Cited by 113SARS-CoV-2 and COVID-19 ResearchAnimal Virus Infections StudiesCOVID-19 Clinical Research Studies

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Neutralizing Antibodies Against Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Variants Induced by Natural Infection or Vaccination: A Systematic Review and Pooled Analysis

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Chen, Xinhua, Chen, Zhiyuan, Azman, Andrew S, Sun, Ruijia, Lu, Wanying, Zheng, Nan, Zhou, Jiaxin, Wu, Qianhui, Deng, Xiaowei, Zhao, Zeyao, Chen, Xinghui, Ge, Shijia, Yang, Juan, Leung, Daniel T, Yu, Hongjie·2022·Clinical Infectious Diseases

DOI 10.1093/cid/ciab646PMC PMC9016754

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Abstract

Recently emerged severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants may pose a threat to immunity. A systematic landscape of neutralizing antibodies against emerging variants is needed. We systematically searched for studies that evaluated neutralizing antibody titers induced by previous infection or vaccination against SARS-CoV-2 variants and collected individual data. We identified 106 studies meeting the eligibility criteria. Lineage B.1.351 (beta), P.1 (gamma) and B.1.617.2 (delta) significantly escaped natural infection–mediated neutralization, with an average of 4.1-fold (95% confidence interval [CI]: 3.6–4.7-fold), 1.8-fold (1.4–2.4-fold), and 3.2-fold (2.4–4.1-fold) reduction in live virus neutralization assay, while neutralizing titers against B.1.1.7 (alpha) decreased slightly (1.4-fold [95% CI: 1.2–1.6-fold]). Serum from vaccinees also led to significant reductions in neutralization of B.1.351 across different platforms, with an average of 7.1-fold (95% CI: 5.5–9.0-fold) for nonreplicating vector platform, 4.1-fold (3.7–4.4-fold) for messenger RNA platform, and 2.5-fold (1.7–2.9-fold) for protein subunit platform. Neutralizing antibody levels induced by messenger RNA vaccines against SARS-CoV-2 variants were similar to, or higher, than that derived from naturally infected individuals.

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Background
Broad neutralization against SARS-CoV-2 variants induced by ancestral and B.1.351 AS03-Adjuvanted recombinant Plant-Derived Virus-Like particle vaccines
Dubé, C., Paris‐Robidas, S., Andreani, G., Gutzeit, C., D’Aoust, M., Ward, B. J., & Trépanier, S. (2022) · Vaccine · doi:10.1016/j.vaccine.2022.05.046 · Cited by 11
VSV-Based Vaccines Reduce Virus Shedding and Viral Load in Hamsters Infected with SARS-CoV-2 Variants of Concern
O’Donnell, K. L., Gourdine, T., Fletcher, P., Shifflett, K., Furuyama, W., Clancy, C. S., & Marzi, A. (2022) · Vaccines · doi:10.3390/vaccines10030435 · Cited by 8
Protective action of natural and induced immunization against the occurrence of delta or alpha variants of SARS-CoV-2 infection: a test-negative case-control study
Corrao, G., Franchi, M., Rea, F., Cereda, D., Barone, A. A., Borriello, C. R., Valle, P. G. D., Ercolanoni, M., Fortino, I., Jara, J., et al. (2022) · BMC Medicine · doi:10.1186/s12916-022-02262-y · Cited by 10
“Levels of neutralising antibodies induced by m-RNA vaccines against SARS-CoV-2 variants have been found to be similar (or higher) than those derived from naturally infected individuals [9].”
Background
Adjuvant-Free COVID-19 Vaccine with Glycoprotein Antigen Oxidized by Periodate Rapidly Elicits Potent Immune Responses
Zhang, R., Zhou, S., Feng, R.-R., Wen, Y., Ding, D., Zhang, Z.-M., Wei, H., & Guo, J. (2023) · ACS Chemical Biology · doi:10.1021/acschembio.3c00050 · Cited by 9
T-Cell Assay after COVID-19 Vaccination Could Be a Useful Tool? A Pilot Study on Interferon-Gamma Release Assay in Healthcare Workers
Seraceni, S., Zocca, E., Cervone, T. E., Tomassetti, F., Polidori, I., Valisi, M., Broccolo, F., Calugi, G., Bernardini, S., & Pieri, M. (2022) · Diseases · doi:10.3390/diseases10030049 · Cited by 9
“However, limited research has been conducted on the T-cell immune response, particularly after vaccination [8,9].”
Background
Kinetics of the Antibody Response to Symptomatic SARS-CoV-2 Infection in Vaccinated and Unvaccinated Individuals in the Blinded Phase of the mRNA-1273 COVID-19 Vaccine Efficacy Trial
Follmann, D. A., Janes, H., Chu, E., Jayashankar, L., Petropoulos, C. J., Serebryannyy, L., Carroll, R., Jean‐Baptiste, N., Narpala, S., Lin, B. C., et al. (2023) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofad069 · Cited by 12
Kinetics of Humoral Immunity against SARS-CoV-2 in Healthcare Workers after the Third Dose of BNT162b2 mRNA Vaccine
Grassi, T., Lobreglio, G., Panìco, A., Rosato, C., Zizza, A., Lazzari, R., Chicone, M., Indino, F., & Bagordo, F. (2022) · Vaccines · doi:10.3390/vaccines10111948 · Cited by 10
“Compared to antibody concentration induced by natural infection, vaccination may induce similar or lower neutralizing antibody levels [10] that decay faster [11].”
Characterization of the antispike IgG immune response to COVID-19 vaccines in people with a wide variety of immunodeficiencies
Zendt, M., Carrillo, F. A. B., Kelly, S., Saturday, T. A., DeGrange, M., Ginigeme, A., Wu, L., Callier, V., Ortega‐Villa, A. M., Faust, M. T., et al. (2023) · Science Advances · doi:10.1126/sciadv.adh3150 · Cited by 11
Persistence at one year of neutralizing antibodies after SARS-CoV-2 infection: Influence of initial severity and steroid use
Épaulard, O., Buisson, M., Némoz, B., Maréchal, M. L., Terzi, N., Payen, J., Froidure, M., Blanc, M., Mounayar, A.-L., Quénard, F., et al. (2021) · Journal of Infection · doi:10.1016/j.jinf.2021.10.009 · Cited by 11
Nano/Micro-Enabled Modification and Innovation of Conventional Adjuvants for Next-Generation Vaccines
Liu, X., Xu, Y., Tao, L., Li, X., Chen, G., & Liu, Q. (2025) · Journal of Functional Biomaterials · doi:10.3390/jfb16050185 · Cited by 8
“The emergence of SARS-CoV-2 variants, for example, has diminished the efficacy of COVID-19 vaccines [5,6].”
Neutralizing Antibodies Response against SARS-CoV-2 Variants of Concern Elicited by Prior Infection or mRNA BNT162b2 Vaccination
Bonura, F., Genovese, D., Amodio, E., Calamusa, G., Sanfilippo, G. L., Cacioppo, F., Giammanco, A., Grazia, S. D., & Ferraro, D. (2022) · Vaccines · doi:10.3390/vaccines10060874 · Cited by 8
Utility of in silico-identified-peptides in spike-S1 domain and nucleocapsid of SARS-CoV-2 for antibody detection in COVID-19 patients and antibody production
Cortés-Sarabia, K., Luna-Pineda, V., Rodríguez-Ruíz, H., Leyva-Vázquez, M., Hernández-Sotelo, D., Beltrán-Anaya, F., Vences-Velázquez, A., del Moral-Hernández, O., & Illades-Aguiar, B. (2022) · Scientific Reports · doi:10.1038/s41598-022-18517-w · Cited by 5
Coronavirus Resistance Database (CoV-RDB): SARS-CoV-2 susceptibility to monoclonal antibodies, convalescent plasma, and plasma from vaccinated personsPreprint
Tzou, P. L., Tao, K., Pond, S. L. K., & Shafer, R. W. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.24.469823 · Cited by 8
SARS-CoV-2 cellular coinfection is limited by superinfection exclusion
Sims, A., Weir, D. J., Cole, S. J., & Hutchinson, E. C. (2025) · Journal of Virology · doi:10.1128/jvi.02077-24 · Cited by 7
An Analysis of the Neutralizing Antibodies against the Main SARS-CoV-2 Variants in Healthcare Workers (HCWs) Vaccinated against or Infected by SARS-CoV-2
Immordino, P., Pisciotta, V., Amodio, E., Bonura, C., Bonura, F., Cacioppo, F., Calamusa, G., Capra, G., Casuccio, A., Grazia, S. D., et al. (2023) · Vaccines · doi:10.3390/vaccines11111702 · Cited by 7
“…since the beginning of the a target of turn, 20]. we SARS-CoV-2 strain, whose spike protein mRNA was included in the vaccine from in have escape the 36]. neutralizing potency when Alpha was not which the nVP population was infected [38], but the lack of protection from subsequent VOCs somewhat…”
Background
Kinetics of severe acute respiratory syndrome coronavirus 2 infection antibody responses
Lin, Y., Zhu, J., Liu, Z., Li, C., Guo, Y., Wang, Y., & Chen, K. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.864278 · Cited by 7
Prediction of vaccine efficacy of the Delta variantPreprint
Chen, X., Azman, A. S., Lu, W., Sun, R., Zheng, N., Ge, S., Deng, X., Yang, J., Leung, D. T., & Yu, H. (2021) · medRxiv · doi:10.1101/2021.08.26.21262699 · Cited by 7
Self-citation
SARS-CoV-2 Neutralizing Antibodies in Chile after a Vaccination Campaign with Five Different Schemes
Aguilera, X., Hormazábal, J., Vial, C., Cortés, J., González, C., Rubilar, P. A., Apablaza, M., Ramírez-Santana, M., Icaza, G., Núñez, L., et al. (2022) · Vaccines · doi:10.3390/vaccines10071051 · Cited by 6
Nature of Acquired Immune Responses, Epitope Specificity and Resultant Protection from SARS-CoV-2
Gorczynski, R. M., Lindley, R. A., Steele, E. J., & Wickramasinghe, N. C. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11121253 · Cited by 7
SARS-CoV-2 Virus-Like Particle Neutralizing Capacity in Blood Donors Depends on Serological Profile and Donor-Declared SARS-CoV-2 Vaccination History
Drews, S. J., Hu, Q., Samson, R., Abe, K. T., Rathod, B., Colwill, K., Gingras, A., Yi, Q., & O’Brien, S. F. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.02262-21 · Cited by 7
IgG4 Neutralization and Sustained Total IgG Fc-Effector Functions Following Repeated SARS-CoV-2 Vaccination with mRNA-1273
Kapłonek, P., Bertera, H. L., Lee, D. W., Cizmeci, D., Yu, W., Wu, K., Chalkias, S., Wahid, R., Edwards, D., Alter, G., et al. (2026) · Infectious Diseases and Therapy · doi:10.1007/s40121-026-01303-w · Cited by 4
Determining the Time of Booster Dose Based on the Half-Life and Neutralization Titers against SARS-CoV-2 Variants of Concern in Fully Vaccinated Individuals
Dai, Y.-C., Lin, Y.-C., Ching, L. L., Tsai, J., Ishikawa, K. M., Tsai, W.-Y., Chen, J. J., Nerurkar, V. R., & Wang, W. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.04081-22 · Cited by 4
Comparison of the immunogenicity of nasal‐spray rVSV vector, adenovirus vector, and inactivated COVID‐19‐based vaccines in rodent models
Zhang, Y., Liu, J., Li, H., Yuan, F., Jiang, C., Cang, T., Li, K., Hu, Q., Liu, J., & Zheng, A. (2023) · Journal of Medical Virology · doi:10.1002/jmv.28806 · Cited by 4
“ranges from 50 to 100.(27) All rVSV‐immunized groups, regardless of whether they received a low (2 × 10(5) FFU) or high (2 × 10(6) FFU) dose, demonstrated significantly higher IC50 titers than the groups that received two‐doses of KCONVAC or Vaxzevria; potent and broad neutralization activities against authentic SARS‐…”
Background
Unravelling humoral immunity in SARS-CoV-2: Insights from infection and vaccination
Najimi, N., Kadi, C., Elmtili, N., Seghrouchni, F., & Bakri, Y. (2024) · Human Antibodies · doi:10.3233/hab-230017 · Cited by 4
“The neutralization of Beta was similarly reduced in an analysis employing serum from vaccine recipients, with an average reduction of 7.1-fold for a non-replicating vector platform and 4.1-fold for an mRNA platform [42].”
Influential
Which test results to believe? Comparison of different ELISA kits for detection of SARS-CoV-2-neutralizing antibody among COVID-vaccinated individuals
Yanamandra, U., Tandel, K., Rayapureddi, K., Singh, S. P., Arivalagan, B., Kalra, D. K., Sahu, R., Menon, A. S., & Kotwal, N. (2024) · Medical Journal Armed Forces India · doi:10.1016/j.mjafi.2024.05.014 · Cited by 3
An Orally Available Cathepsin L Inhibitor Protects Lungs Against SARS-CoV-2-Induced Diffuse Alveolar Damage in African Green MonkeysPreprint
Frueh, F., Maneval, D., Bohm, R., Dufour, J. P., Blair, R., Powell, K., Aye, P., Golden, N. A., Roy, C., Spencer, S., et al. (2021) · bioRxiv · doi:10.1101/2021.07.20.453127 · Cited by 3
Letter to the editor: Vitamin D deficiency in critically ill COVID-19 ARDS patients
dos Santos, M. E. R. A., Barros, W. M. A., Fernandes, M. S. D. S., da Silva, A. B. J., & Souza, V. O. N. (2022) · Clinical Nutrition · doi:10.1016/j.clnu.2022.01.003 · Cited by 3
Reverse vaccinology-based multi-epitope COVID-19 vaccine targeting SARS-CoV-2 structural and non-structural proteins induces immune responses in mice
Fibriani, A., Yamahoki, N., Shani, A. M., Rofiqoh, A., Siregar, A. L. F., Gunawan, C., Mayorga, C. G. D., Tjia, T. O. S., Nugrahapraja, H., Giri-Rachman, E. A., et al. (2025) · Vaccine X · doi:10.1016/j.jvacx.2025.100632 · Cited by 2
Enhanced immunity against SARS-CoV-2 in returning Chinese individuals
Yuan, R., Chen, H., Yi, L., Li, X., Hu, X., Li, X., Zhang, H., Zhou, P., Liang, C., Lin, H., et al. (2024) · Human Vaccines & Immunotherapeutics · doi:10.1080/21645515.2023.2300208 · Cited by 4
Omicron neutralization character in patients with breast cancer and liver cancer after the nationwide omicron outbreak
Zhang, S., Tang, L., Bao, C., Wang, S., Li, B., Huang, L., Song, H., Fu, J., Xu, Z., Meng, F., et al. (2024) · Cancer Medicine · doi:10.1002/cam4.7304 · Cited by 1
An efficient strategy for producing RNA ‐free Nucleocapsid protein of SARS ‐ CoV ‐2 for biochemical and structural investigations
Singh, S., & Gupta, G. D. (2025) · FEBS Open Bio · doi:10.1002/2211-5463.70064 · Cited by 2
Outcome Heterogeneity in Coronavirus Disease 2019 (COVID-19) Patients Receiving Tocilizumab
Niu, M. M., Cao, Y., Li, R., Fan, G. Z., & Hu, P. (2021) · Clinical Infectious Diseases · doi:10.1093/cid/ciab816 · Cited by 2
Comparable Post-Vaccination Decay of Neutralizing Antibody Response to Wild-Type and Delta SARS-CoV-2 Variant in Healthcare Workers Recovered from Mild or Asymptomatic Infection
Vicenti, I., Basso, M., Dragoni, F., Gatti, F., Scaggiante, R., Fiaschi, L., Parisi, S. G., & Zazzi, M. (2022) · Vaccines · doi:10.3390/vaccines10040580 · Cited by 2
“as L452R, P681R, and T478K, a substantial fold reduction in the neutralizing antibodies elicited by vaccination or infection compared to that for reference lineages was previously reported [19].”
Result
SARS-CoV-2 humoral immune response in patients with cardiovascular risk factors: The COmmunity Cohort Study
Bachelet, V. C., Silva-Ayarza, I., & Navarrete, M. S. (2023) · Medwave · doi:10.5867/medwave.2023.11.2787 · Cited by 2
Landscape of SARS-CoV-2 genomic surveillance, public availability extent of genomic data, and epidemic shaped by variants: a global descriptive studyPreprint
Chen, Z., Azman, A. S., Chen, X., Zou, J., Tian, Y., Sun, R., Xu, X., Wu, Y., Lu, W., Ge, S., et al. (2021) · medRxiv · doi:10.1101/2021.09.06.21263152 · Cited by 2
Self-citation
Covid-19 : Natural immunity versus vaccine immunityPreprint
Banoun, H. (2021) · doi:10.32388/dp264j · Cited by 1
Immune response to COVID-19 vaccines in people with immunodeficienciesPreprint
Ricotta, E., Zendt, M., Castillo, F. B., Kelly, S., Saturday, T. A., DeGrange, M., Ginigeme, A., Wu, L., Callier, V., Ortega‐Villa, A. M., et al. (2023) · Research Square · doi:10.21203/rs.3.rs-2514984/v1 · Cited by 2
Epitopes mapped onto SARS-CoV-2 receptor-binding motif by five distinct human neutralising antibodies
Gutiérrez, L. J., Tosso, R. D., Zarycz, M. N. C., Enriz, R. D., & Baldoni, H. A. (2022) · Molecular Simulation · doi:10.1080/08927022.2022.2111421 · Cited by 1
Effective Neutralizing Antibody Response Against SARS-CoV-2 Virus and Its Omicron BA.1 Variant in Fully Vaccinated Hematological Patients
Novellis, D. D., Folliero, V., Giudice, V., Pezzullo, L., Sanna, G., Fontana, R., Guariglia, R., Zannella, C., Mettivier, L., Ferrara, I., et al. (2023) · Clinical and Experimental Medicine · doi:10.1007/s10238-023-01223-w · Cited by 1
“%) in hospitalized COVID-19 patients with severe disease to 71.9%, with high inter-trial variability [31–36].”
BackgroundInfluential
Immunogenicity Assessment of the SARS-CoV-2 Protein Subunit Recombinant Vaccine (CoV2-IB 0322) in a Substudy of a Phase 3 Trial in Indonesia
Shakinah, S., Aini, M. H., Sekartini, R., Soedjatmiko, S., Medise, B. E., Gunardi, H., Yuniar, I., Indawati, W., Koesnoe, S., Harimurti, K., et al. (2024) · Vaccines · doi:10.3390/vaccines12040371 · Cited by 1
“Severely ill patients show higher levels of neutralizing antibody titers compared to mild cases [16–18].”
Background
Genomic and epidemiological analysis of SARS-CoV-2 variants isolated in Guinea: a routine sequencing implementation
Mbaye, A., Diallo, H., Gnimadi, T. A. C., Kadio, K. J. J. O., Soumah, A. K., Koivogui, J., Monemou, J. L., Povogui, M. K., Kaba, D., Hounmenou, C. G., et al. (2025) · BMC Infectious Diseases · doi:10.1186/s12879-024-10411-2 · Cited by 1
Anti-coronavirus vaccines will not accelerate the transition of humanity to a non-pandemic period, but the pandemic will take fewer victims
Oberemok, V. V., Andreeva, O. A., Laikova, K. V., Novikov, I. A., Puzanova, Y. V., & Kubyshkin, A. V. (2022) · Inflammation Research · doi:10.1007/s00011-022-01567-1 · Cited by 1
Evaluation of a novel fully automated and ELISA- based assays for detecting anti- SARS- CoV-2 neutralizing antibodiesPreprint
Zedan, H. T., Yassine, H. M., Al‐Sadeq, D. W., Liu, N., Qotba, H. A., Nicolai, E., Pieri, M., Bernardini, S., Abu-Raddad, L. J., & Nasrallah, G. K. (2022) · Research Square · doi:10.21203/rs.3.rs-1718587/v1 · Cited by 1
Genomic evolution of SARS-CoV-2 variants of concern under in vitro neutralising selection pressure following two doses of the Pfizer-BioNTech BNT162b2 COVID-19 vaccinePreprint
Basile, K., Agius, J. E., Fong, W., McPhie, K. A., Fennel, M., Ko, D., Heuston, L., Lam, C., Arnott, A., Chen, S. C. ‐., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.24.558921 · Cited by 1
Status of Humoral and Cellular Immune Responses within 12 Months Following CoronaVac Vaccination Against COVID-19Preprint
Zhao, W., Chen, W., Li, J., Cheng, M., Li, Q., Lv, M., Zhou, S., Bai, S., Wang, Y., Zhang, L., et al. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3945456

Authors: Chen, X., Chen, Z., Azman, A. S., Sun, R., Lu, W., Zheng, N., Zhou, J., Wu, Q., Deng, X., Zhao, Z., Chen, X., Ge, S., Yang, J., Leung, D. T., & Yu, H.
Affiliations: Fudan University (CN)
University of Geneva (CH)
University of Utah (US)
Corresponding author: Yu, Hongjie
ORCID: Chen, Xinhua
Chen, Zhiyuan
Azman, Andrew S
Sun, Ruijia
Zheng, Nan
Zhou, Jiaxin
Deng, Xiaowei
Zhao, Zeyao
Chen, Xinghui
Yang, Juan
Leung, Daniel T
Yu, Hongjie
Venue: Clinical Infectious Diseases
Publisher: Oxford University Press (OUP)
Published: 2021-07-24
Volume: 74
Issue: 4
Pages: 734-742
ISSN: 1058-4838 (ISSN-L)
1537-6591
DOI: 10.1093/cid/ciab646
PMC: PMC9016754
OpenAlex: W3183560460
Cited by: 113
References: 52
Citations by year: 2026: 2 · 2025: 9 · 2024: 7 · 2023: 20 · 2022: 52 · 2021: 23
FWCI: 2.98
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations: Clinical Infectious Diseases (publishedVersion)
medRxiv (acceptedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
PubMed Central (submittedVersion, cc-by-nc-nd)
Funders: National Science Fund for Distinguished Young Scholars (81525023)
Program of Shanghai Academic Research Leader (18XD1400300)
National Science and Technology Major Project (2018ZX10713001-007, 2017ZX10103009-005, 2018ZX10201001-010)
National Institutes of Health (R01 AI135115)
Topics: Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
Keywords: SARS-CoV-2 variants, neutralizing antibodies, antibody escape, natural infection, COVID-19 vaccines, mRNA vaccines, vector vaccines, subunit vaccine, neutralization titers

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Neutralizing Antibodies Against Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Variants Induced by Natural Infection or Vaccination: A Systematic Review and Pooled Analysis

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