Estimated human health risks from recreational exposures to stormwater runoff containing animal faecal material

https://doi.org/10.1016/j.envsoft.2015.05.018Get rights and content

Highlights

  • We examine the human illness potential from exposure to rainfall-induced runoff.

  • The predicted risks are lower than the benchmark level of protection.

  • This risk assessment should be helpful to inform public health decision-making.

Abstract

Scientific evidence supporting recreational water quality benchmarks primarily stems from epidemiological studies conducted at beaches impacted by human fecal sources. Epidemiological studies conducted at locations impacted by non-human faecal sources have provided ambiguous and inconsistent estimates of risk. Quantitative Microbial Risk Assessment (QMRA) is another tool to evaluate potential human health risks from recreational exposures to non-human faecal contamination. The potential risk differential between human and selected non-human faecal sources has been characterized previously for direct deposition of animal feces to water. In this evaluation, we examine the human illness potential from a recreational exposure to freshwater impacted by rainfall-induced runoff containing agricultural animal faecal material. Risks associated with these sources would be at least an order of magnitude lower than the benchmark level of public health protection associated with current US recreational water quality criteria, which are based on contamination from human sewage sources.

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)

  • V. Letourneau et al.

    Presence of zoonotic pathogens in physico-chemically characterized manures from hog finishing houses using different production systems

    Bioresour. Technol.

    (2010)
  • D. Liu

    Review of mathematical models for health risk assessment: VII. chemical dose

    Environ. Softw.

    (1994)
  • M. López-Vicente et al.

    Runoff simulation with eight different flow accumulation algorithms: recommendations using a spatially distributed and open-source model

    Environ. Model. Softw.

    (2014)
  • R. Luna et al.

    Spatial bioaccumulation modeling in a network of bayous

    Environ. Model. Softw.

    (2006)
  • W. Martens et al.

    Overview of the ability of different treatment methods for liquid and solid manure to inactivate pathogens

    Bioresour. Technol.

    (2009)
  • D.B. May et al.

    Prediction of urban stormwater quality using artificial neural networks

    Environ. Model. Softw.

    (2009)
  • G.J. Medema et al.

    Assessment of the dose-response relationship of Campylobacter jejuni

    Int. J. Food Microbiol.

    (1996)
  • M.E. Schoen et al.

    Evaluating the importance of faecal sources in human-impacted waters

    Water Res.

    (2011)
  • J.A. Soller et al.

    Estimating the primary etiologic agents in recreational freshwaters impacted by human sources of faecal contamination

    Water Res.

    (2010)
  • J.A. Soller et al.

    Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination

    Water Res.

    (2010)
  • S. Tei et al.

    Zoonotic transmission of hepatitis E virus from deer to human beings

    Lancet

    (2003)
  • E. Topp et al.

    Livestock waste treatment systems for reducing environmental exposure to hazardous enteric pathogens: some considerations

    Bioresour. Technol.

    (2009)
  • M.B. Vanotti et al.

    Removal of pathogen and indicator microorganisms from liquid swine manure in multi-step biological and chemical treatment

    Bioresour. Technol.

    (2005)
  • L. Vezzaro et al.

    Application of global sensitivity analysis and uncertainty quantification in dynamic modelling of micropollutants in stormwater runoff

    Environ. Model. Softw.

    (2012)
  • L. Vezzaro et al.

    A model library for dynamic transport and fate of micropollutants in integrated urban wastewater and stormwater systems

    Environ. Model. Softw.

    (2014)
  • B. Vinnerås

    Comparison of composting, storage and urea treatment for sanitising of faecal matter and manure

    Bioresour. Technol.

    (2007)
  • G. Whelan et al.

    An integrated environmental modeling framework for performing quantitative microbial risk assessments

    Environ. Model. Softw.

    (2014)
  • J.W.C. Wong et al.

    Reduction of indicator and pathogenic microorganisms in pig manure through fly ash and lime addition during alkaline stabilization

    J. Hazard. Mater.

    (2009)
  • T.M. Arthur et al.

    Longitudinal study of Escherichia coli O157:H7 in a beef cattle feedlot and role of high-level shedders in hide contamination

    Appl. Environ. Microbiol.

    (2009)
  • J. Bicudo et al.

    Pathogens and manure management systems: a review

    Environ. Technol.

    (2003)
  • S.A. Bradford et al.

    Release of Cryptosporidium and Giardia from dairy calf manure: impact of solution salinity

    Environ. Sci. Technol.

    (2002)
  • D.M. Butler et al.

    Evaluating aeration techniques for decreasing phosphorus export from grasslands receiving manure

    J. Environ. Qual.

    (2008)
  • R. Calderon et al.

    Health effects of swimmers and nonpoint sources of contaminated water

    Int J Environ Health Res.

    (1991)
  • M. Chase-Topping et al.

    Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157

    Nat. Rev. Microbiol.

    (2008)
  • J.M. Colford et al.

    Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination

    Epidemiology

    (2007)
  • R. Collins et al.

    Attenuation of effluent-derived faecal microbes in grass buffer strips

    N. Z. J. Agric. Res.

    (2004)
  • R. Collins et al.

    Overland flow delivery of faecal bacteria to a headwater pastoral stream

    J. Appl. Microbiol.

    (2005)
  • K. Cransberg et al.

    Four cases of hemolytic uremic syndrome–source contaminated swimming water?

    Clin. Nephrol.

    (1996)
  • D. Cunningham et al.

    Best Management Practices for Storing and Applying Poultry Litter

    (2012)
  • C.M. Davies et al.

    Dispersion and transport of Cryptosporidium oocysts from fecal pats under simulated rainfall events

    Appl. Environ. Microbiol.

    (2004)
  • A.P. Dufour et al.

    Water ingestion during swimming activities in a pool: a pilot study

    J. Water Health

    (2006)
  • K.A. Feldman et al.

    A cluster of Escherichia coli O157: nonmotile infections associated with recreational exposure to lake water

    Public Health Rep.

    (2002)
  • C.M. Ferguson et al.

    Field scale quantification of microbial transport from bovine faeces under simulated rainfall events

    J. Water Health

    (2007)
  • C.M. Ferguson et al.

    Quantification of microbial sources in drinking-water catchments

    Crit. Rev. Environ. Sci. Technol.

    (2009)
  • C. Fulhage et al.

    Swine Manune Management Systems in Missouri

    (2001)
  • Gaskin, J., Harris, G., Franzluebbers, A., Andrae, J. (2007), University of Georgia, Cooperative Extension Bulletin...
  • A.K. Guber et al.

    Rainfall-induced release of fecal coliforms and other manure constituents: comparison and modeling

    Appl. Environ. Microb.

    (2006)
  • A.K. Guber et al.

    Comparison of release and transport of manure-borne Escherichia coli and enterococci under grass buffer conditions

    Lett. Appl. Microbiol.

    (2007)
  • A.K. Guber et al.

    Uncertainty in modelling of faecal coliform overland transport associated with manure application in Maryland

    Hydrol. Process

    (2011)
  • C.N. Haas et al.
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