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Journal of the Hellenic Veterinary Medical Society
Vol. 69, 2018
Salmonella spp. in poultry: a constant challenge
and new insights
VELHNER M. Department of clinical
microbiology, Scientific
Veterinary Institute “Novi
Sad”, Novi Sad, Serbia
MILANOV D. Department of clinical
microbiology, Scientific
Veterinary Institute “Novi
Sad”, Novi Sad, Serbia
KOZODEROVIĆ G. Faculty of Education in
Sombor, University of Novi
Sad, Serbia
http://dx.doi.org/10.12681/jhvms.18012
Copyright © 2018 M. VELHNER, D. MILANOV, G.
KOZODEROVIĆ2
To cite this article:
VELHNER, M., MILANOV, D., & KOZODEROVIĆ, G. (2018). Salmonella spp. in poultry: a constant challenge and new
insights. Journal of the Hellenic Veterinary Medical Society, 69(2), 899-910. doi:http://dx.doi.org/10.12681/jhvms.18012
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Salmonella spp. in poultry: a constant challenge and new insights
M. Velhner1, D. Milanov1, G. Kozoderović2*
1 Department of clinical microbiology, Scientic Veterinary Institute “Novi Sad”, Novi Sad, Serbia
2 Faculty of Education in Sombor, University of Novi Sad, Serbia
Corresponding Author:
Gordana Kozoderović
Faculty of Education in Sombor, University of Novi Sad,
Podgorička 4, Sombor 25000, Serbia
E-mail : gocakozoderovic@gmail.com
D a t e o f i n i t i a l s u b m i s s i o n : 3-6-2017
Date of revised submission: 21-6-2017
Date of acceptance: 14-7-2017
Review article
Ανασκόπηση
J HELLENIC VET MED SOC 2018, 69(2): 899-910
ΠΕΚΕ 2018, 69(2): 899-910
ABSTRACT. The knowledge about virulence mechanisms, resistance to antimicrobial agents and the biolm forma-
tion ability of Salmonella spp. in poultry industry has been expanded over the years. However, in spite of the research
efforts and signicant investments to improve management systems in poultry industry, it has become evident that
none of the methods applied in all stages of food production chain are 100% effective in eliminating Salmonella spp.
Different serovars are manifesting different mechanisms of invasiveness which depend on their ability to invade lower
zones of the lamina propria, their ability to gain accesses to parenchymatous organs and survive in macrophages. The
ubiquitous nature of Salmonella spp. due to their adaptation to animal and plant hosts, as well as their survival in hostile
environments and their enhanced capacity to produce biolms, contribute to a long lasting contamination of the envi-
ronment, feed and animals. The emergency and spread of antimicrobial resistances in Salmonella spp. raise additional
concerns.
Keywords: poultry, Salmonella, pathogenesis, biolm, resistance
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900 M. VELHNER, D. MILANOV, G. KOZODEROVIĆ
J HELLENIC VET MED SOC 2018, 69(2)
ΠΕΚΕ 2018, 69(2)
INTRODUCTION
Poultry farming presents one of the most important
food manufacturing industries around the
globe. Therefore, food safety standards are highly
demanding and are generally better maintained in
large scale production facilities than in small ones.
In developing countries, rearing of backyard chicken
flocks contributes to the continuous occurrence of
some viral and bacterial diseases that are less likely
present in well maintained farms. Except for a very
few countries in the world, Salmonella spp. are
detected in environmental specimens in practically
all stages of the food production chain. Out of more
than the 2600 serovars known today, only 10% are
found in the commercial poultry and egg industry.
Two of them, S. Enteritidis and S. Typhimurium, are
of paramount importance to human health and can
colonize the intestines of chickens (Velge et al., 2005).
In most cases, the infected chickens either do not have
clinical symptoms or the symptoms remain unnoticed.
With all this taken into account, it is evident that
control programs for Salmonella spp. have to be
implemented in all stages of the food production
chain, starting from animal farms. According to
European Directive 1003/2005, the occurrence of
S. Enteritidis and S. Typhimurium in adult breeder
flocks has to be < 1%, in EU member states.
However, this directive also targets serovars Hadar,
Virchow and Infantis which are of public health
significance in the EU (Carrique-Mas and Davies,
2008). It is very difcult to accomplish such a goal
in developing countries, since implementing good
management practice is expensive and requires the
participation of educated staff. Even if biosecurity
measures are well established on a farm, salmonellae
can still be found in poultry and premises.
Other available measures to cope with Salmonella
spp. in farms include the use of prebiotics and
probiotics, antimicrobial therapy and vaccination
of the birds. For serovars S. Enteritidis and S.
Typhimurium commercial inactivated and attenuated
vaccines have been developed and used widely. These
vaccines target serogroups D and B respectively,
but do not protect livestock against serovars from
other serogroups. Therefore, vaccination against S.
Enteritidis and S. Typhimurium could lead to the
elimination of these two serovars on farms, opening
a vacant ecological niche, enhancing, thus, the
emergence of new serovars, such as S. Kentucky or S.
Heidelberg (Foley et al., 2011).
The framework of National control programs
in European Union member states includes the
vaccination of layer flocks during rearing which
has to be mandatory in cases of 10% prevalence
of S. Enteritidis (EC No 1168/2006 and EC No
1177/2006). Live vaccines could be used only in
cases when the discrimination of vaccine versus wild
type Salmonella is possible and the ban of antibiotic
use in layers has been initiated (Carrique-Mas and
Davies, 2008). Such high demands have motivated
a number of research works aiming to nd the best
sampling strategy and the best monitoring systems for
Salmonella spp. control all around the world.
The most convenient methods of taking samples for
bacteriological analysis from poultry houses are using
boot swabs or the “step on a drag swab” method
(Buhr et al., 2007). Ofcial sampling is carried out
while birds are in the unit while own checks are
carried out not only while livestock is in the unit but
also after depopulation. Own check programs must be
approved by the competent authorities. The sampling
strategy aiming to detect and control Salmonella spp
in adult breeding ocks of Gallus gallus is dened
in Commission Regulation EU No 200/2010 and
for laying hens in Commission Regulation (EU) No
517/2011. Reduction of the prevalence of the serovars
Enteritidis and Typhimurium in flocks of turkeys
is required and the sampling strategy is dened in
Commission regulation (EC) No 584/2008. After
cleaning and disinfection, swabs are collected from
walls, floor, vents, drinking and feeding systems,
changing rooms and other areas that may be exposed
to external contamination. It is important to collect as
many swabs as possible to determine the success of
cleaning and disinfection. The same strategy applies
for hatcheries which may become contaminated
with the pathogen. In fact, Salmonella spp. can be
effectively disseminated in the hatchery cabinet and
chickens may become infected before removing from
the hatchery (Bailey et al., 1998).
According to a longitudinal study of environmental
Salmonella contamination in caged and free-range
layer ocks carried out by Wales et al. (2007), the
timing of taking samples has been shown to have a
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significant influence on Salmonella spp. isolation.
Flocks that remained longer on the premises yielded
more isolates comparing to the new flocks. The
temperature and the season also had an influence
on Salmonella spp. populations, proving increased
isolation rate during summer. The role of other
animal reservoirs harboring Salmonella in and
outside the farms is also signicant (Guard-Petter,
2001). Salmonella spp. in wildlife vectors correlated
well with the status of the ock and the same serovar
and phage type could be found in wild predators
caught around the farm and poultry. Cleaning and
disinfection in cases when organic matter had
been substantially removed and disinfectants were
adequately applied and in proper concentration, had
a positive inuence on Salmonella control. However,
the wildlife reservoirs, multiage farming and lack
of “all in all out” strategy highlight the need for
vaccination and the use of probiotics in ocks with
high and low incidence of the pathogen’s load or even
in cases that it is absent (Wales et al., 2007). Another
study by Dewaele et al. (2012) which aimed to
examine the Salmonella enterica serovar Enteritidis
environmental contamination on persistently positive
layer farms in Belgium during successive laying
cycles showed that in contaminated poultry houses,
neither vaccination nor cleaning and disinfection
are considered as the only prerequisite for
successful elimination of Salmonella spp. from the
environment and that the chances for Salmonella spp.
elimination were better in less contaminated poultry
farms, comparing to those in highly contaminated
environments. This is even more pronounced
if rodents, flies and mites come into contact with
poultry or equipment. In addition the authors
concluded that there is a possibility that even if
poultry houses are separately cleaned and disinfected,
egg collection areas may still become a reservoir of
Salmonella spp. In fact, the egg collection areas may
become contaminated with a few serovars which are
present on the entire farm.
THE PATHOGENESIS, TISSUE INVASION AND
IMMUNE RESPONSES
Salmonella spp. possesses an arsenal of genetic
determinants responsible for colonization, adhesion,
invasion and proliferation in host cells, including
mbriae, agella, toxins, surface lipopolysaccharides
(LPS), etc. Virulence genes are organized in clusters
and spread throughout the chromosome, such as
Salmonella Pathogenicity Islands 1 and 2 (SPI-1,
SPI-2), or located on virulence plasmids, such as spv
genes (associated with invasive strains). Salmonella
pathogenicity genomic islands carry genes that are
required for successful infection in poultry (Wisner et
al., 2012). Noninvasive strains cause gastroenteritis,
while invasive strains may cause systemic bacteremia
in humans and animals. The outcome of infection
depends on virulence factors, the pathogenesis of
Salmonella spp. and their interaction with the host
organism (Foley et al., 2013). Unlike noninvasive
strains, invasive Salmonella strains penetrate through
the epithelial lining to the lower parts of the lamina
propria. Also, invasive strains are commonly isolated
from parenhymatous organs (spleen, liver, ovaries)
and a small number of bacteria become internalized
by macrophages (Berndt et al., 2007). The survival in
the acidic environment of the stomach is enabled by
the activation of more than 50 acid tolerance response
proteins (Bearson et al., 2006). The first phase of
the infection has to provide a chance for the bacteria
to invade intestinal epithelial cells. This process is
accomplished by proteins encoded by Salmonella
Pathogenicity Island (SPI-1) type III secretion
system (T3SS). These organelles produce a special
structure in the bacterial envelope called “the needle
complex” which delivers toxins and other effector
proteins and injects them into the host cells (Kubori
et al., 2000). Bacterial effector proteins modulate
the host actin cytoskeleton and initiate the signal
transduction pathways required for the internalization
of the bacteria. In addition, invasive strains recruit
their own systems responsible for survival in
macrophages. Salmonella spp. become internalized
in a specific membrane bound compartment called
“Salmonella containing vacuole” (SCV). The
maturation of the SCVs and their migration to the
basal membrane disable the destruction of the bacteria
by phagolysosomes. Such intracellular trafficking
and intracellular pathogenesis is also accomplished
by the activation of the second T3SS encoded by
the SPI-2. Hence, the type III secretory system
encoded by SPI-1 and SPI-2 enables the attachment,
invasion and survival of the pathogen within the
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host cell, as well as the avoidance of antimicrobial
compounds (Hensel, 2000; Foley et al., 2013). Most
of Salmonella serovars contain SPI-1 to -5, while
other pathogenicity islands are not so common. The
colonization of the gastrointestinal tract and of the
internal organs of poultry is enabled by the type
VI secretion system encoded by the SPI-19 locus
present in serovar Gallinarum (Blondel et al., 2010).
In mice infected with serovar Typhimurium, the
SPI-6 was necessary for the intracellular replication
of the pathogen in macrophages and its systemic
dissemination. The experimental work indicates that
T6SS encoded by both SPI-6 and SPI-19 gene clusters
are genetically involved in bacterial pathogenesis
and that T6SS-SPI-6 play a role in gastrointestinal
colonization and systemic spread of serovar
Typhimurium in chickens (Pezoa et al., 2013).
Besides Salmonella pathogenicity islands-1 and 2,
Salmonella strains involved in extraintestinal non-
typhoid disease with bacteremia carry additional
virulence genes in a spv locus, contained on virulence
plasmids (Guiney and Fierer, 2011). Genes spv
were found in serovars Typhimurium, Enteritidis,
Choleraesuis, Abortusovis, Dublin, Gallinarum/
Pullorum and in subspecies arizonae. The plasmid
genes in the spv locus include spvABCD operon
which is positively regulated by the upstream spvR
gene. Only spvR, spvB and spvC are responsible for
spv related virulence phenotype. In spite of having
different biochemical pathways of action, SpvB
and SpvC proteins are eventually involved in late
apoptosis of macrophages, enabling the intracellular
proliferation of Salmonella spp. Subsequent uptake of
apoptotic macrophages by surrounding macrophages,
facilitates cell to cell spread of Salmonella spp.
(Guiney and Lesnick, 2005; Derakhshandeh et al.,
2013). Consequently, it potentiates the systemic
spread of the pathogen instead of causing a self
limited gastroenteritis.
Salmonellae have different invading capacities in
the poultry intestine and parenchymatous organs.
They trigger systemic and local immune response
which is in good correlation with their virulence.
Experimental work was conducted by Berndt
et al., (2007) to measure the immune response in
cecum after the infection of White Leghorn day old
chickens with serovars Enteritidis, Typhimurium,
Hadar and Infantis. At 2, 4 and 7 days post infection
(pi) serovars Hadar and Infantis showed diminished
invading capabilities for liver, compared to serovars
Enteritidis and Typhimurium. S. Enteritidis was
the best invader of the lower zones of the lamina
propria, while S. Infantis was found in epithelial
lining and subepithelial region. The increase
of granulocytes, TCR1 gd and CD8α+ in chicken
cecum was most prominent for serovar Enteritidis,
followed by serovars Typhimurium and Hadar,
while Infantis provoked less significant immune
cell influx. In the same study the reorganization
of the extracellular matrix proteins, notably the
increase of total fibronectin and tanascin-C, has
been more pronounced after the infection of day
old chickens with serovar Enteritidis comparing
to the infection with the non invasive Salmonella
Infantis. Furthermore, enhanced Salmonella spp.
entry and the ability to disseminate in the gut
epithelium support the concept that the most virulent
strains utilize distinctive genetic mechanisms to
invade the intestine and disseminate through the
body, showing an important ability to provoke
better immune responses in infected birds, as well
(Berndt et al., 2009). It was experimentally shown
that S. Infantis was found in higher numbers in avian
macrophages in vitro comparing to S. Typhimurium,
but the number of viable cells inside macrophages
was higher for S. Typhimurium than for S. Infantis
(Braukmann et al., 2015). Both serovars trigger active
immune responses by activating genes involved in
regulating immunological processes. The infection
of avian macrophages with both serovars induced
the increased expression of the immune mediators
up to four hours post infection. The longer survival
of serovar Typhimurium in macrophages was
probably related to a higher and rapid SPI-2 genes
activation, which explains the better invasiveness
and the ability of causing systemic infection,
something observed in serovar Typhimurium, but
not in Infantis. The unmbriated state of Salmonella
spp. and Escherichia coli in chicken intestine are
manifesting good colonizing ability in the intestine
and oviducts of laying hens at 19 weeks of age as
described by De Buck et al. (2004). However, the egg
content, particularly the yolk and the egg shell, was
contaminated by the wild type strain more efciently.
902 M. VELHNER, D. MILANOV, G. KOZODEROVIĆ
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Although the type 1 mbriae decient mutant caused
prolonged bacteraemia in laying hens, the reduced
egg shell contamination in mutant comparing to wild
type strain, has shown that mbriae are important for
causing egg contamination in serovar Enteritidis (De
Buck et al., 2004).
THE PREVALENCE OF SALMONELLA
SEROVARS IN POULTRY FLOCKS
The rise of S. Enteritidis during the 1980s and 1990s
coincided with the extensive measures undertaken
to eradicate S. Gallinarum. It is suggested that S.
Enteritidis has taken the ecologic niche previously
occupied by S. Gallinarum in poultry ocks, via the
mechanism of competitive exclusion, due to their
antigenic similarity (Rabsch et al, 2000). Clearing
the commercial flocks from S. Gallinarum enabled
S. Enteritidis to colonize chickens without signs of
disease (Andino and Hanning, 2015). In addition,
serovar Enteritidis has a wider spectrum of natural
reservoirs which makes it easier to persist on the farms.
It has been isolated from insects, rodents, nematodes,
wild birds and other animal hosts living in and around
hen houses. Thus, after adequate disinfection of
houses and stocking with culture-negative chicken, S.
Enteritidis can be reintroduced from hen house pests,
especially mice (Guard-Petter, 2001).
In the United States of America, S. Enteritidis
which was dominant in the 1990s, was supplanted
by serovar Heidelberg in the period 1997-2006, but
since 2007 S. Kentucky has been the most prevalent
serovar isolated from poultry (Foley et al., 2011).
However, these serovars are less common in humans,
with serovars Enteritidis and Typhimurium being
the leading causes of alimentary toxoinfections in
the USA. There are several possible reasons for the
prevalence of serovars Kentucky and Heidelberg:
ock immunity against S. Enteritidis gained due to
vaccination or exposure might have opened the space
for these two antigenically different serovars to which
the ocks were susceptible (Foley et al., 2011). The
ability of S. Heidelberg to colonize the reproductive
tract in chickens and enter eggs, poses a threat to
public health as another important egg transmitted
pathogen, besides S. Enteritidis and S. Typhimurium
(Gast et al., 2004). Although S. Kentucky is not
so commonly involved in human infections, it is
very successful in colonizing chicken. One of the
reasons might be the acquisition of the virulence
plasmids ColBM and ColV from the avian pathogenic
Escherichia coli (APEC) (Johnson et al., 2010).
In the past few years, the emergence of S. Kentucky
strains resistant to multiple antimicrobial drugs has
become a new threat to human and animal health.
The international trade has facilitated the spread of
those strains to the domestic poultry in the region of
Mediterranean basin (Le Hello et al., 2013).
The experimental infection of two day old broiler
chickens has revealed that serovar Kentucky persisted
longer in the cecum comparing to Typhimurium and
the peak was noted at 25 days pi (Cheng et al., 2015).
Compared to S. Typhimurium, the expression of
genes regulated by RNA polymerase sigma S factor
(rpoS) was more pronounced in serovar Kentucky in
the ceca content. The expression of genes from the
metabolic pathway and the role of curli production
seem to be in correlation with the ability of serovar
Kentucky to colonize and persist in poultry.
Unlike other serovars, S. Gallinarum biovars
Gallinarum and Pullorum are restricted to avian
species and do not pose a risk to human health.
However, among poultry, they cause septicemic fowl
typhoid and pullorum disease (respectively) with high
mortality and morbidity. Strict control programs using
serological tests and elimination of positive birds has
lead to the eradication of diseases from commercial
poultry in the United States of America, Canada
and most of Western Europe, although outbreaks
occasionally occur (Barrow and Freitas Neto, 2011).
In the European Union, harmonized Salmonella
control programs have lead to the overall decrease
in the prevalence of ve serovars (S. Enteritidis, S.
Typhimurium, S. Infantis, S. Hadar, S. Virchow) of the
public health relevance. However, in 2015 there was
a slight increase in S. Enteritidis incidence comparing
to 2014, but S. Infantis was the most prevalent serovar
among domestic fowl (EFSA 2016a).
BIOFILM FORMING CAPACITY OF
SALMONELLA SPP. IN POULTRY AND FEED
INDUSTRY
Because of the profound ability to irreversibly
bind to different types of biotic and abiotic surfaces,
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processing and storage facilities of poultry products
(Gradel et al., 2003; Gradel et al., 2004; McKee et
al., 2008; Díez-García et al., 2012).
Biofilm is an important risk factor in feed
contamination, and one of the critical points of
controlling Salmonella spp. on poultry farms, having
an increasing importance in the last decades (Cox
and Pavic, 2010). The contamination of feed with
Salmonella spp. may occur as a consequence of the
use of contaminated raw materials or it may occur
during the production process, by getting in contact
with contaminated surfaces in production facilities.
Biofilm formation is involved in both processes.
The main components of the Salmonella BF-matrix,
the protein surface aggregative fimbriae (curli)
and the extracellular polysaccharide cellulose, are
required for the colonization of plant surfaces and
for the attachment to the surface of the feed factory
environment. These biolms allow the persistence of
Salmonella spp. in feed and food factory environments
for months, and even years (Vestby et al., 2009;
Schonewille et al., 2012; Prunić et al., 2016).
In slaughterhouses and facilities for processing
poultry carcasses, Salmonella spp. are found
continuously, despite the regular use of strict
measures for the control and reduction of pathogens
(Rose et al., 2000; Joseph et al., 2001; Gradel et
al., 2004; Marin et al., 2009). Research shows that
conventional methods of disinfection are ineffective
in eliminating Salmonella spp. from surfaces on
which fresh meat processing is carried out (McKee
et al., 2008). It is also experimentally evaluated
that only two out of 13 commercially available
disinfectants based on sodium hypochlorite, sodium
chlorite and alkaline peroxide were effective against
Salmonella biofilms formed on galvanized steel
in the presence of organic matter (Ramesh et al.,
2002). In eld conditions, methods of cleansing and
disinfection are often insufcient for Salmonella spp.
elimination from poultry housing facilities (Marin et
al., 2011; Davies and Breslin, 2003). The BF-matrix,
particularly the extracellular polysaccharide
cellulose, is considered to be an important factor for
the protection against chemical agents.
The purpose of maintaining a dry environment in
feed and food factories and low water activity in the
finished product is to reduce pathogens, but these
the Most Prevalent Poultry-associated Salmonella
serotypes (MPPSTs) usually have a capacity of
biofilm (BF) formation on plant surfaces, in the
host organism, as well as in a variety of materials
commonly used in the poultry production and feed
industry (Steenackers et al., 2012; White and Surette,
2006). Hence, BF formation is a common feature
of bacteria and it is characterized as a complex
surface associated community of microorganisms.
Biofilm is defined as matrix-enclosed bacterial
populations adherent to each other and/or on
surfaces or interfaces (Donlan 2002; Donlan and
Costerton 2002). Bacteria with the ability to form
biolms express different genes comparing to their
planktonic counterparts, becoming increasingly
resistant to antibiotics and disinfectants. Indeed,
the resistance of bacteria in the BF may be 10 to
1000 times higher comparing to the bacteria in
suspension, which is most often used for the
examination of the effectiveness of disinfectants or
other antimicrobial compounds, such as antibiotics
(Mah and O’Toole, 2001). Hence, biofilm is the
perfect microenvironment for the horizontal transfer
of genetic material and the emergence of pathogens
with new virulence factors and mechanisms of
antibiotic resistance.
In a number of experimental studies, the ability
of Salmonella to form BF on a variety of materials
such as concrete, glass (Prouty and Gunn, 2003),
cement (Joseph et al., 2001), stainless steel
(Oliveira et al., 2007), plastic (Stepanović et al.,
2004; Solomon et al., 2005), granite and rubber
(Arnold and Yates, 2009) was confirmed (Solano
et al., 2002; Steenackers et al., 2012). Salmonella
spp. can rapidly colonize hydrophobic substrate,
such as plastic, and they commonly produce a
BF on them. Plastic materials are widely used on
farms, in slaughterhouses and in food industry for
the preparation of tanks, pipe-work, accessories
and cutting surfaces (Díez-García et al., 2012). The
microorganism easily forms a BF on galvanized
steel, which is used for making transport containers
for poultry (Ramesh et al., 2002). Various serovars
of Salmonella spp. are characterized by a good
ability to produce BF, which enables their persistence
in poultry facilities, hatcheries, the water supply
systems on farms, slaughterhouses, as well as in
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practice of using antibiotics in animal husbandry.
There is evidence that some resistant Salmonella
strains have increased virulence, which could be a
result of the integration of virulence and resistance
plasmids and their co-selection or up regulation of
the virulence or the improved tness of the bacteria
(Mølbak, 2005).
It is widely considered that antibiotics used in
human medicine should be avoided for the therapy
of animals. Such practice is well established in
developed countries except for rare cases, as for the
treatment of infections caused by susceptible bacteria
(Garcia-Migura et al., 2014). However, travelling
and trade have a high impact on establishing MDR
microorganisms in their communities. Besides the
restrictive use of antibiotics in developed countries,
growth promoter use was also banned in the year
2006 and the overall resistance rate in commensal
and pathogenic bacteria from food producing
animals has been decreasing. In developing countries
resistance to fluoroquinolones and extended
spectrum beta lactames is still worrisome. It has been
recorded that multiple drug resistant S. Kentucky,
S. Typhimurium and S. Infantis have a worldwide
distribution and that poultry present permanent (S.
Infantis, S. Typhimurium) or transient reservoirs
(S. Kentucky). Emerging strains of S. Kentucky
resistant to carbapenems and fluoroquinolones
may cause life threatening disease in humans and
they are among the most dangerous Salmonella
serovars that have been diagnosed recently (LeHello
et al., 2013). The rst report of the occurrence of
extended spectrum β-lactamase (ESBL) resistant S.
Kentucky from poultry specimens (whole chicken,
farm dust and chicken neck skin) in Ireland was
attributed to blaSHV-12 and blaCMY-2 genes. Even though
cephalosporins are not applicable for the therapy
of chickens in Ireland, there is a possibility that
the use of amoxicillin has favored the selection of
β-lactamase producers over the time (Boyle et al.,
2010). Salmonella Kentucky designated CVM29188
isolated from a chicken breast sample in the
year 2003 has shown resistance to streptomycin,
tetracycline, ampicillin and ceftiofur. All the genes
determining resistances (strAB and tetRA, blaCMY-2,
sugE) were found on two large transmissible
plasmids. In addition, the pCVM29188_146 plasmid
measures are not effective in controlling Salmonella
spp. In some Salmonella strains, including those of
serovar Enteritidis, isolated from food products with
low water activity, an increase in virulence and the
reduction of the infective dose was found (Aviles et
al., 2013; Andino et al., 2014). It is believed that the
increasing virulence of Salmonella spp. in products
with low water activity is the result of rpoS activation
(the main stress response regulator), which directly
affects the activation of virulence genes such as the
invA, hilA and sipC (Aviles et al., 2013). However,
experimental studies show that genes invA and hilA in
S. Enteritidis are down regulated in low water activity,
but the exact reason for the increased virulence of this
serovar remains unknown (Andino et al., 2014).
Differences in the ability to produce the BF are
established among different serovars, or strains of
the same Salmonella serovar (Schonewille et al.,
2012). However, in vitro conditions used in research
on BF formation capacities, may not always reect
the conditions required for BF formation in the
environment. Bacteria express important features
that enable them to adapt under various challenges
and the formation of the BF communities presents an
important defense mechanism.
Biolm is a risk that has been recognized recently
as it causes long term contamination and persistency
of some Salmonella serovars in all cycles of the
poultry industry. It also presents actual research
challenge in raising food producing animals and
in safe food production. There are no effective
measures to prevent or remove BF. Starting with
the fact that multiple sources of contamination with
Salmonella spp. are recognized, the only way to cope
with Salmonella spp. in poultry production facilities
is good management practice and high biological
safety. Innovations in the eld of BF control refer to
the compounds that actually inhibit biosynthesis of
signal molecules in BF, but they are not applicable in
poultry and food industry at present.
RESISTANCE TO ANTIMICROBIAL AGENTS
IN SALMONELLA SPP. FROM POULTRY
SPECIMENS
Multiple drug resistance (MDR) of Salmonella spp.
in poultry is developing because of the established
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colisitin was recorded in S. Infantis. High rate of
multi-drug resistance was detected in some EU
countries in Salmonella spp. isolates from turkey
meat. In ocks of boilers, the most prevalent was
S. Infantis with extremely high resistance rate to
ciprooxacin (except in Denmark and Spain). Second
most frequently detected serovar in broilers was S.
Enteritidis with overall resistance to ciprooxacin
and nalidixic acid of 23.3 and 24.6% respectively.
Levels of resistance to ciprofloxacin were high
in Salmonella spp. isolates from layer flocks in
Cyprus, Hungary, Italy and Romania. However,
trends in multi drug resistance were much lower in
Salmonella spp. from layers comparing to broilers
in the EU member states (EFSA 2016b). In the
report of the National Antimicrobial Resistance
Monitoring System (NARMS) USDA of 2011, it
was documented that the most prevalent serovars
from poultry in the USA were: Kentucky, Enteritidis,
Heidelberg, Typhimurum var-5 and Infantis
(NARMS-USDA, 2014). Resistance to beta lactam/
inhibitor combination and cephems was found in
17.9% of serovar Heidelberg isolates and in 0.7%
of serovar Enteritidis isolates, regarding poultry.
Resistance to (fluoro)quinolones was not found,
while resistance to gentamicin was evident in 1.3%
of the serovar Kentucky isolates, 14.3% of the
serovar Heidelberg isolates and in 10.5% of the
serovar Typhimurium var-5 isolates from poultry in
2011 (NARMS-USDA, 2014).
Poultry meat and products therefore present
a significant reservoir of resistant Salmonella all
around the world. However, the resistance patterns
differ markedly from continent to continent and
among countries. In this respect, the highest concern
is the resistance of serovars Kentucky and Infantis
which become well established in poultry ocks and
frequently develop a multidrug resistant phenotype.
CONCLUDING REMARKS
Much effort has been put through to provide safe
poultry meat and products worldwide. In spite of
the fact that many biological, chemical products
and vaccines have been invented and implemented
in poultry production systems, it is still difficult
to eliminate Salmonella spp. from the food chain.
Different Salmonella serovars tend to take place
is genetically similar to the virulence plasmids found
in avian pathogenic Escherichia coli (APEC). These
APEC-like plasmids were probably exchanged
among the two bacteria species in the intestinal
environment and they also possess virulence
elements that have contributed to their establishment
in predominant Salmonella Kentucky strains in
chicken intestines and meat (Fricke et al., 2009).
Serovar Infantis is a typical poultry Salmonella
serovar. It is well established on poultry farms with a
tendency of clonal spread of the multidrug resistance
phenotype. Clonal spread of Salmonella Infantis
in poultry and poultry meat was reported in Japan
(Shahada et al., 2006), Hungary (Nógrády et al.,
2007), Israel (Gal-Mor et al., 2010), Italy (Dionisi
et al., 2011), Germany (Hauser et al., 2012), Serbia
(Rašeta et al., 2014; Velhner et al., 2014) but also in
humans in Argentina (Merino et al., 2003) and Brazil
(Fonseca et al., 2006). All these clonal strains were
resistant to three or more antimicrobials except for
Serbia, where the predominant resistance phenotype
was nalidixic acid (NAL) / tetracycline (TET), while
an approximate 30% of the isolates was showing
resistance to ciprooxacin (CIP), with the minimal
inhibitory concentration (MIC) of > 1mg/L (Velhner
et al., 2014). The resistance to CIP was also found in
some isolates of Salmonella Infantis from Hungary
which belonged to the different pulsotype (Nógrády
et al., 2007). The occurrence of novel multidrug
resistant clones from human, food and poultry
sources in Israel was established in 2007. These
clones were resistant to NAL, TET, nitrofurantoin and
trimethoprim/sulfametoxazole (SXT). It was evident
that the resistance to TET and SXT was encoded by
a 280kb self-transmissible plasmid (pESI) and that
new clones represented 33% of all Salmonella strains
isolated in Israel (Aviv et al., 2014).
The most frequently detected serovars in poultry
meat in the EU were S. Infantis, S. Indiana and S.
Enteritidis. According to the epidemiological cut
off breakpoints (ECOFFs), multi-drug resistance
in Salmonella spp from broiler meat in the year
2014 uctuated from high (Hungary) to low (France
and Lithuania) or complete absence of resistance
(Ireland). Resistance to colisitin was 31.6% in S.
Enteritidis while resistance to ciprofloxacin and
nalidixic acid was 22.4%. No resistance toward
906 M. VELHNER, D. MILANOV, G. KOZODEROVIĆ
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J HELLENIC VET MED SOC 2018, 69(2)
ΠΕΚΕ 2018, 69(2)
eliminate Salmonella spp. from the food production
chain, travelling and trade still pose and will continue
to pose a substantial risk for infection of humans and
efcient dissemination of Salmonella spp. globally.
ACKNOWLEDGMENT
This paper was supported by a grant from the
Ministry of Education, Science and Technological
Development of the Republic of Serbia (Project
number TR 31071).
CONFLICT OF INTEREST STATEMENT
The authors declare no conict of interests.
in commercially produced poultry, as soon as an
ecological niche becomes vacant. In many developed
countries, where measures, such as vaccination, were
undertaken to eradicate certain Salmonella serovars,
other less immunogenic serovars emerge and become
dominant. Salmonella control programs in poultry
industry has to cover all the segments of food
production by implementing various procedures and
strategies in integrated poultry production systems.
It has to follow up new trends in raising free range
chickens with respect to new challenges regarding
food safety in upcoming years. In countries where
comprehensive programs have been implemented to
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