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Longitudinal observation and decline of neutralizing antibody responses in the three months following SARS-CoV-2 infection in humans
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Abstract
Antibody responses to SARS-CoV-2 can be detected in most infected individuals 10-15 d after the onset of COVID-19 symptoms. However, due to the recent emergence of SARS-CoV-2 in the human population, it is not known how long antibody responses will be maintained or whether they will provide protection from reinfection. Using sequential serum samples collected up to 94 d post onset of symptoms (POS) from 65 individuals with real-time quantitative PCR-confirmed SARS-CoV-2 infection, we show seroconversion (immunoglobulin (Ig)M, IgA, IgG) in >95% of cases and neutralizing antibody responses when sampled beyond 8 d POS. We show that the kinetics of the neutralizing antibody response is typical of an acute viral infection, with declining neutralizing antibody titres observed after an initial peak, and that the magnitude of this peak is dependent on disease severity. Although some individuals with high peak infective dose (ID 50 > 10,000) maintained neutralizing antibody titres >1,000 at >60 d POS, some with lower peak ID 50 had neutralizing antibody titres approaching baseline within the follow-up period. A similar decline in neutralizing antibody titres was observed in a cohort of 31 seropositive healthcare workers. The present study has important implications when considering widespread serological testing and antibody protection against reinfection with SARS-CoV-2, and may suggest that vaccine boosters are required to provide long-lasting protection.
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“SARS-CoV-2 infection rapidly elicits nAbs (16, 21–24) that decline, but remain detectable, over several months (25–29).”
From mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection (2021) · cites this paper as [28]
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Persistence of neutralizing antibodies a year after SARS‐CoV‐2 infection in humans
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Neutralisation sensitivity of the SARS-CoV-2 omicron (B.1.1.529) variant: a cross-sectional study
Sheward, D. J., Kim, C., Ehling, R. A., Pankow, A. P., Dopico, X. C., Dyrdak, R., Martin, D. P., Reddy, S. T., Dillner, J., Hedestam, G. B. K., et al. (2022) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(22)00129-3 · Cited by 80
Townsend, J. P., Hassler, H. B., Sah, P., Galvani, A. P., & Dornburg, A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204336119 · Cited by 85
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Robust and durable serological response following pediatric SARS-CoV-2 infection
Renk, H., Dulovic, A., Seidel, A., Becker, M., Fabricius, D., Zernickel, M., Junker, D., Groß, R. M., Müller, J. A., Hilger, A., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-27595-9 · Cited by 81
An Effective COVID-19 Vaccine Needs to Engage T Cells
Sauer, K., & Harris, T. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.581807 · Cited by 85
Neutralizing Antibodies in COVID-19 Patients and Vaccine Recipients after Two Doses of BNT162b2
Favresse, J., Gillot, C., Chiaro, L. D., Eucher, C., Elsen, M., Eeckhoudt, S. V., David, C., Morimont, L., Dogné, J., & Douxfils, J. (2021) · Viruses · doi:10.3390/v13071364 · Cited by 85
Overview of Neutralizing Antibodies and Their Potential in COVID-19
Morales‐Núñez, J. J., Muñóz-Valle, J. F., Torres-Hernández, P. C., & Hernández‐Bello, J. (2021) · Vaccines · doi:10.3390/vaccines9121376 · Cited by 86
“showed that the kinetics of the neutralizing antibody response is typical of an acute viral infection, with declining neutralizing antibody titers observed after an initial peak, and that the magnitude of this peak is dependent on disease severity [100].”
BackgroundSetting the criteria for SARS-CoV-2 reinfection – six possible cases
Tomassini, S., Kotecha, D., Bird, P. W., Folwell, A., Simon, B., & Tang, J. W.-T. (2020) · Journal of Infection · doi:10.1016/j.jinf.2020.08.011 · Cited by 79
Oguntuyo, K. Y., Stevens, C. S., Hung, C.-T., Ikegame, S., Acklin, J. A., Kowdle, S., Carmichael, J. C., Chiu, H.-P., Azarm, K. D., Haas, G. D., et al. (2021) · mBio · doi:10.1128/mbio.02492-20 · Cited by 73
Primary, Recall, and Decay Kinetics of SARS-CoV-2 Vaccine Antibody Responses
Ibarrondo, F. J., Hofmann, C., Fulcher, J. A., Goodman‐Meza, D., Mu, W., Hausner, M. A., Ali, A., Balamurugan, A., Taus, E., Elliott, J. E., et al. (2021) · ACS Nano · doi:10.1021/acsnano.1c03972 · Cited by 79
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“For example, while human influenza virus, coronaviruses (HCoVs), and orthopneumoviruses exhibit an annual increase in incidence during winter (Shaman and Kohn, 2009), some non-polio enteroviruses have seasonal peaks in summer (Pons-Salort et al., 2018).”
Decay of Fc-dependent antibody functions after mild to moderate COVID-19
Lee, W. S., Selva, K. J., Davis, S. K., Wines, B. D., Reynaldi, A., Esterbauer, R., Kelly, H. G., Haycroft, E. R., Tan, H., Juno, J. A., et al. (2021) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100296 · Cited by 81
“Several studies now show neutralizing antibodies decline rapidly during early convalescence,(2,8,9) with the magnitude of the antibody response positively correlating with disease severity.(10,11) Following mild COVID-19, many subjects mount modest neutralizing antibody”
Abayasingam, A., Balachandran, H., Agapiou, D., Hammoud, M., Rodrigo, C., Keoshkerian, E., Li, H., Brasher, N. A., Christ, D., Rouet, R., et al. (2021) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100228 · Cited by 78
“1 4 Age and disease severity have been linked with higher antibody titers and virus-specific neutralizing activity, 5 and it has been suggested that antibody responses may wane more quickly following mild illness, 6 although not all studies support these observations.”
Tan, H., Juno, J. A., Lee, W. S., Barber-Axthelm, I. M., Kelly, H. G., Wragg, K. M., Esterbauer, R., Amarasena, T. H., Mordant, F. L., Subbarao, K., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21665-8 · Cited by 79
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“least from two or three [9,10] to five months [11].”
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Modelling and optimal control of multi strain epidemics, with application to COVID-19
Arruda, E. F., Das, S. S., Dias, C. M., & Pastore, D. H. (2021) · PLoS ONE · doi:10.1371/journal.pone.0257512 · Cited by 85
A single-dose mRNA vaccine provides a long-term protection for hACE2 transgenic mice from SARS-CoV-2
Huang, Q., Ji, K., Tian, S., Wang, F., Huang, B., Tong, Z., Tan, S., Hao, J., Wang, Q., Tan, W., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21037-2 · Cited by 79
Bauer, G. (2021) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2021.01.061 · Cited by 74
The role of B cells in COVID-19 infection and vaccination
Chen, S., Guan, F., Candotti, F., Benlagha, K., Câmara, N. O. S., Herrada, A. A., James, L. K., Lei, J., Miller, H., Kubo, M., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.988536 · Cited by 75
“Moreover, the quick decline of SARS-CoV-2 specific nAb titers (within 2 months) among severe, mild and asymptomatic patients further indicates that the protection from the humoral response is not only time-limited, but it is also insufficient (51, 52).”
BackgroundBruni, M., Cecatiello, V., Díaz‐Basabe, A., Lattanzi, G., Mileti, E., Monzani, S., Pirovano, L., Rizzelli, F., Visintin, C., Bonizzi, G., et al. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9103188 · Cited by 74
Influence of obesity on serum levels of SARS-CoV-2-specific antibodies in COVID-19 patients
Frasca, D., Reidy, L. J., Cray, C., Diaz, A., Romero, M., Kahl, K. W., & Blomberg, B. B. (2021) · PLoS ONE · doi:10.1371/journal.pone.0245424 · Cited by 77
“been shown that individuals with a confirmed PCR diagnosis of infection develop antibodies against the Spike protein [49], how obesity may affect the secretion of SARS-CoV-2-specific IgG is poorly elucidated.”
BackgroundSIRSi compartmental model for COVID-19 pandemic with immunity loss
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Antibody Responses to Natural SARS-CoV-2 Infection or after COVID-19 Vaccination
Altawalah, H. (2021) · Vaccines · doi:10.3390/vaccines9080910 · Cited by 74
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Respiratory mucosal immune memory to SARS-CoV-2 after infection and vaccination
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Toward Achieving a Vaccine-Derived Herd Immunity Threshold for COVID-19 in the U.S.
Gumel, A. B., Iboi, E., Ngonghala, C. N., & Ngwa, G. A. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2021.709369 · Cited by 73
Mahil, S. K., Bechman, K., Raharja, A., Domingo-Vila, C., Baudry, D., Brown, M. A., Cope, A. P., Dasandi, T., Graham, C., Khan, H., et al. (2021) · The Lancet Rheumatology · doi:10.1016/s2665-9913(21)00333-7 · Cited by 77
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Self-citationPersistence of IgG response to SARS-CoV-2
Duysburgh, E., Mortgat, L., Barbezange, C., Dierick, K., Fischer, N., Heyndríckx, L., Hutse, V., Thomas, I., Gucht, S. V., Vuylsteke, B., et al. (2020) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(20)30943-9 · Cited by 68
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“Recent studies have shown that most patients had detectable SARS-CoV-2 antibody responses 6–8 months after infection [6, 12, 16-19].”
Background
Metadata
- Authors
- Seow, J., Graham, C., Merrick, B., Acors, S., Pickering, S., Steel, K. J. A., Hemmings, O., O’Byrne, A., Kouphou, N., Galao, R. P., Betancor, G., Wilson, H. D., Signell, A. W., Winstone, H., Kerridge, C., Huettner, I., Jimenez-Guardeño, J. M., Lista, M. J., Temperton, N., Snell, L. B., Bisnauthsing, K., Moore, A., Green, A., Martinez, L., Stokes, B., Honey, J., Izquierdo-Barras, A., Arbane, G., Patel, A., Tan, M. K. I., O’Connell, L., O’Hara, G., MacMahon, E., Douthwaite, S., Nebbia, G., Batra, R., Martinez-Nunez, R., Shankar-Hari, M., Edgeworth, J. D., Neil, S. J. D., Malim, M. H., & Doores, K. J.
- Affiliations
- King's College London (GB)
- Guy's Hospital (GB)
- Medway School of Pharmacy (GB)
- Guy's and St Thomas' NHS Foundation Trust (GB)
- Corresponding author
- Doores, Katie J.
- ORCID
- Seow, Jeffrey
- Merrick, Blair
- Acors, Sam
- Pickering, Suzanne
- Steel, Kathryn J. A.
- Hemmings, Oliver
- O’Byrne, Aoife
- Kouphou, Neophytos
- Galao, Rui Pedro
- Betancor, Gilberto
- Wilson, Harry D.
- Signell, Adrian W.
- Winstone, Helena
- Jimenez-Guardeño, Jose M.
- Temperton, Nigel
- Snell, Luke B.
- Bisnauthsing, Karen
- Martinez, Lauren
- Stokes, Brielle
- Izquierdo-Barras, Alba
- Patel, Amita
- Tan, Mark Kia Ik
- O’Connell, Lorcan
- O’Hara, Geraldine
- Douthwaite, Sam
- Nebbia, Gaia
- Batra, Rahul
- Shankar-Hari, Manu
- Edgeworth, Jonathan D.
- Neil, Stuart J. D.
- Malim, Michael H.
- Doores, Katie J.
- Venue
- Nature Microbiology
- Published
- 2020-10-26
- Volume
- 5
- Issue
- 12
- Pages
- 1598-1607
- ISSN
- 2058-5276 (ISSN-L)
- PMC
- PMC7610833
- OpenAlex
- W3093667122
- Cited by
- 1,419
- References
- 62
- Citations by year
- 2026: 18 · 2025: 44 · 2024: 75 · 2023: 147 · 2022: 311 · 2021: 615 · 2020: 207
- FWCI
- 41.93
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Microbiology (publishedVersion)
- medRxiv (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Kent Academic Repository (University of Kent) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Research Portal (King's College London) (submittedVersion, other-oa)
- Repositorio Institucional de la Universidad de Málaga (University of Málaga) (submittedVersion, cc-by-nc-nd)
- Funders
- RCUK | Medical Research Council (MC/PC/15068, MR/N013700/1, MR/R015643/1, MC/PC/15068, MR/R015643/1, MR/S023747/1)
- Huo Family Foundation
- Wellcome Trust (WT098049AIA, MR/S023747/1, 106223/Z/14/Z)
- Huo Family Foundation King’s Together Rapid COVID-19 Call award
- DH | National Institute for Health Research (CS-2016-16-011)
- King’s Together Rapid COVID-19 Call award Huo Family Foundation
- Fondation Dormeur, Vaduz King’s Together Rapid COVID-19 Call award Huo Family Foundation
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 detection and testing
- Keywords
- SARS-CoV-2, COVID-19 pandemic, neutralizing antibodies, antibody waning, seroconversion, antibody kinetics, disease severity, infectious dose, reinfection protection, healthcare workers, booster vaccination, serological testing
- MeSH terms
- Seroconversion, COVID-19, SARS-CoV-2, Adult, Aged, Aged, 80 and over, Antibodies, Viral, Female, Humans, Kinetics, Longitudinal Studies, Male, Middle Aged, Severity of Illness Index, Young Adult, Antibodies, Neutralizing
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