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 that decline, but remain detectable, over several months.
“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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Evolution of antibody immunity to SARS-CoV-2
Gaebler, C., Wang, Z., Lorenzi, J. C. C., Muecksch, F., Finkin, S., Tokuyama, M., Cho, A., Jankovic, M., Schaefer-Babajew, D., Oliveira, T. Y., et al. (2021) · Nature · doi:10.1038/s41586-021-03207-w · Cited by 1,674 · see citing works
Popkin, B. M., Du, S., Green, W. D., Beck, M. A., Algaith, T., Herbst, C. H., Alsukait, R. F., Alluhidan, M., Alazemi, N., & Shekar, M. (2020) · Obesity Reviews · doi:10.1111/obr.13128 · Cited by 1,150 · see citing works
SARS-CoV-2 evolution during treatment of chronic infection
Kemp, S. A., Collier, D. A., Datir, R. P., Ferreira, I. A. T. M., Gayed, S., Jahun, A., Hosmillo, M., Rees-Spear, C., Mlcochova, P., Lumb, I. U., et al. (2021) · Nature · doi:10.1038/s41586-021-03291-y · Cited by 1,097 · see citing works
Self-citationImmunological considerations for COVID-19 vaccine strategies
Jeyanathan, M., Afkhami, S., Smaill, F., Miller, M. S., Lichty, B. D., & Xing, Z. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-00434-6 · Cited by 1,015 · see citing works
Antibody Status and Incidence of SARS-CoV-2 Infection in Health Care Workers
Lumley, S. F., O’Donnell, D., Stoesser, N. E., Matthews, P. C., Howarth, A., Hatch, S. B., Marsden, B. D., Cox, S., James, T., Warren, F., et al. (2021) · New England Journal of Medicine · doi:10.1056/nejmoa2034545 · Cited by 940 · see citing works
Virology, transmission, and pathogenesis of SARS-CoV-2
Çevik, M., Kuppalli, K., Kindrachuk, J., & Peiris, M. J. S. (2020) · BMJ · doi:10.1136/bmj.m3862 · Cited by 750 · see citing works
Persistent neurologic symptoms and cognitive dysfunction in non-hospitalized COVID-19 “long haulers”
Graham, E. L., Clark, J. R., Orban, Z. S., Lim, P. H., Szymanski, A. L., Taylor, C., DiBiase, R. M., Jia, D. T., Balabanov, R., Ho, S. U., et al. (2021) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51350 · Cited by 693 · see citing works
Functional SARS-CoV-2-Specific Immune Memory Persists after Mild COVID-19
Rodda, L. B., Netland, J., Shehata, L., Pruner, K. B., Morawski, P. A., Thouvenel, C. D., Takehara, K. K., Eggenberger, J., Hemann, E. A., Waterman, H. R., et al. (2021) · Cell · doi:10.1016/j.cell.2020.11.029 · Cited by 647 · see citing works
Hodgson, S. H., Mansatta, K., Mallett, G., Harris, V., Emary, K. R. W., & Pollard, A. J. (2021) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(20)30773-8 · Cited by 633 · see citing works
mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection
Stamatatos, L., Czartoski, J., Wan, Y.-H., Homad, L. J., Rubin, V., Glantz, H., Neradilek, M., Seydoux, E., Jennewein, M. F., MacCamy, A. J., et al. (2021) · Science · doi:10.1126/science.abg9175 · Cited by 557 · see citing works
Monin, L., Laing, A. G., Muñoz‐Ruiz, M., McKenzie, D. R., del Barrio, I. D. M., Alaguthurai, T., Domingo‐Vila, C., Hayday, T. S., Graham, C., Seow, J., et al. (2021) · The Lancet Oncology · doi:10.1016/s1470-2045(21)00213-8 · Cited by 601 · see citing works
Self-citationImmunity, endothelial injury and complement-induced coagulopathy in COVID-19
Perico, L., Benigni, A., Casiraghi, F., Ng, L. F. P., Rénia, L., & Remuzzi, G. (2020) · Nature Reviews Nephrology · doi:10.1038/s41581-020-00357-4 · Cited by 603 · see citing works
Infection fatality rate of COVID-19 inferred from seroprevalence data
Ioannidis, J. P. A. (2021) · Bulletin of the World Health Organization · doi:10.2471/blt.20.265892 · Cited by 684 · see citing works
Addetia, A., Crawford, K. H. D., Dingens, A., Zhu, H., Roychoudhury, P., Huang, M.-L., Jerome, K. R., Bloom, J. D., & Greninger, A. L. (2020) · Journal of Clinical Microbiology · doi:10.1128/jcm.02107-20 · Cited by 525 · see citing works
SARS-CoV-2 immunity: review and applications to phase 3 vaccine candidates
Poland, G., Ovsyannikova, I., & Kennedy, R. (2020) · The Lancet · doi:10.1016/s0140-6736(20)32137-1 · Cited by 540 · see citing works
Transmission, infectivity, and neutralization of a spike L452R SARS-CoV-2 variant
Deng, X., Garcia-Knight, M. A., Khalid, M. M., Servellita, V., Wang, C., Morris, M. K., Sotomayor-González, A., Glasner, D. R., Reyes, K. R., Gliwa, A. S., et al. (2021) · Cell · doi:10.1016/j.cell.2021.04.025 · Cited by 651 · see citing works
Enhanced SARS-CoV-2 neutralization by dimeric IgA
Wang, Z., Lorenzi, J. C. C., Muecksch, F., Finkin, S., Viant, C., Gaebler, C., Cipolla, M., Hoffmann, H.-H., Oliveira, T. Y., Oren, D. A., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abf1555 · Cited by 475 · see citing works
Antibody responses to the BNT162b2 mRNA vaccine in individuals previously infected with SARS-CoV-2
Ebinger, J. E., Fert‐Bober, J., Printsev, I., Wu, M., Sun, N., Prostko, J. C., Frias, E. C., Stewart, J. L., Eyk, J. E. V., Braun, J. G., et al. (2021) · Nature Medicine · doi:10.1038/s41591-021-01325-6 · Cited by 524 · see citing works
SARS-CoV-2 infection induces long-lived bone marrow plasma cells in humans
Turner, J. S., Kim, W., Kalaidina, E., Goss, C. W., Rauseo, A. M., Schmitz, A. J., Hansen, L., Haile, A., Klebert, M. K., Pusic, I., et al. (2021) · Nature · doi:10.1038/s41586-021-03647-4 · Cited by 515 · see citing works
Abani, O., Abbas, A. H., Abbas, F., Abbas, M. A., Abbasi, S., Abbass, H., Abbott, A., Abdallah, N., Abdelaziz, A., Abdelfattah, M., et al. (2021) · The Lancet · doi:10.1016/s0140-6736(21)00897-7 · Cited by 493 · see citing works
The first 12 months of COVID-19: a timeline of immunological insights
Carvalho, T., Krammer, F., & Iwasaki, A. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00522-1 · Cited by 448 · see citing works
Carter, M. J., Fish, M., Jennings, A., Doores, K. J., Wellman, P., Seow, J., Acors, S., Graham, C., Timms, E., Kenny, J., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1054-6 · Cited by 419 · see citing works
Self-citationSARS-CoV-2-mediated dysregulation of metabolism and autophagy uncovers host-targeting antivirals
Gassen, N. C., Papies, J., Bajaj, T., Emanuel, J., Dethloff, F., Chua, R. L., Trimpert, J., Heinemann, N., Niemeyer, C., Weege, F., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24007-w · Cited by 401 · see citing works
Drugs that inhibit TMEM16 proteins block SARS-CoV-2 spike-induced syncytia
Braga, L., Ali, H., Secco, I., Chiavacci, E., Neves, G., Goldhill, D. H., Penn, R., Jiménez-Guardeño, J. M., Ortega‐Prieto, A. M., Bussani, R., et al. (2021) · Nature · doi:10.1038/s41586-021-03491-6 · Cited by 389 · see citing works
Self-citationTali, S. H. S., LeBlanc, J. J., Sadiq, Z., Oyewunmi, O. D., Camargo, C., Nikpour, B., Armanfard, N., Sagan, S. M., & Jahanshahi‐Anbuhi, S. (2021) · Clinical Microbiology Reviews · doi:10.1128/cmr.00228-20 · Cited by 411 · see citing works
COVID-19 vaccines: The status and perspectives in delivery points of view
Chung, J. Y., Thone, M. N., & Kwon, Y. J. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2020.12.011 · Cited by 375 · see citing works
Antibody response to SARS-CoV-2 infection in humans: A systematic review
Post, N., Eddy, D., Huntley, C., van Schalkwyk, M. C., Shrotri, M., Leeman, D., Rigby, S., Williams, S. V., Bermingham, W. H., Kellam, P., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0244126 · Cited by 367 · see citing works
Evolution of immune responses to SARS-CoV-2 in mild-moderate COVID-19
Wheatley, A. K., Juno, J. A., Wang, J. J., Selva, K. J., Reynaldi, A., Tan, H.-X., Lee, W. S., Wragg, K. M., Kelly, H. G., Esterbauer, R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21444-5 · Cited by 351 · see citing works
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T cell response to SARS-CoV-2 infection in humans: A systematic review
Shrotri, M., van Schalkwyk, M. C., Post, N., Eddy, D., Huntley, C., Leeman, D., Rigby, S., Williams, S. V., Bermingham, W. H., Kellam, P., et al. (2021) · PLoS ONE · doi:10.1371/journal.pone.0245532 · Cited by 349 · see citing works
Aboudounya, M. M., & Heads, R. J. (2021) · Mediators of Inflammation · doi:10.1155/2021/8874339 · Cited by 351 · see citing works
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Neutralizing antibody titres in SARS-CoV-2 infections
Lau, E., Tsang, O., Hui, D. S. C., Kwan, M., Chan, W.-H., Chiu, S., Ko, R. L. W., Chan, K. H., Cheng, S. M. S., Perera, R. A. P. M., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20247-4 · Cited by 320 · see citing works
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Ferretti, A. P., Kula, T., Wang, Y., Nguyen, D. M. V., Weinheimer, A., Dunlap, G. S., Xu, Q., Nabilsi, N., Perullo, C. R., Cristofaro, A. W., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.10.006 · Cited by 318 · see citing works
Bergeri, I., Whelan, M. G., Ware, H., Subissi, L., Nardone, A., Lewis, H. C., Li, Z., Ma, X., Valenciano, M., Cheng, B., et al. (2022) · PLoS Medicine · doi:10.1371/journal.pmed.1004107 · Cited by 313 · see citing works
SARS-CoV-2 501Y.V2 escapes neutralization by South African COVID-19 donor plasma
Wibmer, C. K., Ayres, F., Hermanus, T., Madzivhandila, M., Kgagudi, P., Oosthuysen, B., Lambson, B. E., de Oliveira, T., Vermeulen, M., van der Berg, K., et al. (2021) · doi:10.1101/2021.01.18.427166
Legros, V., Denolly, S., Vogrig, M., Boson, B., Siret, E., Rigaill, J., Pillet, S., Grattard, F., Gonzalo, S., Verhoeven, P. O., et al. (2021) · Cellular and Molecular Immunology · doi:10.1038/s41423-020-00588-2 · Cited by 297 · see citing works
Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection
Cromer, D., Juno, J. A., Khoury, D., Reynaldi, A., Wheatley, A. K., Kent, S. J., & Davenport, M. P. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-021-00550-x · Cited by 265 · see citing works
Nundy, S., Ghosh, A., Mesloub, A., Albaqawy, G. A., & Alnaim, M. M. (2021) · Journal of Cleaner Production · doi:10.1016/j.jclepro.2021.127705 · Cited by 308 · see citing works
SARS-CoV-2 Variants, Vaccines, and Host Immunity
Mistry, P., Barmania, F., Mellet, J., Peta, K. T., Strydom, A., Viljoen, I. M., James, W., Gordon, S., & Pepper, M. S. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2021.809244 · Cited by 293 · see citing works
Muecksch, F., Wise, H., Batchelor, B., Squires, M., Semple, E., Richardson, C., McGuire, J., Clearly, S., Furrie, E., Greig, N., et al. (2021) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiaa659 · Cited by 308 · see citing works
Not just antibodies: B cells and T cells mediate immunity to COVID-19
Cox, R. J., & Brokstad, K. A. (2020) · Nature reviews. Immunology · doi:10.1038/s41577-020-00436-4 · Cited by 291 · see citing works
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SARS-CoV-2 mRNA Vaccines: Immunological Mechanism and Beyond
Bettini, E., & Locci, M. (2021) · Vaccines · doi:10.3390/vaccines9020147 · Cited by 283 · see citing works
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SARS-CoV-2 mRNA vaccination induces functionally diverse antibodies to NTD, RBD, and S2
Amanat, F., Thapa, M., Lei, T., Ahmed, S. M. S., Adelsberg, D. C., Carreño, J. M., Strohmeier, S., Schmitz, A. J., Zafar, S., Zhou, J. Q., et al. (2021) · Cell · doi:10.1016/j.cell.2021.06.005 · Cited by 273 · see citing works
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Self-citationCorrelation of SARS-CoV-2-breakthrough infections to time-from-vaccine
Mizrahi, B., Lotan, R., Kalkstein, N., Peretz, A., Perez, G., Ben-Tov, A., Chodick, G., Gazit, S., & Patalon, T. (2021) · Nature Communications · doi:10.1038/s41467-021-26672-3 · Cited by 261 · see citing works
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Self-citationPeluso, M. J., Deitchman, A. N., Torres, L., Iyer, N. S., Munter, S. E., Nixon, C. C., Donatelli, J. L., Thanh, C., Takahashi, S., Hakim, J. M. C., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109518 · Cited by 241 · see citing works
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Humoral Responses and Serological Assays in SARS-CoV-2 Infections
Galipeau, Y., Greig, M., Liu, C., Driedger, M., & Langlois, M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.610688 · Cited by 239 · see citing works
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COVID-19 Antibody Tests and Their Limitations
Liu, G., & Rusling, J. F. (2021) · ACS Sensors · doi:10.1021/acssensors.0c02621 · Cited by 219 · see citing works
Writing Committee for the REMAP-CAP Investigators, Abdelhady, H., Abdelrazik, M., Abdi, Z., Abdo, D., Abdulle, A., Abel, L., Abouzeenni, S., Abrahamson, G., Abusamra, Y., et al. (2021) · JAMA · doi:10.1001/jama.2021.18178 · Cited by 212 · see citing works
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Large-Scale Study of Antibody Titer Decay following BNT162b2 mRNA Vaccine or SARS-CoV-2 Infection
Israel, A., Shenhar, Y., Green, I., Merzon, E., Golan‐Cohen, A., Schäffer, A. A., Ruppin, E., Vinker, S., & Magen, E. (2021) · Vaccines · doi:10.3390/vaccines10010064 · Cited by 218 · see citing works
The effect of spike mutations on SARS-CoV-2 neutralization
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Discordant neutralizing antibody and T cell responses in asymptomatic and mild SARS-CoV-2 infection
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Self-citationA simple protein-based surrogate neutralization assay for SARS-CoV-2
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Viral persistence, reactivation, and mechanisms of long COVID
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The humoral response and antibodies against SARS-CoV-2 infection
Qi, H., Liu, B., Wang, X., & Zhang, L. (2022) · Nature Immunology · doi:10.1038/s41590-022-01248-5 · Cited by 188 · see citing works
Decline of Humoral Responses against SARS-CoV-2 Spike in Convalescent Individuals
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The durability of immunity against reinfection by SARS-CoV-2: a comparative evolutionary study
Townsend, J. P., Hassler, H. B., Wang, Z., Miura, S., Singh, J., Kumar, S., Ruddle, N. H., Galvani, A. P., & Dornburg, A. (2021) · The Lancet Microbe · doi:10.1016/s2666-5247(21)00219-6 · Cited by 188 · see citing works
Quick COVID-19 Healers Sustain Anti-SARS-CoV-2 Antibody Production
Chen, Y., Zuiani, A., Fischinger, S., Mullur, J., Atyeo, C. G., Travers, M. E., Lelis, F., Pullen, K. M., Martin, H., Tong, P., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.051 · Cited by 179 · see citing works
Inefficiency of SIR models in forecasting COVID-19 epidemic: a case study of Isfahan
Moein, S., Nickaeen, N., Roointan, A., Borhani, N., Heidary, Z., Javanmard, S. H., Ghaisari, J., & Gheisari, Y. (2021) · Scientific Reports · doi:10.1038/s41598-021-84055-6 · Cited by 181 · see citing works
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Kinetics and correlates of the neutralizing antibody response to SARS-CoV-2 infection in humans
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- 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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