Quantitative evaluation of bacteria released by bathers in a marine water

Abstract

Enterococci, a common fecal indicator, and Staphylococcus aureus, a common skin pathogen, can be shed by bathers affecting the quality of recreational waters and resulting in possible human health impacts. Due to limited information available concerning human shedding of these microbes, this study focused on estimating the amounts of enterococci and S. aureus shed by bathers directly off their skin and indirectly via sand adhered to skin. Two sets of experiments were conducted at a marine beach located in Miami-Dade County, Florida. The first study, referred to as the “large pool” study, involved 10 volunteers who immersed their bodies in 4700 L during four 15 min cycles with exposure to beach sand in cycles 3 and 4. The “small pool” study involved 10 volunteers who were exposed to beach sand for 30 min before they individually entered a small tub. After each individual was rinsed with off-shore marine water, sand and rinse water were collected and analyzed for enterococci. Results from the “large pool” study showed that bathers shed concentrations of enterococci and S. aureus on the order of 6×10⁵ and 6×10⁶ colony forming units (CFU) per person in the first 15 min exposure period, respectively. Significant reductions in the bacteria shed per bather (50% reductions for S. aureus and 40% for enterococci) were observed in the subsequent bathing cycles. The “small pool” study results indicated that the enterococci contribution from sand adhered to skin was small (about 2% of the total) in comparison with the amount shed directly from the bodies of the volunteers. Results indicated that bathers transport significant amounts of enterococci and S. aureus to the water column, and thus human microbial bathing load should be considered as a non-point source when designing recreational water quality models.

Introduction

Beaches serve an important role in the US economy. Coastal recreation is estimated to contribute approximately 85% of all US tourist revenues (NRDC, 2005). However, this revenue depends upon the availability of coastal areas that are safe for recreational purposes. According to the latest surveillance of the US Centers for Disease Control (CDC) (Yoder et al., 2004), the largest number of recreational water-associated outbreaks (65 outbreaks causing illness among an estimated 2536 persons) occurred between 2001 and 2002. The National Resources Defense Council (NRDC, 2005) indicates that during 2004, US beaches had 24,853 beach closing and advisory days, the highest in 15 years since the NRDC started reporting this data, a 9% increase from 2003. In 2004, 85% of the total closings and advisories were issued because water quality exceeded the recommended bacterial indicator standards for which the sources of contamination were not identified. The inability to identify sources, in particular when point sources of pollution are not obvious and/or not present, has made it difficult to remediate and prevent the impacts to beaches.

Bathers are considered a potential non-point source of contamination impacting recreational waters. Studies have found that bathers shed appreciable amounts of microbes via their skin into the water column, and swimming related illnesses appear to be associated with the microbial water quality, even in the absence of point sources of fecal contamination. Mallman (1962) and Favero et al. (1964), suggested that large numbers of cocci are washed off the skin of bathers into freshwater swimming pools, and thus concluded that cocci are a valid indicator to measure the recreational quality. Calderon et al. (1991) found that gastrointestinal illnesses observed in swimmers were associated with higher numbers of bathers per day and high densities of S. aureus. Robinton and Mood (1966), Hanes and Fossa (1970), and Smith and Dufour (1993) concluded that high bacterial densities were shed by bathers into the water column, especially S. aureus. Finally, Gerba (2000) and Stewart et al. (2002) found that bathers shed pathogenic organisms via body contact and fecal accidents in drinking water reservoirs, and thus bathers increased the risk of water borne illnesses among drinking water consumers. Of note is that all of these studies were conducted in fresh waters and evaluated the effects of single washing events. Studies are lacking in marine waters and no studies to the authors’ knowledge evaluated the effects from sequential bathing events.

Enterococci and S. aureus were the bacteria chosen for the current study. Enterococci are commonly found in the feces of humans and other warm-blooded animals. Although some Enterococcus species are also found naturally in the environment, the US Environmental Protection Agency recommends the use of enterococci to measure potential fecal contamination in marine waters (Environmental Protection, 1983, Environmental Protection, 1984, Environmental Protection, 2002). S. aureus is a Gram-positive coccus that commonly inhabits the anterior nares of humans and S. aureus is considered one of the common causes of skin infections in the US. S. aureus can survive outside human hosts, and studies have shown correlations between S. aureus skin infections and swimming. Charoenca and Fujioka (1995), and Gabutti et al. (2000) suggested that recreational waters characterized by high S. aureus densities may increase the risk of contracting skin, eye, and ear infections among bathers.

For over four decades, beach sands and sediments in tropical and subtropical environments have been documented to contain high concentrations of the bacterial indicators, E. coli and enterococci, and sand is one of the non-point sources of those indicators. Studies conducted in Hawaii and Guam (Fujioka, 1988; Fujioka and Roll, 1997; Fujioka et al., 1999), and in Puerto Rico (Toranzos and Marcos, 2000) have shown that in the absence of any known sources of human/animal waste, enterococci and E. coli are consistently present and recovered in high concentrations in the subtropical environment. Specifically in South Florida, river bank soils and beach sands have been implicated as the source of indicator microbes to the water column (Desmarais et al., 2002; Rogerson et al., 2003; Shibata et al., 2004). Recent evidence indicated that the significance of beach sands and other environmental sources is not necessarily limited to the sub/tropics. For example, sands have been implicated as a bacterial source in the freshwater beaches of Lake Michigan (Whitman and Nevers, 2003) and Lake Huron (Alm et al., 2006), both in Michigan. Given the high concentrations of indicator bacteria found in beach sands and sediments, bathers can contribute microbes to the water column by carrying sand on their bodies and washing it into the water column as they bath. Note, bacteria densities released from sand adhered to the bodies of bathers represent the total indigenous bacteria attached to sand particulates and those from body contact. No studies have evaluated the contribution of sand carried by bathers as part of the bacterial load to a recreational water body.

In order to fill some of the gaps in human shedding studies, the current study focused on evaluating bacterial shedding in a marine water. Specifically, enterococci and Staphylococcus aureus were quantified by measuring the amount of bacteria shed by bathers directly off their skin and indirectly via sand adhered to skin. Experiments were conducted under controlled conditions where bathers were either washed or immersed in marine waters characterized by low indicator levels. Mass balance considerations were used to calculate the average colony forming units (CFU) of enterococci and Staphylococcus aureus per bather or per bather group.