Do U.S. Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis. (Research Review).

Despite numerous studies, uncertainty remains about how water quality indicators can best be used in the regulation of recreational water. We conducted a systematic review of this topic with the goal of quantifying the association between microbial indicators of recreational water quality and gastrointestinal (GI) illness. A secondary goal was to evaluate the potential for GI illness below current guidelines. We screened 976 potentially relevant studies and from these identified 27 studies. From the latter, we determined summary relative risks for GI illness in relation to water quality indicator density. Our results support the use of enterococci in marine water at U.S. Environmental Protection Agency guideline levels. In fresh water, Escherichia coli was a more consistent predictor of GI illness than are enterococci and other bacterial indicators. A log (base 10) unit increase in enterococci was associated with a 1.34 [95% confidence intervals (CI), 1.00-1.75] increase in relative risk in marine waters, and a log (base 10) unit increase in E. coli was associated with a 2.12 (95% CI, 0.925-4.85) increase in relative risk in fresh water. Indicators of viral contamination were strong predictors of GI illness in both fresh and marine environments. Significant heterogeneity was noted among the studies. In our analysis of heterogeneity, studies that used a nonswimming control group, studies that focused on children, and studies of athletic or other recreational events found elevated relative risks. Future studies should focus on the ability of new, more rapid and specific microbial methods to predict health effects, and estimating the risks of recreational water exposure among susceptible persons. Key words: bathing water, diarrhea, gastrointestinal illness, indicator organisms, meta-analysis, swimming, systematic review, water quality. Environ Health Perspect 111:1102-1109 (2003). doi:10.1289/ehp.6241 available via http://dx.doi.org/[Online 14 April 2003]

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Since the 1950s, numerous studies have examined the association between recreational water quality and health outcomes. Many of these studies have reported an increased risk of illness associated with exposure to recreational water. Several have related the level of contamination in the water, as measured by indicators of water quality, with the magnitude of risk. Despite extensive research on this topic, uncertainty remains about how water quality indicators can best be used in the regulation of recreational water environments. In 1986, the U.S. Environmental Protection Agency (U.S. EPA 1986) published recommended water quality criteria for recreational waters, which proposed the use of enterococci in marine water and enterococci and/or Escherichia coli in fresh water as indicator organisms. That report recommended regulatory levels based on geometric means of at least five samples over a 30-day period of 35 colony-forming units (cfu)/100 mL and 33 cfu/100 mL for enterococci in marine and fresh water, respectively; and 126 cfu/100 mL for E. coli in fresh water (U.S. EPA 1986). Fecal coliforms, which had been previously proposed for use as an indicator, were no longer recommended. The studies upon which these revised guidelines were based (Cabelli 1983; Dufour 1984a) have been criticized (Fleisher 1992), and the draft revised World Health Organization (2001) guidelines have been developed using more recent controlled studies (Kay et al. 1994).

Few attempts have been made to summarize and evaluate the existing literature in a systematic and quantitative framework. Pruss (1998) concluded that the literature strongly suggests a dose-response relationship between fecal contamination and the risk of gastrointestinal (GI) illness but did not examine the relationship between specific water quality indicators and health outcomes.

Our primary goal in this systematic review was to evaluate the evidence linking specific microbial indicators of recreational water quality to specific health outcomes under nonoutbreak conditions. Secondary goals were to identify and describe critical study design issues, to quantify and evaluate sources of heterogeneity among the studies, and to evaluate the potential for health effects at or below the current suggested regulatory standards.

Methods

Literature search. Our literature search included several computerized databases: MEDLINE (http://www.ncbi.nlm.nih.gov/ entrez/query.fcgi?db=PubMed), BIOSIS (www.biosis.org), OLDMEDLINE (http:// gateway.nlm.nih.gov/gw/Cmd), and EMBASE (http://openaccess.dialog.com/med/) for the period from 1950 to the present. We searched dissertations using the UMI/ProQuest Digital Dissertation Database (http://wwwlib.umi.com/ dissertations/gateway). The search terms included key words "recreational water and health" and subject heading searches for "environmental pollutants, adverse effects" or "water pollution, adverse effects." We consulted experts in the field and reviewed the bibliographies of relevant studies for additional references. We reviewed the tides and abstracts of all studies in the searches for relevance, and we flagged potentially relevant studies for further full text review.

We retrieved and reviewed manuscripts for studies whose abstracts appeared to examine health effects in relation to swimming and microbiologic water quality. We also obtained studies that were not in English, provided the abstract was available in English. Conference proceedings, doctoral dissertations, reports, and other unpublished studies when identified were also obtained.

Selection criteria. Studies were included in the review based on the following criteria:

Water exposure. Studies that measured exposure to marine (ocean) or fresh water (lakes, rivers, ponds) were included. Studies of exposure to chlorinated water sources were excluded.

Water quality measures. At least one measure of microbial water quality had to be reported by the authors. Studies that reported water quality but did not relate these measures to human health were excluded.

Health outcomes. Studies had to report at least one measure of health that could potentially be associated with water quality. Studies that only examined infection (i.e., as measured by serology) and examined only typhoid and/or polio were excluded. Although we abstracted data for all types of health outcomes, in this analysis we focused on GI illness because it has been the most extensively studied and because it is the outcome for which current recreational water quality guidelines have been developed.

Study design. We focused on epidemiologic studies that quantified the relationship between water quality indicators and GI illness under endemic, or nonoutbreak, conditions. Risk assessments, case series, case reports, and descriptions of outbreaks were excluded because such studies do not provide evidence of quantitative associations between specific indicators and health outcomes under endemic conditions.

Data abstraction. Two authors (T.J.W. and N.P.) independently abstracted data from all identified studies and conferred to resolve uncertainties. For each study, the following information was abstracted: water quality measure and level, water type (marine, fresh), how water quality was measured in relation to exposure (i.e., same day, at the time of swimming, or over the entire study period), population studied, geographic location, study size, study design, symptom measured, covariates measured, how swimming exposure and outcome were measured, relative risks, and confidence bounds. Correlation coefficients, regression coefficients, p-values, and 95% confidence bounds were also abstracted. When relative risks were not reported, data were abstracted to calculate the relative risk (defined as the ratio of the proportion ill in the exposed to the proportion ill in the unexposed) and its 95% confidence interval (CI). When a p-value was provided rather than a CI, the CI was calculated using published formulas (Greenland 1998). When multiple symptoms were reported, we selected the results based on the following guidelines: a multisymptom definition (e.g., diarrhea occurring with either fever or vomiting), if presented, was preferentially chosen; if only specific symptoms were presented, results associated with "diarrhea" were selected.

Data analysis. We conducted separate analyses for each combination of water quality indicator, health outcome, and water type (fresh vs. marine). When studies reported results within a range of indicator values, we recorded the median value of the reported range as the exposure value. We formed exposure categories based on quartiles, tertiles, or the 50th percentile of the exposure values, depending on the number of estimates available. When a single study reported more than one effect estimate within each of our defined exposure categories, we selected the results associated with the highest exposure measure within each exposure category. For example, if our lowest category included indicator values within a range of 1-20, and a single study reported effect estimates for both the 1-10 and 11-20 range, we selected the effect estimates associated with the 11-20 range. We did this so that a single study would not have greater influence on a single summary relative risk simply because it reported more effect estimates within a smaller range. To evaluate the U.S. EPA guideline values, exposure categories were developed for risk estimates above and below these levels.

We calculated summary relative risks as a weighted average using a random-effects model (DerSimonian and Laird 1986). We included adjusted relative risks whenever available. Heterogeneity was assessed for each exposure category using the Q statistic (DerSimonian and Laird 1986).

To evaluate the continuous relationship between the measured water quality indicators and the effect estimates, we conducted a weighted regression for each water quality indicator wherein the indicator level (log base 10) was modeled as a continuous predictor of the natural log of the relative risk. To account for study size, the models were weighted by the inverse of the standard error of the natural log of the relative risk. Because there were few effect estimates available for nonfecal and viral indicators of water quality, we conducted this regression analysis only for the bacterial fecal water quality measures.

To investigate sources of variability among the studies, we used a random-effects meta-regression model (Thompson and Sharp 1999). The dependent variable was the natural log of the relative risk for GI illness. Independent variables included in the initial model were water type, geographic location (United States, United Kingdom, other European countries, Asia, Africa, Australia), control group (swimmers or nonswimmers), swimming definition (required head immersion or did not require), adjustment for covariates, age of study population, method of exposure measurement (self-report, direct observation, or event participation), length of follow-up period, and study location. The water quality indicator density was included in all models. The final model was selected by excluding covariates with p-values > 0.2.

All analyses were conducted in Stata 7.0 for Windows (Stata Corporation 2002).

Results

We reviewed 976 abstracts or titles for relevance. Fifty-five of the 976 appeared relevant and were selected for further review. Of these, 27 (Table 1) were included in the final review. Of the 28 excluded studies, eight (Balarajan et al. 1991; Calderon and Mood 1981; Fewtrell et al. 1994; Harrington et al. 1993; Jessop et al. 1985; New Jersey Department of Health 1989; Seyfried et al. 1985a; van Asperen et al. 1995) were excluded because the data analysis and reporting were deemed insufficient, 11 were duplicated in other articles or reports (Bandaranayake et al. 1995; Cabelli et al. 1975, 1979, 1982; Dufour 1984b; Jones et al. 1991; Ktsanes et al. 1981; Public Health Laboratory Service 1959; Pike 1990, 1991; Zmirou et al. 1990), five reported outcomes that were not of immediate interest (typhoid, polio, serologic results, or public health impact) (D'Alessio et al. 1981; El-Sharkawi and Hassan 1979; Fleisher et al. 1998; Philipp et al. 1989; Taylor et al. 1995); one examined a water quality measure not reported in any other study (cyanobacteria) (Pilotto et al. 1997); and three did not measure GI illness (Calderon and Mood 1982; Charoenca and Fujioka 1995; Fleisher et al. 1996).

Study methodologies and key characteristics. The sample size of the 27 studies ranged from 247 to 26,686 subjects. Seventeen studies took place in marine water, and 10 in fresh water (Table 1).

Study design. We identified four study designs: traditional prospective studies, prospective studies during recreational events, randomized controlled trails, and cross-sectional studies.

Eighteen of the studies included were traditional prospective studies (Table 1). In these studies, beach-goers were recruited and questioned about their swimming and exposure to water. They were contacted again 3 days to 1 month later and asked about health symptoms they experienced during this period. Water samples were collected periodically, usually at least once each interview day. Subjects were classified as swimmers and nonswimmers, and rates of illnesses in these two groups were compared.

Five of the selected studies were prospective studies of athletic or organized recreational events (Table 1). In these studies, event participants were recruited. The unexposed group consisted of bystanders, event organizers, or participants in a related event that did not involve swimming. Subjects were contacted after the event and asked about the occurrence of illness. Water quality was measured during the event.

A series of randomized trials were conducted in the United Kingdom in the 1990s (Fleisher et al. 1993, 1996; Kay et al. 1994). In these trials, subjects were randomly assigned by investigators to be swimmers or nonswimmers. Investigators observed swimmers who were asked to swim in a prescribed fashion. Water quality was measured at or near the time of swimming.

One cross-sectional study was identified (Foulon et al. 1983). In this study, subjects were questioned about their recent illnesses at the same time as they were questioned about their swimming in the past 4 days.

Exposure assessment. Most studies determined swimming exposure through self-report or through proxy self-report. Three studies reported having directly observed swimming behavior (Fleisher et al. 1993; Haile et al. 1999; Kay et al. 1994) and five determined exposure through participation in an event (Fewtrell et al. 1992; Lee et al. 1997; Medema et al. 1995; Philipp et al. 1985; van Asperen et al. 1998).

Definition of the unexposed group. Studies varied in the way they defined the comparison (unexposed) group. Some studies used nonswimmers for comparison, whereas others used swimmers in relatively better water (as measured by water quality indicators). Other studies included results from both types of comparison groups.

Water quality measures. Water quality measures were determined in one of three ways: a) on the day of exposure (Alexander et al. 1992; Cabelli 1983; Calderon et al. 1991; Cheung et al. 1990; Corbett et al. 1993; Dufour 1984a; Fattal et al. 1986; Fewtrell et al. 1992; Haile et al. 1999; Kueh et al. 1995; Lee et al. 1997; Lightfoot 1989; Marino et al. 1995; McBride et al. 1998; Medema et al. 1995; Philipp et al. 1985; Prieto et al. 2001; Seyfried et al. 1985b; von Schimding et al. 1992); b) at the time of swimming (Fleisher et al. 1993; Kay et al. 1994; van Asperen et al. 1998); or c) aggregated over several days, weeks, or months (Ferley et al. 1989; Foulon et al. 1983; Pike 1994; Stevenson 1953). Although exposure was measured on each interview day for most studies, often it was aggregated in the analyses. This was particularly true for studies that compared illness rates between two or more beaches that differed in overall water quality over the entire study period.

Definition of swimming. The most common definition of swimming required submersion of the head in the water (Cabelli 1983; Calderon et al. 1991; Cheung et al. 1990; Corbett et al. 1993; Dufour 1984a; Fattal et al. 1986; Fleisher et al. 1993; Haile et al. 1999; Kay et al. 1994). Few studies measured duration and intensity of exposure. Those that did found that a higher risk of GI illness was associated with longer or more intense exposure (Corbett et al. 1993; Prieto et al. 2001) or with an increase in the number of times water was swallowed (Lee et al. 1997). More uniform exposure may be more likely in both controlled trials (Fleisher et al. 1993; Kay et al. 1994), where swimming exposure is prescribed and then observed by researchers, and studies of athletic events.

Quantitative relationships between indicators and GI illness: marine water. Bacterial indicators of fecal contamination. Bacterial indicators of fecal contamination considered were enterococci/fecal streptococci, E. coli, fecal coliform, and total coliform (Tables 2 and 3). Although there was some trend toward increasing relative risk for all of the indicators, overall, the strongest trend was associated with enterococci. In the categorical analysis, the relative risk did not continue to increase in studies with densities greater than 104 cfu/100 mL, indicating a potential threshold for risk of GI illness. The relative risk of GI illness, although statistically elevated in all categories of E. coli, was greatest in the highest E. coli category (320-5,207 cfu/100 mL). A consistent increase in the relative risk was also observed for total coliform. Risk of GI illness was statistically elevated in the highest (598-2,000 cfu/100 mL) and lowest (2-65 cfu/100 mL) fecal coliform category, but only one of the four studies reported a significant correlation (Pike 1994).

Results from the weighted regression (Table 3) confirm an association between enterococci density and the natural log relative risk. The relative risk for GI illness increased 1.3 times for every log 10 increase in enterococci density. The relationship between enterococci and the log relative risk is also illustrated graphically in Figure 1. Significant associations were not identified with the other indicators, although positive associations between E. coli and total coliform were also observed.

[FIGURE 1 OMITTED]

Indicators of viral contamination. Two direct indicators of viral contamination in marine waters, enterovirus (or culturable enteric viruses), and bacteriophage were studied. Pike (1994) noted a strong correlation between enterovirus and GI illness (r = 0.84, p < 0.05). Because few studies (Alexander et al. 1992; Haile et al. 1999; Pike 1994) evaluated enterovirus, the results were collapsed into a single exposure category [range, 0.53-4.7 plaque-forming units (pfu)/10 L]. Enterovirus was a strong indicator for GI illness, producing a summary relative risk of GI illness of 2.15 (1.45-3.17)

Only two studies examined bacteriophage and GI illness in marine waters, and one study (von Schirnding et al. 1992) did not find sufficient numbers to conduct an analysis. The most detailed analysis in marine water was the studies conducted by Pike (1994). In this study, no significant correlations were reported.

Nonfecal indicators of water quality. Nonfecal indicators of water quality included Staphylococcus species, Pseudomonas sp., and Aeromonas sp. Two studies (Cabelli 1983; Kueh et al. 1995) found significant relationships between Aeromonas levels and GI illness, although Cabelli (1983) did not note a trend. Pseudomonas sp. and Staphlyococcus sp. were not associated with GI illness (Table 2).

Quantitative relationships between indicators and G1 illness: fresh water. Bacterial indicators of fecal contamination (Tables 3 and 4). E. coli was the only indicator clearly associated with an increase in the relative risk of illness in both the categorical analysis (Table 4) and the weighted regression (Table 3, Figure 2). No increase in relative risk was observed for high levels of enterococci compared with low levels. Risk for GI illness was elevated for both categories of fecal coliform, but no statistically significant correlations were observed. Illness was significantly elevated in the highest total coliform exposure category, but this was based on only one study (Ferley et al. 1989). In the weighted regression analysis, only E. coli was correlated with an increase in the relative risk (Table 3).

[FIGURE 2 OMITTED]

Indicators of viral contamination. Enterovirus was significantly associated with GI illness at both exposure levels. The summary relative risk was considerably elevated in the highest exposure category (relative risk = 4.11, 95% CI, 2.59-6.54), although one study (Lee et al. 1997) reported no correlation. GI illness was also elevated in both bacteriophage exposure categories.

Nonfecal indicators of water quality. Although elevated relative risks were observed in both categories of Staphylococcus sp., there appeared to be no trend with increasing levels. Contradictory results were observed for Pseudomonas sp.: Ferley et al. (1989) observed a strong negative correlation of borderline statistical significance, whereas Lightfoot (1989) observed a positive correlation. Ferley et al. (1989) likewise observed a negative correlation with Aeromonas sp., but the relative risk at the highest category from the same study was elevated. This contradiction likely resulted from the use of geometric means of samples collected over the course of the summer for the relative risk calculation. The correlation, however, was apparently based on individual exposure measures assigned to individual swimmers.

Evaluation of current standards. Marine water. Summary relative risks for GI illness below the U.S. EPA-suggested value (U.S. EPA 1986) for both enterococci and E. coli were lower (and were not statistically significant), whereas relative risks above the suggested values were elevated (and were statistically significant). In contrast, the summary relative risk point estimate for fecal coliform exposure decreased slightly in studies with exposures above the guideline values compared with studies with exposures below this value.

Fresh water. Relatively few studies reported indicator densities above the guideline values. Summary relative risks both above and below the enterococci exposure guideline value were elevated for those exposures both above and below the enterococci guideline value (Table 5). Studies below the guideline value for E. coli were not associated with increased illness, whereas exposures above the guideline level were. Exposures above the previously suggested guideline for fecal coliform were also elevated (and of borderline statistical significance) compared with those below this value.

Sources of heterogeneity. Several summary relative risks were found to exhibit potentially significant heterogeneity (see notes in Tables 2, 4, and 5). To evaluate possible sources of heterogeneity, an analysis was conducted among studies that examined associations between enterococci and GI illness (Table 6). Water source, adjustment for covariates, study design, length of follow-up period (< 1 week or [greater than or equal to] 1 week), swimming definition, and geographic location did not significantly contribute to the variation observed in relative risk, Factors that did significantly contribute to the variability in relative risk were selection of control group (nonswimmers vs. swimmers) and type of study population (athletic event participants vs. beach-goers). Summary relative risks for children (under 18) only were elevated compared with studies that included adults or both adults and children together.

Discussion

Epidemiologic studies of the health risks of recreational water have focused on identification of water quality indicators that can predict illness most effectively. An ideal water quality indicator would be simple to measure and would predict illness consistently and accurately in a variety of environments. Moreover, an increase in the concentration of the indicator measure should increase the risk of illness. Based on the epidemiologic studies conducted to date, it is evident that no single indicator can predict illness consistently in all environments at all times, perhaps because of the wide array of pathogens that have been associated with GI illness in recreational water environments as well as natural variability in pathogen-indicator associations. For example, both bacterial and viral indicators of water quality may correlate poorly with the occurrence of protozoan parasites such as Cryptosporidium parvum, a leading cause of freshwater outbreaks of GI illness (Barwick et al. 2000; Lee et al. 2002). Taken as a whole, however, the body of literature does support the use of enterococci and E. coli as useful predictors of GI illness in marine environments and supports the guideline levels developed by the U.S. EPA. Of the 12 studies in marine water that were above the U.S. EPA enterococci guideline value of 35 cfu/100 mL, eight found statistically significant relative risks of GI illness, and the lowest relative risk observed was 1.31 (Haile et al. 1999). Only two of nine studies with exposures below this level found statistically significant results, and several of these studies found relative risks near or below 1.00 (Fleisher et al. 1993; Foulon et al. 1983; Kay et al. 1994; McBride et al. 1998; Pike 1994). This review also supports the recommended move away from the use of fecal coliform (U.S. EPA 2002) as an indicator because there was no evidence that risk of GI illness increased at levels above the previously proposed guideline value. In fresh water, E. coli was superior to enterococci at predicting illness, and the E. coli guideline level was supported, because exposure below presented no significant risk, whereas exposures above were associated with an elevated and statistically significant increased risk of GI illness.

Among the nonfecal indicators of water quality, Staphylococcus sp. and Pseudomonas sp. are not supported as general predictors of GI illness, whereas the utility of Aeromonas sp. remains unclear. Indicators that measure water quality degradation associated with bather shedding such as Staphylococcus sp. could be useful in some situations, particularly when the body of water is small, there are many swimmers, and there is little water circulation. Staphylococci sp. have been shown to be associated with bather density in swimming pools (Favero et al. 1964), and in an epidemiologic study of a small pond (Calderon et al. 1991), Staphylococci sp. was associated with GI illness.

Our results indicate that indicators of viral contamination (enterovirus and bacteriophage) may be promising predictors of GI illness, although this is based on only a few studies. This observation is consistent with reports of norovirus (Norwalk-like viruses)-associated outbreaks in freshwater lakes and swimming pools (Baron et al. 1982; Barwick et al. 2000; Kappus et al. 1982; Lee et al. 2002; Levy et al. 1998). Noroviruses have also been identified in marine waters (Griffin et al. 2003). These viruses are a leading cause of both GI-related outbreaks (Fankhauser et al. 2002) and endemic GI illness (Mead et al. 1999). We found that enteroviruses, which have been suggested as specific indicators of human contamination (Scott et al. 2002), were strongly associated with GI illness. They may, however, be impractical for use as water quality indicators because they are not easily cultivated in environmental samples (Scott et al. 2002).

The analysis of the sources of heterogeneity among the studies provides some insight regarding the impact of study design features on the association between water quality and GI illness. Studies using nonswimming controls had significantly higher relative risks than studies using swimming controls (Table 6). If the risk associated with swimming is of interest, then the appropriate control group should consist of nonswimmers, because a swimming control group may underestimate the risk associated with entering and recreating in the water, resulting in regulatory levels that are too high.

Characteristics of the study population also impacted the relative risk. The elevated relative risk associated with studies of athletic events may be related to the more intense exposure participants in these events experience compared with the exposure of a more typical beach-goer. The finding that studies that focused only on children produced elevated relative risks indicates that children may be particularly susceptible to illness after recreational water exposure. Lower guideline levels may be warranted to adequately protect the health of children (and other susceptible individuals) and events resulting in prolonged exposure.

Suggested further research. No studies to date have specifically examined the impact of recreational water exposure on persons whose immune systems are compromised because of HIV infection or other conditions. Studies focusing on immunocompromised persons would ultimately provide valuable information towards developing enhanced water quality guidelines for susceptible individuals. Also, although studies of children have been conducted, their susceptibility needs to be better defined.

Research is needed to better understand the ability of rapid and specific microbial methods to predict illness. Standard membrane filtration methods for enterococci require 24-hr incubation (U.S. EPA 1997), making it impossible for recreational water managers to respond quickly to changes in water quality. The use of rapid microbial methods, such as real-time polymerase chain reaction (PCR), could help managers respond more quickly and effectively, but these methods have yet to be studied in conjunction with health effects. Microbial source tracking methods include both phenotypic (e.g., grouping based on antibiotic resistance patterns, or serotype) and genotypic methods (e.g., pulse field gel electrophoresis, PCR, ribotyping, and host-specific molecular markers) (Scott et al. 2002). These methods should be incorporated into future epidemiologic studies to assess the relative impact of human versus nonhuman contamination on illness.

An epidemiologic study that combines self-reported illness symptoms with serology tests for GI pathogens could help identify the specific pathogens responsible for any observed increase in illness. Stool specimens collected from symptomatic (and/or asymptomatic) subjects would also provide valuable pathogen specific information.

Limitations. As with any meta-analysis, the summary relative risks reported should be interpreted cautiously, particularly because significant heterogeneity was noted. As a result, we used a conservative random effects model, which takes into account both within- and between-study variability, to determine summary relative risk and their 95% confidence intervals.

Publication bias--the preferential publication of papers reporting an association--can be a problem with any systematic review or meta-analysis. Although we tried to minimize the potential for publication bias by obtaining unpublished reports and dissertations, it is possible that some unpublished studies were not available for this review. A statistical test (Begg and Madachhanda 1994) indicated a borderline significant rank correlation (p = 0.09) between the log relative risk and the sample variance, an indication of publication bias. As a result, it is possible that the summary relative risks reported here are overestimates, but the true effect of this bias is impossible to evaluate completely.

This review focuses only on GI illness, which, despite being the most extensively studied, may not necessarily be the most appropriate or sensitive health outcome on which recreational water quality guidelines should be based. We are also examining other health outcomes and their relationship to water quality, and plan to report these in future analyses.

Conclusions

Our review suggests that enterococci and, to a lesser extent, E. coli are adequate indicators of GI illness in marine water, but fecal coliforms are not. There was evidence that risk of GI illness was considerably lower in studies with indicator densities below the guidelines proposed by U.S. EPA for both enterococci and E. coli, providing support for use of these values for regulatory purposes. In fresh water, E. coli was a more reliable and consistent predictor of GI illness than is enterococci.

Table 1. Studies included in the review.

                                                   Water     Sample
Reference                          Location         type      size

Stevenson (1953)                USA                Fresh      5,124
Cabelli (1983)                  USA                Marine    26,686
Cabelli (1983)                  Egypt              Marine    23,080
Foulon et al. (1983)            France             Marine     4,921
Dufour (1984b)                  USA                Fresh     21,777
Philipp et al. (1985)           UK                 Marine       247
Seyfried et al. (1985b)         Canada             Fresh      3,967
Fattal et al. (1986)            Israel             Marine     2,231
Lightfoot (1989)                Canada             Fresh      9,296
Ferley et al. (1989)            France             Fresh      5,737
Cheung et al. (1990)            Hong Kong          Marine    18,741
Alexander et al. (1992)         UK                 Marine       703
Calderon et al. (1991)          USA                Fresh        144
von Schirnding et al. (1992)    South Africa       Marine       733
Fewtrell et al. (1992)          UK                 Fresh        516
Pike (1994)                     UK                 Marine    16,569
Corbett et al. (1993)           Australia          Marine     2,968
Fleisher et al. (1993)          UK                 Marine       509
Kay et al. (1994)               UK                 Marine     1,306
Medema et al. (1995)            The Netherlands    Fresh        395
Marino et al. (1995)            Spain              Marine     2,249
Kueh et al. (1995)              Hong Kong          Marine    18,122
Lee et al. (1997)               UK                 Fresh        473
McBride et al. (1998)           New Zealand        Marine     3,887
van Asperen et al. (1998)       The Netherlands    Fresh      1,600
Haile et al. (1999)             USA                Marine    11,686
Prieto et al. (2001)            Spain              Marine     1,858

Reference                         Study type

Stevenson (1953)                Cohort
Cabelli (1983)                  Cohort
Cabelli (1983)                  Cohort
Foulon et al. (1983)            Cross-sectional
Dufour (1984b)                  Cohort
Philipp et al. (1985)           Event
Seyfried et al. (1985b)         Cohort
Fattal et al. (1986)            Cohort
Lightfoot (1989)                Cohort
Ferley et al. (1989)            Cohort
Cheung et al. (1990)            Cohort
Alexander et al. (1992)         Cohort
Calderon et al. (1991)          Cohort
von Schirnding et al. (1992)    Cohort
Fewtrell et al. (1992)          Event
Pike (1994)                     Cohort
Corbett et al. (1993)           Cohort
Fleisher et al. (1993)          Randomized trial
Kay et al. (1994)               Randomized trial
Medema et al. (1995)            Event
Marino et al. (1995)            Cohort
Kueh et al. (1995)              Cohort
Lee et al. (1997)               Event
McBride et al. (1998)           Cohort
van Asperen et al. (1998)       Event
Haile et al. (1999)             Cohort
Prieto et al. (2001)            Cohort

Table 2. Summary relative risks of GI illness by level of exposure to
indicators of water quality: marine water studies.

                                    Relative risk (95% CI), category
                                         level (1 = lowest; 4 =
                                              highest) (a)

Indicator                                  1                2

Fecal bacterial indicators
  Enterococci/fecal streptococci       1.58 *           1.61 *
                                      (1.20-1.96)      (0.997-2.60)
    Range (cfu/100 mL)                 1-20            21-54
    Number of studies                  8                6
  Fecal coliform                       1.40             1.69 *
                                      (1.05-1.88)      (0.88-3.2)
    Range (cfu/100 mL)                 2-65            77-300
    Number of studies                  5                6
  E. coil                              1.80             1.41
                                      (1.30-2.50)      (1.06-1.88)
    Range (cfu/100 mL)                 2-54            55-290
    Number of studies                  3                4
  Total coliform                       1.15             1.79 *
                                      (0.74-1.78)      (0.83-3.83)
    Range (cfu/100 mL)                45-320          700-2,022
    Number of studies                  3                5

Nonfecal bacterial indicators
  Staphylococcus sp.                   1.45 *           0.59 *
                                      (0.2-10.76)      (0.21-1.68)
    Range (cfu/100 mL)                 1-175          250-1,114
    Number of studies                  2                3
  Pseudomonas sp.                      1.44 *           1.47 *
                                      (0.44-4.73)      (0.28-7.86)
    Range (cfu/100 mL)                 0-17            26-220
    Number of studies                  2                2
  Aeromonas sp.                        3.86             3.27
                                      (1.76-8.49)      (1.01-10.57)
    Range (cfu/100 mL)                17              662
    Number of studies                  1                1

                                     Relative risk (95% CI), category
                                    level (1 = lowest; 4 = highest) (a)

Indicator                                   3                4

Fecal bacterial indicators
  Enterococci/fecal streptococci          2.45 *          1.95
                                         (1.56-3.77)     (1.53-2.49)
    Range (cfu/100 mL)                   69-104         123-7,460
    Number of studies                     7               7
  Fecal coliform                          1.41 *          2.02
                                         (0.87-2.28)     (1.46-2.77)
    Range (cfu/100 mL)                  310-550         598-2,000
    Number of studies                     6               7
  E. coil                                 2.46 *
                                         (1.31-4.65)
    Range (cfu/100 mL)                  320-5,207
    Number of studies                     5
  Total coliform                          2.08 *
                                         (0.85-2.08)
    Range (cfu/100 mL)                2,100-5,750
    Number of studies                     4

Nonfecal bacterial indicators
  Staphylococcus sp.
    Range (cfu/100 mL)
    Number of studies
  Pseudomonas sp.
    Range (cfu/100 mL)
    Number of studies
  Aeromonas sp.
    Range (cfu/100 mL)
    Number of studies

                                        Correlation coefficients
Indicator                                   (r, p-value) (b)

Fecal bacterial indicators
  Enterococci/fecal streptococci    0.82, < 0.001 (Cabelli 1983)
                                    0.68, NG (Cabelli 1983)
    Range (cfu/100 mL)              0.32, NS (Cheung et al. 1990)
    Number of studies
  Fecal coliform                    0.51, NG (Cabelli 1983)
                                    0.49, NS (Cheung et al. 1990)
    Range (cfu/100 mL)              0.26, NS (Kueh et al. 1995)
    Number of studies               0.77, < 0.05 (Pike 1994)
  E. coil                           0.54, NG (Cabelli 1983)
                                    0.74, NG (Cabelli 1983)(Egypt)
    Range (cfu/100 mL)              0.51, < 0.05 (Cheung et al. 1990)
    Number of studies               0.28, NS (Kueh et al. 1995):
  Total coliform                    0.65, NG (Cabelli 1983)
                                    0.53, NS (Pike 1994)
    Range (cfu/100 mL)
    Number of studies

Nonfecal bacterial indicators
  Staphylococcus sp.                -0.25, NS (Marino et al. 1995)
                                    0.095, NS (Kueh et at. 1995)
    Range (cfu/100 mL)              0.19, NS (Cheung et al. 1990)
    Number of studies
  Pseudomonas sp.                   -0,05, NS (Marino et al. 1995)
                                    0.59, NG (Cabelli 1983):
    Range (cfu/100 mL)              0.21, NS (Cheung et al. 1990)
    Number of studies
  Aeromonas sp.                     0.52, 0.01 (Kueh et al. 1995)
                                    -0.23, NS (Marino et al. 1995)
    Range (cfu/100 mL)              0.6, NG (Cabelli 1983)
    Number of studies

Abbreviations: NC, not given; NS, not statistically significant,
p-value not provided; (a) Relative risk is the risk versus the summary
relative risk for exposed (swimmers) versus unexposed in each category.
(b) Values reported represent the correlation between illness and
indicator density. * p-Value for test of heterogeneity < 0.2.

Table 3. Model parameters from weighted linear regressions of the
natural log relative risks as a function of indicator density (log base
10). (a)

Indicator            No. (b)     Intercept    Coefficient    p-Value

Marine water
  Enterococci          28         0.099          0.30         0.05
  Fecal coliform       22         0.86          -0.024        0.94
  E. coli              12        -0.071          0.25         0.24
  Total coliform       12        -0.096          0.42         0.25
Fresh water
  Enterococci           8         0.54           0.0078       0.97
  Fecal coliform       11         0.53           0.0058       0.98
  E. coli               5        -1.07           0.75         0.063
Total coliform       Too few
                    estimates

Indicator           r (c)

Marine water
  Enterococci        0.37
  Fecal coliform    -0.017
  E. coli            0.37
  Total coliform     0.36
Fresh water
  Enterococci        0.016
  Fecal coliform     0.0083
  E. coli            0.86
Total coliform

(a) Weights for the model were the inverse of the standard error of the
natural log of the relative risk. (b) Number of effect estimates.
(c) Correlation coefficient.

Table 4. Summary relative risks of GI illness by level of exposure to
indicators of water quality: freshwater studies.

                                    Relative risk (95% CI), category
                                               level (a)

Indicator                                Low              High

Fecal bacterial indicators
  Enterococci/fecal streptococci      2.01 *              1.65
                                     (1.18-3.41)         (1.38-1.98)
    Range (cfu/100 mL)               10-14               16-1,669
    Number of studies                 4                   4
  Fecal coliform                      1.73 *              1.84 *
                                     (1.28-2.33)         (1.10-3.10)
    Range (cfu/100 mL)               22-110             200-18,612
    Number of studies                 7                   4
  E. coli                             1.22                1.78
                                     (0.99-1.51)         (1.45-2.20)
    Range (cfu/100 mL)               45-170             187-204
    Number of studies                 3                   2
  Total coliform                      0.7                 2.40
                                     (0.30-1.62)         (1.68-3.39)
    Range (cfu/1100 mL)             786              24,461
    Number of studies                 1                   1
Viral indicators
  Enterovirus                         1.97 *              4.11
                                     (1.20-3.22          (2.59-6.54)
    Range (pfu/10 L)                  0-0.4               1-198.4
    Number of studies                 2                   2
  Bacteriophage                       2.42                2.80
                                     (1.85-3.17)         (1.30-6.02)
    Range (pfu/100 mL)                0.07-20         1,885
    Number of studies                 2                   1
Nonfecal bacterial indicators
  Staphylococcus sp.                  4.30                2.73
                                     (2.60-6.94)         (1.32-5.63)
    Range (cfu/100 mL)               14                  36-45
    Number of studies                 1                   2
  Pseudomonas sp.                     3.13                0.7
                                     (0.75-12.95)        (0.30-1.60)
    Range (cfu/100 mL)                0                   3
    Number of studies                 1                   1
  Aeromonas sp.                       1.32 *              2.40
                                     (0.31-5.62)         (1.70-3.39)
    Range (cfu/100 mL)              190-235           1,549
    Number of studies                 2                   1

Indicator                             Correlation coefficients (r,
                                              p-values) (b)
Fecal bacterial indicators
  Enterococci/fecal streptococci    0.62, 0.02 (Ferley et al. 1989)
                                    0.67, NS (Dufour 1984a)
                                    0.1, NS (Lightfoot 1989)
    Range (cfu/100 mL)              p = 0.069 (Seyfried et al. 1985b)
    Number of studies
  Fecal coliform                    0.38, 0.2 (Ferley et al. 1989)
                                    -0.081, NS (Dufour 1984a)
    Range (cfu/100 mL)              0.19, 0.15 (Lightfoot 1989)
    Number of studies
  E. coli                           0.81, < 0.05 (Dufour 1984a)
                                    0.18, 0.17 (Lightfoot 1989)
    Range (cfu/100 mL)
    Number of studies
  Total coliform                    0.46, 0.11 (Ferley et al. 1989)
    Range (cfu/1100 mL)
    Number of studies
Viral indicators
  Enterovirus
    Range (pfu/10 L)
    Number of studies
  Bacteriophage
    Range (pfu/100 mL)
    Number of studies
Nonfecal bacterial indicators
  Staphylococcus sp.                0.13, 0.34 (Lightfoot 1989)
    Range (cfu/100 mL)
    Number of studies
  Pseudomonas sp.                   -0.73, 0.06 (Ferley et al. 1989)
                                    0.23, 0.08 (Lightfoot 1989)
    Range (cfu/100 mL)
    Number of studies
  Aeromonas sp.                     -0.43, 0.11 (Ferley et al. 1989)
    Range (cfu/100 mL)
    Number of studies

NS, not statistically significant, p-value not provided. (a) Relative
risk is the risk versus the summary relative risk for exposed
(swimmers) versus unexposed in each category. (b) Values reported
represent the correlation between illness and indicator density.
* p-Value for test of heterogeneity < 0.2.

Table 5. Summary relative risks by U.S. EPA water quality standards.

                                                  Combined relative
                                     Current             risk
                                    standard      below standard (a)
Indicator                          (cfu/100mL)         (95% CI)

Marine water
  Enterococci                           35        1.36 * (0.91-2.03)
    Number of studies                                      9
    Median density (cfu/100 mL)                           20
  E. coli                              126        1.33 * (0.89-1.99)
    Number of studies                                      4
    Median density (cfu/100 mL)                           79
  Fecal coliform                       200        1.74 * (0.86-3.53)
    Number of studies                                      6
    Median density (cfu/100 mL)                          101
Fresh water
  Enterococci                           33        1.94 * (1.33-2.84)
    Number of studies                                      6
    Median density (cfu/100 mL)                           14
  E. coil                              126        1.20 (0.97-1.48)
    Number of studies                                      2
    Median density (cfu/100 mL)                           60
  Fecal coliform                       200        1.58 * (1.22-2.04)
    Number of studies                                      7
    Median density (cfu/100 mL)                           80

                                   Combined relative risk
                                     above standard (a)
Indicator                                 (95% CI)

Marine water
  Enterococci                        2.27 * (1.74-2.96)
    Number of studies                        12
    Median density (cfu/100 mL)             139
  E. coli                            1.94 * (1.27-2.96)
    Number of studies                         7
    Median density (cfu/100 mL)             591
  Fecal coliform                     1.53 * (1.03-2.26)
    Number of studies                         9
    Median density (cfu/100 mL)             862
Fresh water
  Enterococci                        1.61 (1.32-1.96)
    Number of studies                         2
    Median density (cfu/100 mL)             858
  E. coil                            1.81 (1.47-2.22)
  Number of studies                           3
    Median density (cfu/100 mL)             187
    Fecal coliform                   2.11 * (0.98-4.5)
    Number of studies                         3
    Median density (cfu/100 mL)             285

(a) Relative risk is the risk versus the summary relative risk for
exposed (swimmers) versus unexposed in each category.

* p-Value for test of heterogeneity < 0.2.

Table 6. Sources of heterogeneity: results from
meta-regression models for studies of enterococci
and GI illness.

                                             Exponentiated
                                               regression
Covariate                               coefficient (95% CI) (a)

Age of study population                     1.85 (1.06-3.19)
  (children only studies vs. studies
  of adults or studies of all ages)
Control group                               1.88 (1.33-2.67)
  (nonswimmers vs. swimmers)
Study population                            1.39 (1.05-1.84)
  (studies of athletic event
  participants vs. studies of
  beach-goers or general population)

Water quality, as measured by enterococci density, was
also included in the model. Thirty-eight point estimates
from 20 studies were included in the model. Indicator variables
for water source (marine or fresh), study design (randomized
controlled trial, cohort, case-control), study
location, swimming definition; adjustment for covariates;
and follow-up times were included in the initial model but
were removed since they were not significantly associated
to the relative risk (p > 0.2). Exponentiated coefficients can
be interpreted as the impact (on a multiplicative scale) on
the relative risk.

REFERENCES

Alexander LM, Heaven A, Tennant A, Morris R. 1992. Symptomatology of children in contact with sea water contaminated with sewage. J Epidemiol Community Health 46:340-344.

Balarajan R, Soni Raleigh V, Yuen P, Wheeler D, Machin D, Cartwright R. 1991. Health risks associated with bathing in sea water. Br Med J 303:1444-1445.

Bandaranayake DR, Turner SJ, McBride GB, Lewis G, Till D. 1995. Health Effects of Bathing at Selected New Zealand Marine Beaches. Internal Report. Wellington:New Zealand Department of Health.

Baron RC, Murphy FD, Greenberg HB, Davis CE, Bregman DJ, Gary GW, et al. 1982. Norwalk gastrointestinal illness: an outbreak associated with swimming in a recreational lake and secondary person-to-person transmission. Am J Epidemiol 115:163-172.

Barwick RS, Levy DA, Craun GF, Beach MJ, Calderon RI. 2000. Surveillance for waterborne-disease outbreaks: United States, 1997-1998. Morb Mortal Wkly Rep 49:1-36.

Begg CB, Madachhanda M. 1994. Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088-1099.

Cabelli V. 1983. Health Effects Criteria for Marine Recreational Waters. U.S. EPA Report EPA-600/1-80-031. Cincinnati, OH:U.S. Environmental Protection Agency.

Cabelli V, Dufour A, Levin M, Habermann P. 1975. The impact of pollution on marine bathing beaches: an epidemiological study. In: Middle Atlantic Continental Shelf and the New York Bight: Proceedings of the Symposium, American Society of Limnology and Oceanography, New York City, 3-5 November. Lawrence, KS:American Society of Limnology and Oceanography, 424-432.

Cabelli VJ, Dufour AP, Levin MA, McCabe LJ, Haberman PW. 1979. Relationship of microbial indicators to health effects at marine bathing beaches. Am J Public Health 69:690-696.

Cabelli VJ, Dufour AP, McCabe LJ, Levin MA. 1982. Swimming-associated gastroenteritis and water quality. Am J Epidemiol 115:806-616.

Calderon R, Mood E. 1981. Epidemiological Studies of Otitis Externa: Report of a Prospective and of a Retrospective Study of Otitis Externa among Swimmers. Project Summary. EPA-600/S1-81-053. Cincinnati, OH:U.S. Environmental Protection Agency.

--. 1982. An epidemiological assessment of water quality and "swimmer's ear." Arch Environ Health 37:300-305.

Calderon R, Mood E, Dufour A. 1991. Health effects of swimmers and nonpoint sources of contaminated water. Int J Environ Health Res 1:21-31.

Charoenca N, Fujioka R. 1995. Association of staphylococcal skin infections and swimming. Water Sci Technol 31:11-18.

Cheung WH, Chang KC, Hung RP, Kleevens JW. 1990. Health effects of beach water pollution in Hong Kong. Epidemiol Infect 105:139-162.

Corbett SJ, Rubin GL, Curry GK, Kleinbaum DG. 1993. The health effects of swimming at Sydney beaches. The Sydney Beach Users Study Advisory Group. Am J Public Health 83:1701-1706.

D'Alessio D, Minor TE, Allen CI, Tsiatis AA, Nelson DB. 1981. A study of the proportions of swimmers among well controls and children with enterovirus-like illness shedding or not shedding an enterovirus. Am J Epidemiol 113:533-541.

DerSimonian R, Laird N. 1986. Mete-analysis in clinical trials. Control Clin Trials 7:177-188.

Dufour A. 1984a. Health Effects Criteria for Fresh Recreational Waters. EPA-600-1-84-004. Cincinnati, OH:U.S. Environmental Protection Agency.

--. 1984b. Bacterial indicators of recreational water quality. Can J Public Health 75:49-56.

El-Sharkawi F, Hassan F. 1979. The relation between the state of pollution on Alexandria swimming beaches and the occurrence of typhoid among bathers. Bull High Inst Public Health Alexandria 9:337-351.

Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, et al. 2002. Epidemiologic and molecular trends of "Norwalk-like viruses" associated with outbreaks of gastroenteritis in the United States. J Infect Dis 186:1-7.

Fattal B, Peleg-Olevsky E, Yoshpe-Purer Y, Shuval H. 1986. The association between morbidity among bathers and microbial quality of seawater. Wat Sci Technol 18:59-69.

Favero M, Drake C, Randall G. 1964. Use of staphyloccoci as indicators of swimming pool pollution. Public Health Rep 92:245-250.

Ferley JP, Zmirou D, Balducci F, Baleux B, Fera P, Larbaigt G, et al. 1989. Epidemiological significance of microbiological pollution criteria for river recreational waters. Int J Epidemiol 18:198-205.

Fewtrell L, Godfree AF, Jones F, Kay D, Salmon RL, Wyer MD. 1992. Health effects of white-water canoeing. Lancet 339:1587-1589.

Fewtrell L, Kay D, Salmon R, Wyer M, Newman G, Bowering G. 1994. The health effects of low-contact water activities in fresh and estuarine waters. J Inst Water Environ Manag 8:97-101.

Fleisher JM. 1992. U.S. federal bacteriological water quality standards: a re-analysis. In: Recreational Water Quality Management, Vol. 1: Coastal Waters (Kay D, ed). New York: Ellis Horwood, 113-127.

Fleisher JM, Jones F, Kay D, Stanwell-Smith R, Wyer M, Morano R. 1993. Water and non-water-related risk factors for gastroenteritis among bathers exposed to sewage-contaminated marine waters. Int J Epidemiol 22:698-708.

Fleisher JM, Kay D, Salmon RL, Jones F, Wyer MD, Godfree AF. 1996. Marine waters contaminated with domestic sewage: nonenteric illnesses associated with bather exposure in the United Kingdom. Am J Public Health 86:1228-1234.

Fleisher JM, Kay D, Wyer MD, Godfree AF. 1998. Estimates of the severity of illnesses associated with bathing in marine recreational waters contaminated with domestic sewage. Int J Epidemiol 27:722-726.

Foulon G, Maurin J, Quoi N, Martin -Buoyer G. 1983. Etude de la morbidite humaine en relation avec la pollutino bacteriologique des eaux de baignade en mer. Rev Fr Sci Eau 2:127-143.

Greenland S. 1998. Meta analysis. In: Modern Epidemiology (Rothman KJ, Greenland S, eds). Philadelphia, PA:Lippincott-Raven, 647-711.

Griffin DW, Donaldson KA, Paul JH, Rose JB. 2003. Pathogenic human viruses in coastal waters. Clin Microbiol Rev 16:129-143.

Haile RW, Witte JS, Gold M, Cressey R, McGee C, Millikan RC, et al. 1999. The health effects of swimming in ocean water contaminated by storm drain runoff. Epidemiology 10:355-363.

Harrington JF, Wilcox DN, Giles PS, Ashbolt NJ, Evans JC, Kirton HC. 1993. The health of Sydney surfers: an epidemiological study. Water Sci Technol 27:175-181.

Jessop EG, Horsley SD, Wood L. 1985. Recreational use of inland water and health: are Windermere and Coniston water a health hazard? Public Health 99:338-342.

Jones F, Kay D, Stanwell-Smith R, Wyer M. 1991. Results of the first pilot-scale controlled cohort epidemiological investigation into the possible health effects of bathing in seawater at Langland Bay, Swansea. J Int Water Environ Manag 5:91-97.

Kappus KD, Marks JS, Holman RC, Bryant JK, Baker C, Gary GW, et al. 1982. An outbreak of Norwalk gastroenteritis associated with swimming in a pool and secondary person-to-person transmission. Am J Epidemiol 116:834-839.

Kay D, Fleisher JM, Salmon RL, Jones F, Wyer MD, Godfree AF, et al. 1994. Predicting likelihood of gastroenteritis from sea bathing: results from randomised exposure. Lancet 344:905-909.

Ktsanes V, Anderson A, Diem J. 1981. Health Effects of Swimming in Lake Pontchartrain at New Orleans. EPA-600/S1-81-027. Cincinnati, OH:U.S. Environmental Protection Agency.

Kueh CSW, Tam TY, Lee T, Wong SL, Lloyd OL, Yu ITS, et al. 1995. Epidemiological study of swimming-associated illnesses relating to bathing-beach water quality. Water Sci Technol 31:1-4.

Lee JV, Dawson SR, Ward S, Surman SB, Neal KR. 1997. Bacteriophages are a better indicator of illness rates than bacteria amongst users of a white water course fed by a lowland river. Water Sci Technol 35:165-170.

Lee SH, Levy DA, Craub GF, Beach MJ, Calderon RL. 2002. Surveillance for waterborne disease outbreaks: United States, 1999-2000. Morb Mortal Wkly Rep 51:1-45.

Levy DA, Bens MS, Craun GF, Calderon RL, Herwaldt BL. 1998. Surveillance for waterborne-disease outbreaks--United States, 1995-1996. Morb Mortal Wkly Rep 47:1-34.

Lightfoot N. 1989 A prospective study of swimming related illness at six freshwater beaches in southern Ontario [Ph.D. Thesis]. Toronto, Canada:University of Toronto.

Marino F, Morinigo M, Martinez-Manzanares E, Borrego J. 1995. Microbiological-epidemiological study of selected marine beaches in Malaga (Spain). Water Sci Technol 31:5-9.

McBride GB, Salmondo CE, Bandaranayake DR, Turner SJ, Lewis GD, Till DG. 1998. Health effects of marine bathing in New Zealand. Int J Environ Health Res 8:173-189.

Mead PS, Slutsker L, Dietz V, McCraig LF, Bresee JS, Shapiro C, et al. 1999. Food-related illness and death in the United States. Emerg Infect Dis 5:607-625.

Medema G, Van Asperen I, Klokman-Houweling J, Nooitgedagt A, Van de Laar M. 1995. The relationship between health effects in triathletes and microbiological quality of freshwater. Water Sci Technol 31:19-26.

New Jersey Department of Health. 1989. A Study of the Relationship between Illness and Ocean Beach Water Quality. Interim Summary Report. Trenton, NJ:New Jersey Department of Health.

Philipp R, Evans EJ, Hughes AO, Grisdale SK, Enticott RG, Jephcott AE. 1985. Health risks of snorkel swimming in untreated water. Int J Epidemiol 14:624-627.

Philipp R, Waitkins S, Caul O, Roome A, MacMahon S, Enticott R. 1989. Leptospiral and hepatitis A antibodies amongst windsurfers and waterskiers in Bristol city docks. Public Health 103:123-129.

Public Health Laboratory Service. 1959. Sewage contamination of coastal bathing waters in England and Wales. J Hygiene 43:435-472.

Pike E. 1990. Health Effects of Sea Bathing (ET 9511 SLG). Phase I--Pilot Studies at Langland Bay, 1989. WRC Report Number: DoE 2736-M 2518-M. Medmenham, UK:Water Research Centre.

--. 1991. Health Effects of Sea Bathing (EM 9511), Phase II--Studies at Ramsgate and Moreton, 1990. WRC Report Number: DoE 2736-M. Medmenham, UK:Water Research Centre.

--. 1994. Health Effects of Sea Bathing (WMI 9021), Phase III--Final Report to the Department of the Environment. WRC Report Number: DoE 3412/2. Medmenham, UK:Water Research Centre.

Pilotto LS, Douglas RM, Burch MD, Cameron S, Beers M, Rouch GJ, et al. 1997. Health effects of exposure to cyanobacteria (blue-green algae) during recreational water-related activities. Aust N Z J Public Health 21:562-566.

Prieto MD, Lopez B, Juanes JA, Revilla JA, Llorca J, Delgado-Rodriguez M 2001. Recreation risks in coastal waters: health risks associated with bathing in sea water. J Epidemiol Community Health 55:442-447.

Pruss A. 1998. Review of epidemiological studies on health effects from exposure to recreational water. Int J Epidemiol 27:1-9.

Scott TM, Rose JB, Jenkins TM, Farrah SR, Lukasik J. 2002. Microbial source tracking: current methodology and future directions. Appl Environ Microbiol 68:5796-5803.

Seyfried PL, Tobin RS, Brown NE, Ness PF. 1985a. A prospective study of swimming-related illness. I. Swimming-associated health risk. Am J Public Health 75:1068--1070.

--. 1985b. A prospective study of swimming-related illness. II. Morbidity and the microbiological quality of water. Am J Public Health 75:1071-1075.

Stata Corporation. 2002. Stata SE Version 7.0. College Station, TX: Stata Corporation.

Stevenson A. 1953. Studies of bathing water quality and health. Am J Public Health Assoc 43:529-538.

Taylor MB, Becker PJ, Van Rensburg EJ, Harris BN, Bailey IW, Grabow WO. 1995. A serosurvey of water-borne pathogens amongst canoeists in South Africa. Epidemiol Infect 115:299-307.

Thompson SG, Sharp S J. 1999. Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med 18:2693-2708.

U.S. EPA. 1986. Bacteriological Water Quality Criteria for Marine and Fresh Recreational Waters. EPA-440/5-84-002. Cincinnati, OH:U.S. Environmental Protection Agency, Office of Water Regulations and Standards.

--. 1997. Method 1600: Membrane Filter Test for Enterococci in Water. EPA-821-R-97-004. Washington, DC:U.S. Environmental Protection Agency, Office of Water.

--. 2002. Implentation Guidance for Ambient Water Quality Criteria for Bacteria. EPA-823-B-02-003. Washington, DC:U.S. Environmental Protection Agency, Office of Water.

van Asperen IA, de Rover CM, Schijven JF, Oetomo SB, Schellekens JF, van Leeuwen NJ, et al. 1995. Risk of otitis externa after swimming in recreational fresh water lakes containing Pseudomonas aeruginosa. Br Med J 311:1407-1410.

van Asperen IA, Medema G, Borgdorff MW, Sprenger MJ, Havelaar AH. 1998. Risk of gastroenteritis among triathletes in relation to faecal pollution of fresh waters, Int J Epidemiol 27:309-315.

von Schirnding YE, Kfir R, Cabelli V, Franklin L, Joubert G. 1992. Morbidity among bathers exposed to polluted seawater. A prospective epidemiological study. S Afr Mod J 81:543-546.

World Health Organization. 2001. Bathing Water Quality and Human Health: Faecal Pollution. Outcome of an Expert Consultation. Farnham, UK:World Health Organization.

Zmirou D, Fedey JP, Balducci F, Moissonnier B, Blineau A, Boudot J. 1990. Evaluation des indicateurs du risque sanitaire lie' aux baignades en riviere. Rev Epidemiol Sante Publique 38:101-110.

Timothy J. Wade, (1) Nitika Pai, (2) Joseph N.S. Eisenberg, (2) and John M. Colford, Jr. (2)

(1) Epidemiology and Biomarkers Branch, U.S. Environmental Protection Agency, Research Triangle Park, North Carolina, USA; (2) School Public Health, Division of Epidemiology, University of California, Berkeley, California, USA

Address correspondence to John M. Colford, Jr., School of Public Health, University of California, 140 Warren Hall MC 7360, Berkeley, CA 94720 USA. Telephone: [phone]. Fax number: [phone]. E-mail address: [e-mail]

We acknowledge the following for their assistance in finding and obtaining published and unpublished reports: A. Dufour, M. Beach, D. Levy, and S. Lee. We also thank M. Pai for his review of the manuscript. A preliminary draft of this work was prepared for and presented to the National Academy of Sciences, Indicators for Waterborne Pathogens Committee, on 4 September 2002.

Support for work on this grant was funded by Centers for Disease Control and Prevention Cooperative Agreement U50/CCU916961-01.

The authors declare they have no conflict of interest.

Received 29 January 2003; accepted 14 April 2003.