International Journal of Hygiene and Environmental Health 214 (2011) 461–469

Contents lists available at ScienceDirect

International Journal of Hygiene and

Environmental Health
journal homepage: www.elsevier.de/ijheh

Health effects of disinfection by-products in chlorinated swimming pools

Arnaud Florentin a,∗ , Alexis Hautemanière a , Philippe Hartemann a,b
a
DESP, Nancy Université - Faculté de Médecine de Nancy, 9 Avenue de la forêt de Haye BP 184, 54 505 Vandœuvre-lès-Nancy Cedex, France
b
Inserm U954, 9 Avenue de la forêt de Haye BP 184, 54 505 Vandœuvre-lès-Nancy Cedex, France

a r t i c l e i n f o a b s t r a c t

Article history: Increased attendance at swimming pools is correlated with higher input of organic and minerals pollu-
Received 31 December 2010 tants introduced by swimmers in the swimming pool water. In most swimming pools, microbiological
Received in revised form 17 July 2011 control is performed by disinfection with the addition of chlorine. Chlorine is now well-known to lead to
Accepted 28 July 2011
the formation of many disinfection by-products (DBPs) including trihalomethanes and chloramines. The
hypothesis of a link between the presence of eye and skin irritation syndromes in swimmers and contact
Keywords:
with swimming pool water treated with chlorine was initially proposed by Mood (1953). During recent
Disinfection by-products
decades many epidemiological studies have described the importance of DBPs generated with natural or
Chlorinated swimming pools
Trihalomethanes
imported organic matter present in water. Many of these DBPs are suspected to be toxic or even carcino-
Chloramines genic. Trihalomethanes and haloacetic acid families are the most studied but others DBPs, like chloral
Haloacetic acids hydrate, haloacetonitriles, N-nitrosodimethylamine and the bromate ion, are emerging compounds of
Risk assessment interest. Epidemiological data about the risk of cancer are still controversial. However, numerous publi-
cations highlight a toxic risk especially the risk of allergy and respiratory symptoms for babies and elite
swimmers. The few publications dedicated to risk assessment do not suggest increased risk, other than
for elite swimmers. These publications are likely to underestimate the risk associated with DBPs because
of the lack of data in the literature precludes the calculation of risk associated with certain compounds or
certain pathways. Thus for regulations, the need to take into account the risks associated with disinfec-
tion by-products is now important without forgetting the need of the control of microbiological hazards
in swimming pools.
© 2011 Elsevier GmbH. All rights reserved.

Introduction pathogens. Microbiological monitoring of water quality was intro-

Swimming pools have been experiencing growing attendance
for the past three decades. The European Union is ranked sec-
ond with about 4.5 million pools behind the United States (about
9 million) (Francesco, 2010). This development is linked to the
popularity of swimming for leisure activities or exercises. Due to
the complexity of swimming pool water chemistry, human expo-
sure and potential health risks are still poorly known to date.
Swimming pool water chemistry deals with the composition of
the source water, the transformation of this water (e.g. disinfec-
tion processes) and the actions in the swimming pool (disinfection,
swimmers, etc.). Biological health risks were among the first taken
into account. Swimmers introduce undesirable biological mat-
ter (e.g. skin, sweat, urine or fecal matter) possibly containing
∗ Corresponding author at: Département Environnement et Santé Publique
(D.E.S.P.), Service d’Etudes et de Recherches en Environnement et Santé (S.E.R.E.S.),
Faculté de Médecine, 9, avenue de la Forêt de Haye, BP 184, 54 505 Vandœuvre-lès-
Nancy, France.
E-mail address: arnaud.florentin@medecine.uhp-nancy.fr (A. Florentin).
duced to ensure that water is not harmful to human health. In
most swimming pools, microbiological control is performed by dis-
infection with the addition of chlorine (as a gas or bleach). The
disinfection properties of free chlorine are linked to its oxidant
capacity. It is well-known that chlorination of drinking or swim-
ming pool water leads to the formation of disinfection by-products
(DBPs) including chloramines (referred as combined chlorine) or
trihalomethanes (THMs) (WHO, 2006). Some of these chemical
compounds have been associated with health effects. The hypoth-
esis of a link between the presence of eye and skin irritation
syndromes in swimmers and contact with swimming pool water
treated with chlorine was initially proposed by Mood in 1953. This
author developed a theory that the main causal agent of eye irrita-
tion was not chlorine but a combination of chlorine and ammonia
(Mood, 1953). This hypothesis has since been confirmed by other
authors (Bernard et al., 2009; Jacobs et al., 2007; Massin et al., 1998;
Momas et al., 1993; Voisin et al., 2010). Other than some remaining
microbiological risks such as Legionella sp. or Cryptosporidium sp.,
the microbiological quality of swimming pool water is now very
good, with little risk to swimmers (WHO, 2006). Consequently the
potential health risks from chemical exposures linked to swimming

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doi:10.1016/j.ijheh.2011.07.012
462 A. Florentin et al. / International Journal of Hygiene and Environmental Health 214 (2011) 461–469

Table 1
Nitrogen compounds introduced by a swimmer in the swimming pool water (WHO, 2006; AFFSET, 2010).

Nitrogen-containing compounds Sweat Urine By swimmer a

Mean content Portion of total Mean content Portion of total Estimated Estimated
(mg L−1 ) nitrogen (%) (mg L−1 ) nitrogen (%) minimal input maximal input
(mg) (mg)

Urea 680 68 10,240 84 320 840

Ammonia 180 18 560 5 30 60
Amino-acids 45 5 280 2 15 50
Creatinine 7 1 640 5 10 25
Other compounds 80 8 500 4 20 45
Total nitrogen 992 100 12,220 100 400 1000
a
Calculated using Beech (1980) excretion values of sweat and urine.

pools now seem to be a priority. Many recent papers have described
the health consequences linked to these by-products. In this paper,
we will present a review of the literature about the formation of
DBPs, their toxicity, the epidemiological data and finally the risk
assessment for swimming pools.
Formation of disinfection by-products (DPBs)
To control microbiological contamination of pool water, disin-
fectants are used. As with tap water, swimming pool water can
be treated with a variety of disinfectants (chlorine based, bromine
based, ozone and copper/silver). However, also like tap water,
swimming pool water is most often treated with chlorine based
disinfectants (chlorine gas (Cl2 ), sodium or calcium hypochlorite
(NaOCl or Ca(OCl)2 ), chlorinated isocyanurate, chlorine dioxide
(ClO2 )).
The generation of chlorine related DBPs is relatively well known
in tap water. The formation of DBPs occurs with natural or imported
(xenobiotic) organic and inorganic materials present in the water.
In drinking water, natural organic matter is represented by the
total organic carbon (TOC) which includes humic acids, fulvic acids,
hydrophobic acids and hydrophilic acids. In swimming pool water,
we can find this natural organic matter and its DBPS imported
with tap water but external inputs including the swimmers are the
most important source. These additional sources of mineral and
organic compounds will serve as precursors to DBPs. The swim-
ming pool water is characterized by the important external input
of compounds. These compounds include, among others, chemical
and organic materials of cosmetics and sun screens, human body
substances (perspiration, urine, fecal pollution, mucus, skin parti-
cles, hair, etc.), algae and other biota. In case of outdoor swimming
pools, leaves and others materials from surrounding trees (WHO,
2006). In an attempt to account for the contribution of pollution
by bathers, the notion of “equivalent swimmer” was defined as the
statistical activity of n bathers, equivalent to an individual swim-
mer who would bath alone, continuously for 1 h (Seux, 1988). Thus,
the specific flux of pollution provided by one equivalent swim-
mer would be between: 0.55 and 1.0 g of total organic carbon;
0.8 and 0.9 g of Kjeldahl nitrogen; 0.15 and 0.20 g of nitrogen as
ammonia; 1.0 and 1.6 g of urea. According to Beech, a swimmer
staying 2 h in a pool excretes between 20 and 80 mL of urine and
produces between 0.1 and 1 L of sweat for elite swimmers (Beech,
1980). The urine and sweat, consisting essentially of nitrogen com-
pounds (Table 1), can interact with the disinfectant used for water
treatment of swimming pools (WHO, 2006). Some of these interac-
tions may lead to the formation of by-products potentially toxic to
humans.
Despite the public health relevance and long history of chemi-
cal disinfection for swimming pools, the scientific literature is poor
about the generation of DBPs in swimming pool water. Chlorine
related DBPs are the most studied because of their significant use
in the world (AFFSET, 2010; WHO, 2006). However, other disinfec-
tants such as ozone produce also potentially toxic by-products such
as hydrogen peroxide and aldehydes (AFFSET, 2010; WHO, 2006).
Lee et al. (2010) confront three types of disinfection in swimming
pools: chlorine alone, ozone–chlorine association and electro-
chemically generated mixed oxidants (EGMO). DBPs concentration
DBPs vary in terms of concentration and type. For example,
EGMO generate more brominated DBPs than the two others
disinfectants.
Disinfection by-products can be divided in three groups:
organohalogenics, non-halogenic organics and inorganics. Major
DBPs associated with chlorine disinfectant in tap water are pre-
sented in Table 2. More than 600 DBPs have been identified
in tap water, and many of them are mutagenic or carcinogenic
(Richardson et al., 2007). Until recently, research was focused
specifically on the presence of THMs or chloramines in the water
and air of swimming pool. Two studies (Richardson et al., 2010;
Zwiener et al., 2007) describe the DBP’s composition in swim-
ming pool water of European countries. Most THMs were already
known due to their presence in tap water but also new DBPs not
present in tap water were found in pool water such as nitrogen-
containing DBP’s (haloamides, halonitriles, haloamines, etc.). The
authors associated the presence of nitrogen-containing DBPs to
nitrogen-containing precursors provided by swimmers.
Several publications (AFFSET, 2010; Hartemann et al., 1988;
WHO, 2006) highlight, for chlorinated disinfection in pools, that
some DBPs are present in a relatively high concentration in the air
and the water: trichloramine, trihalomethanes (THMs), haloacetic
acids (HAAs), chloral hydrate and haloacetonitriles (HANs).

Table 2
Summary of DBPs for chlorinated disinfectants (WHO, 2006).

Disinfectant Organohalogenic disinfection Non-halogenic organic Inorganic disinfection

by-products disinfection by-products by-products

Chlorine (Cl2 )/hypochloric acid (HOCl)
Trihalomethanes, haloacetic acids, Aldehydes, alkanic acids, Chlorate (particularly the
halocetonitriles, chloral hydrate, benzene, and carboxylic acids application of hypochloric acid)
chloropicrin, halophenols,
N-chloramines, halofuranones, and
bromohydrins
 A. Florentin et al. / International Journal of Hygiene and Environmental Health 214 (2011) 461–469 463

Table 3
Representative compounds of the three groups of HAAs.

Monohaloacetic acids Dihaloacetic acids Trihaloacetic acids

Monochloroacetic acid (MCA) Dichloroacetic acid (DCA) Trichloroacetic acid (TCA)

Monobromoacetic acid (MBA) Dibromoacetic acid (DBA) Bromodichloroacetic acid
Bromochloroacetic acid Chlorodibromoacetic acid
Tribromoacetic acid

Chloramines Trihalomethanes (THM)

In swimming pools, the bathers and the tap water bring dis-
solved organic nitrogen (DON) (i.e. creatinine and amino-acids)
and inorganic nitrogen compounds (i.e. ammonia). Mineral nitro-
gen compounds react with free chlorine to form mono, di and
trichloramine. DON compounds can react with free chlorine to form
organochloramines, which have little or no bactericidal activity.
The general nature of the reactions between DON and free chlorine
(HOCl) is represented by this equation in which R symbolizes side
chains: HClO + R-NH2 → H2 O + R-NHCl (organic monochloramine).
Further reactions with HOCl lead to the formation of di- and trichlo-
ramines.
The mineral chloramines are soluble in water and have the
capacity to transfer to the gaseous phase. The production and
the distribution of monochloramine (NH2 Cl), dichloramine (NHCl2 )
and trichloramine (NCl3 ) is highly dependent upon pH, the ratio
of chlorine to organic-nitrogen, temperature and contact time.
The formation of monochloramine dominates with a pH between
approximately 7.5 and 9.0 and chlorine to ammonia–nitrogen ratio
of 3–5:1. The dichloramine’s and trichloramine’s production dom-
inate for a pH between 4 and 6 and below 4.4 respectively and
for chlorine to ammonia–nitrogen ratio of 5–7.6:1 and above 7.6:1,
respectively. The generation of chloramine decreases with the tem-
perature or the contact time (Wolfe et al., 1984). The volatility of
trichloramine is about 300 higher than monochloramine.
Urea (NH2 CONH2 ) represents up to 85% of the nitrogen con-
tent in urine and about 60% of the nitrogen pollution introduced
by swimmers (De Laat et al., 2011). Urea reacts with chlorine to
form carbon dioxide, dichloramine and trichloramine. The reac-
tion is slow and takes place over several tens of hours. Ammonia
(NH3 ) is the second nitrogen compound introduced by swimmers.
Ammonia reacts rapidly with chlorine to form gaseous nitrogen,
monochloramine, dichloramine, water and hydrochloric acid. The
degradation of creatinine is complex and slow, its products include
chloramines (De Laat et al., 2009).
As for chloramines, THMs are generated from the complex
reaction between chlorine and naturally present or imported
organic matter. Trihalomethanes (THMs) have one atom of carbon
where three hydrogen atoms are substituted by a halogen atom
(chlorine, bromine, fluorine, or iodine). Thus, the composition
of THMs can be represented by this formula: CHX3 , where X
symbolizes a halogen atom. Parameters influencing the formation
of THMs include: organic matter (and its precursors), chlorine
concentration, contact time, water pH, temperature, and bromide
ion concentration (Amy et al., 1987). THMs formation increases
with pH and vice versa. In the presence of bromides, brominated
THMs are formed preferentially. This is linked to the fact that the
bromination reaction is more rapid than chlorination (Hartemann
et al., 1988; Hu et al., 2010; Judd and Jeffrey, 1995). The same
study highlights a tendency to an increase of overall quantities
of THMs in presence of bromide ion. A recent study (Richardson
et al., 2010) has confirmed that the most commonly present THMs
in swimming pool water (like tap water) are chloroform (CHCl3 ),
bromodichloromethane or dichlorobromomethane (CHBrCl2 )
(BDCM), dibromochloromethane or chlorodibromomethane
(CHClBr2 ) (DBCM), and bromoform (CHBr3 ).
Haloacetic acids (HAAs)
Like THM, the formation of HAAs is generated from the complex
reaction between organic carbon matter and disinfectant. HAAs
are based on acetic acid (carboxylic acid) in which halogen atom
can take the place of hydrogen atom. In tap water as in swim-
ming poll water (Health Canada, 2008b; Richardson et al., 2010),
nine common HAAs can be found. There are divided into 3 groups
according to the number of hydrogen substituted atoms: mono-
haloacetic acids, dihaloacetic acids and trihaloacetic acid. The major
representatives of the 3 groups are presented in Table 3. In swim-
ming pool water, dichloroacetic acid (DCAA) and trichloroacetic

Table 4
Concentration of major DBPs in indoor chlorinated swimming pools.

WHO (2006) AFFSET (2010) Richardson et al. (2010)

Air
Chloroform (mg m−3 ) 0.170 0.004–0.136 0.0119–0.0616
Trichloramine (mg m−3 ) 0.2–0.3 0.17–0.43
Water
Chloramines (mg L−1 ) 0.1–1.5a <0.21–1.39b
Trihalomethane (␮g L−1 )
Chloroform 1.7–1630 6.2–140 8.4–20.8
Bromodichloromethane < 0.1–100 1.5–8.7 9.3–26.8
Dibromochloromethane 0.05–30 0.3–3 6.5–22.6
Bromoform 0.03–14 <0.5–2 3.0–16.5
Haloacetic acids (␮g L−1 )
Monochloroacetic acid 2.6–81 9.2–110
Dichloroacetic acid 1.5–192 77–1000
Trichloroacetic acid 3.5–199 104–320
Monobromoacetic acid <0.5–3.3 –
Dibromoacetic acid 0.2–7.7 <5–16.5
a
Mineral and organic chloramines.
b
Mineral chloramine only.
464 A. Florentin et al. / International Journal of Hygiene and Environmental Health 214 (2011) 461–469

acid (TCAA) are the most common. For memory, the formula of Table 5
IARC and US-EPA statements about disinfection by-products.
acetic acid is CH3 COOH and the formula of monochloroacetic acid
(MCA) is ClCH2 COOH. The chlorinated HAAs are generated directly Disinfection by-products IARC evaluationa US-EPA evaluationa
from hypochlorous acid (HOCl) and hypochlorite ion (OCl− ). The Chloramines
brominated HAAs are generated indirectly. HOCl and OCl− react Monochloramine 3 D
with the bromide ions to form hypobromous acid (HOBr) which Trihalomethanes (THMs)
will react with natural organic matter to form brominated HAAs. In Chloroform 2B B2
Bromoform 3 B2
swimming pool water (Richardson et al., 2010), chlorinated HAAs
Bromodichloromethane 2B B2
dominate by 2–20 times more than brominated HAAs due to the Dibromochloromethane 3 C
low concentration of bromide. HAAs formation tends to decrease Haloacetic acids (HAAs)
with increasing pH. Longer contact times and higher water tem- Monochloroacetic acid ∅ ∅
Monobromoacetic acid ∅ ∅
peratures increase HAAs formations (Kanan and Karanfil, 2011).
Dichloroacetic acid 2B B2
Dibromoacetic acid ∅ ∅
Haloacetonitriles (HANs) Trichloroacetic acid 3 C
Haloacetonitriles (HANs)
HANs are the result of a complex reaction between dissolved Dichloroacetonitrile 3 C
Trichloroacetonitrile 3 ∅
organic nitrogen (DON) (i.e. creatinine and amino-acids) and free
Bromochloroacetonitrile 3 ∅
chlorine. HANs are based on acetonitrile (CH3 -CN) in which halogen Dibromoacetonitrile 3 ∅
atom can take the place of hydrogen atom. Five haloacetonitriles Others
have been measured in swimming pool water by a recent study Bromate ion 2B B1
Chloral hydrate 3 C
(Richardson et al., 2010): bromoacetonitrile, dichloroacetonitrile,
N-nitrosodimethylamine 2A B2
bromochloroacetonitrile, dibromoacetonitrile, and trichloroace-
a
tonitrile. IARC 2010 and IRIS EPA 2010.

Others DBPs of interest mainly affected by the monochloramine/dichloramine ratio and

As mentioned by Richardson et al. (2010), several others families
of DBPs can be found in swimming pools water. Also, some DBPs
have not been yet identified. Nevertheless, these other DBPs are
less known by the scientific community as they do not appear in
tap water and so of lower priority for the research. Among these
we can cite the aldehydes, the chloropicrin, the haloketones, the N-
nitrosodimethylamine (NDMA), the chloral hydrate or the bromate
ions.
As we discussed there are various mechanisms of formation of
DBPs The parameters that influence the formation of DBPs can be
summarized as the type of disinfectant, the disinfectant dose, the
disinfectant residue, the nature of the material in water and the
circumstances of disinfection (reaction time, temperature, and pH).
The study of Lee et al. (2010) describes the difference in DBPs forma-
tion between three types of disinfectant chlorine, ozone followed
by chlorine as a secondary disinfectant and electrochemically gen-
erated mixed oxidants (EGMOs). The DBPs were likely the same and
were dependent of the total organic matter, the pH, the temper-
ature. The EGMOs disinfectant generates more brominated DBPs.
The concentration of major DBPs found in swimming pool water is
presented in Table 4.
Toxicology of DBPs
The toxicology of DBPs present in tap water has been actively
studied. Among these, we found the four major families of swim-
ming pools water DBPs: chloramines, trihalomethanes (THMs),
haloacetic acids (HAAs), and haloacetonitriles (HANs). In recent
years, the toxicity of the newly discovered DBPs has been stud-
ied as NDMA, chloral hydrate or the bromate ion. The IARC and
US-EPA classification of the majors DBPs of swimming pool water
are resumed in Table 5.
Chloramines
No data about toxicity of di-, tri- and organo-chloramine can
be found in the literature. Chloramines are suspected to have a
major role in causing irritation of the eyes and respiratory tract.
One study highlighted irritation in rats by inhalation of trichlo-
ramine (Barbee et al., 1983). The odor and taste of water is
the trichloramine concentration. The literature is more abundant
on monochloramine to link with its use as a disinfectant (Abdel-
Rahman et al., 1983) described the kinetics of monochloramine
with 36 Cl after oral administration in rats. The half-life absorp-
tion was 2.49 h and the elimination from plasma was 38.8 h. The
peak plasma level was reached in 8 h. Monochloramine’s activity
was the highest in the blood and the lowest in the liver, ileum
and fat. In one human study (Kotiaho et al., 1992), most of the
monochloramine ingested from drinking water seems to reach
the stomach intact. However, monochloramine is rapidly degraded
by stomach fluid so monochloramine is not expected to enter
the systemic circulation. In animals, in vivo subchronic studies
highlight a weight loss of the body and also some organs such
as the liver (Daniel et al., 1990). Two human studies (Lubbers
et al., 1982; Wones et al., 1993) fail to demonstrate a toxic effect
of monochloramine following oral administration (0–24 mg L−1 ).
A non-volunteer exposure of 100 dialysis patients to monochlo-
ramine of water led to the development of haemolytic anemia in
41 patients (Tipple et al., 1988). The haemolytic anemia is linked
with monochloramine exposition because monochloramine oxi-
dizes haemoglobin to methaemoglobin and induces damage to the
hexose monophosphate shunt (HMPS), which protects the red cells
from oxidant damage (Kjellstrand et al., 1974).
To date, no data on carcinogenicity, genotoxicity, mutagenicity,
reproductive toxicity and teratogenicity of trichloramine is men-
tioned in the literature.
Trihalomethanes (THMs)
THMs are generally well absorbed, metabolized, and rapidly
eliminated by mammals after oral or inhalation exposure. THMs
are distributed throughout the whole body, with levels being high-
est in the fat, blood, liver, kidneys, lungs, and nervous system (IPCS,
2000). An important number of tissues can metabolize THMs; the
most important being the liver. THMs are metabolized primarily to
carbon dioxide and/or carbon monoxide.
Chloroform is the most studied of THMs. Chloroform is absorbed
through the skin, the respiratory tracts. Humans absorbed at least
50% of the air concentration by inhalation (Fry et al., 1972). A signif-
icant dermal absorption of chloroform from water while showering
has been demonstrated (Jo et al., 1990). Distribution is dependent
 A. Florentin et al. / International Journal of Hygiene and Environmental Health 214 (2011) 461–469
on exposure route; extrahepatic tissues receive a higher dose from
inhaled or dermally absorbed chloroform than from ingested chlo-
roform. Placental transfer of chloroform has been demonstrated
in several animal species and humans (Dowty et al., 1976). Chlo-
roform has two metabolism pathways: oxidation via cytochrome
P450-dependent activation step and reductive pathway associ-
ated with theta-class glutathione-S-transferase T1-1 (GSTT1-1).
The metabolism of chloroform generates some toxic metabolites
such as phosgene (Health Canada, 2006). The first elimination path-
way is the elimination of unchanged form by the expired air (IPCS,
2000). At acutely toxic doses, chloroform induces central nervous
system depression and cardiac effects. In animals, subchronic oral
or respiratory exposure induced liver and renal toxicity, lesions of
the nasal epithelium (Larson et al., 1996, Templin et al., 1996a,b,
1998). In mice and rats, chronic exposure to chloroform induces an
increase in the incidence of kidney tumors (Jorgenson et al., 1985).
No teratogen, reproductive or development effects have been found
in rodents and non-rodents.
As with chloroform, brominated THMs are metabolized into
phosgene or brominated-analogues of phosgene. One study
assessed the pharmacokinetics of BDCM in humans. This study
showed that BDCM occurred at much higher concentrations in the
blood after dermal exposure compared with oral exposure (Leavens
et al., 2007). In subchronic studies in animals, bromoform, BDCM
and DBCM were found to be hepatotoxic and nephrotoxic. DBCM
has also demonstrated cardiotoxicity in rats. (French et al., 1999;
IPCS, 2000). In one chronic assay, BDCM induced an increased
incidence of renal tumors (NTP, 1987). No actual study has demon-
strated a carcinogenicity potential of bromoform and DBCM. The
mutagenicity of brominated THMs is linked with the pathway of
activation GSTT1. No effect of bromoform on reproduction or fer-
tility has been demonstrated in animal studies. DBCM and BDCM
exposition of the mother, a lower weight of newborns and viability
of neonates was observed for rodents.
Haloacetic acids (HAAs)
HAAs are rapidly absorbed into the bloodstream from the
gastro-intestinal tract following oral exposure in both rats and
humans. Dermal absorption is of very minor or no significance
(Health Canada, 2008b). The authors related the low absorption
to the ionization form of the HAAs tested. The main forms of HAAs
are metabolized to the simplest form (MCA or MBA) and there-
after degrade to oxalic acids and carbon dioxide. MCA, DCA and
TCA are primarily distributed in the liver and the muscles but can
also be found in all tissues. They are rapidly metabolized or excreted
unchanged in the urine. Following sub-chronic exposure to MCA,
mice and rats develop hepatic lesions and cardio, hepatic and renal
lesions (Bryant et al., 1992). Long-term administration with MCA
failed to produce tumors in rodents. DCA, TCA and DBA produced
liver tumors in rodents. In rats treated with DBA, tumors in other
organs were detected (Health Canada, 2008b). DCA and TCA induce
developmental and teratogen effects like a lower weight of new-
borns, cardiovascular and urogenital malformations. DCA and DBA
induce reprotoxic effects represented by lower sperm numeration
(Health Canada, 2008b).
Chloral hydrate
After ingestion, chloral hydrate is metabolized firstly into
trichloroethanol by erythrocytes and plasma esterase and secondly
into trichloroacetic acid by the liver. In animals and humans, chlo-
ral hydrate causes sedation and hypnotic. Oral administration of
high doses (2.5 g) causes stomach irritation, nausea and vomiting or
gastrointestinal bleeding and gastric perforations (Health Canada,
2008a). In vitro assays demonstrated genotoxic effects (Harrington-
465
Brock et al., 1998) and 3 studies in mice showed the induction of
liver tumors (Daniel et al., 1992; Leakey et al., 2003). In humans,
there is no study to date demonstrating a carcinogenic effect chlo-
ral hydrate. There are very poor data about reproductive toxicity
and teratogenicity.
Epidemiological data
Toxicological data on animals or humans are usually based on
studies of single agents. As discussed above, tap and swimming pool
waters contain complex mixtures of DBPs. Epidemiological stud-
ies tend to describe the adverse effects of global DPBs mixtures.
Most available studies focus on the tap water. However, the com-
parability of the two types of water may appear limited due to the
difference in content and presence of DPBs and in the ways of expo-
sure. Indeed, Richardson et al. (2010) emphasized higher levels of
chloramine and THMs in swimming pool water and the presence
of compounds were not identified in tap water. Nevertheless, the
same study attributes an equivalent mutagenicity in the two types
of water (Richardson et al., 2010). Firstly, we will discuss epidemio-
logical studies focused on carcinogenicity and then epidemiological
evidence of other health effects.
Carcinogenicity
As previously reported, some DBPs are classified by IARC or US-
EPA as possibly carcinogen for humans (Table 5). The decisions are
essentially due to the lake of epidemiological studies at the time
of their reaction. They are a lot of studies where a link between
bladder cancer and consumption of tap water has been demon-
strated (Costet et al., 2011; Rahman et al., 2010). Costet et al. (2011)
meta-analysis includes 3 European case–controls studies (France,
Finland and Spain). This study analyzes the relation between total
THMs levels, duration of exposure to chlorinated surface water,
cumulative total THMs ingestion and bladder cancer risk. For the
relation between average residential total THMs level and risk of
bladder cancer in men, an odds ratio of 1.27 (CI: 1.03–1.58) was
found similar as in North-American studies (OR 1.31) (Cantor et al.,
1998; King and Marrett, 1996; Lynch et al., 1989). Two others stud-
ies (Villanueva et al., 2006, 2007) emphasized a relation between
tap water exposure (ingestion, showering) and bladder cancer. In
this study, an average exposure to trihalomethanes (>35 ␮g/day) is
linked with an odds-ratio of 1.61 (CI: 1.06; 2.44). Cantor et al. (2010)
studied the relation between polymorphism of three enzymes
implicated in the metabolism of THMs and HAAs. This study geno-
typed the subjects of the case–control study of Villanueva et al.
(2007) for the enzymes GSTT1, GSTZ1 and CYP2E1 and highlighted
the important role of brominated THMs and HAAs relative to muta-
genicity. A combined genotype present in 25% of the population of
western Europe and U.S. putting them at a 6-fold increased risk
for bladder cancer from using chlorinated water-primarily from
bathing, swimming and showering.
Two others studies linked tap water consumption with an
increased risk of colorectal cancers (Nieuwenhuijsen et al., 2009;
Rahman et al., 2010). Rahman et al. (2010) perform a meta-analysis
on colon and rectal cancer risk. This meta-analysis includes 13 stud-
ies (3 cohorts and 10 case–controls). The pooled RR estimates were
1.27 (1.08–1.50) and 1.30 (1.06–1.59) for colon and rectal cancer
respectively. The risk increases with the concentration of THMs and
the duration of exposure.
Most of the epidemiological studies do not target the use of
swimming pools. Only the two studies of Villanueva et al. empha-
sized a link between bladder cancers, tap water consumption and
swimming pools attendance for Spain’s population. They have
466 A. Florentin et al. / International Journal of Hygiene and Environmental Health 214 (2011) 461–469
established that the attendance of swimming pools is associated
with an odds ratio of 1.6 (CI: 1.2–2.2) (Villanueva et al., 2006, 2007).
Only one study can be found in the literature about the geno-
toxicity of swimming pool water on humans. This study (Kogevinas
et al., 2010) collected blood, urine and exhaled air samples from 49
adults before and after they swan for 40 min in an indoor chlori-
nated pool. Genotoxicity was then estimated on blood lymphocytes
(Comet assay, Micronucleus assay) and urine (Ames assay). In this
analysis genotoxicity was shown to be increased and associated
with brominated THMs and not chloroform. An unpublished study
by the authors has established similar results with blood lympho-
cytes of elite’s swimmers.
Very few epidemiological studies are available on the rela-
tionship between cancer incidence and attendance of pools.
Nevertheless, the results of studies on drinking water induce a
reasonable doubt that further studies should elucidate.
Others health’s effects: asthma and respiratory symptoms
The literature is rich with epidemiological studies on respira-
tory irritation induced by swimming. This is certainly due to the
frequency of complaints for eyes and respiratory irritation by per-
sonal of indoor pools (Jacobs et al., 2007; Massin et al., 1998).
Studies on elite swimmers were among the first to suggest that
the chlorinated atmosphere of indoor pools could be detrimen-
tal to the lung by increasing the risk of asthma, bronchial hyper
reactivity and airways inflammation (Bernard et al., 2007; Fisk
et al., 2010; Helenius et al., 1998, 2002; Helenius and Haahtela,
2000). In two studies, the presence of chloramines in the air of
swimming pools was associated with an increased prevalence of
allergic symptoms (conjunctivitis, rhinitis, laryngitis) and asthma
in elite swimmers (Goodman and Hays, 2008; Thickett et al., 2002).
In three studies (Bernard et al., 2008; Carbonnelle et al., 2002,
2008), the link between exposure to trichloramine during swim-
ming and lung alteration (proteins, epithelium) were inconsistent.
One recent paper failed to demonstrate any change in respiratory
biomarkers after 40 min swimming in chlorinated indoor pools
(Font-Ribera et al., 2010). Elite swimmers are not necessarily to
the most exposed group in swimming pools. Lifeguards and others
workers spending many hours a day near the water were checked
for health status (Jacobs et al., 2007; Massin et al., 1998; Thickett
et al., 2002). Jacobs et al. (2007) showed that the lifeguards have a
greater risk of suffering from sinusitis, sore throat or chronic cough
that the employees less exposed to byproducts of disinfection such
as reception or food service staff. This study also shows that the pool
staff is at 40% increased risk of developing bronchial spasms and 7
times more likely to suffer from effort dyspnea than the general
population.
Children, in particular babies, are a potential over-risked pop-
ulation because of the immaturity of the respiratory tract. They
may experience acute and chronic effects. Few studies on chil-
dren attending indoor chlorinated swimming pools have shown
that exposition to trichloramine can damage the lung epithelium
and promote the development of asthma, particularly among chil-
dren with higher concentrations of total serum immunoglobin
IgE (Bernard et al., 2003, 2007; Bernard and Nickmilder, 2006;
Carbonnelle et al., 2002). Other studies performed on recreational
swimmers have provided further evidence that exposure to indoor
chlorinated pools might contribute to the development of allergic
diseases (Kohlhammer et al., 2006; Lagerkvist et al., 2004; Stav and
Stav, 2005). A recent paper (Schoefer et al., 2008) demonstrated,
during a 6-year follow-up of a prospective birth cohort study, some
relationships between swimming pool attendance and health prob-
lem for swimming babies. Babies who did not participate in baby
swimming programs had lower rates of infection in the first year
of life (diarrhea: OR 0.68; otitis media: OR 0.81; airways infections:
OR 0.85). No clear association could be found between late or non-
swimmers and atopic dermatitis or hay until the age of 6 years,
while higher rates of asthma were found OR: 2.15. All these stud-
ies are cross-sectional studies. Only one prospective cohort study
can be found in the literature (Font-Ribera et al., 2011). This study
included 5738 children of Avon’s county in England born in 1991
and 1992. Swimming pool attendance, asthma and allergic symp-
toms were collected by questionnaire. Swimming pool attendance
in infantile and childhood were not associated with increase of
asthma and others allergic symptoms at 7 and 10 years (OR: 0.88
and 0.5). In addition, swimming pools attendance was associated
with increased lung function and lower risk of asthma symptoms.
To note, no data on swimming pools including DBPs dose was
described in this publication.
One paper took into account outdoor swimming pools. Outdoor
swimming pools are usually disinfected with chlorinated isocyanu-
rates as they are more resistant to UV degradation than chlorine.
(Bernard et al., 2008) illustrated a significantly increase of asthma
with the lifetime number of hours spent in outdoor pools by up
to four and eight times, respectively, among adolescents with the
highest attendance (>500 h) and a low exposure to indoor pools
(>250 h). Use of residential outdoor pools was also associated with
higher risks of elevated exhaled nitric oxide and sensitivity to car
or house dust mite allergens. Thus even outdoor chlorinated swim-
ming pool attendance is associated, according to this study, with
higher risks of asthma, airways inflammation and some respira-
tory allergies whatever outdoor swimming pools water contained
lower levels of volatile toxic compounds such as chloramines or
THMs than that of a covered pools, because of the transfer phase
(water–air).
Risk assessment for swimming pools
Many researches have been carried out in various countries, to
determine the exposure and doses of DBPs through domestic uses
of drinking water. Others European studies have tried to deter-
mine the exposure during swimming activities (Aggazzotti et al.,
1998; Caro and Gallego, 2007; Erdinger et al., 2004; Fantuzzi et al.,
2001). THMs in pool water may experience much higher concen-
trations than those normally found and regulated in drinking water
(Chu and Nieuwenhuijsen, 2002; Erdinger et al., 2004). Given their
volatility, THMs can be found in the airspace above the water and
the air in indoor swimming pool. In the experience of the authors,
one accident was reported but not published in the scientific liter-
ature, where young children suffered of respiratory problems and
blackout due to the narcotic properties of chloroform, leading to
the need of artificial ventilation and hospitalization, after exposure
to highly THMs contaminated air in a recreational water center.
Thus they may be taken up by swimmers through the skin, but
also through ingestion and by inhalation, as by inhalation and con-
tact with ocular mucosa by the people working around basins. In
recent years, few studies have been performed for a better determi-
nation of DBPs in swimming pools and the factors leading to their
production or control. Chloroform is the dominant and most abun-
dant species in the pools treated with chlorine and ozone/chlorine.
Brominated THMs are higher in pools treated with electrochemi-
cally generated mixed oxidants than with chlorine (Lee et al., 2010).
Numerous publications on the risk assessment of DBPs in tap
water are available in the literature. These various researches were
the scientific bases for setting guideline values for DBPs in tap
water. The guideline values of the major DBPs in tap water are
presented in Table 6. Recent studies have focused on the concen-
trations of disinfection by-products of chlorinated swimming pools.
The syntheses of the WHO, AFFSET and a recent study by Richard-
son et al. are shown in Table 4. All of these publications show high
 A. Florentin et al. / International Journal of Hygiene and Environmental Health 214 (2011) 461–469
Table 6
Maximum acceptable concentration or guideline values for major DBPs in tap water.
WHO US-EPA Europe
Trihalomethane (␮g L−1 )
Chloroform 300
Bromodichloromethane 60
Dibromochloromethane 100
Bromoform 100
Total 4 THMs 80 100
Haloacetic acids (␮g L−1 )
Monochloroacetic acid
Dichloroacetic acid 50
Trichloroacetic acid 100
Monobromoacetic acid
Dibromoacetic acid
Total 5 HAAs 60
concentrations of chloroform and trichloramine in water and air.
Swimmers and technical staff are in contact with water and air
of the swimming pools. Consequently, three pathways are identi-
fied: ingestion, dermal or mucosal contact and inhalation. The oral
pathway is related to voluntary or accidental ingestion of swim-
ming pool water. The volume of ingestion is related to age and
types of activity. One study (Dufour et al., 2006) estimated that
the average volume of water absorbed by a baby swimmer was
50 mL h−1 and up to 171 mL h−1 for an athlete swimmer. The muco-
cutaneous pathway is linked to contact with water. Some DBPs
including THMs could cross the muco-cutaneous barrier (Xu et al.,
2002). No studies on the transcutaneous passage of chloramines
are available. The limited data available make difficult to calculate
the correct exposure. For inhalation pathway, DBPs in the air pene-
trate into the respiratory tract depending on the mode of breathing,
nasal or oral (Bernard et al., 2007).
Three recent studies undertook risk assessments of swimming
pools (AFFSET, 2010; Lee et al., 2009; Panyakapo et al., 2008). Two
of them focus more specifically on THMs. For Panyakapo et al., the
assessment of cancer risk of swimmers from exposure to THMs
at the highest and the average concentrations led to values of
1.47 × 10−3 and 7.99 × 10−4 , respectively, which can be classified
as unacceptable risk according to the standards of US-EPA. For non-
swimmers, assessment of cancer risk is below to 10−5 at the highest
and the average concentration. This study took into account the
three routes of exposure: ingestion, inhalation, transdermal pas-
sage. They conclude that risk of cancer from skin exposure while
swimming represents 94.2% of the total risk of cancer. Lee et al.
highlighted a higher risk for inhalation pathway of exposure. They
estimated the cancer risk linked with an average THMs inhalation
in swimming pools between 7.77 × 10−4 and 1.36 × 10−3 . With the
highest concentrations, the risk of cancer reached 3.46 × 10−3 for
female. Ingestion and dermal pathways were associated with a can-
cer risk below 10−6 (Lee et al., 2009). Those two studies assessed a
risk linked to dermal pathway. Nevertheless, dermal absorption of
THMs and the others DBPs are poorly understood. For this reason,
the third study, performed by the AFFSET, ignored this pathway
for risk calculation. They assessed the risk of major DBPs found in
swimming pools water and air. They did not find an excess of can-
cer or toxic risk for the selected DBPs. They draw attention to the
less known DBPs such as bromate ion and NDMA. Risk assessment
was not possible for these two compounds due to the lack of con-
centration data in swimming pools water. Indeed, they calculated
the maximum acceptable concentrations for a 10−5 risk: NDMA
between 0.0051 mg L−1 and 0.00012 mg L−1 , bromates between
0.372 mg L−1 and 0.0087 mg L−1 respectively for occasional swim-
mers and elite swimmers. This study did not take into account the
exposures associated with tap water.
Risk assessments of trichloramine, chloral hydrate and for spe-
cific pathway of exposure are not achievable due to lack of data
467
on slope factors and reference dose. This lack of data is proba-
bly due to an underestimation of risks associated with disinfection
Canada by-products.
Conclusion
16
The increased prevalence of asthma or atopic dermatitis among
100 children and adolescents in Europe is certainly due to multi-
ple factors. Nevertheless this raises questions about the role of
the attendance at chlorinated swimming pools, mandatory during
school activities in many countries. The debate about the potential
risks from chlorinated swimming pools is beginning to be con-
ducted in public and some associations now consider this to be a
80
public health problem. Thus research has to be performed to ensure
the efficiency and absence of harm of new methods of water dis-
infection and/or limiting the amounts of harmful products founds
in the water and air of chlorinated pools. Nevertheless, the need to
take into account the risks associated with disinfection by-products
must not mean that the importance of controlling microbiological
hazards in swimming pools is ignored.
Acknowledgement
We would like to thank Paul Hunter for the time he dedicated
in reading of this publication.
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