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In recent years, important changes in the ecology, epidemiology, and evolution of this virus have been reported, with an unprecedented global diffusion and variety of affected birds and mammalian species. After the two consecutive and devastating epidemic waves in Europe in — and —, with the second one recognized as one of the largest epidemics recorded so far, this clade has begun to circulate endemically in European wild bird populations. This study used the complete genomes of 1, European HPAI A H5Nx viruses to investigate the virus evolution during this varying epidemiological outline. We demonstrated the high genetic diversity of the circulating viruses, which have undergone frequent reassortment events, providing for the first time a complete overview and a proposed nomenclature of the multiple genotypes circulating in Europe in — We described the emergence of a new genotype with gull adapted genes, which offered the virus the opportunity to occupy new ecological niches, driving the disease endemicity in the European wild bird population. The high propensity of the virus for reassortment, its jumps to a progressively wider number of host species, including mammals, and the rapid acquisition of adaptive mutations make the trend of virus evolution and spread difficult to predict in this unfailing evolving scenario. In late and early , multiple outbreaks were reported almost simultaneously in poultry in several East Asian countries Li et al. The situation dramatically changed in spring , when, following a mass die-off of wild migratory birds infected with A H5N1 in Qinghai Lake in central China Chen et al. The global circulation of this lineage has led to the diversification of the hemagglutinin HA gene segment into ten first-order clades and multiple second to fifth-order subclades Smith and Donis Since , subclade 2. The — epidemic was predominantly caused by HPAI A H5N8 viruses, which affected most European countries with a significant impact on both wild 1, cases and domestic birds 1, outbreaks Adlhoch et al. Over the following years, — and —, two minor incursions were reported, with a limited number of countries affected during the winter seasons. Since October , consecutive epidemic waves have been reported in Europe Floyd et al. The first epidemic wave lasted from October to September , with 3, HPAI A H5Nx detections 2, in wild birds and 1, in domestic birds across thirty-one European countries. This was followed by an even larger second wave, which lasted from October to September , counting a total of 6, HPAI A H5Nx detections 3, in wild and 2, in domestic birds reported across thirty-seven countries. In , for the first time the virus caused several mass mortality events in wild birds during the summer months, likely due to the virus spreading to seabird breeding colonies, a category of wild birds, which had very rarely been affected before by HPAI A H5Nx Adlhoch et al. The — and — waves were characterized by the circulation of different subtypes and genotypes, as a result of reassortment events with low pathogenicity avian influenza LPAI viruses Lewis et al. While the A H5N8 subtype mainly drove the first — epidemic wave, A H5N1 was responsible for the majority of the — and — outbreaks Adlhoch et al. These epidemics did not affect only Europe, but had global impact. From late , A H5N1 viruses of clade 2. In December , the A H5N1 clade 2. At the beginning of , a new introduction into North America via the Pacific flyway of an A H5N1 related to the viruses circulating in Japan was identified Alkie et al. In October , A H5N1 viruses spread for the first time to Mexico and soon after to South America, with mass mortality events reported in wild birds Adlhoch et al. We demonstrated the high genetic diversity of the circulating viruses, which underwent frequent reassortment events, and suggested a nomenclature to describe the circulating genotypes. Importantly, we described the relevant changes between the two epidemic waves in terms of spatiotemporal dynamics of virus spread and host range, which have dramatically modified the disease epidemiology in Europe with serious consequences for the poultry industry, wild bird populations such as sea birds , and farmed carnivores e. The samples originated from thirty-two European countries with being collected during the — wave and 1, during the — wave— up to August Among avian hosts, we identified five different host categories: domestic birds Galliformes, Anseriformes, and others , waterfowls mainly Anseriformes and Charadriformes , raptors, colony breeding seabirds mainly Laridae and Sulidae , and others Supplementary Table S1. FigTree v1. The identification of the genotype was based on the phylogenetic tree topology. A reference sequence was selected among the donors for each gene segment and each cluster, to represent the potential progenitor virus of that cluster. An identification ID number cluster ID was assigned to each cluster and the combination of the eight IDs one for each gene segment defined a genotype Fig. Graphical representation of the A H5Nx genotypes identified in Europe during the first — and second — epidemic wave. A number and associated colour code is assigned to each gene based on its genetic clustering in the phylogenetic trees. The reference sequences represent the possible progenitor virus for each specific gene. To investigate the spatial spread of the 2. Sequences were phylogenetically analysed together with the HA gene sequences of the European viruses; all the HA sequences that shared a common progenitor with the European viruses were retained for the following analyses about 3, sequences. For each trait geographic area , the number of sequences ranged from 47 the Middle East to Europe , for a total of sequences. To explore the dynamics of virus spread within Europe, we generated two datasets, one for each epidemic wave. The European dataset of the first epidemic wave — included sequences, whereas the one generated for the second epidemic wave — included sequences collected up to August MCMC chains were run for — million iterations and convergence was assessed using Tracer v1. To explore the pattern of spatial diffusion among the geographic regions, discrete phylogeographic analyses using location as a trait were performed Lemey et al. We assumed an asymmetric non-reversible transition model and incorporated Bayesian stochastic search variable selection Lemey et al. Spread D3 v0. We employed the Markov jump counts to measure the number of viral movements along the branches of the phylogeny and estimated the Markov rewards to quantify the time the virus spent in each geographical region Minin and Suchard ML phylogenetic analysis of the eight gene segments was used to assess the number and variety of co-circulating genotypes, each defined by a unique gene composition inferred from tree topologies and inconsistencies among the genetic clustering of the eight gene segments Supplementary Figs. The first identified A H5Nx viral genome showing a particular gene constellation was used as a reference strain for a specific genotype e. In order to make communication easier and to distinguish the genotypes identified during each epidemic wave, we named them with the indication of the lineage e. EA, Eurasian , the year of identification and with letters—a single letter i. A, B, C for the genotypes which had originated during the — wave and two letters i. AA, AB, ac for the genotypes of the — wave e. Overall, we defined fifty different A H5Nx genotypes from multiple inter- and intra-subtype reassortment events Fig. The highest genetic diversity in terms of number of co-circulating genotypes from 13 to 25 was observed during the winter months in both waves: January—March and November —February Fig. Of note, the frequency of reassortment was not homogenous among the eight gene segments. While the HA and matrix M gene segments were stable, multiple switches were observed for the polymerase basic PB 2, PB1, polymerase acidic PA , and nucleoprotein NP segments that were classified into 14, 12, 11, and 16 clusters, respectively. Each colour represents a different genotype. The great majority of the viruses As genotype EAC H5N1 had never been identified before October in other areas outside Europe, it was assumed to have emerged in Europe from the A H5N8 subtype through a single reassortment event involving six gene segments PB2, PB1, PA, NP, neuraminidase NA , and non-structural NS , although it is not possible to discount that this occurred in a step-wise manner involving un-sampled intermediates including outside Europe. The EAA genotype appeared to dominate over all the other genotypes until August With the beginning of the second wave in Europe in October and the rise in the number of A H5Nx virus detections, we witnessed a dramatic shift in the genetic composition of circulating subtypes and genotypes Fig. While in —, A H5N8 had been the most prevalent subtype, the — wave was dominated almost exclusively by A H5N1. Unfortunately, the scarcity of genetic data from countries outside Europe makes it impossible to assess for certain the geographic source area of the different genotypes. Overall, thirty-four different genotypes, thirty belonging to the A H5N1 subtype, were characterized during the — wave, indicating that the diversity of genotypes detected was even greater than in the previous wave. With a frequency of At the beginning of this epidemic wave, a rise of genotype EAC was observed in Europe, likely as a result of a combination between an increase in the number of local cases and novel virus incursions probably from Russia of the same genotype. Indeed, the topology of the phylogenetic trees revealed that the — European viruses of the EAC genotype split into two sub-clusters, one comprising the A H5N1 viruses collected in European countries since October , the other including A H5N1 collected in Russia since the beginning of October and subsequently end of October in Europe Supplementary Figs. During the — and — epidemic waves, multiple spillover events from birds to ten different mammalian species were reported Adlhoch et al. Panel A—bars represent the distribution of the genetically characterized complete genome A H5Nx viruses collected from mammals in Europe from December to August , by month of detection, coloured according to the genotype. Panel B—frequency of the molecular markers of mammalian adaptation in the PB2 protein A, K, N identified in viruses collected from mammalian species in Europe between October and August Conversely, during the second wave, genotype EAC showed a remarkable geographical expansion twenty-one countries in — vs eleven countries in — Fig. Geographic distribution of the major A H5Nx genotypes represented by at least three viruses in Europe during the first —, left panel and second —, right panel epidemic wave. The pie charts display the frequency of the genotype in each country. The size of the circle is proportional to the number of sequences analysed. The highest genotype diversity was observed in the Netherlands fifteen genotypes , France twelve genotypes , Sweden eleven genotypes , and Germany ten genotypes , followed by Belgium, Croatia, Czech Republic, Denmark, Ireland, Italy, Poland, Romania, Slovenia, and the UK, with five to ten circulating genotypes Fig. Specifically, during the — wave, the highest genotype diversity 5—9 genotypes was detected in Northern Europe Denmark, Germany, the Netherlands, Sweden, and the UK , while during the — wave, a more widespread genotype diversity was observed, with the Czech Republic, France, Germany, Italy, the Netherlands, Poland, Romania, and the UK having four to nine genotypes each. Domestic birds both Galliformes and Anseriformes and waterfowl Anseriformes are the host categories harbouring the highest genetic diversity among the detected viruses, while the lowest was observed in seabirds Fig. In this latter group, the frequency of the detected genotypes also differed considerably from what was noted in the other host categories domestic, waterfowl, raptors , showing a higher level of circulation of genotype EAC during the — wave and of genotype EABB during the — wave compared to other host categories Fig. Distribution of the different genotypes by bird host categories during the first —, left panel and second —, right panel epidemic wave. The colours assigned to the four major genotypes are reported in the figure legend. According to the most probable location at the root of the MCC tree of the HA gene, the Middle East seems to be the most likely geographical source of this virus, which, between the second half of and the beginning of , reached Central Asia Supplementary Fig. S1 , which agrees with earlier studies Lewis et al. Our analysis indicates that Central Asia, which represents one of the most important breeding sites for multiple wild bird species, was a key source of the virus for most of the other geographic locations S14 indicated that the viruses had been introduced from Central Asia to the different geographic areas over the same time period summer — autumn during both epidemic waves. Europe proved to be the major source of the virus for Africa and North America. Markov rewards, which estimate the proportion of time the A H5Nx virus spent in each geographical area, revealed that at a global level the virus spent most of the time in East Asia Global migration rates among the geographic regions of clade 2. Pattern of geographic jumps and hotspots obtained from the analyses of A global dataset, B European dataset—first wave — , and C European dataset—second wave — The three heatmaps on the left indicate the frequency of transitions between locations estimated using a discrete trait phylogenetic model. The number of location transitions was determined using Markov jumps. The bar charts on the right indicate the proportion of time the virus spent in each location. Analyses confirmed Central Asia as being the major source of the virus for the whole of Europe during both epidemic waves Fig. Estimation of the time the A H5Nx had remained in each region using Markov rewards demonstrated that the virus had spent most of the time in North-Central Europe A H5Nx spent the least amount of time in the South-Eastern and North-Eastern regions of Europe, although bias due to different intensity of genomic surveillance in each geographic region cannot be excluded. Migration rates between European regions of clade 2. Molecular analyses of the European A H5Nx viruses investigated in this study October —August indicate that they retained the avian-type-receptor-binding signature Q and G H5 numbering in the HA receptor binging site Stevens et al. However, we identified several mutations with a varying frequency, which have been previously demonstrated to affect the biological characteristics of avian influenza viruses Suttie et al. These include mutations associated with 1 enhanced polymerase activity and replication in mammals or mammalian cells, 2 increased virulence in mammals or avian species, 3 antiviral drug resistance, and 4 increased in vitro binding to human-type receptors alpha-2,6-linked sialic acids. The phenotypic effect of most of these mutations on the biological characteristics of the viruses is still unknown and further studies are needed to improve existing knowledge. Among the mutations in the HA protein that have proved to increase in vitro binding to human-type receptors, some i. Moreover, we identified 84 viruses carrying mutations in the second sialic acid-binding site contact residues 2SBS of the NA, which can affect the binding and cleavage of receptors and virus replication. A single mutation in this position of the N1 protein has been demonstrated to disrupt 2SBS and negatively affect N1 activity Du et al. This mutation has been observed in all N1 sequences from human seasonal and H1N1pdm09 pandemic viruses and in several other viruses adapted to mammalian host species. Despite these markers being only sporadically detected in birds, it is worth noting that eleven out of the seventeen of the sequences showing the PBK were detected in viruses collected from a cluster of outbreaks in poultry in Germany, as previously described King et al. Mutations associated with antiviral resistance were identified occasionally. BTN3A3 is a major histocompatibility complex associated protein constitutively expressed in human airways and is a potent inhibitor of avian but not human influenza A viruses Pinto et al. Norway, Iceland, and Svalbard Islands Madslien et al. In this study, we explored the changing pattern of the HPAI virus evolution between and in Europe, one of the most affected continents in terms of geographical spread, number of poultry outbreaks, and number of affected wild bird species. The complete data from the — wave were not available at the time of our analyses; therefore, they have not been included in the present paper. In agreement with previous studies Lewis et al. In spring , viruses closely related to those collected in poultry in the Middle East were first identified in wild birds in Central Asia and then in Europe, which suggests that the virus may have jumped from the domestic to the wild bird population, although unsampled ancestry makes definitive assessment challenging. However, where this jump occurred—in the Middle East, Russia, or elsewhere—cannot be ascertained based on the available data. A similar scenario was observed in , when one A H5N8 reassortant virus of clade 2. Despite data indicating that new hotspots i. At the European level, North-Central Europe emerged as the major source of A H5Nx viruses for the rest of Europe and the area where the virus was detected for the longest period of time. The coastal area of North-Central Europe i. A caveat of this study is that phylodynamic analyses rely on the availability of sequences; big efforts were made to increase wild bird surveillance and to generate sequencing data. The structure, design, and implementation of surveillance for wild birds across Europe are highly variable i. Furthermore, additional bias cannot be excluded given the different resources and sequencing capabilities of the different countries. Clade 2. However, compared to the previously described epidemic waves in Europe Bragstad et al. The greater genetic diversity in the second wave may be explained by the unprecedented number of cases and geographical extent thirty-seven European affected countries observed in —, which represents the most devastating HPAI A H5N1 epidemic affecting Europe to date. The highest number of reassortment events were observed for the gene segments encoding for the polymerase complex PB1, PB1, and PA and the nucleoprotein gene, while the HA and M genes—during the first wave—and the HA, NA, and M genes—during the second wave—were very stable. It has recently been suggested that the M gene of clade 2. An M-HA effective cooperation has been demonstrated to be necessary for efficient virus replication Webster, Kawaoka, and Bean ; Scholtissek et al. Moreover, Campbell et al. However, it spread globally and, in the subsequent epidemic wave, it became clearly dominant in Europe, which suggests that it may have had a higher fitness advantage than the other subtypes. Among the characterized genotypes, EABB A H5N1 —which had emerged in spring from reassortment events with H13 LPAI viruses, a subtype circulating primarily in gulls, with unique species-specific gene signatures emerging for prolonged genetic isolation and co-evolution with this species Olsen et al. In the summer , this genotype had been detected mainly in European herring gulls in Northern Europe France, Belgium, the Netherlands, and occasionally in the UK. However, starting from autumn , a southward spread of this genotype to Spain and then Italy, Switzerland, and Austria, followed by an eastward and northward spread to Poland, the Czech Republic, Croatia, Sweden, Norway, and Denmark, was reported Adlhoch et al. The ongoing and widespread circulation of this genotype in the gull population, with black-headed gulls representing the most affected species since winter —, highlights the serious threat posed by this variant to the sea-bird population, with mass mortality events persistently reported in several colonies of gulls and terns from different countries Adlhoch et al. Of note, the association of this genotype with the infection in Laridae may indicate it is well adapted to the members of this family. Gull-specific clades have previously been demonstrated for the PB2, NP, and NS gene segments, regardless of the geographical region. Moreover, the NP and PA genes have been shown to share a common evolutionary history in different host species, which suggests they tend not to reassort independently Webster et al. Viruses of the A H13 subtype do not readily infect ducks when they are inoculated experimentally Fouchier et al. Of note, this genotype possesses mutations in the NP and NA proteins that can contribute to increase its zoonotic potential Du et al. Whether the zoonotic potential of this genotype is higher than that of the other genotypes is unknown. Based on the available data, the majority of the infections in mammalian species have been caused by genotypes circulating with the highest frequency in birds at the time of the infection, suggesting direct and separate spillover events from birds to scavenging mammals in particular. Of note, our data indicate that mutations in the polymerase proteins associated with adaptation to mammalian species can be rapidly acquired by the virus during replication in a mammalian host, which seems to indicate that mammals may represent an important source of viruses with an increased zoonotic potential. However, recent serological evidence of A H5Nx infections in wild and domestic mammals, including pets reared or living in farms where poultry outbreaks were reported, clearly suggests that we have likely uncovered only the tip of the iceberg Chestakova et al. This would provide health authorities with adequate information for a proper management of outbreaks in species belonging to this class. For the first time, this study presents a complete overview of the multiple genotypes that had been circulating in Europe from October to August , providing information on their geographic and host distribution. However, such data should always be interpreted taking into account the sampling bias within wild bird surveillance towards sick or dead birds, rather than resilient or asymptomatic birds. We assigned each genotype a name to simplify and encourage discussion between European laboratories. This changing ecology, accompanied by viruses endemically circulating in wild birds in Europe in a progressively wider number of hosts, may change both the hot spots and the target species for virus surveillance, making trends of virus evolution and spread difficult to predict. However, the present article is published under the sole responsibility of the author Francesca Baldinelli and may not be considered as an EFSA scientific output. Support for this work was provided by the European Commission within the framework of the activities foreseen by the European Union Reference Laboratory for Avian Influenza and Newcastle Disease under grant agreement SI2. Abed Y. Google Scholar. Abolnik C. Adams S. Adlhoch C. European Food Safety Authority , 21 : e Alkie T. Ayllon J. Bielejec F. Bordes L. Bortz E. Bourmakina S. Bragstad K. Briand F. Bruno A. Buranathai C. Bussey K. Caliendo V. Campbell P. Chen H. Chen L. Chernomor O. Chestakova I. Cheung C. Chizhmakov I. Drummond A. Elgendy E. Elleman C. Engelsma M. Floyd T. Food Safety Authority, E. Fornek J. Fouchier R. Fusaro A. Gabriel G. Gao Y. Gao W. Govorkova E. Grant M. Gubareva L. Hagag N. Hatta H. Hatta M. Herfst S. Hoffmann T. SS et al. Hurt A. Ilyushina N. Imai H. Isoda N. Jackson D. Jiao P. Katoh K. Kim J. King J. Kiso M. Kode S. Kuo R. Labadie K. Lan Y. Lee D. Leguia M. Lemey P. Letsholo S. Lewis N. Leyson C. Lindh E. Lycett S. Madslien K. Makalo M. Manzoor R. Mehle A. Meseko C. Minin V. More S. European Food Safety Authority , 15 : e Moreno A. Munier S. Nagy A. Nguyen L. Oliver I. Olsen B. Ouoba L. Pinto R. Pohlmann A. Puthavathana P. Rameix-Welti M. Richard M. Rosone F. Sagong M. Salaheldin A. Salomon R. Samson M. Sanogo I. Scheiffarth G. Scholtissek C. Shapiro B. Shinya K. Smith G. Song W. Sonnberg S. Sorrell E. Soubies S. Spesock A. Steel J. Stevens J. Subbarao E. Suchard M. Suttie A. Swieton E. Taft A. Tammiranta N. Thi Hoang D. Verhagen J. Vreman S. Wang W. Watanabe Y. Webster R. Wille M. Xiao C. Xie R. Yamada S. Yamayoshi S. Yang Z. Youk S. Zhang J. Zhang G. Zhou H. Zhu W. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign in through your institution. Advanced Search. Search Menu. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents Abstract. Materials and methods. Supplementary data. Conflict of interest:. Data Availability. Journal Article. High pathogenic avian influenza A H5 viruses of clade 2. Alice Fusaro , Alice Fusaro. Oxford Academic. Bianca Zecchin. Edoardo Giussani. Elisa Palumbo. Claudia Bachofen. Fereshteh Banihashem. Ashley C Banyard. Nancy Beerens. Department of Virology Wageningen Bioveterinary Research. Manon Bourg , Manon Bourg. Francois-Xavier Briand. Ian H Brown. Brigitte Brugger. Icelandic Food and Veterinary Authority. Alexander M P Byrne. Armend Cana. Vasiliki Christodoulou. Zuzana Dirbakova. Teresa Fagulha. Ron A M Fouchier. Department of Viroscience, Erasmus MC. Laura Garza-Cuartero. George Georgiades. Britt Gjerset. Beatrice Grasland. Oxana Groza. Timm Harder. Ana Margarida Henriques. Charlotte Kristiane Hjulsager. Emiliya Ivanova. Zygimantas Janeliunas. Laura Krivko. Ken Lemon. Yuan Liang. Aldin Lika. Michael J McMenamy. Alexander Nagy. Imbi Nurmoja. Iuliana Onita. Anne Pohlmann. Vladimir Savic. Croatian Veterinary Institute, Poultry Centre. Brigita Slavec. Krzysztof Smietanka. Chantal J Snoeck. Mieke Steensels. Avian Virology and Immunology, Sciensano. Edyta Swieton. Niina Tammiranta. Martin Tinak. Steven Van Borm. Siamak Zohari. Cornelia Adlhoch. European Centre for Disease Prevention and Control. Francesca Baldinelli. Calogero Terregino. Isabella Monne. Revision received:. Editorial decision:. Corrected and typeset:. Select Format Select format. Permissions Icon Permissions. Figure 1. Open in new tab Download slide. Figure 2. Figure 3. Figure 4. Figure 5. Figure 6. Figure 7. Figure 8. Table 1. Open in new tab. Google Scholar Crossref. Search ADS. Google Scholar PubMed. Asymptomatic Infection with Clade 2. A New Clade 2. Emergence of a Reassortant 2. Has Epizootic Become Enzootic? Emergence of Clade 2. Thi Hoang. World Health Organization. Published by Oxford University Press. For commercial re-use, please contact reprints oup. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals. Download all slides. Views 4, More metrics information. Total Views 4, Email alerts Article activity alert. Advance article alerts. New issue alert. In progress issue alert. Receive exclusive offers and updates from Oxford Academic. Citing articles via Web of Science 5. Latest Most Read Most Cited Long-read transcriptomics of Ostreid herpesvirus 1 uncovers a conserved expression strategy for the capsid maturation module and pinpoints a mechanism for evasion of the ADAR-based antiviral defence. Genomic epidemiology reveals the variation and transmission properties of SARS-CoV-2 in a single-source community outbreak. On the importance of assessing topological convergence in Bayesian phylogenetic inference. More from Oxford Academic. Biological Sciences. Evolutionary Biology. Medicine and Health. Public Health and Epidemiology. Science and Mathematics. Authoring Open access Purchasing Institutional account management Rights and permissions. Get help with access Accessibility Contact us Advertising Media enquiries. Zhang et al. Bussey et al. Gao et al. Hu et al. Yamayoshi et al. Song et al. Xiao et al. Bortz et al. Taft et al. Elgendy et al. Xu et al. Zhu et al. Gabriel, Herwig, and Klenk , Gabriel et al. Ayllon et al. Li et al. Su et al. Yang et al. Wang et al. Watanabe et al. Chen et al. Yamada et al. Kim et al. Jiao et al. Kuo and Krug ; Spesock et al. Jackson et al. Kode et al. Adams et al. Gubareva et al. Samson et al. Hurt et al. Govorkova et al. Abed, Goyette, and Boivin ; Cheung et al. Chizhmakov et al. Cheung et al. Buranathai et al. Imai et al. Du et al. Pinto et al. Hoffmann et al.

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