The main food-borne pathogens causing the majority of food-borne diseases in humans in modern times, e.g. Salmonella, Campylobacter,E. coli O157, originate from healthy farm animals that excrete them faecally.
These pathogens enter the food chain by a variety of routes (e.g.
guts–environment–contaminated animal coats–carcass–meat) and their control during the post-farm phase is neither easy nor always efficient.
Therefore, it is important to understand their spread, and to consider any related controls, of these pathogens on farms. This could minimize further transference of food safety hazards to subsequent phases of the food chain.
The significance of the on-farm presence of food-borne pathogens can be illustrated by data on the occurrence of E. coli O157 in healthy cattle: herd prevalence is highly variable and can be anything between 40% and 75%, whilst prevalence in individual animals may be between <1% and >20%.
The main route of transmission for food-borne pathogens in farm animals is faecal–oral.
Role of animal diet/feeds
Contaminated feed can be a very important source of food-borne pathogens, e.g. Salmonella spp., particularly in poultry and pigs. Usually, the most persistent contaminants are ‘local’ Salmonella spp., whilst ‘exotic’
Salmonella spp. are often transient and associated with imported feed compounds or components (e.g. protein-based). Feeds can also be contaminated with pathogens excreted by vermin (rodents, birds).
Therefore, feeds are sometimes fermented, e.g. liquid feeds for pigs in order to reduce the risk of Salmonellainfection. Feeds can also be acidified by the addition of acidulants, or heat treated to reduce or eliminate pathogens. In fermented silage production, rapid fermentation by dominant lactic acid bacteria and suppression of food-borne pathogens is required. It is a two-step process, starting with aerobic fermentation, which consumes available oxygen and produces heat, followed by anaerobic fermentation and accumulation of lactic acid that lowers pH. If air is not properly (or rapidly) excluded, poor-quality silage can result, in which some pathogens such as Listeria monocytogenescan proliferate and be spread to animals.
Also, numerous studies have been published in which effects of the diet type on shedding of pathogens were examined, e.g. the ongoing debate about whether shedding of E. coli O157 is greater in grain-fed or hay-fed cattle. However, because faecal shedding of this or other pathogens is affected by numerous factors other than diet, but acting simultaneously, the actual relevance of diet itself is presently unclear. On the other hand, it
had been advocated in the past that the total amount of faeces – and hence the prevalence or levels of food-borne pathogens excreted by animals – could be reduced by total withdrawal of feed for 1–2 days before slaughter.
However, some studies have shown that feed withdrawal can actually increase shedding of pathogens, e.g. E. coliO157 in cattle.
With respect to animal diet-based control measures to reduce faecal shedding of pathogens on farms, two approaches have attracted significant attention:
● use of probiotics, which involves feeding animals viable pre-selected microorganisms (usually, lactic acid bacteria) to suppress targeted pathogen(s) within the animal gut either through changing the gut environmental factors or via production of antimicrobial compounds (e.g. bacteriocins); and
● use of competitive exclusion, which involves feeding animals with complex mixtures of bacteria that ‘saturate’ locations on the gut mucosa needed for attachment of pathogens, hence preventing/
reducing colonization of the animal gut by the pathogens. For example, Salmonella spp. can be competitively excluded in intensively reared chicks by feeding them with diluted minced gut content of mature hens (anaerobically fermented gut contents).
Unfortunately, both approaches suppress faecal shedding of pathogens in monogastric animals (poultry and pigs) better than in ruminants. In ruminants, it is more difficult to change gut microflora via these oral treatments, due to physiological/microbiological processes occurring in the rumen. Nevertheless, attempts have been made to overcome such difficulties by application of the treatments via rumen-resistant boluses.
Role of stress
The gut microflora of animals start to establish from birth and, once stable and well-balanced, provide good protection against gut colonization by pathogens, e.g. Salmonella spp. However, stress (alone or in combination with antibiotic therapy) can disturb the balance of the microflora and render animals more susceptible to colonization. Therefore, it could be assumed that stress can cause an increase in shedding of pathogens.
Stressors include parturition (e.g. calving/farrowing), weaning, sudden changes in diet that alter gut pH and select for particular bacteria, transportation (stress increases with journey length, unloading and reloading) and mixing of animals (on-farm and also at markets, lairage).
Effect of animal age
In some on-farm studies of E. coli O157, gut colonization was more frequent in young cattle. Experimentally infected calves can shed around
1 log higher levels, and also for around 3 months longer, than can adult cattle. Also, it is considered that the biggest reservoir of Salmonella spp. is growers and finishers, but younger animals are more likely to be affected.
Spread between animals
It is generally believed that indoor farming (i.e. group housing) increases horizontal transmission of pathogens, as compared to outdoor farming, due to closer contacts between animals (including social contact such as licking/grooming) and/or between animals and the contaminated environment. For example, oral secretions and regurgitation of organisms in cattle contribute to the spread of E. coli O157 between neighbouring animals and even between neighbouring pens. Vertical transmission can also occur, but is probably less important due to some protection from maternal antibodies for up to 7 weeks. In addition, introduction of novel shedding-positive animals to established groups increases on-farm spread of pathogens.
Role of vectors
Spread can occur between distant pens or indeed between farms via vermin, wild animals, farm staff and farm equipment. Humans, through their daily activities on-farm, are one of the biggest causes of on-farm spread of pathogens. Rodents (mice and rats) are also very important; a Salmonella-shedding mouse can excrete up to 5–7 logs of the pathogen’s cells in its faeces in one day, which can be sufficient to infect an animal.
Some studies found 1–3% of gulls from intertidal sediments harboured E.
coliO157. A study carried out in the USA showed that E. coli O157 can be isolated from deer sharing grazing land with cattle.
Survival in the environment
Pathogens can survive for long periods in farm environment-related substrates such as soil, faeces and building materials for extended periods (days to weeks). Pathogens can be attached to dust particles and liquid droplets, and then carried by winds or aerosols (hosing, rain) for considerable distances. Generally, pathogens die off to a large extent when exposed to a combination of higher temperatures and drying, but at lower temperatures and in water (or damp substrates) they survive very well. All water drinkers used by more than one animal can serve as a route for between-animal spread. Water troughs are clearly proven as a source of E. coliO157 infections and re-infections on farms; the pathogen survives in the water for several months and can even multiply in the sediment. This means that the pathogen can survive between two grazing seasons (e.g. over winter).
Recycling of pathogens via organic fertilizers
Animal wastes, such as farmyard manure, slurry and certain abattoir wastes (lairage wastes and gut contents; see Chapter 2.4) often contain food-borne pathogens faecally shed by farm animals. Animal wastes in solid (manure) and liquid (slurry) form can be stored on the farm, transported for use elsewhere, or deposited directly onto land. Storage can reduce levels of pathogens; e.g. appropriate storage of farmyard manure can lead to their
‘auto-heating’ (composting) to pasteurization temperatures (e.g. >60°C), that can destroy vegetative forms of pathogens. Spreading untreated wastes on pasture or agricultural land for crop production can mediate further infections or re-infections of animals with pathogens through either grazing, or feeding contaminated feeds produced on contaminated land. Survival periods of pathogens in soil are variable and affected by numerous factors, but some studies indicate survival periods of >2 years forSalmonellaspp. and around 10 months for L. monocytogenes. Pathogens’
survival is better if the organic wastes are applied on land by the injection method (often used for odour control purposes) than by surface spreading;
in the latter case, pathogens are more intensively exposed to antimicrobial factors, including drying and sunlight.
Summary of existing on-farm control measures
Presently, the main on-farm control measures for pathogens are based on hygiene and biosecurity incorporated in Good Farming Practices/Good Hygiene Practices (GFP/GHP) – and HACCP-based principles:
● operate an all-in, all-out policy;
● disinfect pens between batches of animals;
● avoid mixing animals (new or by age group);
● use a reliable pathogen-free source of livestock;
● disinfect vehicles used for transportation;
● train staff to disinfect boots and equipment, and keep work clothes on site;
● operate an effective programme for control of vermin;
● clean and disinfect water troughs regularly;
● avoid grazing animals on land newly applied with slurry or manure;
ideally store waste for 3 months prior to application onto land;
● restrict access of visitors to units;
● manage feed properly; reliable source, proper production of silage;
● monitor pathogen presence in animals, e.g. ‘ZAP’ Salmonella pro- gramme in the UK; and
● vaccinate animals against pathogens, e.g. Salmonellain poultry.
Future on-farm control measures, that are not being routinely used but are under intensive research and development, include in particular:
(i) vaccinations against a range of pathogens including such as Campylobacter and E. coli O157; and (ii) bacteriophage therapy based on viruses which attack and targeted pathogenic bacteria.
Further Reading
Anon. (2000) Opinion of the Scientific Committee on Veterinary Measures Relating to Human Health on Food-borne zoonoses. European Commission Health and Consumer Protection Directorate-General, Brussels.
Hinton, M.H. (2000) Infections and intoxications associated with animal feed and forage which may represent a hazard to human health. Veterinary Journal159, 124–138.
Johnston, A.M. (2000) HACCP and farm production. In: Brown, M. (ed.) HACCP in the Meat Industry. Woodhead Publishing Ltd, Cambridge, UK.
Maunsell, B. and Bolton, D.J. (2004) Guidelines for Food Safety Management on Farms. Teagasc – The National Food Centre, Dublin.
Stanfield, G. and Dale, P. (2002) Assessment of Risk to food Safety Associated with the Spreading of Animal Manure and Abattoir Wastes on Agricultural Land. Final Report to the Food Standards Agency, Report No. UC6029, London.
2.4 Animal By-products, Wastes and the Environment
Animal by-products and wastes produced by abattoirs have not been well regulated in the past; many of them were frequently applied on agricultural land without any treatment. This practice carries the risk of re- cycling of public health hazards from shedding animals – through the environment – back to grazing animals or those fed by crops harvested from the environment. Additionally, these hazards can contaminate crops grown on the land and intended for human consumption, e.g. root vegetables, salads, etc.
Surveys of abattoir wastes conducted in the UK between 1999 and 2001 indicated that most abattoirs used to discharge effluents and wastes onto agricultural land, either directly or via sub-contraction to secondary companies. Abattoir wastes varied greatly with respect to: (i) types (e.g.
lairage manure-based wastes, gut contents, blood, etc.); (ii) volume stored at the premises (e.g. 1–200 tonnes); (iii) conditions of storage (e.g. in tanks, hips, etc.); and (iv) the length of time they were stored on the premises before being disposed of (e.g. between 1 day and 2 years). These variations were much larger among red meat abattoirs, whilst wastes from poultry abattoirs were more uniform. In the surveys, particularly food-borne protozoan pathogens and, to a lesser extent, bacterial pathogens, were found in abattoir wastes, which confirms the public health relevance of abattoir waste handling.
Subsequently, EU regulation EC 1774/2002 has provided health rules concerning animal by-products not intended for human consumption.
This new legislation divides animal by-products into three categories, described below.
Category 1 by-products
These by-products represent the highest risk category. The main hazard in Category 1 by-products are TSE-BSE agents, so the controls are designed to target particularly specified risk materials (SRM), i.e. to limit their spread. This category includes:
1. By-products from animals:
● infected by TSE;
● killed for TSE eradication;
● other than farmed or wild (pet, zoo, circus);
● including experimental animals;
● including wild animals suspected of harbouring communicable dis- eases; and
● with prohibited chemical residues.
2. Animal material collected in waste water treatment from Category 1 processing plants.
3. Catering waste from international transport. This is considered as high- risk material from a public health perspective, since effective, cross-border controls are non-existent.
4. Mixtures of Category 1 with Category 2 or Category 3 materials.
Disposal of Category 1 by-products
1. Directly incinerated in a registered plant.
2. Processed in a plant using any of methods 1 to 5 (Table 2.5)and then incinerated.
3. If the by-products do not contain SRM, those processed in a plant by method 1 must later be buried in a landfill.
4. Catering waste from international transport is disposed of by burial in a landfill.
Category 2 by-products
These by-products represent a medium risk to public health. The category of manure and digestive tract contents must be treated as if they contain organisms pathogenic to humans. If Category 2 by-products are contaminated with category 1 by-products, then their risk level increases and they must be treated as Category 1 by-products. This category includes:
1. Manure and digestive tract contents.
2. Animal material collected in waste water treatment from Category 2 processing plants, or from abattoirs other than those covered under Category 1.
Table 2.5. Treatment methods for animal by-products.
Material first reduced Treatments Method to particle size (mm) (°C/min)
1a ⱕ50 >133/ⱖ20/ⱖ3 bars
2 ⱕ150 >100/ⱖ125 or
>110/ⱖ120 or
>120/ⱖ50
3 ⱕ30 >100/ⱖ95 or
>110/ⱖ55 or
>120/ⱖ13
4 ⱕ30 >100/ⱖ16 or
>110/ⱖ13 or
>130/ⱖ3
5 ⱕ20 >80/ⱖ120 or
>100/ⱖ60 Other If approved and validated
aMethod 1 is regarded as suitable for destruction of TSE agents. The particle size is a critical part of the processing, since varying particles will conduct heat to differing degrees.
3. Animal products containing residues of veterinary drugs or other contaminants.
4. Animal products other than Category 1, if imported but non-compliant.
5. From animals, other than under Category 1, that died not by slaughter for human consumption.
6. Mixtures of Category 2 and Category 3 materials.
7. Animal by-products other than Category 1 or Category 3.
Disposal of Category 2 by-products
In theory, all Category 2 by-products can be disposed of in the same manner as the higher-risk Category 1 by-products. However, these by-products can be commercially valuable, so may be treated by the following methods.
1. Directly incinerated in a plant.
2. Processed in a plant by any of methods 1 to 5 (Table 2.5).
3. Processed in a plant by method 1 and marked, followed by incineration or, in the case of rendered fats, further processed into organic fertilizers/improvers.
4. Processed in a plant by method 1 and marked, followed by:
● if proteinaceous, used as organic fertilizers/improvers if scientifically justified;
● used as raw material in biogas or compost production; or
● burial in a landfill.
5. Fish material ensiled or composted.
6. Manure, digestive tract contents (separated from the tract), milk and colostrums, if they originate from animals free from communicable diseases, can be disposed of:
● as raw material in biogas or composting plant; or
● by application to land as specified. The legislation specifically states that these wastes may be applied on agricultural land, but not on land used for grazing.
7. Wild animals with no communicable disease can be processed for trophy production in a plant.
Category 3 By-products
Category 3 by-products are the lowest public health risk, and originate from animals with no communicable diseases, which are fit for human con- sumption, or unfit parts if no communicable diseases. This category includes:
1. Hides and skins, hooves and horns, pig bristles and feathers; from the abattoir and from fit animals.
2. Blood from fit, non-ruminant animals; blood, hides and skins, hooves, feathers, wool, horns, hair and fur from animals with no communicable disease from abattoirs.
3. Raw milk and former foodstuffs of animal origin with no health risks;
catering waste other than that covered under Category 1.
4. Fish and sea animals, except mammals from the open sea, for fishmeal.
5. Shells, hatchery by-products and cracked egg by-products from animals with no communicable disease.
Disposal of Category 3 by-products 1. Directly incinerated in a plant.
2. Processed in a plant by any of methods 1 to 5 (Table 2.5) and marked, followed by incineration in a plant.
3. Processed in a Category 3 plant.
4. Transformed into petfood or in a technical plant.
5. Transformed in a biogas or composting plant.
6. Catering waste can be transformed in a biogas plant or composted.
7. Fish origin material ensiled or composted.