Safety and Cross-Variant Immunogenicity of a Three-dose COVID-19 mRNA Vaccine Regimen in Kidney Transplant Recipients
Filippo Massa, PhD,
Marion Cremoni, MD,
Alexandre Gérard, MD,
Hanen Grabsi,
Lory Rogier,
Mathilde Blois, MD,
Chloé Couzin, MD,
Nadia Ben Hassen,
Matthieu Rouleau, PhD,
Susana Barbosa, PhD,
Emanuela Martinuzzi, PhD,
Julien Fayada,
Ghislaine Bernard, MD-PhD,
Guillaume Favre, MD-PhD,
Paul Hofman, MD-PhD,
Vincent L.M. Esnault, MD-PhD,
Cecil Czerkinsky, MD-PhD,
Barbara Seitz-Polski, MD-PhD,
Nicolas Glaichenhaus, PhD,
Antoine Sicard, MD-PhD
Affiliations
Filippo Massa, PhD
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France; Laboratory of Molecular Physio Medicine, University Côte d'Azur, CNRS, 28 Avenue de Valombrose, 06107, Nice, France; Clinical Research Unit Côte d'Azur (UR2CA), University Côte d'Azur, 28 Avenue de Valombrose, 06107, Nice, France
Marion Cremoni, MD
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France; Clinical Research Unit Côte d'Azur (UR2CA), University Côte d'Azur, 28 Avenue de Valombrose, 06107, Nice, France
Alexandre Gérard, MD
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France
Hanen Grabsi
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France
Lory Rogier
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France
Mathilde Blois, MD
Department of Immunology, L'Archet Hospital, Nice University Hospital, 151 Route de Saint-Antoine, 06200, Nice, France
Chloé Couzin, MD
Polyvalent laboratory, Lenval hospital, Nice University Hospital, 57 Avenue de la Californie, 06200 Nice, France.
Nadia Ben Hassen
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France; Clinical Research Unit Côte d'Azur (UR2CA), University Côte d'Azur, 28 Avenue de Valombrose, 06107, Nice, France
Matthieu Rouleau, PhD
Laboratory of Molecular Physio Medicine, University Côte d'Azur, CNRS, 28 Avenue de Valombrose, 06107, Nice, France
Susana Barbosa, PhD
Institute of Molecular and Cellular Pharmacology, University Côte d'Azur, CNRS, 660 Route des Lucioles, 06560 Valbonne, France
Emanuela Martinuzzi, PhD
Institute of Molecular and Cellular Pharmacology, University Côte d'Azur, CNRS, 660 Route des Lucioles, 06560 Valbonne, France
Julien Fayada
Laboratory of Clinical and Experimental Pathology, Pasteur Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France.
Ghislaine Bernard, MD-PhD
Department of Immunology, L'Archet Hospital, Nice University Hospital, 151 Route de Saint-Antoine, 06200, Nice, France
Guillaume Favre, MD-PhD
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France; Laboratory of Molecular Physio Medicine, University Côte d'Azur, CNRS, 28 Avenue de Valombrose, 06107, Nice, France
Paul Hofman, MD-PhD
Laboratory of Clinical and Experimental Pathology, Pasteur Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France.
Vincent L.M. Esnault, MD-PhD
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France; Laboratory of Molecular Physio Medicine, University Côte d'Azur, CNRS, 28 Avenue de Valombrose, 06107, Nice, France; Clinical Research Unit Côte d'Azur (UR2CA), University Côte d'Azur, 28 Avenue de Valombrose, 06107, Nice, France
Cecil Czerkinsky, MD-PhD
Institute of Molecular and Cellular Pharmacology, University Côte d'Azur, CNRS, 660 Route des Lucioles, 06560 Valbonne, France
Barbara Seitz-Polski, MD-PhD
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France; Clinical Research Unit Côte d'Azur (UR2CA), University Côte d'Azur, 28 Avenue de Valombrose, 06107, Nice, France; Department of Immunology, L'Archet Hospital, Nice University Hospital, 151 Route de Saint-Antoine, 06200, Nice, France
Nicolas Glaichenhaus, PhD
Clinical Research Unit Côte d'Azur (UR2CA), University Côte d'Azur, 28 Avenue de Valombrose, 06107, Nice, France; Institute of Molecular and Cellular Pharmacology, University Côte d'Azur, CNRS, 660 Route des Lucioles, 06560 Valbonne, France
Antoine Sicard, MD-PhD
Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France; Laboratory of Molecular Physio Medicine, University Côte d'Azur, CNRS, 28 Avenue de Valombrose, 06107, Nice, France; Clinical Research Unit Côte d'Azur (UR2CA), University Côte d'Azur, 28 Avenue de Valombrose, 06107, Nice, France; Corresponding author. Antoine Sicard. Department of Nephrology, Dialysis and Transplantation, Pasteur 2 Hospital, Nice University Hospital, 30 voie Romaine, 06300, Nice, France. Tel. +33(0)492037918.
Background: The immunogenicity of a two-dose mRNA COVID-19 vaccine regimen is low in kidney transplant (KT) recipients. Here, we provide a thorough assessment of the immunogenicity of a three-dose COVID-19 vaccine regimen in this population. Methods: We performed a prospective longitudinal study in sixty-one KT recipients given three doses of the BNT162b2 COVID-19 vaccine. We performed semi-structured pharmacovigilance interviews and monitored donor-specific antibodies and kidney function. We compared levels of anti-spike IgG, pseudo-neutralization activity against vaccine homologous and heterologous variants, frequency of spike-specific interferon (IFN)-γ-secreting cells, and antigen-induced cytokine production 28 days after the second and third doses. Findings: Reactions to vaccine were mild. One patient developed donor-specific anti-HLA antibodies after the second dose which could be explained by non-adherence to immunosuppressive therapy. Spike-specific IgG seroconversion raised from 44·3% (n=27) after the second dose to 62·3% (n=38) after the third dose (p<0·05). The mean level of spike-specific IgG increased from 1620 (SD, 3460) to 8772 (SD, 16733) AU/ml (p<0·0001). Serum neutralizing activity increased after the third dose for all variants of concern tested including the Delta variant (p<0·0001). The frequency of spike-specific IFN-γ-secreting cells increased from 19·9 (SD, 56·0) to 64·0 (SD, 76·8) cells/million PBMCs after the third dose (p<0·0001). A significant increase in IFN-γ responses was also observed in patients who remained seronegative after three doses (p<0·0001). Interpretation: A third dose of the BNT162b2 vaccine increases both cross-variant neutralizing antibody and cellular responses in KT recipients with an acceptable tolerability profile. Funding: Nice University Hospital, University Cote d'Azur.