Expanded cocirculation of stable subtypes, emerging lineages, and new sporadic reassortants of porcine influenza viruses in swine populations in Northwest Germany

Journal of Virology

Volumn 87, Issue 19, 2013, Pages 10460-10476

  Harder, Timm C ^a   Grosse Beilage, Elisabeth ^b   Lange, Elke ^c   Meiners, Carolin ^b   Döhring, Stefanie ^b   Pesch, Stefan ^d   Noé, Thomas ^d   Grund, Christian ^a   Beer, Martin ^a   Starick, Elke ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^c Institute of Infectology   (Germany)

^d Vaxxinova GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS HEMAGGLUTININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; FEMALE; GENETIC REASSORTMENT; GERMANY; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H1N2; INFLUENZA VIRUS A H3N2; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; POPULATION DENSITY; PRIORITY JOURNAL; SPECIES DIVERSITY; SWINE INFLUENZA; UNINDEXED SEQUENCE; VIRUS DETECTION; VIRUS GENOME; VIRUS TRANSMISSION;

ANIMALS; CELL LINEAGE; GERMANY; INFLUENZA A VIRUS, H1N2 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; LUNG; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; PHYLOGENY; RESPIRATORY DISTRESS SYNDROME, ADULT; RNA, VIRAL; SWINE; SWINE DISEASES;

EID: 84885994732     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00381-13     Document Type: Article

References (63)

1. Olsen CW, Brown IH, Easterday BC, van Reeth K. 2006. Swine influenza, p 469-482. In Straw BE, Zimmerman JJ, D'Allaire S, Taylor DJ (ed), Diseases of swine, 9th ed. Blackwell Publishing, Oxford, United Kingdom.
2. Thacker E, Janke B. 2008. Swine influenza virus: zoonotic potential and vaccination strategies for the control of avian and swine influenzas. J. Infect. Dis. 197(Suppl 1):S19-S24.
3. Torremorell M, Allerson M, Corzo C, Diaz A, Gramer M. 9 January 2012. Transmission of influenza A virus in pigs. Transbound. Emerg. Dis. [Epub ahead of print.] doi:10.1111/j.1865-1682.2011.01300.x.
4. Irvine RM, Brown IH. 2009. Novel H1N1 influenza in people: global spread from an animal source? Vet. Rec. 164:577-578.
5. Brown IH. 2013. History and epidemiology of swine influenza in Europe. Curr. Top. Microbiol. Immunol. 370:133-146.
6. Van Reeth K, Brown IH, 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 Respi. Viruses 2:99-105.
7. Kuntz-Simon G, Madec F. 2009. Genetic and antigenic evolution of swine influenza viruses in Europe and evaluation of their zoonotic potential. Zoonoses Public Health 56:310-325.
8. Brockwell-Staats C, Webster RG, Webby RJ. 2009. Diversity of influenza viruses in swine and the emergence of a novel human pandemic influenza A (H1N1). Influenza Other Respi. Viruses 3:207-213.
9. Starick E, Lange E, Fereidouni S, Bunzenthal C, Höveler C, Kuczka A, Grosse Beilage E, Hamann HP. 2011. Re-assorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J. Gen. Virol. 92:1184-1188.
10. Starick E, Lange E, Grund C, Grosse Beilage E, Döhring S, Maas A, Noé T, Beer M, Harder TC. 2012. Reassortants of pandemic influenza A virus H1N1/2009 and endemic porcine HxN2 viruses emerge in swine populations in Germany. J. Gen. Virol. 93:1658-1663.
11. Kitikoon P, Vincent AL, Jones KR, Nilubol D, Yu S, Janke BH, Thacker BJ, Thacker EL. 2009. Vaccine efficacy and immune response to swine influenza virus challenge in pigs infected with porcine reproductive and respiratory syndrome virus at the time of SIV vaccination. Vet. Microbiol. 139:235-244.
12. Loeffen WL, Heinen PP, Bianchi AT, Hunneman WA, Verheijden JH. 2003. Effect of maternally derived antibodies on the clinical signs and immune response in pigs after primary and secondary infection with an influenza H1N1 virus. Vet. Immunol. Immunopathol. 92:23-35.
13. Vijaykrishna D, Smith GJ, Pybus OG, Zhu H, Bhatt S, Poon LL, Riley S, Bahl J, Ma SK, Cheung CL, Perera RA, Chen H, Shortridge KF, Webby RJ, Webster RG, Guan Y, Peiris JS. 2011. Long-term evolution and transmission dynamics of swine influenza A virus. Nature 473:519-522.
14. Fereidouni SR, Harder TC, Gaidet N, Ziller M, Hoffmann B, Hammoumi S, Globig A, Starick E. 2012. Saving resources: avian influenza surveillance using pooled swab samples and reduced reaction volumes in real-time RT-PCR. J. Virol. Methods 186:119-125.
15. Hoffmann B, Depner K, Schirrmeier H, Beer M. 2006. A universal heterologous internal control system for duplex real-time RT-PCR assays used in a detection system for pestiviruses. J. Virol. Methods 136:200-209.
16. Gall A, Hoffmann B, Harder T, Grund C, Beer M. 2008. Universal primer set for amplification and sequencing of HA0 cleavage sites of all influenza A viruses. J. Clin. Microbiol. 46:2561-2567.
17. Gall A, Hoffmann B, Harder T, Grund C, Ehricht R, Beer M. 2009. Rapid and highly sensitive neuraminidase subtyping of avian influenza viruses by use of a diagnostic DNA microarray. J. Clin. Microbiol. 47: 2985-2988.
18. Lange E, Kalthoff D, Blohm U, Teifke JP, Breithaupt A, Maresch C, Starick E, Fereidouni S, Hoffmann B, Mettenleiter TC, Beer M, Vahlenkamp TW. 2009. Pathogenesis and transmission of the novel swineorigin influenza virus A/H1N1 after experimental infection of pigs. J. Gen. Virol. 90:2119-2123.
19. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. 2001. Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 146:2275-2289.
20. Li OT, Barr I, Leung CY, Chen H, Guan Y, Peiris JS, Poon LL. 2007. Reliable universal RT-PCR assays for studying influenza polymerase subunit gene sequences from all 16 haemagglutinin subtypes. J. Virol. Methods 142:218-222.
21. Katoh K, Asimenos G, Toh H. 2009. Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 537:39-64.
22. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. 2009. Jalview version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191.
23. Posada D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256.
24. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307-321.
25. Smith GJD, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, 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.
26. Seo J, Gordish-Dressman H, Hoffman EP. 2006. An interactive power analysis tool for microarray hypothesis testing and generation. Bioinformatics 22:808-814.
27. Lai AC, Wu WL, Lau SY, Guan Y, Chen H. 2012. Two-dimensional antigenic dendrogram and phylogenetic tree of avian influenza virus H5N1. FEMS Immunol. Med. Microbiol. 64:205-211.
28. Whitley RJ, Boucher CA, Lina B, Nguyen-Van-Tam J, Osterhaus A, Schutten M, Monto AS. 2013. Global assessment of resistance to neuraminidase inhibitors, 2008-2011: the Influenza Resistance Information Study (IRIS). Clin. Infect. Dis. 56:1197-1205.
29. Lu G, Rowley T, Garten R, Donis RO. 2007. FluGenome: a web tool for genotyping influenza A virus. Nucleic Acids Res. 35(Web Server issue): W275-W279.
30. Dunham EJ, Dugan VG, Kaser EK, Perkins SE, Brown IH, Holmes EC, Taubenberger JK. 2009. Different evolutionary trajectories of European avian H1N1-like and classical swine H1N1 influenza A viruses. J. Virol. 83:5485-5494.
31. Krumbholz A, Philipps A, Oehring H, Schwarzer K, Eitner A, Wutzler P, Zell R. 2011. Current knowledge on PB1-F2 of influenza A viruses. Med. Microbiol. Immunol. 200:69-75.
32. Conenello GM, Zamarin D, Perrone LA, Tumpey T, Palese P. 2007. A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog. 3:1414-1421.
33. Jagger BW, Wise HM, Kash JC, Walters KA, Wills NM, Xiao YL, Dunfee RL, Schwartzman LM, Ozinsky A, Bell GL, Dalton RM, Efstathiou S, Atkins JF, Firth AE, Taubenberger JK, Digard P. 2012. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337:199-204.
34. Shi M, Jagger BW, Wise HM, Digard P, Holmes EC, Taubenberger JK. 2012. Evolutionary conservation of the PA-X open reading frame in segment 3 of influenza A virus. J. Virol. 86:12411-12413.
35. Moreno A, Chiapponi C, Boniotti MB, Sozzi E, Foni E, Barbieri I, Zanoni MG, Faccini S, Lelli D, Cordioli P. 2012. Genomic characterization of H1N2 swine influenza viruses in Italy. Vet. Microbiol. 156:265-276.
36. Obenauer JC, Denson J, Mehta PK, Su X, Mukatira S, Finkelstein DB, Xu X, Wang J, Ma J, Fan Y, Rakestraw KM, Webster RG, Hoffmann E, Kraus S, Zheng J, Zhang Z, Naeve CW. 2006. Large-scale sequence analysis of avian influenza isolates. Science 311:1576-1580.
37. Krumbholz A, Schmidtke M, Bergmann S, Motzke S, Bauer K, Stech J, Dürrwald R, Wutzler P, Zell R. 2009. High prevalence of amantadine resistance among circulating European porcine influenza A viruses. J. Gen. Virol. 90:900-908.
38. Wiley DC, Wilson IA, Shekel JJ. 1981. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289:373-378.
39. Takemae N, Parchariyanon S, Ruttanapumma R, Hiromoto Y, Hayashi T, Uchida Y, Saito T. 2011. Swine influenza virus infection in different age groups of pigs in farrow-to-finish farms in Thailand. Virol. J. 8:537. doi:10.1186/1743-422X-8-537.
40. Williamson SM, Tucker AW, McCrone IS, Bidewell CA, Brons N, Habernoll H, Essen SC, Brown IH, COSI, Wood JL. 2012. Descriptive clinical and epidemiological characteristics of influenza A H1N1 2009 virus infections in pigs in England. Vet. Rec. 171:271. doi:10.1136/vr .100673.
41. Fablet C, Marois C, Kuntz-Simon G, Rose N, Dorenlor V, Eono F, Eveno E, Jolly JP, Le Devendec L, Tocqueville V, Quéguiner S, Gorin S, Kobisch M, Madec F. 2011. Longitudinal study of respiratory infection patterns of breeding sows in five farrow-to-finish herds. Vet. Microbiol. 147:329-339.
42. Madec F, Kaiser C, Gourreau JM, Martinat-Botte F. 1989. Pathologic consequences of a severe influenza outbreak (swine virus A/H1N1) under natural conditions in the non-immune sow at the beginning of pregnancy. Comp. Immunol. Microbiol. Infect. Dis. 12:17-27. (In French.)
43. Wesley RD. 2004. Exposure of sero-positive gilts to swine influenza virus may cause a few stillbirths per litter. Can. J. Vet. Res. 68:215-217.
44. Opriessnig T, Giménez-Lirola LG, Halbur PG. 2011. Polymicrobial respiratory disease in pigs. Anim. Health Res. Rev. 12:133-148.
45. Ellis J, Clark E, Haines D, West K, Krakowka S, Kennedy S, Allan GM. 2004. Porcine circovirus-2 and concurrent infections in the field. Vet. Microbiol. 98:159-163.
46. Jung K, Renukaradhya GJ, Alekseev KP, Fang Y, Tang Y, Saif LJ. 2009. Porcine reproductive and respiratory syndrome virus modifies innate immunity and alters disease outcome in pigs subsequently infected with porcine respiratory coronavirus: implications for respiratory viral coinfections. J. Gen. Virol. 90:2713-2723.
47. Wellenberg GJ, Bouwkamp FT, Wolf PJ, Swart WA, Mombarg MJ, de Gee AL. 2010. A study on the severity and relevance of porcine circovirus type 2 infections in Dutch fattening pigs with respiratory diseases. Vet. Microbiol. 142:217-224.
48. Deblanc C, Robert F, Pinard T, Gorin S, Quéguiner S, Gautier-Bouchardon AV, Ferré S, Garraud JM, Cariolet R, Brack M, Simon G. 29 November 2012, posting date. Pre-infection of pigs with Mycoplasma hyopneumoniae induces oxidative stress that influences outcomes of a subsequent infection with a swine influenza virus of H1N1 subtype. Vet. Microbiol. doi:10.1016/j.vetmic.2012.11.028.
49. Kyriakis CS, Brown IH, Foni E, Kuntz-Simon G, Maldonado L, Madec F, Essen SC, Chiapponi C, Van Reeth K. 2011. Virological surveillance and preliminary antigenic characterization of influenza viruses in pigs in five European countries from 2006 to 2008. Zoonoses Public Health 58: 93-101.
50. Kyriakis CS, Rose N, Foni E, Maldonado J, Loeffen WLA, Madec F, Simon G, Van Reeth K. 14 November 2012, posting date. Influenza A virus infection dynamics in swine farms in Belgium, France, Italy and Spain, 2006-2008. Vet. Microbiol. doi:10.1016/j.vetmic.2012.11.014.
51. Buda S, Haas W, Baillot A, Beyrer K, Monazahian M, Pulz M, Benzler J, Harder TC, Schweiger B. 2011. Human infections with porcine influenza viruses. Epidemiol. Bull. RKI 39:357-359. (In German.)
52. Lang C, Palzer A, Dürrwald R, Selbitz HJ, Ritzmann M. 2010. Analysis of the situation of swine influenza in the districts Upper Bavaria, Swabia, Freiburg and Tübingen based on antibody profiles of piglets from Bavarian breeding farms. Berl. Munch. Tierarztl. Wochenschr. 123:385-391. (In German.)
53. Lentz HH, Konschake M, Teske K, Kasper M, Rother B, Carmanns R, Petersen B, Conraths FJ, Selhorst T. 2011. Trade communities and their spatial patterns in the German pork production network. Prev. Vet. Med. 98:176-181.
54. Rautureau S, Dufour B, Durand B. 2012. Structural vulnerability of the French swine industry trade network to the spread of infectious diseases. Animal 6:1152-1162.
55. Nfon CK, Berhane Y, Hisanaga T, Zhang S, Handel K, Kehler H, Labrecque O, Lewis NS, Vincent AL, Copps J, Alexandersen S, Pasick J. 2011. Characterization of H1N1 swine influenza viruses circulating in Canadian pigs in 2009. J. Virol. 85:8667-8679.
56. Schulze IT. 1997. Effects of glycosylation on the properties and functions of influenza virus hemagglutinin. J. Infect. Dis. 176(Suppl 1):S24-S28.
57. Vigerust DJ, Shepard VL. 2007. Virus glycosylation: role in virulence and immune interaction. Trends Microbiol. 15:211-218.
58. Lycett SJ, Bailie G, Coulter E, Bhatt S, Kellam P, McCauley JW, Wood JL, Brown IH, Pybus OG, Leigh Brown AJ. 2012. Estimating reassortment rates in co-circulating Eurasian swine influenza viruses. J. Gen. Virol. 93:2326-2336.
59. Ducatez MF, Hause B, Stigger-Rosser E, Darnell D, Corzo C, Juleen K, Simonson R, Brockwell-Staats C, Rubrum A, Wang D, Webb A, Crumpton JC, Lowe J, Gramer M, Webby RJ. 2011. Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg. Infect. Dis. 17:1624-1628.
60. McDonald NJ, Smith CB, Cox NJ. 2007. Antigenic drift in the evolution of H1N1 influenza A viruses resulting from deletion of a single amino acid in the haemagglutinin gene. J. Gen. Virol. 88:3209-3213.
61. 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 PA, Saito R, Suzuki H, Furuta Y, Yamashita M, Mitamura K, Nakano K, Nakamura M, Brockman-Schneider R, Mitamura H, Yamazaki M, Sugaya N, Suresh M, Ozawa M, Neumann G, Gern J, Kida H, Ogasawara K, Kawaoka Y. 2009. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 460:1021-1025.
62. Brookes SM, Núñez A, Choudhury B, Matrosovich M, Essen SC, Clifford D, Slomka MJ, Kuntz-Simon G, Garcon F, Nash B, Hanna A, Heegaard PM, Quéguiner S, Chiapponi C, Bublot M, Garcia JM, Gardner R, Foni E, Loeffen W, Larsen L, Van Reeth K, Banks J, Irvine RM, Brown IH. 2010. Replication, pathogenesis and transmission of pandemic (H1N1) 2009 virus in non-immune pigs. PLoS One 5:e9068. doi:10.1371/journal.pone.0009068.
63. Vincent AL, Lager KM, Faaberg KS, Harland M, Zanella EL, Ciacci-Zanella JR, Kehrli ME, Jr, Janke BH, Klimov A. 2010. Experimental inoculation of pigs with pandemic H1N1 2009 virus and HI crossreactivity with contemporary swine influenza virus antisera. Influenza Other Respi. Viruses 4:53-60.