ImmunosuppressiveTherapies Differently Modulate Humoral- and T-Cell-Specific Responses to COVID-19 mRNA Vaccine in Rheumatoid Arthritis Patients
To assess in rheumatoid arthritis (RA) patients, treated with different immunosuppressive therapies, the induction of SARS-CoV-2-specific immune response after vaccination in terms of anti-region-binding-domain (RBD)-antibody- and T-cell-specific responses against spike, and the vaccine safety in te...
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| Vydané v: | Frontiers in immunology Ročník 12; s. 740249 |
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| Hlavní autori: | , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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Switzerland
Frontiers Media S.A
14.09.2021
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| ISSN: | 1664-3224, 1664-3224 |
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| Abstract | To assess in rheumatoid arthritis (RA) patients, treated with different immunosuppressive therapies, the induction of SARS-CoV-2-specific immune response after vaccination in terms of anti-region-binding-domain (RBD)-antibody- and T-cell-specific responses against spike, and the vaccine safety in terms of clinical impact on disease activity.
Health care workers (HCWs) and RA patients, having completed the BNT162b2-mRNA vaccination in the last 2 weeks, were enrolled. Serological response was evaluated by quantifying anti-RBD antibodies, while the cell-mediated response was evaluated by a whole-blood test quantifying the interferon (IFN)-γ-response to spike peptides. FACS analysis was performed to identify the cells responding to spike stimulation. RA disease activity was evaluated by clinical examination through the DAS28crp, and local and/or systemic clinical adverse events were registered. In RA patients, the ongoing therapeutic regimen was modified during the vaccination period according to the American College of Rheumatology indications.
We prospectively enrolled 167 HCWs and 35 RA patients. Anti-RBD-antibodies were detected in almost all patients (34/35, 97%), although the titer was significantly reduced in patients under CTLA-4-inhibitors (median: 465 BAU/mL, IQR: 103-1189, p<0.001) or IL-6-inhibitors (median: 492 BAU/mL, IQR: 161-1007, p<0.001) compared to HCWs (median: 2351 BAU/mL, IQR: 1389-3748). T-cell-specific response scored positive in most of RA patients [24/35, (69%)] with significantly lower IFN-γ levels in patients under biological therapy such as IL-6-inhibitors (median: 33.2 pg/mL, IQR: 6.1-73.9, p<0.001), CTLA-4-inhibitors (median: 10.9 pg/mL, IQR: 3.7-36.7, p<0.001), and TNF-α-inhibitors (median: 89.6 pg/mL, IQR: 17.8-224, p=0.002) compared to HCWs (median: 343 pg/mL, IQR: 188-756). A significant correlation between the anti-RBD-antibody titer and spike-IFN-γ-specific T-cell response was found in RA patients (rho=0.432, p=0.009). IFN-γ T-cell response was mediated by CD4
and CD8
T cells. Finally, no significant increase in disease activity was found in RA patients following vaccination.
This study showed for the first time that antibody-specific and whole-blood spike-specific T-cell responses induced by the COVID-19 mRNA-vaccine were present in the majority of RA patients, who underwent a strategy of temporary suspension of immunosuppressive treatment during vaccine administration. However, the magnitude of specific responses was dependent on the immunosuppressive therapy administered. In RA patients, BNT162b2 vaccine was safe and disease activity remained stable. |
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| AbstractList | To assess in rheumatoid arthritis (RA) patients, treated with different immunosuppressive therapies, the induction of SARS-CoV-2-specific immune response after vaccination in terms of anti-region-binding-domain (RBD)-antibody- and T-cell-specific responses against spike, and the vaccine safety in terms of clinical impact on disease activity.ObjectiveTo assess in rheumatoid arthritis (RA) patients, treated with different immunosuppressive therapies, the induction of SARS-CoV-2-specific immune response after vaccination in terms of anti-region-binding-domain (RBD)-antibody- and T-cell-specific responses against spike, and the vaccine safety in terms of clinical impact on disease activity.Health care workers (HCWs) and RA patients, having completed the BNT162b2-mRNA vaccination in the last 2 weeks, were enrolled. Serological response was evaluated by quantifying anti-RBD antibodies, while the cell-mediated response was evaluated by a whole-blood test quantifying the interferon (IFN)-γ-response to spike peptides. FACS analysis was performed to identify the cells responding to spike stimulation. RA disease activity was evaluated by clinical examination through the DAS28crp, and local and/or systemic clinical adverse events were registered. In RA patients, the ongoing therapeutic regimen was modified during the vaccination period according to the American College of Rheumatology indications.MethodsHealth care workers (HCWs) and RA patients, having completed the BNT162b2-mRNA vaccination in the last 2 weeks, were enrolled. Serological response was evaluated by quantifying anti-RBD antibodies, while the cell-mediated response was evaluated by a whole-blood test quantifying the interferon (IFN)-γ-response to spike peptides. FACS analysis was performed to identify the cells responding to spike stimulation. RA disease activity was evaluated by clinical examination through the DAS28crp, and local and/or systemic clinical adverse events were registered. In RA patients, the ongoing therapeutic regimen was modified during the vaccination period according to the American College of Rheumatology indications.We prospectively enrolled 167 HCWs and 35 RA patients. Anti-RBD-antibodies were detected in almost all patients (34/35, 97%), although the titer was significantly reduced in patients under CTLA-4-inhibitors (median: 465 BAU/mL, IQR: 103-1189, p<0.001) or IL-6-inhibitors (median: 492 BAU/mL, IQR: 161-1007, p<0.001) compared to HCWs (median: 2351 BAU/mL, IQR: 1389-3748). T-cell-specific response scored positive in most of RA patients [24/35, (69%)] with significantly lower IFN-γ levels in patients under biological therapy such as IL-6-inhibitors (median: 33.2 pg/mL, IQR: 6.1-73.9, p<0.001), CTLA-4-inhibitors (median: 10.9 pg/mL, IQR: 3.7-36.7, p<0.001), and TNF-α-inhibitors (median: 89.6 pg/mL, IQR: 17.8-224, p=0.002) compared to HCWs (median: 343 pg/mL, IQR: 188-756). A significant correlation between the anti-RBD-antibody titer and spike-IFN-γ-specific T-cell response was found in RA patients (rho=0.432, p=0.009). IFN-γ T-cell response was mediated by CD4+ and CD8+ T cells. Finally, no significant increase in disease activity was found in RA patients following vaccination.ResultsWe prospectively enrolled 167 HCWs and 35 RA patients. Anti-RBD-antibodies were detected in almost all patients (34/35, 97%), although the titer was significantly reduced in patients under CTLA-4-inhibitors (median: 465 BAU/mL, IQR: 103-1189, p<0.001) or IL-6-inhibitors (median: 492 BAU/mL, IQR: 161-1007, p<0.001) compared to HCWs (median: 2351 BAU/mL, IQR: 1389-3748). T-cell-specific response scored positive in most of RA patients [24/35, (69%)] with significantly lower IFN-γ levels in patients under biological therapy such as IL-6-inhibitors (median: 33.2 pg/mL, IQR: 6.1-73.9, p<0.001), CTLA-4-inhibitors (median: 10.9 pg/mL, IQR: 3.7-36.7, p<0.001), and TNF-α-inhibitors (median: 89.6 pg/mL, IQR: 17.8-224, p=0.002) compared to HCWs (median: 343 pg/mL, IQR: 188-756). A significant correlation between the anti-RBD-antibody titer and spike-IFN-γ-specific T-cell response was found in RA patients (rho=0.432, p=0.009). IFN-γ T-cell response was mediated by CD4+ and CD8+ T cells. Finally, no significant increase in disease activity was found in RA patients following vaccination.This study showed for the first time that antibody-specific and whole-blood spike-specific T-cell responses induced by the COVID-19 mRNA-vaccine were present in the majority of RA patients, who underwent a strategy of temporary suspension of immunosuppressive treatment during vaccine administration. However, the magnitude of specific responses was dependent on the immunosuppressive therapy administered. In RA patients, BNT162b2 vaccine was safe and disease activity remained stable.ConclusionThis study showed for the first time that antibody-specific and whole-blood spike-specific T-cell responses induced by the COVID-19 mRNA-vaccine were present in the majority of RA patients, who underwent a strategy of temporary suspension of immunosuppressive treatment during vaccine administration. However, the magnitude of specific responses was dependent on the immunosuppressive therapy administered. In RA patients, BNT162b2 vaccine was safe and disease activity remained stable. ObjectiveTo assess in rheumatoid arthritis (RA) patients, treated with different immunosuppressive therapies, the induction of SARS-CoV-2-specific immune response after vaccination in terms of anti-region-binding-domain (RBD)-antibody- and T-cell-specific responses against spike, and the vaccine safety in terms of clinical impact on disease activity.MethodsHealth care workers (HCWs) and RA patients, having completed the BNT162b2-mRNA vaccination in the last 2 weeks, were enrolled. Serological response was evaluated by quantifying anti-RBD antibodies, while the cell-mediated response was evaluated by a whole-blood test quantifying the interferon (IFN)-γ-response to spike peptides. FACS analysis was performed to identify the cells responding to spike stimulation. RA disease activity was evaluated by clinical examination through the DAS28crp, and local and/or systemic clinical adverse events were registered. In RA patients, the ongoing therapeutic regimen was modified during the vaccination period according to the American College of Rheumatology indications.ResultsWe prospectively enrolled 167 HCWs and 35 RA patients. Anti-RBD-antibodies were detected in almost all patients (34/35, 97%), although the titer was significantly reduced in patients under CTLA-4-inhibitors (median: 465 BAU/mL, IQR: 103-1189, p<0.001) or IL-6-inhibitors (median: 492 BAU/mL, IQR: 161-1007, p<0.001) compared to HCWs (median: 2351 BAU/mL, IQR: 1389-3748). T-cell-specific response scored positive in most of RA patients [24/35, (69%)] with significantly lower IFN-γ levels in patients under biological therapy such as IL-6-inhibitors (median: 33.2 pg/mL, IQR: 6.1-73.9, p<0.001), CTLA-4-inhibitors (median: 10.9 pg/mL, IQR: 3.7-36.7, p<0.001), and TNF-α-inhibitors (median: 89.6 pg/mL, IQR: 17.8-224, p=0.002) compared to HCWs (median: 343 pg/mL, IQR: 188-756). A significant correlation between the anti-RBD-antibody titer and spike-IFN-γ-specific T-cell response was found in RA patients (rho=0.432, p=0.009). IFN-γ T-cell response was mediated by CD4+ and CD8+ T cells. Finally, no significant increase in disease activity was found in RA patients following vaccination.ConclusionThis study showed for the first time that antibody-specific and whole-blood spike-specific T-cell responses induced by the COVID-19 mRNA-vaccine were present in the majority of RA patients, who underwent a strategy of temporary suspension of immunosuppressive treatment during vaccine administration. However, the magnitude of specific responses was dependent on the immunosuppressive therapy administered. In RA patients, BNT162b2 vaccine was safe and disease activity remained stable. To assess in rheumatoid arthritis (RA) patients, treated with different immunosuppressive therapies, the induction of SARS-CoV-2-specific immune response after vaccination in terms of anti-region-binding-domain (RBD)-antibody- and T-cell-specific responses against spike, and the vaccine safety in terms of clinical impact on disease activity. Health care workers (HCWs) and RA patients, having completed the BNT162b2-mRNA vaccination in the last 2 weeks, were enrolled. Serological response was evaluated by quantifying anti-RBD antibodies, while the cell-mediated response was evaluated by a whole-blood test quantifying the interferon (IFN)-γ-response to spike peptides. FACS analysis was performed to identify the cells responding to spike stimulation. RA disease activity was evaluated by clinical examination through the DAS28crp, and local and/or systemic clinical adverse events were registered. In RA patients, the ongoing therapeutic regimen was modified during the vaccination period according to the American College of Rheumatology indications. We prospectively enrolled 167 HCWs and 35 RA patients. Anti-RBD-antibodies were detected in almost all patients (34/35, 97%), although the titer was significantly reduced in patients under CTLA-4-inhibitors (median: 465 BAU/mL, IQR: 103-1189, p<0.001) or IL-6-inhibitors (median: 492 BAU/mL, IQR: 161-1007, p<0.001) compared to HCWs (median: 2351 BAU/mL, IQR: 1389-3748). T-cell-specific response scored positive in most of RA patients [24/35, (69%)] with significantly lower IFN-γ levels in patients under biological therapy such as IL-6-inhibitors (median: 33.2 pg/mL, IQR: 6.1-73.9, p<0.001), CTLA-4-inhibitors (median: 10.9 pg/mL, IQR: 3.7-36.7, p<0.001), and TNF-α-inhibitors (median: 89.6 pg/mL, IQR: 17.8-224, p=0.002) compared to HCWs (median: 343 pg/mL, IQR: 188-756). A significant correlation between the anti-RBD-antibody titer and spike-IFN-γ-specific T-cell response was found in RA patients (rho=0.432, p=0.009). IFN-γ T-cell response was mediated by CD4 and CD8 T cells. Finally, no significant increase in disease activity was found in RA patients following vaccination. This study showed for the first time that antibody-specific and whole-blood spike-specific T-cell responses induced by the COVID-19 mRNA-vaccine were present in the majority of RA patients, who underwent a strategy of temporary suspension of immunosuppressive treatment during vaccine administration. However, the magnitude of specific responses was dependent on the immunosuppressive therapy administered. In RA patients, BNT162b2 vaccine was safe and disease activity remained stable. |
| Author | Repele, Federica Salmi, Andrea Nicastri, Emanuele Laganà, Bruno Cimini, Eleonora Grassi, Germana Maffongelli, Gaetano Salemi, Simonetta Palazzolo, Claudia Vita, Serena Leone, Sara Lapa, Daniele Ippolito, Giuseppe 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 Goletti, Delia Najafi Fard, Saeid Capobianchi, Maria Rosaria Cuzzi, Gilda |
| AuthorAffiliation | 3 Laboratory of Cellular Immunology, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy 8 Scientific Direction, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy 4 Laboratory of Virology, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy 6 Clinical Division of Infectious Diseases, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy 1 Department of Clinical and Molecular Medicine, “Sapienza” University, S. Andrea University Hospital , Rome , Italy 2 Translational Research Unit, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy 5 Unità Operativa Semplice (UOS) Professioni Sanitarie Tecniche, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy 7 UOC Emerging Infections and Centro di Riferimento AIDS (CRAIDS), National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy |
| AuthorAffiliation_xml | – name: 5 Unità Operativa Semplice (UOS) Professioni Sanitarie Tecniche, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy – name: 6 Clinical Division of Infectious Diseases, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy – name: 1 Department of Clinical and Molecular Medicine, “Sapienza” University, S. Andrea University Hospital , Rome , Italy – name: 4 Laboratory of Virology, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy – name: 2 Translational Research Unit, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy – name: 3 Laboratory of Cellular Immunology, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy – name: 8 Scientific Direction, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy – name: 7 UOC Emerging Infections and Centro di Riferimento AIDS (CRAIDS), National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34594343$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2021 Picchianti-Diamanti, Aiello, Laganà, Agrati, Castilletti, Meschi, Farroni, Lapa, Najafi Fard, Cuzzi, Cimini, Grassi, Vanini, Di Rosa, Salemi, Nalli, Salmi, Repele, Altera, Maffongelli, Palazzolo, Vita, Leone, Puro, Capobianchi, Ippolito, Nicastri and Goletti. Copyright © 2021 Picchianti-Diamanti, Aiello, Laganà, Agrati, Castilletti, Meschi, Farroni, Lapa, Najafi Fard, Cuzzi, Cimini, Grassi, Vanini, Di Rosa, Salemi, Nalli, Salmi, Repele, Altera, Maffongelli, Palazzolo, Vita, Leone, Puro, Capobianchi, Ippolito, Nicastri and Goletti 2021 Picchianti-Diamanti, Aiello, Laganà, Agrati, Castilletti, Meschi, Farroni, Lapa, Najafi Fard, Cuzzi, Cimini, Grassi, Vanini, Di Rosa, Salemi, Nalli, Salmi, Repele, Altera, Maffongelli, Palazzolo, Vita, Leone, Puro, Capobianchi, Ippolito, Nicastri and Goletti |
| Copyright_xml | – notice: Copyright © 2021 Picchianti-Diamanti, Aiello, Laganà, Agrati, Castilletti, Meschi, Farroni, Lapa, Najafi Fard, Cuzzi, Cimini, Grassi, Vanini, Di Rosa, Salemi, Nalli, Salmi, Repele, Altera, Maffongelli, Palazzolo, Vita, Leone, Puro, Capobianchi, Ippolito, Nicastri and Goletti. – notice: Copyright © 2021 Picchianti-Diamanti, Aiello, Laganà, Agrati, Castilletti, Meschi, Farroni, Lapa, Najafi Fard, Cuzzi, Cimini, Grassi, Vanini, Di Rosa, Salemi, Nalli, Salmi, Repele, Altera, Maffongelli, Palazzolo, Vita, Leone, Puro, Capobianchi, Ippolito, Nicastri and Goletti 2021 Picchianti-Diamanti, Aiello, Laganà, Agrati, Castilletti, Meschi, Farroni, Lapa, Najafi Fard, Cuzzi, Cimini, Grassi, Vanini, Di Rosa, Salemi, Nalli, Salmi, Repele, Altera, Maffongelli, Palazzolo, Vita, Leone, Puro, Capobianchi, Ippolito, Nicastri and Goletti |
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| DOI | 10.3389/fimmu.2021.740249 |
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| Keywords | COVID-19 antibody response T cell response biological therapy whole blood DMARD (disease modifying anti-rheumatic drug) rheumatoid arthritis mRNA vaccine |
| Language | English |
| License | Copyright © 2021 Picchianti-Diamanti, Aiello, Laganà, Agrati, Castilletti, Meschi, Farroni, Lapa, Najafi Fard, Cuzzi, Cimini, Grassi, Vanini, Di Rosa, Salemi, Nalli, Salmi, Repele, Altera, Maffongelli, Palazzolo, Vita, Leone, Puro, Capobianchi, Ippolito, Nicastri 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: Trine N. Jorgensen, Case Western Reserve University, United States Reviewed by: Balaji Banoth, St. Jude Children’s Research Hospital, United States; Cate Speake, Benaroya Research Institute, United States Members of INMI COVID-19 Vaccine Study Group are listed in the Acknowledgments ORCID: Alessandra Aiello, orcid.org/0000-0003-2681-9383; Chiara Farroni, orcid.org/0000-0002-2425-9936; Federica Repele, orcid.org/0000-0002-2780-4100; Anna Maria Gerarda Altera, orcid.org/0000-0002-6593-5232; Saied Najafi Fard, orcid.org/0000-0001-9957-8934; Valentina Vanini, orcid.org/0000-0001-8476-964X; Delia Goletti, orcid.org/0000-0001-8360-4376 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 |
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| PublicationTitle | Frontiers in immunology |
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| Title | ImmunosuppressiveTherapies Differently Modulate Humoral- and T-Cell-Specific Responses to COVID-19 mRNA Vaccine in Rheumatoid Arthritis Patients |
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