1887

Abstract

In 2013/2014, Italy experienced one of the largest community-wide prolonged outbreaks of hepatitis A virus (HAV) throughout the country. The article provides a comprehensive description of the outbreak and the investigation carried out by a multidisciplinary National Task Force, in collaboration with regional and local public health authorities. Control strategies of food-borne HAV infection in both the human and food sectors are also described.

Enhanced human epidemiological and microbiological surveillance together with microbiological monitoring of HAV in food and trace-back investigation were conducted.

A total of 1803 HAV cases were identified from 1 January 2013 to 31 August 2014, in Italy. Sequencing was possible for 368 cases (20.4 %), mostly collected between 1 January 2013 and 28 February 2014, and 246 cases (66.8 %) harboured an HAV outbreak strain. Imported frozen berries contaminated with HAV were identified as the vehicle of the outbreak which also involved many other European countries in 2013 and 2014. Epidemiological evidence obtained through a case–control study was supported by the finding of a 100 % nucleotide similarity of the VP1/2A sequences of HAVs detected in human and food samples. Trace-back investigation revealed an extremely complex supplying network with no possibility for a point source potentially explaining the vast contamination of berries found in Italy.

The investigation benefited from an excellent collaboration among different sectors who shared proactively the available information. Our findings highlight the importance of considering frozen berries among the highest risk factors for HAV.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000433
2017-03-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jmm/66/3/342.html?itemId=/content/journal/jmm/10.1099/jmm.0.000433&mimeType=html&fmt=ahah

References

  1. Vaughan G, Forbi JC, Xia GL, Fonseca-Ford M, Vazquez R et al. Full-length genome characterization and genetic relatedness analysis of hepatitis A virus outbreak strains associated with acute liver failure among children. J Med Virol 2014; 86:202–208 [View Article][PubMed]
    [Google Scholar]
  2. European Centre for Disease Prevention and Control Hepatitis A Virus in the EU/EEA, 1975-2014 Stockholm: ECDC; 2016
    [Google Scholar]
  3. World Health Organization, Department of Immunization, Vaccines and Biologicals The Global Prevalence of Hepatitis A Virus Infection and Susceptibility: a Systematic Review Geneva, Switzerland: World Health Organization; 2010 WHO/IVB/10.01
    [Google Scholar]
  4. Jacobsen KH, Wiersma ST. Hepatitis A virus seroprevalence by age and world region, 1990 and 2005. Vaccine 2010; 28:6653–6657 [View Article]
    [Google Scholar]
  5. Tosti ME, Spada E, Romanò L, Zanetti A, Mele A et al. Acute hepatitis A in Italy: incidence, risk factors and preventive measures. J Viral Hepat 2008; 15:26–32 [View Article][PubMed]
    [Google Scholar]
  6. Istituto Superiore di Sanità The Italian integrated epidemiological system for acute viral hepatitis (SEIEVA). Incidence rates of hepatitis A by age and year of notification. www.iss.it/binary/seie2/cont/Tassi_Epatite_A_2014.pdf [accessed 13 January 2016]
  7. Chironna M, Prato R, Sallustio A, Martinelli D, Tafuri S et al. Hepatitis A in Puglia (south Italy) after 10 years of universal vaccination: need for strict monitoring and catch-up vaccination. BMC Infect Dis 2012; 12:271 [View Article][PubMed]
    [Google Scholar]
  8. Gentile C, Alberini I, Manini I, Rossi S, Montomoli E et al. Hepatitis A seroprevalence in Tuscany, Italy. Euro Surveill 2009; 14:19146[PubMed]
    [Google Scholar]
  9. Pontrelli G, Boccia D, Di Renzi M, Massari M, Giugliano F et al. Epidemiological and virological characterization of a large community-wide outbreak of hepatitis A in southern Italy. Epidemiol Infect 2008; 136:1027–1034 [View Article][PubMed]
    [Google Scholar]
  10. Conferenza Permanente per i Rapporti tra il Governo Piano Nazionale Prevenzione Vaccinale (PNPV) 2012–2014 Roma, Italy: 2012
    [Google Scholar]
  11. Rizzo C, Alfonsi V, Bruni R, Busani L, Ciccaglione A et al. Ongoing outbreak of hepatitis A in Italy: preliminary report as of 31 May 2013. Eurosurveillance 2013:18
    [Google Scholar]
  12. Mele A, Rosmini F, Zampieri A, Gill ON. Integrated epidemiological system for acute viral hepatitis in Italy (SEIEVA): description and preliminary results. Eur J Epidemiol 1986; 2:300–304 [View Article][PubMed]
    [Google Scholar]
  13. Montano-Remacha C, Ricotta L, Alfonsi V, Bella A, Tosti M et al. Hepatitis A outbreak in Italy, 2013: a matched case-control study. Euro Surveill 2014; 19:20906 [View Article][PubMed]
    [Google Scholar]
  14. Bruni R, Taffon S, Equestre M, Chionne P, Madonna E et al. Key role of sequencing to trace hepatitis A viruses circulating in Italy during a large multi-country European foodborne outbreak in 2013. PLoS One 2016; 11:e0149642 [View Article][PubMed]
    [Google Scholar]
  15. Le Guyader F, Dubois E, Menard D, Pommepuy M. Detection of hepatitis A virus, rotavirus, and enterovirus in naturally contaminated shellfish and sediment by reverse transcription-seminested PCR. Appl Environ Microbiol 1994; 60:3665–3671[PubMed]
    [Google Scholar]
  16. Chiapponi C, Pavoni E, Bertasi B, Baioni L, Scaltriti E et al. Isolation and genomic sequence of hepatitis A virus from mixed frozen berries in Italy. Food Environ Virol 2014; 6:202–206 [View Article][PubMed]
    [Google Scholar]
  17. Butot S, Putallaz T, Amoroso R, Sánchez G. Inactivation of enteric viruses in minimally processed berries and herbs. Appl Environ Microbiol 2009; 75:4155–4161 [View Article][PubMed]
    [Google Scholar]
  18. Italian Ministry of Health 2013; Press release n. 199: hepatitis "A" and frozen berries consumption. Update and reccomendations by the Ministry of Health [Italian]. www.salute.gov.it/portale/news/p3_2_4_1_1_stampa.jsp?id=4095 [accessed 5 December 2016]
  19. Italian Ministry of Health 2013; Alert on the presence of hepatitis A virus in frozen berries [Italian]. www.trovanorme.salute.gov.it/norme/renderNormsanPdf?anno=0&codLeg=46736&parte=1%20&serie= [accessed 5 December 2016]
  20. Ford L, Miller M, Cawthorne A, Fearnley E, Kirk M. Approaches to the surveillance of foodborne disease: a review of the evidence. Foodborne Pathog Dis 2015; 12:927–936 [View Article][PubMed]
    [Google Scholar]
  21. Gossner CM, Severi E. Three simultaneous, food-borne, multi-country outbreaks of hepatitis A virus infection reported in EPIS-FWD in 2013: what does it mean for the European Union?. Euro Surveill 2014; 19:20941 [View Article][PubMed]
    [Google Scholar]
  22. Severi E, Verhoef L, Thornton L, Guzman-Herrador BR, Faber M 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; 20:21192 [View Article][PubMed]
    [Google Scholar]
  23. Fitzgerald M, Thornton L, O'Gorman J, O'Connor L, Garvey P et al. Outbreak of hepatitis A infection associated with the consumption of frozen berries, Ireland, 2013 – linked to an international outbreak. Euro Surveill 2014; 19:20942 [View Article][PubMed]
    [Google Scholar]
  24. Gossner C, Severi E, Danielsson N, Hutin Y, Coulombier D. Changing hepatitis A epidemiology in the European Union: new challenges and opportunities. EuroSurveill 2015; 20:21101 [View Article]
    [Google Scholar]
  25. Maunula L, Kaupke A, Vasickova P, Söderberg K, Kozyra I et al. Tracing enteric viruses in the European berry fruit supply chain. Int J Food Microbiol 2013; 167:177–185 [View Article]
    [Google Scholar]
  26. Tavoschi L, Severi E, Niskanen T, Boelaert F, Rizzi V et al. Food-borne diseases associated with frozen berries consumption: a historical perspective, European Union, 1983 to 2013. Euro Surveill 2015; 20:21193 [View Article][PubMed]
    [Google Scholar]
  27. Koopmans M, Duizer E. Foodborne viruses: an emerging problem. Int J Food Microbiol 2004; 90:23–41 [View Article]
    [Google Scholar]
  28. Verhaelen K, Bouwknegt M, Carratalà A, Lodder-Verschoor F, Diez-Valcarce M et al. Virus transfer proportions between gloved fingertips, soft berries, and lettuce, and associated health risks. Int J Food Microbiol 2013; 166:419–425 [View Article]
    [Google Scholar]
  29. European Centre for Disease Preventikn and Control 2014; Food- and waterborne diseases and zoonoses in: Annual epidemiological report, 2014. Food- and waterborne diseases and zoonoses. http://ecdc.europa.eu/en/publications/_layouts/forms/Publication_DispForm.aspx?List=4f55ad51-4aed-4d32-b960-af70113dbb90&ID=1210 [accessed 15 January 2016]
  30. European Food Safety Authority Scientific opinion on the risk posed by pathogens in food of non-animal origin. Part 2. EFSA Journal 2014; 12: [View Article]
    [Google Scholar]
  31. European Food Safety Authority Tracing of food items in connection to the multinational hepatitis A virus outbreak in Europe. EFSA Journal 2014; 12: [View Article]
    [Google Scholar]
  32. European centre for disease prevention and control 2014; Outbreak of hepatitis A in EU/EEA countries – Secondupdate, 11 April 2014. Stockholm: ECDC. http://ecdc.europa.eu/en/publications/Publications/ROA-Hepatitis%20A%20virus-Italy%20Ireland%20Netherlands%20Norway%20France%20Germany%20Sweden%20United%20Kingdom%20-%20final.pdf [accessed 5 December 2016]
  33. 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; 5:162–168 [View Article]
    [Google Scholar]
  34. Nordic Outbreak Investigation Team Joint analysis by the Nordic countries of a hepatitis A outbreak, October 2012 to June 2013: frozen strawberries suspected. EuroSurveill 2013:18
    [Google Scholar]
  35. Swinkels HM, Kuo M, Embree G, Andonov A, Henry B et al. Hepatitis A outbreak in British Columbia, Canada: the roles of established surveillance, consumer loyalty cards and collaboration, February to May 2012. Euro Surveill 2014; 19:20792 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000433
Loading
/content/journal/jmm/10.1099/jmm.0.000433
Loading

Data & Media loading...

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