1887
  1. Home
  2. Eurosurveillance
  3. Volume 25, Issue 37, 17/Sep/2020
  4. Article
Outbreaks Open Access
Like 0
Download

Abstract

Following outbreaks linked to frozen strawberries in Sweden and Austria in 2018, 65 cases linked to the same hepatitis A virus strain were detected in Germany between October 2018 and January 2020, presenting in two waves. Two case–control studies and a comparison of cases’ consumption frequencies with purchase data from a large consumer panel provided strong evidence for frozen strawberry cake as the main vehicle of transmission. Of 46 cases interviewed, 27 reported consuming frozen strawberry cake and 25 of these identified cake(s) from brand A spontaneously or in product picture-assisted recall. Trace back investigations revealed that the Polish producer involved in the previous outbreaks in Sweden and Austria had received frozen strawberries from Egypt via a wholesaler that also delivered frozen strawberries to manufacturer of brand A. Phylogenetic analyses linked the outbreak strain to similar strains formerly isolated from sewage, stool and strawberries in Egypt. Complete trace back and timely recall of products with strong evidence of contamination is important to control an outbreak and prevent later resurgence, particularly for food items with a long shelf life. Continued molecular surveillance of hepatitis A is needed to identify outbreaks and monitor the success of food safety interventions.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2020.25.37.1900670
2020-09-17
2024-12-21
/content/10.2807/1560-7917.ES.2020.25.37.1900670
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/25/37/eurosurv-25-37-3.html?itemId=/content/10.2807/1560-7917.ES.2020.25.37.1900670&mimeType=html&fmt=ahah

References

  1. Heymann DL, editor. Control of communicable diseases manual. 20th ed. Washington, DC: American Public Health Association; 2015.
  2. Sattar SA, Jason T, Bidawid S, Farber J. Foodborne spread of hepatitis A: Recent studies on virus survival, transfer and inactivation. Can J Infect Dis. 2000;11(3):159-63.  https://doi.org/10.1155/2000/805156  PMID: 18159284 
  3. European Centre for Disease Prevention and Control (ECDC). Hepatitis A. In: Annual epidemiological report for 2016. Stockholm; ECDC; Jan 2019. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/AER-2016-hepatitis-A.pdf
  4. Werber D, Michaelis K, Hausner M, Sissolak D, Wenzel J, Bitzegeio J, et al. Ongoing outbreaks of hepatitis A among men who have sex with men (MSM), Berlin, November 2016 to January 2017 - linked to other German cities and European countries. Euro Surveill. 2017;22(5).  https://doi.org/10.2807/1560-7917.ES.2017.22.5.30457  PMID: 28183391 
  5. Ndumbi P, Freidl GS, Williams CJ, Mårdh O, Varela C, Avellón A, et al. Hepatitis A outbreak disproportionately affecting men who have sex with men (MSM) in the European Union and European Economic Area, June 2016 to May 2017. Euro Surveill. 2018;23(33).  https://doi.org/10.2807/1560-7917.ES.2018.23.33.1700641  PMID: 30131095 
  6. Nordic Outbreak Investigation Team. Joint analysis by the Nordic countries of a hepatitis A outbreak, October 2012 to June 2013: frozen strawberries suspected. Euro Surveill. 2013;18(27):20520.  https://doi.org/10.2807/1560-7917.ES2013.18.27.20520  PMID: 23870076 
  7. Scavia G, Alfonsi V, Taffon S, Escher M, Bruni R, Medici D, et al. A large prolonged outbreak of hepatitis A associated with consumption of frozen berries, Italy, 2013-14. J Med Microbiol. 2017;66(3):342-9.  https://doi.org/10.1099/jmm.0.000433  PMID: 28086079 
  8. Enkirch T, Eriksson R, Persson S, Schmid D, Aberle SW, Löf E, et al. Hepatitis A outbreak linked to imported frozen strawberries by sequencing, Sweden and Austria, June to September 2018. Euro Surveill. 2018;23(41).  https://doi.org/10.2807/1560-7917.ES.2018.23.41.1800528  PMID: 30326994 
  9. Costafreda MI, Bosch A, Pintó RM. Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Appl Environ Microbiol. 2006;72(6):3846-55.  https://doi.org/10.1128/AEM.02660-05  PMID: 16751488 
  10. Michaelis K, Wenzel JJ, Stark K, Faber M. Hepatitis A virus infections and outbreaks in asylum seekers arriving to Germany, September 2015 to March 2016. Emerg Microbes Infect. 2017;6(4):e26.  https://doi.org/10.1038/emi.2017.11  PMID: 28442750 
  11. Hamza H, Abd-Elshafy DN, Fayed SA, Bahgat MM, El-Esnawy NA, Abdel-Mobdy E. Detection and characterization of hepatitis A virus circulating in Egypt. Arch Virol. 2017;162(7):1921-31.  https://doi.org/10.1007/s00705-017-3294-4  PMID: 28303345 
  12. Sofy AR, Hmed AA, Sharaf AMA, El-Dougdoug KA. Human hepatitis A virus isolate Straw-HAV-Egy polyprotein gene, partial cds. GenBank: MF802728.1. Human Foodborne Viruses with other Pathogens and Implementation of Promising Alternatives for Strategies Control. Bethesda: National Center for Biotechnology Information (NCBI) GenBank. [Accessed 4 Sep 2020]. (Forthcoming). Available from: https://www.ncbi.nlm.nih.gov/nuccore/MF802728
  13. European Commission (EC). Rapid Alert System for Food and Feed (RASFF) portal. Foodborne outbreak suspected to be caused by and hepatitis A virus (present) in frozen strawberries from Poland. RASFF 2018.1813. Brussels: EC. [Accessed15 May 2020]. Available from: https://webgate.ec.europa.eu/rasff-window/portal/?event=notificationDetail&NOTIF_REFERENCE=2018.1813
  14. Fitzgerald M, Thornton L, O’Gorman J, O’Connor L, Garvey P, Boland M, et al. Outbreak of hepatitis A infection associated with the consumption of frozen berries, Ireland, 2013--linked to an international outbreak. Euro Surveill. 2014;19(43):20942.  https://doi.org/10.2807/1560-7917.ES2014.19.43.20942  PMID: 25375902 
  15. Guzman-Herrador B, Jensvoll L, Einoder-Moreno M, Lange H, Myking S, Nygard K, et al. Ongoing hepatitis A outbreak in Europe 2013 to 2014: imported berry mix cake suspected to be the source of infection in Norway. Euro Surveill. 2014;19(15):20775.  https://doi.org/10.2807/1560-7917.ES2014.19.15.20775  PMID: 24762662 
  16. Wenzel JJ, Schemmerer M, Oberkofler H, Kerschner H, Sinha P, Koidl C, et al. Hepatitis A Outbreak in Europe: Imported Frozen Berry Mix Suspected to be the Source of At least One Infection in Austria in 2013. Food Environ Virol. 2014;6(4):297-300.  https://doi.org/10.1007/s12560-014-9165-1  PMID: 25183415 
  17. Severi E, Verhoef L, Thornton L, Guzman-Herrador BR, Faber M, Sundqvist L, et al. Large and prolonged food-borne multistate hepatitis A outbreak in Europe associated with consumption of frozen berries, 2013 to 2014. Euro Surveill. 2015;20(29):21192.  https://doi.org/10.2807/1560-7917.ES2015.20.29.21192  PMID: 26227370 
  18. Wang Q, Hirneisen KA, Markland SM, Kniel KE. Survival of murine norovirus, Tulane virus, and hepatitis A virus on alfalfa seeds and sprouts during storage and germination. Appl Environ Microbiol. 2013;79(22):7021-7.  https://doi.org/10.1128/AEM.01704-13  PMID: 24014537 
  19. Shaheen MNF, Elmahdy EM, Chawla-Sarkar M. Quantitative PCR-based identification of enteric viruses contaminating fresh produce and surface water used for irrigation in Egypt. Environ Sci Pollut Res Int. 2019;26(21):21619-28.  https://doi.org/10.1007/s11356-019-05435-0  PMID: 31129895 
  20. Sun B, Bosch A, Myrmel M. Extended direct lysis method for virus detection on berries including droplet digital RT-PCR or real time RT-PCR with reduced influence from inhibitors. J Virol Methods. 2019;271:113638.  https://doi.org/10.1016/j.jviromet.2019.04.004  PMID: 30953663 
  21. Schrader C, Schielke A, Ellerbroek L, Johne R. PCR inhibitors - occurrence, properties and removal. J Appl Microbiol. 2012;113(5):1014-26.  https://doi.org/10.1111/j.1365-2672.2012.05384.x  PMID: 22747964 
  22. Mäde D, Trübner K, Neubert E, Höhne M, Johne R. Detection and Typing of Norovirus from Frozen Strawberries Involved in a Large-Scale Gastroenteritis Outbreak in Germany. Food Environ Virol. 2013;5(3):162-8.  https://doi.org/10.1007/s12560-013-9118-0  PMID: 23888384 
  23. Bernard H, Faber M, Wilking H, Haller S, Höhle M, Schielke A, et al. Large multistate outbreak of norovirus gastroenteritis associated with frozen strawberries, Germany, 2012. Euro Surveill. 2014;19(8):20719.  https://doi.org/10.2807/1560-7917.ES2014.19.8.20719  PMID: 24602278 
  24. Buchholz U, Bernard H, Werber D, Böhmer MM, Remschmidt C, Wilking H, et al. German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med. 2011;365(19):1763-70.  https://doi.org/10.1056/NEJMoa1106482  PMID: 22029753 
Resurgence of an international hepatitis A outbreak linked to imported frozen strawberries, Germany, 2018 to 2020
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Claudia+Ruscher&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ruscher Claudia</a>, <a href="/search?value1=Mirko+Faber&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Faber Mirko</a>, <a href="/search?value1=Dirk+Werber&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Werber Dirk</a>, <a href="/search?value1=Klaus+Stark&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Stark Klaus</a>, <a href="/search?value1=Julia+Bitzegeio&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bitzegeio Julia</a>, <a href="/search?value1=Kai+Michaelis&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Michaelis Kai</a>, <a href="/search?value1=Daniel+Sagebiel&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sagebiel Daniel</a>, <a href="/search?value1=J%C3%BCrgen+J+Wenzel&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wenzel Jürgen J</a>, <a href="/search?value1=Julia+Enkelmann&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Enkelmann Julia</a></span>. Resurgence of an international hepatitis A outbreak linked to imported frozen strawberries, Germany, 2018 to 2020. <a href="/content/ecdc">Euro Surveill.</a> 2020;25(37):pii=1900670. <a href="https://doi.org/10.2807/1560-7917.ES.2020.25.37.1900670" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2020.25.37.1900670</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 01 Nov 2019;&nbsp;&nbsp; <span class="generated">Accepted</span>: 21 Jul 2020 </span> </p>
/content/10.2807/1560-7917.ES.2020.25.37.1900670
/content/10.2807/1560-7917.ES.2020.25.37.1900670
Loading

Data & Media loading...

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error