0
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Comparative analysis of eleven SARS-CoV-2 immunoassays and neutralisation data: time to enhance standardisation and correlation of protection

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, , ORCID Icon, , , ORCID Icon, , , ORCID Icon & ORCID Icon show all
Received 15 Nov 2023, Accepted 15 Jul 2024, Published online: 24 Jul 2024

References

  • Addetia A, Crawford KHD, Dingens A, et al. Neutralizing antibodies correlate with protection from SARS-CoV-2 in humans during a fishery vessel outbreak with a high attack rate. J Clin Microbiol. 2020;58(11):e02107-20. doi: 10.1128/jcm.02107-20.
  • Houlihan CF, Beale R. The complexities of SARS-CoV-2 serology. Lancet Infect Dis. 2020;20(12):1350–1351. doi: 10.1016/S1473-3099(20)30699-X.
  • Weidner L, Gänsdorfer S, Unterweger S, et al. Quantification of SARS-CoV-2 antibodies with eight commercially available immunoassays. J Clin Virol. 2020;129:104540–104540. doi: 10.1016/j.jcv.2020.104540.
  • Carter JA, Freedenberg AT, Romeiser JL, et al. Impact of serological and PCR testing requirements on the selection of COVID-19 convalescent plasma donors. Transfusion. 2021;61(5):1461–1470. doi: 10.1111/trf.16293.
  • SARS-CoV-2 vaccines | vaccination | JAMA | JAMA Network.; n.d. [cited 2022 Jun 27]. Available from: https://jamanetwork.com/journals/jama/article-abstract/2777059.
  • Min L, Sun Q. Antibodies and vaccines target RBD of SARS-CoV-2. Front Mol Biosci. 2021;8:671633. doi: 10.3389/fmolb.2021.671633.
  • Li T, Wang L, Wang H, et al. Serum SARS-COV-2 nucleocapsid protein: a sensitivity and specificity early diagnostic marker for SARS-COV-2 infection. Front Cell Infect Microbiol. 2020;10:470. doi: 10.3389/fcimb.2020.00470.
  • Mazzini L, Martinuzzi D, Hyseni I, et al. Comparative analyses of SARS-CoV-2 binding (IgG, IgM, IgA) and neutralizing antibodies from human serum samples. J Immunol Methods. 2021;489:112937. doi: 10.1016/j.jim.2020.112937.
  • Khoury DS, Cromer D, Reynaldi A, et al. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat Med. 2021;27(7):1205–1211. doi: 10.1038/s41591-021-01377-8.
  • Chi W-Y, Li Y-D, Huang H-C, et al. COVID-19 vaccine update: vaccine effectiveness, SARS-CoV-2 variants, boosters, adverse effects, and immune correlates of protection. J Biomed Sci. 2022;29(1):82. doi: 10.1186/s12929-022-00853-8.
  • Earle KA, Ambrosino DM, Fiore-Gartland A, et al. Evidence for antibody as a protective correlate for COVID-19 vaccines. Vaccine. 2021;39(32):4423–4428. doi: 10.1016/j.vaccine.2021.05.063.
  • Goldblatt D, Alter G, Crotty S, et al. Correlates of protection against SARS-CoV-2 infection and COVID-19 disease. Immunol Rev. 2022;310(1):6–26. doi: 10.1111/imr.13091.
  • Khoury DS, Schlub TE, Cromer D, et al. Correlates of protection, thresholds of protection, and immunobridging among persons with SARS-CoV-2 infection. Emerg Infect Dis. 2023;29(2):381–388. doi: 10.3201/eid2902.221422.
  • Lukaszuk K, Kiewisz J, Rozanska K, et al. Usefulness of IVD Kits for the Assessment of SARS-CoV-2 Antibodies to Evaluate the Humoral Response to Vaccination. Vaccines (Basel). 2021;9(8):840. doi: 10.3390/vaccines9080840.
  • Leuzinger K, Osthoff M, Dräger S, et al. Comparing immunoassays for SARS-CoV-2 antibody detection in patients with and without laboratory-confirmed SARS-CoV-2 infection. J Clin Microbiol. 2021;59(12):e0138121. doi: 10.1128/JCM.01381-21.
  • Trabaud M-A, Icard V, Milon M-P, et al. Comparison of eight commercial, high-throughput, automated or ELISA assays detecting SARS-CoV-2 IgG or total antibody. J Clin Virol. 2020;132:104613. doi: 10.1016/j.jcv.2020.104613.
  • Wakita M, Idei M, Saito K, et al. Comparison of the clinical performance and usefulness of five SARS-CoV-2 antibody tests. PLOS One. 2021;16(2):e0246536. doi: 10.1371/journal.pone.0246536.
  • Perkmann T, Perkmann-Nagele N, Koller T, et al. Anti-spike protein assays to determine SARS-CoV-2 antibody levels: a head-to-head comparison of five quantitative assays. Microbiol Spectr. 2021;9(1):e00247–21. doi: 10.1128/Spectrum.00247-21.
  • Ekelund O, Ekblom K, Somajo S, et al. High-throughput immunoassays for SARS-CoV-2 – considerable differences in performance when comparing three methods. Infect Dis. 2021;53(10):805–810. doi: 10.1080/23744235.2021.1931434.
  • Manenti A, Gianchecchi E, Dapporto F, et al. Evaluation and correlation between SARS-CoV-2 neutralizing and binding antibodies in convalescent and vaccinated subjects. J Immunol Methods. 2022;500:113197. doi: 10.1016/j.jim.2021.113197.
  • Müller L, Kannenberg J, Biemann R, et al. Comparison of the measured values of quantitative SARS-CoV-2 spike antibody assays. J Clin Virol. 2022;155:105269. doi: 10.1016/j.jcv.2022.105269.
  • Taniguchi Y, Suemori K, Tanaka K, et al. Long-term transition of antibody titers in healthcare workers following the first to fourth doses of mRNA COVID-19 vaccine: comparison of two automated SARS-CoV-2 immunoassays. J Infect Chemother. 2023;29(5):534–538. doi: 10.1016/j.jiac.2023.01.007.
  • Springer DN, Perkmann T, Jani CM, et al. Reduced sensitivity of commercial spike-specific antibody assays after primary infection with the SARS-CoV-2 omicron variant. Microbiol Spectr. 2022;10(5):e02129–22. doi: 10.1128/spectrum.02129-22.
  • Lippi G, Adeli K, Plebani M. Commercial immunoassays for detection of anti-SARS-CoV-2 spike and RBD antibodies: urgent call for validation against new and highly mutated variants. Clin Chem Lab Med. 2022;60(3):338–342. doi: 10.1515/cclm-2021-1287.
  • Migueres M, Chapuy-Regaud S, Miédougé M, et al. Current immunoassays and detection of antibodies elicited by Omicron SARS-CoV-2 infection. J Med Virol. 2023;95(1):e28200. doi: 10.1002/jmv.28200.
  • Rössler A, Knabl L, Raschbichler L-M, et al. Reduced sensitivity of antibody tests after omicron infection. Lancet Microbe. 2023;4(1):e10–1–e11. doi: 10.1016/S2666-5247(22)00222-1.
  • Feng S, Phillips DJ, White T, et al. Correlates of protection against symptomatic and asymptomatic SARS-CoV-2 infection. Nat Med. 2021;27(11):2032–2040. doi: 10.1038/s41591-021-01540-1.
  • Nie J, Li Q, Wu J, et al. Quantification of SARS-CoV-2 neutralizing antibody by a pseudotyped virus-based assay. Nat Protoc. 2020;15(11):3699–3715. doi: 10.1038/s41596-020-0394-5.
  • Wickham H. GGPLOT2: elegant graphics for data analysis. New York Springer-Verlag; 2016.
  • Kristiansen PA, Page M, Bernasconi V, et al. WHO International Standard for anti-SARS-CoV-2 immunoglobulin. Lancet. 2021;397(10282):1347–1348. doi: 10.1016/S0140-6736(21)00527-4.
  • Van Elslande J, Oyaert M, Lorent N, et al. Lower persistence of anti-nucleocapsid compared to anti-spike antibodies up to one year after SARS-CoV-2 infection. Diagn Microbiol Infect Dis. 2022;103(1):115659. doi: 10.1016/j.diagmicrobio.2022.115659.
  • Brlić PK, Pavletić M, Lerga M, et al. SARS-CoV-2 spike and nucleocapsid antibody response in vaccinated Croatian healthcare workers and infected hospitalized patients: a single center cohort study. Viruses. 2022;14(9):1966. doi: 10.3390/v14091966.
  • Verkerke HP, Damhorst GL, Graciaa DS, et al. Nucleocapsid antigenemia is a marker of acute SARS-CoV-2 infection. J Infect Dis. 2022;226(9):1577–1587. doi: 10.1093/infdis/jiac225.
  • Halfon P, Jordana S, Blachier S, et al. Anti-spike protein to determine SARS-CoV-2 antibody levels: is there a specific threshold conferring protection in immunocompromised patients? PLOS One. 2023;18(4):e0281257. doi: 10.1371/journal.pone.0281257.
  • Infantino M, Pieri M, Nuccetelli M, et al. The WHO International Standard for COVID-19 serological tests: towards harmonization of anti-spike assays. Int Immunopharmacol. 2021;100:108095. doi: 10.1016/j.intimp.2021.108095.
  • Kroidl I, Winter S, Rubio-Acero R, et al. Studying temporal titre evolution of commercial SARS-CoV-2 assays reveals significant shortcomings of using BAU standardization for comparison. Virol J. 2023;20(1):200. doi: 10.1186/s12985-023-02167-z.
  • Steenhuis M, Wouters E, Schrezenmeier H, et al. Quality assessment and harmonization of laboratories across Europe for multiple SARS-CoV-2 serology assays. Vox Sang. 2023;118(8):666–673. doi: 10.1111/vox.13480.
  • Abu Jabal K, Ben-Amram H, Beiruti K, et al. Impact of age, ethnicity, sex and prior infection status on immunogenicity following a single dose of the BNT162b2 mRNA COVID-19 vaccine: real-world evidence from healthcare workers, Israel, December 2020 to January 2021. Euro Surveill Bull Eur Sur Mal Transm Eur Commun Dis Bull. 2021;26(6):2100096. doi: 10.2807/1560-7917.ES.2021.26.6.2100096.
  • Kriss JL, Reynolds LE, Wang A, CDC COVID-19 Vaccine Task Force., et al. COVID-19 vaccine second-dose completion and interval between first and second doses among vaccinated persons—United States, December 14, 2020 − February 14, 2021. MMWR Morb Mortal Wkly Rep. 2021;70(11):389–395. doi: 10.15585/mmwr.mm7011e2.
  • The Oxford/AstraZeneca (ChAdOx1-S [recombinant] vaccine) COVID-19 vaccine: what you need to know; n.d. [cited 2022 Nov 15]. Available from: https://www.who.int/news-room/feature-stories/detail/the-oxford-astrazeneca-covid-19-vaccine-what-you-need-to-know.
  • Greaney AJ, Starr TN, Gilchuk P, et al. Complete mapping of mutations to the SARS-CoV-2 spike receptor-binding domain that escape antibody recognition. Cell Host Microbe. 2021;29(1):44–57.e9. doi: 10.1016/j.chom.2020.11.007.
  • McCallum M, De Marco A, Lempp FA, et al. N-terminal domain antigenic mapping reveals a site of vulnerability for SARS-CoV-2. Cell. 2021;184(9):2332–2347.e16. doi: 10.1016/j.cell.2021.03.028.
  • Wisnewski AV, Redlich CA, Liu J, et al. Immunogenic amino acid motifs and linear epitopes of COVID-19 mRNA vaccines. PLOS One. 2021;16(9):e0252849. doi: 10.1371/journal.pone.0252849.
  • Zheng X, Duan RH, Gong F, et al. Accuracy of serological tests for COVID-19: a systematic review and meta-analysis. Front Public Health. 2022;10:923525. doi: 10.3389/fpubh.2022.923525.
  • Takei S, Ai T, Yamamoto T, et al. Performance evaluation of the Roche Elecsys® anti-SARS-CoV-2 immunoassays by comparison with neutralizing antibodies and clinical assessment. PLOS One. 2022;17(9):e0274181. doi: 10.1371/journal.pone.0274181.
  • Fajfr M, Pajer P, Ruzek D, et al. Multicentric evaluation of sensitivity of eight commercial anti-SARS-CoV-2 antibody assays and their correlation to virus neutralization titers in seropositive subjects. Sci Rep. 2024;14(1):1421. doi: 10.1038/s41598-024-51968-x.
  • Shrestha LB, Foster C, Rawlinson W, et al. Evolution of the SARS-CoV-2 omicron variants BA.1 to BA.5: implications for immune escape and transmission. Rev Med Virol. 2022;32(5):e2381. doi: 10.1002/rmv.2381.
  • Tang L, Zhang R, Cui M, et al. Omicron-adapted vaccines might require longer follow-up to reveal true benefits. Lancet Microbe. 2023;4(1):e12. doi: 10.1016/S2666-5247(22)00292-0.
  • Barros-Martins J, Hammerschmidt SI, Morillas Ramos G, et al. Omicron infection-associated T- and B-cell immunity in antigen-naive and triple-COVID-19-vaccinated individuals. Front Immunol. 2023;14:1166589. doi: 10.3389/fimmu.2023.1166589.
  • Aguilar-Bretones M, Fouchier RA, Koopmans MP, et al. Impact of antigenic evolution and original antigenic sin on SARS-CoV-2 immunity. J Clin Invest. 2023;133(1):e162192. doi: 10.1172/JCI162192.
  • Bratcher-Bowman N. On titers for hyperimmune plasma (FDA); 2021. Available from: https://www.fdanews.com/ext/resources/files/2021/02-05-21-COVID19.pdf?1612723531.