Archives of Virology

, Volume 135, Issue 1–2, pp 101–114 | Cite as

Influenza virus subtypes in aquatic birds of eastern Germany

  • J. Süss
  • J. Schäfer
  • H. Sinnecker
  • R. G. Webster
Original Papers


We report the findings of a 12-year surveillance study (1977–89) of avian influenza A viruses in eastern Germany. Viruses were isolated directly from feral ducks (n=236) and other wild birds (n=89); from domestic ducks (n=735) living on a single farm; and from white Pekin ducks (n=193) used as sentinels for populations of wild aquatic birds; mainly sea birds. The efficiency of virus isolation was 9.9% overall, with considerable variability noted among species: 8.7% in wild ducks, 0.9% in other feral birds and 38% in Pekin ducks. Use of sentinel ducks in wild pelagic bird colonies improved virus detection rates fivefold, suggesting that this approach is advantageous in ecological studies. Among the 40 different combinations of hemagglutinin (HA) and neuraminidase (NA) subtypes we identified, H6N1 predominated (23.6% for all avian species), followed by H4N6 (11%). Among individual species, the frequency profiles favored H2N3 (20.8%) and H4N6 (20.3%) in feral ducks; H7N7 (22.3%), H4N6 (24.4%) and H2N3 (10.4%) in Pekin ducks used as sentinels; and H6N1 (34.8%) and H6N6 (15.1%) in domestic ducks maintained on a single farm. By relying on sentinel birds for serological assays, it was possible to trace an “influenza season” in feral swan populations, beginning in August and continuing through the winter months. Comparison of subtype distribution of influenza viruses for Europe and North American showed significant differences. This supports the fact of two geographically distinct gene pools of influenza viruses in birds connected with their distinct flyways of each hemisphere. The high frequency of isolation of H2 influenza viruses is of considerable interest to those interested in the recycling of this subtype in humans. Similarly the frequent isolation of H7N7 influenza viruses raises concern about reservoirs of potentially pathogenic influenza virus for domestic poultry. Our results confirm the existence of a vast reservoir of influenza A viruses in European aquatic birds, which possesses sufficient diversity to account for strains that infect lower animals and humans.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Aminoff D (1961) Methods for the quantitative estimation of N-acetyl-neuraminic acid and their application to hydrolysates of sialomucoids. Biochem J 81: 384–392Google Scholar
  2. 2.
    Bean WJ, Schell M, Katz J, Kawaoka Y, Naeve C, Gorman O, Webster RG (1992) Evolution of the H3 influenza virus hemagglutinin from human and nonhuman hosts. J Virol 66: 1129–1138Google Scholar
  3. 3.
    Donis RO, Bean WJ, Kawaoka Y, Webster RG (1989) Distinct lineages of influenza virus H4 hemagglutinin genes in different regions of the world. Virology 169: 408–417Google Scholar
  4. 4.
    Halvorson D, Karunakaran D, Senne D, Kelleher C, Bailey C, Abraham A, Hinshaw VS, Newman J (1983) Epizootiology of avian influenza-simultaneous monitoring of sentinel ducks and turkeys in Minnesota. Avian Dis 27: 77–85Google Scholar
  5. 5.
    Halvorson DA, Kelleher CJ, Pomeroy BS, Sivanandan V, Abraham AS, Newman JA, Karunakaran D, Poss PE, Senne DA, Pearson JE (1986) Surveillance procedures for avian influenza. Proc. 2nd Int. Symp. Avian Influenza. US Animal Health Association, pp 155–162Google Scholar
  6. 6.
    Hannoun C, Devaux JM (1980) Circulation enzootique permanente de virus grippaux dans la baie de la Somme. Comp Immunol Microbiol Infect Dis 3: 177–183Google Scholar
  7. 7.
    Hinshaw VS, Bean WJ, Webster RG, Easterday BC (1978a) The prevalence of influenza viruses in swine and the antigenic and genetic relatedness of influenza viruses from man and swine. Virology 84: 51–62Google Scholar
  8. 8.
    Hinshaw VS, Webster RG, Turner B (1978b) Novel influenza A viruses isolated from Canadian feral ducks including strains antigenically related to swine influenza (Hsw 1N1) viruses. J Gen Virol 41: 115–127Google Scholar
  9. 9.
    Hinshaw VS, Webster RG, Turner B (1979) Waterborne transmission of influenza viruses? Intervirology 2: 66–68Google Scholar
  10. 10.
    Hinshaw VS, Bean WJ, Webster RG, Sriram G (1980a) Genetic reassortment of influenza A viruses in the intestinal tract of ducks. Virology 102: 412–419Google Scholar
  11. 11.
    Hinshaw VS, Webster RG, Turner B (1980b) The perpetuation of ortho- and paramyxoviruses in Canadian water fowl. Can J Microbiol 26: 622–627Google Scholar
  12. 12.
    Hinshaw VS, Webster RG (1982) The natural history of influenza A viruses. In: Beare AS (ed) Basic and applied influenza research. CRC Press, Boca Raton, pp 79–104Google Scholar
  13. 13.
    Hinshaw VS, Wood J, Webster RG, Deibel R, Turner B (1985) Circulation of influenza viruses and paramyxoviruses in waterfowl: comparison of different migratory flyways in North America. Bull World Health Organ 63: 711–719.Google Scholar
  14. 14.
    Laver WG, Webster RG (1979) Ecology of influenza viruses in lower mammals and birds. Br Med J 35: 29–35Google Scholar
  15. 15.
    Lipkind MA, Weisman Y, Shihmanter E, Shoham D (1979) The first isolation of animal influenza virus in Israel. Vet Rec 105: 510–511Google Scholar
  16. 16.
    Ludwig S, Scholtissek C (1992) Recent influenza infections in turkeys and pigs in Northern Europe. Proc. 3rd Int. Symp Avian Influenza. US Animal Health Association, Madison, pp 131–135Google Scholar
  17. 17.
    Lvov DK, Zhdanov VM (1987) Circulation of influenza virus genes in the biosphere. Sov Med Rev Virol 1: 129–152Google Scholar
  18. 18.
    Mackenzie JS, Edwards EC, Holmes RM, Hinshaw VS (1984) Isolation of ortho-and paramyxoviruses from wild birds in Western Australia, and the characterization of novel influenza A viruses. Aust J Exp Biol Med Sci 62: 89–99Google Scholar
  19. 19.
    Ottis K, Bachmann PA (1980) Occurrence of Hsw 1N1 subtype influenza A viruses in wild ducks in Europe. Arch Virol 63: 185–190Google Scholar
  20. 20.
    Ottis K, Bachmann PA (1983) Isolation and characterization of ortho-and paramyxoviruses from feral birds in Europe. Zentralbl Veterinärmed [B] 30: 22–35Google Scholar
  21. 21.
    Palmer DF, Coleman MT, Dowdle WR, Schild GC (1975) Advanced laboratory techniques for influenza diagnosis. U.S. Department of Health, Education, and Welfare, AtlantaGoogle Scholar
  22. 22.
    Schäfer J, Kawaoka Y, Bean WJ, Süss J, Senne D, Webster RG (1993) Origin of the pandemic 1957 H2 influenza a virus and the persistence of its progenitors in the avian reservoir. Virology 194: 781–788Google Scholar
  23. 23.
    Scholtissek C (1978) The genome of influenza virus. Curr Top Microbiol Immunol 80: 139–169Google Scholar
  24. 24.
    Scholtissek C, Rohde W, von Hoyningen V, Rott R (1978) On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 87: 13–20Google Scholar
  25. 25.
    Scholtissek C, Burger H, Bachmann PA, Hannoun C (1983) Genetic relatedness of hemagglutinins of the H1 subtype of influenza A viruses isolated from swine and birds. Virology 129: 521–523Google Scholar
  26. 26.
    Scholtissek C, Burger H, Kistner O, Shortridge KF (1985) The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 147: 287–294Google Scholar
  27. 27.
    Sharp GB, Kawaoka Y, Wright SM, Turner B, Hinshaw V, Webster RG (1993) Wild ducks are the reservoir for only a limited number of influenza A subtypes. Epidemiol Infect 110: 161–176Google Scholar
  28. 28.
    Shortridge KF (1982) Avian influenza A viruses of southern China and Hong Kong: ecological aspects and implications for man. Bull World Health Organ 60: 129–135Google Scholar
  29. 29.
    Shortridge KF (1988) Pandemic influenza — a blueprint for control at source. Chin J Exp Clin Virol 3: 75–88Google Scholar
  30. 30.
    Sinnecker H, Sinnecker R, Zilske E (1982a) Detection of influenza A viruses by sentinel domestic ducks in an ecological survey. Acta Virol 26: 102–104Google Scholar
  31. 31.
    Sinnecker H, Sinnecker R, Zilske E, Koehler D (1982b) Detection of influenza A viruses and influenza epidemics in wild pelagic birds by sentinels and population studies. Zentralbl Bakt Hyg F Abt Orig A253: 297–304Google Scholar
  32. 32.
    Sinnecker R, Sinnecker H, Zilske E, Koehler D (1983) Surveillance of pelagic birds for influenza A viruses. Acta Virol 27: 75–79Google Scholar
  33. 33.
    Sinnecker H, Egert J, Eggert HJ, Gogolin J, Gümpel S, Schrader C, Sinnecker R, Zilske E (1986) Studies of some biological and molecular characteristics of avian influenza A/H7 (Hav1) subtypes. Acta Virol 30: 25–34Google Scholar
  34. 34.
    Sinnecker H, Sinnecker R (1987) Naturgeschichte des Influenzavirus A: Epizootiologie, Ökologie und Evolution. In: Süss J (ed) Influenza. Fischer, Jena, pp 251–277Google Scholar
  35. 35.
    Tsobokura M, Otsuki K, Kawaoka Y, Yanagawa R (1981) Isolation of influenza A viruses from migratory waterfowls in San-in district, western Japan in 1979–1980. Zentralbl Bakt Hyg I Abt Orig B 173: 494–500Google Scholar
  36. 36.
    Webster RG, Morita M, Pridgen G, Tumova B (1976) Ortho-and paramyxoviruses from migrating feral ducks: characterization of a new group of influenza A viruses. J Gen Virol 32: 217–225Google Scholar
  37. 37.
    Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG (1978) Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 84: 263–278Google Scholar
  38. 38.
    Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56: 152–178Google Scholar
  39. 39.
    Yamane N, Odagisi T, Arikawa J (1978) Isolation of orthomyxoviruses from migrating and domestic ducks in Northern Japan in 1976–1979. Jpn J Med Sci Biol 31: 407–415Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • J. Süss
    • 1
  • J. Schäfer
    • 2
  • H. Sinnecker
    • 2
  • R. G. Webster
    • 3
  1. 1.Institute of Veterinary Medicine of the Federal Health OfficeBerlin
  2. 2.German Institute for Human NutritionBergholz-RehbrückeFederal Republic of Germany
  3. 3.Department of Virology and Molecular BiologySt. Jude Children's Research HospitalMemphisUSA

Personalised recommendations