Longitudinal immunogenicity cohort study of SARS-CoV-2 mRNA vaccines across individuals with different immunocompromising conditions: heterogeneity in the immune response and crucial role of Omicron-adapted booster dosesResearch in context

Summary: Background: Individuals with primary and secondary immunodeficiencies, being more susceptible to infections, are a priority for vaccination. Here, we determined and compared in a longitudinal study the immune response elicited by SARS-CoV-2 vaccination across different groups of individual...

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Main Authors: Annalisa Ciabattini, Elena Pettini, Fabio Fiorino, Jacopo Polvere, Simone Lucchesi, Chiara Coppola, Simone Costagli, Gabiria Pastore, Anna Sicuranza, Monica Tozzi, Arianna Lippi, Francesca Panza, Monica Bocchia, Alessandro Bucalossi, Guido Garosi, David Bennett, Sonia Bernazzali, Massimiliano Fabbiani, Francesca Montagnani, Donata Medaglini
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Language:English
Published: Elsevier 2025-03-01
Series:EBioMedicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352396425000210
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author Annalisa Ciabattini
Elena Pettini
Fabio Fiorino
Jacopo Polvere
Simone Lucchesi
Chiara Coppola
Simone Costagli
Gabiria Pastore
Anna Sicuranza
Monica Tozzi
Arianna Lippi
Francesca Panza
Monica Bocchia
Alessandro Bucalossi
Guido Garosi
David Bennett
Sonia Bernazzali
Massimiliano Fabbiani
Francesca Montagnani
Donata Medaglini
author_facet Annalisa Ciabattini
Elena Pettini
Fabio Fiorino
Jacopo Polvere
Simone Lucchesi
Chiara Coppola
Simone Costagli
Gabiria Pastore
Anna Sicuranza
Monica Tozzi
Arianna Lippi
Francesca Panza
Monica Bocchia
Alessandro Bucalossi
Guido Garosi
David Bennett
Sonia Bernazzali
Massimiliano Fabbiani
Francesca Montagnani
Donata Medaglini
author_sort Annalisa Ciabattini
collection DOAJ
description Summary: Background: Individuals with primary and secondary immunodeficiencies, being more susceptible to infections, are a priority for vaccination. Here, we determined and compared in a longitudinal study the immune response elicited by SARS-CoV-2 vaccination across different groups of individuals who are immunocompromised. Methods: In the PatoVac_COV longitudinal prospective single-centre study, the spike-specific B cell and antibody responses to SARS-CoV-2 mRNA vaccination were compared across 5 different groups of individuals with haematological malignancies, hematopoietic stem cell (HCT) or solid organ transplantation (SOT), undergoing haemodialysis, and people living with HIV (PLWH), for a total of 585 participants. Data from participants who were immunocompromised were compared to a group of 123 participants who were immunocompetent. Blood samples were collected before and after each vaccine administration, up to 2 years. Findings: A different immune responsiveness was observed after the first two vaccine doses, with haematological, haemodialysis, and SOT participants showing reduced responsiveness compared to HCT and PLWH, and relative to the comparison group. Spike-specific B cell response was both slower and lower in all groups except in PLWH when compared to participants who were immunocompetent. However, the first booster dose enhanced both the B and the antibody responses in all groups, that persisted up to 2 years after the first vaccine administration. The administration of Omicron-adapted booster vaccines promoted a primary BA.2 RBD-specific B cell response, especially in participants who were immunocompromised. Despite repeated vaccinations, a subset of persistent low-responders, especially among SOT, was identified. Interpretation: Our study highlights the heterogeneous immune response across individuals with different pathologies, the pivotal role of the first booster dose, the primary activation of Omicron-specific B cells elicited by updated variant-adapted vaccines and the persistence of low-responders despite multiple vaccine administrations. These aspects have a clinical relevance for planning vaccination schedules tailored for individuals with different immunocompromising conditions. Funding: This work was supported by funds from the Department of Medical Biotechnologies of the University of Siena, and from EU within the NextGenerationEU-MUR PNRR Tuscany Health Ecosystem (Project no ECS00000017-THE).
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spelling doaj-art-801e6607cbf94ea19cf63abd42f041982025-02-06T05:12:00ZengElsevierEBioMedicine2352-39642025-03-01113105577Longitudinal immunogenicity cohort study of SARS-CoV-2 mRNA vaccines across individuals with different immunocompromising conditions: heterogeneity in the immune response and crucial role of Omicron-adapted booster dosesResearch in contextAnnalisa Ciabattini0Elena Pettini1Fabio Fiorino2Jacopo Polvere3Simone Lucchesi4Chiara Coppola5Simone Costagli6Gabiria Pastore7Anna Sicuranza8Monica Tozzi9Arianna Lippi10Francesca Panza11Monica Bocchia12Alessandro Bucalossi13Guido Garosi14David Bennett15Sonia Bernazzali16Massimiliano Fabbiani17Francesca Montagnani18Donata Medaglini19Laboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, Italy; Corresponding author. Department of Medical Biotechnologies, University of Siena, Siena, Italy.Laboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, ItalyLaboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, Italy; Department of Medicine and Surgery, LUM University “Giuseppe Degennaro”, Bari, ItalyLaboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, ItalyLaboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, ItalyLaboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, ItalyLaboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, ItalyLaboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, ItalyHaematology Unit, Department of Medical Science, Surgery and Neuroscience, University Hospital of Siena, Siena, ItalyCellular Therapy Unit, Department of Innovation, Experimentation, Clinical and Translational Research, University Hospital of Siena, Siena, ItalyDepartment of Medical Sciences, Infectious and Tropical Diseases Unit, University Hospital of Siena, Siena, Italy; Department of Medical Biotechnologies, University of Siena, Siena, ItalyDepartment of Medical Sciences, Infectious and Tropical Diseases Unit, University Hospital of Siena, Siena, Italy; Department of Medical Biotechnologies, University of Siena, Siena, ItalyHaematology Unit, Department of Medical Science, Surgery and Neuroscience, University Hospital of Siena, Siena, ItalyCellular Therapy Unit, Department of Innovation, Experimentation, Clinical and Translational Research, University Hospital of Siena, Siena, ItalyDepartment of Medical Science, Nephrology, Dialysis and Transplantation Unit, University Hospital of Siena, ItalyRespiratory Disease and Lung Transplant Unit, University of Siena, University Hospital of Siena, ItalyDepartment of Cardiac Surgery, University of Siena, Siena, ItalyDepartment of Medical Sciences, Infectious and Tropical Diseases Unit, University Hospital of Siena, Siena, Italy; Department of Medical Biotechnologies, University of Siena, Siena, ItalyDepartment of Medical Sciences, Infectious and Tropical Diseases Unit, University Hospital of Siena, Siena, Italy; Department of Medical Biotechnologies, University of Siena, Siena, ItalyLaboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, ItalySummary: Background: Individuals with primary and secondary immunodeficiencies, being more susceptible to infections, are a priority for vaccination. Here, we determined and compared in a longitudinal study the immune response elicited by SARS-CoV-2 vaccination across different groups of individuals who are immunocompromised. Methods: In the PatoVac_COV longitudinal prospective single-centre study, the spike-specific B cell and antibody responses to SARS-CoV-2 mRNA vaccination were compared across 5 different groups of individuals with haematological malignancies, hematopoietic stem cell (HCT) or solid organ transplantation (SOT), undergoing haemodialysis, and people living with HIV (PLWH), for a total of 585 participants. Data from participants who were immunocompromised were compared to a group of 123 participants who were immunocompetent. Blood samples were collected before and after each vaccine administration, up to 2 years. Findings: A different immune responsiveness was observed after the first two vaccine doses, with haematological, haemodialysis, and SOT participants showing reduced responsiveness compared to HCT and PLWH, and relative to the comparison group. Spike-specific B cell response was both slower and lower in all groups except in PLWH when compared to participants who were immunocompetent. However, the first booster dose enhanced both the B and the antibody responses in all groups, that persisted up to 2 years after the first vaccine administration. The administration of Omicron-adapted booster vaccines promoted a primary BA.2 RBD-specific B cell response, especially in participants who were immunocompromised. Despite repeated vaccinations, a subset of persistent low-responders, especially among SOT, was identified. Interpretation: Our study highlights the heterogeneous immune response across individuals with different pathologies, the pivotal role of the first booster dose, the primary activation of Omicron-specific B cells elicited by updated variant-adapted vaccines and the persistence of low-responders despite multiple vaccine administrations. These aspects have a clinical relevance for planning vaccination schedules tailored for individuals with different immunocompromising conditions. Funding: This work was supported by funds from the Department of Medical Biotechnologies of the University of Siena, and from EU within the NextGenerationEU-MUR PNRR Tuscany Health Ecosystem (Project no ECS00000017-THE).http://www.sciencedirect.com/science/article/pii/S2352396425000210ImmunocompromisedVaccine immunogenicitymRNA vaccinesMemory B cellsSARS-CoV-2
spellingShingle Annalisa Ciabattini
Elena Pettini
Fabio Fiorino
Jacopo Polvere
Simone Lucchesi
Chiara Coppola
Simone Costagli
Gabiria Pastore
Anna Sicuranza
Monica Tozzi
Arianna Lippi
Francesca Panza
Monica Bocchia
Alessandro Bucalossi
Guido Garosi
David Bennett
Sonia Bernazzali
Massimiliano Fabbiani
Francesca Montagnani
Donata Medaglini
Longitudinal immunogenicity cohort study of SARS-CoV-2 mRNA vaccines across individuals with different immunocompromising conditions: heterogeneity in the immune response and crucial role of Omicron-adapted booster dosesResearch in context
EBioMedicine
Immunocompromised
Vaccine immunogenicity
mRNA vaccines
Memory B cells
SARS-CoV-2
title Longitudinal immunogenicity cohort study of SARS-CoV-2 mRNA vaccines across individuals with different immunocompromising conditions: heterogeneity in the immune response and crucial role of Omicron-adapted booster dosesResearch in context
title_full Longitudinal immunogenicity cohort study of SARS-CoV-2 mRNA vaccines across individuals with different immunocompromising conditions: heterogeneity in the immune response and crucial role of Omicron-adapted booster dosesResearch in context
title_fullStr Longitudinal immunogenicity cohort study of SARS-CoV-2 mRNA vaccines across individuals with different immunocompromising conditions: heterogeneity in the immune response and crucial role of Omicron-adapted booster dosesResearch in context
title_full_unstemmed Longitudinal immunogenicity cohort study of SARS-CoV-2 mRNA vaccines across individuals with different immunocompromising conditions: heterogeneity in the immune response and crucial role of Omicron-adapted booster dosesResearch in context
title_short Longitudinal immunogenicity cohort study of SARS-CoV-2 mRNA vaccines across individuals with different immunocompromising conditions: heterogeneity in the immune response and crucial role of Omicron-adapted booster dosesResearch in context
title_sort longitudinal immunogenicity cohort study of sars cov 2 mrna vaccines across individuals with different immunocompromising conditions heterogeneity in the immune response and crucial role of omicron adapted booster dosesresearch in context
topic Immunocompromised
Vaccine immunogenicity
mRNA vaccines
Memory B cells
SARS-CoV-2
url http://www.sciencedirect.com/science/article/pii/S2352396425000210
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