Applied and Environmental Microbiology-2019-Ferrari-e00591-19.Full
Applied and Environmental Microbiology-2019-Ferrari-e00591-19.Full
Applied and Environmental Microbiology-2019-Ferrari-e00591-19.Full
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a Molecular and Analytical Laboratory Center, Department of Food Technology, Faculty of Veterinary, Federal Fluminense University, Niterói, Brazil
ABSTRACT Salmonella spp. are among the most important foodborne pathogens and
the third leading cause of human death among diarrheal diseases worldwide. Animals
are the primary source of this pathogen, and animal-based foods are the main transmis-
sion route to humans. Thus, understanding the global epidemiology of Salmonella sero-
vars is key to controlling and monitoring this bacterium. In this context, this study
aimed to evaluate the prevalence and diversity of Salmonella enterica serovars in animal-
based foods (beef, pork, poultry, and seafood) throughout the five continents (Africa, the
Americas [North and Latin America], Asia, Europe, and Oceania). The meta-analysis con-
sisted of a chemometric assessment (hierarchical cluster analysis and principal compo-
nent analysis) to identify the main epidemiological findings, including the prevalence
and diversity of the Salmonella serovars in each matrix. Regarding the serovar distribu-
tion, S. Typhimurium presented a cosmopolitan distribution, reported in all four assessed
matrices and continents; poultry continues to play a central role in the dissemination of
the Enteritidis serovar to humans, and Anatum and Weltevreden were the most fre-
quently found in beef and seafood, respectively. Additionally, we recommended careful
monitoring of certain serovars, such as Derby, Agona, Infantis, and Kentucky. Finally,
given the scientific data regarding the most frequently reported serovars and which ma-
trices constitute the main vehicles for the transmission of this pathogen, control pro-
grams may be improved, and specific interventions may be implemented in an attempt
to reduce the risk of this pathogen reaching humans.
IMPORTANCE Salmonellosis is caused by Salmonella spp. and is the third leading
cause of death among food-transmitted diseases. This pathogen is commonly dis-
Citation Ferrari RG, Rosario DKA, Cunha-Neto
seminated in domestic and wild animals, and the infection’s symptoms are charac- A, Mano SB, Figueiredo EES, Conte-Junior CA.
terized by acute fever, nausea, abdominal pain, and diarrhea. The animals are the 2019. Worldwide epidemiology of Salmonella
primary source of salmonellae, and animal-based foods are the main transmission serovars in animal-based foods: a meta-
analysis. Appl Environ Microbiol 85:e00591-19.
route to humans. Therefore, data collected from these sources could contribute to https://doi.org/10.1128/AEM.00591-19.
future global interventions for effective control and surveillance of Salmonella along Editor Johanna Björkroth, University of Helsinki
the food chain. In light of this, the importance of our research is in identifying the Copyright © 2019 American Society for
prevalence of Salmonella serovars in four animal-based food matrices (pork, poultry, Microbiology. All Rights Reserved.
beef, and seafood) and to evaluate the importance that each matrix has as the pri- Address correspondence to Carlos A. Conte-
Junior, [email protected].
mary source of this pathogen to humans.
R.G.F. and A.C.-N. contributed equally to this
work.
KEYWORDS beef, pork, poultry, Salmonella, seafood
Received 15 March 2019
Accepted 25 April 2019
Accepted manuscript posted online 3 May
July 2019 Volume 85 Issue 14 e00591-19 Applied and Environmental Microbiology aem.asm.org 1
Ferrari et al. Applied and Environmental Microbiology
RESULTS
Literature search. A total of 1,023 articles (210, pork; 528, poultry; 258, beef; 27,
seafood) were identified at the PubMed database, 393 articles (76, pork; 210, poultry;
93, beef; 14, seafood) at Web of Science, and 1,247 (312, pork; 785, poultry; 137, beef;
13, seafood) at Scopus, totaling 2,663 articles. Of these, 82 were duplicates or triplicates
and were excluded. A total of 2,581 remained after exclusion of repeated papers. After
screening the titles and abstracts, only 266 papers were adequate for the purpose of
the study, since they dealt with both matrix and Salmonella serovars (Fig. 1).
Salmonella serovars around the world. First, considering all matrices around the
world, according to the continued linkage distance, serovars were separated into
cluster A and cluster B (see Fig. S1 in the supplemental material). The decision to
separate the clusters was determined by two factors: prevalence and global distribu-
tion. Serovars with major global importance are presented in cluster A (Fig. S2). Second,
five clusters were obtained, where clusters 1, 2, and 3 are subdivisions of cluster A (Fig.
S1). The Typhimurium serovar, indicated as cluster 2, individually represents the most
(Australia) removes its global relevance. Because of this, this serovar is presented in
cluster 4. Finally, cluster 5 presents serovars with unimportant worldwide relevance.
Salmonella serovars in pork. PCA factors 1, 2, and 3 explain 85.64% of the data
variance (Fig. S3) for serovars in pork. According to continent and serovars contributions
(loadings) to factor construction (Table S2a), factor 1 represents Typhimurium and
Derby in Europe, Oceania, Asia, and North America as the most prevalent serovars (Fig.
S3A). However, the location of Europe and Oceania above the factor 2 central axis line,
as well as serovar Typhimurium, indicates that this serovar was more prevalent than
Derby on these continents. Similarly, the location of Asia below the factor 2 central axis
line indicates that Derby was more prevalent on this continent; this was not observed
for North America, since similar locations for both Derby and Typhimurium indicate that
these serovars present the same importance. Factor 2 indicates that Hadar was the
most prevalent serovar in Africa. On the other hand, factor 3 (Fig. S3B) indicates
DISCUSSION
Salmonella serovars worldwide. The results reported here confirm that the Typhi-
murium serovar displays a cosmopolitan profile and is considered an example of a
generalist serovar (Fig. 3). Thus, it is not surprising that it occupies the second position
in Europe (20) and third in the United States (19) in human salmonellosis reports. Pig
meat was the matrix most associated with S. Typhimurium and its monophasic variant
(20, 26). Therefore, from a worldwide point of view, these results corroborate those
reported by the CDC (26) and EFSA (20), confirming that pig and pork meat are the
main sources of this pathogen.
According to experimental studies, pigs can asymptomatically carry high S. Typhi-
murium concentrations in the tonsils, gut, and mesenteric lymph nodes, and during
their slaughter, these tissues frequently disseminate the bacterium to carcasses (27–31).
In addition, the presence of S. Typhimurium in the parotid glands can also be a hazard
during sanitary inspection due to cross-contamination generated by the incision. Once
this occurs, Salmonella organisms spread out throughout the processing line and can
be isolated from machinery, knives, carcasses, and employee hands (32, 33).
Serovar Enteritidis was the most frequently reported in human salmonellosis cases
in the European Union, followed by S. Typhimurium and its monophasic variant,
1,4,[5],12:i:⫺. EFSA, in agreement with our results, indicates that this serovar was first
associated with broiler flocks and meat (57.2%), followed by layer (37.1%) and turkey
(3.9%) sources (20). In the United States, S. Enteritidis is the second most isolated
serovar from chicken carcasses and is the most frequent serovar associated with human
disease (34). Hence, with regard to poultry from a worldwide view, these results
corroborated the aforementioned reports, indicating that this matrix continues to play
a crucial role in the delivery of this bacterium to humans.
Concerning Anatum, the most noteworthy serovar in beef (Fig. 2B), the studies
reported here (see Table S8 in the supplemental material) do not discuss why this
serovar is found so frequently in this matrix. Moreover, until the elaboration of this
research, no studies concerning the pathogenesis of this serovar were found in the
literature. It is hoped that this gap is an incentive for future studies, considering the
relevance that this serovar presents regarding its prevalence in beef. From reported
outbreaks by this serovar, it appears the twenty most prevalent are in Asia, Africa (3),
and the United States (19).
Originating in India, the Weltevreden serovar became the most prevalent NTS in
South and Southeast Asia due to its special capacity for commensalism, which can
cause zoonosis worldwide through the consumption of contaminated foods and
seafood. This serovar emerged as a dominant serovar isolated from fish production
systems and aquatic foods (35) and is considered an important pathogen in the context
of public health, especially in coastal areas of China (36). Noor Uddin et al. (37) reported
closely related or identical pulse types of S. Weltevreden profiles from distinct shrimp
farms. These findings suggested a clonal strain resulting from a common feed, fecal
source, or animal, i.e., rodent, reptile, or bird. In addition, it has been proposed that this
serovar is more adapted for survival than other Salmonella serovars. Additionally, an
antimicrobial profile similar to that of S. Typhimurium DT 104 was noted, which
presents resistance to florfenicol and chloramphenicol, related to the floR gene. This
indicates that future molecular studies must be carried out in order to determine the
factors that may be associated with increased survival in aquatic environments and
whether resistant patterns are related to the floR gene (37).
Salmonella serovars in pork. Pigs are one of the most common sources of
Salmonella infections in humans (38–40), and in some countries it is indicated as the
most important source of salmonellosis, as in a great part of Europe and the United
States (19, 40). This is because these animals are frequently asymptomatic carriers and
disseminators of this pathogen throughout the production chain. Even if the preva-
lence of Salmonella in these animals varies depending on the different stages of
production (ranging from 3% to 33%), it is relevant in a food safety context to
understand and control pig infection under slaughter conditions (18, 41). Salmonella
spp. may spread among pigs through the fecal-oral route, direct contact between
snouts, feed, and aerosols. Additionally, as this pathogen is present in the animal
intestines, mesenteric lymph nodes, throat, stomach, and feces (32, 42–44), pigs under
slaughter conditions can quickly develop resurgent infections before processing, in-
creasing the number of impaired animals and the risk of spreading this microorganism
in slaughterhouses (45–50).
S. Typhimurium presented a ubiquitous profile, since all continents reported this
serovar in pork (Fig. 4A). This finding is supported by the fact that this serovar is
described in outbreaks worldwide involving pork (3, 51, 52). According to Hendriksen
et al. (3), S. Typhimurium is the most common serovar in humans in North American and
Oceania, regardless of the source, followed by Enteritidis. In contrast, in the European
Union, S. Enteritidis ranked as the most common serovar, with Typhimurium second.
However, in the present study, S. Enteritidis was reported in pork only in Africa and Asia,
in both cases in the 8th position. This is due to the secondary importance that this
matrix has in the dissemination of this serovar to humans. In fact, several studies
suggest eggs, chicken meat, and derivatives as the main culprits in the dissemination
of this serovar (53–60). Therefore, when the source is attributed, studies indicate that
pork and pork-based food are the main S. Typhimurium transmission vehicle in Africa
and Asia (19, 20, 61).
The Typhimurium serovar, including its monophasic variant, when isolated from
swine, presents a diverse phenotypic and genotypic profile. Studies have reported that
multidrug-resistant (MDR) S. Typhimurium phage type U 288, DT 120, and DT 193 are
the most prevalent in swine (39, 62–72) and DT 193 in both humans and pigs (62, 72,
73). Some researchers have suggested that the prevalence of phage type DT 193 has
increased in humans over the past 10 years due to its association with the dominant
clone of monophasic S. Typhimurium (39, 73–76), although this clonal line is a heter-
In Latin America, the Meleagridis serovar was the most described in pork, followed
by Anatum and Agona (Fig. 4A). This study also indicates this serovar is found in beef
(3rd) and chicken (11th) on this continent (Table S7). This is interesting, since this
serovar is the 4th leading cause of outbreaks in this region (3), suggesting that pork and
derivatives represent one of the main sources of this serovar for humans. Few studies
regarding the characterization of the Meleagridis serovar and a plausible explanation of
why this serovar is so isolated in swine are found in the literature. Some studies (90–93)
have reported S. Meleagridis is one of the most prevalent in pork serovars, and its
characterization by MLST indicates ST463 and ST64 with an MDR profile.
Concerning the Hadar serovar in Africa, generally associated with poultry (94–97),
the present study indicates that pork and seafood presented a higher prevalence,
followed by poultry, ranked 2nd. Thus, pork meat cannot be identified as the main
potential vehicle of this serovar to humans on this continent. However, these results
due to its pathogenicity mechanism. In this regard, the diarrheal characteristics pro-
duced by S. Typhimurium in calves are similar to the pathological and clinical signs seen
in humans (136–139). Thus, upon oral infection, calves develop clinical signs of infec-
tion, presenting anorexia, diarrhea, dehydration, fever, and prostration (136, 139). The
Salmonella plasmid virulence (spv) genes and SPI-2, in contrast to the Dublin serovar (an
invasive serovar to calves), have little or no importance during localized infection
caused by the Typhimurium serovar. These findings suggest, as commented above, that
the majority of the Typhimurium serovars in calves remains restricted to the gut and
mesenteric lymph nodes (139). However, an increased risk of the presence of this
serovar in beef leading to human illness is demonstrated by a number of outbreaks
linked to this matrix. Confirming this, reports in the United States (129) and the
European Union (20) point out that the most common serovar responsible for out-
breaks with beef as a vehicle was S. Typhimurium.
Salmonella serovar, and epidemiological investigations using PFGE, currently the gold
standard method, are limited in their ability to differentiate strains implicated in
epidemic outbreaks (151). However, a recent study performed by Lalsiamthara and Lee
(152) reported that cattle are commonly affected by this serovar and indicated that this
serovar is more adapted to chicken than other animals, suggesting that poultry is the
primary reservoir. However, interesting information corroborating the findings reported
here indicates that although outbreaks in the United States caused by the Montevideo
serovar increased in ten years (2002 to 2012) from 728 to 1,203, the prevalence of this
bacterium in poultry meat was reduced from 0.25% to 0.1% in this same period,
coherent with a negative relationship. In addition, the prevalence of S. Montevideo in
beef increased from 0.3% to 0.5%, indicating a robust positive correlation (105). This
information denotes that this matrix is probably related to human infections, although
more studies about this serovar are required in order to clarify this hypothesis.
survival and multiplication in HeLa cells than the Typhimurium serovar. These
authors noted that this serovar could not survive intracellularly in HeLa cells once
the sseC gene was deleted, indicating that this gene plays a central role in the
persistence of this serovar inside cells.
S. Newport is the most prevalent serovar in North America (Fig. S6) and an important
human pathogen, found in a wide range of hosts, including poultry, water birds, swine,
and cattle, as well as aquatic organisms. This serovar causes over 100,000 infections a
year (171), and in North America it is the 3rd most common serovar involved in human
outbreaks (3). In addition, outbreaks in different parts of the world have been linked to
several kinds of foods, including ground beef (125), mangos (172), unpasteurized
cheese (173), and tomatoes (174). A notable fact is the absence of this serovar in the
other three assessed matrices, suggesting that seafood represents an actual threat
responsible for transmitting this pathogen to humans. S. Newport is polyphyletic,
while another is not, as in the case of seafood. Finally, this study aimed to subsidize
prevention actions and specific control programs for each continent and for
animal-based products.
SUPPLEMENTAL MATERIAL
Supplemental material for this article may be found at https://doi.org/10.1128/AEM
.00591-19.
SUPPLEMENTAL FILE 1, PDF file, 1.9 MB.
ACKNOWLEDGMENTS
We thank Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (process no.
E-26/201.577/2018, FAPERJ, Brazil), Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq) (process no. 311422/2016-0, CNPq, Brazil), and Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (process no. 125, CAPES/
Embrapa 2014, CAPES, Brazil). This study was financed in part by the CAPES (Brazil),
Finance Code 001. We have no conflicts of interest to declare.
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