Introduction

Advances in molecular methods provide new opportunities for directly measuring pathogens or host-associated markers of fecal pollution instead of relying on fecal indicator bacteria (FIB) alone for beach water quality monitoring. Adoption of new indicators depends on identifying relationships between either the presence or concentration of the indicators and illness among swimmers. Here we present results from three epidemiologic studies in which a broad range of bacterial and viral indicators of fecal contamination were measured simultaneously by either culture or molecular methods along with Enterococcus to assess whether they provide better health risk prediction than current microbial indicators of recreational water quality.

Methods

We conducted prospective cohort studies at three California beaches -- Avalon Bay (Avalon), Doheny State Beach (Doheny), Surfrider State Beach (Malibu) -- during the summers of 2007, 2008 and 2009. The studies enrolled 10,785 swimmers across the beaches and recorded each swimmer's water exposure. Water and sand samples were collected several times per day at multiple locations at each beach and analyzed for up to 41 target indicators using 67 different methodologies. Interviewers contacted participants by phone 10-14 days later and recorded symptoms of gastrointestinal illness occurring after their beach visit. Regression models were used to evaluate the association between water quality indicators and gastrointestinal illness among swimmers at each beach.

Results

F+ coliphage (measured using EPA Method 1602) exhibited a stronger association with GI illness than did EPA Method 1600 at the two beaches where it was measured, while a molecular method, F+ RNA Coliphage Genotype II, was the only indicator significantly associated with GI illness at Malibu. MRSA, a known pathogen, had the strongest association with GI illness of any microbe measured at Avalon. There were two methods targeting human-associated fecal anaerobic bacteria that were more strongly associated with GI illness than EPA Method 1600, but only at Avalon. No indicator combinations consistently had a higher odds ratio than EPA Method 1600, but one composite indicator, based on the number of pathogens detected at a beach, was significantly associated with gastrointestinal illness at both Avalon and Doheny when freshwater flow was high.

Discussion

While EPA Method1600 performed adequately at two beaches based on its consistency of association with gastrointestinal illness and the precision of its estimated associations, F+ coliphage measured by EPA Method 1602 had a stronger association with GI illness under high risk conditions at the two beaches where it was measured. One indicator, F+ Coliphage Genotype II was the only indicator significantly associated with GI illness at Malibu. Several indicators, particularly those targeting human associated bacteria, exhibited relationships with GI illness that were equal to or greater than that of EPA Method 1600 at Avalon, which has a focused human fecal source. Our results suggest that site-specific conditions at each beach determine which indicator or indicators best predict GI illness.

In urban areas, untreated stormwater runoff can pollute downstream surface waters. To intercept and treat runoff, low-impact or "green infrastructure" approaches such as using biofilters are adopted. Yet, actual biofilter pollutant removal is poorly understood; removal is often studied in laboratory columns, with variable removal of viable and culturable microbial cell numbers including pathogens. Here, to assess bacterial pollutant removal in full-scale planted biofilters, stormwater was applied, unspiked or spiked with untreated sewage, in simulated storm events under transient flow conditions, during which biofilter influents versus effluents were compared. Based on microbial biomass, sequences of bacterial community genes encoding 16S rRNA, and gene copies of the human fecal marker HF183 and of the Enterococcus spp. marker Entero1A, removal of bacterial pollutants in biofilters was limited. Dominant bacterial taxa were similar for influent versus effluent aqueous samples within each inflow treatment of either spiked or unspiked stormwater. Bacterial pollutants in soil were gradually washed out, albeit incompletely, during simulated storm flushing events. In post-storm biofilter soil cores, retained influent bacteria were concentrated in the top layers (0-10 cm), indicating that the removal of bacterial pollutants was spatially limited to surface soils. To the extent that plant-associated processes are responsible for this spatial pattern, treatment performance might be enhanced by biofilter designs that maximize influent contact with the rhizosphere.

Background

Studies of health risks associated with recreational water exposure require investigators to make choices about water quality indicator averaging techniques, exposure definitions, follow-up periods, and model specifications; however, investigators seldom describe the impact of these choices on reported results. Our objectives are to report illness risk from swimming at a marine beach affected by nonpoint sources of urban runoff, measure associations between fecal indicator bacteria levels and subsequent illness among swimmers, and investigate the sensitivity of results to a range of exposure and outcome definitions.

Methods

In 2009, we enrolled 5674 people in a prospective cohort at Malibu Beach, a coastal marine beach in California, and measured daily health symptoms 10-19 days later. Concurrent water quality samples were analyzed for indicator bacteria using culture and molecular methods. We compared illness risk between nonswimmers and swimmers, and among swimmers exposed to various levels of fecal indicator bacteria.

Results

Diarrhea was more common among swimmers than nonswimmers (adjusted odds ratio = 1.88 [95% confidence interval = 1.09-3.24]) within 3 days of the beach visit. Water quality was generally good (fecal indicator bacteria levels exceeded water quality guidelines for only 7% of study samples). Fecal indicator bacteria levels were not consistently associated with swimmer illness. Sensitivity analyses demonstrated that overall inference was not substantially affected by the choice of exposure and outcome definitions.

Conclusions

This study suggests that the 3 days following a beach visit may be the most relevant period for health outcome measurement in recreational water studies. Under the water quality conditions observed in this study, fecal indicator bacteria levels were not associated with swimmer illness.

Use of fecal indicator bacteria (FIB) for monitoring beach water quality is based on their co-occurrence with human pathogens, a relationship that can be dramatically altered by fate and transport processes after leaving the human intestine. We conducted a prospective cohort study at Avalon Beach, California (USA), where the indicator relationship is potentially affected by the discharge of sewage-contaminated groundwater and by solar radiation levels at this shallow, relatively quiescent beach. The goals of this study were to determine: 1) if swimmers exposed to marine water were at higher risk of illness than non-swimmers; 2) if FIB measured in marine water were associated with swimmer illness, and; 3) if the associations between FIB and swimmer health were modified by either submarine groundwater discharge or solar radiation levels. There were 7317 individuals recruited during the summers of 2007-08, 6165 (84%) of whom completed follow-up within two weeks of the beach visit. A total of 703 water quality samples were collected across multiple sites and time periods during recruitment days and analyzed for FIB using both culture-based and molecular methods. Adjusted odds ratios (AOR) indicated that swimmers who swallowed water were more likely to experience Gastrointestinal Illness (GI Illness) within three days of their beach visit than non-swimmers, and that this risk was significantly elevated when either submarine groundwater discharge was high (AOR [95% CI]:2.18 [1.22-3.89]) or solar radiation was low (2.45 [1.25-4.79]). The risk of GI Illness was not significantly elevated for swimmers who swallowed water when groundwater discharge was low or solar radiation was high. Associations between GI Illness incidence and FIB levels (Enterococcus EPA Method 1600) among swimmers who swallowed water were not significant when we did not account for groundwater discharge, but were strongly associated when groundwater discharge was high (1.85 [1.06, 3.23]) compared to when it was low (0.77 [0.42, 1.42]; test of interaction: P = 0.03). These results demonstrate the need to account for local environmental conditions when monitoring for, and making decisions about, public health at recreational beaches. The views expressed in this article are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency.