Case Study 4: Recreational Waters

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QMRA of Recreational Waters

Team Members: Espinosa-Garcia, A.C., Suzuki, E., Rivera, I., Pogreba-Brown, K., Verhougstraete, M.P., Magri, M.E.


The Problem

It is known that exposure to poor water quality at recreational beaches can result in acute human illnesses. Epidemiological studies performed since the 1950’s, mainly in the United States, provided vital information for recreational water quality criteria development. Stevenson (1953) first described that illness incidences occurred more frequently in swimmers than in non-swimmers using fecal coliforms as indicators.

Between 1997 and 2006, 100 outbreaks and 3,021 cases of illness (e.g. gastrointestinal, skin irritation, respiratory/ear/eye infection) were associated with ambient recreational waters of the United States (Barwick et al. 2000; Lee et al. 2002; Dziuban et al. 2006; Yoder et al., 2008). Fleisher et al. (1998) suggested a significant underreporting of illness associated with contaminated recreational water with a maximum reporting rate of 22.2%.

Reviews of the multiple recreational epidemiological studies by Prüss (1998), Wade et al. (2003), Zmirou et al. (2003), and Wade et al. (2006) found strongest correlations between the GI illness and predictors (enterococci and E. coli) which supported the EPA’s total body contact criteria (USEPA 2009) below which no illness could be observed. Similar results between fecal streptococci and adverse health effects (i.e. diarrhea, vomiting, etc.) were observed by Kay et al. (1994) following an epidemiological study undertaken at four sites around Kingdom coast.

Additional epidemiological studies identified children were at an increased risk of illness compared to adult swimmers due to less developed immune systems (Parkins et al. 2003; White and Fenner 1994).

This study aimed to address the importance of using regional epidemiological studies and dose-response models to develop recreational water quality criteria. Specifically, the objectives of this study were 1) define the dose-response parameters for Brazil based on a local epidemiological study; 2) compare gastrointestinal illness risk using Brazilian and World Health Organization (WHO) dose-response models based on enterococci at human impacted beaches in three distinct countries.

The study areas comprised beaches from the countries: United States, Brazil and Venezuela.

The single USA beach included in this study was Newport Beach, California, USA. In Brazil five beaches in São Paulo State were selected for the study: Bertioga, Pitangueiras, Astúrias, Aparecida, and Ocian. For Venezuela eight beaches were selected: Morrocoy National park, Varadero, Mayorquina, Sombrero, Sal, Muerto, Ninos and Sur. The main pollution sources for USA, Brazil and Venezuela are storm water runoff, partially treated sewage, and uncontrolled wastewater discharges, respectively.

Surface water quality is subject to frequent, dramatic changes in microbial composition due to many anthropogenic activities: discharge of raw sewage, treated effluents, storm water runoff and/or other non-point sources.

Bathing water quality is assessed according to concentrations of indicator bacteria. The use of bacteria as indicators of the sanitary quality of water dates back to 1880 (WHO, 2001). In 1979, 1980 and 1982: Enterococci, E. coli and fecal coliforms were used as indicators and classified the beaches in categories A and B. In 1986, the criteria document includes EPA recommendations to use enterococci for marine and fresh recreational waters (a GM of 33 enterococci cfu per 100 mL in fresh water and 35 enterococci cfu per 100 mL in marine water) and E. coli for fresh recreational waters (a GM of 126 E. coli cfu per 100 mL) (EPA, 1986).A direct linear relationship was observed between highly credible gastrointestinal illness and bacterial densities of two indicators of fecal contamination, enterococci and E. coli (EPA, 1986). Enterococci has been suggested as a more protective estimation of water quality compared to E. coli (Kinzelman et al. 2003).

Enterococci are part of the normal intestinal flora of humans and animals but are also important pathogens responsible for serious infections. The genus Enterococcus includes more than 17 species, but only a few cause clinical infections in humans. With increasing antibiotic resistance, enterococci are recognized as feared nosocomial pathogens that can be challenging to treat. Only a few species of Enterococci are pathogens, but they are excreted in feces and are commonly used as indicators for fecal contamination of water bodies.

Enterococci are typically more human-specific than the larger fecal streptococcus group. All faecal streptococci at pH 9.6, 10° and 45°C and in 6.5% NaCl. Nearly all are members of the genus Enterococcus, and also fulfil the following criteria: resistance to 60°C for 30 min and ability to reduce 0.1% methylene blue.

Infectious or disease associated with recreational waters contact fall into two categories:

1. Gastroenteritis resulting from unintentional ingestion of water contaminated with fecal wastes. Enteric microorganisms that have been shown to cause gastroenteritis from recreational waters contact include: Giardia, Cryptosporidium, Shigella, Salmonella, E.coli O157:H7, Hepatitis A, Coxsackie A and B, and Norwalk virus.

2. Infections or disease associated mainly with microorganisms that are indigenous to the environment, which include: Pseudomonas aeruginosa, Staphylococcus sp., Legionella sp., Naegleria fowleri, Mycobacterium sp., and Vibrio sp. (dermatites, otitis externa, pontiac fever, granulomas, primary ameba meningoencephalitis (PAM) and conjunctivitis (APHA, 1998).

For the exposure assessment several steps were done for collecting and processing data. At first data for Enterococcus spp. were collected from water quality monitoring programs from the three study areas, followed by conducting the distribution fitting. MatLab was used to fit the data to a distribution (MLE). As a last step the exposure routes were studied and determined.

The distribution fitting output summaries are provided in Table 1.

Table 1. Distribution and descriptive statistics of Enterococci at the three study areas (Enterococci parameters are described as CFU/100 ml).

United States Venezuela Brazil
Distribution lognormal lognormal lognormal
Log Likelihood -4498.55 -193.509 -528.838
Mean 13.0449 113.428 114.044
Variance 793.704 65279.7 154509
mu(std. error) 1.70131(0.0361775) 3.82918(0.22703) 3.45876(0.16067)
sigma(std. error) 1.31688(0.0255958) 1.34313(0.164089) 1.59864(0.114481)

The primary exposure route for enterococci at the beach is water ingestion. Other routes of exposure can be cited as aerosol ingestion or contact with sand, with contamination of hands and subsequent oral contamination, or direct ingestion of sand. For the purpose of this study direct water ingestion was considered.

The primary transmission route of enterococci is the fecal-oral route. The water ingestion rates of bathers, both children and non-children, was estimated for 10 minute exposures with a minimum of 3 head exposures, similar to WHO guidelines. Ingestion volumes were extrapolated from Dufour et al. (2006) for a 10 minute swim and determined to be 8.2 ml and 3.6 ml for children and non-children, respectively. We applied a maximum conservative approach and used the maximum ingestion volume for all bathers (i.e. adults and children ingested 8,2 ml of water during each swim exposure). The bacterial ingestion for each study area is shown in table 2.

Table 2. Exposure and dose information for each study area.

Study area 10 minute ingestion volume Concentration of enterococci/1ml Enterococci Ingestion CFUs/10minute
Brazil 8.22 Mean:1.14 Mean:9.38
United States 8.22 Mean:0.13 Mean:1.07
Venezuela 8.22 Mean:1.13 Mean:9.32

Dose-Response Model 1 - World Health Organization

The first Dose-Response model was based in data utilized by the World Health Organization for recreational waters. Data was obtained from Kay et al. (1994). Based on that data a dose-response model was done, fitting data in exponential equation.


P = a + [(1 - a)(1 - exp^(-c*k)]

Figure 1 presents the dose-response model with the Enterococci(CFU) verses cases of GI illness for model 1.


Dose-Response Model 2 – Brazil Beach Case-Control Study

In January and February in 1999, CETESB (São Paulo State Environmental Company - Companhia Estadual de Meio Ambiente de São Paulo) conducted a simultaneous case-control study and environmental survey of 5 separate beaches in the São Paulo coastal area. For five weeks in the high season families were interviewed on the beach to determine their exposure to water and other possible sources of exposure to pathogens (sand, food prepared at the beach, etc).

Basic epidemiologic analyses found that risk was variable for adults verses children (defined here as under 19 to match existing study) and among children, contact with sand increased the risk compared to those who did not contact the sand.

Based on that data a dose-response model was done, fitting data in either exponential and beta-poisson equations. The best fitting was given by beta-poisson equation.

Beta-Poisson equation

P = a + (1-a)*(1 - [1 + c/N50)*(2^(1/alpha)-1)]^-alpha

Figure 2 presents the dose-response model with the Enterococci(CFU) verses cases of GI illness for model 2.


The probabilities of GI illness were calculated using the indicator Enterococci dose-response relationships modeled from the literature data (Kay et al., 1994) and from an epidemiological study conducted in 1999 by the São Paulo State Environmental Company (CETESB) in Brazil, as described in the dose-response item. As following step Monte Carlo simulations were conducted with data from the three study areas.

The input parameters for running the Monte-Carlo simulations are described in table 3.

Parameters Brazil United States Venezuela
Dose-response model 1 - WHO data
concentration (CFU/100mL) 114.04 13.04 113.43
dose (CFU) 9.38 1.07 9.33
k (mean; 5%; 95%) 0.0025 (0,0028; 0,0017; 0,0042) 0.0025 (0,0028; 0,0017; 0,0042) 0.0025 (0,0028; 0,0017; 0,0042)
Dose-response model 2 - Brazil beach case-control study
concentration (CFU/100mL) 114.04 13.04 113.43
dose (CFU) 9.38 1.07 9.33
N50 (min; max) 494.15 (404,45; 10138,53) 494.15 (404,45; 10138,53) 494.15 (404,45; 10138,53)
alpha (min; max) 26428.04 (0,14; 26419,79) 26428.04 (0,14; 26419,79) 26428.04 (0,14; 26419,79)

The results from the simulation are presented in figures 3, 4, 5, 6, 7 and 8.

Figure 3 presents the quantitative model for Brazil with the dose-response model 1 - WHO. Fig 3.jpg Median: 0.09; 90th percentile: 0.54

Figure 4 presents the quantitative model for Brazil with the dose-response model 2. Fig 4.jpg Median: 0.04; 90th percentile: 0.28

Figure 5 presents the quantitative model for the US with the dose-response model 1 - WHO. Fig 5.jpg Median: 0.12; 90th percentile: 0.15

Figure 6 presents the quantitative model for the US with the dose-response model 2. Fig 6.jpg Median: 0.01; 90th percentile: 0.04

Figure 7 presents the quantitative model for Venezuela with the dose-response model 1 - WHO. Fig 7.jpg Median: 0.13; 90th percentile: 0.57

Figure 8 presents the quantitative model for Venezuela with the dose-response model 2. Fig 8.jpg Median: 0.06; 90th percentile: 0.29

Some questions are important and can be highlighted for risk management:

WHO dose-response model should be preferred since its results were more conservative according to this study case.

Understand and accept that recreational water cannot be treated as drinking water or disinfected as a biosolid. The only way to preserve it is implementing programs for water pollution control.

Control of the main pollution sources: local untreated wastewater, solid waste, urban drainage.

Education is the key for residents and authorities (stakeholders): in order to maintain their health as to maintain the tourist business.

Establish protocols to control pollution events and to reduce users exposure.

Stakeholders committee sensitized with a vision of sustainability.

Regulation and surveillance to compliance (e.g. Plan to monitoring water quality and data analysis, regular training of operators);

City planning (think about the future from a sustainability perspective).

Educational incentives to local communities.

The Problem

Barwick, R.S., Levy, D.A., Craun, G.F., Beach, M.J., and Calderon, R.L. (2000). Surveillance for waterborne-disease outbreaks, United States, 1997-1998. Morbidity and Mortality Weekly Report (MMWR), CDC Surveillance Summaries. 49; 1-35. Centers for Disease Control and Prevention (CDC), Atlanta, Georgia.

Dziuban, E.J., Liang, J.L., Craun, G.F., Hill, V., Yu, P.A. , Painter, J., Moore, M.R., Calderon, R.L., Roy, S.L. and Beach, M.J. (2006). Surveillance for waterborne disease and outbreaks associated with recreational water - United States, 2003-2004. Morbidity and Mortality Weekly Report (MMWR), CDC Surveillance Summaries. 55(SS12); 1-24. Centers for Disease Control and Prevention (CDC), Atlanta, Georgia.

Fleisher J.M., Kay D., Wyer, M.D., and Godfree, A.F. (1998). Estimates of the severity of illnesses associated with bathing in marine waters contaminated with domestic sewage. International Journal of Epidemiology, 27, 722-726.

Kay, D., J.M Fleisher, A.F Godfree, F Jones, R.L Salmon, R Shore, M.D Wyer, R Zelenauch-Jacquotte. (1994) Predicting likelihood of gastroenteritis from sea bathingresults from randomised exposure.Lancet, 344, pp. 905–909.

Lee, S.H., Levy, D.A., Craun, G.F., Beach, M.J., and Calderon, R.L. (2002). Surveillance of waterborne-disease outbreaks, United States, 1999-2000. CDC. Retrieved from (

Parkins, R.T., Soller, J.A., and Olivieri, A.W. (2003). Incorporating susceptible subpopulations in microbial risk assessment: Pediatric exposures to enteroviruses in river water. Journal of Exposure Analysis and Environmental Epidemiology, 13, 161-168.

Prüss, A. (1998). Review of epidemiological studies on health effects from exposure to recreational water. International Journal of Epidemiology, 27, 1-9.

Stevenson, A.H. (1953). Studies of bathing water quality and health. Journal of American Public Health Association, 43, 529-538.

United States Environmental Protection Agency (USEPA), O. of W. (1986). Ambient water quality criteria for bacteria - 1986, (EPA440/5-8).

United States Environmental Protection Agency (USEPA). (2009). Review of published studies to characterize relative risks from different sources of fecal. (EPA 822-R-09-001).

Wade, T.J., Calderon, R.L., Sams, E., Beach, M., Brenner, K.P., Williams, A.H., and Dufour, A.P. (2006). Rapidly measured indicators of recreational water quality are predictive of swimming-associated gastrointestinal illness. Environmental Health Perspectives, 114, 24-28.

Wade, T.J., Pai, N., Eisenberg, J.N.S., and Colford J.M. (2003). Do US EPA water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis. Environmental Health Perspectives, 111, 1102-1109.

White, D.O. and Fenner, F.J. (1994). Medical Virology, 4th edition. New York, NY, USA: Academic Press.

Yoder, J.S., Hlavsa, M.C., Craun, G.F., Hill, V., Roberts, V., Yu, P.A., Hicks, L.A., Alexander, N.T., Calderon, R.L., Roy, S.L., and Beach, M.J. (2008). Surveillance for waterborne disease and outbreaks associated with recreational water use and other aquatic facility-associated health events - United States, 2005-2006. Morbidity and Mortality Weekly Report (MMWR), CDC Surveillance Summaries 57 (SS09); 1-29. Centers for Disease Control and Prevention (CDC), Atlanta, Georgia.

Zmirou, D., Pena, L., Ledrans, M., and Letertre, A. (2003). Risks associated with the microbiological quality of bodies of fresh and marine water used for recreational purposes: Summary estimates based on published epidemiological studies. Archives of Environmental Health, 53, 703-711.

Hazard ID

American Public Health Organization. Recreational waters. IN: APHA. Standard Methods for the examination of water and wastewater. 20th Ed., Washington, D.C.: APHA, AWWA, WEF, 1998.

Kinzelman, J., Ng, C., Jackson, E., Gradus, S., and Bagley, R. (2003). Enterococci as indicators of Lakes Michigan recreational water quality: Comparison of two methodologies and their impacts on public health regulatory events. Applied and Environmental Microbiology, 69, 92-96.

United States Environmental Protection Agency (USEPA), O. of W. (1986). Ambient water quality criteria for bacteria - 1986, (EPA440/5-8).

World Health Organization (WHO). 2001. Water quality: Guidelines, Standards and Health. Fewtrell, L and Bartram, J. IWA Publishing, London, U.K. ISBN: 1 900222 28 0.

Exposure Assessment

Dufour, A.P., Evans, O., Behymer, T., Cantu, R., 2006. Water ingestion during swimming activities in a pool: a pilot study. J. Water Health 4 (4), 425-430.