Pandemic preparedness through vaccine development for avian influenza viruses

References

• Dadonaite B, Gilbertson B, Knight ML, Trifkovic S, Rockman S, Laederach A, Brown LE, Fodor E, Bauer DLV. The structure of the influenza a virus genome. Nat Microbiol. 2019;4(11):1781–14. doi:10.1038/s41564-019-0513-7.
   PubMed Web of Science ®Google Scholar
• Krammer F, Smith GJD, Fouchier RAM, Peiris M, Kedzierska K, Doherty PC, Palese P, Shaw ML, Treanor J, Webster RG. et al. Influenza. Nat Rev Dis Primers. 2018;4(1):3. doi:10.1038/s41572-018-0002-y.
   PubMed Web of Science ®Google Scholar
• Fereidouni S, Starick E, Karamendin K, Genova CD, Scott SD, Khan Y, Harder T, Kydyrmanov A. Genetic characterization of a new candidate hemagglutinin subtype of influenza a viruses. Emerg Microbes Infect. 2023;12(2):2225645. doi:10.1080/22221751.2023.2225645.
   PubMed Web of Science ®Google Scholar
• Berhane Y, Hisanaga T, Kehler H, Neufeld J, Manning L, Argue C, Handel K, Hooper-McGrevy K, Jonas M, Robinson J. et al. Highly pathogenic avian influenza virus a (H7N3) in domestic poultry, Saskatchewan, Canada, 2007. Emerg Infect Dis. 2009;15(9):1492–5. doi:10.3201/eid1509.080231.
   PubMed Web of Science ®Google Scholar
• Banet-Noach C, Perk S, Simanov L, Grebenyuk N, Rozenblut E, Pokamunski S, Pirak M, Tendler Y, Panshin A. H9N2 influenza viruses from Israeli poultry: a five-year outbreak. Avian Dis. 2007;51(s1):290–6. doi:10.1637/7590-040206R1.1.
   PubMedGoogle Scholar
• Sonnberg S, Phommachanh P, Naipospos TS, McKenzie J, Chanthavisouk C, Pathammavong S, Darnell D, Meeduangchanh P, Rubrum AM, Souriya M. et al. Multiple introductions of avian influenza viruses (H5N1), laos, 2009–2010. Emerg Infect Dis. 2012;18(7):1139–43. doi:10.3201/eid1807.111642.
   PubMed Web of Science ®Google Scholar
• Kosik I, Yewdell JW. Influenza hemagglutinin and neuraminidase: Yin–Yang Proteins coevolving to thwart immunity. Viruses. 2019;11(4):346. doi:10.3390/v11040346.
   PubMed Web of Science ®Google Scholar
• Liu C, Eichelberger MC, Compans RW, Air GM. Influenza type a virus neuraminidase does not play a role in viral entry, replication, assembly, or budding. J Virol. 1995;69(2):1099–106. doi:10.1128/JVI.69.2.1099-1106.1995.
   PubMed Web of Science ®Google Scholar
• Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus AD, Fouchier RA. Global patterns of influenza a virus in wild birds. Science. 2006;312(5772):384–8. doi:10.1126/science.1122438.
   PubMed Web of Science ®Google Scholar
• Normile D. Avian influenza. Evidence points to migratory birds in H5N1 spread. Science. 2006;311(5765):1225. doi:10.1126/science.311.5765.1225.
   PubMed Web of Science ®Google Scholar
• Spackman E. A brief introduction to avian influenza virus. Methods Mol Biol. 2020;2123:83–92. doi:10.1007/978-1-0716-0346-8_7.
   PubMedGoogle Scholar
• Steinhauer DA. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology. 1999;258(1):1–20. doi:10.1006/viro.1999.9716.
   PubMed Web of Science ®Google Scholar
• Bosch FX, Garten W, Klenk HD, Rott R. Proteolytic cleavage of influenza virus hemagglutinins: primary structure of the connecting peptide between HA1 and HA2 determines proteolytic cleavability and pathogenicity of Avian influenza viruses. Virology. 1981;113(2):725–35. doi:10.1016/0042-6822(81)90201-4.
   PubMed Web of Science ®Google Scholar
• Zhang G, Xu L, Zhang J, Fang Q, Zeng J, Liu Y, Ke C. A H9N2 human case and surveillance of avian influenza viruses in live poultry markets — Huizhou City, Guangdong Province, China, 2021. China CDC Wkly. 2022;4(1):8–10. doi:10.46234/ccdcw2021.273.
   PubMedGoogle Scholar
• Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K. et al. Human infection with a novel avian-origin influenza a (H7N9) virus. N Engl J Med. 2013;368(20):1888–97. doi:10.1056/NEJMoa1304459.
   PubMed Web of Science ®Google Scholar
• Gu W, Shi J, Cui P, Yan C, Zhang Y, Wang C, Zhang Y, Xing X, Zeng X, Liu L. et al. Novel H5N6 reassortants bearing the clade 2.3.4.4b HA gene of H5N8 virus have been detected in poultry and caused multiple human infections in China. Emerg Microbes Infect. 2022;11(1):1174–85. doi:10.1080/22221751.2022.2063076.
   PubMed Web of Science ®Google Scholar
• Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, Perdue M, Swayne D, Bender C, Huang J. et al. Characterization of an avian influenza a (H5N1) virus isolated from a child with a fatal respiratory illness. Science. 1998;279(5349):393–6. doi:10.1126/science.279.5349.393.
   PubMed Web of Science ®Google Scholar
• Kim H, Webster RG, Webby RJ. Influenza virus: dealing with a drifting and shifting pathogen. Viral Immunol. 2018;31:174–83. doi:10.1089/vim.2017.0141.
   PubMed Web of Science ®Google Scholar
• Caceres CJ, Seibert B, Cargnin Faccin F, Cardenas-Garcia S, Rajao DS, Perez DR. Influenza antivirals and animal models. FEBS Open Bio. 2022;12(6):1142–65. doi:10.1002/2211-5463.13416.
   PubMed Web of Science ®Google Scholar
• Qi L, Pujanauski LM, Davis AS, Schwartzman LM, Chertow DS, Baxter D, Scherler K, Hartshorn KL, Slemons RD, Walters K-A. et al. Contemporary avian influenza a virus subtype H1, H6, H7, H10, and H15 hemagglutinin genes encode a mammalian virulence factor similar to the 1918 pandemic virus H1 hemagglutinin. mBio. 2014;5(6):e02116. doi:10.1128/mBio.02116-14.
   PubMed Web of Science ®Google Scholar
• Yu Z, Song Y, Zhou H, Xu X, Hu Q, Wu H, Zhang A, Zhou Y, Chen J, Dan H. et al. Avian influenza (H5N1) virus in waterfowl and chickens, central China. Emerg Infect Dis. 2007;13(5):772–5. doi:10.3201/eid1305.061209.
   PubMed Web of Science ®Google Scholar
• de Vries E, Guo H, Dai M, Rottier PJ, van Kuppeveld FJ, de Haan CA. Rapid emergence of highly pathogenic avian influenza subtypes from a subtype H5N1 hemagglutinin variant. Emerg Infect Dis. 2015;21(5):842–6. doi:10.3201/eid2105.141927.
   PubMed Web of Science ®Google Scholar
• Wan XF. Lessons from emergence of A/goose/Guangdong/1996-like H5N1 highly pathogenic avian influenza viruses and recent influenza surveillance efforts in southern China. Zoonoses Public Health. 2012;59(Suppl2):32–42. doi:10.1111/j.1863-2378.2012.01497.x.
   PubMedGoogle Scholar
• Bruno A, Alfaro-Nunez A, de Mora D, Armas R, Olmedo M, Garces J, Garcia-Bereguiain MA. First case of human infection with highly pathogenic H5 avian influenza a virus in South America: a new zoonotic pandemic threat for 2023? J Travel Med. 2023;30(5). doi:10.1093/jtm/taad032.
   Web of Science ®Google Scholar
• Li H, Li Q, Li B, Guo Y, Xing J, Xu Q, Liu L, Zhang J, Qi W, Jia W. et al. Continuous reassortment of clade 2.3.4.4 H5N6 highly pathogenetic avian influenza viruses demonstrating high risk to public health. Pathogens. 2020;9(8):670. doi:10.3390/pathogens9080670.
   PubMed Web of Science ®Google Scholar
• Imai M, Herfst S, Sorrell EM, Schrauwen EJ, Linster M, De Graaf M, Fouchier RAM, Kawaoka Y. Transmission of influenza A/H5N1 viruses in mammals. Virus Res. 2013;178(1):15–20. doi:10.1016/j.virusres.2013.07.017.
   PubMed Web of Science ®Google Scholar
• Banks J, Speidel EC, McCauley JW, Alexander DJ. Phylogenetic analysis of H7 haemagglutinin subtype influenza a viruses. Arch Virol. 2000;145(5):1047–58. doi:10.1007/s007050050695.
   PubMed Web of Science ®Google Scholar
• Li C, Chen H. H7N9 Influenza Virus in China. Cold Spring Harb Perspect Med. 2021;11(8):a038349. doi:10.1101/cshperspect.a038349.
   PubMed Web of Science ®Google Scholar
• Wang X, Wu P, Pei Y, Tsang TK, Gu D, Wang W, Zhang J, Horby PW, Uyeki TM, Cowling BJ. et al. Assessment of human-to-human transmissibility of avian influenza A(H7N9) virus across 5 waves by analyzing clusters of case patients in Mainland China, 2013–2017. Clin Infect Dis. 2019;68(4):623–31. doi:10.1093/cid/ciy541.
   PubMed Web of Science ®Google Scholar
• Belser JA, Gustin KM, Pearce MB, Maines TR, Zeng H, Pappas C, Sun X, Carney PJ, Villanueva JM, Stevens J. et al. Pathogenesis and transmission of avian influenza a (H7N9) virus in ferrets and mice. Nature. 2013;501(7468):556–9. doi:10.1038/nature12391.
   PubMed Web of Science ®Google Scholar
• Peacock THP, James J, Sealy JE, Iqbal M. A global perspective on H9N2 avian influenza virus. Viruses. 2019;11(7):620. doi:10.3390/v11070620.
   PubMed Web of Science ®Google Scholar
• Wang Y, Niu S, Zhang B, Yang C, Zhou Z. WITHDRAWN: the whole genome analysis for the first human infection with H10N3 influenza virus in China. J Infect. 2021. doi:10.1016/j.jinf.2021.06.021.
   Google Scholar
• Guan Y, Shortridge KF, Krauss S, Webster RG. Molecular characterization of H9N2 influenza viruses: were they the donors of the “internal” genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci USA. 1999;96:9363–7. doi:10.1073/pnas.96.16.9363.
   PubMed Web of Science ®Google Scholar
• Li F, Liu J, Yang J, Sun H, Jiang Z, Wang C, Zhang X, Yu Y, Zhao C, Pu J. et al. H9N2 virus-derived M1 protein promotes H5N6 virus release in mammalian cells: mechanism of avian influenza virus inter-species infection in humans. PLOS Pathog. 2021;17(12):e1010098. doi:10.1371/journal.ppat.1010098.
   PubMed Web of Science ®Google Scholar
• Pu J, Wang S, Yin Y, Zhang G, Carter RA, Wang J, Xu G, Sun H, Wang M, Wen C. et al. Evolution of the H9N2 influenza genotype that facilitated the genesis of the novel H7N9 virus. Proc Natl Acad Sci USA. 2015;112(2):548–53. doi:10.1073/pnas.1422456112.
   PubMed Web of Science ®Google Scholar
• Liu J, Zhang J, Huang F, Zhang Y, Luo H, Zhang H. Complex reassortment of polymerase genes in Asian influenza a virus H7 and H9 subtypes. Infect Genet Evol. 2014;23:203–8. doi:10.1016/j.meegid.2014.02.016.
   PubMed Web of Science ®Google Scholar
• Zhang M, Zhao C, Chen H, Teng Q, Jiang L, Feng D, Li X, Yuan S, Xu J, Zhang X. et al. Internal gene cassette from a human-origin H7N9 influenza virus promotes the pathogenicity of H9N2 avian influenza virus in mice. Front Microbiol. 2020;11:1441. doi:10.3389/fmicb.2020.01441.
   PubMed Web of Science ®Google Scholar
• Yu H, Hua RH, Wei TC, Zhou YJ, Tian ZJ, Li GX, Liu T-Q, Tong G-Z. Isolation and genetic characterization of avian origin H9N2 influenza viruses from pigs in China. Vet Microbiol. 2008;131(1–2):82–92. doi:10.1016/j.vetmic.2008.02.024.
   PubMed Web of Science ®Google Scholar
• Zhang C, Xuan Y, Shan H, Yang H, Wang J, Wang K, Li G, Qiao J. Avian influenza virus H9N2 infections in farmed minks. Virol J. 2015;12(1):180. doi:10.1186/s12985-015-0411-4.
   PubMedGoogle Scholar
• Peiris M, Yuen KY, Leung CW, Chan KH, Ip PL, Lai RW, Orr WK, Shortridge KF. Human infection with influenza H9N2. The Lancet. 1999;354(9182):916–7. doi:10.1016/s0140-6736(99)03311-5.
   PubMed Web of Science ®Google Scholar
• The Government of the Hong Kong Special Administrative Region. CHP reports investigation progress of case of influenza a (H9) infection. 2024. https://www.info.gov.hk/gia/general/202402/23/P2024022300566.htm#:~:text=The%20Centre%20for%20Health%20Protection,Services%20Branch%20of%20the%20CHP.
   Google Scholar
• Uyeki TM, Chong YH, Katz JM, Lim W, Ho YY, Wang SS, Tsang TH., Au, WWY, Chan, S.C., Rowe T, et al. Lack of evidence for human-to-human transmission of avian influenza a (H9N2) viruses in Hong Kong, China 1999. Emerg Infect Dis. 2002;8(2):154–9. doi:10.3201/eid0802.010148.
   PubMed Web of Science ®Google Scholar
• Alexander PE, De P, Rave S. Is H9N2 avian influenza virus a pandemic potential? Can J Infect Dis Med Microbiol. 2009;20:e35–6. doi:10.1155/2009/578179.
   PubMedGoogle Scholar
• Mifsud EJ, Kuba M, Barr IG. Innate immune responses to influenza virus infections in the upper respiratory tract. Viruses. 2021;13(10):2090. doi:10.3390/v13102090.
   PubMed Web of Science ®Google Scholar
• Nichol KL, Treanor JJ. Vaccines for seasonal and pandemic influenza. J Infect Dis. 2006;194(2):S111–8. doi:10.1086/507544.
   PubMed Web of Science ®Google Scholar
• Shi J, Zeng X, Cui P, Yan C, Chen H. Alarming situation of emerging H5 and H7 avian influenza and effective control strategies. Emerg Microbes Infect. 2023;12(1):2155072. doi:10.1080/22221751.2022.2155072.
   PubMed Web of Science ®Google Scholar
• Boivin S, Cusack S, Ruigrok RW, Hart DJ. Influenza a virus polymerase: structural insights into replication and host adaptation mechanisms. J Biol Chem. 2010;285:28411–7. doi:10.1074/jbc.R110.117531.
   PubMed Web of Science ®Google Scholar
• Harvey AG, Graves AM, Uppalapati CK, Matthews SM, Rosenberg S, Parent EG, Fagerlie MH, Guinan J, Lopez BS, Kronstad LM. et al. Dendritic cell-natural killer cell cross-talk modulates T cell activation in response to influenza A viral infection. Front Immunol. 2022;13:1006998. doi:10.3389/fimmu.2022.1006998.
   PubMed Web of Science ®Google Scholar
• Janssens Y, Joye J, Waerlop G, Clement F, Leroux-Roels G, Leroux-Roels I. The role of cell-mediated immunity against influenza and its implications for vaccine evaluation. Front Immunol. 2022;13:959379. doi:10.3389/fimmu.2022.959379.
   PubMed Web of Science ®Google Scholar
• Rajao DS, Perez DR. Universal vaccines and vaccine platforms to protect against influenza viruses in humans and agriculture. Front Microbiol. 2018;9:123. doi:10.3389/fmicb.2018.00123.
   PubMed Web of Science ®Google Scholar
• Chen J, Wang J, Zhang J, Ly H. Advances in development and application of influenza vaccines. Front Immunol. 2021;12:711997. doi:10.3389/fimmu.2021.711997.
   PubMed Web of Science ®Google Scholar
• Lai L, Rouphael N, Xu Y, Sherman AC, Edupuganti S, Anderson EJ, Lankford-Turner P, Wang D, Keitel W, McNeal MM. et al. Baseline levels of influenza-specific B cells and T cell responses modulate human immune responses to swine variant influenza A/H3N2 vaccine. Vaccines. 2020;8(1):126. doi:10.3390/vaccines8010126.
   Web of Science ®Google Scholar
• Sun W, Wang Z, Sun Y, Li D, Zhu M, Zhao M, Wang Y, Xu J, Kong Y, Li Y. et al. Safety, immunogenicity, and protective efficacy of an H5N1 chimeric cold-adapted attenuated virus vaccine in a mouse model. Viruses. 2021;13(12):2420. doi:10.3390/v13122420.
   PubMed Web of Science ®Google Scholar
• Boni MF. Vaccination and antigenic drift in influenza. Vaccine. 2008;26(3):C8–14. doi:10.1016/j.vaccine.2008.04.011.
   PubMedGoogle Scholar
• Steel J. New strategies for the development of H5N1 subtype influenza vaccines: progress and challenges. BioDrugs. 2011;25(5):285–98. doi:10.1007/BF03256169.
   PubMed Web of Science ®Google Scholar
• Morens DM, Fauci AS. Emerging infectious diseases in 2012: 20 years after the institute of medicine report. mBio. 2012;3(6). doi:10.1128/mBio.00494-12.
   Web of Science ®Google Scholar
• Claas EC, de Jong JC, van Beek R, Rimmelzwaan GF, Osterhaus AD. Human influenza virus A/HongKong/156/97 (H5N1) infection. Vaccine. 1998;16(9–10):977–8. doi:10.1016/s0264-410x(98)00005-x.
   PubMed Web of Science ®Google Scholar
• Lu X, Tumpey TM, Morken T, Zaki SR, Cox NJ, Katz JM. A mouse model for the evaluation of pathogenesis and immunity to influenza a (H5N1) viruses isolated from humans. J Virol. 1999;73(7):5903–11. doi:10.1128/JVI.73.7.5903-5911.1999.
   PubMed Web of Science ®Google Scholar
• Suartha IN, Suartini GAA, Wirata IW, Dewi N, Putra GNN, Kencana GAY, Mahardika GN. Intranasal administration of inactivated avian influenza virus of H5N1 subtype vaccine-induced systemic immune response in chicken and mice. Vet World. 2018;11(2):221–6. doi:10.14202/vetworld.2018.221-226.
   PubMedGoogle Scholar
• Sjolander A, van’t Land B, Lovgren Bengtsson K. Iscoms containing purified quillaja saponins upregulate both Th1-like and Th2-like immune responses. Cell Immunol. 1997;177:69–76. doi:10.1006/cimm.1997.1088.
   PubMed Web of Science ®Google Scholar
• Abel LC, Chen S, Ricca LG, Martins MF, Garcia M, Ananias RZ, Mussalem JS, Squaiella CC, Shaw RJ, Longo‐Maugéri IM. et al. Adjuvant effect of LPS and killed Propionibacterium acnes on the development of experimental gastrointestinal nematode infestation in sheep. Parasite Immunol. 2009;31(10):604–12. doi:10.1111/j.1365-3024.2009.01132.x.
   PubMed Web of Science ®Google Scholar
• Ducatez MF, Webb A, Crumpton JC, Webby RJ. Long-term vaccine-induced heterologous protection against H5N1 influenza viruses in the ferret model. Influenza other Respir Viruses. 2013;7(4):506–12. doi:10.1111/j.1750-2659.2012.00423.x.
   PubMed Web of Science ®Google Scholar
• Nakayama M, Shichinohe S, Itoh Y, Ishigaki H, Kitano M, Arikata M, Pham VL, Ishida H, Kitagawa N, Okamatsu M. et al. Protection against H5N1 highly pathogenic avian and pandemic (H1N1) 2009 influenza virus infection in cynomolgus monkeys by an inactivated H5N1 whole particle vaccine. PloS One. 2013;8(12):e82740. doi:10.1371/journal.pone.0082740.
   PubMed Web of Science ®Google Scholar
• Seo SH, Kim HS. Inactivated antigen of the H7N9 influenza virus protects mice from its lethal infection. Viral Immunol. 2016;29(4):235–43. doi:10.1089/vim.2015.0103.
   PubMed Web of Science ®Google Scholar
• Chang H, Duan J, Zhou P, Su L, Zheng D, Zhang F, Fang F, Li X, Chen Z. Single immunization with MF59-adjuvanted inactivated whole-virion H7N9 influenza vaccine provides early protection against H7N9 virus challenge in mice. Microbes Infect. 2017;19(12):616–25. doi:10.1016/j.micinf.2017.08.012.
   PubMed Web of Science ®Google Scholar
• Hatta M, Zhong G, Chiba S, Lopes TJS, Neumann G, Kawaoka Y. Effectiveness of whole, inactivated, low pathogenicity influenza A(H7N9) vaccine against antigenically distinct, highly pathogenic H7N9 virus. Emerg Infect Dis. 2018;24(10):1910–13. doi:10.3201/eid2410.180403.
   PubMed Web of Science ®Google Scholar
• Wong SS, Jeevan T, Kercher L, Yoon SW, Petkova AM, Crumpton JC, Franks J, Debeauchamp J, Rubrum A, Seiler P. et al. A single dose of whole inactivated H7N9 influenza vaccine confers protection from severe disease but not infection in ferrets. Vaccine. 2014;32(35):4571–7. doi:10.1016/j.vaccine.2014.06.016.
   PubMed Web of Science ®Google Scholar
• Pan W, Han L, Dong Z, Niu X, Li Z, Bao L, Li C, Luo Q, Yang Z, Li X. et al. Induction of neutralizing antibodies to influenza a virus H7N9 by inactivated whole virus in mice and nonhuman primates. Antiviral Res. 2014;107:1–5. doi:10.1016/j.antiviral.2014.04.003.
   PubMed Web of Science ®Google Scholar
• Qin T, Yin Y, Huang L, Yu Q, Yang Q, Burns DL. H9N2 influenza whole inactivated virus combined with polyethyleneimine strongly enhances mucosal and systemic immunity after intranasal immunization in mice. Clin Vaccine Immunol. 2015;22(4):421–9. doi:10.1128/CVI.00778-14.
   PubMedGoogle Scholar
• Wegmann F, Gartlan KH, Harandi AM, Brinckmann SA, Coccia M, Hillson WR, Kok WL, Cole S, Ho L-P, Lambe T. et al. Polyethyleneimine is a potent mucosal adjuvant for viral glycoprotein antigens. Nat Biotechnol. 2012;30(9):883–8. doi:10.1038/nbt.2344.
   PubMed Web of Science ®Google Scholar
• Park SJ, Kang YM, Cho HK, Kim DY, Kim S, Bae Y, Kim J, Kim G, Lee Y-J, Kang H-M. et al. Cross-protective efficacy of inactivated whole influenza vaccines against Korean Y280 and Y439 lineage H9N2 viruses in mice. Vaccine. 2021;39(42):6213–20. doi:10.1016/j.vaccine.2021.09.028.
   PubMed Web of Science ®Google Scholar
• Nakayama M, Ozaki H, Itoh Y, Soda K, Ishigaki H, Okamatsu M, Sakoda Y, Park C-H, Tsuchiya H, Kida H. et al. Vaccination against H9N2 avian influenza virus reduces bronchus-associated lymphoid tissue formation in cynomolgus macaques after intranasal virus challenge infection. Pathol Int. 2016;66(12):678–86. doi:10.1111/pin.12472.
   PubMed Web of Science ®Google Scholar
• Miyaki C, Quintilio W, Miyaji EN, Botosso VF, Kubrusly FS, Santos FL, Iourtov D, Higashi HG, Raw I. Production of H5N1 (NIBRG-14) inactivated whole virus and split virion influenza vaccines and analysis of immunogenicity in mice using different adjuvant formulations. Vaccine. 2010;28(13):2505–9. doi:10.1016/j.vaccine.2010.01.044.
   PubMed Web of Science ®Google Scholar
• Wong SS, Duan S, DeBeauchamp J, Zanin M, Kercher L, Sonnberg S, Fabrizio T, Jeevan T, Crumpton J-C, Oshansky C. et al. The immune correlates of protection for an avian influenza H5N1 vaccine in the ferret model using oil-in-water adjuvants. Sci Rep. 2017;7(1):44727. doi:10.1038/srep44727.
   PubMedGoogle Scholar
• Ruat C, Caillet C, Bidaut A, Simon J, Osterhaus AD. Vaccination of macaques with adjuvanted formalin-inactivated influenza a virus (H5N1) vaccines: protection against H5N1 challenge without disease enhancement. J Virol. 2008;82(5):2565–9. doi:10.1128/JVI.01928-07.
   PubMed Web of Science ®Google Scholar
• Duan Y, Gu H, Chen R, Zhao Z, Zhang L, Xing L, Lai C, Zhang P, Li Z, Zhang K. et al. Response of mice and ferrets to a monovalent influenza A (H7N9) split vaccine. PloS One. 2014;9(6):e99322. doi:10.1371/journal.pone.0099322.
   PubMed Web of Science ®Google Scholar
• Stadlbauer D, Waal L, Beaulieu E, Strohmeier S, Kroeze E, Boutet P, Osterhaus ADME, Krammer F, Innis BL, Nachbagauer R. et al. AS03-adjuvanted H7N9 inactivated split virion vaccines induce cross-reactive and protective responses in ferrets. NPJ Vaccines. 2021;6(1):40. doi:10.1038/s41541-021-00299-3.
   PubMed Web of Science ®Google Scholar
• Nogales A, Martinez-Sobrido L. Reverse genetics approaches for the development of influenza vaccines. Int J Mol Sci. 2016;18(1):20. doi:10.3390/ijms18010020.
   PubMed Web of Science ®Google Scholar
• Hickman D, Hossain MJ, Song H, Araya Y, Solorzano A, Perez DR. An avian live attenuated master backbone for potential use in epidemic and pandemic influenza vaccines. J Gen Virol. 2008;89:2682–90. doi:10.1099/vir.0.2008/004143-0.
   PubMed Web of Science ®Google Scholar
• Steel J, Lowen AC, Pena L, Angel M, Solórzano A, Albrecht R, Perez DR, García-Sastre A, Palese P. Live attenuated influenza viruses containing NS1 truncations as vaccine candidates against H5N1 highly pathogenic avian influenza. J Virol. 2009;83(4):1742–53. doi:10.1128/JVI.01920-08.
   PubMed Web of Science ®Google Scholar
• Watanabe T, Watanabe S, Kim JH, Hatta M, Kawaoka Y. Novel approach to the development of effective H5N1 influenza a virus vaccines: use of M2 cytoplasmic tail mutants. J Virol. 2008;82(5):2486–92. doi:10.1128/JVI.01899-07.
   PubMed Web of Science ®Google Scholar
• Caceres CJ, Cardenas-Garcia S, Jain A, Gay LC, Carnaccini S, Seibert B, Ferreri LM, Geiger G, Jasinskas A, Nakajima R, et al. Development of a novel live attenuated influenza a virus vaccine encoding the IgA-inducing protein. Vaccines. 2021;9. doi:10.3390/vaccines9070703.
   Web of Science ®Google Scholar
• Pena L, Sutton T, Chockalingam A, Kumar S, Angel M, Shao H, Chen H, Li W, Perez DR. Influenza viruses with rearranged genomes as live-attenuated vaccines. J Virol. 2013;87(9):5118–27. doi:10.1128/JVI.02490-12.
   PubMed Web of Science ®Google Scholar
• Ren W, Pei S, Jiang W, Zhao M, Jiang L, Liu H, Yi Y, Hui M, Li J. A replication-deficient H9N2 influenza virus carrying H5 hemagglutinin conferred protection against H9N2 and H5N1 influenza viruses in mice. Front Microbiol. 2022;13:1042916. doi:10.3389/fmicb.2022.1042916.
   PubMed Web of Science ®Google Scholar
• Lee YH, Jang YH, Seong BL. Cell-cultured, live attenuated, X-31ca-based H5N1 pre-pandemic influenza vaccine. Virology. 2017;504:73–8. doi:10.1016/j.virol.2017.01.021.
   PubMed Web of Science ®Google Scholar
• Suguitan AL Jr., McAuliffe J, Mills KL, Jin H, Duke G, Lu B, Luke CJ, Murphy B, Swayne DE, Kemble G. et al. Live, attenuated influenza a H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Med. 2006;3(9):e360. doi:10.1371/journal.pmed.0030360.
   PubMed Web of Science ®Google Scholar
• Fan S, Gao Y, Shinya K, Li CK, Li Y, Shi J, Jiang Y, Suo Y, Tong T, Zhong G. et al. Immunogenicity and protective efficacy of a live attenuated H5N1 vaccine in nonhuman primates. PloS Pathog. 2009;5(5):e1000409. doi:10.1371/journal.ppat.1000409.
   PubMed Web of Science ®Google Scholar
• Yang W, Yin X, Guan L, Li M, Ma S, Shi J, Deng G, Suzuki Y, Chen H. A live attenuated vaccine prevents replication and transmission of H7N9 highly pathogenic influenza viruses in mammals. Emerg Microbes Infect. 2018;7(1):1–0. doi:10.1038/s41426-018-0154-6.
   PubMedGoogle Scholar
• Yang X, Zhao J, Wang C, Duan Y, Zhao Z, Chen R, Zhang L, Xing L, Lai C, Zhang S. et al. Immunization with a live attenuated H7N9 influenza vaccine protects mice against lethal challenge. PloS One. 2015;10(4):e0123659. doi:10.1371/journal.pone.0123659.
   PubMed Web of Science ®Google Scholar
• Rudenko L, Kiseleva I, Krutikova E, Stepanova E, Isakova-Sivak I, Donina S, Rekstin A, Pisareva M, Bazhenova E, Kotomina T. et al. Two live attenuated vaccines against recent low–and highly pathogenic H7N9 influenza viruses are safe and immunogenic in ferrets. Vaccines. 2018;6(4):74. doi:10.3390/vaccines6040074.
   Web of Science ®Google Scholar
• Kong H, Zhang Q, Gu C, Shi J, Deng G, Ma S, Liu J, Chen P, Guan Y, Jiang Y. et al. A live attenuated vaccine prevents replication and transmission of H7N9 virus in mammals. Sci Rep. 2015;5(1):11233. doi:10.1038/srep11233.
   PubMedGoogle Scholar
• Chen H, Matsuoka Y, Swayne D, Chen Q, Cox NJ, Murphy BR. et al. Generation and characterization of a cold-adapted influenza a H9N2 reassortant as a live pandemic influenza virus vaccine candidate. Vaccine. 2003;21(27–30):4430–6. doi:10.1016/s0264-410x(03)00430-4.
   PubMed Web of Science ®Google Scholar
• Matsuoka Y, Suguitan A Jr., Orandle M, Paskel M, Boonnak K, Gardner DJ, Feldmann F, Feldmann H, Marino M, Jin H. et al. African green monkeys recapitulate the clinical experience with replication of live attenuated pandemic influenza virus vaccine candidates. J Virol. 2014;88(14):8139–52. doi:10.1128/JVI.00425-14.
   PubMed Web of Science ®Google Scholar
• Lin J, Zhang J, Dong X, Fang H, Chen J, Su N, Gao Q, Zhang Z, Liu Y, Wang Z. et al. Safety and immunogenicity of an inactivated adjuvanted whole-virion influenza a (H5N1) vaccine: a phase I randomised controlled trial. Lancet. 2006;368(9540):991–7. doi:10.1016/S0140-6736(06)69294-5.
   PubMed Web of Science ®Google Scholar
• van Boxtel RA, Verdijk P, de Boer OJ, van Riet E, Mensinga TT, Luytjes W. Safety and immunogenicity of influenza whole inactivated virus vaccines: a phase I randomized clinical trial. Hum Vaccin Immunother. 2015;11(4):983–90. doi:10.1080/21645515.2015.1012004.
   PubMed Web of Science ®Google Scholar
• Duong TN, Thiem VD, Anh DD, Cuong NP, Thang TC, Huong VM, Chien VC, Phuong NTL, Montomoli E, Holt R. et al. A phase 2/3 double blinded, randomized, placebo-controlled study in healthy adult participants in Vietnam to examine the safety and immunogenicity of an inactivated whole virion, alum adjuvanted, A(H5N1) influenza vaccine (IVACFLU-A/H5N1). Vaccine. 2020;38(6):1541–50. doi:10.1016/j.vaccine.2019.11.059.
   PubMed Web of Science ®Google Scholar
• Wang S, Xie Z, Huang L, Zhou X, Luo J, Yang Y, Li C, Duan P, Xu W, Chen D. et al. Safety and immunogenicity of an alum-adjuvanted whole-virion H7N9 influenza vaccine: a randomized, blinded, clinical trial. Clin Microbiol Infect. 2020;27(5):775–81. doi:10.1016/j.cmi.2020.07.033.
   Web of Science ®Google Scholar
• Aichinger G, Grohmann-Izay B, van der Velden MV, Fritsch S, Koska M, Portsmouth D, Hart MK, El-Amin W, Kistner O, Barrett PN. et al. Phase I/II randomized double-blind study of the safety and immunogenicity of a nonadjuvanted vero cell culture-derived whole-virus H9N2 influenza vaccine in healthy adults. Clin Vaccine Immunol. 2015;22(1):46–55. doi:10.1128/CVI.00275-14.
   PubMedGoogle Scholar
• Stephenson I, Nicholson KG, Gluck R, Mischler R, Newman RW, Palache AM, Verlander NQ, Warburton F, Wood JM, Zambon MC. et al. Safety and antigenicity of whole virus and subunit influenza A/Hong Kong/1073/99 (H9N2) vaccine in healthy adults: phase I randomised trial. Lancet. 2003;362(9400):1959–66. doi:10.1016/S0140-6736(03)15014-3.
   PubMed Web of Science ®Google Scholar
• Beyer WE, Nauta JJ, Palache AM, Giezeman KM, Osterhaus AD. Immunogenicity and safety of inactivated influenza vaccines in primed populations: a systematic literature review and meta-analysis. Vaccine. 2011;29(34):5785–92. doi:10.1016/j.vaccine.2011.05.040.
   PubMed Web of Science ®Google Scholar
• FDA. Clinical data needed to support the licensure of pandemic influenza vaccines. Center for Biologics Evaluation and Research (CBER). 2007. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/clinical-data-needed-support-licensure-pandemic-influenza-vaccines.
   Google Scholar
• Bresson JL, Perronne C, Launay O, Gerdil C, Saville M, Wood J, Höschler K, Zambon MC. Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet. 2006;367(9523):1657–64. doi:10.1016/S0140-6736(06)68656-X.
   PubMed Web of Science ®Google Scholar
• Levie K, Leroux-Roels I, Hoppenbrouwers K, Kervyn AD, Vandermeulen C, Forgus S, Leroux‐Roels G, Pichon S, Kusters I. An adjuvanted, low-dose, pandemic influenza a (H5N1) vaccine candidate is safe, immunogenic, and induces cross-reactive immune responses in healthy adults. J Infect Dis. 2008;198(5):642–9. doi:10.1086/590913.
   PubMed Web of Science ®Google Scholar
• Leroux-Roels I, Van der Wielen M, Kafeja F, Vandermeulen C, Lazarus R, Snape MD, John T, Carre C, Nougarede N, Pepin S. et al. Humoral and cellular immune responses to split-virion H5N1 influenza vaccine in young and elderly adults. Vaccine. 2009;27(49):6918–25. doi:10.1016/j.vaccine.2009.08.110.
   PubMed Web of Science ®Google Scholar
• Lazarus R, Kelly S, Snape MD, Vandermeulen C, Voysey M, Hoppenbrouwers K, Hens A, Van Damme P, Pepin S, Leroux-Roels I. et al. Antibody persistence and booster responses to split-virion H5N1 avian influenza vaccine in young and elderly adults. PLOS ONE. 2016;11(11):e0165384. doi:10.1371/journal.pone.0165384.
   PubMed Web of Science ®Google Scholar
• Chotpitayasunondh T, Thisyakorn U, Pancharoen C, Pepin S, Nougarede N. Safety, humoral and cell mediated immune responses to two formulations of an inactivated, split-virion influenza A/H5N1 vaccine in children. PLOS ONE. 2008;3(12):e4028. doi:10.1371/journal.pone.0004028.
   PubMed Web of Science ®Google Scholar
• Langley JM, Frenette L, Ferguson L, Riff D, Sheldon E, Risi G, Johnson C, Li P, Kenney R, Innis B. et al. Safety and cross-reactive immunogenicity of candidate AS03-adjuvanted prepandemic H5N1 influenza vaccines: a randomized controlled phase 1/2 trial in adults. J Infect Dis. 2010;201(11):1644–53. doi:10.1086/652701.
   PubMed Web of Science ®Google Scholar
• Langley JM, Risi G, Caldwell M, Gilderman L, Berwald B, Fogarty C, Poling T, Riff D, Baron M, Frenette L. et al. Dose-sparing H5N1 A/Indonesia/05/2005 pre-pandemic influenza vaccine in adults and elderly adults: a phase III, placebo-controlled, randomized study. J Infect Dis. 2011;203(12):1729–38. doi:10.1093/infdis/jir172.
   PubMed Web of Science ®Google Scholar
• Izurieta P, Kim WJ, Wie SH, Lee J, Lee JS, Drame M, Vaughn DW, Schuind A. Immunogenicity and safety of an AS03-adjuvanted H5N1 pandemic influenza vaccine in Korean adults: a phase IV, randomized, open-label, controlled study. Vaccine. 2015;33(24):2800–7. doi:10.1016/j.vaccine.2015.04.027.
   PubMed Web of Science ®Google Scholar
• Diez-Domingo J, Garces-Sanchez M, Baldo JM, Planelles MV, Ubeda I, JuBert A, Marés J, Moris P, Garcia-Corbeira P, Dramé M. et al. Immunogenicity and safety of H5N1 A/Vietnam/1194/2004 (Clade 1) AS03-adjuvanted prepandemic candidate influenza vaccines in children aged 3 to 9 years: a phase ii, randomized, open, controlled study. Pediatr Infect Dis J. 2010;29(6):e35–46. doi:10.1097/INF.0b013e3181daf921.
   PubMed Web of Science ®Google Scholar
• Chanthavanich P, Anderson E, Kerdpanich P, Bulitta M, Kanesa-Thasan N, Hohenboken M. Safety, tolerability and immunogenicity of an MF59-adjuvanted, Cell Culture-derived, A/H5N1, subunit influenza virus vaccine: results from a Dose-finding Clinical Trial in healthy pediatric subjects. Pediatr Infect Dis J. 2019;38:757–64. doi:10.1097/INF.0000000000002345.
   PubMed Web of Science ®Google Scholar
• Peterson J, Van Twuijver E, Versage E, Hohenboken M. Phase 3 randomized, multicenter, placebo-controlled study to evaluate safety, immunogenicity, and lot-to-lot consistency of an adjuvanted cell culture-derived, H5N1 subunit influenza virus vaccine in healthy adult subjects. Vaccines. 2022;10(4):497. doi:10.3390/vaccines10040497.
   Web of Science ®Google Scholar
• Frey SS, Versage E, Van Twuijver E, Hohenboken M. Antibody responses against heterologous H5N1 strains for an MF59-adjuvanted cell culture–derived H5N1 (aH5n1c) influenza vaccine in adults and older adults. Hum Vaccin Immunother. 2023;19(1):2193119. doi:10.1080/21645515.2023.2193119.
   PubMed Web of Science ®Google Scholar
• Frey SE, Shakib S, Chanthavanich P, Richmond P, Smith T, Tantawichien T, Kittel C, Jaehnig P, Mojares Z, Verma B. et al. Safety and Immunogenicity of MF59-Adjuvanted Cell Culture–derived A/H5N1 subunit influenza virus vaccine: Dose-Finding Clinical Trials in adults and the elderly. Open Forum Infect Dis. 2019;6(4):ofz107. doi:10.1093/ofid/ofz107.
   PubMed Web of Science ®Google Scholar
• Vanni T, Thome BC, Sparrow E, Friede M, Fox CB, Beckmann AM, Huynh C, Mondini G, Silveira DH, Viscondi JYK. et al. Dose-sparing effect of two adjuvant formulations with a pandemic influenza A/H7N9 vaccine: a randomized, double-blind, placebo-controlled, phase 1 clinical trial. PLOS ONE. 2022;17(10):e0274943. doi:10.1371/journal.pone.0274943.
   PubMed Web of Science ®Google Scholar
• Ortiz JR, Spearman PW, Goepfert PA, Cross K, Buddy Creech C, Chen WH, Parker S, Overton ET, Dickey M, Logan HL. et al. Safety and immunogenicity of monovalent H7N9 influenza vaccine with AS03 adjuvant given sequentially or simultaneously with a seasonal influenza vaccine: a randomized clinical trial. Vaccine. 2022;40(23):3253–62. doi:10.1016/j.vaccine.2022.03.055.
   PubMed Web of Science ®Google Scholar
• Madan A, Segall N, Ferguson M, Frenette L, Kroll R, Friel D, Soni J, Li P, Innis BL, Schuind A. Immunogenicity and safety of an AS03-adjuvanted H7N9 pandemic influenza vaccine in a randomized trial in healthy adults. J Infect Dis. 2016;214(11):1717–27. doi:10.1093/infdis/jiw414.
   PubMed Web of Science ®Google Scholar
• Madan A, Collins H, Sheldon E, Frenette L, Chu L, Friel D, Drame M, Vaughn DW, Innis BL, Schuind A. et al. Evaluation of a primary course of H9N2 vaccine with or without AS03 adjuvant in adults: a phase I/II randomized trial. Vaccine. 2017;35(35):4621–8. doi:10.1016/j.vaccine.2017.07.013.
   PubMed Web of Science ®Google Scholar
• Atmar RL, Keitel WA, Patel SM, Katz JM, She D, El Sahly H, Pompey J, Cate TR, Couch RB. Safety and immunogenicity of nonadjuvanted and MF59-adjuvanted influenza A/H9N2 vaccine preparations. Clin Infect Dis. 2006;43(9):1135–42. doi:10.1086/508174.
   PubMed Web of Science ®Google Scholar
• Nicolodi C, Groiss F, Kiselev O, Wolschek M, Seipelt J, Muster T. Safety and immunogenicity of a replication-deficient H5N1 influenza virus vaccine lacking NS1. Vaccine. 2019;37(28):3722–9. doi:10.1016/j.vaccine.2019.05.013.
   PubMed Web of Science ®Google Scholar
• Rudenko L, Desheva J, Korovkin S, Mironov A, Rekstin A, Grigorieva E, Donina S, Gambaryan A, Katlinsky A. Safety and immunogenicity of live attenuated influenza reassortant H5 vaccine (phase I–II clinical trials). Influenza Other Respir Viruses. 2008;2(6):203–9. doi:10.1111/j.1750-2659.2008.00064.x.
   PubMed Web of Science ®Google Scholar
• Karron RA, Talaat K, Luke C, Callahan K, Thumar B, Dilorenzo S, McAuliffe J, Schappell E, Suguitan A, Mills K. et al. Evaluation of two live attenuated cold-adapted H5N1 influenza virus vaccines in healthy adults. Vaccine. 2009;27(36):4953–60. doi:10.1016/j.vaccine.2009.05.099.
   PubMed Web of Science ®Google Scholar
• Pitisuttithum P, Boonnak K, Chamnanchanunt S, Puthavathana P, Luvira V, Lerdsamran H, Kaewkungwal J, Lawpoolsri S, Thanachartwet V, Silachamroon U. et al. Safety and immunogenicity of a live attenuated influenza H5 candidate vaccine strain A/17/turkey/Turkey/05/133 H5N2 and its priming effects for potential pre-pandemic use: a randomised, double-blind, placebo-controlled trial. Lancet Infect Dis. 2017;17(8):833–42. doi:10.1016/S1473-3099(17)30240-2.
   PubMed Web of Science ®Google Scholar
• Romanova J, Krenn BM, Wolschek M, Ferko B, Romanovskaja-Romanko E, Morokutti A, Shurygina A-P, Nakowitsch S, Ruthsatz T, Kiefmann B. et al. Preclinical Evaluation of a Replication-Deficient Intranasal ΔNS1 H5N1 Influenza Vaccine. PLOS ONE. 2009;4(6):e5984. doi:10.1371/journal.pone.0005984.
   PubMed Web of Science ®Google Scholar
• Rudenko L, Isakova-Sivak I, Naykhin A, Kiseleva I, Stukova M, Erofeeva M, Korenkov D, Matyushenko V, Sparrow E, Kieny M-P. et al. H7N9 live attenuated influenza vaccine in healthy adults: a randomised, double-blind, placebo-controlled, phase 1 trial. Lancet Infect Dis. 2016;16(3):303–10. doi:10.1016/S1473-3099(15)00378-3.
   PubMed Web of Science ®Google Scholar
• Kiseleva I, Isakova-Sivak I, Stukova M, Erofeeva M, Donina S, Larionova N, Krutikova E, Bazhenova E, Stepanova E, Vasilyev K. et al. A phase 1 randomized placebo-controlled study to assess the safety, immunogenicity and genetic stability of a new potential pandemic H7N9 live attenuated influenza vaccine in healthy adults. Vaccines. 2020;8(2):296. doi:10.3390/vaccines8020296.
   Web of Science ®Google Scholar
• Sobhanie M, Matsuoka Y, Jegaskanda S, Fitzgerald T, Mallory R, Chen Z, Luke C, Treanor J, Subbarao K. Evaluation of the safety and immunogenicity of a Candidate pandemic live attenuated influenza vaccine (pLAIV) against influenza A(H7N9). J Infect Dis. 2016;213(6):922–9. doi:10.1093/infdis/jiv526.
   PubMed Web of Science ®Google Scholar
• Karron RA, Callahan K, Luke C, Thumar B, McAuliffe J, Schappell E, Joseph T, Coelingh K, Jin H, Kemble G, et al. A live attenuated H9N2 influenza vaccine is well tolerated and immunogenic in healthy adults. J Infect Dis. 2009;199(5):711–6. doi:10.1086/596558.
   PubMed Web of Science ®Google Scholar
• Krammer F, Palese P. Universal influenza virus vaccines that target the conserved hemagglutinin stalk and conserved sites in the head domain. J Infect Dis. 2019;219(Supplement_1):62–7. doi:10.1093/infdis/jiy711.
   Google Scholar
• Krammer F, Palese P, Steel J. Advances in universal influenza virus vaccine design and antibody mediated therapies based on conserved regions of the hemagglutinin. Curr Top Microbiol Immunol. 2015;386:301–21. doi:10.1007/82_2014_408.
   PubMed Web of Science ®Google Scholar
• Galarza JM, Latham T, Cupo A. Virus-like particle (VLP) vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol. 2005;18:244–51. doi:10.1089/vim.2005.18.244.
   PubMed Web of Science ®Google Scholar
• Kapczynski DR, Tumpey TM, Hidajat R, Zsak A, Chrzastek K, Tretyakova I, Pushko P. Vaccination with virus-like particles containing H5 antigens from three H5N1 clades protects chickens from H5N1 and H5N8 influenza viruses. Vaccine. 2016;34(13):1575–81. doi:10.1016/j.vaccine.2016.02.011.
   PubMed Web of Science ®Google Scholar
• Ren Z, Ji X, Meng L, Wei Y, Wang T, Feng N, Zheng X, Wang H, Li N, Gao X. et al. H5N1 influenza virus-like particle vaccine protects mice from heterologous virus challenge better than whole inactivated virus. Virus Res. 2015;200:9–18. doi:10.1016/j.virusres.2015.01.007.
   PubMed Web of Science ®Google Scholar
• Hu J, Zhang Q, Peng P, Li R, Li J, Wang X, Gu M, Hu Z, Hu S, Liu X. et al. Baculovirus-derived influenza virus-like particle confers complete protection against lethal H7N9 avian influenza virus challenge in chickens and mice. Vet Microbiol. 2022;264:109306. doi:10.1016/j.vetmic.2021.109306.
   PubMed Web of Science ®Google Scholar
• Pushko P, Tumpey TM, Bu F, Knell J, Robinson R, Smith G. Influenza virus-like particles comprised of the HA, NA, and M1 proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine. 2005;23(50):5751–9. doi:10.1016/j.vaccine.2005.07.098.
   PubMed Web of Science ®Google Scholar
• Pushko P, Tumpey TM, Van Hoeven N, Belser JA, Robinson R, Nathan M, Smith G, Wright DC, Bright RA. Evaluation of influenza virus-like particles and Novasome adjuvant as candidate vaccine for avian influenza. Vaccine. 2007;25(21):4283–90. doi:10.1016/j.vaccine.2007.02.059.
   PubMed Web of Science ®Google Scholar
• Tretyakova I, Pearce MB, Florese R, Tumpey TM, Pushko P. Intranasal vaccination with H5, H7 and H9 hemagglutinins co-localized in a virus-like particle protects ferrets from multiple avian influenza viruses. Virology. 2013;442(1):67–73. doi:10.1016/j.virol.2013.03.027.
   PubMed Web of Science ®Google Scholar
• Pillet S, Couillard J, Trepanier S, Poulin JF, Yassine-Diab B, Guy B, Ward BJ, Landry N. Immunogenicity and safety of a quadrivalent plant-derived virus like particle influenza vaccine candidate—two randomized phase II clinical trials in 18 to 49 and ≥50 years old adults. PLOS ONE. 2019;14(6):e0216533. doi:10.1371/journal.pone.0216533.
   PubMed Web of Science ®Google Scholar
• Lopez-Macias C, Ferat-Osorio E, Tenorio-Calvo A, Isibasi A, Talavera J, Arteaga-Ruiz O, Arriaga-Pizano L, Hickman SP, Allende M, Lenhard K. et al. Safety and immunogenicity of a virus-like particle pandemic influenza a (H1N1) 2009 vaccine in a blinded, randomized, placebo-controlled trial of adults in Mexico. Vaccine. 2011;29(44):7826–34. doi:10.1016/j.vaccine.2011.07.099.
   PubMed Web of Science ®Google Scholar
• Landry N, Ward BJ, Trepanier S, Montomoli E, Dargis M, Lapini G, Vézina L-P. Preclinical and clinical development of plant-made virus-like particle vaccine against avian H5N1 influenza. PloS One. 2010;5(12):e15559. doi:10.1371/journal.pone.0015559.
   PubMed Web of Science ®Google Scholar
• Chung KY, Coyle EM, Jani D, King LR, Bhardwaj R, Fries L, Smith G, Glenn G, Golding H, Khurana S. et al. ISCOMATRIX™ adjuvant promotes epitope spreading and antibody affinity maturation of influenza a H7N9 virus like particle vaccine that correlate with virus neutralization in humans. Vaccine. 2015;33(32):3953–62. doi:10.1016/j.vaccine.2015.06.047.
   PubMed Web of Science ®Google Scholar
• Turner JS, O’Halloran JA, Kalaidina E, Kim W, Schmitz AJ, Zhou JQ, Lei T, Thapa M, Chen RE, Case JB. et al. SARS-CoV-2 mRNA vaccines induce persistent human germinal centre responses. Nature. 2021;596(7870):109–13. doi:10.1038/s41586-021-03738-2.
   PubMed Web of Science ®Google Scholar
• Furey C, Ye N, Kercher L, DeBeauchamp J, Crumpton JC, Jeevan T, Patton C, Franks J, Alameh MG, Fan SH, Phan AT. Development of a nucleoside-modified mRNA vaccine against clade 2.3.4.4b H5 highly pathogenic avian influenza virus. bioRxiv. 2023. doi:10.1101/2023.04.30.538854.
   Google Scholar
• Bahl K, Senn JJ, Yuzhakov O, Bulychev A, Brito LA, Hassett KJ, Laska ME, Smith M, Almarsson Ö, Thompson J. et al. Preclinical and clinical demonstration of immunogenicity by mRNA vaccines against H10N8 and H7N9 influenza viruses. Mol Ther. 2017;25(6):1316–27. doi:10.1016/j.ymthe.2017.03.035.
   PubMed Web of Science ®Google Scholar
• Xiong F, Zhang C, Shang B, Zheng M, Wang Q, Ding Y, Luo J, Li X. An mRNA-based broad-spectrum vaccine candidate confers cross-protection against heterosubtypic influenza a viruses. Emerg Microbes Infect. 2023;12(2):2256422. doi:10.1080/22221751.2023.2256422.
   PubMed Web of Science ®Google Scholar
• Feldman RA, Fuhr R, Smolenov I, Mick Ribeiro A, Panther L, Watson M, Senn JJ, Smith M, Almarsson Ӧ, Pujar HS. et al. mRNA vaccines against H10N8 and H7N9 influenza viruses of pandemic potential are immunogenic and well tolerated in healthy adults in phase 1 randomized clinical trials. Vaccine. 2019;37(25):3326–34. doi:10.1016/j.vaccine.2019.04.074.
   PubMed Web of Science ®Google Scholar
• Pillet S, Aubin E, Trepanier S, Poulin JF, Yassine-Diab B, Ter Meulen J, Ward BJ, Landry N. Humoral and cell-mediated immune responses to H5N1 plant-made virus-like particle vaccine are differentially impacted by alum and GLA-SE adjuvants in a phase 2 clinical trial. NPJ Vaccines. 2018;3(1):3. doi:10.1038/s41541-017-0043-3.
   PubMedGoogle Scholar
• Treanor JJ, Chu L, Essink B, Muse D, El Sahly HM, Izikson R, Goldenthal KL, Patriarca P, Dunkle LM. Stable emulsion (SE) alone is an effective adjuvant for a recombinant, baculovirus-expressed H5 influenza vaccine in healthy adults: a phase 2 trial. Vaccine. 2017;35(6):923–8. doi:10.1016/j.vaccine.2016.12.053.
   PubMed Web of Science ®Google Scholar
• Treanor JJ, Essink B, Hull S, Reed S, Izikson R, Patriarca P, Goldenthal KL, Kohberger R, Dunkle LM. Evaluation of safety and immunogenicity of recombinant influenza hemagglutinin (H5/Indonesia/05/2005) formulated with and without a stable oil-in-water emulsion containing glucopyranosyl-lipid a (SE+GLA) adjuvant. Vaccine. 2013;31(48):5760–5. doi:10.1016/j.vaccine.2013.08.064.
   PubMed Web of Science ®Google Scholar
• Stadlbauer D, Rajabhathor A, Amanat F, Kaplan D, Masud A, Treanor JJ, Izikson R, Cox MM, Nachbagauer R, Krammer F. et al. Vaccination with a recombinant H7 hemagglutinin-based influenza virus vaccine induces broadly reactive antibodies in humans. mSphere. 2017;2(6). doi:10.1128/mSphere.00502-17.
   PubMed Web of Science ®Google Scholar