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. 1997 Aug;71(8):6128–6135. doi: 10.1128/jvi.71.8.6128-6135.1997

Coinfection of wild ducks by influenza A viruses: distribution patterns and biological significance.

G B Sharp 1, Y Kawaoka 1, D J Jones 1, W J Bean 1, S P Pryor 1, V Hinshaw 1, R G Webster 1
PMCID: PMC191873  PMID: 9223507

Abstract

Coinfection of wild birds by influenza A viruses is thought to be an important mechanism for the diversification of viral phenotypes by generation of reassortants. However, it is not known whether coinfection is a random event or follows discernible patterns with biological significance. In the present study, conducted with viruses collected throughout 15 years from a wild-duck population in Alberta, Canada, we identified three discrete distributions of coinfections. In about one-third of the events, which involved subtypes of viruses that appear to be maintained in this duck reservoir, coinfection occurred at rates either close to or significantly lower than one would predict from rates of single-virus infection. Apparently, the better adapted an influenza A virus is to an avian population, the greater is its ability to prevent coinfections. Conversely, poorly adapted, nonmaintained viruses were significantly overrepresented as coinfectants. Rarely encountered subtypes appear to represent viruses whose chances of successfully infiltrating avian reservoirs are increased by coinfection. Mallards (Anas platyrhynchos) and pintails (A. acuta) were significantly more likely to be infected by a single influenza A virus than were the other species sampled, but no species was significantly more likely to be coinfected. These observations provide the first evidence of nonrandom coinfection of wild birds by influenza A viruses, suggesting that reassortment of these viruses in a natural population does not occur randomly. These results suggest that even though infections may occur in a species, all subtypes are not maintained by all avian species. They also suggest that specific influenza A virus subtypes are differentially adapted to different avian hosts and that the fact that a particular subtype is isolated from a particular avian species does not mean that the virus is maintained by that species.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aymard-Henry M., Coleman M. T., Dowdle W. R., Laver W. G., Schild G. C., Webster R. G. Influenzavirus neuraminidase and neuraminidase-inhibition test procedures. Bull World Health Organ. 1973;48(2):199–202. [PMC free article] [PubMed] [Google Scholar]
  2. Becker W. B. The isolation and classification of Tern virus: influenza A-Tern South Africa--1961. J Hyg (Lond) 1966 Sep;64(3):309–320. doi: 10.1017/s0022172400040596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Castrucci M. R., Donatelli I., Sidoli L., Barigazzi G., Kawaoka Y., Webster R. G. Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology. 1993 Mar;193(1):503–506. doi: 10.1006/viro.1993.1155. [DOI] [PubMed] [Google Scholar]
  4. Claas E. C., Kawaoka Y., de Jong J. C., Masurel N., Webster R. G. Infection of children with avian-human reassortant influenza virus from pigs in Europe. Virology. 1994 Oct;204(1):453–457. doi: 10.1006/viro.1994.1553. [DOI] [PubMed] [Google Scholar]
  5. Downie J. C., Laver W. G. Isolation of a type A influenza virus from an Australian pelagic bird. Virology. 1973 Feb;51(2):259–269. doi: 10.1016/0042-6822(73)90426-1. [DOI] [PubMed] [Google Scholar]
  6. Gorman O. T., Bean W. J., Kawaoka Y., Donatelli I., Guo Y. J., Webster R. G. Evolution of influenza A virus nucleoprotein genes: implications for the origins of H1N1 human and classical swine viruses. J Virol. 1991 Jul;65(7):3704–3714. doi: 10.1128/jvi.65.7.3704-3714.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gorman O. T., Donis R. O., Kawaoka Y., Webster R. G. Evolution of influenza A virus PB2 genes: implications for evolution of the ribonucleoprotein complex and origin of human influenza A virus. J Virol. 1990 Oct;64(10):4893–4902. doi: 10.1128/jvi.64.10.4893-4902.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hinshaw V. S., Bean W. J., Webster R. G., Sriram G. Genetic reassortment of influenza A viruses in the intestinal tract of ducks. Virology. 1980 Apr 30;102(2):412–419. doi: 10.1016/0042-6822(80)90108-7. [DOI] [PubMed] [Google Scholar]
  9. Hinshaw V. S., Webster R. G., Turner B. Novel influenza A viruses isolated from Canadian feral ducks: including strains antigenically related to swine influenza (Hsw1N1) viruses. J Gen Virol. 1978 Oct;41(1):115–127. doi: 10.1099/0022-1317-41-1-115. [DOI] [PubMed] [Google Scholar]
  10. Hinshaw V. S., Webster R. G., Turner B. The perpetuation of orthomyxoviruses and paramyxoviruses in Canadian waterfowl. Can J Microbiol. 1980 May;26(5):622–629. doi: 10.1139/m80-108. [DOI] [PubMed] [Google Scholar]
  11. Hinshaw V. S., Webster R. G., Turner B. Water-bone transmission of influenza A viruses? Intervirology. 1979;11(1):66–68. doi: 10.1159/000149014. [DOI] [PubMed] [Google Scholar]
  12. Ito T., Gorman O. T., Kawaoka Y., Bean W. J., Webster R. G. Evolutionary analysis of the influenza A virus M gene with comparison of the M1 and M2 proteins. J Virol. 1991 Oct;65(10):5491–5498. doi: 10.1128/jvi.65.10.5491-5498.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kawaoka Y., Yamnikova S., Chambers T. M., Lvov D. K., Webster R. G. Molecular characterization of a new hemagglutinin, subtype H14, of influenza A virus. Virology. 1990 Dec;179(2):759–767. doi: 10.1016/0042-6822(90)90143-f. [DOI] [PubMed] [Google Scholar]
  14. Kida H., Ito T., Yasuda J., Shimizu Y., Itakura C., Shortridge K. F., Kawaoka Y., Webster R. G. Potential for transmission of avian influenza viruses to pigs. J Gen Virol. 1994 Sep;75(Pt 9):2183–2188. doi: 10.1099/0022-1317-75-9-2183. [DOI] [PubMed] [Google Scholar]
  15. Kida H., Yanagawa R., Matsuoka Y. Duck influenza lacking evidence of disease signs and immune response. Infect Immun. 1980 Nov;30(2):547–553. doi: 10.1128/iai.30.2.547-553.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lipkind M., Bürger H., Rott R., Scholtissek C. Genetic characterization of influenza A viruses isolated from birds in Israel. A contribution to the ecology of avian influenza viruses. Zentralbl Veterinarmed B. 1984 Dec;31(10):721–728. doi: 10.1111/j.1439-0450.1984.tb01356.x. [DOI] [PubMed] [Google Scholar]
  17. Otsuki K., Kariya H., Matsuo K., Sugiyama S., Hoshina K., Yoshikane T., Matsumoto A., Tsubokura M. Isolation of influenza A viruses from migratory waterfowls in San-In District Japan in the winter of 1984-1985. Nihon Juigaku Zasshi. 1987 Aug;49(4):721–723. doi: 10.1292/jvms1939.49.721. [DOI] [PubMed] [Google Scholar]
  18. Otsuki K., Takemoto O., Fujimoto R., Kawaoka Y., Tsubokura M. Isolation of influenza A viruses from migratory waterfowls in San-in District, Western Japan in winters of 1980-1982. Zentralbl Bakteriol Mikrobiol Hyg A. 1987 Jun;265(1-2):235–242. doi: 10.1016/s0176-6724(87)80171-2. [DOI] [PubMed] [Google Scholar]
  19. Otsuki K., Takemoto O., Fujimoto R., Yamazaki K., Kubota N., Hosaki H., Kawaoka Y., Tsubokura M. Isolation of influenza A viruses from migratory waterfowls in San-in District, Western Japan, in the winter of 1982-1983. Acta Virol. 1987 Sep;31(5):439–442. [PubMed] [Google Scholar]
  20. Otsuki K., Takemoto O., Fujimoto R., Yamazaki K., Kubota N., Hosaki H., Mitani T., Tsubokura M. Isolation of influenza A viruses from migratory waterfowl in San-in District, western Japan in the winter of 1983-1984. Res Vet Sci. 1987 Sep;43(2):177–179. [PubMed] [Google Scholar]
  21. Röhm C., Zhou N., Süss J., Mackenzie J., Webster R. G. Characterization of a novel influenza hemagglutinin, H15: criteria for determination of influenza A subtypes. Virology. 1996 Mar 15;217(2):508–516. doi: 10.1006/viro.1996.0145. [DOI] [PubMed] [Google Scholar]
  22. Saito T., Kawaoka Y., Webster R. G. Phylogenetic analysis of the N8 neuraminidase gene of influenza A viruses. Virology. 1993 Apr;193(2):868–876. doi: 10.1006/viro.1993.1196. [DOI] [PubMed] [Google Scholar]
  23. 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 Dec;147(2):287–294. doi: 10.1016/0042-6822(85)90131-x. [DOI] [PubMed] [Google Scholar]
  24. Scholtissek C., Ludwig S., Fitch W. M. Analysis of influenza A virus nucleoproteins for the assessment of molecular genetic mechanisms leading to new phylogenetic virus lineages. Arch Virol. 1993;131(3-4):237–250. doi: 10.1007/BF01378629. [DOI] [PubMed] [Google Scholar]
  25. Sharp G. B., Kawaoka Y., Wright S. M., Turner B., Hinshaw V., Webster R. G. Wild ducks are the reservoir for only a limited number of influenza A subtypes. Epidemiol Infect. 1993 Feb;110(1):161–176. doi: 10.1017/s0950268800050780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shortridge K. F. Avian influenza A viruses of southern China and Hong Kong: ecological aspects and implications for man. Bull World Health Organ. 1982;60(1):129–135. [PMC free article] [PubMed] [Google Scholar]
  27. Sinnecker R., Sinnecker H., Zilske E., Köhler D. Surveillance of pelagic birds for influenza A viruses. Acta Virol. 1983 Jan;27(1):75–79. [PubMed] [Google Scholar]
  28. Slemons R. D., Easterday B. C. Virus replication in the digestive tract of ducks exposed by aerosol to type-A influenza. Avian Dis. 1978 Jul-Sep;22(3):367–377. [PubMed] [Google Scholar]
  29. Slemons R. D., Johnson D. C., Osborn J. S., Hayes F. Type-A influenza viruses isolated from wild free-flying ducks in California. Avian Dis. 1974 Jan-Mar;18(1):119–124. [PubMed] [Google Scholar]
  30. Stallknecht D. E., Shane S. M., Zwank P. J., Senne D. A., Kearney M. T. Avian influenza viruses from migratory and resident ducks of coastal Louisiana. Avian Dis. 1990 Apr-Jun;34(2):398–405. [PubMed] [Google Scholar]
  31. Stünzner D., Thiel W., Pötsch F., Sixl W. Isolation of influenza viruses from exotic and Central European birds. Zentralbl Bakteriol A. 1980 Jun;247(1):8–17. doi: 10.1016/s0172-5599(80)80015-0. [DOI] [PubMed] [Google Scholar]
  32. Süss J., Schäfer J., Sinnecker H., Webster R. G. Influenza virus subtypes in aquatic birds of eastern Germany. Arch Virol. 1994;135(1-2):101–114. doi: 10.1007/BF01309768. [DOI] [PubMed] [Google Scholar]
  33. Tsubokura M., Otsuki K., Kawaoka Y., Yanagawa R. Isolation of influenza A viruses from migratory waterfowls in San-in District, Western Japan in 1979-1980. Zentralbl Bakteriol Mikrobiol Hyg B. 1981 Sep;173(6):494–500. [PubMed] [Google Scholar]
  34. Webster R. G., Bean W. J., Gorman O. T., Chambers T. M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992 Mar;56(1):152–179. doi: 10.1128/mr.56.1.152-179.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Webster R. G., Yakhno M., Hinshaw V. S., Bean W. J., Murti K. G. Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology. 1978 Feb;84(2):268–278. doi: 10.1016/0042-6822(78)90247-7. [DOI] [PMC free article] [PubMed] [Google Scholar]

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