CDC REVIEW ARTICLE Edited by: Larry K. Pickering, MD Editor s Note: Outbreaks of recreational water-related illnesses have shown an increasing trend over the past 10 years. Strategies for prevention and control include recruiting health care professionals to educate their patient populations about healthy swimming habits. This article highlights important issues and directions the medical community can implement to reduce recreational water-related infectious diseases. Reducing Illness Transmission From Disinfected Recreational Water Venues Swimming, Diarrhea and the Emergence of a New Public Health Concern Mei Lin Castor, MD, and Michael J. Beach, PhD* Abstract: Recreational water-related illnesses are associated with swimming in contaminated water venues. The transmission of diarrheal illness in disinfected settings is influenced by several factors which include: chlorine resistance in waterborne pathogens; poor facility maintenance of disinfectant levels; and lack of healthy swimming habits. Health care providers can help to disseminate healthy swimming messages to their patients and help to prevent and control this emerging public health concern. Key Words: recreational water illnesses, swimming, Cryptosporidium, swimming pools, education, shiga toxinproducing Escherichia coli, Giardia, Escherichia coli O157:H7 (Pediatr Infect Dis J 2004;23: 866 870) Water, both drinking and recreational, is a well-documented transmission vehicle for infectious diseases throughout the world. 1 Recreational water-related illnesses refer to the spectrum of illnesses associated with swimming in contaminated recreational water venues such as swimming pools, hot tubs, lakes, rivers and the ocean. Recreational water-related illnesses include diarrhea and skin, ear, eye, neurologic, respiratory and wound infections. 2 11 Some of the consequences of these waterborne infections are serious and life-threatening, particularly in the young, the elderly, the pregnant and the immunosuppressed. 12 14 The complex nature of recreational water-related illness transmission requires that a multifaceted approach be integrated into any proposed prevention plan. This should include participation of the health care community in implementing educational and behavioral modification strategies. This review focuses on the occurrence of diarrheal illness transmitted through exposure to disinfected or treated swimming venues. In this article, we discuss: (1) the biologic, environmental and behavioral factors contributing to recreational waterrelated illnesses in the United States; (2) surveillance data documenting increasing occurrence of diarrheal illness associated with recreational water use; (3) swimming pool inspection data revealing pool maintenance inadequacies; (4) investigations demonstrating the impact of recreational water-related illnesses on the swimming public; and (5) proposed guidelines highlighting the critical role that health care providers can play in prevention of diarrheal illness. Accepted for publication June 14, 2004. From the *Division of Parasitic Diseases, National Center for Infectious Diseases, and the Preventive Medicine Residency Program, Epidemiology Program Office, Centers for Disease Control and Prevention, Atlanta, GA Reprints not available. Copyright 2004 by Lippincott Williams & Wilkins ISSN: 0891-3668/04/2309-0866 DOI: 10.1097/01.inf.0000138081.84891.30 BIOLOGIC, ENVIRONMENTAL AND BEHAVIORAL FACTORS CONTRIBUTING TO TRANSMISSION OF RECREATIONAL WATER-RELATED ILLNESSES Waterborne pathogens present unique challenges for aquatics venues. Pathogen characteristics such as environmental stability of pathogens, high concentrations of organ- 866 The Pediatric Infectious Disease Journal Volume 23, Number 9, September 2004
The Pediatric Infectious Disease Journal Volume 23, Number 9, September 2004 Recreational Water-Related Illnesses isms, and low infectious doses are important factors in potential for transmission. In disinfected aquatics venues, chlorination is the main barrier to infectious disease transmission. The parasites Cryptosporidium spp. and Giardia spp. and the noroviruses (Norwalk-like viruses) have varying degrees of chlorine resistance. 15 18 Cryptosporidium oocysts can survive for days at chlorine concentrations typically found in swimming venues making traditional pool chlorination ineffective as a barrier to Cryptosporidium transmission. Although most fecal orally transmitted bacteria, such as Escherichia coli O157:H7, are chlorine-susceptible, outbreaks caused by this pathogen have occurred in treated recreational water facilities because of poor maintenance of disinfectant concentrations. 19 21 Cryptosporidium and Giardia have low infectious doses ( 132 oocysts and 10 cysts, respectively) and high excretion concentrations (up to 10 6 oocysts or cysts per g of stool); a single fecal accident can be all that is necessary to contaminate a water park containing millions of gallons of water. 22 25 In these settings, swallowing only a few mouthfuls of contaminated water is sufficient for disease transmission. In addition, Cryptosporidium and Giardia are often shed at low concentrations for weeks after cessation of diarrhea. 23,26 This facilitates disease transmission not only from swimmers who have diarrheal illness but also from people who are recovering from illness. Diarrheal illness and fecal contamination of swimming venues are common in the United States. Approximately 11% of the U.S. population have had diarrhea in the prior month, indicating that there is at least 1 diarrheal episode/person/ year. 27 In addition, 2% of the population were reported to be fecally incontinent in a Wisconsin community survey; 70% of this fecally incontinent population were younger than 65 years of age. 28 The high proportion of diarrheal illness in the population and the increase in reported outbreaks make it likely that persons ill with diarrhea commonly are visiting swimming venues. The communal nature and shared water aspects of swimming facilitates transmission of waterborne pathogens having fecal-oral spread. High usage during peak swim season including heavy use of swimming pools by diapered and toddler age children contributes to the possibility of fecal contamination in these settings. Fecal accidents are common events, sometimes occurring daily in the same venue. 29 Even in the absence of fecal accidents, a lack of showering before entering swimming pools may contribute to contamination from swimmers bodies. An average of 0.14 g of feces is present on the perianal surface of persons; in children, the amount may be up to 10 g/child. 30 Exposure to recreational water venues is extremely high in the United States. As the second most popular exercise activity in the United States, 61 million persons older than 7 years swim at least 6 times per year. Fifty-seven percent of children in the United States 7 17 years of age swim at least 6 times per year. At a minimum, 368 million annual person-visits occur at U.S. swimming venues. 31 These biologic, environmental and behavioral factors contribute to the emergence of recreational water-related illnesses, particularly in disinfected aquatic venues. Understanding these contributing factors is critical to the development and implementation of effective recreational waterrelated illness prevention and control measures. SURVEILLANCE FINDINGS Surveillance for recreational water-related illness outbreaks of gastrointestinal tract illness has documented a statistically significant increase in the number of reported outbreaks during the past 2 decades (Fig. 1). 32 This trend is primarily driven by a steady increase in outbreaks associated with disinfected swimming venues versus outbreaks occurring in fresh water venues such as lakes and rivers (Fig. 2). 32 Pathogens contributing to these outbreaks vary depending on the type of swimming venue (Fig. 3), and surveillance data have revealed the importance of pathogens such as Cryptosporidium and shiga toxin-producing E. coli. 32 36 In fresh water venues, E. coli O157:H7 and Shigella spp. account for most outbreaks where a pathogen is identified. In treated water venues, Cryptosporidium accounts for 66% of reported outbreaks of diarrheal illness in the United States. 32 36 This may be in large part because of the extreme chlorine resistance exhibited by the parasite, which renders pool chlorination an ineffective barrier to transmission. National surveillance data for Cryptosporidium and Giardia also demonstrate a marked seasonality with peaks for transmission occurring during the summer months. 37 38 This coincides with the annual swim season and further supports findings that recreational water plays a key role in transmission of these parasites. As illustrated in Figure 3, pathogens such as E. coli O157:H7 and Shigella cause 12% of reported outbreaks in FIGURE 1. Recreational water-related illness outbreaks of gastroenteritis: United States, 1978 2000. 32 Total number of outbreaks, 145. 2004 Lippincott Williams & Wilkins 867
Castor and Beach The Pediatric Infectious Disease Journal Volume 23, Number 9, September 2004 FIGURE 2. Recreational water-related illness outbreaks of gastroenteritis: United States, 1985 2000. 32 Total number of outbreaks, 134. indicates disinfected venues;, freshwater venues. disinfected venues. These outbreaks underscore the importance of proper pool maintenance because these chlorinesusceptible pathogens would have been susceptible to typical disinfection procedures had they been implemented properly. Assurance of adequate pool maintenance is complicated by a lack of federal regulation and oversight that has resulted in varied state and local regulations, enforcement and compliance throughout the country. In U.S. surveillance data from 22,000 swimming pool inspections performed during the summer of 2002, 54% of inspections had 1 or more violations (range, 1 12 violations). Eight percent of inspections resulted in immediate pool closure, reinforcing the need for increased efforts to assure a higher standard of pool operation throughout the country. 39 OUTBREAK CASE STUDIES Two outbreak investigations illustrate how chlorine resistance of waterborne pathogens and inadequate pool maintenance contribute to the occurrence of recreational water-related illness outbreaks. The first was a cryptosporidiosis outbreak in Nebraska in 2000. 40 The outbreak was detected initially when the state surveillance system noted an increase in the number of cryptosporidiosis cases reported compared with the same period in previous years. The investigation documented 200 cases of diarrhea caused by Cryptosporidium confirmed by clinical evaluation and/or laboratory tests. All infections were associated with the use of 2 swimming pools. Water samples from both pools were positive for Cryptosporidium oocysts. Control measures consisted of closure and hyperchlorination of both pools. Hyperchlorination protocols to inactivate Cryptosporidium typically require chlorine concentrations that exceed acceptable swimming levels, making pool closure necessary. Despite these control measures, the outbreak expanded to include additional community pools. The initial closure of the 2 implicated pools had resulted in the use of other community pools by ill swimmers. Interviews revealed that 18% of ill persons continued swimming despite being symptomatic and that 32% swam during illness or during the 2 weeks after illness when transmission could still occur. This outbreak highlights: (1) that even properly maintained swimming pools can spread illness when chlorine-resistant pathogens are involved; and (2) how behaviors, such as swimming when ill with diarrhea, can initiate or contribute to the occurrence and amplification of enteric illness outbreaks in a community. Extensive education about healthy swimming habits may have reduced further amplification of this outbreak. The second outbreak occurred in a recreational water park in Georgia in 1998. 41 A child-care center coordinator reported several children ill with bloody diarrhea including one hospitalized with hemolytic-uremic syndrome secondary to E. coli O157:H7 infection. The investigation documented 26 persons with E. coli O157:H7 infections; 7 were hospitalized and 1 death occurred. All ill persons had visited the Georgia water park and played in one particular kiddie pool. The suspect kiddie pool had a low disinfectant level that was believed to have contributed to the outbreak. This out- FIGURE 3. Pathogens identified in recreational water-related illness outbreaks of gastroenteritis (gastro): United States, 1991 2000. 32 36 Disinfected venues, n 53; the Other category includes Campylobacter, norovirus and Salmonella. Freshwater venues, n 53. 868 2004 Lippincott Williams & Wilkins
The Pediatric Infectious Disease Journal Volume 23, Number 9, September 2004 Recreational Water-Related Illnesses break highlights: (1) the role of poor facility maintenance in promoting outbreaks; (2) the need for education of pool operators about the transmission risk of recreation waterrelated illnesses from poor facility maintenance; and (3) how behaviors, such as swimming when ill with diarrhea, can contribute to the occurrence of recreational water-related illness outbreaks. PREVENTION AND CONTROL STRATEGIES: THE ROLE OF THE HEALTH CARE COMMUNITY Any prevention and control strategy must address several issues: technologic challenges related to adequate disinfection procedures; management and maintenance lapses; training deficiencies; and the general public s lack of awareness concerning healthy swimming habits. Because of this, prevention strategies must incorporate a multidisciplinary approach that targets the general public, aquatics facilities staff, public health practitioners and health care providers. Prevention measures should include critical components such as the redesign of aquatics facilities and increased governmental oversight of swimming pool maintenance and aquatics staff training, and education of the general public about healthy swimming habits. As part of an effort to understand what the public thinks about swimming and disease transmission, the Centers for Disease Control and Prevention conducted a series of focus discussion groups with parents of young swimmers. Findings revealed that parents lacked awareness of the potential for disease transmission in swimming pools. They did not equate swimming in chlorinated pools with communal bathing or water sharing. They believed that chlorination killed organisms instantaneously and rendered the water sterile. Finally they were not aware of the existence of chlorine-resistant pathogens. Parents were open to learning and changing their swimming behaviors and suggested multiple avenues for recreational water-related illness education such as the media, schools, child-care centers and aquatics centers. However, they preferred to receive education about recreational water-related illnesses from a trusted source such as a pediatrician or other health care provider. 42 Multiple challenges face health care providers in educating patients about recreational water-related illnesses. These include several myths that should be dispelled: (1) chlorine kills all organisms instantaneously and leaves pool water sterile; (2) it is acceptable to swim when ill with diarrhea; and (3) it is safe to swallow pool water. As demonstrated by the outbreak in Nebraska, even a well-maintained pool is only as safe as the health of the swimmers who use it. Healthy swimming messages need to be disseminated to the general public, especially patients with diarrhea and parents of diapered and toddler age children. In addition, groups at risk for serious complications from enteric infections such as the young, the elderly, the pregnant and the immunosuppressed should receive targeted health education messages. Health care providers can play a key role by providing anticipatory guidance and/or health education materials to parents of ill children and patients. This information can influence and guide behaviors. These simple and practical messages (also posted at www.healthyswimming.org) include the following: (1) don t swim when you have diarrhea; (2) don t swallow pool water; (3) shower with soap and water before swimming; (4) wash your hands with soap and water after using a toilet or after changing diapers; (5) take your children on bathroom breaks or check diapers often; (5) change diapers in a bathroom and not at poolside; and (6) wash your child thoroughly with soap and water before swimming. It may also be judicious to recommend that patients ill with infectious diarrhea refrain from swimming for 2 weeks after cessation of diarrhea, particularly if they are infected with Cryptosporidium or Giardia, which may be excreted for several weeks after symptoms resolve. These prevention measures also should be reinforced with patients using recreational water when traveling domestically and/or internationally. By educating themselves and their patients about recreational water-related illnesses and healthy swimming behaviors, health care providers can have a significant impact on the morbidity and mortality associated with recreational water-related illnesses and can contribute to the prevention of this emerging public health concern. ACKNOWLEDGMENTS We thank Dr. Larry Pickering for the support he has given the Healthy Swimming Project. REFERENCES 1. Pruss A, Kay D, Fewtrell L, Bartram J. Estimating the burden of disease from water, sanitation, and hygiene at a global level. Environ Health Perspect. 2002;110:537 542. 2. Pruss A. Review of epidemiological studies on health effects from exposure to recreational water. Int. J Epidemiol. 1998;27:1 9. 3. McAnulty JM, Fleming DW, Gonzalez A. A community-wide outbreak of cryptosporidiosis associated with swimming at a wave pool. JAMA. 1994;272:1597 1600. 4. Cabelli VJ, Dufour AP, McCabe LJ, et al. Swimming-associated gastroenteritis and water quality. Am J Epidemiol. 1982;115:606 616. 5. Jones F, Bartlett CL. Infections associated with whirlpools and spas. Soc Appl Bacteriol Symp Ser. 1985;14:61S 66S. 6. Calderon R, Mood E, Dufour A. Health effects of swimmers and nonpoint sources of contaminated water. Int J Environ Health Res. 1991;1:21 31. 7. Caldwell GG, Lindsey NJ, Wulff H, et al. Epidemic of adenovirus type 7 acute conjunctivitis in swimmers. Am J Epidemiol. 1974;99:230 234. 8. Visvesvara G, Stehr-Green J. Epidemiology of free-living ameba infections. J Protozool. 1990;37:26S 33S. 9. Khoor A, Leslie KO, Tazelaar HD, et al. Diffuse pulmonary disease caused by nontuberculous mycobacteria in immunocompetent people (hot tub lung). Am J Clin Pathol. 2001;115:755 762. 10. Mangione EJ, Remis RS, Tait KA, et al. An outbreak of Pontiac fever 2004 Lippincott Williams & Wilkins 869
Castor and Beach The Pediatric Infectious Disease Journal Volume 23, Number 9, September 2004 related to whirlpool use, Michigan 1982. JAMA. 1985;253:535 539. 11. Hollyoak V, Allison D, Summers J. Pseudomonas aeruginosa wound infection associated with a nursing home s whirlpool bath. Commun Dis Rep CDR Rev. 1995;5:R100 R102. 12. Frisby HR, Addiss DG, Reiser WJ, et al. Clinical and epidemiologic features of a massive waterborne outbreak of cryptosporidiosis in persons with HIV infection. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;16:367 373. 13. Guerrant R. Cryptosporidiosis: an emerging, highly infectious threat. Emerg Infect Dis. 1997;3:51 57. 14. Hoxie NJ, Davis JP, Vergeront JM, et al. Cryptosporidiosis-associated mortality following a massive waterborne outbreak in Milwaukee, Wisconsin. Am J Public Health. 1997;87:2032 2035. 15. Korich D, Mead J, Madore M, et al. Effects of ozone, chlorine dioxide, chlorine, and monochloramine on Cryptosporidium parvum oocyst viability. Appl Environ Microbiol. 1990;56:1423 1428. 16. Chauret C, Nolan K, Chen P, et al. Aging of Cryptosporidium parvum oocysts in river water and their susceptibility to disinfection by chlorine and monochloramine. Can J Microbiol. 1998;44:1154 1160. 17. Jarroll EJ. Effect of disinfectants on Giardia cysts. Crit Rev Environ Control. 1988;18:1 28. 18. Keswick B, Satterwhite T, Johnson P, et al. Inactivation of Norwalk virus in drinking water by chlorine. Appl Environ Microbiol. 1985;50: 261 264. 19. Rice E, Clark R, Johnson C. Chlorine inactivation of Escherichia coli 0157:H7. Emerg Infect Dis. 1999;5:461 464. 20. Friedman M, Roels T, Koehler J, et al. Escherichia coli 0157:H7 outbreak associated with an improperly chlorinated swimming pool. Clin Infect Dis. 1999;29:298 303. 21. Hildebrand JM, Maguire HC, Holliman RE, et al. An outbreak of Escherichia coli O157 infection linked to paddling pools. Commun Dis Rep CDR Rev. 1996;6:R33 R36. 22. DuPont H, Chappell C, Sterling C, et al. The infectivity of Cryptosporidium parvum in healthy volunteers. N Engl J Med. 1995;332:855 859. 23. Rendtorff R. The experimental transmission of human intestinal protozoan parasites, II: Giardia lamblia cysts given in capsules. Am J Hyg. 1954;59:209 220. 24. Goodgame RW, Genta RM, White AC, et al. Intensity of infection in AIDS-associated cryptosporidiosis. J Infect Dis. 1993;167:705 709. 25. Danciger M, Lopez M. Numbers of Giardia in the feces of infected children. Am J Trop Med Hyg. 1975;24:237 242. 26. Stehr-Green J, McCaig L, Remsen H, et al. Shedding of oocysts in immunocompetent individuals infected with Cryptosporidium. Am J Trop Med Hyg. 1987;36:338 342. 27. Mead P, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg Infect Dis. 1999;5:607 625. 28. Nelson R, Norton N, Cautley E, et al. Community-based prevalence of anal incontinence. JAMA. 1995;274:559 561. 29. CDC. Prevalence of parasites in fecal material from chlorinated swimming pools: United States, 1999. MMWR. 2001;50:410 412. 30. Gerba CP. Assessment of enteric pathogen shedding by bathers during recreational activity and its impact on water quality. Quant Microbiol. 2000;2:55 68. 31. United States Bureau of the Census. Statistical abstract of the United States. 115th ed. Washington, DC: US Bureau of the Census; 1995. 32. Lee SH, Levy DA, Craun GF, et al. Surveillance for waterborne-disease outbreaks: United States, 1999 2000. MMWR Surveill Summ. 2002;51: 1 47. 33. Barwick RS, Levy DA, Beach MJ, et al. Surveillance for waterbornedisease outbreaks, United States, 1997 1998. MMWR Surveill Summ. 2000;49:1 35. 34. Levy DA, Bens MS, Craun GF, et al. Surveillance for waterborne disease outbreaks: United States, 1995 1996. MMWR Surveill Summ. 1998;47:1 34. 35. Kramer MH, Herwaldt BL, Craun GF, et al. Surveillance for waterborne disease outbreaks: United States, 1993 1994. MMWR Surveill Summ. 1996;45:1 33. 36. Moore AC, Herwaldt BL, Craun GF, et al. Surveillance for waterborne disease outbreaks: United States, 1991 1992. MMWR Surveill Summ. 1993;42:1 22. 37. Dietz V, Roberts JM. National surveillance for infection with Cryptosporidium parvum, 1995 1998: what have we learned? Public Health Rep. 2000;115:358 363. 38. Furness BW, Beach MJ, Roberts JM. Giardiasis surveillance, United States, 1992 1997. MMWR Surveill Summ. 2000;49(SS-7):1 13. 39. CDC. Surveillance data from swimming pool inspections: selected states and counties, United States, May-September 2002. June 6, 2003. MMWR. 2003;52:513 516. 40. CDC. Protracted outbreaks of cryptosporidiosis associated with swimming pool use: Ohio and Nebraska, 2000. MMWR. 2001;50:406 410. 41. Gilbert L, Blake P. Outbreak of Escherichia coli 0157:H7 infections associated with a water park. Georgia Epidemiol Rep. 1998;14:1 6. 42. Macro International. Cryptosporidium and waterparks: an opportunity for disease prevention. Internal report to CDC, 1999. 870 2004 Lippincott Williams & Wilkins