Molecular epidemiology and evolution of influenza viruses circulating within European swine between 2009 and 2013

Journal of Virology

Volumn 89, Issue 19, 2015, Pages 9920-9931

  Watson, Simon J ^a   Langat, Pinky ^a   Reid, Scott M ^b   Lam, Tommy Tsan Yuk ^c,q   Cotten, Matthew ^a   Kelly, Michael ^b   Van Reeth, Kristien ^d   Qiu, Yu ^d   Simon, Gaëlle ^e   Bonin, Emilie ^e   Foni, Emanuela ^f   Chiapponi, Chiara ^f   Larsen, Lars ^g   Hjulsager, Charlotte ^g   Markowska Daniel, Iwona ^h   Urbaniak, Kinga ^h   Dürrwald, Ralf ⁱ   Schlegel, Michael ⁱ   Huovilainen, Anita ^j   Davidson, Irit ^k   Dán, Ádám ^l   Loeffen, Willie ^m   Edwards, Stephanie ^a   Bublot, Michel ⁿ   Vila, Thais ⁿ   Maldonado, Jaime ^o   Valls, Laura ^o   Brown, Ian H ^b   Pybus, Oliver G ^c   Kellam, Paul ^a,p   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b VETERINARY LABORATORIES AGENCY   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d GHENT UNIVERSITY   (Belgium)

^e FRENCH AGENCY FOR FOOD   (France)

^f ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA LOMBARDIA E DELL EMILIA ROMAGNA   (Italy)

^g TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^h NATIONAL VETERINARY RESEARCH INSTITUTE   (Poland)

ⁱ IDT Biologika GmbH   (Germany)

^j NATL VET AND FOOD RES INSTITUTE   (Finland)

^k KIMRON VETERINARY INSTITUTE   (Israel)

^l CENTRAL VETERINARY INSTITUTE   (Hungary)

^m WAGENINGEN UNIVERSITY   (Netherlands)

ⁿ BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^o LABORATORIOS HIPRA S A   (Spain)

^p UNIVERSITY COLLEGE LONDON   (United Kingdom)

^q THE UNIVERSITY OF HONG KONG   (Hong Kong)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; GENE FREQUENCY; GENETIC REASSORTMENT; GENETIC VARIABILITY; INFLUENZA A VIRUS (H1N1); MOLECULAR CLOCK; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; PIG; PRIORITY JOURNAL; TREND STUDY; VIRUS GENOME; VIRUS ISOLATION; VIRUS TRANSMISSION; ANIMAL; EPIDEMIOLOGICAL MONITORING; EUROPE; GENETICS; GENOTYPE; HUMAN; INFLUENZA A VIRUS; INFLUENZA A VIRUS (H1N2); INFLUENZA A VIRUS (H3N2); INFLUENZA, HUMAN; ISOLATION AND PURIFICATION; ORTHOMYXOVIRIDAE INFECTIONS; PHYLOGENY; SWINE DISEASES; VETERINARY; VIROLOGY;

ANIMALS; EPIDEMIOLOGICAL MONITORING; EUROPE; EVOLUTION, MOLECULAR; GENOTYPE; HUMANS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H1N2 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; MOLECULAR EPIDEMIOLOGY; ORTHOMYXOVIRIDAE INFECTIONS; PHYLOGENY; REASSORTANT VIRUSES; SUS SCROFA; SWINE; SWINE DISEASES;

EID: 84940991966     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00840-15     Document Type: Article

References (55)

1. Brown I. 2000. The epidemiology and evolution of influenza viruses in pigs. Vet Microbiol 74:29-46. http://dx.doi.org/10.1016/S0378-1135(00)00164-4.
2. Zell R, Scholtissek C, Ludwig S. 2012. Genetics, evolution, and the zoonotic capacity of European swine influenza viruses, p 29-55. In Richt JA, Webby RJ (ed), Swine influenza. Springer, Berlin, Germany.
3. Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG. 2006. Molecular virology: was the 1918 pandemic caused by a bird flu? Was the 1918 flu avian in origin? (Reply.) Nature 440:E9-E10. http://dx.doi.org/10.1038/nature04825.
4. Worobey M, Han G-Z, Rambaut A. 28 April 2014, posting date. Genesis and pathogenesis of the 1918 pandemic H1N1 influenza A virus. Proc Natl Acad Sci U S A http://dx.doi.org/10.1073/pnas.1324197111.
5. Lange J, Groth M, Kanrai P, Pleschka S, Scholtissek C, Dürrwald R, Platzer M, Sauerbrei A, Zell R. 2014. Circulation of classical swine influenza virus in Europe between the wars? Arch Virol 159:1467-1473. http://dx.doi.org/10.1007/s00705-013-1950-x.
6. Dunham EJ, Dugan VG, Kaser EK, Perkins SE, Brown I, Holmes EC, Taubenberger JK. 2009. Different evolutionary trajectories of European avian-like and classical swine H1N1 influenza A viruses. J Virol 83:5485-5494. http://dx.doi.org/10.1128/JVI.02565-08.
7. Bhatt S, Lam TT, Lycett SJ, Leigh Brown AJ, Bowden TA, Holmes EC, Guan Y, Wood JLN, Brown I, Kellam P, Combating Swine Influenza Consortium, Pybus O. 2013. The evolutionary dynamics of influenza A virus adaptation to mammalian hosts. Philos Trans R Soc Lond B Biol Sci 368:20120382. http://dx.doi.org/10.1098/rstb.2012.0382.
8. Pensaert M, Ottis K, Vandeputte J, Kaplan MM, Bachmann PA. 1981. Evidence for the natural transmission of influenzaAvirus from wild ducks to swine and its potential importance for man. Bull World Health Organ 59:75-78.
9. Castrucci MR, Donatelli I, Sidoli L, Barigazzi G, Kawaoka Y, Webster RG. 1993. Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology 193:503-506. http://dx.doi.org/10.1006/viro.1993.1155.
10. Schrader C, Süss J. 2004. Molecular epidemiology of porcine H3N2 influenza A viruses isolated in Germany between 1982 and 2001. Intervirology 47:72-77. http://dx.doi.org/10.1159/000077829.
11. Van Reeth K, Brown I, Dürrwald R, Foni E, Labarque G, Lenihan P, Maldonado J, Markowska Daniel I, Pensaert M, Pospisil Z, Koch G. 2008. Seroprevalence of H1N1, H3N2 and H1N2 influenza viruses in pigs in seven European countries in 2002-2003. Influenza Other Respir Viruses 2:99-105. http://dx.doi.org/10.1111/j.1750-2659.2008.00043.x.
12. Brown I, Harris PA, McCauley JW, Alexander DJ. 1998. Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. J Gen Virol 79(Pt 12):2947-2955.
13. Lam TT, Hon C-C, Wang Z, Hui RK-H, Zeng F, Leung FC-C. 2008. Evolutionary analyses of European H1N2 swine influenza A virus by placing timestamps on the multiple reassortment events. Virus Res 131:271-278. http://dx.doi.org/10.1016/j.virusres.2007.08.012.
14. Smith GJD, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus O, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JSM, Guan Y, Rambaut A. 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459:1122-1125. http://dx.doi.org/10.1038/nature08182.
15. Neumann G, Noda T, Kawaoka Y. 2009. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931-939. http://dx.doi.org/10.1038/nature08157.
16. Guan Y, Poon LLM, Cheung CY, Ellis TM, Lim W, Lipatov AS, Chan KH, Sturm-Ramirez KM, Cheung CL, Leung YHC, Yuen KY, Webster RG, Peiris JSM. 2004. H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci U S A 101:8156-8161. http://dx.doi.org/10.1073/pnas.0402443101.
17. Breiman RF, Nasidi A, Katz MA, Njenga MK, Vertefeuille J. 2007. Preparedness for highly pathogenic avian influenza pandemic in Africa. Emerg Infect Dis 13:1453-1458. http://dx.doi.org/10.3201/eid1310.070400.
18. Deng Y-M, Iannello P, Smith I, Watson J, Barr IG, Daniels P, Komadina N, Harrower B, Wong FYK. 2012. Transmission of influenza A(H1N1) 2009 pandemic viruses in Australian swine. Influenza Other Respir Viruses 6:e42-e47. http://dx.doi.org/10.1111/j.1750-2659.2012.00337.x.
19. Nelson MI, Gramer MR, Vincent AL, Holmes EC. 2012. Global transmission of influenza viruses from humans to swine. J Gen Virol 93:2195-2203. http://dx.doi.org/10.1099/vir.0.044974-0.
20. Nelson MI, Wentworth DE, Culhane MR, Vincent AL, Viboud C, LaPointe MP, Lin X, Holmes EC, Detmer SE. 2014. Introductions and evolution of human-origin seasonal influenza a viruses in multinational swine populations. J Virol 88:10110-10119. http://dx.doi.org/10.1128/JVI.01080-14.
21. Liang H, Lam TT, Fan X, Chen X, Zeng Y, Zhou J, Duan L, Tse M, Chan C-H, Li L, Leung T-Y, Yip C-H, Cheung CL, Zhou B, Smith DK, Poon LL-M, Peiris M, Guan Y, Zhu H. 9 July 2014, posting date. Expansion of genotypic diversity and establishment of 2009 H1N1 pandemic-origin internal genes in pigs in China. J Virol http://dx.doi.org/10.1128/JVI.01327-14.
22. Vijaykrishna D, Smith GJD, Pybus O, Zhu H, Bhatt S, Poon LLM, Riley S, Bahl J, Ma SK, Cheung CL, Perera RAPM, Chen H, Shortridge KF, Webby RJ, Webster RG, Guan Y, Peiris JSM. 2011. Long-term evolution and transmission dynamics of swine influenza A virus. Nature 473:519-522. http://dx.doi.org/10.1038/nature10004.
23. Anderson TK, Nelson MI, Kitikoon P, Swenson SL, Korslund JA, Vincent AL. 2013. Population dynamics of cocirculating swine influenza A viruses in the United States from 2009 to 2012. Influenza Other Respir Viruses 7(Suppl 4):42-51. http://dx.doi.org/10.1111/irv.12193.
24. Nelson MI, Detmer SE, Wentworth DE, Tan Y, Schwartzbard A, Halpin RA, Stockwell T, Lin X, Vincent A, Gramer MR, Holmes EC. 2012. Genomic reassortment of influenza A virus in North American swine, 1998-2011. J Gen Virol http://dx.doi.org/10.1099/vir.0.045930-0.
25. Simon G, Larsen LE, Dürrwald R, Foni E, Harder TC, Van Reeth K, Markowska Daniel I, Reid SM, Dan A, Maldonado J, Huovilainen A, Billinis C, Davidson I, Agüero M, Vila T, Hervé S, Breum SØ, Chiapponi C, Urbaniak K, Kyriakis CS, ESNIP3 consortium, Brown I, Loeffen W. 2014. European surveillance network for influenza in pigs: surveillance programs, diagnostic tools and swine influenza virus subtypes identified in 14 European countries from 2010 to 2013. PLoS One 9:e115815. http://dx.doi.org/10.1371/journal.pone.0115815.
26. Bin Zhou, Donnelly ME, Scholes DT, George KS, Hatta M, Kawaoka Y, Wentworth DE. 15 July 2009. Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and swine origin human influenza A viruses. J Virol http://dx.doi.org/10.1128/JVI.01109-09.
27. Baillie GJ, Galiano M, Agapow PM, Myers R, Chiam R, Gall A, Palser AL, Watson SJ, Hedge J, Underwood A. 2012. Evolutionary dynamics of local pandemic H1N1/2009 influenza virus lineages revealed by wholegenome analysis. J Virol 86:11-18. http://dx.doi.org/10.1128/JVI.05347-11.
28. Quail MA, Kozarewa I, Smith F, Scally A, Stephens PJ, Durbin R, Swerdlow H, Turner DJ. 2008. A large genome center's improvements to the Illumina sequencing system. Nat Methods 5:1005-1010. http://dx.doi.org/10.1038/nmeth.1270.
29. Watson SJ, Welkers MRA, Depledge DP, Coulter E, Breuer JM, de Jong MD, Kellam P. 2013. Viral population analysis and minority-variant detection using short read next-generation sequencing. Philos Trans R Soc Lond B Biol Sci 368:20120205. http://dx.doi.org/10.1098/rstb.2012.0205.
30. Hunt M, Gall A, Ong SH, Brener J, Ferns B, Goulder P, Nastouli E, Keane JA, Kellam P, Otto TD. 28 February 2015, posting date. IVA: accurate de novo assembly of RNA virus genomes. Bioinformatics http://dx.doi.org/10.1093/bioinformatics/btv120.
31. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079. http://dx.doi.org/10.1093/bioinformatics/btp352.
32. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, Ostell J, Lipman D. 17 October 2007. The Influenza Virus Resource at the National Center for Biotechnology Information. http://dx.doi.org/10.1128/JVI.02005-07.
33. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. http://dx.doi.org/10.1093/nar/gkh340.
34. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729. http://dx.doi.org/10.1093/molbev/mst197.
35. Stamatakis A, Ludwig T, Meier H. 2005. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456-463. http://dx.doi.org/10.1093/bioinformatics/bti191.
36. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755. http://dx.doi.org/10.1093/bioinformatics/17.8.754.
37. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. http://dx.doi.org/10.1093/bioinformatics/btg180.
38. Drummond A, Rambaut A. 8 November 2007, posting date. BEAST: Bayesian evolutionary analysis by sampling trees. BMCEvol Biol http://dx.doi.org/10.1186/1471-2148-7-214.
39. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969-1973. http://dx.doi.org/10.1093/molbev/mss075.
40. Minin VN, Bloomquist EW, Suchard MA. 2008. Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol Biol Evol 25:1459-1471. http://dx.doi.org/10.1093/molbev/msn090.
41. Parker J, Rambaut A, Pybus O. 2008. Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol 8:239-246. http://dx.doi.org/10.1016/j.meegid.2007.08.001.
42. Moreno A, Gabanelli E, Sozzi E, Lelli D, Chiapponi C, Ciccozzi M, Zehender G, Cordioli P. 2013. Different evolutionary trends of swine H1N2 influenza viruses in Italy compared to European viruses. Vet Res 44:112. http://dx.doi.org/10.1186/1297-9716-44-112.
43. Welsh MD, Baird PM, Guelbenzu-Gonzalo MP, Hanna A, Reid SM, Essen S, Russell C, Thomas S, Barrass L, McNeilly F, McKillen J, Todd D, Harkin V, McDowell S, Choudhury B, Irvine RM, Borobia J, Grant J, Brown I. 2010. Initial incursion of pandemic (H1N1) 2009 influenza A virus into European pigs. Vet Rec 166:642-645. http://dx.doi.org/10.1136/vr.4851.
44. Wong KK, Greenbaum A, Moll ME, Lando J, Moore EL, Ganatra R, BiggerstaffM, Lam E, Smith EE, Storms AD, Miller JR, Dato V, Nalluswami K, Nambiar A, Silvestri SA, Lute JR, OstroffS, Hancock K, Branch A, Trock SC, Klimov A, Shu B, Brammer L, Epperson S, Finelli L, Jhung MA. 2012. Outbreak of influenza A (H3N2) variant virus infection among attendees of an agricultural fair, Pennsylvania, USA, 2011. Emerging Infect Dis 18:1937-1944. http://dx.doi.org/10.3201/eid1812.121097.
45. Bedford T, Suchard MA, Lemey P, Dudas G, Gregory V, Hay AJ, McCauley JW, Russell CA, Smith DJ, Rambaut A. 2014. Integrating influenza antigenic dynamics with molecular evolution. eLife 3:e01914. http://dx.doi.org/10.7554/eLife.01914.
46. Vijaykrishna D, Holmes EC, Joseph U, Fourment M, Su YCF, Halpin R, Lee RTC, Deng Y-M, Gunalan V, Lin X, Stockwell TB, Fedorova NB, Zhou B, Spirason N, Kühnert D, Boskova V, Stadler T, Costa A-M, Dwyer DE, Huang QS, Jennings LC, Rawlinson W, Sullivan SG, Hurt AC, Maurer-Stroh S, Wentworth DE, Smith GJD, Barr I. 2015. The contrasting phylodynamics of human influenza B viruses. eLife 4:e05055. http://dx.doi.org/10.7554/eLife.05055.
47. Bedford T, Cobey S, Pascual M. 2011. Strength and tempo of selection revealed in viral gene genealogies. BMCEvol Biol 11:220. http://dx.doi.org/10.1186/1471-2148-11-220.
48. Maes D, Deluyker H, Verdonck M, Castryck F, Miry C, Vrijens B, de Kruif A. 2000. Herd factors associated with the seroprevalences of four major respiratory pathogens in slaughter pigs from farrow-to-finish pig herds. Vet Res 31:313-327. http://dx.doi.org/10.1051/vetres:2000122.
49. Starick E, Lange E, Fereidouni S, Bunzenthal C, Höveler R, Kuczka A, Grosse Beilage E, Hamann H-P, Klingelhöfer I, Steinhauer D, Vahlenkamp T, Beer M, Harder TC. 2011. Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J Gen Virol 92:1184-1188. http://dx.doi.org/10.1099/vir.0.028662-0.
50. Lange J, Groth M, Schlegel M, Krumbholz A, Wieczorek K, Ulrich R, Köppen S, Schulz K, Appl D, Selbitz H-J, Sauerbrei A, Platzer M, Zell R, Dürrwald R. 2013. Reassortants of the pandemic (H1N1) 2009 virus and establishment of a novel porcine H1N2 influenza virus, lineage in Germany. Vet Microbiol 167:345-356. http://dx.doi.org/10.1016/j.vetmic.2013.09.024.
51. Howard WA, Essen SC, Strugnell BW, Russell C, Barrass L, Reid SM, Brown I. 2011. Reassortant pandemic (H1N1) 2009 virus in pigs, United Kingdom. Emerg Infect Dis http://dx.doi.org/10.3201/eid/1706.101886.
52. Harder TC, Grosse Beilage E, Lange E, Meiners C, Döhring S, Pesch S, Noé T, Grund C, Beer M, Starick E. 2013. Expanded cocirculation of stable subtypes, emerging lineages, and new sporadic reassortants of porcine influenza viruses in swine populations in northwest Germany. J Virol 87:10460-10476. http://dx.doi.org/10.1128/JVI.00381-13.
53. Mastin A, Alarcon P, Pfeiffer D, Wood J, Williamson S, Brown I, COSI Consortium, Wieland B. 2011. Prevalence and risk factors for swine influenza virus infection in the English pig population. PLoS Curr 3:RRN1209.
54. Kitikoon P, Nelson MI, Killian ML, Anderson TK, Koster L, Culhane MR, Vincent AL. 2013. Genotype patterns of contemporary reassorted H3N2 virus in US swine. J Gen Virol 94:1236-1241. http://dx.doi.org/10.1099/vir.0.051839-0.
55. Lindstrom S, Garten R, Balish A, Shu B, Emery S, Berman L, Barnes N, Sleeman K, Gubareva L, Villanueva J, Klimov A. 2012. Human infections with novel reassortant influenza A(H3N2)v viruses, United States, 2011. Emerg Infect Dis 18:834-837. http://dx.doi.org/10.3201/eid1805.111922.