Zoonotic agents from livestock and wildlife in water in temperate climates

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

8.6×10(

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)

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

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.

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.

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.