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Eurosurveillance, Volume 10, Issue 38, 22 September 2005
Articles

Citation style for this article: Falkenhorst G, Krusell L, Lisby M, Madsen SB, Böttiger BE, Mølbak K. Imported frozen raspberries cause a series of norovirus outbreaks in Denmark, 2005. Euro Surveill. 2005;10(38):pii=2795. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2795

Imported frozen raspberries cause a series of norovirus outbreaks in Denmark, 2005

Gerhard Falkenhorst1,2 (GFA@ssi.dk), Lars Krusell3, Morten Lisby4, Søren Bo Madsen5, Blenda Böttiger 6 and Kåre Mølbak1

1Department of Epidemiology, Statens Serum Institut, Copenhagen, Denmark
2European Programme for Intervention Epidemiology Training (EPIET)
3Regional Food Inspection Authority Århus, Denmark
4Regional Food Inspection Authority Northeast-Sjælland, Denmark
5Regional Food Inspection Authority Copenhagen, Denmark
6Department of Virology, Statens Serum Institut, Copenhagen, Denmark

A total of six point source outbreaks of norovirus infection from June to September 2005 in Denmark have now been linked to frozen raspberries imported from Poland. This number includes two outbreaks reported on previously [1]. All outbreaks occurred in institutions or commercial catering settings (Table). A cold dish prepared from frozen raspberries, which had not been heated, had been served one day before the start of each outbreak. In the first five outbreaks, frozen raspberry pieces had been used, which could be traced to the same large batch imported to Denmark from Poland in spring 2005. With more than 1000 people affected in total, this batch has caused the largest number of foodborne infections attributable to a single vehicle in Denmark in many years.

Table. Outbreaks of norovirus infection caused by contaminated frozen raspberries, Denmark 2005

Place Start date Cases

Microbiology

(stool investigations)

Aalborg hospital (Jutland) 21 May about 450 patients and staff noro GG II.7
Nursing home, Greater Copenhagen 30 May about 70 residents and staff clinically noro (by Kaplan criteria [2]) *
Meals-on-wheels service, Copenhagen area 2 June about 400 clients noro GG II.4
Private function at a restaurant, Sjælland 7 August about 40 participants noro GG II.b
Nursing home, Greater Copenhagen 16 August about 50 residents and staff noro GG II.7
Clothing company, Jutland 7 September 33 employees noro (typing results pending)

* stool samples for norovirus testing were not available, because the outbreak was reported after a delay of 5 weeks

Frozen raspberry pieces were first identified as the likely outbreak vehicle through case-control studies done during the first outbreak, which occurred in Aalborg hospital at the end of May 2005. After being informed of this result by the food authorities, the importer withdrew the incriminated batch of frozen raspberry pieces from the market. Delays in the implementation of the withdrawal resulted in a second large outbreak among elderly clients of a meals-on-wheels service in early June. An estimated 400 people (median age 85 years, range 41–102) were affected and at least 23 required hospital admission.

Cohort studies and microbiological investigations of the two outbreaks in August provided evidence that the withdrawal had not been effectively implemented, even by then. The findings prompted a public warning by the Danish Veterinary and Food Administration (DVFA) against the use of frozen raspberry pieces from this particular imported batch by a press release with a link to their homepage, where details about the product were provided [3]. The withdrawal process is also the subject of discussion by the Danish parliamentary committee overseeing the food and agricultural policies. As far as is known, the implicated raspberry pieces have only been sold to commercial and institutional caterers (in bags of 2.5kg) and not to the general public.

The latest outbreak in September 2005 occurred after consumption of a dish prepared with whole frozen raspberries, supplied by a different Polish producer to a different Danish importer. A cohort study among all employees of the affected company in Jutland showed that having eaten hindbærkoldskål (a traditional Danish cold dish made from buttermilk, fromage frais, sugar and vanilla sugar with raspberries added) in the company canteen, was associated with illness with a risk ratio of 12.2 (95% CI 3.2-47). The attack rate was 82% among the exposed and 31 of 33 patients recalled eating the raspberry dish (preliminary data).

Other food items (pineapple, chickenburger, tomatoes), which were associated with illness in the univariable analysis, showed no significant association in the multivariable analysis. A sample of the frozen raspberries is currently being tested for norovirus. Theoretically, one of the other ingredients of the hindbærkoldskål could have caused the outbreak, although, of all the ingredients, only frozen raspberries have previously been reported as a vehicle of norovirus outbreaks (in Finland 1998 [4], Sweden 2001 [5], France 2005 [6]). The DVFA immediately issued a press release with information about the incriminated raspberry batch [7].

Stool samples were available from patients in five of the outbreaks. Positive results for norovirus polymerase chain reaction (PCR) assays confirmed the cause of all five outbreaks. Surprisingly, different types of norovirus were found: genogroup (GG) II.4 and GG II.b in one outbreak each, and GG II.7 in two outbreaks whereas all samples from any given outbreak showed an identical norovirus strain. All bacteriological stool tests were negative.

Enquiries into the origin of the raspberries provided some clues as to why several different norovirus strains were found: what arrived in Denmark as one large batch of frozen raspberries was composed of raspberries originally grown on several different small-scale farms in Poland. The raspberries were purchased during summer 2004 by a Polish company, which froze and packed them in 2.5kg plastic bags, before exporting them.

Contamination with norovirus may have occurred at farm level by faecally-contaminated irrigation water, during harvesting by infected farm workers and/or during processing and freezing by infected workers at company level. Our hypothesis is that several independent contamination events took place; this would explain the heterogeneous distribution of norovirus strains in the shipment to Denmark. We have asked the Polish food authorities to investigate, whether the frozen raspberry pieces and the whole frozen raspberries originate from the same farms or processing company.

The Danish findings, including information about the exporters, were reported to the European Early Warning and Response System (EWRS), the Rapid Alert System for Food and Feed (RASFF, http://europa.eu.int/comm/food/food/rapidalert/index_en.htm) and the Foodborne Viruses in Europe network (FBVE, http://www.eufoodborneviruses.co.uk). As a short term measure to prevent further outbreaks, it seems advisable to heat frozen raspberries before consumption. For a more causal prevention, the cultivation and production process of raspberries should be scrutinised.

As Polish frozen raspberries are known to be exported to several European countries, it would be extremely surprising, if Denmark were the only country where there were recent outbreaks due to frozen raspberries. The authors would be very interested in information about norovirus outbreaks associated with frozen raspberries or other berries from other countries. People with information should contact Gerhard Falkenhorst, at GFA@ssi.dk

References:
  1. Korsager B, Hede S, Bøggild H, Böttiger B, Mølbak K. Two outbreaks of norovirus infections associated with the consumption of imported frozen raspberries, Denmark, May-June 2005. Eurosurveillance 2005;10(25): 050623. (http://www.eurosurveillance.org/ew/2005/050623.asp#1)
  2. Kaplan JE, Gary GW, Baron RC, Singh N, Schonberger LB, Feldman R, et al. Epidemiology of Norwalk gastroenteritis and the role of Norwalk virus in outbreaks of acute non-bacterial gastroenteritis. Ann Intern Med 1982; 96: 756-61.
  3. Ministeriet for Familie-og Forbrugeranliggender. Foedevarestyrelsen. Storkøkkener bør tjekke frossen hindbærsmuld. Press release, 24 August 2005. (http://www.foedevarestyrelsen.dk/Presserum/Pressemeddelelser/Arkiv/2005/Storkokkener_bor_tjekke_frossen_hindbaersmuld.htm)
  4. Pönkä A, Maunula L, von Bonsdorff CH, Lyytikäinen O. An outbreak of calicivirus associated with consumption of frozen raspberries. Epidemiol Infect 1999; 123(3): 469-74.
  5. Le Guyader FS, Mittelholzer C, Haugarreau L, Hedlund KO, Alsterlund R, Pommepuy M, Svensson L. Detection of noroviruses in raspberries associated with a gastroenteritis outbreak. Int J Food Microbiol 2004; 97(2): 179-86.
  6. Cotterelle B, Drougard C, Rolland J, Becamel M, Boudon M, Pinede S, et al. Outbreak of norovirus infection associated with the consumption of frozen raspberries, France, March 2005. Eurosurveillance 2005; 10(17): 050428. (http://www.eurosurveillance.org/ew/2005/050428.asp#1)
  7. Ministeriet for Familie-og Forbrugeranliggender. Foedevarestyrelsen. Hindbær skyld i nyt sygdomsudbrud. Press release, 16 September 2005. (http://www.foedevarestyrelsen.dk/Presserum/Pressemeddelelser/Hindbaer+skyld+i+nyt+sygdomsudbrud.htm)

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