Contamination of crops with domestic and feral animal faeces

For the purposes of risk assessment, animals can be divided into two categories; wildlife and domesticated.  It is easier to control the hazards associated with domesticated animals because their movements and behaviours are controlled to some extent by humans.  Furthermore, any apparent infections in domesticated livestock are likely to be treated which is not the case with feral animals.

The greatest hazard associated with either wild or domesticated animals is that they are infected with a zoonotic agent (a zoonotic agent is an infection of an animal with Salmonella or E. coli O157 or similar which does not appear to upset the animal in any way; however the same infectious agent causes illness in humans if it is passed on to them).  Animals infected with a zoonotic agent do not show any clinical symptoms and if they defaecate on, or near, crops they can directly or indirectly contaminate these foods causing illness in humans when the contaminated crops are eaten.

In the UK there is a one in three chance overall that manure from cattle, sheep, pigs or chickens will contain either Campylobacter jejuni, E. coli O157, any sort of Salmonella, Cryptosporidium parvum, Listeria monocytogenes or Listeria ivanovii.  Collectively, these five species of microorganisms cause over 70% of non-viral foodborne or waterborne illnesses in the UK.  Thus it is important to ensure that grazing livestock do not gain access to any adjacent fields growing crops destined for human consumption.

Domestic pets such as cats and dogs can also carry enteric human pathogens such as Salmonella without any clinical symptoms (Carter and Quinn, 2000). Dogs can become infected simply by gnawing on an uncooked bone from an infected meat animal.  Some estimates of the asymptomatic carriage of Salmonella in dogs are as high as 43% of all animals (Carter and Quinn, 2000).  Estimates of Salmonella infections for cats are lower at 19% (Carter and Quinn, 2000).  The vectors of infection for cats and dogs are summarised in figure 1 below.

Figure 1  Vectors of direct infection and factors which moderate infection severity in cats and dogs (adapted from Carter and Quinn, 2000)

It is also important to recognise that cross infection routinely and commonly occurs between wildlife and domestic animals. A recent study on a British farm trapped and tested a variety of wildlife and domesticated livestock and pets for Salmonella.  The purpose of the study was to determine how Salmonella spreads through the animals in an environment and becomes chronically established in a particular area (Liebana et al, 2003).  Sophisticated genetic fingerprinting of the Salmonella isolates was used to unequivocally determine identical Salmonella strains. The results showed that mice, rats, arthropods (which includes woodlice, spiders and other 'creepy crawlies'), beetles, flies and foxes all harboured identical strains of Salmonella that were also found in domesticated poultry.  However, the order of infection from animal to animal was not clearly determined.

In comparison to domestic livestock, comparatively little is known about the prevalence and numbers of zoonotic agents present in manure from wildlife.  A comprehensive review has however been published by Simpson (2008).   A brief, and by no means complete, summary of what common indigenous British wildlife are known to harbour is shown in Table 1 below.  There are known examples of the same zoonotic agent being present on fresh produce, in irrigation water and in wildlife (but its rarely clear if the water or crop infected the wildlife or vice versa).  Table 1 attempts to include infectious agents and wildlife that may not have been previously considered by growers as credible threats to the microbiological quality of their crops.

Table 1  A small selection of the zoonotic agents that can be shed by wildlife in the UK 

Animal

 Zoonotic Agent

Reference

Deer Salmonella Fletcher et al., 1997
Bats Lyssavirus (rabies) Johnson et al, 2003
Earthworms E. coli O157 Williams et al., 2006
Crows Campylobacter Simpson, 2008
Ticks Bartonella Guptill, 2010
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

Badger 

Mycobacterium bovis   Chambers, 2009
Gulls Salmonella Simpson, 2008
Otter Brucella Simpson, 2008
Rabbits E. coli O157 Simpson, 2008
Beetle Salmonella Liebana et al, 2003

References

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, 482–484

Byzov, B.A., Nechitaylo, T.Y., Bumazhkin, B.K., Kurakov, A.V., Golyshin, P.N. and Zvyagintsev, D.G. (2009) Culturable microorganisms from the earthworm digestive tract. Microbiology 78, 360-368.

Carter, M. E and Quinn, P. J. 2000.  Salmonella infections in dogs and cats.  In Salmonella in domestic animals.  Edited by Wray, C. and Wray, A, CABI publishing Wallingford Oxon UK.  ISBN 0 85199 261 7.

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 (reference is not available electronically)

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

Liebana, E., Garcia-Migura, L., Clouting, C., Clifton-Hadley, F. A., Breslin, M. and Davies, R. H. 2003.  Molecular fingerprinting evidence of the contribution of wildlife vectors in the maintenance of Salmonella Enteritidis infection in layer farms.  J. Appl. Microbiol. 94, 1024–1029.

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

Philipp, R, Waitkins, S, Caul, O, Roome, A, McMahon, S, Enticott, R. Leptospiral and hepatitis A antibodies amongst windsurfers and waterskiers in Bristol city docks. Public Health, 103, 123–9.

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

Williams,A.P., Roberts,P., Avery,L.M., Killham,K. and Jones,D.L. (2006) Earthworms as vectors of Escherichia coliO157:H7 in soil and vermicomposts. FEMS Microbiology Ecology 58, 54-64.