Prevalence of influenza A virus in live-captured North Atlantic gray seals: A possible wild reservoir

Emerging Microbes and Infections

Volumn 5, Issue 8, 2016, Pages

  Puryear, Wendy Blay ^a   Keogh, Mandy ^b   Hill, Nichola ^a   Moxley, Jerry ^c   Josephson, Elizabeth ^d   Davis, Kimberly Ryan ^a   Bandoro, Chistopher ^a   Lidgard, Damian ^e   Bogomolni, Andrea ^f   Levin, Milton ^g   Lang, Shelley ^h   Hammill, Michael ^h   Bowen, Don ^h   Johnston, David W ^c   Romano, Tracy ^b   Waring, Gordon ^d   Runstadler, Jonathan ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Mystic Aquarium and Institute for Exploration   (United States)

^c DUKE UNIVERSITY   (United States)

^d NORTHEAST FISHERIES SCIENCE CENTER   (United States)

^e DALHOUSIE UNIVERSITY   (Canada)

^f WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^g UNIVERSITY OF CONNECTICUT   (United States)

^h FISHERIES AND OCEANS CANADA   (Canada)

Author keywords

gray seal; Halichoerus grypus; influenza; pinniped; reservoir; telemetry

Indexed keywords

VIRUS RNA; VIRUS ANTIBODY;

ADULT; ANIMAL HEALTH; ARTICLE; CANADA; CONTROLLED STUDY; ENDEMIC DISEASE; FORAGING; HALICHOERUS GRYPUS; HEMAGGLUTINATION INHIBITION; INFLUENZA A; NONHUMAN; NORTH AMERICA; NOVA SCOTIA; PREVALENCE; PRIORITY JOURNAL; SEROPREVALENCE; VIRUS CARRIER; VIRUS DETECTION; VIRUS SHEDDING; ANIMAL; BLOOD; DISEASE CARRIER; EPIDEMIOLOGICAL MONITORING; GENETICS; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS; INFLUENZA, HUMAN; ISOLATION AND PURIFICATION; ORTHOMYXOVIRIDAE INFECTIONS; PHOCIDAE; POLYMERASE CHAIN REACTION; TELEMETRY; TRANSMISSION; UNITED STATES; VETERINARY; VIROLOGY; WILD ANIMAL;

ANIMALS; ANIMALS, WILD; ANTIBODIES, VIRAL; CANADA; DISEASE RESERVOIRS; EPIDEMIOLOGICAL MONITORING; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; NOVA SCOTIA; ORTHOMYXOVIRIDAE INFECTIONS; POLYMERASE CHAIN REACTION; PREVALENCE; RNA, VIRAL; SEALS, EARLESS; TELEMETRY; UNITED STATES;

EID: 84981314722     PISSN: None     EISSN: 22221751     Source Type: Journal    
DOI: 10.1038/emi.2016.77     Document Type: Article

References (63)

1. Greig DJ. Health, disease, mortality and survival in wild, rehabilitated harbor seals (Phoca vitulina) inthe San Francisco Bay area and along the central California coast. PhD thesis, University of St Andrews, St Andrews, UK, 2011.
2. Goldstein T, Mena I, Anthony SJ, et al. Pandemic H1N1 influenza isolated from freeranging Northern Elephant Seals in 2010 off the central California coast. PLoS One 2013; 8: 1-9.
3. Anthony SJ, St Leger JA, Pugliares K, et al. Emergence of fatal avian influenza in New England harbor seals. MBio 2012; 3: 1-9.
4. Blanc A, Ruchansky D, Clara M, et al. Serologic evidence of influenza A and B viruses in South American fur seals (Arctocephalus australis). J Wildl Dis 2009; 45: 519-521.
5. Osterhaus ADME, Rimmelzwaan GF, Martina BEE, Bestebroer TM, Fouchier RAM. Influenza B virus in seals. Science 2000; 288: 1051-1053.
6. Ohishi K, Kishida N, Ninomiya A, et al. Antibodies to human-related H3 influenza A virus in Baikal seals (Phoca sibirica) and ringed seals (Phoca hispida) in Russia. Microbiol Immunol 2004; 48: 905-909.
7. Webster RG, Hinshaw VS, Bean WJ, et al. Characterization of an influenza A virus from seals. Virology 1981; 113: 712-724.
8. Hinshaw VS, Bean WJ, Webster RG, et al. Are seals frequently infected with avian influenza viruses ? J Virol 1984; 51: 863-865.
9. Callan RJ, Early G, Kida H, Hinshaw VS. The appearance of H3 influenza viruses in seals. J Gen Virol 1995; 76: 199-203.
10. Runstadler J, Hill N, Hussein ITM, Puryear W, Keogh M. Connecting the study of wild influenza with the potential for pandemic disease. Infect Genet Evol 2013; 17: 162-187.
11. Zohari S, Neimanis A, Harkonen T, Moraeus C, Valarcher J. Avian influenza A(H10N7) virus involvement in mass mortality of harbour seals (Phoca vitulina) in Sweden, March through October 2014. Eurosurveillance 2014; 19: 1-6.
12. Bodewes R, Bestebroer TM, van der Vries E, et al. Avian influenza A(H10N7) virusassociated mass deaths among harbor seals. Emerg Infect Dis 2015; 21: 720-722.
13. Krog JS, Hansen MS, Holm E, et al. Influenza A(H10N7) virus in dead harbor seals, Denmark. Emerg Infect Dis J 2015; 21: 684-687.
14. Fereidouni S, Munoz O, Von Dobschuetz S, De Nardi M. Influenza virus infection of marine mammals. Ecohealth 2016; 13: 161-170.
15. Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus ADME, et al. Global patterns of influenza a virus in wild birds. Science 2006; 312: 384-388.
16. Bodewes R, Garcia AR, Brasseur SM, Sanchez GJ. Seroprevalence of antibodies against seal influenza A (H10N7) virus in harbor seals and gray seals from the Netherlands. PLoS One 2015; 10: 1-9.
17. Mandl JN, Ahmed R, Barreiro LB, et al. Reservoir host immune responses to emerging zoonotic viruses. Cell 2014; 160: 20-35.
18. Bean AGD, Baker ML, Stewart CR, et al. Studying immunity to zoonotic diseases in the natural host -keeping it real. Nat Rev Immunol 2013; 13: 851-861.
19. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK. Identifying reservoirs of infection : a conceptual and practical challenge. Emerg Infect Dis 2002; 8: 1468-1473.
20. Peiris JSM, Poon LLM, Guan Y. Surveillance of animal influenza for pandemic preparedness. Science 2012; 335: 1173-1174.
21. Richard M, De Graaf M, Herfst S. Avian influenza A viruses: from zoonosis to pandemic. Future Virol 2014; 9: 513-524.
22. Taubenberger JK, Morens DM. Influenza: the once and future pandemic. Public Health Rep 2010; 125: 16-26.
23. Bowen WD, Den Heyer C, Hammil M. Pup production at Scotian Shelf Grey Seal (Halichoerus grypus) colonies in 2010. Canadian Stock Assessment Secretariat. Can Sci Advis Secr Res Doc 2011; 2011/066: 1-31.
24. Natural Environment Research Council. Scientific Advice on Matters Related to the Management of Seal Populations: 2014. SCOS: UK, 2014. Available at http://www. smru.st-andrews.ac.uk/documents/2589.pdf.
25. Waring GT, Josephson E, Maze-Foley K, Rosel PE, editors. US Atlantic and Gulf of Mexico Marine Mammal Stock Assessments -2014, 169-177. US: NOAA, 2015. Available at http://www.nefsc.noaa.gov/publications/tm/tm231/169-grayseal- F2014August.pdf.
26. Roman J, Dunphy-Daly MM, Johnston DW, Read AJ. Lifting baselines to address the consequences of conservation success. Trends Ecol Evol 2015; 30: 299-302.
27. Johnston DW, Frungillo J, Smith A, et al. Trends in stranding and by-catch rates of gray and harbor seals along the Northeastern coast of the United States: evidence of divergence in the abundance of two sympatric Phocid species? PLoS One 2015; 10: 1-12.
28. Brasseur S, Czeck R, Diederichs B, et al. Grey Seal surveys in the Wadden Sea and Helgoland in 2014-2015. Common Wadden Sea Secretariat: Wilhelmshaven, Germany, 2014. Available at http://www.waddensea-secretariat.org/sites/default/files/downloads/tmap/MarineMammals/GreySeals/grey-seal-report-2015.pdf.
29. Rifkin JL, Nunn CL, Garamszegi LZ. Do animals living in larger groups experience greater parasitism? A meta-analysis. Am Nat 2012; 180: 70-82.
30. Harkonen T, Dietz R, Reijnders P, et al. The 1988 and 2002 phocine distemper virus epidemics in European harbour seals. Dis Aquat Organ 2006; 68: 115-130.
31. Geraci JR, St Aubin DJ, Barker IK, et al. Mass mortality of harbor seals: pneumonia associated with influenza A virus. Science 1982; 215: 1129-1131.
32. Boness DJ, James H. Reproductive behaviour of the Grey seal (Halichoerus grypus) on Sable Island, Nova Scotia. J Zool 1979; 188: 477-500.
33. Murray MJ. Behavioral Interactions Between Harbor Seals (Phoca vitulina) and Gray Seals (Halichoerus grypus) on Cape Cod, Massachusetts, Northeastern University: Boston, MA, USA, 2008. Available at http://hdl.handle.net/2047/d10016624.
34. Thompson D, Onoufriou J, Bronlow A, Bishop A. Marine Mammal Scientific Support Research Programme MMSS/001/11. Preliminary report on predation by adult grey seals on grey seal pups as a possible explanation for corkscrew injury patterns seen in the unexplained seal deaths: addendum. UK: Sea Mammal Research Unit, 2015. Available at http://www.smru.st-andrews.ac.uk/documents/scotgov/USD1and6-addendum- report-VF2.pdf.
35. Van Neer A, Jensen LF, Siebert U. Grey seal (Halichoerus grypus) predation on harbour seals (Phoca vitulina) on the island of Helgoland, Germany. J Sea Res 2015; 97: 1-4.
36. Stringell T, Hill D, Rees D, Rees F, Rees P, et al.. Short note: predation of harbour porpoises (Phocoena phocoena) by grey seals (Halichoerus grypus) in Wales. Aquat Mamm 2015; 41: 188-191.
37. Haelters J, Kerckhof F, Jauniaux T, Degraer S. The grey seal (Halichoerus grypus) as a predator of harbour porpoises (Phocoena phocoena)? Aquat Mamm 2012; 38: 343-353.
38. Grant DR, Bourne WRP. Grey Seals and Seabirds. The Seabird Group: Aberdeen, 1971-1972, pp. 52-53. Available at http://www.seabirdgroup.org.uk/journals/seabird-3.pdf.
39. Lucas Z, McLaren IA. Apparent predation by grey seals, Halichoerus grypus, on seabirds around Sable Island, Nova Scotia. Can Field-Naturalist 1988; 102: 675-678.
40. Bowen WD, McMillan J, Mohn R. Sustained exponential population growth of grey seals at Sable Island, Nova Scotia. ICES J Mar Sci 2003; 60: 1265-1274.
41. Jessopp M, Cronin M, Hart T. Habitat-mediated dive behavior in free-ranging grey seals. PLoS One 2013; 8: 1-7.
42. Lidgard DC, Bowen WD, Jonsen ID, Iverson SJ. Animal-borne acoustic transceivers reveal patterns of at-sea associations in an upper-trophic level predator. PLoS One 2012; 7: 1-8.
43. Spackman E, Senne DA, Myers TJ, et al. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the Avian H5 and H7 hemagglutinin subtypes development of a real-time reverse transcriptase PCR assay for type A influenza virus and the Avian H5 and H7 hemagglutini. J Clin Microbiol 2002; 40: 3256-3260.
44. Slomka MJ, Densham ALE, Coward VJ, et al. Real time reverse transcription (RRT)-polymerase chain reaction (PCR) methods for detection of pandemic (H1N1) 2009 influenza virus and European swine influenza A virus infections in pigs. Influenza Other Respi Viruses 2010; 4: 277-293.
45. USDA Wildlife Services. USDA/APHIS/Wildlife Services Instructions for NAHLN Laboratories Testing Wild Bird Samples. Manhattan: USDA, 2010. Available at https://www.aphis.usda.gov/wildlife-damage/nwdp/pdf/2010%20NAHLN%20labs%20 testing%20WS%20wild%20bird%20samples.pdf.
46. Munster VJ, Baas C, Lexmond P, et al. Practical considerations for high-throughput influenza A virus surveillance studies of wild birds by use of molecular diagnostic tests. J Clin Microbiol 2009; 47: 666-673.
47. Moresco KA, Stallknecht DE, Swayne DE. Evaluation of different embryonating bird eggs and cell cultures for isolation efficiency of avian Influenza A Virus and Avian paramyxovirus serotype 1 from real-time reverse transcription polymerase chain reaction-positive wild bird surveillance samples. J Vet Diagn Invest 2012; 24: 563-567.
48. Lindsay LL, Kelly TR, Plancarte M, et al. Avian influenza: mixed infections and missing viruses. Viruses 2013; 5: 1964-1977.
49. Brown JD, Poulson R, Carter DL, Lebarbenchon C, Stallknecht DE. Infectivity of avian influenza virus-positive field samples for mallards: what do our diagnostic results mean? J Wildl Dis 2013; 49: 180-185.
50. Lin HT, Hsu CH, Tsai HJ, et al. Influenza A plasma and serum virus antibody detection comparison in dogs using blocking enzyme-linked immunosorbent assay. Vet World 2015; 8: 580-583.
51. Shriner SA, VanDalen KK, Root JJ, Sullivan HJ. Evaluation and optimization of a commercial blocking ELISA for detecting antibodies to influenza A virus for research and surveillance of mallards. J Virol Methods 2016; 228: 130-134.
52. Pederson JC. Hemagglutination inhibition test for avian influenza virus subtype identification and the detection and quantitation of serum antibodies to the avian influenza virus. In: Spackman E (ed). Avian Influenza Virus. Totowa, New Jersey: Humana Press; 2004, pp 53-66.
53. Killian ML. Hemagglutination assay for the avian influenza virus. In: Spackman E (ed). Avian Influenza Virus. Totowa, New Jersey: Humana Press; 2004, pp 47-52.
54. Cox N, Webster RG, Krauss S, et al. WHO Manual on Animal Influenza Diagnosis and Surveillance, 2nd edn, Geneva: WHO, 2002. Available at http://www.who.int/csr/resources/publications/influenza/whocdscsrncs20025rev.pdf.
55. Eriksson L, Andersson PL, Johansson E, Tysklind M. Megavariate analysis of environmental QSAR data. Part I -a basic framework founded on principal component analysis (PCA), partial least squares (PLS), and statistical molecular design (SMD). Mol Divers 2006; 10: 169-186.
56. Saltelli A. Sensitivity analysis for importance assessment. Risk Anal 2002; 22: 579-590.
57. Lehnert K, Muller S, Weirup L, et al. Molecular biomarkers in grey seals (Halichoerus grypus) to evaluate pollutant exposure, health and immune status. Mar Pollut Bull 2014; 88: 311-318.
58. Beck CA, Bowen WD, McMillan JI, Iverson SJ. Sex differences in the diving behaviour of a size-dimorphic capital breeder: the grey seal. Anim Behav 2003; 66: 777-789.
59. Lidgard DC, Boness DJ, Bowen WD, McMillan JI. Diving behaviour during the breeding season in the terrestrially breeding male grey seal: implications for alternative mating tactics. Can J Zool 2003; 81: 1025-1033.
60. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992; 56: 152-179.
61. Wood SA, Frasier TR, McLeod BA, et al. The genetics of recolonization: an analysis of the stock structure of grey seals (Halichoerus grypus) in the northwest Atlantic. Can J Zool 2011; 89: 490-497.
62. Stallknecht DE, Luttrell MP, Poulson R, et al. Detection of avian influenza viruses from shorebirds: evaluation of surveillance and testing approaches. J Wildl Dis 2012; 48: 382-393.
63. Hinshaw VS, Air GM, Gibbs AJ, et al. Antigenic and genetic characterization of a novel hemagglutinin subtype of influenza A viruses from gulls. J Virol 1982; 42: 865-872.