Surveillance and outbreak report Open Access
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This report describes an outbreak investigation starting with two closely related suspected food-borne clusters of Dutch hepatitis A cases, nine primary cases in total, with an unknown source in the Netherlands. The hepatitis A virus (HAV) genotype IA sequences of both clusters were highly similar (459/460 nt) and were not reported earlier. Food questionnaires and a case–control study revealed an association with consumption of mussels. Analysis of mussel supply chains identified the most likely production area. International enquiries led to identification of a cluster of patients near this production area with identical HAV sequences with onsets predating the first Dutch cluster of cases. The most likely source for this cluster was a case who returned from an endemic area in Central America, and a subsequent household cluster from which treated domestic sewage was discharged into the suspected mussel production area. Notably, mussels from this area were also consumed by a separate case in the United Kingdom sharing an identical strain with the second Dutch cluster. In conclusion, a small number of patients in a non-endemic area led to geographically dispersed hepatitis A outbreaks with food as vehicle. This link would have gone unnoticed without sequence analyses and international collaboration.


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  1. Food and Agriculture Organization of the United Nations/World Health Organization (FAO/WHO). 2008. Viruses in Food: Scientific advice to support risk management activities: meeting report. Microbiological Risk Assessment Series, No. 13. [Accessed 17 Feb 2012]. Available from: http://www.who.int/foodsafety/publications/micro/Viruses_in_food_MRA.pdf
  2. Petrignani M, Verhoef L, Vennema H, van Hunen R, Baas D, van Steenbergen JE, et al. Underdiagnosis of foodborne hepatitis A, The Netherlands, 2008-2010(1.). Emerg Infect Dis. 2014;20(4):596-602.  https://doi.org/10.3201/eid2004.130753  PMID: 24655539 
  3. Petrignani M, Harms M, Verhoef L, van Hunen R, Swaan C, van Steenbergen J, et al. Update: a food-borne outbreak of hepatitis A in the Netherlands related to semi-dried tomatoes in oil, January-February 2010. Euro Surveill. 2010;15(20):19572. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19572 PMID: 20504389 
  4. Fournet N, Baas D, van Pelt W, Swaan C, Ober H, Isken L, et al. Another possible food-borne outbreak of hepatitis A in the Netherlands indicated by two closely related molecular sequences, July to October 2011. Euro Surveill. 2012;17(6):20079. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20079 PMID: 22340976 
  5. Gillesberg Lassen S, Soborg B, Midgley SE, Steens A, Vold L, Stene-Johansen K, et al. Ongoing multi-strain food-borne hepatitis A outbreak with frozen berries as suspected vehicle: four Nordic countries affected, October 2012 to April 2013. Euro Surveill. 2013;18(17):20467. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20467 PMID: 23647625 
  6. European Centre for Disease Prevention and Control (ECDC). Joint ECDC-EFSA assessment: outbreak of hepatitis A virus infection in residents and travellers to Italy. Stockholm: ECDC; 2013. [Accessed 17 Oct 2014]. Available from: http://ecdc.europa.eu/en/publications/Publications/hepatitis-A-outbreak-of-hepatitis-A-virus-infection-in-residents-and-travellers-to-Italy.pdf
  7. Centres for Disease Control and Prevention (CDC). Multistate outbreak of hepatitis A virus infections linked to pomegranate seeds from Turkey. Atlanta: CDC; 28 Oct 2013. Available from: http://www.cdc.gov/hepatitis/Outbreaks/2013/A1b-03-31/
  8. European Food Safety Authority (EFSA). Tracing of food items in connection to the multinational hepatitis A virus outbreak in Europe. EFSA Journal 2014;12(9):3821. Available from: http://www.efsa.europa.eu/sites/default/files/scientific_output/files/main_documents/3821.pdf
  9. Jacobsen K. The global prevalence of hepatitis A virus infection and susceptibility: a systematic review. World Health Organization: Geneva; 2009. Available from: http://apps.who.int/iris/bitstream/10665/70180/1/WHO_IVB_10.01_eng.pdf
  10. Grinde B, Stene-Johansen K, Sharma B, Hoel T, Jensenius M, Skaug K. Characterisation of an epidemic of hepatitis A virus involving intravenous drug abusers--infection by needle sharing? J Med Virol. 1997;53(1):69-75.  https://doi.org/10.1002/(SICI)1096-9071(199709)53:1<69::AID-JMV12>3.0.CO;2-S  PMID: 9298735 
  11. Stene-Johansen K, Tjon G, Schreier E, Bremer V, Bruisten S, Ngui SL, et al. Molecular epidemiological studies show that hepatitis A virus is endemic among active homosexual men in Europe. J Med Virol. 2007;79(4):356-65.  https://doi.org/10.1002/jmv.20781  PMID: 17311331 
  12. Friesema IHM, van Gageldonk-Lafeber AB, van Pelt W. Extension of traditional infectious disease surveillance with a repeated population survey. Eur J Public Health. 2015;25(1):130-4.  https://doi.org/10.1093/eurpub/cku122  PMID: 25085476 
  13. CEN/ISO. Microbiology of food and animal feed - Horizontal method for determination of hepatitis A virus and norovirus in food using real-time RT-PCR. 2013. CEN ISO/TS 15216-2.
  14. Tang YW, Wang JX, Xu ZY, Guo YF, Qian WH, Xu JX. A serologically confirmed, case-control study, of a large outbreak of hepatitis A in China, associated with consumption of clams. Epidemiol Infect. 1991;107(3):651-7.  https://doi.org/10.1017/S0950268800049347  PMID: 1661240 
  15. Sánchez G, Pintó RM, Vanaclocha H, Bosch A. Molecular characterization of hepatitis a virus isolates from a transcontinental shellfish-borne outbreak. J Clin Microbiol. 2002;40(11):4148-55.  https://doi.org/10.1128/JCM.40.11.4148-4155.2002  PMID: 12409389 
  16. Shieh YC, Khudyakov YE, Xia G, Ganova-Raeva LM, Khambaty FM, Woods JW, et al. Molecular confirmation of oysters as the vector for hepatitis A in a 2005 multistate outbreak. J Food Prot. 2007;70(1):145-50. PMID: 17265873 
  17. Pintó RM, Costafreda MI, Bosch A. Risk assessment in shellfish-borne outbreaks of hepatitis A. Appl Environ Microbiol. 2009;75(23):7350-5.  https://doi.org/10.1128/AEM.01177-09  PMID: 19820160 
  18. Conaty S, Bird P, Bell G, Kraa E, Grohmann G, McAnulty JM. Hepatitis A in New South Wales, Australia from consumption of oysters: the first reported outbreak. Epidemiol Infect. 2000;124(1):121-30.  https://doi.org/10.1017/S0950268899003386  PMID: 10722139 
  19. Croci L, Ciccozzi M, De Medici D, Di Pasquale S, Fiore A, Mele A, et al. Inactivation of hepatitis A virus in heat-treated mussels. J Appl Microbiol. 1999;87(6):884-8.  https://doi.org/10.1046/j.1365-2672.1999.00935.x  PMID: 10664911 
  20. Croci L, De Medici D, Di Pasquale S, Toti L. Resistance of hepatitis A virus in mussels subjected to different domestic cookings. Int J Food Microbiol. 2005;105(2):139-44.  https://doi.org/10.1016/j.ijfoodmicro.2005.04.008  PMID: 16054720 
  21. European Commission. Commission Decision of 11 December 1992 approving certain treatments to inhibit the development of pathogenic micro-organisms in bivalve molluscs and marine gastropods (93/25/EEC). Official Journal of the European Communities. 25.1.1993:L 16. Available from: http://eur-lex.europa.eu/legal-content/EN/ALL/?uri=CELEX:31993D0025
  22. Millard J, Appleton H, Parry JV. Studies on heat inactivation of hepatitis A virus with special reference to shellfish. Part 1. Procedures for infection and recovery of virus from laboratory-maintained cockles. Epidemiol Infect. 1987;98(3):397-414.  https://doi.org/10.1017/S0950268800062166  PMID: 3036554 
  23. World Health Organization/Food and Agriculture Organization of the United Nations (WHO/FAO). Guidelines on the Application of General Principles of Food Hygiene to the Control of Viruses in Food’. CAC/GL-79-2012. Rome: WHO/FAO; 2012. [Accessed 31 Mar 2015]. Available from: http://www.codexalimentarius.org/standards/list-of-standards/
  24. European Commission. Community Guide to the Principles of Good Practice for the Microbiological Classification and Monitoring of Bivalve Mollusc Production and Relaying Areas with regard to Regulation 854/2004. Luxembourg: European Commission. Issue 2, January 2014. Available from: http://ec.europa.eu/food/food/biosafety/hygienelegislation/docs/community_guide_microbiological_monitoring_bivalve_mollusc_harvesting_ar.pdf

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