0.57 mg/L) of filling tap water (WRISMG,008).

TOC ranged from 0.5 to 7.0 mg/L for chlorine-treated water,.7 to 3.9 mg/L for ozone/chlorine-treated water, and 1.9 to.8 mg/L for EGMO-treated water. The ranges of TOC in all swim-ing pool waters were significantly higher than filling tap water

0.3–1.4 mg/L) (WRISMG, 2008). This result implies that a largeroportion of the organic matter in the pools may come from swim-ers especially in summer (Chu and Nieuwenhuijsen, 2002). It is

nown that swimmers’ origin including hair, sun block lotion, salivand urine can increase the level of TOC in swimming pool waterKim et al., 2002).

Table 1 also shows that the amount of KMnO4 consump-ion ranged from 0.9 to 13.5 mg/L for chlorine-treated water,.3 to 1.83 mg/L for ozone/chlorine-treated water, and 8.7 to1.4 mg/L for EGMO-treated water. KMnO4 consumption (mean

evel: 15.2 mg/L) in the EGMO treated water was especiallyigher than in the chlorine- (4.6 mg/L) and ozone/chlorine-treated0.7 mg/L) samples. The high levels of KMnO4 consumption arettributable to the contaminants in the salts used in the EGMOrocess (White, 2009). The salts used in the EGMO processsually contain not only sodium chloride but also other sub-tances such as calcium, magnesium, and sulfate ion. KMnO4

an be used for oxidizing not only organic but also inorganicubstances.

The ranges of pH are 7.6–8.2 for chlorine-treated water, 7.1–8.0or ozone/chlorine-treated water, and 7.6–8.0 for EGMO-treated

2.9 2.2 N.D.–8.02.2 1.8 N.D.–6.88.5 2.1 N.D.–23.4

.8 �g/L of THANs, and 0.7–4.6 �g/L of CH (WRISMG, 2008).

water, respectively. The level of pH in the pool waters was a lit-tle higher than level of pH in filling tap water. The tap water inSeoul is known to have a pH range of 6.8–7.8 (WRISMG, 2008). Forthe chlorine- and ozone/chlorine-treated pools, sodium hypochlo-rite (NaOCl) has been used as a disinfectant. It is known thatthe addition of sodium hypochlorite (NaOCl) tends to increasepH since the hypochlorite ion (OCl−) is a base (Nazaoroff andAlvarez-Cohen, 2000). Also, the primary oxidant formed in EGMOdisinfection is also known as chlorine in the form of HOCl and OCl−

depending on pH. Besides, hydroxide ion (OH−) is produced duringelectrolysis in the EGMO disinfection method. In fact, accordingto Korean water quality standards for swimming pool (KMCST,2004), pool waters can have a pH value of between 5.8 and8.6.

The disinfecting ability of HOCl is generally regarded to begreater than that of OCl−. At pH value below 7.5, HOCl is predom-inates while above pH 7.5, OCl− is the predominant species, sodisinfection is more efficient at lower pH (Snoeyink and Jenkins,1980; AWWA, 1999). Therefore, for the effective disinfection andflocculation, the addition of weak acid in the swimming pools isneeded.

The average concentration of NO3− in filling tap water in Seoul is

1.5 (1.1–1.9 mg/L) mg/L (WRISMG, 2008). Table 1 shows that NO3−

ranged from 6.6 to 23.8 mg/L for chlorine-treated water, 1.2 to22.0 mg/L for ozone/chlorine-treated water, and 10.9 to 49.2 mg/Lfor EGMO-treated water, respectively. The concentrations of NO3

−

in pool water were much higher than that in tap water. This resultimplies that a large proportion of the organic nitrogen compoundsin the pools may be derived from swimmers, such as hair, sweat,and urine (Kim et al., 2002; Li and Blatchley, 2007).

J. Lee et al. / International Journal of Hygiene and Environmental Health 213 (2010) 465–474 469

a Chlorine b Ozone/chlorine

c EGMO

CH, 10.3%

THAAs,72.6%

THANs,3.4%

TTHMs,13.7%

TTHMs,25.5%

HAA0.8%

CH, 7.1%THANs,

6.6%

CH, 8.3%THANs,

6.0%

THAAs,64.3%

TTHMs,21.4%

samp

T

bafifiothTd

cffooptr

(1o

T6

Fig. 1. Distribution of DBPs for swimming pool water

he pattern of DBP production in different disinfection methods

The concentrations of THMs (chloroform, BDCM, DBCM, andromoform), HAAs (DCAA and TCAA), HANs (DCAN, TCAN, BCAN,nd DBAN), and CH in swimming pool water samples disin-ected with chlorine, ozone/chlorine, and EGMO are summarizedn Table 2. The note in Table 2 also shows the level of DBPs in poollling the tap water in Seoul (3.9–13.5 �g/L of TTHMs, N.D.–8.3 �g/Lf THAAs, N.D.–2.8 �g/L of THANs, and 0.7–4.6 �g/L of CH, respec-ively) (WRISMG, 2008). The levels of DBPs in pools water wereigher than reported values of DBPs in pool filling the tap water.his result implies that most of the DBPs were produced duringisinfection of pool waters.

Table 2 shows that chloroform was found at the highest con-entration (approximately 90% of total THM) among the THMs,ollowed by BDCM, and the concentrations of DBCM and bromo-orm were below the limit of detection (0.2 �g/L) in chlorine- andzone/chlorine-treated swimming pool waters. The same orderf THM production was obtained in EGMO disinfection, but theroportions of each THM were different: chloroform (38.7% ofotal THMs), BDCM (26.8%), DBCM (23.7%), and bromoform (10.8%),espectively.

Among the THMs, chloroform was the dominant speciesmean levels: chlorine, 20.9 �g/L; ozone/chlorine, 7.4 �g/L; EGMO,4.5 �g/L) in pool waters treated with different disinfection meth-ds. Interestingly, the concentrations of brominated THMs, such

s,

les treated with three different disinfection methods.

as BDCM (10.11�g/L), DBCM (8.9 �g/L), and bromoform (4.1 �g/L),in the EGMO-disinfected pools were much higher than those forsamples treated with chlorine (2.1 �g/L, N.D., and N.D.) or withozone/chlorine (1.1 �g/L, N.D., and N.D.).

In the case of HANs, DCAN showed the highest concentrationsin the chlorine-, ozone/chlorine-, and EGMO-disinfection pools(74.7%, 63.7%, and 38.6% of total HANs, respectively), followedby BCAN (15.8%, 18.9%, and 35.3%, respectively), and DBCN (9.5%,17.4%, and 26.1%, respectively), and TCAN was below the limit ofdetection (0.2 �g/L). The concentrations of brominated HANs, suchas BCAN (3.5 �g/L) and DBCN (2.6 �g/L), in the EGMO-disinfectedpools were much higher than those for samples treated with chlo-rine (0.8 �g/L and 0.4 �g/L) or with ozone/chlorine (0.4 �g/L and0.4 �g/L).

The production of HANs in pool water during disinfection needsnitrogenous compounds along with organic compounds. WHOreported in the Guidelines for Safe Recreational Water Environ-ments that the most abundant nitrogenous compounds come fromsweat and urine in humans containing urea, ammonia, creatinineand amino acids (WHO, 2006). Reactions between these organic-Ncompounds and disinfectant are known to contribute to HANs for-mation in swimming pools (Li and Blatchley, 2007; Weaver et al.,

2009).

With regard to HAAs, the dominant species formed in swimmingpools treated with chlorine, ozone/chlorine, and EGMO was TCAA(69.6%, 59.3%, and 74.2% of total HAA, respectively), followed by

470 J. Lee et al. / International Journal of Hygiene and Environmental Health 213 (2010) 465–474

a b

c d

disinfection method

Chlorine Ozone/chlorine EGMO Chlorine Ozone/chlorine EGMO

Chlorine Ozone/chlorine EGMO Chlorine Ozone/chlorine EGMO

TT

HM

s (u

g/ L

)

0

20

40

60

80

100

120

disinfection method

TH

AA

s (u

g/L)

0

200

400

600

800

disinfection method

TH

AN

s (u

g/L)

0

5

10

15

20

25

disinfection method

CH

(ug

/L)

0

10

20

30

40

F s trea( hloral2 s. (Fort

Dad

Cm

(wwwoCrs

atfrTF

ig. 2. The comparison of DBPs concentration of the swimming pool water sampleb) THAAs (total haloacetic acids), (c) THANs (total haloacetonitriles), and (d) CH (c5th, 50th, 75th and 90th percentiles and points denote the 5th and 95th percentileo the web version of this article.)

CAA (30.4%, 40.7%, and 25.8%, respectively). CH was also detectedt considerable levels in all swimming pools using the differentisinfection methods.

omparison of DBP production among different disinfectionethods

Fig. 1 shows the distribution of TTHMs (total THMs), THAAstotal HAAs), THANs (total HANs), and CH in the swimming poolater samples treated with different disinfection methods. Inaters treated with chlorine, ozone/chlorine, and EGMO, THAAsere found at the highest concentrations (72.6%, 64.3%, and 60.8%

f total DBPs), followed by TTHMs (13.7%, 21.4%, and 25.5%),H (10.3%, 8.3%, and 7.1%), and THANs (3.4%, 6.0%, and 6.6%),espectively. The patterns of DBP concentrations were similar forwimming pool waters treated with all three disinfection methods.

A comparison of the concentrations of TTHMs, THAAs, THANs,nd CH in the swimming pool water samples treated with the

hree different disinfection methods is also shown in Fig. 2. Theour classes of DBPs in the swimming pools treated with chlorineanged from N.D. to 49.0 �g/L for TTHMs, 35.2 to 747.1 �g/L forHAAs, 0.8 to 14.3 �g/L for THANs, and 5.1 to 34.9 �g/L for CH.or the ozone/chlorine-treated samples, the levels ranged from

ted with three different disinfection methods: (a) TTHMs (total trihalomethanes),hydrate). The box-plots indicate the mean concentrations (red line) and the 10th,interpretation of the references to color in this figure legend, the reader is referred

N.D. to 23.5 �g/L for TTHMs, 3.0 to 111.9 �g/L for THAAs, 0.3 to4.5 �g/L for THANs, and N.D. to 1.9 �g/L for CH. In the EGMO-disinfected samples, the levels ranged from N.D. to 118.6 �g/L forTTHMs, 4.1 to 511.5 �g/L for THAAs, N.D. to 23.2 �g/L for THANs,and N.D. to 23.4 �g/L for CH. Interestingly, the mean concentra-tions of TTHMs, THAAs, THANs, and CH differed significantly amongtreatment methods (P < 0.01; Fig. 2).

Most recent studies have indicated that TTHMs are presentat the highest levels followed by THAAs, and THANs and CHwere usually detected but at lower concentrations in chlori-nated water samples (Lee et al., 2001; Rodriguez et al., 2004;Malliarou et al., 2005). However, our results indicated that THAAsconcentrations were much higher than those of TTHMs. As swim-ming pool water is continuously polluted by swimmers and isrecycled with a long replacement time, the pool waters aredisinfected frequently to prevent outbreaks of waterborne dis-ease (Kim and Weisel, 1998; Chu and Nieuwenhuijsen, 2002;Erdinger et al., 2004). Therefore, chlorine doses used in swim-ming pools are usually higher than those in drinking water. It

is reported that higher chlorine doses favor the formation ofHAAs over THMs (Singer, 1994). Due to this reason, the concen-trations of THAAs in pool water might be higher than TTHMs.Also, this result shows the indirect evidence of most frequent

J. Lee et al. / International Journal of Hygiene and Environmental Health 213 (2010) 465–474 471

Table 3Spearman’s correlation coefficients between TTHMs, THAAs, THANs, CH, and DBPsfor swimming pool water samples treated with three different disinfection methods.

TTHMs THAAs THANs CH DBPs

ChlorineTTHMs 1 0.49** 0.02 0.42* 0.58**

THAAs 1 0.02 0.36 0.95**

THANs 1 0.67** 0.09CH 1 0.51**

DBPs 1Ozone/chlorine

TTHMs 1 −0.15 0.29 0.55** 0.40*

THAAs 1 0.24 0.41* 0.80**

THANs 1 0.6** 0.33CH 1 0.63*

DBPs 1EGMO

TTHMs 1 0.20 0.42* 0.36 0.46*

THAAs 1 0.45* 0.69** 0.94**

THANs 1 0.62** 0.53**

CH 1 0.73**

DBPs 1

TTHMs, addition of chloroform, BDCM, DBCM, and bromoform; THAAs, addition ofDo

dc

ppbv

C

DwacowtTa

bprrDTmpi

C

erstpui

Table 4Spearman’s correlation coefficients of four classes of DBPs and other environmentalfactors for swimming pool water samples treated with three different disinfectionmethods.

TTHMs THAAs THANs CH DBPs

ChlorineTOC 0.55** 0.74** 0.30 0.68** 0.82**

KMnO4 consumption 0.47* 0.45* 0.39* 0.69** 0.53**

Free chlorine residual 0.21 0.32 −0.33 −0.18 0.20pH 0.04 0.05 −0.49** −0.20 0.04NO3

− 0.49** 0.54** 0.50** 0.52** 0.58**

Ozone/chlorineTOC 0.22 0.37* 0.37* 0.60** 0.52**

KMnO4 consumption 0.34 0.16 0.38* 0.7** 0.33*

Free chlorine residual 0.06 0.03 0.06 0.29 0.07pH 0.02 0.12 0.09 0.12 0.06NO3

− 0.22 0.52** 0.32* 0.63** 0.60**

EGMOTOC 0.32 0.40* 0.22 0.65** 0.39*

KMnO4 consumption 0.05 0.45* 0.25 0.63* 0.36Free chlorine residual 0.07 −0.06 −0.06 0.01 −0.03pH −0.53 −0.13 −0.44* −0.33 −0.27NO3

− −0.25 −0.53** −0.58** −0.60** −0.53**

TTHMs, addition of chloroform, BDCM, DBCM, and bromoform; THAAs, addition ofDCAA and TCAA; THANs, addition of DCAN, TCAN, BDAN and DBAN; DBPs, additionof TTHMs, THAAs, THANs, and CH.

* P < 0.05.

CAA and TCAA; THANs, addition of DCAN, TCAN, BDAN and DBAN; DBPs, additionf TTHMs, THAAs, THANs, and CH.

* P < 0.05.** P < 0.01.

isinfection of pool waters in Seoul compared to other sites andountries.

THMs also can be volatilized relatively easily from swimmingool water into the air, while HAAs are relatively nonvolatile com-ared to THMs. The amounts of splashing and the turbulence causedy swimmers’ movements could have a significant influence on theolatilization of THMs into the air (Aggazzotti et al., 1995, 1998).

orrelations between DBPs

The correlations between TTHMs, THAAs, THANs, CH, andBPs are shown in Table 3. In chlorine-treated swimming poolaters, there were moderate positive correlations between TTHMs

nd THAAs, and between TTHMs and CH with correlation coeffi-ients of r = 0.49 (P < 0.01) and r = 0.42 (P < 0.05), respectively. Forzone/chlorine-treated swimming pools, TTHMs were correlatedith CH (r = 0.55, P < 0.01). However, in the EGMO-treated samples,

he concentrations of TTHMs were not significantly correlated withHAAs or CH. Instead, a correlation was observed between TTHMsnd THANs (r = 0.42, P < 0.01).

Table 3 also shows that the strongest correlation was observedetween the concentrations of THAAs and DBPs in swimmingool waters treated with all three disinfection methods (chlo-ine, r = 0.95; ozone/chlorine, r = 0.80; EGMO, r = 0.94, P < 0.01). Thisesult was not surprising because THAA comprise the bulk of theBP values. In addition, analysis of all water samples showed thatHM were not always correlated with individual DBPs. This resultay be originated from the volatilization of THMs from swimming

ool water into the air and therefore, THM levels cannot be as goodndicator for DBPs levels in swimming pool waters.

orrelations of DBPs with other environmental parameters

The correlations between TTHMs, THAAs, THANs, CH, DBPs, andnvironmental parameters, such as TOC, KMnO4 consumption, freeesidual chlorine, pH, and nitrate were examined and the results are

hown in Table 4. TOC showed good correlations with the concen-rations of TTHMs, THAAs, THANs, CH, and DBPs (r = 0.37–0.82) inools treated with chlorine and ozone/chlorine. For pools treatedsing the EGMO disinfection method, TOC showed moderate pos-

tive correlations with THAAs, CH, and DBPs (r = 0.39–0.65). These

** P < 0.01.

observations indicated that TOC is the most important determinantin the formation of DBPs in swimming pools. KMnO4 consumptionis known as a measure of the organic content of water, and thereforethis parameter was also strongly correlated with the four classes ofDBPs for the chlorine- and ozone/chlorine-treated pools, as shownin Table 4.

Table 4 shows that TOC and DBP concentrations showed fairlygood correlations in the pool waters treated with all disinfectionmethods. This result is not surprising because DBPs are known to beproduced in the presence of high concentrations of organic mattersindicated by TOC levels during chlorination (AWWA, 1999; Kim etal., 2002; Judd and Bullock, 2003; Chen et al., 2008). Thus, the TOCconcentration should be reduced to prevent the formation of DBPsin swimming pool waters.

Interestingly, nitrate (NO3−) was highly correlated with the con-

centrations of TTHMs, THAAs, THANs, CH, and DBPs (r = 0.49–0.58)in pools treated with chlorine (Table 4). For pools disinfectedwith ozone/chlorine, nitrate showed moderate positive correla-tions with THAAs, THANs, CH, and DBPs (r = 0.32–0.63). However,in the EGMO-treated samples, nitrate was negative correlated withTHAAs, THANs, CH, and DBPs (r = −0.53 to −0.60) in pools (Table 4).It was reported that nitrate is a stable end-product in the reac-tion between chlorine and ammonia. Moreover, higher nitrate levelcan be related with the excessive bather loading combined withextended operation with insufficient dilution with fresh water(Judd and Bullock, 2003). It is also reported that ozone is also morecapable of oxidizing ammonia into nitrate (Singer and Zilli, 1975).Therefore, nitrate might be accumulated in swimming pools treatedwith chlorine and ozone/chlorine.

However, in the EGMO-treated samples, NO3− was not accumu-

lated, suggesting that chemical mechanism for the degradation oforganic nitrogen compounds by EGMO. In fact, it was found thatthe organic nitrogen compound is ultimately discharged as nitro-gen gas (N2) through the breakpoint reaction of inorganic nitrogenfragments and ammonia in EGMO disinfection method (Bradford

−

and Dempsey, 2009). This result indicates that NO3 levels can beused as good indicator for DBPs levels in swimming pools treatedwith chlorine and ozone/chlorine without measuring all DBPs.

472J.Lee

etal./InternationalJournalofH

ygieneand

EnvironmentalH

ealth213 (2010) 465–474

Table 5Comparison of trihalomethanes and haloacetic acids concentrations measured in indoor swimming pool water with the literature values.

Study Country Disinfection by-product concentration (�g/L) Pool type Disinfection method

Chloroform BDCM DBCM Bromoform DCAA TCAA

Mean Range Mean Range Mean Range Mean Range Mean Range Mean Range

Our study Korea 20.9 N.D.–45.8 2.1 N.D.–7.0 N.D. N.D. N.D. N.D. 68.3 14.1–246 180.9 19.7–636 Indoor Chlorine7.4 N.D.–21.2 1.1 N.D.–2.5 N.D. N.D. N.D. N.D. 12 N.D.–31.9 24.6 1.3–85.8 Indoor Ozone/chlorine

14.5 N.D.–40.1 10.1 N.D.–34.1 8.9 N.D.–32.3 4.1 N.D.–18.0 33.7 1.5–98.5 97.2 1.0–413 Indoor EGMOAggazzotti et al. (1995) Italy 93.7 9–179 Indoor ChlorineAggazzotti et al. (1998) Italy 33.7 25–43 2.3 1.8–2.8 0.8 0.5–10 0.1 0.1 Indoor ChlorineBerg et al. (2000) Switzerland 76 0.9–240 44.9 17.1–94.7 Indoor ChlorineCaro and Gallego (2007) Spain 95–145 2–2.4 Indoor ChlorineChu and Nieuwenhuijsen (2002) UK 121.1 45–212 8.3 2.5–23 2.7 0.67–7 0.9 0.67–2 Indoor ChlorineErdinger et al. (2004) Germany 7.1–24.8 Indoor ChlorineKim and Weisel (1998) USA 419 52–647 420 57–871 Indoor ChlorineLee et al. (2009) Korea 40.7 0.2–101.7 3.0 N.D.–10.5 0.5 N.D.–5.6 N.D. N.D. Indoor Chlorine

28.5 0.2–64.9 2.4 N.D.–5.7 0.2 N.D.–3.4 N.D. N.D. Indoor Ozone/chlorine27.3 6.8–55.6 9.8 1.6–26.9 9.1 N.D.–30.1 18.8 N.D.–36.2 Indoor EGMO

Panyakapo et al. (2008) Thailand 20.32 9.50–36.97 13.21 8.90–18.01 10.2 5.19–22.78 2.98 N.D.–2.98 Indoor ChlorineStottmeister and Naglitsch (1996)a Germany 23 1.5–192 42 3.5–199 Indoor ChlorineVillanueva et al. (2007) France 66.5 47–81.7 9.3 5.1–11.9 3.2 1.4–4.6 1.4 1–1.9 Indoor Chlorine

a Adapted from WHO (2006).

Table 6Comparison of haloacetonitriles and chloral hydrate concentrations measured in indoor swimming pool water with the literature values.

Study Country Disinfection by-product concentration (�g/L) Pool type Disinfection method

DCAN TCAN BCAN DBAN CH

Mean Range Mean Range Mean Range Mean Range Mean Range

Our study Korea 3.9 0.5–12.2 N.D. N.D. 0.8 N.D.–1.9 0.5 N.D.–0.9 16.9 5.1–34.9 Indoor Chlorine1.3 0.2–3.2 N.D. N.D. 0.4 N.D.–0.6 0.4 N.D.–0.8 3.6 N.D.–10.4 Indoor Ozone/chlorine3.5 N.D.–8.0 N.D. N.D. 3.8 N.D.–9.0 2.6 N.D.–6.8 10.2 N.D.–23.4 Indoor EGMO

Baudisch et al. (1997)a Germany 24 265 Indoor ChlorineKim, 1997 USA 110–380 Indoor ChlorineMannschott et al. (1995)a Germany 0.5–104 indoor chlorinePuchert (1994)a Germany 6.7–18.2 Indoor ChlorineStottmeister (1998)a Germany 13 0.13–148 1.7 <0.01–11 2.3 <0.01–24 Indoor Chlorine

a Adapted from WHO (2006).

e and

C

He1eactwrdmscpee(

csmtpDDwr(

iHtbotmdedD

C

mriTaoBEtTitNtot

h

J. Lee et al. / International Journal of Hygien

omparison with other studies

Tables 5 and 6 compare the concentrations of THMs, HAAs,ANs, and CH measured in this study with those reported in the lit-rature (Aggazzotti et al., 1995, 1998; Kim, 1997; Kim and Weisel,998; Berg et al., 2000; Chu and Nieuwenhuijsen, 2002; Erdingert al., 2004; WHO, 2006; Caro and Gallego, 2007; Villanueva etl., 2007; Panyakapo et al., 2008; Lee et al., 2009). As shown,hlorine is most widely used disinfection method in most coun-ries. In addition, the concentrations of THMs observed in the poolater samples in the present study were generally within the

ange reported in the literature, while HAA levels were significantlyifferent from those in other studies (Table 5). The differencesay have been due to the amounts of chlorine used to disinfect

wimming pools, differences in sample collection time relative tohlorination of the water, addition or exchange of water in theools, number of swimmers, temperature, management practices,tc. These factors are known to have a marked influence on HAA lev-ls due to the nonvolatility of these substances compared to THMsWHO, 2006).

Table 6 shows the comparisons of HANs and CH levels inhlorine-, ozone/chlorine- and EGMO-treated pool waters in thistudy and with other studies. DCAN was the dominant andost abundant HAN species in the samples treated with all

hree disinfection methods. For EGMO-treated pool water sam-les, the concentrations of brominated HANs, such as BCAN andBAN, were highest and more variable. The BCAN (3.5 �g/L) andBAN (2.6 �g/L) concentrations in the EGMO-disinfected poolsere much higher than those in the samples treated with chlo-

ine (0.8 �g/L, 0.5 �g/L) or ozone/chlorine (0.4 �g/L and 0.4 �g/L)Table 6).

The patterns of THM, HAA, and HAN concentrations were sim-lar for chlorinated and ozone-chlorinated swimming pool water.owever, samples disinfected with EGMO had higher concentra-

ions and wider variations of brominated DBPs (BDCM, DBCM andromoform in THMs; BCAN and DBAN in HANs). The higher levelsf brominated byproducts in the EGMO-treated pools were due tohe presence of bromide ions from NaCl salt (NaCl salt is obtained

ostly from seawater containing bromide ion) used in the EGMOisinfection method (Duong et al., 2003; Whitaker et al., 2003; Leet al., 2009). This result implicates that using pure salts in EGMOisinfection is important to reduce the production of brominatedBPs.

onclusions

In this study, we measured the levels of DBPs in indoor swim-ing pools treated with three different disinfection methods; the

esults indicated that the production and composition of DBPs var-ed among the three swimming pool water disinfection methods.he levels of THAAs were highest, followed by TTHMs, then CH,nd finally THANs in swimming pool water treated with chlorine,zone/chlorine, and EGMO. The brominated byproducts, such asDCM, DBCM, bromoform, BCAN, and DBAN, in pools treated withGMO disinfection showed higher concentrations and wider varia-ions than those in chlorine- and ozone/chlorine disinfected pools.OC was highly correlated with the concentrations of total DBPsn all swimming pools, indicating that TOC in pool waters washe dominant factor governing the amounts of DBP in pool water.itrate concentration also exhibited a moderate positive correla-

ion with total DBPs in swimming pools treated with chlorine andzone/chlorine, while it was negative correlated with total DBPs inhe EGMO treated samples.

Our results suggest the importance of minimizing potentiallyarmful DBPs by choosing a suitable disinfection method to main-

Environmental Health 213 (2010) 465–474 473

tain the positive health effects of swimming. Moreover, measuresto control the formation of DBPs should include application of tech-nological treatments, such as new oxidation and filtration methods,and assuring the cleanliness of swimmers.

References

Aggazzotti, G., Fantuzzi, G., Righi, E., Predieri, G., 1995. Environmental and biologi-cal monitoring of chloroform in indoor swimming pools. J. Chromatogr. A 710,181–190.

Aggazzotti, G., Fantuzzi, G., Righi, E., Predieri, G., 1998. Blood and breath analyses asbiological indicators of exposure to trihalomethanes in indoor swimming pools.Sci. Total Environ. 217, 155–163.

Alvarez-Uriate, J.I., Iriarte-Velasco, U., Chimeno-Alanis, N., Gonzalez-Velasco, J.R.,2010. The effect of mixed oxidants and powdered activated carbon on theremoval of natural organic matter. J. Hazard. Mater. 181, 426–431.

American Water Works Association (AWWA), 1999. Water Quality and Treatment:A Handbook of Community Water Supplies, 5th ed., vol. 12. McGraw-Hill, NewYork, pp. 11–42.

American Public Health Association (APHA), 1998. Standard Methods for the Exam-ination of Water and Wastewater, 20th ed. American Public Health Association,Maryland, pp. 5–13.

Baytak, D., Sofuoglu, A., Inal, F., Sofuoglu, S.C., 2008. Seasonal variation in drink-ing water concentrations of disinfection by-products in IZMIR and associatedhuman health risks. Sci. Total Environ. 407, 286–296.

Berg, M., Müller, S.R., Mühlemann, J., Wiedmer, A., Schwarzenbach, R.P., 2000. Con-centrations and mass fluxes of chloroacetic acids and trifluoroacetic acid in rainand natural waters in Switzerland. Envrion. Sci. Technol. 34, 2675–2683.

Bradford, W.L., Dempsey, R., 2009. Observation on the use of mixed oxidants inswimming pools, http://coachsci.sdsu.edu/swimming/chlorine/MIOXBrad.pdf.

Bull, R.J., Meier, J.R., Robunson, M., Ringhand, H.P., Laurie, R.D., Stober, J.A., 1985. Eval-uation of mutagenic and carcinogenic properties of brominated and chlorinatedacetonitriles: by-products of chlorination. Fundam. Appl. Toxicol. 5, 1065–1074.

Caro, J., Gallego, M., 2007. Assessment of exposure of workers and swimmersto trihalomethanes in an indoor swimming pool. Environ. Sci. Technol. 41,4793–4798.

Chen, C., Zhang, X.J., Zhu, L.X., Liu, J., He, W.J., Han, H.D., 2008. Disinfection by-products and their precursors in a water treatment plant in North China:seasonal changes and fraction analysis. Sci. Total Environ. 397, 140–147.

Chu, H., Nieuwenhuijsen, M.J., 2002. Distribution and determinants of tri-halomethane concentrations in indoor swimming pools. Occup. Environ. Med.59, 243–247.

Daniel, F.B., Schenck, K.M., Mattox, J.K., Lin, E.L.C., Haas, D.L., Pereira, M.A., 1986.Genotoxic properties of haloacetonitriles: drinking water by-products of chlo-rine disinfection. Fundam. Applied. Toxicol. 6, 447–453.

Digital Information Center for Environment Research (DICER), 2004. KoreanDrinking Water Standard Method, http://www.dicer.org/dicerDB/new/html/n3 main body 09.html.

Drees, K.P., Abbaszadegan, M., Maier, R.M., 2003. Comparative electrochemical inac-tivation of bacteria and bacteriophage. Water Res. 37, 2291–2300.

Duong, H.A., Berg, M., Hoang, M.H., Pham, H.V., Gallard, H., Giger, W., Gunten, U.V.,2003. Trihalomethane formation by chlorination of ammonium- and bromide-containing groundwater in water supplies of Hanoi, Vietnam. Water Res. 37,3242–3252.

Erdinger, L., Kühn, K.P., Kirsh, F., Feldhues, R., Fröbel, T., Nohynek, B., Garbrio, T., 2004.Pathways of trihalomethane uptake in swimming pools. Int. J. Hyg. Environ.Health 207, 571–575.

Golfinopoulos, S.K., Nikolaou, A.D., Lekkas, T.D., 2003. The occurrence of disinfectionby-products in the drinking water of Athenes, Greece. Environ. Sci. Pollut. Res.10, 368–372.

Gunten, U.V., Driedger, A., Gallard, H., Salhi, E., 2001. By-products formation duringdrinking water disinfection: a tool to assess disinfection efficiency. Water Res.35, 2095–2099.

Jo, W.K., Kwon, K.D., Dong, J.I., Chung, Y., 2005. Muti-route trihalomethane exposurein households using municipal tap water treated with chlorine or ozone-chlorine. Sci. Total Environ. 339, 143–152.

Judd, S.J., Bullock, G., 2003. The fate of chlorine and organic materials in swimmingpools. Chemosphere 51, 869–879.

Kerwick, M.I., Reddy, S.M., Chamberlain, A.H.L., Holt, D.M., 2005. Electrochemicaldisinfection, an environmentally acceptable method of drinking water disinfec-tion? Electrochim. Acta 50, 5270–5277.

Kim, H., 1997. Human exposure to dichloroacetic acid and trichloroacetic acid fromchlorinated water during household use and swimming. Ph.D. Dissertation, TheState University of New Jersey and University of medicine and Dentistry of NewJersey, Rutgers.

Kim, H., Weisel, C.P., 1998. Dermal absorption of dichloro- and trichloroacetic acidsfrom chlorinated water. J. Exp. Environ. Epidemiol. 8, 30–39.

Kim, H., Shim, J., Lee, S., 2002. Formation of disinfection by-products in chlorinated

swimming pool water. Chemosphere 46, 123–130.

Kleiser, G., Frimmel, F.H., 2000. Removal of precursors for disinfection by-products(DBPs) – differences between ozone- and OH-radical-include oxidation. Sci.Total Environ. 256, 1–9.

Korean Ministry of Culture, Sports and Tourisim (KMCST), 2004. Water quality stan-dards for swimming pool, http://www.mcst.go.kr.

4 e and

L

L

L

L

L

M

M

N

N

N

N

N

N

O

P

P

R

S

Environ. Epidemiol. 13, 17–23.White, G.C., 2009. The Handbook of Chlorination and Alternative Disinfection, 5th

74 J. Lee et al. / International Journal of Hygien

ee, K.J., Kim, B.H., Hong, J.E., Pyo, H.S., Park, S.J., Lee, D.W., 2001. A study on thedistribution of chlorination by-products (CBPs) in treated water in Korea. WaterRes. 35, 2861–2872.

ee, J., Ha, K.T., Zoh, K.D., 2009. Characteristics of trihalomethane (THM) productionand associated health risk assessment in swimming pool waters treated withdifferent disinfection methods. Sci. Total Environ. 407, 1990–1997.

i, J., Blatchley III, E.R., 2007. Volatile disinfection byproduct formation resultingfrom chlorination of organic-nitrogen precursors in swimming pools. Environ.Sci. Technol. 41, 6732–6739.

in, L.C., Daniel, F.B., Herren Freund, S.L., Pereira, M.A., 1986. Haloacetonitriles:metabolism, genotoxicity, and tumor-initiating activity. Environ. Health Per-spect. 69, 67–71.

iang, L., Singer, P.C., 2003. Factors influencing the formation and relative distri-bution of haloacetic acids and trihalomethanes in drinking water. Environ. Sci.Technol. 37, 2920–2928.

alliarou, E., Collins, C., Graham, N., Nieuwenhuijsen, M.J., 2005. Haloacetic acids indrinking water in the United Kingdom. Water Res. 39, 2722–2730.

uellner, M.G., Wagner, E.D., Mccalla, K., Richardson, S.D., Woo, Y.T., Plewa, M.J.,2007. Haloacetonitriles vs. regulated haloacetic acids: are nitrogen-containingDBPs more toxic? Environ. Sci. Technol. 41, 645–651.

akajima, N., Nakano, T., Harada, F., Taniguchi, H., Yokoyama, I., Hirose, J., Sano, K.,2004. Evaluation of disinfective potential of reactivated free chlorine in pooledtap water by electrolysis. J. Microbiol. Methods 57, 163–173.

ational Institute of Environmental Research (NIER), 2004. Korean standard methodfor the examination of water and wastewater, http://www.water.nier.go.kr.

azaoroff, W.W., Alvarez-Cohen, L., 2000. Environmental Engineering Science. JohnWiley & Sons, Inc., New York.

ieuwenhuijsen, M.J., Toledano, M.B., Eaton, N.E., Fawell, J., Elliott, P., 2000a. Chlo-rination disinfection byproducts in water and their association with adversereproductive outcomes: a review. Occup. Environ. Med. 57, 73–85.

ieuwenhuijsen, M.J., Toledano, M.B., Elliott, P., 2000b. Uptake of chlorination dis-infection by-products; a review and discussion of its implications for exposureassessment in epidemiological studies. J. Expo. Anal. Environ. Epidemiol. 10,586–599.

ikolaou, A.D., Golfinopoulos, S.K., Lekkas, T.D., Arhonditsis, G., 2004. Factorsaffecting the formation of organic by-products during water chlorination: abench-scale study. Water Air Soil Pollut. 159, 357–371.

liver, B.G., 1983. Dihaloacetonitriles in drinking water: alage and fulvic acid asprecursor. Envrion. Sci. Technol. 17, 80–83.

anyakapo, M., Soontorchai, S., Paopuree, P., 2008. Cancer risk assessment fromexposure to trihalomethanes in tap water and swimming pool water. J. Environ.Sci. 20, 372–378.

atermarakis, G., Fountoukidis, E., 1990. Disinfection of water by electrochemical

treatment. Water Res. 24, 1491–1496.

odriguez, M.J., Sérodes, J.B., Levallois, P., 2004. Behavior of trihalomethanesand haloacetic acids in a drinking water distribution system. Water Res. 38,4367–4382.

inger, P.C., 1994. Control of disinfection by-products in drinking water. J. Environ.Eng. 120, 727–744.

Environmental Health 213 (2010) 465–474

Singer, P.C., Zilli, W.B., 1975. Ozonation of ammonia in wastewater. Water Res. 9,127–134.

Snoeyink, V.L., Jenkins, D., 1980. Water Chemistry. John Wiley & Sons, Inc., USA, pp.386–403.

USACHPPM, 2006. Electrochemically generated oxidant disinfection in theuse of individual water purification devices, http://chppm-www.apgea.army.mil/WPD/PDFDocs/TIP Version 31-003 EO INFORMATION PAPER(2).pdf.

US EPA Method 524.2, 1995. Measurement of Purgeable Organic Compounds inWater by Capillary Column Gas Chromatography/Mass Spectrometry. NationalExposure Research Laboratory Office of Research and Development.

US EPA Method 552.2, 1995. Determination of Haloacetic Acids and Dalapon inDrinking Water by Liquid–Liquid Extraction, Derivatization and Gas Chromatog-raphy with Electron Capture Detection. National Exposure Research LaboratoryOffice of Research and Development.

US EPA Method 551.1, 1995. Determination of Chlorination Disinfection Byprod-ucts, Chlorinated Solvents, and Halogenated Pesticides/Herbicides in DrinkingWater by Liquid–Liquid Extraction and Gas Chromatography with Electron-capture Detection. National Exposure Research Laboratory Office of Researchand Development.

US EPA, 2006. National primary drinking water regulations: disinfectants and disin-fection byproducts Final Rule; 40CFR Parts 9, 14 and 142. Federal Register PartII, vol. 71, pp. 387–493.

US EPA, 2008. Integrated Risk Information System. http://cfpub.epa.gov/ncea/iris/index.cfm.

Uyak, V., Toroz, I., 2007. Investigation of bromide ion effects on disinfection by-products formation and speciation in an Istanbul water supply. J. Hazard. Mater.149, 445–451.

Villanueva, C.M., Gagniere, B., Monfort, C., Nieuwenhuijsen, M.J., Cordier, S., 2007.Sources of variability in levels and exposure to trihalomethanes. Environ. Res.103, 211–220.

Venczel, L.V., Arrowood, M., Hurd, M., Sobsey, M.D., 1997. Inactivation ofCryptosporidium parvum Oocysts and Clostridium perfringens spores by amixed-oxidant disinfectant and by free chlorine. Appl. Environ. Microbiol. 63,1598–1601.

Waterworks Research Institute Seoul Metropolitan Government (WRISMG), 2008.http://wri.seoul.go.kr.

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 swimmingpools. Water Res. 43, 3308–3318.

Whitaker, H., Nieuwenhuijsenm, M.J., Best, N., Fawell, J., Gowers, A., Elliot, P., 2003.Desciption of trihalomethane levels in three UK water suppliers. J. Expo. Anal.

ed. John Wiley & Sons, Inc., New Jersey, pp. 528–571.World Health Organization (WHO), 2006. Guidelines for Safe Recreational

Water Environments, http://www.who.int/water sanitation health/bathing/srwe2chap4.pdf.