Reassortants of the pandemic (H1N1) 2009 virus and establishment of a novel porcine H1N2 influenza virus, lineage in Germany

Veterinary Microbiology

Volumn 167, Issue 3-4, 2013, Pages 345-356

  Lange, Jeannette ^a   Groth, Marco ^b   Schlegel, Michael ^c   Krumbholz, Andi ^a,d   Wieczorek, Kerstin ^c   Ulrich, Roswitha ^c   Köppen, Simone ^c   Schulz, Katrin ^c   Appl, Dorit ^c   Selbitz, Hans Joachim ^c   Sauerbrei, Andreas ^a   Platzer, Matthias ^b   Zell, Roland ^a   Dürrwald, Ralf ^c  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b FRITZ LIPMANN INSTITUTE   (Germany)

^c IDT Biologika GmbH   (Germany)

^d UNIVERSITY OF KIEL   (Germany)

Author keywords

Next generation sequencing; Phylogenetic analysis; Reassortant; Serosurvey; Swine influenza A virus; Zoonotic infection

Indexed keywords

ANIMAL TISSUE; ARTICLE; GENOTYPE; GERMANY; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H1N2; NONHUMAN; PHYLOGENY; SEROLOGY; SWINE;

AVES; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE; SUIDAE; SUS; SWINE INFLUENZA VIRUS;

NEXT GENERATION SEQUENCING; PHYLOGENETIC ANALYSIS; REASSORTANT; SEROSURVEY; SWINE INFLUENZA A VIRUS; ZOONOTIC INFECTION;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; GERMANY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H1N2 SUBTYPE; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE INFECTIONS; PHYLOGENY; REASSORTANT VIRUSES; SEROEPIDEMIOLOGIC STUDIES; SWINE; SWINE DISEASES;

EID: 84888044401     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2013.09.024     Document Type: Article

References (43)

1. Ali A., Khatri M., Wang L., Saif Y.M., Lee C.W. Identification of swine H1N2/pandemic H1N1 reassortant influenza virus in pigs, United States. Vet. Microbiol. 2012, 158:60-68.
2. Bachmann P.A. Swine influenza virus. Virus infections of porcines 1989, vol. 2:193-207. Amsterdam, Elsevier. C. Horzinek (Ed.).
3. Bentley D.R., et al. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 2008, 456:53-59.
4. Brookes S.M., Núñez A., Choudhury B., Matrosovich M., Essen S.C., Clifford D., Slomka M.J., Kuntz-Simon G., Garcon F., Nash B., Hanna A., Heegaard P.M., Quéguiner S., Chiapponi C., Bublot M., Garcia J.M., Gardner R., Foni E., Loeffen W., Larsen L., Van Reeth K., Banks J., Irvine R.M., Brown I.H. Replication, pathogenesis and transmission of pandemic (H1N1) 2009 virus in non-immune pigs. PLoS ONE 2010, 5(2):e9068.
5. Centers for Disease Control and Prevention (CDC) Swine influenza A (H1N1) infection in two children - Southern California, March-April 2009. Morb. Mortal Wkly. Rep. 2009, 58:400-402.
6. Centers for Disease Control and Prevention (CDC) Swine-origin influenza A (H3N2) virus infection in two children - Indiana and Pennsylvania, July-August 2011. MMWR Morb. Mortal Wkly. Rep. 2011, 60:1213-1215.
7. Choi Y.K., Pascua P.N.Q., Song M.S. Swine influenza viruses: an Asian perspective. Curr. Top. Microbiol. Immunol. 2013, 370:147-172.
8. Ducatez M.F., Hause B., Stigger-Rosser E., Darnell D., Corzo C., Juleen K., Simonson R., Brockwell-Staats C., Rubrum A., Wang D., Webb A., Crumpton J.C., Lowe J., Gramer M., Webby R.J. Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United states. 2011. Emerg. Inf. Dis. 2011, 17(9):1624-1629.
9. Dürrwald R., Krumbholz A., Baumgarte S., Schlegel M., Vahlenkamp T.W., Selbitz H.J., Wutzler P., Zell R. Swine influenza A vaccines, pandemic (H1N1) 2009 virus, and cross-reactivity. Emerg. Inf. Dis. 2010, 16(6):1029-1030.
10. Fan X., Zhu H., Zhou B., Smith D.K., Chen X., Lam T.T., Poon L.L., Peiris M., Guan Y. Emergence and dissemination of a swine H3N2 reassortant influenza virus with 2009 pandemic H1N1 genes in pigs in China. J. Virol. 2012, 86(4):2375-2378.
11. Fouchier R.A.M., Bestebroer T.M., Herfst S., Van der Kemp L., Rimmelzwaan G.F., Osterhaus A.D.M.E. Detection of influenza A viruses from different species by PCR amplification of conserved sequences in the matrix gene. J. Clin. Microbiol. 2000, 38(11):4096-4101.
12. Garten R.J., Davis C.T., Russell C.A., Shu B., Lindstrom S., Balish A., Sessions W.M., Xu X., Skepner E., Deyde V., Okomo-Adhiambo M., Gubareva L., Barnes J., Smith C.B., Emery S.L., Hillman M.J., Rivailler P., Smagala J., de Graaf M., Burke D.F., Foucher R.A.M., Pappas C., Alpuche-Aranda C.M., Lopez-Gatell H., Olivera H., Lopez I., Myers C.A., Faix D., Blair P.J., Yu C., Keene K.M., Dotson P.D., Boxrud D., Sambol A.R., Abid S.H., St George K., Bannerman T., Moore A.L., Stringer D.J., Blevins P., Demmler-Harrison G.J., Ginsberg M., Kriner P., Waterman S., Smole S., Guevara H.F., Belongia E.A., Clark P.A., Beatrice S.T., Donis R., Katz J., Finelli L., Bridges C.B., Shaw M., Jernigan D.B., Uyeki T.M., Smith D.J., Klimov A.I., Cox N. Antigenic and genetic characterization of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009, 325:197-201.
13. Han J.Y., Park S.J., Kim H.K., Rho S., Nguyen G.V., Song D., Kang B.K., Moon H.J., Park B.K. Identification of reassortant pandemic H1N1 influenza virus in Korean pigs. J. Microbiol. Biotechnol. 2012, 22(5):699-707.
14. Hofshagen M., Gjerset B., Er C., Tarpai A., Brun E., Dannevig B., Bruheim T., Fostad I.G., Iversen B., Hungnes O., Lium B. Pandemic influenza A(H1N1)v: human to pig transmission in Norway?. Eurosurveillance 2009, 14. pii=19406.
15. Howard W.A., Essen S.C., Strugnell B.W., Russell C., Barass L., Reid S.M., Brown I.H. Reassortant Pandemic (H1N1) 2009 virus in pigs, United Kingdom. Emerg. Infect. Dis. 2011, 17(6):1049-1052.
16. Howden K.J., Brockhoff E.J., Caya F.D., McLeod L.J., Lavoie M., Ing J.D., Bystrom J.M., Alexandersen S., Pasick J.M., Berhane Y., Morrison M.E., Keenliside J.M., Laurendeau S., Rohonczy E.B. An investigation into human pandemic influenza virus (H1N1) 2009 on an Alberta swine farm. Can. Vet. J. 2009, 50:1153-1161.
17. Itoh Y., Shinya K., Kiso M., Watanabe T., Sakoda Y., Hatta M., Muramoto Y., Tamura D., Sakai-Tagawa Y., Noda T., Sakabe S., Imai M., Hatta Y., Watanabe S., Li C., Yamada S., Fujii K., Murakami S., Imai H., Kakugawa S., Ito M., Takano R., Iwatsuki-Horimoto K., Shimojima M., Horimoto T., Goto H., Takahashi K., Makino A., Ishigaki H., Nakayama M., Okamatsu M., Takahashi K., Warshauer D., Shult P.A., Saito R., Suzuki H., Furuta Y., Yamashita M., Mitamura K., Nakano K., Nakamura M., Brockman-Schneider R., Mitamura K., Yamazaki M., Sugaya N., Suresh M., Ozawa M., Neumann G., Gern J., Kida H., Ogasawara K., Kawaoka Y. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 2009, 460(August):1021-1027.
18. Lange E., Kalthoff D., Blohm U., Teifke J.P., Breithaupt A., Maresch C., Starick E., Fereidouni S., Hoffmann B., Mettenleiter T.C., Beer M., Vahlenkamp T.W. Pathogenesis and transmission of the novel swine-origin influenza virus A/H1N1 after experimental infection of pigs. J. Gen. Virol. 2009, 90:2119-2123.
19. Lee M.-S., Chang P.-C., Shien J.-H., Cheng M.-C., Shieh H.K. Identification and subtyping of avian influenza viruses by reverse transcription PCR. J. Virol. Methods 2001, 97:13-22.
20. Liu Q., Ma J., Liu H., Qi W., Anderson J., Henry S.C., Hesse R.A., Richt J.A., Ma W. Emergence of novel reassortant H3N2 swine influenza viruses with the 2009 pandemic H1N1 genes in the United States. Arch. Virol. 2012, 157(3):555-562.
21. Lorusso A., Vincent A.L., Gramer M.R., Lager K.M., Ciacci-Zanella J.R. Contemporary epidemiology of North American lineage triple reassortant influenza A viruses in pigs. Curr. Top. Microbiol. Immunol. 2013, 370:113-132.
22. Moreno A., Di Trani L., Alborali L., Vaccari G., Barbieri I., Falcone E., Sozzi E., Puzelli S., Ferri G., Cordioli P. First pandemic H1N1 outbreak from a pig farm in Italy. Open Virol. J. 2010, 4:52-56.
23. Moreno A., Di Trani L., Faccini S., Vaccari G., Nigrelli D., Boniotti M.B., Falcone E., Boni A., Chiapponi C., Sozzi E., Cordioli P. Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus?. Vet. Microbiol. 2011, 149(3-4):472-477.
24. Ning Z., Cox A.J., Mullikin J.C. SSAHA: a fast search method for large DNA databases. Genome Res. 2001, 11:1725-1729.
25. Pascua P.N.Q., Song M.S., Lee J.H., Park K.J., Kwon H.I., Baek Y.H., Hong S.P., Rho J.B., Kim C.J., Poo H., Ryoo T.S., Sung M.H., Choi Y.K. Evaluation of the efficacy and cross-protectivity of recent human and swine vaccines against the pandemic (H1N1) 2009 virus infection. PLoS ONE 2009, 4:e8431.
26. Pasma T., Joseph T. Pandemic (H1N1) 2009 infection in swine herds, Manitoba, Canada. Emerg. Infect. Dis. 2010, 16:706-708.
27. Pereda A., Cappuccio J., Quiroga M.A., Baumeister E., Insarralde L., Ibar M., Sanguinetti R., Cannilla M.L., Franzese D., Escobar Cabrera O.E., Craig M.I., Rimondi A., Machuaca M., Debenedetti R.T., Zenobi C., Barral L., Balzano R., Capalbo S., Risso A., Perfumo C.J. Pandemic (H1N1) 2009 outbreak on pig farm, Argentina. Emerg. Infect. Dis. 2010, 16:304-307.
28. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
29. Scholtissek C., Bürger H., Kistner O., Shortridge K.F. The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 1985, 147:287-294.
30. Smith G.J.D., Vijaykrishna D., Bahl J., Lycett S.J., Worobey M., Pybus O.G., Ma S.K., Cheung C.L., Raghwani J., Bhatt S., Peiris J.S.M., Guan Y., Rambaut A. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 2009, 459:1122-1125.
31. Song M.S., Lee J.H., Pascua P.N., Baek Y.H., Kwon H.I., Park K.J., Choi H.W., Shin Y.K., Song J.Y., Kim C.J., Choi Y.K. Evidence of human-to-swine transmission of the pandemic (H1N1) 2009 influenza virus in South Korea. J. Clin. Microbiol. 2010, 48:3204-3211.
32. 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 T. Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J. Gen. Virol. 2011, 92:1184-1188.
33. Starick E., Lange E., Grund C., grosse Beilage E., Döhring S., Maas A., Noé T., Beer M., Harder T.C. Reassortants of pandemic influenza A virus H1N1/2009 and endemic porcine HxN2 viruses emerge in swine population in Germany. J. Gen. Virol. 2012, 93:1658-1663.
34. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28(10):2731-2739.
35. Tong X., Li Y., Rivailler P., Conrardy C., Alvarez Castillo D.A., Chen L.M., Recuenco S., Ellison J.A., Davis C.T., York I.A., Turmelle A.S., Moran D., Rogers S., Shi M., Tao Y., Weil M.R., Tang K., Rowe L.A., Sammons S., Xu X., Frace M., Lindblade K.A., Cox N.J., Anderson L.J., Rupprecht C.E., Donis R.O. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:4269-4274.
36. Van Reeth K., Brown I.H., Dürrwald R., Foni E., Labarque G., Lenihan P., Maldonado J., Markowska-Daniel I., Pensaert M., Pospisil Z., Koch G. Seroprevalence of H1N1, H3N2 and H1N2 influenza viruses in pigs in seven European countries in 2002-2003. Influenza Other Respi. Viruses 2008, 2:99-105.
37. Vijaykrishna D., Poon L.L.M., Zhu H.C., Ma S.K., Li O.T.W., Cheung C.L., Smith G.J.D., Peiris J.S.M., Guan Y. Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 2010, 328:1529.
38. Weingartl H.M. Did the 2009 pandemic influenza virus originate in humans. Future Microbiol. 2010, 5(7):989-991.
39. Weingartl H.M., Berhane Y., Hisanage T., Neufeld J., Kehler H., Emburry-Hyatt C., Hooper-McGreevy K., Kasloff S., Dalman B., Bystrom J., Alexandersen S., Li Y., Pasick J. Genetic and pathobiologic characterization of pandemic H1N1 2009 influenza viruses from a naturally infected swine herd. J. Virol. 2010, 84:2245-2256.
40. Welsh M.D., Baird P.M., Guelbenzu-Gonzalo M.P., Hanna A., Reid S.M., Essen S., Russell C., Thomas S., Barrass L., McNeilly F., McKillen J., Todd D., Harkin V., McDowell S., Choudhury B., Irvine R.M., Borobia J., Grant J., Brown I.H. Initial incursion of pandemic (H1N1) 2009 influenza A virus into European pigs. Vet. Rec. 2010, 166:642-645.
41. Zell R., Motzke S., Krumbholz A., Wutzler P., Herwig V., Dürrwald R. Novel reassortant of swine influenza H1N2 virus in Germany. J. Gen. Virol. 2008, 89:271-276.
42. Zell R., Scholtissek C., Ludwig S. Genetics, evolution, and the zoonotic capacity of European swine influenza viruses. Curr. Top. Microbiol. Immunol. 2013, 370:29-55.
43. Zhu H., Zhou B., Fan X., Lam T.T.Y., Wang J., Chen A., Chen X., Chen H., Webster R.G., Webby R., Peiris J.S.M., Smith D.K., Guan Y. Novel reassortment of Eurasian avian-like and pandemic/2009 influenza viruses in swine: infectious potential for humans. J. Virol. 2011, 85(20):10432-10439.