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Downloaded from WHO Flunet ( Flunet/En/ (Accessed on 30 March 2020)) Article Diversity in the Circulation of Influenza A(H3N2) Viruses in the Northern Hemisphere in the 2018–19 Season Rakefet Pando 1,2,†, Shahar Stern 2,† , Ital Nemet 2, Aharona Glatman-Freedman 1,3, Hanna Sefty 1, Neta S. Zuckerman 1, Yaron Drori 2, Nehemya Friedman 2, John W. McCauley 4 , Lital Keinan-Boker 1,5, Ella Mendelson 2,3, Rodney S. Daniels 4 and Michal Mandelboim 2,3,* 1 The Israel Center for Disease Control, Israel Ministry of Health, Tel-Hashomer, Ramat-Gan 52621, Israel; [email protected] (R.P.); [email protected] (A.G.-F.); [email protected] (H.S.); [email protected] (N.S.Z.); [email protected] (L.K.-B.) 2 Chaim Sheba Medical Center, Central Virology Laboratory, Ministry of Health, Ramat-Gan 52621, Israel; [email protected] (S.S.); [email protected] (I.N.); [email protected] (Y.D.); [email protected] (N.F.); [email protected] (E.M.) 3 Department of Epidemiology and Preventive Medicine, Sackler Faculty of Medicine, School of Public Health, Tel-Aviv University, Tel-Aviv 6997801, Israel 4 Worldwide Influenza Center, The Francis Crick Institute, London NW1 1AT, UK; [email protected] (J.W.M.); [email protected] (R.S.D.) 5 School of Public Health, University of Haifa, Haifa 3498838, Israel * Correspondence: [email protected] † Equal contribution. Citation: Pando, R.; Stern, S.; Abstract: While vaccination is considered the most effective means to prevent influenza infection, its Nemet, I.; Glatman-Freedman, A.; seasonal effectiveness varies, depending on the circulating influenza strains. Here, we characterized Sefty, H.; Zuckerman, N.S.; Drori, Y.; the circulation of influenza strains in October-2018 and March-2019 around the world. For this, Friedman, N.; McCauley, J.W.; we used nasopharyngeal samples collected from outpatient and hospitalized patients in Israel and Keinan-Boker, L.; et al. Diversity in data reported in ECDC, CDC, and WHO databases. Influenza A(H3N2) was dominant in Israel, the Circulation of Influenza A(H3N2) while in Europe, Asia, and USA, A(H1N1)pdm09 virus circulated first, and then the A(H3N2) virus Viruses in the Northern Hemisphere in the 2018–19 Season. Vaccines 2021, also appeared. Phylogenetic analysis indicated that A(H3N2) viruses circulating in Israel belonged 9, 375. https://doi.org/10.3390/ to clade-3C.3a, while in Europe, Asia, and USA, A(H3N2) viruses belonged to subclade-3C.2a1, vaccines9040375 but were later replaced by clade-3C.3a viruses in USA. The vaccine A(H3N2) components of that year, A/Singapore/INFIMH-16-0019/2016-(H3N2)-like-viruses, belonged to subclade-3C.2a1. The Academic Editor: Andrew Pekosz circulation of different influenza subtypes and clades of A(H3N2) viruses in a single season highlights the need for universal influenza vaccines. Received: 23 January 2021 Accepted: 26 March 2021 Keywords: influenza A; circulation; clade; vaccine Published: 13 April 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- Influenza viruses cause contagious respiratory disease [1] and are classified as types iations. A, B, and C, with the first two significantly impacting human health each year [2]. Type A viruses are divided into subtypes determined by their hemagglutinins (HA) and neu- raminidases (NA), with A(H3N2) and A(H1N1)pdm09 subtypes currently circulating in humans [1,3]. While in most years a single subtype predominates, the two type A virus sub- Copyright: © 2021 by the authors. types can co-circulate [4,5]. Similarly, there are two lineages of type B viruses—B/Yamagata Licensee MDPI, Basel, Switzerland. and B/Victoria—which also co-circulate, but with one lineage predominating [6,7], al- This article is an open access article though in some seasons, circulation of type B viruses is negligible [8]. However, influenza distributed under the terms and viruses undergo genetic change in the course of their evolution, markedly so in the genes conditions of the Creative Commons encoding HA and NA with resultant amino acid substitutions permitting escape from host Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ immune responses, a process termed antigenic drift, which results in recurrent seasonal 4.0/). influenza outbreaks/epidemics [9–11]. Vaccines 2021, 9, 375. https://doi.org/10.3390/vaccines9040375 https://www.mdpi.com/journal/vaccines Vaccines 2021, 9, 375 2 of 12 Vaccination is considered the most effective way of preventing influenza infection [12–14]. The composition of the annual vaccines follows recommendations developed by the World Health Organization (WHO), based on worldwide surveillance conducted by the Global In- fluenza Surveillance and Response System (GISRS) [13]. Recommendations are announced each year at the end of February for the northern hemisphere and in September for the southern hemisphere [15]. For the 2017–18 season, the vaccine virus recommendations for the North- ern hemisphere were A/Michigan/45/2015 (H1N1) pdm09-like; A/Hong Kong/4801/2014 (H3N2)-like; B/Brisbane/60/2008-like (B/Victoria/2/87 lineage); and B/Phuket/3073/2013- like (B/Yamagata/16/88 lineage) [16]. For the 2018–19 season, two vaccine component changes were recommended to an A/Singapore/INFIMH-16-0019/2016 (H3N2)-like virus and a B/Colorado/06/2017-like virus (B/Victoria/2/87 lineage) [17]. Since 2009, A(H3N2) viruses have undergone significant genetic drift (new clades and subclades), with some associated antigenic drift, that has led to multiple changes in the recommended A(H3N2) vaccine virus over the past 12 years [15]. In recent winter seasons, the majority of A(H3N2) viruses had belonged to the HA phylogenetic subclade-3C.2a1b; however, the number of clade-3C.3a viruses increased substantially from November 2018 in several geographic regions [18]. The aim of this study was to review what influenza strains circulated around the world in 2018–19 and to investigate whether they resembled those used in the vaccine. We review influenza circulation in Israel, Europe, Asia, and USA over the 2018–2019 winter, with focus on the unusual pattern observed in Israel. A(H3N2) viruses of clade-3C.3a predominated in Israel from the start of the season, while the same season in Europe, Asia, and USA was biphasic, with A(H1N1) pdm09 viruses dominating for most of the season, with co-circulation of subclade-3C.2a1 A(H3N2) viruses, followed by a second phase, which was dominated by clade-3C.3a A(H3N2) viruses. Consequently, most of the A(H3N2) viruses in circulation differed from the subclade-3C.2a1, A/Singapore/INFIMH- 16-0019/2016-(H3N2)-like, vaccine viruses. 2. Materials and Methods 2.1. Ethics Approval Respiratory samples from hospitalized and non-hospitalized patients with clinical symptoms of influenza-like-illness (ILI) were analyzed for the presence of respiratory viruses as part of routine testing performed in the Sheba Medical Centre (SMC), Israel. The SMC institutional review board (IRB) approved this research (Helsinki Number 1967-15- SMC). Informed consent was not required for this study. 2.2. Sample Collection Nasopharyngeal samples of patients presenting with ILI were collected into ∑-Virocult (mwe, Manchester, UK) virus transport medium. Samples (n = 1487) were collected between October 2018 and March 2019 in outpatient clinics located in different geographic parts of Israel as part of annul surveillance conducted by the Israel Influenza Surveillance Network (IISN). In addition, samples were collected from all hospitalized patients at the SMC (n = 7310) that suffered from ILI in 2018–19. 2.3. Nucleic Acid Extraction and Detection of Influenza Viruses Viral RNA (vRNA) was extracted from all samples using MagNA PURE 96 (Roche, Mannheim, Germany), following the manufacturer’s instructions. All samples were then tested for the presence of influenza viruses (types A and B) and respiratory syncytial virus (RSV), in a single real-time reverse transcriptase polymerase chain reaction (RT- PCR) performed using Ambion Ag-Path master mix (Thermo Fisher Scientific, Waltham, MA, USA) and TaqMan Chemistry (qRT-PCR), on an ABI 7500 platform, as described previously [19]. Vaccines 2021, 9, 375 3 of 12 2.4. Phylogenetic Bayesian Evolutionary Analysis by Sampling Trees (BEAST) Analysis Influenza A(H3N2) HA gene-specific RT-PCR primers were used to amplify 1701 base-pair fragments, as described in WHO protocols [20]. The amplified products were then sequenced using ABI PRISM Dye Deoxy Terminator cycle sequencing kits (Applied Biosystems, Foster City, CA, USA) and Applied Biosystems model 3100 DNA automatic sequencing systems. The Sequencher® 5.0 program (Gencodes Corporation, Ann Arbor, MI, USA) was used to prepare FASTA files for further analysis. The evolutionary relationships for the influenza A(H3N2) HA sequences were inferred using the general time-reversible model, with proportion of invariable sites and gamma plus invariant sites-distributed rate heterogeneity (GTR+G+I), chosen using JModelTest [21]. A Bayesian Markov chain Monte Carlo (MCMC) method was run for 10 million iterations, with a relaxed clock and 10% burn-in period, with samples saved every 10,000 iterations, using BEAST version 1.8 [22]. Phylogenetic trees were visualized in FigTree version 1.4.3 (http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 30 March 2020)). A random selection of 259 influenza A(H3N2) HA gene sequences from Israeli, Euro- pean, Asian, and USA samples for the years 2009–2019 used in this analysis were down- loaded from the EpiFluTM database of the Global Initiative on Sharing All Influenza Data (GISAID) (www.gisaid.org (accessed on 30 March 2020)). GISAID sequences used in this manuscript are listed in Supplementary Table S1. 2.5. Data Distribution from Europe, Asia, and USA Data from seasonal surveillance of influenza in Europe, Asia, and USA were col- lected from open-access databases.
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