1887

Abstract

This study investigated the pathogenicity and transmissibility of a reverse-genetics-derived highly pathogenic avian influenza (HPAI) H5N1 lineage influenza A virus that was isolated from a human, A/Iraq/755/06. We also examined surface gene reassortant viruses composed of the haemagglutinin and neuraminidase from A/Iraq/755/06 and the internal genes of a 2009 pandemic H1N1 virus, A/New York/18/2009 (2Iraq/06 : 6NY/09 H5N1), and haemagglutinin and neuraminidase from A/New York/18/2009 with the internal genes of A/Iraq/755/06 (2NY/09 : 6Iraq/06 H1N1). The parental A/Iraq/755/06 caused little to no lesions in swine, limited virus replication was observed in the upper respiratory and lower respiratory tracts and transmission was detected in 3/5 direct-contact pigs based on seroconversion, detection of viral RNA or virus isolation. In contrast, the 2Iraq/06 : 6NY/09 H5N1 reassortant caused mild lung lesions, demonstrated sustained virus replication in the upper and lower respiratory tracts and transmitted to all contacts (5/5). The 2NY/09 : 6Iraq/06 H1N1 reassortant also caused mild lung lesions, there was evidence of virus replication in the upper respiratory and lower respiratory tracts and transmission was detected in all contacts (5/5). These studies indicate that an HPAI-derived H5N1 reassortant with pandemic internal genes may be more successful in sustaining infection in swine and that HPAI-derived internal genes were marginally compatible with pandemic 2009 H1N1 surface genes. Comprehensive surveillance in swine is critical to identify a possible emerging HPAI reassortant in all regions with HPAI in wild birds and poultry and H1N1pdm09 in pigs or other susceptible hosts.

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2017-02-20
2019-09-18
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References

  1. Wallace RG, Hodac H, Lathrop RH, Fitch WM. A statistical phylogeography of influenza A H5N1. Proc Natl Acad Sci USA 2007;104:4473–4478 [CrossRef][PubMed]
    [Google Scholar]
  2. Xu X, Subbarao, Cox NJ, Guo Y. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 1999;261:15–19 [CrossRef][PubMed]
    [Google Scholar]
  3. Kandun IN, Wibisono H, Sedyaningsih ER, Yusharmen, Hadisoedarsuno W et al. Three Indonesian clusters of H5N1 virus infection in 2005. N Engl J Med 2006;355:2186–2194 [CrossRef][PubMed]
    [Google Scholar]
  4. Ungchusak K, Auewarakul P, Dowell SF, Kitphati R, Auwanit W et al. Probable person-to-person transmission of avian influenza A (H5N1). N Engl J Med 2005;352:333–340 [CrossRef][PubMed]
    [Google Scholar]
  5. WHO Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to WHO. 2014; Available fromhttp://www.who.int/influenza/human_animal_interface/EN_GIP_20140124CumulativeNumberH5N1cases.pdf?ua=1
  6. Salzberg SL, Kingsford C, Cattoli G, Spiro DJ, Janies DA et al. Genome analysis linking recent European and African influenza (H5N1) viruses. Emerg Infect Dis 2007;13:713–718 [CrossRef][PubMed]
    [Google Scholar]
  7. Pasick J, Berhane Y, Joseph T, Bowes V, Hisanaga T et al. Reassortant highly pathogenic influenza A H5N2 virus containing gene segments related to Eurasian H5N8 in British Columbia, Canada, 2014. Sci Rep 2015;5:9484 [CrossRef][PubMed]
    [Google Scholar]
  8. Ip HS, Torchetti MK, Crespo R, Kohrs P, Debruyn P et al. Novel Eurasian highly pathogenic avian influenza A H5 viruses in wild birds, Washington, USA, 2014. Emerg Infect Dis 2015;21:886–890 [CrossRef][PubMed]
    [Google Scholar]
  9. Byrd-Leotis L, Liu R, Bradley KC, Lasanajak Y, Cummings SF et al. Shotgun glycomics of pig lung identifies natural endogenous receptors for influenza viruses. Proc Natl Acad Sci USA 2014;111:E2241E2250 [CrossRef][PubMed]
    [Google Scholar]
  10. Connor RJ, Kawaoka Y, Webster RG, Paulson JC. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 1994;205:17–23 [CrossRef][PubMed]
    [Google Scholar]
  11. Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S et al. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 1998;72:7367–7373[PubMed]
    [Google Scholar]
  12. Nicholls JM, Chan RW, Russell RJ, Air GM, Peiris JS. Evolving complexities of influenza virus and its receptors. Trends Microbiol 2008;16:149–157 [CrossRef][PubMed]
    [Google Scholar]
  13. Nelli RK, Kuchipudi SV, White GA, Perez BB, Dunham SP et al. Comparative distribution of human and avian type sialic acid influenza receptors in the pig. BMC Vet Res 2010;6:4 [CrossRef][PubMed]
    [Google Scholar]
  14. Nicholls JM, Bourne AJ, Chen H, Guan Y, Peiris JS. Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses. Respir Res 2007;8:73 [CrossRef][PubMed]
    [Google Scholar]
  15. Shinya K, Ebina M, Yamada S, Ono M, Kasai N et al. Avian flu: influenza virus receptors in the human airway. Nature 2006;440:435–436 [CrossRef][PubMed]
    [Google Scholar]
  16. Yao L, Korteweg C, Hsueh W, Gu J. Avian influenza receptor expression in H5N1-infected and noninfected human tissues. FASEB J 2008;22:733–740 [CrossRef][PubMed]
    [Google Scholar]
  17. van Poucke SG, Nicholls JM, Nauwynck HJ, van Reeth K. Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution. Virol J 2010;7:38 [CrossRef][PubMed]
    [Google Scholar]
  18. Walther T, Karamanska R, Chan RW, Chan MC, Jia N et al. Glycomic analysis of human respiratory tract tissues and correlation with influenza virus infection. PLoS Pathog 2013;9:e1003223 [CrossRef][PubMed]
    [Google Scholar]
  19. Chan RW, Karamanska R, van Poucke S, van Reeth K, Chan IW et al. Infection of swine ex vivo tissues with avian viruses including H7N9 and correlation with glycomic analysis. Influenza Other Respir Viruses 2013;7:1269–1282 [CrossRef][PubMed]
    [Google Scholar]
  20. Suzuki Y, Ito T, Suzuki T, Holland RE, Chambers TM et al. Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 2000;74:11825–11831 [CrossRef][PubMed]
    [Google Scholar]
  21. Sriwilaijaroen N, Kondo S, Yagi H, Takemae N, Saito T et al. N-glycans from porcine trachea and lung: predominant NeuAcα2-6Gal could be a selective pressure for influenza variants in favor of human-type receptor. PLoS One 2011;6:e16302 [CrossRef][PubMed]
    [Google Scholar]
  22. Trebbien R, Larsen LE, Viuff BM. Distribution of sialic acid receptors and influenza A virus of avian and swine origin in experimentally infected pigs. Virol J 2011;8:434 [CrossRef][PubMed]
    [Google Scholar]
  23. Chen LM, Blixt O, Stevens J, Lipatov AS, Davis CT et al. In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity. Virology 2012;422:105–113 [CrossRef][PubMed]
    [Google Scholar]
  24. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 2012;336:1534–1541 [CrossRef][PubMed]
    [Google Scholar]
  25. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012;486:420–428 [CrossRef][PubMed]
    [Google Scholar]
  26. Linster M, van Boheemen S, de Graaf M, Schrauwen EJ, Lexmond P et al. Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus. Cell 2014;157:329–339 [CrossRef][PubMed]
    [Google Scholar]
  27. Zhang Y, Zhang Q, Kong H, Jiang Y, Gao Y et al. H5N1 hybrid viruses bearing 2009/H1N1 virus genes transmit in guinea pigs by respiratory droplet. Science 2013;340:1459–1463 [CrossRef][PubMed]
    [Google Scholar]
  28. Cao N, Zhu W, Chen Y, Tan L, Zhou P et al. Avian influenza A (H5N1) virus antibodies in pigs and residents of swine farms, southern China. J Clin Virol 2013;58:647–651 [CrossRef][PubMed]
    [Google Scholar]
  29. Choi YK, Nguyen TD, Ozaki H, Webby RJ, Puthavathana P et al. Studies of H5N1 influenza virus infection of pigs by using viruses isolated in Vietnam and Thailand in 2004. J Virol 2005;79:10821–10825 [CrossRef][PubMed]
    [Google Scholar]
  30. Nidom CA, Takano R, Yamada S, Sakai-Tagawa Y, Daulay S et al. Influenza A (H5N1) viruses from pigs, Indonesia. Emerg Infect Dis 2010;16:1515–1523 [CrossRef][PubMed]
    [Google Scholar]
  31. Song XH, Xiao H, Huang Y, Fu G, Jiang B et al. Serological surveillance of influenza A virus infection in swine populations in Fujian Province, China: no evidence of naturally occurring H5N1 infection in pigs. Zoonoses Public Health 2010;57:291–298 [CrossRef][PubMed]
    [Google Scholar]
  32. Li X, Jin M, Yu Z, Zhang A, Chen H et al. Pathogenicity of a goose isolate of highly pathogenic H5N1 influenza A virus for chickens, mice, and pigs. Acta Virol 2008;52:41–46[PubMed]
    [Google Scholar]
  33. Lipatov AS, Kwon YK, Sarmento LV, Lager KM, Spackman E et al. Domestic pigs have low susceptibility to H5N1 highly pathogenic avian influenza viruses. PLoS Pathog 2008;4:e1000102. [CrossRef][PubMed]
    [Google Scholar]
  34. Balzli C, Lager K, Vincent A, Gauger P, Brockmeier S et al. Susceptibility of swine to H5 and H7 low pathogenic avian influenza viruses. Influenza Other Respir Viruses 2016;10:346–352 [CrossRef][PubMed]
    [Google Scholar]
  35. de Vleeschauwer A, Atanasova K, van Borm S, van den Berg T, Rasmussen TB et al. Comparative pathogenesis of an avian H5N2 and a swine H1N1 influenza virus in pigs. PLoS One 2009;4:e6662 [CrossRef][PubMed]
    [Google Scholar]
  36. Brockhoff EJ. Clinical presentation and epidemiology of human pandemic influenza virus (H1N1) 2009 on an Alberta swine farm. Adv Pork Prod 2010;21:137–147
    [Google Scholar]
  37. Brookes SM, Irvine RM, Nunez A, Clifford D, Essen S et al. Influenza A (H1N1) infection in pigs. Vet Rec 2009;164:760–761[PubMed][CrossRef]
    [Google Scholar]
  38. Forgie SE, Keenliside J, Wilkinson C, Webby R, Lu P et al. Swine outbreak of pandemic influenza A virus on a Canadian research farm supports human-to-swine transmission. Clin Infect Dis 2011;52:10–18 [CrossRef][PubMed]
    [Google Scholar]
  39. Howden KJ, Brockhoff EJ, Caya FD, Mcleod LJ, Lavoie M et al. An investigation into human pandemic influenza virus (H1N1) 2009 on an Alberta swine farm. Can Vet J 2009;50:1153–1161[PubMed]
    [Google Scholar]
  40. Itoh Y, Shinya K, Kiso M, Watanabe T, Sakoda Y et al. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 2009;460:1021–1025 [CrossRef][PubMed]
    [Google Scholar]
  41. Lange E, Kalthoff D, Blohm U, Teifke JP, Breithaupt A et al. Pathogenesis and transmission of the novel swine-origin influenza virus A/H1N1 after experimental infection of pigs. J Gen Virol 2009;90:2119–2123 [CrossRef][PubMed]
    [Google Scholar]
  42. Pasma T, Joseph T. Pandemic (H1N1) 2009 infection in swine herds, Manitoba, Canada. Emerg Infect Dis 2010;16:706–708 [CrossRef][PubMed]
    [Google Scholar]
  43. Vincent AL, Lager KM, Harland M, Lorusso A, Zanella E et al. Absence of 2009 pandemic H1N1 influenza A virus in fresh pork. PLoS One 2009;4:e8367 [CrossRef][PubMed]
    [Google Scholar]
  44. Keenliside J. Regulatory and industry response to pandemic H1N1 2009 influenza virus in an Alberta Swine Herd. Adv Pork Prod 2010;21:129
    [Google Scholar]
  45. Song MS, Lee JH, Pascua PN, Baek YH, Kwon HI et al. Evidence of human-to-swine transmission of the pandemic (H1N1) 2009 influenza virus in South Korea. J Clin Microbiol 2010;48:3204–3211 [CrossRef][PubMed]
    [Google Scholar]
  46. ProMED-mail Influenza pandemic (H1N1) 2009, animal (04): Global, update. 2010 31 Jan. Contract No.: 20100131.0337.
  47. Nelson MI, Stratton J, Killian ML, Janas-Martindale A, Vincent AL. Continual reintroduction of human pandemic H1N1 influenza A viruses into swine in the United States, 2009 to 2014. J Virol 2015;89:6218–6226 [CrossRef][PubMed]
    [Google Scholar]
  48. Keenliside J. Pandemic influenza A H1N1 in swine and other animals. Curr Top Microbiol Immunol 2013;370:259–271 [CrossRef][PubMed]
    [Google Scholar]
  49. Liang H, Lam TT, Fan X, Chen X, Zeng Y et al. Expansion of genotypic diversity and establishment of 2009 H1N1 pandemic-origin internal genes in pigs in China. J Virol 2014;88:10864–10874 [CrossRef][PubMed]
    [Google Scholar]
  50. Nelson MI, Vincent AL, Kitikoon P, Holmes EC, Gramer MR. Evolution of novel reassortant A/H3N2 influenza viruses in North American swine and humans, 2009-2011. J Virol 2012;86:8872–8878 [CrossRef][PubMed]
    [Google Scholar]
  51. Neumann G. H5N1 influenza virulence, pathogenicity and transmissibility: what do we know?. Future Virol 2015;10:971–980 [CrossRef][PubMed]
    [Google Scholar]
  52. Stevens J, Blixt O, Chen LM, Donis RO, Paulson JC et al. Recent avian H5N1 viruses exhibit increased propensity for acquiring human receptor specificity. J Mol Biol 2008;381:1382–1394 [CrossRef][PubMed]
    [Google Scholar]
  53. Lee JH, Pascua PN, Song MS, Baek YH, Kim CJ et al. Isolation and genetic characterization of H5N2 influenza viruses from pigs in Korea. J Virol 2009;83:4205–4215 [CrossRef][PubMed]
    [Google Scholar]
  54. Alexander DJ. Summary of avian influenza activity in Europe, Asia, Africa, and Australasia, 2002–2006. Avian Dis 2007;51:161–166 [CrossRef][PubMed]
    [Google Scholar]
  55. Brown IH. Summary of avian influenza activity in Europe, Asia, and Africa, 2006–2009. Avian Dis 2010;54:187–193 [CrossRef][PubMed]
    [Google Scholar]
  56. Capua I, Alexander DJ. Animal and human health implications of avian influenza infections. Biosci Rep 2007;27:359–372 [CrossRef][PubMed]
    [Google Scholar]
  57. Lebarbenchon C, Stallknecht DE. Host shifts and molecular evolution of H7 avian influenza virus hemagglutinin. Virol J 2011;8:328 [CrossRef][PubMed]
    [Google Scholar]
  58. Röhm C, Horimoto T, Kawaoka Y, Süss J, Webster RG. Do hemagglutinin genes of highly pathogenic avian influenza viruses constitute unique phylogenetic lineages?. Virology 1995;209:664–670 [CrossRef][PubMed]
    [Google Scholar]
  59. Smith GJ, Donis RO.World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization (WHO/OIE/FAO) H5 Evolution Working Group Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013-2014. Influenza Other Respir Viruses 2015;9:271–276 [CrossRef][PubMed]
    [Google Scholar]
  60. Vijaykrishna D, Bahl J, Riley S, Duan L, Zhang JX et al. Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. PLoS Pathog 2008;4:e1000161 [CrossRef][PubMed]
    [Google Scholar]
  61. Bragstad K, Jørgensen PH, Handberg K, Hammer AS, Kabell S et al. First introduction of highly pathogenic H5N1 avian influenza A viruses in wild and domestic birds in Denmark, Northern Europe. Virol J 2007;4:43 [CrossRef][PubMed]
    [Google Scholar]
  62. Chen H, Smith GJ, Li KS, Wang J, Fan XH et al. Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc Natl Acad Sci USA 2006;103:2845–2850 [CrossRef][PubMed]
    [Google Scholar]
  63. Chen H, Smith GJ, Zhang SY, Qin K, Wang J et al. Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 2005;436:191–192 [CrossRef][PubMed]
    [Google Scholar]
  64. Ducatez MF, Olinger CM, Owoade AA, de Landtsheer S, Ammerlaan W et al. Avian flu: multiple introductions of H5N1 in Nigeria. Nature 2006;442:37 [CrossRef][PubMed]
    [Google Scholar]
  65. Li KS, Guan Y, Wang J, Smith GJ, Xu KM et al. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 2004;430:209–213 [CrossRef][PubMed]
    [Google Scholar]
  66. Dung Nguyen T, Vinh Nguyen T, Vijaykrishna D, Webster RG, Guan Y et al. Multiple sublineages of influenza A virus (H5N1), Vietnam, 2005-2007. Emerg Infect Dis 2008;14:632–636 [CrossRef][PubMed]
    [Google Scholar]
  67. Krauss S, Stallknecht DE, Slemons RD, Bowman AS, Poulson RL et al. The enigma of the apparent disappearance of Eurasian highly pathogenic H5 clade 2.3.4.4 influenza A viruses in North American waterfowl. Proc Natl Acad Sci USA 2016;113:9033–9038 [CrossRef][PubMed]
    [Google Scholar]
  68. Bevins SN, Dusek RJ, White CL, Gidlewski T, Bodenstein B et al. Widespread detection of highly pathogenic H5 influenza viruses in wild birds from the Pacific Flyway of the United States. Sci Rep 2016;6:28980 [CrossRef][PubMed]
    [Google Scholar]
  69. Nelson MI, Lemey P, Tan Y, Vincent A, Lam TT et al. Spatial dynamics of human-origin H1 influenza A virus in North American swine. PLoS Pathog 2011;7:e1002077 [CrossRef][PubMed]
    [Google Scholar]
  70. Nelson MI, Vincent AL. Reverse zoonosis of influenza to swine: new perspectives on the human–animal interface. Trends Microbiol 2015;23:142–153 [CrossRef][PubMed]
    [Google Scholar]
  71. Nelson MI, Wentworth DE, Culhane MR, Vincent AL, Viboud C et al. Introductions and evolution of human-origin seasonal influenza a viruses in multinational swine populations. J Virol 2014;88:10110–10119 [CrossRef][PubMed]
    [Google Scholar]
  72. Watson SJ, Langat P, Reid SM, Lam TT, Cotten M et al. Molecular epidemiology and evolution of influenza viruses circulating within European Swine between 2009 and 2013. J Virol 2015;89:9920–9931 [CrossRef][PubMed]
    [Google Scholar]
  73. Nelson MI, Viboud C, Vincent AL, Culhane MR, Detmer SE et al. Global migration of influenza A viruses in swine. Nat Commun 2015;6:6696 [CrossRef][PubMed]
    [Google Scholar]
  74. Nelson MI, Detmer SE, Wentworth DE, Tan Y, Schwartzbard A et al. Genomic reassortment of influenza A virus in North American swine, 1998-2011. J Gen Virol 2012;93:2584–2589 [CrossRef][PubMed]
    [Google Scholar]
  75. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA et al. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol 2007;171:1215–1223 [CrossRef][PubMed]
    [Google Scholar]
  76. Short KR, Richard M, Verhagen JH, van Riel D, Schrauwen EJ et al. One health, multiple challenges: the inter-species transmission of influenza A virus. One Health 2015;1:1–13 [CrossRef][PubMed]
    [Google Scholar]
  77. Jackson S, van Hoeven N, Chen LM, Maines TR, Cox NJ et al. Reassortment between avian H5N1 and human H3N2 influenza viruses in ferrets: a public health risk assessment. J Virol 2009;83:8131–8140 [CrossRef][PubMed]
    [Google Scholar]
  78. Kimble JB, Sorrell E, Shao H, Martin PL, Perez DR. Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proc Natl Acad Sci USA 2011;108:12084–12088 [CrossRef][PubMed]
    [Google Scholar]
  79. Li C, Hatta M, Nidom CA, Muramoto Y, Watanabe S et al. Reassortment between avian H5N1 and human H3N2 influenza viruses creates hybrid viruses with substantial virulence. Proc Natl Acad Sci USA 2010;107:4687–4692 [CrossRef][PubMed]
    [Google Scholar]
  80. Chen LM, Davis CT, Zhou H, Cox NJ, Donis RO. Genetic compatibility and virulence of reassortants derived from contemporary avian H5N1 and human H3N2 influenza A viruses. PLoS Pathog 2008;4:e1000072 [CrossRef][PubMed]
    [Google Scholar]
  81. Cline TD, Karlsson EA, Freiden P, Seufzer BJ, Rehg JE et al. Increased pathogenicity of a reassortant 2009 pandemic H1N1 influenza virus containing an H5N1 hemagglutinin. J Virol 2011;85:12262–12270 [CrossRef][PubMed]
    [Google Scholar]
  82. Octaviani CP, Ozawa M, Yamada S, Goto H, Kawaoka Y. High level of genetic compatibility between swine-origin H1N1 and highly pathogenic avian H5N1 influenza viruses. J Virol 2010;84:10918–10922 [CrossRef][PubMed]
    [Google Scholar]
  83. Song MS, Pascua PN, Lee JH, Baek YH, Park KJ et al. Virulence and genetic compatibility of polymerase reassortant viruses derived from the pandemic (H1N1) 2009 influenza virus and circulating influenza A viruses. J Virol 2011;85:6275–6286 [CrossRef][PubMed]
    [Google Scholar]
  84. Schrauwen EJ, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, Fouchier RA et al. Reassortment between Avian H5N1 and human influenza viruses is mainly restricted to the matrix and neuraminidase gene segments. PLoS One 2013;8:e59889 [CrossRef][PubMed]
    [Google Scholar]
  85. Lu L, Lycett SJ, Leigh Brown AJ. Reassortment patterns of avian influenza virus internal segments among different subtypes. BMC Evol Biol 2014;14:16 [CrossRef][PubMed]
    [Google Scholar]
  86. Duan L, Campitelli L, Fan XH, Leung YH, Vijaykrishna D et al. Characterization of low-pathogenic H5 subtype influenza viruses from Eurasia: implications for the origin of highly pathogenic H5N1 viruses. J Virol 2007;81:7529–7539 [CrossRef][PubMed]
    [Google Scholar]
  87. Guan Y, Peiris M, Kong KF, Dyrting KC, Ellis TM et al. H5N1 influenza viruses isolated from geese in Southeastern China: evidence for genetic reassortment and interspecies transmission to ducks. Virology 2002;292:16–23 [CrossRef][PubMed]
    [Google Scholar]
  88. Neumann G, Fujii K, Kino Y, Kawaoka Y. An improved reverse genetics system for influenza A virus generation and its implications for vaccine production. Proc Natl Acad Sci USA 2005;102:16825–16829 [CrossRef][PubMed]
    [Google Scholar]
  89. Neumann G, Kawaoka Y. Reverse genetics systems for the generation of segmented negative-sense RNA viruses entirely from cloned cDNA. Curr Top Microbiol Immunol 2004;283:43–60[PubMed]
    [Google Scholar]
  90. Jin H, Urabe M, Tobita K. A variant of MDCK cell line which restricted growth of influenza viruses mainly through suppression of viral primary transcription. Arch Virol 1996;141:923–933 [CrossRef][PubMed]
    [Google Scholar]
  91. Richmond JY, Nesby-O'Dell SL. Laboratory security and emergency response guidance for laboratories working with select agents. Centers for Disease Control and Prevention. MMWR 2002;RR-19:1–6
    [Google Scholar]
  92. Kitikoon P, Nilubol D, Erickson BJ, Janke BH, Hoover TC et al. The immune response and maternal antibody interference to a heterologous H1N1 swine influenza virus infection following vaccination. Vet Immunol Immunopathol 2006;112:117–128 [CrossRef][PubMed]
    [Google Scholar]
  93. Spackman E, Suarez DL. Type A influenza virus detection and quantitation by real-time RT-PCR. Methods Mol Biol 2008;436:19–26 [CrossRef][PubMed]
    [Google Scholar]
  94. Gauger PC, Vincent AL, Loving CL, Henningson JN, Lager KM et al. Kinetics of lung lesion development and pro-inflammatory cytokine response in pigs with vaccine-associated enhanced respiratory disease induced by challenge with pandemic (2009) A/H1N1 influenza virus. Vet Pathol 2012;49:900–912 [CrossRef][PubMed]
    [Google Scholar]
  95. Halbur PG, Paul PS, Frey ML, Landgraf J, Eernisse K et al. Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol 1995;32:648–660[PubMed][CrossRef]
    [Google Scholar]
  96. Khurana S, Loving CL, Manischewitz J, King LR, Gauger PC et al. Vaccine-induced anti-HA2 antibodies promote virus fusion and enhance influenza virus respiratory disease. Sci Transl Med 2013;5:200ra114 [CrossRef][PubMed]
    [Google Scholar]
  97. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  98. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312–1313 [CrossRef][PubMed]
    [Google Scholar]
  99. Pattengale ND, Alipour M, Bininda-Emonds OR, Moret BM, Stamatakis A. How many bootstrap replicates are necessary?. J Comput Biol 2010;17:337–354 [CrossRef][PubMed]
    [Google Scholar]
  100. Burke DF, Smith DJ. A recommended numbering scheme for influenza A HA subtypes. PLoS One 2014;9:e112302 [CrossRef][PubMed]
    [Google Scholar]
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