Ann Rheum Dis. 2014 Oct;73(10):1793-6.

High frequency of reactive arthritis in adults after Yersinia pseudotuberculosis O:1 outbreak caused by contaminated grated carrots.

Vasala M1, Hallanvuo S2, Ruuska P3, Suokas R4, Siitonen A5, Hakala M6.
  • 1Department of Medicine, Kainuu Central Hospital, Kajaani, Finland.
  • 2Finnish Food Safety Authority Evira, Helsinki, Finland.
  • 3Northern Finland Laboratory Centre (NordLab), Kainuu Central Hospital, Kajaani, Finland.
  • 4Department of Pediatrics, Kainuu Central Hospital, Kajaani, Finland.
  • 5Bacteriology Unit, National Institute for Health and Welfare (THL), Helsinki, Finland.
  • 6Department of Musculoskeletal Medicine and Rehabilitation, Medical School, University of Tampere, Tampere, Finland Division of Rheumatology, Department of Medicine and Rehabilitation Center, Päijät-Häme Central Hospital, Lahti, Finland.



OBJECTIVE: We describe the epidemiological and microbiological process in the clearing of a foodborne outbreak of Yersinia pseudotuberculosis O:1 linked to raw carrots and frequency of the associated reactive extra-gastrointestinal manifestations.

METHODS: The patient samples were investigated by routine culture or antibody testing methods. The real-time bacterial PCR was used to detect Y pseudotuberculosis in samples from the grated carrots and in those taken from the carrot storage. Genotype of bacterial isolates was determined by pulsed-field gel electrophoresis. For case identification, we retrospectively looked over the laboratory files of the central hospital focusing on the time period of the outbreak.

RESULTS: Altogether 49 case patients were identified. Y pseudotuberculosis was detected by real-time PCR analysis in samples taken from grated carrots and from the carrot distributor. Bacterial isolates originating from the farm environment showed identical serotype (O:1) and genotype (S12) with the patients’ isolates. Among 37 adults, reactive arthritis (ReA) was found in 8 (22%) and three adults had probable ReA. Six (67%) out of nine human leucocyte antigen (HLA) typed patients with ReA were HLA-B27 positive. Erythema nodosum was found in 42% of the 12 children, whereas none of them had definite ReA.

CONCLUSIONS: In this outbreak, Y pseudotuberculosis was for the first time detected in both patient and food samples. ReA was more common than earlier reported in the outbreaks associated with this pathogen; the reason may be that the previous outbreaks have occurred among children. HLA-B27 frequency was higher than usually reported in single-source outbreaks of ReA.

KEYWORDS: Epidemiology; Infections; Reactive arthritis; Spondyloarthritis

PMID: 23852698



The term reactive arthritis (ReA) was launched 40 years ago in the connection of arthritis triggered by the enteric pathogen Yersinia enterocolitica. (1) Among the other well-known enteric bacteria causing ReA are Salmonella, Shigella and Campylobacter. According to the reports hitherto, Yersinia pseudotuberculosis serotype O:3 has an association with ReA, whereas the association is weak with serotype O:1.

In 2008, a widespread foodborne outbreak of Y pseudotuberculosis infection occurred in Kainuu Region, in Finland. First cases of gastroenteritis appeared at June in the workers who had dined in the same company canteen. Later also nursery and school children developed symptoms compatible with foodborne epidemics. It was found that the same distributor had delivered carrots stored over the winter from a single farm to 57 different canteens.

Approximately 2 weeks after the suspicion of the outbreak, Y pseudotuberculosis could be detected by real-time PCR from samples taken from the grated carrots in one of the canteen kitchens involved and samples taken from the carrot distributor. Actually, this is the first time when Y pseudotuberculosis was detected in the grated carrots collected from the canteen kitchen during the outbreak investigations. Y pseudotuberculosis was also isolated from samples originating from the carrot storage floor and plastic covering of storage box and from conveyor belt of the carrot processing machine. The isolates showed serotype of O:1 and genotype S12 identical with the Y pseudotuberculosis isolates from the patient stool samples.

In Finland, carrots are harvested during September–October and stored at 1°C–2°C. Yersinia bacteria are able to multiply in this temperature. If the carrots have become contaminated by Y pseudotuberculosis during some phase of the process, the prolonged storage provides circumstances for the bacteria to multiply. In this case, carrots stored over the winter were delivered to the canteens where grated carrots are a common vegetable of the menus.

Y pseudotuberculosis infections occur primarily in the northern hemisphere. In recent years, outbreaks of Y pseudotuberculosis linked to fresh produce have been detected repeatedly in Finland, and in some cases, the origin of the contaminated vegetable could have been traced. The origin of the causative Y pseudotuberculosis serotype O:3 strains has been iceberg lettuce and that of O:1 strains carrots.

To our knowledge, this is the first report on a high frequency of ReA (16%) in association with Y pseudotuberculosis O:1 infection. It is to be noted that ReA presented only in the adults, that is, 22% of the 37 infected adult patients had definite ReA and three (8%) additional patients had a probable ReA.

As earlier reported, erythema nodosum was more typical in children (42%) than in adults (22%). Thus, it seems that the musculoskeletal manifestations after Y pseudotuberculosis O:1 infection are diverse, that is, ReA is typical in adults while it is rare in children who are prone to erythema nodosum.

Interestingly, ReA is associated with HLA-B27, whereas erythema nodosum is not. In the present study, 67% of the nine HLA typed patients with ReA were HLA-B27 positive. The frequency was higher than that usually reported in the single source outbreaks of ReA (30%–50%). Does this mean that arthritogenity of Y pseudotuberculosis is low and it often needs HLA-B27 for ReA to be manifest? It is to be noted that HLA-B27 frequency in Finnish population is 14%, which is higher than that usually presented in white populations (8%).

Recent findings, which refer to the central role of interleukin (IL)-23 and IL-23R receptor gene polymorphism in the pathogenesis of spondyloarthtropathies have shed light on the old theory of the connection between gut inflammation and spondyloarthopathies. HLA-B27 can misfold, triggering a cellular stress response in the production of IL-23, and for example, subclinical gut inflammation in ankylosing spondylitis has been shown to be associated with an overexpression of IL-23. In an experimental model of enthesopathy in rats with systemic IL-23 overexpression, Sherlock et al. showed that in the area of enthesitis there are local IL-23R+ resident cells, which are primed to respond immediately to IL-23. (2) According to this theory, gut is the source of production of IL-23 in spondyloarthropathies and the circulating cytokine acts on the tissue resident cells in the joints and entheses inducing inflammation. How this applies to ReA with different sites of primary mucosal immune responses in enteroarthritis and uroarthritis remains to be clarified.

There is weak evidence that early antibiotic treatment at the time of primary infection could prevent the onset of ReA. In the present series, the proportion of patients treated with antibiotics did not differ between patients with and without ReA, however.

In conclusion, finding of Y pseudotuberculosis in stool samples of the diarrhoeal patients and prompt initiation of environmental trace-back investigations enabled early detection of the source of Y pseudotuberculosis O:1 infection. The close collaboration between the microbiologists and epidemiologists as well as the health and food authorities was important in the prevention of further spread of the outbreak. According to our results, ReA is commonly seen in adults after Y pseudotuberculosis O:1 outbreak. The earlier findings of low ReA incidence are from outbreaks in children.



  1. Ahvonen P, Sievers K, Aho K. Arthritis associated with Yersinia enterocolitica infection. Acta Rheumatol Scand 1969;15:232–53.
  2. Sherlock JP, Joyce-Shaikh B, Turner SP, et al. IL-23 induces spondyloarthropathy by acting on ROR-γt+ CD3+CD4-CD8-entheseal resident T cells. Nat Med 2012;18:1069–76.
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