Skip to main content
SpringerLink
Log in

Norovirus GII.17 Caused Five Outbreaks Linked to Frozen Domestic Bilberries in Finland, 2019

  • Research
  • Published:
Food and Environmental Virology Aims and scope Submit manuscript

Abstract

In March 2019, the Finnish Institute for Health and Welfare and Finnish Food Authority started an outbreak investigation after a notification of food business operators’ recall of frozen bilberries due to a norovirus finding. A retrospective search was conducted in the food and waterborne outbreak notification system to identify the notifications linked to norovirus and consumption of bilberries in January–March 2019. Five outbreaks were found in which norovirus GII or GII.17 had been detected in patient samples. A pooled retrospective cohort study was performed for those four in which a questionnaire study had been done. A case was defined as a person with diarrhoea or vomiting within 2 days after consuming a meal studied at one of the outbreak locations. Of 79 participants, 45 (57%) cases were identified. Persons that had consumed foods containing unheated bilberries were three times more likely to get ill than those who had not consumed them (RR 3.1, CI 95% 1.2–8.1, p = 0.02). Norovirus GII.17 was found in 16/17 patient samples sent for further typing. Identical norovirus GII.17 was detected in frozen Finnish bilberries and patient samples. At the berry packaging premises, signs of norovirus GII contamination were found in packaging lines. A new procedure for extracting viral nucleic acid from food and environmental samples was used during the outbreak investigation. Consumption of industrially packed frozen berries as heated would be one of the means to prevent norovirus infections.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Boundary data © National Land Survey of Finland, 2022. Other data © Finnish Food Authority, 2022

Similar content being viewed by others

Data Availability

Individual survey data cannot be shared due to EU’s general data protection regulation and Finnish data protection law connected to it.

References

  • Ahmed, S., Hall, A., Robinson, A., Verhoef, L., Premkumar, P., Parashar, U., Koopmans, M., & Lopman, B. (2014). Global prevalence of norovirus in cases of gastroenteritis: A systematic review and meta-analysis. Lancet Infectious Diseases, 14(8), 725–730.

    Article  PubMed  Google Scholar 

  • Atmar, R., Opekun, A., Gilger, M., Estes, M., Crawford, S., Neill, F., & Graham, D. (2008). Norwalk virus shedding after experimental human infection. Emerging Infectious Diseases, 14, 1553–1557.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barrabeig, I., Rovira, A., Buesa, J., Bartolomé, R., Pintó, R., Prellezo, H., & Domínguez, À. (2010). Foodborne norovirus outbreak: The role of an asymptomatic food handler. BMC Infectious Diseases, 10, 269.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bennett, S., Sodha, S., Ayers, T., Lynch, M., Gould, L., & Tauxe, R. (2018). Produce-associated foodborne disease outbreaks, USA, 1998–2013. Epidemiology and Infection, 146, 1397–1406.

    Article  CAS  PubMed  Google Scholar 

  • Bernard, H., Faber, M., Wilking, H., Haller, S., Höhle, M., Schielke, A., Ducomble, T., Siffczyk, C., Merbecks, S. S., Fricke, G., Hamouda, O., Stark, K., & Werber, D. (2014). Large multistate outbreak of norovirus gastroenteritis associated with frozen strawberries, Germany, 2012. Eurosurveillance, 19, 20719.

    Article  CAS  PubMed  Google Scholar 

  • Bouwknegt, M., Verhaelen, K., Rzezutka, A., Kozyra, I., Maunula, L., von Bonsdorff, C.-H., Vantarakis, A., Kokkinos, P., Petrovic, T., Lazic, S., Pavlik, I., Vasickova, P., Willems, K. A., Havelaar, A. H., Rutjes, A. S., & de Roda, H. A. M. (2015). Quantitative farm-to-fork risk assesment model for norovirus and hepatitis a virus in European leafy green vegetable and berry fruit supply chains. International Journal of Food Microbiology, 198, 50–58.

    Article  PubMed  Google Scholar 

  • Boxman, I., Dijkman, R., Verhoef, L., Maat, A., van Dijk, G., Vennema, H., & Koopmans, M. (2009). Norovirus on swabs taken from hands illustrate route of transmission: A case study. Journal of Food Protection, 72, 1753–1755.

    Article  PubMed  Google Scholar 

  • Bozkurt, H., Phan-Thien, K.-Y., van Ogtrop, F., Bell, T., & McConchie, R. (2021). Outbreaks, occurrence, and control of norovirus and hepatitis a virus contamination in berries: A review. Critical Reviews in Food Science and Nutrition, 61(1), 116–138.

    Article  CAS  PubMed  Google Scholar 

  • Cook, N., Williams, L., & D’Agostino, M. (2019). Prevalence of norovirus in produce sold at retail in the United Kingdom. Food Microbiology, 79, 85–89.

    Article  PubMed  Google Scholar 

  • De Keuckelaere, A., Li, D., Deliens, B., Stals, A., & Uyttendaele, M. (2015). Batch testing for noroviruses in frozen raspberries. International Journal of Food Microbiology, 192, 43–50.

    Article  PubMed  Google Scholar 

  • Derrick, J., Hollinghurst, P., O’Brien, S., Elviss, N., Allen, D., & Iturriza-G’omara, M. (2021). Measuring transfer of human norovirus during sandwich production: Simulating the role of food, food handlers and the environment. International Journal of Food Microbiology, 348, 109151.

    Article  CAS  PubMed  Google Scholar 

  • Elviss, N., Allen, D., Kelly, D., Akello, J., Hau, S., Fox, A., Hopkins, M., Derrick, J., O’Brien, S., & Iturriza-Gomara, M. (2022). Norovirus attribution study: Detection of norovirus from the commercial food preparation environment in outbreak and non-outbreak premises. Journal of Applied Microbiology, 00, 1–13.

    Google Scholar 

  • European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). (2015). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA Journal, 13(4329), 190.

    Google Scholar 

  • European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). (2016). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. EFSA Journal, 14(e04634), 231.

    Google Scholar 

  • European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). (2017). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA Journal, 15(e05077), 228.

    Google Scholar 

  • European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). (2018). The European Union summary report on trends and source of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA Journal, 16(5500), 262.

    Google Scholar 

  • European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). (2019). The European Union One Health 2018 Zoonoses Report. EFSA Journal, 17(5926), 276.

    Google Scholar 

  • European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). (2021). The European Union one health 2019 zoonoses report. EFSA Journal, 19(6406), 286.

    Google Scholar 

  • Gao, X., Wang, Z., Wang, Y., Liu, Z., Guan, X., Ma, Y., Zhou, H., Jiang, Y., Cui, W., Wang, L., & Xu, Y. (2019). surveillance of norovirus contamination in commercial fresh/Frozen Berries from Heilongjiang Province, China, using a taqman real-time RT-PCR assay. Food Microbiology, 82, 119–126.

    Article  CAS  PubMed  Google Scholar 

  • Hardstaff, J., Clough, H., Lutje, V., McIntyre, M., Harris, J., Garner, P., & O’Brien, S. (2018). Foodborne and food-handler norovirus outbreaks: A systematic review. Foodborne Pathogens and Disease, 15(10), 589–597.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kendra, J., Tohma, K., & Parra, G. (2022). Global and regional circulation trends of norovirus genotypes and recombinants, 1995–2019: A comprehensive review of sequences from public databases. Reviews in Medical Virology. https://doi.org/10.1002/rmv.2354

    Article  PubMed  PubMed Central  Google Scholar 

  • Kojima, S., Kageyama, T., Fukushi, S., Hoshino, F., Shinohara, M., Uchida, K., Natori, K., Takeda, N., & Katayama, K. (2002). Genogroup-specific PCR primers for detection of Norwalk-like viruses. Journal of Virological Methods, 100, 107–114.

    Article  CAS  PubMed  Google Scholar 

  • Kokkinos, P., Kozyra, I., Lazic, S., Bouwknegt, M., Rutjes, S., Willem, K., Moloney, R., de Roda, H. A., Kaupke, A., Legaki, E., D’Agostino, M., Cook, N., Rzezutka, A., Petrovic, T., & Vantrakis, A. (2012). Harmonised investigation of the occurrence of human enteric viruses in the leafy green vegetable supply chain in three European countries. Food and Environmental Virology, 4, 179–191.

    Article  CAS  PubMed  Google Scholar 

  • Kokkinos, P., Kozyra, I., Lazic, S., Söderberg, K., Vasickova, P., Bouwknegt, M., Rutjes, S., Willems, K., Moloney, R., de Roda Husman, A. M., Kaupke, A., Legaki, E., D’Agostino, M., Cook, N., von Bonsdorff, C.-H., Rzezutka, A., Petrovic, T., Maunula, L., Pavlik, I., & Vantarakis, A. (2017). Virological quality of irrigation water in leafy green vegetables and berry fruits production chains. Food and Environmental Virology, 9, 72–78.

    Article  CAS  PubMed  Google Scholar 

  • Kroneman, A., Vega, E., Vennema, H., Vinjé, J., White, P. A., Hansman, G., Green, K., Martella, V., Katayama, K., & Koopmans, M. (2013). Proposal for a unified norovirus nomenclature and genotyping. Archives of Virology, 158, 2059–2068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kroneman, A., Verhoef, L., Harris, J., Vennema, H., Duizer, E., van Duynhoven, Y., Gray, J., Iturriza, M., Böttiger, B., Falkenhorst, G., Johnsen, C., von Bonsdorff, C.-H., Maunula, L., Kuusi, M., Pothier, P., Gallay, A., Schreier, E., Höhne, M., Koch, J., Szücs, G., et al. (2008). analysis of integrated virological and epidemiological reports of norovirus outbreaks collected within the foodborne viruses in Europe Network from 1 July 2001 to 30 June 2006. Journal of Clinical Microbiology, 46, 2959–2965.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumthip, K., Khamrin, P., Ushijima, H., & Maneekarn, N. (2021). Molecular detection and characterization of norovirus in asymptomatic food handlers in Chiang Mai, Thailand. Infection, Genetics and Evolution, 89, 104725.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Fan, X., Yu, G., Wei, P., Wang, Y., & Guo, H. (2021). An acute gastroenteritis outbreak associated with breakfast contaminated with norovirus by asymptotic food handler at a kindergarten in Shenzhen, China. BMC Infectious Diseases, 21, 54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loisy, F., Atmar, R., Guillon, P., Le Cann, P., Pommepuy, M., & Le Guyader, F. (2005). Real-time RT-PCR for norovirus screening in shellfish. Journal Virological Methods, 123, 1–7.

    Article  CAS  Google Scholar 

  • Loutreul, J., Cazeaux, C., Levert, D., Nicolas, A., Vautier, S., Le Sauvage, A., Perelle, S., & Morin, T. (2014). Prevalence of human norovirus in frozen marketed shellfish, red fruits and fresh vegetables. Food and Environmental Virology, 6, 157–168.

    Article  CAS  PubMed  Google Scholar 

  • Mathijs, E., Stals, A., Baert, L., Botteldoorn, N., Denayer, S., Mauroy, A., Scipioni, A., Daube, G., Dierick, K., Herman, L., van Coillie, E., Uyttendaele, M., & Thiry, E. (2012). A review of known and hypothetical transmission routes for noroviruses. Food and Environmental Virology, 4, 131–152.

    Article  PubMed  Google Scholar 

  • Mattison, K., Harlow, J., Morton, V., Cook, A., Pollari, F., Bidawid, S., & Farber, J. (2010). Enteric viruses in ready-to-eat packaged leafy greens. Emerging Infectious Diseases, 16, 1815–1817.

    Article  PubMed  PubMed Central  Google Scholar 

  • Maunula, L., Kaupke, A., Vasickova, P., Söderberg, K., Kozyra, I., Lazic, S., van der Poel, W. H. M., Bouwknegt, M., Rutjes, S., Willem, K. A., Moloney, R., D’Agostino, M., de Roda Husman, A. M., von Bonsdorff, C.-H., Rzezutka, A., Pavlik, I., Petrovic, T., & Cook, N. (2013). Tracking enteric viruses in the European berry fruit supply chain. International Journal of Food Microbiology, 167, 177–185.

    Article  PubMed  Google Scholar 

  • Nicolay, N., McDermott, R., Kelly, M., Gorby, M., Prendergast, T., Tuite, G., Coughlan, S., McKeown, P., & Sayers, G. (2011). Potential role of asymptomatic kitchen food handlers during a food-borne outbreak of norovirus infection, Dublin, Ireland, March 2009. Euro Surveillance, 16(30), 19931.

    PubMed  Google Scholar 

  • Niskanen, T., Johansson, T., Kuusi, M., Raahenmaa, M., Siitonen, A., & Tuominen, P. (2006). Foodborne and waterborne outbreaks in Finland 2005. Evira Publications, 2, 52p.

    Google Scholar 

  • Oteiza, J., Prez, V., Pereyra, D., Jaureguiberry, M., Sánchez, G., Sant’Ana, A., & Barril, P. (2022). Occurrence of norovirus, rotavirus, hepatitis a virus, and enterovirus in berries in Argentina. Food and Environmental Virology, 14, 170–177.

    Article  CAS  PubMed  Google Scholar 

  • Pavoni, E., Bertasi, B., Galuppini, E., Mangeri, L., Meletti, F., Tilola, M., Carta, V., Todeschi, S., & Losio, M.-N. (2022). Detection of hepatitis a virus and norovirus in different food categories: A 6-year survey in Italy. Food and Environmental Virology, 14, 69–76.

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Rodríquez, F., González-García, P., Valero, A., Hernández, M., & Rodríquez-Lázaro, D. (2014). Impact of the prevalence of different pathogens on the performance of sampling plans in lettuce products. International Journal of Food Microbiology, 184, 69–73.

    Article  Google Scholar 

  • Persson, S., Nybogård, L., Simonsson, M., & Eriksson, R. (2020). Optimisation and evaluation of an automated system for extraction of viral RNA from oysters. International Journal of Food Microbiology, 315, 108386.

    Article  CAS  PubMed  Google Scholar 

  • Pihlajasaari, A., Leinonen, E., Markkula, A., Miettinen, I., Rimhanen-Finne, R., Summa, M., & Zacheus, O. (2021). Foodborne and waterborne outbreaks in Finland in 2017–2019. Finnish Food Authority Publications, 7(2021), 80.

    Google Scholar 

  • Pihlajasaari, A., Leinonen, E., Miettinen, I., Rimhanen-Finne, R., Simola, M., Tuutti, E., Huusko, S., & Zacheus, O. (2019). Foodborne and waterborne outbreaks in Finland 2014–2016. Finnish Food Authority Publications, 2(2019), 68.

    Google Scholar 

  • Pönkä, A., Maunula, L., von Bonsdorff, C.-H., & Lyytikäinen, O. (1999). An outbreak of calicivirus associated with consumption of frozen raspberries. Epidemiology and Infection, 123, 469–474.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rönnqvist, M., Aho, E., Mikkelä, A., Ranta, J., Tuominen, P., Rättö, M., & Maunula, L. (2014). Norovirus transmission between hands, gloves, utensils, and fresh produce during simulated food handling. Applied and Environmental Microbiology, 80, 5403–5410.

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Sarvikivi, E., Roivainen, M., Maunula, L., Niskanen, T., Korhonen, T., Lappalainen, M., & Kuusi, M. (2012). Multiple norovirus outbreaks linked to imported frozen raspberries. Epidemiology and Infection, 140, 260–267.

    Article  CAS  PubMed  Google Scholar 

  • Stals, A., Baert, L., Jasson, V., van Coillie, E., & Uyttendaele, M. (2011). Screening of fruit products for norovirus and the difficulty of interpreting positive PCR results. Journal of Food Protection, 74, 425–431.

    Article  PubMed  Google Scholar 

  • Stals, A., Uyttendaele, M., Baert, L., & van Coillie, E. (2013). Norovirus transfer between foods and food contact materials. Journal of Food Protection, 76, 1202–1209.

    Article  PubMed  Google Scholar 

  • Steele, M., Lambert, D., Bissonnette, R., Yamamoto, E., Hardie, K., & Locas, A. (2022). Norovirus GI and GII and hepatitis A virus in berries and pomegranate arils in Canada. International Journal of Food Microbiology, 379, 109840.

    Article  CAS  PubMed  Google Scholar 

  • Summa M. (2019). Human Noroviruses: Detection in Food and New Transmission Routes. University of Helsinki, http://urn.fi/URN:ISBN:978-951-51-5335-7.

  • Tavoschi, L., Severi, E., Niskanen, T., Boelaert, F., Rizzi, V., Gomes Dias, J., Nichols, G., Takkinen, J., & Coulombier, D. (2015). Food-borne diseases associated with frozen berries consumption: a historical perspective, European Union, 1983 to 2013. Eurosurveillance, 20, 21193.

    Article  CAS  PubMed  Google Scholar 

  • Torok, V., Hodgson, K., Jolley, J., Turnbull, A., & McLeod, C. (2019). Estimating risk associated with human norovirus and hepatitis A virus in fresh Australian leafy greens and berries at retail. International Journal of Food Microbiology, 309, 108327.

    Article  CAS  PubMed  Google Scholar 

  • Tuladhar, E., Hazeleger, W., Koopmans, M., Zwietering, M., Duizer, E., & Beumer, R. (2013). Transfer of noroviruses between fingers and fomites and food products. International Journal of Food Microbiology, 167, 346–352.

    Article  PubMed  Google Scholar 

  • Verhaelen, K., Bouwknegt, M., Carratala, A., Lodder-Verschoor, F., Diez-Valcarce, M., Rodriguez-Lazaro, D., de Roda, H. A., & Rutjes, S. (2013). Virus transfer proportions between gloved fingertips, soft berries, and lettuce, and associated health risks. International Journal of Food Microbiology, 166, 419–425.

    Article  PubMed  Google Scholar 

  • Vinjé, J., Hamidjaja, R., & Sobsey, M. (2004). Development and application of a capsid VP1 (region D) based reverse transcription PCR assay for genotyping of genogroup I and II noroviruses. Journal of Virological Methods, 116, 109–117.

    Article  PubMed  Google Scholar 

  • Wei, J., & Kniel, K. (2010). Pre-harvest viral contamination of crops originating from fecal matter. Food and Environmental Virology, 2, 195–206.

    Article  Google Scholar 

  • White, A., Tillman, A., Hedberg, C., Bruce, B., Batz, M., Seys, S., Dewey-Mattia, D., Bazaco, M., & Scallan, W. E. (2022). Foodborne illness outbreaks reported to national Surveillance, United States, 2009–2018. Emerging Infectious Diseases, 28(6), 1117–1127.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Many thanks to all laboratory personnel and staff in the FFA and FIHW, as well as the local food safety authorities, for their valuable contributions.

Funding

No funds, grant, or other support was received.

Author information

Authors and Affiliations

  1. Microbiology Unit, Laboratory and Research Division, Finnish Food Authority, Helsinki, Finland

    Maija Summa

  2. Food Chain Division, Microbiological Food Safety Unit, Finnish Food Authority, Helsinki, Finland

    Enni Tuutti

  3. Expert Microbiology Unit, Finnish Institute for Health and Welfare, Helsinki, Finland

    Haider Al-Hello

  4. Infectious Disease Control and Vaccinations Unit, Finnish Institute for Health and Welfare, Helsinki, Finland

    Liisa-Maija Huttunen & Ruska Rimhanen-Finne

Authors
  1. Maija Summa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Enni Tuutti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haider Al-Hello
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Liisa-Maija Huttunen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruska Rimhanen-Finne
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.S. was responsible for laboratory analyses of food and environmental samples and sequence comparison of all samples and drafted the first version of the manuscript. E.T. was responsible for trace back investigation of the bilberries. H.A-H. was responsible for laboratory analyses of human samples. L-M.H. collected and analyzed epidemiological data. R.R-F. was responsible for coordination of the outbreak investigation and the epidemiological investigation. All authors participated in writing and reviewing the manuscript.

Corresponding author

Correspondence to Maija Summa.

Ethics declarations

Competing Interests

The authors have no competing interests to declare that are relevant to the content of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Summa, M., Tuutti, E., Al-Hello, H. et al. Norovirus GII.17 Caused Five Outbreaks Linked to Frozen Domestic Bilberries in Finland, 2019. Food Environ Virol (2024). https://doi.org/10.1007/s12560-024-09587-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12560-024-09587-2

Keywords

Search

Navigation