Wildlife

Zoonotic pathogens from livestock and wildlife in water in temperate climates

One of the greatest risks to food safety for the fresh produce industry are zoonotic pathogens shed into livestock manures. In plain language, zoonotic pathogens are bacteria, viruses and other infectious agents that might cause illness in animals but can be passed to humans, where they cause disease.  Sometimes zoonotic agents can be carried without apparent symptoms or discomfort in their host animals. Campylobacters in chickens is a good example of asymptomatic carriage of a zoonotic agent in poultry. Other common examples of zoonotic agents in the UK are Salmonella in poultry, and E. coli O157 in cattle. When livestock and wildlife are infected with a zoonotic pathogen, their manures will contain human infectious pathogens. Contaminated manure is the primary route for the release of zoonotic pathogens into an environment. Once the environment is contaminated, there are a number of ways the infectious pathogen can spread. Rainfall can wash the zoonotic pathogen into watercourses; insects such as filth flies can land on the manure, pick up pathogens on their feet and bodies and transfer them the next place they land; and wildlife living in and around water sources such as rats or some wildfowl can scavenge manures for insect larvae, thereby becoming infected themselves and further transmitting the infection. There are a large number of potential vectors for the transfer of zoonotic pathogens into the food chain. A comprehensive review of the issues for domestic livestock manures in the UK from both intensive (in sheds) and extensive (in fields) farming written in 2000 is available below.

In the UK, around 70 million tonnes of manure is generated from intensively farmed livestock and a similar amount is generated from extensive livestock farming (Hutchison et al., 2000). Although not all manures will contain zoonotic pathogens, around 10-30% of fresh manures contain microorganisms that can infect humans (Table 1). Work commissioned by the Food Standards Agency in the early 2000's surveyed farms in England, Scotland and Wales to determine prevalence (the percentage) of manures containing zoonotic pathogens. The numbers of zoonotic pathogens in those positive samples has been reported by Hutchison et al., 2004. A summary of these reports relating to five common causes of foodborne illness in the UK are shown in the Tables 1 and 2 below.

  Livestock and waste category              
Zoonotic pathogen Cattle   Pig   Poultry   Sheep  
  Fresh Stored Fresh Stored Fresh Stored Fresh Stored
E. coli O157 13.2% 9.1% 11.9% 15.5% ND ND 20.8% 22.2%
Salmonella 7.7% 10.0% 7.9% 5.2% 17.9% 11.5% 8.3% 11.1%
Listeria 29.8% 31.0% 19.8% 19% 19.4% 15.4% 29.2% 44.4%
Campylobacter 12.8% 9.8% 13.5% 10.3% 19.4% 7.7% 20.8% 11.1%
Cryptosporidium parvum 5.4% 2.8% 13.5%

5.2%

ND ND 29.2% 0%
Giardia intestinalis 3.6% 2.6% 2.4%

1.7%

ND ND 20.8% 0%

Table 1 The percentages of GB domestic livestock wastes that tested positive for each of the zoonotic agents listed. ND = not determined.

Table 1 The percentages of GB domestic livestock wastes that tested positive for each of the zoonotic agents listed. ND = not determined.

In comparison to domestic livestock, comparatively little is known about the prevalence and numbers of zoonotic pathogens present in manure from wildlife. A comprehensive review has been published by Simpson (2008). A brief, and by no means complete, summary of what common indigenous British wildlife are known to harbour zoonotic pathogens is shown in Table 2 below. There are known examples of the same zoonotic pathogen being present on fresh produce, in irrigation water and in wildlife (but it is rarely clear if the water or crop infected the wildlife or vice versa). Table 2 attempts to include pathogens and wildlife that may not have been previously considered by growers as credible threats to the microbiological quality of their crops.

  Livestock and waste category  
Animal Zoonotic Agent Reference
Deer Salmonella Fletcher et al., 1997
Deer Mycobacterium bovis Fletcher et al., 1997
Deer E. coli O157:H7 Laidler et al., 2013; García-Sánchez et al., 2007
Reindeer Bacillus anthracis Carlson et., 2019
Bats Lyssavirus (rabies) Johnson et al, 2003
Earthworms E. coli O157 Williams et al., 2006
NB: study used artificially contaminated manure because no naturally infected livestock wastes were available
Crows Campylobacter Simpson 2008
Ticks Bartonella Guptill, 2010
Unknown water-borne organism Hepatitis A Philipp et al., 1989
Pheasant Newcastle virus Aldous et al., 2007
Voles Cowpox Simpson 2008
Rats Leptospirosis Cutler et al., 2010
Weasels Mycobacterium avium paratuberculosis Stevenson et al., 2009
Geese Cryptosporidium parvum Wells et al 2019
Badgers Mycobacterium bovis Chambers 2009
Goats Bacillus anthracis Carlson et al., 2019
Goats Mycobacterium avium paratuberculosis Barkema et al., 2010
Hedgehogs Listeria monocytogenes Hydeskov et al., 2019
Sheep Bacillus anthracis Carlson et al., 2019
Sheep Listeria monocytogenes Hutchison et al., 2004
Gulls Salmonella Simpson 2008
Otters Brucella Simpson 2008
Rabbits E. coli O157 Simpson 2008
Cattle Bacillus anthracis Carlson et al., 2019
Cattle Mycobacterium bovis Reis et al., 2020
Cattle Cryptosporidium parvum Wells et al 2019
Pigs Bacillus anthracis Carlson et al., 2019
Pigs Salmonella Hutchison et al., 2004
Beavers Giardia intestinalis Horton et al., 2019
Table 2 A selection of the zoonotic pathogens that can colonise animals in the UK

References 

(click a reference to read it (where it is available); some require purchase from the publisher) 

Aldous, E.W, Manvell, R.J, Cox W.J, Ceeraz, V, Harwood, D.G, Shell, W, et al. (2007) Outbreak of Newcastle disease in pheasants (Phasianus colchicus) in south-east England in July 2005. Vet Rec. 160, 482–4.

Barkema, H.W., Hesselink, J.W., McKenna, S.L.B., Benedictus, G. and Groenendaal, H. (2010) Global Prevalence and Economics of Infection with Mycobacterium avium subsp paratuberculosis in Ruminants. Wallingford: Cabi Publishing-C a B Int.

Carlson, C.J., Kracalik, I.T., Ross, N. et al. (2019) The global distribution of Bacillus anthracis and associated anthrax risk to humans, livestock and wildlife. Nat Microbiol 4, 1337–1343.

Chambers, M.,A. (2009) Review of the diagnosis and study of Tuberculosis in non-bovine wildlife species using immunological methods Transboundry and Emerging Dis. 56,215-227.

Cutler, S.J., Fooks, A.R., and van der Poel W.,H.,M. (2010) Public Health Threat of New, Reemerging, and Neglected Zoonoses in the Industrialized World. Emerging Infectious Dis. 16, 1.

Feng, Y.Y. (2010) Cryptosporidium in wild placental mammals. Experiment. Parasitol. 124, 128-137.

Fletcher,T.J. (1997) European perspectives on the public health risks posed by farmed game mammals. Revue Scientifique et Technique de l Office International des Epizooties 16, 571-578.

García-Sánchez, A., Sánchez, S., Rubio, R., Pereira, G., Alonso, J.M., Hermoso de Mendoza, J. and Rey, J. (2007) Presence of Shiga toxin-producing E. coli O157:H7 in a survey of wild artiodactyls. Veterinary Microbiology 121, 373-377.

Guptill, L. (2010) Bartonellosis. Vet Microbiol 140, 347-59.

Horton, B., Bridle, H., Alexander, C.L. and Katzer, F. (2019) Giardia duodenalis in the UK: current knowledge of risk factors and public health implications. Parasitology 146, 413-424.

Hutchison, M.L., Nicholson,F.A., Smith, K.A., Keevil,C.W., Chambers,B.J, and Moore,A. (2000). A study on farm manure applications to agricultural land and an assessment of the risks of pathgen transfer into the food chain. MAFF London (2002).

Hutchison,M.L., Walters,L.D., Avery,S.M., Synge,B.A. and Moore,A. (2004) Levels of zoonotic agents in British livestock manures. Letters in Applied Microbiology 39, 207-214.

Hutchison,M.L., Walters,L.D., Moore,T., Thomas,D.J.I. and Avery,S.M. (2005) Fate of pathogens present in livestock wastes spread onto fescue plots. Applied and Environmental Microbiology 71, 691-696.

Hydeskov, H.B., Amar, C.F.L., Fernandez, J.R.R., John, S.K., Macgregor, S.K., Cunningham, A.A. and Lawson, B. (2019) Listeria monocytogenes infection of free-living Western European hedgehogs (Erinaceaus europaeus). J Zoo Wildl Med 50, 183-189.

Johnson C.N., Selden, D., Parsons, G., Healy, D., Brookes, S.M., McElhinney, L.M., Hutson, A.M., and Fooks, A.R. (2003) Isolation of a European bat lyssavirus type 2 from a Daubenton's bat in the United Kingdom. Vet. Rec. 152, 383-387.

Laidler, M.R., Tourdjman, M., Buser, G.L., Hostetler, T., Repp, K.K., Leman, R., Samadpour, M. and Keene, W.E. (2013) Escherichia coli O157:H7 Infections Associated With Consumption of Locally Grown Strawberries Contaminated by Deer. Clinical Infectious Diseases 57, 1129-1134.

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Reis, A.C., Ramos, B., Pereira, A.C. and Cunha, M.V. (2020) Global trends of epidemiological research in livestock tuberculosis for the last four decades. Transbound Emerg Dis, 14.

Simpson, V. (2008) Wildlife as reservoirs of zoonotic diseases in the UK. In Practice 30, 486-494.

Stevenson,K., Alvarez,J., Bakker,D., Biet,F., de Juan, L., Denham, S., et al. (2009) Occurrence of Mycobacterium avium subspecies paratuberculosis across host species and European countries with evidence for transmission between wildlife and domestic ruminants BMC Microbiology 9, Article No.212.

Wells, B., Paton, C., Bacchetti, R., Shaw, H., Stewart, W., Plowman, J., Katzer, F. and Innes, E.A. (2019) Cryptosporidium Prevalence in Calves and Geese Co-Grazing on Four Livestock Farms Surrounding Two Reservoirs Supplying Public Water to Mainland Orkney, Scotland. Microorganisms 7, 11.

Williams,A.P., Roberts,P., Avery,L.M., Killham,K. and Jones,D.L. (2006) Earthworms as vectors of Escherichia coli O157:H7 in soil and vermicomposts. FEMS Microbiology Ecology 58, 54-64.