Homologous or heterologous administration of mRNA or adenovirus-vectored vaccines show comparable immunogenicity and effectiveness against the SARS-CoV-2 Omicron variant

References

• Dejnirattisai W, Shaw RH, Supasa P, et al. Reduced neutralisation of SARS-CoV-2 omicron B.1.1.529 variant by post-immunisation serum. Lancet. 2022;399(10321):234–236. doi: 10.1016/S0140-6736(21)02844-0
   PubMed Web of Science ®Google Scholar
• Lau JJ, Cheng SMS, Leung K, et al. Real-world COVID-19 vaccine effectiveness against the omicron BA.2 variant in a SARS-CoV-2 infection-naive population. Nat Med. 2023;29(2):348–357. doi: 10.1038/s41591-023-02219-5
   PubMed Web of Science ®Google Scholar
• Dejnirattisai W, Huo J, Zhou D, et al. SARS-CoV-2 omicron-B.1.1.529 leads to widespread escape from neutralizing antibody responses. Cell. 2022;185(3):467–484.e15. doi: 10.1016/j.cell.2021.12.046
   PubMed Web of Science ®Google Scholar
• Macchia A, Ferrante D, Bouzas MB, et al. Immunogenicity induced by the use of alternative vaccine platforms to deal with vaccine shortages in a low- to middle-income country: results of two randomized clinical trials. The Lancet Regional Health – Americas [Internet]. 2022;9:100196. [cited 2023 Oct 17]. Available from: https://www.thelancet.com/journals/lanam/article/PIIS2667-193X(22)00013-8/fulltext
   PubMedGoogle Scholar
• Webster P. Russian COVID-19 vaccine in jeopardy after Ukraine invasion. Nature Med Internet. 2022; [cited 2023 Oct 17]. Available from: https://www.nature.com/articles/d41591-022-00042-y
   Google Scholar
• Schneider J, Gilbert SC, Blanchard TJ, et al. Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nat Med. 1998;4(4):397–402. doi: 10.1038/nm0498-397
   PubMed Web of Science ®Google Scholar
• Hanke T, Samuel RV, Blanchard TJ, et al. Effective induction of simian immunodeficiency virus-specific cytotoxic T lymphocytes in macaques by using a multiepitope gene and DNA prime-modified vaccinia virus ankara boost vaccination regimen. J Virol. 1999;73(9):7524–7532. doi: 10.1128/JVI.73.9.7524-7532.1999
   PubMed Web of Science ®Google Scholar
• Robinson HL, Montefiori DC, Johnson RP, et al. Neutralizing antibody-independent containment of immunodeficiency virus challenges by DNA priming and recombinant pox virus booster immunizations. Nat Med. 1999;5(5):526–534. doi: 10.1038/8406
   PubMed Web of Science ®Google Scholar
• Lu S. Heterologous prime–boost vaccination. Curr Opin Immunol. 2009;21(3):346–351. doi: 10.1016/j.coi.2009.05.016
   PubMed Web of Science ®Google Scholar
• Ramshaw IA, Ramsay AJ. The prime-boost strategy: exciting prospects for improved vaccination. Immunol Today. 2000;21(4):163–165. doi: 10.1016/S0167-5699(00)01612-1
   PubMedGoogle Scholar
• Lapuente D, Fuchs J, Willar J, et al. Protective mucosal immunity against SARS-CoV-2 after heterologous systemic prime-mucosal boost immunization. Nat Commun. 2021;12(1):6871. doi: 10.1038/s41467-021-27063-4
   PubMed Web of Science ®Google Scholar
• Ciabattini A, Pettini E, Fiorino F, et al. Heterologous prime-boost combinations highlight the crucial role of adjuvant in priming the immune system. Front Immunol. 2018;9:380. doi: 10.3389/fimmu.2018.00380
   PubMed Web of Science ®Google Scholar
• Pettini E, Prota G, Ciabattini A, et al. Vaginal immunization to elicit primary T-cell activation and dissemination. PLoS One. 2013;8(12):e80545. doi: 10.1371/journal.pone.0080545
   PubMed Web of Science ®Google Scholar
• Ciabattini A, Pettini E, Fiorino F, et al. Modulation of primary immune response by different vaccine adjuvants. Front Immunol. 2016;7:427. doi: 10.3389/fimmu.2016.00427
   PubMed Web of Science ®Google Scholar
• Ciabattini A, Prota G, Christensen D, et al. Characterization of the Antigen-Specific CD4(+) T cell response induced by prime-boost strategies with CAF01 and CpG adjuvants administered by the intranasal and subcutaneous routes. Front Immunol. 2015;6:430. doi: 10.3389/fimmu.2015.00430
   PubMed Web of Science ®Google Scholar
• Fiorino F, Pettini E, Pozzi G, et al. Prime-boost strategies in mucosal immunization affect local IgA production and the type of Th response. Front Immunol. 2013;4:128. doi: 10.3389/fimmu.2013.00128
   PubMed Web of Science ®Google Scholar
• Zhang Y, Guo X, Guo M, et al. Combined prime-boost immunization with systemic and mucosal pneumococcal vaccines based on pneumococcal surface protein a to enhance protection against lethal pneumococcal infections. Immunol Res. 2019;67(4–5):398–407. doi: 10.1007/s12026-019-09107-6
   PubMed Web of Science ®Google Scholar
• Lapuente D, Viherlehto V, Fuchs J, et al. Adenoviral vector vaccines are effective mucosal booster modalities to elevate systemic and establish mucosal immunity against SARS-CoV-2. J Immunol. 2023;210(1_Supplement):253.01. doi: 10.4049/jimmunol.210.Supp.253.01
   Web of Science ®Google Scholar
• Christensen D, Polacek C, Sheward DJ, et al. Protection against SARS-CoV-2 transmission by a parenteral prime—intranasal boost vaccine strategy. EBioMedicine [Internet]. 2022;84:104248. [cited 2024 Mar 11]. Available from: https://www.thelancet.com/journals/ebiom/article/PIIS2352-3964(22)00430-3/fulltext
   PubMed Web of Science ®Google Scholar
• Nuñez NG, Schmid J, Power L, et al. High-dimensional analysis of 16 SARS-CoV-2 vaccine combinations reveals lymphocyte signatures correlating with immunogenicity. Nat Immunol. 2023;24(6):941–954. doi: 10.1038/s41590-023-01499-w
   PubMed Web of Science ®Google Scholar
• Atmar RL, Lyke KE, Deming ME, et al. Homologous and heterologous Covid-19 booster vaccinations. N Engl J Med. 2022;386(11):1046–1057. doi: 10.1056/NEJMoa2116414
   PubMed Web of Science ®Google Scholar
• Pérez-Then E, Lucas C, Monteiro VS, et al. Neutralizing antibodies against the SARS-CoV-2 delta and omicron variants following heterologous CoronaVac plus BNT162b2 booster vaccination. Nat Med. 2022;28(3):481–485. doi: 10.1038/s41591-022-01705-6
   PubMed Web of Science ®Google Scholar
• Wagner A, Ohradanova-Repic A, Gebetsberger L, et al. Full seroconversion in initial non-responders with higher antibody levels after heterologous COVID-19 vaccination schedule. Immunol Lett. 2022;250:1–6. doi: 10.1016/j.imlet.2022.09.001
   PubMed Web of Science ®Google Scholar
• Regan JJ, Moulia DL, Link-Gelles R. Use of updated COVID-19 vaccines 2023–2024 formula for persons aged ≥6 months: recommendations of the Advisory Committee on Immunization Practices — United States, September 2023. MMWR Morb Mortal Wkly Rep [Internet]. 2023;72(42):1140–1146. [cited 2023 Oct 19]. Available from https://www.cdc.gov/mmwr/volumes/72/wr/mm7242e1.htm
   PubMed Web of Science ®Google Scholar
• Lucchesi S, Furini S, Medaglini D, et al. From bivariate to multivariate analysis of cytometric data: overview of computational methods and their application in vaccination studies. Vaccines (Basel). 2020;8(1):8. doi: 10.3390/vaccines8010138
   Web of Science ®Google Scholar
• Lucchesi S, Nolfi E, Pettini E, et al. Computational analysis of multiparametric flow cytometric data to dissect B cell subsets in vaccine studies. Cytometry Pt A. 2020;97(3):259–267. doi: 10.1002/cyto.a.23922
   PubMed Web of Science ®Google Scholar
• Ciabattini A, Pastore G, Fiorino F, et al. Evidence of SARS-CoV-2-specific memory B cells six months after vaccination with the BNT162b2 mRNA vaccine. Front Immunol. 2021;12:740708. doi: 10.3389/fimmu.2021.740708
   PubMed Web of Science ®Google Scholar
• Fiorino F, Sicuranza A, Ciabattini A, et al. The slower antibody response in myelofibrosis patients after two doses of mRNA SARS-CoV-2 vaccine calls for a third dose. Biomedicines. 2021;9(10):1480. doi: 10.3390/biomedicines9101480
   PubMed Web of Science ®Google Scholar
• Tan CW, Chia WN, Qin X, et al. A SARS-CoV-2 surrogate virus neutralization test based on antibody-mediated blockage of ACE2–spike protein–protein interaction. Nat Biotechnol. 2020;38(9):1073–1078. doi: 10.1038/s41587-020-0631-z
   PubMed Web of Science ®Google Scholar
• Ciabattini A, Pastore G, Lucchesi S, et al. Trajectory of spike-specific B cells elicited by two doses of BNT162b2 mRNA vaccine. Cells. 2023;12(13):1706. doi: 10.3390/cells12131706
   PubMed Web of Science ®Google Scholar
• Van Gassen S, Callebaut B, Van Helden MJ, et al. FlowSOM: using self-organizing maps for visualization and interpretation of cytometry data. Cytometry Pt A. 2015;87(7):636–645. doi: 10.1002/cyto.a.22625
   PubMedGoogle Scholar
• Malek M, Taghiyar MJ, Chong L, et al. flowDensity: reproducing manual gating of flow cytometry data by automated density-based cell population identification. Bioinformatics. 2015;31(4):606–607. doi: 10.1093/bioinformatics/btu677
   PubMed Web of Science ®Google Scholar
• Wickham H. ggplot2 [Internet]. Cham: Springer International Publishing; 2016 [cited 2023 Nov 20]. Available from: http://doi.org/10.1007/978-3-319-24277-4
   Google Scholar
• Habibzadeh F, Habibzadeh P, Yadollahie M. On measuring vaccine effectiveness with observational study designs. Acta Med Acad. 2022;51(2):134–146. doi: 10.5644/ama2006-124.383
   PubMedGoogle Scholar
• Yoshimura M, Sakamoto A, Ozuru R, et al. The appearance of anti-spike receptor binding domain immunoglobulin G4 responses after repetitive immunization with messenger RNA-based COVID-19 vaccines. Int J Infect Dis. 2024;139:1–5. doi: 10.1016/j.ijid.2023.11.028
   PubMed Web of Science ®Google Scholar
• Irrgang P, Gerling J, Kocher K, et al. Class switch toward noninflammatory, spike-specific IgG4 antibodies after repeated SARS-CoV-2 mRNA vaccination. Sci Immunol. 2022;8(79):eade2798. doi: 10.1126/sciimmunol.ade2798
   Web of Science ®Google Scholar
• Cocherie T, Zafilaza K, Leducq V, et al. Epidemiology and characteristics of SARS-CoV-2 variants of concern: the impacts of the Spike Mutations. Microorganisms. 2022;11(1):30. doi: 10.3390/microorganisms11010030
   PubMed Web of Science ®Google Scholar
• National Institutes of Health [Internet]. Coronavirus Disease 2019 (COVID-19) Treatment Guidelines. [cited 2024 Jan 9]. Available from: https://www.covid19treatmentguidelines.nih.gov/overview/clinical-spectrum/
   Google Scholar
• Guerrini G, Magrì D, Gioria S, et al. Characterization of nanoparticles-based vaccines for COVID-19. Nat Nanotech. 2022;17(6):570–576. doi: 10.1038/s41565-022-01129-w
   PubMed Web of Science ®Google Scholar
• Carreño JM, Singh G, Tcheou J, et al. mRNA-1273 but not BNT162b2 induces antibodies against polyethylene glycol (PEG) contained in mRNA-based vaccine formulations. Vaccine. 2022;40:6114–6124. doi: 10.1016/j.vaccine.2022.08.024
   PubMed Web of Science ®Google Scholar
• Chapin-Bardales J, Gee J, Myers T. Reactogenicity following receipt of mRNA-based COVID-19 vaccines. JAMA. 2021;325(21):2201–2202. doi: 10.1001/jama.2021.5374
   PubMed Web of Science ®Google Scholar
• Guerrini G, Gioria S, Sauer AV, et al. Monitoring anti-PEG antibodies level upon repeated lipid nanoparticle-based COVID-19 vaccine administration. Int J Mol Sci. 2022;23(16):8838. doi: 10.3390/ijms23168838
   PubMed Web of Science ®Google Scholar
• Buhre JS, Pongracz T, Künsting I, et al. mRNA vaccines against SARS-CoV-2 induce comparably low long-term IgG fc galactosylation and sialylation levels but increasing long-term IgG4 responses compared to an adenovirus-based vaccine. Front Immunol. 2022;13:1020844. doi: 10.3389/fimmu.2022.1020844
   PubMed Web of Science ®Google Scholar
• Pillai S. Is it bad, is it good, or is IgG4 just misunderstood? Sci Immunol. 2023;8(81):eadg7327. doi: 10.1126/sciimmunol.adg7327
   PubMed Web of Science ®Google Scholar
• Rispens T, Huijbers MG. The unique properties of IgG4 and its roles in health and disease. Nat Rev Immunol. 2023;23(11):763–778. doi: 10.1038/s41577-023-00871-z
   PubMed Web of Science ®Google Scholar
• Vidarsson G, Dekkers G, Rispens T. IgG subclasses and Allotypes: from structure to effector functions. Front Immunol [Internet]. 2014;5. [cited 2024 Mar 8]. Available from: https://www.frontiersin.org/journals/immunology/articles/10.3389/fimmu.2014.00520/full
   PubMed Web of Science ®Google Scholar
• Röltgen K, Nielsen SCA, Silva O, et al. Immune imprinting, breadth of variant recognition, and germinal center response in human SARS-CoV-2 infection and vaccination. Cell. 2022;185(6):1025–1040.e14. doi: 10.1016/j.cell.2022.01.018
   PubMed Web of Science ®Google Scholar
• Uversky VN, Redwan EM, Makis W, et al. IgG4 antibodies induced by repeated vaccination may generate immune tolerance to the SARS-CoV-2 Spike Protein. Vaccines. 2023;11(5):991. doi: 10.3390/vaccines11050991
   Web of Science ®Google Scholar
• Pape KA, Dileepan T, Kabage AJ, et al. High-affinity memory B cells induced by SARS-CoV-2 infection produce more plasmablasts and atypical memory B cells than those primed by mRNA vaccines. Cell Rep. 2021;37(2):109823. doi: 10.1016/j.celrep.2021.109823
   PubMed Web of Science ®Google Scholar
• Courey-Ghaouzi A-D, Kleberg L, Sundling C. Alternative B cell differentiation during infection and inflammation. Front Immunol [Internet]. 2022;13. [cited 2022 Oct 20]. Available from: https://www.frontiersin.org/articles/10.3389/fimmu.2022.908034
   PubMed Web of Science ®Google Scholar
• Moir S, Ho J, Malaspina A, et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med. 2008;205(8):1797–1805. doi: 10.1084/jem.20072683
   PubMed Web of Science ®Google Scholar
• Weiss GE, Crompton PD, Li S, et al. Atypical memory B cells are greatly expanded in individuals living in a Malaria-Endemic Area. J Immunol. 2009;183(3):2176–2182. doi: 10.4049/jimmunol.0901297
   PubMed Web of Science ®Google Scholar
• Wei C, Anolik J, Cappione A, et al. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J Immunol. 2007;178(10):6624–6633. doi: 10.4049/jimmunol.178.10.6624
   PubMed Web of Science ®Google Scholar
• Andrews SF, Chambers MJ, Schramm CA, et al. Activation dynamics and immunoglobulin evolution of pre-existing and newly generated human memory B cell responses to influenza Hemagglutinin. Immunity. 2019;51(2):398–410.e5. doi: 10.1016/j.immuni.2019.06.024
   PubMed Web of Science ®Google Scholar
• Sutton HJ, Aye R, Idris AH, et al. Atypical B cells are part of an alternative lineage of B cells that participates in responses to vaccination and infection in humans. Cell Rep [Internet]. 2021;34(6):108684. [cited 2022 Nov 15] Available from: https://www.cell.com/cell-reports/abstract/S2211-1247(20)31673-9
   PubMed Web of Science ®Google Scholar
• Ferreira IATM, Lee CYC, Foster WS, et al. Atypical B cells and impaired SARS-CoV-2 neutralization following heterologous vaccination in the elderly. Cell Rep. 2023;42(8):112991. doi: 10.1016/j.celrep.2023.112991
   PubMed Web of Science ®Google Scholar
• Polvere J, Fabbiani M, Pastore G, et al. B cell response after SARS-CoV-2 mRNA vaccination in people living with HIV. Commun Med (Lond). 2023;3(1):13. doi: 10.1038/s43856-023-00245-5
   PubMedGoogle Scholar
• Zhang Z, Mateus J, Coelho CH, et al. Humoral and cellular immune memory to four COVID-19 vaccines. Cell. 2022;185(14):2434–2451.e17. doi: 10.1016/j.cell.2022.05.022
   PubMed Web of Science ®Google Scholar
• Fedele G, Trentini F, Schiavoni I, et al. Evaluation of humoral and cellular response to four vaccines against COVID-19 in different age groups: a longitudinal study. Front Immunol [Internet]. 2022;13. [cited 2023 Jun 12]. Available from: https://www.frontiersin.org/articles/10.3389/fimmu.2022.1021396
   Web of Science ®Google Scholar
• Pettini E, Ciabattini A, Pastore G, et al. A third dose of mRNA-1273 vaccine improves SARS-CoV-2 immunity in HCT recipients with low antibody response after 2 doses. Blood Adv. 2022;6(7):2247–2249. doi: 10.1182/bloodadvances.2021006599
   PubMed Web of Science ®Google Scholar
• Pettini E, Medaglini D, Ciabattini A. Profiling the B cell immune response elicited by vaccination against the respiratory virus SARS-CoV-2. Front Immunol [Internet]. 2022;13. [cited 2022 Nov 24]. Available from: https://www.frontiersin.org/articles/10.3389/fimmu.2022.1058748
   Web of Science ®Google Scholar
• Structures of the omicron spike trimer with ACE2 and an anti-omicron antibody. Science [Internet]. [cited 2023 Oct 23]. Available from: https://www.science.org/doi/10.1126/science.abn8863
   Google Scholar
• Goel RR, Painter MM, Lundgreen KA, et al. Efficient recall of omicron-reactive B cell memory after a third dose of SARS-CoV-2 mRNA vaccine. Cell. 2022;185(11):1875–1887.e8. doi: 10.1016/j.cell.2022.04.009
   PubMed Web of Science ®Google Scholar
• Wu M, Wall EC, Carr EJ, et al. Three-dose vaccination elicits neutralising antibodies against omicron. Lancet. 2022;399(10326):715–717. doi: 10.1016/S0140-6736(22)00092-7
   PubMed Web of Science ®Google Scholar
• Popowicz GM, Pyrc K, Hadian K. Vaccination versus SARS-CoV-2 omicron: three vaccine doses win the battle. Sig Transduct Target Ther. 2022;7(1):1–2. doi: 10.1038/s41392-022-01000-3
   PubMed Web of Science ®Google Scholar
• Garcia-Beltran WF, St Denis KJ, Hoelzemer A, et al. mRNA-based COVID-19 vaccine boosters induce neutralizing immunity against SARS-CoV-2 omicron variant. Cell. 2022;185(3):457–466.e4. doi: 10.1016/j.cell.2021.12.033
   PubMed Web of Science ®Google Scholar
• Psaridi L, Maltezou HC, Simonidou S, et al. Neutralizing antibody responses in healthcare personnel after three doses of mRNA BNT162b2 vaccine and association with baseline characteristics and past SARS-CoV-2 infection. Vaccine. 2022;40(40):5752–5756. doi: 10.1016/j.vaccine.2022.08.031
   PubMed Web of Science ®Google Scholar
• Sokal A, Broketa M, Barba-Spaeth G, et al. Analysis of mRNA vaccination-elicited RBD-specific memory B cells reveals strong but incomplete immune escape of the SARS-CoV-2 omicron variant. Immunity. 2022;55(6):1096–1104.e4. doi: 10.1016/j.immuni.2022.04.002
   PubMed Web of Science ®Google Scholar
• Yang L, Van Beek M, Wang Z, et al. Antigen presentation dynamics shape the antibody response to variants like SARS-CoV-2 omicron after multiple vaccinations with the original strain. Cell Rep. 2023;42(4):112256. doi: 10.1016/j.celrep.2023.112256
   PubMed Web of Science ®Google Scholar
• Moss P. The T cell immune response against SARS-CoV-2. Nat Immunol. 2022;23(2):186–193. doi: 10.1038/s41590-021-01122-w
   PubMed Web of Science ®Google Scholar
• Schmidt T, Klemis V, Schub D, et al. Immunogenicity and reactogenicity of heterologous ChAdOx1 nCoV-19/mRNA vaccination. Nat Med. 2021;27(9):1530–1535. doi: 10.1038/s41591-021-01464-w
   PubMed Web of Science ®Google Scholar
• Maringer Y, Nelde A, Schroeder SM, et al. Durable spike-specific T cell responses after different COVID-19 vaccination regimens are not further enhanced by booster vaccination. Sci Immunol. 2022;7(78):eadd3899. doi: 10.1126/sciimmunol.add3899
   PubMed Web of Science ®Google Scholar