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 titles 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

Do U.S. Environmental Protection Agency Water Quality Guidelines for

Recreational Waters Prevent Gastrointestinal Illness? A Systematic Review

and Meta-analysis

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

1Epidemiology and Biomarkers Branch, U.S. Environmental Protection Agency, Research Triangle Park, North Carolina, USA; 2School of

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: (510) 643-1076. Fax number: (510) 643-

5163. E-mail address: jcolford@socrates.berkeley.edu

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.

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]

1102 VOLUME 111 | NUMBER 8 | June 2003 • Environmental Health Perspectives

Research | Review
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 metaregression 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; ElSharkawi 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).

Review | Recreational water quality and GI illness

Environmental Health Perspectives • VOLUME 111 | NUMBER 8 | June 2003 1103

Table 1. Studies included in the review.

Reference Location Water type Sample size Study type

Stevenson (1953) USA Fresh 5,124 Cohort

Cabelli (1983) USA Marine 26,686 Cohort

Cabelli (1983) Egypt Marine 23,080 Cohort

Foulon et al. (1983) France Marine 4,921 Cross-sectional

Dufour (1984b) USA Fresh 21,777 Cohort

Philipp et al. (1985) UK Marine 247 Event

Seyfried et al. (1985b) Canada Fresh 3,967 Cohort

Fattal et al. (1986) Israel Marine 2,231 Cohort

Lightfoot (1989) Canada Fresh 9,296 Cohort

Ferley et al. (1989) France Fresh 5,737 Cohort

Cheung et al. (1990) Hong Kong Marine 18,741 Cohort

Alexander et al. (1992) UK Marine 703 Cohort

Calderon et al. (1991) USA Fresh 144 Cohort

von Schirnding et al. (1992) South Africa Marine 733 Cohort

Fewtrell et al. (1992) UK Fresh 516 Event

Pike (1994) UK Marine 16,569 Cohort

Corbett et al. (1993) Australia Marine 2,968 Cohort

Fleisher et al. (1993) UK Marine 509 Randomized trial

Kay et al. (1994) UK Marine 1,306 Randomized trial

Medema et al. (1995) The Netherlands Fresh 395 Event

Marino et al. (1995) Spain Marine 2,249 Cohort

Kueh et al. (1995) Hong Kong Marine 18,122 Cohort

Lee et al. (1997) UK Fresh 473 Event

McBride et al. (1998) New Zealand Marine 3,887 Cohort

van Asperen et al. (1998) The Netherlands Fresh 1,600 Event

Haile et al. (1999) USA Marine 11,686 Cohort

Prieto et al. (2001) Spain Marine 1,858 Cohort
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 selfreport 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 Schirnding 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;

Review | Wade et al.

1104 VOLUME 111 | NUMBER 8 | June 2003 • Environmental Health Perspectives

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 3 4 Correlation coefficients (r, p-value)b

Fecal bacterial indicators

Enterococci/fecal streptococci 1.58* 1.61* 2.45* 1.95 0.82, < 0.001 (Cabelli 1983)

(1.20–1.96) (0.997–2.60) (1.56–3.77) (1.53–2.49) 0.68, NG (Cabelli 1983)

Range (cfu/100 mL) 1–20 21–54 69–104 123–7,460 0.32, NS (Cheung et al. 1990)

Number of studies 8 6 7 7

Fecal coliform 1.40 1.69* 1.41* 2.02 0.51, NG (Cabelli 1983)

(1.05–1.88) (0.88–3.2) (0.87–2.28) (1.46–2.77) 0.49, NS (Cheung et al. 1990)

Range (cfu/100 mL) 2–65 77–300 310–550 598–2,000 0.26, NS (Kueh et al. 1995)

Number of studies 5 6 6 7 0.77, < 0.05 (Pike 1994)

E. coli 1.80 1.41 2.46* 0.54, NG (Cabelli 1983)

(1.30–2.50) (1.06–1.88) (1.31–4.65) 0.74, NG (Cabelli 1983) (Egypt)

Range (cfu/100 mL) 2–54 55–290 320–5,207 0.51, < 0.05 (Cheung et al. 1990)

Number of studies 3 4 5 0.28, NS (Kueh et al. 1995):

Total coliform 1.15 1.79* 2.08* 0.65, NG (Cabelli 1983)

(0.74–1.78) (0.83–3.83) (0.85–2.08) 0.53, NS (Pike 1994)

Range (cfu/100 mL) 45–320 700–2,022 2,100–5,750

Number of studies 3 5 4

Nonfecal bacterial indicators

Staphylococcus sp. 1.45* 0.59* –0.25, NS (Marino et al. 1995)

(0.2–10.76) (0.21–1.68) 0.095, NS (Kueh et al. 1995)

Range (cfu/100 mL) 1–175 250–1,114 0.19, NS (Cheung et al. 1990)

Number of studies 2 3

Pseudomonas sp. 1.44* 1.47* –0.05, NS (Marino et al. 1995)

(0.44–4.73) (0.28–7.86) 0.59, NG (Cabelli 1983):

Range (cfu/100 mL) 0–17 26–220 0.21, NS (Cheung et al. 1990)

Number of studies 2 2

Aeromonas sp. 3.86 3.27 0.52, 0.01 (Kueh et al. 1995)

(1.76–8.49) (1.01–10.57) –0.23, NS (Marino et al. 1995)

Range (cfu/100 mL) 17 662 0.6, NG (Cabelli 1983)

Number of studies 1 1

Abbreviations: NG, 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.
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.

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 GI 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).

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

Review | Recreational water quality and GI illness

Environmental Health Perspectives • VOLUME 111 | NUMBER 8 | June 2003 1105

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 rc

Marine water

Enterococci 28 0.099 0.30 0.05 0.37

Fecal coliform 22 0.86 –0.024 0.94 –0.017

E. coli 12 –0.071 0.25 0.24 0.37

Total coliform 12 –0.096 0.42 0.25 0.36

Fresh water

Enterococci 8 0.54 0.0078 0.97 0.016

Fecal coliform 11 0.53 0.0058 0.98 0.0083

E. coli 5 –1.07 0.75 0.063 0.86

Total coliform Too few estimates

a Weights for the model were the inverse of the standard error of the natural log of the relative risk. bNumber of effect

estimates. cCorrelation coefficient.

10 100 1,000 10,000

Enterococci (cfu/100 mL)

Relative risk (natural log)

2.0

1.5

1.0

0.5

0.0

●

●

●

●

●

●

●

●

●

●●

●

●

●

● ●

●

●

●

●

●

●

● ●

● ●

●

Weighted least-squares regression

U.S. EPA guideline value

Slope = 0.30 (p = 0.051)

r = 0.37

Figure 1. Scatterplot and weighted regression line (weighted by the inverse of the standard error of the

natural log relative risk) of natural log relative risks of GI illness from marine water studies as a function of

enterococci density.
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

≥ 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

Review | Wade et al.

1106 VOLUME 111 | NUMBER 8 | June 2003 • Environmental Health Perspectives

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

studies.

Relative risk (95% CI), category levela

Indicator Low High Correlation coefficients (r, p-values)b

Fecal bacterial indicators

Enterococci/fecal streptococci 2.01* 1.65 0.62, 0.02 (Ferley et al. 1989)

(1.18–3.41) (1.38–1.98) 0.67, NS (Dufour 1984a)

0.1, NS (Lightfoot 1989)

Range (cfu/100 mL) 10–14 16–1,669 p = 0.069 (Seyfried et al. 1985b)

Number of studies 4 4

Fecal coliform 1.73* 1.84* 0.38, 0.2 (Ferley et al. 1989)

(1.28–2.33) (1.10–3.10) –0.081, NS (Dufour 1984a)

Range (cfu/100 mL) 22–110 200–18,612 0.19, 0.15 (Lightfoot 1989)

Number of studies 7 4

E. coli 1.22 1.78 0.81, < 0.05 (Dufour 1984a)

(0.99–1.51) (1.45–2.20) 0.18, 0.17 (Lightfoot 1989)

Range (cfu/100 mL) 45–170 187–204

Number of studies 3 2

Total coliform 0.7 2.40 0.46, 0.11 (Ferley et al. 1989)

(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 0.13, 0.34 (Lightfoot 1989)

(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 –0.73, 0.06 (Ferley et al. 1989)

(0.75–12.95) (0.30–1.60) 0.23, 0.08 (Lightfoot 1989)

Range (cfu/100 mL) 0 3

Number of studies 1 1

Aeromonas sp. 1.32* 2.40 –0.43, 0.11 (Ferley et al. 1989)

(0.31–5.62) (1.70–3.39)

Range (cfu/100 mL) 190–235 1,549

Number of studies 2 1

NS, not statistically significant, p-value not provided. aRelative risk is the risk versus the summary relative risk for

exposed (swimmers) versus unexposed in each category. bValues reported represent the correlation between illness and

indicator density. *p-Value for test of heterogeneity < 0.2.
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

Review | Recreational water quality and GI illness

Environmental Health Perspectives • VOLUME 111 | NUMBER 8 | June 2003 1107 Relative risk (natural log)

1.0

0.8

0.6

0.4

0.2

50 60 70 80 90 100 200

E. coli (cfu/100 mL)

Weighted least-squares regression

U.S. EPA guideline value

Slope = 0.75 (p = 0.063) r = 0.86

●

●

●

●

●

Figure 2. Scatterplot and weighted regression line (weighted by the inverse of the standard error of the

natural log relative risk) of the natural log relative risk of GI illness from freshwater studies as a function of

E. coli density.

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

Combined relative risk Combined relative risk

Current standard below standarda above standarda

Indicator (cfu/100mL) (95% CI) (95% CI)

Marine water

Enterococci 35 1.36* (0.91–2.03) 2.27* (1.74–2.96)

Number of studies 9 12

Median density (cfu/100 mL) 20 139

E. coli 126 1.33* (0.89–1.99) 1.94* (1.27–2.96)

Number of studies 4 7

Median density (cfu/100 mL) 79 591

Fecal coliform 200 1.74* (0.86–3.53) 1.53* (1.03–2.26)

Number of studies 6 9

Median density (cfu/100 mL) 101 862

Fresh water

Enterococci 33 1.94* (1.33–2.84) 1.61 (1.32–1.96)

Number of studies 6 2

Median density (cfu/100 mL) 14 858

E. coli 126 1.20 (0.97–1.48) 1.81 (1.47–2.22)

Number of studies 2 3

Median density (cfu/100 mL) 60 187

Fecal coliform 200 1.58* (1.22–2.04) 2.11* (0.98–4.5)

Number of studies 7 3

Median density (cfu/100 mL) 80 285

aRelative 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.
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 metaanalysis. 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.

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 Rl. 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. Swimmingassociated gastroenteritis and water quality. Am J Epidemiol

115:606–616.

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. Meta-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:LippincottRaven, 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.

Review | Wade et al.

1108 VOLUME 111 | NUMBER 8 | June 2003 • Environmental Health Perspectives
Review | Recreational water quality and GI illness

Environmental Health Perspectives • VOLUME 111 | NUMBER 8 | June 2003 1109

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, DelgadoRodriguez 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 SJ. 1999. Explaining heterogeneity in metaanalysis: 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 Med 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, Ferley 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.