Date Published: June 29, 2012
Publisher: BioMed Central
Author(s): Karin Söderqvist, Sofia Boqvist, Georges Wauters, Ivar Vågsholm, Susanne Thisted-Lambertz.
Pigs are regarded as the main reservoir for human pathogenic Yersinia enterocolitica, which is dominated by bioserotype 4/O:3. Other animals, including sheep, have occasionally been reported as carriers of pathogenic strains of Y. enterocolitica. To our knowledge, this is the first study performed in the Nordic countries in which the presence of Y. enterocolitica in sheep is investigated.
Tonsils and faecal samples collected from sheep slaughtered on the island Gotland (Sweden) from September 2010 through January 2011 were analysed for presence of Y. enterocolitica. In an attempt to maximize recovery, several cultural strategies were applied. Various non-selective media were used and different temperatures and durations of the enrichment were applied before subculturing on Cefsulodin Irgasan Novobiocin (CIN) agar. Presumptive Y. enterocolitica colonies were subjected to urease, API 20E and agglutination test. Yersinia enterocolitica isolates were biotyped, serotyped, and tested for pathogenicity using a TaqMan PCR directed towards the ail-gene that is associated with human pathogenic strains of Y. enterocolitica.
The samples collected from 99 sheep yielded 567 presumptive Y. enterocolitica colonies. Eighty urease positive isolates, from 35 sheep, were identified as Y. enterocolitica by API 20E. Thirty-four of 35 further subtyped Y. enterocolitica isolates, all from faecal samples, belonged to biotype 1A serotype O:5, O:6. O:13,7 and O:10. One strain was Yersinia mollaretii serotype O:62. No human pathogenic strains of Y. enterocolitica were found in the investigated sheep. Other species identified were Y. kristensenii (n = 4), Y. frederiksenii/intermedia (n = 3), Providencia rettgeri (n = 2), Serratia marcescens (n = 1) and Raoultella ornithinolytica (n = 1).
This study does not support the hypothesis that sheep play an important role in transmission of the known human pathogenic Y. enterocolitica in the studied geographical region. However, because there are studies indicating that some strains of Y. enterocolitica biotype 1A may cause disease in humans, the relative importance of sheep as carriers of human pathogenic strains of Y. enterocolitica remains unclear. Tonsils do not appear to be favourable sites for Y. enterocolitica biotype 1A in sheep.
Human pathogenic strains of Yersinia enterocolitica cause yersiniosis, a food-borne zoonosis. It is a gastrointestinal pathogen causing symptoms which vary depending on the age of the host and the bioserotype of the infecting strain. The most commonly reported symptoms are diarrhea, vomiting, abdominal pain, and fever. There is also a considerable risk of sequelae; reactive arthritis and erythema nodosum are common [1,2] but inflammatory bowel disease and irritable bowel syndrome are also reported . Yersiniosis is the third most commonly reported zoonosis in Sweden, as well as in the EU. Nearly all cases appear sporadically and outbreaks are very rare . In Sweden, yersiniosis is notifiable, and from 2001 through 2010 the annual incidence for the whole country ranged from 3 to 9 cases per 100 000 inhabitants, but was 5 to 16 on the island Gotland . It is important to note that approximately 30% of the cases reported in Sweden are children under five years of age .
This study shows the presence of Y. enterocolitica in tonsil and faecal samples of sheep. The sheep were bred and slaughtered on Gotland, a Swedish island that also has swine and cattle production. In this study no human pathogenic biotype was isolated and no ail-gene was detected. However, a whole set of Y. enterocolitica biotype 1A was found, where 34 out of 35 bioserotyped isolates belonged to this biotype. The absence of human pathogenic Y. enterocolitica strains in this study is at variance with findings in studies outside Sweden. Bioserotype 4/O:3 has been isolated from the rectal content in 12% of lambs (33/281) in a survey from New Zealand  and bioserotype 3/O:5,27 has been isolated from faeces in 3% of sheep (30/973) in a British study . A high seroprevalence (56%) of yersinia antibodies was found in sheep in Northern Germany . However, another German study detected the ail-gene only in 5% (3/64) of the sheep tonsil samples and in none of 200 analysed faecal samples . A study in Nigeria detected the ail-gene in 1% (2/200) of faeces samples in investigated sheep .
Sheep from Gotland do not appear to be important in the transmission of traditionally pathogenic strains of Y. enterocolitica to humans. There is a high frequency of Y. enterocolitica biotype 1A in the faecal samples from the investigated sheep but not in the tonsils. It appears that when studying new potential reservoirs for Y. enterocolitica it is important to use methods that do not discriminate certain serotypes and therefore bias the results. The zoonotic potential of biotype 1A has received more attention recently and identification of pathogenic subgroups is a future challenge for research.
The authors declare that they have no competing interests.
SB, STL and IV initiated and designed the study, STL being responsible for the bacteriological analysis. KS carried out the bacteriological analysis, and drafted the manuscript. GW gave assistance on the bioserotyping. All authors were involved in the interpretation of results and drawing of conclusions, and have given helpful advice in writing the paper. All authors have read and approved the final manuscript.