Rev. sci. tech. Off. int. Epiz.

, 2006, 25 (2), 541-554

Salmonella contamination:
a signicant challenge to
the global marketing of animal food products
L. Plym Forshell
(1)
& M. Wierup
(2)
(1) Swedish National Food Administration, Box 622, 75126 Uppsala, Sweden
(2) Swedish University of Agricultural Sciences, Faculty of Veterinary Medicine and Animal Science,
Box 7084, 75007 Uppsala, Sweden
Summary
Salmonellosis is the most common food-borne bacterial disease in the world.
Salmonella is a signicant pathogen for food-producing animals and these
animals are the primary source of salmonellosis. It is estimated that herd
prevalence varies between 0% and 90%, depending on the animal species and
region. The pathogen is spread by trade in animals and non-heated animal food
products. The emergence of strains that are resistant to antimicrobials, often as
a result of antimicrobial usage in animals, is a public health hazard of great
concern. It is increasingly accepted that the prevalence of Salmonella in animal
production must be decreased and, in the European Union, plans to achieve this
are currently being implemented. In this paper, the authors propose various risk
mitigation strategies. Successful control must focus on a range of preventive
actions because there is no simple silver bullet solution to reduce Salmonella
contamination. The authors conclude that the key to controlling Salmonella is to
follow the general rules that have been successfully applied to other infectious
diseases.
Keywords
Animal products Antimicrobial resistance Control Disease Epidemiology
Monitoring Pre-harvest control Risk mitigation Salmonella Salmonella
contamination Salmonella pathogenicity island Salmonellosis Virulence.
Introduction
In most parts of the world, countries have seen dramatic
and continuous increases in human outbreaks of
salmonellosis, caused by infections in animals. In 2004, in
the European Union (EU) alone, 192,703 human cases of
salmonellosis were reported (17). These and similar data
from other countries almost certainly underestimate the
magnitude of the problem, as many cases of salmonellosis
are not reported. Often, the infected person does not visit
a doctor, or no specimen is obtained for laboratory tests or
laboratory ndings are not reported. Taking into account
this degree of under-reporting, the Centers for Disease
Control estimate the annual number of non-typhoidal
salmonellosis cases in the United States of America (USA)
to be approximately 1.4 million (41).
In addition to human health implications, Salmonella is a
pathogen of signicant importance in worldwide animal
production and the emergence of antibiotic-resistant
strains, due principally to the therapeutic use of
antimicrobials in animals, is a further threat to human and
animal health. Increasing attention has been focused on
the prevention and control of Salmonella in animal
production, as this is the main source of outbreaks in
humans (19, 66, 75). The need for global co-operation in
controlling salmonellosis was emphasised at an early stage
by the World Health Organization (WHO) (8). This is
readily understandable since Salmonella infections are also
spread through international trade in animal feed, live
animals and food. The control of Salmonella is thus an
urgent challenge confronted by Veterinary Services and
producers as they seek to produce safe foods of animal
origin. A stable-to-the-table approach is needed to
implement stringent disease control measures. In this
paper, the authors examine preventive measures at the pre-
harvest level.
Salmonella
Nomenclature/taxonomy
The genus Salmonella belongs to the family
Enterobacteriaceae. Salmonellae are facultative anaerobic,
Gram-negative, oxidase-negative, rod-shaped bacteria. The
genus Salmonella consists of two species, Salmonella
enterica and S. bongori. Salmonella enterica is further
divided into six subspecies:
S. enterica subsp. enterica
S. enterica subsp. salamae
S. enterica subsp. arizonae
S. enterica subsp. diarizonae
S. enterica subsp. houtenae
S. enterica subsp. indica.
More than 2,400 serovars are known. Serovars that are
frequently isolated in human or veterinary medicine have
historically been given names denoting syndrome (e.g.
S. Typhi), host-specicity (e.g. S. Choleraesuis) or the
geographical origin of the rst isolation of a new serovar
(e.g. S. Dublin).
Salmonellae cause disease in both humans and animals.
The serovar S. Typhi and most S. Paratyphi strains (A, B
and C), which cause serious systemic infections in
humans, are specic human pathogens. These pathogens
have no animal reservoir and so are not dealt with in this
paper. Instead, the authors focus on the remaining
serovars, usually known as the zoonotic Salmonella spp.,
which cause so-called non-typhoidal salmonellosis
in humans and sometimes also in animals.
Virulence
Understanding the mechanisms behind the survival of
Salmonella bacteria, as they invade an exposed animal, and
their ability to cause disease would enable researchers to
prevent much of the suffering and economic losses caused
by this pathogen. However, despite substantial research
efforts, progress has been limited. The current knowledge
may be summarised as follows.
Following oral uptake, Salmonella is successively exposed
to:
a) low pH in the stomach
b) the strong antimicrobial effect of bile
c) decreasing oxygen supply
d) normal gut ora and metabolites
e) intestinal peristalsis
f) cationic antimicrobial peptides present on the surface of
epithelial cells (50).
These encounters with stressful environments induce the
expression of a number of genes whose products are
essential for Salmonella to invade the intestinal epithelium
and infect the host.
The ability to cause disease relies on several virulence
determinants. Some of these may be seen as virulence
determinants in the broad sense, including genes involved
in nutrient biosynthesis/uptake, stress response (both in
and outside the host) and repair of cell damage. These
genes may be considered housekeeping genes and are
present in other closely related bacteria, such as Escherichia
coli (5).
Another group of virulence genes specic for the genus
Salmonella encode adaptations to overcome host defence
mechanisms and may therefore be called true virulence
determinants.
The expression of both groups of virulence genes is
regulated in response to environmental signals in the host.
The regulatory genes mediating this control may also be
considered virulence determinants (5).
The genetic control of Salmonella virulence is not fully
known. However, both plasmid and chromosomal genes
are involved. Many of the virulence genes of S. enterica are
located on pathogenicity islands of the chromosomes,
referred to as Salmonella pathogenicity islands (SPI).
These genes are believed to have been acquired by
Salmonella from other bacterial species through horizontal
gene transfer (62). They include functions such as host cell
invasion and intracellular pathogenesis. Thus far, 12
different SPI have been described. The roles of some SPI in
the pathogenesis of Salmonella spp. are well described but
the function in virulence of many genes within SPI is not
yet understood (27).
At least six serovars of Salmonella (Abortusovis,
Choleraesuis, Dublin, Enteritidis, Gallinarum/Pullorum
and Typhimurium) harbour a virulence plasmid (although
not all isolates of these serovars do). These plasmids vary
Rev. sci. tech. Off. int. Epiz., 25 (2) 542
in size among the serovars. All these plasmids contain the
Salmonella plasmid virulence (spv) locus. This locus
harbours ve genes designated spvRABCD (62). The rst
gene spvR encodes an activator of spvABCD, but the exact
function of the encoded proteins is not fully known. These
genes are induced by growth restriction, reduced nutrient
supply or lowered pH and are involved in intra-
macrophage survival of Salmonella (51).
Other virulence factors of Salmonella include
the production of endotoxins and exotoxins, and the
presence of mbriae and agellae. The role of these factors
in the pathogenesis of Salmonella spp. is not fully
established (62).
Salmonella infections
Salmonella infections in humans
Non-typhoid salmonellosis in humans is usually
manifested as a localised enterocolitis. The incubation
period ranges from ve hours (h) to seven days, but
clinical signs usually begin 12 h to 36 h after ingestion of
a contaminated food. Shorter incubation periods are
generally associated with either higher doses of the
pathogen or highly susceptible people. Clinical signs
include diarrhoea, nausea, abdominal pain, mild fever and
chills. The diarrhoea varies from a few thin vegetable-soup-
like stools to massive evacuations with accompanying
dehydration. Vomiting, prostration, anorexia, headache
and malaise may also occur. The syndrome usually lasts for
two to seven days. Systemic infections sometimes occur,
and usually involve the very young, the elderly or the
immuno-compromised. A fatal outcome is rare. The
excreta of infected patients contain large numbers of
Salmonella spp. at the onset of illness. Those numbers
decrease with the passing of time. Some patients become
carriers, and some are still excreting Salmonella spp. after
three months. Non-typhoid salmonellosis can later give
rise to chronic diseases, including localised infections in
specic tissues or organs and reactive arthritis, as well as
neurological and neuromuscular illnesses. Subclinical
infections and/or carriers also occur and investigations
have found that 7% to 66% of infected humans are
subclinical carriers (2).
Salmonella infections in animals
As with humans, Salmonella-infected animals may or may
not develop disease. Those serovars that were initially
observed to cause disease were found to be adapted to
specic animal species, that is:
S. Abortus ovis (sheep)
S. Cholerae suis (pigs)
S. Gallinarum (poultry)
S. Abortus equi (horses)
S. Dublin (cattle).
These serovars cause disease in the species to which they
are adapted and are considered less pathogenic to people.
However, when humans become infected, the same
serovars often cause severe septicaemia (1, 54). These host-
adapted serovars primarily cause abortions or severe
gastroenteritis in their animal hosts.
A group of more frequently isolated serovars, such as
S. Typhimurium, S. Enteritidis, S. Hadar and S. Infantis
(among others), readily affect both humans and animals. In
food animals, these serovars manifest themselves clinically
through per-acute septicaemia, acute enteritis or chronic
enteritis. In the subclinical form of the disease, the animal
may either have a latent infection or become a temporary
or persistent carrier (47).
The remaining, less frequently isolated serovars can
colonise animals, usually without signicant clinical signs,
but they are all considered capable of causing gastro-
intestinal infection of varying severity in humans.
In summary, in most food animal species, Salmonellae
usually establish a clinically inapparent infection of
variable duration, which is signicant as a potential
zoonosis. However, under various stress conditions,
serovars that are usually non-pathogenic may also cause
disease in food animal species.
No data are available to give the true prevalence of
Salmonella in animal production or to provide true
comparisons between countries. Existing data indicate that
the herd prevalence, depending on animal species and
region, may vary between 0% and 90% (in swine, cattle
and poultry) (10, 11, 17, 56). Interestingly, Sweden,
Finland and Norway have achieved virtually Salmonella-
free animal production as the result of an intervention
strategy, implemented some time ago, which proposed zero
tolerance for Salmonella (17).
Serovars involved in human illness
Any serovar is considered capable of causing gastro-
intestinal illness of varying severity in humans. In a global
survey covering the years 1990 and 1995, S. Enteritidis
and S. Typhimurium were the two most frequently isolated
serovars among human isolates (29). These serovars were
also the most frequently found in human outbreaks of
salmonellosis in Europe in the period 1993 to 1998, being
responsible for 77.1% of the recorded outbreaks and
occurring in a ratio of approximatively 3:1 (77). In
2004, S. Enteritidis and S. Typhimurium were still the
Rev. sci. tech. Off. int. Epiz., 25 (2) 543
most frequently reported serovars, accounting for 76% and
14%, respectively, of human isolates reported in
the EU (17).
However, the current situation could easily change, as
exemplied when an apparently new virulent strain of
S. Enteritidis appeared in the 1980s, with the ability to
infect the eggs of poultry. This resulted in a pandemic
spread, combined with severe outbreaks in poultry but
also in humans, with contaminated eggs and egg products
being the principal vehicle (30). Similarly, the spread of the
multi-antibiotic-resistant strain of S. Typhimurium (see
below) demonstrated that dynamic spread of certain
strains of Salmonella can easily occur. In particular, the
pandemic spread of S. Enteritidis prompted a more active
approach to the control of Salmonella (48).
Epidemiology
Animals infected after exposure to infected animals, feed or
environmental conditions excrete Salmonella bacteria by
faecal shedding. Faecal/intestinal contamination
of carcasses is the principal source of human food-borne
infections. The exception is when Salmonella is directly
transmitted into the food product, for example,
S. Enteritidis into eggs and sometimes other Salmonella
serovars into milk. Humans excrete the microbe as animals
do. Salmonella bacteria can survive for long periods in the
environment, although in general no significant
multiplication occurs. Salmonella infections in wild fauna,
such as rodents, are usually secondary to the infection of
farm animals, even though infection cycles may continue
independently of any continuous input of Salmonella
bacteria from farm animals, as described by Henzler and
Opitz (28). In a review on the survival of Salmonella in the
environment, Murray (43) concludes that control
of Salmonella must start with a signicant decrease in the
number of organisms that are discharged into the
environment. Animal and human faecal contamination of
water and soil is also part of the epidemiological cycle and
can contaminate, for example, vegetables, which then also
become a source of food-borne human infections.
Animal sources of food-borne salmonellosis
An EU scientic committee concluded that the food
categories that possibly pose the greatest hazard to public
health include:
raw meat and some meat products intended to be
eaten raw
raw or undercooked poultry meat products
eggs and products containing raw eggs
unpasteurised milk and some milk products.
Sprouted seeds, unpasteurised fruit juices and home-made
mayonnaise are also of concern (54).
More correctly estimating the contributions of various food
products to human outbreaks of Salmonella would require
more detailed data. Situations are likely to vary between
countries, according to different levels of Salmonella
contamination and patterns of consumption. Two
examples are available.
In the Netherlands, the estimated contributions of travel,
farm animals and various animal products towards human
salmonellosis are presented in the 2003 annual report of
the Netherlands National Institute for Public Health and
the Environment. Using typing data of Salmonella spp.
isolates from laboratory surveillance, researchers estimated
which fractions of human salmonellosis cases were
attributable to which category of farm animals and their
products, as well as which fraction was of unknown origin,
including the possible cause of travel (Fig. 1). In 2003, the
assessed total number of human salmonellosis cases
amounted to 50,000 (308 cases per 100,000 head of
population).
The estimated mean number of human cases in Denmark
(per 100,000 inhabitants) that could be attributed to
various sources is presented in Figure 2.
Transmission through trade and travelling
Salmonella is spread by the trade of live animals within and
between countries. In Europe, the spread of infection with
S. Typhimurium is typically seen as a result of trade in
calves (7), and by parent and grandparent ocks in poultry
production (45). Trade in contaminated animal feed
products has also signicantly contributed to the spread of
Salmonella (59, 66), and several large outbreaks in humans
have been traced back to contaminated animal feed (12).
However, Salmonella is also spread by non-heat-treated
animal products. In Sweden, in the 1950s, 500 people
were reported to have been infected by S. Montevideo from
meat imported from South America (55). Moreover, recent
data from Denmark estimate the contribution from
imported non-heat-treated meat (duck, turkey, chicken,
beef and pork) to human cases of salmonellosis to be
between 13.8% and 26.8% (Fig. 2).
Many countries have trade restrictions for Salmonella and
trade between countries has often been interrupted by
Salmonella-contaminated consignments (40). There have
also been numerous alerts concerning Salmonella-
contaminated meat, meat products and poultry notied
through the rapid alert system for food and feed
(RASFF) (49).
Salmonella is additionally spread between countries by
humans as a result of food-borne infections acquired
Rev. sci. tech. Off. int. Epiz., 25 (2) 544
Rev. sci. tech. Off. int. Epiz., 25 (2) 545
0
1,000
2,000
3,000
4,000
5,000
6,000
7,000
8,000
9,000
1985 1987 1989 1991 1993 1995 1997 1999 2001 2003 2005
0
25,000
50,000
75,000
100,000
125,000
150,000
Broilers/products Layers/eggs Pigs Cattle Travel/other
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Year
Travel
(mean: 26.6%)
Imported duck
(0.1%-0.8%)
Outbreaks of unknown source
(3.3%)
Unknown
(23.9%-31.3%)
Pork
(7.1%-11.4%) Beef
(1.0%-2.0%)
Table eggs
(5.0%-8.2%)
Imported pork
(4.4%-8.7%)
Ducks
(0.2%-1.7%)
Broilers
(2.4%-6.5%)
Imported beef
(0.4%-0.9%)
Imported chicken
(7.1%-12.1%)
Imported turkey
(1.8%-4.3%)
Fig. 1
Estimated contributions of travel and farm animals and their products to laboratory-conrmed human salmonellosis cases and
estimated salmonellosis cases in the general population of the Netherlands, 1995-2005 (33, 34)
Fig. 2
Estimated sources of 1,538 cases of human salmonellosis in Denmark, 2004 (3)
abroad. The overall importance of this route of
transmission may reect the prevalence of Salmonella
contamination of food (including food of animal origin) in
a particular country. In low-prevalence countries, such as
Finland, Norway and Sweden, > 80% of human cases of
salmonellosis are attributed to visits abroad (3). This is in
marked contrast to countries such as Denmark and the
Netherlands (Figs 1 and 2), where roughly the opposite
situation exists.
Risk mitigation options
In 1980, WHO had already formulated three lines of
defence against Salmonella, which still comprise valid
strategic approaches to risk mitigation (71):
a) the rst approach focuses on controlling Salmonella in
the food-producing animal (pre-harvest control)
b) the second approach involves improving hygiene during
the slaughter and further processing of the meat (harvest
control)
c) the third approach targets the nal preparation of food
by educating the food industry and consumers about good
hygiene practices (post-harvest control).
Successful prevention of food-borne salmonellosis
originating from animal production must involve all three
lines of defence. The previously supported strategy that it
is possible to control Salmonella only at consumer level, i.e.
only at the third line of defence, has been abandoned (67).
Pre-harvest control of Salmonella at the farm level has long
been considered an important part of pathogen reduction
schemes (61), not least because traditional meat inspection
cannot control Salmonella-contaminated carcasses. Indeed,
the latter demonstrate how the industrialisation of animal
production opened the door of the food chain to
pathogens like Salmonella.
Pre-harvest control
General aspects
There have been numerous international workshops and
consultations on microbiological control and Salmonella
reduction schemes in farming (35, 72, 73, 74, 75, 76). In
addition, national inquiries directed principally at
controlling Salmonella in poultry have been conducted in
several countries in Europe, as well as Canada and the
USA. A presentation of the Swedish Salmonella
programme, supported by WHO, was of special
interest (45).
In a review for the World Organisation for Animal Health
(OIE) (66), on knowledge and experience in the
prevention of salmonellosis on livestock farms, it was
concluded that Salmonella control programmes should
follow the same general rules that have been successfully
applied to other infectious diseases (69). It is fundamental
that monitoring programmes should be established to
identify Salmonella-infected herds and animals and that
efforts are made to nd and control the sources of infection
and prevent further spread. The ultimate objective is to
produce Salmonella-free animals. It should also be
emphasised that Salmonella is a pathogen and not a
ubiquitous bacterium or a normal inhabitant of the
intestinal ora of domestic animals, as has sometimes been
claimed previously (66).
Specic aspects
Serovars to be controlled
Since any serovar, including those that infect animals or
colonise their intestine, is a potential hazard to human
health, measures to prevent food-borne salmonellosis must
be directed at all serovars of Salmonella. However, a
Salmonella reduction strategy which is limited to a few
selected serovars should also have a preventive effect on
most other serovars since the same advice for reducing any
serovar applies. If such a strategy is implemented, a
supporting surveillance programme will also be needed to
detect the prevalence of zoonotic serovars and prevent
their build-up in the production chain. If no interventions
are made at this early stage, these serovars could later
spread widely, perhaps reaching epidemic proportions.
Live animals as a source of infection
Salmonella-infected food-producing animals excrete
Salmonella bacteria in large numbers, sometimes
intermittently during their entire economic life. Excreted
bacteria infect neighbouring animals on the farm and
contamination of the environment takes place, with
infections being transmitted to rodents and other wild
fauna. When moved, the Salmonella-infected animals are
effective at introducing the infection into their new
holdings.
In the absence of guaranteed Salmonella-free replacement
animals, other methods must be used to limit the risk of
introducing Salmonella with incoming animals. In general,
animals should be introduced only from herds of the same
or a higher health status. Integrated production limits the
need to introduce animals from other herds and thus the
risk of introducing Salmonella-infected livestock.
Networking between producers is an effective way to
prevent respiratory and enteric infections in pig
production, and should also prove suitable for limiting the
risk of Salmonella.
Rev. sci. tech. Off. int. Epiz., 25 (2) 546
Diagnosis and monitoring methods
To combat the source of infection, the rst requirement is
to identify all Salmonella-infected animals on a livestock
farm. Methods for this have been summarised in a WHO
consultation report (76) on poultry production.
Corresponding detailed guidelines have not yet been
developed for other areas, e.g. for swine or beef/dairy
production, but have long been applied successfully in
Scandinavian countries.
Two principal methods are available:
bacteriological
immunological.
Bacteriological methods express the actual infection status
of the animal, including recent transmission or
contamination. They detect all serovars. The actual
infectious agent (or, in the case of multiple infections,
agents) is isolated, which makes further characterisation
(e.g. serovar and antimicrobial resistance prole) possible.
However, the analytical procedure is laborious.
Immunological methods identify previous exposure by
detecting the presence of specific antibodies against
Salmonella. This method can identify carriers or animals
that are already clear of infection. It detects only those
(most common) serogroups (O-antigens) included in the
test and therefore new emerging serovars may not be
detected. These methods are automated and less laborious.
A control programme also needs a supporting monitoring
programme. Monitoring using bacteriological methods is
needed to obtain a true picture of Salmonella status (38).
Serological methods can be recommended, especially in
medium- and high-prevalence countries, since they are
cheap, fast and suitable for large-scale use, but their
limitations should also be considered. They should be
supplemented by the strategic use of bacteriological
methods to ensure that emerging serovars, which might
not otherwise be included in the tests, are also detected.
Hygiene and husbandry
Optimal hygiene and management routines are of major
importance in aiding animals to withstand exposure to
Salmonella, and to minimise the possible subsequent
spread of the agent on the farm. Improvements in hygiene
and management procedures must be continually
implemented as a natural part of Salmonella control.
Guidelines and recommendations have been presented by
WHO (72), Blood and Radostits (7) and Schwartz (53).
Raising livestock in separate groups, without mixing
animals from different sources and ages, has proved to be
an effective health measure. The all-in, all-out system,
with careful cleaning and disinfection between batches, has
long been essential in broiler production (6), and is now
also routine in Salmonella control programmes for beef and
swine production. (This involves entirely emptying the
stable/pen of animals before any new ones are introduced,
so that infection cannot be passed on to incoming
livestock.)
Violating these procedures has been empirically shown to
result in deteriorating health status. In the advanced
Salmonella control policies applied in poultry production,
good hygiene routines have proved to be of basic
importance (66). In a study involving several EU Member
States, it was found that the risk of swine at slaughter
testing seropositive for Salmonella infection was twice as
high in herds with a continuous production system as in
herds with a batch production system (37). The
importance of providing good herd and pen hygiene in pig
production, especially by limiting the faecal-oral
transmission route, is further emphasised in a recent report
by the European Food Safety Authority (EFSA) (16).
The control and eradication of immunodeciency-causing
diseases have been found to have signicant health-
supporting effects, in addition to the direct gains due to the
absence of clinical disease. These diseases include the
following:
bovine virus diarrhoea
enzootic bovine leukosis
caprine arthritis/encephalitis in goats
maedi-visna in sheep
infectious bursal disease in poultry
Aujeszkys disease (pseudorabies) in pigs.
Other enzootic diseases can thus predispose or increase the
susceptibility of animals to Salmonella exposure.
Biosecurity systems should also prevent the introduction of
Salmonella into a herd through, for example, wild animals,
visitors or machinery (63). The importance of hygienic
handling of manure is obvious, particularly considering
that Salmonella is transmitted by faecal shedding and that
the average number of animals per farm is increasing.
Jones (31) reviewed the question of Salmonella in animal
waste and presented recommendations for the storage and
spread of manure, especially slurry.
According to several studies, improving hygiene and
husbandry management programmes, as described above,
is generally very cost effective (64).
Feed
In all countries, there is a constant risk that animals will be
exposed to Salmonella through their feed (14, 21).
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Rev. sci. tech. Off. int. Epiz., 25 (2) 548
Considerable efforts should therefore be made to limit this
exposure to an absolute minimum. Feed controls should
follow the procedure described by Hggblom (24, 25). As
Salmonella can seldom be detected in the nal feed, unless
the feed is heavily contaminated, it cannot be emphasised
enough that control measures must be implemented before
that stage. Programmes to prevent Salmonella in feedstuffs
must be based on detecting the bacterium as early as
possible in the production chain. A protocol involving
hazard analysis at critical control points in the feed mill,
including procedures for efficient cleaning and
disinfection, should ensure that the processing line is not
contaminated with Salmonella (59).
As shown by Edel et al. (13), pelleting can greatly reduce
Salmonella contamination of the nished feed.
Certain feeds, such as fermented liquid feed used as a wet
feeding system, and acidied feed or drinking water, have
been found to reduce Salmonella in pig production (63).
Competitive exclusion
The use of competitive exclusion, in which the normal
intestinal flora protects the host against invading
pathogens, is a valuable part of Salmonella control in
poultry farming. Competitive exclusion cultures have been
used and tested in various countries, as reviewed by
Schneitz and Mead (52). Positive results from the use of
competitive exclusion have also been reported in pigs (22).
Vaccines
Many efforts have been made to nd effective vaccines
against Salmonella infections, especially in cattle and
poultry but also in swine. A live attenuated vaccine against
S. Gallinarum in poultry is available and there is currently
demand for a vaccine to control Salmonella infections
associated with human food poisoning, in particular,
S. Enteritidis (20). However, due to the complicated
pathogenesis of Salmonella infection, no significant
breakthrough has been achieved (9). Vaccines to control
Salmonella infections, especially inactivated vaccines, are in
use all over the world. In recent years, increasing numbers
of live vaccines have been developed but most of them are
not yet authorised. Vaccination can play an important role
in intervening against Salmonella in high-prevalence herds
(23, 39, 46, 58). However, immunisation should not be
conducted in isolation but always in combination with
other measures, such as veterinary hygiene and improved
management.
Antimicrobials
The use of antimicrobials to prevent suffering and
economic losses in individual animals and herds can be
justied, but should always be combined with other
Salmonella reduction measures. Antibiotics have sometimes
been used to prevent animals shedding Salmonella (36),
but the use of antibiotics in pigs with enterocolitis has not
been found to reduce the prevalence, magnitude or
duration of Salmonella shedding by sick or recovered
animals (70). Earlier, similar observations were made for
experimental and natural S. Dublin infections in cattle
(65). Both these ndings agree with results from the use of
antibiotics in human salmonellosis, i.e. that they have long
been recognised to prolong the carrier state (4).
The use of antimicrobials for therapy or growth promotion
may also disrupt the gut ora, which often increases the
susceptibility of pigs to Salmonella infection. The use of
antibiotics may thus act as a trigger to spread Salmonella
infection throughout a herd, which would not have
occurred if the animals remained untreated. This
phenomenon has been thoroughly documented in poultry
(57) and is also likely to occur in other animal species. The
EFSA recently gave an opinion on the use of antibiotics to
control Salmonella in poultry (15), which concurred with
that of WHO (74), i.e. that Salmonella control should not
be based on antibiotics. The emergence of antibiotic
resistance is another serious reason why antibiotics should
be used with great care, as demonstrated by the emergence
and fast spread of the multi-resistant S. Typhimurium
denitive phage type (DT) 104 (60).
In developed countries, it is also becoming increasingly
accepted that a majority of the resistant strains of zoonotic
Salmonella spp. have acquired that resistance in an animal
host before being transmitted to humans through the food
chain (42, 60). The prevalence of resistant isolates in
countries where intensive animal production is practised is
between 10% and 30%. When herds are held under strong
antibiotic selective pressures, due to the intensive use of
antibiotics, the prevalence of resistant strains rises to
between 60% and 90% (26). As these bacterial strains are
of considerable potential clinical importance to human
health, this is a matter of real concern.
Strategies for implementation
The implementation of the mitigation options summarised
above should all have a Salmonella-preventing effect.
However, effective interventions also need specic targets
and strategies for their application. In addition, if
Salmonella does occur, despite these interventions, a
progressive disease control plan should already have been
prepared. Possible strategies for such approaches to control
Salmonella have previously been formulated (66, 68). An
intervention strategy should be based on the situation in
the targeted herd, region or country.
In summary, the control of Salmonella at pre-harvest level
must focus on preventive action because there is no silver
bullet through which the level of Salmonella
contamination can be simply reduced. No single vaccine
Rev. sci. tech. Off. int. Epiz., 25 (2) 549
can prevent the infection, and the use of antimicrobials
not only results in prolonged carriership but is also
associated with the risk of developing antimicrobial-
resistant strains. Both consequences pose public health
hazards. Preventive action should follow the general rules
that have already been successfully applied to control other
infectious diseases.
In poultry production, rapid and positive results were
demonstrated after the introduction of nationwide
Salmonella reduction schemes. In Denmark, the prevalence
of infection in broiler ocks declined from 12.9% in 1997
to 1.5% in 2002, resulting in an estimated 78% reduction
of human cases related to domestically produced poultry
products (44). Corresponding results have also been
demonstrated in swine production, e.g. from Denmark
(10). However, due to the more complex nature of swine,
beef and dairy production, achieving positive results on a
national basis would probably require a more long-term
control programme, covering all steps of the production
chain (32). A step-by-step approach to targeted
interventions is advisable. The results should be viewed
from a long-term perspective and the programme should
be regularly re-evaluated to ensure compliance, efcacy
and modication, if necessary.
Valuable experience can be gained from the EU, whose
focus on preventing the spread of Salmonella in poultry is
now directed to other animal species. Detailed rules are
being established for harmonised Salmonella monitoring
throughout the Community, to be followed by targets for
reducing the prevalence of Salmonella serotypes with
public health signicance in pig herds. These will be based
on appropriate legislation (18, 19). Within 18 months of
these targets being set, Member States shall prepare and
submit national control programmes to be approved by the
Commission. The deadline for setting targets in pig
production is December 2007 for breeding pigs and
December 2008 for slaughter pigs.
Follow-up at harvest and post-harvest levels
If such pre-harvest Salmonella reduction interventions are
supported by similar measures at harvest and post-harvest
levels (which are, however, outside the scope of this
paper), human exposure to Salmonella bacteria from
animal food products should be considerably reduced. In
Denmark, the herd prevalence of Salmonella in swine is
estimated to have decreased from 22% to 11% in the four
years following the implementation (1993/1994) of a
Salmonella control programme (10). Through further
interventions during slaughter, primarily hygienic killing
procedures which avoid faecal contamination of carcasses,
the prevalence of Salmonella in swine carcasses has been
brought down to approximately 1% (17).
Infection Salmonella : une grave menace pour le commerce
mondial des produits alimentaires dorigine animale
L. Plym Forshell & M. Wierup
Rsum
La salmonellose constitue la maladie bactrienne dorigine alimentaire la plus
frquente du monde. Salmonella est un agent pathogne important des animaux
destins la consommation et ces animaux sont la source principale de
salmonellose. Selon les estimations, la prvalence lchelle des troupeaux
varie entre 0 et 90 %, selon lespce animale et la rgion. Lagent pathogne se
propage lors du commerce danimaux et de produits alimentaires dorigine
animale non cuits. Lapparition de souches rsistantes aux antimicrobiens,
souvent la suite de lutilisation dantimicrobiens chez les animaux, reprsente
une menace grave pour la sant publique. Il est de plus en plus admis que la
prvalence de Salmonella dans la production animale doit tre rduite et, dans
lUnion europenne, des plans visant cet objectif sont actuellement mis en
uvre. Dans cet article, les auteurs proposent diffrentes stratgies
dattnuation du risque. Une prophylaxie russie doit tre axe sur un ensemble
dactions prventives car il nexiste pas de solution miracle pour rduire la
contamination par Salmonella. Les auteurs concluent que pour lutter contre
Salmonella, il faut suivre les rgles gnrales qui ont t appliques avec
succs dautres maladies infectieuses.
Mots-cls
Attnuation du risque pidmiologie lot de pathognicit lis Salmonella
Maladie Produit dorigine animale Prophylaxie Prophylaxie avant abattage
Rsistance aux antimicrobiens Salmonella Salmonellose Suivi Virulence.
Rev. sci. tech. Off. int. Epiz., 25 (2) 550
La salmonelosis: un importante problema para la comercializacin
a escala mundial de productos alimentarios de origen animal
L. Plym Forshell & M. Wierup
Resumen
La salmonelosis es la ms frecuente de las enfermedades bacterianas que se
transmiten por va alimentaria en el mundo. Salmonella es un patgeno
importante para los animales de los que se alimenta el hombre, animales que son
a su vez la fuente primaria de salmonelosis. Se estima que la prevalencia del
patgeno en los rebaos oscila entre un 0% y un 90%, segn la especie animal y
la regin de que se trate. La actividad comercial es el cauce por el que las
salmonelas se transmiten entre animales y contaminan productos alimentarios
no cocinados. La aparicin de cepas resistentes a los antimicrobianos, que
suele ser consecuencia del uso de estos frmacos en animales, constituye un
riesgo de salud pblica que suscita gran preocupacin. Cada vez est ms claro
que hay que reducir la prevalencia de Salmonella en la produccin animal, y
actualmente se estn aplicando planes para lograr ese objetivo en la Unin
Europea. Los autores proponen varias estrategias para mitigar riesgos. Dado
que no existe una nica solucin mgica que pueda reducir los niveles de
contaminacin, la lucha contra la enfermedad, para resultar ecaz, debe
integrar un conjunto de medidas preventivas. Los autores llegan a la conclusin
de que la clave para luchar contra Salmonella estriba en seguir las reglas
generales que se han aplicado con xito en el caso de otras enfermedades
infecciosas.
Palabras clave
Control Control previo al sacrificio Enfermedad Epidemiologa Isla de
patogenicidad de Salmonella Mitigacin de riesgos Productos de origen animal
Resistencia a los antimicrobianos Salmonella Salmonelosis Vigilancia Virulencia.
Rev. sci. tech. Off. int. Epiz., 25 (2) 551
References
1. Acha P.N. & Szyfres B. (1987). Salmonella. In Zoonoses and
communicable diseases common to man and animals.
Pan American Health Organization (PAHO), Washington,
DC, 147-155.
2. Anon. (1999). Salmonella, strategidokument [in Swedish].
Socialstyrelsen, Stockholm.
3. Anon. (2005). Erratum. In Annual report of zoonoses in
Denmark 2004. Ministry of Family and Consumer Affairs,
Copenhagen, 11-12.
4. Aserkoff B. & Bennett J.V. (1969). Effect of antibiotic
therapy in acute salmonellosis on the fecal excretion of
salmonellae. N. Engl. J. Med., 281 (12), 636-640.
5. Bumler A.J., Tsolis R.M. & Heffron F. (2000). Virulence
mechanisms of Salmonella and their genetic basis. In
Salmonella in domestic animals (C. Wray & A. Wray, eds).
CABI Publishing, Wallingford, Oxfordshire, 57-72.
6. Berndtson E. (1996). Campylobacter in broiler chickens: the
mode of spread in chicken ocks with special reference to
food hygiene. Dissertation. Swedish University of
Agricultural Sciences, Uppsala, Sweden.
7. Blood D.C. & Radostits O.M. (1989). Diseases caused by
bacteria, III. In Veterinary medicine: a textbook of the
diseases of cattle, sheep, pigs, goats and horses (D.C. Blood,
O.M. Radostits, J.H. Arundel & C.C. Gay, eds), 7th Ed.
Ballire Tindall, London, 643-655.
8. Bgel K. (1991). Global cooperation in the control of
salmonellosis. In Proc. Symposium on the Diagnosis and
Control of Salmonella (G.H. Snoeyenbos, ed.), San Diego,
California, 29 October. United States Animal Health
Association, Richmond, Virginia, 1-5.
9. Chiu C.H., Su L.H. & Chu C. (2004). Salmonella enterica
serotype Choleraesuis: epidemiology, pathogenesis, clinical
disease, and treatment. Clin. Microbiol. Rev., 17 (2), 311-322.
10. Christensen J., Baggesen D.L., Nielsen B. & Stryhn H. (2002).
Herd prevalence of Salmonella spp. in Danish pig herds after
implementation of the Danish Salmonella control program
with reference to a pre-implementation study. Vet. Microbiol.,
88 (2), 175-188.
11. Cook A.J.C., Miller A., Snow L. & Davies R.H. (2005).
Epidemiological studies of Salmonella infection in pigs.
In Proc. Med-Vet-Net 1st General Scientific Meeting,
Winchester, United Kingdom, 29 June 1 July. Available at:
www.medvetnet.org/cms/ (accessed on 13 July 2006).
12. Crump J.A., Grifn P.M. & Angulo F.J. (2002). Bacterial
contamination of animal feed and its relationship to human
foodborne illness. Clin. infect. Dis., 35 (7), 859-865. Epub.:
5 September 2002.
13. Edel W., van Schothorst M., Guinee P.A.M. &
Kampelmacher E.H. (1970). Effect of feeding pellets on the
prevention and sanitation of Salmonella infections in fattening
pigs. Zentralbl. Veterinrmed., B, 17 (7), 730-738.
14. Edel W., van Schothorst M., Guinee P.A.M. &
Kampelmacher E.H. (1974). Salmonella in pigs on farms
feeding pellets and on farms feeding meal. Zentralbl.
Bakteriol., Orig. A, 226 (3), 314-323.
15. European Food Safety Authority (EFSA) (2004). Opinion of
the scientic panel on biological hazards on a request from
the Commission related to the use of antimicrobials for the
control of Salmonella in poultry. EFSA J., 115, 1-76.
16. European Food Safety Authority (EFSA) (2005). Opinion of
the scientic panel on animal health and welfare on a request
from the Commission related to welfare of weaners and
rearing pigs: effects of different space allowances and oor
types. Adopted on 13 September, Question No. EFSA-Q-
2004-077. Available at www.efsa.eu.int/science/ahaw/ahaw
_opinions/1203_en.html (accessed on 23 April 2005).
17. European Food Safety Authority (EFSA) (2006). Trends and
sources of zoonoses, zoonotic agents and antimicrobial
resistance in the European Union in 2004. EFSA J.,
310, 10; 23-95.
18. European Union (2003). Directive 2003/99/EC of the
European Parliament and of the Council of 17 November
2003 on the monitoring of zoonoses and zoonotic agents,
amending Council Decision 90/424/EEC and repealing
Council Directive 92/117/EEC. Off. J. Eur. Union,
L 325 of 12.12.2003, 31-40.
19. European Union (2003). Regulation (EC) No. 2160/2003 of
the European Parliament and of the Council of 17 November
2003 on the control of salmonella and other specied food-
borne zoonotic agents. Off. J. Eur. Union, L 325 of
12.12.2003, 1-15.
20. Feberwee A., de Vries T.S., Hartman E.G., de Wit J.J., Elbers
A.R. & de Jong W.A. (2001). Vaccination against Salmonella
enteritidis in Dutch commercial layer ocks with a vaccine
based on a live Salmonella gallinarum 9R strain: evaluation of
efcacy, safety, and performance of serologic Salmonella tests.
Avian Dis., 45 (1), 83-91.
21. Fedorka-Cray P.J., Hogg A., Gray J.T., Lorenzen K., Velasquez
J. & von Behren P. (1997). Feed and feed trucks as sources
of Salmonella contamination in swine. J. Swine Hlth Prod.,
5 (5), 189-193.
22. Genovese K.J., Anderson R.C., Harvey R.B., Callaway T.R.,
Poole T.L., Edrington T.S., Fedorka-Cray P.J. & Nisbet D.J.S.
(2003). Competitive exclusion of Salmonella from the gut of
neonatal and weaned pigs. J. Food Protec., 66 (8), 1353-1359.
Rev. sci. tech. Off. int. Epiz., 25 (2) 552
23. Haesebrouck F., Pasmans F., Chiers K., Maes D., Ducatelle R.
& Decostre A. (2004). Efcacy of vaccines against bacterial
diseases in swine: what can we expect? Vet. Microbiol.,
100 (3-4), 255-268.
24. Hggblom P. (1994). Cleaning of feed mills. In Report of the
National Veterinary Institute (NVI) (Sweden)/World Health
Organization (WHO) International Course on Salmonella
control in animal production and products (S. ijeberg-
Bengtsson, ed.), Malm, Sweden, 21-27 August 1993.
WHO/CDS/ VPH/93.126. NVI, Uppsala, Sweden, 185-
188. Available at: www.sva.se (accessed on 13 July 2006).
25. Hggblom P. (1994). Monitoring and control of Salmonella
in animal feed. In Report of the National Veterinary Institute
(NVI) (Sweden)/World Health Organization (WHO)
International Course on Salmonella control in animal
production and products (S. ijeberg-Bengtsson, ed.),
Malm, Sweden, 21-27 August 1993. WHO/CDS/VPH/
93.126. NVI, Uppsala, Sweden, 127-137. Available at:
www.sva.se (accessed on 13 July 2006).
26. Helmuth R. (2000). Antibiotic resistance in Salmonella.
In Salmonella in domestic animals (C. Wray & A. Wray, eds).
CABI Publishing, Wallingford, Oxfordshire, 89-106.
27. Hensel M. (2004). Evolution of pathogenicity islands of
Salmonella enterica. Int. J. med. Microbiol., 294 (2-3), 95-102.
28. Henzler D.J. & Opitz H.M. (1992). The role of mice in the
epizootiology of Salmonella enteritidis infection on chicken
layer farms. Avian Dis., 36 (3), 625-631.
29. Herikstad H., Motarjemi Y. & Tauxe R.V. (2002). Salmonella
surveillance: a global survey of public health serotyping.
Epidemiol. Infect., 129 (1), 1-8.
30. Humphrey T. (2000). Public-health aspects of Salmonella
infection. In Salmonella in domestic animals (C. Wray &
A. Wray, eds). CABI Publishing, Wallingford, Oxfordshire,
245-263.
31. Jones P.W. (1992). Salmonellas in animal wastes and
hazards for other animals and humans from handling animal
wastes. In Proc. Int. Symposium on Salmonella and
salmonellosis, Ploufragan, France, 15-17 September.
Zoopole, Ploufragan, 280-284.
32. Kaesbohrer A. (1999). Control strategies for Salmonella in
the pig to pork chain in the European Union. In Proc. 3rd
International Symposium on the epidemiology and control of
Salmonella in pork (ISECSP), Washington, DC, 5-7 August.
College of Veterinary Medicine, University of Illinois, Urbana-
Champaign, United States of America, 358-361.
33. Korver H., Mooijman K.A., Nagelkerke N.J.D., van de
Giessen A.W. & Henken A.M. (2003). European Union
collaborative study VI (2002) on bacteriological detection of
Salmonella spp. Report No. 330300 001. National Institute
for Public Health and the Environment, Bilthoven, the
Netherlands.
34. Korver H., Nagelkerke N.J.D., van de Giessen A.W. &
Mooijman K.A. (2005). European Union interlaboratory
comparison study VII (2003) on bacteriological detection of
Salmonella spp. Report No. 330300 004. National Institute
for Public Health and the Environment, Bilthoven, the
Netherlands.
35. Larsen E. (ed.) (1984). Priority aspects of salmonellosis
research. Commission of the European Communities (CEC),
Luxembourg.
36. Laval A., Morvan H., Disperez G. & Corbion B. (1992).
Salmonellosis in swine. In Proc. International Symposium on
Salmonella and salmonellosis, Ploufragan, France,
15-17 September. Zoopole, Ploufragan, 164-175.
37. Lo Fo Wong D.M., Dahl J., von Altrock A., Grafanakis S.,
Thorberg B.M. & van der Wolf P.J. (1999). Herd-level risk
factors for the introduction and spread of Salmonella in pig
herds. In Proc. 3rd International Symposium on the
epidemiology and control of Salmonella in pork (ISECSP),
Washington, DC, 5-7 August. College of Veterinary Medicine,
University of Illinois, Urbana-Champaign, United States of
America, 151-154.
38. Lo Fo Wong D.M., Dahl J., Stege H., van der Wolf P.J.,
Leontides L., von Altrock A. & Thorberg B.M. (2004).
Herd-level risk factors for subclinical Salmonella infection in
European finishing-pig herds. Prev. vet. Med., 62 (4),
253-266.
39. Lumsden J.S. & Wilkie B.N. (1992). Immune response of
pigs to parenteral vaccination with an aromatic-dependent
mutant of Salmonella typhimurium. Can. J. vet. Res., 56 (4),
296-302.
40. Matthews K.H. Jr., Bernstein J. & Buzby J.C. (2003).
International trade of meat/poultry products and food safety
issues. In International trade and food safety: economic
theory and case studies (J.C. Buzby, ed.), Chapter 4. United
States Department of Agriculture (USDA)/Economic Research
Service (ERS) Agricultural Economic Report No. 828.
USDA/ERS, Washington, DC, 48-74.
41. Mead P.S., Slutsker L., Dietz V., McCaig L.F., Bresee J.S.,
Shapiro C., Grifn P.M. & Tauxe R.V. (1999). Food-related
illness and death in the United States. Emerg. infect. Dis.,
5 (5), 607-625.
42. Mlbak K., Gerner-Smidt P. & Wegener H.C. (2002).
Increasing quinolone resistance in Salmonella enterica
serotype Enteritidis. Emerg. infect. Dis., 8 (5), 514-515.
43. Murray C.J. (1991). Salmonellae in the environment.
In Animals, pathogens and the environment. Rev. sci. tech. Off.
int. Epiz., 10 (3), 765-785.
44. Mygind J. (2004). The Danish Salmonella control
programme for the production of table eggs and broilers: an
overview. In Proc. Symposium of the Public Danish Plan for
control of Salmonella in poultry, Danish Veterinary and Food
Administration, Copenhagen, 23 March. Available at:
http://www.uk.foedevarestyrelsen.dk/Animal/Zoonoses/Symp
osium_on_Salmonella_Control.htm (accessed in 2006).
Rev. sci. tech. Off. int. Epiz., 25 (2) 553
45. National Veterinary Institute (NVI) (Sweden)/World Health
Organization (WHO) (1993). Report of the National
Veterinary Institute (NVI) (Sweden)/World Health
Organization (WHO) International Course on Salmonella
control in animal production and products (S. ijeberg-
Bengtsson, ed.), Malm, Sweden, 21-27 August 1993.
WHO/CDS/ VPH/93.126. NVI, Uppsala, Sweden. Available
at: www.sva.se (accessed on 13 July 2006).
46. Ortmann R. (1999). Immunisierungsversuche mit der
Salmonella Typhimurium Lebendvakzine Salmoporc R zur
Bekmpfung von Salmonellen Infektionen in
Ferkelerzeugerbetrieben. Hanover, Tierarztl. Hochsch., Diss.,
1999.
47. Quinn P.J., Markey B.K., Carter M.E., Donnelly W.J.C. &
Leonard F.C. (2002). Veterinary microbiology and microbial
disease. Blackwell Science, Oxford.
48. Rabsch W., Tschpe H. & Bumler A.J. (2001). Non-
typhoidal salmonellosis: emerging problems. Microbes Infect.,
3 (3), 237-247.
49. Rapid Alert System for Food and Feed (RASFF) (2005).
Annual report of the functioning of the RASFF 2002, 2003,
2004. Available at: http://europa.eu.int/comm/food/
rapidalert/resources/publications_en.htm_(accessed in 2006).
50. Rychlik I. & Barrow P.A. (2005). Salmonella stress
management and its relevance to behaviour during intestinal
colonisation and infection. FEMS Microbiol. Rev., 29 (5),
1021-1040. Epub.: 29 June 2005.
51. Rychlik I., Gregorova D. & Hradecka H. (2006).
Distribution and function of plasmids in Salmonella enterica.
Vet. Microbiol., 112 (1), 1-10. Epub.: 21 November 2005.
52. Schneitz C. & Mead G.C. (2000). Competitive exclusion. In
Salmonella in domestic animals (C. Wray & A. Wray, eds).
CABI Publishing, Wallingford, Oxfordshire, 301-322.
53. Schwartz K.J. (1999). Salmonellosis. In Diseases of swine
(B.E. Straw, S. DAllaire, W.L. Mengeling & D.J. Taylor, eds),
8th Ed. Blackwell Science, Oxford, 535-551.
54. Scientic Committee on Veterinary Measures relating to
Public Health (SCVPH) (2003). European Union
(EU)/SANCO. Opinion of the SCVPH on Salmonellae in
foodstuffs. Adopted on 14-15 April. SCVPH, Brussels.
55. Silverstolpe L. & Wranne N. (1955). Salmonella outbreaks
in Sweden in the county of stergtland in 1953 [in
Swedish]. Nord. Hyg. Tidskr., 36 (11-12), 213-229.
56. Smith B.P., Da Roden L., Thurmond M.C., Dilling G.W.,
Konrad H., Pelton J.A. & Picanso J.P. (1994). Prevalence of
salmonellae in cattle and in the environment on California
dairies. JAVMA, 205 (3), 467-471.
57. Smith H.W. & Tucker J.F. (1978). The effect of antimicrobial
feed additives on the colonization of the alimentary tract of
chickens by Salmonella typhimurium. J. Hyg. (Lond.), 80 (2),
217-231.
58. Springer S., Lindner T., Steinbach G. & Selbitz H.J. (2001).
Investigation of the efcacy of a genetically-stabile live
Salmonella typhimurium vaccine for use in swine. Berl. Mnch.
tierrztl. Wochenschr., 114 (9-10), 342-345.
59. Sternberg S., Boqvist S., Engstrm B. & Hggblom P. (2005).
The effective control of hazards in Swedish poultry: the case
for Sweden. In Food safety control in the poultry industry
(G.C. Mead, ed.). Woodhead Publishing, Cambridge, 195-
215.
60. Threlfall E.J. (2002). Antimicrobial drug resistance in
Salmonella: problems and perspectives in food- and water-
borne infections. FEMS Microbiol. Rev., 26 (2), 141-148.
61. United States Department of Agriculture (USDA) (1993).
Proc. World Congress on meat and poultry inspection, Texas,
10-14 October. USDA, Washington, DC.
62. Van Asten A.J.A.M. & van Dijk J.E. (2005). Distribution of
classic virulence factors among Salmonella spp. FEMS
Immunol. med. Microbiol., 44 (3), 251-259.
63. Van der Wolf P.J., Lo Fo Wong D.M., Wolbers W.B., Elbers
A.R., van der Heijden H.M., van Schie F.W., Hunneman W.A.,
Willeberg P. & Tielen M.J. (2001). A longitudinal study of
Salmonella enterica infections in high- and low-seroprevalence
nishing swine herds in the Netherlands. Vet. Q., 23 (3),
116-121.
64. Wallgren P.T. (1994). The importance of diseases for daily
growth of pigs. Proc. Nord. Vet. Congr., 17 (2), 106-110.
65. Wierup M. (1983). Salmonella och antibiotika [the
influence of antibiotics on Salmonella infections] [in
Swedish]. In Allmnt Veterinrmte Kompendium. Sveriges
Veterinrfrb [Swedish Veterinary Association], Uppsala,
115-122.
66. Wierup M. (1994). Control and prevention of salmonellosis
in livestock farms. In Comprehensive report on technical
items presented to the International Committee or to
Regional Commissions. World Organisation for Animal
Health (OIE), Paris, 249-269.
67. Wierup M. (1995). Preharvest control of salmonellosis.
World Health Organisation (WHO)/USAA Consultation on
economical implication of foodborne disease and
consequences on animal production food hygiene,
Washington, DC, 8-10 June. WHO, Geneva
68. Wierup M. (1997). Principles for integrated surveillance
and control of Salmonella in swine production. In Proc. 2nd
International Symposium on epidemiology and control of
Salmonella in pork (ISECSP), Copenhagen, 20-22 August.
Danish Bacon & Meat Council, Copenhagen, 42-49.
..
69. Wierup M. (2002). Strategies for avoiding health problems
of farmed animals: sustainable animal production. In Proc.
Workshop on Sustainable Animal Production (F. Ellendorff,
V. Moennig, J. Ladewig & L. Babiuk, eds), Institute for
Animal Science and Animal Behaviour and Federal
Agricultural Research Centre (FAL), Mariensee, Germany,
4-5 September 2000. Landbauforschung (FAL), Sonderheft
227, 103-105.
70. Wilcock B.P. & Schwartz K.J. (1992). Salmonellosis. In
Diseases of swine (A. Leman, B.E. Straw, W.L. Mengelin,
S. DAllaire & D.J. Taylor, eds). Iowa State University Press,
Ames, Iowa, 570-583.
71. World Health Organization (WHO) (1980). Report of the
WHO/World Association of Veterinary Food Hygienists
(WAVFH) round table conference on the present status of the
Salmonella problem (prevention and control), Bilthoven, the
Netherlands, 6-10 October. WHO/VPH/81.27. WHO,
Bilthoven.
72. World Health Organization (WHO) (1983). Guidelines on
prevention and control of salmonellosis (A. Linton, ed.).
WHO, Geneva.
73. World Health Organization (WHO) (1989). Report of
WHO Consultation on epidemiological emergency in poultry
and egg salmonellosis, Geneva, 20-23 March. WHO, Geneva.
74. World Health Organization (WHO) (1992). Report on
WHO Consultation on national and local schemes of
Salmonella control in poultry, Ploufragan, France,
18-19 September. WHO/CDS/VPH/92.110. WHO, Geneva.
75. World Health Organization (WHO) (1993). Report of the
WHO Consultation on control of Salmonella infections in
animals: prevention of foodborne Salmonella infections in
humans, Jena, Germany, 21-26 November.
WHO/CDS/VPH/93.129. WHO, Geneva.
76. World Health Organization (WHO) (1994). Guidelines on
detection and monitoring of Salmonella infected poultry
ocks with particular reference to Salmonella Enteritidis:
report of a WHO Consultation on strategies for detection and
monitoring of Salmonella infected poultry ocks (C. Wray &
R.H. Davies, eds), Graz, Austria, 11-15 April.
WHO/ZOON/94.173. WHO Veterinary Public Health Unit,
Geneva.
77. World Health Organization (WHO) (2001). WHO
Surveillance Programme for control of foodborne infections
and intoxications in Europe, 7th Report 1993-1998
(K. Schmidt & C. Tirado, eds). Federal Institute for Health
Protection of Consumers and Veterinary Medicine, Berlin.
Rev. sci. tech. Off. int. Epiz., 25 (2) 554