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10 August 2021 The Occurrence of N-nitrosodimethylamine (NDMA) in Swimming Pools: An Overview
Saheed Mustapha, Tijani Jimoh, Muhammed Ndamitso, Saka Ambali Abdulkareem, Shuaib Damola Taye, Abdul Kabir Mohammed, Azeezah Taiwo Amigun
Author Affiliations +
Abstract

The occurrence of several disinfectant byproducts has been investigated in swimming pools. Until now, there are only a few studies on nitrosamine, particularly N-nitrosodimethylamine in swimming pool water. This could be due to the lack of a suitable method that is sensitive enough for the measurement of N-nitrosodimethylamine in pool waters. Other disinfectant byproducts formed in pool water widely documented are trihalomethanes, haloacetic acids, halonitromethanes, and chloramines but inadequate information on N-nitrosodimethylamine. This paper provides a review of the nitrogenous disinfectant byproduct in swimming pools and its health implications. Anthropogenic substances introduced by swimmers such as sweat, lotions, and urine contribute to the formation of N-nitrosodimethylamine. The reaction of secondary amines such as dimethylamine with mono/dichloroamines produced dimethyl hydrazine and further undergo oxidation to form N-nitrosodimethylamine. The reaction of chlorine and other disinfectants with these anthropogenic sources in swimming pools cause cancer and asthma in human tissues. Thus, the assessment of N-nitrosodimethylamine in the swimming pool is less well documented. Therefore, the health consequences, mutagenic, and genotoxic potentials of N-nitrosodimethylamine should be the focus of more research studies.

Introduction

Numerous emerging micro-pollutants have been detected at trace concentrations in waters, especially in drinking water globally. Some of them have been connected with ecological influences, even at these very low concentrations. Researchers have placed so much emphasis on micro-pollutants in public health assessments and environmental risk assessment in drinking water, focusing less on swimming pool water. Therefore, providing clean water without harmful disinfection byproducts is needed for supplying safe swimming pool water. Chlorine, chlorine dioxide, ozone, and chloramines are the most common disinfectants in use today. Although these disinfectants can effectively kill microbial pathogens, they oxidize anthropogenic contaminants and other organic materials naturally present in source waters due to their strong oxidizing properties, leading to the formation of disinfection by-products (DBPs), such as carbonaceous and nitrogenous disinfectant compounds.1

The consumption of chlorinated water creates an increased risk of deleterious health outcomes which poses serious challenges. Therefore, researchers have focused on most of these emerging contaminants in water, such as disinfection by-products which include nitrosamines and their precursors.2 One of these nitrosamines is N-nitrosodimethylamine (NDMA) which has been identified as a carcinogenic, mutagenic, and teratogenic compound. NDMA was shown to be a major contributor to increased lifetime cancer risk in humans.3 Report by the U.S. Environmental Protection Agency (EPA) has identified nitrosamines to be among the potential carcinogenic contaminants emphasized for monitoring action.4 The first documented report on the presence of NDMA in the waters was in the 1970s.5 Several nitrosamines subjected to carcinogenicity tests were also found in animals while other sources include cigarette smoke, effluents from pesticides, cosmetics, metals, rubber, and tannery industries.6

Other nitrosamines include nitrosomethylethylamine (NMEA), nitrosodiethylamine (NDEA), nitrosodi-n-butylamine (NDBA), nitrosopyrrolidine (NPyr), nitrosupiperidine (NPip), and nitrosomorpholine (NMor).7 In most cases, disinfected water treatment companies are the principal sources of nitrosamine8 while other sources include alcoholic beverages and food,9 meats,10 cigarette smoke,11 and cosmetics.12 The level of NDMA becomes high in chlorinated pools as a result of an increase in anthropogenic activities. Sensitive analytical methods have detected nitrosamines in the water at very low concentrations as low as nanograms per liter (ng/L). Detecting nitrosamines at these low levels are good for proper monitoring and control. These determinations are performed based on extraction and detection. Examples are solid-phase extraction (SPE) and solid-phase microextraction followed by either gas chromatography/mass spectrometry (GC/MS) or liquid chromatography/mass spectrometry (LC/MS) analysis.1317

Different methods have been adopted for the control of NDMA in the water, namely; degradation of NDMA after its formation and removal of its precursors to prevent the formation of NDMA. Among the treatment techniques used are adsorption, ultraviolet (UV) photolysis, bioremediation, zeolite entrapment, reverse osmosis, and advanced oxidation processes. Beita-Sandí et al15 examined the removal of NDMA precursors by powdered activated carbon (PAC) adsorption during water treatment and found that the combination of biodegradation, photolysis, and adsorption reduces the precursors. Seid et al18 investigated NDMA removal in water using UV/sulphite chemistry and discovered that bromide ions reduce NDMA formation during chloramination.

This paper reviews the formation and detection of NDMA in swimming pools because of preliminary findings which showed adverse health implications for swimmers exposed to it during swimming.

Nitrosamines

Nitrosamines (NAs), particularly NDMA, are popularly known as B2 carcinogens by U.S. Environmental Protection Agency19 and they are categorized as nitrogenous disinfection byproducts. NAs are reported to be more carcinogenic than carbonaceous DBPs, such as trihalomethanes (THMs) and haloacetic acids (HAAs).20 N-nitrosamines occur in water as disinfection by-products (DBPs) during chlorination, chloramination, and ozonation and they have been known for centuries. Barnes and Magee21 discovered their carcinogenic properties of these compounds and this is confirmed by Nawrocki and Andrzejewski.5 These compounds have been reported to be present in food products, soil, wastewater, drinking water, and swimming pools.

Ayanaba and Alexander22 detected NDMA in treated sewage and environmental waters. In the early 1990s, NDMA was detected in drinking water in Canada, while in the last few decades, researchers have revealed that disinfected drinking water is not the only route of exposure to nitrosamines but bathing and anthropogenic activities lead to high levels to these chemical compounds. Due to the growing concern regarding the health effects of nitrosamines as a result of their potential carcinogenicity, their characteristics have been summarized in Table 1.

Table 1.

Properties of nitrosamines.

10.1177_11786302211036520-table1.tif

The Formation Mechanism of N-nitrosodimethylamine

The formation of NDMA involves the reaction of secondary amines such as dimethylamine with mono or dichloroamines. It was noticed that dichloramine reacts with dimethylamine to produce an unsymmetrical dimethylhydrazine (UDMH) intermediate. This intermediate undergoes oxidation by monochloramine, to give the targeted carcinogenic compound, NDMA, as shown in Figure 1.

Figure 1.

Mechanism modification of N-nitrosodimethylamine (NDMA) formation.

10.1177_11786302211036520-fig1.tif

This consists of (i) the formation of monochloramiine (a result of the reaction between hypochlorite and ammonia), (ii) the reaction of monochloramine with dimethylamine (DMA) for the formation of the dimethyl chloroamine (DMCA) through chlorine transfer, (iii) the formation of dimethylhydrazine via Raschig synthesis followed by (iv) the oxidation of UDMH by monochloramine and hydrolysis to give NDMA. However, the overall mechanistic reaction indicated that chlorination of nitrite in the presence of nitrosamine precursors leads to the formation of nitrosamine as explained by Soltermann et al.23 Apart from chlorine and ammonia addition during the formation of NDMA, the reaction of water treatment polymers such as poly(diallyldimethylammonium chloride) (polyDADMAC) and poly(epichlorohydrin dimethylamine) (polyamine) have been found to lead to the formation of NDMA. As suggested by Padhye et al,24 the reaction of polyDADMAC and chlorine to produce NDMA involves Hofmann elimination occurring at the β-H to the quaternary amine, leading to the formation of tertiary amine via cleavage from the -carbon to nitrogen. The tertiary amine produced DMA upon reacting with monochloramine/dichloramine. In another study by Park et al,25 the polyDADMAC and polyamine upon reaction with chlorine formed tertiary amines which degraded to secondary amines through electrophilic substitution reaction. In the same vein, the formation of NDMA was as a result of nucleophilic substitution between secondary amine and chloramine.

Some N-N-dimethylhydrazine compounds have been found to form a considerable amount of NDMA during ozonation resulting in the release of DMA, leading to the formation of NDMA. The mechanism of the NDMA formation using this treatment method produced N-N-dimethylhydrazine compounds (UDMH and DMZ) as proposed in Figure 2 by Lim et al.26 During this process, the reaction pathways involved hemolytic cleavage forming N-oxide and singlet oxygen and a heterolytic cleavage forming N-oxide radical, oxygen radical, amine radical, and ozonide radical. The N-oxide reacted with ozone to form N-N-hydroxyl oxide and subsequently degraded into (NDMA and water) and (NDMA and SCA) for UDMH and DMZ, respectively.

Figure 2.

Initial reactions (A), reactions of N-oxide intermediates (B) and reactions of N-oxide radical intermediate of UDMH and UMZ (C).

10.1177_11786302211036520-fig2.tif

Occurrence of NDMA

Swimming pool

Chlorine gas and sodium or calcium hypochlorite are important chemicals used for the disinfection of swimming pool water. Besides their disinfecting properties, chlorine reacts with organic matter introduced into water by the bathers to produce hazardous disinfection by-products (DBPs), such as inorganic chloramines and organohalogenated byproducts. Exposure to these disinfection by-products has resulted in a lot of health problems, according to the work of several researchers.27 In water, NDMA is formed by the addition of chlorine to the water, which undergoes oxidation and reduction reaction forming hydrochloric acid (HCl) and hypochlorous acid (HOCl). The presence of organic substances such as ammonia (NH3) in the chlorinated water results in the formation of monochloroamine, dichloroamine, or trichloroamine depending on the pH of the swimming pool water. The rapid reaction of monochloroamine with ammonia would account for the production of NDMA. The following equations describe the various forms of chloramines formed in this process.

(1)

10.1177_11786302211036520-eq1.tif

(2)

10.1177_11786302211036520-eq2.tif

(3)

10.1177_11786302211036520-eq3.tif

(4)

10.1177_11786302211036520-eq4.tif

(5)

10.1177_11786302211036520-eq5.tif

A study conducted by Kim and Han28 on 3 public indoor pools in Chuncheon, Korea detected nitrosamines at measurable concentrations in chlorinated indoor pool water. The nitrosamines, NMOR, NDMA, and NDEA were found at higher concentrations in swimming pool waters than in the chlorinated drinking water samples. The high levels of these substances were said to be probably as a result of swimming activities in these pools. The authors suggested that the subsequent release of these carcinogenic substances in swimming pools could be declined via a better understanding of several swimming pools. A similar experiment was done by Jurado-Sánchez et al,29 but adequate documentation was not provided on the effect of nitrosamines in pool waters.

The formation of N-Nitrosamine (1%-2%) was postulated to be due to the reactions of oxides of nitrogen such as nitric oxide (NO) and peroxynitrite (ONOO) with the secondary amines in the presence of ultraviolet irradiation by Soltermann et al.23 Thus, the formation of nitrosamines plays a major role in chloraminated pool water containing secondary amines. In another study carried out by Soltermann et al,30 it was reported that trichloramine was the principal precursor that is formed through the reaction of urea with chlorine and hypochlorous acid in pool waters. The authors stated that the formation of trichloramine was due to the swimmers’ activities based on the reaction of chlorine and nitrogen-containing precursors. The reduction of the precursors in water has been a necessary preventive strategy suggested by these authors since the degradation of NDMA is very difficult. The formation of NDMA was not analyzed and quantified during their investigation. This could be a result of the complexity in the mechanism of the formation of nitrosamines in pool waters or the limitation of their study plan.

In the study of Lee et al,31 NDMA was successfully detected in the 4 pools that were studied and the occurrence of other nitrosamines was monitored using UV photolysis and Griess reagent. This method’s detection limits for the 8 N-nitrosamines ranged from 4 to 27.6 ng/L. The examined total level of nitrosamines followed the order: UV/chlorinated pool water (149 mM) >chlorinated pool water (16-38 nM) >chlorinated, ozonated, and activated carbon treated pool water (6 nM). About 78% of UV-resistant compounds were detected in the pool water and 3 nitrosamines, namely; NDMA, NDPA, and NDBA were detected. Nitrosamine is a disinfection by-product in chlorinated swimming pools that was quantified by Walse and Mitch.32 They pointed out that the use of chlorine with the increase of water temperature, the presence of amines, and nitrogen oxide as precursors contributed to the significant occurrence of the compound in swimming pools.

Kulshrestha et al33 reported the NDMA range of 3% to 46% in 6 disinfected swimming pool water. Nitrite and S-nitrosothiols were the major precursors but they can be removed from the system through biological pretreatment methods. Fu et al34 found that NDMA had the highest concentration (100 ng/L) among the nitrosamines determined in experimental samples of swimming pool water. It was established that the amount of this carcinogenic substance depends on the disinfectant applied and the precursors of oxidative nitrosamines formed which could also be harmful to swimmers.

Interest has waned in the last few years about the presence of NDMA in swimming pool water. This could be as a result of limited or lack of no information on a specified regulatory limit for NDMA in swimming pools in most countries. Although before the disinfection process in swimming pool maintenance, appropriate attention has been paid to the disinfection by-products (DBPs). On the other hand, these chemicals may be undesirable to the swimmer when exposed to during swimming.

Swimming pool users introduce anthropogenic substances such as cosmetic products, saliva, urine, and sweat to pool waters.35 Sharifan et al36 and Teo et al37 concluded that these products from humans increase the DBPs in chlorinated swimming pools. The presence of these chemical contaminants is influenced by the types of pools, kind of disinfectants, disinfectant dosages, bather loads, temperature, and pH of the water. They also reported that the reaction of parabens and ultraviolet (UV) filters with these disinfectants could be toxic and may lead to serious health implications. The concentration of water quality parameters such as total nitrogen, dissolved organic carbon, chloride, nitrate, and sulfate strengthen NDMA and other forms of nitrosamines in swimming pools via the organic and inorganic substances for bathers.28 In another study by Knon et al38 and Guo et al,39 they discussed the UV-photolytic mechanisms of NDMA degradation. Following the excitation of NDMA by UV light, it undergoes photolysis, oxidation, bond cleavage, and hydrolysis. The reaction steps are as follows:

(6)

10.1177_11786302211036520-eq6.tif

(7)

10.1177_11786302211036520-eq7.tif

(8)

10.1177_11786302211036520-eq8.tif

(9)

10.1177_11786302211036520-eq9.tif

(10)

10.1177_11786302211036520-eq10.tif

A study found other types of DBPs in swimming pools besides NDMA. This raised important questions about previous researchers’ findings on what could be responsible for the lack of detection of NDMA in swimming pool water. Some of these questions include (i) was there a lack of sufficient analytical methods for identifying NDMA? and (ii) what is the level of NDMA that will not be deleterious to human health? For example, Manasfi et al40 examined trichloroacetic acid, chloral hydrate, dichloroacetonitrile, 1,1,1-trichloropropanone, dibromoacetic acid, bromoform, dibromoacetonitile, and chloroform in fresh and seawater swimming pools. They elucidated that the safety of swimming pool water could be achieved by reducing or eliminating the production of DBPs. Trihalomethanes (THMs) were the most common DBPs found in outdoor swimming pool water, according to Peng et al,41 due to the presence of organic and inorganic micropollutants in the water. Their findings contradicted the outcomes of Berg et al,42 who discovered haloacetic acids (HAAs) in greater concentrations than THMs in swimming pool water.

The level of a carbonaceous DBP in chlorinated outdoor swimming pool water was investigated by Tang and Xie.43 It was reported that at low contact time, residual chlorine was present in the swimming pool water. It is expected that if a further analysis was conducted, there could be a possible formation of nitrosamines either as intermediates or final products. Hang et al44 studied the level of DBPs in 13 public indoor swimming pools in Nanjing, China. Among the dominant carbonaceous DBPs found in the studies were trihalomethanes, haloacetonitriles, haloketones, and trichloronitromethane. The DBPs concentrations were affected by chlorination, thus making it possible to correlate DBPs and water quality parameters in swimming pools. The DBPs that were identified in swimming pools are highlighted in Table 2.

Table 2.

DBPs in swimming pools.

10.1177_11786302211036520-table2.tif

The noticeable prevalent compound was chlorine. Therefore, there could be possible sources of DBPs such as nitrosamines when there are subsequent reactions of the aforementioned by-products with disinfectants and natural organic substances.

Analytical Techniques for Detecting NDMA

Several established methods for the detection and control of NDMA in swimming pools have helped in providing disinfectant residues in the distribution network during water treatment. The monitoring of this contaminant in parts per trillion levels has been a serious challenge for most water establishments across the globe. The measurement of N-nitrosamine concentration levels is generally achieved using analytical methods such as either gas chromatography or high-pressure liquid chromatography coupled with tandem mass spectrometry detector.58,59 Nitrosamines found in swimming pools could be quite different in composition due to various operating conditions such as pH, precursor identity, and residual disinfectant concentrations.

Soltermann et al23 analyzed and quantified NDMA in swimming pools using high-performance chromatography (HPLC) and solid-phase extraction (SPE). From their findings, potential precursors for NDMA were degraded via photolysis, and approximately 1% to 2% NDMA was formed as a result of the reaction of nitric oxide or peroxynitrate with secondary aminyl radicals. It was observed that NDMA in treated pool water can be significantly degraded by using the UV treatment method in experiments that compared treated pool water to untreated pool water. The result of this study signifies that the occurrence of nitrosamines as emerging contaminants in swimming pools is a result of frequent chlorination and swimmers are unprotected from these compounds in urban regions.

Automated SPE and gas chromatography coupled with mass spectrometer were developed for the detection of NDMAs in swimming pools.29 Among the analyzed pool water samples, NDMA was found to be of the highest concentration in the range of 5.0 to 5.9 ng/L. The chlorination of swimming pool water for disinfection purposes and the presence of amine precursors of urine and sweat from swimmers were the key factors pointed out to be responsible for the rise in NAs in the pool water samples. Thus, simple measures such as public awareness and periodic change of water were advocated to be necessary for the improvement of the qualities of swimming pool water.

The SPE and HPLC-Post Column UV photolysis/Griess reaction (PCUV) methods were used to determine the concentrations of nitrosamine compounds in 4 swimming pool waters with and without disinfection by Lee et al.31 The nitrosamine compounds analyzed and identified NDMA, NDPA, and NDBA. It was established that pools that were treated by chlorination and UV irradiation had the highest concentration of nitrosamines, followed by those that were only chlorinated and then those that were treated by a combination of chlorination, ozonation, and treatment with activated carbon. However, employing UV irradiation is advantageous because it is cheap and easy to implement. According to Tardif et al,60 UV causes an increase in DBPs such as halonitromethanes, haloketones, and trihalomethanes in water but it causes a reduction in the concentrations of NDMA in pool water. To minimize false-positive responses from impurities (nitrite producing compounds upon UV irradiation) present in the extraction solvent, the introduction of UV pre-treatment N-nitro(so) compounds and nitrite-producing compounds to confirm specific N-nitrosamines such as NDMA based on their photostability among peaks that were found in water samples. Walse and Mitch32 established that concentrations of NDMA detected in the indoor pools were far greater than the outdoor pools. They concluded that the level of this water contaminant was reduced upon the treatment of pool water by combining UV and a low dose of chlorine treatment. Therefore, the need for preventing swimmers from getting infections can be achieved by the replacement of the pool waters frequently and using UV treatment.

Solid-phase extraction (SPE) and gas chromatography/mass spectrometry (GC/MS) coupled with chemical ionization (CI) were used for the determination of N-nitrosamines in water samples from 5 swimming pools from Bologna, Italy by Pozzi et al.2 In their study, N-nitrosopyrrolidine (NPYR) was detected at concentrations ranging from 53 to 127 ng/L. In another study Italian pools by Kanan,61 NDMA was found to be less than 1 ng/L in the indoor pools, but higher levels were found in indoor pools from South and North Carolina, United States of America in the range of 2 to 83 ng/L. The researchers concluded that DBPs were formed from nitrogen precursors introduced by swimmers.

In the study of Lashgari et al,62 N-nitrosamines in swimming pool water were determined and quantified by micro-solid-phase extraction (µ-SPE) and gas chromatography-tandem mass spectrometry with electron impact ionization (EI) and triple quadrupole analyzer (GC-EI-MS/MS). The concentrations of these compounds greater than 2 ng/cm3 were determined in the swimming pool water. The study suggested that there is a need for proper monitoring of NAs in pool water by regulatory bodies and organizations. This will help to determine the contamination of nitrosamines and prove if its precursor occurs as a result of swimming activities.

Health Implication of NDMA

Numerous investigations have demonstrated the occurrence of adverse health effects of NDMA in swimming pools and a schematic diagram of its health implications on human is shown in Figure 3. According to United States National Institutes of Health,63 epidemiological studies have revealed an increased risk of bladder cancer as a result of the use of chlorinated water in swimming pools. Other diseases for epidemiological studies include upper digestive tract cancers,64 brain cancer,65,66 bladder cancer,67 gastric cancer,68,69 and liver damage.70,71 Studies on the relationship between swimming and the occurrence of asthma in swimmers have been conducted because there is already a link between swimmers’ professions and respiratory syndromes.72 Trichloramine, an NDMA precursor, is a respiratory irritant produced by chlorine in the water, the swimmers, water temperature, and ventilation of the swimming pool, as well as the presence of some undesired products used for maintenance purposes.73 It has been found to have negative health consequences according to the California Department of Public Health.74 There are potential risks from chlorinated swimming pools including cancer and asthma among swimmers. Thus, there is a need to find approaches for controlling hazardous substances in swimming pools. Manasfi et al,75 evaluated some NDMA precursors and their adverse health effects upon human exposure. From their study, epidemiologic studies showed that exposure to these DBPs has adverse effects on respiration and they may cause bladder cancer. There are also indications that trichloramine from swimming pools facilitates the occurrence of asthma in swimmers.76 This respiratory health problem, they asserted, is as a result of accidental exposure to chlorine by swimmers.

Figure 3.

Effect of pool water on the human body.

10.1177_11786302211036520-fig3.tif

Although these disinfectants reduce the microbial pathogen growth in swimming pools, they interact with natural organic matter and organic micro-pollutants excreted in the pools by swimmers forming hazardous compounds as disinfection by-products (DBPs).77 These hazardous compounds or teratogenic and embryopathy organic substances in swimming pools are known to be highly carcinogenic to the bladder tissues and are biomarkers of bladder cancer in humans. They can be generated from the reaction of nitrosating agents and secondary amines. Sanagi et al78 reported that nitrosamines are metabolically triggered via interactions with cytochrome-P450 enzymes and they exert their carcinogenic properties in the human body as shown in the schematic diagram. Weisel et al 200979 and Walse and Mitch32 found NDMA in swimming pools to be most abundant and the epidemiological results suggested a link between nitrosamine in swimming pools and bladder cancer. In the reports by Moore et al80 and Davis et al,81 nitrosamines were indicator biomarkers of bladder cancer in human and carcinogenic bladder tissue. Furthermore, the study of Tardif et al60 revealed the presence of NDMA contaminants in swimming pool water, indicating the high potential of health risk to workers and bathers.

Conclusions and Suggestion

A review of the occurrence and existence of NDMA in swimming pool water has been presented in this review and some negative impacts of the nitrogenous disinfectant byproducts are highlighted. NDMA is a human carcinogen and its formation is triggered by the activities of swimmers such as the introduction of their sweats or other body fluids, lotions, and urine. However, information on the existence and degradation of NDMA in swimming pool water is still relatively scanty. Therefore, there is a need for the development of techniques for monitoring, assessing, and removing this potentially toxic nitrogenous compound from swimming pools.

The quantification of NDMA in swimming pools is challenging and this has become a serious issue noticed globally. Numerous studies have focused on the detection and control of NDMA in drinking water and industrial effluents. The gap analysis in the review of NDMA, exposure to it, and the human health effect needs to be critically evaluated. These are some suggestions about future work that should be done to evaluate and control NDMA in swimming pools.

  • The identification and quantification of NDMA in swimming pools should be conducted on swimming pools that have undergone full-scale advanced treatments at the pilot and bench scale.

  • Better understanding and assessment of the integration of analytical tools in water samples from indoor and outdoor pools should be checked to facilitate good management practices. This approach will help to remove NDMA and its precursors from disinfected swimming pools.

  • The release of nitrogenous DBPs via used cosmetics, urine, skin, and hair lotions by swimmers should be addressed. There should be rules and regulations requiring showering by swimmers and pool attendants before they enter the pool. This policy will reduce organic and inorganic water toxicity, DBPs formation, and exposure of swimmers to NDMA.

Author Contributions

SM drafted the article critically for important intellectual content. All authors substantially contributed to the conception and design of the article and interpreting the relevant literature.

REFERENCES

1.

Song B , Zhang C , Zeng G , Gong J , Chang Y , Jiang Y. Antibacterial properties and mechanism of graphene oxide-silver nanocomposites as bactericidal agents for water disinfection. Arch Biochem Biophys. 2016;604:167–176. Google Scholar

2.

Pozzi R , Bocchini P , Pinelli F , Galletti GC. Determination of nitrosamines in water by gas chromatography/chemical ionization/selective ion trapping mass spectrometry. J Chromatogr A. 2011;1218:1808–1814. Google Scholar

3.

Sakai H , Tokuhara S , Murakami M , Kosaka K , Oguma K , Takizawa S. Comparison of chlorination and chloramination in carbonaceous and nitrogenous disinfection byproduct formation potentials with prolonged contact time. Water Res. 2016;88:661–670. Google Scholar

4.

Roberson JA. Regulatory options for nitrosamines. Proceedings of the 2011 AWWA Annual Conference and Exposition; June 12-16, 2011. Washington, DC. Google Scholar

5.

Nawrocki J , Andrzejewski P . Nitrosamines and water. J Hazard Mater. 2011;189:1–18. Google Scholar

6.

Planas C , Palacios O , Ventura F , Rivera F , Caixach J. Analysis of nitosamines in water by automated SPE and isotope dilution GC/HRMS. Talanta. 2008;76:906–913. Google Scholar

7.

U.S. Environmental Protection Agency. Contaminant candidate list 3-CCL3. 2015. November 12, 2014. Accessed February 12, 2015.  http://www2.epa.gov/ccl/contaminant-candidate-list-3-ccl-3 Google Scholar

8.

Suez Environment. Internal report, 2007. Google Scholar

9.

Sen NP. Formation and occurrence of nitrosamines in food. In: Reddy BS , Cohen LA , eds. Diet, Nutrition, and Cancer: A Critical Evaluation. CRC Press; 2018;135–160. Google Scholar

10.

De Mey E , De Maere H , Paelinck H , Fraeye I . Volatile N-nitrosamines in meat products: potential precursors, influence of processing, and mitigation strategies. Crit Rev Food Sci Nutr. 2017;57:2909–2923. Google Scholar

11.

Ravi Mehrotra MD . Alarmingly high levels of nicotine and carcinogenic nitrosamines in smokeless tobacco products sold worldwide. Nicotine Tob Res. 2021;621:622. Google Scholar

12.

Alhooshani K. Determination of nitrosamines in skin care cosmetics using Ce-SBA-15 based stir bar-supported micro-solid-phase extraction coupled with gas chromatography mass spectrometry. Arab J Chem. 2020;13:2508–2516. Google Scholar

13.

Selbes M , Kim D , Ates N , Karanfil T. The roles of tertiary amine structure, background organic matter and chloramine species on NDMA formation. Water Res. 2013;47:945–953. Google Scholar

14.

Bei E , Shu Y , Li S , et al. Occurrence of nitrosamines and their precursors in drinking water systems around mainland China. Water Res. 2016;98:168–175. Google Scholar

15.

Beita-Sandí W , Ersan MS , Uzun H , Karanfil T. Removal of N-nitrosodimethylamine precursors with powdered activated carbon adsorption. Water Res. 2016;88:711–718. Google Scholar

16.

Choi NR , Kim YP , Ji WH , Hwang GS , Ahn YG. Identification and quantification of seven volatile n-nitrosamines in cosmetics using gas chromatography/chemical ionization–mass spectrometry coupled with head space-solid phase microextraction. Talanta. 2016;148:69–74. Google Scholar

17.

Woods GC , Dickenson ERV . Natural attenuation of NDMA precursors in an urban, wastewater-dominated wash. Water Res. 2016;89:293–300. Google Scholar

18.

Seid MG , Cho K , Hong SW. UV/sulfite chemistry to reduce N-nitrosodimethylamine formation in chlor(am)inated water. Water Res. 2020;185:116243. Google Scholar

19.

U.S. Environmental Protection Agency. Contaminant candidate list 3. 2012. Accessed November 12, 2013.  http://water.epa.gov/scitech/drinkingwater/dws/ccl/ccl3.cfm Google Scholar

20.

Liao X , Bei E , Li S , et al. Applying the polarity rapid assessment method to characterize nitrosamine precursors and to understand their removal by drinking water treatment processes. Water Res. 2015;87:292–298. Google Scholar

21.

Barnes JM , Magee PN. Some toxic properties of dimethylnitrosamine. Br J Ind Med. 1954;11:167–174. Google Scholar

22.

Ayanaba A , Alexander M. Transformations of methylamines and formation of a hazardous product, dimethylnitrosamine, in samples of treated sewage and lake water. J Environ Qual. 1974;3:83–89. Google Scholar

23.

Soltermann F , Lee M , Canonica S , von Gunten U. Enhanced N-nitrosamine formation in pool water by UV irradiation of chlorinated secondary amines in the presence of monochloramine. Water Res. 2013;47:79–90. Google Scholar

24.

Padhye L , Luzinova Y , Cho M , Mizaikoff B , Kim JH , Huang CH. PolyDADMAC and dimethylamine as precursors of N-nitrosodimethylamine during ozonation: reaction kinetics and mechanisms. Environ Sci Technol. 2011;45:4353–4359. Google Scholar

25.

Park SH , Padhye LP , Wang P , Cho M , Kim JH , Huang CH. N-nitrosodimethylamine (NDMA) formation potential of amine-based water treatment polymers: effects of in situ chloramination, breakpoint chlorination, and pre-oxidation. J Hazard Mater. 2015;282:133–140. Google Scholar

26.

Lim S , Lee W , Na S , Shin J , Lee Y. N-nitrosodimethylamine (NDMA) formation during ozonation of N, N-dimethylhydrazine compounds: reaction kinetics, mechanisms, and implications for NDMA formation control. Water Res. 2016;105:119–128. Google Scholar

27.

Tardif R , Catto C , Haddad S , Simard S , Rodriguez M. Assessment of air and water contamination by disinfection by-products at 41 indoor swimming pools. Environ Res. 2016;148:411–420. Google Scholar

28.

Kim H , Han K. Swimmers contribute to additional formation of N-nitrosamines in chlorinated pool water. Toxicol Environ Health Sci. 2011;3:168–174. Google Scholar

29.

Jurado-Sánchez B , Ballesteros E , Gallego M. Screening of N-nitrosamines in tap and swimming pool waters using fast gas chromatography. J Sep Sci. 2010;33:610–616. Google Scholar

30.

Soltermann F , Widler T , Canonica S , von Gunten U. Comparison of a novel extraction-based colorimetric (ABTS) method with membrane introduction mass spectrometry (MIMS): trichloramine dynamics in pool water. Water Res. 2014;58:258–268. Google Scholar

31.

Lee M , Lee Y , Soltermann F , von Gunten U. Analysis of N-nitrosamines and other nitro(so) compounds in water by high-performance liquid chromatography with post-column UV photolysis/Griess reaction. Water Res. 2013;47:4893–4903. Google Scholar

32.

Walse SS , Mitch WA. Nitrosamine carcinogens also swim in chlorinated pools. Environ Sci Technol. 2008;42:1032–1037. Google Scholar

33.

Kulshrestha P , McKinstry KC , Fernandez BO , Feelisch M , Mitch WA. Application of an optimized total N-nitrosamine (TONO) assay to pools: placing N-nitrosodimethylamine (NDMA) determinations into perspective. Environ Sci Technol. 2010;44:3369–3375. Google Scholar

34.

Fu SC , Tzing SH , Chen HC , Wang YC , Ding WH. Dispersive micro-solid phase extraction combined with gas chromatography–chemical ionization mass spectrometry for the determination of N-nitrosamines in swimming pool water samples. Anal Bioanal Chem. 2012;402:2209–2216. Google Scholar

35.

Chowdhury S , Alhooshani K , Karanfil T. Disinfection byproducts in swimming pool: occurrences, implications and future needs. Water Res. 2014;53:68–109. Google Scholar

36.

Sharifan H , Klein D , Morse AN. UV filters interaction in the chlorinated swimming pool, a new challenge for urbanization, a need for community scale investigations. Environ Res. 2016;148:273–276. Google Scholar

37.

Teo TL , Coleman HM , Khan SJ. Chemical contaminants in swimming pools: occurrence, implications and control. Environ Int. 2015;76:16–31. Google Scholar

38.

Knon BG , Kim J , Namkung KC. The formation of reactive species having hydroxyl radical like reactivity from UV photolysis of N-nitrosodimethylamine (NDMA): kinetics and mechanism. Sci Total Environ. 2012;437:237–244. Google Scholar

39.

Guo X , Shao H , Kong L , et al. Probing the effect of nanotubes on N-nitrosodimethylamine photocatalytic degradation efficiency and reaction pathway. Chem Eng Sci. 2016;144:1–6. Google Scholar

40.

Manasfi T , DeMéo M , Coulomb B , Di Giorgio C , Boudenne J. Identification of disinfection by-products in freshwater and seawater swimming pools and evaluation of genotoxicity. Environ Int. 2016;88:94–102. Google Scholar

41.

Peng D , Saravia F , Abbt-Braun G , Horn H. Occurrence and simulation of trihalomethanes in swimming pool water: a simple prediction method based on DOC and mass balance. Water Res. 2016;88:634–642. Google Scholar

42.

Berg AP , Fang TA , Tang HL. Unlocked disinfection by-product formation potential upon exposure of swimming pool water to additional stimulants. Front Environ Sci Eng. 2019;13:10. Google Scholar

43.

Tang HL , Xie YF. Biologically active carbon filtration for haloacetic acid removal from swimming pool water. Sci Total Environ. 2015;541:58–64. Google Scholar

44.

Hang C , Zhang B , Gong T , Xian Q. Occurrence and health risk assessment of halogenated disinfection byproducts in indoor swimming pool water. Sci Total Environ. 2016;543:425–431. Google Scholar

45.

Cheema WA , Andersen HR , Kaarsholm KMS . Improved DBP elimination from swimming pool water by continuous combined UV and ozone treatment. Water Res. 2018;147:214–222. Google Scholar

46.

van Veldhoven K , Keski-Rahkonen P , Barupal DK , et al. Effects of exposure to water disinfection by-products in a swimming pool: a metabolome-wide association study. Environ Int. 2018;111:60–70. Google Scholar

47.

Avsar E , Avsar DD , Hayta S. Evaluation of disinfection by-product (DBP) formation and fingerprint in a swimming pool in Bitlis/Turkey: a case study. Environ Forensics. 2020;21:375–385. Google Scholar

48.

Spiliotopoulou A , Hansen KMS , Andersen HR . Disinfection by-product formation of UV treated swimming pool water. In: 6th International Conference Swimming Pool & Spa; March 17-20, 2015; Amsterdam, The Netherlands. Google Scholar

49.

Bahmani P , Ghahramani E. Disinfection byproducts in swimming pool water in Sanandj, Iran. J Adv Environ Health Res. 2018;6:136–143. Google Scholar

50.

Yang F , Yang Z , Li H , Jia F , Yang Y. Occurrence and factors affecting the formation of trihalomethanes, haloacetonitriles and halonitromethanes in outdoor swimming pools treated with trichloroisocyanuric acid. Environ Sci Water Res Technol. 2018;4:218–225. Google Scholar

51.

Yang L , Schmalz C , Zhou J , et al. An insight of disinfection by-product (DBP) formation by alternative disinfectants for swimming pool disinfection under tropical conditions. Water Res. 2016;101:535–546. Google Scholar

52.

Cimetiere N , De Laat J. Effects of UV-dechloramination of swimming pool water on the formation of disinfection by-products: a lab-scale study. Microchem J. 2014;112:34–41. Google Scholar

53.

Chowdhury S , Mazumder AJ , Husain T. Predicting bromide incorporation in a chlorinated indoor swimming pool. Environ Sci Pollut Res. 2016;23:12174–12184. Google Scholar

54.

Carter RAA , Allard S , Croué JP , Joll CA . Occurrence of disinfection by-products in swimming pools and the estimated resulting cytotoxicity. Sci Total Environ. 2019;664:851–864. Google Scholar

55.

Wu H , Long K , Lu D , Mo Y , Yang Q , Wei X. Occurrence and formation of halobenzoquinones in indoor and outdoor swimming pool waters of Nanning City, Southwest China. Environ Sci Pollut Res. 2019;26:31537–31545. Google Scholar

56.

Peng F , Peng J , Li H , Li Y , Wang B , Yang Z. Health risks and predictive modeling of disinfection byproducts in swimming pools. Environ Int. 2020;139:105726. Google Scholar

57.

Liu Y , Chen CY , Wang GS. Bench-scale assessment of the formation and control of disinfection byproducts from human endogenous organic precursors in swimming pools. Chemosphere. 2019;224:607–615. Google Scholar

58.

Munch JW , Bassett MV. Determination of nitrosamines in drinking water by solid phase extraction and capillary column gas chromatography with large volume injection and chemical ionization tandem mass spectrometry. U.S. Environmental Protection Agency; 2004. Report EPA/600/R-05/054. Google Scholar

59.

Fujioka T , Tu KL , Khan SJ , et al. Rejection of small solutes by reverse osmosis membranes for water reuse applications: a pilot-scale study. Desalination. 2014;350:28–34. Google Scholar

60.

Tardif R , Rodriguez M , Catto C , Charest-Tardif C , Simard S. Concentrations of disinfection by-products in swimming pool following modifications of the water treatment process: an exploratory study. J Environ Sci. 2017;58:163–172. Google Scholar

61.

Kanan AA (2010) Occurrence and formation of disinfection by-products in indoor swimming pools water. Doctoral Dissertation, Clemson University. Google Scholar

62.

Lashgari M , Yamini Y , Basheer C , Lee HK. Ordered mesoporous carbon as sorbent for the extraction of N-nitrosamines in wastewater and swimming pool water. J Chromatogr A. 2017;1513:35–41. Google Scholar

63.

United States National Institutes of Health. 2009.  www.cancer.gov/cacertopic/commoncancers Google Scholar

64.

Rogers MAM , Vaughn TL , Davis S , Thomas BD . Consumption of nitrate, nitrite, and nitrosodimethylamine and the risk of upper aerodigestive tract cancer. Cancer Epidemiol Biomarkers Prev. 1995;4:29–36. Google Scholar

65.

Giles GG , McNeil JJ , Donnan G , et al. Dietary factors and the risk of glioma in adults: results of a case-control study in Melbourne, Australia. Int J Cancer. 1994;59:357–362. Google Scholar

66.

Preston-Martin S. Epidemiological studies of perinatal carcinogenesis. IARC Sci Publ. 1989;96:289–314. Google Scholar

67.

Villanueva CM , Fernandez F , Malats N , Grimalt JO , Kogevinas M. Meta-analysis of studies on individual consumption of chlorinated drinking water and bladder cancer. J Epidemiol Community Health. 2003;57:166–173. Google Scholar

68.

González CA , Riboli E , Badosa J , et al. Nutritional factors and gastric cancer in Spain. Am J Epidemiol. 1994;139:466–473. Google Scholar

69.

Pobel D , Riboli E , Cornée J , Hémon B , Guyader M. Nitrosamine, nitrate and nitrite in relation to gastric cancer: a case-control study in Marseille, France. Eur J Epidemiol. 1995;11:67–73. Google Scholar

70.

Cooper SW , Kimbrough RD. Acute dimethylnitrosamine poisoning outbreak. J Forensic Sci. 1980;25:874–882. Google Scholar

71.

Pedal I , Bresserer K , Goerttler K. Fatal nitrosamine poisoning. Arch Toxicol. 1982;50:101–112. Google Scholar

72.

Valeriani F , Protano C , Vitali M , Romano Spica V. Swimming attendance during childhood and development of asthma: meta-analysis. Pediatr Int. 2017;59:614–621. Google Scholar

73.

Florentin A , Hautemanière A , Hartemann P. Health effects of disinfection by-products in chlorinated swimming pools. Int J Hyg Environ Health. 2011;214:461–469. Google Scholar

74.

California Department of Public Health. NDMA and Other Nitrosamines – Drinking Water Issues. California Department of Public Health; 2007. Google Scholar

75.

Manasfi T , Coulomb B , Boudenne J. Occurrence, origin, and toxicity of disinfection byproducts inchlorinated swimming pools: an overview. Int J Hyg Environ Health. 2017;220:591–603. Google Scholar

76.

Richardson S , DeMarini DDM , Kogevinas M , et al. What’s in the pool? A comprehensive identification of disinfection by-products and assessment of mutagenicity of chlorinated and brominated swimming pool water. Environ Health Perspect. 2010;118:1523–1530. Google Scholar

77.

Yeh RY , Farré MJ , Stalter D , Tang JY , Molendijk J , Escher BI. Bioanalytical and chemical evaluation of disinfection by-products in swimming pool water. Water Res. 2014;59:172–184. Google Scholar

78.

Sanagi MM , Chong MH , Endud S , Wan WA , Ali II . Microporous and mesoporous materials nano iron porphyrinated poly (Amidoamine) Dendrimer mobil composition matter-41 for extraction of N -nitrosodiphenylamine Nitrosamine from water samples. Microporous Mesoporous Mater. 2015;213:68–77. Google Scholar

79.

Weisel CP , Richardson SD , Nemery B , et al. Childhood asthma and environmental exposures at swimming pools: state of the science and research recommendations. Environ Health Perspect. 2009;117:500–507. Google Scholar

80.

Moore CM , Goodall CM , Beagley KW , Stephens OB , Horne L , Noronha RL. Mutagenic activation of dialkylnitrosamines by intact urothelial cells. Mutat Res. 1985;157:95–105. Google Scholar

81.

Davis CP , Cohen MS , Hackett RL , Anderson MD , Warren MM. Urothelial hyperplasia and neoplasia. III. Detection of nitrosamine production with different bacterial genera in chronic urinary tract infections of rats. J Urol. 1991;145:875–880. Google Scholar
© The Author(s) 2021
Saheed Mustapha, Tijani Jimoh, Muhammed Ndamitso, Saka Ambali Abdulkareem, Shuaib Damola Taye, Abdul Kabir Mohammed, and Azeezah Taiwo Amigun "The Occurrence of N-nitrosodimethylamine (NDMA) in Swimming Pools: An Overview," Environmental Health Insights 15(1), (10 August 2021). https://doi.org/10.1177/11786302211036520
Received: 26 April 2021; Accepted: 12 July 2021; Published: 10 August 2021
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