Prevalence of pathogenic Yersinia enterocolitica in pigs slaughtered at a Swiss abattoir
Introduction
Yersinia enterocolitica is a foodborne pathogen that can cause acute gastroenteritis and mesenteric lymphadenitis mimicking appendicitis (Bottone, 1997). Human yersiniosis is the third most common enteric disease after campylobacteriosis and salmonellosis in many European countries (EFSA, 2006). However, epidemiological data on the prevalence of pathogenic Y. enterocolitica in animals in EU-member states are missing as the reporting of this pathogen in animals is not mandatory in most countries. Pigs and mainly their tonsils are assumed to be the main reservoir of pathogenic Y. enterocolitica because pig is so far the only animal species from which pathogenic strains have frequently been isolated. Furthermore, high similarity between pig and human strains has been demonstrated with several DNA-based methods (Fredriksson-Ahomaa et al., 2006a, Kuehni-Boghenbor et al., 2006).
There are some difficulties associated with isolating Y. enterocolitica from naturally contaminated samples. The culture methods have several limitations, such as low sensitivity and lack of discrimination between pathogenic and non-pathogenic strains. However, it is important to assess the pathogenicity of Y. enterocolitica isolates, since the majority of the isolates recovered from asymptomatic carriers, food and environmental samples are non-pathogenic having no clinical importance (Fredriksson-Ahomaa and Korkeala, 2003). One of the chromosomal encoded genes required for the virulence of Y. enterocolitica is the ail-gene, which is only present in biotypes associated with human disease (Miller et al., 1990). Using PCR, ail-positive Y. enterocolitica can be detected in natural samples with high sensitivity and specificity (Fredriksson-Ahomaa et al., 2007).
However, in order to get epidemiological information, Y. enterocolitica isolates are needed. Thus, at least one culture method has to be used in parallel to PCR method. Selective enrichment is needed, especially when food samples are studied. However, no single procedure is currently available which will recover all bioserotypes. The most commonly used selective broth is the irgasan-ticarcillin-potassium chlorate (ITC) broth, which has been useful in recovery of bioserorype 4/O:3 (Fredriksson-Ahomaa and Korkeala, 2003).
Bio-and serotyping have been extensively used to characterise Y. enterocolitica isolates. The biotyping scheme proposed by Wauters, Kandolo and Janssens (1987) has been universally adopted. Pathogenic isolates belonging to biotypes 1B, 2-5 can be differentiated from non-pathogenic isolates belonging to biotype 1A with pyrazinamidase test, which is included in this biotyping scheme. Serotypes like O:3, O:5 and O:8 associated with human disease can also be found in non-pathogenic Y. enterocolitica strains and even in various Yersinia species. Thus, an accurate biochemical characterisation is needed before or after serological typing for correct assessment of the relevance of the strains especially from food and the environment, since related species and biotype 1A strains are widely distributed in these samples. In addition, subtyping of Y. enterocolitica strains belonging to the same bioserotype is sometimes necessary, for example to study animal reservoirs or to recognise outbreaks. Pulse-field gel electrophoresis (PFGE) and amplified fragment length polymorphism (AFLP) techniques have shown to be effective in molecular epidemiological studies of Y. enterocolitica (Fearnley et al., 2005, Fredriksson-Ahomaa et al., 2006a, Kuehni-Boghenbor et al., 2006).
Nation-specific data on the prevalence of pathogenic Y. enterocolitica using different detection methods is needed to get an overall epidemiological view. So far, only very few data is available from Switzerland. Thus, the aims of this study were i) to describe the prevalence of ail-positive Y. enterocolitica in tonsils of pigs at slaughter using real-time PCR and culture methods and ii) to further pheno-and genotype the isolates to get more epidemiological information on the current situation in Switzerland.
Section snippets
Sampling and sample preparation
Tonsils of 212 finishing pigs were sampled from a slaughterhouse in Switzerland during February and March 2006. Seventeen to 35 samples were collected from two different herds on 8 different days (Table 2). The 212 tonsil samples represent 16 farms that are located in the central and north-eastern region of Switzerland, which is the region with the highest density of pig farms. The tonsils were cut out from unsplit heads with sterilised instruments at the slaughterline and put into sterile
Results and discussion
The prevalence of ail-positive Y. enterocolitica in tonsils of slaughter pigs in the sampled herds was shown to be high using real-time PCR. The prevalence rates were 88% and 85% using SYBRGreen and probe approaches, respectively (Table 1). The PCR method has been applied in only a few studies investigating the prevalence of pathogenic Y. enterocolitica in pigs (Fredriksson-Ahomaa et al., 2000, Boyapalle et al., 2001, Korte et al., 2004, Bhaduri et al., 2005). In these studies, the detection
Conclusions
The prevalence of ail-positive Y. enterocolitica was high in tonsils of slaughter pigs using real-time PCR. Strains of bioserotype 4/O:3 but also of bioserotypes 2/O:5,27 and 2/O:9 could be isolated. Serotypes O:5,27 and O:9 belonging to biotype 2 were distinguished from each other using PCR serotyping, PFGE typing and resistance pattern. All pathogenic Y. enterocolitica isolates showed a high degree of susceptibility to antimicrobial agents used to treat human infections.
Acknowledgements
We thank A.M. Zychowska from the slaughterhouse of Zurich for her help in collecting the tonsil samples.
References (32)
- et al.
Isolation and characterization of Yersinia enterocolitica from swine feces recovered during the National Animal Health Monitoring System Swine 2000 Study
Journal of Food Protection
(2006) - et al.
Detection of Salmonella spp., Yersinia enterocolitica and verocytotoxin-producing Escherichia coli O157 in pigs at slaughter in Italy
International Journal of Food Microbiology
(2003) - et al.
Comparison of culture, multiplex, and 5′ nuclease polymerase chain reaction assay for the rapid detection of Yersinia enterocolitica in swine and pork products
Journal of Food Protection
(2001) - et al.
Short-coming of irgasan ticarcillin chlorate broth for the enrichment of Y. enterocolitica biotype 2, serotype O:9 from meat
International Journal of Food Microbiology
(1994) - et al.
Prevalence and characterization of pathogenic Yersinia enterocolitica in pig tonsils from different slaughterhouses
Food Microbiology
(2000) - et al.
High prevalence of Yersinia enterocolitica 4:O3 on pig offal: a slaughtering technique problem
Systematic and Applied Microbiology
(2001) - et al.
Different Yersinia enterocolitica 4/O:3 genotypes found in pig tonsils in Southern Germany and Finland
Systematic and Applied Microbiology
(2003) - et al.
In vitro susceptibility of Yersinia enterocolitica isolated from the oral cavity of swine
Journal of Food Protection
(2000) - et al.
A real-time PCR assay for the specific identification of serotype O:9 of Yersinia enterocolitica
Journal of Microbiological Methods
(2005) - et al.
Testing of pathogenic Yersinia enterocolitica in pig herds based on the natural dynamic of infection
International Journal of Food Microbiology
(2006)
Evaluation of a 5′-nuclease (TagMan) Assay for the detection of virulent strains of Yersinia enterocolitica in raw meat and tofu samples
Journal of Food Protection
Antimicrobial resistance of Yersinia enterocolitica strains from human patients, pigs and retail pork in Switzerland
International Journal of Food Microbiology
Prevalence of pathogenic Yersinia enterocolitica strains in pigs in the United States
Applied and Environmental Microbiology
Yersinia enterocolitica: the charisma continues
Clinical Microbiology Reviews
The serodiagnosis of human infections with Yersinia enterocolitica and Yersinia pseudotuberculosis
FEMS Immunology and Medical Microbiology
The community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborme outbreaks in the European Union in 2005
The EFSA Journal
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2021, International Dairy JournalCitation Excerpt :Infections normally occur through ingestion of contaminated food. Pigs are considered the principal reservoir of Y. enterocolitica and pork meat and product thereof are the main source of human infection (Fredriksson-Ahomaa, Stolle, & Stephan, 2007). However, different epidemiological studies indicate other animal species as Y. enterocolitica carriers and pathogenic strains have been detected from food of various origin and from the environment (Favier, Escudero, & de Guzmán, 2005; Le Guern, Martin, Savin, & Carniel, 2016; Lucero-Estrada, Favier, & Escudero, 2020; Rahimi, Sepehri, Safarpoor Dehkordi, Shaygan, & Momtaz, 2014).