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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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Dufour, J., Marjot, T., Becchetti, C., & Tilg, H. (2022) · Gut · doi:10.1136/gutjnl-2021-326792 · Cited by 89
Protection of Omicron sub-lineage infection against reinfection with another Omicron sub-lineage
(2022) · doi:10.1038/s41467-022-32363-4 · Cited by 84
“Aliquots of UTM were: (1) extracted on KingFisher Flex (Thermo Fisher Scientific, USA), MGISP-960 (MGI, China), or ExiPrep 96 Lite (Bioneer, South Korea), followed by testing with RT-qPCR using TaqPath COVID-19 Combo Kits (Thermo Fisher Scientific, USA) on an ABI 7500 FAST (Thermo Fisher Scientific, USA); (2) tested d…”
MethodReinscheid, M., Luxenburger, H., Karl, V., Graeser, A., Giese, S., Ciminski, K., Reeg, D. B., Oberhardt, V., Roehlen, N., Lang‐Meli, J., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32324-x · Cited by 79
SARS-CoV-2 Omicron sublineages exhibit distinct antibody escape patterns
Gruell, H., Vanshylla, K., Korenkov, M., Tober‐Lau, P., Zehner, M., Münn, F., Janicki, H., Augustin, M., Schommers, P., Sander, L. E., et al. (2022) · Cell Host & Microbe · doi:10.1016/j.chom.2022.07.002 · Cited by 77
“Although prolonged vaccine dosing intervals and booster immunizations based on the ancestral Wu01 strain elicit Omicron-neutralizing serum activity, titers against Omicron are considerably lower compared with those against other variants (Garcia-Beltran et al., 2022; Gruell et al., 2022a; Pérez-Then et al., 2022; Schm…”
InfluentialAntibody modulation of B cell responses—Incorporating positive and negative feedback
Cyster, J. G., & Wilson, P. C. (2024) · Immunity · doi:10.1016/j.immuni.2024.06.009 · Cited by 78
Zhou, H., Møhlenberg, M., Thakor, J. C., Tuli, H. S., Wang, P., Assaraf, Y. G., Dhama, K., & Jiang, S. (2022) · Clinical Microbiology Reviews · doi:10.1128/cmr.00014-22 · Cited by 78
“Neutralizing titers against the Omicron variant were substantial in all persons who previously had COVID-19 disease and then were fully vaccinated, as well as those who had received three regimens of an mRNA vaccine (57).”
BackgroundEvolution of the SARS-CoV-2 Omicron spike
Parsons, R., & Acharya, P. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113444 · Cited by 79
“4,18 Several studies have noted decreased binding of antibodies from SARS-CoV-2-infected individuals to the Omicron S protein, 18–29 with neutralization titers of plasma specimens obtained from individuals infected with the Omicron variant up to ~50 times lower than for the wild-type (WT) S protein.”
BackgroundEpistasis lowers the genetic barrier to SARS-CoV-2 neutralizing antibody escape
Witte, L., Baharani, V. A., Schmidt, F., Wang, Z., Cho, A., Raspe, R., Guzmán-Cardozo, C., Muecksch, F., Canis, M., Park, D., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-35927-0 · Cited by 68
“Introduction Consecutive waves of SARS-CoV-2 infection have been driven in part by the repeated emergence of variants with mutations that confer resistance to neutralizing antibodies[1-8] Nevertheless, prolonged or repeated antigen exposure generates diverse memory B-cells [9-14] that can produce affinity matured rece…”
BackgroundInfluentialSelf-citationEstcourt, L. J., Cohn, C. S., Pagano, M. B., Iannizzi, C., Kreuzberger, N., Skoetz, N., Allen, E. S., Bloch, E. M., Beaudoin, G., Casadevall, A., et al. (2022) · Annals of Internal Medicine · doi:10.7326/m22-1079 · Cited by 70
Brüssow, H. (2022) · Microbial Biotechnology · doi:10.1111/1751-7915.14064 · Cited by 70
“Mutations were located in the N-terminal part of the spike protein as well as in the furin cleavage site explaining the decreased syncytium formation by the mutated virus (Shiliaev et al., 2021).”
BackgroundCOVID-19 vaccination in pregnancy
Kalafat, E., Heath, P. T., Prasad, S., O’Brien, P., & Khalil, A. A. (2022) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2022.05.020 · Cited by 70
“Booster shots seem to be the most effective option for protection against infection with the Omicron variant, which has substantial immune escape from humoral immunity elicited by mRNA vaccines.(70)”
Wang, Z., Zhou, P., Muecksch, F., Cho, A., Tanfous, T. B., Canis, M., Witte, L., Johnson, B., Raspe, R., Schmidt, F., et al. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20221006 · Cited by 61
“WT and Omicron BA.1 NT50 values are derived from two previous reports (Gaebler et al., 2022; Schmidt et al., 2022).”
MethodSelf-citationMao, T., Israelow, B., Suberi, A., Zhou, L., Reschke, M., Peña-Hernández, M. A., Dong, H., Homer, R. J., Saltzman, W., & Iwasaki, A. (2022) · bioRxiv · doi:10.1101/2022.01.24.477597 · Cited by 57
“These data suggest that either IN unadjuvanted spike or mRNA-PACE encoding spike sufficiently boost mucosal immunity to protect from COVID-19 like pulmonary disease and mortality in a preclinical mouse model.”
InfluentialSARS-CoV-2 variants – Evolution, spike protein, and vaccines
Chen, K.-W. K., Huang, D. T., & Huang, L. (2022) · Biomedical Journal · doi:10.1016/j.bj.2022.04.006 · Cited by 63
“and then vaccinated [69,72] and individuals vaccinated with boosters (third dose with mRNA vaccines) [61,70e72] showed detectable neutralizing antibodies against BA.”
College openings in the United States increase mobility and COVID-19 incidence
Andersen, M. S., Bento, A. I., Basu, A., Marsicano, C. R., & Simon, K. I. (2022) · PLoS ONE · doi:10.1371/journal.pone.0272820 · Cited by 61
Babalghith, A. O., Al-Kuraishy, H. M., Al-Gareeb, A. I., WAARD, M. M. D., Sabatier, J., Saad, . M., & Batiha, G. E. (2022) · Diagnostics · doi:10.3390/diagnostics12092051 · Cited by 62
“The last SARS-CoV-2 variant was Omicron, which was declared by the World Health Organization (WHO) on 26 November 2021 and spread to more than 136 countries [3,4].”
BackgroundSARS‐CoV‐2 and its variants of concern including Omicron: A never ending pandemic
Mohapatra, R. K., Kuppili, S., Suvvari, T. K., Kandi, V., Behera, A., Verma, S., Kudrat‐E‐Zahan, Biswal, S. K., AL-Noor, T. H., El‐ajaily, M. M., et al. (2022) · Chemical Biology & Drug Design · doi:10.1111/cbdd.14035 · Cited by 59
“Six months after complete vaccination, a booster dose with mRNA vaccineinduced Omicron neutralizing antibodies (Schmidt et al., 2021).”
BackgroundSkarbinski, J., Wood, M. S., Chervo, T. C., Schapiro, J. M., Elkin, E. P., Valice, E., Amsden, L. B., Hsiao, C. A., Quesenberry, C. P., Corley, D. A., et al. (2022) · The Lancet Regional Health - Americas · doi:10.1016/j.lana.2022.100297 · Cited by 60
Durability of Heterologous and Homologous COVID-19 Vaccine Boosts
Tan, C. S., Collier, A.-R. Y., Yu, J., Liu, J., Chandrashekar, A., McMahan, K., Jacob-Dolan, C., He, X., Roy, V., Hauser, B. M., et al. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.26335 · Cited by 57
Recent insights into SARS‐CoV‐2 omicron variant
da Silva, S. J. R., Kohl, A., Pena, L., & Pardee, K. (2022) · Reviews in Medical Virology · doi:10.1002/rmv.2373 · Cited by 56
“studies from different parts of the world using selected samples (sera/plasma).(18,80,81)”
BackgroundSARS-CoV-2 Omicron variant emerged under immune selection
Tan, C. W., Chia, W. N., Zhu, F., Young, B. E., Chantasrisawad, N., Hwa, S.-H., Yeoh, A. Y.-Y., Lim, B. L., Yap, W. C., Pada, S., et al. (2022) · Nature Microbiology · doi:10.1038/s41564-022-01246-1 · Cited by 55
Medigeshi, G. R., Batra, G., Murugesan, D. R., Thiruvengadam, R., Chattopadhyay, S., Das, B., Gosain, M., Ayushi, A., Singh, J., Anantharaj, A., et al. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.103938 · Cited by 51
Jurdi, A. A., Gassen, R. B., Borges, T. J., Lape, I. T., Morená, L., Efe, O., Solhjou, Z., Fekih, R. E., Deban, C. A., Bohan, B., et al. (2022) · Kidney International · doi:10.1016/j.kint.2022.04.009 · Cited by 53
Lapointe, H. R., Mwimanzi, F. M., Cheung, P. K., Sang, Y., Yaseen, F., Umviligihozo, G., Kalikawe, R., Speckmaier, S., Moran-Garcia, N., Datwani, S., et al. (2022) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiac229 · Cited by 54
Challenges of the Omicron (B.1.1.529) Variant and Its Lineages: A Global Perspective
Mohapatra, R. K., Kandi, V., Verma, S., & Dhama, K. (2022) · ChemBioChem · doi:10.1002/cbic.202200059 · Cited by 51
Arunachalam, P. S., Feng, Y., Ashraf, U., Hu, M., Walls, A. C., Edara, V. V., Zarnitsyna, V. I., Aye, P. P., Golden, N., Miranda, M. C., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abq4130 · Cited by 53
Immune Escape Associated with RBD Omicron Mutations and SARS-CoV-2 Evolution Dynamics
Kudriavtsev, A. V., Vakhrusheva, A., Novoseletsky, V. N., Bozdaganyan, M. E., Шайтан, К. В., Kirpichnikov, M. P., & Sokolova, O. S. (2022) · Viruses · doi:10.3390/v14081603 · Cited by 52
“Thus, booster immunization by vaccines significantly increases the neutralization level titer against Omicron [53,54,55,87,88,89,90,91,92,93].”
BackgroundResultStructural Plasticity and Immune Evasion of SARS-CoV-2 Spike Variants
Ghimire, D., Han, Y., & Lu, M. (2022) · Viruses · doi:10.3390/v14061255 · Cited by 44
Resistance of SARS-CoV-2 Omicron variant to convalescent and CoronaVac vaccine plasma
Wang, Y.-D., Ma, Y., Xu, Y., Liu, J., Li, X., Chen, Y., Chen, Y., Xie, J., Xiao, L., Xiang, Z., et al. (2022) · Emerging Microbes & Infections · doi:10.1080/22221751.2022.2027219 · Cited by 50
Benning, L., Morath, C. P., Bartenschlager, M., Kim, H., Reineke, M., Beimler, J., Buylaert, M., Nußhag, C., Kälble, F., Reichel, P., et al. (2022) · American Journal of Transplantation · doi:10.1111/ajt.17054 · Cited by 51
Arora, P., Zhang, L., Krüger, N., Rocha, C., Sidarovich, A., Schulz, S. R., Kempf, A. M., Graichen, L., Moldenhauer, A.-S., Cossmann, A., et al. (2022) · Cell Host & Microbe · doi:10.1016/j.chom.2022.04.017 · Cited by 45
“…and these allow for higher evasion from neutralizing antibodies than other variants of concern (VOCs) (Carreno et al., 2022; Dejnirattisai et al., 2022; Garcia-Beltran et al., 2022; Hoffmann et al., 2022; Rossler et al., 2022; Schmidt et al., 2022; VanBlargan et al., 2022; Zhang et al., 2022).”
InfluentialThe Robustness of Cellular Immunity Determines the Fate of SARS-CoV-2 Infection
Moga, E., Lynton‐Pons, E., & Domingo, P. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.904686 · Cited by 48
Moore, S. C., Kronsteiner, B., Longet, S., Adele, S., Deeks, A. S., Liu, C., Dejnirattisai, W., Silva-Reyes, L., Meardon, N., Faustini, S. E., et al. (2023) · Med · doi:10.1016/j.medj.2023.02.004 · Cited by 56
Chatterjee, D., Tauzin, A., Marchitto, L., Gong, S. Y., Boutin, M., Bourassa, C., Beaudoin-Bussières, G., Bo, Y., Ding, S., Laumaea, A., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110429 · Cited by 46
Thakur, N., & Han, C. Y. (2022) · COVID · doi:10.3390/covid2080076 · Cited by 50
Gagné, M., Moliva, J. I., Foulds, K. E., Andrew, S. F., Flynn, B. J., Werner, A. P., Wagner, D. A., Teng, I., Lin, B. C., Moore, C. A., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.03.479037 · Cited by 47
“…reduction for convalescent sera and a 20- to 130-fold reduction for vaccinee sera (Edara et al., 2021a; Hoffmann et al., 2021; Muik et al., 2022; Schmidt et al., 2021). mRNA-1273 vaccine efficacy against breakthrough cases of Omicron in the first few months after immunization has been estimated…”
BackgroundFurukawa, K., Tjan, L. H., Kurahashi, Y., Sutandhio, S., Nishimura, M., Arii, J., & Mori, Y. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.10780 · Cited by 47
Antibody Titers and Protection against Omicron (BA.1 and BA.2) SARS-CoV-2 Infection
Dimeglio, C., Migueres, M., Bouzid, N., Chapuy‐Regaud, S., Gernigon, C., Da-Silva, I., Porcheron, M., Martin‐Blondel, G., Hérin, F., & Izopet, J. (2022) · Vaccines · doi:10.3390/vaccines10091548 · Cited by 45
Liang, Q., Huang, Y., Wang, M., Kuang, D., Yang, J., Yi, Y., Shi, H., Li, J., Yang, J. A., & Li, G. (2022) · Chemical Engineering Journal · doi:10.1016/j.cej.2022.139646 · Cited by 46
Yang, L., Beek, M. V., Wang, Z., Muecksch, F., Canis, M., Hatziioannou, T., Bieniasz, P. D., Nussenzweig, M. C., & Chakraborty, A. K. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112256 · Cited by 50
“In addition, better Omicron responses are consistently observed after the third dose in a diverse group of individuals.(10) We hope that our results and mechanistic insights will motivate other fundamental studies into how the humoral immune response is influenced by antigen presentation dynamics.”
Self-citationDynamics of a national Omicron SARS-CoV-2 epidemic during January 2022 in England
Elliott, P., Eales, O. D., Bodinier, B., Tang, D. G., Wang, H., Jonnerby, J., Haw, D., Elliott, J., Whitaker, M. D., Walters, C. E., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32121-6 · Cited by 46
Mazzoni, A., Vanni, A., Spinicci, M., Capone, M., Lamacchia, G., Salvati, L., Coppi, M., Antonelli, A., Carnasciali, A., Farahvachi, P., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.801431 · Cited by 44
“Recent evidences are now demonstrating that the antibody neutralization capacity is significantly reduced against Omicron both in previously SARSCoV-2 infected and vaccinated subjects (8), although a third, booster, vaccine administration seems to partially restore the neutralizing capability (9).”
BackgroundAriën, K. K., Heyndríckx, L., Míchiels, J., Vereecken, K., Lent, K. V., Coppens, S., Willems, B., Pannus, P., Martens, G. A., Esbroeck, M. V., et al. (2022) · npj Vaccines · doi:10.1038/s41541-022-00459-z · Cited by 44
Broad-spectrum pan-genus and pan-family virus vaccines
Tan, C. W., Valkenburg, S., Poon, L. L. M., & Wang, L. (2023) · Cell Host & Microbe · doi:10.1016/j.chom.2023.05.017 · Cited by 42
“1 are the most potent in escaping nAbs directed against the ancestral Wuhan strain,(97) and these variants most likely emerged under immune selective pressure.(93,110) After breakthrough infection, there is a significant increase in overall nAb titers and induce mucosal immunity against SARS-CoV-2.”
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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