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

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

doi:10.1093/cid/ciab646

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

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 +7 more·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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The Alpha variant is susceptible to neutralization by most neutralizing mAbs as well as by most plasma samples from previously infected persons.
“The Alpha variant is susceptible to neutralization by most neutralizing mAbs as well as by most plasma samples from previously infected persons 97,102,121,149,159,[203][204][205][206] (fIg.5).”
From The biological and clinical significance of emerging SARS-CoV-2 variants (2021) · cites this paper as [97]
The Alpha variant has displayed 3-fold to 10-fold reduced susceptibility to approximately 15% of plasma samples from recipients of an authorized mRNA vaccine.
“The Alpha variant has displayed 3-fold to 10-fold reduced susceptibility to approximately 15% of plasma samples from recipients of an authorized mRNA vaccine 97,102,121,148,149,152,159,204,208,209 .”
From The biological and clinical significance of emerging SARS-CoV-2 variants (2021) · cites this paper as [97]
Of plasma samples from persons receiving one of the two authorized mRNA vaccines, about 60% had 3-fold to 10-fold and 5% had >10-fold reduced neutralizing activity to the Gamma variant.
“Of plasma samples from persons receiving one of the two authorized mRNA vaccines, about 60% had 3-fold to 10-fold and 5% had >10-fold reduced neutralizing activity 97,103,117,167,217,230 (fIg.5).”
From The biological and clinical significance of emerging SARS-CoV-2 variants (2021) · cites this paper as [97]
Of convalescent plasma samples obtained from persons infected with early pandemic variants or with the Alpha variant, about 20% had 3-fold to 10-fold and 10% had >10-fold reduced neutralizing activity to the Gamma variant.
“Of convalescent plasma samples obtained from persons infected with early pandemic variants or with the Alpha variant, about 20% had 3-fold to 10-fold and 10% had >10-fold reduced neutralizing activity 97,103,117,203,217,228,229 (fIg.5).”
From The biological and clinical significance of emerging SARS-CoV-2 variants (2021) · cites this paper as [97]
Of plasma samples obtained from persons receiving one of the mRNA vaccines, 45% had 3-fold to 10-fold and 30% had >10-fold reduced Beta variant neutralizing activity.
“Of plasma samples obtained from persons receiving one of the mRNA vaccines, 45% had 3-fold to 10-fold and 30% had >10-fold reduced Beta variant neutralizing activity 97,104,117,121,151,204,208,209,222,223 (fIg.5).”
From The biological and clinical significance of emerging SARS-CoV-2 variants (2021) · cites this paper as [97]

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Coronavirus Resistance Database (CoV-RDB): SARS-CoV-2 susceptibility to monoclonal antibodies, convalescent plasma, and plasma from vaccinated persons
Tzou, P. L., Tao, K., Pond, S. L. K., & Shafer, R. W. (2022) · PLoS ONE · doi:10.1371/journal.pone.0261045 · Cited by 124 · see citing works
Risk Factors of Severe COVID-19: A Review of Host, Viral and Environmental Factors
Zsichla, L., & Müller, V. (2023) · Viruses · doi:10.3390/v15010175 · Cited by 113 · see citing works
Predictors and Dynamics of the Humoral and Cellular Immune Response to SARS-CoV-2 mRNA Vaccines in Hemodialysis Patients: A Multicenter Observational Study
Praet, J. T. V., Reynders, M., Bacquer, D. D., Viaene, L., Schoutteten, M., Caluwé, R., Doubel, P., Heylen, L., Bel, A. V. D., Vlem, B. V., et al. (2021) · Journal of the American Society of Nephrology · doi:10.1681/asn.2021070908 · Cited by 89 · see citing works
Recognition of Variants of Concern by Antibodies and T Cells Induced by a SARS-CoV-2 Inactivated Vaccine
Melo-González, F., Soto, J. A., González, L. A., Fernández, J. O., Duarte, L. F., Schultz, B. M., Gálvez, N. M. S., Pacheco, G. A., Ríos, M., Vázquez, Y., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.747830 · Cited by 78 · see citing works
Effectiveness of COVID-19 vaccines against SARS-CoV-2 variants of concern in real-world: a literature review and meta-analysis
Shao, W.-H., Chen, X.-R., Zheng, C.-F., Liu, H.-S., Wang, G.-L., Zhang, B., Li, Z., & Zhang, W. (2022) · Emerging Microbes and Infections · doi:10.1080/22221751.2022.2122582 · Cited by 64 · see citing works
“Nevertheless, the neutralizing response against Beta, Delta and Gamma variants was significantly reduced compared with wild type [21].”
BackgroundSelf-citation
A systematic review of Vaccine Breakthrough Infections by SARS-CoV-2 Delta Variant
Zhang, M., Liang, Y., Yu, D., Du, B., Cheng, W., Li, L., Yu, Z., Luo, S., Zhang, Y., Wang, H., et al. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.68973 · Cited by 66 · see citing works
“It has also been proven that P681R is located near the host protease binding site and it is likely the main mutation that drives the cleavage of the S protein and enhances the infectivity of the virus (Table 2) [85, 86].”
Background
SARS-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 61 · see citing works
Lower vaccine-acquired immunity in the elderly population following two-dose BNT162b2 vaccination is alleviated by a third vaccine dose
Rénia, L., Goh, Y. S., Rouers, A., Bert, N. L., Chia, W. N., Chavatte, J., Fong, S., Chang, Z. W., Zhuo, N. Z., Tay, M. Z., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32312-1 · Cited by 58 · see citing works
Casirivimab and Imdevimab for the Treatment of Hospitalized Patients With COVID-19
Somersan-Karakaya, S., Mylonakis, E. E., Menon, V. P., Wells, J. C., Ali, S., Sivapalasingam, S., Sun, Y., Bhore, R., Mei, J., Miller, J., et al. (2022) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiac320 · Cited by 53 · see citing works
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 · see citing works
SARS-CoV-2 journey: from alpha variant to omicron and its sub-variants
Hattab, D., Amer, M. F. A., Al‐Alami, Z. M., & Bakhtiar, A. (2024) · Infection · doi:10.1007/s15010-024-02223-y · Cited by 44 · see citing works
Inactivated vaccine-elicited potent antibodies can broadly neutralize SARS-CoV-2 circulating variants
Liu, Y., Wang, Z., Zhuang, X., Zhang, S., Chen, Z., Zou, Y., Sheng, J., Li, T., Tai, W., Yu, J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37926-7 · Cited by 42 · see citing works
Self-citation
SARS-CoV-2—The Role of Natural Immunity: A Narrative Review
Diani, S., Leonardi, E. A., Cavezzi, A., Ferrari, S., Iacono, O., Limoli, A., Bouslenko, Z., Natalini, D., Conti, S., Mantovani, M., et al. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11216272 · Cited by 44 · see citing works
“There are studies that indicate that vaccination in recovered patients increases the antibody titer [164,171,175,176] or improve the outcome of the disease [150,170] but in some cases these studies have been carried out only in vitro, and therefore do not consider the clinical aspects (see for instance [177–179]).”
Background
A Third Dose of an Inactivated Vaccine Dramatically Increased the Levels and Decay Times of Anti-SARS-CoV-2 Antibodies, but Disappointingly Declined Again: A Prospective, Longitudinal, Cohort Study at 18 Serial Time Points Over 368 Days
Liang, X., Xu, Q., Jia, Z.-J., Wu, M., Liu, Y., Lin, L., Liu, L., & Yang, T. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.876037 · Cited by 42 · see citing works
Self-Adjuvanting Lipoprotein Conjugate αGalCer-RBD Induces Potent Immunity against SARS-CoV-2 and its Variants of Concern
Wang, J., Wen, Y., Zhou, S., Zhang, H., Peng, X., Zhang, R., Yin, X., Qiu, H. Y., Gong, R., Yang, G., et al. (2022) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.1c02000 · Cited by 42 · see citing works
SARS-CoV-2 infections elicit higher levels of original antigenic sin antibodies compared with SARS-CoV-2 mRNA vaccinations
Anderson, E. M., Li, S. H., Awofolaju, M., Eilola, T., Goodwin, E. C., Bolton, M. J., Gouma, S., Manzoni, T. B., Hicks, P. D., Goel, R. R., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111496 · Cited by 35 · see citing works
“Studies have shown that antibodies elicited by vaccination and infections differentially recognize and neutralize SARS-CoV-2 variants (Chen et al., 2021; Cho et al., 2021; Goel et al., 2021b; Greaney et al., 2021; Planas et al., 2021; Stamatatos et al., 2021; Starr et al., 2021; Wang et al., 2021a).”
SARS-CoV-2 Variants: A Synopsis of In Vitro Efficacy Data of Convalescent Plasma, Currently Marketed Vaccines, and Monoclonal Antibodies
Focosi, D., Tuccori, M., Baj, A., & Maggi, F. (2021) · Viruses · doi:10.3390/v13071211 · Cited by 37 · see citing works
Status of Humoral and Cellular Immune Responses within 12 Months following CoronaVac Vaccination against COVID-19
Zhao, W., Chen, W., Li, J., Chen, M., Li, Q., Lv, M., Zhou, S., Bai, S., Wang, Y., Zhang, L., et al. (2022) · mBio · doi:10.1128/mbio.00181-22 · Cited by 37 · see citing works
Investigating vaccine-induced immunity and its effect in mitigating SARS-CoV-2 epidemics in China
Liu, H., Zhang, J., Cai, J., Deng, X., Peng, C., Chen, X., Yang, J., Wu, Q., Chen, X., Chen, Z., et al. (2022) · BMC Medicine · doi:10.1186/s12916-022-02243-1 · Cited by 37 · see citing works
Self-citation
Viral Load in COVID-19 Patients: Implications for Prognosis and Vaccine Efficacy in the Context of Emerging SARS-CoV-2 Variants
da Silva, S. J. R., de Lima, S. C., da Silva, R. C., Kohl, A., & Pena, L. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2021.836826 · Cited by 36 · see citing works
Evaluation of commercially available fully automated and ELISA-based assays for detecting anti-SARS-CoV-2 neutralizing antibodies
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) · Scientific Reports · doi:10.1038/s41598-022-21317-x · Cited by 35 · see citing works
Immune correlates of protection for SARS-CoV-2, Ebola and Nipah virus infection
Escudero-Pérez, B., Lawrence, P., & Castillo-Olivares, J. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1156758 · Cited by 32 · see citing works
The intestinal microbiota and improving the efficacy of COVID-19 vaccinations
Chen, J., Vitetta, L., Henson, J. D., & Hall, S. (2021) · Journal of Functional Foods · doi:10.1016/j.jff.2021.104850 · Cited by 32 · see citing works
Detection of Major SARS-CoV-2 Variants of Concern in Clinical Samples via CRISPR-Cas12a-Mediated Mutation-Specific Assay
Liang, Y., Zou, L., Lin, H., Li, B., Zhao, J., Wang, H., Sun, J., Chen, J., Mo, Y., Yang, X., et al. (2022) · ACS Synthetic Biology · doi:10.1021/acssynbio.1c00643 · Cited by 28 · see citing works
Self-citation
Research progress on vaccine efficacy against SARS-CoV-2 variants of concern
Bian, L., Liu, J., Gao, F., Gao, Q., He, Q., Mao, Q., Wu, X., Xu, M., & Liang, Z. (2022) · Human Vaccines & Immunotherapeutics · doi:10.1080/21645515.2022.2057161 · Cited by 29 · see citing works
Prediction of long-term kinetics of vaccine-elicited neutralizing antibody and time-varying vaccine-specific efficacy against the SARS-CoV-2 Delta variant by clinical endpoint
Chen, X., Wang, W., Chen, X., Wu, Q., Sun, R., Ge, S., Zheng, N., Lu, W., Yang, J., Rodewald, L. E., et al. (2022) · BMC Medicine · doi:10.1186/s12916-022-02249-9 · Cited by 25 · see citing works
“Compared to neutralizing antibody levels induced by natural infection, vaccination may induce similar or lower neutralizing antibody levels [3] that decay faster [4].”
BackgroundMethodSelf-citation
Real-world effectiveness and factors associated with effectiveness of inactivated SARS-CoV-2 vaccines: a systematic review and meta-regression analysis
Xu, S. S., Li, J., Wang, H., Wang, F., Yin, Z., & Wang, Z. (2023) · BMC Medicine · doi:10.1186/s12916-023-02861-3 · Cited by 27 · see citing works
“” Data in one article was of the WT strain, and the study showed that antibodies in vaccine-induced serum largely retained neutralizing response against Alpha [26], so we merged the evaluation of the WT strain with the Alpha strain data.”
Result
Six-month follow-up of a booster dose of CoronaVac in two single-centre phase 2 clinical trials
Xin, Q., Wu, Q., Chen, X., Han, B., Chu, K., Song, Y., Jin, H., Chen, P., Lu, W., Yang, T., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30864-w · Cited by 25 · see citing works
Self-citation
Factors Affecting the Antibody Immunogenicity of Vaccines against SARS-CoV-2: A Focused Review
Cheng, Z. J., Xue, M., Zheng, P., Lyu, J., Zhan, Z., Hu, H., Zhang, Y., Zhang, X. D., & Sun, B. (2021) · Vaccines · doi:10.3390/vaccines9080869 · Cited by 25 · see citing works
Contamination of Hospital Surfaces with Bacterial Pathogens under the Current COVID-19 Outbreak
Pochtovyi, A. A., Vasina, D. V., Kustova, D. D., Divisenko, E. V., Kuznetsova, N. A., Burgasova, O., Kolobukhina, L. V., Петрович, Т. А., Gushchin, V. А., & Al, G. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18179042 · Cited by 22 · see citing works
Correlation of the Commercial Anti-SARS-CoV-2 Receptor Binding Domain Antibody Test with the Chemiluminescent Reduction Neutralizing Test and Possible Detection of Antibodies to Emerging Variants
Morinaga, Y., Tani, H., Terasaki, Y., Nomura, S., Kawasuji, H., Shimada, T., Igarashi, E., Saga, Y., Yoshida, Y., Yasukochi, R., et al. (2021) · Microbiology Spectrum · doi:10.1128/spectrum.00560-21 · Cited by 24 · see citing works
“also reports that variant neutralizing activity is similar to WT (14, 29, 30), our findings”
Result
RBD conjugate vaccine with a built-in TLR1/2 agonist is highly immunogenic against SARS-CoV-2 and variants of concern
Zhou, S., Zhang, R., Zhang, H.-W., Liu, Y., Wen, Y., Wang, J., Li, Y., You, Z.-W., Yin, X., Qiu, H. Y., et al. (2022) · Chemical Communications · doi:10.1039/d1cc06520c · Cited by 24 · see citing works
Immune Evasive Effects of SARS-CoV-2 Variants to COVID-19 Emergency Used Vaccines
Zhang, Y., Ndzouboukou, J. B., Gan, M., Lin, X., & Fan, X. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.771242 · Cited by 21 · see citing works
Rates of COVID-19 Among Unvaccinated Adults With Prior COVID-19
Ridgway, J. P., Tideman, S., Wright, B. J., & Robicsek, A. A. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.7650 · Cited by 18 · see citing works
Serological response after SARS-CoV2 vaccination in healthcare workers: a multicenter study
Visci, G., Zunarelli, C., Mansour, I., Porru, S., Palma, G. D., Duval, X., Monaco, M. G. L., Spiteri, G., Carta, A., Lippi, G., et al. (2022) · La Medicina del Lavoro · doi:10.23749/mdl.v113i2.13017 · Cited by 18 · see citing works
A comprehensive account of SARS-CoV-2 genome structure, incurred mutations, lineages and COVID-19 vaccination program
Rajpal, V. R., Sharma, S. K., Sehgal, D., Singh, A., Kumar, A., Vaishnavi, S., Tiwari, M., Bhalla, H., Goel, S., & Raina, S. (2022) · Future Virology · doi:10.2217/fvl-2021-0277 · Cited by 17 · see citing works
Evaluation of a Rapid and Accessible Reverse Transcription-Quantitative PCR Approach for SARS-CoV-2 Variant of Concern Identification
Yeung, P. S.-W., Wang, H., Sibai, M., Solis, D., Yamamoto, F. F., Iwai, N., Jiang, B., Hammond, N. A., Truong, B., Bihon, S., et al. (2022) · Journal of Clinical Microbiology · doi:10.1128/jcm.00178-22 · Cited by 17 · see citing works
The efficacy of COVID-19 vaccines against the B.1.617.2 (delta) variant
Cai, C., Liu, Y., Zeng, S., Shen, H., & Han, Y. (2021) · Molecular Therapy · doi:10.1016/j.ymthe.2021.09.024 · Cited by 17 · see citing works
“Chen et al.(10) found that mRNAbased vaccines produced the highest level of neutralizing antibodies in both normal vaccinated humans and in patients infected with delta variant, which is consistent with the efficacy analysis.”
Salivary, serological, and cellular immune response to the CoronaVac vaccine in health care workers with or without previous COVID-19
Ortega, M. M., da Silva, L. T., Candido, E. D., Zheng, Y., Tiyo, B. T., Ferreira, A. E. F., Correa‐Silva, S., Scagion, G. P., Leal, F. B., Chalup, V. N., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-14283-x · Cited by 16 · see citing works
Epidemiology and genetic diversity of SARS-CoV-2 lineages circulating in Africa
Okoh, O. S., Nii-Trebi, N. I., Jakkari, A., Olaniran, T. T., Senbadejo, T. Y., Kafintu-kwashie, A. A., Dairo, E. O., Ganiyu, T. O., Akaninyene, I. E., Ezediuno, L. O., et al. (2022) · iScience · doi:10.1016/j.isci.2022.103880 · Cited by 13 · see citing works
Evaluation of the immune response to COVID-19 vaccine mRNA BNT162b2 and correlation with previous COVID-19 infection
Bongiovanni, M., Liuzzi, G., Schiavon, L., Gianturco, L., & Giuliani, G. (2021) · Journal of Clinical Virology · doi:10.1016/j.jcv.2021.104962 · Cited by 14 · see citing works
Covid-19 vaccination programme effectiveness against SARS-CoV-2 related infections, hospital admissions and deaths in the Apulia region of Italy: a one-year retrospective cohort study
Homan, T., Mazzilli, S., Chieti, A., Musa, A., Roth, A., Fortunato, F., Bisceglia, L., Prato, R., Lopalco, P. L., & Martinelli, D. (2022) · Scientific Reports · doi:10.1038/s41598-022-23235-4 · Cited by 14 · see citing works
SARS-CoV-2 Neutralizing Antibody Levels Post COVID-19 Vaccination Based on ELISA Method—A Small Real-World Sample Exploration
Li, X., Liang, C., & Xiao, X. (2021) · Vaccines · doi:10.3390/vaccines9101139 · Cited by 14 · see citing works
Evaluation of antibody kinetics and durability in healthy individuals vaccinated with inactivated COVID-19 vaccine (CoronaVac): A cross-sectional and cohort study in Zhejiang, China
Zhang, H., Hua, Q., Xu, N., Zhang, X., Chen, B., Xi-jun, M., Hu, J., Chen, Z., Yu, P., Lei, H., et al. (2023) · eLife · doi:10.7554/elife.84056 · Cited by 14 · see citing works
Self-citation
Kinetics of neutralizing antibodies against SARS-CoV-2 infection according to sex, age, and disease severity
Kim, Y., Bae, J., Kwon, K. T., Chang, H., Lee, W. K., Park, H., Kim, J., Choi, I., Park, M., & Kim, S. (2022) · Scientific Reports · doi:10.1038/s41598-022-17605-1 · Cited by 11 · see citing works
Seeing the T cell Immunity of SARS-CoV-2 and SARS-CoV: Believing the Epitope-Oriented Vaccines
Yue, C., Wang, P., Tian, J., Gao, G. F., Liu, K., & Liu, W. J. (2023) · International Journal of Biological Sciences · doi:10.7150/ijbs.80468 · Cited by 12 · see citing works
An Integrated Platform for Serological Detection and Vaccination of COVID-19
Wei, S.-C., Hsu, W.-T., Chiu, C.-H., Chang, F., Lo, H.-R., Liao, C.-Y., Yang, H., Chou, Y., Tsai, C.-H., & Chao, Y. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.771011 · Cited by 11 · see citing works
“, its neutralizing antibody titers may decrease upon encountering Beta variants, but not in the case of Alpha and Gamma variants (24, 73).”
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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
“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 10 · see citing works
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 9 · see citing works
“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 · see citing works
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 9 · see citing works
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 · see citing works
“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 7 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“…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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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IgG4 Neutralization and Sustained Total IgG Fc-Effector Functions Following Repeated SARS-CoV-2 Vaccination with mRNA-1273
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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
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Comparison of the immunogenicity of nasal‐spray rVSV vector, adenovirus vector, and inactivated COVID‐19‐based vaccines in rodent models
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“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
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Influential
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Omicron neutralization character in patients with breast cancer and liver cancer after the nationwide omicron outbreak
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Result
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BackgroundInfluential
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Background
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Neutralizing Antibodies Against SARS-CoV-2 Variants Induced by Natural Infection or Vaccination: A Systematic Review and Individual Data Meta-AnalysisPreprint
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Neutralization of B.1.617.2 variant through antibodies elicited by ChAdOx1‐S, BBIBP‐CorV, and Gam‐COVID‐Vac in an Argentinean cohort
Blanco, S., Aguilar, J. J., Spinsanti, L., Díaz, A., Beranek, M., Rivarola, M. E., Fernández, E. A., Mangeaud, A. P., Konigheim, B. S., & Gallego, S. V. (2022) · Journal of Medical Virology · doi:10.1002/jmv.28286

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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