One of the greatest risks to food safety for the fresh produce industry are zoonotic agents shed into livestock manures. In plain language, zoonotic agents are bacteria, viruses and other infectious agents that are carried without apparent symptoms in animals, but which cause illness in humans. Common examples of zoonotic agents in the UK are Salmonella and Campylobacter from poultry, and E. coli O157 from cattle. When livestock and wildlife are infected with a zoonotic agent, their manures will contain human infectious pathogens. Contaminated manure is the primary route for the release of zoonotic agents into an environment. Once the environment is contaminated, there are a number of ways the infectious agent cans spread. Rainfall can wash the zoonotic agents into watercourses; insects such as filth flies can land on the manure, pick up infectious agents 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 agents 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 here.
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 agents, a considerable proportion do. Work commissioned by the Food Standards Agency in the early 2000s surveyed farms in England, Scotland and Wales to determine prevalence (the percentage of manures containing a zoonotic agent) and the numbers of zoonotic agents in those positive samples has been reported by Hutchison et al., 2004. A summary of these reports relating to the five most common causes of food borne illness in the UK are shown in the Tables 1 and 2 below.
Livestock and waste category |
||||||||
Zoonotic agent |
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% |
C. parvum |
5.4% |
2.8% |
13.5% |
5.2% |
ND |
ND |
29.2% |
0% |
G. 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.
Levels of pathogens (CFU g-1) found in positive livestock waste types |
||||||||||
Zoonotic agent |
|
Cattle |
Pig |
Poultry |
Sheep |
|
||||
|
Fresh |
Stored |
Fresh |
Stored |
Fresh |
Stored |
Fresh |
Stored
|
|
|
E. coli O157 |
A G M n |
2.9×106 1.2×103 2.6×108 107 |
8.6×103 2.6×102 7.5×104 39 |
6.9×104 3.9×103 7.5×105 15 |
4.5×103 1.3×103 1.8×104 9 |
ND |
ND |
1.1×104 7.8×102 4.9×104 5 |
2.5×103 2.5×102 5.0×103 2 |
|
Salmonella |
A G M n |
3.9×104 2.1×103 5.8×105 62 |
1.9×105 2.5×103 7.2×106 43 |
9.6×103 6.0×102 7.8×104 10 |
8.9×102 6.1×102 2.0×103 3 |
5.0×103 2.2×102 2.2×104 12 |
4.7×103 4.0×103 8.0×103 3 |
1.1×103 7.1×102 2.0×103 2 |
5.8×103 5.8×103 5.8×103 1 |
|
Listeria |
A G M n |
1.5×104 1.1×103 4.2×105 241 |
2.2×104 1.1×103 9.8×105 133 |
4.6×104 3.1×103 9.7×105 25 |
1.6×104 6.1×102 1.5×105 11 |
3.2×104 8.3×102 1.9×105 13 |
5.6×102 3.3×102 1.3×103 4 |
4.5×102 2.0×102 1.7×103 7 |
2.1×103 3.0×102 8.1×103 4 |
|
Campylobacter |
A G M n |
7.6×103 3.2×102 1.5×105 104 |
1.1×104 5.3×102 1.5×105 42 |
1.9×103 3.1×102 1.5×104 17 |
2.6×104 1.6×103 1.0×105 6 |
4.2×103 2.6×102 2.9×104 13 |
6.4×102 5.9×102 8.7×102 2 |
8.6×102 ( 3.9×102 2.1×103 5 |
1.0×102 1.0×102 1.0×102 1 |
|
C. parvum |
A G M n |
2.7×102 1.9×101 3.5×103 44 |
6.6×101 1.0×101 4.8×102 12 |
3.0×102 5.8×101 3.6×103 17 |
1.4×102 3.3×101 3.1×102 3 |
ND |
ND |
5.3×101 1.0×101 2.5×102 7 |
—
0 |
|
G. intestinalis |
A G M n |
2.2×102 1.0×101 5.0×103 29 |
5.9×100 3 3.6×101 11 |
5.3×104 6.8×101 1.6×105 3 |
1.2×101 1.2×101 1.2×101 1 |
ND |
ND |
3.8×102 2.0×101 1.2×103 5 |
—
0 |
Table 2 A summary of the levels of zoonotic pathogens observed in British livestock manures containing zoonotic agents. Data shown are calculated as both arithmetic (A) and geometric (G) means for positive isolations only. Highest levels observed for each pathogen and manure type are also shown (M). The number of positive isolations used to calculate each mean is shown (n). ND = Not determined. Additional information on the difference between an arithmetic and a geometric mean is available within the total aerobic counts section here.
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 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 3 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 3 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.
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 NB: study used artificially contaminated material 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 |
Badger |
Mycobacterium bovis | Chambers 2009 |
Gulls | Salmonella | Simpson 2008 |
Otter | Brucella | Simpson 2008 |
Rabbits | E. coli O157 | Simpson 2008 |
Table 3 A small selection of the zoonotic agents that can be shed by wildlife in the UK
References (click a reference to read it (where it's available); some require purchase from the publisher)
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.