Estimates of fecal contamination in wet sand measured by molecular methods (Enterococcus and Bacteroidales) and culture-based methods (Enterococcus) were positively associated with enteric illness among those digging in sand and being buried in sand at two recreational beach sites. This association was observed for a definition of enteric illness based on composite symptoms (GI illness) and a more narrow definition (diarrhea alone). Although there was some evidence of positive associations between sand-contact activities and enteric illness for culture-based F+ coliphage and molecular fecal Bacteroides and Clostridium spp. estimates, there was inconsistency across the exposure classifications considered (above vs. below the median and tertiles). Our ability to make conclusions for the F+ coliphage measure was limited because of its low frequency of detection in beach sand samples (17%).
This is one of the first studies to show an association between beach sand contact and enteric illness as a function of microbial sand quality. One previous study observed a relationship between sand contact and GI illness, but exposure was assessed as a function of time spent in contact with wet sand, not as a function of an objective measure of microbial sand quality.35
Two other studies of beach sand exposure and health effects (which included objective measures of beach sand fecal indicator densities) did not show consistent relationships between fecal contamination in beach sand, sand-contact activities, and illness (including GI illness).36,37
which lacked objective measures of fecal contamination of sand, observed an increased risk of enteric illness associated with beach sand contact activities (digging in sand and being buried in sand).
Investigators have observed many-fold higher concentrations of fecal microbial indicators (including E. coli
) in beach sand compared with nearby bathing water.36,37
Halliday and Gast7
recently completed a comprehensive review of studies of fecal microbial pollution of beach sand and observed that densities of fecal indicator bacteria in wet sand were up to thirty-eight times higher than in nearby bathing waters. It has been hypothesized that sand could serve as a source of fecal contamination for bathing water, especially the surf zone along the shoreline.3,4,38
Others have demonstrated that sand can serve as both a source and a sink of fecal microbial contamination.14
Debate continues about the applicability of fecal indicator bacteria (e.g., E. coli
) as a measure of beach water quality and fecal contamination of beach sand.4,39,40
Several studies have examined potential for re-growth of E. coli
Beach sand may serve as a source of autochthonous fecal indicator bacteria (E. coli; Enterococcus
) to nearby bathing water in the absence of inputs from point sources of fecal contamination (and associated pathogens). Beach sand has been implicated as contributing unnecessarily to beach advisories based on results of water-quality fecal indicator bacteria tests.4,14
EPA guidelines for monitoring fresh and marine recreational waters are based on E. coli
but no guidelines exist for fecal contamination of sand.
Our results suggest that Enterococcus
density in sand increases the rate of GI illness and diarrhea among beachgoers who have contact with sand. The positive association of a qPCR-based measure of Enterococcus
in sand with enteric illness was more consistent than that observed for a traditional culture-based measure of Enterococcus
and several alternative measures of sand fecal pollution (culture-based F+
coliphage, and qPCR-based Bacteroidales
, fecal Bacteroides
, and Clostridium
spp.). These alternative measures have been considered by some to be more specific indicators of human sewage sources of fecal contamination.43
Previous research has demonstrated a consistent positive association between Enterococcus
calibrator cell equivalents and swimming-associated illness among both adults and children.21,22
Culturable fecal indicator bacteria cells (e.g., total and fecal coliforms, E. coli
, and Enterococcus
) are considered a better measure of viable bacteria associated with fecal pollution than qPCR-based measures, which reflect the genetic material of bacterial cells and may have differential environmental fates.44–48
The two beaches were located near publicly owned treatment-works sewage outfalls. It is possible that fecal contamination from municipal sewage reached recreational beaches through tidal flow, wave action, on-shore wind direction, or currents. However, some evidence suggests that diffuse sources (including coastal birds, other animal populations, bather density, and run-off) may contribute most of the fecal contamination to beach sand.49,50
It is unclear if the observed relationships of Enterococcus
with enteric illness can be generalized to beaches not influenced by municipal sewage outfalls (i.e., non-point source pollution beaches), to freshwater beaches, or to tropical beaches where the population dynamics of fecal indicators in sand may be different.
Swimming was strongly associated with sand contact; 81% of swimmers vs. 19% of non-swimmers reported digging in sand and 89% of swimmers vs. 11% of non-swimmers reported being buried in sand. As a result, our study has little power to evaluate associations between sand contact and illness among non-swimmers because there were very few sand-exposed cases among non-swimmers. For example, among non-swimmers who dug in sand with Enterococcus in the highest tertile, there were no exposed diarrhea cases and one exposed GI illness case. Therefore, although we adjusted for swimming in all analyses of sand contact, it is possible that associations between sand contact and illness reflect exposure to contaminated water as well as sand. In our previous study,51 which included more beaches but lacked measures of fecal contamination of sand, digging in sand was associated with GI illness (adjusted incidence proportion ratio = 1.26 [95% CI = 1.03–1.54]) and diarrhea (1.26 [0.98–1.62]) among non-swimmers, suggesting that sand may be an additional route of exposure to pathogens.
Beachgoers’ contact with sand was assessed by questionnaire and included a question asking if they had contact with wet or dry sand. However, only wet sand was collected and analyzed for microbial measurements. We used microbial quality in wet sand as a proxy for quality of all sand. To examine the potential influence of misclassification of exposure by wet versus dry sand contact, we examined associations restricted to participants with wet sand contact only. The results were similar to those among all participants. For example, among tertiles of the qPCR-based Enterococcus measure, the aORs of associations with GI illness among those digging in wet sand only were 1.02 (95% CI = 0.58–1.80), 1.31 (0.71–2.43), and 2.48 (1.46–4.21), respectively.
Overall, associations were stronger among those buried in sand (which represents a more intense form of sand exposure) than among those digging in sand. Defining sand exposure as any sand contact, including either digging in the sand or buried in the sand, did not alter our conclusions (data not shown).
Research on health effects among beachgoers has focused largely on swimming-associated illness and microbial water quality. We show a relation of sand contact activities with GI illness and diarrhea as a function of objective measures of fecal pollution of 5beach sand. Limitations of the study include a small sample size for investigation of associations among subgroups (children, non-swimmers), use of wet sand as a proxy for exposure to dry sand contact activities, lack of tests of specific enteric pathogens in beach sand, lack of analyses taking account of water quality, and lack of objective measures of enteric illness self-reports by microbial or immunologic tests of biospecimens. Laboratory confirmation of infection with pathogens via tests of saliva, blood, or stool could improve the classification of incident symptoms.
Further investigation of sand exposure and its association with enteric and non-enteric illness appears warranted based on these results. It is unknown whether the relation of Enterococcus in sand with GI illness and diarrhea can be extended to non-enteric illnesses (e.g., skin rash, upper respiratory illness, eye irritation, earache, infected cuts/wounds). Further studies at a broader geographic range of beach sites, including non-point source runoff, freshwater, and tropical beaches, may advance understanding of sand exposures associated with illness risk and the association of densities of fecal-indicator organisms in beach sand with illness risk among beachgoers.