Frontiers in Immunology (Sep 2024)
Robust and persistent B-cell responses following SARS-CoV-2 vaccine determine protection from SARS-CoV-2 infection
- Joanne Byrne,
- Joanne Byrne,
- Lili Gu,
- Alejandro Garcia-Leon,
- Colette Marie Gaillard,
- Gurvin Saini,
- Dana Alalwan,
- Julen Tomás-Cortázar,
- Grace Kenny,
- Grace Kenny,
- Sean Donohue,
- Bearach Reynolds,
- Tessa O’Gorman,
- Tessa O’Gorman,
- Alan Landay,
- Peter Doran,
- Jannik Stemler,
- Jannik Stemler,
- Philipp Koehler,
- Philipp Koehler,
- Rebecca Jane Cox,
- Ole F. Olesen,
- Jean-Daniel Lelievre,
- Cathal O’Broin,
- Cathal O’Broin,
- Stefano Savinelli,
- Stefano Savinelli,
- Eoin R. Feeney,
- Eoin R. Feeney,
- Jane A. O’Halloran,
- Jane A. O’Halloran,
- Aoife Cotter,
- Aoife Cotter,
- Mary Horgan,
- Mary Horgan,
- Christine Kelly,
- Christine Kelly,
- Corrina Sadlier,
- Eoghan de Barra,
- Eoghan de Barra,
- Oliver A. Cornely,
- Oliver A. Cornely,
- Oliver A. Cornely,
- Virginie Gautier,
- Patrick WG Mallon,
- Patrick WG Mallon,
- All Ireland Infectious Diseases cohort study and VACCELERATE consortium,
- A. Cotter,
- E. Muldoon,
- G. Sheehan,
- T. McGinty,
- J. S. Lambert,
- T. O’Gorman,
- C. Kelly,
- K. Leamy,
- J. Byrne,
- G. Kenny,
- K. McCann,
- R. McCann,
- C. O’Broin,
- S. Savinelli,
- J. O’Halloran,
- E. Feeney,
- P. W. G. Mallon,
- A. Garcia Leon,
- S. Miles,
- D. Alalwan,
- R. Negi,
- G. Saini,
- E. Moore,
- E. de Barra,
- S. McConkey,
- K. Hurley,
- B. Jacob,
- F. Lyons,
- M. Horgan,
- C. Sadlier,
- T. Bracken,
- B. Whelan,
- J Low,
- O Yousif,
- B. McNicholas,
- G. Courtney,
- C. O’Maoldomhnaigh,
- P. Gavin,
- Julia M. Neuhann,
- Jannik Stemler,
- Ullrich Bethe,
- Sarah Heringer,
- Jon Salmanton-Garcı́a,
- Lea Tischmann,
- Arnd Cüppers,
- Jan Grothe,
- Philipp Koehler,
- Oliver A. Cornely,
- Antonio J. Carcas,
- Jesús Frías-Iniesta,
- Murat Akova,
- Alejandro Garcia Leon,
- Patrick Mallon,
- Riya Negi,
- Colette Gaillard,
- Gurvin Saini,
- Christine Lammens,
- An Hotterbeekx,
- Katherine Loens,
- Surbhi Malhotra-Kumar,
- Herman Goossens,
- Samir Kumar-Singh,
- Franz König,
- Lusine Yeghiazaryan,
- Martin Posch
Affiliations
- Joanne Byrne
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Joanne Byrne
- Department of Infectious Diseases, St Vincent’s University Hospital, Dublin, Ireland
- Lili Gu
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Alejandro Garcia-Leon
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Colette Marie Gaillard
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Gurvin Saini
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Dana Alalwan
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Julen Tomás-Cortázar
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Grace Kenny
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Grace Kenny
- Department of Infectious Diseases, St Vincent’s University Hospital, Dublin, Ireland
- Sean Donohue
- Department of Infectious Diseases, St Vincent’s University Hospital, Dublin, Ireland
- Bearach Reynolds
- Department of Infectious Diseases, St Vincent’s University Hospital, Dublin, Ireland
- Tessa O’Gorman
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Tessa O’Gorman
- Department of Infectious Diseases, Mater Misericordiae University Hospital, Dublin, Ireland
- Alan Landay
- Department of Internal Medicine, University of Texas Medical Branch, Galveston, TX, United States
- Peter Doran
- School of Medicine, University College Dublin, Dublin, Ireland
- Jannik Stemler
- Faculty of Medicine and University Hospital Cologne, Department I of Internal Medicine, University of Cologne, Cologne, Germany
- Jannik Stemler
- Faculty of Medicine Institute of Translational Research, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany
- Philipp Koehler
- Faculty of Medicine and University Hospital Cologne, Department I of Internal Medicine, University of Cologne, Cologne, Germany
- Philipp Koehler
- Faculty of Medicine Institute of Translational Research, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany
- Rebecca Jane Cox
- Influenza Centre, Department of Clinical Science, University of Bergen, Bergen, Norway
- Ole F. Olesen
- European Vaccine Initiative, Heidelberg, Germany
- Jean-Daniel Lelievre
- 0Vaccine Research Institute, Université Paris Est Créteil, Paris, France
- Cathal O’Broin
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Cathal O’Broin
- Department of Infectious Diseases, St Vincent’s University Hospital, Dublin, Ireland
- Stefano Savinelli
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Stefano Savinelli
- Department of Infectious Diseases, St Vincent’s University Hospital, Dublin, Ireland
- Eoin R. Feeney
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Eoin R. Feeney
- Department of Infectious Diseases, St Vincent’s University Hospital, Dublin, Ireland
- Jane A. O’Halloran
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Jane A. O’Halloran
- Department of Infectious Diseases, St Vincent’s University Hospital, Dublin, Ireland
- Aoife Cotter
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Aoife Cotter
- School of Medicine, University College Dublin, Dublin, Ireland
- Mary Horgan
- Department of Infectious Diseases, Mater Misericordiae University Hospital, Dublin, Ireland
- Mary Horgan
- School of Medicine, University College Dublin, Dublin, Ireland
- Christine Kelly
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Christine Kelly
- School of Medicine, University College Dublin, Dublin, Ireland
- Corrina Sadlier
- 1Department of Infectious Diseases, Cork University Hospital, Cork, Ireland
- Eoghan de Barra
- 2Department of Infectious Diseases, Beaumont Hospital, Dublin, Ireland
- Eoghan de Barra
- 3Department of International Health and Tropical Medicine, Royal College of Surgeons in Ireland, Dublin, Ireland
- Oliver A. Cornely
- Faculty of Medicine and University Hospital Cologne, Department I of Internal Medicine, University of Cologne, Cologne, Germany
- Oliver A. Cornely
- Faculty of Medicine Institute of Translational Research, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany
- Oliver A. Cornely
- 4Partner Site Bonn-Cologne Department Cologne, German Centre for Infection Research (DZIF), Cologne, Germany
- Virginie Gautier
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Patrick WG Mallon
- Centre for Experimental Pathogen Host Research (CEPHR), University College Dublin, Dublin, Ireland
- Patrick WG Mallon
- Department of Infectious Diseases, St Vincent’s University Hospital, Dublin, Ireland
- All Ireland Infectious Diseases cohort study and VACCELERATE consortium
- A. Cotter
- E. Muldoon
- G. Sheehan
- T. McGinty
- J. S. Lambert
- T. O’Gorman
- C. Kelly
- K. Leamy
- J. Byrne
- G. Kenny
- K. McCann
- R. McCann
- C. O’Broin
- S. Savinelli
- J. O’Halloran
- E. Feeney
- P. W. G. Mallon
- A. Garcia Leon
- S. Miles
- D. Alalwan
- R. Negi
- G. Saini
- E. Moore
- E. de Barra
- S. McConkey
- K. Hurley
- B. Jacob
- F. Lyons
- M. Horgan
- C. Sadlier
- T. Bracken
- B. Whelan
- J Low
- O Yousif
- B. McNicholas
- G. Courtney
- C. O’Maoldomhnaigh
- P. Gavin
- Julia M. Neuhann
- Jannik Stemler
- Ullrich Bethe
- Sarah Heringer
- Jon Salmanton-Garcı́a
- Lea Tischmann
- Arnd Cüppers
- Jan Grothe
- Philipp Koehler
- Oliver A. Cornely
- Antonio J. Carcas
- Jesús Frías-Iniesta
- Murat Akova
- Alejandro Garcia Leon
- Patrick Mallon
- Riya Negi
- Colette Gaillard
- Gurvin Saini
- Christine Lammens
- An Hotterbeekx
- Katherine Loens
- Surbhi Malhotra-Kumar
- Herman Goossens
- Samir Kumar-Singh
- Franz König
- Lusine Yeghiazaryan
- Martin Posch
- DOI
- https://doi.org/10.3389/fimmu.2024.1445653
- Journal volume & issue
-
Vol. 15
Abstract
IntroductionA clear immune correlate of protection from severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection has not been defined. We explored antibody, B-cell, and T-cell responses to the third-dose vaccine and relationship to incident SARS-CoV-2 infection.MethodsAdults in a prospective cohort provided blood samples at day 0, day 14, and 10 months after the third-dose SARS-CoV-2 vaccine. Participants self-reported incident SARS-CoV-2 infection. Plasma anti–SARS-CoV-2 receptor-binding domain (RBD) and spike-subunit-1 and spike-subunit-2 antibodies were measured. A sub-study assessed SARS-CoV-2–specific plasma and memory B-cell and memory T-cell responses in peripheral blood mononuclear cells by enzyme-linked immunospot. Comparative analysis between participants who developed incident infection and uninfected participants utilised non-parametric t-tests, Kaplan–Meier survival analysis, and Cox proportional hazard ratios.ResultsOf the 132 participants, 47 (36%) reported incident SARS-CoV-2 infection at a median 16.5 (16.25–21) weeks after the third-dose vaccination. RBD titres and B-cell responses, but not T-cell responses, increased after the third-dose vaccine. Whereas no significant difference in day 14 antibody titres or T-cell responses was observed between participants with and without incident SARS-CoV-2 infection, RBD memory B-cell frequencies were significantly higher in those who did not develop infection [10.0% (4.5%–16.0%) versus 4.9% (1.6%–9.3%), p = 0.01]. RBD titres and memory B-cell frequencies remained significantly higher at 10 months than day 0 levels (p < 0.01).DiscussionRobust antibody and B-cell responses persisted at 10 months following the third-dose vaccination. Higher memory B-cell frequencies, rather than antibody titres or T-cell responses, predicted protection from subsequent infection, identifying memory B cells as a correlate of protection.
Keywords