Kinetics of the B- and T-Cell Immune Responses After 6 Months From SARS-CoV-2 mRNA Vaccination in Patients With Rheumatoid Arthritis
To assess the kinetics of the humoral and cell-mediated responses after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in rheumatoid arthritis (RA) patients treated with different immunosuppressive therapies. Following vaccine completed schedule, health care workers (HCWs,...
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| Vydáno v: | Frontiers in immunology Ročník 13; s. 846753 |
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| Hlavní autoři: | , , , , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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Switzerland
Frontiers Media S.A
28.02.2022
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| ISSN: | 1664-3224, 1664-3224 |
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| Abstract | To assess the kinetics of the humoral and cell-mediated responses after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in rheumatoid arthritis (RA) patients treated with different immunosuppressive therapies.
Following vaccine completed schedule, health care workers (HCWs, n = 49) and RA patients (n = 35) were enrolled at 5 weeks (T1) and 6 months (T6) after the first dose of BNT162b2-mRNA vaccination. Serological response was assessed by quantifying anti-receptor-binding domain (RBD)-specific immunoglobulin G (IgG) and SARS-CoV-2 neutralizing antibodies, while cell-mediated response was assessed by a whole-blood test quantifying the interferon (IFN)-γ response to spike peptides. B-cell phenotype and IFN-γ-specific T-cell responses were evaluated by flow cytometry.
After 6 months, anti-RBD antibodies were still detectable in 91.4% of RA patients, although we observed a significant reduction of the titer in patients under Cytotoxic T-Lymphocyte Antigen 4 (CTLA-4)-Ig [median: 16.4 binding antibody units (BAU)/ml, interquartile range (IQR): 11.3-44.3, p < 0.0001] or tumor necrosis factor (TNF)-α inhibitors (median: 26.5 BAU/ml, IQR: 14.9-108.8, p = 0.0034) compared to controls (median: 152.7 BAU/ml, IQR: 89.3-260.3). All peripheral memory B-cell (MBC) subpopulations, in particular, the switched IgG
MBCs (CD19
CD27
IgD
IgM
IgG
), were significantly reduced in RA subjects under CTLA-4-Ig compared to those in HCWs (p = 0.0012). In RA patients, a significantly reduced anti-RBD IgG titer was observed at T6 vs. T1, mainly in those treated with CTLA-4-Ig (p = 0.002), interleukin (IL)-6 inhibitors (p = 0.015), and disease-modifying antirheumatic drugs (DMARDs) ± corticosteroids (CCSs) (p = 0.015). In contrast, a weak nonsignificant reduction of the T-cell response was reported at T6 vs. T1. T-cell response was found in 65.7% of the RA patients at T6, with lower significant magnitude in patients under CTLA-4-Ig compared to HCWs (p < 0.0001). The SARS-CoV-2 IFN-γ-S-specific T-cell response was mainly detected in the CD4
T-cell compartment.
In this study, in RA patients after 6 months from COVID-19 vaccination, we show the kinetics, waning, and impairment of the humoral and, to a less extent, of the T-cell response. Similarly, a reduction of the specific response was also observed in the controls. Therefore, based on these results, a booster dose of the vaccine is crucial to increase the specific immune response regardless of the immunosuppressive therapy. |
|---|---|
| AbstractList | To assess the kinetics of the humoral and cell-mediated responses after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in rheumatoid arthritis (RA) patients treated with different immunosuppressive therapies.
Following vaccine completed schedule, health care workers (HCWs, n = 49) and RA patients (n = 35) were enrolled at 5 weeks (T1) and 6 months (T6) after the first dose of BNT162b2-mRNA vaccination. Serological response was assessed by quantifying anti-receptor-binding domain (RBD)-specific immunoglobulin G (IgG) and SARS-CoV-2 neutralizing antibodies, while cell-mediated response was assessed by a whole-blood test quantifying the interferon (IFN)-γ response to spike peptides. B-cell phenotype and IFN-γ-specific T-cell responses were evaluated by flow cytometry.
After 6 months, anti-RBD antibodies were still detectable in 91.4% of RA patients, although we observed a significant reduction of the titer in patients under Cytotoxic T-Lymphocyte Antigen 4 (CTLA-4)-Ig [median: 16.4 binding antibody units (BAU)/ml, interquartile range (IQR): 11.3-44.3, p < 0.0001] or tumor necrosis factor (TNF)-α inhibitors (median: 26.5 BAU/ml, IQR: 14.9-108.8, p = 0.0034) compared to controls (median: 152.7 BAU/ml, IQR: 89.3-260.3). All peripheral memory B-cell (MBC) subpopulations, in particular, the switched IgG
MBCs (CD19
CD27
IgD
IgM
IgG
), were significantly reduced in RA subjects under CTLA-4-Ig compared to those in HCWs (p = 0.0012). In RA patients, a significantly reduced anti-RBD IgG titer was observed at T6 vs. T1, mainly in those treated with CTLA-4-Ig (p = 0.002), interleukin (IL)-6 inhibitors (p = 0.015), and disease-modifying antirheumatic drugs (DMARDs) ± corticosteroids (CCSs) (p = 0.015). In contrast, a weak nonsignificant reduction of the T-cell response was reported at T6 vs. T1. T-cell response was found in 65.7% of the RA patients at T6, with lower significant magnitude in patients under CTLA-4-Ig compared to HCWs (p < 0.0001). The SARS-CoV-2 IFN-γ-S-specific T-cell response was mainly detected in the CD4
T-cell compartment.
In this study, in RA patients after 6 months from COVID-19 vaccination, we show the kinetics, waning, and impairment of the humoral and, to a less extent, of the T-cell response. Similarly, a reduction of the specific response was also observed in the controls. Therefore, based on these results, a booster dose of the vaccine is crucial to increase the specific immune response regardless of the immunosuppressive therapy. To assess the kinetics of the humoral and cell-mediated responses after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in rheumatoid arthritis (RA) patients treated with different immunosuppressive therapies.ObjectiveTo assess the kinetics of the humoral and cell-mediated responses after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in rheumatoid arthritis (RA) patients treated with different immunosuppressive therapies.Following vaccine completed schedule, health care workers (HCWs, n = 49) and RA patients (n = 35) were enrolled at 5 weeks (T1) and 6 months (T6) after the first dose of BNT162b2-mRNA vaccination. Serological response was assessed by quantifying anti-receptor-binding domain (RBD)-specific immunoglobulin G (IgG) and SARS-CoV-2 neutralizing antibodies, while cell-mediated response was assessed by a whole-blood test quantifying the interferon (IFN)-γ response to spike peptides. B-cell phenotype and IFN-γ-specific T-cell responses were evaluated by flow cytometry.MethodsFollowing vaccine completed schedule, health care workers (HCWs, n = 49) and RA patients (n = 35) were enrolled at 5 weeks (T1) and 6 months (T6) after the first dose of BNT162b2-mRNA vaccination. Serological response was assessed by quantifying anti-receptor-binding domain (RBD)-specific immunoglobulin G (IgG) and SARS-CoV-2 neutralizing antibodies, while cell-mediated response was assessed by a whole-blood test quantifying the interferon (IFN)-γ response to spike peptides. B-cell phenotype and IFN-γ-specific T-cell responses were evaluated by flow cytometry.After 6 months, anti-RBD antibodies were still detectable in 91.4% of RA patients, although we observed a significant reduction of the titer in patients under Cytotoxic T-Lymphocyte Antigen 4 (CTLA-4)-Ig [median: 16.4 binding antibody units (BAU)/ml, interquartile range (IQR): 11.3-44.3, p < 0.0001] or tumor necrosis factor (TNF)-α inhibitors (median: 26.5 BAU/ml, IQR: 14.9-108.8, p = 0.0034) compared to controls (median: 152.7 BAU/ml, IQR: 89.3-260.3). All peripheral memory B-cell (MBC) subpopulations, in particular, the switched IgG+ MBCs (CD19+CD27+IgD-IgM-IgG+), were significantly reduced in RA subjects under CTLA-4-Ig compared to those in HCWs (p = 0.0012). In RA patients, a significantly reduced anti-RBD IgG titer was observed at T6 vs. T1, mainly in those treated with CTLA-4-Ig (p = 0.002), interleukin (IL)-6 inhibitors (p = 0.015), and disease-modifying antirheumatic drugs (DMARDs) ± corticosteroids (CCSs) (p = 0.015). In contrast, a weak nonsignificant reduction of the T-cell response was reported at T6 vs. T1. T-cell response was found in 65.7% of the RA patients at T6, with lower significant magnitude in patients under CTLA-4-Ig compared to HCWs (p < 0.0001). The SARS-CoV-2 IFN-γ-S-specific T-cell response was mainly detected in the CD4+ T-cell compartment.ResultsAfter 6 months, anti-RBD antibodies were still detectable in 91.4% of RA patients, although we observed a significant reduction of the titer in patients under Cytotoxic T-Lymphocyte Antigen 4 (CTLA-4)-Ig [median: 16.4 binding antibody units (BAU)/ml, interquartile range (IQR): 11.3-44.3, p < 0.0001] or tumor necrosis factor (TNF)-α inhibitors (median: 26.5 BAU/ml, IQR: 14.9-108.8, p = 0.0034) compared to controls (median: 152.7 BAU/ml, IQR: 89.3-260.3). All peripheral memory B-cell (MBC) subpopulations, in particular, the switched IgG+ MBCs (CD19+CD27+IgD-IgM-IgG+), were significantly reduced in RA subjects under CTLA-4-Ig compared to those in HCWs (p = 0.0012). In RA patients, a significantly reduced anti-RBD IgG titer was observed at T6 vs. T1, mainly in those treated with CTLA-4-Ig (p = 0.002), interleukin (IL)-6 inhibitors (p = 0.015), and disease-modifying antirheumatic drugs (DMARDs) ± corticosteroids (CCSs) (p = 0.015). In contrast, a weak nonsignificant reduction of the T-cell response was reported at T6 vs. T1. T-cell response was found in 65.7% of the RA patients at T6, with lower significant magnitude in patients under CTLA-4-Ig compared to HCWs (p < 0.0001). The SARS-CoV-2 IFN-γ-S-specific T-cell response was mainly detected in the CD4+ T-cell compartment.In this study, in RA patients after 6 months from COVID-19 vaccination, we show the kinetics, waning, and impairment of the humoral and, to a less extent, of the T-cell response. Similarly, a reduction of the specific response was also observed in the controls. Therefore, based on these results, a booster dose of the vaccine is crucial to increase the specific immune response regardless of the immunosuppressive therapy.ConclusionsIn this study, in RA patients after 6 months from COVID-19 vaccination, we show the kinetics, waning, and impairment of the humoral and, to a less extent, of the T-cell response. Similarly, a reduction of the specific response was also observed in the controls. Therefore, based on these results, a booster dose of the vaccine is crucial to increase the specific immune response regardless of the immunosuppressive therapy. ObjectiveTo assess the kinetics of the humoral and cell-mediated responses after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in rheumatoid arthritis (RA) patients treated with different immunosuppressive therapies.MethodsFollowing vaccine completed schedule, health care workers (HCWs, n = 49) and RA patients (n = 35) were enrolled at 5 weeks (T1) and 6 months (T6) after the first dose of BNT162b2-mRNA vaccination. Serological response was assessed by quantifying anti-receptor-binding domain (RBD)-specific immunoglobulin G (IgG) and SARS-CoV-2 neutralizing antibodies, while cell-mediated response was assessed by a whole-blood test quantifying the interferon (IFN)-γ response to spike peptides. B-cell phenotype and IFN-γ-specific T-cell responses were evaluated by flow cytometry.ResultsAfter 6 months, anti-RBD antibodies were still detectable in 91.4% of RA patients, although we observed a significant reduction of the titer in patients under Cytotoxic T-Lymphocyte Antigen 4 (CTLA-4)-Ig [median: 16.4 binding antibody units (BAU)/ml, interquartile range (IQR): 11.3–44.3, p < 0.0001] or tumor necrosis factor (TNF)-α inhibitors (median: 26.5 BAU/ml, IQR: 14.9–108.8, p = 0.0034) compared to controls (median: 152.7 BAU/ml, IQR: 89.3–260.3). All peripheral memory B-cell (MBC) subpopulations, in particular, the switched IgG+ MBCs (CD19+CD27+IgD-IgM-IgG+), were significantly reduced in RA subjects under CTLA-4-Ig compared to those in HCWs (p = 0.0012). In RA patients, a significantly reduced anti-RBD IgG titer was observed at T6 vs. T1, mainly in those treated with CTLA-4-Ig (p = 0.002), interleukin (IL)-6 inhibitors (p = 0.015), and disease-modifying antirheumatic drugs (DMARDs) ± corticosteroids (CCSs) (p = 0.015). In contrast, a weak nonsignificant reduction of the T-cell response was reported at T6 vs. T1. T-cell response was found in 65.7% of the RA patients at T6, with lower significant magnitude in patients under CTLA-4-Ig compared to HCWs (p < 0.0001). The SARS-CoV-2 IFN-γ-S-specific T-cell response was mainly detected in the CD4+ T-cell compartment.ConclusionsIn this study, in RA patients after 6 months from COVID-19 vaccination, we show the kinetics, waning, and impairment of the humoral and, to a less extent, of the T-cell response. Similarly, a reduction of the specific response was also observed in the controls. Therefore, based on these results, a booster dose of the vaccine is crucial to increase the specific immune response regardless of the immunosuppressive therapy. |
| Author | Repele, Federica Salmi, Andrea Nicastri, Emanuele Laganà, Bruno Vaia, Francesco Grassi, Germana Maffongelli, Gaetano Casetti, Rita Petrone, Linda Salemi, Simonetta Colavita, Francesca Corpolongo, Angela Altera, Anna Maria Gerarda Castilletti, Concetta Picchianti-Diamanti, Andrea Farroni, Chiara Di Rosa, Roberta Nalli, Gabriele Aiello, Alessandra Meschi, Silvia Puro, Vincenzo Agrati, Chiara Vanini, Valentina Sesti, Giorgio Goletti, Delia Cuzzi, Gilda |
| AuthorAffiliation | 6 Unità Operativa Semplice (UOS) Professioni Sanitarie Tecniche, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy 2 Department of Clinical and Molecular Medicine, “Sapienza” University, S. Andrea University Hospital , Rome , Italy 4 Laboratory of Cellular Immunology, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy 8 Unità Operativa Complessa (UOC) Emerging Infections and Centro di Riferimento AIDS (CRAIDS), National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy 1 Translational Research Unit, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy 5 Laboratory of Virology, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricover |
| AuthorAffiliation_xml | – name: 1 Translational Research Unit, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy – name: 2 Department of Clinical and Molecular Medicine, “Sapienza” University, S. Andrea University Hospital , Rome , Italy – name: 8 Unità Operativa Complessa (UOC) Emerging Infections and Centro di Riferimento AIDS (CRAIDS), National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy – name: 3 Clinical Division of Infectious Diseases, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy – name: 4 Laboratory of Cellular Immunology, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy – name: 6 Unità Operativa Semplice (UOS) Professioni Sanitarie Tecniche, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy – name: 7 Unità Operativa Complessa (UOC) Direzione Sanitaria, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy – name: 5 Laboratory of Virology, National Institute for Infectious Diseases Lazzaro Spallanzani-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) , Rome , Italy |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35309297$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2022 Farroni, Picchianti-Diamanti, Aiello, Nicastri, Laganà, Agrati, Castilletti, Meschi, Colavita, Cuzzi, Casetti, Grassi, Petrone, Vanini, Salmi, Repele, Altera, Maffongelli, Corpolongo, Salemi, Di Rosa, Nalli, Sesti, Vaia, Puro and Goletti. Copyright © 2022 Farroni, Picchianti-Diamanti, Aiello, Nicastri, Laganà, Agrati, Castilletti, Meschi, Colavita, Cuzzi, Casetti, Grassi, Petrone, Vanini, Salmi, Repele, Altera, Maffongelli, Corpolongo, Salemi, Di Rosa, Nalli, Sesti, Vaia, Puro and Goletti 2022 Farroni, Picchianti-Diamanti, Aiello, Nicastri, Laganà, Agrati, Castilletti, Meschi, Colavita, Cuzzi, Casetti, Grassi, Petrone, Vanini, Salmi, Repele, Altera, Maffongelli, Corpolongo, Salemi, Di Rosa, Nalli, Sesti, Vaia, Puro and Goletti |
| Copyright_xml | – notice: Copyright © 2022 Farroni, Picchianti-Diamanti, Aiello, Nicastri, Laganà, Agrati, Castilletti, Meschi, Colavita, Cuzzi, Casetti, Grassi, Petrone, Vanini, Salmi, Repele, Altera, Maffongelli, Corpolongo, Salemi, Di Rosa, Nalli, Sesti, Vaia, Puro and Goletti. – notice: Copyright © 2022 Farroni, Picchianti-Diamanti, Aiello, Nicastri, Laganà, Agrati, Castilletti, Meschi, Colavita, Cuzzi, Casetti, Grassi, Petrone, Vanini, Salmi, Repele, Altera, Maffongelli, Corpolongo, Salemi, Di Rosa, Nalli, Sesti, Vaia, Puro and Goletti 2022 Farroni, Picchianti-Diamanti, Aiello, Nicastri, Laganà, Agrati, Castilletti, Meschi, Colavita, Cuzzi, Casetti, Grassi, Petrone, Vanini, Salmi, Repele, Altera, Maffongelli, Corpolongo, Salemi, Di Rosa, Nalli, Sesti, Vaia, Puro and Goletti |
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| Keywords | COVID-19 DMARD (disease-modifying antirheumatic drug) antibody response biological therapy whole blood rheumatoid arthritis T-cell response mRNA vaccine |
| Language | English |
| License | Copyright © 2022 Farroni, Picchianti-Diamanti, Aiello, Nicastri, Laganà, Agrati, Castilletti, Meschi, Colavita, Cuzzi, Casetti, Grassi, Petrone, Vanini, Salmi, Repele, Altera, Maffongelli, Corpolongo, Salemi, Di Rosa, Nalli, Sesti, Vaia, Puro and Goletti. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Luca Quartuccio, University of Udine, Italy Members of INMI COVID-19 Vaccine Study Group are listed in the Acknowledgments section These authors have contributed equally to this work and share first authorship This article was submitted to Autoimmune and Autoinflammatory Disorders, a section of the journal Frontiers in Immunology Present address:Concetta Castilletti, Department of Infectious, Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, Negrar di Valpolicella, Verona, Italy Reviewed by: Silvia Piantoni, ASST-Spedali Civili and University of Brescia, Italy; Rossana Domenis, University of Udine, Italy |
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| SubjectTerms | Abatacept Antibodies, Viral antibody response Antirheumatic Agents - therapeutic use Arthritis, Rheumatoid - drug therapy BNT162 Vaccine COVID-19 COVID-19 - prevention & control COVID-19 Vaccines Humans Immunity Immunoglobulin G Immunology Kinetics mRNA vaccine rheumatoid arthritis RNA, Messenger SARS-CoV-2 T-cell response T-Lymphocytes Vaccination whole blood |
| Title | Kinetics of the B- and T-Cell Immune Responses After 6 Months From SARS-CoV-2 mRNA Vaccination in Patients With Rheumatoid Arthritis |
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