Safety and immunogenicity of a heterologous booster with an RBD virus-like particle vaccine following two- or three-dose inactivated COVID-19 vaccine

References

• Goldberg Y, Mandel M, Bar-On YM, Bodenheimer O, Freedman L, Haas EJ, Milo R, Alroy-Preis S, Ash N, Huppert A. Waning immunity after the BNT162b2 vaccine in Israel. N Engl J Med. 2021;385:e85. doi:10.1056/NEJMoa2114228.
   PubMed Web of Science ®Google Scholar
• Andrews N, Stowe J, Kirsebom F, Toffa S, Rickeard T, Gallagher E, Gower C, Kall M, Groves N, O’Connell A-M, et al. Covid-19 vaccine effectiveness against the Omicron (B.1.1.529) variant. N Engl J Med. 2022;386:1532–12. doi:10.1056/NEJMoa2119451.
   PubMed Web of Science ®Google Scholar
• Abu-Raddad LJ, Chemaitelly H, Bertollini R, National Study Group for C-V. Waning mRNA-1273 vaccine effectiveness against SARS-CoV-2 infection in Qatar. N Engl J Med. 2022;386:1091–3. doi:10.1056/NEJMc2119432.
   PubMed Web of Science ®Google Scholar
• Zeng G, Wu Q, Pan H, Li M, Yang J, Wang L, Wu Z, Jiang D, Deng X, Chu K, et al. Immunogenicity and safety of a third dose of CoronaVac, and immune persistence of a two-dose schedule, in healthy adults: interim results from two single-centre, double-blind, randomised, placebo-controlled phase 2 clinical trials. Lancet Infect Dis. 2022;22:483–95. doi:10.1016/S1473-3099(21)00681-2.
   PubMed Web of Science ®Google Scholar
• Li J, Hou L, Guo X, Jin P, Wu S, Zhu J, Pan H, Wang X, Song Z, Wan J, et al. Heterologous AD5-nCOV plus CoronaVac versus homologous CoronaVac vaccination: a randomized phase 4 trial. Nat Med. 2022;28:401–9. doi:10.1038/s41591-021-01677-z.
   PubMed Web of Science ®Google Scholar
• Munro APS, Janani L, Cornelius V, Aley PK, Babbage G, Baxter D, Bula M, Cathie K, Chatterjee K, Dodd K, et al. Safety and immunogenicity of seven COVID-19 vaccines as a third dose (booster) following two doses of ChAdOx1 nCov-19 or BNT162b2 in the UK (COV-BOOST): a blinded, multicentre, randomised, controlled, phase 2 trial. Lancet. 2021;398:2258–76. doi:10.1016/S0140-6736(21)02717-3.
   PubMed Web of Science ®Google Scholar
• Callaway E. COVID vaccine boosters: the most important questions. Nature. 2021;596:178–80. doi:10.1038/d41586-021-02158-6.
   PubMed Web of Science ®Google Scholar
• Costa Clemens SA, Weckx L, Clemens R, Almeida Mendes AV, Ramos Souza A, Silveira MBV, da Guarda SNF, de Nobrega MM, de Moraes Pinto MI, Gonzalez IGS, et al. Heterologous versus homologous COVID-19 booster vaccination in previous recipients of two doses of CoronaVac COVID-19 vaccine in Brazil (RHH-001): a phase 4, non-inferiority, single blind, randomised study. Lancet. 2022;399:521–9. doi:10.1016/S0140-6736(22)00094-0.
   PubMed Web of Science ®Google Scholar
• Pérez-Then E, Lucas C, Monteiro VS, Miric M, Brache V, Cochon L, Vogels CBF, Malik AA, De la Cruz E, Jorge A, et al. Neutralizing antibodies against the SARS-CoV-2 Delta and Omicron variants following heterologous CoronaVac plus BNT162b2 booster vaccination. Nat Med. 2022;28:481–5. doi:10.1038/s41591-022-01705-6.
   PubMed Web of Science ®Google Scholar
• Cheng SMS, Mok CKP, Leung YWY, Ng SS, Chan KCK, Ko FW, Chen C, Yiu K, Lam BHS, Lau EHY, et al. Neutralizing antibodies against the SARS-CoV-2 Omicron variant BA.1 following homologous and heterologous CoronaVac or BNT162b2 vaccination. Nat Med. 2022;28:486–9. doi:10.1038/s41591-022-01704-7.
   PubMed Web of Science ®Google Scholar
• Dolgin E. Omicron thwarts some of the world’s most-used COVID vaccines. Nature. 2022;601:311. doi:10.1038/d41586-022-00079-6.
   PubMed Web of Science ®Google Scholar
• McMenamin ME, Nealon J, Lin Y, Wong JY, Cheung JK, Lau EHY, Wu P, Leung GM, Cowling BJ. Vaccine effectiveness of one, two, and three doses of BNT162b2 and CoronaVac against COVID-19 in Hong Kong: a population-based observational study. Lancet Infect Dis. 2022;22:1435–43. doi:10.1016/s1473-3099(22)00345-0.
   PubMed Web of Science ®Google Scholar
• Jara A, Undurraga EA, Zubizarreta JR, González C, Pizarro A, Acevedo J, Leo K, Paredes F, Bralic T, Vergara V, et al. Effectiveness of homologous and heterologous booster doses for an inactivated SARS-CoV-2 vaccine: a large-scale prospective cohort study. Lancet Glob Health. 2022;10:e798–e806. doi:10.1016/s2214-109x(22)00112-7.
   PubMed Web of Science ®Google Scholar
• Yu X, Wei D, Xu W, Li Y, Li X, Zhang X, Qu J, Yang Z, Chen E. Reduced sensitivity of SARS-CoV-2 Omicron variant to antibody neutralization elicited by booster vaccination. Cell Discov. 2022;8:4. doi:10.1038/s41421-022-00375-5.
   PubMed Web of Science ®Google Scholar
• Melo-González F, Méndez C, Peñaloza HF, Schultz BM, Piña-Iturbe A, Ríos M, Moreno-Tapia D, Pereira-Sanchez P, Leighton D, Orellana C, Covarrubias C. Humoral and cellular response induced by a second booster of an inactivated SARS-CoV-2 vaccine in adults. medRxiv 2022:2022.08.22.22279080. doi:10.1101/2022.08.22.22279080.
   Google Scholar
• Ranzani OT, Hitchings MDT, de Melo RL, de França GVA, Fernandes CDFR, Lind ML, Torres MSS, Tsuha DH, David LCS, Said RFC, et al. Effectiveness of an inactivated Covid-19 vaccine with homologous and heterologous boosters against Omicron in Brazil. Nat Commun. 2022;13:5536. doi:10.1038/s41467-022-33169-0.
   PubMed Web of Science ®Google Scholar
• Huang Z, Xu S, Liu J, Wu L, Qiu J, Wang N, Ren J, Li Z, Guo X, Tao F, et al. Effectiveness of inactivated and Ad5-nCov COVID-19 vaccines against SARS-CoV-2 Omicron BA. 2 variant infection, severe illness, and death. BMC Med. 2022;20:400. doi:10.1186/s12916-022-02606-8.
   PubMed Web of Science ®Google Scholar
• Dai L, Gao GF. Viral targets for vaccines against COVID-19. Nat Rev Immunol. 2021;21:73–82. doi:10.1038/s41577-020-00480-0.
   PubMed Web of Science ®Google Scholar
• Li Y, Zhang Y, Zhou Y, Li Y, Xu J, Ai Y, Xu L, Xiao X, Zhang B, Jin J, et al. An RBD virus-like particle vaccine for SARS-CoV-2 induces cross-variant antibody responses in mice and macaques. Signal Transduct Target Ther. 2023;8:173. doi:10.1038/s41392-023-01425-4.
   PubMed Web of Science ®Google Scholar
• Bruun TUJ, Andersson AC, Draper SJ, Howarth M. Engineering a rugged nanoscaffold to enhance plug-and-display vaccination. Acs Nano. 2018;12:8855–66. doi:10.1021/acsnano.8b02805.
   PubMed Web of Science ®Google Scholar
• Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol. 2010;10:787–96. doi:10.1038/nri2868.
   PubMed Web of Science ®Google Scholar
• Lin YJ, Shih YJ, Chen CH, Fang CT. Aluminum salts as an adjuvant for pre-pandemic influenza vaccines: a meta-analysis. Sci Rep. 2018;8:11460. doi:10.1038/s41598-018-29858-w.
   PubMed Web of Science ®Google Scholar
• Sahin U, Muik A, Derhovanessian E, Vogler I, Kranz LM, Vormehr M, Baum A, Pascal K, Quandt J, Maurus D, et al. COVID-19 vaccine BNT162b1 elicits human antibody and T(H)1 T cell responses. Nature. 2020;586:594–9. doi:10.1038/s41586-020-2814-7.
   PubMed Web of Science ®Google Scholar
• Song JY, Choi WS, Heo JY, Lee JS, Jung DS, Kim SW, Park K-H, Eom JS, Jeong SJ, Lee J, et al. Safety and immunogenicity of a SARS-CoV-2 recombinant protein nanoparticle vaccine (GBP510) adjuvanted with AS03: a randomised, placebo-controlled, observer-blinded phase 1/2 trial. EClinicalMedicine. 2022;51:101569. doi:10.1016/j.eclinm.2022.101569.
   PubMedGoogle Scholar
• Ward BJ, Gobeil P, Seguin A, Atkins J, Boulay I, Charbonneau PY, Couture M, D’Aoust M-A, Dhaliwall J, Finkle C, et al. Phase 1 randomized trial of a plant-derived virus-like particle vaccine for COVID-19. Nat Med. 2021;27:1071–8. doi:10.1038/s41591-021-01370-1.
   PubMed Web of Science ®Google Scholar
• Zhang Z, He Q, Zhao W, Li Y, Yang J, Hu Z, Chen X, Peng H, Fu Y-X, Chen L, et al. A heterologous V-01 or variant-matched bivalent V-01D-351 booster following primary series of inactivated vaccine enhances the neutralizing capacity against SARS-CoV-2 Delta and Omicron strains. J Clin Med. 2022;11:11. doi:10.3390/jcm11144164.
   Web of Science ®Google Scholar
• Ai J, Wang X, He X, Zhao X, Zhang Y, Jiang Y, Li M, Cui Y, Chen Y, Qiao R, et al. Antibody evasion of SARS-CoV-2 Omicron BA.1, BA.1.1, BA.2, and BA.3 sub-lineages. Cell Host Microbe. 2022;30:1077–83 e4. doi:10.1016/j.chom.2022.05.001.
   PubMed Web of Science ®Google Scholar
• Nilles EJ, Paulino CT, de St Aubin M, Duke W, Jarolim P, Sanchez IM, Murray KO, Lau CL, Gutiérrez EZ, Ramm RS, et al. Tracking immune correlates of protection for emerging SARS-CoV-2 variants. Lancet Infect Dis. 2023;23:153–4. doi:10.1016/s1473-3099(23)00001-4.
   PubMed Web of Science ®Google Scholar
• Lang-Meli J, Luxenburger H, Wild K, Karl V, Oberhardt V, Salimi Alizei E, Graeser A, Reinscheid M, Roehlen N, Reeg DB, et al. SARS-CoV-2-specific T-cell epitope repertoire in convalescent and mRNA-vaccinated individuals. Nat Microbiol. 2022;7:675–9. doi:10.1038/s41564-022-01106-y.
   PubMed Web of Science ®Google Scholar
• Keeton R, Tincho MB, Ngomti A, Baguma R, Benede N, Suzuki A, Khan K, Cele S, Bernstein M, Karim F, et al. Author correction: T cell responses to SARS-CoV-2 spike cross-recognize Omicron. Nature. 2022;604:E25. doi:10.1038/s41586-022-04708-y.
   PubMed Web of Science ®Google Scholar
• Assawakosri S, Kanokudom S, Suntronwong N, Auphimai C, Nilyanimit P, Vichaiwattana P, Thongmee T, Duangchinda T, Chantima W, Pakchotanon P, Srimuan D. Neutralizing activities against the Omicron variant after a heterologous booster in healthy adults receiving two doses of CoronaVac vaccination. J Infect Dis. 2022;226:1372–1381. doi:10.1101/2022.01.28.22269986.
   PubMed Web of Science ®Google Scholar
• Filardi BA, Monteiro VS, Schwartzmann PV, Do Prado Martins V, Zucca LER, Baiocchi GC, Malik AA, Silva J, Hahn AM, Chen NF, et al. Age-dependent impairment in antibody responses elicited by a homologous CoronaVac booster dose. Sci Transl Med. 2023;15:eade6023. doi:10.1126/scitranslmed.ade6023.
   PubMed Web of Science ®Google Scholar
• Zhu FC, Guan XH, Li YH, Huang JY, Jiang T, Hou LH, Li J-X, Yang B-F, Wang L, Wang W-J, et al. Immunogenicity and safety of a recombinant adenovirus type-5-vectored COVID-19 vaccine in healthy adults aged 18 years or older: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet. 2020;396:479–88. doi:10.1016/s0140-6736(20)31605-6.
   PubMed Web of Science ®Google Scholar
• Grifoni A, Weiskopf D, Ramirez SI, Mateus J, Dan JM, Moderbacher CR, Rawlings SA, Sutherland A, Premkumar L, Jadi RS, et al. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell. 2020;181:1489–501 e15. doi:10.1016/j.cell.2020.05.015.
   PubMed Web of Science ®Google Scholar
• Sette A, Crotty S. Pre-existing immunity to SARS-CoV-2: the knowns and unknowns. Nat Rev Immunol. 2020;20:457–8. doi:10.1038/s41577-020-0389-z.
   PubMed Web of Science ®Google Scholar