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Plasma Neutralization of the SARS-CoV-2 Omicron Variant
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Abstract
BACKGROUND: The Omicron SARS-CoV-2 variant has spread internationally and is responsible for rapidly increasing case numbers. The emergence of divergent variants in the context of a heterogeneous and evolving neutralizing antibody response in host populations might compromise protection afforded by vaccines or prior infection. METHODS: We measured neutralizing antibody titers in 169 longitudinally collected plasma samples using pseudotypes bearing the Wuhan-hu-1 or the Omicron variant or a laboratory-designed neutralization-resistant SARS-CoV-2 spike (PMS20). Plasmas were obtained from convalescents who did or did not subsequently receive an mRNA vaccine, or naive individuals who received 3-doses of mRNA or 1-dose Ad26 vaccines. Samples were collected approximately 1, 5-6 and 12 months after initial vaccination or infection. RESULTS: Like PMS20, the Omicron spike protein was substantially resistant to neutralization compared to Wuhan-hu-1. In convalescent plasma the median deficit in neutralizing activity against PMS20 or Omicron was 30- to 60-fold. Plasmas from recipients of 2 mRNA vaccine doses were 30- to 180- fold less potent against PMS20 and Omicron than Wuhan-hu-1. Notably, previously infected or two-mRNA dose vaccinated individuals who received additional mRNA vaccine dose(s) had 38 to 154-fold and 35 to 214-fold increases in neutralizing activity against Omicron and PMS20 respectively. CONCLUSIONS: Omicron exhibits similar distribution of sequence changes and neutralization resistance as does a laboratory-designed neutralization-resistant spike protein, suggesting natural evolutionary pressure to evade the human antibody response. Currently available mRNA vaccine boosters, that may promote antibody affinity maturation, significantly ameliorate SARS-CoV-2 neutralizing antibody titers.
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“However, due to escape of the Omicron variant from current approved vaccines, the efficacy of all current vaccines is reduced and a new variant-specific analysis is therefore required [13][14][15] .”
From Safety and immunogenicity of a prefusion non-stabilized spike protein mRNA COVID-19 vaccine: a phase I trial (2022) · cites this paper as [14]
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Kase, Y., Sonn, I., Goto, M., Murakami, R., Sato, T., & Okano, H. (2023) · Experimental Neurology · doi:10.1016/j.expneurol.2023.114379 · Cited by 23
“…three pseudotyped lentiviruses were prepared based on the first SARS-CoV-2 strain reported in the world (original strain) (Wu et al., 2020), the so-called Delta variant (B.1.617.2 strain) (Cherian et al., 2021; Planas et al., 2021), and the Omicron variant (B.1.1.529 strain) (Schmidt et al., 2022).”
MethodInfluentialKörper, S., Grüner, B., Zickler, D., Wiesmann, T., Wuchter, P., Blasczyk, R., Zacharowski, K. D., Spieth, P. M., Tonn, T., Rosenberger, P., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci163657 · Cited by 20
“Therefore, for future CCP programs, priority should be given to superimmunized donors with very high antibody concentration due to previous SARS-CoV-2 infection and vaccination (54, 55, 57).”
COVID-19 Vaccine: Between Myth and Truth
Piccaluga, P. P., Guardo, A. D., Lagni, A., Lotti, V., Diani, E., Navari, M., & Gibellini, D. (2022) · Vaccines · doi:10.3390/vaccines10030349 · Cited by 22
Oh, D., Hölzer, M., Paraskevopoulou, S., Trofimova, M., Hartkopf, F., Budt, M., Wedde, M., Richard, H., Haldemann, B., Domaszewska, T., et al. (2022) · Clinical Infectious Diseases · doi:10.1093/cid/ciac399 · Cited by 23
Antibody evolution to SARS-CoV-2 after single-dose Ad26.COV2.S vaccine in humans
Cho, A., Muecksch, F., Wang, Z., Tanfous, T. B., DaSilva, J., Raspe, R., Johnson, B., Bednarski, E., Ramos, V., Schaefer-Babajew, D. J., et al. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20220732 · Cited by 22
“529) have been described before (9, 10, 43) and were generated by introduction of 100 substitutions using synthetic gene fragments (IDT) or overlap extension PCR mediated 101 mutagenesis and Gibson assembly.”
MethodSelf-citationKreuzberger, N., Hirsch, C., Andreas, M., Böhm, L., Bröckelmann, P. J., Cristanziano, V. D., Golinski, M., Hausinger, R. I., Mellinghoff, S. C., Lange, B., et al. (2022) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd015021 · Cited by 22
The importance of booster vaccination in the context of Omicron wave
Wei, Z., He, J., Wang, C., Bao, J., Leng, T., & Chen, F. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.977972 · Cited by 23
Pei, L., Chen, Y., Zheng, X., Gong, F., Liu, W., Lin, J., Zheng, R., Yang, Z., Bi, Y., & Chen, E. (2022) · Journal of Infection and Public Health · doi:10.1016/j.jiph.2022.12.003 · Cited by 22
“Reduced neutralization of the omicron variant has been reported in studies [20-22] using plasma specimens from”
BackgroundMethodRavussin, A., Robertson, A. H., Wolf, A., Blix, K., Kjønstad, I. F., Solum, G., Feiring, B., Strand, B. H., Lund‐Johansen, F., Munthe, L. A., et al. (2023) · The Lancet Healthy Longevity · doi:10.1016/s2666-7568(23)00055-7 · Cited by 22
Minka, S. O., & Minka, F. H. (2022) · Immunology Letters · doi:10.1016/j.imlet.2022.02.002 · Cited by 20
Álvarez-Díaz, D. A., Muñoz, A. L., Tavera-Rodríguez, P., Herrera-Sepúlveda, M. T., Ruiz-Moreno, H. A., Laiton‐Donato, K., Franco-Muñoz, C., Peláez‐Carvajal, D., Cuellar, D., Muñoz-Suarez, A. M., et al. (2022) · Vaccines · doi:10.3390/vaccines10020180 · Cited by 20
“, who reported lower neutralization titers against Mu relative to a parental D614G variant and Gamma [23], the magnitude of the difference was more noticeable in the present study.”
BackgroundResultMolecular variants of SARS-CoV-2: antigenic properties and current vaccine efficacy
Damavandi, A. R., Dowran, R., Sharif, S. A., Kashanchi, F., & Jafari, R. (2022) · Medical Microbiology and Immunology · doi:10.1007/s00430-022-00729-6 · Cited by 21
“Even though it largely escapes the immunity by two-dose vaccination with BNT162b2 [160, 161], multiple studies suggest that the booster dose could improve the protection against this variant [162, 163].”
BackgroundWang, Y.-D., Zhan, W., Liu, J., Wang, Y., Zhang, X., Zhang, M., Han, L., Ma, Y., Lu, L., Wen, Y., et al. (2022) · Cell Research · doi:10.1038/s41422-022-00684-0 · Cited by 19
Curlin, M. E., Bates, T. A., Guzman, G., Schoen, D., McBride, S. K., Carpenter, S. D., & Tafesse, F. (2022) · Med · doi:10.1016/j.medj.2022.09.001 · Cited by 21
Qu, P., Faraone, J. N., Evans, J. P., Zou, X., Zheng, Y.-M., Carlin, C., Bednash, J. S., Lozanski, G., Mallampalli, R. K., Saif, L. J., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.16.492158 · Cited by 21
“…the emergence of SARS-CoV-2 in the human population in 2019, the virus has evolved increased transmissibility (Abdool Karim and de Oliveira, 2021; Scobie et al., 2021; Singh et al., 2021; Washington et al., 2021; Yurkovetskiy et al., 2020) and resistance to vaccine- and infection-induced…”
BackgroundCOVID ‐19 mRNA vaccine‐related interstitial lung disease: Two case reports and literature review
So, C., Izumi, S., Ishida, A., Hirakawa, R., Kusaba, Y., Hashimoto, M., Ishii, S., Miyazaki, H., Iikura, M., & Hojo, M. (2022) · Respirology Case Reports · doi:10.1002/rcr2.938 · Cited by 18
Hewins, B., Rahman, M., Bermejo-Martín, J. F., Kelvin, A. A., Richardson, C. D., Rubino, S., Kumar, A., Ndishimye, P., Ostadgavahi, A. T., Mahmud-Al-Rafat, A., et al. (2022) · Frontiers in Virology · doi:10.3389/fviro.2022.849936 · Cited by 21
Tissue immunity to SARS‐CoV‐2: Role in protection and immunopathology*
Rybkina, K., Davis‐Porada, J., & Färber, D. L. (2022) · Immunological Reviews · doi:10.1111/imr.13112 · Cited by 19
Alam, M. S. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e13285 · Cited by 22
Memory B cell development elicited by mRNA booster vaccinations in the elderly
Wang, Z., Muecksch, F., Raspe, R., Johannsen, F., Turroja, M., Canis, M., ElTanbouly, M. A., Santos, G. S. S., Johnson, B., Baharani, V. A., et al. (2023) · The Journal of Experimental Medicine · doi:10.1084/jem.20230668 · Cited by 19
Self-citationMäkelä, A. R., Uğurlu, H., Hannula, L., Kant, R., Salminen, P., Fagerlund, R., Mäki, S., Haveri, A., Strandin, T. M., Kareinen, L., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37290-6 · Cited by 22
MultiSero: An Open-Source Multiplex-ELISA Platform for Measuring Antibody Responses to Infection
Byrum, J. R., Waltari, E., Janson, O., Guo, S.-M., Folkesson, J., Chhun, B. B., Vinden, J., Ivanov, I. E., Forst, M. L., Li, H., et al. (2023) · Pathogens · doi:10.3390/pathogens12050671 · Cited by 17
“While the study reported here measures early pandemic sera antibody titers to SARS-CoV-2 Wuhan-Hu-1 antigens, multiplexed serology using more recent sera will benefit from the inclusion of a panel of SARS-CoV-2 variant antigens, given that antibody responses can differ based on circulating variants and/or vaccine form…”
BackgroundCovid-19 vaccines, immunity, and boosters
Richterman, A. G., Scott, J. A., & Çevik, M. (2021) · BMJ · doi:10.1136/bmj.n3105 · Cited by 20
Deng, Y., Li, J., Sun, C., Chi, H., Luo, D., Wang, R., Qiu, H., Zhang, Y., Wu, M. L., Zhang, X., et al. (2022) · Advanced Materials · doi:10.1002/adma.202200443 · Cited by 19
Comparison of the immunogenicity of five COVID‐19 vaccines in Sri Lanka
Jeewandara, C., Aberathna, I. S., Danasekara, S., Gomes, L., Fernando, S., Guruge, D., Ranasinghe, T., Gunasekera, B., Kamaladasa, A., Kuruppu, H., et al. (2022) · Immunology · doi:10.1111/imm.13535 · Cited by 18
“A 41-fold decline in Nabs elicited by the Pfizer-BioNTech vaccine and 30- to 60-fold reduction of Nabs in convalescent plasma was observed for the omicron variant [10, 11].”
Thakur, N. (2022) · Data · doi:10.3390/data7080109 · Cited by 19
Humoral immunity and B-cell memory in response to SARS-CoV-2 infection and vaccination
Fryer, H. A., Hartley, G. E., Edwards, E. S. J., O’Hehir, R. E., & van Zelm, M. C. (2022) · Biochemical Society Transactions · doi:10.1042/bst20220415 · Cited by 16
Chang, M., Ke, H., Coherd, C. D., Wang, Y., Mashima, K., Kastrunes, G. M., Huang, C., & Marasco, W. A. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.104025 · Cited by 20
Zhu, D. Y., Gorman, M. J., Yuan, D., Yu, J., Mercado, N. B., McMahan, K., Borducchi, E. N., Lifton, M. A., Liu, J., Nampanya, F., et al. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001609 · Cited by 18
Tenforde, M. W., Self, W. H., Zhu, Y., Naioti, E. A., Gaglani, M., Ginde, A. A., Jensen, K., Talbot, H. K., Casey, J. D., Mohr, N. M., et al. (2022) · Clinical Infectious Diseases · doi:10.1093/cid/ciac381 · Cited by 21
“Recent increases in 21 SARS-CoV-2 incidence were caused almost exclusively by the Omicron variant and subvariants which 22 evade vaccine-associated immunity to a greater extent than prior circulating variants [21, 27].”
BackgroundSeidel, A., Zanoni, M., Groß, R. M., Krnavek, D., Erdemci-Evin, S., von Maltitz, P., Albers, D., Conzelmann, C., Liu, S., Weil, T., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.882918 · Cited by 17
Selvavinayagam, S. T., Yong, Y. K., Joseph, N. M. S., Hemashree, K., Tan, H. Y., Zhang, Y., Rajeshkumar, M., Kumaresan, A., Kalpana, R., Kalaivani, V., et al. (2022) · Frontiers in Public Health · doi:10.3389/fpubh.2022.1018399 · Cited by 17
The potential molecular implications of adiponectin in the evolution of SARS-CoV-2: Inbuilt tendency
Al-Kuraishy, H. M., Al-Gareeb, A. I., BUNGAU, S. G., Radu, A.-F., & Batiha, G. E. (2022) · Journal of King Saud University - Science · doi:10.1016/j.jksus.2022.102347 · Cited by 18
“COVID-19 leads to pulmonary and extrapulmonary manifestations with critical complications mainly in severely affected patient (Schmidt et al., 2021).”
BackgroundEmmelot, M. E., Vos, M. W., Boer, M. C., Rots, N. Y., van Els, C. A. C. M., & Kaaijk, P. (2022) · Viruses · doi:10.3390/v15010101 · Cited by 17
Pan-sarbecovirus prophylaxis with human anti-ACE2 monoclonal antibodies
Zhang, F., Jenkins, J., de Carvalho, R. A., Nakandakari-Higa, S., Chen, T., Abernathy, M. E., Baharani, V. A., Nyakatura, E. K., Andrew, D. P., Lebedeva, I. V., et al. (2023) · Nature Microbiology · doi:10.1038/s41564-023-01389-9 · Cited by 21
Self-citationImmune imprinting as a barrier to effective COVID-19 vaccines
Faraone, J. N., & Liu, S. (2023) · Cell Reports Medicine · doi:10.1016/j.xcrm.2023.101291 · Cited by 18
“4 Since then, the virus has evolved into numerous Omicron subvariants, including the most recent XBB variants.”
BackgroundModelling SARS-CoV-2 Binding Antibody Waning 8 Months after BNT162b2 Vaccination
Hatzakis, A. E., Karabinis, A., Roussos, S., Pantazis, N., Degiannis, D., Chaidaroglou, A. S., Petsios, K. T., Pavlopoulou, I. D., Tsiodras, S., Paraskevis, D. N., et al. (2022) · Vaccines · doi:10.3390/vaccines10020285 · Cited by 17
Can the SARS-CoV-2 Omicron Variant Confer Natural Immunity against COVID-19?
Abas, A. H., Marfuah, S., Idroes, R., Kusumawaty, D., Fatimawali, F., Park, M. N., Siyadatpanah, A., Alhumaydhi, F. A., Mahmud, S., Tallei, T. E., et al. (2022) · Molecules · doi:10.3390/molecules27072221 · Cited by 18
“A study found that 20 mutations in the poly-mutant spike protein (PMS20) are sufficient to prevent polyclonal neutralizing antibodies from individuals exposed to SARSCoV-2 or those who have received the vaccine twice [69].”
BackgroundInfluentialConserved Neutralizing Epitopes on the N-Terminal Domain of Variant SARS-CoV-2 Spike ProteinsPreprint
Wang, Z.-J., Muecksch, F., Cho, A., Gaebler, C., Hoffmann, H., Ramos, V. A., Zong, S., Cipolla, M., Johnson, B., Schmidt, F., et al. (2022) · bioRxiv · doi:10.1101/2022.02.01.478695 · Cited by 20
Self-citation
Metadata
- Authors
- Schmidt, F., Muecksch, F., Weisblum, Y., Da Silva, J., Bednarski, E., Cho, A., Wang, Z., Gaebler, C., Caskey, M., Nussenzweig, M. C., Hatziioannou, T., & Bieniasz, P. D.
- Affiliations
- Rockefeller University (US)
- Rockefeller University, New York, NY
- Corresponding author
- Bieniasz, Paul D.
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2022-02-10
- Volume
- 386
- Issue
- 6
- Pages
- 599-601
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- PMC
- PMC8687470
- OpenAlex
- W4205145778
- Cited by
- 432
- References
- 22
- Citations by year
- 2026: 9 · 2025: 16 · 2024: 24 · 2023: 68 · 2022: 307
- FWCI
- 32.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- medRxiv (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion, cc-by-nc-nd)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (2U19AI111825, P01-AI138398-S1, R01AI501111, R01AI78788, R37AI64003)
- National Center for Advancing Translational Sciences (UL1 TR001866)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Keywords
- Omicron variant, neutralizing antibodies, plasma neutralization, spike protein mutations, receptor binding domain, N-terminal domain, antibody escape, Wuhan-Hu-1, COVID-19 recovery, mRNA vaccines, neutralization titers
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