Literature DB >> 19046537

Yersinia pseudotuberculosis O:1 traced to raw carrots, Finland.

Susanna Kangas, Johanna Takkinen, Marjaana Hakkinen, Ulla-Maija Nakari, Tuula Johansson, Heikki Henttonen, Laura Virtaluoto, Anja Siitonen, Jukka Ollgren, Markku Kuusi.   

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Year:  2008        PMID: 19046537      PMCID: PMC2634618          DOI: 10.3201/eid1412.080284

Source DB:  PubMed          Journal:  Emerg Infect Dis        ISSN: 1080-6040            Impact factor:   6.883


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To the Editor: Illness caused by Yersinia pseudotuberculosis is mainly characterized by fever and acute abdominal pain due to mesenteric lymphadenitis that mimics appendicitis. Secondary manifestations include erythema nodosum and reactive arthritis (). Outbreaks have been reported in the Northern Hemisphere, including Canada (,), Japan (), and Russia (). Several community outbreaks have also been reported in Finland since 1982 (,–). Only in a few of the outbreaks has the vector or source of the infection been identified. Recently, fresh produce, such as iceberg lettuce () and carrots (), has been implicated by epidemiologic investigations as a source of infection, but mechanisms of contamination of fresh produce have remained unknown. On April 8, 2004, the National Public Health Institute of Finland was informed of several cases of gastroenteritis in schoolchildren in 1 municipality in northern Finland. On April 13, 2004, stool samples from symptomatic schoolchildren confirmed Y. pseudotuberculosis infections. At the same time, an increase occurred in Y. pseudotuberculosis cases reported to the National Infectious Disease Register (NIDR) from other parts of the country. We conducted epidemiologic, microbiologic, trace-back, and environmental investigations to determine the source of the outbreak and the origin of contamination. In the school outbreak, a survey concerning symptoms of gastrointestinal illness was conducted among all schoolchildren (7–18 years of age) and personnel (N = 900) of the 7 schools in the municipality. A case was defined as a laboratory-confirmed Y. pseudotuberculosis infection in a child or staff member who attended a school that received lunches from the school central kitchen, or as abdominal pain and fever, or erythema nodosum with illness onset from March 8 through March 28, 2004. Of respondents to the survey, 53 met the case definition. Among these respondents, Y. pseudotuberculosis was isolated from stool samples of 5 persons. A case–control study was conducted to identify the source of infection; self-administered questionnaires asked about consumption of items on school menus from March 8 through March 26, 2004. For each of the 53 case-patients identified in the survey, 3 controls were selected from the same class; 39 cases and 107 controls were included the analysis. Univariate analysis showed that a vegetable mixture of carrots and white cabbage served on March 8 and a mixture of cucumber and white cabbage served on March 25 were associated with illness. Multivariate analysis showed that only the carrot–white cabbage mixture was associated with illness. We also conducted a case–control study by mailing questionnaires to 37 persons with microbiologically confirmed Y. pseudotuberculosis infections reported to the NIDR from March 15 through May 7, 2004. These cases were from other parts of the country and were not associated with the school outbreak. For each case, 4 controls matched by age, sex, and municipality were randomly selected from the national population registry. Risk of illness increased with increased frequency of eating fresh carrots. Carrots served in the school were traced back to the farm level. Samples checked included grated carrots, which were available from the school kitchen. The kitchen had received all vegetables from 1 fresh-food processing plant. Samples were taken from the carrot-peeling line, carrot-peeling leftovers, grated carrots, and other vegetable-processing lines at the plant. Carrots originated from only 2 farms, which were inspected, and samples were obtained for bacteriologic examination. Small mammals at the farms were caught in carrot fields and investigated microbiologically to identify the reservoir of Y. pseudotuberculosis. This bacterium was isolated from 1 environmental sample from the carrot-peeling line in the fresh-food processing plant, from spoiled carrots, from fluid draining from spoiled carrots, and from a pooled sample of common shrew (Sorex araneus) intestines from 1 farm. Human and environmental isolates obtained were serotype O:1, subtype O:1b. Pulsed-field gel electrophoresis (PFGE) profiles of isolates from schoolchildren, fluid of spoiled carrots at the infected farm, and shrew intestines were indistinguishable. All 22 isolates from NIDR cases belonged to 2 PFGE genotypes. One genotype had a PFGE profile that was indistinguishable from the profile of the school outbreak isolates and the other genotype differed from these isolates by only 1 fragment. Our study provides microbiologic and epidemiologic evidence that the school outbreak was caused by carrots contaminated at the production farm. We isolated a Y. pseudotuberculosis subtype from human patients that was indistinguishable from isolates from the implicated source and a potential animal reservoir. Although the association between shrews and carrots is uncertain, shrews may have been picked up with carrots by harvesting machinery and ended up dead in wooden storage frames with the carrots. If carrots become contaminated, long storage at cold temperatures favors growth of Y. pseudotuberculosis and may result in human infections. Further studies are needed to determine the mechanism of contamination and other natural reservoirs. After the outbreak, the Finnish Food Safety Authority recommended controlling contamination at the farm level by removing spoiled carrots and paying attention to any subsequent spoilage during handling procedures.
  8 in total

1.  Outbreak of Yersinia pseudotuberculosis in British Columbia--November 1998.

Authors:  E Nowgesic; M Fyfe; J Hockin; A King; H Ng; A Paccagnella; A Trinidad; L Wilcott; R Smith; A Denney; L Struck; G Embree; K Higo; J I Chan; P Markey; S Martin; D Bush
Journal:  Can Commun Dis Rep       Date:  1999-06-01

2.  Multiple outbreaks of Yersinia pseudotuberculosis infections in Finland.

Authors:  Katri Jalava; S Hallanvuo; U-M Nakari; P Ruutu; E Kela; T Heinäsmäki; A Siitonen; J P Nuorti
Journal:  J Clin Microbiol       Date:  2004-06       Impact factor: 5.948

3.  An outbreak of gastrointestinal illness and erythema nodosum from grated carrots contaminated with Yersinia pseudotuberculosis.

Authors:  Katri Jalava; Marjaana Hakkinen; Miia Valkonen; Ulla-Maija Nakari; Taito Palo; Saija Hallanvuo; Jukka Ollgren; Anja Siitonen; J Pekka Nuorti
Journal:  J Infect Dis       Date:  2006-09-27       Impact factor: 5.226

4.  Community outbreak of Yersinia pseudotuberculosis.

Authors:  M Inoue; H Nakashima; O Ueba; T Ishida; H Date; S Kobashi; K Takagi; T Nishu; M Tsubokura
Journal:  Microbiol Immunol       Date:  1984       Impact factor: 1.955

5.  Clinical manifestations of Yersinia pseudotuberculosis infection in children.

Authors:  R Tertti; R Vuento; P Mikkola; K Granfors; A L Mäkelä; A Toivanen
Journal:  Eur J Clin Microbiol Infect Dis       Date:  1989-07       Impact factor: 3.267

6.  Clinical and microbiological follow-up of an outbreak of Yersinia pseudotuberculosis serotype Ib.

Authors:  N Press; M Fyfe; W Bowie; M Kelly
Journal:  Scand J Infect Dis       Date:  2001

7.  A widespread outbreak of Yersinia pseudotuberculosis O:3 infection from iceberg lettuce.

Authors:  J Pekka Nuorti; Taina Niskanen; Saija Hallanvuo; Janne Mikkola; Eija Kela; Maija Hatakka; Maria Fredriksson-Ahomaa; Outi Lyytikainen; Anja Siitonen; Hannu Korkeala; Petri Ruutu
Journal:  J Infect Dis       Date:  2004-02-16       Impact factor: 5.226

8.  An outbreak of Yersinia pseudotuberculosis infection.

Authors:  R Tertti; K Granfors; O P Lehtonen; J Mertsola; A L Mäkelä; I Välimäki; P Hänninen; A Toivanen
Journal:  J Infect Dis       Date:  1984-02       Impact factor: 5.226

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Authors:  T Ringwood; B P Murphy; N Drummond; J F Buckley; A P Coveney; H P Redmond; J P Power; S Fanning; M B Prentice
Journal:  Eur J Clin Microbiol Infect Dis       Date:  2012-06-03       Impact factor: 3.267

2.  Population structure and evolution of pathogenicity of Yersinia pseudotuberculosis.

Authors:  Shear Lane Ch'ng; Sophie Octavia; Qiuyu Xia; An Duong; Mark M Tanaka; Hiroshi Fukushima; Ruiting Lan
Journal:  Appl Environ Microbiol       Date:  2010-12-03       Impact factor: 4.792

3.  Yersinia pseudotuberculosis IP32953 survives and replicates in trophozoites and persists in cysts of Acanthamoeba castellanii.

Authors:  Jennifer Santos-Montañez; Javier A Benavides-Montaño; Angela K Hinz; Viveka Vadyvaloo
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4.  Customizable PCR-microplate array for differential identification of multiple pathogens.

Authors:  Abdela Woubit; Teshome Yehualaeshet; Sherrelle Roberts; Martha Graham; Moonil Kim; Temesgen Samuel
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5.  National outbreak of Yersinia enterocolitica infections in military and civilian populations associated with consumption of mixed salad, Norway, 2014.

Authors:  Emily MacDonald; Margot Einöder-Moreno; Katrine Borgen; Lin Thorstensen Brandal; Lore Diab; Øivind Fossli; Bernardo Guzman Herrador; Ammar Ali Hassan; Gro S Johannessen; Eva Jeanette Johansen; Roger Jørgensen Kimo; Tore Lier; Bjørn Leif Paulsen; Rodica Popescu; Charlotte Tokle Schytte; Kristin Sæbø Pettersen; Line Vold; Øyvind Ørmen; Astrid Louise Wester; Marit Wiklund; Karin Nygård
Journal:  Euro Surveill       Date:  2016-08-25

6.  Genomic Insights into a Sustained National Outbreak of Yersinia pseudotuberculosis.

Authors:  Deborah A Williamson; Sarah L Baines; Glen P Carter; Anders Gonçalves da Silva; Xiaoyun Ren; Jill Sherwood; Muriel Dufour; Mark B Schultz; Nigel P French; Torsten Seemann; Timothy P Stinear; Benjamin P Howden
Journal:  Genome Biol Evol       Date:  2016-12-01       Impact factor: 3.416

7.  Low prevalence of human enteropathogenic Yersinia spp. in brown rats (Rattus norvegicus) in Flanders.

Authors:  Lieze Oscar Rouffaer; Kristof Baert; Anne-Marie Van den Abeele; Ivo Cox; Gerty Vanantwerpen; Lieven De Zutter; Diederik Strubbe; Katleen Vranckx; Luc Lens; Freddy Haesebrouck; Michel Delmée; Frank Pasmans; An Martel
Journal:  PLoS One       Date:  2017-04-12       Impact factor: 3.240

8.  Landscape, Water Quality, and Weather Factors Associated With an Increased Likelihood of Foodborne Pathogen Contamination of New York Streams Used to Source Water for Produce Production.

Authors:  Daniel Weller; Alexandra Belias; Hyatt Green; Sherry Roof; Martin Wiedmann
Journal:  Front Sustain Food Syst       Date:  2020-02-06

9.  Presence of Salmonella spp., Yersinia enterocolitica, Yersinia pseudotuberculosis and Escherichia coli O157:H7 in wild boars.

Authors:  A Sannö; A Aspán; G Hestvik; M Jacobson
Journal:  Epidemiol Infect       Date:  2014-02-06       Impact factor: 4.434

10.  Comparative Genomic Hybridization Analysis of Yersinia enterocolitica and Yersinia pseudotuberculosis Identifies Genetic Traits to Elucidate Their Different Ecologies.

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