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Eurosurveillance, Volume 21, Issue 13, 31 March 2016
Rapid communication
Broberg, Melidou, Prosenc, Bragstad, Hungnes, and on behalf of the WHO European Region and the European Influenza Surveillance Network members of the reporting countries: Predominance of influenza A(H1N1)pdm09 virus genetic subclade 6B.1 and influenza B/Victoria lineage viruses at the start of the 2015/16 influenza season in Europe

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Citation style for this article: Broberg E, Melidou A, Prosenc K, Bragstad K, Hungnes O, on behalf of the WHO European Region and the European Influenza Surveillance Network members of the reporting countries. Predominance of influenza A(H1N1)pdm09 virus genetic subclade 6B.1 and influenza B/Victoria lineage viruses at the start of the 2015/16 influenza season in Europe. Euro Surveill. 2016;21(13):pii=30184. DOI: http://dx.doi.org/10.2807/1560-7917.ES.2016.21.13.30184

Received:09 March 2016; Accepted:31 March 2016


For the current northern hemisphere season, several reports have indicated intense influenza activity [1-5]. We analysed virological surveillance data from 20 European countries to study the genetic and antigenic characteristics of the circulating influenza viruses and compare them with the vaccine viruses and previously circulating strains.

Virological influenza surveillance in Europe, influenza season 2015/16

Virological influenza surveillance data in the World Health Organization (WHO) European Region are collected on a weekly basis and reported to The European Surveillance System (TESSy), a database hosted by the European Centre for Disease Prevention and Control (ECDC), as previously described [6]. From week 40/2015 to week 4/2016, 49 Member States of the Region reported influenza virus detections to TESSy, including 20 Member States (Belgium, Croatia, Czech Republic, Denmark, Finland, Germany, Greece, Ireland, Latvia, Netherlands, Norway, Portugal, Romania, Russia, Slovakia, Slovenia, Spain, Sweden, Switzerland, and the United Kingdom (UK)) that also reported antigenic or genetic characterisation data.

The antigenic and genetic reporting categories for TESSy are predefined by the WHO Collaborating Centre for Reference and Research on Influenza, London, for each influenza season. For antigenic characterisation, to denote a virus isolate as being like a vaccine or reference virus its haemagglutination inhibition (HI) titre with post-infection ferret antiserum raised against the reference virus should differ by no more than fourfold. For genetic characterisation, the allocation to reporting category is based on the phylogenetic and amino acid sequence analyses of haemagglutinin (HA) gene.

The summary analysis of the data are presented weekly in the Joint ECDC–WHO Regional Office for Europe weekly ‘Flu News Europe’ (http://flunewseurope.org/). Data on detections, antigenic and genetic characterisations were extracted on 8 February 2016 for analysis.

Between week 40/2015 and week 4/2016, influenza viruses were detected in 1,879 (19%) of 9,882 sentinel specimens tested in the 20 countries also reporting on virus characterisation. Of these 1,879 specimens, 1,512 (80%) were positive for type A influenza virus and 367 (20%) for type B. Of 1,441 subtyped influenza A viruses, 1,268 (88%) were A(H1N1)pdm09. Of 129 type B viruses with known lineage, 115 (89%) were of the B/Victoria/2/1987 lineage.

Virus characterisation

Between weeks 40/2015 and 4/2016, 447 (24%) of 1,879 influenza viruses were attributed to a genetic group by 16 countries (Belgium, Czech Republic, Denmark, Finland, Germany, Greece, Ireland, Netherlands, Norway, Portugal, Romania, Russia, Slovenia, Spain, Sweden and UK), and 429 (23%) were attributed to an antigenic category by also 16 reporting countries (Croatia, Czech Republic, Denmark, Finland, Germany, Greece, Latvia, Netherlands, Portugal, Romania, Russia, Slovakia, Slovenia, Spain, Switzerland and UK) (Table 1).

Table 1

Viruses attributed to genetic and antigenic groupsa, weeks 40/2015–04/2016

Genetic group Number of viruses Antigenic group Number of viruses
A(H1N1)pdm09 A/South Africa/3626/2013 (subgroup 6B)b 313 A(H1N1)pdm09 A/California/7/2009-like 379
A(H3N2) A/Hong Kong/4801/2014 (subgroup 3C.2a)b 50 A(H3N2) A/Hong Kong/4801/2014-like 6
A(H3N2) A/Samara/73/2013 (subgroup 3C.3)c 1 No separate antigenic category; expected to resemble A/Stockholm/28/2014
A(H3N2) A/Stockholm/28/2014 (subgroup 3C.3b)c 0 A(H3N2) A/ Stockholm/28/2014-like 0
A(H3N2) A/Switzerland/9715293/2013 (subgroup 3C.3a)b 26 A(H3N2) A/Switzerland/9715293/2013 14
B/Phuket/3073/2013 (Yamagata lineage clade 3)b 13 B/Phuket/3073/2013 (Yamagata lineage) -like 1
B/Brisbane/60/2008 (Victoria lineage clade 1A)d 44 B/Brisbane/60/2008 (Victoria lineage) -like 29

The viruses which were genetically characterised are not necessarily the same than the viruses that were antigenically characterised.

a Genetic and antigenic groups used for reporting into The European Surveillance System are defined by World Health Organization Collaborating Centre for Reference and Research on Influenza for each influenza season. For antigenic characterisation, to denote a virus isolate as being like a vaccine or reference virus its haemagglutination inhibition (HI) titre with post-infection ferret antiserum raised against the reference virus should differ by no more than fourfold. For genetic characterisation, the allocation to reporting category is based on the phylogenetic and amino acid sequence analyses of haemagglutinin (HA) gene.

b These genetic groups contain viruses with antigenic properties similar to the viruses included in the trivalent influenza vaccine for 2015/16.

c These genetic groups contain viruses with antigenic properties dissimilar to the viruses included in the trivalent influenza vaccine for 2015/16.

d Viruses in this genetic group have antigenic properties similar to those of the vaccine component (B/Brisbane/60/2008) recommended for use in quadrivalent influenza vaccines for 2015/16.

The majority (68%) of all genetic characterisations were reported from Norway (n=84), Spain (n=66), Germany (n=54), Russia (n=54) and Sweden (n=46). The majority (70%) of antigenic reports were from Russia (n=124), Portugal (n=99) and Germany (n=78). For 150 viruses, reported in strain-based manner, both genetic and antigenic data were available.

All 313 A(H1N1)pdm09 viruses characterised genetically fell in clade 6, subgroup 6B, represented by A/South Africa/3626/2013. Viruses falling in this genetic subgroup, were all attributed to an antigenic category A/California/7/2009 that corresponds to the component included in the 2015/16 northern hemisphere vaccines.

Of the 77 A(H3N2) viruses attributed to a genetic group, 50 (65%) fell into genetic subgroup 3C.2a (represented by A/Hong Kong/4801/2014) that has been shown to be antigenically similar to A/Hong Kong/4801/2014 and also to the current A(H3N2) vaccine virus A/Switzerland/9715293/2013 (Table 1). Twenty-six A(H3N2) viruses fell into the vaccine virus category of 3C.3a subgroup. Viruses in subgroup 3C.3b (represented by A/Stockholm/28/2014) constituted a substantial part (98/401) of the A(H3N2) viruses in Europe in the 2014/15 season [7], but none were yet reported by week 4/2016 (Table 1). Of 20 A(H3N2) viruses attributed to an antigenic category, 14 were A/Switzerland/9715293/2013-like and thus similar to the northern hemisphere 2015/16 vaccine component and six were A/Hong Kong/4801/2014-like, similar to the southern hemisphere 2016 vaccine component and recommendation for northern hemisphere 2016/17 season.

All of the 44 B/Victoria lineage viruses characterised genetically to date fell in the clade 1A, represented by B/Brisbane/60/2008 which is included in quadrivalent vaccines for northern hemisphere 2015/16. The 13 B/Yamagata lineage viruses all genetically resembled B/Phuket/3073/2013 recommended for inclusion in trivalent vaccines for northern hemisphere 2015/16. Thirty influenza B viruses were antigenically characterised, 29 as B/Brisbane/60/2008-like and one as B/Phuket/3073/2013-like.

Analysis of A(H1N1)pdm09 HA gene sequences from 12 countries (Czech Republic, Finland, Greece, Ireland, Netherlands, Norway, Portugal, Romania, Russia, Slovenia, Spain and Sweden) reported to TESSy, with provision of accession numbers in publicly accessible databases, confirmed that all these analysed viruses possessed the signature amino acid variations that define subgroup 6B viruses: D97N, K163Q, S185T, K283E and A256T [7-9]. All 215 analysed sequences, apart from two viruses isolated in Russia, also carried P83S and I321V substitutions in HA1.

The majority of sequences (173 of 215 TESSy-reported viruses) also possessed the amino acid signature of subclade 6B.1 and formed a separate branch in the phylogenetic analysis (Figure 1, Figure 2). The 6B.1 subclade is characterised by the amino acid substitutions S84N (present in a wider subgroup), S162N and I216T [8]. Six viruses carried amino acid substitutions V152T, V173I, D501E (the latter in HA2) characterising 6B.2 subclade. In addition the five most recently sampled of these six 6B.2 viruses all possessed the R113K, D127E and E374Q substitutions (Figure 1).

Figure 1

Phylogenetic analysis of A(H1N1)pdm09 haemagglutinin (HA) nt sequences reported from European countries, between week 40/2015 and 4/2016

/images/dynamic/articles/21431/16-00195-f1

Some sequences obtained in this study were not used to construct the phylogenetic tree because they were identical and redundant. The sequences used for the phylogenetic analysis were moreover only those of suitable length, and encode HA1 amino acids 3–327. These included sequences reported by the Czech Republic, Finland, Greece, Netherlands, Norway, Portugal, Romania, Russia, Slovenia, Spain and Sweden as well as sequences from reference A(H1N1)pdm09 viruses. The tree was constructed with the neighbour-joining method, using Kimura-2 parameter-corrected distances and bootstrapped with 1,000 replicates, Molecular Evolutionary Genetics Analysis (MEGA) software version 5.0.

Figure 2

Protein structure model (FluSurver-JSmol) of the haemagglutinin protein monomer of A(H1N1)pdm09 subclade 6B.1, represented by A/Norway/2650/2015 (left), and subclade 6B.2, represented by A/Norway/2658/2015 (right)

/images/dynamic/articles/21431/16-00195-f2

Amino acid differences compared with A/California/07/2009 are indicated in colour. Well-known differences are marked in blue. Common variant marker positions are indicated in green. Amino acid involved in virulence or antigenic drift is marked in orange. Amino acid not previously associated with a specific feature is marked in grey. Amino acid that creates a new potential N-glycosylation site is marked in magenta.

The highest number of accumulated variations in the known antigenic sites were observed in the antigenic site Ca. All subgroup 6B viruses possessed the K163Q substitution, while the vast majority (173/215; 80%) also possessed the S162N substitution in HA1, resulting in a gain of a potential glycosylation site. Additional variations observed were S162K, D168N, K170E, R205K, A215G, E235D and a partial A139D. Cb antigenic site variation A73S was observed in four viruses from Spain, one of which also possessed substitution N156K in Sa antigenic site. Another Norwegian virus had a N156S substitution in Sa antigenic site. Notably, all 6B.2 viruses and also two of the 6B viruses not belonging to any of the newly identified subgroups possessed substitutions affecting the loop that consists of amino acid positions 151 to 159 located adjacent to the receptor binding site.

When comparing the A(H1N1)pdm09 strains with the corresponding strain in the current northern hemisphere influenza vaccine, A/California/7/2009, the HA1 sequences (nt 1–981, amino acids 1–327) exhibited nt similarity of 96.8 to 98.0% and deduced amino acid similarity of 95.4 to 96.3%. Viruses within subclade 6B.1 exhibited higher HA nt heterogeneity, with similarities ranging between 98.8 and 100%, while within subclade 6B.2 strains exhibited higher nt similarity, ranging between 99.3 and 100%, as the group consists of fewer sequences and most of them from one region only. The viruses analysed phylogenetically are listed in Table 2.

Table 2

Details of the A(H1N1)pdm09 sequences retrieved from the Global Initiative on Sharing All Influenza Data (GISAID)’s EpiFlu Database or GenBank, for haemagglutinin-gene-based phylogenetic analysis in this study

ID Country Strain name Collection date Originating laboratory Submitting laboratory
EPI685415 Netherlands A/Netherlands/2916/2015 6/11/2015 National Institute for Public Health and the Environment (RIVM) National Institute for Public Health and the Environment (RIVM)
EPI674853 Sweden A/Stockholm/46/2015 9/10/2015 Swedish Institute for Infectious Disease Control
EPI674745 Sweden A/Stockholm/47/2015 22/10/2015 Swedish Institute for Infectious Disease Control
EPI674753 Sweden A/Stockholm/48/2015 24/10/2015 Swedish Institute for Infectious Disease Control
EPI674841 Sweden A/Karlstad/4/2015 25/10/2015 Swedish Institute for Infectious Disease Control
EPI674777 Sweden A/Stockholm/49/2015 7/11/2015 Swedish Institute for Infectious Disease Control
EPI686820 Sweden A/Skovde/6/2015 18/11/2015 Swedish Institute for Infectious Disease Control
EPI686772 Sweden A/Stockholm/ 57/2015 18/11/2015 Swedish Institute for Infectious Disease Control
EPI674785 Sweden A/Stockholm/50/2015 11/11/2015 Swedish Institute for Infectious Disease Control
EPI674793 Sweden A/Stockholm/51/2015 11/11/2015 Swedish Institute for Infectious Disease Control
EPI674801 Sweden A/Stockholm/52/2015 11/11/2015 Swedish Institute for Infectious Disease Control
EPI674847 Sweden A/Stockholm/53/2015 12/11/2015 Swedish Institute for Infectious Disease Control
EPI674809 Sweden A/Stockholm/55/2015 10/11/2015 Swedish Institute for Infectious Disease Control
EPI686764 Sweden A/Stockholm/56/2015 18/11/2015 Swedish Institute for Infectious Disease Control
EPI686799 Sweden A/Stockholm/59/2015 19/11/2015 Swedish Institute for Infectious Disease Control
EPI686828 Sweden A/Stockholm/60/2015 25/11/2015 Swedish Institute for Infectious Disease Control
EPI686844 Sweden A/Stockholm/62/2015 26/11/2015 Swedish Institute for Infectious Disease Control
EPI687173 Sweden A/Stockholm/66/2015 23/11/2015 Swedish Institute for Infectious Disease Control
EPI687199 Sweden A/Stockholm/67/2015 21/11/2015 Swedish Institute for Infectious Disease Control
EPI674825 Sweden A/Sweden/35/2015 12/11/2015 Swedish Institute for Infectious Disease Control
EPI686852 Sweden A/Uppsala/8/2015 27/11/2015 Swedish Institute for Infectious Disease Control
EPI686892 Sweden A/Sweden/37/2015 26/11/2015 Swedish Institute for Infectious Disease Control
EPI686900 Sweden A/Sweden/38/2015 2/12/2015 Swedish Institute for Infectious Disease Control
EPI686908 Sweden A/Sweden/39/2015 2/12/2015 Swedish Institute for Infectious Disease Control
EPI694343 Sweden A/Uppsala/1/2016 11/1/2016 Swedish Institute for Infectious Disease Control
EPI671518 Norway A/Norway/2625/2015 21/10/2015 Sorlandet Sykehus HF, Dept. of Medical Microbiology Norwegian Institute of Public Health
EPI675750 Norway A/Norway/2659/2015 3/11/2015 Drammen Hospital / Vestreviken HF, Department for Medical Microbiology section Drammen Norwegian Institute of Public Health
EPI675751 Norway A/Norway/2660/2015 3/11/2015 Drammen Hospital / Vestreviken HF, Department for Medical Microbiology section Drammen Norwegian Institute of Public Health
EPI675754 Norway A/Norway/2672/2015 1/11/2015 Oslo University Hospital, Ulleval Hospital, Dept. of Microbiology Norwegian Institute of Public Health
EPI675756 Norway A/Norway/2680/2015 12/11/2015 Ostfold Hospital - Fredrikstad, Dept. of Microbiology Norwegian Institute of Public Health
EPI675760 Norway A/Norway/2687/2015 13/11/2015 Norwegian Institute of Public Health
EPI695284 Norway A/Norway/2711/2015 18/11/2015 Norwegian Institute of Public Health
EPI695299 Norway A/Norway/2914/2015 14/12/2015 Sorlandet Sykehus HF, Dept. of Medical Microbiology Norwegian Institute of Public Health
EPI695310 Norway A/Norway/3004/2015 15/12/2015 Innlandet Hospital Trust, Division Lillehammer, Department for Microbiology Norwegian Institute of Public Health
EPI695311 Norway A/Norway/3018/2015 26/12/2015 Norwegian Institute of Public Health
EPI695313 Norway A/Norway/3038/2015 26/12/2015 Aalesund sjukehus Norwegian Institute of Public Health
EPI695343 Norway A/Norway/174/2016 7/1/2016 St. Olavs Hospital HF, Dept. of Medical Microbiology Norwegian Institute of Public Health
EPI695344 Norway A/Norway/178/2016 6/1/2016 Health Forde, Department of Microbiology Norwegian Institute of Public Health
EPI695349 Norway A/Norway/209/2016 8/1/2016 Stavanger Universitetssykehus, Avd. for Medisinsk Mikrobiologi Norwegian Institute of Public Health
EPI677648 Finland A/Finland/541/2015 9/11/2015 Helsinki University Central Hospital, Laboratory Services (HUSLAB) National Institute for Health and Welfare
EPI677651 Finland A/Finland/543/2015 19/11/2015 Helsinki University Central Hospital, Laboratory Services (HUSLAB) National Institute for Health and Welfare
EPI678232 Finland A/Finland/544/2015 13/11/2015 Helsinki University Central Hospital, Laboratory Services (HUSLAB) National Institute for Health and Welfare
EPI696158 Russia A/Tomsk/154/2015 19/11/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696470 Russia A/IIV-Moscow/211/2015 23/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696478 Russia A/IIV-Moscow/212/2015 23/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI690291 Spain A/Aragon/16005/2015 21/12/2015 Servicio de Microbiología Hospital Miguel Servet Instituto de Salud Carlos III
EPI671520 Norway A/Norway/2631/2015 26/10/2015 Sorlandet Sykehus HF, Dept. of Medical Microbiology Norwegian Institute of Public Health
EPI671521 Norway A/Norway/2633/2015 27/10/2015 Haukeland University Hospital, Dept. of Microbiology Norwegian Institute of Public Health
EPI671522 Norway A/Norway/2634/2015 27/10/2015 Haukeland University Hospital, Dept. of Microbiology Norwegian Institute of Public Health
EPI671525 Norway A/Norway/2650/2015 3/11/2015 Ostfold Hospital - Fredrikstad, Dept. of Microbiology Norwegian Institute of Public Health
EPI675748 Norway A/Norway/2651/2015 2/11/2015 Mikrobiologisk laboratorium, Sykehuset i Vestfold Norwegian Institute of Public Health
EPI675749 Norway A/Norway/2658/2015 4/11/2015 Drammen Hospital / Vestreviken HF, Department for Medical Microbiology section Drammen Norwegian Institute of Public Health
EPI695334 Norway A/Norway/139/2016 4/1/2016 Haukeland University Hospital, Dept. of Microbiology Norwegian Institute of Public Health
EPI695336 Norway A/Norway/141/2016 4/1/2016 Unilabs Telelab, Laboratory for Medical Microbiology Norwegian Institute of Public Health
EPI695339 Norway A/Norway/150/2016 12/1/2016 Stavanger Universitetssykehus, Avd. for Medisinsk Mikrobiologi Norwegian Institute of Public Health
EPI695340 Norway A/Norway/151/2016 12/1/2016 Stavanger Universitetssykehus, Avd. for Medisinsk Mikrobiologi Norwegian Institute of Public Health
EPI695287 Norway A/Norway/2734/2015 13/11/2015 Innlandet Hospital Trust, Division Lillehammer, Department for Microbiology Norwegian Institute of Public Health
EPI695304 Norway A/Norway/2945/2015 16/12/2015 Norwegian Institute of Public Health
EPI695314 Norway A/Norway/3039/2015 28/12/2015 Aalesund sjukehus Norwegian Institute of Public Health
EPI695326 Norway A/Norway/3114/2015 28/12/2015 Drammen Hospital / Vestreviken HF, Department for Medical Microbiology section Drammen Norwegian Institute of Public Health
EPI678234 Finland A/Finland/545/2015 19/11/2015 Helsinki University Central Hospital, Laboratory Services (HUSLAB) National Institute for Health and Welfare
EPI678238 Finland A/Finland/550/2015 4/12/2015 National Institute for Health and Welfare National Institute for Health and Welfare
EPI678240 Finland A/Finland/553/2015 6/12/2015 NordLab Oulu National Institute for Health and Welfare
EPI693689 Finland A/Finland/556/2015 16/12/2015 National Institute for Health and Welfare National Institute for Health and Welfare
EPI687734 Finland A/Finland/557/2015 15/12/2015 National Institute for Health and Welfare National Institute for Health and Welfare
EPI693690 Finland A/Finland/558/2015 19/12/2015 National Institute for Health and Welfare National Institute for Health and Welfare
EPI693691 Finland A/Finland/559/2015 14/12/2015 National Institute for Health and Welfare National Institute for Health and Welfare
EPI693692 Finland A/Finland/560/2015 18/12/2015 National Institute for Health and Welfare National Institute for Health and Welfare
EPI674284 Portugal A/Lisboa/31/2015 19/11/2015 Instituto Nacional de Saude INSA National Institute of Health Portugal
EPI674285 Portugal A/Lisboa/32/2015 18/11/2015 Instituto Nacional de Saude INSA National Institute of Health Portugal
EPI678690 Portugal A/Lisboa/33/2015 25/11/2015 Instituto Nacional de Saude INSA National Institute of Health Portugal
EPI678691 Portugal A/Lisboa/36/2015 2/12/2015 Instituto Nacional de Saude INSA National Institute of Health Portugal
EPI692997 Portugal A/Lisboa/53/2015 22/12/2015 Instituto Nacional de Saude INSA National Institute of Health Portugal
EPI678693 Portugal A/Lisboa/niSU82_15–16/2015 2/12/2015 Instituto Nacional de Saude INSA National Institute of Health Portugal
EPI699780 Greece A/Athens.GR/18/2016 4/1/2016 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI699778 Greece A/Athens.GR/19/2016 4/1/2016 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI699774 Greece A/Athens.GR/29/2016 7/1/2016 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI699772 Greece A/Athens.GR/38/2016 7/1/2016 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI699770 Greece A/Athens.GR/40/2016 7/1/2016 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI699766 Greece A/Athens.GR/54/2016 8/1/2016 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI699764 Greece A/Athens.GR/55/2016 8/1/2016 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI670326 Romania A/Iasi/187166/2015 13/10/2015 Cantacuzino Institute Cantacuzino Institute
EPI690111 Romania A/Bucuresti/649-c7807/2015 22/12/2015 Cantacuzino Institute Cantacuzino Institute
EPI699023 Romania A/Bucuresti/190460/2016 19/1/2016 Cantacuzino Institute Cantacuzino Institute
EPI696174 Russia A/IIV-Moscow/158/2015 12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696182 Russia A/IIV-Moscow/159/2015 12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696198 Russia A/IIV-Moscow/161/2015 14/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696246 Russia A/IIV-Moscow/169/2015 17/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696270 Russia A/IIV-Moscow/174/2015 16/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696278 Russia A/IIV-Moscow/176/2015 15/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696286 Russia A/IIV-Moscow/177/2015 16/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696326 Russia A/IIV-Moscow/183/2015 21/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696382 Russia A/IIV-Moscow/191/2015 20/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696414 Russia A/IIV-Moscow/195/2015 22/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI687093 Russia A/Saint-Petersburg/RII349/2015 25/11/2015 WHO National Influenza Centre Russian Federation
EPI696574 Russia A/Saint-Petersburg/RII350/2015 30/11/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696486 Russia A/Saint-Petersburg/RII01/2016 19/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696494 Russia A/Saint-Petersburg/RII02/2016 21/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696502 Russia A/Saint-Petersburg/RII03/2016 21/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696510 Russia A/Saint-Petersburg/RII04/2016 21/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696166 Russia A/IIV-Moscow/155/2015 7/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696518 Russia A/Saint-Petersburg/RII05/2016 14/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696526 Russia A/Saint-Petersburg/RII06/2016 14/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696534 Russia A/Saint-Petersburg/RII07/2016 21/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696542 Russia A/Saint-Petersburg/RII08/2016 22/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696558 Russia A/Saint-Petersburg/RII10/2016 23/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696566 Russia A/Saint-Petersburg/RII11/2016 24/12/2015 WHO National Influenza Centre Russian Federation WHO National Influenza Centre Russian Federation
EPI696222 Russia A/IIV-Moscow/166/2015 16/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696238 Russia A/IIV-Moscow/168/2015 15/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696254 Russia A/IIV-Moscow/171/2015 17/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696294 Russia A/IIV-Moscow/178/2015 17/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696318 Russia A/IIV-Moscow/182/2015 18/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696334 Russia A/IIV-Moscow/185/2015 18/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696366 Russia A/IIV-Moscow/189/2015 19/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696374 Russia A/IIV-Moscow/190/2015 20/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696398 Russia A/IIV-Moscow/193/2015 21/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696406 Russia A/IIV-Moscow/194/2015 20/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696422 Russia A/IIV-Moscow/196/2015 22/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696430 Russia A/IIV-Moscow/199/2015 22/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696446 Russia A/IIV-Moscow/203/2015 22/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696454 Russia A/IIV-Moscow/204/2015 22/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI696462 Russia A/IIV-Moscow/208/2015 23/12/2015 D.I. Ivanovsky Research Institute of virology MoPH of RF,Moscow WHO National Influenza Centre Russian Federation
EPI686526 Spain A/Madrid/1858/2015 22/12/2015 Servicio de Microbiología Hospital Ramón y Cajal Instituto de Salud Carlos III
EPI690296 Spain A/Madrid/1859/2015 23/12/2015 Servicio de Microbiología Hospital Ramón y Cajal Instituto de Salud Carlos III
EPI672780 Spain A/Madrid/SO13656/2015 21/10/2015 Instituto de Salud Carlos III Instituto de Salud Carlos III
EPI674599 Spain A/Madrid/SO13670/2015 20/10/2015 Instituto de Salud Carlos III Instituto de Salud Carlos III
EPI680490 Spain A/Madrid/SO13763/2015 8/12/2015 Instituto de Salud Carlos III Instituto de Salud Carlos III
EPI699957 Spain A/Madrid/41/2016 13/1/2016 Instituto de Salud Carlos III Instituto de Salud Carlos III
EPI699959 Spain A/Madrid/68/2016 12/1/2016 Servicio de Microbiología Hospital Ramón y Cajal Instituto de Salud Carlos III
EPI699960 Spain A/Madrid/69/2016 12/1/2016 Servicio de Microbiología Hospital Ramón y Cajal Instituto de Salud Carlos III
EPI690298 Spain A/Navarra/16004/2015 27/12/2015 Servicio de Microbiología Complejo Hospitalario de Navarra Instituto de Salud Carlos III
EPI686527 Spain A/Navarra/1829/2015 15/12/2015 Servicio de Microbiología Complejo Hospitalario de Navarra Instituto de Salud Carlos III
EPI686528 Spain A/Navarra/1850/2015 17/12/2015 Servicio de Microbiología Complejo Hospitalario de Navarra Instituto de Salud Carlos III
EPI690302 Spain A/Navarra/26/2016 3/1/2016 Servicio de Microbiología Complejo Hospitalario de Navarra Instituto de Salud Carlos III
EPI699967 Spain A/Navarra/50/2016 11/1/2016 Servicio de Microbiología Complejo Hospitalario de Navarra Instituto de Salud Carlos III
EPI699973 Spain A/Navarra/74/2016 14/1/2016 Servicio de Microbiología Complejo Hospitalario de Navarra Instituto de Salud Carlos III
EPI699974 Spain A/Navarra/75/2016 12/1/2016 Servicio de Microbiología Complejo Hospitalario de Navarra Instituto de Salud Carlos III
EPI699975 Spain A/Navarra/76/2016 14/1/2016 Servicio de Microbiología Complejo Hospitalario de Navarra Instituto de Salud Carlos III
EPI699977 Spain A/Navarra/78/2016 14/1/2016 Servicio de Microbiología Complejo Hospitalario de Navarra Instituto de Salud Carlos III
EPI672781 Spain A/PaisVasco/1683/2015 21/10/2015 Servicio de Microbiología Hospital Donostia Instituto de Salud Carlos III
EPI686529 Spain A/PaisVasco/1844/2015 15/12/2015 Servicio de Microbiología Hospital Donostia Instituto de Salud Carlos III
EPI687827 Slovenia A/Slovenia/2903/2015 26/10/2015 Laboratory for Virology, National Institute of Public Health Crick Worldwide Influenza Centre
KU558983 Czech Republic A/Czech Republic/95/2015 1/12/2015 National Institute of Public Health National Institute of Public Health
EPI699832 Greece A/Athens.GR/2395/2015 23/12/2015 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI699830 Greece A/Athens.GR/2407/2015 28/12/2015 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI699827 Greece A/Athens.GR/2413/2015 29/12/2015 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI699824 Greece A/Athens.GR/12/2016 5/1/2016 Hellenic Pasteur Institute Hellenic Pasteur Institute
EPI698911 Romania A/Dambovita/190170/2016 18/1/2016 Cantacuzino Institute Cantacuzino Institute
EPI698910 Romania A/Galati/190006/2016 8/1/2016 Cantacuzino Institute Cantacuzino Institute
EPI699021 Romania A/Vrancea/190182/2016 18/1/2016 Cantacuzino Institute Cantacuzino Institute
EPI699023 Romania A/Bucuresti/190324/2016 19/1/2016 Cantacuzino Institute Cantacuzino Institute
EPI699059 Romania A/Bucuresti/190434/2016 23/1/2016 Cantacuzino Institute Cantacuzino Institute
EPI698912 Romania A/Dambovita/190171/2016 18/1/2016 Cantacuzino Institute Cantacuzino Institute
EPI699024 Romania A/Dambovita/190341/2016 21/1/2016 Cantacuzino Institute Cantacuzino Institute
EPI699000 Romania A/Vrancea/190181/2016 11/1/2016 Cantacuzino Institute Cantacuzino Institute
EPI672779 Spain A/Aragon/1615/2015 29/9/2015 Servicio de Microbiología Hospital Miguel Servet Instituto de Salud Carlos III
EPI690293 Spain A/Asturias/1862/2015 17/12/2015 Servicio de Microbiología Hospital Central Universitario de Asturias Instituto de Salud Carlos III
EPI699955 Spain A/Baleares/16036/2015 30/12/2015 Servicio de Microbiología Hospital Universitario Son Espases Instituto de Salud Carlos III
EPI699956 Spain A/Baleares/35/2016 5/1/2016 Servicio de Microbiología Hospital Universitario Son Espases Instituto de Salud Carlos III
EPI690295 Spain A/CastillaLaMancha/16013/2015 30/12/2015 Instituto de Salud Carlos III Instituto de Salud Carlos III
EPI624748 Russia A/St-Petersburg/122/2015 26/2/2015 WHO National Influenza Centre Russian Federation Crick Worldwide Influenza Centre
EPI624673 Cameroon A/Cameroon/15V-3814/2015 7/5/2015 Centre Pasteur du Cameroun Crick Worldwide Influenza Centre
EPI624730 Norway A/Norway/1690/2015 17/3/2015 WHO National Influenza Centre Crick Worldwide Influenza Centre
EPI630638 Mauritius A/Mauritius/I-463/2015 18/5/2015 Central Health Laboratory Crick Worldwide Influenza Centre
EPI621835 Madagascar A/Madagascar/1566/2015 15/4/2015 Institut Pasteur de Madagascar Crick Worldwide Influenza Centre
EPI630634 Hong Kong SAR A/Hong Kong/12243/2015 14/6/2015 Government Virus Unit Crick Worldwide Influenza Centre
EPI630684 South Africa A/South Africa/R3723/2015 29/6/2015 Sandringham, National Institute for Communicable D Crick Worldwide Influenza Centre
EPI630676 South Africa A/South Africa/R2977/2015 5/6/2015 Sandringham, National Institute for Communicable D Crick Worldwide Influenza Centre
EPI630652 Slovenia A/Slovenia/1314/15 5/3/2015 Laboratory for Virology, National Institute of Public Health Crick Worldwide Influenza Centre
EPI624706 Russia A/IIV-Moscow/94/2015 12/3/2015 Ivanovsky Research Institute of Virology RAMS Crick Worldwide Influenza Centre
EPI624704 Russia A/IIV-Moscow/93/2015 10/3/2015 Ivanovsky Research Institute of Virology RAMS Crick Worldwide Influenza Centre
EPI589565 Jordan A/Jordan/20241/2015 22/3/2015 Laboratory Directorate Crick Worldwide Influenza Centre
EPI253705 Germany A/Bayern/69/2009 1/1/2009 Robert-Koch-Institute Robert-Koch-Institute
EPI278607 New Zealand A/Christchurch/16/2010 12/7/2010 Canterbury Health Services WHO Collaborating Centre for Reference and Research on Influenza
EPI319590 Russia A/Astrakhan/1/2011 28/2/2011 WHO National Influenza Centre Russian Federation National Institute for Medical Research
EPI319527 Russia A/St. Petersburg/27/2011 14/2/2011 WHO National Influenza Centre Russian Federation National Institute for Medical Research
EPI416411 Norway A/Norway/120/2013 2/1/2013 WHO National Influenza Centre National Institute for Medical Research
EPI574439 Ghana A/Ghana/DILI-14–0620/2014 7/7/2014 University of Ghana National Institute for Medical Research
EPI390473 Hong Kong SAR A/Hong Kong/5659/2012 21/5/2012 Government Virus Unit National Institute for Medical Research
EPI326206 Hong Kong SAR A/Hong Kong/3934/2011 29/3/2011 Government Virus Unit National Institute for Medical Research
EPI466626 South Africa A/South Africa/3626/2013 6/6/2013 Sandringham, National Institute for Communicable D National Institute for Medical Research
EPI539472 Senegal A/Dakar/04/2014 3/2/2014 Institut Pasteur de Dakar National Institute for Medical Research
EPI417122 Senegal A/Dakar/20/2012 9/12/2012 Institut Pasteur de Dakar National Institute for Medical Research
EPI319447 Czech Republic A/Czech Republic/32/2011 18/1/2011 National Institute of Public Health National Institute for Medical Research
EPI215957 Ukraine A/Lviv/N6/2009 27/10/2009 Ministry of Health of Ukraine National Institute for Medical Research
EPI320141 Russia A/St. Petersburg/100/2011 14/3/2011 Russian Academy of Medical Sciences Centers for Disease Control and Prevention
EPI626148 Bangladesh A/Bangladesh/3003/2015 4/5/2015 Institute of Epidemiology Disease Control and Research (IEDCR) and Bangladesh National Influenza Centre (NIC) Centers for Disease Control and Prevention
EPI626140 Bangladesh A/Bangladesh/01/2015 10/5/2015 Institute of Epidemiology Disease Control and Research (IEDCR) and Bangladesh National Influenza Centre (NIC) Centers for Disease Control and Prevention
EPI176620 United States A/California/07/2009 9/4/2009 Naval Health Research Center Centers for Disease Control and Prevention
EPI624468 French Guiana A/Guyane/1759/2015 9/4/2015 Institut Pasteur Institut Pasteur

ID: identity; SAR: Special Administrative Region; WHO: World Health Organization.

Discussion

Continuous surveillance of influenza viruses is essential for detecting emerging new variant strains and providing viruses for vaccine production [10]. In Europe, within the detected A subtypes, influenza A(H1N1)pdm09 predominated during 2010/11, 2012/13 and 2013/14 seasons and concerned 97% [11], 62% [12] and 53% [13] of subtyped influenza viruses respectively, with variation in country-specific proportions. The A(H1N1)pdm09 vaccine component A/California/7/2009 has not been changed since the 2009 pandemic and the circulating A(H1N1)pdm09 viruses have remained antigenically similar to the virus included in the vaccines throughout the influenza 2009/10 to 2015/16 seasons. However, since 2013, several reports have indicated the emergence of an expanding subgroup of A(H1N1)pdm09 viruses, designated 6B [1,8,9]. This subgroup appeared in 2012/13 and became predominant in 2013/14 [14].

In this study, we observe the further emergence of a subclade within the 6B subgroup, designated 6B.1 [15], which accounted for the majority of the A(H1N1)pdm09 viruses detected across the WHO European Region during the first weeks of the 2015/16 influenza season. In addition, the surveillance data show a change in the predominant B virus lineage from B/Yamagata which predominated in the preceding three seasons in Europe to B/Victoria.

Our data are preliminary for this season and are based on influenza surveillance without detailed reporting of clinical symptoms or vaccination status. Our genetic analysis was only based on the HA gene and does not extend to changes e.g. in genes encoding internal proteins of influenza viruses. The data reported to TESSy do not include antigenic titres and therefore no direct analysis of antigenic properties was possible. However, the antigenic reports rely on national influenza centres’ antigenic analysis that the viruses reported as like to vaccine virus were not more than fourfold different in HI titres from the vaccine or reference viruses.

The data supporting the predominance of the 6B.1 subclade stem from the subset of 12 European countries that reported virus characterisation data referring to sequences available in publically accessible databases. These countries are well spread across Europe which corroborates the conclusion of widespread 6B.1 subclade circulation. Data from the WHO Collaborating Centres indicate that the new subgroup remains antigenically similar to the vaccine component A/California/7/2009 [1], but some recent A(H1N1)pdm09 viruses within the 6B.1 and 6B.2 subclades reacted poorly with sera from individuals vaccinated with A/California/7/2009-like-strain-containing vaccine [15].

The emergence of a new A(H1N1)pdm09 subclade may eventually affect the susceptibility of the population to the currently circulating A(H1N1)pdm09 viruses, e.g. by viruses drifting closer to become immune escape variants. It is not clear whether the emergence and predominance of subclade 6B.1 has been driven by immune selection or what its impact on vaccine effectiveness may be and this needs assessment e.g. by generating lineage-specific estimation of vaccine effectiveness. Early vaccine effectiveness estimates for A(H1N1)pdm09 this season compared with the previous ones are not significantly different [16] from previous seasons. As to the severity observed this season [1-4], similar observations have been made also in earlier seasons e.g. in 2010/11 in the United Kingdom, which experienced notably severe A(H1N1)pdm09 impact in the first post-pandemic season.

Notably, recent studies have demonstrated that antigenic change in A(H1N1)pdm09 viruses is mainly caused by single amino acid substitutions affecting the loop located adjacent to the receptor binding site [17]; eight of the 215 analysed 2015/16 viruses possessed such substitutions, all six of the viruses in subclade 6B.2 and two in 6B subgroup, that do not belong to any of the newly emerged subclades.

Further enhancement of the antigenicity and virulence of influenza virus has been attributed to shielding of the major antigenic epitopes by alteration of N-linked glycosylation sites [18]. D127E substitution seen in 6B.2 has been associated with antigenic change of other influenza viruses through modelling [17]. The change at position 173 (V173I) also in the 6B.2 subclade of viruses is located in antigenic site Ca1 (position 169–173), and therefore a change here could contribute to antigen drift. It has been proposed that the evolution of A(H1N1)pdm09 will involve the acquisition of additional glycosylations, as for former seasonal A(H1N1) HA [19]. Noteworthy, 80% of the analysed HA sequences have gained a potential glycosylation site S162N. No D222G/E/N substitutions were detected, nor N129D which was recently identified in India in two severe or fatal cases [9]. If the emerging groups continue to diversify from the vaccine component, their antigenic properties may change and the vaccine effectiveness might be reduced. WHO recommended not to change the vaccine component of A(H1N1)pdm09 for the northern hemisphere 2016/17 season [20].

Early vaccine effectiveness estimates for 2015/16 are not yet available for A(H3N2) and B viruses which have been detected in lower numbers in most countries. The B/Victoria virus component is available only in the quadrivalent vaccines in the northern hemisphere for this season. As the majority of the countries use trivalent vaccines, the lineage switch from B/Yamagata to B/Victoria may contribute to lower vaccine effectiveness against influenza B. For A(H3N2), the current component of influenza vaccines is expected to have improved vaccine effectiveness compared with the two previous seasons [21,22]. In the southern hemisphere, seasonal influenza vaccine has been demonstrated to have an overall effectiveness against A(H3N2) of 36% (95% confidence interval (CI): 11–54)) for general practice encounters and 50% (95%-CI: 20–68) for hospitalisations in 2015 [23]. Despite the changes in the genetic makeup of influenza A(H1N1)pdm09 viruses and the predominance of B/Victoria lineage over B/Yamagata lineage, seasonal influenza vaccine remains the single most effective measure to prevent severe outcomes of influenza.


Disclaimer

The authors alone are responsible for the views expressed in this article and they do not necessarily represent the views, decisions or policies of the institutions with which they are affiliated.

Members of the World Health Organization European Region and European Influenza Surveillance Network of the reporting countries

Belgium: Isabelle Thomas, Anneleen Hombrouck, Nathalie Bossuyt, Sarah Moreels, Viviane Van Casteren; Croatia: Vladimir Drazenovic; Czech Republic: Martina Havlickova, Helena Jiřincová, Jan Kyncl; Denmark: Ramona Trebbien, Lisbet Krause Knudsen, Tyra Grove Krause, Thea Kølsen Fischer; Finland: Niina Ikonen, Anu Haveri, Outi Lyytikäinen, Satu Murtopuro; Germany: Brunhilde Schweiger, Marianne Wedde, Barbara Biere, Silke Buda; Greece: Athanasios Kossyvakis, Spala Georgia, Andreas Mentis, Nikolaos Malisiovas; Ireland: Lisa Domegan, Joan O’Donnell, Darina O´Flanagan, Joanne Moran, Grainne Tuite, Margaret Duffy, Jeff Connell, Cillian De Gascun; Latvia: Raina Nikiforova, Gatis Pakarna, Natalija Zamjatina; Netherlands: Adam Meijer, Anne Teirlinck, Frederika Dijkstra, Ge Donker, Guus Rimmelzwaan, Marit de Lange; Norway: Olav Hungnes, Karoline Bragstad, Siri Helene Hauge, Ragnhild Tønnessen, Susanne Gjeruldsen Dudman, Karine Nordstrand, Tora Schraffenberg, Gry Grøneng.; Portugal: Raquel Guiomar, Pedro Pechirra, Paula Cristovão, Inês Costa, Patrícia Conde, Baltazar Nunes, Ana Rodrigues; Romania: Emilia Lupulescu, Rodica Popescu, Odette Popovici, Florin Popovici; Russia: Elena Burtseva, Anna Sominina, Andrey Komissarov, Artem Fadeev, Elena Kirillova; Slovakia: Elena Tichá, Edita Staroňová, Ján Mikas; Slovenia: Katarina Prosenc, Nataša Berginc, Maja Sočan; Spain: Inmaculada Casas, Amparo Larrauri, Francisco Pozo, Concha Delgado, Jesús Oliva; Sweden: Mia Brytting, Annasara Carnahan, Åsa Wiman; Switzerland: Rita Born, Samuel Cordey; United Kingdom: Peter Coyle, Alasdair MacLean, Rory Gunson, Mary Sinnanthamby, Praveen Sebastian Pillai, Cathriona Kearns, Maria Zambon, Christopher Nugent, Catherine Moore, Nick Phin, Richard Pebody, Simon de Lusignan, Simon Cottrell, Jim McMenamin, Lucy Jessop; European Centre for Disease Prevention and Control: Cornelia Adlhoch, Adrian Prodan, René Snacken, Pasi Penttinen; WHO Collaborating Centre for Reference and Research on Influenza London: John McCauley, Rod Daniels; WHO Regional Office for Europe: Dmitriy Pereyaslov, Sergejs Nikišins.

Acknowledgements

We acknowledge the authors, originating and submitting laboratories of the sequences from GISAID’s EpiFlu Database on which the phylogenetic analysis is based (Figure 1; Accession numbers shown in Table 2). All submitters of data may be contacted directly via the GISAID website www.gisaid.org.

We thank Julien Beauté, Phillip Zucs, Denis Coulombier and Piotr Kramarz (ECDC) for improving this article, and Torstein Aune (Norway) for technical assistance in the analysis. We would also like to thank Caroline Brown from the WHO Regional Office for Europe for our joint collaboration on influenza surveillance.

We would additionally like to acknowledge all members of the Spanish Influenza Surveillance System (SISS) for the contribution in this study. Sequences from Spain were obtained in the Centro Nacional de Microbiología (ISCIII) from influenza viruses sent by the following laboratories: Hospital Miguel Servet de Zaragoza-Aragón, Hospital Universitario Central de Asturias, Hospital Universitario Son Espases de Palma de Mallorca-Baleares, Hospital San Pedro de Alcántara Cáceres-Extremadura, Hospital Donostia-País Vasco, Hospital San Pedro Logroño-La Rioja, Complejo Hospitalario Universitario de Vigo-Galicia.

Conflict of interest

None declared.

Authors’ contributions

Eeva Broberg: Data extraction, data maintenance, first draft of the manuscript, study design, revisions of the article. Angeliki Melidou: data processing, phylogenetic analysis and text. Katarina Prosenc: data processing, analysis, text. Karoline Bragstad: data processing, amino acid analysis, text. Olav Hungnes: data processing, analysis, text. ECDC and WHO Regional Office for Europe staff: influenza surveillance data maintenance, management and analysis. Country experts: surveillance systems, data collection, data analysis at national level and reporting to TESSy.


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