, Volume 11, Issue 1, pp 94–108 | Cite as

Success Factors for Avian Influenza Vaccine Use in Poultry and Potential Impact at the Wild Bird–Agricultural Interface

  • David E. SwayneEmail author
  • Erica Spackman
  • Mary Pantin-Jackwood


Thirty-two epizootics of high pathogenicity avian influenza (HPAI) have been reported in poultry and other birds since 1959. The ongoing H5N1 HPAI epizootic that began in 1996 has also spilled over to infect wild birds. Traditional stamping-out programs in poultry have resulted in eradication of most HPAI epizootics. However, vaccination of poultry was added as a control tool in 1995 and has been used during five epizootics. Over 113 billion doses of AI vaccine have been used in poultry from 2002 to 2010 as oil-emulsified, inactivated whole AIV vaccines (95.5%) and live vectored vaccines (4.5%). Over 99% of the vaccine has been used in the four H5N1 HPAI enzootic countries: China including Hong Kong (91%), Egypt (4.7%), Indonesia (2.3%), and Vietnam (1.4%) where vaccination programs have been nationwide and routine to all poultry. Ten other countries used vaccine in poultry in a focused, risk-based manner but this accounted for less than 1% of the vaccine used. Most vaccine “failures” have resulted from problems in the vaccination process; i.e., failure to adequately administer the vaccine to at-risk poultry resulting in lack of population immunity, while fewer failures have resulted from antigenic drift of field viruses away from the vaccine viruses. It is currently not feasible to vaccinate wild birds against H5N1 HPAI, but naturally occurring infections with H5 low pathogenicity avian influenza viruses may generate cross-protective immunity against H5N1 HPAI. The most feasible method to prevent and control H5N1 HPAI in wild birds is through control of the disease in poultry with use of vaccine to reduce environmental burden of H5N1 HPAIV, and eventual eradication of the virus in domestic poultry, especially in domestic ducks which are raised in enzootic countries on range or in other outdoor systems having contact with wild aquatic and periurban terrestrial birds.


Avian influenza disease poultry vaccination vaccines wild birds 



The concepts presented in this review paper were initially developed and studied during a sabbatical to World Organization for Animal Health by the senior author (DES) and were refocused by two authors (DES and ES) during a recent workshop titled, Vaccines and Diagnostics for Transboundary Animal Diseases, 17–19 September 2012 held in Ames, Iowa (Swayne and Spackman 2013). The authors thank Drs. M. Jeggo, Peter Daniels, and Colin Butter for the invitation to write this review paper, and the helpful critique from the two reviewers.


  1. Abbas,MA, Spackman E, Fouchier R, Smith D, Ahmed Z, Siddique N, Sarmento L, Naeem K, McKinley ET, Hameed A, Rehmani S, Swayne DE (2011) H7 avian influenza virus vaccines protect chickens against challenge with antigenically diverse isolates. Vaccine 29:7424-7429.PubMedCrossRefGoogle Scholar
  2. Becker,WB (1967) Experimental infection of common terns with Tern virus: influenza virus A-Tern-South Africa-1961. Journal of Hygiene 65:61-65.PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bertelsen,MF, Klausen J, Holm E, Grondahl C, Jorgensen PH (2007) Serological response to vaccination against avian influenza in zoo-birds using an inactivated H5N9 vaccine. Vaccine 25:4345-4349.PubMedCrossRefGoogle Scholar
  4. Boltz,DA, Douangngeun B, Sinthasak S, Phommachanh P, Midouangchanh P, Walker D, Keating R, Khalenkov AM, Kumar M, Webster RG (2009) Field assessment of an H5N1 inactivated vaccine in chickens and ducks in Lao PDR. Archives of Virology 154:939-944.PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bouma,A, Muljono AT, Jatikusumah A, Nell A, Mudjiartiningsih S, Dharmayanti I, Siregar E Sawitri, Claassen I, Koch G, Stegeman JA (2008) Field trial for assessment of avian influenza vaccination effectiveness in Indonesia. Revue Scientifique et Technique Office International des Epizooties 27:633-642.Google Scholar
  6. Bouma A, Tiensin T, Claassen I, Nielen M, van Boven M, Stegeman JA (2007) Estimation of the Critical Proportion of Chickens in a Flock to be Immunized to Prevent Major Outbreaks of HPAI H5N1. OIE/FAO/IZSVe Scientific Conference—Vaccination: a tool for the control of avian influenza, 20–22 March 2007, Verona, Italy, p 60Google Scholar
  7. Breedlove,C, Minc JK, Tang DC, van Santen VL, van Ginkel FW, Toro H (2011) Avian influenza adenovirus-vectored in ovo vaccination: target embryo tissues and combination with Marek’s disease vaccine. Avian Diseases 55:667-673.PubMedCrossRefGoogle Scholar
  8. Brown,JD, Stallknecht DE, Berghaus RD, Swayne DE (2009) Infectious and lethal doses of H5N1 highly pathogenic Avian influenza virus for house sparrows (Passer domesticus) and rock pigeons (Columbia livia). Journal of Veterinary Diagnostic Investigation 21:437-445.PubMedCrossRefGoogle Scholar
  9. Brugh,M, Beard CW, Stone HD (1979) Immunization of chickens and turkeys against avian influenza with monovalent and polyvalent oil emulsion vaccines. American Journal of Veterinary Research 40:165-169.PubMedGoogle Scholar
  10. Bublot,M, Pritchard N, Swayne DE, Selleck P, Karaca K, Suarez DL, Audonnet JC, Mickle TR (2006) Development and use of fowlpox vectored vaccines for avian influenza. Annals of the New York Academy of Sciences 1081:193-201.PubMedCrossRefGoogle Scholar
  11. Bublot,M, Richard-Mazet A, Chanavat-Bizzini S, Le Gros FX, Duboeuf M, Stoll A, Palfi V, Niqueux E, Guionie O, Dren N (2010) Immunogenicity of poxvirus vector avian influenza vaccines in muscovy and pekin ducks. Avian Diseases 54:232-238.PubMedCrossRefGoogle Scholar
  12. Cagle,C, To TL, Nguyen T, Wasilenko J, Adams SC, Cardona CJ, Spackman E, Suarez DL, Pantin-Jackwood MJ (2011) Pekin and Muscovy ducks respond differently to vaccination with a H5N1 highly pathogenic avian influenza (HPAI) commercial inactivated vaccine. Vaccine 29:6549-6557.PubMedCrossRefGoogle Scholar
  13. Cattoli G, Monne I, Fusaro A, Joannis TM, Lombin LH, Aly MM, Arafa AS, Sturm-Ramirez KM, Couacy-Hymann E, Awuni JA, Batawui KB, Awoume KA, Aplogan GL, Sow A, Ngangnou AC, El Nh I, Gamatie D, Dauphin G, Domenech JM, Capua I (2009) Highly pathogenic avian influenza virus subtype H5N1 in Africa: a comprehensive phylogenetic analysis and molecular characterization of isolates. PLoS One 4:e4842Google Scholar
  14. CEVA (2013) Ceva develops Vectormune HVT AIV vaccine to combat avian influenza. Accessed on March 21, 2013 from
  15. Chambers,TM, Kawaoka Y, Webster RG (1988) Protection of chickens from lethal influenza infection by vaccine-expressed hemagglutinin. Virology 167:414-421.PubMedCrossRefGoogle Scholar
  16. Chen,H (2009) Avian influenza vaccination: the experience in China. Revue Scientifique et Technique - Office International des Epizooties 28:267-274.Google Scholar
  17. Costa,TP, Brown JD, Howerth EW, Stallknecht DE (2010) 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 Diseases 54:1286-1291.PubMedCrossRefGoogle Scholar
  18. Crawford,J, Wilkinson B, Vosnesensky A, Smith G, Garcia M, Stone H, Perdue ML (1999) Baculovirus-derived hemagglutinin vaccines protect against lethal influenza infections by avian H5 and H7 subtypes. Vaccine 17:2265-2274.PubMedCrossRefGoogle Scholar
  19. EFSA (2007) Opinion of the Scientific Panel on Animal Health and Welfare (AHAW) on a request from the Commission related with the vaccination against avian influenza of H5 and H7 subtypes as a preventive measure carried out in Member States in birds kept in zoos under Community approved programmes. The EFSA Journal 450. Accessed on 19 July, 2011 from doi: 10.2903/j.efsa.2007.450
  20. Eggert,D, Swayne DE (2010) Single vaccination provides limited protection to ducks and geese against H5N1 high pathogenicity avian influenza virus. Avian Diseases 54:1224-1229.PubMedCrossRefGoogle Scholar
  21. Eggert,D, Thomas C, Spackman E, Pritchard N, Rojo F, Bublot M, Swayne DE (2010) Characterization and efficacy determination of commercially available Central American H5N2 avian influenza vaccines for poultry. Vaccine 28:4609-4615.PubMedCrossRefGoogle Scholar
  22. Ellis,TM, Barry BR, Bissett LA, Dyrting KC, Luk GSM, Tsim ST, Sturm-Ramirez K, Webster RG, Guan Y, Peiris JSM (2004) Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002. Avian Pathology 33:492-505.PubMedCrossRefGoogle Scholar
  23. Ely,CR, Hall JS, Schmutz JA, Pearce JM, Terenzi J, Sedinger JS, Ip HS (2013) Evidence that Life History Characteristics of Wild Birds Influence Infection and Exposure to Influenza A Viruses. PLoS ONE 8:e57614.PubMedCentralPubMedCrossRefGoogle Scholar
  24. Escorcia,M, Vazquez L, Mendez ST, Rodriguez-Ropon A, Lucio E, Nava GM (2008) Avian influenza: genetic evolution under vaccination pressure. Virology Journal 5:15.PubMedCentralPubMedCrossRefGoogle Scholar
  25. Feare,CJ (2010) Role of wild birds in the spread of highly pathogenic avian influenza virus H5N1 and implications for global surveillance. Avian Diseases 54:201-212.PubMedCrossRefGoogle Scholar
  26. Furger,M, Hoop R, Steinmetz H, Eulenberger U, Hatt J (2008) Humoral immune response to avian influenza vaccination over a six-month period in different species of captive wild birds. Avian Diseases 52:222-228.PubMedCrossRefGoogle Scholar
  27. Gao,W, Soloff AC, Lu X, Montecalvo A, Nguyen DC, Matsuoka Y, Robbins PD, Swayne DE, Donis RO, Katz JM, Barratt-Boyes SM, Gambotto A (2006) Protection of mice and poultry from lethal H5N1 avian influenza virus through adenovirus-based immunization. Journal of Virology 80:1959-1964.PubMedCentralPubMedCrossRefGoogle Scholar
  28. Ge,J, Deng G, Wen Z, Tian G, Wang Y, Shi J, Wang X, Li Y, Hu S, Jiang Y, Yang C, Yu K, Bu Z, Chen H (2007) Newcastle disease virus-based live attenuated vaccine completely protects chickens and mice from lethal challenge of homologous and heterologous H5N1 avian influenza viruses. Journal of Virology 81:150-158.PubMedCentralPubMedCrossRefGoogle Scholar
  29. Gilbert,M, Xiao X, Pfeiffer DU, Epprecht M, Boles S, Czarnecki C, Chaitaweesub P, Kalpravidh W, Minh PQ, Otte MJ, Martin V, Slingenbergh J (2008) Mapping H5N1 highly pathogenic avian influenza risk in Southeast Asia. Proceedings of the National Academy of Sciences of the United States of America 105:4769-4774.PubMedCentralPubMedCrossRefGoogle Scholar
  30. Goot,JA, Koch G, Jong MC, Boven Mv (2003) Transmission dynamics of low- and high-pathogenicity A/Chicken/Pennsylvania/83 avian influenza viruses. Avian Diseases 47:939-941.PubMedCrossRefGoogle Scholar
  31. Grund C, Abdelwhab E, Arafa AS, Ziller M, Hassan MK, Aly MM, Hafez HM, Harder TC, Beer M (2011) Highly pathogenic avian influenza virus H5N1 from Egypt escapes vaccine-induced immunity but confers clinical protection against a heterologous clade 2.2.1 Egyptian isolate. Vaccine 29:5567–5573Google Scholar
  32. Guan,Y, Smith GJD, Webby R, Webster RG (2009) Molecular epidemiology of H5N1 avian influenza. Revue Scientifique et Technique Office International des Epizooties 28:39-47.Google Scholar
  33. Hulse-Post,DJ, Sturm-Ramirez KM, Humberd J, Seiler P, Govorkova EA, Krauss S, Scholtissek C, Puthavathana P, Buranathai C, Nguyen TD, Long HT, Naipospos TSP, Chen H, Ellis TM, Guan Y, Peiris JSM, Webster RG (2005) Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proceedings of the National Academy of Sciences of the United States of America 102:10682-10687.PubMedCentralPubMedCrossRefGoogle Scholar
  34. Hunt,LA, Brown DW, Robinson HL, Naeve CW, Webster RG (1988) Retrovirus-expressed hemagglutinin protects against lethal influenza virus infections. Journal of Virology 62:3014-3019.PubMedCentralPubMedGoogle Scholar
  35. Hwang,SD, Kim HS, Cho SW, Seo SH (2011) Single dose of oil-adjuvanted inactivated vaccine protects chickens from lethal infections of highly pathogenic H5N1 influenza virus. Vaccine 29:2178-2186.PubMedCrossRefGoogle Scholar
  36. Kalthoff,D, Giritch A, Geisler K, Bettmann U, Klimyuk V, Hehnen HR, Gleba Y, Beer M (2010) Immunization with plant-expressed hemagglutinin protects chickens from lethal highly pathogenic avian influenza virus H5N1 challenge infection. Journal of Virology 84:12002-12010.PubMedCentralPubMedCrossRefGoogle Scholar
  37. Keawcharoen,J, van Riel D, van Amerongen G, Bestebroer T, Beyer WE, van Lavieren R, Osterhaus Albert DME, Fouchier Ron AM, Kuiken T (2008) Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5NI). Emerging Infectious Diseases 14:600-607.PubMedCentralPubMedCrossRefGoogle Scholar
  38. Kilany WH, Abdelwhab EM, Arafa AS, Selim A, Safwat M, Nawar AA, Erfan AM, Hassan MK, Aly MM, Hafez HM (2011) Protective efficacy of H5 inactivated vaccines in meat turkey poults after challenge with Egyptian variant highly pathogenic avian influenza H5N1 virus. Veterinary Microbiology 150:28–34Google Scholar
  39. Kim,JK, Negovetich NJ, Forrest HL, Webster RG (2009) Ducks: the “Trojan horses” of H5N1 influenza. Influenza and other Respiratory Viruses 3:121-128.PubMedCentralPubMedCrossRefGoogle Scholar
  40. Koch,G, Steensels M, Berg Tvd (2009) Vaccination of birds other than chickens and turkeys against avian influenza. Revue Scientifique et Technique - Office International des Epizooties 28:307-318.Google Scholar
  41. Kou Z, Lei FM, Yu J, Fan ZJ, Yin ZH, Jia C, X, Xiong KJ, Sun YH, Zhang XW, Wu XM, Gao XB, Li TX (2005) New genotype of avian influenza H5N1 viruses isolated from tree sparrows in China. Journal of Virology 79:15460–15466Google Scholar
  42. Layton,SL, Kapczynski DR, Higgins S, Higgins J, Wolfenden AD, Liljebjelke KA, Bottje WG, Swayne D, Berghman LR, Kwon YM, Hargis BM, Cole K (2009) Vaccination of chickens with recombinant Salmonella expressing M2e and CD154 epitopes increases protection and decreases viral shedding after low pathogenic avian influenza challenge. Poultry Science 88:2244-2252.PubMedCrossRefGoogle Scholar
  43. Lee,CW, Senne DA, Suarez DL (2004) Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. Journal of Virology 78:8372-8381.PubMedCentralPubMedCrossRefGoogle Scholar
  44. Liu,J, Chen P, Jiang Y, Wu L, Zeng X, Tian G, Ge J, Kawaoka Y, Bu Z, Chen H (2011) A duck enteritis virus-vectored bivalent live vaccine provides fast and complete protection against H5N1 avian influenza virus infection in ducks. Journal of Virology 85:10989-10998.PubMedCentralPubMedCrossRefGoogle Scholar
  45. Maas R, Rosema S, Van ZD, Venema S (2011) Maternal immunity against avian influenza H5N1 in chickens: limited protection and interference with vaccine efficacy. Avian Pathology 40:87–92Google Scholar
  46. Magalhaes,RJS, Pfeiffer DU, Otte J (2010) Evaluating the control of HPAIV H5N1 in Vietnam: virus transmission within infected flocks reported before and after vaccination. BMC Veterinary Research 6:31.CrossRefGoogle Scholar
  47. Middleton,D, Bingham J, Selleck P, Lowther S, Gleeson L, Lehrbach P, Robinson S, Rodenberg J, Kumar M, Andrew M (2007) Efficacy of inactivated vaccines against H5N1 avian influenza infection in ducks. Virology 359:66-71.PubMedCrossRefGoogle Scholar
  48. Nettles,VF, Wood JM, Webster RG (1985) Wildlife surveillance associated with an outbreak of lethal H5N2 avian influenza in domestic poultry. Avian Diseases 29:733-741.PubMedCrossRefGoogle Scholar
  49. Niqueux,E, Guionie O, Schmitz A, Hars J, Jestin V (2010) Presence of serum antibodies to influenza a subtypes H5 and N1 in swans and ibises in French wetlands, irrespective of highly pathogenic H5N1 natural infection. Avian Diseases 54:502-508.PubMedCrossRefGoogle Scholar
  50. OIE (2007) Avian Influenza Vaccination: OIE Information Document And Verona Recommendations. Accessed March 23, 2011 from, Paris: OIE
  51. OIE (2012a) Highly Pathogenic Avian Influenza, Australia (Follow-Up Report No. 1). OIE Disease Information 25(47). Accessed 29 November, 2012 from, Paris: OIE
  52. OIE (2012b) Highly Pathogenic Avian Influenza, Mexico. OIE Disease Information 25(25). Accessed 2 August, 2012 from, Paris: OIE
  53. OIE (2012c) Highly Pathogenic Avian Influenza, Mexico; Follow-Up Report No. 8 (12/12/2012). OIE Disease Information 25(50). Accessed 21 March 2013 from, Paris: OIE
  54. Pan,Z, Zhang X, Geng S, Cheng N, Sun L, Liu B, Huang J, Jiao X (2009) Priming with a DNA vaccine delivered by attenuated Salmonella typhimurium and boosting with a killed vaccine confers protection of chickens against infection with the H9 subtype of avian influenza virus. Vaccine 27:1018-1023.PubMedCrossRefGoogle Scholar
  55. Pantin-Jackwood,MJ, Smith DM, Wasilenko JL, Cagle C, Shepherd E, Sarmento L, Kapczynski DR, Afonso CL (2012) Effect of age on the pathogenesis and innate immune responses in Pekin ducks infected with different H5N1 highly pathogenic avian influenza viruses. Virus Research 167:196-206.PubMedCrossRefGoogle Scholar
  56. Park,MS, Steel J, Garcia-Sastre A, Swayne D, Palese P (2006) Engineered viral vaccine constructs with dual specificity: avian influenza and Newcastle disease. Proceedings of the National Academy of Sciences of the United States of America 103:8203-8208.PubMedCentralPubMedCrossRefGoogle Scholar
  57. Pavade,G, Awada L, Hamilton K, Swayne DE (2011) Analysis of economic indicators, poultry density and performance of veterinary services for control of high pathogenicity avian influenza in poultry. Revue Scientifique et Technique - Office International des Epizooties 30:661-671.Google Scholar
  58. Pavlova,SP, Veits J, Mettenleiter TC, Fuchs W (2009) Live vaccination with an H5-hemagglutinin-expressing infectious laryngotracheitis virus recombinant protects chickens against different highly pathogenic avian influenza viruses of the H5 subtype. Vaccine 27:5085-5090.PubMedCrossRefGoogle Scholar
  59. Pepin,KM, Wang J, Webb CT, Smith GJ, Poss M, Hudson PJ, Hong W, Zhu H, Riley S, Guan Y (2012) Multiannual patterns of influenza A transmission in Chinese live bird market systems. Influenza and other Respiratory Viruses 7:97-107.PubMedCrossRefGoogle Scholar
  60. Pfeiffer,J, Suarez DL, Sarmento L, To TL, Nguyen T, Pantin-Jackwood MJ (2010) Efficacy of commercial vaccines in protecting chickens and ducks against H5N1 highly pathogenic avian influenza viruses from Vietnam. Avian Diseases 54:262-271.PubMedCrossRefGoogle Scholar
  61. Philippa,J, Baas C, Beyer W, Bestebroer T, Fouchier R, Smith D, Schaftenaar W, Osterhaus A (2007) Vaccination against highly pathogenic avian influenza H5N1 virus in zoos using an adjuvanted inactivated H5N2 vaccine. Vaccine 25:3800-3808.PubMedCrossRefGoogle Scholar
  62. Philippa,JD, Munster VJ, Bolhuis H, Bestebroer TM, Schaftenaar W, Beyer WE, Fouchier RA, Kuiken T, Osterhaus AD (2005) Highly pathogenic avian influenza (H7N7): vaccination of zoo birds and transmission to non-poultry species. Vaccine 23:5743-5750.PubMedCrossRefGoogle Scholar
  63. Qiu,B, Guo Y, Liu D, Zhang Q, Qiu L, Tan Z, Fan Z, He S, Tang X, Zeng S, Peng J, Wu W, Huang Y, Liu G, Lu X, Zhang C (2007) Immunological efficacy of three kinds of avian influenza inactivated vaccines in rural backyard ducks. China Poultry 29:17-19.Google Scholar
  64. Rao,S, Kong WP, Wei C-J, Yang ZY, Nason M, Styles D, DeTolla L, Sorrell E, Song H, Wan H, Ramirez-Nieto G, Perez D, Nabel G (2008) Multivalent HA DNA Vaccination Protects against Highly Pathogenic H5N1 Avian Influenza Infection in Chickens and Mice. PLoS ONE 3:e2432.PubMedCentralPubMedCrossRefGoogle Scholar
  65. Rauw,F, Palya V, Van BS, Welby S, Tatar-Kis T, Gardin Y, Dorsey KM, Aly MM, Hassan MK, Soliman MA, Lambrecht B, van den Berg T (2011) Further evidence of antigenic drift and protective efficacy afforded by a recombinant HVT-H5 vaccine against challenge with two antigenically divergent Egyptian clade 2.2.1 HPAI H5N1 strains. Vaccine 29:2590-2600.PubMedCrossRefGoogle Scholar
  66. Rohm,C, Horimoto T, Kawaoka Y, Suss J, Webster RG (1995) Do hemagglutinin genes of highly pathogenic avian influenza viruses constitute unique phylogenetic lineages? Virology 209:664-670.PubMedCrossRefGoogle Scholar
  67. Sasaki,T, Kokumai N, Ohgitani T, Sakamoto R, Takikawa N, Lin Z, Okamatsu M, Sakoda Y, Kida H (2009) Long lasting immunity in chickens induced by a single shot of influenza vaccine prepared from inactivated non-pathogenic H5N1 virus particles against challenge with a highly pathogenic avian influenza virus. Vaccine 27:5174-5177.PubMedCrossRefGoogle Scholar
  68. Schultz-Cherry,S, Dybing JK, Davis NL, Williamson C, Suarez DL, Johnston R, Perdue ML (2000) Influenza virus (A/HK/156/97) hemagglutinin expressed by an alphavirus replicon system protects chickens against lethal infection with Hong Kong-origin H5N1 viruses. Virology 278:55-59.PubMedCrossRefGoogle Scholar
  69. Song,H, Nieto GR, Perez DR (2007) A new generation of modified live-attenuated avian influenza viruses using a two-strategy combination as potential vaccine candidates. Journal of Virology 81:9238-9248.PubMedCentralPubMedCrossRefGoogle Scholar
  70. Steel J, Burmakina SV, Thomas C, Spackman E, Garcia-Sastre A, Swayne DE, Palese P (2008) A combination in ovo vaccine for avian influenza virus and Newcastle disease virus. Vaccine 26:522–531Google Scholar
  71. Steensels M, Bublot M, Van Borm S, De Vriese J, Lambrecht B, Richard-Mazet A, Chanavat-Bizzini S, Duboeuf M, Le Gros FX, van den BT (2009) Prime-boost vaccination with a fowlpox vector and an inactivated avian influenza vaccine is highly immunogenic in Pekin ducks challenged with Asian H5N1 HPAI. Vaccine 27:646–654Google Scholar
  72. Steensels,M, Van Borm S, Lambrecht B, De Vriese J, Le Gros FX, Bublot M, van den Berg T (2007) Efficacy of an inactivated and a fowlpox-vectored vaccine in Muscovy ducks against an Asian H5N1 highly pathogenic avian influenza viral challenge. Avian Diseases 51:325-331.PubMedCrossRefGoogle Scholar
  73. Stone,H, Mitchell B, Brugh M (1997) In ovo vaccination of chicken embryos with experimental Newcastle disease and avian influenza oil-emulsion vaccines. Avian Diseases 41:856-863.PubMedCrossRefGoogle Scholar
  74. Stone,HD (1987) Efficacy of avian influenza oil-emulsion vaccines in chickens of various ages. Avian Diseases 31:483-490.PubMedCrossRefGoogle Scholar
  75. Sturm-Ramirez,KM, Hulse-Post DJ, Govorkova EA, Humberd J, Seiler P, Puthavathana P, Buranathai C, Nguyen TD, Chaisingh A, Long HT, Naipospos TSP, Chen H, Ellis TM, Guan Y, Peiris JSM, Webster RG (2005) Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? Journal of Virology 79:11269-11279.PubMedCentralPubMedCrossRefGoogle Scholar
  76. Suarez,DL, Schultz-Cherry S (2000) The effect of eukaryotic expression vectors and adjuvants on DNA vaccines in chickens using an avian influenza model. Avian Diseases 44:861-868.PubMedCrossRefGoogle Scholar
  77. Swayne,DE (2006) Principles for vaccine protection in chickens and domestic waterfowl against avian influenza: Emphasis on Asian H5N1 high pathogenicity avian influenza. Annals of the New York Academy of Sciences 1081:174-181.PubMedCrossRefGoogle Scholar
  78. Swayne,DE (2008a) Avian influenza vaccines and therapies for poultry. Comparative Immunology, Microbiology and Infectious Diseases 32:351-363.PubMedCrossRefGoogle Scholar
  79. Swayne DE (2008b) Epidemiology of avian influenza in agricultural and other man-made systems. In: Avian Influenza, Swayne DE (editor), Ames: Wylie-Blackwell Publishing, pp 59–85Google Scholar
  80. Swayne,DE (2012a) Impact of vaccines and vaccination on global control of avian influenza. Avian Diseases 56:818-828.PubMedCrossRefGoogle Scholar
  81. Swayne,DE (2012b) The role of vaccines and vaccination in high pathogenicity avian influenza control and eradication. Expert Review of Vaccines 11:877-880.PubMedCrossRefGoogle Scholar
  82. Swayne DE, Kapczynski DR (2008) Vaccines, vaccination and immunology for avian influenza viruses in poultry. In: Avian Influenza, DE Swayne (editor), Ames: Blackwell Publishing, pp 407–451.CrossRefGoogle Scholar
  83. Swayne,DE, Spackman E (2013) Current status and future needs in diagnostics and vaccines for high pathogenicity avian influenza. Developments in Biologicals (Basel) 135:79-94.Google Scholar
  84. Swayne DE, Beck JR, Garcia M, Stone HD (1999) Influence of virus strain and antigen mass on efficacy of H5 avian influenza inactivated vaccines. Avian Pathology 28:245–255.CrossRefGoogle Scholar
  85. Swayne,DE, Beck JR, Kinney N (2000) Failure of a recombinant fowl poxvirus vaccine containing an avian influenza hemagglutinin gene to provide consistent protection against influenza in chickens preimmunized with a fowl pox vaccine. Avian Diseases 44:132-137.PubMedCrossRefGoogle Scholar
  86. Swayne,DE, Beck JR, Mickle TR (1997) Efficacy of recombinant fowl pox vaccine in protecting chickens against highly pathogenic Mexican-origin H5N2 avian influenza virus. Avian Diseases 41:910-922.PubMedCrossRefGoogle Scholar
  87. Swayne,DE, Eggert D, Beck JR (2012) Reduction of high pathogenicity avian influenza virus in eggs from chickens once or twice vaccinated with an oil-emulsified inactivated H5 avian influenza vaccine. Vaccine 30:4964-4970.PubMedCrossRefGoogle Scholar
  88. Swayne DE, Suarez DL, Sims LD (2013) Influenza. In: Diseases of Poultry, Swayne DE, Glisson JR, McDougald LR, Nair V, Nolan LK, Suarez Dl (editors), Ames: Wiley-BlackwellGoogle Scholar
  89. Swayne,DE, Pavade G, Hamilton K, Vallat B, Miyagishima K (2011) Assessment of national strategies for control of high pathogenicity avian influenza and low pathogenicity notifiable avian influenza in poultry, with emphasis on vaccines and vaccination. Revue Scientifique et Technique - Office International des Epizooties 30:839-870.Google Scholar
  90. Swayne,DE, Suarez DL, Schultz-Cherry S, Tumpey TM, King DJ, Nakaya T, Palese P, Garcia-Sastra A (2003) Recombinant Paramyxovirus type 1-avian influenza-H7 virus as a vaccine for protection of chickens against influenza and Newcastle disease. Avian Diseases 47:1047-1050.PubMedCrossRefGoogle Scholar
  91. Tian,G, Zhang S, Li Y, Bu Z, Liu P, Zhou J, Li C, Shi J, Yu K, Chen H (2005) Protective efficacy in chickens, geese and ducks of an H5N1-inactivated vaccine developed by reverse genetics. Virology 341:153-162.PubMedCrossRefGoogle Scholar
  92. Toffan A, Beato MS, De Nardi R, Bertoli E, Cattoli G, Terregino C, Capua I (2007) Vaccination prevents viral colonization of muscles in experimentally infected turkeys challenged with highly pathogenic and low pathogenicity avian influenza viruses of the H7N1 subtype. OIE/FAO/IZSVe Scientific Conference—Vaccination: a tool for the control of avian influenza, 20–22 March 2007, Verona, Italy, p 64Google Scholar
  93. Veits,J, Luschow D, Kindermann K, Werner O, Teifke JP, Mettenleiter TC, Fuchs W (2003) Deletion of the non-essential UL0 gene of infectious laryngotracheitis (ILT) virus leads to attenuation in chickens, and UL0 mutants expressing influenza virus haemagglutinin (H7) protect against ILT and fowl plague. Journal of General Virology 84:3343-3352.PubMedCrossRefGoogle Scholar
  94. Webster,RG, Webby RJ, Hoffmann E, Rodenberg J, Kumar M, Chu HJ, Seiler P, Krauss S, Songserm T (2006) The immunogenicity and efficacy against H5N1 challenge of reverse genetics-derived H5N3 influenza vaccine in ducks and chickens. Virology 351:303-311.PubMedCrossRefGoogle Scholar
  95. Wilson,HM, Hall JS, Flint PL, Franson JC, Ely CR, Schmutz JA, Samuel MD (2013) High Seroprevalence of Antibodies to Avian Influenza Viruses among Wild Waterfowl in Alaska: Implications for Surveillance. PLoS ONE 8:e58308.PubMedCentralPubMedCrossRefGoogle Scholar
  96. Yamamoto,Y, Nakamura K, Yamada M, Mase M (2010) Comparative pathology of chickens and domestic ducks experimentally infected with highly pathogenic avian influenza viruses (H5N1) isolated in Japan in 2007 and 2008. Japan Agricultural Research Quarterly 44:73-80.CrossRefGoogle Scholar
  97. Zhang,P, Tang Y, Liu X, Xue F, Qiu X, Cao Y, Gao S, Wu Y, Liu X (2005) Comparison of protective efficacy of H5N2 and H5N1 subtype inactivated oil-emulsion vaccine against H5N1 avian influenza virus (AIV) in ducks and effects of maternal antibody on immune response. China Poultry 27:8-11.Google Scholar
  98. Zhang,W, Tu J, Zhao Z, Chen H, Jin M (2012) The new temperature-sensitive mutation PA-F35S for developing recombinant avian live attenuated H5N1 influenza vaccine. Virology Journal 9:97.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health (outside the USA) 2013

Authors and Affiliations

  • David E. Swayne
    • 1
    Email author
  • Erica Spackman
    • 1
  • Mary Pantin-Jackwood
    • 1
  1. 1.Exotic and Emerging Avian Viral Diseases Research Unit, Southeast Poultry Research Laboratory, Agricultural Research ServiceUnited States Department of AgricultureAthensUSA

Personalised recommendations