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medRxiv

Dynamics and significance of the antibody response to SARS-CoV-2 infection

Anita S.Iyer,View ORCID ProfileForrest K.Jones,ArianaNodoushani,MeaganKelly,MargaretBecker,DamienSlater,RachelMills,EricaTeng,MohammadKamruzzaman,Wilfredo F.Garcia-Beltran,MichaelAstudillo,DianeYang,Tyler E.Miller,ElizabethOliver,StephanieFischinger,CarolineAtyeo,A. JohnIafrate,Stephen B.Calderwood,Stephen A.Lauer,JingyouYu,ZhenfengLi,JaredFeldman,Blake M.Hauser,Timothy M.Caradonna,John A.Branda,Sarah E.Turbett,Regina C.LaRocque,GuillaumeMellon,Dan H.Barouch,Aaron G.Schmidt,Andrew S.Azman,GalitAlter,Edward TRyan,Jason B.Harris,Richelle C.Charles
doi: https://doi.org/10.1101/2020.07.18.20155374
Anita S. Iyer
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
bDepartment of Medicine, Harvard Medical School, Boston, MA,USA
Forrest K. Jones
cDepartment of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD,USA
Ariana Nodoushani
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
Meagan Kelly
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
Margaret Becker
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
Damien Slater
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
Rachel Mills
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
Erica Teng
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
Mohammad Kamruzzaman
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
Wilfredo F. Garcia-Beltran
dDepartment of Pathology, Massachusetts General Hospital, Boston, MA,USA
Michael Astudillo
dDepartment of Pathology, Massachusetts General Hospital, Boston, MA,USA
Diane Yang
dDepartment of Pathology, Massachusetts General Hospital, Boston, MA,USA
Tyler E. Miller
dDepartment of Pathology, Massachusetts General Hospital, Boston, MA,USA
Elizabeth Oliver
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
Stephanie Fischinger
eRagon Institute of MGH, MIT, and Harvard, Cambridge, MA,USA
Caroline Atyeo
eRagon Institute of MGH, MIT, and Harvard, Cambridge, MA,USA
A. John Iafrate
dDepartment of Pathology, Massachusetts General Hospital, Boston, MA,USA
Stephen B. Calderwood
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
bDepartment of Medicine, Harvard Medical School, Boston, MA,USA
fDepartment of Microbiology, Harvard Medical School, Boston, MA,USA
Stephen A. Lauer
cDepartment of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD,USA
Jingyou Yu
gCenter for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA,USA
Zhenfeng Li
gCenter for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA,USA
Jared Feldman
eRagon Institute of MGH, MIT, and Harvard, Cambridge, MA,USA
Blake M. Hauser
eRagon Institute of MGH, MIT, and Harvard, Cambridge, MA,USA
Timothy M. Caradonna
eRagon Institute of MGH, MIT, and Harvard, Cambridge, MA,USA
John A. Branda
dDepartment of Pathology, Massachusetts General Hospital, Boston, MA,USA
Sarah E. Turbett
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
bDepartment of Medicine, Harvard Medical School, Boston, MA,USA
dDepartment of Pathology, Massachusetts General Hospital, Boston, MA,USA
Regina C. LaRocque
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
bDepartment of Medicine, Harvard Medical School, Boston, MA,USA
Guillaume Mellon
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
Dan H. Barouch
eRagon Institute of MGH, MIT, and Harvard, Cambridge, MA,USA
gCenter for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA,USA
Aaron G. Schmidt
eRagon Institute of MGH, MIT, and Harvard, Cambridge, MA,USA
fDepartment of Microbiology, Harvard Medical School, Boston, MA,USA
Andrew S. Azman
cDepartment of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD,USA
Galit Alter
eRagon Institute of MGH, MIT, and Harvard, Cambridge, MA,USA
Edward T Ryan
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
bDepartment of Medicine, Harvard Medical School, Boston, MA,USA
hDepartment of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA,USA
Jason B. Harris
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
iDepartment of Pediatrics, Harvard Medical School, Boston, MA,USA
Richelle C. Charles
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, MA,USA
bDepartment of Medicine, Harvard Medical School, Boston, MA,USA
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ABSTRACT

BACKGROUND Characterizing the humoral immune response to SARS-CoV-2 and developing accurate serologic assays are needed for diagnostic purposes and estimating population-level seroprevalence.

METHODS We measured the kinetics of early antibody responses to the receptor-binding domain (RBD) of the spike (S) protein of SARS-CoV-2 in a cohort of 259 symptomatic North American patients infected with SARS-CoV-2 (up to 75 days after symptom onset) compared to antibody levels in 1548 individuals whose blood samples were obtained prior to the pandemic.

RESULTS Between 14-28 days from onset of symptoms, IgG, IgA, or IgM antibody responses to RBD were all accurate in identifying recently infected individuals, with 100% specificity and a sensitivity of 97%, 91%, and 81% respectively. Although the estimated median time to becoming seropositive was similar across isotypes, IgA and IgM antibodies against RBD were short-lived with most individuals estimated to become seronegative again by 51 and 47 days after symptom onset, respectively. IgG antibodies against RBD lasted longer and persisted through 75 days post-symptoms. IgG antibodies to SARS-CoV-2 RBD were highly correlated with neutralizing antibodies targeting the S protein. No cross-reactivity of the SARS-CoV-2 RBD-targeted antibodies was observed with several known circulating coronaviruses, HKU1, OC 229 E, OC43, and NL63.

CONCLUSIONS Among symptomatic SARS-CoV-2 cases, RBD-targeted antibodies can be indicative of previous and recent infection. IgG antibodies are correlated with neutralizing antibodies and are possibly a correlate of protective immunity.

Competing Interest Statement

JAB has been a consultant for T2 Biosystems, DiaSorin and Roche Diagnostics

Clinical Protocols

https://www.protocols.io/view/sars-cov-2-rbd-elisa-bikbkcsn

Funding Statement

This work was supported in part by Centers for Disease Control and Prevention (U01CK000490 to E.T.R, R.C.L., R.C.C, J.B.H, G.M., E.O., S.E.T.), the National Institutes of Health (R01 AI146779 to A.G.S; T32 GM007753 to B.M.H and T.M.C.; T32 AI007245 to J.F) and MassCPR grant to A.G.S.

Author Declarations

I confirm all relevant ethical guidelines have been followed, and any necessary IRB and/or ethics committee approvals have been obtained.

Yes

The details of the IRB/oversight body that provided approval or exemption for the research described are given below:

All research was approved by the Institutional Review Board for Human Subjects Research at Massachusetts General Hospital.

All necessary patient/participant consent has been obtained and the appropriate institutional forms have been archived.

Yes

I understand that all clinical trials and any other prospective interventional studies must be registered with an ICMJE-approved registry, such as ClinicalTrials.gov. I confirm that any such study reported in the manuscript has been registered and the trial registration ID is provided (note: if posting a prospective study registered retrospectively, please provide a statement in the trial ID field explaining why the study was not registered in advance).

Yes

I have followed all appropriate research reporting guidelines and uploaded the relevant EQUATOR Network research reporting checklist(s) and other pertinent material as supplementary files, if applicable.

Yes

Data Availability

We plan to make the data available on Zenodo and at the GitHub repository with the link below after publication.

https://github.com/fjones2222/covid19-serodynamics

Copyright 
The copyright holder for this preprint is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license.
Posted July 20, 2020.
Email
Dynamics and significance of the antibody response to SARS-CoV-2 infection
Anita S.Iyer,Forrest K.Jones,ArianaNodoushani,MeaganKelly,MargaretBecker,DamienSlater,RachelMills,EricaTeng,MohammadKamruzzaman,Wilfredo F.Garcia-Beltran,MichaelAstudillo,DianeYang,Tyler E.Miller,ElizabethOliver,StephanieFischinger,CarolineAtyeo,A. JohnIafrate,Stephen B.Calderwood,Stephen A.Lauer,JingyouYu,ZhenfengLi,JaredFeldman,Blake M.Hauser,Timothy M.Caradonna,John A.Branda,Sarah E.Turbett,Regina C.LaRocque,GuillaumeMellon,Dan H.Barouch,Aaron G.Schmidt,Andrew S.Azman,GalitAlter,Edward TRyan,Jason B.Harris,Richelle C.Charles
medRxiv2020.07.18.20155374;doi: https://doi.org/10.1101/2020.07.18.20155374
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