Food safety and animal production systems: controlling zoonoses at

Rev. sci. tech. Off. int. Epiz., 2004, 23 (2), 685-700

Food safety and animal production systems:controlling zoonoses at farm level

J.D. Collins (1) & P.G. Wall (2)

(1) Department of Large Animal Clinical Studies, Faculty of Veterinary Medicine, University College Dublin,National University of Ireland, Belfield Campus, Dublin 4, Ireland(2) Centre for Food Safety, University College Dublin, National University of Ireland, Belfield Campus, Dublin 4, Ireland

SummaryControlling zoonotic agents in animal and poultry reservoirs has the effect ofreducing the challenge to food safety management systems in processing andfurther along the food chain. Producing and maintaining healthy stock requiresgood husbandry practices, which include stock selection and veterinaryattention. Feed is a key input, both as a source of pathogen-free nutrients and asa balanced diet to maintain healthy livestock. Safe water, appropriate vermin andwildlife control and an optimum environment to reduce stress are important ifanimals are to perform. Farms are not sterile environments and initiatives toreduce the zoonotic hazards have to be practical, economically feasible andflexible, depending on the scale of the enterprise, the species being farmed, andthe epidemiology of the zoonotic agents in the particular geographical region.Education of farmers and stockmen is crucial to successful on-farm control ofzoonoses, as an understanding of why control measures are necessary, and howthey can be applied, will improve compliance with protocols and procedures.This understanding is a first step towards the implementation of a longitudinalintegrated food safety assurance approach to zoonosis control in the pre-harvest phase of the food chain.

KeywordsBiosecurity – Epidemiology – Food safety – Herd health – Preventive medicine – Zoonosis control.

IntroductionEnsuring that food is safe from the hazard of zoonoticagents requires controls along the entire continuum fromfarm to fork. To reduce the challenge to food safetymanagement systems further along the food chain, it isimportant that everything that is reasonable, practical andeconomically feasible is achieved on the farm, in the pre-harvest phases. The on-going risk has to behighlighted for management at all stages and any residualrisk communicated to the final consumer.

The health of food animals is inextricably linked to theproduction of safe food and the health of humans.Increasing stocking density, associated with the drive forthe economies of scale required to maintain commercialviability in an increasingly competitive global food market,presents the opportunity for build up, and transmission, of

infectious agents. Furthermore, global distribution ofanimal feed permits the dissemination of pathogens togeographical areas, individual farms and susceptiblelivestock that were previously unexposed. In addition,livestock moving between farms and between countriesfacilitates transmission of disease. This is oftencompounded by the stress associated with the transportand the mixing of strange groups of animals.

A series of problems in the food industry, culminating inbovine spongiform encephalopathy, has focused thespotlight on practices in feed mills and farms. The Public Health consequences of failure of controls andinappropriate practices at this level emphasise the fact thatfarming and milling are food businesses and are just asmuch an integral part of the food chain as caterers, retailers

or manufacturers (9). The major retailers andmanufacturers are fully aware that their brands andreputations can be irreparably damaged by being linked tofood-related incidents or outbreaks or even from beingassociated with a food scare that has no resulting adversehuman health effects. Consumers seek safe food of goodquality produced in an environmentally-friendly way withthe highest animal welfare standards possible. Farms arenot sterile environments; however, an expectation thatlivestock will receive safe feed, safe water, optimumhusbandry and veterinary care, that infected wildlife arecontrolled and that there is effective effluent management,is not unreasonable.

There are primary biosecurity measures, based on a riskassessment, that are applicable in different farmingenterprises that will reduce the incidence of most zoonoticagents. However, different enterprises and different countriesrequire additional controls depending on the epidemiologyof the zoonotic agents present in their livestock and in thelocal human populations and the intensity of their farmingoperations. The relative importance of different zoonosesvaries greatly in different regions of the world in terms oftheir impact on public health, animal health and the trade inlivestock, animal feed and human food. The World TradeOrganization Agreement on the Application of Sanitary andPhytosanitary Measures requires that sanitary andphytosanitary measures be scientifically based (42). The keyelements of this agreement are risk analysis, regionalisation,harmonisation, equivalence and transparency. Two of theseelements, namely risk analysis and regionalisation, aredependent on information derived from epidemiologicalsurveillance. This approach provides a basis for the practicalapplication of the so-called ‘precautionary principle’ inregard to the importation of animals and animal products.Increasing globalisation and liberalisation of trade present amajor challenge as rearing environments, breeds of livestock,husbandry practices, animal diets, exposure to disease,approaches to animal welfare, staff training and perceptionsof risk vary greatly between regions. If the goal is enhancedconsumer protection there is little point if one country, orregion, places legal requirements on their farmers for highstandards and the cost of compliance makes them non-competitive and they lose market share to cheaper importswhich may not meet similar exacting standards. The drive bythe major retailers for global food safety standards isencouraging the development of accredited quality assuranceschemes to ensure consistently safe, top quality product nomatter what the country of origin. These schemes are quiteprescriptive regarding the procedures that must be adheredto in the pre-harvest phase and often stipulate requirementsabove those that are mandatory in law.

A sustained supply of safe food products requires goodcommunication between the risk assessors, regulators andfood safety agencies throughout the global village in whichwe now live. A multidisciplinary approach with all the

stakeholders and professionals along the food chainworking in unison will deliver optimum results. It isimportant to have feedback from medical epidemiologistson the disease agents of public health significance.Monitoring trends in human disease, detecting emergingpathogens and identifying food vehicles of infection andother modes of transmission of zoonotic agents are allimportant if interventions on farms are to be efficient and targeted appropriately. Communicating with farmersand millers about the risks and how, and why, those risksshould be managed in a ‘common sense’ and practical wayappropriate to the scale of the enterprise, will improvecompliance.

Food chain issuesAll recent international trade agreements have stressed theimportance of risk analysis and the application,throughout the food chain, of prevention systems based onhazard analysis and critical control point. The risksinvolved are very real when one considers the persistenceof such human parasitic diseases as trichinosis andtaeniasis and bacterial zoonoses such ascampylobacteriosis and salmonellosis, conditions whichare invariably associated with exposure to contaminatedfood. Detection and elimination from the food chain ofmeat derived from visibly diseased animals has beeneffectively accomplished by the traditional meat inspectionprocedures, which date from the mid-1800s. Today,however, the main human health hazards originate withthe carriage, at the time of slaughter, of the causative agentsby clinically healthy animals and poultry. Current methodsof inspection used in the regulatory control of meat andmeat products are limited in their effectiveness in detectingthese hidden food-borne hazards. Therefore, themaintenance of good hygiene practices during processingis the most important factor in consumer protection.

Classifying pig farms on the basis of meat juice enzyme-linked immunosorbent assay screening forsalmonella, as developed in Denmark, demonstrates howmodern technology and feedback from processors to farmsare driving standards up and contributing to a saferproduct. The operation of salmonella-free pig and poultryunits, by reducing the number of pathogens entering thefood chain at the initial production stage, reduces thepathogen load and serves as an example as to howbiosecurity on farms can directly contribute to animprovement in the health status of the consumer of theseproducts. Likewise, the implementation of preventivemeasures promoted by the Department for Environment,Food and Rural Affairs in Great Britain, reduced theprevalence of salmonella in pig and poultry productionunits, but had little effect on the prevalence ofcampylobacter (3). While the results were encouraging, the

Rev. sci. tech. Off. int. Epiz., 23 (2)686

setting at the start, followed by farm inspections and clinical examination of animals, data monitoring andherd/flock problem analysis and prevention. The approachhas to be adapted depending on the species of animalinvolved and the intensity of the farming enterprise (6).These protocols define the farm objectives, which thenprovide the basis for the analysis of production and otherdata, the interpretation of collected information includingputative risk factors for disease occurrence, and thedevelopment and application of preventive procedures andcritical monitoring of the effectiveness, or otherwise, oftheir implementation.

Some infections cause no morbidity in animals (e.g. Escherichia coli O157 and other verocytotoxigenic E. coli [VTEC]) yet can cause serious illness in humans,whereas other diseases such as brucellosis, salmonellosisand leptospirosis are important from both a public healthand animal health standpoint. With the operation ofcontrol and eradication programmes and good hygienepractices in the food chain a further category of zoonoseshas emerged, namely, those involving zoonotic agents thatcan now be regarded as animal production diseases thathave a minimal impact on public health.

Awareness on the part of food animal producers and themeat, poultry and dairy industries that zoonotic hazardsexist is the first step towards their control. It is the primaryproducer who must take all reasonable measures to preventthe entry of pathogenic agents onto his or her holding.They are responsible for the health of their stock and mustadopt a positive approach to animal health on the farm withthe objective of eliminating or minimising exposure offood-producing animals to zoonotic agents. This is anessential component of the longitudinal integrated safetyassurance (LISA) schemes now being adopted in manydeveloped countries. This forms an integral part of foodquality and safety assurance schemes and is a naturaldevelopment of modern farming practice and veterinarypreventive medicine in relation to the production of foodsof animal origin for human consumption. The objectivesare to ensure that the food, as produced on the farm, is bothwholesome and marketable, that the efficiency of theanimal as a food-producing animal is not compromised,and that the animal itself is dealt with in a humane mannerthroughout its life. In addition to mandatory requirements,many supermarket companies now require their suppliersto participate in approved food quality and safety assuranceschemes, components of which include comprehensivespecifications regarding animal health and welfare status.Compliance with recognised norms of animal health andwelfare, therefore, is now a commercial necessity forprimary producers, the demands of which in many casesare greater than those of the regulatory authority.

As a starting point, maintenance of the integrity of the herdor flock as a distinct and self-contained entity, if possible,

Rev. sci. tech. Off. int. Epiz., 23 (2) 687

impact of these measures was not assessed. The studyemphasised the need for on-going surveillance in both theanimal and human populations over time and on a multi-agency basis in order to determine the true value of suchpreventive measures at farm level. Developments inbiotechnology, notably those relating to rapid methods forthe detection of unwanted contaminants, biological orotherwise, provide a new and practical approach to foodsafety assurance based on statistical sampling programmes,internal quality control systems and real-time feedback to farms.

The European Commission White Paper on Food Safety(9) acknowledged the need to ensure that there is ascientific basis for decision making within the food safetyprogramme. Accordingly all the elements of risk analysisare seen to apply to each phase of the food chain, and tothe pre-harvest phase in the first instance. The latter meansthat on-farm quality risk management programmes have tobe developed and implemented (29). The need to ensurethe safety of food of animal origin in respect of thepotential risk posed by the transmissible spongiform encephalopathies (TSEs) of animals hasincreased the importance of sound data on the quality andsafety of animal feedstuffs, the traceability of food animalsand their products and the dynamics of internal trade inanimals in each country and region. The recent move toactive surveillance of TSEs has provided further data on theregional and national incidence of these diseases for use inthe strategic design of control and preventive measuresbased on quantitative risk analysis. This pro-activeapproach serves as a model for the surveillance of zoonoticagents associated with livestock production and has animmediate application in the assessment of the risk posedby a wide range of food-borne agents such as theCampylobacter spp., Toxoplasma spp. and Salmonella spp.

A herd/flock health approach tozoonosis controlFood animal production methods have undergonesubstantial changes over the past fifty years. The rate ofchange has varied from country to country and,worldwide, from region to region, with consequentialdifferences in the nature and quality of the productsproduced under the different regimes in operation in eachregion. Herd health and production managementprogrammes are examples of this development. The mainfocus of these programmes is on-farm economics andespecially operational management through theapplication of veterinary-zootechnical skills and a widerknowledge of the commercial and societal consequences ofdisease in the food-producing animal (30). Key elements insuch a programme include risk assessment and priority


remains a key objective of health control in food animalproduction. To begin with, where stock has to bepurchased, it is essential to ascertain the origin of suchstock so as to define as far as possible the health status ofthe herd of origin and to ensure the traceability of theanimal and its produce as it moves through the food chain.Traceability of all inputs to the farming enterprise, bothgoods and stock, is important because if a farm manager isunaware of the origin of inputs, he/she cannot be assuredthat best practices were adhered to in its production.

Selective pressure associated with the inappropriate use ofantimicrobials can generate multidrug-resistant organismswhich can become a public health problem and which canalso damage consumer confidence when reports of‘superbugs’ and ‘residues in food’ appear in the media. Forexample, multiresistant strains of Salmonella newport andSalmonella typhimurium DT 104 are a cause of majorconcern for both humans and animals. Antibiotics arenecessary to control disease and prevent animal suffering,but they should not be a substitute for good husbandrypractices and should be used prudently under veterinarysupervision. This is all the more relevant to the currentsituation, as it has recently been recognised that the patternof antimicrobial resistance exhibited by enteric isolatesrecovered from pig farmers may mimic that seen in the pigsthey attend to in the course of their work (2). In recentyears in Northern Europe the withdrawal from use ofantimicrobials used in the past for growth promotion hashad no negative consequences for farmers’ profits oranimal health in the case of both pig and broilerproduction. The effect of such withdrawal in thesecountries has been a decrease in antimicrobial resistance inanimals, food products and humans (13, 37, 39).Vaccination can raise herd immunity and reduce the risk ofdisease and the consequent need for antibiotics. Probioticscan have a role in promoting enteric health. Husbandrypractices such as segregating age cohorts, feedingcolostrum, isolating sick animals and adequate disinfectioncan prevent the spread of disease and contribute tomaintaining the health of the herd or flock. Appropriateecto- and endo-parasite control prevent animals becomingdebilitated and more susceptible to other diseases. Policiesfor the use of animal remedies should be science-based andall use should be documented and continuously reviewed.

Operating a quality management system can be easier inlarger enterprises where procedures can be documentedand a more regimented approach adopted. In smallerenterprises much knowledge remains in the heads of thefarm owner or a small number of staff who are engaged ina wide range of activities. If free trade is to be safe trade,governments and farmers’ organisations have to ensure theprovision of training, education and support appropriate tothe scale of the farming enterprise so as to maintainconsistent high-standard output from their farming sector.Confirmation of the disease-free status of recently

purchased animals is best achieved through pre-purchasetesting and segregation before such animals are allowed tojoin the flock/herd. This concept of quarantine is bestcontinued throughout the production system, with personsother than farm personnel directly engaged on the farmbeing allowed only limited access to animals or feedstuffs.

The enforcement of sanitation rules including the use ofdisinfectants at key points and the wearing of protectiveclothing and footwear, together with effective controls onthe hygienic quality of feedstuffs and water sources,including rodent and pest control, are standard biosecuritypractices which are necessary if the integrity of theproduction unit is to be maintained. The practice of an “allin/all out” policy of stock movement together with theearly segregation of all clinically ill animals offer a directmeans of enforcing disease control and prevention at theherd or flock level. The increased volume of animal slurriesproduced on farms and in particular, their disposal, is acause of public health concern since, unlike manure, suchmaterials are not composted and are likely to contain highnumbers of pathogens voided by infected animals (in somecases infected animals may continue to void pathogens forup to one year). The need for care in dealing with animalskept under intensive conditions or in large numbers on thefarm is therefore all the greater, from the public healthviewpoint. This is especially the case in both pig andpoultry production, where the prevalence of infection withsuch agents as salmonellas and campylobacters may beconsiderable, irrespective of the fact that, generally, theextent of clinical disease associated with these infections islow. Furthermore, in the eradication of diseases such asbovine brucellosis, proper effluent control on farms and inmeat plants receiving known infected cases has now beenrecognised as an essential element in preventing the spreadof Brucella abortus onto neighbouring farms. The adoptionof good agricultural practices and the implementation ofpractical minimum guidelines for the management and useof animal effluents provide a suitable environment for theproduction of safe food from healthy animals.

Validation of herd and flock health records and husbandrypractices are now integral parts of contract purchasing onthe part of supermarket chains and is a development whichemphasizes the importance and relevance of the LISA system approach. As an integral component of thefood chain, this provides the foundation for a betterworking relationship between millers, livestock producersand their veterinary and other advisers, in response to thedemands of international as well as local trade.

In 1995 a group of leading public health specialists in theAnimal Production Technical Analysis Group on Risk andHealth Impact in the United States of America (USA)ranked food-borne pathogens according to acute andchronic human health effects in the USA. The top six

priority food-borne agents were adjudged to be: Salmonella spp. (non-typhoid), Campylobacter jejuni/coli,Toxoplasma gondii, E. coli O157:H7, Listeria monocytogenesand jointly, Yersinia enterocolitica and Trichinella spiralis. Ofthese, Listeria is a particularly challenging organism tocontrol as, in addition to being a zoonotic agent, it can beubiquitous in many environments. The entry of animalsinfected or colonised with some of these species into meatplants poses risks for operatives, in addition to the foodsafety risks. More recently, Hensel and Neubauer (19)extended this list to include a number of viral agents andalso considered the effects of recent environmental andindustrial changes that have increased risks associated withmodern on-farm practices.

The protozoan parasite, T. gondii, is a frequent cause ofovine abortion. The sheep is an intermediate host, as arehumans (24). This agent is acquired by the ewe frominfected feral cats through the inhalation or ingestion ofinfective oocysts. Avoidance of undercooked mutton andother meats could reduce human exposure by between30% and 63% (10). The prevention of toxoplasmosis insheep is difficult; vaccines are available which reduceabortion rates, but these do not entirely protect the ewe.

A summary of the effectiveness of on-farm control measuresagainst microbiological hazards that do not necessarilycause clinical disease in animals, but which are associatedwith food animal production, is presented in Table I.

The prevention of contamination of the food product withzoonotic hazards at farm level rather than the‘detection/inspection’ which is intrinsic to theimplementation of food safety control programmes atfactory or ‘post-harvest’ level, is and remains, a primaryobjective. In achieving product protection at the ‘pre-harvest’ level in integrated systems of beef, pig andpoultry production, these principles will already have beenapplied by both the farm manager and the fieldveterinarian. This will have been carried out in the courseof assessing, for example, water and feed quality, animalhealth and performance records, animal welfare, the levelof safety applied in the choice and use of therapeuticagents, and the clinical condition of the food animals, aswell as the safety of the environment as affected by thestandard of animal effluent management and utilisation onthe farm (20). On this basis a reasoned conclusion can bereached concerning the (relative) safety of the food animaland its suitability for slaughter for human consumption.Such information is a basic requirement of LISA-basedprogrammes and for the extended health control of foodsof animal origin, which includes the following elements:

– approval of production holding, water supply andfeedstuffs

– on-farm identification and health examination ofanimals (on-site screening and laboratory support whereapplicable)

– veterinary certification of animal health at the farm gate

– animal transport controls

– in-plant ante-mortem examination

– carcass identification and post-mortem examination (on-site screening and laboratory support where applicable)

– veterinary health certification of carcass and offals

– cold-line/processing/transport/distribution controls.

Further examples of zoonoses that may arise on farms andaffect farming personnel as well as food industryemployees and consumers are presented in Table II.

Food safety and the importanceof appropriate animal transportThe stress of transport suffered by animals, due to, forexample, poor ventilation, noxious odours, uncomfortableconditions, loading density and lack of space, predisposeslatently infected animals to shed large numbers of


Table IFactors affecting the microbial safety of foods of animal origin:the effectiveness of implementing control measures at certainstages in the production process

Control measures *

Salmonella spp. +++ n/a ++ ++

Listeria spp. + ++ + +

Aeromonas spp. ++ n/a n/a ~

Escherichia coli O157:H7 + n/a + +

Campylobacter spp. ++ ~ ++ +

Yersinia + n/a ~ ~

Clostridium spp. ++ + ++ ~

Leptospira serovars ++ ++ ++ ~

Cryptosporidium spp. + n/a + ~

Taenia saginata ++ n/a + n/a

Toxoplasma gondii ++ ~ ~ n/a

Brucella abortus + n/a ++ ++

Mycobacterium bovis + ~ + ++

Enteroviruses + ~ + ~

Mycotoxins ++ + n/a n/a

+ of limited effect ++ partially effective +++ effective~ importance unknown* Other control measures include:– identification of animal/farm of origin/carrier and segregation of clinical cases– identification and approval of casualty/emergency cases for slaughter for humanconsumptionn/a: not applicable – there are no known implications for control

Microbial agents

of concernProviding

safe feed

and water

Increasing

dry matter

content

of silage

Effective

effluent

management

Hygiene

and stress

reduction

during transport


Table IIExamples of the risks associated with zoonotic diseases related to food animal production

Zoonosis Animal source Environmental factors Particular risk Comments

Particular hazards for farming families

Tuberculosis (Mycobacterium bovis) * Cattle, goats, Closed housing, slurry, Raw milk, Care must be taken when spreading manureinfected wildlife equipment clinical cases (land spreading) and caution should be

exercised with tuberculin reactors

Brucellosis (contagious abortion)* Cattle Abortion, cleansings, Abortions, Aerosol spread at abortions and during land calving, slurry, equipment raw milk spreading

LeptspirosisLeptospira icterohaemorrhagiae Cattle Contaminated urine, acute Milking parlour Highly infectious

/jaundiced cases, rodentsLeptospira hardjo Cattle Abortion, cleansings Vaccination available

Salmonellosis * Cattle, sheep, Clinical cases: abortions, Enteric cases, Aerosol spread during land spreading can resultpigs, poultry, enteric disease, abortions, in exposure of personnel and livestockpets, horses febrile conditions raw milk

leading to excretionin slurries

Toxoplasmosis * Sheep, cats Detritus of abortion in Contamination Undercooked mutton is a major source ofewes on land, contaminated of feed infection for pregnant women; exposure to cat droppings from feral cats droppings is a risk for both pregnant women

and children

Chlamydiosis Sheep Abortion Pregnant women should not assist at lambing

Multi-resistant bacteria * Pigs, poultry Survive in slurry Resistant Bacteria are carried over from live animals to pathogens: carcasses and raw foodsplasmid-mediatedresistant strains

Orf Sheep, at and Infected fleece Handling lambs Highly infectious; skin lesions persist, e.g. on armafter lambing during orf

vaccination

Dermatomycosis (ringworm) Cattle, especially Contaminated pens Handling Highly contagious for other personscalves, horses affected calves

Taeniasis (Taenia saginata, Cattle exposed to Leaks from septic tanks are Keeping young stock Cysts that are infectious for humans can be foundthe beef tapeworm)* human excreta a source of ova for cattle near the farm house in the muscles when animals are slaughtered

Hazards for consumers of foods of animal origin

Campylobacteriosis All animals, Readily established Prevalence increases The most common food-borne bacterial disease inespecially poultry in housed populations; during transit Ireland; difficult to control at all stages

usually asymptomatic

Listeriosis Cattle, sheep Present in the environment, Silage-fed cattle; Contaminant of raw dairy products; pregnant on soil, in silage raw milk from women are vulnerable

clinical cases

Verotoxin-producing Escherichia coli Cattle, sheep, Excreted in faeces by See ‘clean cattle Difficult to prevent risk of carcass contaminationpigs asymptomatic animals schedule’ (Fig. 1) at carcass dressing; contaminated raw milk

and vegetables are examples of other sources;acute disease in human patients may result

Other conditions under consideration

Paratuberculosis Cattle, sheep, Persists in soil; Raw milk from Excreted in the milk of a proportion of non-clinicalgoats present in slurry clinical and non- cows; a causal relationship to human Crohn’s

clinical cases in disease has been proposed but not proveninfected herds

Cryptosporidiosis Calves Water, other unknown Contaminated wells Links with human cases are not clearorigins, present in faecesof clinical enteric cases

Anthrax All species Persists in soil Clinical cases Contact with exudated blood

* Also of concern to food processors and consumers of food of animal origin

pathogens. For example, the stress associated with roadtransportation can lead to a ten-fold increase in thenumbers of campylobacters in the alimentary tract ofbroilers by the time they arrive at the poultry meat plant(41). This is likely to result in the contamination of trucksand the general environment of the lairage, as well as theslaughter hall and eventually equipment and the carcassitself. This is the basis for insisting that only animals asclean as practically possible are presented for loading andtransport for slaughter and that all animals, includingpoultry, that are presented in an unclean state for slaughterat meat plants should be rejected on health and safetygrounds. There is also a challenge here for engineers anddesigners of vehicles and other equipment if theconsiderable losses directly attributed to faulty design andoperation are to be avoided. Greater attention must begiven to the sanitation design aspects of such vehicles, asefficient cleaning and disinfection as assessed by directvisual inspection at meat plants, as well as at frontier posts,is now integrated into animal health control systems inmost countries.

Safe unloading and animal handling facilities undersatisfactory lighting conditions are essential at this stage;failure to provide such facilities compromises the efficiencyof safe food assurance programmes, as follows:

– the identity of each animal may not be verifiable

– moribund animals and animals in an advanced stage ofclinical disease and unsuitable for entry into a foodpremises, or which need to be diverted to a sanitaryslaughter facility immediately, cannot be identified

– animals whose hides or skins are grossly contaminatedwith faecal and other material may not be identified andthey will therefore not be immediately rejected asunsuitable for slaughter for human consumption.

The latter condition is exemplified by the concernsexpressed regarding the introduction of large numbers ofVTEC organisms into meat plants by cattle in a grosslycontaminated state. A proportion of these organisms may behuman-pathogenic VTEC (HP-VTEC). Examples of cattlethat are in an acceptable hygienic state and fit for slaughter,and of others that are not, are presented in Figure 1.

Examples of farm-level controlof food-borne zoonoses ofcurrent concernMany biosecurity measures are general and not specific toparticular zoonoses and should be part of good farmingpractice. The authors have selected, as an example, thecontrol of Campylobacter spp., but elements of

campylobacter control can be applied in principle to the prevention of exposure to other zoonotic agents in avariety of animals, particularly those reared under intensive conditions.

On-farm control of Campylobacter spp.Campylobacter spp. of public health concern, notably C. jejuni and C. coli, are widespread in the intestinal tract ofdomestic animals, including food animals and householdpets (1, 38). The prevalence of intestinal colonisation withCampylobacter spp. varies from time to time in any groupof animals and is a function of a number of factors,including the general health of the individual animal andthe risk of exposure to Campylobacter spp. posed by theanimal’s environment (15, 21).

Infection with C. jejuni and C. coli rarely causes clinicaldisease in animals, although a variable proportion ofanimals in populations of cattle, sheep and pigs, as well aspoultry, should be regarded as carriers of these organisms.Therefore, in terms of risk management, it is reasonable to


Fig. 1Examples of categories of cattle according to theiracceptability, on hygiene grounds, for slaughter for humanconsumption

proceed on the basis that all flocks and herds containanimals that are likely to be colonised with and excretingconsiderable numbers of C. jejuni, C. coli and otherCampylobacter spp. of public health importance. Themanagement of risk in relation to such populations mustbe undertaken on a whole herd/flock basis at all stages ofproduction, processing and distribution.

Wild birds are considered to be an important reservoir ofinfection for domestic and food animals.Campylobacter spp. have been found in domestic pets aswell as in rodents, flies and other insects (23).Campylobacter coli is particularly associated with pigs.Because Campylobacter spp. are ubiquitous in animalpopulations, no animal can be excluded as a potentialsource of human infection.

Campylobacter spp. have a low infective dose and thereforeare a hazard for visitors to farms if good hygiene is notobserved. Recently published revised guidelines for openfarms are available (11, 18). These containrecommendations regarding farm layout, animal contact,eating areas, washing facilities, information and signs,training and supervision, livestock management, andmanure and compost heaps.

Beef, dairy and pig productionIn beef and dairy production units, and in pig production,the housing together of animals from different sources atvarious stages of production represents a significant risk ofintroduction and spread of Campylobacter spp. (27).Animals of different ages have a different immune statusand gut microflora and the mixing of different age cohortsintroduces stress, thus facilitating the transmission ofzoonotic agents from infected or colonised animals tosusceptible ones. Likewise, Campylobacter spp. can befound in dairy herds and may, therefore, be present in rawmilk as a result of faecal contamination.

Poultry productionOnce exposed, the alimentary tract of a bird is rapidlycolonised by Campylobacter spp. and othermicroorganisms and within a relatively short periodfollowing initial exposure a high proportion of thepopulation become lifelong excreters of large numbers ofthese microorganisms. The source of colonisation is notalways clear, but it is often attributed to the introduction ofthe organisms by way of contaminated boots and clothing(22). Depletion of poultry houses in three or four phases(i.e. thinning) presents a clear opportunity for farm-to-farm spread of Campylobacter spp. via the personnelinvolved. Consequently, this practice should bediscontinued. The possibility of vertical transmission

(i.e. from breeder flocks to progeny) has been suggested(33), but is not widely accepted.

Provided proprietary animal feed is properly protectedfrom contamination at the point of consumption, it isgenerally not regarded as a primary source of infection forCampylobacter. If adequate protection measures are not inplace the animal’s food and water supply may becomecontaminated shortly before consumption by droppingsfrom infected rodents, birds, and other animals and mayalso contain infected insects, in which case transmission ofCampylobacter spp. may ensue.

The essential elements of a campylobacter controlprogramme in poultry production include the measuresdescribed below.

Structural and general measures

a) an “all-in/all-out” policy regarding the movement ofstock into and out of houses and preferably, into and outof individual sites, should be practised

b) in all cases, the poultry houses should be sound instructure and be capable of being cleaned and disinfected

c) the poultry houses should be vermin-proof and rodentsshould be controlled by systematic baiting in thesurrounds

d) the site should be maintained in a tidy state and thegrowth of grass and vegetative cover (including shrubs,trees) should be controlled

e) entrances into poultry houses should have a welldrained, concreted surround

f) where there are exit points for the air ducts at the sideof the poultry house, the surrounding area should beconcreted and be maintained in a tidy state at all times

g) each poultry house should have a separate lobby insidethe entrance that is suitable for changing into and out ofprotective clothing and footwear, and hand washingfacilities should be provided

h) litter removal and disposal points outside the housesshould be located in well drained, concreted areas, beclearly marked and be maintained in a clean and tidy stateat all times

i) spillage from feed bins should be removed promptly

j) shavings storage facilities should be kept tidy and berodent-, bird- and pet-proof

k) the water supply to poultry houses should meetbacteriological standards comparable to those required ofpotable water.

Operational measures during production

a) cleaning and disinfection facilities for footwear shouldbe provided at the entry point(s) into each house and theyshould be regularly replenished; personnel must follow a


strict procedure of cleaning and disinfection each time theyenter a poultry house

b) separate protective clothing and footwear should beworn when entering each poultry house

c) personnel should use the hand-washing facility eachtime they enter a poultry house

d) the number of visitors entering poultry houses shouldbe minimised

e) visitors should be provided with protective clothing andfootwear and be required to follow exactly the sameprocedures as staff when entering poultry houses

f) the practices of thinning and point-selling duringproduction represent a serious possibility of introducingCampylobacter spp. The industry should, therefore, operatean “all-in/all-out” policy

g) all dead birds should be promptly removed anddisposed of in a hygienic manner

h) all animal waste and unused feed should be removedfrom houses and be disposed of hygienically

i) pets should not be allowed to enter poultry houses atany time

j) where rigorous biosecurity measures are in place, thesemeasures could be part of a sequence leading to a timewhen producers could eventually label their products ‘thiscomes from a flock tested as campylobacter-free’.

Operational measures when the site is entirely de-stocked

a) all animal wastes and leftover feed should be removedand disposed of hygienically

b) the interior of the houses, including all water and feeddistribution equipment, should be thoroughly cleaned

c) the concreted areas at personnel entry points, litterremoval points and around side extraction air ducts shouldbe cleaned and disinfected

d) all gross debris should be removed from cleaned areasand be disposed of hygienically and these areas shouldthen be cleaned and disinfected

e) the use of an insecticide prior to or following cleaningand disinfection should be considered

f) in cases where the flock in question has been found tohave been infected with Campylobacter spp., the house(s)should be examined using drag swabs or by other means,in order to assess the efficacy of the cleaning anddisinfection procedures followed

g) following cleaning and disinfection, each house shouldbe allowed to dry before being re-stocked

h) in all cases the time and details of the sanitationprogramme as applied, together with the names of thepersonnel involved, should be recorded

i) a written sanitation programme should be drawn upwith the agreement of the personnel concerned and this

programme should then be the subject of an independentaudit. The outcome of any such audit, including a siteinspection, should be made known to the management ofthe integrated production/processing operation before re-stocking is allowed to commence.

Biosecurity measures such as these have enabled theelimination of Campylobacter spp. from up to 60% of commercial broiler flocks in Sweden and havereportedly reduced the within flock prevalence from 50%to 10% (28). The approved control measures must beefficiently implemented as standard operating proceduresat a consistently high standard at all stages and at all timesif elimination of Campylobacter spp. is to be effective.

Other control measuresCompetitive exclusion exploits the principle ofcompetition between microorganisms for similar ecologicalniches. The technique has been applied as a component ofa successful strategy for the control of some bacterialinfections, including salmonellosis in poultry. To date, thisapproach has been unsuccessful. However, somecompetitive exclusion experiments have been shown toreduce the numbers of campylobacters in the caeca oftreated birds (26). Effective vaccine strategies directedagainst infection with Campylobacter spp. in broilerchickens have yet to be developed.

Overall, it is far from clear if sustained campylobacter-freestatus can be achieved on poultry farms under commercialconditions, with even the most intensive level ofbiosecurity that is practicable. However, the slaughter ofbirds from flocks shown to have been free of infectionimmediately prior to despatch and which are transportedunder strict hygienic conditions to the poultry meat plantand slaughtered separately from other birds, should beencouraged. Such a procedure is feasible and can lead toreductions in contamination rates in the dressed carcasses.

Zoonotic tuberculosis caused byMycobacterium bovisTuberculosis in cattle and its importance as a cause ofdisease in some human populations represents one of theprincipal reasons for the introduction of direct inspectionmethods for meat control and the pasteurisation of dairyproducts. As a clinical entity in cattle this disease has nowbeen almost completely eradicated in most developedcountries. Isolated incidences in which there is directinvolvement of infected cattle as the source ofMycobacterium bovis infection in humans still occur (12,31, 36). In a number of developing countries, where the


disease in cattle and related species is not controlled due tolack of national funds, the disease poses the same if not agreater threat to human health as it did a century ago inmost developed countries of today, since immuno-compromised individuals are particularly susceptible.

One of the beneficial effects of national bovine tuberculosiseradication programmes has been the effective removal ofmost infected cattle before they reach the clinical stages ofthe disease and before the major organs show overt signs ofinvolvement. Animals which show a high responsiveness tobovine tuberculin are the animals most likely to display grosslesions at slaughter. This demonstrates that the tuberculintest is an effective screening test and it may, therefore,provide a basis for the strategic removal of reactors at local orregional level in countries in which financial constraintsprevent the implementation of a national eradicationprogramme for this disease. Meanwhile, every effort shouldbe made to prevent the entry of such infection into herds ofcattle and, in some regions, sheep flocks and herds of goatsand deer as well, through the unwitting purchase of infectedstock or contact with neighbouring infected herds or flocksand tuberculous wildlife (8). Segregation of stock of differingages, effective composting of manure, attention to sanitaryissues, including disinfection and a prudent cullingprogramme, are of significant importance in maintaining atuberculosis-free herd or flock, particularly in regions inwhich the prevalence of tuberculosis in the animalpopulation is a concern.

Paratuberculosis (Johne’s disease) caused by Mycobacterium aviumparatuberculosisMycobacterium avium paratuberculosis (MAP) is thecausative agent of paratuberculosis ( Johne’s disease), aproduction disease in ruminants, and a hypothesis existsthat MAP may be involved in the aetiology of Crohn’sdisease, a chronic inflammatory bowel disease in humans.The hypothesis is not proven, but the general principle thatdiseased animals should not be used as a source of food forhumans should be adhered to. However, control of Johne’sdisease in dairy herds is difficult and is based on twoprinciples, namely, the identification and elimination ofinfected animals and the prevention of new infections (34).Essential to this process is a clear understanding on thepart of the herd owner of the fundamental processesinvolved. These include the following:– determining the prevalence of the disease in the herd– culling clinical and subclinical cases identified by thediagnostic tests available

– reducing the contact between newborn calves and theirdams where the status of the dam is unknown– ensuring that replacement heifers are fed pasteurisedmilk replacer and colostum from Johne’s disease-free cows – managing the farm and its environment so as to ensurethat stock do not graze on contaminated pasture– strictly assessing the status of bought-in stock based onserological testing and the history of the herd of origin– vaccinating, where permitted, to reduce faecal sheddingof the organism and the number of clinical cases (this maynot affect the prevalence of infection) (40).

Verocytotoxigenic Escherichia coliThe VTEC is present in the gut and faeces of healthy cattleand sheep and these animals therefore act as reservoirsfrom which humans can become infected. Livestock are areservoir for most VTEC, with cattle being the principalsource of E. coli O157:H7 and other VTEC. Studies fromthe United Kingdom (UK) and the USA have shown thatVTEC is, at least occasionally, present on most farms (16).In these studies, when faecal samples, from both beef anddairy cattle, were examined over the course of a year,prevalence rates for VTEC ranged from 0.5% to over 36%,with an annual average of 15.7% (7, 16). A recent study inthe UK showed that VTEC was isolated from 752 (15.7%)of 4,800 cattle and the monthly prevalence rates werebetween 4.8% and 36.8% (7). As animals carrying VTECshow no clinical signs, visual inspection will notdistinguish carriers of VTEC from non-carriers. Thesebacteria have become part of the normal gut flora ofhealthy livestock; at any time, an unknown proportion ofthese may be HP-VTEC.

The organism can survive in soil for several months (4).Cases in farm families and farm visitors have resulted fromdirect contact with livestock or faeces or from drinkingunpasteurised milk. The effects of animal husbandrypractices on the prevalence of VTEC in animals are to aconsiderable extent unknown. Moreover, no definedcarrier state has been identified which can be targeted foran intervention programme. Therefore, eradication ofVTEC from the farm livestock or farm environment doesnot seem to be a reasonable goal. However, risk reductionmeasures can be implemented on-farm to minimise therisk of VTEC infections (14). Examples of these measuresare outlined below.

Water and feedsWater troughs on farms have been frequently found tocontain VTEC and, as a result, contaminated water troughs


and water have a role in the transmission of the organism(17). The VTEC survives in water trough sediments for atleast four months and appears to multiply there, especiallyin warm weather. Water troughs should be cleanedfrequently to prevent the accumulation of sediments.Escherichia coli O157:H7 does not survive in silage (5) andfeeding hay, grass, or silage high in propionic or aceticacids may reduce the likelihood of VTEC shedding bycattle (25).

Animal slurryThe role of spreading slurry and manure on land in thetransmission of VTEC between livestock has not beenestablished (16). However, it is good practice to withholdlivestock from pastures for four to six weeks after thespreading of slurry. The use of raw manure or slurry on ornear the vicinity of crops, particularly fruit and vegetablesto be eaten raw, is potentially hazardous, as VTEC canpersist in animal faeces (4).

Unpasteurised milkSerious outbreaks of VTEC infections have been associatedwith the consumption of raw or unpasteurised milk; VTECmay be present in milk, even when produced under,apparently, hygienic conditions, as a result of faecalcontamination.

Cleanliness of animals on leaving farms forslaughterThe immediate source of most bacteria, including VTEC,on carcasses after slaughter is the soiled hide (32). Effortsto reduce the level of hide soiling are warranted for thecontrol of VTEC and other food-borne disease-causingorganisms. Certain diets will result in the production oflarge quantities of watery dung. Wilting of silage toincrease the dry matter content and free access to strawhelps to reduce this problem. Poor housing design andmanagement contribute significantly to contamination ofanimal hides. Clipping the backs of finishing cattle athousing reduces sweating and the risk of wet dirty hides.Stocking rates should be appropriate to the size of thecattle. In slatted units, as animals are removed for dispatchto slaughter, the area for the remaining cattle should bereduced. Slurry storage space and removal frequencyshould be adequate to prevent blocked slats. Solid floorareas at the end of slats should be sloped to minimise thebuild up of manure and this area should be cleanedregularly. In certain circumstances it may be necessary tomove some animals from slatted sheds to straw-beddedhousing for a period prior to dispatch. A generalprogramme of animal health should include the provisionof a well balanced diet, prevention of infections by good

hygiene and appropriate parasite control to reduce scours.Any changes in diet should be gradual to allow the animalsto adapt.

It is crucial that farmers be aware of their responsibility tosend animals to slaughter in a clean and dry condition.Carcasses contaminated during the slaughtering anddressing process represent an important route by whichVTEC and other disease-causing organisms can enter thefood chain (32). As abattoirs are in the food business, withcattle and sheep their raw ingredients, the hygienic qualityof the primary raw materials, such as cattle and sheep, willinfluence the safety of the end product. Abattoirmanagement must accept their responsibility to protect thehealth of the public by ensuring that only clean cattle areaccepted at the meat plant. That responsibility also extendsto the food processor, distributor and the consumer, and itis particularly important when one considers the enhancedvulnerability of the elderly and other groups of society. It isessential that this shared responsibility is communicated toall sectors, by publications such as the one illustrated inFigure 2, and by other means.


Fig. 2Series of advisory leaflets on the prevention of exposure ofconsumers to Escherichia coli O157:H7 illustrating theresponsibility of each sectorSource: Food Safety Authority of Ireland (www.fsai.ie)

Contagious abortion in cattlecaused by Brucella abortusBrucellosis is an infectious disease of man (undulant fever)and animals, mainly cattle, caused by the bacterium,Brucella abortus. Infection with this organism causescontagious abortion in cows and deer when large numbersof organisms are shed into the environment. Infection isacquired from infected females at, or following, abortion,from contaminated milk, sexually transmitted frominfected bulls, or acquired from a contaminatedenvironment. Infected animals harbour the bacterium intheir lymph nodes, udder and uterus, and in the case ofbulls, the male genitalia and related lymph nodes. Thebacterium survives for upwards of six months incontaminated slurry and can be spread from farm to farm,and can infect people, during spreading.

The disease is or has been the subject of an eradicationprogramme in many countries. Control programmesemploy two principal methods, namely, vaccination andthe removal for slaughter of infected and exposed animalsbased on serological testing. These measures are supportedby movement controls and quarantine on infected farms(35). Unless infected cows are identified early, and areremoved immediately, they are a source of infection forother animals and people, either through direct or indirectexposure. Furthermore, farmers and their families, alongwith their workers, can be exposed to infection bydrinking raw milk produced by infected cows. Likewise,dairy products made from unpasteurised milk from B. abortus infected cows are a possible source of thisinfection for consumers. Pasteurisation makes dairyproducts safe, but does not deal with the issue of the director indirect contact routes of transmission to humans or thedisastrous animal production consequences of the disease.The most effective approach, however, is the earlyidentification and removal for slaughter of all B. abortus infected cattle from the national herd.

The mimimum precautions to be taken to reduce the riskof human infection with B. abortus on farms include:

– operating a closed herd, or alternatively, purchasingessential replacement stock from verifiable disease-freeherds and subjecting these animals to post-purchase testsfor brucellosis while in isolation before releasing them intothe herd

– segregating pregnant heifers and cows by their expectedcalving dates

– using calving pens, with strict disinfection precautions atall times

– using proper arm gloves and in some cases face maskswhen assisting calvings

– disposing of cleansings (afterbirths) hygienically

– treating all abortions as potential brucellosis cases andreporting them, seeking veterinary advice and assistance– withholding milk for human use from herds in which B. abortus infection may be considered to be present,pending proof of the contrary– boiling or otherwise heat-treating all milk before use onthe farm or elsewhere.

Goats and sheep may also acquire infection with Brucellaspp.; these animals are more prone to infection with B. melitensis, which is the more common cause of undulantfever in Mediterranean countries and of which theepidemiology and control measures are similar to B. abortus. Brucella suis causes clinical disease in pigpopulations in a number of countries; biovars 1 and 3 areof considerable importance as a zoonosis for pig workersand meat plant operatives, as well as consumers, in thesecountries (35).

ConclusionZoonotic hazards that are associated with food animalproduction and food processing may arise on the farm, inthe food plant and in the distribution chain. Awareness onthe part of food animal producers and the members of thefood industry that such hazards may exist in foods is thefirst step towards their control. A positive approach toanimal health on the farm with the objective of eliminatingor minimising exposure of food-producing animals tothese hazards, supported by ante-and post-mortemveterinary examination of all food animals at meat plants,effectively removes overtly diseased animals from the foodchain. Good hygiene practices throughout processing and,finally, cooking, provide further safeguards for theconsumer. These control measures are the cornerstones offood hygiene practice and are essential to providing a levelof safety assurance approaching that required by theconsumer and by international trade. Meanwhile, thecurrent system deserves the full support of the scientificcommunity at the national and international level so as toensure that any shortfalls in terms of zoonosis control areaddressed.

In view of the evolving nature of food animal productionthere is also a need for further and continuing research intothe origins of food-borne disease and the means for theirprevention. Basic and applied research both have acontribution to make to the further maintenance of asupply of healthy food which is acceptable to consumersboth at home and abroad. Such measures as are currentlyemployed to prevent or control the transmission ofzoonotic agents via the food chain in the post-harvestphases are unlikely to be successful in isolation. Effectivecontrol relies upon the implementation of a consistentlyhigh level of production hygiene at all stages of production


both on the farm and in the processing plant, andthroughout the remainder of the food chain. In this respectthe role of education remains paramount for allstakeholders at every level of the food industry. Inparticular, attention is drawn to the need for training andeducation of the food animal producer, as it is possible bythis means, and with the collaboration of veterinarypractices and other advisory agencies, to reduce the level ofexposure of livestock to microorganisms which are ofpublic health concern, and thereby reduce the initialloading of the meat, poultry meat or dairy product withthese contaminants. In this regard the need to address thedangers posed by the emergence of antimicrobial resistanceand to quantify and limit the impact of such emergence isall the greater now that the human food chain is recognised

as an important route for the passive transfer of resistantpathogens from animals to humans.

The food quality assurance schemes operated in manydeveloped countries have a high educational componentand place considerable emphasis upon on-farm hygieneand animal health and welfare criteria which are imposedas a condition of entry into the programme. Amultidisciplinary approach to zoonosis control will deliveroptimum results and existing approaches need to beflexible to incorporate advances in the breeding of diseaseresistant stock, new vaccines, new approaches to nutrition,and innovative ways to educate farmers, as the primaryfood producers.


J.D. Collins & P.G. Wall

RésuméLa maîtrise des agents zoonotiques au niveau des réservoirs animaux et avicolescontribue à limiter les problèmes auxquels sont confrontés les systèmes degestion de la sécurité sanitaire des aliments, que ce soit au niveau de latransformation ou des opérations réalisées en aval dans la chaîne alimentaire.L’adoption de bonnes pratiques d’élevage (la sélection des animaux et le suivivétérinaire, par exemple) est indispensable pour assurer une productiond’animaux sains inscrite dans la durée. Les aliments pour animaux constituent unélément clé, dans la mesure où ils procurent des éléments nutritifs dépourvusd’agents pathogènes et assurent le régime équilibré nécessaire au maintien dubétail en bonne santé. L’apport d’eau claire, la parfaite maîtrise des animauxnuisibles et sauvages et un environnement optimalisé pour réduire le stress ontune grande importance pour l’amélioration des performances animales. Lesélevages n’offrant pas de conditions stériles, les mesures mises en place pourréduire les risques de zoonoses seront pragmatiques, économiques et souples.Elles tiendront compte de la taille de l’exploitation, de l’espèce animale et del’épidémiologie des agents zoonotiques présents dans la zone géographique. Laformation des éleveurs et des ouvriers de ferme est cruciale pour le succès desmesures de contrôle des zoonoses introduites dans les exploitations. En effet,une prise de conscience de la nécessité de ces mesures et de leurs modalitésd’application se traduira par un respect plus fidèle des protocoles et desprocédures. Cette sensibilisation des intéressés sera un premier pas dans lamise en œuvre d’une approche intégrée et longitudinale visant à garantir lasécurité sanitaire des aliments par le contrôle des zoonoses en amont de lachaîne alimentaire.

Mots-clésBiosécurité – Épidémiologie – Maîtrise des zoonoses – Médecine préventive – Santé des troupeaux – Sécurité sanitaire des aliments.

La sécurité sanitaire des aliments et les systèmes de productionanimale : la maîtrise des zoonoses dans les élevages

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J.D. Collins & P.G. Wall

ResumenLa lucha contra la presencia de agentes zoonóticos en los reservorios animalesy aviares tiene por efecto reducir el nivel de peligro a que hacen frente lossistemas de gestión sanitaria de los alimentos, tanto en el procesamiento deéstos como en todas las etapas subsiguientes de la cadena alimentaria. Paraproducir y mantener animales sanos se requieren buenas prácticas zootécnicas,lo que incluye aspectos como la selección de los animales o la atenciónveterinaria. Los alimentos constituyen un ingrediente clave no sólo para aportarnutrientes desprovistos de patógenos sino también para ofrecer unaalimentación equilibrada que mantenga sanos a los animales. Para obtener deéstos un buen rendimiento es importante proporcionarles agua salubre y unentorno idóneo, que reduzca sus niveles de estrés, y también instituir un controladecuado de los parásitos y la fauna salvaje. Dado que la explotaciónagropecuaria no es un medio estéril, las iniciativas para luchar contra losriesgos zoonóticos deben ser prácticas, económicamente viables y flexibles yadaptadas a las proporciones de la empresa, las especies de que se trate y laepidemiología de los agentes zoonóticos presentes en cada región geográfica.Para que la lucha contra las zoonosis en la explotación tenga éxito esfundamental llevar a cabo una labor pedagógica dirigida a granjeros y pastores,pues cuando éstos entienden el porqué de las medidas de control, así como laforma idónea de aplicarlas, mejora el nivel de observancia de los protocolos yprocedimientos. Esta comprensión es un primer paso hacia la aplicación de unplanteamiento longitudinal e integrado en materia de higiene de los alimentospara luchar contra las zoonosis en las etapas de la cadena alimentaria previasal sacrificio de los animales.

Palabras claveEpidemiología – Inocuidad de los alimentos – Lucha contra las zoonosis – Medicina preventiva – Salud de los rebaños – Seguridad biológica.

Inocuidad de los alimentos y sistemas de producción animal:lucha contra las zoonosis desde la explotación


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Food safety and animal production systems: controlling zoonoses at