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Rapid communications Start of the 2014/15 influenza season in : drifted influenza A(H3N2) viruses circulate as dominant subtype

E Broberg ([email protected])1, R Snacken1, C Adlhoch1, J Beauté1, M Galinska2, D Pereyaslov2, C Brown2, P Penttinen1, on behalf of the WHO European Region and the European Influenza Surveillance Network3 1. European Centre for Disease Prevention and Control (ECDC), , 2. World Health Organization (WHO) Regional Office for Europe, Copenhagen, 3. The members of the network are listed at the end of the article

Citation style for this article: Broberg E, Snacken R, Adlhoch C, Beauté J, Galinska M, Pereyaslov D, Brown C, Penttinen P, on behalf of the WHO European Region and the European Influenza Surveillance Network. Start of the 2014/15 influenza season in Europe: drifted influenza A(H3N2) viruses circulate as dominant subtype. Euro Surveill. 2015;20(4):pii=21023. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=21023

Article submitted on 22 January 2015 / published on 29 January 2015

The influenza season 2014/15 started in Europe in influenza (timing and spread), its impact and sever- week 50 2014 with influenza A(H3N2) viruses predomi- ity (groups which are most affected), the predominat- nating. The majority of the A(H3N2) viruses character- ing influenza type and subtype, as well as analyses of ised antigenically and/or genetically differ from the virus strains to support the WHO recommendations for northern hemisphere vaccine component which may the composition of seasonal influenza vaccines (www. result in reduced vaccine effectiveness for the season. flunewseurope.org). The northern hemisphere influ- We therefore anticipate that this season may be more enza vaccine composition recommendation is given by severe than the 2013/14 season. Treating influenza WHO at the end of February each year. with antivirals in addition to prevention with vaccina- tion will be important. Influenza surveillance in Europe is mainly based on primary care sentinel sites collecting specimens from Influenza activity started increasing in the west- patients with ILI and/or ARI [1,3]. Data are collected ern part of the World Health Organization (WHO) at the national level and reported to the European European Region during week 50 2014, when Malta, level according to standardised case definitions [4,5]. the Netherlands and Sweden reported medium inten- The national influenza centres perform antigenic and sity of influenza activity which refers to usual activ- genetic characterisation of influenza viruses as well as ity of influenza season [1]. Rates of influenza-like antiviral susceptibility testing of a representative sam- illness (ILI) and/or acute respiratory infection (ARI) ple of virus isolates. have continued to increase, and in week 2 2015, 13 countries (Albania, Finland, , , Iceland, In addition to the primary care surveillance, particu- Malta, the Netherlands, , , , larly since the 2009 influenza A(H1N1) pandemic, hos- Sweden, , the (UK)) in pital surveillance of laboratory-confirmed influenza the WHO European Region reported medium intensity cases has been conducted, including for this season, and Albania, the Netherlands, Portugal, Spain and in Finland, France, Ireland, Spain, Sweden and the UK. Switzerland had ILI rates above the epidemic thresh- Additionally, sentinel severe acute respiratory infec- old for the pre-season [2]. Of the 13 countries report- tion (SARI) surveillance is in place in 13 countries [1]. ing medium intensity, six (Finland, the Netherlands, Portugal, Slovenia, Sweden and the UK (England)) Virological situation in primary healthcare reported patterns of widespread activity with labora- The overall proportion of influenza-positive sentinel tory-confirmed influenza cases in 50% or more of their specimens increased from 4% to 39% from week 47 administrative units (or reporting sites). 2014 to week 2 2015, indicating the start of the sea- son at a similar time to the previous season (Figure 1). Influenza surveillance in Europe The season threshold of 10% was exceeded in season Since October 2014, all 53 Member States of the WHO 2011/12 and 2013/14 in week 51, in 2012/13 in week 49, European Region report their epidemiological and viro- and in the current season during week 50 (Figure 1). logical influenza surveillance data to The European Surveillance System (TESSy), hosted by the European In most countries, influenza A(H3N2) virus was the Centre for Disease Prevention and Control (ECDC) [1]. dominant subtype in both sentinel and non-sentinel The data are jointly published with the WHO European specimens in week 2 2015. In the sentinel systems, Regional Office to describe the annual occurrence of since week 40, 1,134 (10%) of the 11,854 specimens

www.eurosurveillance.org 1 Figure 1 Number of influenza virus-positive sentinel specimens by (sub)type and week, and proportion of positive specimens compared to three previous seasons, World Health Organization European Region, weeks 40 2014–2 2015 for season 2014/15

500 Influenza B, 2014/15 70 Influenza A(H3N2), 2014/15 Influenza A(H1N1)pdm09, 2014/15 450 Influenza A not subtyped, 2014/15 Positive specimens (%), 2014/15 60 Positive specimens (%), 2011/12 400

s Positive specimens (%), 2012/13 P

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0 0 40 41 42 43 44 45 46 47 48 49 50 51 52 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

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collected in 35 countries tested positive for influenza, containing antigenic drift variants compared with A/ 901 (79%) for type A influenza virus and 233 (21%) for Texas/50/2012, the vaccine component for the north- type B (Figure 1). Of the 831 type A viruses subtyped, ern hemisphere 2014/15 season [6]. 688 (83%) were A(H3N2) and 143 (17%) were A(H1N1) pdm09 by week 2 2015 (Figure 1). The lineage of 87 For 63 viruses, , Spain and Sweden reported type B viruses was determined: six were B/Victoria lin- the haemagglutinin gene sequence accession num- eage and 81 B/Yamagata lineage. ber for the Global Initiative on Sharing All Influenza Data (GISAID) EpiFlu database. The maximum like- The antigenic characteristics of 117 influenza viruses lihood phylogenetic tree of these viruses together and the genetic characteristics of 202 influenza with the A(H3N2) reference viruses shows that the viruses were reported to TESSy by 16 countries mainly current circulating viruses cluster mainly with the in the western countries of the Region. Of 68 influenza genetic subgroups 3C.3, 3C.3a together with the A/ A(H3N2) viruses antigenically characterised, 40 were Switzerland/9715293/2013, and 3C.2a with the A/ reported by the national influenza centres as A(H3N2) Hong Kong/5738/2014, and show genetic drift from the A/Texas/50/2012-like (vaccine-like) and 26 were A/ current vaccine virus (Figure 2). The antigenic drift of Switzerland/9715293/2013-like (antigenically different viruses clustering with the A/Newcastle/22/2014 has from the vaccine); two viruses could not be ascribed not yet been shown. to an antigenic category. All 21 A(H1N1)pdm09 viruses characterised were A/California/7/2009-like (vaccine Ninety-three influenza A(H3N2) viruses, 20 A(H1N1) strain). Of the 30 influenza B viruses characterised, pdm09 and four influenza B viruses have been 28 were of the B/Yamagata/16/88-lineage (10 were tested phenotypically or genotypically for neuramini- reported as B/Massachusetts/02/2012-like viruses, one dase inhibitor susceptibility. None showed evidence B/Wisconsin/1/2010-like and 17 B/Phuket/3073/2013- of reduced susceptibility to either oseltamivir or like) and two were B/Brisbane/60/2008-like viruses of zanamivir. the Victoria lineage.

Of the 160 genetically characterised A(H3N2) viruses, 110 (69%) fall in two genetic subgroups

2 www.eurosurveillance.org Figure 2 Laboratory-confirmed hospitalised Maximum likelihood phylogenetic tree of haemagglutinin influenza cases nucleotide sequences (1,063 nucleotides) from influenza Current surveillance systems reporting laboratory- A(H3N2) viruses reported to the European Surveillance System and reference A(H3N2) viruses, weeks 40 2014–1 confirmed hospitalised influenza cases to TESSy, while 2015 not being representative on a population basis in all A/Norway/3104/2014 EPI553159 countries, provide information on groups being hos- 63 A/Norway/3011/2014 EPI552640 A/Norway/3030/2014 EPI552641 pitalised due to influenza as well as risk factors for A/Malmoe/5/2014 EPI552706 A/Stockholm/28/2014 EPI552698 severe disease. This season, as of week 40 2014, six A/Newcastle/22/2014 EPI539874 countries with a monitoring system for laboratory-con- A/Norway/3041/2014 EPI552644 A/Norway/3101/2014 EPI553157 firmed hospitalised influenza cases reported 719 labo- A/Norway/3051/2014 EPI552647 96 83 A/Norway/3048/2014 EPI552646 ratory-confirmed hospitalised cases. In intensive care A//13347/2014 EPI539598 units (ICU), 671 cases were reported: three in Finland, A/Norway/3002/2014 EPI552638 A/Norway/3004/2014 EPI552639 101 in France, 20 in Spain, five in Sweden and 542 in A/LaRioja/2053/2014 EPI552658 89 65 the UK. In comparison, for season 2013/14, by week 2 A/LaRioja/2052/2014 EPI552657 71 A/LaRioja/2051/2014 EPI552656 2014, France had reported 77, Ireland two, Spain 227 A/LaRioja/2050/2014 EPI552655 A/Aragon/2062/2014 EPI553188 and Sweden 11 ICU cases. The UK had not reported a 68 A/Aragon/2031/2014 EPI552654 3C.3 single severe case by week 2 2014 and the surveillance A/Iceland/08202/2014 EPI536340 A/Galicia/1786/2014 EPI539568 system there has not changed. A/South Africa/4655/2013 EPI466802 A/Samara/73/2013 EPI460558 A/PaisVasco/1979/2014 EPI552653 62 Of the 719 laboratory-confirmed hospitalised influenza A/Galicia/2085/2014 EPI553191 99 A/Galicia/2084/2014 EPI553187 cases, 682 (95%) were positive for influenza A virus 93 A/Galicia/2055/2014 EPI552660 A/Galicia/2054/2014 EPI552659 (197 subtyped: 149 A(H3N2) and 48 A(H1N1)pdm09) and 63 A/Dakar/13/2014 EPI539794 37 (5%) for influenza B virus, which reflects the over- A/Extremadura/2061/2014 EPI553190 A/Ghana/DILI-0428/2014 EPI541428 all predominance of A(H3N2) and co-circulation of the A/Gothenburg/4/2014 EPI552674 98 A(H1N1)pdm09 and B viruses. 91 A/Stockholm/26/2014 EPI552425 3C.3a A/Switzerland/9715293/2013 EPI530687 79 A/Malmoe/4/2014 EPI548118 A/Sweden/76/2014 EPI552682 Of the 671 cases admitted to ICU, 642 (96%) were posi- A/South Australia/55/2014 EPI541463 A/Norway/1903/2014 EPI539623 tive for influenza A virus (170 subtyped: 126 A(H3N2) A/Hong Kong/146/2013 EPI426061 and 44 A(H1N1)pdm09) and 29 (4%) for influenza B A/Nebraska/4/2014 EPI539619 A/Norway/3067/2014 EPI553153 virus. Half of the cases admitted to ICU for which infor- A/Stockholm/21/2014 EPI544663 mation on age was available (61/128) were aged 65 A/Hong Kong/5738/2014 EPI539806 A/Norway/3086/2014 EPI553156 85 years or older. The median age at admission to ICU was A/Norway/3031/2014 EPI552642 87 A/Norway/3109/2014 EPI553161 64 years (mean 61.6 years, range 1–93 years). In the 72 94 A/Norway/3046/2014 EPI552645 2013/14 influenza season (up to week 2 2014 and dur- A/Sweden/75/2014 EPI552722 A/Norway/3103/2014 EPI553158 ing the whole season), the majority of ICU cases had A/Asturias/1951/2014 EPI552652 A/Norway/3037/2014 EPI552643 been 40–64 years old, with influenza A(H1N1)pdm09 A/Norway/2431/2014 EPI552637 3C.2a 3C.2 virus as the dominating subtype [7]. 61 A/Stockholm/29/2014 EPI552690 94 A/Stockholm/25/2014 EPI548102 A/Galicia/2056/2014 EPI552661 A/Karlstad/1/2014 EPI552417 Discussion and conclusions A/Stockholm/23/2014 EPI548110 The influenza season in Europe has started and contin- A/Stockholm/22/2014 EPI548094 A/Asturias/1949/2014 EPI552651 ues to expand according to the clinical, epidemiologi- A/Texas/50/2012 EPI391247 A/Victoria/361/2011 EPI349106 cal and virological indicators. The season is dominated A/Maevatanana/974/2013 EPI466784 by influenza A(H3N2) viruses, although both A(H1N1) A/ GR/112/2012 EPI358885 84 A/Cameroon/12V-5062/2012 EPI438725 pdm09 and B viruses co-circulate. This is similar to the A/Stockholm/18/2011 EPI326139 A/Madagascar/0648/2011 EPI319276 influenza activity in the other parts of northern hemi- 69 A/Minnesota/10/2012 EPI376512 sphere, e.g. the United States (US), where the influ- A/Johannesburg/3495/2012 EPI405940 86 A/Perth/16/2009 EPI211334 enza activity has continued to increase with influenza 99 A/Norway/1186/2011 EPI326137 A(H3N2) viruses predominating [8]. A/Norway/1330/2010 EPI302231 A/Alabama/05/2010 EPI278808

99 A/Israel/20/2013 EPI426077 85 A/Iowa/19/2010 EPI335923 The last influenza seasons in Europe dominated by 85 A/Galicia/RR9911/2012 EPI426125 A(H3N2) viruses were seasons 2011/12 [9,10] and 0.005 2012/13 [3,11], when A(H1N1)pdm09 and A(H3N2)

 Northern hemisphere vaccine str ain viruses co-dominated. These seasons were estimated

 Southern hemisphere vaccine strain as moderately severe based on ILI/ARI consultation  N orway, 2014 rates, although the /European Economic  S pain, 2014  Sweden, 2014 Area (EU/EEA) still lacks agreed criteria for severity of influenza. The current season has started earlier in the US where higher influenza-related hospitalisation All sequences have been retrieved from GISAID EpiFlu database rates are being reported as compared with the past (accession numbers indicated in the tree) A(H3N2)-dominated seasons [12]. As shown for Europe, the 2014/15 season has started at a similar time and

www.eurosurveillance.org 3 : Martina Havlickova, Helena Jiřincová, Jan with similar impact in primary care as the previous sea- Kyncl son. Since A(H3N2)-dominated seasons usually cause Denmark: Lisbet Krause Knudsen, Anne Mazick, Ramona more severe outcomes among the elderly and other Trebbien, Thea Kølsen Fischer risk groups than A(H1N1)pdm09 or B seasons [13,14], Estonia: Liisa Lilje, Lesja Pokras, Natalja Kuznetsova, Olga the current influenza epidemic in Europe is expected to Sadikova Finland: Niina Ikonen, Outi Lyytikäinen, Satu Murtopuro cause an increased number of severe infections, hos- France: Vincent Enouf, Bruno Lina, Martine Valette, Sylvie pitalisations, ICU admissions and deaths in the elderly Van der Werf, Isabelle Bonmarin, Behillil Sylvie, Blanchon than the 2013/14 influenza season. This has already Thierry, Clement Turbelin, Emmanuel Belchior been observed in ICU admissions reported from the UK Georgia: Ann Machablishvili, Khatuna Zakhashvili this season in comparison with the previous season. : Silke Buda, Brunhilde Schweiger Greece: Athanassios Kossivakis, Spala Georgia, Andreas Mentis, Nikolaos Malisiovas In September 2014, the WHO consultation and infor- : Ágnes Csohán, Mónika Rózsa, Istvan Jankovics, mation meeting on the composition of influenza virus Zsuzsanna Molnár vaccines indicated an emergence of two new genetic Iceland: Arthur Löve, Guðrún Sigmundsdóttir, Thorolfur clades of A(H3N2) viruses (clades 3C.2a and 3C.3a) Gudnason Ireland: Lisa Domegan, Darina O´Flanagan, Derval Igoe, containing antigenic drift viruses of previously circulat- Allison Waters, Margaret Duffy, Suzie Coughlan, Joan ing viruses [15]. The US Centers for Disease Control and O’Donnell Prevention subsequently posted a health alert network Israel: Zalman Kaufman, Michal Mandelboim notification [16], and ECDC issued a risk assessment : Isabella Donatelli, Antonino Bella, Caterina Rizzo, [17] concerning the continued circulation and transmis- Maria Grazia Pompa, Simona Puzelli, Maria Rita Castrucci Kazakhstan: Aigul Katrenova, Gaukhar Nusupbaeva sion of these viruses. Kyrgyzstan: Kalia Kasymbekova, Dinagul Otorbaeva : Raina Nikiforova, Natalija Zamjatina Based on our analysis and the current knowledge of Liechtenstein: Sabine Erne the circulating viruses [18], the northern hemisphere Lithuania: Algirdas Griškevicius, Vilnele Lipnickiene vaccine may not offer desired protection against the : Joël Mossong, Matthias Opp Malta: Christopher Barbara, Tanya Melillo, Jackie Maistre circulating A(H3N2) viruses. However, for the A(H1N1) Melillo, Graziella Zahra pdm09 and B/Victoria lineage viruses, only limited : Bozidarka Rakocevic, Zoran Vratnica drift has been observed and protection against the Netherlands: Adam Meijer, Anne Teirlinck, Frederika Dijkstra, circulating influenza A(H1N1)pdm09 viruses is still con- Ge Donker, Guus Rimmelzwaan, Marit de Lange ferred by the vaccine. Norway: Olav Hungnes, Karoline Bragstad, Siri Helene Hauge, Ragnhild Tønnessen, Susanne Gjeruldsen Dudman : Karolina Bednarska, Lidia B. Brydak, Andrzej The vaccine effectiveness for this season for the Zielinski A(H3N2) and possibly the B component is expected to Portugal: Raquel Guiomar, Pedro Pechirra, Paula Cristovão, be reduced as already seen in the US [19] and in pre- Inês Costa, Baltazar Nunes, Ana Rodrigues. vious seasons in Europe [20,21]. However, the vaccine Republic of Moldova: Veronica Eder, Constantin Spinu : Viorel Alexandrescu, Emilia Lupulescu, Florin is anticipated to prevent some infections, improve the Popovici course or shorten the duration of influenza in infected Russian Federation: Elena Burtseva, Anna Sominina individuals, and is likely to reduce the number of severe : Dragana Dimitrijevic, Slavica Rakic Adrovic outcomes and mortality. It therefore remains the meas- : Edita Staroňová, Ján Mikas ure of choice to prevent severe illness and possibly Slovenia: Katarina Prosenc, Nataša Berginc, Maja Sočan Spain: Inmaculada Casas, Amparo Larrauri, Francisco Pozo, fatal outcomes in risk groups. The circulating viruses Raul Ortiz de Lejarazu, Tomas Pumarola are susceptible to the antiviral drugs oseltamivir and Sweden: Mia Brytting, Hélène Englund, Åsa Wiman, Nasser zanamivir and these drugs are therefore an important Nuru Mahmud adjunct in the treatment of influenza. Switzerland: Rita Born, Samuel Cordey Tajikistan: Farida Tishkova, Mirali Kamolov The Former Yugoslav Republic of Macedonia: Golubinka Bosevska, Gordana Kuzmanovska Members of the WHO European Region and European : Selmur Topal, Gülay Korukluoğlu Influenza Surveillance Network Turkmenistan: Amansoltan Ashirova, Gurbangul Ovliyakulova : Iryna Demchyshyna, Tatiana Dykhanovska, Alla Albania: Majlinda Kota, Artan Simaku Mironenko Armenia: Shushan Sarkisian, Liana Torosyan United Kingdom: Peter Coyle, Alasdair MacLean, Rory : Therese Popow-Kraupp, Pamela Rendi-Wagner, Gunson, Helen Green, Cathriona Kearns, Maria Zambon, Daniela Schmid Christopher Nugent, Catherine Moore, Nick Phin, Richard Azerbaijan: Nazakat Abdullayeva, Oleg Salimov Pebody, Simon Cottrell, Jim McMenamin, Lucy Jessop Belarus: Natalia Gribkova, Veronika Shimanovich Uzbekistan: Sultana Dzemileva, Ravshan Rakhimov : Isabelle Thomas, Anneleen Hombrouck, Nathalie WHO Collaborative Centre : John McCauley, Rod Bossuyt, Sarah Moreels, Viviane Van Casteren Daniels Bosnia and Herzegovina: Amela Dedejic Ljubovic, Nina Vukmir Rodic Bulgaria: Neli Korsun, Mira Kojouharova, Teodora Georgieva Acknowledgements : Vladimir Drazenovic : Despo Bagatzouni, Maria Koliou We acknowledge the authors, originating and submitting laboratories of the sequences from GISAID’s EpiFlu Database on which the phylogenetic analysis is based (Figure 2;

4 www.eurosurveillance.org Accession numbers shown). All submitters of data may be 9. European Centre for Disease Prevention and Control (ECDC). contacted directly via the GISAID website www.gisaid.org. Surveillance report. Influenza in Europe – Season 2011-2012. Stockholm: ECDC. October 2012. Available from: http://www. We acknowledge also the support of Dr. Heli Harvala- ecdc.europa.eu/en/publications/Publications/Influenza- Simmonds (EUPHEM fellow, Folkhälsomyndigheten, Sweden) Europe-2011-2012-surveillance-report.pdf. in the phylogenetic analysis. 10. World Health Organization (WHO) Regional Office for Europe. We thank Adrian Prodan and Gaëtan Guyodo for the support Summary of the 2011-2012 influenza season in the WHO in data management. European Region. Copenhagen: WHO. [Accessed 22 Jan 2015]. Available from: http://www.euro.who.int/en/health-topics/ We would additionally like to acknowledge all members of communicable-diseases/influenza/publications/2012/ the Spanish Influenza Surveillance System (SISS) for the summary-of-the-2011-2012-influenza-season-in-the-who- contribution in this study. Sequences from Spain were ob- european-region. tained in the Centro Nacional de Microbiología (ISCIII) from 11. World Health Organization (WHO) Regional Office for Europe. influenza viruses sent by the following laboratories: Hospital Summary of the 2012-2013 influenza season in the WHO European Region. Copenhagen: WHO. [Accessed 22 Jan 2015]. Miguel Servet de Zaragoza-Aragón, Hospital Na Sra de Available from: http://www.euro.who.int/en/health-topics/ Covadonga de Oviedo-Asturias, Hospital Son Dureta Palma communicable-diseases/influenza/publications/2013/ de Mallorca-Baleares, Hospital San Pedro de Alcántara summary-of-the-20122013-influenza-season-in-the-who- Cáceres-Extremadura, Hospital Donostia-País Vasco, european-region. Hospital San Pedro Logroño-La Rioja, Complejo Hospitalario 12. Centers for Disease Control and Prevention (CDC). CDC: Flu de Vigo-Galicia. Activity Expands; Severity Similar to Past H3N2 Seasons. Atlanta: CDC. 5 Jan 2015. Available from: http://www.cdc.gov/ flu/news/flu-activity-expands.htm. 13. Lee BE, Mukhi SN, Drews SJ. Association between patient Conflict of interest age and influenza A subtype during influenza outbreaks. Infect Control Hosp Epidemiol. 2010;31(5):535-7. http://dx.doi. None declared. org/10.1086/652159 PMID:20334548 14. Kaji M, Watanabe A, Aizawa H. 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