Dynamics of virus shedding and antibody responses in influenza A virus-infected feral swine

Journal of General Virology

Volumn 96, Issue 9, 2015, Pages 2569-2578

  Sun, Hailiang ^a   Cunningham, Fred L ^b   Harris, Jillian ^a   Xu, Yifei ^a   Long, Li Ping ^a   Hanson Dorr, Katie ^b   Baroch, John A ^b   Fioranelli, Paul ^b   Lutman, Mark W ^c   Li, Tao ^d   Pedersen, Kerri ^c   Schmit, Brandon S ^b   Cooley, Jim ^a   Lin, Xiaoxu ^d   Jarman, Richard G ^d   Deliberto, Thomas J ^b   Wan, Xiu Feng ^a  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b NATIONAL WILDLIFE RESEARCH CENTER   (United States)

^c UNITED STATES DEPARTMENT OF AGRICULTURE   (United States)

^d WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID ANALYSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE SEQUENCE; HEMAGGLUTINATION INHIBITION TEST; INFLUENZA A VIRUS; NONHUMAN; PIG; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEROLOGY; SWINE INFLUENZA; VIRUS DETECTION; VIRUS INFECTIVITY; VIRUS SHEDDING; ANIMAL; BLOOD; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS (H3N2); ORTHOMYXOVIRIDAE INFECTIONS; PHYSIOLOGY; SWINE DISEASES; VETERINARY; VIROLOGY; WILD ANIMAL;

VIRUS ANTIBODY;

ANIMALS; ANIMALS, WILD; ANTIBODIES, VIRAL; INFLUENZA A VIRUS, H3N2 SUBTYPE; ORTHOMYXOVIRIDAE INFECTIONS; SWINE; SWINE DISEASES; VIRUS SHEDDING;

EID: 84941588113     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000225     Document Type: Article

References (56)

1. Alexander, D. J. & Brown, I. H. (2000). Recent zoonoses caused by influenza A viruses. Rev Sci Tech 19, 197–225.
2. Allerson, M. W., Cardona, C. J. & Torremorell, M. (2013). Indirect transmission of influenza A virus between pig populations under two different biosecurity settings. PLoS One 8, e67293.
3. Bevins, S. N., Pedersen, K., Lutman, M. W., Gidlewski, T. & DeLiberto, T. J. (2014). Consequences associated with the recent expansion of nonnative feral swine. Bioscience 64, 291–299.
4. Bowman, A. S., Nolting, J. M., Nelson, S. W. & Slemons, R. D. (2012). Subclinical influenza virus A infections in pigs exhibited at agricultural fairs, Ohio, USA, 2009–2011. Emerg Infect Dis 18, 1945–1950.
5. Bragstad, K., Vinner, L., Hansen, M. S., Nielsen, J. & Fomsgaard, A. (2013). A polyvalent influenza A DNA vaccine induces heterologous immunity and protects pigs against pandemic A(H1N1)pdm09 virus infection. Vaccine 31, 2281–2288.
6. Choi, Y. K., Nguyen, T. D., Ozaki, H., Webby, R. J., Puthavathana, P., Buranathal, C., Chaisingh, A., Auewarakul, P., Hanh, N. T. & other authors (2005). Studies of H5N1 influenza virus infection of pigs by using viruses isolated in Vietnam and Thailand in 2004. J Virol 79, 10821–10825.
7. Clavijo, A., Nikooienejad, A., Esfahani, M. S., Metz, R. P., Schwartz, S., Atashpaz-Gargari, E., Deliberto, T. J., Lutman, M. W., Pedersen, K. & other authors (2012). Identification and analysis of the first 2009 pandemic H1N1 influenza virus from U.S. feral swine. Zoonoses Public Health 60, 327–335.
8. De Vleeschauwer, A., Atanasova, K., Van Borm, S., van den Berg, T., Rasmussen, T. B., Uttenthal, A. & Van Reeth, K. (2009a). Comparative pathogenesis of an avian H5N2 and a swine H1N1 influenza virus in pigs. PLoS One 4, e6662.
9. De Vleeschauwer, A., Van Poucke, S., Braeckmans, D., Van Doorsselaere, J. & Van Reeth, K. (2009b). Efficient transmission of swine-adapted but not wholly avian influenza viruses among pigs and from pigs to ferrets. J Infect Dis 200, 1884–1892.
10. Feng, Z., Baroch, J. A., Long, L. P., Xu, Y., Cunningham, F. L., Pedersen, K., Lutman, M. W., Schmit, B. S., Bowman, A. S. & other authors (2014). Influenza A subtype H3 viruses in feral swine, United States, 2011–2012. Emerg Infect Dis 20, 843–846.
11. Ferrari, M., Borghetti, P., Foni, E., Robotti, C., Di Lecce, R., Corradi, A., Petrini, S. & Bottarelli, E. (2010). Pathogenesis and subsequent cross-protection of influenza virus infection in pigs sustained by an H1N2 strain. Zoonoses Public Health 57, 273–280.
12. Fogarty, E. (2007). National distribution of and stakeholder attitudes toward feral hogs. Thesis, Mississippi State University, Mississippi State, MS, USA.
13. Guan, Y., Shortridge, K. F., Krauss, S., Li, P. H., Kawaoka, Y. & Webster, R. G. (1996). Emergence of avian H1N1 influenza viruses in pigs in China. J Virol 70, 8041–8046.
14. Hause, B. M., Oleson, T. A., Bey, R. F., Stine, D. L. & Simonson, R. R. (2010). Antigenic categorization of contemporary H3N2 Swine influenza virus isolates using a high-throughput serum neutralization assay. J Vet Diagn Invest 22, 352–359.
15. Hoffmann, E., Stech, J., Guan, Y., Webster, R. G. & Perez, D. R. (2001). Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146, 2275–2289.
16. Keawcharoen, J., Oraveerakul, K., Kuiken, T., Fouchier, R. A., Amonsin, A., Payungporn, S., Noppornpanth, S., Wattanodorn, S., Theambooniers, A. & other authors (2004). Avian influenza H5N1 in tigers and leopards. Emerg Infect Dis 10, 2189–2191.
17. Kida, H., Ito, T., Yasuda, J., Shimizu, Y., Itakura, C., Shortridge, K. F., Kawaoka, Y. & Webster, R. G. (1994). Potential for transmission of avian influenza viruses to pigs. J Gen Virol 75, 2183–2188.
18. Ko, J. C., Williams, B. L., Smith, V. L., McGrath, C. J. & Jacobson, J. D. (1993). Comparison of Telazol, Telazol-ketamine, Telazol-xylazine, and Telazol-ketamine-xylazine as chemical restraint and anesthetic induction combination in swine. Lab Anim Sci 43, 476–480.
19. Koboldt, D. C., Zhang, Q., Larson, D. E., Shen, D., McLellan, M. D., Lin, L., Miller, C. A., Mardis, E. R., Ding, L. & Wilson, R. K. (2012). VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 22, 568–576.
20. Kyriakis, C. S., Rose, N., Foni, E., Maldonado, J., Loeffen, W. L., Madec, F., Simon, G. & Van Reeth, K. (2013). Influenza A virus infection dynamics in swine farms in Belgium, France, Italy and Spain, 2006–2008. Vet Microbiol 162, 543–550.
21. Langmead, B. & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat Methods 9, 357–359.
22. Lee, B. W., Bey, R. F., Baarsch, M. J. & Larson, M. E. (1995). Class specific antibody response to influenza A H1N1 infection in swine. Vet Microbiol 43, 241–250.
23. Liang, Y., Hong, Y. & Parslow, T. G. (2005). Cis-Acting packaging signals in the influenza virus PB1, PB2, and PA genomic RNA segments. J Virol 79, 10348–10355.
24. Lorusso, A., Vincent, A. L., Harland, M. L., Alt, D., Bayles, D. O., Swenson, S. L., Gramer, M. R., Russell, C. A., Smith, D. J. & other authors (2011). Genetic and antigenic characterization of H1 influenza viruses from United States swine from 2008. J Gen Virol 92, 919–930.
25. Mahy, B. (1997). Influenza A virus (FLUA). In A Dictionary of Virology, 2nd edn., pp. 170–171.Edited by B. W. J. Mahy. San Diego, CA: Academic Press.
26. Mase, M., Tanimura, N., Imada, T., Okamatsu, M., Tsukamoto, K. & Yamaguchi, S. (2006). Recent H5N1 avian influenza A virus increases rapidly in virulence to mice after a single passage in mice. J Gen Virol 87, 3655–3659.
27. Muster, T., Subbarao, E. K., Enami, M., Murphy, B. R. & Palese, P. (1991). An influenza A virus containing influenza B virus 59 and 39 noncoding regions on the neuraminidase gene is attenuated in mice. Proc Natl Acad Sci U S A 88, 5177–5181.
28. Nelson, M. I., Vincent, A. L., Kitikoon, P., Holmes, E. C. & Gramer, M. R. (2012). Evolution of novel reassortant A/H3N2 influenza viruses in North American swine and humans, 2009–2011. J Virol 86, 8872–8878.
29. Ng, S. S., Li, O. T., Cheung, T. K., Malik Peiris, J. S. & Poon, L. L. (2008). Heterologous influenza vRNA segments with identical noncoding sequences stimulate viral RNA replication in trans. Virol J 5, 2.
30. Olsen, C. W. (2002). The emergence of novel swine influenza viruses in North America. Virus Res 85, 199–210.
31. Olsen, B., Munster, V. J., Wallensten, A., Waldenström, J., Osterhaus, A. D. & Fouchier, R. A. (2006a). Global patterns of influenza a virus in wild birds. Science 312, 384–388.
32. Olsen, C. W., Karasin, A. I., Carman, S., Li, Y., Bastien, N., Ojkic, D., Alves, D., Charbonneau, G., Henning, B. M. & other authors (2006b). Triple reassortant H3N2 influenza A viruses, Canada, 2005. Emerg Infect Dis 12, 1132–1135.
33. Panyasing, Y., Goodell, C. K., Giménez-Lirola, L., Kittawornrat, A., Wang, C., Schwartz, K. J. & Zimmerman, J. J. (2013). Kinetics of influenza A virus nucleoprotein antibody (IgM, IgA, and IgG) in serum and oral fluid specimens from pigs infected under experimental conditions. Vaccine 31, 6210–6215.
34. Peiris, J. S., Guan, Y., Markwell, D., Ghose, P., Webster, R. G. & Shortridge, K. F. (2001). Cocirculation of avian H9N2 and contemporary ‘‘human’’ H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? J Virol 75, 9679–9686.
35. Peiris, J. S., de Jong, M. D. & Guan, Y. (2007). Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 20, 243–267.
36. Reed, L. J. & Muench, H. (1938). A simple method of estimating fifty percent endpoints. Am J Epidemiol 27, 5.
37. Richt, J. A., Lager, K. M., Janke, B. H., Woods, R. D., Webster, R. G. & Webby, R. J. (2003). Pathogenic and antigenic properties of phylogenetically distinct reassortant H3N2 swine influenza viruses cocirculating in the United States. J Clin Microbiol 41, 3198–3205.
38. Scholtissek, C. (1994). Source for influenza pandemics. Eur J Epidemiol 10, 455–458.
39. Shu, B., Garten, R., Emery, S., Balish, A., Cooper, L., Sessions, W., Deyde, V., Smith, C., Berman, L. & other authors (2012). Genetic analysis and antigenic characterization of swine origin influenza viruses isolated from humans in the United States, 1990-2010. Virology 422, 151–160.
40. Sun, H., Jiao, P., Jia, B., Xu, C., Wei, L., Shan, F., Luo, K., Xin, C., Zhang, K. & Liao, M. (2011). Pathogenicity in quails and mice of H5N1 highly pathogenic avian influenza viruses isolated from ducks. Vet Microbiol 152, 258–265.
41. Sun, H., Yang, J., Zhang, T., Long, L. P., Jia, K., Yang, G., Webby, R. J. & Wan, X. F. (2013). Using sequence data to infer the antigenicity of influenza virus. MBio 4, e00230–e00213.
42. Sun, H., Cui, P., Song, Y., Qi, Y., Li, X., Qi, W., Xu, C., Jiao, P. & Liao, M. (2015). PB2 segment promotes high-pathogenicity of H5N1 avian influenza viruses in mice. Front Microbiol 6, 73.
43. Tellier, R. (2006). Review of aerosol transmission of influenza A virus. Emerg Infect Dis 12, 1657–1662.
44. Van Reeth, K., Braeckmans, D., Cox, E., Van Borm, S., van den Berg, T., Goddeeris, B. & De Vleeschauwer, A. (2009). Prior infection with an H1N1 swine influenza virus partially protects pigs against a low pathogenic H5N1 avian influenza virus. Vaccine 27, 6330–6339.
45. Vincent, A. L., Lager, K. M., Ma, W., Lekcharoensuk, P., Gramer, M. R., Loiacono, C. & Richt, J. A. (2006). Evaluation of hemagglutinin subtype 1 swine influenza viruses from the United States. Vet Microbiol 118, 212–222.
46. Vincent, A. L., Ma, W., Lager, K. M., Janke, B. H. & Richt, J. A. (2008). Swine influenza viruses a North American perspective. Adv Virus Res 72, 127–154.
47. Vincent, A. L., Ma, W., Lager, K. M., Gramer, M. R., Richt, J. A. & Janke, B. H. (2009). Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States. Virus Genes 39, 176–185.
48. Wahl, A., Schafer, F., Bardet, W., Buchli, R., Air, G. M. & Hildebrand, W. H. (2009). HLA class I molecules consistently present internal influenza epitopes. Proc Natl Acad Sci U S A 106, 540–545.
49. Wallace, G. D. (1979). Natural history of influenza in swine in Hawaii: swine influenza virus (Hsw1N1) in herds not infected with lungworms. Am J Vet Res 40, 1159–1164.
50. Watanabe, T., Watanabe, S., Noda, T., Fujii, Y. & Kawaoka, Y. (2003). Exploitation of nucleic acid packaging signals to generate a novel influenza virus-based vector stably expressing two foreign genes. J Virol 77, 10575–10583.
51. Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M. & Kawaoka, Y. (1992). Evolution and ecology of influenza A viruses. Microbiol Rev 56, 152–179.
52. Wei, K., Sun, H., Sun, Z., Sun, Y., Kong, W., Pu, J., Ma, G., Yin, Y., Yang, H. & other authors (2014). Influenza A virus acquires enhanced pathogenicity and transmissibility after serial passages in swine. J Virol 88, 11981–11994.
53. Wyckoff, A. C., Henke, S. E., Campbell, T. A., Hewitt, D. G. & VerCauteren, K. C. (2009). Feral swine contact with domestic swine: a serologic survey and assessment of potential for disease transmission. J Wildl Dis 45, 422–429.
54. Zhang, G., Kong, W., Qi, W., Long, L. P., Cao, Z., Huang, L., Qi, H., Cao, N., Wang, W. & other authors (2011). Identification of an H6N6 swine influenza virus in southern China. Infect Genet Evol 11, 1174–1177.
55. Zheng, H., Palese, P. & García-Sastre, A. (1996). Nonconserved nucleotides at the 39 and 59 ends of an influenza A virus RNA play an important role in viral RNA replication. Virology 217, 242–251.
56. Zhou, B., Donnelly, M. E., Scholes, D. T., St George, K., Hatta, M., Kawaoka, Y. & Wentworth, D. E. (2009). Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and Swine origin human influenza a viruses. J Virol 83, 10309–10313.