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Improving preparedness to respond to cross-border hepatitis A outbreaks in the European Union/European Economic Area: towards comparable sequencing of hepatitis A virus
- Theresa Enkirch1,2 , Ettore Severi3,4 , Harry Vennema5 , Lelia Thornton6 , Jonathan Dean7 , Maria-Louise Borg8 , Anna Rita Ciccaglione9 , Roberto Bruni9 , Iva Christova10 , Siew Lin Ngui11 , Koye Balogun11 , Vratislav Němeček12 , Mia Kontio13 , Mária Takács14 , Andrea Hettmann14 , Rita Korotinska15 , Arthur Löve16 , Ana Avellón17 , Milagros Muñoz-Chimeno17 , Rita de Sousa18 , Denisa Janta19 , Jevgenia Epštein20 , Sofieke Klamer21 , Vanessa Suin22 , Stephan W Aberle23 , Heidemarie Holzmann23 , Kassiani Mellou24 , Josefine Lundberg Ederth1 , Lena Sundqvist1 , Anne-Marie Roque-Afonso25 , Sanja Kurečić Filipović26 , Mario Poljak27 , Line Vold28 , Kathrine Stene-Johansen28 , Sofie Midgley29 , Thea Kølsen Fischer29,30 , Mirko Faber31 , Jürgen J Wenzel32 , Johanna Takkinen3 , Katrin Leitmeyer3
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View Affiliations Hide AffiliationsAffiliations: 1 Public Health Agency of Sweden, Solna, Sweden 2 European Programme for Public Health Microbiology Training (EUPHEM), European Centre for Disease Prevention and Control (ECDC), Solna, Sweden 3 European Centre for Disease Prevention and Control (ECDC), Solna, Sweden 4 Karolinska Institutet, Stockholm, Sweden 5 National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands 6 HSE - Health Protection Surveillance Centre, Dublin, Ireland 7 National Virus Reference Laboratory, Dublin, Ireland 8 Ministry of Health, Msida, Malta 9 National Institute of Health, Rome, Italy 10 National Center of Infectious and Parasitic Diseases, Sofia, Bulgaria 11 Public Health England (PHE), London, United Kingdom 12 National Institute of Public Health, Prague, Czech Republic 13 National Institute for Health and Welfare (THL), Helsinki, Finland 14 National Public Health Institute, Budapest, Hungary 15 Centre for Disease Prevention and Control, Riga, Latvia 16 Landspitali- National University Hospital, Reykjavik, Iceland 17 Carlos III Institute of Health, Madrid, Spain 18 National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, Portugal 19 National Institute of Public Health, Bucharest, Romania 20 Health Board, Tallinn, Estonia 21 Scientific Institute of Public Health, Brussels, Belgium 22 Sciensano, Directorate Infectious diseases in humans, Brussels, Belgium 23 Center for Virology, Medical University of Vienna, Vienna, Austria 24 Hellenic Centre for Disease Control and Prevention, Athens, Greece 25 National Reference Centre for Hepatitis A, Villejuif, France 26 Croatian Institute of Public Health, Zagreb, Croatia 27 Institute of Microbiology and Immunology, Ljubljana, Slovenia 28 Norwegian institute of Public Health, Oslo, Norway 29 Statens Serum Institut (SSI), Copenhagen, Denmark 30 Department of Infectious Diseases and Global Health, University of Southern Denmark, Odense, Denmark 31 Robert Koch Institute (RKI), Berlin, Germany 32 National Reference Laboratory for HAV, Regensburg University Medical Center, Regensburg, GermanyTheresa EnkirchTheresa.Enkirch folkhalsomyndigheten.se
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Citation style for this article: Enkirch Theresa, Severi Ettore, Vennema Harry, Thornton Lelia, Dean Jonathan, Borg Maria-Louise, Ciccaglione Anna Rita, Bruni Roberto, Christova Iva, Ngui Siew Lin, Balogun Koye, Němeček Vratislav, Kontio Mia, Takács Mária, Hettmann Andrea, Korotinska Rita, Löve Arthur, Avellón Ana, Muñoz-Chimeno Milagros, de Sousa Rita, Janta Denisa, Epštein Jevgenia, Klamer Sofieke, Suin Vanessa, Aberle Stephan W, Holzmann Heidemarie, Mellou Kassiani, Ederth Josefine Lundberg, Sundqvist Lena, Roque-Afonso Anne-Marie, Filipović Sanja Kurečić, Poljak Mario, Vold Line, Stene-Johansen Kathrine, Midgley Sofie, Fischer Thea Kølsen, Faber Mirko, Wenzel Jürgen J, Takkinen Johanna, Leitmeyer Katrin. Improving preparedness to respond to cross-border hepatitis A outbreaks in the European Union/European Economic Area: towards comparable sequencing of hepatitis A virus. Euro Surveill. 2019;24(28):pii=1800397. https://doi.org/10.2807/1560-7917.ES.2019.24.28.1800397 Received: 19 Jul 2018; Accepted: 18 Feb 2019
Abstract
Sequence-based typing of hepatitis A virus (HAV) is important for outbreak detection, investigation and surveillance. In 2013, sequencing was central to resolving a large European Union (EU)-wide outbreak related to frozen berries. However, as the sequenced HAV genome regions were only partly comparable between countries, results were not always conclusive.
The objective was to gather information on HAV surveillance and sequencing in EU/European Economic Area (EEA) countries to find ways to harmonise their procedures, for improvement of cross-border outbreak responses.
In 2014, the European Centre for Disease Prevention and Control (ECDC) conducted a survey on HAV surveillance practices in EU/EEA countries. The survey enquired whether a referral system for confirming primary diagnostics of hepatitis A existed as well as a central collection/storage of hepatitis A cases’ samples for typing. Questions on HAV sequencing procedures were also asked. Based on the results, an expert consultation proposed harmonised procedures for cross-border outbreak response, in particular regarding sequencing. In 2016, a follow-up survey assessed uptake of suggested methods.
Of 31 EU/EEA countries, 23 (2014) and 27 (2016) participated. Numbers of countries with central collection and storage of HAV positive samples and of those performing sequencing increased from 12 to 15 and 12 to 14 respectively in 2016, with all countries typing an overlapping fragment of 218 nt. However, variation existed in the sequenced genomic regions and their lengths.
While HAV sequences in EU/EEA countries are comparable for surveillance, collaboration in sharing and comparing these can be further strengthened.
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References
-
World Health Organization (WHO). WHO position paper on hepatitis A vaccines – June 2012. Wkly Epidemiol Rec. 2012;87(28/29):261-76. PMID: 22905367
-
Vos T, Allen C, Arora M, Barber RM, Bhutta ZA, Brown A, et al. GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388(10053):1545-602. https://doi.org/10.1016/S0140-6736(16)31678-6 PMID: 27733282
-
Jacobsen KH, Wiersma ST. Hepatitis A virus seroprevalence by age and world region, 1990 and 2005. Vaccine. 2010;28(41):6653-7. https://doi.org/10.1016/j.vaccine.2010.08.037 PMID: 20723630
-
Jeong SH, Lee HS. Hepatitis A: clinical manifestations and management. Intervirology. 2010;53(1):15-9. https://doi.org/10.1159/000252779 PMID: 20068336
-
European Centre for Disease Prevention and Control (ECDC). Hepatitis A. In: ECDC. Annual epidemiological report for 2016. Stockholm: ECDC; 2019. Available from: https://ecdc.europa.eu/sites/portal/files/documents/AER_for_2016-hepatitis-A_0.pdf
-
European Centre for Disease Prevention and Control (ECDC). Surveillance Atlas of Infectious Diseases. Stockholm: ECDC; 2019. Available from: https://ecdc.europa.eu/en/surveillance-atlas-infectious-diseases
-
Carrillo-Santisteve P, Tavoschi L, Severi E, Bonfigli S, Edelstein M, Byström E, et al. ECDC HAV Expert Panel. Seroprevalence and susceptibility to hepatitis A in the European Union and European Economic Area: a systematic review. Lancet Infect Dis. 2017;17(10):e306-19. https://doi.org/10.1016/S1473-3099(17)30392-4 PMID: 28645862
-
Beauté J, Westrell T, Schmid D, Müller L, Epstein J, Kontio M, et al. Travel-associated hepatitis A in Europe, 2009 to 2015. Euro Surveill. 2018;23(22):1700583. https://doi.org/10.2807/1560-7917.ES.2018.23.22.1700583 PMID: 29871720
-
Sane J, MacDonald E, Vold L, Gossner C, Severi E, on behalf of the International Outbreak Investigation Team. Multistate foodborne hepatitis A outbreak among European tourists returning from Egypt--need for reinforced vaccination recommendations, November 2012 to April 2013. Euro Surveill. 2015;20(4):21018. https://doi.org/10.2807/1560-7917.ES2015.20.4.21018 PMID: 25655054
-
MacDonald E, Steens A, Stene-Johansen K, Gillesberg Lassen S, Midgley S, Lawrence J, et al. Increase in hepatitis A in tourists from Denmark, England, Germany, the Netherlands, Norway and Sweden returning from Egypt, November 2012 to March 2013. Euro Surveill. 2013;18(17):20468. PMID: 23647624
-
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):30457. https://doi.org/10.2807/1560-7917.ES.2017.22.5.30457 PMID: 28183391
-
Beebeejaun K, Degala S, Balogun K, Simms I, Woodhall SC, Heinsbroek E, et al. Outbreak of hepatitis A associated with men who have sex with men (MSM), England, July 2016 to January 2017. Euro Surveill. 2017;22(5):30454. https://doi.org/10.2807/1560-7917.ES.2017.22.5.30454 PMID: 28183392
-
Freidl GS, Sonder GJ, Bovée LP, Friesema IH, van Rijckevorsel GG, Ruijs WL, et al. Hepatitis A outbreak among men who have sex with men (MSM) predominantly linked with the EuroPride, the Netherlands, July 2016 to February 2017. Euro Surveill. 2017;22(8):30468. https://doi.org/10.2807/1560-7917.ES.2017.22.8.30468 PMID: 28251892
-
European Centre for Disease Prevention and Control (ECDC). Hepatitis A outbreaks in the EU/EEA mostly affecting men who have sex with men - third update, 28 June 2017. Stockholm: ECDC. 2017. Available from: https://ecdc.europa.eu/en/publications-data/rapid-risk-assessment-hepatitis-outbreak-eueea-mostly-affecting-men-who-have-sex
-
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):1700641. https://doi.org/10.2807/1560-7917.ES.2018.23.33.1700641 PMID: 30131095
-
Latash J, Dorsinville M, Del Rosso P, Antwi M, Reddy V, Waechter H, et al. Notes from the Field: Increase in Reported Hepatitis A Infections Among Men Who Have Sex with Men - New York City, January-August 2017. MMWR Morb Mortal Wkly Rep. 2017;66(37):999-1000. https://doi.org/10.15585/mmwr.mm6637a7 PMID: 28934181
-
Rivas V, Barrera A, Pino K, Núñez R, Caceres CJ, Lopez-Lastra M, et al. Hepatitis A outbreak since November 2016 affecting men who have sex with men (MSM) in Chile connected to the current outbreak in MSM in Europe, situation up to October 2017. Euro Surveill. 2018;23(9):1800060. https://doi.org/10.2807/1560-7917.ES.2018.23.9.18-00060 PMID: 29510780
-
Gozlan Y, Bar-Or I, Rakovsky A, Savion M, Amitai Z, Sheffer R, et al. Ongoing hepatitis A among men who have sex with men (MSM) linked to outbreaks in Europe in Tel Aviv area, Israel, December 2016 - June 2017. Euro Surveill. 2017;22(29):30575. https://doi.org/10.2807/1560-7917.ES.2017.22.29.30575 PMID: 28749336
-
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
-
Bruni R, Taffon S, Equestre M, Chionne P, Madonna E, Rizzo C, 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(2):e0149642. https://doi.org/10.1371/journal.pone.0149642 PMID: 26901877
-
Costa-Mattioli M, Di Napoli A, Ferré V, Billaudel S, Perez-Bercoff R, Cristina J. Genetic variability of hepatitis A virus. J Gen Virol. 2003;84(Pt 12):3191-201. https://doi.org/10.1099/vir.0.19532-0 PMID: 14645901
-
Lemon SM, Jansen RW, Brown EA. Genetic, antigenic and biological differences between strains of hepatitis A virus. Vaccine. 1992;10(Suppl 1):S40-4. https://doi.org/10.1016/0264-410X(92)90540-Z PMID: 1335657
-
Robertson BH, Jansen RW, Khanna B, Totsuka A, Nainan OV, Siegl G, et al. Genetic relatedness of hepatitis A virus strains recovered from different geographical regions. J Gen Virol. 1992;73(Pt 6):1365-77. https://doi.org/10.1099/0022-1317-73-6-1365 PMID: 1318940
-
Desbois D, Couturier E, Mackiewicz V, Graube A, Letort MJ, Dussaix E, et al. Epidemiology and genetic characterization of hepatitis A virus genotype IIA. J Clin Microbiol. 2010;48(9):3306-15. https://doi.org/10.1128/JCM.00667-10 PMID: 20592136
-
Kroneman A, de Sousa R, Verhoef L, Koopmans MPG, Vennema HOn Behalf Of The HAVNet Network. Usability of the international HAVNet hepatitis A virus database for geographical annotation, backtracing and outbreak detection. Euro Surveill. 2018;23(37):1700802. https://doi.org/10.2807/1560-7917.ES.2018.23.37.1700802 PMID: 30229723
-
Aragonès L, Bosch A, Pintó RM. Hepatitis A virus mutant spectra under the selective pressure of monoclonal antibodies: codon usage constraints limit capsid variability. J Virol. 2008;82(4):1688-700. https://doi.org/10.1128/JVI.01842-07 PMID: 18057242
-
National Institute for Public Health and the Environment (RIVM). HAVNet. Bilthoven: RIVM. Available from: https://www.rivm.nl/documenten/typing-protocol-havnet-vp1p2a.
-
European Commission. Commission Regulation (EC) No 2018/945 of 22 June 2018 on the communicable diseases and related special health issues to be covered by epidemiological surveillance as well as relevant case definitions under Decision No 1082/2013/EU of the European Parliament and of the Council of 22 October 2013. Official Journal of the European Union. Luxembourg: Publications Office of the European Union. 06/072018: L 170. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32018D0945&from=EN#page=22
-
European Centre for Disease Control and Prevention (ECDC). ECDC Map Maker (EMMa). Stockhom: ECDC. [Accessed 18 Jan 2018]. Available from: https://emma.ecdc.europa.eu/
-
Nordic Outbreak Investigation Team C. 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
-
Mellou K, Chrisostomou A, Sideroglou T, Georgakopoulou T, Kyritsi M, Hadjichristodoulou C, et al. Hepatitis A among refugees, asylum seekers and migrants living in hosting facilities, Greece, April to December 2016. Euro Surveill. 2017;22(4):30448. https://doi.org/10.2807/1560-7917.ES.2017.22.4.30448 PMID: 28181904
-
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):1800528. https://doi.org/10.2807/1560-7917.ES.2018.23.41.1800528 PMID: 30326994
-
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
-
Costa-Mattioli M, Cristina J, Romero H, Perez-Bercof R, Casane D, Colina R, et al. Molecular evolution of hepatitis A virus: a new classification based on the complete VP1 protein. J Virol. 2002;76(18):9516-25. https://doi.org/10.1128/JVI.76.18.9516-9525.2002 PMID: 12186933
-
Brown EA, Jansen RW, Lemon SM. Characterization of a simian hepatitis A virus (HAV): antigenic and genetic comparison with human HAV. J Virol. 1989;63(11):4932-7. PMID: 2552172
-
Wang H, Zheng H, Cao J, Zhou W, Yi Y, Jia Z, et al. Genetic diversity of hepatitis A virus in China: VP3-VP1-2A genes and evidence of quasispecies distribution in the isolates. PLoS One. 2013;8(9):e74752. https://doi.org/10.1371/journal.pone.0074752 PMID: 24069343
-
Vaughan G, Xia G, Forbi JC, Purdy MA, Rossi LM, Spradling PR, et al. Genetic relatedness among hepatitis A virus strains associated with food-borne outbreaks. PLoS One. 2013;8(11):e74546. https://doi.org/10.1371/journal.pone.0074546 PMID: 24223112
-
Food and Drug Administration bacteriological analytical manual (BAM). Detection of hepatitis A in foods. BAM; [Accessed 08 Jan 2018]. Available from: http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm374006.htm
-
Bruni R, Taffon S, Equestre M, Cella E, Lo Presti A, Costantino A, et al. Hepatitis a virus genotypes and strains from an endemic area of Europe, Bulgaria 2012-2014. BMC Infect Dis. 2017;17(1):497. https://doi.org/10.1186/s12879-017-2596-1 PMID: 28705178
-
European Centre for Disease Prevention and Control (ECDC). Expert opinion on whole genome sequencing for public health surveillance. Stockholm: ECDC; 2016. Available from: https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/whole-genome-sequencing-for-public-health-surveillance.pdf
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