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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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BackgroundThe association between obesity and peak antibody titer response in COVID‐19 infection
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“Some of the recoverees tend to have robust and long lasting immunity while others display a waning of their neutralizing antibodies [6,11].”
BackgroundSARS-CoV-2 Seroprevalence in Household Domestic Ferrets (Mustela putorius furo)
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“In COVID-19, kinetics of the neutralizing antibody response is typical of an acute viral infection, with declining neutralizing antibody titers observed after an initial peak, which depends on disease severity (6).”
BackgroundMultiplexed, quantitative serological profiling of COVID-19 from blood by a point-of-care test
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Multidisciplinary Center Care for Long COVID Syndrome–A Retrospective Cohort Study
Bailey, J. I., Lavelle, B., Miller, J. L., Jimenez, M., Lim, P. H., Orban, Z. S., Clark, J. R., TOMAR, R., Ludwig, A., Ali, S. T., et al. (2023) · The American Journal of Medicine · doi:10.1016/j.amjmed.2023.05.002 · Cited by 55
SARS-CoV-2 population-based seroprevalence studies in Europe: a scoping review
Grant, R., Dub, T., Andrianou, X. D., Nohynek, H., Wilder‐Smith, A., Pezzotti, P., & Fontanet, A. L. (2021) · BMJ Open · doi:10.1136/bmjopen-2020-045425 · Cited by 49
Buonfrate, D., Piubelli, C., Gobbi, F. G., Martini, D., Bertoli, G., Ursini, T., Moro, L., Ronzoni, N., Angheben, A., Rodari, P., et al. (2021) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2021.07.024 · Cited by 50
Lee, H., Knabl, L., Moliva, J. I., Knabl, L., Werner, A. P., Boyoglu-Barnum, S., Kapferer, S., Pateter, B., Walter, M., Sullivan, N. J., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110680 · Cited by 47
Brazeau, N. F., Verity, R., Jenks, S. J., Fu, H. J., Whittaker, C., Winskill, P., Dorigatti, I., Walker, P. G. T., Riley, S., Schnekenberg, R. P., et al. (2022) · Communications Medicine · doi:10.1038/s43856-022-00106-7 · Cited by 50
SARS-CoV-2 evolution influences GBP and IFITM sensitivity
Mesner, D., Reuschl, A., Whelan, M. V. X., Bronzovich, T., Haider, T., Thorne, L., Ragazzini, R., Bonfanti, P., Towers, G. J., & Jolly, C. L. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2212577120 · Cited by 54
Protection against reinfection with D614- or G614-SARS-CoV-2 isolates in golden Syrian hamster
Brustolin, M., Rodon, J., de la Concepción, M. L. R., Ávila‐Nieto, C., Cantero, G., Pérez, M., Te, N., Noguera-Julián, M., Guallar, V., Valencia, A., et al. (2021) · Emerging Microbes & Infections · doi:10.1080/22221751.2021.1913974 · Cited by 50
Ansari, A., Arya, R. K., Sachan, S., Jha, S. N., Kalia, A., Lall, A., Sette, A., Grifoni, A., Weiskopf, D., Coshic, P., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.636768 · Cited by 50
“However, there has been a concern over the decline of antibodies within first few months after SARS-CoV-2 infection (12, 13).”
BackgroundDiagnostics and analysis of SARS-CoV-2: current status, recent advances, challenges and perspectives
Dong, T., Wang, M., Liu, J., Ma, P., Pang, S., Liu, W., & Liu, A. (2023) · Chemical Science · doi:10.1039/d2sc06665c · Cited by 50
Dalai, S. C., Dines, J. N., Snyder, T. M., Gittelman, R., Newman-Eerkes, T., Vaney, P., Howard, S., Akers, K., Skewis, L. R., Monteforte, A. J., et al. (2022) · Clinical Infectious Diseases · doi:10.1093/cid/ciac353 · Cited by 49
Muecksch, F., Wise, H. M., Templeton, K. E., Batchelor, B., Squires, M., McCance, K., JARVIS, L. M., Malloy, K., Furrie, E., Richardson, C., et al. (2022) · The Lancet Microbe · doi:10.1016/s2666-5247(22)00090-8 · Cited by 48
Plausibility of a third wave of COVID-19 in India
Mandal, S., Arinaminpathy, N., Bhargava, B., & Panda, S. (2021) · The Indian Journal of Medical Research · doi:10.4103/ijmr.ijmr_1627_21 · Cited by 50
Targeting intra-viral conserved nucleocapsid (N) proteins as novel vaccines against SARS-CoVs
Thura, M., Sng, J., Ang, K. H., Li, J., Gupta, A. K., Hong, J. M., Hong, C. W., & Zeng, Q. (2021) · Bioscience Reports · doi:10.1042/bsr20211491 · Cited by 48
Shervani, Z., Khan, I., Khan, T., & Qazi, U. Y. (2020) · Advances in Infectious Diseases · doi:10.4236/aid.2020.103020 · Cited by 48
Complement Factors in COVID-19 Therapeutics and Vaccines
Kurtovic, L., & Beeson, J. G. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.12.002 · Cited by 47
“antibodies are also thought to contribute to protective immunity [28].”
Goh, Y. S., Chavatte, J., Jieling, A. L., Lee, B. T. K., Hor, P. X., Amrun, S. N., Lee, C. Y., Chee, R. S., Wang, B., Lee, C. Y., et al. (2020) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100193 · Cited by 48
“32–35 Although there is likely a decrease in IgG levels over time, 36,37 it is also possible that the lack of IgG binding could be, in part, due to a prozone effect.”
Immunologic memory to SARS-CoV-2 in convalescent COVID-19 patients at 1 year postinfection
Hou, H., Zhang, Y., Tang, G., Luo, Y., Liu, W., Cheng, C., Jiang, Y., Xiong, Z., Wu, S., Sun, Z., et al. (2021) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2021.09.008 · Cited by 49
“However, nAb titers gradually decline after an initial peak in convalescent patients, and most convalescent plasma samples obtained from individuals who recover from COVID-19 do not contain high levels of neutralizing activity.(11,12) Notably, nAb titers are positively correlated with COVID-19 severity.”
BackgroundResultMoustafa, J. S. E.-S., Jackson, A., Brotman, S. M., Guan, L., Villicaña, S., Roberts, A. L., Zito, A., Bonnycastle, L. L., Erdos, M. R., Narisu, N., et al. (2022) · International Journal of Obesity · doi:10.1038/s41366-022-01136-w · Cited by 48
“Presence of immunoglobulin G (IgG) to SARS-CoV-2 nucleoprotein (N) and spike (S) in serum from TwinsUK participants was measured using ELISA as previously described [42, 43].”
Self-citationSARS-CoV-2 Proteome-Wide Analysis Revealed Significant Epitope Signatures in COVID-19 Patients
Schwarz, T., Heiß, K., Mahendran, Y., Casilag, F., Kurth, F., Sander, L. E., Wendtner, C., Hoechstetter, M. A., Müller, M. A., Sekul, R., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.629185 · Cited by 45
“In general, there are reports demonstrating that antibody titers are higher in patients with severe disease (23, 33, 37, 40, 66, 67), however others show the contrary (68).”
Seo, Y. B., Suh, Y. S., Ryu, J. I., Jang, H., Oh, H., Koo, B., Seo, S. H., Hong, J. J., Song, M., Kim, S.-J., et al. (2021) · Vaccines · doi:10.3390/vaccines9040307 · Cited by 48
Follicular Helper T Cells in the Immunopathogenesis of SARS-CoV-2 Infection
Cui, D., Tang, Y., Jiang, Q., Jiang, D., Zhang, Y., Lv, Y., Xu, D., Wu, J., Xie, J., Wen, C., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.731100 · Cited by 47
Castillo‐Olivares, J., Wells, D. A., Ferrari, M., Chan, A. C. Y., Smith, P., Nadesalingam, A., Paloniemi, M., Carnell, G., Ohlendorf, L., Cantoni, D. M., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.748291 · Cited by 42
“Consistent with published data (8, 11, 43, 44), we found a very strong correlation between nAb, as measured by the pMN assay, and severity of disease.”
ResultSelf-citationAtti, A., Insalata, F., Carr, E. J., Otter, A. D., Castillo‐Olivares, J., Wu, M., Harvey, R., Howell, M. T., Chan, A., Lyall, J., et al. (2022) · Journal of Infection · doi:10.1016/j.jinf.2022.09.004 · Cited by 45
Self-citationBalachandran, H., Phetsouphanh, C., Agapiou, D., Adhikari, A., Rodrigo, C., Hammoud, M., Shrestha, L. B., Keoshkerian, E., Gupta, M., Turville, S. G., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110345 · Cited by 45
“Following acute infection, neutralizing antibody titers decline significantly during the convalescent phase and continue to slowly decline 3–8 months postinfection (Abayasingam et al., 2021; Sakharkar et al., 2021; Seow et al., 2020).”
BackgroundInfluentialSeow, J., Khan, H., Rosa, A., Calvaresi, V., Graham, C., Pickering, S., Pye, V. E., Cronin, N., Huettner, I., Malim, M. H., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111276 · Cited by 41
Self-citationSARS-CoV-2 Antigens Expressed in Plants Detect Antibody Responses in COVID-19 Patients
Makatsa, M. S., Tincho, M. B., Wendoh, J. M., Ismail, S. D., Nesamari, R., Pêra, F. F. P. G., Beer, S., David, A., Jugwanth, S., Gededzha, M. P., et al. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.589940 · Cited by 49
Seroprevalence of SARS-CoV-2 Antibodies Among Children in School and Day Care in Montreal, Canada
Zinszer, K., McKinnon, B., Bourque, N., Pierce, L., Saucier, A., Otis, A., Cheriet, I., Papenburg, J., Hamelin, M., Charland, K., et al. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2021.35975 · Cited by 46
SARS-CoV-2 antibody testing for estimating COVID-19 prevalence in the population
Vogl, T. J., Leviatan, S., & Segal, E. (2021) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100191 · Cited by 44
Dogra, P., Ruiz-Ramírez, J., Sinha, K., Butner, J. D., Peláez, M. J., Rawat, M., Yellepeddi, V., Pasqualini, R., Arap, W., Sostman, H. D., et al. (2020) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.0c00183 · Cited by 45
Cook, A. M., Faustini, S. E., Williams, L. J., Cunningham, A. F., Drayson, M. T., Shields, A. M., Kay, D., Taylor, L., Plant, T., Huissoon, A. P., et al. (2021) · Journal of Immunological Methods · doi:10.1016/j.jim.2021.113046 · Cited by 42
Harrington, P., de Lavallade, H., Doores, K. J., O’Reilly, A., Seow, J., Graham, C., Lechmere, T., Radia, D. H., Dillon, R. J., Shanmugharaj, Y., et al. (2021) · Leukemia · doi:10.1038/s41375-021-01300-7 · Cited by 44
Self-citationDorigatti, I., Lavezzo, E., Manuto, L., Ciavarella, C., Pacenti, M., Boldrin, C., Cattai, M., Saluzzo, F., Franchin, E., Vecchio, C. D., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24622-7 · Cited by 44
Chen, J., Liu, X., Zhang, X., Lin, Y., Liu, D., Xun, J., Wang, Z., Gu, L., Li, Q., Yin, D., et al. (2021) · Clinical & Translational Immunology · doi:10.1002/cti2.1319 · Cited by 44
“Recent studies also revealed that the neutralising antibody waned after the titre peaked, which was detected 3–4 weeks after infection.(6,21) Taken together, these results support the notion that the humoral response against SARS-CoV-2 is a typical response after an acute viral infection.”
ResultSARS-CoV-2 reinfection in patients negative for immunoglobulin G following recovery from COVID-19
Ali, A. M., Ali, K., Fatah, M. H., Tawfeeq, H. M., & Rostam, H. M. (2021) · New Microbes and New Infections · doi:10.1016/j.nmni.2021.100926 · Cited by 46
Montesinos, I., Dahma, H., Wolff, F., Dauby, N., Delaunoy, S., Wuyts, M., Detemmerman, C., Duterme, C., Vandenberg, O., Martin, C., et al. (2021) · Journal of Clinical Virology · doi:10.1016/j.jcv.2021.104988 · Cited by 44
A point-of-care lateral flow assay for neutralising antibodies against SARS-CoV-2
Fulford, T. S., Văn, H. T., Gherardin, N. A., Zheng, S., Ciula, M., Drummer, H. E., Redmond, S. J., Tan, H., Boo, I., Li, F., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103729 · Cited by 47
Havervall, S., Falk, A. J., Klingström, J., Ng, H., Greilert‐Norin, N., Gabrielsson, L., Salomonsson, A., Isaksson, E., Rudberg, A., Hellström, C., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0262169 · Cited by 45
Hong, L., Alu, A., Yang, J., Ren, W., He, C., Lan, T., He, X., Yang, L., Li, J., Wang, Z., et al. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01002-1 · Cited by 43
COVID ‐19 and plasma cells: Is there long‐lived protection?*
Nguyen, D. C., Lamothe, P. A., Woodruff, M. C., Saini, A. S., Faliti, C. E., Sanz, I., & Lee, F. E.-H. (2022) · Immunological Reviews · doi:10.1111/imr.13115 · Cited by 48
Mucosal immunity to severe acute respiratory syndrome coronavirus 2 infection
Fröberg, J., & Diavatopoulos, D. A. (2021) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0000000000000724 · Cited by 45
The impact of Spike mutations on SARS-CoV-2 neutralizationPreprint
Rees-Spear, C., Muir, L., Griffith, S. A., Heaney, J., Aldon, Y., Snitselaar, J. L., Pataillot-Meakin, T., Graham, C., Seow, J., Lee, N., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.15.426849 · Cited by 45
Self-citation
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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