Health effects of disinfection by-products in chlorinated swimming pools

International Journal of Hygiene and Environmental Health

Volumn 214, Issue 6, 2011, Pages 461-469

  Florentin, Arnaud ^a   Hautemanière, Alexis ^a   Hartemann, Philippe ^a,b  

^a UNIVERSITÉ DE LORRAINE   (France)

^b INSERM   (France)

Author keywords

Chloramines; Chlorinated swimming pools; Disinfection by products; Haloacetic acids; Risk assessment; Trihalomethanes

Indexed keywords

CARCINOGEN; CHLORAMINE DERIVATIVE; TRIHALOMETHANE;

ARTICLE; ASTHMA; CHEMICALLY INDUCED DISORDER; DISINFECTION; HUMAN; RISK ASSESSMENT; SWIMMING POOL;

ASTHMA; CARCINOGENS; CHLORAMINES; DISINFECTION; HUMANS; RISK ASSESSMENT; SWIMMING POOLS; TRIHALOMETHANES;

EID: 81555204450     PISSN: 14384639     EISSN: 1618131X     Source Type: Journal    
DOI: 10.1016/j.ijheh.2011.07.012     Document Type: Article

References (85)

1. Abdel-Rahman M.S., Waldron D.M., Bull R.J. A comparative kinetics study of monochloramine and hypochlorous acid in rat. J. Appl. Toxicol. 1983, 3(4):175-179.
2. AFFSET Evaluation des risques sanitaires liés aux piscines Partie I: piscines réglementées: 244 2010.
3. Aggazzotti G., Fantuzzi G., Righi E., Predieri G. Blood and breath analyses as biological indicators of exposure to trihalomethanes in indoor swimming pools?. Sci. Total Environ. 1998, 217(1-2):155-163.
4. Amy G.L., Chadik P.A., Chowdhury Z.K. Developing models for predicting trihalomethane formation potential and kinetics. J. Am. Water Works Assoc. 1987, 79:89.
5. Barbee S.J., Thackara J.W., Rinehart W.E. Acute inhalation toxicology of nitrogen trichloride. Am. Ind. Hyg. Assoc. J. 1983, 44(2):145-146.
6. Beech J.A. Estimated worst case trihalomethane body burden of a child using a swimming pool. Med. Hypotheses 1980, 6(3):303-307.
7. Bernard A., Carbonnelle S., Dumont X., Nickmilder M. Infant swimming practice, pulmonary epithelium integrity, and the risk of allergic and respiratory diseases later in childhood. Pediatrics 2007, 119(6):1095-1103.
8. Bernard A., Carbonnelle S., Michel O., Higuet S., De Burbure C., Buchet J.P., Doyle I. Lung hyperpermeability and asthma prevalence in schoolchildren: unexpected associations with the attendance at indoor chlorinated swimming pools. Occup. Environ. Med. 2003, 60(6):385-394.
9. Bernard A., Nickmilder M. Respiratory health and baby swimming. Arch. Dis. Child 2006, 91(7):620-621.
10. Bernard A., Nickmilder M., Voisin C. Outdoor swimming pools and the risks of asthma and allergies during adolescence. Eur. Respir. J. 2008, 32(4):979-988.
11. Bernard A., Nickmilder M., Voisin C., Sardella A. Impact of chlorinated swimming pool attendance on the respiratory health of adolescents. Pediatrics 2009, 124(4):1110-1118.
12. Bryant B.J., Jokinen M.P., Eustis S.L., Thompson M.B., Abdo K.M. Toxicity of monochloroacetic acid administered by gavage to F344 rats and B6C3F1 mice for up to 13 weeks. Toxicology 1992, 72(1):77-87.
13. Cantor K.P., Lynch C.F., Hildesheim M.E., Dosemeci M., Lubin J., Alavanja M., Craun G. Drinking water source and chlorination byproducts. I. Risk of bladder cancer. Epidemiology 1998, 9(1):21-28.
14. Cantor K.P., Villanueva C.M., Silverman D.T., Figueroa J.D., Real F.X., Garcia-Closas M., Kogevinas M. Polymorphisms in GSTT1, GSTZ1, and CYP2E1, disinfection by-products, and risk of bladder cancer in Spain. Environ. Health Perspect. 2010, 118(11):1545-1550.
15. Carbonnelle S., Bernard A., Doyle I.R., Grutters J., Francaux M. Fractional exhaled NO and serum pneumoproteins after swimming in a chlorinated pool. Med. Sci. Sports Exerc. 2008, 40(8):1472-1476.
16. Carbonnelle S., Francaux M., Doyle I., Dumont X., de Burbure C., Morel G., Bernard A. Changes in serum pneumoproteins caused by short-term exposures to nitrogen trichloride in indoor chlorinated swimming pools. Biomarkers 2002, 7(6):464-478.
17. Caro J., Gallego M. Assessment of exposure of workers and swimmers to trihalomethanes in an indoor swimming pool. Environ. Sci. Technol. 2007, 41(13):4793-4798.
18. Chu H., Nieuwenhuijsen M.J. Distribution and determinants of trihalomethane concentrations in indoor swimming pools. Occup. Environ. Med. 2002, 59(4):243-247.
19. Costet N., Villanueva C.M., Jaakkola J.J., Kogevinas M., Cantor K.P., King W.D., Cordier S. Water disinfection by-products and bladder cancer: is there a European specificity? A pooled and meta-analysis of European case-control studies. Occup. Environ. Med. 2011, 68(5):379-385.
20. Daniel F.B., Condie L.W., Robinson M., Stober J.A., York R.G., Olson G.R., Wang S.R. Comparative subchronic toxicity studies of three disinfectants. J. Am. Water Works Assoc. 1990, 82(10):61.
21. Daniel F.B., DeAngelo A.B., Stober J.A., Olson G.R., Page N.P. Hepatocarcinogenicity of chloral hydrate, 2-chloroacetaldehyde, and dichloroacetic acid in the male B6C3F1 mouse. Fundam. Appl. Toxicol. 1992, 19(2):159-168.
22. De Laat J., Berne F., Brunet R., Hue C. Sous-produits de chloration formés lors de la désinfection des eaux de piscines. Etude bibliographique. Eur. J. Water Qual. 2009, 40:109-128.
23. De Laat J., Feng W., Freyfer D.A., Dossier-Berne F. Concentration levels of urea in swimming pool water and reactivity of chlorine with urea. Water Res. 2011, 45(3):1139-1146.
24. Dowty B.J., Laseter J.L., Storer J. The transplacental migration and accumulation in blood of volatile organic constituents. Pediatr. Res. 1976, 10(7):696-701.
25. Dufour A.P., Evans O., Behymer T.D., Cantu R. Water ingestion during swimming activities in a pool: a pilot study. J. Water Health 2006, 4(4):425-430.
26. Erdinger L., Kuhn K.P., Kirsch F., Feldhues R., Frobel T., Nohynek B., Gabrio T. Pathways of trihalomethane uptake in swimming pools. Int. J. Hyg. Environ. Health 2004, 207(6):571-575.
27. Fantuzzi G., Righi E., Predieri G., Ceppelli G., Gobba F., Aggazzotti G. Occupational exposure to trihalomethanes in indoor swimming pools. Sci. Total Environ. 2001, 264(3):257-265.
28. Fisk M.Z., Steigerwald M.D., Smoliga J.M., Rundell K.W. Asthma in swimmers: a review of the current literature. Phys. Sports Med. 2010, 38(4):28-34.
29. Font-Ribera L., Kogevinas M., Zock J.P., Gomez F.P., Barreiro E., Nieuwenhuijsen M.J., Villanueva C.M. Short-term changes in respiratory biomarkers after swimming in a chlorinated pool. Environ. Health Perspect. 2010, 118(11):1538-1544.
30. Font-Ribera L., Villanueva C.M., Nieuwenhuijsen M.J., Zock J.P., Kogevinas M., Henderson J. Swimming pool attendance, asthma, allergies, and lung function in the Avon Longitudinal Study of Parents and Children cohort. Am. J. Respir. Crit. Care Med. 2011, 183(5):582-588.
31. Francesco C. Market Data 2009 2010, http://www.eusaswim.eu/Documentation/downloads/EUSA-market-data.pdf (Retrieved 28 June 2011).
32. French A.S., Copeland C.B., Andrews D., Wiliams W.C., Riddle M.M., Luebke R.W. Evaluation of the potential immunotoxicity of bromodichloromethane in rats and mice. J. Toxicol. Environ. Health A 1999, 56(5):297-310.
33. Fry B.J., Taylor T., Hathway D.E. Pulmonary elimination of chloroform and its metabolite in man. Arch. Int. Pharmacodyn. Ther. 1972, 196(1):98-111.
34. Goodman M., Hays S. Asthma and swimming: a meta-analysis. J. Asthma 2008, 45(8):639-647.
35. Harrington-Brock K., Doerr C.L., Moore M.M. Mutagenicity of three disinfection by-products: di- and trichloroacetic acid and chloral hydrate in L5178Y/TK+/- (-)3.7.2C mouse lymphoma cells. Mutat. Res. 1998, 413(3):265-276.
36. Hartemann P., Gehin C., Paquin J.L., Français T., Morlot M. Haloform contents of water in public swimming pools and the consequences for users and legislation. J. Fr. Hydrol. 1988, 19(2):231-240.
37. Health Canada Guidelines for Canadian Drinking Water Quality: Guideline Technical Document - Trihalomethanes 2006, Water Quality and Health Bureau, Healthy Environments and Consumer Safety Branch, Health Canada, Ottawa, Ontario.
38. Health Canada Guidance for Chloral Hydrate in Drinking Water 2008, Water, Air and Climate Change Bureau, Healthy Environments and Consumer Safety Branch, Health Canada, Ottawa, Ontario.
39. Health Canada Guidelines for Canadian Drinking Water Quality: Guideline Technical Document Haloacetic Acids 2008, Water, Air and Climate Change Bureau, Healthy Environments and Consumer Safety Branch, Health Canada, Ottawa, Ontario.
40. Helenius I., Haahtela T. Allergy and asthma in elite summer sport athletes. J. Allergy Clin. Immunol. 2000, 106(3):444-452.
41. Helenius I., Rytila P., Sarna S., Lumme A., Helenius M., Remes V., Haahtela T. Effect of continuing or finishing high-level sports on airway inflammation, bronchial hyperresponsiveness, and asthma: a 5-year prospective follow-up study of 42 highly trained swimmers. J. Allergy Clin. Immunol. 2002, 109(6):962-968.
42. Helenius I.J., Tikkanen H.O., Sarna S., Haahtela T. Asthma and increased bronchial responsiveness in elite athletes: atopy and sport event as risk factors. J. Allergy Clin. Immunol. 1998, 101(5):646-652.
43. Hu J., Song H., Karanfil T. Comparative analysis of halonitromethane and trihalomethane formation and speciation in drinking water: the effects of disinfectants, pH, bromide, and nitrite. Environ. Sci. Technol. 2010, 44(2):794-799.
44. IPCS Disinfectants and disinfectant by-products. Environmental Health Criteria 216 International Programme on Chemical Safety 2000, World Health Organization, Geneva.
45. Jacobs J.H., Spaan S., van Rooy G.B., Meliefste C., Zaat V.A., Rooyackers J.M., Heederik D. Exposure to trichloramine and respiratory symptoms in indoor swimming pool workers. Eur. Respir. J. 2007, 29(4):690-698.
46. Jo W.K., Weisel C.P., Lioy P.J. Routes of chloroform exposure and body burden from showering with chlorinated tap water. Risk Anal. 1990, 10(4):575-580.
47. Jorgenson T.A., Meierhenry E.F., Rushbrook C.J., Bull R.J., Robinson M. Carcinogenicity of chloroform in drinking water to male Osborne-Mendel rats and female B6C3F1 mice. Fundam. Appl. Toxicol. 1985, 5(4):760-769.
48. Judd S.J., Jeffrey J.A. Trihalomethane formation during swimming pool water disinfection using hypobromous and hypochlorous acids. Water Res. 1995, 29(4):1203-1206.
49. Kanan A., Karanfil T. Formation of disinfection by-products in indoor swimming pool water: the contribution from filling water natural organic matter and swimmer body fluids. Water Res. 2011, 45(2):926-932.
50. King W.D., Marrett L.D. Case-control study of bladder cancer and chlorination by-products in treated water (Ontario, Canada). Cancer Causes Control 1996, 7(6):596-604.
51. Kjellstrand C.M., Eaton J.W., Yawata Y., Swofford H., Kolpin C.F., Buselmeier T.J., Jacob H.S. Hemolysis in dialyzed patients caused by chloramines. Nephron 1974, 13:427.
52. Kogevinas M., Villanueva C.M., Font-Ribera L., Liviac D., Bustamante M., Espinoza F., Marcos R. Genotoxic effects in swimmers exposed to disinfection by-products in indoor swimming pools. Environ. Health Perspect. 2010, 118(11):1531-1537.
53. Kohlhammer Y., Doring A., Schafer T., Wichmann H.E., Heinrich J. Swimming pool attendance and hay fever rates later in life. Allergy 2006, 61(11):1305-1309.
54. Kotiaho T., Wood J.M., Wick P.L., Dejarme L.E., Ranasinghe A., Cooks R.G., Ringhand H.P. Time persistence of monochloramine in human saliva and stomach fluid. Environ. Sci. Technol. 1992, 26(2):302.
55. Lagerkvist B.J., Bernard A., Blomberg A., Bergstrom E., Forsberg B., Holmstrom K., Nordberg G. Pulmonary epithelial integrity in children: relationship to ambient ozone exposure and swimming pool attendance. Environ. Health Perspect. 2004, 112(17):1768-1771.
56. Leakey J.E., Seng J.E., Latendresse J.R., Hussain N., Allen L.J., Allaben W.T. Dietary controlled carcinogenicity study of chloral hydrate in male B6C3F1 mice. Toxicol. Appl. Pharmacol. 2003, 193(2):266-280.
57. Leavens T.L., Blount B.C., DeMarini D.M., Madden M.C., Valentine J.L., Case M.W., Pegram R.A. Disposition of bromodichloromethane in humans following oral and dermal exposure. Toxicol. Sci. 2007, 99(2):432-445.
58. Lee J., Ha K.T., Zoh K.D. Characteristics of trihalomethane (THM) production and associated health risk assessment in swimming pool waters treated with different disinfection methods. Sci. Total Environ. 2009, 407(6):1990-1997.
59. Lee J., Jun M.J., Lee M.H., Lee M.H., Eom S.W., Zoh K.D. Production of various disinfection byproducts in indoor swimming pool waters treated with different disinfection methods. Int. J. Hygiene Environ. Health 2010, 213(6):465-474.
60. Lubbers J.R., Chauan S., Bianchine J.R. Controlled clinical evaluations of chlorine dioxide, chlorite and chlorate in man. Environ. Health Perspect. 1982, 46:57-62.
61. Lynch C.F., Woolson R.F., O'Gorman T., Cantor K.P. Chlorinated drinking water and bladder cancer: effect of misclassification on risk estimates. Arch. Environ. Health 1989, 44(4):252-259.
62. Massin N., Bohadana A.B., Wild P., Hery M., Toamain J.P., Hubert G. Respiratory symptoms and bronchial responsiveness in lifeguards exposed to nitrogen trichloride in indoor swimming pools. Occup. Environ. Med 1998, 55(4):258-263.
63. Momas I., Brette F., Spinasse A., Squinazi F., Dab W., Festy B. Health effects of attending a public swimming pool: follow up of a cohort of pupils in Paris. J. Epidemiol. Commun. Health 1993, 47(6):464-468.
64. Mood E.W. Development and application of high-free residual chlorination in the treatment of swimming pool water. Am. J. Public Health Nations Health 1953, 43(10):1258-1264.
65. Nieuwenhuijsen M.J., Smith R., Golfinopoulos S., Best N., Bennett J., Aggazzotti G., Kogevinas M. Health impacts of long-term exposure to disinfection by-products in drinking water in Europe: HIWATE. J. Water Health 2009, 7(2):185-207.
66. NTP Toxicology and Carcinogenesis Studies of Bromodichloromethane (CAS No. 75-27-4) in F344/N Rats and B6C3F1 Mice (Gavage Studies). NTP TR 321, National Toxicology Program 1987, U.S. Department of Health and Human Services, Research Triangle Park, NC.
67. Panyakapo M., Soontornchai S., Paopuree P. Cancer risk assessment from exposure to trihalomethanes in tap water and swimming pool water. J. Environ. Sci. China 2008, 20(3):372-378.
68. Rahman M.B., Driscoll T., Cowie C., Armstrong B.K. Disinfection by-products in drinking water and colorectal cancer: a meta-analysis. Int. J. Epidemiol. 2010, 39(3):733-745.
69. Richardson S.D., Demarini D.M., Kogevinas M., Fernandez P., Marco E., Lourencetti C., Villanueva C.M. 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.
70. Richardson S.D., Plewa M.J., Wagner E.D., Schoeny R., Demarini D.M. Occurrence, genotoxicity, and carcinogenicity of regulated and emerging disinfection by-products in drinking water: a review and roadmap for research. Mutat. Res. 2007, 636(1-3):178-242.
71. Schoefer Y., Zutavern A., Brockow I., Schafer T., Kramer U., Schaaf B., Heinrich J. Health risks of early swimming pool attendance?. Int. J. Hyg. Environ. Health 2008, 211(3-4):367-373.
72. Seux R. Evolution de la pollution apportée par les baigneurs dans les eaux de piscines sous l'action du chlore. J. Fr. Hydrol. 1988, 19(2):151-168.
73. Stav D., Stav M. Asthma and whirlpool baths. N. Engl. J. Med. 2005, 353(15):1635-1636.
74. Templin M.V., Jamison K.C., Sprankle C.S., Wolf D.C., Wong B.A., Butterworth B.E. Chloroform-induced cytotoxicity and regenerative cell proliferation in the kidneys and liver of BDF1 mice. Cancer Lett. 1996, 108(2):225-231.
75. Templin M.V., Larson J.L., Butterworth B.E., Jamison K.C., Leininger J.R., Mery S., Morgan K.T., Wong B.A., Wolf D.C., et al. A 90-day chloroform inhalation study in F-344 rats: profile of toxicity and relevance to cancer studies. Fundam. Appl. Toxicol. 1996, 32(1):109-125.
76. Thickett K.M., McCoach J.S., Gerber J.M., Sadhra S., Burge P.S. Occupational asthma caused by chloramines in indoor swimming-pool air. Eur. Respir. J. 2002, 19(5):827-832.
77. Tipple M.A., Bland L.A., Favero M.S., Jarvis W.R. Investigation of hemolitic anaemia after chloramine exposure in a dialysis center. Am. Soc. Artif. Intern. Organs (ASAIO) Trans. 1988, 34(4):1060.
78. Villanueva C.M., Cantor K.P., Grimalt J.O., Malats N., Silverman D., Tardon A., Kogevinas M. Bladder cancer and exposure to water disinfection by-products through ingestion, bathing, showering, and swimming in pools. Am. J. Epidemiol. 2007, 165(2):148-156.
79. Villanueva C.M., Cantor K.P., King W.D., Jaakkola J.J., Cordier S., Lynch C.F., Kogevinas M. Total and specific fluid consumption as determinants of bladder cancer risk. Int. J. Cancer 2006, 118(8):2040-2047.
80. Voisin C., Sardella A., Marcucci F., Bernard A. Infant swimming in chlorinated pools and the risks of bronchiolitis, asthma and allergy. Eur. Respir. J. 2010, 36(1):41-47.
81. WHO Guidelines for Safe Recreational Waters. Volume 2. Swimming Pools and Similar Recreational-water Environments 2006, WHO, Geneve, p. 118.
82. Wolfe R.L., Ward N.R., Olson B.H. Inorganic chloramines as drinking water disinfectants: a review. J. Am. Water Works Assoc. 1984, 76(5):74.
83. Wones R.G., Deck C.C., Stadler B., Roark S., Hogg E., Frohman L.A. Effects of drinking water monochloramine on lipid and thyroid metabolism in healthy men. Environ. Health Perspect. 1993, 99:369-374.
84. Xu X., Mariano T.M., Laskin J.D., Weisel C.P. Percutaneous absorption of trihalomethanes, haloacetic acids, and haloketones. Toxicol. Appl. Pharmacol. 2002, 184(1):19-26.
85. Zwiener C., Richardson S.D., DeMarini D.M., Grummt T., Glauner T., Frimmel F.H. Drowning in disinfection byproducts? Assessing swimming pool water. Environ. Sci. Technol. 2007, 41(2):363-372.