1887

Abstract

Low-pathogenicity avian influenza virus (LPAIV) can lead to epizootics that cause economic losses in poultry or the emergence of human-infectious strains. LPAIVs experience a complex immunity landscape as they are endemic in numerous host species, and many antigenically distinct strains co-circulate. Prevention and control of emergence of detrimental strains requires an understanding of infection/transmission characteristics of the various subtypes in different hosts, including interactions between subtypes. In order to develop analytical frameworks for examining control efficacy, quantification of heterosubtypic immunity interactions is fundamental. However, these data are scarce, especially for wild avian subtypes in natural hosts. Consequently, in this study, three host species (mallards, quail and pheasants) were infected with two LPAIV subtypes isolated from wild birds: H3N8 and H4N6. The recovered hosts were also reinfected with the alternate subtype to measure the effects of heterosubtypic immunity. Oropharyngeal and cloacal swabs were collected and viral RNA load was quantified by real-time RT-PCR. For secondary infections in recovered hosts, peak viral load was up to four orders of magnitude lower and shedding length was up to 4 days shorter. However, both the magnitude and presence of heterosubtypic immunity varied across specific host species/subtype combinations. Using a mathematical model of virus replication, the variation in virus replication dynamics due to host individuals was quantified. It was found that accounting for individual heterogeneity is important for drawing accurate conclusions about treatment effects. These results are relevant for developing epidemiological models to inform control practices and for analysing virus replication data.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.045427-0
2012-12-01
2021-08-01
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/12/2575.html?itemId=/content/journal/jgv/10.1099/vir.0.045427-0&mimeType=html&fmt=ahah

References

  1. Agüero M., San Miguel E., Sánchez A., Gómez-Tejedor C., Jiménez-Clavero M. A. 2007; A fully automated procedure for the high-throughput detection of avian influenza virus by real-time reverse transcription-polymerase chain reaction. Avian Dis 51:Suppl.235–241 [View Article][PubMed]
    [Google Scholar]
  2. Berhane Y., Leith M., Embury-Hyatt C., Neufeld J., Babiuk S., Hisanaga T., Kehler H., Hooper-McGrevy K., Pasick J. 2010; Studying possible cross-protection of Canada geese preexposed to North American low pathogenicity avian influenza virus strains (H3N8, H4N6, and H5N2) against an H5N1 highly pathogenic avian influenza challenge. Avian Dis 54:Suppl.548–554 [View Article][PubMed]
    [Google Scholar]
  3. Campitelli L., Fabiani C., Puzelli S., Fioretti A., Foni E., De Marco A., Krauss S., Webster R. G., Donatelli I. 2002; H3N2 influenza viruses from domestic chickens in Italy: an increasing role for chickens in the ecology of influenza?. J Gen Virol 83:413–420
    [Google Scholar]
  4. Capua I., Alexander D. J. 2004; Avian influenza: recent developments. Avian Pathol 33:393–404 [View Article][PubMed]
    [Google Scholar]
  5. Costa T. P., Brown J. D., Howerth E. W., Stallknecht D. E. 2010a; Effect of a prior exposure to a low pathogenic avian influenza virus in the outcome of a heterosubtypic low pathogenic avian influenza infection in mallards (Anas platyrhynchos). Avian Dis 54:1286–1291 [View Article][PubMed]
    [Google Scholar]
  6. Costa T. P., Brown J. D., Howerth E. W., Stallknecht D. E. 2010b; The effect of age on avian influenza viral shedding in mallards (Anas platyrhynchos). Avian Dis 54:Suppl.581–585 [View Article][PubMed]
    [Google Scholar]
  7. Daoust P. Y., Kibenge F. S. B., Fouchier R. A. M., van de Bildt M. W. G., van Riel D., Kuiken T. 2010; Replication of low pathogenic avian influenza virus in naturally infected mallard ducks (Anas platyrhynchos) causes no morphologic lesions. J Wildl Dis 47:401–409 [CrossRef]
    [Google Scholar]
  8. Deliberto T. J., Swafford S. R., Nolte D. L., Pedersen K., Lutman M. W., Schmit B. B., Baroch J. A., Kohler D. J., Franklin A. 2009; Surveillance for highly pathogenic avian influenza in wild birds in the USA. Integr Zool 4:426–439 [View Article][PubMed]
    [Google Scholar]
  9. Fereidouni S. R., Starick E., Beer M., Wilking H., Kalthoff D., Grund C., Häuslaigner R., Breithaupt A., Lange E., Harder T. C. 2009; Highly pathogenic avian influenza virus infection of mallards with homo- and heterosubtypic immunity induced by low pathogenic avian influenza viruses. PLoS ONE 4:e6706 [View Article][PubMed]
    [Google Scholar]
  10. Hoye B. J., Fouchier R. A. M., Klaassen M. 2012; Host behaviour and physiology underpin individual variation in avian influenza virus infection in migratory Bewick’s swans. Proc Biol Sci 279:529–534 [View Article][PubMed]
    [Google Scholar]
  11. Imai K., Nakamura K., Mase M., Tsukamoto K., Imada T., Yamaguchi S. 2007; Partial protection against challenge with the highly pathogenic H5N1 influenza virus isolated in Japan in chickens infected with the H9N2 influenza virus. Arch Virol 152:1395–1400 [View Article][PubMed]
    [Google Scholar]
  12. Jindal N., de Abin M., Primus A. E., Raju S., Chander Y., Redig P. T., Goyal S. M. 2010; Comparison of cloacal and oropharyngeal samples for the detection of avian influenza virus in wild birds. Avian Dis 54:115–119 [View Article][PubMed]
    [Google Scholar]
  13. Jourdain E., Gunnarsson G., Wahlgren J., Latorre-Margalef N., Bröjer C., Sahlin S., Svensson L., Waldenström J., Lundkvist A., Olsen B. 2010; Influenza virus in a natural host, the mallard: experimental infection data. PLoS ONE 5:e8935 [View Article][PubMed]
    [Google Scholar]
  14. Kramer-Schadt S., Fernandez N., Eisinger D., Grimm V., Thulke H.-H. 2009; Individual variations in infectiousness explain long-term disease persistence in wildlife populations. Oikos 118:199–208 [View Article]
    [Google Scholar]
  15. Krauss S., Walker D., Pryor S. P., Niles L., Chenghong L., Hinshaw V. S., Webster R. G. 2004; Influenza A viruses of migrating wild aquatic birds in North America. Vector Borne Zoonotic Dis 4:177–189 [View Article][PubMed]
    [Google Scholar]
  16. Krauss S., Obert C. A., Franks J., Walker D., Jones K., Seiler P., Niles L., Pryor S. P., Obenauer J. C. other authors 2007; Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog 3:e167 [View Article][PubMed]
    [Google Scholar]
  17. Lloyd-Smith J. O., Schreiber S. J., Kopp P. E., Getz W. M. 2005; Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359 [View Article][PubMed]
    [Google Scholar]
  18. Lupiani B., Reddy S. M. 2009; The history of avian influenza. Comp Immunol Microbiol Infect Dis 32:311–323 [View Article][PubMed]
    [Google Scholar]
  19. Nolting J., Fries A. C., Slemons R. D., Courtney C., Hines N., Pedersen J. 2012; Recovery of H14 influenza A virus isolates from sea ducks in the Western Hemisphere. PLoS Curr 4:RRN1290 [View Article][PubMed]
    [Google Scholar]
  20. Panigrahy B., Senne D. A., Pedersen J. C. 2002; Avian influenza virus subtypes inside and outside the live bird markets, 1993–2000: a spatial and temporal relationship. Avian Dis 46:298–307 [View Article][PubMed]
    [Google Scholar]
  21. Paull S. H., Song S., McClure K. M., Sackett L. C., Kilpatrick A. M., Johnson P. T. J. 2012; From superspreaders to disease hotspots: linking transmission across hosts and space. Front Ecol Environ 10:75–82 [View Article]
    [Google Scholar]
  22. Pepin K. M., Wang J., Webb C. T., Smith G. J. D., Poss M., Hudson P. J., Hong W., Zhu H., Riley S., Guan Y. 2012; Multiannual patterns of influenza A transmission in Chinese live-bird market systems. Influenza Other Resp (in press) [View Article]
    [Google Scholar]
  23. Piaggio A. J., Shriner S. A., VanDalen K. K., Franklin A. B., Anderson T. D., Kolokotronis S.-O. 2012; Molecular surveillance of low pathogenic avian influenza viruses in wild birds across the United States: inferences from the hemagglutinin gene. PLoS ONE (in press)
    [Google Scholar]
  24. Reed L. J., Muench H. 1938; A simple method of estimating fifty per cent endpoints. Am J Epi 27:493–497
    [Google Scholar]
  25. Saif Y. M., Fadly A. M., Glisson J. R., McDougald R., Nolan L. K., Swayne D. E. 2008 Diseases of Poultry, 12th edn. Ames, IA: Blackwell Publishing;
    [Google Scholar]
  26. Spackman E. 2008; Methods in Molecular Biology, Vol. 436: Avian Influenza Virus . New York: Springer-Verlag;
    [Google Scholar]
  27. Spackman E., Senne D. A., Bulaga L. L., Myers T. J., Perdue M. L., Garber L. P., Lohman K., Daum L. T., Suarez D. L. 2003; Development of real-time RT-PCR for the detection of avian influenza virus. Avian Dis 47:Suppl.1079–1082 [View Article][PubMed]
    [Google Scholar]
  28. Szretter K. J., Balish A. L., Katz J. M. 2006; Influenza: propagation, quantification, and storage. Current Protocols in Microbiology 3:15G.1.1–15G.1.22
    [Google Scholar]
  29. USDA 2006; An early detection system for highly pathogenic H5N1 avian influenza in wild migratory birds: U.S. Interagency Strategic Plan. US Department of Agriculture. http://www.aphis.usda.gov/wildlife_damage/nwdp/pdf/wildbirdstrategicplanpdf.pdf
  30. VanDalen K. K., Anderson T. D., Killian M. L., Pedersen J. C., Franklin A. B., Piaggio A. J. 2008; Increased detection of influenza A H16 in the United States. Arch Virol 153:1981–1983 [View Article][PubMed]
    [Google Scholar]
  31. VanDalen K. K., Franklin A. B., Mooers N. L., Sullivan H. J., Shriner S. A. 2010; Shedding light on avian influenza H4N6 infection in mallards: modes of transmission and implications for surveillance. PLoS ONE 5:e12851 [View Article][PubMed]
    [Google Scholar]
  32. 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
    [Google Scholar]
  33. Webster R. G., Krauss S., Hulse-Post D., Sturm-Ramirez K. 2007; Evolution of influenza A viruses in wild birds. J Wildl Dis 43:S1–S6 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.045427-0
Loading
/content/journal/jgv/10.1099/vir.0.045427-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error