Estimated human health risks from recreational exposures to stormwater runoff containing animal faecal material
Introduction
Epidemiology studies have linked swimming-associated illnesses with faecal indicator bacteria (FIB) densities in sewage-impacted recreational waters (Prüss, 1998, Wade et al., 2003, Zmirou et al., 2003). In those epidemiology studies, elevated FIB levels represent the potential presence of human faecal contamination (NRC, 2004). Although several epidemiology studies have considered non-point sources of contamination, FIB densities do not consistently correspond to risks in waters that are impacted predominantly by non-human sources, such as agricultural animals (Calderon et al., 1991, Colford et al., 2007, Colford et al., 2012, McBride et al., 1998). Human health effects associated with animal-impacted waters may differ from those associated with human sewage-impacted waters because the mix and densities of FIB and pathogens in animal manure are different from those in municipal wastewater. In particular, human enteric viruses are thought to be a major cause of recreator illness in human impacted waters (Sinclair et al., 2009, Soller et al., 2010a) and these gastrointestinal viruses are rarely zoonotic (Midgley et al., 2012, Oliver et al., 2003, Tei et al., 2003). Moreover, pathogen loading to recreational water from animal manure is often event-driven (e.g. rainfall), whereas wastewater outfall loading is relatively continuous, with increases of untreated or poorly treated sewage during rain events. Because of these issues, it is technically and logistically difficult to conduct epidemiology studies on predominately agricultural animal-impacted sites.
Quantitative microbial risk assessment (QMRA) is emerging as a complement to epidemiology for understanding risks in recreational waters, developing recreational water standards, and making beach management decisions. To encourage its application and use for public health protection efforts, we conducted a series of QMRA-based studies and developed an approach to compare the potential health risks associated with various faecal contamination sources in recreational waters (Ashbolt et al., 2010, Schoen and Ashbolt, 2010). To more comprehensively understand the risks associated with human impacted waters, we evaluated the reported results from the 2003–2004 Great Lakes epidemiologic studies (Wade et al., 2006, Wade et al., 2008) and showed that human enteric viruses were the likely aetiologic agents of primary concern and that using Norovirus as a reference pathogen accounted for the vast majority of the estimated gastrointestinal (GI) illness risk (Soller et al., 2010a). We then evaluated the implications of mixtures of human sources impacting a recreational waterbody. Our results illustrate that the source contributing the majority of risk in a waterbody impacted by a mixture of sources may not be the source that contributes the majority of the FIB when the FIB are enumerated by a culture-based method (Schoen et al., 2011). We also investigated whether the relative risks from exposure to recreational waters impacted by direct contamination from gull, chicken, pig, and/or cattle excreta were substantially different than those associated with human-impacted waters. Waters containing seagull excreta and primary sewage effluent were compared at the same FIB density. The result was a lower predicted illness risk from largely seagull-impacted waters (Schoen and Ashbolt, 2010). The results from agricultural-animal impacted-waters indicate that GI illness risks associated with exposure to recreational waters directly impacted by fresh cattle faeces may not be substantially different from waters impacted by human sources, but the risks associated with exposure to recreational waters impacted by fresh chicken, or pig faecal material appear substantially lower than waters impacted by human sources at the FIB water quality limit (Soller et al., 2010b).
Whereas our previous analyses assumed fresh faecal material was deposited directly into recreational water (Soller et al., 2010b), this study considers indirect contamination in which FIB and pathogens from manure-applied land are mobilised into surface water via a rainfall event. Application of animal manure on land is a common practice in the United States and many other countries. Modelling of runoff and stormwater contamination is a well-documented research activity (e.g., (Bhattarai et al., 2011, Burian et al., 2001, Kara et al., 2012, Liu, 1994, López-Vicente et al., 2014, Luna et al., 2006, May and Sivakumar, 2009, Vezzaro and Mikkelsen, 2012, Vezzaro et al., 2014, Whelan et al., 2014)) Prior studies of pathogen and indicator mobilisation via overland flow from land applied manures have explored the influence that numerous factors have on mobilisation (Cardoso et al., 2012, Ferguson et al., 2007, Muirhead et al., 2006, Stout et al., 2005). Those factors include manure type and method of land application (e.g., Hodgson et al., 2009, Miller and Beasley, 2008, Ramirez et al., 2009, Saini et al., 2003, Thurston-Enriquez et al., 2005), slope and ground cover (e.g., Cardoso et al., 2012, Davies et al., 2004, Ferguson et al., 2007, Hodgson et al., 2009, Miller and Beasley, 2008, Stout et al., 2005, Thurston-Enriquez et al., 2005, Trask et al., 2004, Winkworth et al., 2008, Yeghiazarian et al., 2004), rainfall intensity and antecedent soil moisture (Bradford and Schijven, 2002, Davies et al., 2004, Ramirez et al., 2009, Saini et al., 2003, Schijven et al., 2004, Sistani et al., 2009, Yeghiazarian et al., 2004), and chemical properties (e.g., Bradford and Schijven, 2002, Davies et al., 2004). Not surprisingly, mobilisation fractions (i.e., proportion of organisms in land-applied manures that are mobilised during a rain event) reported in the literature vary widely (Hodgson et al., 2009, Stout et al., 2005, Trask et al., 2004). Hence, rather than exploring all the conditions and factors described above, we conducted a series of pilot-scale experiments to characterize mobilisation of indicator organism and zoonotic pathogens from an intense rainfall event for one pasture condition.
Runoff of microorganisms from land is the net effect of multiple hydrologic processes. During our simulated rain events, some microorganisms in land-applied wastes were mobilised and transported in overland flow, while others could have been transported in the vadose zone, infiltrated into the groundwater or were retained in the manure matrix. Among the microorganisms that did mobilise and were transported, some were probably retained on plants or soil surfaces. During these transport processes, microorganisms in land-applied wastes, on soils or in runoff die or may experience regrowth, with the time for a 90% reduction in microorganism density varying widely among microbial groups and for microorganisms in different matrices. In our fate and transport model, die-off and regrowth of pathogens and indicators were not considered because the mobilisation fractions used in this study were based on data from the plots for which rainfall simulation began immediately following manure application.
Section snippets
Methods
We use QMRA to investigate potential impacts from indirect contamination of recreational water by livestock wastes. First, a “forward” QMRA was used to estimate risk associated with recreational exposure in undiluted runoff from freshly-applied livestock wastes. The forward QMRA is the familiar application of QMRA in which pathogen exposure is estimated based on source pathogen density and a fate and transport model (in this case including a mobilisation component) and risk is estimated using
Results
The zero-intercept linear regression between average (Cave) and composite (Ccomposite) densities is presented in Fig. 3 for the indicator data. The strong correlation in composite and average densities indicated that using the indicator and pathogen densities in the composite samples does not introduce undue error in the estimated mobilisation fraction (described below). However, the high degree of correlation observed between the composite and average densities may be specific to the
Discussion
Risk assessment is widely used by governmental and regulatory agencies worldwide to aid in protecting public health following exposure to a myriad of contaminants through numerous routes of exposure. Air pollution regulations, protection of the food supply chain, and drinking water regulations are large-scale examples that illustrate the effective use of risk assessment methodologies within an environmental regulatory context. To date, epidemiology studies have been the primary tool used to
Conclusion
The results of this risk assessment should be helpful to inform public health decision-making in regards to recreational waters affected primarily by non-human faecal contamination. In contrast to the traditional epidemiological-based approach for evaluating potential human health risks in recreational waters, the QMRA-based approach described above allowed the quantitative characterization of the risks posed by non-human faecal contamination. We incorporated field measurements of pathogen and
Acknowledgements
The research described in this article was funded by the U.S. EPA Office of Water, Office of Science and Technology. This work has been subject to formal Agency review, but does not necessarily reflect the views of the Agency, and no official endorsement should be inferred. We gratefully acknowledge Gunther Craun, Martha Embrey, Mark Gibson, Jose Sobrinho, Shamima Akhter, Elizabeth Doyle, Sharon Nappier, Grace Robiou, Cindy Roberts, and Susan Petterson for their support, critiques, and review
References (100)
- et al.
Predicting pathogen risks to aid beach management: the real value of quantitative microbial risk assessment (QMRA)
Water Res.
(2010) - et al.
Development of a physically-based model for transport of Cryptosporidium parvum in overland flow
Environ. Model. Softw.
(2011) - et al.
Modeling the atmospheric deposition and stormwater washoff of nitrogen compounds
Environ. Model. Softw.
(2001) - et al.
Effectiveness of vegetated filter strips in retention of Escherichia coli and Salmonella from swine manure slurry
J. Environ. Manage
(2012) - et al.
Using rapid indicators for enterococcus to assess the risk of illness after exposure to urban runoff contaminated marine water
Water Res.
(2012) - et al.
Development of a risk-based index for source water protection planning, which supports the reduction of pathogens from agricultural activity entering water resources
J. Environ. Manag.
(2008) - et al.
Evaluating manure release parameters for nonpoint contaminant transport model KINEROS2/STWIR
Ecol. Model
(2013) - et al.
Methods to reduce pathogen microorganisms in manure
Livest. Sci.
(2006) - et al.
Time-scale dependence in numerical simulations: assessment of physical, chemical, and biological predictions in a stratified lake at temporal scales of hours to months
Environ. Model. Softw.
(2012) - et al.
A review of composting as a management alternative for beef cattle feedlot manure in southern Alberta, Canada
Bioresour. Technol.
(2007)
Presence of zoonotic pathogens in physico-chemically characterized manures from hog finishing houses using different production systems
Bioresour. Technol.
Review of mathematical models for health risk assessment: VII. chemical dose
Environ. Softw.
Runoff simulation with eight different flow accumulation algorithms: recommendations using a spatially distributed and open-source model
Environ. Model. Softw.
Spatial bioaccumulation modeling in a network of bayous
Environ. Model. Softw.
Overview of the ability of different treatment methods for liquid and solid manure to inactivate pathogens
Bioresour. Technol.
Prediction of urban stormwater quality using artificial neural networks
Environ. Model. Softw.
Assessment of the dose-response relationship of Campylobacter jejuni
Int. J. Food Microbiol.
Evaluating the importance of faecal sources in human-impacted waters
Water Res.
Estimating the primary etiologic agents in recreational freshwaters impacted by human sources of faecal contamination
Water Res.
Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination
Water Res.
Zoonotic transmission of hepatitis E virus from deer to human beings
Lancet
Livestock waste treatment systems for reducing environmental exposure to hazardous enteric pathogens: some considerations
Bioresour. Technol.
Removal of pathogen and indicator microorganisms from liquid swine manure in multi-step biological and chemical treatment
Bioresour. Technol.
Application of global sensitivity analysis and uncertainty quantification in dynamic modelling of micropollutants in stormwater runoff
Environ. Model. Softw.
A model library for dynamic transport and fate of micropollutants in integrated urban wastewater and stormwater systems
Environ. Model. Softw.
Comparison of composting, storage and urea treatment for sanitising of faecal matter and manure
Bioresour. Technol.
An integrated environmental modeling framework for performing quantitative microbial risk assessments
Environ. Model. Softw.
Reduction of indicator and pathogenic microorganisms in pig manure through fly ash and lime addition during alkaline stabilization
J. Hazard. Mater.
Longitudinal study of Escherichia coli O157:H7 in a beef cattle feedlot and role of high-level shedders in hide contamination
Appl. Environ. Microbiol.
Pathogens and manure management systems: a review
Environ. Technol.
Release of Cryptosporidium and Giardia from dairy calf manure: impact of solution salinity
Environ. Sci. Technol.
Evaluating aeration techniques for decreasing phosphorus export from grasslands receiving manure
J. Environ. Qual.
Health effects of swimmers and nonpoint sources of contaminated water
Int J Environ Health Res.
Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157
Nat. Rev. Microbiol.
Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination
Epidemiology
Attenuation of effluent-derived faecal microbes in grass buffer strips
N. Z. J. Agric. Res.
Overland flow delivery of faecal bacteria to a headwater pastoral stream
J. Appl. Microbiol.
Four cases of hemolytic uremic syndrome–source contaminated swimming water?
Clin. Nephrol.
Best Management Practices for Storing and Applying Poultry Litter
Dispersion and transport of Cryptosporidium oocysts from fecal pats under simulated rainfall events
Appl. Environ. Microbiol.
Water ingestion during swimming activities in a pool: a pilot study
J. Water Health
A cluster of Escherichia coli O157: nonmotile infections associated with recreational exposure to lake water
Public Health Rep.
Field scale quantification of microbial transport from bovine faeces under simulated rainfall events
J. Water Health
Quantification of microbial sources in drinking-water catchments
Crit. Rev. Environ. Sci. Technol.
Swine Manune Management Systems in Missouri
Rainfall-induced release of fecal coliforms and other manure constituents: comparison and modeling
Appl. Environ. Microb.
Comparison of release and transport of manure-borne Escherichia coli and enterococci under grass buffer conditions
Lett. Appl. Microbiol.
Uncertainty in modelling of faecal coliform overland transport associated with manure application in Maryland
Hydrol. Process
Cited by (59)
Assessing the defecation practices of unsheltered individuals and their contributions to microbial water quality in an arid, urban watershed
2024, Science of the Total EnvironmentSocial perception and risk assessment of domestic uses of solar pasteurized rainwater in an informal settlement community
2023, Journal of Environmental Chemical Engineering
- 1
Currently at the University of Alberta, Edmonton, AB T6G 2G7, Canada.