In Summary
- Livestock and wildlife pose risks to crops, particularly from transmission of pathogens in their faeces/manure.
- Once ground is contaminated by pathogens in the manure, various routes can then directly contaminate crops (e.g. rainfall run off and splashes, insect transfer of pathogens, wildlife transmission). Between 10-30% of fresh manures contain foodborne pathogens.
- Both wildlife and domestic livestock can be carriers of foodborne disease pathogens.
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% |
|
ND | ND | 29.2% | 0% | |
| Giardia intestinalis | 3.6% | 2.6% | 2.4% |
|
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.
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 |
References
(click a reference to read it (where it is available); some require purchase from the publisher)
Feng, Y.Y. (2010) Cryptosporidium in wild placental mammals. Experiment. Parasitol. 124, 128-137.
Guptill, L. (2010) Bartonellosis. Vet Microbiol 140, 347-59.
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).
Simpson, V. (2008) Wildlife as reservoirs of zoonotic diseases in the UK. In Practice 30, 486-494.