Exposure to disinfection by-products in swimming pools and biomarkers of genotoxicity and respiratory damage – The PISCINA2 Study
Open accessAbstract
BACKGROUND: Swimming in pools is a healthy activity that entails exposure to disinfection by-products (DBPs), some of which are irritant and genotoxic. OBJECTIVES: We evaluated exposure to DBPs during swimming in a chlorinated pool and the association with short-term changes in genotoxicity and lung epithelium permeability biomarkers. METHODS: Non-smoker adults (N = 116) swimming 40 min in an indoor pool were included. We measured a range of biomarkers before and at different times after swimming: trihalomethanes (THMs) in exhaled breath (5 min), trichloroacetic acid (TCAA) in urine (30 min), micronuclei in lymphocytes (1 h), serum club cell protein (CC16) (1 h), urine mutagenicity (2 h) and micronuclei in reticulocytes (4 days in a subset, N = 19). Several DBPs in water and trichloramine in air were measured, and physical activity was extensively assessed. We estimated interactions with polymorphisms in genes related to DBP metabolism. RESULTS: , respectively. Creatinine-adjusted urinary TCAA increased by 3.1 μmol/mol. Micronuclei in lymphocytes and reticulocytes, urine mutagenicity and serum CC16 levels remained unchanged after swimming. Spearman correlation coefficients showed no association between DBP exposure and micronuclei in lymphocytes, urine mutagenicity and CC16. Moderate associations were observed for micronuclei in reticulocytes and DBP exposure. CONCLUSIONS: The unchanged levels of the short-term effect biomarkers after swimming and null associations with personal estimates of exposure to DBPs suggest no measurable effect on genotoxicity in lymphocytes, urine mutagenicity and lung epithelium permeability at the observed exposure levels. The moderate associations with micronuclei in reticulocytes require cautious interpretation given the reduced sample size.
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In a cross-sectional study of healthy adult nonsmokers in Spain, levels of CC16 were unchanged after swimming.
“Levels of CC16 were unchanged after swimming.”
From Inorganic chloramines: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting (2020) · cites this paper as Font-Ribera et al. (2019)
Competitive swimmers have been shown to suffer from high rates of asthma and airway hyperresponsiveness attributed to HOCl and volatile DBP exposure.
“For example, competitive swimmers have been shown to suffer from high rates of asthma and airway hyperresponsiveness attributed to HOCl and volative DBP exposure (149, 150).”
From Hypochlorous Acid: From Innate Immune Factor and Environmental Toxicant to Chemopreventive Agent Targeting Solar UV-Induced Skin Cancer (2022) · cites this paper as [150]
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RICHARDSON, S., PLEWA, M., WAGNER, E., SCHOENY, R., & DEMARINI, D. (2007) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2007.09.001 · Cited by 3,317 · see citing works
Richardson, S. D., DeMarini, D. M., Kogevinas, M., Fernandez, P., Marco, E., Lourencetti, C., Ballesté, C., Heederik, D., Meliefste, K., McKague, A. B., et al. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.1001965 · Cited by 327 · see citing works
Self-citationExposure to chloramines in the atmosphere of indoor swimming pools
HERY, M. (1995) · The Annals of Occupational Hygiene · doi:10.1016/0003-4878(95)00013-5 · Cited by 167 · see citing works
Genotoxic effects in swimmers exposed to disinfection by-products in indoor swimming pools
Kogevinas, M., Villanueva, C. M., Font-Ribera, L., Liviac, D., Bustamante, M., Espinoza, F., Nieuwenhuijsen, M. J., Espinosa, A., Fernandez, P., DeMarini, D. M., et al. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.1001959 · Cited by 144 · see citing works
Self-citationCarbonnelle, S., Francaux, M., Doyle, I., Dumont, X., Burbure, C. D., Morel, G., Michel, O., & Bernard, A. (2002) · Biomarkers · doi:10.1080/13547500210166612 · Cited by 131 · see citing works
Short-Term Changes in Respiratory Biomarkers after Swimming in a Chlorinated Pool
Font-Ribera, L., Kogevinas, M., Zock, J.-P., Gómez, F. P., Barreiro, E., Nieuwenhuijsen, M. J., Fernandez, P., Lourencetti, C., Pérez-Olabarría, M., Bustamante, M., et al. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.1001961 · Cited by 119 · see citing works
Self-citationFractional exhaled NO and serum pneumoproteins after swimming in a chlorinated pool
CARBONNELLE, S., BERNARD, A., DOYLE, I. R., GRUTTERS, J., & FRANCAUX, M. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181733159 · Cited by 34 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- [2]2. [Nordberg, G.F., Lundstrom, N.G., Forsberg, B., Hagenbjork-Gustafsson, A., Lagerkvist, B.J., Nilsson, J., et al., 2012. Lung function in volunteers before and after exposure to trichloramine in indoor pool environments and asthma in a cohort of pool workers. BMJ Open 2, e000973.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0140)
- [3]3. Plewa MJ, Wagner ED, Muellner MG, Hsu KM, Richardson SD. 2008. Comparative mammalian cell toxicity of N-DBPs and C-DBPs, in: T. Karanfil, S.W. Krasner, P. Westerhoff, Y. Xie (Eds.), Occurrence, Formation, Health Effects and Control of Disinfection By-products in Drinking Water. American Chemical Society, Washington, DC, Symposium Series No. 995, 36.
- [4]4. [Provost, E.B., Chaumont, A., Kicinski, M., Cox, B., Fierens, F., Bernard, A., Nawrot, T.S., 2014. Serum levels of club cell secretory protein (Clara) and short- and long-term exposure to particulate air pollution in adolescents. Environ. Int. 68, 66-70.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0145)
- [7]7. [Stayner, L.T., Pedersen, M., Patelarou, E., Decordier, I., Vande Loock, K., Chatzi, L., et al., 2014. Exposure to brominated trihalomethanes in water during pregnancy and micronuclei frequency in maternal and cord blood lymphocytes. Environ. Health](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0160) [Perspect. 122, 100-106.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0160) - [Stockfelt, L., Sallsten, G., Olin, A.C., Almerud, P., Samuelsson, L., Johannesson, S., et al., 2012. Effects on airways of short-term exposure to two kinds of wood smoke in a chamber study of healthy humans. Inhal. Toxicol. 24, 47-59.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0165) - [Stopper, H., Hempel, K., Reiners, C., Vershenya, S., Lorenz, R., Vukicevic, V., et al., 2005. Pilot study for comparison of reticulocyte-micronulei with lymphocyte-micronuclei in human biomonitoring. Toxicol. Lett. 156, 351-360.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0170) - [Thomas, P., Holland, N., Bolognesi, C., Kirsch-Volders, M., Bonassi, S., Zeiger, E., et al., 2009. Buccal micronucleus cytome assay. Nat. Protoc. 4, 825-837.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0175) - [van Veldhoven, K., Keski-Rahkonen, P., Barupal, D.K., Villanueva, C.M., Font-Ribera, L., Scalbert, A., et al., 2018. Effects of exposure to water disinfection by-products in a swimming pool: a metabolome-wide association study. Environ. Int. 111, 60-70.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0180) - [Villanueva, C.M., Font-Ribera, L., 2012. Health impact of disinfection by-products in swimming pools. Ann. Ist. Super. Sanita 48, 387-396.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0185) - [Villanueva, C.M., Cantor, K.P., Cordier, S., Jaakkola, J.J., King, W.D., Lynch, C.F., et al., 2004. Disinfection byproducts and bladder cancer: a pooled analysis. Epidemiology 15, 357-367.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0190) - [Villanueva, C.M., Cantor, K.P., Grimalt, J.O., Malats, N., Silverman, D., Tardon, A., et al., 2007. Bladder cancer and exposure to water disinfection by-products through ingestion, bathing, showering, and swimming in pools. Am. J. Epidemiol. 165, 148-156.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0195) - [Vlaanderen, J., van Veldhoven, K., Font-Ribera, L., Villanueva, C.M., Chadeau-Hyam, M., Portengen, L., et al., 2017. Acute changes in serum immune markers due to swimming in a chlorinated pool. Environ. Int. 105, 1-11.](http://refhub.elsevier.com/S0160-4120(19)30465-9/rf0200)
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Snell, J. A., Jandova, J., & Wondrak, G. T. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.887220 · Cited by 37 · see citing works
Wastensson, G., & Eriksson, K. (2020) · Critical Reviews in Toxicology · doi:10.1080/10408444.2020.1744514 · Cited by 30 · see citing works
- Authors
- Font-Ribera, L., Marco, E., Grimalt, J. O., Pastor, S., Marcos, R., Abramsson-Zetterberg, L., Pedersen, M., Grummt, T., Junek, R., Barreiro, E., Heederik, D., Spithoven, J., Critelli, R., Naccarati, A., Schmalz, C., Zwiener, C., Liu, J., Zhang, X., Mitch, W., Gracia-Lavedan, E., Arjona, L., de Bont, J., Tarès, L., Vineis, P., Kogevinas, M., & Villanueva, C. M.
- Affiliations
- Universitat Pompeu Fabra (ES)
- Consejo Superior de Investigaciones Científicas (ES)
- Universitat Autònoma de Barcelona (ES)
- National Food Administration (SE)
- University of Copenhagen (DK)
- German Environment Agency (DE)
- Utrecht University (NL)
- Italian institute for Genomic Medicine (IT)
- University of Tübingen (DE)
- Hong Kong University of Science and Technology (HK)
- Stanford University (US)
- Imperial College London (GB)
- ORCID
- Venue
- Environment International
- Publisher
- Elsevier BV
- Published
- 2019-10
- Volume
- 131
- Pages
- 104988
- ISSN
- 0160-4120 (ISSN-L)
- OpenAlex
- W2959808631
- Cited by
- 38
- References
- 7
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 5 · 2023: 9 · 2022: 8 · 2021: 5 · 2020: 5 · 2019: 1
- FWCI
- 2.05
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Environment International (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by-nc-nd)
- Repositori digital de la UPF (Universitat Pompeu Fabra) (publishedVersion, cc-by-nc-nd)
- Dipòsit Digital de Documents de la UAB (Universitat Autònoma de Barcelona) (submittedVersion, cc-by-nc-nd)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Rare & Special e-Zone (The Hong Kong University of Science and Technology) (submittedVersion)
- Spiral (Imperial College London) (submittedVersion, other-oa)
- Funders
- Instituto de Salud Carlos III
- European Commission
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Water Treatment and Disinfection
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Carcinogens and Genotoxicity Assessment
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Indoor Air Quality and Microbial Exposure
- Keywords
- disinfection by-products, swimming pools, chlorinated water, trihalomethanes, trichloroacetic acid, genotoxicity, micronuclei, trichloramine, biomarkers of exposure
- MeSH terms
- Adult, Disinfectants, DNA Damage, Female, Humans, Male, Polymorphism, Genetic, Spain, Swimming Pools, Water Pollutants, Chemical, Biomarkers, Respiratory Mucosa, Young Adult
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