Persistence of serum and saliva antibody responses to SARS-CoV-2 spike antigens in COVID-19 patients

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Abstract

Saliva is an alternative biofluid to serum for detecting and monitoring IgG to SARS-CoV-2 spike and RBD antigens in COVID-19.

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  1. SciScore for 10.1101/2020.08.01.20166553: (What is this?)

    Please note, not all rigor criteria are appropriate for all manuscripts.

    Table 1: Rigor

    Institutional Review Board StatementConsent: Consecutive out-patients diagnosed at the same 4 hospitals prior to March 15th and on a convenience sample of later days were approached for consent to collect serum and saliva at 4–12 weeks PSO.
    IRB: All samples were collected after Research Ethics Board (REB) review (see Sample section above for the individual REB approval numbers).
    RandomizationNo randomization was performed, since this is an observational study.
    Blindingnot detected.
    Power Analysisnot detected.
    Sex as a biological variablenot detected.
    Cell Line Authenticationnot detected.

    Table 2: Resources

    Antibodies
    SentencesResources
    This observational study focused on monitoring the levels of antibodies to SARS-CoV-2 antigens in serum and saliva of patients with confirmed SARS-CoV-2 infection.
    SARS-CoV-2
    suggested: None
    After washing 4 times, 10 μl of one of the following secondary antibodies (all from Jackson ImmunoResearch) diluted in 1% BLOTTO in PBS-T were added at the indicated concentrations followed by incubation for 2 hr at room temperature: Goat anti-human IgG Fcy – HRP (#109-035-098; 1:40,000 or 0.2 ng per well), Goat anti-human IgM Fc5u – HRP (#109035-129; 1:12,000 or 0.66 ng per well) or Goat anti-human IgA a chain – HRP (#109-035-127; 1:10,000 or 0.8 ng per well).
    anti-human IgG
    suggested: (Jackson ImmunoResearch Labs Cat# 109-035-098, RRID:AB_2337586)
    anti-human IgM
    suggested: (Jackson ImmunoResearch Labs Cat# 109-035-129, RRID:AB_2337588)
    anti-human IgA
    suggested: None
    Antibodies used for the standard curves were: Human anti-spike S1 IgG (A02038, GenScript), anti-spike S1 IgM (A02046, GenScript) and Ab01680 anti-spike IgA (Ab01680-16, Absolute Antibody), all used at 0.5 to 10ng per well.
    anti-spike S1 IgG
    suggested: None
    A02038
    suggested: None
    anti-spike S1 IgM
    suggested: None
    A02046
    suggested: (GenWay Biotech Inc. Cat# GWB-A02046, RRID:AB_10276779)
    anti-spike IgA
    suggested: None
    Anti-human Ig antibody (Southern Biotech, 2010–01) diluted 1:1000 in PBS was added to 96-well Nunc MaxiSorp™ plates (ThermoFisher, 44-2404-21).
    Anti-human Ig antibody
    suggested: None
    Anti-human Ig
    suggested: None
    HRP-conjugated secondary antibodies against IgA, IgG, and IgM (goat anti-human IgA- and IgG-HRP, Southern Biotech, IgA: 2053–05, IgG: 2044–05, IgM: 2023–05) were added to the appropriate wells at 1:1000 in 2.5% BLOTTO and incubated for 1 hour at 37°C.
    HRP-conjugated secondary antibodies against IgA, IgG, and IgM (goat anti-human IgA- and IgG-HRP, Southern Biotech, IgA: 2053–05, IgG: 2044–05, IgM: 2023–05)
    suggested: None
    HRP-conjugated secondary antibodies against IgA, IgG
    suggested: None
    goat anti-human IgA-
    suggested: (InvivoGen Cat# fab-iga, RRID:AB_11125122)
    Horseradish peroxidase (HRP)-conjugated Goat anti human-IgG, IgA, and anti-IgM secondary antibodies (Southern Biotech, IgG: 2044–05, IgA: 2053–05, IgM: 2023–05) were added to wells at dilutions of 1:1000, 1:2000 and 1:1000 in 2.5% BLOTTO, respectively, and incubated for 1 hour at 37°C.
    anti human-IgG, IgA,
    suggested: None
    anti human-IgG, IgA
    suggested: None
    anti-IgM
    suggested: (SouthernBiotech Cat# 2023-01, RRID:AB_2795619)
    For serum samples, seven multivariable linear regression models were constructed (one for each of anti-RBD IgA, anti-S IgA, anti-RBD IgG, anti-S IgG, anti-RBD IgM, anti-spike IgM, neutralizing antibody).
    anti-RBD IgA
    suggested: None
    anti-S IgA
    suggested: None
    anti-RBD IgG
    suggested: None
    anti-S IgG
    suggested: None
    anti-RBD IgM
    suggested: None
    anti-spike IgM
    suggested: None
    Development and validation of manual colorimetric and automated chemiluminescent assays for monitoring RBD and spike trimers antibodies in serum or plasma. Fig. S2.
    S2
    suggested: None
    Effect of heat versus detergent inactivation of saliva samples on the detection of anti-RBD antibodies in a manual, colourimetric ELISA. Fig. S5.
    anti-RBD
    suggested: None
    S5
    suggested: None
    Experimental Models: Cell Lines
    SentencesResources
    To stabilize the spike protein in a trimeric form, the cDNA was cloned in-frame with the human resistin cDNA (aa 23–108) containing a C-terminal FLAG-(His)6 tag (Cricetulus griseus codon bias, GenScript) into a modified cumate-inducible pTT241 expression plasmid and transfected in CHO2353 cells (Stuible et al, manuscript in preparation) followed by methionine sulfoximine selection for 14 days to generate a stable CHO pool.
    CHO2353
    suggested: None
    Viral stock was expanded using Vero E6 as previously described such that stored aliquots of stock contain 2% FBS.
    Vero E6
    suggested: RRID:CVCL_XD71)
    Initial experiments were done with Triton X-100 (Sigma-Aldrich) serially diluted and applied to Vero-E6 cells in 96-well flat bottom plates to determine the minimum concentration required to prevent toxicity to cells.
    Vero-E6
    suggested: None
    Software and Algorithms
    SentencesResources
    Spike trimer was expressed as follows: the SARS-CoV-2 spike sequence (aa 1–1208 from Genebank accession number MN908947 with the S1/S2 furin site (residues 682–685) mutated [RRAR->GGAS] and K986P / V987P stabilizing mutations was codon-optimized (Cricetulus griseus codon bias) and synthesized by Genscript.
    Genebank
    suggested: None
    These analyses were performed in Prism (GraphPad), Version 8.3.
    Prism
    suggested: (PRISM, RRID:SCR_005375)
    References and Notes:
    Notes
    suggested: None

    Results from OddPub: We did not detect open data. We also did not detect open code. Researchers are encouraged to share open data when possible (see Nature blog).


    Results from LimitationRecognizer: An explicit section about the limitations of the techniques employed in this study was not found. We encourage authors to address study limitations.

    Results from TrialIdentifier: No clinical trial numbers were referenced.


    Results from Barzooka: We did not find any issues relating to the usage of bar graphs.


    Results from JetFighter: We did not find any issues relating to colormaps.


    Results from rtransparent:
    • Thank you for including a conflict of interest statement. Authors are encouraged to include this statement when submitting to a journal.
    • Thank you for including a funding statement. Authors are encouraged to include this statement when submitting to a journal.
    • No protocol registration statement was detected.

    About SciScore

    SciScore is an automated tool that is designed to assist expert reviewers by finding and presenting formulaic information scattered throughout a paper in a standard, easy to digest format. SciScore checks for the presence and correctness of RRIDs (research resource identifiers), and for rigor criteria such as sex and investigator blinding. For details on the theoretical underpinning of rigor criteria and the tools shown here, including references cited, please follow this link.

  2. SciScore for 10.1101/2020.08.01.20166553: (What is this?)

    Please note, not all rigor criteria are appropriate for all manuscripts.

    Table 1: Rigor

    Institutional Review Board StatementConsecutive out-patients diagnosed at the same 4 hospitals prior to March 15th and on a convenience sample of later days were approached for consent to collect serum and saliva at 412 weeks post onset of symptoms.Randomizationnot detected.Blindingnot detected.Power Analysisnot detected.Sex as a biological variablenot detected.Cell Line Authenticationnot detected.

    Table 2: Resources

    Antibodies
    SentencesResources
    After washing 4 times, 10 µl of one of the following secondary antibodies (all from Jackson ImmunoResearch) diluted in 1% BLOTTO in PBS-T were added at the indicated concentrations followed by incubation for 2 hr at room temperature: Goat anti-human IgG Fcy – 035-129; 1:12,000 or 0.66 ng per well) or Goat anti-human IgA a chain - HRP (#109-035-127; 1:10,000 or 0.8 ng per well).
    anti-human IgG
    suggested: (Jackson ImmunoResearch Labs Cat# 109-035-127, RRID:AB_2337587)
    anti-human IgA
    suggested: None
    Antibodies used for the standard curves were: Human anti-spike S1 IgG (A02038, GenScript), anti-spike S1 IgM (A02046, GenScript) and Ab01680 anti-spike IgA (Ab01680-16, Absolute Antibody), all used at 0.5 to 10ng per well.
    anti-spike S1 IgG
    suggested: None
    A02038
    suggested: None
    anti-spike S1 IgM
    suggested: None
    A02046
    suggested: (GenWay Biotech Inc. Cat# GWB-A02046, RRID:AB_10276779)
    anti-spike IgA
    suggested: None
    Anti-human Ig antibody (Southern Biotech, 2010-01) diluted 1:1000 in PBS was added to 96-well Nunc MaxiSorp™ plates (ThermoFisher, 44-2404-21).
    Anti-human Ig antibody
    suggested: (SouthernBiotech Cat# 2010-01, RRID:AB_2687525)
    Anti-human Ig
    suggested: (SouthernBiotech Cat# 2010-01, RRID:AB_2687525)
    HRP-conjugated secondary antibodies against IgA and IgG (goat anti-human IgA- and IgG-HRP, Southern Biotech, IgA: 2053-05, IgG: 2044-05) were added to the appropriate wells at 1:1000 in 2.5% BLOTTO and incubated for 1 hour at 37oC.
    HRP-conjugated secondary antibodies against IgA and IgG (goat anti-human IgA- and IgG-HRP, Southern Biotech, IgA: 2053-05, IgG: 2044-05)
    suggested: None
    HRP-conjugated secondary antibodies against IgA and IgG
    suggested: None
    goat anti-human IgA-
    suggested: (InvivoGen Cat# hrp-iga, RRID:AB_11124937)
    Horseradish peroxidase (HRP)-conjugated Goat anti human-IgA and anti-IgG secondary antibodies (Southern Biotech, 2053-05 and 2044-05) were added to wells at dilutions of 1:2000 and 1:1000 in 2.5% BLOTTO, respectively, and incubated for 1 hour at 37oC.
    Goat anti human-IgA
    suggested: None
    anti human-IgA
    suggested: None
    anti-IgG
    suggested: None
    Experimental Models: Cell Lines
    SentencesResources
    To stabilize the spike protein in a trimeric form, the cDNA was cloned in-frame with the human resistin cDNA (aa 23-108) containing a Cterminal FLAG-(His)6 tag (Cricetulus griseus codon bias, GenScript) into a modified cumateinducible pTT241 expression plasmid and transfected in CHO2353 cells (Stuible et al.,
    CHO2353
    suggested: None
    Viral stock was expanded using Vero E6 as previously described such that stored aliquots of stock contain 2% FBS.
    Vero E6
    suggested: RRID:CVCL_XD71)
    Initial experiments were done with Triton X-100 (Sigma-Aldrich) serially diluted and applied to Vero-E6 cells in 96-well flat bottom plates to determine the minimum concentration required to prevent toxicity to cells.
    Vero-E6
    suggested: None
    Software and Algorithms
    SentencesResources
    Antigen production – serum assays Spike trimer was expressed as follows: the SARS-CoV-2 spike sequence (aa 1-1208 from Genebank accession number MN908947 with the S1/S2 furin site (residues 682–685) mutated [RRAR->GGAS] and K986P / V987P stabilizing mutations was codon-optimized (Cricetulus griseus codon bias) and synthesized by Genscript.
    Genebank
    suggested: None
    A fourparameter logistic curve was used to determine the line of best fit for the standard curve, and sample Ig quantities were interpolated accordingly, using Prism Graphpad, Version 8.3.
    Graphpad
    suggested: (GraphPad, RRID:SCR_000306)
    All analysis was performed in SAS 9.4M6 (SAS Institute, Cary, NC).
    SAS Institute
    suggested: (Statistical Analysis System, RRID:SCR_008567)

    Results from OddPub: We did not detect open data. We also did not detect open code. Researchers are encouraged to share open data when possible (see Nature blog).


    Results from LimitationRecognizer: An explicit section about the limitations of the techniques employed in this study was not found. We encourage authors to address study limitations.


    Results from Barzooka: We did not find any issues relating to the usage of bar graphs.


    Results from JetFighter: We did not find any issues relating to colormaps.


    About SciScore

    SciScore is an automated tool that is designed to assist expert reviewers by finding and presenting formulaic information scattered throughout a paper in a standard, easy to digest format. SciScore checks for the presence and correctness of RRIDs (research resource identifiers), and for rigor criteria such as sex and investigator blinding. For details on the theoretical underpinning of rigor criteria and the tools shown here, including references cited, please follow this link.