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Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
Ensuring Food Safety Throughout the Food Supply Chain
Convenor: S. K. Crerar
Australia New Zealand Food Authority
Monitoring and Surveillance Program, PO Box 7186 Canberra MC ACT 2610
ABSTRACT: New food production and distribution methods provide the potential for large and widespread foodborne
disease outbreaks. Such factors, together with the changing epidemiology of foodborne disease, present enormous challenges to
ensuring food safety. As human health hazards have the potential to be introduced and/or magnified at any phase along the food
supply chain, food safety must be a major focus of all sectors throughout this entire continuum including primary production,
processing, retail service and the consumer. While Hazard Analysis and Critical Control Point is acknowledged to be the best system
currently available for the control of hazards in foods, it may not be appropriate for some sectors, for example that of the pre-harvest
stage. For this reason, practical and effective food safety risk management strategies need to be developed and catered for within
each food sector. Such programs should emphasise preventative approaches and utilise scientific risk assessment principles. Risk
assessment methodologies are rapidly developing with quantitative modelling techniques now being employed for estimating the
public health risk from microbiological foodborne hazards. However, the application of quantitative risk models is often limited by a
lack of epidemiological and ecological data on foodborne hazards. Efforts to improve surveillance by collecting human illness and
epidemiological data by undertaking further research on the ecology of foodborne hazards, and by investigating novel ways of
controlling potential pathogens along the food supply continuum, need to be further encouraged.
Key Words: Food safety, Food Supply Chain, Food-borne Hazards, Safety Strategies
INTRODUCTION
Food safety has taken on increased importance in
recent years. The impetus to address food safety has
consequently grown throughout the food supply chain.
Arguably the major focus throughout the 1990s has
been on microbiological food hazards and their control.
The now famous 1993 ‘Jack in the Box’ hamburger E.
coli O157:H7 outbreak in the United States (Bell et al.,
1994) signalled the need to rethink our approach,
particularly to microbial food safety. Globally, a
number of countries have responded to this heightened
food safety awareness and activity by developing
major strategies encompassing the whole food supply
continuum. Notable amongst these have been the
United Kingdom, Canada and New Zealand each
having proposed and/or established nationally
integrated food safety agencies. The United States
Government has committed many millions of dollars
across a number of agencies to integrate and enhance
food safety regulation, surveillance and research.
Until recently, Australia has lacked an integrated
national Government approach to food safety. Industry
efforts have forged ahead in this area, driven by strong
market and export forces. The development of the
Australia New Zealand Food Authority’s (ANZFA)
Food Safety Standards (ANZFA, 1996) together with
the commissioning of the Blair Review of Food
Regulation (Food Regulation Review Committee,
1998) are initiatives that advocate a more integrated
and coordinated national food regulatory system,
starting at the farm and extending through to the
consumer.
THE NEED FOR A MORE PREVENTATIVE
AND INTEGRATED APPROACH TO FOOD
SAFETY
S. K. Crerar
ANZFA, Monitoring and Surveillance Program,
PO Box 7186 Canberra Mail Centre, ACT 2610
Whilst improved hygiene and public health have
contributed enormously to the global decline of several
communicable diseases such as poliomyelitis and
typhoid fever, foodborne diseases appear to have
defied these advances and continue to have significant
health, economic and social impact worldwide
(Council for Agricultural Science and Technology,
1994; Desmarchelier, 1996; ANZFA, 1999a).
Moreover, industrialised countries have witnessed
steady increases in the number of cases of foodborne
diseases over the last two decades including changes to
the epidemiology of foodborne disease (Hedberg et al,
1994; Crerar et al, 1996). These phenomena have been
attributed to factors including the following:
Greater tendency to consume minimally processed,
undercooked, raw and ready-to-eat foods, combined
with a higher proportion of meals eaten outside the
home (Alterkruse and Swerdlow, 1996).
New production and distribution of food and food
products providing the potential for larger and more
widespread foodborne disease outbreaks (Henessey et
al, 1996).
Increased at risk population including those with
weakened immune states and a greater proportion of
elderly people (Alterkruse and Swerdlow, 1996).
Emerging pathogens such as enterohaemorrhagic E.
coli, Salmonella Enteritidis and S. Typhimurium
DT104 capable of causing disease at very low
infectious doses (Hedberg et al, 1993; Bell et al 1994;
Cameron et al, 1995; Cowden et al., 1995; Bean et al.,
1996; Besser et al, 1997); and a greater diversity of
contaminated food products such as fresh fruit juice
Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
and produce demonstrated as vehicles of infection
(Hedberg et al, 1994; CDC 1997a; CDC 1997b).
Challenges to ensuring food safety
The aforementioned epidemiological factors further
strengthen the need to redirect the approach to food
safety away from traditional regulatory approaches
such as visual appraisal and end product testing
towards that of preventative programs based on hazard
analysis and critical control point (HACCP) principles.
Internationally, there is now widespread recognition
that a more preventative approach, such as that
advocated by the HACCP concept, is the best way to
control contemporary microbiological and chemical
hazards along the food supply chain (World Health
Organisation, 1997; Codex Alimentarius Commission,
1998). In addition, international trade agreements now
demand that regulation of food product trade be subject
to science-based standards (for example the Sanitary
and Phytosanitary Agreement), so that increasingly,
interventions need to be designed using the best
possible risk assessment analysis (Codex Alimentarius
Commission, 1998).
Overall there are major new challenges confronting the
broader food industry. The complex interactions
between foodborne disease pathogens, the host and the
food vehicle mean that no single intervention is likely
to prevent foodborne illness. Ensuring food safety,
therefore, must be an essential part in every step in
food production and preparation, from paddock to
plate. An inter-disciplinary and co-ordinated approach
across the food supply chain with shared responsibility
and utilisation of preventative risk based approaches
needs to be encouraged.
A new food regulatory environment
The Food Safety Standards (FSS) as proposed by
ANZFA, comprise an important component of a
broader national food safety regulatory system. The
pivotal philosophy behind the FSS is the requirement
that all food businesses, from farm to plate, establish
and implement preventative food safety management
programs. Such programs will need to consider and
assess all potential food safety hazards within an
enterprise and subsequently demonstrate how they will
manage those hazards based on their attendant risk.
Consideration of hazards and the assessment of their
risk are required to be based on sound science and riskbased principles as proposed by the Codex
Alimentarius Commission (Codex Alimentarius
Commission, 1998).
Written documentation of
programs that specify the food safety control points for
particular food safety hazards within a business’
operation is also required. The business must comply
with its food safety program and ensure that an
accredited audit is carried out regularly.
Such
requirements promote a shared responsibility to food
safety. All stages of the food supply chain must
therefore play their part, with over-reliance on any one
sector resulting in a false sense of security.
Benefits of preventative food safety programs and
risk assessment
There are benefits to enhancing an enterprise or
sector’s approach to food safety. As mentioned, new
and emerging pathogens combined with apparently
novel products capable of transmitting disease mean
that the food industry has to be better prepared to
ensure that preventative strategies are in place and they
have the capacity to respond to emerging issues. By
comprehensively examining the potential hazards
within a product and/or enterprise through a formal risk
assessment process, industries will be better informed
of potential food hazards and risks, and able to
prioritise risk management strategies and allocate
resources more effectively (Lammerding, 1997). Risk
assessment can also identify knowledge gaps and the
data required to address these deficiencies. Programs
on research in human and veterinary public health,
food safety and microbiology may be guided by risk
assessment results (Cassin et al, 1998).
Underpinning strategies with science will become
increasingly important to demonstrate to trading
partners that food safety policies and regulations are
soundly based. A natural consequence of a greater
science- or data-based environment is that agencies
will place a greater emphasis on pathogen and disease
surveillance data to establish and evaluate food safety
polices and programs (Angulo et al, 1998).
The role of surveillance and research data:
monitoring and surveillance data
All parts of the food supply chain must contribute to
and support the need for better information on food
hazards. Comprehensive national foodborne disease
surveillance information is another key component of
an effective national food safety agenda (Crerar, 1999).
It should have the capacity to determine the incidence
of known and newly emerging foodborne diseases in
Australia and provide knowledge on the following:
• The temporal and spatial distribution of disease.
• Specific risk factors for infection.
• The public health impact of specific pathogens.
• The social and economic burden attributed to
pathogen.
• Points in the food supply chain that may be
amenable to prevention.
A National Foodborne Disease Surveillance System
should incorporate appropriate links to other data on
food and animal pathogens including that of industry,
other food/animal and human disease databases,
surveys and research (Crerar, 1999). The system needs
to be continuously updated, analysed and the
information disseminated in a timely fashion and in a
manner appropriate to those who will be using the data
(see Figure 1).
Research
Food safety research is a vital tool that assists in
assessing the effectiveness of food safety programs and
policy. To effectively address the safety of various
food commodities we need to know more about the
hazards in these products and their relation to adverse
health outcomes.
Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
Research into foodborne pathogens must be broad to
address information needs at all points along the farmto-table continuum. The research agenda should be
guided by public health concerns, the requirement to
underpin HACCP and preventative food safety
programs and regulations with science, and the
international recognition that food safety policy be
based on risk assessment (United States Department of
Agriculture, 1997; Crerar, 1999).
Figure 1: Integrating surveillance data sources and
disseminating information (modified from Crerar,
1999)
Data dissemination
and feedback
•Standards/legislation
•Cost/benefit analysis
•Emerging hazards
Environment water, wildlife
•monitoring
•Risk assessment
•Program development
•Program modification
Primary food
production farm, sea
•surveillance
•surveys
•investigations
Processing
•HACCP/surveys
Retail and
service
•food
surveys
•HACCP
Human illness
surveillance
•laboratory
•sentinel
•investigations
•consumer complaints
Database on foodborne hazards pathogens, vehicles and contributing factors
Consolidation, analysis and
interpretation of data
Risk assessment has also become the means of
ensuring that countries establish food safety
requirements that are scientifically sound and a means
for determining equivalent levels of food safety
between countries in international trade (Lammerding,
1997).
It must be recognised that the science of risk
assessment, particularly quantitative methods for
microbial pathogens, is in a developmental stage and
further work is necessary. Furthermore, it is crucial
that federal and State agencies work closely with each
other to improve the scientific basis for establishing
food safety programs, standards and policies for
microbial pathogens.
A nationally coordinated research program on food
safety is urgently needed for Australia. Areas of
research that should be considered include the
following.
The need for population-based studies to obtain valid
measures of the incidence of human disease due to the
major foodborne pathogens and their association with
specific food vehicles.
More rapid and sensitive laboratory methods for the
diagnosis of foodborne pathogens such as Salmonella,
Campylobacter and enterohaemorrhagic E. coli.
Collection of pre-harvest (on the farm and preslaughter) pathogen data to encourage the development
of preventative controls at the animal production level.
Conduct of microbiological baseline studies for
various animal species and the relationships between
various husbandry practices and the levels of these
microorganisms.
The relationship between bacterial numbers on raw
product and foodborne illness.
Consideration of world best practice models for
microbial risk assessment and the development of a
consistent framework for Australian industries.
Comprehensive surveillance and research on foodborne
disease, including studies that determine the incidence
and impact of disease and improve our understanding
of the epidemiology of disease, is the cornerstone on
which preventative programs and policies must be
based and evaluated throughout the food supply chain.
CONTROL OF FOOD-BORNE HAZARDS
DURING THE PRE-HARVEST PERIOD –
OPPORTUNITIES AND CONSTRAINTS
D. Jordan
New South Wales Agriculture, Wollongbar
Agricultural Institute, Wollongbar, NSW 2477
Consumers, food-manufacturers and regulators are
demanding that livestock managers pay greater
attention to product safety. However, outside the
agricultural sector there is often a poor appreciation of
the technical and practical problems faced by livestock
managers in achieving the food-safety goals set by the
larger community. Unlike some food-processing
establishments or the kitchen, farm animals and their
environments are not easily manipulated to minimise
the occurrence of hazards. Yet in some cases where the
farm is the point of entry of hazard into the food chain
there may be an opportunity during animal production
to exert a powerful influence on public health
outcomes. This paper discusses opportunities for preharvest control of the most important hazards found in
meat and milk products and by necessity focuses on
microbial pathogens because of their profound impact
on health outcomes and the economics of food
production.
Food Hazards in animal populations
Several classes of human-health hazards can be
introduced into animals and animal products during the
agricultural phase of food production. Physical
contaminants such as needle tips lodged in muscle
tissue, although rare, are capable of injuring
consumers. Such incidents may also induce a large
financial loss for a food producer through legal
proceedings. Chemical toxins can occur in raw-foods
as a result of inappropriate use or accidental misuse of
antibiotics, pesticides, anthelmintics and herbicides
(Waltner-Toews and McEwen, 1994) but there is little
evidence that routine use of agricultural chemicals in
developed countries contaminates food to the extent
required to cause ill-effects in humans (Nicholls,
2000). A possible exception to the latter is when a
contaminant induces an allergic reaction in a sensitised
individual although most such incidents appear
attributable to manufacturing and packing faults.
Natural toxins such as alkaloids derived from plants do
occur in animal products but their importance to public
health is not well understood. The hazards having by
far the greatest impact on human health, and which are
responsible for the largest economic loss are the
Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
microbial pathogens (Council for Agricultural Science
and Technology, 1994). Amongst these the gut-borne
bacteria such as Salmonella, Campylobacter and
Listeria spp and enterohaemorrhagic Escherichia coli
(EHEC) are of special importance because minute
numbers may induce illness or death when consumed
by people and because they are sufficiently common in
animal products to necessitate the imposition of
expensive control measures. In addition, there is
enormous global concern amongst governments and
consumers about those bacteria found in animalderived foods that carry genes coding for resistance to
antibiotics (U.S. Congress Office of Technology
Assessment, 1995; MAFF, 1998; JETACAR, 1999).
Some of these bacteria may be commensals in animals
but pathogenic in humans (e.g. E. coli O157), or
pathogenic for both animals and humans (e.g.
Salmonella Typhimurium DT104) while others are
commensals in all hosts but may offer their resistance
genes for uptake by human pathogens.
Behaviour of microbial hazards
Although microbial hazards do have the greatest public
health impact, opportunities for their control within
livestock systems are restricted by uncertainty about
their ecology. Most problematic are those organisms
having the ability to survive or multiply away from
animal hosts and these include the gut born pathogens
that are of major public health significance
(Salmonella, Campylobacter, Listeria and EHEC).
These organisms are also faecal-borne and so they
inevitably contaminate products as a result of imperfect
hygiene during slaughter and milking. Study of the
ecology of these organisms has proved troublesome
because of the complex interactions amongst bacteria
in the gut of animals and because of the difficulty in
detecting and enumerating the very small number of
organisms capable of causing human illness (Jordan
and McEwen, 1998). For example, although the
behaviour of E. coli O157:H7 in cattle has been
extensively researched since the early 1990’s a
convincing and comprehensive account of its
behaviour in the cattle population is yet to be
published.
In contrast to the gut-borne microbial hazards those
pathogens that are substantively parasitic such as
Mycobacterium bovis and Brucella spp have been more
effectively dealt with by the veterinary profession.
Their parasitic behaviour has made them much more
amenable to study and has allowed tests to be
developed for the detection of carriers, which has in
turn provided the means of eliminating infection
through culling. Thus brucellosis and bovine
tuberculosis are of minor importance as food-safety
risks in developed countries largely because there has
been progress in eradication of these infections from
farm animals. However, eradication has not been
successful where wildlife reservoirs of infection (such
as badgers in Ireland and possums in New Zealand)
have thwarted the test and cull strategy that has
succeeded in eradicating bovine tuberculosis elsewhere
(Tweedle and Livingstone, 1994; Griffin et al., 1996).
Pre-harvest control of microbial hazards
Pre-harvest management may be used to regulate the
entry of microbial hazards into the food chain. General
mechanisms for this purpose have been classified with
respect to the contamination of meat carcases (Jordan
et al., 1999a) and are discussed under the following
headings.
1. Prevalence reduction
Livestock managers can reduce the quantity of
microbial hazards entering the food chain by treating or
eliminating infected animals and by manipulating
husbandry to prevent infections (Huis in't Veld et al.,
1994). To meet this aim research is increasingly being
directed at novel technological solutions such as
probiotics (Zhao et al., 1998) and vaccines (Wray,
1987) that can prevent animals from being colonised
with food-borne pathogens or eliminate existing
infections. Concurrently, epidemiologists are actively
searching for those risk factors that can be manipulated
to reduce animal prevalence of shedding for specific
pathogens (Dargatz et al., 1997; Hancock et al., 1997).
More general progress may be achieved by identifying
the ‘community of risk factors’ common to groups of
important food-borne pathogens in each livestock
production system (Noordhuizen and Frankena, 1999).
It is common for disease-causing agents to be strongly
clustered within particular herds (Donald et al., 1994).
Consequently, it may be attractive for an industry to
target those ‘problem herds’ which account for a
disproportionate volume of microbial hazard in
product. The objective would be to reduce the
prevalence of herds infected with the hazard (this is the
basis of bovine tuberculosis eradication mentioned
previously). The economic and public health rewards
from this approach are in part determined by the ability
of livestock managers and veterinary authorities to
maintain herds free of infection.
2. Reduced severity of shedding
If the shedding of pathogens by animals cannot be
totally eliminated then it may be possible to suppress
the concentration of pathogen in faeces to a level that
delivers a more acceptable public health risk.
Manipulation of livestock rations to induce gut
conditions unfavourable for the growth of pathogens is
one aspect that has been studied with respect to EHEC
infection in ruminants (Rasmussen et al., 1993; Kudva
et al., 1995). Similarly, vaccines and probiotics may
not succeed in total elimination of infection but may
suppress the shedding of pathogen. These solutions are
appealing because they appear to offer a convenient
remedy, but there are few (if any) examples of where
vaccines, probiotics, or diet changes have been
successfully applied in a broad industry setting to
suppress the number of gut borne pathogens in faeces.
3. Reduced cross contamination
Cross contamination of product consignments and
product items at all stages of production are a vexing
and pervasive issue. Cross contamination is most
critical during manufacturing and food preparation but
may also be important in the pre-harvest period. For
Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
example, livestock may depart the farm in a clean state
but arrive for slaughter shedding Salmonella in their
faeces because of exposure to other animals en-route to
the abattoir (Grau et al., 1967; Grau and Smith, 1974).
In the dairy industry, hazards can be introduced into
previously wholesome consignments of milk through
the bulk collection process although, for microbial
pathogens, pasteurisation has done much to alleviate
the public health consequences of this practice. Thus
the way animals and animal products are marketed has
a role in the introduction and dissemination of hazards
in the food-chain. Where the hazards are microbial the
contamination may initially be trivial but there is the
potential for multiplication to harmful levels during
later stages of production. Consequently, pre-harvest
measures against cross-contamination are often
expected to be effective beyond the farm gate and this
is being addressed by the trend for more direct-toslaughter marketing systems, control of the slaughter
sequence of cattle (Ridell and Korkeala, 1993) and
generally stricter supervision of ante-mortem hygiene.
4. Reduced transfer of pathogens from live animal
to carcase
When pathogens are present in gut contents the
quantity of faeces transferred to carcases becomes a
determinant of the likelihood of human illness (Cassin
et al., 1998). Thus, a cornerstone of modern meat
hygiene has been the minimisation of faecal
contamination of carcases. Despite many recent
advances in biotechnology and the availability of
carcase decontamination equipment, the prevention of
faecal contamination remains a necessary ingredient of
the control of important pathogens (Pennington Group,
1997). Regardless of whether or not pathogens are
present in the animal being slaughtered less faecal
contamination improves the shelf life of meat products.
Moreover, the minimisation of faecal contamination
provides a non-specific benefit by exerting
simultaneous control over more than one pathogen (if
present) and spoilage organisms. Further, a reduction
in carcase contamination alleviates the need for
removal of faecal material by trimming affected areas
of the carcase – a procedure which carries with it the
potential for cross-contamination by contact with
unclean equipment and abattoir workers (Peel and
Simmons, 1978). The investigation of outbreaks of
meat-related illness and new research increasingly
points to the advantages of better management of hide
and fleece contamination in animals prior to slaughter
as an effective method of minimising the transfer of
pathogens onto carcases (Biss and Hathaway, 1995,
1996; Pennington Group, 1997). However, in some
intensive husbandry systems capital improvements to
housing and manure disposal systems may be required
to ensure that all animals are presented for slaughter in
a clean state. In some circumstances there may also be
scope to reduce the exposure of slaughter animals to
manure during transportation and marketing prior to
slaughter. The costs of such actions dictate that a
stronger financial incentive may be needed to
encourage livestock managers to implement the
required changes. At the heart of this issue is the need
for a reliable method of describing the extent of soiling
of animal hides (Jordan et al., 1999b).
Coordination of pre and post-harvest controls
The safety of animal products at the moment of
consumption is often heavily influenced by an array of
post-harvest factors. Thus the extent to which primary
producers have been obliged to contribute to product
safety has not always been clear. Nevertheless,
consumers, governments, processors and regulators
now demand that each section of the food chain
contributes to improved product safety. This means
that in the future livestock managers should aim to
produce commodities that meet the expectations of
consumers rather than merely satisfying the safety
requirements of the dairy factory or abattoir
(Noordhuizen and Frankena, 1999). In response to this
need producers are increasingly adopting quality
assurance programs such as the HACCP approach that
can dovetail with similar control systems being
implemented in the post-harvest phase of food
production.
The challenge facing livestock producers is to meet
community expectations for standards of food safety
without suffering a loss of flexibility in management or
a decline in farm profit. The adoption of quality
assurance programs will inevitably increase farm costs
and so there is a need to compensate producers by
rewarding those who market low-risk commodities.
Moreover, it is important to ensure that quality
assurance measures in the pre-harvest period are based
on objective evidence of their efficacy so that the
efforts of livestock producers do not go to waste but
form part a coordinated strategy that reduces the risk of
foodborne illness in consumers.
FOOD SAFETY STRATEGIES
THROUGHOUT THE FOOD SUPPLY
CHAIN
P. B. Vanderlinde
Food Science Australia, PO Box 3312 Tingalpa
DC, QLD 4170
The majority of foodborne outbreaks are a result of
bacterial infections. In Australia it is estimated that
53% of all foodborne disease outbreaks between 1980
and 1995 were a result of bacterial agents present in the
food (Crerar et al, 1996). This compares with the
estimated 66% of cases in the US (Bean et al, 1990).
Clearly, while other foodborne hazards exist, bacterial
hazards are responsible for the vast majority of
outbreaks. In those outbreaks where a specific food
vehicle could be identified 33% could be attributed to
meat and meat products. Bacterial hazards present in
meat and meat products will be discussed in this paper,
although the same principles can be applied to other
hazard/food combinations.
In Australia, the incidence of a number of foodborne
diseases has increased in recent years (Figure 2). While
some of this increase can be attributed to better
surveillance, it is likely that there has been a real
increase. There are a number of possible reasons for
this; changing demographics and consumption patterns,
Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
Managing food safety
There are a number of steps to follow for managing
food safety hazards. The first is to conduct a risk
assessment. Risk assessments can be either qualitative
or quantitative. The choice of risk assessment depends
on the seriousness of the problem and the resources,
time and information available. The outcome of a risk
assessment is a statement of the probability of exposure
to a hazard and the severity of the consequences of
exposure.
A number of risk management options are available.
These include the establishment of food safety
objectives, the setting of microbiological criteria and
the use of acceptance procedures.
Figure 2: Salmonellosis and campylobacteriosis in
Australia, 1952-1998 (updated from Crerar et al, 1996)
120
Rate per 100,000
population
more meals being prepared or consumed out of the
home environment, changes in the susceptibility of the
population.
The cost of these foodborne illnesses is high. It has
been estimated that in Australia there are 11,500 cases
of foodborne disease every day costing the community
over 2.6 billion dollars per year (ANZFA, 1999a). The
cost to industry can also be quite high. The recent
foodborne outbreak linked to peanut paste was
estimated to have cost the company $55 million.
The long-term effects of some foodborne illness can
exacerbate the cost of foodborne disease to the
community. For example, Salmonella infections have
been linked to the onset of aseptic reactive arthritis and
Reiter’s syndrome; while Campylobacter infections
may lead to long term effect such as Guillain-Barré
syndrome (Doyle et al, 1997). These sequelae are only
just being considered when estimating the cost of
foodborne disease.
In order to ensure the food we eat is safe, the major
focus at all levels of food production, processing,
preparation and service should be food safety. Every
stage in the process including harvesting, storage and
transportation of raw material; processing, packaging,
storage and transportation of the processed product;
receiving of the processed product at the point of sale;
subsequent storage of the product; preparation of the
product for consumption and the storage of leftovers
must be carefully controlled to ensure a safe product.
For a bacterial foodborne outbreak to occur it is usually
necessary for several events to happen in sequence.
Initially there must be a source of the pathogen in the
environment or in the raw material. Opportunities
must then be created for the pathogen to contaminate
the food. It may be necessary for the pathogen to grow
to reach an infective dose or for toxin to be expressed.
Clearly these events are not contained within a single
link in the food supply chain. Therefore, food safety
becomes the responsibility of all sections within this
continuum.
Campylobacteriosis
100
80
Salmonellosis
60
40
20
0
1950
1960
1970 1980
Year
1990
2000
Food Safety Objectives (FSO’s)
FSO’s are usually established through the risk
assessment and risk management process. Risk
assessment is a systematic process by which elements
in a process can be assessed for their importance in
determining the overall risk, in most cases as measured
by the likelihood of disease from the consumption of a
specific food.
A FSO is a statement of the maximum level of hazard
considered to be acceptable for consumer protection. A
FSO can be a simple statement such as the frequency
or maximum concentration of a hazard allowed in a
certain product. It can also be a description of the
desired outcome of a process ie. a specified reduction
in the concentration of the hazard.
Performance Criteria
A performance criterion is the required outcome
necessary to achieve a FSO. For example, in order to
meet a FSO of less than 100 Listeria monocytogenes
per gram of ice cream might require the manufacturer
to ensure a) pasteurisation of the ice cream mix to
achieve a 6-log reduction in L. monocytogenes
(performance criterion), b) control of re-contamination
(good hygienic practices). Other examples include
cooking and cooling requirements for meat products.
When
establishing
a
performance
criterion
consideration must be given to the initial level of
contamination and changes that might occur during
production,
processing,
distribution,
storage,
preparation and use. A performance criterion can be
defined by the equation:
∑ R + ∑ G = FSO − H O
Where: ΣR = total reduction effect during processing
(negative by definition)
ΣG = total growth (increase) during
processing
HO = initial level of hazard
Process Criteria
In contrast to performance criteria, process criteria
specify parameters in the process that need to be
controlled in order to achieve the desired outcome. For
example, the process criterion for cooking meat in
Australia is 650C for 10 s. Process criteria by definition
usually appear as critical limits for critical control
points in HACCP plans.
Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
Acceptance procedures
In the absence of an FSO it may be appropriate to
set acceptance procedures based on expert opinion.
This serves as a fail-safe control but has the
disadvantage of being less flexible, as they assume
‘worst-case’ situations. An example of an acceptance
procedure or default performance criterion would be
the ANZFA 3-log reduction in E. coli required for
comminuted fermented meat products. Acceptance
procedures also provide a safe harbour for processors
that lack either the resources or the desire to develop
their own performance criteria adapted to their specific
operations.
Control Measures
Control measures are the actions or activities
undertaken in order to eliminate a hazard or reduce the
hazard to acceptable limits. Generally control measures
fall into two main programs, good hygiene practices
(GHP) and HACCP. GHP and HACCP can be applied
at all levels of the food chain. Although application of
HACCP on-farm and in the home has not progressed as
well as in other areas.
GHP
The major components of GHP are:
• design of facilities
• control of process operations
• maintenance and cleaning
• personal hygiene
• transportation
• product information and consumer awareness
• training
GHP are not usually product and process specific,
providing guidelines for the whole operation. The
effective application of GHP provides a good
foundation for HACCP. Indeed selected aspects of a
GHP component that are significant in determining the
risk should be incorporated into the HACCP plan.
HACCP
The HACCP system is more focused than GHP and
recognises the uniqueness of different food operations
and their associated hazards. The HACCP system has
been applied to a large variety of products and
processes. The Australian meat industry has adopted
the principles of HACCP in its Meat Safety Quality
Assurance (MSQA) program.
HACCP is a systematic process. Hazards need to be
identified and critical control points determined. As
well as this critical limits need to be set and corrective
actions put in place. HACCP is the best system
currently available for the control of hazards in foods
from farm to table. A more detailed discussion on the
principles of HACCP (ICMSF, 1988).
Control measures from farm-to-plate
In the past organoleptic inspection and
microbiological testing of end products was the only
available control measure for ensuring food safety.
Today it is generally agreed that such an approach
offers little in the way of protection for the consumer.
Generally the level of bacteria present in the food at the
time of manufacture is low; this coupled with the low
frequency of contamination often makes testing
impractical. In addition it has been demonstrated that
there is not always a direct correlation between
organoleptic status and product safety. A far better
approach is to ensure that all stages in a process are
under control.
Control options that can be instigated on-farm have
been put forward by other researchers. Garber et al
(1999) identified on-farm factors that correlated
strongly with the prevalence of enterohaemorrhagic E.
coli O157:H7 in cattle. Factors included the season,
geographical location, herd size and the use of water
for removing manure. The authors concluded that cattle
sampled in summer months had a higher incidence of
shedding of this pathogen than animals sampled in
spring. Similarly, animals from small herds had a lower
prevalence, as did animals from farms not utilising
water for removal of manure. How these factors apply
to Australian cattle is not known. Feed has also been
identified as an important factor in determining the
degree of shedding of pathogens in cattle (Herriott et
al, 1998), as has feeding practices prior to slaughter
(Grau et al, 1968). It is possible that by taking these
options into consideration the prevalence and
concentration of pathogens in the food chain can be
reduced.
Control measures applied during processing should
be focused on those areas that have been identified as
critical control points in the HACCP program. For beef
abattoirs these may include initial carcass
contamination, cross-contamination and growth during
chilling.
For carcass meat, control measures have
traditionally focused on decreasing the numbers of
bacteria present on the carcass after slaughter.
However, effective strategies can also include
operations that prevent or minimise the initial
contamination. For example, the cleanliness of the
animals presented for slaughter, hygienic hide removal
and correct knife sanitation. Even the way in which the
carcass is presented to the worker has been shown to
have an effect on the numbers of bacteria. Bell and
Hathaway (1996) found that sheep dressed in an
inverted position had lower total counts than sheep
processed conventionally.
Chilling can be effective in reducing the numbers
of bacteria present on animal carcasses after slaughter
if performed correctly. Although not usually regarded
as a decontamination procedure chilling has been
shown to reduce the numbers of bacteria such as
Campylobacter spp. (Grau, 1988) and Escherichia coli
(Gill and Jones, 1997) on carcasses.
While control measures can be applied at any stage
during processing, in the meat industry the focus has
been on the application of decontamination strategies.
A number of techniques have been evaluated for the
decontamination of food animal carcasses. The most
common approaches can be divided into four main
types, physical, thermal, chemical and radiation. All
have been shown to be effective to varying degrees,
Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
although some do not have general support in the
scientific community. The physical removal of bacteria
for example by high-pressure water washes is generally
not regarded as a decontamination strategy and has
little effect on the numbers of bacteria present on the
carcass surface. Similarly, trimming of animal
carcasses has been shown to result in large reductions
in the numbers of inoculated bacteria (Sofos and
Smith, 1998), however, its effectiveness in removing
naturally contaminating bacteria has been questioned
(Prasai et al, 1998).
The most favoured intervention in the meat
processing industry is chemical or thermal carcass
decontamination. Decontamination strategies have
been reviewed extensively in the literature with
varying claims being made as to their efficacy (see
Dorsa, 1997 and Farkas, 1998). While radiation has
been shown to be effective it still does not have wide
support in the community although this is changing.
Chemical treatments such as organic acid washes have
varying effects on the numbers of bacteria, presumably
as a result of varying acid resistance in the
contaminating flora. The most acceptable forms of
carcass decontamination use thermal energy to
inactivate bacteria. Of these the most common of the
commercially available systems use hot water or steam.
Other factors that need to be considered when
looking at controlling the risk of disease include host
susceptibility, storage time and temperature and the
cooking temperature. It is unlikely that much can be
done about the susceptibility of the consumer, although
education programs can ensure that susceptible
individuals are aware of the risk posed by certain
foods. An example of this is the education program
initiated by ANZFA (1999b), aimed at informing
pregnant women of the risk of Listeria monocytogenes
in certain foods.
Similar education programs aimed at introducing
food safety concepts in the service industry and in the
home could also help reduce the incidence of
foodborne disease (Beard, 1991). Improper storage or
holding temperature was the factor most often reported
in foodborne disease outbreaks in the US (Kanabel,
1995). A number of control options are available to the
risk manager in the home and include:
• the proper handling and transport of food from the
time of purchase to the home
• storing food properly
• preparing food correctly
• storing prepared food correctly
• practicing good hygiene
While the HACCP system is perhaps beyond most
households, consumers should be made more aware of
the potential hazards of handling foods in their
households and of the control measures available to
them. If they can be encouraged to use a basic HACCP
approach there should be a flow-on to improved food
safety. Governments can also apply the principles of
HACCP when developing educational material for
consumers. Studies in the US would suggest that the
current level of knowledge in the community with
regards to food safety is low (Woodburn and Raab,
1997). This is supported by more limited data from
Australia (Jay et al, 1999).
Deciding where in the food chain to apply control
measures is a difficult task. In the past there was no
objective method available to help the risk manager to
make decisions on where to allocate resources to
achieve the greatest level of risk reduction.
Risk assessment provides the tool that can allow
risk managers to make these decisions. As part of the
risk assessment process a sensitivity analysis is often
performed.
This is particularly the case for
quantitative risk assessments. A sensitivity analysis
identifies the stages in the process that impact most on
the final risk. The degree of confidence in the final
estimation depends on the variability, uncertainty and
assumptions associated with the parameters in the
model.
There are a number of examples of sensitivity
analysis in the literature. Cassin et al. (1998) described
a process risk model looking at enterohaemorrhagic E.
coli in ground beef in the US. Their study provides a
good example of the construction of a process
risk model and the usefulness of a sensitivity analysis.
Cassin et al. (1998) reported the correlation of
various model inputs to the estimated probability of
illness from the consumption of a hamburger meal in
the US (Figure 3). They found the risk to be most
sensitive to the concentration of E. coli O157:H7 in the
faeces of the animals prior to slaughter and to the
susceptibility of the consumer. By using such results
regulators and industry can focus resources on those
factors that have the most influence on the risk.
Figure 3: Correlation between the estimated
probability of illness and the most important predictive
factors of the model (adapted from Cassin et al, 1998)
Conc. In faeces
Host susceptability
Carcass contamination
Cooking preference
Retail temperature
Decontamination
Growth during processing
Retail storage time
Prevalence in faeces
Cross contamination
-0.4 -0.2 0.0 0.2 0.4 0.6 0.8
When determining the risk consideration needs to be
given to the variability and uncertainty associated with
the model inputs. Variability is a measure of the spread
of possible values a factor may have and is a general
indication of the lack of control we have over that
factor. Factors identified to be important in the overall
risk and that are highly variable should be highlighted
and efforts made to reduce their variability. An
example of this may be the quality of the raw material
Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
used in a process. Unlike variability, uncertainty is a
measure of how well we understand the behaviour of a
factor. Factors that have a large amount of uncertainty
associated with them require additional research to
increase our understanding of their behaviour.
CONCLUSIONS
There are many causes of foodborne disease,
many points at which foods may become contaminated,
and numerous factors that make certain individuals and
groups of people more susceptible.
No single
preventive measure is likely to ensure the safety of our
food supply. Initiatives to protect the food supply need
to focus on the hazards and foods that present the
greatest risks to public health, and emphasise
development and implementation of preventive
controls of those risks. They should seek, where
possible, opportunities for such controls through
collaborations with various government and industry
sectors and other stakeholders.
REFERENCES
Alterkruse, S. F. and D. L. Swerdlow, 1996. The changing
epidemiology of foodborne diseases. Am. J. Med.
Sciences, 311: 23-29.
Angulo, F. J., A. C. Voetsch, and D. Vugia, 1998.
Determining the burden of human illness from foodborne
diseases. Vet. Clin. Nth. Am: Food. Anim. Pract., 14:
165-172.
ANZFA, 1996. Proposal to develop a national food hygiene
standard. Australia New Zealand Food Authority, PO
Box 7186, Canberra MC, ACT 2610, Australia
ANZFA, 1999a. Food Safety Standards Costs and Benefits:
Regulatory impact of the proposed national food safety
reforms. Australian New Zealand Food Authority, PO
Box 7186, Canberra MC, ACT 2610, Australia.
ANZFA, 1999b. Listeria and Pregnancy. Australian New
Zealand Food Authority, PO Box 7186, Canberra MC,
ACT 2610, Australia.
Bean, N. H., P. M. Griffin, J. S. Goulding, C. B. Ivey, 1990.
Foodborne disease outbreak 5-year summary, 1983-1987.
J. Food Prot., 53: 711.
Bean, N. H., J. S. Goulding, C. Lao, and F. J. Angulo, 1996.
Surveillance for foodborne disease outbreaks -United
States, 1988-1992. MMWR, 45: 1-66.
Beard, T. D., 1991. HACCP and the home: the need for
consumer education. Food Technol., 45: 123-124.
Bell, BP, M. Goldoft and P. M. Griffin, 1994. A multi-state
outbreak of Escherichia coli O157:H7- associated bloody
diarrhoea and haemolytic uraemic syndrome from
hamburgers. JAMA, 272: 1349-1353.
Bell, R. G. and S. C. Hathaway. 1996. The hygienic
efficiency of conventional and inverted lamb dressing
systems. J. App. Bacteriol., 81: 225-234.
Besser TE, C. C. Gay and G. M. Gay, 1997. Salmonellosis
associated with S. Typhimurium DT104 in the USA. Vet.
Rec, 140: 75.
Biss, M. E. and S. C. Hathaway, 1995. Microbiological and
visible contamination of lamb carcasses according to preslaughter presentation status: implications for HACCP. J.
Food Prot., 58: 776-783.
Biss, M. E. and S. C. Hathaway, 1996. Effect of pre-slaughter
washing of lambs on the microbiological and visible
contamination of the carcass. Vet. Rec., 128: 82-86.
Cameron, S, W. Walker, and M. Beers, 1995.
Enterohaemorrhagic E. coli outbreak in South Australia
associated with the consumption of mettwurst. Commun.
Dis. Intell., 19: 70-71.
Cassin, M. H., A. M. Lammerding, E. C. D. Todd, W. Ross,
and R. S. McColl, 1998. Quantitative risk assessment for
Escherichia coli O157:H7 in ground beef hamburgers.
Int. J. Food Microbiol., 41: 21-44.
Centers for Disease Control and Prevention, 1997a.
Outbreaks of Escherichia coli O157:H7 infection
associated with eating alfalfa sprouts- Michigan and
Virginia, June-July 1997. MMWR, 46: 4-8.
Centers for Disease Control and Prevention, 1997b.
Outbreaks of Escherichia coli O157:H7 infection and
cryptosporidiosis associated with drinking unpasteurised
apple cider- Connecticut and New York, October 1996.
MMWR, 46: 741-744.
Codex Alimentarius Commission, 1998. Draft principles and
guidelines for the conduct of microbiological risk
assessment. ALINORM 99/13A, FAO, Rome.
Council for Agricultural Science and Technology, 1994.
Foodborne pathogens, risks and consequences. CAST
Task Force Report no 122. Ames, IA.
Cowden, J. M., P. G. Wall, G. Adak, S. Le-Baigue and D.
Ross, 1995. Outbreaks of foodborne infectious disease in
England and Wales, 1992 and 1993. CDR, 5: R109–17.
Crerar, S. K, C. B. Dalton, H. M. Longbottom and E. Kraa,
1996. Foodborne disease: current trends and future
surveillance needs in Australia. Med. J. Aust., 165: 672675.
Crerar, S. K., 1999. Key information underpinning an
effective national food safety strategy. Food Aust., 51:
556-559.
Dargatz, D.A., S. J. Wells, L. A. Thomas, D. D. Hancock
and L. P. Garber, 1997. Factors associated with the
presence of Escherichia coli O157 in feces of feedlot
cattle. J. Food Prot., 60: 466-470.
Desmarchelier, P. M., 1996. Foodborne diseases: emerging
problems and solutions. Med. J. Aust., 165: 668-671.
Donald, A. W., I. A. Gardner, and A. D. Wiggins, 1994. Cutoff points for aggregate herd testing in the presence of
disease clustering and correlation of test errors. Prev. Vet.
Med., 19: 167-187.
Dorsa, W. J., 1997. New and established carcass
decontamination procedures commonly used in the beefprocessing industry. J. Food Prot., 60: 1146-1151.
Doyle, M. P., L. R. Beuchat and T. J. Montville (Eds,), 1997.
Food Microbiology: Fundamentals and Frontiers. ASM
Press, Washington DC.
Farkas, J., 1998. Irradiation as a method for decontaminating
food; A review. Int. J. Food Microbiol., 44,:189-204.
Food Regulation Review Committee, 1998. Food a growth
industry: the report of the Food Regulation Review. Food
Regulation Review Committee, Canberra.
Garber, L., S. Wells, L. Schroeder-Tucker and K. Ferris,
1999. Factors associated with faecal shedding of
verotoxin-producing Escherichia coli O157 on dairy
farms. J. Food Prot. 62: 307-312.
Gill, C. O. and T. Jones, 1997. Assessment of the hygienic
performance of an air-cooling process for lamb carcasses
and a spray-cooling process for pig carcasses. Int. J. Food
Microbiol., 38: 85-93.
Grau, F. H., 1988. Campylobacter jejuni and Campylobacter
hyointestinalis in the intestinal tract and on the carcasses
of calves and cattle. J. Food Prot., 51: 857-861.
Grau, F. H., L. E. Brownlie and E. A. Roberts, 1968. Effect
of some preslaughter treatments on the Salmonella
population in the bovine rumen and faeces. J. App.
Bacteriol., 31: 157-163.
Grau, F.H. and M. G. Smith,
1974. Salmonella
contamination of sheep and mutton carcasses related to
Asian-Aus. J. Anim. Sci. 13 Supplement July 2000 C: 376-385
pre-slaughter holding conditions. J. Appl. Bacteriol., 37:
111-116.
Griffin, J. M., S. W. Martin, M. A. Thorburn, J. A. Eves and
R. F. Hammond, 1996. A case-control study on the
association of selected risk factors with the occurrence of
bovine tuberculosis in the Republic of Ireland. Prev. Vet.
Med., 27: 75-87.
Hancock, D. D., D. H. Rice, L. A. Thomas, D. A. Dargatz
and T. E. Besser, 1997. Epidemiology of Escherichia coli
O157 in feedlot cattle. J. Food Prot., 60: 462-465.
Hedberg, C. W., M. J. David, K. E. White, K. L. MacDonald
and M. T. Osterholm, 1993. Role of egg consumption in
sporadic Salmonella Enteritidis and Salmonella
Typhimurium infections in Minnesota. J. Infect. Dis.,
167: 107-111.
Hedberg, C. W., K. L. MacDonald and M. T. Osterholm,
1994. Changing epidemiology of foodborne diseases: a
Minnesota perspective. Clin. Infect. Dis., 18: 671-680.
Henessey, T. W., C. W. Hedberg and L. Slutsker, 1996. A
national outbreak of Salmonella Enteritidis infections
from ice cream. N. Eng. J. Med., 334: 1281–6.
Herriot, D. E., D. D. Hancock, E. D. Ebel, L. V. Carpenter,
D. H. Rice and T. E. Besser, 1998. Association of herd
management factor with colonisation of dairy cattle by
Shiga toxin-positive Escherichia coli O157. J. Food
Prot., 61: 802-807.
Huis in't Veld, J. H. J., R. W. A. W. Mulder and J. M. A.
Snijders, 1994. Impact of animal husbandry and slaughter
technologies on microbial contamination of meat:
monitoring and control. Meat Sci., 36: 123-154.
ICMSF, 1988. Microorganisms in foods 4. Application of the
Hazard Analysis Critical Control Point (HACCP) system
to ensure microbiological safety and quality. Blackwell
Scientific Publications, Oxford.
Jay, L. S., D. Comar and L. D. Govenlock, 1999. A video
study of Australian domestic food-handling practices. J.
Food Prot., 62: 1285-1296.
JETACAR, 1999. The use of antibiotics in food-producing
animals: antibiotic resistant bacteria in animals and
humans. Report of the Joint Expert Advisory Committee
on Antibiotic Resistance (JETACAR). Commonwealth
Department of Health and Aged Care, Commonwealth
Department of Agriculture, Fisheries and Forestry Australia.
Jordan, D. and S. A. McEwen, 1998. Effect of duration of
fasting and a short-term high-roughage ration on the
concentration of Escherichia coli biotype 1 in cattle
feces. J. Food Prot., 61: 531-534.
Jordan, D., S. A. McEwen, A. M. Lammerding, W. B.
McNab and J. B. Wilson, 1999a. A simulation model for
studying the role of pre-slaughter effects on the exposure
of beef carcasses to human microbial hazards. Prev. Vet.
Med., 41: 37-54.
Jordan, D., S. A. McEwen, W. B. McNab, A. M.
Lammerding, and J. B. Wilson, 1999b. Reliability of an
ordinal rating system for assessing the amount of mud
and feces (tag) on cattle hides at slaughter. J. Food Prot.,
62: 520-525.
Kanabel, S. J., 1995. Foodborne Illness: Role of home food
handling practices. Food Technol., 49,:119-131.
Kudva, I. T., P. G. Hatfield and C. J. Hovde, 1995. Effect of
diet on the shedding of Escherichia coli O157:H7 in a
sheep model. Appl. Environ. Microbiol., 61: 1363-1370.
Lammerding A. M., 1997. An overview of microbial food
safety risk assessment. J. Food. Protect., 60: 1420-1425.
MAFF, 1998. A Review of Antimicrobial Resistance in the
Food Chain. MAFF, UK.
Nicholls, T. J., 2000. Contamination of food is a public
health, public perception and trade issue. Aust. Vet. J.,
78: 32-33.
Noordhuizen, J. P. T. M. and K. Frankena, 1999.
Epidemiology and quality assurance: applications at farm
level. Prev. Vet. Med., 39: 93-110.
Peel, B. and G. C. Simmons, 1978. Factors in the spread of
Salmonellas in meatworks with special reference to
contamination of knives. Aust. Vet. J., 54: 106-110.
Pennington Group, 1997. Report on the circumstances
leading to the 1996 outbreak of infection with E.coli
O157 in Central Scotland, the implications for food
safety and the lessons to be learned. The Stationary
Office, Edinburgh.
Prasai, R. K., R. E. Campbell, L. R. Vogt, C. L. Kastner and
D. Y. C. Fung, 1995. Hot-fat trimming effects on the
microbiological quality of beef carcasses and subprimals.
J. Food Prot., 58: 990-992.
Rasmussen, M. A., W. C. Cray, T. A. Casey and S. C.
Whipp, 1993. Rumen contents as a reservoir of
enterohemorrhagic Escherichia coli. FEMS Microbiol.
Lett., 114: 79-84.
Ray, B., 1996. Microbial Foodborne Diseases. In
Fundamental Food Microbiology. CRC Press Inc.,
Florida.
Ridell, J. and H. Korkeala, 1993. Special treatment during
slaughter in Finland of cattle carrying an excessive load
of dung; meat hygienic aspects. Meat Sci., 35: 223-228.
Sofos, J. N. and G. C. Smith, 1998. Nonacid meat
decontamination technologies: Model studies and
commercial applications. Int. J. Food Microbiol., 44:
171-188.
Tweedle, N.E. and P. Livingstone, 1994. Bovine tuberculosis
control and eradication programs in Australia and New
Zealand. Vet. Microbiol., 40: 23-39.
United States Congress Office of Technology Assessment,
1995. Impacts of Antibiotic-Resistant Bacteria, OTA-H629. U.S. Government Printing Office, Washington, DC.
United States Department of Agriculture, 1997. Food safety
research agenda, directions for the future. USDA, Food
Safety and Inspection Service. USDA, Washington.
Waltner-Toews, D. and S. A. McEwen, 1994. Chemical
residues in foods of animal origin: overview and risk
assessment. Prev. Vet. Med., 20: 161-178.
Woodburn, M. J. and C. A. Raab, 1997. Household food
preparers’ food-safety knowledge and practices following
widely publicized outbreaks of foodborne illness. J. Food
Prot., 60: 1105-1109.
World Health Organisation, 1997. International code of
practice - general principles of food hygiene. CAC/ECP
1, Rev. 3. FAO/WHO, Rome.
Wray, C., 1987. Salmonella vaccines for cattle: their use and
future developments. State Vet. J, 41: 147-152.
Zhao, T., M. P. Doyle, B. G. Harmon, C. A. Brown, P. O. E.
Mueller, and A. H. Parks, 1998. Reduction of carriage of
enterohemorrhagic Escherichia coli O157:H7 in cattle by
inoculation with probiotic bacteria. J. Clin. Microbiol.,
36: 641-647.
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