The risk of contracting infectious diseases in public swimming pools. A review

Annali dell'Istituto Superiore di Sanita

Volumn 48, Issue 4, 2012, Pages 374-386

  Barna, Zsófia ^a   Kádár, Mihály ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH   (Hungary)

Author keywords

Hot tub; Man made water recreational environment; Risk of infection; Swimming pool; Waterborne disease outbreaks

Indexed keywords

EID: 84872029386     PISSN: 00212571     EISSN: None     Source Type: Journal    
DOI: 10.4415/ANN_12_04_05     Document Type: Review

References (119)

1. World Health Organization. Guidelines for safe recreational water environments. Vol. 2. Swimming pools and similar environments. Geneva: WHO; 2006.
2. The Association of Pool & Spa Professionals. US swimming pool and hot tub market 2011. Available from: www.cdc.gov/healthywater/swimming/fast-facts. html#one.
3. Sherline HL, et al. Surveillance for waterborne-disease outbreaks. United States, 1999-2000. MMRW Surveillance Summaries 2002:51(SS08);1-28. Available from: www.cdc.gov/mmwr/preview/mmwrhtml/ss5108a1.htm#tab9.
4. Yoder JS, et al. Surveillance for waterborne disease and outbreaks associated with recreational water. United States, 2001-2002. MMRW Surveillance Summaries 2004:53(SS08);1-22. Available from: www.cdc.gov/mmwr/preview/mmwrhtml/ ss5308a1.htm.
5. Dziuban EJ. Surveillance for waterborne disease and outbreaks associated with recreational water. United States, 2003-2004. MMRW Surveillance Summaries 2006:55(SS12);1-24. Available from: www.cdc.gov/mmwr/preview/mmwrhtml/ss5512a1. htm#tab7.
6. Yoder JS, et al. Surveillance for waterborne disease and outbreaks associated with recreational water use and other aquatic facility-associated health events. United States, 2005-2006. MMRW Surveillance Summaries 2008:57(SS09);1-29. Available from: www.cdc.gov/mmwr/preview/mmwrhtml/ss5709a1. htm#tab7.
7. Hlavsa MC, et al. Surveillance for waterborne disease outbreaks and other health events associated with recreational water. United States, 2007-2008. MMRW Surveillance Summaries, 2011/60(ss12);1-32. Available from: www.cdc.gov/mmwr/preview/mmwrhtml/ss6012a1. htm.
8. Centers for Disease Control and Prevention. Surveillance summaries for waterborne disease and outbreaks. Atlanta: CDC. Available from: www.cdc.gov/healthywater/statistics/wbdoss/surveillance.html.
9. Bunning VK, et al. Chronic health effects of microbial foodborne disease. World Health Stat Quarterly 1997;50:51-6.
10. Shields JM et al. Inactivation of Cryptosporidium parvum under chlorinated recreational water conditions. J Wat Health 2008;6:513-20. http://dx.doi.org/10.2166/wh.2008.068
11. Koch J, et al. Norovirus infections in Germany. Bundesgesundheitsb - Gesundheitsforsch - Gesundheitschutz 2006;49: 296-309. [In German].
12. Frost FJ et al. Serological evidence of endemic waterborne Cryptosporidium infections. Ann Epidemiol;12:222-7. http://dx.doi.org/10.1016/ S1047-2797(01)00313-1
13. Smith A, et al. Outbreaks of waterborne infectious intestinal disease in England and Wales, 1992-2003. Epidemiol Infect 2006;134:1141-9. http://dx.doi.org/10.1017/S0950268806006406
14. Yang HH, et al. An outbreak of Salmonella Paratyphi A in a boarding school: a community-acquired enteric fever and carriage investigation. Epidemiol Infect 138:1765-74. http://dx.doi.org/10.1017/S0950268810001986
15. Kanungo S, et al. Epidemiology of typhoid and paratyphoid fever in India. J Infect Develop Countries 2:454-60.
16. Karch H et al. Long-term shedding and clonal turnover of enterohemorrhagic E. coli O157 in diarrheal diseases. J Clin Microbiol 1995;33:1602-5.
17. Robert Koch Institut. Information about the EHEC-/HUS outbreak of May- July 2011 in Germany. End of the outbreak. Epid Bull 2011;31:295-6.
18. Public Health Agency of Canada. Escherichia coli, enterohemorrhagic. Material safety data sheets (MSDS). Available from: www.phac-aspc.gc.ca/lab-bio/ res/psds-ftss/msds63eeng. php
19. Brewster DH, et al. An outbreak of E. coli 0157 associated with a children's paddling pool. Epid Infect 1994;112:441-7.
20. Friedman MS, et al. E. coli O157:H7 outbreak associated with an improperly chlorinated swimming pool. Clin Infect Dis 1999;29:298-303. http://dx.doi.org/10.1086/520204
21. Rangel JM, et al. Epidemiology of E. coli O157:H7 outbreaks, United States, 1982-2002. Emerg Infect Dis 2005;11:603-9. http://dx.doi.org/10.3201/ eid1104.040739
22. World Health Organization. Initiative for vaccine research. Shigellosis. Available from: www.who.int/vaccine-research/diseases/diarrhoeal/en/index6.html.
23. Todar K. Shigella and shigellosis. In: Todar's online textbook of bacteriology. Available from: http://textbookofbacteriology. net/Shigella.html.
24. DuPont, HL. Shigella species (bacillary dysentery). In: Mandell, et al. (Eds.). Douglas, and Bennett's principles and practice of infectious diseases. Fifth edition, Philadelphia, Pa: Churchill Livingstone; 2005. p. 2363-9.
25. DuPont HL, et al. Inoculum size in shigellosis and implications for expected mode of transmission. J Infect Dis 1989; 159:1126-8. http://dx.doi.org/10.1093/infdis/159.6.1126
26. Keene WE, et al. A swimming associated outbreak of hemorrhagic colitis caused by E. coli O157:H7 and Shigella sonnei. New Engl J Med 1994;331:579-84. http://dx.doi.org/10.1056/NEJM199409013310904
27. Hunter PR. Waterborne disease epidemiology and ecology. Chichester, UK: Wiley & Sons Ltd; 1998.
28. Said B, et al. Outbreaks of infectious disease associated with private drinking water supplies in England and Wales 1970- 2000. Epid Infect 2003;130:469-79. http://dx.doi.org/10.1017/S0950268803008495
29. Lund V. Evaluation of E. coli as an indicator for the presence of Campylobacter jejuni and Yersinia enterocolitica in chlorinated and untreated oligotrophic lake water. Wat Res 1996;30:1528-34.http://dx.doi.org/10.1016/0043- 1354(96)00034-6
30. International Committee on Taxonomy of Viruses. Official taxonomy of adenoviruses. Available from: www.vmri.hu/~harrach/AdVtaxlong.htm.
31. Mena KD, Gerba CP. Waterborne adenovirus. Rev Environ Contam Toxicol 2009;198:133-67. http://dx.doi.org/10.1007/978-0-387-09647-6-4
32. Puig M, et al. Detection of adenoviruses and enteroviruses in polluted water by nested PCR amplification. Appl Environ Microbiol 1994;60:2963:70.
33. Bofill-Mas S, et al. Quantification of human adenoviruses in European recreational waters. Food and Environmental Virology 2010;2:101-9. Available from: www springerlink.com/content/e75q7m17k5731452/fulltext. html#CR24#CR24.
34. Crabtree KD, et al. Waterborne adenovirus: a risk assessment. Wat Sci Technol 1996;35:1-6. http://dx.doi.org/10.1016/S0273-1223(97)00225-4
35. Sinclair RG, Jones EL, Gerba CP. Viruses in recreational water- borne disease outbreaks: a review. J Appl Microbiol 2009; 107:1769-80. http://dx.doi.org/10.1111/j.1365-2672.2009.04367.x
36. Artieda J, et al. A swimming pool-related outbreak of pharyngoconjunctival fever in children due to adenovirus type 4, Gipuzkoa, Spain, 2008. Eurosurveillance 2009;14:7-8.
37. World Health Organization. New and under-utilized vaccines implementation (NUVI). Decision making and implementation of rotaviruses vaccines. Disease Burden. Available from: www.who.int/nuvi/rotavirus/decision-implementation/en/ index.html.
38. Atkinson, et al. (Eds.). Epidemiology and prevention of vaccine-preventable diseases. 12th ed. Atlanta: CDC; 2012. Available from: www.cdc.gov/vaccines/pubs/pinkbook/downloads/rota.pdf.
39. Centers for Disease Control and Prevention. About norovirus overview. Available from: www.cdc.gov/norovirus/about/overview.html.
40. Morillo SG, Timenetsky MCST. Norovirus: an overwiev. Rev Assoc Med Bras 2011;57:453-8. http://dx.doi.org/10.1590/S0104-42302011000400023
41. Hedberg CW, Osterholm MT. Outbreaks of food-borne and waterborne viral gastroenteritis. Clin Microbiol Rev 1993; 6:199-210.
42. Tao HW, et al. Waterborne outbreak of rotavirus diarrhea in adults in China caused by a novel rotavirus. Lancet 1:1139-42.http://dx.doi.org/10.1016/ S0140-6736(84)91391-6
43. Hopkins RS, et al. A community waterborne gastroenteritis outbreak: evidence for rotavirus as the agent. Amer J Publ Health 1984;74:263-5. http://dx.doi.org/10.2105/AJPH.74.3.263
44. Gallay A, et al. A large multi-pathogen waterborne community outbreak linked to faecal contamination of a groundwater system, France, 2000. Clin Microbiol Infect 2006;12:561- 70. http://dx.doi.org/10.1111/j.1469-0691.2006. 01441.x
45. Parrino TA, et al. Clinical immunity in acute gastroenteritis caused by Norwalk agent. N Engl J Med 1977;297:86-9. http://dx.doi.org/10.1056/ NEJM197707142970204
46. Maunula L, et al. Wading pool water contaminated with both noroviruses and astroviruses as the source of a gastroenteritis outbreak. Epid Infect 2004;132:737-43. http://dx.doi.org/10.1017/S0950268804002249
47. Anon. Frequent occurrence of Enterovirus-71-Infections in Germany, 2010. Epid Bull 2012;13:108-9. [In German]. Available from: www.rki.de/DE/Content/ Infekt/EpidBull/Archiv/2012/Ausgaben/13-12.pdf?-blob=publicationFile.
48. Bloch A, et al. Recovery of hepatitis A virus from a water supply responsible for a common source outbreak of hepatitis A. Amer J Publ Health 1990;80:428-30. http://dx.doi.org/10.2105/AJPH.80.4.428
49. Fogarty J, et al. Illness in a community associated with an episode of water contamination with sewage. Epid Infect 1995;114:289-95. http://dx.doi.org/10.1017/S0950268800057952
50. Jothikumar N, et al. Detection of hepatitis E virus in raw and treated wastewater with the polymerase chain reaction. Appl Environ Microbiol 1993;59:2558-62. http://dx.doi.org/10.1016/S0043-1354(00)00551-0
51. Taylor MB, et al. The occurrence of hepatitis A and astrovirus in selected river and dam waters in South Africa. Wat Res 2001;35:2653-60.
52. Pond K. Water recreation and disease. Geneva: WHO; 2005.
53. Lane S, Lloyd D. Current trends in research into the waterborne parasite Giardia. Crit Rev Microbiol 2002;28:123-47. http://dx.doi.org/10.1080/1040- 840291046713
54. Chute CG, et al. Risk factors for endemic giardiasis. Amer J Publ Health 1987;77:585-7. http://dx.doi.org/10.2105/AJPH.77.5.585
55. Cotruvo J, et al. (Ed.). Waterborne zoonoses: identification, causes and control. Geneva: WHO; 2004.
56. Pickering LK, et al. Occurrence of Giardia lamblia in children in day care centers. J Pediatr 1984;104:522-6. http://dx.doi.org/10.1016/S0022-3476(84) 80540-5
57. Lee SC, et al. Microsporidia evolved from ancestral sexual fungi. Curr Biol 2008;18:1675-9. http://dx.doi.org/10.1016/j.cub.2008.09.030
58. Weiss LM. Microsporidia: emerging pathogenic protists. Acta Trop 2001;78:89-102. http://dx.doi.org/10.1016/S0001-706X(00)00178-9
59. Campocasso A, et al. Description of two novel Legionella species isolated from environmental water samples. Int J Syst Evol Microbiol 2012. http://dx.doi.org/10.1099/ijs.0.037853-0
60. Fliermans CB, et al. Ecological distribution of Legionella pneumophila. Appl Environ Microbiol 1981;41:9-16.
61. Newton HJ, et al. Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 2010; 23:274-98. http://dx.doi.org/ 10.1128/CMR.00052-09
62. Glick TH, et al. Pontiac fever. An epidemic of unknown etiology in a health department: I. Clinical and epidemiologic aspects. Am J Epid 1978;107:149-60.
63. Bartram J, et al. (Eds.). Legionella and the prevention of legionellosis. Geneva: WHO; 2007.
64. Wadowsky RM, et al. Growth-supporting activity for legionella pneumophila in tap water cultures and implication of hartmannellid amoebae as growth factors. Appl Environ Microbiol 1988;54:2677-82.
65. Yee RB, Wadowsky RM. Multiplication of Legionella pneumophila in unsterilized tap water. Appl Environ Microbiol 1982;43:1330-4.
66. Neumeister B, et al. Influence of Acanthamoeba castellanii on intracellular growth of different Legionella species in human monocytes. Appl Environ Microbiol 2000;66:914-9. http://dx.doi.org/10.1128/AEM.66.3.914-919.2000
67. Lau HY, Ashbolt NJ. The role of biofilms and protozoa in Legionella pathogenesis: implications for drinking water. J Appl Microbiol 2009;107:368-78. http://dx.doi.org/10.1111/j.1365-2672.2009.04208.x
68. Swanson MS, Hammer BK. Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Ann Rev Microbiol 2000;54:567-613. http://dx.doi.org/10.1146/annurev.micro.54.1.567
69. Bornstein N, et al. Exposure to Legionellaceae at a hot spring spa: a prospective clinical and serological study. Epid Infect 1989;102:31-6. http://dx.doi.org/10.1017/S0950268800029654
70. García-Fulgueiras A, et al. Legionnaires' disease outbreak in Murcia, Spain. Emerg Inf Dis 2003 Aug. Available from: wwwnc. cdc.gov/eid/article/9/8/03-0337.htm.
71. Neil K, Berkelman R. Increasing incidence of legionellosis in the US, 1995-2005: changing epidemiologic trends. Clin Infect Dis 2008;47:591-9. http://dx.doi.org/10.1086/590557
72. European Centre for Disease Prevention and Control. Legionnaires' disease in Europe 2009. Stockholm: ECDC; 2011.
73. European Centre for Disease Prevention and Control. Outbreak of Legionnaires' disease in a hotel in Calpe, Spain. November 2011 - June 2012. Stockholm: ECDC; 2012. Available from: http://ecdc.europa.eu/en/publications/ Publications/1207-TERRapid- risk-assessment-legionnaires-disease.pdf.
74. Den Boer JW, et al. A large outbreak of Legionnaires' disease at a Dutch flower show. Emerg Inf Dis 2002;8:1. http://dx.doi.org/10.3201/eid0801.010176
75. De Schrijver K, et al. An outbreak of legionnaires' disease among visitors to a fair in Belgium, 1999. Eurosurveillance 2000;5:115-9. http://dx.doi.org/10.1016/S0033-3506(02)00011-2
76. McEvoy M, et al. A cluster of cases of legionnaires' disease associated with exposure to a spa pool on display. Commun Dis Publ Health 2000;3:43-5.
77. Leoni E, et al. Prevalence of Legionella spp. in swimming pool environment. Wat Res 2001;35:3749-53. http://dx.doi.org/10.1016/S0043-1354(01) 00075-6
78. World Health Organization. Sanitation on ships. Compendium of outbreaks of foodborne and waterborne diseases and Legionnaires' disease associated with ships 1970-2000. Geneva: WHO; 2001.
79. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999;284(5418):1318-22.http://dx.doi. org/10.1126/science.284.5418.1318
80. Rusin PA, et al. Risk assessment of opportunistic bacterial pathogens in drinking water. Rev Environ Contam Toxicol 1997;152:57-83. http://dx.doi.org/10. 1007/978-1-4612-1964-4-2
81. Cogen AL, Nizet V, Gallo RL. Skin microbiota: a source of disease or defence? Br J Dermatol 2008;158:442-55. http://dx.doi.org/10.1111/j.1365-2133. 2008.08437.x
82. Rahme LG, et al. Plants and animals share functionally common bacterial virulence factors. Proc Nat Acad Sci USA 2000;97(16).http://dx.doi.org/10.1073/ pnas.97.16.8815
83. Poole K. Efflux-mediated multiresistance in Gram-negative bacteria. Clin Microbiol Inf 2004;10:12-6. http://dx.doi.org/10.1111/j.1469-0691.2004.00763.x
84. Trautmann M, Lepper PM, Haller M. Ecology of Pseudomonas aeruginosa in the intensive care unit and the evolving role of water outlets as a reservoir of the organism. Am J Infect Control 2005;33(5 Suppl.) :S41-9.http://dx.doi.org/ 10.1016/j.ajic.2005.03.006
85. Salmen P, et al. Whirlpool-associated Pseudomonas aeruginosa urinary tract infections. JAMA 1983;250(15):2025-6. http://dx.doi.org/10.1001/jama.250. 15.2025
86. Watt KB, Swarbrick HA. Microbial keratitis in overnight orthokeratology. Review of the first 50 cases. Eye & Contact Lens: Science & Clinical Practice. 2005;31:201-8. http://dx.doi.org/10.1097/01.icl.0000179705.23313.7e
87. Centers for Disease Control and Prevention. Pseudomonas dermatitis/folliculitis associated with pools and hot tubs; Colorado and Maine, 1999-2000. JAMA 2001;285(2):157-8.
88. Gustafson TL, et al. Pseudomonas folliculitis: an outbreak and review. Rev Infect Dis 1983;5:1-8. http://dx.doi.org/10.1093/clinids/5.1.1
89. Ratnam S, et al. Whirlpool-associated folliculitis caused by Pseudomonas aeruginosa. Report of an outbreak and review. J Clin Microbiol 1986;23:655-9.
90. Price D, Ahearn DG. Incidence and persistence of Pseudomonas aeruginosa in whirlpools. J Clin Microbiol 1988;26:1650-54.
91. Van Asperen IA, et al. Risk of otitis externa after swimming in recreational fresh water lakes containing Pseudomonas aeruginosa. Br Med J 1995;311:1407-10.http://dx.doi.org/10.1136/bmj.311.7017.1407
92. Fiorillo L, et al. The Pseudomonas hot foot syndrome. N Engl J Med 2001;345:335-8. http://dx.doi.org/10.1056/NEJM200108023450504
93. Salmen P, et al. Whirlpool associated Pseudomonas aeruginosa urinary tract infections. JAMA 1983; 250(15):2025-6. Available from: www.ncbi.nlm.nih.gov/pubmed/6413703. http://dx.doi.org/10.1001/jama.250.15.2025
94. Rice SA, et al. A risk assessment of Pseudomonas aeruginosa in swimming pools: a review. J Wat Health 2012;10:181-96. http://dx.doi.org/10.2166/wh.2012. 020
95. Collins CH, et al. Mycobacteria in water. A review. J Appl Bact 1984;57:193-211. http://dx.doi.org/10.1111/j.1365-2672.1984.tb01384.x
96. Falkinham JO, et al. Factors influencing numbers of Mycobacterium avium, Mycobacterium intracellulare, and other mycobacteria in drinking water distribution systems. Appl Environ Microbiol 2001;67:1225-31. http://dx.doi.org/10.1128/AEM.67.3.1225-1231.2001
97. Cirillo JD, et al. Interaction of Mycobacterium avium with environmental amoebae enhances virulence. Infect Immun 1997;65:3759-67.
98. Aubuchon C. Atypical mycobacterial infection of soft tissue associated with use of a hot tub. J Bone and Joint Surg 1986;68-A:766-8.
99. Simon A, et al. Hygienic requirements for the medical care of patients suffering form cystic fibrose (mucoviscidose). mhp-Verlag GmbH; 2012. [In German]. Available from: http://muko. info/fileadmin/redaktion/Forschung/ Therapiefoerderung/CFLeitlinie-Hygiene.pdf.
100. Gregor WM, Keskin N. Atypical mycobacteria in the Niagara peninsula. Can Med Assoc J 1967;96:312-8.
101. Collins CH, et al. Mycobacterium marinum infections in man. J Hyg Camb 1985;94:135-49.
102. http://dx.doi.org/10.1017/S0022172400061349
103. Lumb R, et al. Investigation of spa pools associated with lung disorders caused by Mycobacterium avium Complex in immunocompetent adults. Appl Environ Microbiol 2004; 70:4906-10. http://dx.doi.org/10.1128/AEM.70.8.4906-4910.2004
104. Khoor A, et al. Diffuse pulmonary disease caused by Nontuberculous mycobacteria in immunocompetent people (Hot Tub Lung). Am J Clin Pathol 2001;115:755-62.
105. Heggie TW. Swimming with death. Naegleria fowleri infections in recreational waters. Travel Med Inf Dis 2010;8:201-6. http://dx.doi.org/10.1016/ j.tmaid.2010.06.001
106. Cerva L, et al. An outbreak of acute, fatal amebic meningoencephalitis. Amer J Epid 1968;88:436-44.
107. Caumo K, Rott MB. Acanthamoeba T3, T4 and T5 in swimming-pool waters from Southern Brasil. Acta Tropica 2011;117:233-5. http://dx.doi.org/10.1016/j. actatropica.2010.12.008
108. Radford CF, et al. Acanthamoeba keratitis: multicentre survey in England 1992-6. Br J Ophthalmol 1998;82:1387-92. http://dx.doi.org/10.1136/bjo.82.12. 1387
109. Gianinazzi C, et al. Potentially human pathogenic acanthamoeba isolated from a heated indoor swimming pool in Switzerland. Exp Parasit 2009;121:180-6. http://dx.doi.org/10.1016/j.exppara.2008.11.001
110. Rose CS, et al. "Lifeguard Lung": endemic granulomatous pneumonitis in an indoor swimming pool. Amer J Publ Health 1998;88:1795:800. http://dx.doi.org/10.2105/AJPH.88.12.1795
111. Robinton ED Mood EW. A quantitative qualitative appraisal of microbial pollution of water by swimmers a Preliminary Report. J Hyg (London) 1966;64489-99. Httpdx.doi.org10.1017S0022172400040808
112. Begier EM, et al. A high-morbidity outbreak of methicillin- resistant Staphylococcus aureus among players on a college football team, facilitated by cosmetic body shaving and turf burns. Clin Infect Dis 2004;39:1446-53. http://dx.doi.org/10.1086/425313
113. Favero MS, et al. Use of staphylococci as indicators of swimming pool pollution. Publ Health Rep 1964;79:61-70. http://dx.doi.org/10.2307/4592053
114. Pereire-Neves A, Benchimol M. Trichomonas vaginalis. In vitro survival in swimming pool water samples. Exp Parasit 2008;118:438-41. http://dx.doi.org/10. 1016/j.exppara.2007.09.005
115. Nett G, Schär M. Transmission of Trichomonas vaginalis in swimming pools? Soz Praventivmed 1986;31:247-8.
116. Castilla MT, et al. Molluscum contagiosum in children and its relationship to attendance at swimming-pools: an epidemiological study. Dermatology 1995;191:65. http://dx.doi.org/10.1159/000246540
117. Anon. Molluscum (Molluscum contagiosum). Center for Disease Control and Prevention. http://www.cdc.gov/ncidod/dvrd/molluscum/faq/everyone.htm#whogets.
118. Van Haalen FM, et al. Warts in primary schoolchildren: prevalence and relation with environmental factors. Brit J Dermatol 2009;161:148-52. http://dx.doi.org/10.1111/j.1365-2133.2009.09160.x
119. Seebacher C, et al. Updates on the epidemiology of dermatophyte infections. Mycopathologia 2008;166:335-52. http://dx.doi.org/10.1007/s11046- 008-9100-9