Influenza A virus hemagglutinin protein subunit vaccine elicits vaccine-associated enhanced respiratory disease in pigs

Vaccine

Volumn 32, Issue 40, 2014, Pages 5170-5176

  Rajão, Daniela S ^a   Loving, Crystal L ^a   Gauger, Phillip C ^b   Kitikoon, Pravina ^a,c   Vincent, Amy L ^a  

^a NATIONAL ANIMAL DISEASE CENTER   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c Merck Animal Health   (United States)

Author keywords

Hemagglutinin; Influenza; Pigs; Vaccine; VAERD

Indexed keywords

GAMMA INTERFERON; INFLUENZA A VIRUS HEMAGGLUTININ PROTEIN SUBUNIT VACCINE; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 8; NEUTRALIZING ANTIBODY; SUBUNIT VACCINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; LIVE VACCINE; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BRONCHIOLITIS; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RESPONSE; INFLUENZA VACCINATION; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H1N2; LUNG LESION; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN SUBUNIT; RESPIRATORY TRACT DISEASE; TRACHEA DISEASE; VACCINE ASSOCIATED ENHANCED RESPIRATORY DISEASE; VIRAL CLEARANCE; VIRUS SHEDDING; ANIMAL; BLOOD; CHEMICALLY INDUCED; IMMUNOLOGY; LUNG; ORTHOMYXOVIRIDAE INFECTIONS; PATHOLOGY; SWINE; SWINE DISEASES; TRACHEA; VETERINARY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; LUNG; ORTHOMYXOVIRIDAE INFECTIONS; RESPIRATORY TRACT DISEASES; SWINE; SWINE DISEASES; TRACHEA; VACCINES, ATTENUATED; VACCINES, SUBUNIT; VIRUS SHEDDING;

EID: 84906053484     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2014.07.059     Document Type: Article

References (30)

1. Brown I.H. The epidemiology and evolution of influenza viruses in pigs. Vet Microbiol 2000, 74(1-2):29-46.
2. Zhou N.N., Senne D.A., Landgraf J.S., Swenson S.L., Erickson G., Rossow K., et al. Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J Virol 1999, 73(10):8851-8856.
3. Olsen C.W. The emergence of novel swine influenza viruses in North America. Virus Res 2002, 85(2):199-210.
4. Vincent A.L., Ma W., Lager K.M., Janke B.H., Richt J.A. Swine influenza viruses: a North American perspective. Adv Virus Res 2008, 127-154. Academic Press, Burlington. K. Maramorosch, A.J. Shatkin, F.A. Murphy (Eds.).
5. Lorusso A., Vincent A.L., Gramer M.E., Lager K.M., Ciacci-Zanella J.R. Contemporary epidemiology of North American lineage triple reassortant influenza A viruses in pigs. Curr Top Microbiol Immunol 2013, 370:113-132.
6. Webby R.J., Swenson S.L., Krauss S.L., Gerrish P.J., Goyal S.M., Webster R.G. Evolution of swine H3N2 influenza viruses in the United States. J Virol 2000, 74(18):8243-8251.
7. Kitikoon P., Nelson M.I., Killian M.L., Anderson T.K., Koster L., Culhane M.R., et al. Genotype patterns of contemporary reassorted H3N2 virus in US swine. J Gen Virol 2013, 94(Pt 6):1236-1241.
8. Gamblin S.J., Skehel J.J. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem 2010, 285(37):28403-28409.
9. Vincent A.L., Lager K.M., Janke B.H., Gramer M.R., Richt J.A. Failure of protection and enhanced pneumonia with a US H1N2 swine influenza virus in pigs vaccinated with an inactivated classical swine H1N1 vaccine. Vet Microbiol 2008, 126(4):310-323.
10. Ma W., Richt J.A. Swine influenza vaccines: current status and future perspectives. Anim Health Res Rev 2010, 11(1):81-96.
11. Van Reeth K., Brown I., Essen S., Pensaert M. Genetic relationships, serological cross-reaction and cross-protection between H1N2 and other influenza A virus subtypes endemic in European pigs. Virus Res 2004, 103(1-2):115-124.
12. Vincent A.L., Ma W., Lager K.M., Janke B.H., Webby R.J., Garcia-Sastre A., et al. Efficacy of intranasal administration of a truncated NS1 modified live influenza virus vaccine in swine. Vaccine 2007, 25(47):7999-8009.
13. Gauger P.C., Vincent A.L., Loving C.L., Henningson J.N., Lager K.M., Janke B.H., et al. Kinetics of lung lesion development and pro-inflammatory cytokine response in pigs with vaccine-associated enhanced respiratory disease induced by challenge with pandemic (2009) A/H1N1 influenza virus. Vet Pathol 2012, 49(6):900-912.
14. Gauger P.C., Vincent A.L., Loving C.L., Lager K.M., Janke B.H., Kehrli M.E., et al. Enhanced pneumonia and disease in pigs vaccinated with an inactivated human-like (delta-cluster) H1N2 vaccine and challenged with pandemic 2009 H1N1 influenza virus. Vaccine 2011, 29(15):2712-2719.
15. Khurana S., Loving C.L., Manischewitz J., King L.R., Gauger P.C., Henningson J., et al. Vaccine-induced anti-HA2 antibodies promote virus fusion and enhance influenza virus respiratory disease. Sci Transl Med 2013, 5(200):200ra114.
16. Pena L., Vincent A.L., Ye J., Ciacci-Zanella J.R., Angel M., Lorusso A., et al. Modifications in the polymerase genes of a swine-like triple-reassortant influenza virus to generate live attenuated vaccines against 2009 pandemic H1N1 viruses. J Virol 2011, 85(1):456-469.
17. Vincent A.L., Ma W., Lager K.M., Richt J.A., Janke B.H., Sandbulte M.R., et al. Live attenuated influenza vaccine provides superior protection from heterologous infection in pigs with maternal antibodies without inducing vaccine-associated enhanced respiratory disease. J Virol 2012, 86(19):10597-10605.
18. Kitikoon P., Nilubol D., Erickson B.J., Janke B.H., Hoover T.C., Sornsen S.A., et al. The immune response and maternal antibody interference to a heterologous H1N1 swine influenza virus infection following vaccination. Vet Immunol Immunopathol 2006, 112(3-4):117-128.
19. Reed l.J., Muench H. A simple method of estimating fifty per cent endpoints. Am J Epidemiol 1938, 27(3):493-497.
20. Halbur P.G., Paul P.S., Frey M.L., Landgraf J., Eernisse K., Meng X.J., et al. Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol 1995, 32(6):648-660.
21. World Health Organization WHO manual on animal influenza diagnosis and surveillance 2002, Available from: http://www.who.int/csr/resources/publications/influenza/en/whocdscsrncs20025rev.pdf [accessed 11.06.13]. 2nd ed.
22. Braucher D.R., Henningson J.N., Loving C.L., Vincent A.L., Kim E., Steitz J., et al. Intranasal vaccination with replication-defective adenovirus type 5 encoding influenza virus hemagglutinin elicits protective immunity to homologous challenge and partial protection to heterologous challenge in pigs. Clin Vaccine Immunol 2012, 19(11):1722-1729.
23. Van Reeth K., Ma W. Swine influenza virus vaccines: to change or not to change - that's the question. Curr Top Microbiol Immunol 2013, 370:173-200.
24. Lorusso A., Vincent A.L., Harland M.L., Alt D., Bayles D.O., Swenson S.L., et al. Genetic and antigenic characterization of H1 influenza viruses from United States swine from 2008. J Gen Virol 2011, 92(Pt 4):919-930.
25. Loving C.L., Vincent A.L., Pena L., Perez D.R. Heightened adaptive immune responses following vaccination with a temperature-sensitive, live-attenuated influenza virus compared to adjuvanted, whole-inactivated virus in pigs. Vaccine 2012, 30(40):5830-5838.
26. Monsalvo A.C., Batalle J.P., Lopez M.F., Krause J.C., Klemenc J., Hernandez J.Z., et al. Severe pandemic 2009 H1N1 influenza disease due to pathogenic immune complexes. Nat Med 2011, 17(2):195-199.
27. Van Reeth K., Nauwynck H., Pensaert M. Bronchoalveolar interferon-alpha, tumor necrosis factor-alpha, interleukin-1, and inflammation during acute influenza in pigs: a possible model for humans?. J Infect Dis 1998, 177(4):1076-1079.
28. Van Reeth K., Van Gucht S., Pensaert M. Correlations between lung proinflammatory cytokine levels, virus replication, and disease after swine influenza virus challenge of vaccination-immune pigs. Viral Immunol 2002, 15(4):583-594.
29. Gauger P.C., Loving C.L., Lager K.M., Janke B.H., Kehrli M.E., Roth J.A., et al. Vaccine-associated enhanced respiratory disease does not interfere with the adaptive immune response following challenge with pandemic A/H1N1 2009. Viral Immunol 2013, 26(5):314-321.
30. Heinen P.P., Rijsewijk F.A., de Boer-Luijtze E.A., Bianchi A.T. Vaccination of pigs with a DNA construct expressing an influenza virus M2-nucleoprotein fusion protein exacerbates disease after challenge with influenza A virus. J Gen Virol 2002, 83(Pt 8):1851-1859.