title: Molecular Epidemiology and Evolution of Influenza Viruses Circulating within European Swine between 2009 and 2013.
abstract: The emergence in humans of the A(H1N1)pdm09 influenza virus, a complex reassortant virus of swine origin, highlighted the importance of worldwide influenza virus surveillance in swine. To date, large-scale surveillance studies have been reported for southern China and North America, but such data have not yet been described for Europe. We report the first large-scale genomic characterization of 290 swine influenza viruses collected from 14 European countries between 2009 and 2013. A total of 23 distinct genotypes were identified, with the 7 most common comprising 82% of the incidence. Contrasting epidemiological dynamics were observed for two of these genotypes, H1huN2 and H3N2, with the former showing multiple long-lived geographically isolated lineages, while the latter had short-lived geographically diffuse lineages. At least 32 human-swine transmission events have resulted in A(H1N1)pdm09 becoming established at a mean frequency of 8% across European countries. Notably, swine in the United Kingdom have largely had a replacement of the endemic Eurasian avian virus-like ("avian-like") genotypes with A(H1N1)pdm09-derived genotypes. The high number of reassortant genotypes observed in European swine, combined with the identification of a genotype similar to the A(H3N2)v genotype in North America, underlines the importance of continued swine surveillance in Europe for the purposes of maintaining public health. This report further reveals that the emergences and drivers of virus evolution in swine differ at the global level.
  
  
  OBJECTIVE
  The influenza A(H1N1)pdm09 virus contains a reassortant genome with segments derived from separate virus lineages that evolved in different regions of the world. In particular, its neuraminidase and matrix segments were derived from the Eurasian avian virus-like ("avian-like") lineage that emerged in European swine in the 1970s. However, while large-scale genomic characterization of swine has been reported for southern China and North America, no equivalent study has yet been reported for Europe. Surveillance of swine herds across Europe between 2009 and 2013 revealed that the A(H1N1)pdm09 virus is established in European swine, increasing the number of circulating lineages in the region and increasing the possibility of the emergence of a genotype with human pandemic potential. It also has implications for veterinary health, making prevention through vaccination more challenging. The identification of a genotype similar to the A(H3N2)v genotype, causing zoonoses at North American agricultural fairs, underlines the importance of continued genomic characterization in European swine.
authors.affiliation: Wellcome Trust Sanger Institute, Hinxton, United Kingdom.
authors.forename: Simon J
authors.initials: SJ
authors.lastname: Watson
authors.affiliation: Wellcome Trust Sanger Institute, Hinxton, United Kingdom.
authors.forename: Pinky
authors.initials: P
authors.lastname: Langat
authors.affiliation: Animal and Plant Health Agency, Addlestone, Surrey, United Kingdom.
authors.forename: Scott M
authors.initials: SM
authors.lastname: Reid
authors.affiliation: Department of Zoology, University of Oxford, Oxford, United Kingdom.
authors.forename: Tommy Tsan-Yuk
authors.initials: TT
authors.lastname: Lam
authors.affiliation: Wellcome Trust Sanger Institute, Hinxton, United Kingdom.
authors.forename: Matthew
authors.initials: M
authors.lastname: Cotten
authors.affiliation: Animal and Plant Health Agency, Addlestone, Surrey, United Kingdom.
authors.forename: Michael
authors.initials: M
authors.lastname: Kelly
authors.affiliation: Laboratory of Virology, Ghent University, Merelbeke, Belgium.
authors.forename: Kristien
authors.initials: K
authors.lastname: Van Reeth
authors.affiliation: Laboratory of Virology, Ghent University, Merelbeke, Belgium.
authors.forename: Yu
authors.initials: Y
authors.lastname: Qiu
authors.affiliation: Anses, Ploufragan-Plouzané Laboratory, Swine Virology Immunology Unit, Ploufragan, France.
authors.forename: Gaëlle
authors.initials: G
authors.lastname: Simon
authors.affiliation: Anses, Ploufragan-Plouzané Laboratory, Swine Virology Immunology Unit, Ploufragan, France.
authors.forename: Emilie
authors.initials: E
authors.lastname: Bonin
authors.affiliation: Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna, Parma, Italy.
authors.forename: Emanuela
authors.initials: E
authors.lastname: Foni
authors.affiliation: Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna, Parma, Italy.
authors.forename: Chiara
authors.initials: C
authors.lastname: Chiapponi
authors.affiliation: Department of Veterinary Diagnostics and Research, Technical University of Denmark, Copenhagen, Denmark.
authors.forename: Lars
authors.initials: L
authors.lastname: Larsen
authors.affiliation: Department of Veterinary Diagnostics and Research, Technical University of Denmark, Copenhagen, Denmark.
authors.forename: Charlotte
authors.initials: C
authors.lastname: Hjulsager
authors.affiliation: Department of Swine Diseases, Panstwowy Instytut Weterynaryjny, Pulawy, Poland.
authors.forename: Iwona
authors.initials: I
authors.lastname: Markowska-Daniel
authors.affiliation: Department of Swine Diseases, Panstwowy Instytut Weterynaryjny, Pulawy, Poland.
authors.forename: Kinga
authors.initials: K
authors.lastname: Urbaniak
authors.affiliation: IDT Biologika GmbH, Dessau-Roßlau, Germany.
authors.forename: Ralf
authors.initials: R
authors.lastname: Dürrwald
authors.affiliation: IDT Biologika GmbH, Dessau-Roßlau, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Schlegel
authors.affiliation: Finnish Food Safety Authority EVIRA, Helsinki, Finland.
authors.forename: Anita
authors.initials: A
authors.lastname: Huovilainen
authors.affiliation: Division of Avian Diseases, Kimron Veterinary Institute, Bet Dagan, Israel.
authors.forename: Irit
authors.initials: I
authors.lastname: Davidson
authors.affiliation: National Food Chain Safety Office, Budapest, Hungary.
authors.forename: Ádám
authors.initials: Á
authors.lastname: Dán
authors.affiliation: Central Veterinary Institute, Wageningen UR, Lelystad, The Netherlands.
authors.forename: Willie
authors.initials: W
authors.lastname: Loeffen
authors.affiliation: Wellcome Trust Sanger Institute, Hinxton, United Kingdom.
authors.forename: Stephanie
authors.initials: S
authors.lastname: Edwards
authors.affiliation: Virology Department, Discovery Research, Merial, Lyon, France.
authors.forename: Michel
authors.initials: M
authors.lastname: Bublot
authors.affiliation: Virology Department, Discovery Research, Merial, Lyon, France.
authors.forename: Thais
authors.initials: T
authors.lastname: Vila
authors.affiliation: Veterinary Diagnostic Services DIAGNOS, Laboratorios HIPRA SA, Gerona, Spain.
authors.forename: Jaime
authors.initials: J
authors.lastname: Maldonado
authors.affiliation: Veterinary Diagnostic Services DIAGNOS, Laboratorios HIPRA SA, Gerona, Spain.
authors.forename: Laura
authors.initials: L
authors.lastname: Valls
authors.affiliation: Animal and Plant Health Agency, Addlestone, Surrey, United Kingdom.
authors.forename: Ian H
authors.initials: IH
authors.lastname: Brown
authors.affiliation: Department of Zoology, University of Oxford, Oxford, United Kingdom.
authors.forename: Oliver G
authors.initials: OG
authors.lastname: Pybus
authors.affiliation: Wellcome Trust Sanger Institute, Hinxton, United Kingdom Division of Infection & Immunity, University College London, London, United Kingdom pk5@sanger.ac.uk.
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authors.lastname: Kellam
mesh_terms: D000818:Animals; D062665:Epidemiological Monitoring / Q000662:veterinary; D005060:Europe / Q000453:epidemiology; D019143:Evolution, Molecular; D005838:Genotype; D006801:Humans; D053118:Influenza A Virus, H1N1 Subtype / Q000235:genetics / Q000302:isolation & purification; D057221:Influenza A Virus, H1N2 Subtype / Q000235:genetics / Q000302:isolation & purification; D053122:Influenza A Virus, H3N2 Subtype / Q000235:genetics / Q000302:isolation & purification; D009980:Influenza A virus / Q000235:genetics* / Q000302:isolation & purification; D007251:Influenza, Human / Q000453:epidemiology / Q000821:virology; D017720:Molecular Epidemiology; D009976:Orthomyxoviridae Infections / Q000453:epidemiology / Q000662:veterinary* / Q000821:virology; D010802:Phylogeny; D016865:Reassortant Viruses / Q000235:genetics; D034421:Sus scrofa / Q000821:virology*; D013552:Swine; D013553:Swine Diseases / Q000453:epidemiology* / Q000821:virology*