Open Access

Review

Methods Top

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/gate​way ). 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 Conference proceedings, doctoral dissertations, reports, and other unpublished studies when identified were also obtained.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 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 Top

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 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; 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).

Table 1.

Table 2.

Table 3.

Table 4.

Table 5.

Table 6.

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.

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.

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).

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.

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 ≥ 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 Top

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 Top

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 Top

1. 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. Find this article online
2. 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. Find this article online
3. 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.
4. 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. Find this article online
5. 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. Find this article online
6. Begg CB, Madachhanda M. 1994. Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1099. Find this article online
7. 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.
8. 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.
9. 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. Find this article online
10. Cabelli VJ, Dufour AP, McCabe LJ, Levin MA. 1982. Swimming-associated gastroenteritis and water quality. Am J Epidemiol 115:606–616. Find this article online
11. 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.
12. ------ 1982. An epidemiological assessment of water quality and "swimmer's ear." Arch Environ Health 37:300–305. Find this article online
13. 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. Find this article online
14. Charoenca N, Fujioka R.. 1995. Association of staphylococcal skin infections and swimming. Water Sci Technol 31:11–18. Find this article online
15. Cheung WH, Chang KC, Hung RP, Kleevens JW. 1990. Health effects of beach water pollution in Hong Kong. Epidemiol Infect 105:139–162. Find this article online
16. 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. Find this article online
17. 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. Find this article online
18. DerSimonian R, Laird N.. 1986. Meta-analysis in clinical trials. Control Clin Trials 7:177–188. Find this article online
19. Dufour A. 1984a. Health Effects Criteria for Fresh Recreational Waters. EPA-600-1-84-004. Cincinnati, OH:U.S. Environmental Protection Agency.
20. ------ 1984b. Bacterial indicators of recreational water quality. Can J Public Health 75:49–56. Find this article online
21. 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. Find this article online
22. 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. Find this article online
23. 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. Find this article online
24. Favero M, Drake C, Randall G.. 1964. Use of staphyloccoci as indicators of swimming pool pollution. Public Health Rep 92:245–250. Find this article online
25. 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. Find this article online
26. Fewtrell L, Godfree AF, Jones F, Kay D, Salmon RL, Wyer MD. 1992. Health effects of white-water canoeing. Lancet 339:1587–1589. Find this article online
27. 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. Find this article online
28. 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.
29. 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. Find this article online
30. 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. Find this article online
31. 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. Find this article online
32. 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. Find this article online
33. Greenland S. 1998. Meta analysis. In: Modern Epidemiology (Rothman KJ, Greenland S, eds). Philadelphia, PA:Lippincott-Raven, 647-711.
34. Griffin DW, Donaldson KA, Paul JH, Rose JB. 2003. Pathogenic human viruses in coastal waters. Clin Microbiol Rev 16:129–143. Find this article online
35. 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. Find this article online
36. 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. Find this article online
37. 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. Find this article online
38. 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. Find this article online
39. 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. Find this article online
40. 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. Find this article online
41. 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.
42. 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. Find this article online
43. 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. Find this article online
44. 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. Find this article online
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. Find this article online
46. 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.
47. 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. Find this article online
48. 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. Find this article online
49. 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. Find this article online
50. 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 fresh-water. Water Sci Technol 31:19–26. Find this article online
51. 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.
52. 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. Find this article online
53. 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. Find this article online
54. Public Health Laboratory Service 1959. Sewage contamination of coastal bathing waters in England and Wales. J Hygiene 43:435–472. Find this article online
55. 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.
56. ------. 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.
57. ------. 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.
58. 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. Find this article online
59. 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. Find this article online
60. Pruss A.. 1998. Review of epidemiological studies on health effects from exposure to recreational water. Int J Epidemiol 27:1–9. Find this article online
61. 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. Find this article online
62. 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. Find this article online
63. ------ 1985b. A prospective study of swimming-related illness. II. Morbidity and the microbiological quality of water. Am J Public Health 75:1071–1075. Find this article online
64. Stata Corporation. 2002. Stata SE Version 7. 0. College Station, TX: Stata Corporation.
65. Stevenson A.. 1953. Studies of bathing water quality and health. Am J Public Health Assoc 43:529–538. Find this article online
66. 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. Find this article online
67. Thompson SG, Sharp SJ. 1999. Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med 18:2693–2708. Find this article online
68. 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.
69. ------. 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.
70. ------. 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.
71. 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. Find this article online
72. 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. Find this article online
73. 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. Find this article online
74. World Health Organization. 2001. Bathing Water Quality and Human Health: Faecal Pollution. Outcome of an Expert Consultation. Farnham, UK:World Health Organization.
75. 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. Find this article online