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  • Original Article
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Incorporating susceptible subpopulations in microbial risk assessment: pediatric exposures to enteroviruses in river water

Abstract

The City of Stockton, California operates a wastewater treatment facility that discharges treated effluent to the San Joaquin River. During a recent discharge permit renewal, the question was raised whether pathogenic microorganisms in the effluent may cause an unacceptably high health risk for body contact recreation in the vicinity of the discharge. An investigation was initiated to characterize the risk to public health via body contact recreation in the San Joaquin River under various flow and treatment scenarios. In this investigation, a disease transmission model was applied to quantitatively characterize the relative risk associated with various treatment and flow scenarios for the City of Stockton's wastewater treatment facility. An important component of the investigation was to assess the feasibility of quantitatively characterizing the risk to highly susceptible subpopulations for effluent-related exposures to enteroviruses. This paper presents the methods used to conduct the feasibility assessment, the conclusions drawn for this project, and our recommendations to improve exposure assessments of susceptible subpopulations' contact with microbial pathogens in recreational water.

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References

  • Anderson M.A., Stewart M., Yates M.V., and Gerba C.P. Modeling the impact of body-contact recreation on pathogen concentrations in a source drinking water reservoir. Water Res 1998: 32: 3293–3306.

    Article  CAS  Google Scholar 

  • Anderson R.M., and May R. Infectious Diseases of Humans: Dynamics and Control. Oxford University Press; New York, NY, 1991.

    Google Scholar 

  • Balbus J., Parkin R., and Embrey M. Susceptibility in microbial risk assessment: definitions and research needs. Environ Health Perspect 2000: 108: 901–905.

    Article  CAS  Google Scholar 

  • Balbus J., Parkin R., Makri A, Ragain L., Embrey M., and Hauchman F. Defining susceptibility for microbial risk assessment: results of a workshop. Risk Anal 2003 (in press).

  • Brion G.M., Meschke J.S., and Sobsey M.D. F-specific RNA coliphages: occurrence types, and survival in natural waters. Water Res 2002: 36: 2419–2425.

    Article  CAS  Google Scholar 

  • Cabelli V.J., Dufour A.P., McCabe L.J., and Levin M.A. Swimming-associated gastroenteritis and water quality. Am J Epidemiol 1982: 115: 606–616.

    Article  CAS  Google Scholar 

  • California Regional Water Quality Control Board (CA RWQCB). Waste Discharge Requirements for the City of Stockton Regional Water Quality Control Plant. 1994: Order 94–324.

  • Centers for Disease Control and Prevention (CDC). Surveillance for waterborne disease outbreaks, 1985. MMWR 1988: 49: 15–24.

  • Centers for Disease Control and Prevention (CDC). Surveillance for waterborne disease outbreaks, 1986–1988. MMWR 1990: 39: 1–13.

  • Centers for Disease Control and Prevention (CDC). Surveillance for waterborne disease outbreaks, 1989–1990. MMWR 1991: 40: 1–21.

  • Centers for Disease Control and Prevention (CDC). Surveillance for waterborne disease outbreaks—United States, 1991–1992. MMWR 1993: 42: SSO5.

  • Centers for Disease Control and Prevention (CDC). Surveillance for waterborne disease outbreaks—United States, 1993–1994. MMWR 1996: 45: SSO1.

  • Centers for Disease Control and Prevention (CDC). Surveillance for waterborne disease outbreaks—United States, 1995–1996. MMWR 1998: 47: SSO5.

  • Centers for Disease Control and Prevention (CDC). Surveillance for waterborne disease outbreaks—United States, 1997–1998. MMWR 2000: 49: SSO4.

  • Cooper R.C., Olivieri A.W., Danielson R.E., Badger, P.E., Spear R.C., and Selvin S. Evaluation of military field water-quality, vol 5: infectious organisms of military concern associated with consumption. Assessment of health risks and recommendations for establishing related standards. Report No. UCRL-21008, Lawrence Livermore Laboratory, Livermore, CA, 1986.

  • D'Alessio D.J., Minor T.E., Allen C.I., Tsiatis A.A., and Nelson D.B. A study of the proportions of swimmers among well controls and children with enterovirus-like illness shedding or not shedding enterovirus. Am J Epidemiol 1981: 113: 533–541.

    Article  CAS  Google Scholar 

  • Danes L., Havelkova M., and Prochazkova I. Prevalence of infection with nonpolio enteroviruses among healthy children from a children's home and in a summer camp. J Hyg Epidemiol Microbiol Immunol 1983: 27: 163–172.

    CAS  PubMed  Google Scholar 

  • Denis F.A., Blanchouin E., DeLignieres A., and Flamen P. Coxsackie A16 infection from lake water. JAMA 1974: 228: 1370–1371.

    Article  CAS  Google Scholar 

  • Eisenberg J.N.S., Brookhart M.A., Rice G., Brown M., and Colford J.M. Disease transmission models for public health decision-making: analysis of epidemic and endemic conditions caused by waterborne pathogens. Environ Health Perspect 2002 Aug;110 (8): 783–790.

    Article  Google Scholar 

  • Eisenberg J.N.S., Seto E.Y.W., Colford J.M., Olivieri A., and Spear R.C. An analysis of the Milwaukee cryptosporidiosis outbreak based on a dynamic model of the infection process. Epidemiology 1998: 9: 255–263.

    Article  CAS  Google Scholar 

  • Eisenberg J.N., Seto E.Y.W., Olivieri A., and Spear R.C. Quantifying water pathogen risk in an epidemiological framework. Risk Anal 1996: 16: 549–563.

    Article  CAS  Google Scholar 

  • Embrey M., Parkin R., and Balbus J. Handbook of CCL Microbes in Drinking Water. American Water Works Association, Denver, CO, 2002.

    Google Scholar 

  • EOA Inc. City of Stockton Health Risk Assessment Phase II. Prepared by Soller J. and Olivieri, A. for the City of Stockton, 2002.

  • EOA Inc., U.C. Berkeley. Microbial risk assessment for reclaimed water. Prepared for the Irvine Ranch Water District and the National Water Resource Association, 1995.

  • EOA Inc., U.C. Berkeley. Evaluation of pathogen risk assessment framework. Prepared by Soller J.A., Eisenberg J.N., and Olivieri A.W. for ILSI Risk Science Institute, 1999.

  • Fankhauser R.L., Noel J.S., Monroe S.S., Ando T., Glass R.I. Molecular epidemiology of “Norwalk-like viruses” in outbreaks of gastroenteritis in the United States. J Infect Dis 1998: 178: 1571–1578.

    Article  CAS  Google Scholar 

  • Field P.R., Murphy A.M., Gibson H.B., and Rennie T.F. An outbreak of gastro-enteritis associated with echovirus type 1. Med J Aust 1968: 9–11.

  • Fuhs G.W. A probabilistic model of bathing beach safety. Sci Total Environ 1975: 4: 165–175.

    Article  CAS  Google Scholar 

  • Gantzer C., Gillerman L., Kuznetsov M., and Oron G. Adsorption and survival of faecal coliforms, somatic coliphages and F-specific RNA phages in soil irrigated with wastewater. Symposium of the First World Water Congress International Water Association “Health Related Water Microbiology”, Paris, France, 2000.

  • Gelfand H.M., Holguin A.H., Marchetti G.E., and Feorino P.M. A continuing surveillance of enterovirus infections in healthy children in six United States cities. I. Viruses isolated during 1960 and 1961. Am J Hyg 1963: 78: 358–375.

    CAS  PubMed  Google Scholar 

  • Gosbell I., Robinson D., Chant K, and Crone S. Outbreak of echovirus 30 meningitis in Wingecarribee Shire, New South Wales. Commun Dis Intell 2000: 24: 121–124.

    CAS  PubMed  Google Scholar 

  • Haas C.N. Estimation of risk due to low doses of microorganisms: a comparison of alternative methodologies. Am J Epidemiol 1983: 55: 573–582.

    Article  Google Scholar 

  • Harris J.R., Cohen M.L., and Lippy E.C. Water-related disease outbreaks in the United States. J Infect Dis 1983: 148: 759–762.

    Article  CAS  Google Scholar 

  • Hawley H.B., Morin D.P., Geraghty M.E., Tomkow J., and Phillips C.A. Coxsackievirus B epidemic at a boys’ summer camp. JAMA 1973: 226: 33–36.

    Article  CAS  Google Scholar 

  • Hethcote H. Qualitative analyses of communicable disease models. Math Biosci 1976: 28: 335–356.

    Article  Google Scholar 

  • Kee F., McElroy G., Stewart D., Coyle P., and Watson J. A community outbreak of echovirus infection associated with outdoor swimming pool. J Public Health Med 1994: 16: 145–148.

    Article  CAS  Google Scholar 

  • Koopman J.S., and Longini I.M. The ecological effects of individual exposures and nonlinear disease dynamics in populations. Am J Public Health 1994: 84: 836–842.

    Article  CAS  Google Scholar 

  • Koopman J.S., Longini I.M., Jacquez J.A., and Simon C.P. Assessing risk factors for transmission of infection. Am J Epidemiol 1991: 133: 1199–1209.

    Article  CAS  Google Scholar 

  • Levine W.C., and Stephenson W.T. Waterborne disease outbreaks 1986–1988. MMWR 1990: 39: SS-l.

    Google Scholar 

  • Makri A., Modarres R., and Parkin R. Cryptosporidiosis in New York City: a case study of incorporating susceptibility into microbial risk assessment. Report to the Office of Water of the US Environmental Protection Agency, Washington, DC, 2002.

  • Matsura K., Hasegawa S., Nakayama T., Morita O., and Uetake H. Viral pollution of the rivers in Toyama City. Microbiol Immunol 1984: 28: 575–588.

    Article  Google Scholar 

  • McLaughlin M.R., and Rose J.B. Evaluation of the bacteroides fragilis phage as an alternative indicator of sewage pollution. Symposium of the first World Water Congress International Water Association, “Health Related Water Microbiology”, Paris, France, 2000.

  • Mead P.S., Slutsker L., Dietz V., McCaig L.F., Bresee J.S., Shapiro C., Griffin P.M., and Tauxe R.V. Food related illness and death in the United States. Emerg Infect Dis 1999: 5(5): 1–28.

    Article  Google Scholar 

  • Miyama K., Yamashita K., Yamadera S., Kato N., Akatsuka M., Hara M., and Inouye S., Yamazaki S. Poliovirus surveillance: isolation of poliovirus in Japan, 1980–1991. Jpn J Med Sci Biol 1992: 45: 203–214.

    Article  Google Scholar 

  • Miller S.I., and Pegues D.A. Salmonella species, including Salmonella typhi. In: Mandell G.L., Bennett J.E., and Dolin R. (Eds.). Principles and Practice of Infectious Diseases, 4th edn. Churchill Livingstone, Inc., New York, NY, 1995, pp. 2344–2363.

    Google Scholar 

  • Modlin JF. Introduction to Picomaviridae. In: Mandell GL, Bennett J.E., and Dolin R. (Eds.). Principles and Practice of Infectious Diseases, 5th edn. Churchill Livingstone, Inc., Philadelphia, PA, 2000, pp. 1888–1895.

    Google Scholar 

  • Morens D.M., and Pallansch M.A. Epidemiology. In: Rotbart H.A. (Ed.). Human Enterovirus Infections. American Society of Microbiology, Washington, DC, 1995, pp. 3–23.

    Google Scholar 

  • Mulders M.N., Reimerink J.H.J., Koopmans M.P.G, and van Loon A.M., van der Avoort H.G.A.M. Genetic analysis of wild-type poliovirus importation into the Netherlands (1979–1995). J Infect Dis 1997: 176: 617–624.

    Article  CAS  Google Scholar 

  • National Research Council. Risk Assessment in the Federal Government, Managing the Process. National Academy Press, Washington, DC, 1983.

  • Okhuysen P.C., Chappell C.L., Crabb J.H., Sterling C.R., and DuPont H.L. Virulence of three distinct Cryptosporidium parvum isolates for healthy adults. J Infect Dis 1999: 180: 1275–1281.

    Article  CAS  Google Scholar 

  • Oostvort P.M., van Wijngaarden J.K., van der Avoort H.G.A.M., Mulders M.N, Conyn-van Spaendonck M.A.E., Rumke H.C., van Steenis G., and van Loon A.M. Poliomyelitis outbreak in an unvaccinated community in the Netherlands, 1992–1993. Lancet 1994: 344: 665–670.

    Article  Google Scholar 

  • Palmateer G.A., Dutka B.J., Janzen E.M., Meissner S.M., and Sakellaris M.G. Coliphage and bacteriophage as indicators of recreational water quality. Water Res 1991: 25: 355–357.

    Article  Google Scholar 

  • Payment P., Affoyon F., and Trudel M. Detection of animal and human enteric viruses in water from the Assomption River and its tributaries. Can J Microbiol 1988: 34: 967–973.

    Article  CAS  Google Scholar 

  • Perz J.F., Ennever F.K., and Le Blancq S.M. Cryptosporidium in tap water: comparison of predicted risks with observed levels of disease. Am J Epidemiol 1998: 147: 289–301.

    Article  CAS  Google Scholar 

  • Regli S., Rose J.B., Haas C.N., and Gerba C.P. Modeling the risk from Giardia and viruses in drinking water. J Am Water Works Assoc 1991: 83: 76–84.

    Article  CAS  Google Scholar 

  • Rodriguez A., Westbo S., Adam B., Langkop C., and Francis B.J. Outbreak of aseptic meningitis — Whiteside County, Illinois, 1995. MMWR 1997: 46: 221–224.

    Google Scholar 

  • Rumke H.C., Oostvogel P.M., van Steenis G., and van Loon A.M. Poliomyelitis in the Netherlands: a review of population immunity and exposure between the epidemics in 1978 and 1992. Epidemiol Infect 1995: 115: 289–298.

    Article  CAS  Google Scholar 

  • Sobsey M., Battigelli D.A., Handzel T.R., and Schwab K.J. Male-specific Coliphages as Indicators of Viral Contamination of Drinking Water. AWWA and AWWA Research Foundation; Denver, CO, 1995.

    Google Scholar 

  • Soller J.A., Olivieri A., Crook J., Cooper R., Parkin R., Spear R., and Tchobanoglous G. Characterizing the public health benefit of incremental wastewater treatment via microbial risk assessment. Env Sci Technol 2003a (under review).

  • Soller J.A., Olivieri A., Eisenberg J., Tchobanoglous G., and Cooper R. A public health evaluation of recreational water impairment: part II: risk characterization and data interpretation. Water Environ Res 2003b (in press).

  • Tani N., Dohi Y., Kurumatani N., and Yonemasu K. Seasonal distribution of adenoviruses, enteroviruses and reoviruses in urban river water. Microbiol Immunol 1995: 39: 577–580.

    Article  CAS  Google Scholar 

  • Taylor A., Craun G.F., Faich G.A., McCabe L.J., and Gangarosa E.J. Outbreaks of waterborne disease in the United States, 1961–1970. J Infect Dis 1972: 125: 329–331.

    Article  Google Scholar 

  • Van der Avoort H.G.A.M., Reimerink J.H.J., Ras A., Mulders M.N., and van Loon A.M. Isolation of epidemic poliovirus from sewage during the 1992–3 type 3 outbreak in the Netherlands. Epidemiol Infect 1995: 114: 481–491.

    Article  CAS  Google Scholar 

  • World Health Organization. Health based monitoring of recreational waters: the feasibility of a new approach (The ‘Annapolis Protocol’), WHO/SDE/WSH/99.1. WHO, Geneva, 1999.

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Acknowledgements

Funding for this investigation was provided by the City of Stockton, Municipal Utilities Department. We thank Mr. Don Dodge and Mr. Morris Allen for their support of this investigation and Mr. Robert Hultquist, Dr. Steven Book, and Mr. Carl Lischeske of the California Department of Health Services for their constructive input and review. We also acknowledge Lisa Ragain, Martha Embrey, and Bridget Ambrose for their technical assistance in preparing this publication.

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Correspondence to Rebecca T Parkin.

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Parkin, R., Soller, J. & Olivieri, A. Incorporating susceptible subpopulations in microbial risk assessment: pediatric exposures to enteroviruses in river water. J Expo Sci Environ Epidemiol 13, 161–168 (2003). https://doi.org/10.1038/sj.jea.7500265

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