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Microbial pollution of water by livestock: approaches to risk assessment and mitigation

Published online by Cambridge University Press:  01 May 2009

A. J. A. Vinten ,
J. Potts ,
L. Avery  and
N. J. C. Strachan
A. J. A. Vinten*
Affiliation:
Catchment Management Group, Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
J. Potts
Affiliation:
BioSS, Craigiebuckler, Aberdeen AB15 8QH, UK
L. Avery
Affiliation:
Catchment Management Group, Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
N. J. C. Strachan
Affiliation:
Aberdeen University, School of Biological Sciences, Aberdeen AB24 2TZ, UK
*
E-mail: a.vinten@macaulay.ac.uk
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Abstract

In this study, we investigate the extent to which the incidence of Escherichia coli O157:H7 can be predicted in human faeces, from human intake and infection via water contaminated by livestock and carrying this zoonotic pathogen in North-East (NE) and South-West (SW) regions of Scotland. In SW Scotland, there is a risk of coastal recreational waters failing EU standards for faecal indicator organisms, and this is assumed to be the main potential waterborne route of infection. In NE Scotland, the main waterborne route is assumed to be the many private drinking water supplies; these are mainly derived from shallow groundwater and surveys show that there is potential for significant levels of microbial contamination from livestock. The risk to human health from these sources has been assessed using a combination of process models, epidemiological risk-assessment methods and survey data. A key assumption in the calculations is the amount of mixing of pathogenic and non-pathogenic E. coli between animal faecal sources and contaminated water intake by humans. Using the probability distributions of the E. coli O157 content of individual faecal pat material (which would imply no mixing between source and human intake), based on three recent surveys of animal faeces in Scotland, led to predicted annual risks of infection slightly higher than observed human infection incidence. Using the geometric mean to represent partial mixing (which theoretically may over- or underestimate incidence with a concave dose–response curve) gave infection rates similar to those observed for two of the three faecal surveys. Using the arithmetic mean led to over-prediction of risk. This is to be expected if the true dose–response curve is (such as the Beta-Poisson curve used here) concave. Other factors that may lead to over-prediction of incidence are discussed, including under-reporting, loss of infectivity as a result of environmental exposure, immunity and the appropriateness of the Beta-Poisson curve. It is concluded that better epidemiological data for calibration of the dose–response curve, better knowledge of the degree of mixing and understanding of immunity are key requirements for progress in process model-based predictions of infection rate. The paper also explores the potential of improved farm and catchment scale management to deliver cost-effective mitigation of pollution of bathing and drinking water by livestock zoonoses.

Keywords

E. coliriskwaterlivestock zoonosesmitigation
Type
Full Paper
Information
animal , Volume 3 , Issue 5 , May 2009 , pp. 744 - 752
Copyright
Copyright © The Animal Consortium 2009

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References

Aitken, MN, Merrilees, DW, Duncan, A 2001. Impact of agricultural practices and catchment characteristics on Ayrshire bathing waters. Retrieved November 28, 2006, from http://www.scotland.gov.uk/cru/kd01/green/bathing-00.htmGoogle Scholar
Chase-Topping, ME, McKendrick, IJ, Pearce, MC, MacDonald, P, Matthews, L, Halliday, J, Allison, L, Fenlon, D, Low, JC, Gunn, G, Woolhouse, MEJ 2007. Risk factors for the presence of high-level shedders of Escherichia coli O157 on Scottish farms. Journal of Clinical Microbiology 45, 1594–1603.CrossRefGoogle ScholarPubMed
Coleman, ME, Marks, HM 2000. Mechanistic modelling of Salmonellosis. Quantitative Microbiology 2, 227–247.CrossRefGoogle Scholar
Crowther, J, Kay, D, Wyer, MD 2002. Faecal indicator concentrations in waters draining lowland catchments in the UK: relationships with land use and farming practices. Water Research 36, 1725–1734.CrossRefGoogle ScholarPubMed
Crump, KS 1998. On summarizing group exposures in risk assessment: is an arithmetic mean or a geometric mean more appropriate? Risk Analysis 18, 293–297.CrossRefGoogle ScholarPubMed
Curriero, FC, Patz, JA, Rose, JB, Lele, S 2001. The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994. American Journal of Public Health 91, 1194–1199.CrossRefGoogle ScholarPubMed
Cuttle, SP, Macleod, CJA, Chadwick, DR, Scholefield, D, Haygarth, PM, Newell-Price, P, Harris, D, Shepherd, MA, Chambers, BJ, Humphrey, R 2007. An inventory of methods to control diffuse water pollution from agriculture (DWPA). Defra Project ES0203. Retrieved June 18, 2007, from: http://www.defra.gov.uk/farm/environment/water/csf/pdf/UserManual_Jan07.pdfGoogle Scholar
Dickson, JW, Edwards, T, Jeffrey, WA, Merrilees, D, Kay, D 2005. Catchment scale appraisal of best management practices (BMPs) for the improvement of bathing water – Brighouse Bay – March 2005. Report for Scottish Environment Protection Agency (SEPA), reference 230/4187. Retrieved May 25, 2005, from http://www.scotland.gov.uk/Resource/Doc/1057/0012161.pdfGoogle Scholar
European Centre for Disease Prevention and Control 2007. Annual epidemiological report on communicable diseases in Europe. Retrieved June 7, 2007, from http://ecdc.europa.eu/pdf/ECDC_epi_report_2007.pdfGoogle Scholar
Frost, FJ, Roberts, M, Kunde, TR, Craun, G, Tollestrup, K, Harter, L, Muller, T 2005. How clean must our drinking water be: the importance of protective immunity. Journal of Infectious Diseases 191, 809–814.CrossRefGoogle ScholarPubMed
Haas, CN, Thayyar-Madabusi, A, Rose, JB, Gerba, CP 2000. Development of a dose–response relationship for Escherichia coli O157:H7. International Journal of Food Microbiology 56, 153–159.CrossRefGoogle ScholarPubMed
Halliday, JEB, Chase-Topping, ME, Pearce, MC, McKendrick, IJ, Allison, L, Fenlon, D, Low, C, Mellor, DJ, Gunn, GJ, Woolhouse, EJ 2006. Herd-level risk factors associated with the presence of phage type 21/28 E. coli O157 on Scottish cattle farms. BMC Microbiology 6, 9910.1186/1471-2180-6-99.CrossRefGoogle ScholarPubMed
Hutchison, M, Walters, LD, Avery, JM, Synge, BA, Moore, A 2004. Levels of zoonotic agents in British livestock manures. Letters in Applied Microbiology 39, 207–214.CrossRefGoogle ScholarPubMed
Hutchison, ML, Walters, LD, Avery, JM, Munro, F, Moore, A 2005. Analyses of livestock production, waste storage, and pathogen levels and prevalences in farm manures. Applied and Environmental Microbiology 71, 1231–1236.CrossRefGoogle ScholarPubMed
Ihekweazu, C, Barlow, M, Roberts, S, Christensen, H, Guttridge, B, Lewis, D, Painter, S 2006. Outbreak of E. coli O157 infection in the south west of the UK: risks from streams crossing seaside beaches. Eurosurveillance 11, 128–130.CrossRefGoogle ScholarPubMed
Kay, D, Aitken, M, Crowther, J, Dickson, I, Edwards, AC, Francis, C, Hopkinds, M, Jeffrey, W, Kay, C, McDonald, AT, McDonald, D, Stapleton, CM, Watkins, J, Wilkinson, J, Wyer, MD 2007. Reducing fluxes of faecal indicator compliance parameters to bathing waters from diffuse agricultural sources: the Brighouse Bay study, Scotland. Environmental Pollution 147, 138–149.CrossRefGoogle ScholarPubMed
Larney, FJ, Yanke, JL, Miller, JJ, McAllister, TA 2003. Fate of coliform bacteria in composted beef cattle feedlot manure. Journal of Environmental Quality 32, 1508–1515.CrossRefGoogle ScholarPubMed
Licence, K, Oates, KR, Synge, BA, Reid, TMS 2001. An outbreak of E. coli O157 infection with evidence of spread from animals to man through contamination of a private water supply. Epidemiology and Infection 126, 135–138.CrossRefGoogle Scholar
Mubiru, DN, Coyne, MS, Grove, JH 2000. Mortality of Escherichia coli O157:H7 in two soils with different physical and chemical properties. Journal of Environmental Quality 29, 1821–1825.CrossRefGoogle Scholar
Nicholson, FA, Groves, SJ, Chambers, BJ 2005. Pathogen survival during livestock manure storage and following land application. Bioresource Technology 96, 135–143.CrossRefGoogle ScholarPubMed
Omisakin, F, MacRae, M, Ogden, ID, Strachan, NJC 2003. Concentration and prevalence of Escherichia coli O157 in cattle feces at slaughter. Applied and Environmental Microbiology 69, 2444–2447.CrossRefGoogle ScholarPubMed
Reddy, KR, Khaleel, R, Overcash, MR 1981. Behavior and transport of microbial pathogens and indicator organisms in soils treated with organic wastes. Journal of Environmental Quality 10, 255–266.CrossRefGoogle Scholar
Reid, DC, Edwards, AC, Cooper, D, Wilson, E, McGaw, BA 2003. The quality of drinking water from private water supplies in Aberdeenshire, UK. Water Research 37, 245–254.CrossRefGoogle ScholarPubMed
Reilly, WJ, Browning, LM 2002. Zoonoses in Scotland – food, water or contact? In Waterborne zoonoses: identification causes and control (ed. JA Cotnivo, A Dufour, G Rees, J Bartram, R Carr, DO Oliver, GF Craun, R Fayer and VPJ Gannon), pp. 167–190. IWA Publishing, London, UK.Google Scholar
Roseberry, AM, Burmaster, DE 1992. Lognormal distributions for water intake by children and adults. Risk Analysis 12, 99–104.CrossRefGoogle ScholarPubMed
Scottish Environment Protection Agency (SEPA) 2002. A study of bathing waters compliance with EC Directive 76/160/EEC: the relationship between exceedence of standards and antecedent rainfall. Retrieved May 31, 2002, from http://products.ihs.com/Ohsis-SEO/473575.htmlGoogle Scholar
SEERAD (Scottish Executive Environment and Rural Affairs Department) 2002. Blue-green algae (Cyanobacteria) in inland waters: assessment and control of risks to public health. Extract on exposure guidelines from the WHO Document – Annex G. Guidelines for Safe Recreational-water Environments Draft for Consultation – vol. 1: Coastal and Fresh-waters – October 1998. Retrieved March 28, 2006, from http://www.scottishexecutive.gov.uk/Publications/2002/05/14852/5359Google Scholar
SEERAD 2004. Aerial survey of Scottish beaches, July–September 2003 Environment Group Research Report 2004/04. Retrieved March 15, 2007, from http://www.scotland.gov.uk/Resource/Doc/47237/0014589.pdfGoogle Scholar
SNIFFER (Scotland & Northern Ireland Forum for Environmental Research) 2006. Provision of a screening tool to identify and characterise diffuse pollution pressures: Phase II. Project WFD19 (230/8050). Retrieved May 20, 2007, from http://www.sniffer.org.uk/Resources/WFD19/Layout_Default/0.aspx?backurl=http%3a%2f%2fwww.sniffer.org.uk%3a80%2fproject-search-results.aspx%3fsearchterm%3dWFD19&selectedtab=completedGoogle Scholar
Soderhall, M, Normark, S, Ishikawa, K, Karlsson, K-A, Teneberg, S, Winberg, J, Mollby, R 1997. Induction of protective immunity after Escherichia coli bladder infection in primates. Dependence of the globoside-specific P-fimbrial tip adhesin and its cognate receptor. Journal of Clinical Investigation 100, 364–372.CrossRefGoogle ScholarPubMed
Strachan, NJC, Doyle, T, Kasugac, F, Rotariu, O, Ogden, ID 2005. Dose–response modelling of Escherichia coli O157 incorporating data from foodborne and environmental outbreaks. International Journal of Food Microbiology 103, 35–47.CrossRefGoogle ScholarPubMed
Strachan, NJC, Dunn, GM, Locking, ME, Reid, TMS, Ogden, ID 2006. Escherichia coli O157: burger bug or environmental pathogen? International Journal of Food Microbiology 112, 129–137.CrossRefGoogle ScholarPubMed
Tate, KW, Atwill, ER, Bartolomew, JW, Nader, G 2006. Significant Escherichia coli attenuation by vegetative buffers on annual grasslands. Journal of Environmental Quality 35, 795–805.CrossRefGoogle ScholarPubMed
Teunis, PFM, Ogden, ID, Strachan, NJC 2008. Hierarchical dose response of E. coli O157:H7 from human outbreaks incorporating heterogeneity in exposure. Epidemiology and Infection 136, 761–770.CrossRefGoogle ScholarPubMed
Topp, E, Welsh, M, Tien, Y-C, Dang, A, Lazarovits, G, Conn, K, Zhu, H 2003. Strain-dependent variability in growth and survival of Escherichia coli in agricultural soil. FEMS Microbiology Ecology 44, 303–308.CrossRefGoogle ScholarPubMed
Torres, AG, Zhou, X, Kaper, JB 2005. Adherence of diarrheagenic Escherichia coli strains to epithelial cells. Infection and Immunity 73, 18–29.CrossRefGoogle ScholarPubMed
Vinten, AJA, Lewis, DR, McGechan, M, Duncan, A, Aitken, M, Hill, C, Crawford, C 2004. Predicting the effect of livestock inputs of E. coli on microbiological compliance of bathing waters. Water Research 38, 3215–3224.CrossRefGoogle ScholarPubMed
Vinten, AJA, Sym, G, Avdic, K, Crawford, C, Duncan, A, Merrilees, DW 2008. Faecal indicator pollution from a dairy farm in Ayrshire, Scotland: source apportionment, risk assessment and potential of mitigation measures. Water Research 42, 997–1012.CrossRefGoogle ScholarPubMed