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Impact of Exposure to Vaccination and Infection on Cellular and Antibody Response to SARS-CoV-2 in CVID Patients Through COVID-19 Pandemic

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Abstract

Purpose

The purpose of this study is to investigate the kinetics of response against SARS-CoV-2 elicited by vaccination and/or breakthrough infection (occurred after 3 doses of BNT162b2) in a cohort CVID patients.

Methods

We measured humoral and cellular immunity using quantitative anti-spike antibody (anti-S-IgG) and neutralization assay and specific interferon-gamma release assay (IGRA) before and after the third or fourth dose of BNT162b2 and/or after COVID-19.

Results

In CVID, 58.3% seroconverted after 2 doses that increased to 77.8% after 3 doses. Between the second and third dose, there was a decline in humoral compartment that led to titers below the cutoff of 1:10 (MNA90%) in CVID. This was paralleled by a significantly lower proportion (30%) and reduced magnitude of the residual cellular response among CVID. The third dose achieved a lower titer of anti-S and nAb against the Wuhan strain than HC and significantly decreased the rate of those showing solely a positive neutralizing activity and those with simultaneous negativity of IGRA and nAbs; the differences in IGRA were overall reduced with respect to HC. At further sampling after breakthrough SARS-COV-2 infection, mostly in the omicron era, or fourth dose, 6 months after the last event, the residual nAb titer to Wuhan strain was still significantly higher in HC, while there was no significant difference of nAbs to BA.1. The rate of IGRA responders was 65.5% in CVID and 90.5% in HC (p=0.04), while the magnitude of response was similar. None of CVID had double negativity to nAbs and IGRA at the last sampling.

Conclusion

This data shows an increase of adaptive immunity in CVID after mRNA vaccination in parallel to boosters, accrual number of exposures and formation of hybrid immunity.

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Data Availability

Data is available upon reasonable request to the corresponding author.

Abbreviations

CLIA:

Chemiluminescent analytical system

COVID-19:

Coronavirus disease 2019

HC:

Healthy controls

MNA:

Microneutralization test

RBD:

Receptor binding domain

SARS-CoV-2:

Severe acute respiratory syndrome coronavirus 2

References

  1. Sahin U, Muik A, Derhovanessian E, Vogler I, Kranz LM, Vormehr M, et al. COVID-19 vaccine BNT162b1 elicits human antibody and TH1 T cell responses. Nature. 2020;586(7830):594–9. https://doi.org/10.1038/s41586-020-2814-7.

    Article  CAS  PubMed  Google Scholar 

  2. Goel RR, Painter MM, Apostolidis SA, Mathew D, Meng W, Rosenfeld AM, et al. mRNA vaccines induce durable immune memory to SARS-CoV-2 and variants of concern. Science. 2021;374(6572):abm0829. https://doi.org/10.1126/science.abm0829.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Katzenstein TL, Rasmussen LD, Drabe CH, Larsen CS, Hansen A-BE, Stærkind M, et al. Outcome of SARS-CoV-2 infection among patients with common variable immunodeficiency and a matched control group: a Danish nationwide cohort study. Front Immunol. 2022;13:994253. https://doi.org/10.3389/fimmu.2022.994253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Shields AM, Burns SO, Savic S, Richter AG. Consortium UPC-. COVID-19 in patients with primary and secondary immunodeficiency: the United Kingdom experience. J Allergy Clin Immunol. 2021;147(3):870–5 e1. https://doi.org/10.1016/j.jaci.2020.12.620.

    Article  CAS  PubMed  Google Scholar 

  5. Paris R. SARS-CoV-2 infection and response to COVID-19 vaccination in patients with primary immunodeficiencies. J Infect Dis. 2023;228(Supplement_1):S24–33. https://doi.org/10.1093/infdis/jiad145.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Milito C, Cinetto F, Garzi G, Palladino A, Puca M, Brambilla E, et al. Safety of mRNA COVID-19 vaccines in patients with inborn errors of immunity: an Italian multicentric study. J Clin Immunol. 2022:1–9. https://doi.org/10.1007/s10875-022-01402-6.

  7. Farmer JR, Galbraith A, Ong M-S. Association of inborn errors of immunity with severe COVID-19 and post-acute sequelae of COVID-19. J Allergy Clin Immunol In Pract. 2023; https://doi.org/10.1016/j.jaip.2023.05.029.

  8. Milito C, Firinu D, Bez P, Villa A, Punziano A, Lagnese G, et al. A beacon in the dark: COVID-19 course in CVID patients from two European countries: different approaches, similar outcomes. Front Immunol. 2023;14:1093385. https://doi.org/10.3389/fimmu.2023.1093385.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. McDonnell JC. COVID-19 vaccination in patients with inborn errors of immunity reduces hospitalization and critical care needs related to COVID-19: a USIDNET report. Res Sq. 2023; https://doi.org/10.21203/rs.3.rs-3194637/v1.

  10. Arroyo-Sanchez D, Cabrera-Marante O, Laguna-Goya R, Almendro-Vazquez P, Carretero O, Gil-Etayo FJ, et al. Immunogenicity of anti-SARS-CoV-2 vaccines in common variable immunodeficiency. J Clin Immunol. 2022;42(2):240–52. https://doi.org/10.1007/s10875-021-01174-5.

    Article  CAS  PubMed  Google Scholar 

  11. Pulvirenti F, Fernandez Salinas A, Milito C, Terreri S, Piano Mortari E, Quintarelli C, et al. B Cell response induced by SARS-CoV-2 infection is boosted by the BNT162b2 vaccine in primary antibody deficiencies. Cells. 2021;10(11). https://doi.org/10.3390/cells10112915.

  12. Carabelli AM, Peacock TP, Thorne LG, Harvey WT, Hughes J, de Silva TI, et al. SARS-CoV-2 variant biology: immune escape, transmission and fitness. Nat Rev Microbiol. 2023;21(3):162–77. https://doi.org/10.1038/s41579-022-00841-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Murray CE, O’Brien C, Alamin S, Phelan SH, Argue R, Kiersey R, et al. Cellular and humoral immunogenicity of the COVID-19 vaccine and COVID-19 disease severity in individuals with immunodeficiency. Front Immunol. 2023;14

  14. Levin EG, Lustig Y, Cohen C, Fluss R, Indenbaum V, Amit S, et al. Waning immune humoral response to BNT162b2 Covid-19 vaccine over 6 months. N Engl J Med. 2021;385(24):e84. https://doi.org/10.1056/NEJMoa2114583.

    Article  CAS  PubMed  Google Scholar 

  15. Bobrovitz N, Ware H, Ma X, Li Z, Hosseini R, Cao C, et al. Protective effectiveness of previous SARS-CoV-2 infection and hybrid immunity against the omicron variant and severe disease: a systematic review and meta-regression. Lancet Infect Dis. 2023;23(5):556–67. https://doi.org/10.1016/S1473-3099(22)00801-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. van Leeuwen LPM, Grobben M, GeurtsvanKessel CH, Ellerbroek PM, de Bree GJ, Potjewijd J, et al. Immune responses 6 months after mRNA-1273 COVID-19 vaccination and the effect of a third vaccination in patients with inborn errors of immunity. J Clin Immunol. 2023:1–14. https://doi.org/10.1007/s10875-023-01514-7.

  17. Chen P, Bergman P, Blennow O, Hansson L, Mielke S, Nowak P, et al. Real-world assessment of immunogenicity in immunocompromised individuals following SARS-CoV-2 mRNA vaccination: a one-year follow-up of the prospective clinical trial COVAXID. EBioMedicine. 2023;94:104700. https://doi.org/10.1016/j.ebiom.2023.104700.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Erra L, Uriarte I, Colado A, Paolini MV, Seminario G, Fernández JB, et al. COVID-19 vaccination responses with different vaccine platforms in patients with inborn errors of immunity. J Clin Immunol. 2023;43(2):271–85. https://doi.org/10.1007/s10875-022-01382-7.

    Article  CAS  PubMed  Google Scholar 

  19. Sauerwein KMT, Geier CB, Stemberger RF, Rossmanith R, Akyaman H, Illes P, et al. Functionally impaired antibody response to BNT162b2 booster vaccination in CVID IgG responders. J Allergy Clin Immun. 2023;151(4):922–5. https://doi.org/10.1016/j.jaci.2022.11.013.

    Article  CAS  PubMed  Google Scholar 

  20. Shields AM, Faustini SE, Hill HJ, Al-Taei S, Tanner C, Ashford F, et al. SARS-CoV-2 Vaccine responses in individuals with antibody deficiency: findings from the COV-AD study. J Clin Immunol. 2022;42(5):923–34. https://doi.org/10.1007/s10875-022-01231-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Milota T, Smetanova J, Skotnicova A, Rataj M, Lastovicka J, Zelena H, et al. Clinical outcomes, immunogenicity, and safety of BNT162b2 vaccine in primary antibody deficiency. J Allergy Clin Immunol Pract. 2023;11(1):306–14e2. https://doi.org/10.1016/j.jaip.2022.10.046.

    Article  CAS  PubMed  Google Scholar 

  22. Mazzoni A, Vanni A, Spinicci M, Lamacchia G, Kiros ST, Rocca A, et al. SARS-CoV-2 infection and vaccination trigger long-lived B and CD4+ T lymphocytes with implications for booster strategies. J Clin Invest. 2022;132(6). https://doi.org/10.1172/JCI157990.

  23. Jyssum I, Kared H, Tran TT, Tveter AT, Provan SA, Sexton J, et al. Humoral and cellular immune responses to two and three doses of SARS-CoV-2 vaccines in rituximab-treated patients with rheumatoid arthritis: a prospective, cohort study. Lancet Rheumatol. 2022;4(3):e177–e87. https://doi.org/10.1016/S2665-9913(21)00394-5.

    Article  CAS  PubMed  Google Scholar 

  24. Rydyznski Moderbacher C, Ramirez SI, Dan JM, Grifoni A, Hastie KM, Weiskopf D, et al. Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell. 2020;183(4):996–1012e19. https://doi.org/10.1016/j.cell.2020.09.038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Gao Y, Cai C, Grifoni A, Muller TR, Niessl J, Olofsson A, et al. Ancestral SARS-CoV-2-specific T cells cross-recognize the Omicron variant. Nat Med. 2022;28(3):472–6. https://doi.org/10.1038/s41591-022-01700-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Calabrese CM, Kirchner E, Husni EM, Moss BP, Fernandez AP, Jin Y, et al. Breakthrough SARS-CoV-2 infections in patients with immune-mediated disease undergoing B cell-depleting therapy: a retrospective cohort analysis. Arthritis Rheumatol. 2022;74(12):1906–15. https://doi.org/10.1002/art.42287.

    Article  CAS  PubMed  Google Scholar 

  27. Salinas AF, Mortari EP, Terreri S, Quintarelli C, Pulvirenti F, Di Cecca S, et al. SARS-CoV-2 vaccine induced atypical immune responses in antibody defects: everybody does their best. J Clin Immunol. 2021;41(8):1709–22. https://doi.org/10.1007/s10875-021-01133-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Goldblatt D, Alter G, Crotty S, Plotkin SA. Correlates of protection against SARS-CoV-2 infection and COVID-19 disease. Immunol Rev. 2022;310(1):6–26. https://doi.org/10.1111/imr.13091.

    Article  CAS  PubMed  Google Scholar 

  29. Malato J, Ribeiro RM, Fernandes E, Leite PP, Casaca P, Antunes C, et al. Stability of hybrid versus vaccine immunity against BA.5 infection over 8 months. Lancet Infect Dis. 2023;23(2):148–50. https://doi.org/10.1016/S1473-3099(22)00833-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Seidel MG, Kindle G, Gathmann B, Quinti I, Buckland M, van Montfrans J, et al. The European Society for Immunodeficiencies (ESID) Registry working definitions for the clinical diagnosis of inborn errors of immunity. J Allergy Clin Immunol Pract. 2019;7(6):1763–70. https://doi.org/10.1016/j.jaip.2019.02.004.

    Article  PubMed  Google Scholar 

  31. Chapel H, Lucas M, Patel S, Lee M, Cunningham-Rundles C, Resnick E, et al. Confirmation and improvement of criteria for clinical phenotyping in common variable immunodeficiency disorders in replicate cohorts. J Allergy Clin Immunol. 2012;130(5):1197–8 e9. https://doi.org/10.1016/j.jaci.2012.05.046.

    Article  PubMed  Google Scholar 

  32. Nielsen BU, Drabe CH, Barnkob MB, Johansen IS, Hansen AKK, Nilsson AC, et al. Antibody response following the third and fourth SARS-CoV-2 vaccine dose in individuals with common variable immunodeficiency. Front Immunol. 2022;13:934476. https://doi.org/10.3389/fimmu.2022.934476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Sanna G, Marongiu A, Firinu D, Piras C, Franci G, Galdiero M, et al. Neutralizing antibodies responses against SARS-CoV-2 in a Sardinian Cohort Group up to 9 months after BNT162b2 vaccination. Vaccines (Basel). 2022;10(4):531. https://doi.org/10.3390/vaccines10040531.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Dalakas MC, Bitzogli K, Alexopoulos H. Anti-SARS-CoV-2 antibodies within IVIg preparations: cross-reactivities with seasonal coronaviruses, natural autoimmunity, and therapeutic implications. Front Immunol. 2021;12:627285. https://doi.org/10.3389/fimmu.2021.627285.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Lindahl H, Chen P, Aberg M, Ljunggren HG, Buggert M, Aleman S, et al. SARS-CoV-2 antibodies in commercial immunoglobulin products show markedly reduced cross-reactivities against Omicron Variants. J Clin Immunol. 2023;43(6):1075–82. https://doi.org/10.1007/s10875-023-01486-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Ameratunga R, Leung E, Woon S-T, Chan L, Steele R, Lehnert K, et al. SARS-CoV-2 Omicron: light at the end of the long pandemic tunnel or another false dawn for immunodeficient patients? J Allergy Clin Immunol Pract. 2022;10(9):2267–73. https://doi.org/10.1016/j.jaip.2022.06.011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Fagni F, Simon D, Tascilar K, Schoenau V, Sticherling M, Neurath MF, et al. COVID-19 and immune-mediated inflammatory diseases: effect of disease and treatment on COVID-19 outcomes and vaccine responses. Lancet Rheumatol. 2021;3(10):e724–e36. https://doi.org/10.1016/S2665-9913(21)00247-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Løken RØ, Fevang B. Cellular immunity in COVID-19 and other infections in common variable immunodeficiency. Front Immunol. 2023;14:1124279. https://doi.org/10.3389/fimmu.2023.1124279.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Durkee-Shock JR, Keller MD. Immunizing the imperfect immune system: coronavirus disease 2019 vaccination in patients with inborn errors of immunity. Ann Allergy Asthma Immunol. 2022;129(5):562–71e1. https://doi.org/10.1016/j.anai.2022.06.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hagin D, Freund T, Navon M, Halperin T, Adir D, Marom R, et al. Immunogenicity of Pfizer-BioNTech COVID-19 vaccine in patients with inborn errors of immunity. J Allergy Clin Immunol. 2021;148(3):739–49. https://doi.org/10.1016/j.jaci.2021.05.029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Bergman P, Wullimann D, Gao Y, Wahren Borgström E, Norlin A-C, Lind Enoksson S, et al. Elevated CD21low B cell frequency is a marker of poor immunity to Pfizer-BioNTech BNT162b2 mRNA vaccine against SARS-CoV-2 in patients with common variable immunodeficiency. J Clin Immunol. 2022;42(4):716–27. https://doi.org/10.1007/s10875-022-01244-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ainsua-Enrich E, Pedreño-Lopez N, Bracke C, Ávila-Nieto C, Rodríguez de la Concepción ML, Pradenas E et al. Kinetics of immune responses elicited after three mRNA COVID-19 vaccine doses in predominantly antibody-deficient individuals. iScience. 2022;25(11):105455. doi:10.1016/j.isci.2022.105455.

  43. Zimmerman O, Altman Doss AM, Kaplonek P, Liang CY, VanBlargan LA, Chen RE, et al. mRNA vaccine boosting enhances antibody responses against SARS-CoV-2 Omicron variant in individuals with antibody deficiency syndromes. Cell Rep Med. 2022;3(6):100653. https://doi.org/10.1016/j.xcrm.2022.100653.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Zendt M, Bustos Carrillo FA, Kelly S, Saturday T, DeGrange M, Ginigeme A, et al. Characterization of the antispike IgG immune response to COVID-19 vaccines in people with a wide variety of immunodeficiencies. Sci Adv. 2023;9(41):eadh3150. https://doi.org/10.1126/sciadv.adh3150.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. La Civita E, Zannella C, Brusa S, Romano P, Schettino E, Salemi F, et al. BNT162b2 Elicited an efficient cell-mediated response against SARS-CoV-2 in kidney transplant recipients and common variable immunodeficiency patients. Viruses. 2023;15(8):1659. https://doi.org/10.3390/v15081659.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lin FJ, Doss AMA, Davis-Adams HG, Adams LJ, Hanson CH, VanBlargan LA, et al. SARS-CoV-2 booster vaccination rescues attenuated IgG1 memory B cell response in primary antibody deficiency patients. Front Immunol. 2022;13:1033770. https://doi.org/10.3389/fimmu.2022.1033770.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Piano Mortari E, Pulvirenti F, Marcellini V, Terreri S, Salinas AF, Ferrari S, et al. Functional CVIDs phenotype clusters identified by the integration of immune parameters after BNT162b2 boosters. Front Immunol. 2023;14:1194225. https://doi.org/10.3389/fimmu.2023.1194225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Steiner S, Schwarz T, Corman VM, Jeworowski LM, Bauer S, Drosten C, et al. Impaired B cell recall memory and reduced antibody avidity but robust T cell response in CVID patients after COVID-19 vaccination. J Clin Immunol. 2023;43(5):869–81. https://doi.org/10.1007/s10875-023-01468-w.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Amodio D, Ruggiero A, Sgrulletti M, Pighi C, Cotugno N, Medri C, et al. Humoral and cellular response following vaccination with the BNT162b2 mRNA COVID-19 vaccine in patients affected by primary immunodeficiencies. Front Immunol. 2021;12:727850. https://doi.org/10.3389/fimmu.2021.727850.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Gernez Y, Murugesan K, Cortales CR, Banaei N, Hoyte L, Pinsky BA, et al. Immunogenicity of a third COVID-19 messenger RNA vaccine dose in primary immunodeficiency disorder patients with functional B-cell defects. J Allergy Clin Immunol Pract. 2022;10(5):1385–8.e2. https://doi.org/10.1016/j.jaip.2022.02.030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Barros-Martins J, Hammerschmidt SI, Morillas Ramos G, Cossmann A, Hetzel L, Odak I, et al. Omicron infection-associated T- and B-cell immunity in antigen-naive and triple-COVID-19-vaccinated individuals. Frontiers in Immunology. 2023;14:1166589. https://doi.org/10.3389/fimmu.2023.1166589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Medits I, Springer DN, Graninger M, Camp JV, Höltl E, Aberle SW, et al. Different neutralization profiles after primary SARS-CoV-2 Omicron BA.1 and BA.2 infections. Front Immunol. 2022;13:946318. https://doi.org/10.3389/fimmu.2022.946318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Lindahl H, Klingstrom J, Da Silva RR, Christ W, Chen P, Ljunggren HG, et al. Neutralizing SARS-CoV-2 antibodies in commercial immunoglobulin products give patients with X-linked agammaglobulinemia limited passive immunity to the Omicron variant. J Clin Immunol. 2022;42(6):1130–6. https://doi.org/10.1007/s10875-022-01283-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Al-Dury S, Waldenström J, Ringlander J, Einarsdottir S, Andersson M, Hamah Saed H, et al. Catch-up antibody responses and hybrid immunity in mRNA vaccinated patients at risk of severe COVID-19. Infect Dis (London, England). 2023:1–7. https://doi.org/10.1080/23744235.2023.2230289.

  55. Muller TR, Sekine T, Trubach D, Niessl J, Chen P, Bergman P, et al. Additive effects of booster mRNA vaccination and SARS-CoV-2 Omicron infection on T cell immunity across immunocompromised states. Sci Transl Med. 2023;15(704):eadg9452. https://doi.org/10.1126/scitranslmed.adg9452.

    Article  CAS  PubMed  Google Scholar 

  56. Ukey R, Bruiners N, Mishra H, Mishra PK, McCloskey D, Onyuka A, et al. Dichotomy between the humoral and cellular responses elicited by mRNA and adenoviral vector vaccines against SARS-CoV-2. BMC Med. 2022;20(1):32. https://doi.org/10.1186/s12916-022-02252-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This research was supported by Fondazione di Sardegna (year 2021 n. F73C22001270007); EU funding within the NextGeneration EU-MUR PNRR Extended Partnership initiative on Emerging Infectious Diseases (Project n. PE00000007, INF-ACT); and Associazione per l’Avanzamento della Ricerca per i Trapianti O.D.V. The funding sources had no role in study design, collection, data interpretation, and decision to submit.

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Author notes

  1. Giulia Anna Maria Luigia Costanzo and Carla Maria Deiana contributed equally to this work.

Authors and Affiliations

  1. Department of Medical Sciences and Public Health, University of Cagliari, 09100, Cagliari, Italy

    Giulia Anna Maria Luigia Costanzo, Carla Maria Deiana, Marcello Campagna, Andrea Giovanni Ledda, Luchino Chessa, Stefano Del Giacco & Davide Firinu

  2. Microbiology and Virology Unit, Department of Biomedical Sciences, University of Cagliari, 09042, Monserrato, Italy

    Giuseppina Sanna, Vanessa Palmas & Aldo Manzin

  3. Oncology and Molecular Pathology Unit, Department of Biomedical Sciences, University of Cagliari, 09100, Cagliari, Italy

    Andrea Perra

  4. Laboratory Clinical Chemical Analysis and Microbiology, University Hospital of Cagliari, 09042, Monserrato, Italy

    Ferdinando Coghe & Riccardo Cappai

  5. Unit of Internal Medicine, Policlinico Universitario – AOU di Cagliari, Cagliari, Italy

    Davide Firinu

  6. Azienda Ospedaliero Universitaria, SS 554-Bivio Sestu, 09042, Monserrato, CA, Italy

    Davide Firinu

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  1. Giulia Anna Maria Luigia Costanzo
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Contributions

G.C., C.M.D., G.S., A.P., and D.F. analyzed the data. G.C., C.M.D., and D.F. were responsible for study design and prepared the manuscript. F.C., L.C., M.C.,V.P., A.M., R.C., and S.D.G., contributed to data collection and immunologic data analysis. L.C., A.M., S.D.G., and D.F. provided funding for the study. All coauthors provided a critical review of the manuscript.

Corresponding author

Correspondence to Davide Firinu.

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The study has been approved by the Ethical Committee of the A.O.U. di Cagliari University Hospital (CORIMUN STUDY: May 27th, 2020 protocol n. GT/2020/10894 and extension approved Jan 27th, 2021).

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Costanzo, G.A.M.L., Deiana, C.M., Sanna, G. et al. Impact of Exposure to Vaccination and Infection on Cellular and Antibody Response to SARS-CoV-2 in CVID Patients Through COVID-19 Pandemic. J Clin Immunol 44, 12 (2024). https://doi.org/10.1007/s10875-023-01616-2

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