, Volume 13, Issue 1, pp 161–170 | Cite as

Influenza Virus Infection of Marine Mammals

  • Sasan Fereidouni
  • Olga Munoz
  • Sophie Von Dobschuetz
  • Marco De Nardi


Interspecies transmission may play a key role in the evolution and ecology of influenza A viruses. The importance of marine mammals as hosts or carriers of potential zoonotic pathogens such as highly pathogenic H5 and H7 influenza viruses is not well understood. The fact that influenza viruses are some of the few zoonotic pathogens known to have caused infection in marine mammals, evidence for direct transmission of influenza A virus H7N7 subtype from seals to man, transmission of pandemic H1N1 influenza viruses to seals and also limited evidence for long-term persistence of influenza B viruses in seal populations without significant genetic change, makes monitoring of influenza viruses in marine mammal populations worth being performed. In addition, such monitoring studies could be a great tool to better understand the ecology of influenza viruses in nature.


marine mammals influenza viruses zoonotic diseases 



This review has been shared with the consortium of the EFSA (European Food Safety Authority) funded FLURISK project ( The main objective of FLURISK is the development of an epidemiological and virological evidence-based risk assessment framework (RAF) to assess the Influenza A Virus (IAV) strains circulating in the animal population according to their potential to cross the species barrier and cause infections in humans. This work has therefore contributed to the FLURISK task of reviewing the overall circulation of influenza virus in animal populations. The authors thank Timm Harder and Francesca Ellero for editorial advice during the preparation of the manuscript.


  1. Anthony SJ, St Leger JA, Pugliares K, Ip HS, Chan JM, Carpenter ZW, et al. (2012) Emergence of fatal avian influenza in New England harbor seals. mBio 31;3(4):e00166-12Google Scholar
  2. Arbiza J, Blanc A, Castro-Ramos M, Katz H, Ponce de León A, Clara M (2012) Uruguayan pinnipeds (Arctocephalus australis and Otaria flavescens): evidence of influenza virus and mycobacterium pinnipedii infections. In: New Approaches to the Study of Marine Mammals, Romero A (editor). InTech, pp 151–182Google Scholar
  3. Austin FJ, Webster RG (1993) Evidence of ortho- and paramyxoviruses in fauna from Antarctica. Journal of Wildlife Diseases 29:568-671CrossRefPubMedGoogle Scholar
  4. Blanc A, Ruchansky D, Clara M, Achaval F, Le Bas A, Arbiza J (2009) Serologic evidence of influenza A and B viruses in South American fur seals (Arctocephalus australis). Journal of Wildlife Diseases 45:519-521CrossRefPubMedGoogle Scholar
  5. Bodewes R, Morick D, de Mutsert G, Osinga N, Bestebroer T, van der Vliet S, et al. (2013) Recurring influenza B virus infections in seals. Emerging Infectious Diseases 19:511-512CrossRefPubMedPubMedCentralGoogle Scholar
  6. de Boer GF, Back W, Osterhaus AD (1990) An ELISA for detection of antibodies against influenza A nucleoprotein in humans and various animal species. Archives of Virology 115:47-61CrossRefPubMedGoogle Scholar
  7. Callan RJ, Early G, Kida H, Hinshaw VS (1995) The appearance of H3 influenza viruses in seals. Journal of General Virology 76:199-203CrossRefPubMedGoogle Scholar
  8. Calle PP, Seagars DJ, McClave C, Senne D, House C, House JA (2002) Viral and bacterial serology of free-ranging Pacific walrus. Journal of Wildlife Diseases 38:93-100CrossRefPubMedGoogle Scholar
  9. Calle PP, Seagars DJ, McClave C, Senne D, House C, House JA (2008) Viral and bacterial serology of six free-ranging bearded seals Erignathus barbatus. Diseases of Aquatic Organisms 81:77-80CrossRefPubMedGoogle Scholar
  10. Danner GR, McGregor MW, Zarnke RL, Olsen CW (1998) Serologic evidence of influenza virus infection in a ringed seal (Phoca hispida) from Alaska. Marine Mammal Science 14:380-384CrossRefGoogle Scholar
  11. Duignan PJ (2000) Diseases in New Zealand sea mammals. Surveillance 27:9-15Google Scholar
  12. Fouchier RAM, Bestebroer TM, Martina BEE, Rimmelzwaan GF, Osterhaus ADME (2001) Infection of grey seals and harbour seals with influenza B virus. International Congress Series 1219:225-231CrossRefGoogle Scholar
  13. Fujii K, Kakumoto C, Kobayashi M, Saito S, Kariya T, Watanabe Y, et al. (2007) Serological evidence of influenza A virus infection in Kuril harbor seals (Phoca vitulina stejnegeri) of Hokkaido, Japan. The Journal of Veterinary Medical Science 69:259-263CrossRefPubMedGoogle Scholar
  14. Geraci JR, St Aubin DJ, Barker IK, Webster RG, Hinshaw VS, Bean WJ, et al. (1982) Mass mortality of harbor seals: pneumonia associated with influenza A virus. Science 215:1129-1131CrossRefPubMedGoogle Scholar
  15. Goldstein T, Mena I, Anthony SJ, Medina R, Robinson PW, Greig DJ, et al. (2013) Pandemic H1N1 influenza isolated from free-ranging Northern Elephant Seals in 2010 off the central California coast. PLoS One 15;8(5):e62259CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hinshaw VS, Air GM, Gibbs AJ, Graves L, Prescott B, Karunakaran D (1982) Antigenic and genetic characterization of a novel hemagglutinin subtype of influenza A viruses from gulls. Journal of Virology 42:865-872PubMedPubMedCentralGoogle Scholar
  17. Hinshaw VS, Bean WJ, Webster RG, Rehg JE, Fiorelli P, Early G, et al. (1984) Are seals frequently infected with avian influenza viruses? Journal of Virology 51:863-865PubMedPubMedCentralGoogle Scholar
  18. Hinshaw VS, Bean WJ, Geraci JR, Fiorelli P, Early G, Webster RG (1986) Characterization of two influenza A viruses from a pilot whale. Journal of Virology 58:655-656PubMedPubMedCentralGoogle Scholar
  19. Hunt TD, Ziccardi MH, Gulland FM, Yochem PK, Hird DW, Rowles T, et al. (2008) Health risks for marine mammal workers. Diseases of Aquatic Organisms 81:81-92CrossRefPubMedGoogle Scholar
  20. Ito T, Kawaoka Y, Nomura A, Otsuki K (1999) Receptor specificity of influenza A viruses from sea mammals correlates with lung sialyloligosaccharides in these animals. The Journal of Veterinary Medical Science 61:955-958CrossRefPubMedGoogle Scholar
  21. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, et al. (2006) Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nature Medicine 12:1203-1207CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kida H, Brown LE, Webster RG (1982) Biological activity of monoclonal antibodies to operationally defined antigenic regions on the hemagglutinin molecule of A/Seal/Massachusetts/1/80 (H7N7) influenza virus. Virology 122:38-47CrossRefPubMedGoogle Scholar
  23. Lang G, Gagnon A, Geraci JR (1981) Isolation of an influenza A virus from seals. Archives of Virology 68:189-195CrossRefPubMedGoogle Scholar
  24. Li SQ, Orlich M, Rott R (1990) Generation of seal influenza virus variants pathogenic for chickens, because of hemagglutinin cleavage site changes. Journal of Virology 64:3297-3303PubMedPubMedCentralGoogle Scholar
  25. Lvov DK, Zdanov VM, Sazonov AA, Braude NA, Vladimirtceva EA, Agafonova LV, et al. (1978) Comparison of influenza viruses isolated from man and from whales. Bulletin of the World Health Organization 56:923-930PubMedPubMedCentralGoogle Scholar
  26. Lynch M, Nielsen O, Duignan PJ, Kirkwood R, Hoskins A, Arnould JP (2011) Serologic survey for potential pathogens and assessment of disease risk in Australian fur seals. Journal of Wildlife Diseases 47:555-565CrossRefPubMedGoogle Scholar
  27. Mandler J, Gorman OT, Ludwig S, Schroeder E, Fitch WM, Webster RG, et al. (1990) Derivation of the nucleoproteins (NP) of influenza A viruses isolated from marine mammals. Virology 176:255-261CrossRefPubMedGoogle Scholar
  28. Murphy BR, Harper J, Sly DL, London WT, Miller NT, Webster RG (1983) Evaluation of the A/Seal/Mass/1/80 virus in squirrel monkeys. Infection and Immunity 42:424-426PubMedPubMedCentralGoogle Scholar
  29. Naeve CW, Webster RG (1983) Sequence of the hemagglutinin gene from influenza virus A/Seal/Mass/1/80. Virology 129:298-308CrossRefPubMedGoogle Scholar
  30. Nielsen O, Clavijo A, Boughen JA (2001) Serologic evidence of influenza A infection in marine mammals of arctic Canada. Journal of Wildlife Diseases 37:820-825CrossRefPubMedGoogle Scholar
  31. Ohishi K (2002) Influenza virus infection in marine mammals. Otsuchi Marine Science 27:7-12Google Scholar
  32. Ohishi K, Ninomiya A, Kida H, Park CH, Maruyama T, Arai T, et al. (2002) Serological evidence of transmission of human influenza A and B viruses to Caspian seals (Phoca caspica). Microbiolgy and Immunology 46:639-644CrossRefGoogle Scholar
  33. Ohishi K, Kishida N, Ninomiya A, Kida H, Takada Y, Miyazaki N, et al. (2004) Antibodies to human-related H3 influenza A virus in Baikal seals (Phoca sibirica) and ringed seals (Phoca hispida) in Russia. Microbiolgy and Immunology 48:905-909CrossRefGoogle Scholar
  34. Ohishi K, Maruyama T, Ninomiya A, Kida H, Zenitani R, Bando T, et al. (2006) Serologic investigation of influenza a virus infection in cetaceans from the western North Pacific and the Southern Oceans. Marine Mammal Science 22:214-221CrossRefGoogle Scholar
  35. Osterhaus AD, Rimmelzwaan GF, Martina BE, Bestebroer TM, Fouchier RA (2000) Influenza B virus in seals. Science 288:1051-1053CrossRefPubMedGoogle Scholar
  36. Reperant AL, Osterhaus AD, Kuiken T (2012) Influenza in aquatic mammals. In: Infectious diseases of wild animals and birds in Europe, Gavier-Widen D, Meredith A, Duff JP (editors), Wiley-Blackwell Press, pp 53–55Google Scholar
  37. Reperant LA, Rimmelzwaan GF, Kuiken T (2009). Avian influenza viruses in mammals. Revue scientifique et technique 28:137-159CrossRefPubMedGoogle Scholar
  38. Ramis AJ, van Riel D, van de Bildt MW, Osterhaus A, Kuiken T (2012) Influenza A and B virus attachment to respiratory tract in marine mammals. Emerging Infectious Diseases 18:817-820CrossRefPubMedPubMedCentralGoogle Scholar
  39. Scheiblauer H, Kendal AP, Rott R (1995) Pathogenicity of influenza A/Seal/Mass/1/80 virus mutants for mammalian species. Archives of Virology 140:341-348CrossRefPubMedGoogle Scholar
  40. Stuen S, Have P, Osterhaus AD, Arnemo JM, Moustgaard A (1994) Serological investigation of virus infections in harp seals (Phoca groenlandica) and hooded seals (Cystophora cristata). Veterinary Record 134:502-503CrossRefPubMedGoogle Scholar
  41. Taylor HR, Turner AJ (1977) A case report of fowl plague keratoconjunctivitis. British Journal of Ophthalmology 61:86-88CrossRefPubMedPubMedCentralGoogle Scholar
  42. Tryland M, Lunestad B, Nesbakken T, Robertson L, Skjerve E, Grahek-Ogden D (2011) Human pathogens in marine mammal meat. Norwegian Scientific Committee for Food Safety. Document number: 08/108-final.Google Scholar
  43. Van Bressem MF, Van Waerebeek K, Raga JA (1999) A review of virus infections of cataceans and the potential impact of morbilliviruses, poxviruses and papillomaviruses on host population dynamics. Diseases of Aquatic Organisms 38:53-65CrossRefPubMedGoogle Scholar
  44. Waltzek TB, Cortés-Hinojosa G, Wellehan JF Jr, Gray GC (2012) Marine mammal zoonoses: a review of disease manifestations. Zoonoses and Public Health 59:521-535CrossRefPubMedGoogle Scholar
  45. Webster RG, Hinshaw VS, Bean WJ, Van Wyke KL, Geraci JR, St Aubin DJ, et al. (1981a) Characterisation of an influenza A virus from seals. Virology 113:712-724CrossRefPubMedGoogle Scholar
  46. Webster RG, Geraci J, Petursson G, Skirnisson K (1981b) Conjunctivitis in human beings caused by influenza A virus of seals. The New England Journal of Medicine 304:911PubMedGoogle Scholar
  47. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiology and Molecular Biology Reviews 56:152-179Google Scholar

Copyright information

© International Association for Ecology and Health 2014

Authors and Affiliations

  • Sasan Fereidouni
    • 1
    • 2
  • Olga Munoz
    • 3
  • Sophie Von Dobschuetz
    • 4
    • 5
  • Marco De Nardi
    • 3
    • 6
  1. 1.Friedrich-Loeffler-Institute, Federal Research Institute for Animal HealthRiemsGermany
  2. 2.WESCA Wildlife NetworkGreifswaldGermany
  3. 3.Istituto Zooprofilattico Sperimentale delle VeneziePaduaItaly
  4. 4.Food and Agriculture Organization of the United Nations (FAO)RomeItaly
  5. 5.Royal Veterinary College (RVC)LondonUK
  6. 6.SAFOSO AGBernSwitzerland

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