The first detection of Salmonella enterica subspecies enterica serovar
Choleraesuis in farm-raised pigs in Serbia, 2019
Bozidar Savic1,2*, Nemanja
Zdravkovic1, Oliver Radanovic1,
Nemanja Jezdimirovic1, Branislav
Kureljusic1, Ognjen Stevancevic2
1Institute of Veterinary Medicine Belgrade, J.
Janulisa 14, 11 000 Belgrade, Serbia
2Agriculture Faculty Department for Veterinary
Medicine University of Novi Sad, Dositej Obradovic Square 8, 21 000 Novi
Sad, Serbia
*Corresponding author. Bozidar Savic, Institute of Veterinary Medicine
Belgrade, J. Janulisa 14, 11 000 Belgrade, Serbia. Tel.: + 381 11 2851
065, Fax: + 381 11 2851 065, E – mail address:
savic.bozidar@hotmail.com
(Savic. B)
Summary
Salmonella enterica subspecies enterica serovar Choleraesuis is rarely
detected in Europe, but the clinical disease in pigs, was reported in
wild boars. Salmonellosis caused by S. Choleraesuis has never been
confirmed in Serbia, as in many other countries in Europe. In April
2019, on one large farrow-to-finish pig farm, an increase in mortality
in weaned piglets with lethargy, anorexia, pyrexia and respiratory
distress was reported. Gross pathology revealed dermal cyanosis,
mesenteric lymphadenopathy, splenomegaly, hepatomegaly, interstitial
pneumonia and colitis. By direct culturing of lung, liver, spleen and
lymph nodes S. Choleraesuis variant Kunzendorf was isolated. This is the
first report on the detection of S. Choleraesuis in domestic pigs in
Serbia and re-appearance of salmonellosis due to S. Choleraesuis after
decades of absence of disease on pig farms in Europe, which provides
useful information about the epidemiology of this agent on the European
continent. However, the definitive source for this outbreak and origin
of infection still have to be elucidated.
Keywords
Salmonella Choleraesuis; outbreak investigation; farm pigs; Serbia
Introduction
Host-adapted S. Choleraesuis is isolated almost exclusively from
diseased swine and is usually manifested as septicemia (Griffith et al.,
2019). S. Choleraesuis var. Kunzendorf is currently highly prevalent in
North America and Asia (Luk-in et al., 2018), but is rare in Australia
and the European Union (EU) (Fedorka-Cray et al., 2000). In Europe, S.
Choleraesuis is not considered a dominant serovar, in slaughter pigs and
breeding herds and only a few outbreaks have been reported, among pig
herds within the last decades; 1999–2000 and 2012–2013 (Baggesen et
al., 2000; Pedersen et al., 2015) (in Denmark), but it is occasionally
reported, such as in 2009 (EFSA 2008, 2009), 2011 (EFSA 2013) and 2014
(EFSA 2014) with a low frequency in a few European countries. However,
several cases of outbreak of the septicaemic form, caused by S.
Choleraesuis var. Kunzendorf, were reported in Europe in wild boars: in
Spain in 1999 (Perez et al., 1999); in Thuringia between 2006 and 2008
(Methner et al., 2010); in central‐western Spain between 2010 and 2016
(Gil Molino et al., 2019), in Italy from February 2012 until June 2015
(Longo et al., 2019); and in the German federal state North
Rhine-Westphalia in 2017 (Methner et al., 2018). In Serbia, the most
common Salmonella serovars in pigs are Salmonella enterica serovar
Typhimurium, S. Derby, S. Infantis and S. Enteritidis (Stojanac et al.,
2014; Kureljusic et al., 2017). These serovars may also cause clinical
salmonellosis in pigs, however except in sporadic reports, the extent of
clinical salmonellosis in pigs in Serbia is uncertain. Furthermore, in
Serbia, until 2019 there was no reported salmonellosis caused by S.
Choleraesuis. Here, we describe clinical symptoms, pathological changes
and microbiological features of swine Salmonellosis caused by Salmonella
Choleraesuis in weaned pigs on a farrow-to-finish pig farm in Serbia, as
well as determining the in vitro susceptibilities of the S. Choleraesuis
isolate against commonly used antimicrobials.
Material and methods
In April 2019, on a farrow-to-finish pig farm in south-west Vojvodina
province in the northern region of Serbia, an increase in mortality from
2.3 to 5% in weaned piglets was reported. The herd had an inventory of
1300 sows on a single-site, and the farm practices continuous flow
operations on the basis of weekly management. In every segment of the
production cycle the “all in-all out” principle is used, and all
facilities are cleaned, washed and disinfected after emptying, before
being re-populated in 3-4 days. There were three nursery buildings on
the farm housing approximately 2000 weaned piglets per building, as well
as additional facilities for housing of other phases of swine
production. The piglets were fed with a complete feed mixture for weaned
pigs purchased from local feed mills, and the farm also prepared and
used its own feed. The farm vaccinates against neonatal colibacillosis
and Clostridium infections, Mycoplasma hyopneumoniae (Mh), Classical
Swine Fever (CSF), Aujeszky’s disease, erysipelas, porcine parvovirus
(PPV) Porcine circovirus 2 (PCV2) and Porcine Reproductive and
Respiratory Syndrome Virus (PRRSV) (sows at weaning). In the previous 8
months the farm had experienced an episode of a severe outbreak of
Porcine Epidemic Diarrhea Virus (PEDV) infection. Also, in the previous
1.5 years, problems related to mycotoxicoses in different phases, had
regularly occurred on the farm. The history of salmonellosis on the farm
was unknown. During the previous 2 years, the farm had imported about
200 gilts and 7 boars from the EU, but the farm also regularly traded
pigs with other swine farms within Serbia.
The outbreak of disease was observed in a nursery building in which
there were 900 piglets size 15-20 kg. About 120 piglets out of 900,
displayed clinical symptoms including lethargy, inappetence, reluctance
to move, and cyanosis of ears, extremities and abdomen, while
approximately 50 piglets with such clinical symptomatology were also
febrile with temperatures of 39.5–41.5 °C and had shallow cough and
hard breathing (thumping) giving the impression of severe pneumonia. The
same clinical symptomatology was also observed in the other two nursery
buildings a day later, and approximately 460 of, in total, 6000 weaned
piglets at the farm showed a similar clinical picture. To control the
outbreak, some management procedures (isolation of sick piglets), in the
pens with clinical disease was implemented to reduce infection and
contamination within nurseries, and antibiotic treatment was initiated.
The disease outbreak in nurseries associated with observed clinical
signs lasted for 3 weeks. Morbidity reached 10% among weaned piglets,
and the mortality increased to approximately 5%. Of the 460 diseased
piglets, 152 died, reaching 100% morbidity, with a case fatality rate
of 33%.
In the examined piglets, a necropsy performed by veterinarians and a
pathologist from the Veterinary Institute, at the farm, revealed
emaciated carcasses and rough hair. Most carcasses showed distal
cyanosis of skin, especially ears, nose, ventral neck, feet and ventral
part of the abdomen. In piglets that had survived for a few days, the
tips of ears were dry and dark-red, with sloughed portions (Figure 1a).
Lymph nodes especially the mesenteric, were enlarged, dark purple and
moist (Figure 1b). In most cases, the spleen was enlarged
(splenomegaly), dark-purple and pulpy while the liver was moderately
enlarged (hepatomegaly), frequently with scattered small (≈1.5 mm) white
spots (foci of parenchymal necrosis) (Figure 1b). In all cases, the
lungs were resilient, non-collapsed slightly firm with red fluid that
separated lobules, and lesions affected either the cranial or the apical
lobes. Colitis was found in some piglets. The mucosae of the colon from
those animals were slightly thickened and multifocally covered by
adherent gray-yellow fibrinous membranes (Figure 1c). Samples of
different organs (lungs, liver, spleen, and lymph nodes) from six
animals were sent to the National Reference Laboratory for Salmonella
(Institute of Veterinary Medicine, Belgrade) for Salmonella
identification and serotyping. In addition, at the pathology department,
tissue samples of these organs were fixed in 10% neutral buffered
formalin for histopathological examination. Tissue sections were
embedded in paraffin, cut at 5 μm, stained with H&E and examined under
the microscope.
All samples were cultured on blood agar, McConkey agar, and
xyloselysine-desoxicholate agar (XLD) in aerobic conditions for 24 hr.
at 37°C. Compatible colonies were confirmed by detection of invE and
invA genes by PCR (Stone et al., 1994) and biochemically using BBL
Crystal™ Identification Systems Enteric/Nonfermenter id kit. Serogroup
identification was performed by using Salmonella Sero-Quick Group kit
(SSI Diagnostica). The identification of serotypes was conducted
according to the Kauffmann-White scheme (Popoff 2001). Salmonella
isolates that belonged to C1 group, serotype 6,7:c:1,5 were further
sequenced for the fliC gene using flinC-F and flinC-R primers described
by Chiu et al., 2005. The sequences were queried in the NCBI Genbank
base to identify best match with the fliC gene from Salmonella. The 871
base-pair sequence of the fliC flagellin gene of Salmonella from this
study was submitted to the GenBank database under-accession number
MN563751. For antimicrobial sensitivity and resistance testing, isolates
were tested by disc diffusion against a panel of 12 antimicrobials from
different families which are routinely used in farms (Table1).
Results and discussion
A tentative diagnosis of salmonellosis caused by S. Choleraesuis was
based on clinical signs and postmortem lesions. The observed clinical
symptoms indicated respiratory infections, and also fitted the clinical
presentation of salmonellosis due to S. Choleraesuis. Lesions detected
by necropsy of piglets that died, indicated a septicaemic processes, and
this was confirmed by the isolation of S. Choleraesuis from different
organs in the examined animals. Congestion and foci of necrosis with
interstitial infiltration with mononuclear cells in the liver (Figure
1d); diffuse interstitial pneumonia with septal thickening accompanied
with suppurative bronchopneumonia, oedema and congestion in the lung;
congestion, increase of white pulp and foci of necrosis in the spleen;
hyperemia, with areas of cellular necrosis in the lymph nodes were the
hallmarks of histology findings.
Six bacterial strains that were recovered from different animals
directly without pre-enrichment in buffered peptone water were
classified as S. Choleraesuis var. Kunzendorf by phenotypic serotyping
and biochemical tests. All isolates were assigned to the antigenic
formula 6,7:c:1,5 and were Vi capsular polysaccharide (Vi antigen)
negative, showing the following biochemical features: dulcitol (–), H2S
(+) and mucate (–). All isolates generated the 963 bp. PCR product of
the fliC gene. The reverse primer FlinC-R amplified a unique sequence
specific for S. Choleraesuis and S. Paratyphi C. Because S. Paratyphi C
infects only humans and not swine, and as isolates were Vi antigen
negative, the positive signal of the fliC gene from these isolates is
conclusive for S. Choleraesuis. Regarding antibiotic groups, isolates
showed resistance to penicillins, tetracyclines, phenicols, and
streptomycin and could be considered multiresistant, while all isolates
showed sensitivity to aminoglycosides, cephalosporins, quinolones,
sulfonamides and colistin.
Our findings presented here show the first case of salmonellosis caused
by S. Choleraesuis in farm-raised pigs in Serbia. In our case, the
disease occurred in nurseries and that age of piglets has been described
in the literature as the most susceptible to disease. Many studies (Chiu
et al., 2004; Pedersen et al., 2015; Gil Molino et al., 2019) emphasize
the importance of stress factors, such as weaning and grouping animals,
the triggering effect of immunosuppressive viruses (such as PCV2, PRRSV)
and the fact that the piglets aged 2-3 months have the lowest level of
antibodies since birth (Tizard, 2009), as activators of various types of
infections in weaned piglets. This also applies to Salmonella species,
and the ability of the strains of Salmonella to persist for long periods
of time in asymptomatic carriers, and then to be activated by stress
factors. In this case, the farm had no known previous confirmed history
of salmonellosis and it was not known whether S. Choleraesuis already
persisted or not, in weaned piglets and on the farm at all. Furthermore,
the farm applies vaccination against major and specific pig pathogens
including vaccination of piglets against M. hyopneumoniae, PCV2,
porcine pseudorabies virus (PRV), CSF-virus and erysipelas, and only a
couple of months before the outbreak of the S. Choleraesuis there was an
outbreak of severe PEDV infection. However, as we did not know the
history of salmonellosis on the farm or whether S. Choleraesuis persists
at all, it can only be speculated whether PEDV infection in this case
has contributed to the severity of the S. Choleraesuis outbreak in
weaned piglets. On the other hand, if asymptomatic S. Choleraesuis
infection was already present (in small numbers) in weaned piglets, then
its activation, and subsequent acute outbreak of the disease could be
associated to the triggering effect of predisposing factors such as
underlying diseases and conditions (e.g. mycotoxicoses), decreased
antibody levels, especially the level of antibodies against PRRSV, (as
only sows are vaccinated), and therefore the onset of active PRRSV
infection in piglets (Wills et al., 2000), and stress-induced
immuno-suppression. Also, an additional explanation for the outbreak of
S. Choleraesuis in weaned piglets may be that S. Choleraesuis does not
need any previous immunosuppressant infections to develop a pathological
process, as recently described in outbreaks of S. Choleraesuis in wild
boars in Spain and Italy (Gil Molino et al., 2018; Longo et al., 2019).
The outbreak of the disease from our study, was characterized by a high
mortality rate of 33%, which is the same rate reported in outbreaks of
salmonellosis due to S. Choleraesuis in four Danish pig farms in
2012–2013, with the exception that in our case there were no obvious
concomitant infections during the disease. Clinical symptoms and
pathological findings of the affected piglets were fully compatible with
those described in the literature for farm-raised weaned pigs, and
comparable to those described in similar processes affecting wild boars
(Methner et al., 2018; Gil Molino 2018), with addition of findings of
colitis in several cases which is uncommonly a pathological feature of
septicaemic salmonellosis caused by S. Choleraesuis.
The most likely source of infection in this case is live carrier pigs,
although other sources such as feed, wild boars or even humans as
passive vectors although unlikely, cannot be entirely ruled out (Hilbert
et al., 2012). The farm had successively imported a large number of pigs
(gilts and boars) in the previous two years from the EU, but it had also
purchased pigs from farms in Serbia. Therefore, it is possible that
during an import or by purchasing of pigs from farms in Serbia, S.
Choleraesuis was introduced onto the farm, by undetected carrier
animals. However, the lack of reports on S. Choleraesuis infections on
pig farms from neighboring and many European countries does not allow us
to hypothesize on the possible wider origin of the infection. Also, from
the authors’ knowledge, until now S. Choleraesuis has not been detected
in Serbia, though owing to intensive imports of pigs into the country
for the last two decades from many EU countries, we cannot with
certainty exclude the possibility that S. Choleraesuis, undetected,
could have been present in asymptomatic pigs on certain farms in the
country, or in the wild boar population and even in the pig food chain,
spread by carriers among pig herds all over the country, including
spreading to the farm from this case, primarily due to insufficient
detection of Salmonella on pig farms at the national level. On the other
hand, clinical salmonellosis caused by S. Choleraesuis can hardly pass
undetected on farms by either the owner or a veterinarian without
reporting this and, thereby, allowing a persistent infection. It is
generally accepted that S. Choleraesuis is rarely found in pig feed, and
in Serbia there is no stock of wild boars in the area, and the farm from
this case is relatively well managed, with a good biosecurity, and
finally during epidemiological investigation we could find no evidence
that the employees at the farm were the vectors of infection, so all
these potential reservoirs of Salmonella were ruled out, as possible
sources or vectors of the infection on the farm.
In conclusion, this is the first report on the septicaemic form of
salmonellosis caused by S. Choleraesuis var. Kunzendorf, in farm-raised
weaned pigs from Serbia, and beside a few outbreaks of S. Choleraesuis
reported in Danish pig farms during 1999-2000 and 2012-2013, this is
also the first report of S. Choleraesuis infection on pig farms in
Europe in the last several decades. The infection on the farm was most
likely introduced by live asymptomatic carrier pigs, either imported or
originating from swine herds from Serbia. However, only molecular typing
and comparison of our isolates with isolates from other European
countries may allow a better conclusion on the potential source and
tracing the origin of the infection which could not be done in the
current investigation. Undetected, asymptomatic infection on the farm
had probably persisted for some time and then was activated by
stress-induced immuno-suppression, thus triggering the clinical outbreak
of disease among weaned piglets. In spite of low-prevalence of S.
Choleraesuis as a cause of salmonellosis in pig farms in Europe, it
appears from this study that S. Choleraesuis could be underestimated as
a pathogen in farm pigs, and that its prevalence, as an asymptomatic
infection, may be higher than assumed owing to the fact that the number
of wild boars, that serve as a most likely reservoir of S. Choleraesuis,
has significantly increased on the European continent in the last
decades, and that contacts of humans with the wild environment are more
frequent, thus increasing the risk of occurrence and transmission of
diseases to farmed pigs (Ruiz-Fons, 2017). Our finding of salmonellosis
caused by S. Choleraesuis in farm-raised pigs re-emphasizes the
importance of hygiene and biosecurity measures in the herds for
preventing the introduction of specific pathogens and spreading of
diseases. Particular care must be taken towards trucks which deliver
live pigs directly to the farm from an area, or pass through areas, of
Europe or Serbia, where S. Choleraesuis may be present, which are not
being properly cleaned and disinfected.
Acknowledgements
This work was partially funded by Serbian Ministry of Education, Science
and Technological Development (contract number:
451-03-68/2020-14/200030). We thank the veterinary practitioners for the
farm information and aid during necropsy and sampling as well as to the
technical staff from the Department of Bacteriology and Pathology of the
Institute of Veterinary Medicine Belgrade, Serbia.
Conflict of interest statement
All authors have declared no conflict of interest.
Ethical approval
The authors confirm that the ethical policies of the journal, as noted
on the journals author guidelines page, have been adhered to. No ethical
approval was required as this article describes field data and no live
animals were handled to obtain tissues.
Data viability statement
The data that support the findings of this study are available from the
corresponding author upon reasonable request. The sequence used to
support the finding of this study is available in GenBank at
https://www.ncbi.nlm.nih.gov reference number MN563751.
Orcid
Savic Bozidar:
https://orcid.org/0000-0001-7705-6457
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Table 1
Susceptibility of 6 tested S. Choleraesuis isolates to antimicrobials.