Comparison of long-term anti-RBD SARS-CoV-2 antibody response following different vaccination schemes in Tunisia

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Published Jul 28, 2024
https://doi.org/10.62438/tunismed.v102i8.4944
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Vol. 102 No. 8 (2024): Tunis Med aug 2024

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Awatef Ben Jemaa
Biodhaouadi Laboratory, Center for Medical Analysis and Reproduction Biology, Bizerte, Unit IMEC-Immunology Microbiology Environmental and Carcinogenesis, Faculty of Science of Bizerte, Bizerte. Department of Biology, Faculty of science of Gafsa, ,University of Gafsa, Gafsa, Tunisia
Rihab Bouabsa
Biodhaouadi Laboratory, Center for Medical Analysis and Reproduction Biology, Bizerte, Tunisia
Meriam Ben Othmen
Biodhaouadi Laboratory, Center for Medical Analysis and Reproduction Biology, Bizerte, Tunisia
Ridha Oueslati
Unit IMEC-Immunology Microbiology Environmental and Carcinogenesis, Faculty of Science of Bizerte, Bizerte, Tunisia.
Hamdi Dhaouadi
Biodhaouadi Laboratory, Center for Medical Analysis and Reproduction Biology, Bizerte, Tunisia

Abstract

Aim: The study aimed to compare long-term vaccine-induced humoral immunity following different vaccines regimens.


Methods: Anti-S-RBD total antibody levels were measured in blood samples of 167 participants nearly 6 months post-vaccination. Participants had received one; two or four doses of Pfizer vaccine or who received a third dose of mRNA vaccine (Pfizer) and primed with mRNA (Pfizer/Moderna), adenoviral (AstraZeneca/Jonson & Jonson) or inactivated (CoronaVac/Sinopharm) vaccine.


Results: Among all vaccination regimens, fourth dose of Pfizer achieved the highest S-RBD antibody titers. Nevertheless, the third dose of mRNA vaccine primed with adenoviral vaccine achieved the lowest titers of S-RBD antibody. Notably, the group that received a third dose of mRNA primed with two doses of mRNA vaccine exhibited higher S-RBD antibody compared to groups inoculated with a third dose of mRNA and primed with inactivated or adenovirus vaccine.


Conclusion: Our data showed the superiority of three mRNA vaccinations compared to third heterologous vaccine (inactivated of adenoviral) including mRNA as booster in terms of humoral immunogenicity. Our findings supporting the use of additional booster shot from a more potent vaccine type such as mRNA vaccines. Nevertheless, due to the limited number of subjects, it is difficult to extrapolate the results of our study to the whole of Tunisian population. Future studies should investigate a larger cohort and other potential correlates of protection, such as cellular immunity and how it is affected by different vaccination schemes after long-term post-vaccination.

Keywords:

COVID-19, mRNA, adenoviral, inactivated, humoral immunity

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This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

References

  1. World Health Organization (WHO). Weekly epidemiological update on COVID-19 - 22 March 2023 (who.int). Available from: https://www.who.int/publications/m/item/weekly-epidemiological-update-on-covid-19---22-march-2023. Accessed on 30 March 2023.
  2. McDonald I, Murray SM, Reynolds CJ, Altmann DM, Boyton RJ. Comparative systematic review and meta-analysis of reactogenicity, immunogenicity and efficacy of vaccines against SARS-CoV-2. NPJ Vaccines 2021; 6: 74.
  3. Sadarangani M, Marchant A, Kollmann TR. Immunological mechanisms of vaccine-induced protection against COVID-19 in humans. Nat Rev Immuno 2021; 21: 475-84.
  4. Ben Ahmed M, Bellali H, Gdoura M, Zamali I, Kallala O, Ben Hmid A et al. Humoral and Cellular Immunogenicity of Six Different Vaccines against SARS-CoV-2 in Adults: A Comparative Study in Tunisia (North Africa). Vaccines (Basel) 2022; 10: 1189.
  5. Zhang X, Wu S, Wu B, Yang Q, Chen A, Li Y et al. SARS-CoV-2 Omicron strain exhibits potent capabilities for immune evasion and viral entrance. Signal Transduct Target Ther 2021; 17: 430.
  6. Cherif I, Kharroubi G, Chaabane S, Yazidi R, Dellagi M, Snoussi MA et al. COVID-19 in Tunisia (North Africa): Seroprevalence of SARS-CoV-2 in the General Population of the Capital City Tunis. Diagnostics (Basel) 2022; 12: 971.
  7. Addo IY, Dadzie FA, Okeke SR, Boadi C, Boadu EF. Duration of immunity following full vaccination against SARS-CoV-2: a systematic review. Arch Public Health 2022; 80: 200.
  8. Ministry of Health. Point de situation en Tunisie-Coronavirus. Available online. https://coronavirus.rns.tn/point-de-situation-en-tunisie/. Accessed on 10 January 2022.
  9. Patalon T, Saciuk Y, Peretz A, Perez G, Lurie Y, Maor Y et al. Waning Effectiveness of the Third Dose of the BNT162b2 mRNA COVID-19 Vaccine. Nat Commun 2022; 13: 3203.
  10. Planas D, Saunders N, Maes P, Guivel-Benhassine F, Planchais C, Buchrieser J, et al. Considerable escape of SARS-CoV-2 Omicron to antibody neutralization. Nature 2022; 602: 671-5.
  11. Zhang W, Huang L, Ye G, Geng Q, Ikeogu N, Harris M et al. Vaccine booster efficiently inhibits entry of SARS-CoV-2 omicron variant. Cell Mol Immunol 2022; 19: 445-6.
  12. Dimeglio C, Migueres M, Mansuy JM, Saivin S, Miedougé M, Chapuy-Regaud S et al. Antibody titers and breakthrough infections with Omicron SARS-CoV-2. J Infect 2022; 84: e13-e15.
  13. Simon G, Favresse J, Gillot C, Closset M, Catry É, Dogné JM et al., Kinetics and ability of binding antibody and surrogate virus neutralization tests to predict neutralizing antibodies against the SARS-CoV-2 Omicron variant following BNT162b2 booster administration. Clin Chem Lab Med 2023; 61: 1875-85.
  14. Kuhlmann C, Mayer CK, Claassen M, Maponga T, Burgers WA, Keeton R et al. Breakthrough infections with SARS-CoV-2 omicron despite mRNA vaccine booster dose. Lancet 2022; 399:625-6.
  15. Bar-On YM, Goldberg Y, Mandel M, Bodenheimer O, Amir O, Freedman L et al. Protection by a fourth dose of BNT162b2 against Omicron in Israel. N Engl J Med 2022; 386:1712-20.
  16. Krammer F. SARS-CoV-2 vaccines in development. Nature 2020 ; 586 :516–27.
  17. Kyriakidis NC, López-Cortés A, González EV, Grimaldos AB, Prado EO. SARSCoV-2 vaccines strategies: a comprehensive review of phase 3 candidates. NPJ Vaccines 2021;6:28.
  18. Resman Rus K, Korva M, Knap N, Avšič Županc T, Poljak M. Performance of the rapid high-throughput automated electrochemiluminescence immunoassay targeting total antibodies to the SARS-CoV-2 spike protein receptor binding domain in comparison to the neutralization assay. J Clin Virol 2021;139:104820.
  19. Garcia-Beltran WF, St Denis KJ, Hoelzemer A, Lam EC, Nitido AD, Sheehan ML et al. mRNA-based COVID-19 vaccine boosters induce neutralizing immunity against SARS-CoV-2 Omicron variant. Cell 2022; 185: 457-466.e4.
  20. Ferdinands JM, Rao S, Dixon BE, Mitchell PK, DeSilva MB, Irving SA et al. Waning 2-dose and 3-dose effectiveness of mRNA vaccines against COVID-19-associated emergency department and urgent care encounters and hospitalizations among adults during periods of Delta and Omicron variant predominance—VISION Network, 10 States, August 2021-January 2022. MMWR Morb Mortal Wkly Rep 2022; 71: 255-63.
  21. Favresse J, Bayart JL, Mullier F, Elsen M, Eucher C, Van Eeckhoudt S et al. Antibody titres decline 3- month post-vaccination with BNT162b2. Emerg Microbes Infect 2021; 10: 1495-8.
  22. Tartof SY, Slezak JM, Fischer H, Hong V, Ackerson BK, Ranasinghe ON et al. Effectiveness of mRNA BNT162b2 COVID-19 vaccine up to 6 months in a large integrated health system in the USA: a retrospective cohort study. Lancet 2021; 398:1407-16.
  23. Saciuk Y, Kertes J, Shamir Stein N, Ekka Zohar A. Effectiveness of a third dose of BNT162b2 mRNA vaccine. J Infect Dis 2022; 225: 30-3.
  24. Bai J, Chiba A, Murayama G, Kuga T, Tamura N, Miyake S. Sex, Age, and Ethnic Background Shape Adaptive Immune Responses Induced by the SARS-CoV-2 mRNA Vaccine. Front Immunol 2022; 13: 786586.
  25. Li Z, Xiang T, Liang B, Deng H, Wang H, Feng X et al. Characterization of SARS-CoV-2-Specific Humoral and Cellular Immune Responses Induced by Inactivated COVID-19 Vaccines in a Real-World Setting. Front Immunol 2021; 12: 802858.
  26. Groß R, Zanoni M, Seidel A, Conzelmann C, Gilg A, Krnavek D et al. Heterologous ChAdOx1 nCoV-19 and BNT162b2 prime-boost vaccination elicits potent neutralizing antibody responses and T cell reactivity against prevalent SARS-CoV-2 variants. EBioMedicine 2022; 75: 103761.
  27. Levine-Tiefenbrun M, Yelin I, Alapi H, Herzel E, Kuint J, Chodick G et al. Waning of SARSCoV-2 booster viral-load reduction effectiveness. Nat Commun 2022; 13: 1237.
  28. Gazit S, Saciuk Y, Perez G, Peretz A, Pitzer VE, Patalon T. Short term, relative effectiveness of four doses versus three doses of BNT162b2 vaccine in people aged 60 years and older in Israel: retrospective, test negative, case-control study. BMJ 2022; 377: e071113.
  29. Tanir F, Mete B, Demirhindi H, Kara E, Nazlican E, Dağlıoğlu G et al. Protectivity of COVID-19 Vaccines and Its Relationship with Humoral Immune Response and Vaccination Strategy: A One-Year Cohort Study. Vaccine 2022;10:1177.
  30. Li M, Wang H, Tian L, Pang Z, Yang Q, Huang T et al. COVID-19 vaccine development: Milestones, lessons and prospects. Signal Transduct Target Ther 2022; 7:146.
  31. Khandker SS, Godman B, Jawad MI, Meghla BA, Tisha TA, Khondoker MU et al. A Systematic Review on COVID-19 Vaccine Strategies, Their Effectiveness, and Issues. Vaccines (Basels) 2021; 9: 1387.
  32. Muena NA, García-Salum T, Pardo-Roa C, Avendaño MJ, Serrano EF, Levican J et al. Induction of SARS-CoV-2 neutralizing antibodies by CoronaVac and BNT162b2 vaccines in naïve and previously infected individuals. EBioMedicine 2022; 78: 103972.
  33. Pérez-Then E, Lucas C, Monteiro VS, Miric M, Brache V, Cochon L et al. Neutralizing antibodies against the SARS-CoV-2 Delta and omicron variants following heterologous CoronaVac plus BNT162b2 booster vaccination. Nat Med 2022; 28: 481-5.
  34. Menegale F, Manica M, Zardini A, Guzzetta G, Marziano V, d'Andrea V et al. Evaluation of Waning of SARS-CoV-2 Vaccine-Induced Immunity: A Systematic Review and Meta-analysis. JAMA Netw Open 2023; 6: e2310650.
  35. Andersson NW, Thiesson EM, Baum U, Pihlström N, Starrfelt J, Faksová K et al. Comparative effectiveness of heterologous third dose vaccine schedules against severe covid-19 during omicron predominance in Nordic countries: population based cohort analyses. BMJ 2023; 382: e074325.
  36. Mondaca S, Walbaum B, Le Corre N, Ferrés M, Valdés A, Martínez-Valdebenito C et al. Influence of SARS-CoV-2 mRNA Vaccine Booster among Cancer Patients on Active Treatment Previously Immunized with Inactivated versus mRNA Vaccines: A Prospective Cohort Study. Vaccines (Basel) 2023; 11 : 1193.
  37. Belik M, Jalkanen P, Lundberg R, Reinholm A, Laine L, Väisänen E et al. Comparative analysis of COVID-19 vaccine responses and third booster dose induced neutralizing antibodies against Delta and Omicron variants. Nat Commun 2022; 13: 2476.
  38. Bonifacius A, Tischer-Zimmermann S, Dragon AC, Gussarow D, Vogel A, Krettek U et al. COVID-19 immune signatures reveal stable antiviral T cell function despite declining humoral responses. Immunity 2021; 54:340-54.e6.
  39. Li Q, Wang Y, Sun Q, Knopf J, Herrmann M, Lin L et al. Immune response in COVID-19: What is next?. Cell Death Differ 2022; 29: 1107-22.
  40. Chouikha A, Fares W, Laamari A, Haddad-Boubaker S, Belaiba Z, Ghedira K et al. Molecular Epidemiology of SARS-CoV-2 in Tunisia (North Africa) through Several Successive Waves of COVID-19. Viruses 2022; 14: 624.
  41. Lee N, Jeong S, Lee SK, Cho EJ, Hyun J, Park MJ et al. Quantitative Analysis of Anti-N and Anti-S Antibody Titers of SARS-CoV-2 Infection after the Third Dose of COVID-19 Vaccination. Vaccines 2022; 10, 1143.