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Primary SARS-CoV-2 infection in patients with immune-mediated inflammatory diseases: long-term humoral immune responses and effects on disease activity

BACKGROUND: Patients with immune-mediated inflammatory diseases (IMIDs) on immunosuppressants (ISPs) may have impaired long-term humoral immune responses and increased disease activity after SARS-CoV-2 infection. We aimed to investigate long-term humoral immune responses against SARS-CoV-2 and incre...

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Autores principales: van Dam, Koos P. J., Volkers, Adriaan G., Wieske, Luuk, Stalman, Eileen W., Kummer, Laura Y. L., van Kempen, Zoé L. E., Killestein, Joep, Tas, Sander W., Boekel, Laura, Wolbink, Gerrit J., van der Kooi, Anneke J., Raaphorst, Joost, Takkenberg, R. Bart, D’Haens, Geert R. A. M., Spuls, Phyllis I., Bekkenk, Marcel W., Musters, Annelie H., Post, Nicoline F., Bosma, Angela L., Hilhorst, Marc L., Vegting, Yosta, Bemelman, Frederike J., Voskuyl, Alexandre E., Broens, Bo, Sanchez, Agner Parra, van Els, Cécile A. C. M., de Wit, Jelle, Rutgers, Abraham, de Leeuw, Karina, Horváth, Barbara, Verschuuren, Jan J. G. M., Ruiter, Annabel M., van Ouwerkerk, Lotte, van der Woude, Diane, Allaart, Renée C. F., Teng, Y. K. Onno, van Paassen, Pieter, Busch, Matthias H., Jallah, Papay B. P., Brusse, Esther, van Doorn, Pieter A., Baars, Adája E., Hijnen, Dirk Jan, Schreurs, Corine R. G., van der Pol, W. Ludo, Goedee, H. Stephan, Steenhuis, Maurice, Keijzer, Sofie, Keijser, Jim B. D., Cristianawati, Olvi, ten Brinke, Anja, Verstegen, Niels J. M., van Ham, S. Marieke, Rispens, Theo, Kuijpers, Taco W., Löwenberg, Mark, Eftimov, Filip
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10189216/
https://www.ncbi.nlm.nih.gov/pubmed/37198536
http://dx.doi.org/10.1186/s12879-023-08298-6
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author van Dam, Koos P. J.
Volkers, Adriaan G.
Wieske, Luuk
Stalman, Eileen W.
Kummer, Laura Y. L.
van Kempen, Zoé L. E.
Killestein, Joep
Tas, Sander W.
Boekel, Laura
Wolbink, Gerrit J.
van der Kooi, Anneke J.
Raaphorst, Joost
Takkenberg, R. Bart
D’Haens, Geert R. A. M.
Spuls, Phyllis I.
Bekkenk, Marcel W.
Musters, Annelie H.
Post, Nicoline F.
Bosma, Angela L.
Hilhorst, Marc L.
Vegting, Yosta
Bemelman, Frederike J.
Voskuyl, Alexandre E.
Broens, Bo
Sanchez, Agner Parra
van Els, Cécile A. C. M.
de Wit, Jelle
Rutgers, Abraham
de Leeuw, Karina
Horváth, Barbara
Verschuuren, Jan J. G. M.
Ruiter, Annabel M.
van Ouwerkerk, Lotte
van der Woude, Diane
Allaart, Renée C. F.
Teng, Y. K. Onno
van Paassen, Pieter
Busch, Matthias H.
Jallah, Papay B. P.
Brusse, Esther
van Doorn, Pieter A.
Baars, Adája E.
Hijnen, Dirk Jan
Schreurs, Corine R. G.
van der Pol, W. Ludo
Goedee, H. Stephan
Steenhuis, Maurice
Keijzer, Sofie
Keijser, Jim B. D.
Cristianawati, Olvi
ten Brinke, Anja
Verstegen, Niels J. M.
van Ham, S. Marieke
Rispens, Theo
Kuijpers, Taco W.
Löwenberg, Mark
Eftimov, Filip
author_facet van Dam, Koos P. J.
Volkers, Adriaan G.
Wieske, Luuk
Stalman, Eileen W.
Kummer, Laura Y. L.
van Kempen, Zoé L. E.
Killestein, Joep
Tas, Sander W.
Boekel, Laura
Wolbink, Gerrit J.
van der Kooi, Anneke J.
Raaphorst, Joost
Takkenberg, R. Bart
D’Haens, Geert R. A. M.
Spuls, Phyllis I.
Bekkenk, Marcel W.
Musters, Annelie H.
Post, Nicoline F.
Bosma, Angela L.
Hilhorst, Marc L.
Vegting, Yosta
Bemelman, Frederike J.
Voskuyl, Alexandre E.
Broens, Bo
Sanchez, Agner Parra
van Els, Cécile A. C. M.
de Wit, Jelle
Rutgers, Abraham
de Leeuw, Karina
Horváth, Barbara
Verschuuren, Jan J. G. M.
Ruiter, Annabel M.
van Ouwerkerk, Lotte
van der Woude, Diane
Allaart, Renée C. F.
Teng, Y. K. Onno
van Paassen, Pieter
Busch, Matthias H.
Jallah, Papay B. P.
Brusse, Esther
van Doorn, Pieter A.
Baars, Adája E.
Hijnen, Dirk Jan
Schreurs, Corine R. G.
van der Pol, W. Ludo
Goedee, H. Stephan
Steenhuis, Maurice
Keijzer, Sofie
Keijser, Jim B. D.
Cristianawati, Olvi
ten Brinke, Anja
Verstegen, Niels J. M.
van Ham, S. Marieke
Rispens, Theo
Kuijpers, Taco W.
Löwenberg, Mark
Eftimov, Filip
author_sort van Dam, Koos P. J.
collection PubMed
description BACKGROUND: Patients with immune-mediated inflammatory diseases (IMIDs) on immunosuppressants (ISPs) may have impaired long-term humoral immune responses and increased disease activity after SARS-CoV-2 infection. We aimed to investigate long-term humoral immune responses against SARS-CoV-2 and increased disease activity after a primary SARS-CoV-2 infection in unvaccinated IMID patients on ISPs. METHODS: IMID patients on active treatment with ISPs and controls (i.e. IMID patients not on ISP and healthy controls) with a confirmed SARS-CoV-2 infection before first vaccination were included from an ongoing prospective cohort study (T2B! study). Clinical data on infections and increased disease activity were registered using electronic surveys and health records. A serum sample was collected before first vaccination to measure SARS-CoV-2 anti-receptor-binding domain (RBD) antibodies. RESULTS: In total, 193 IMID patients on ISP and 113 controls were included. Serum samples from 185 participants were available, with a median time of 173 days between infection and sample collection. The rate of seropositive IMID patients on ISPs was 78% compared to 100% in controls (p < 0.001). Seropositivity rates were lowest in patients on anti-CD20 (40.0%) and anti-tumor necrosis factor (TNF) agents (60.5%), as compared to other ISPs (p < 0.001 and p < 0.001, respectively). Increased disease activity after infection was reported by 68 of 260 patients (26.2%; 95% CI 21.2–31.8%), leading to ISP intensification in 6 out of these 68 patients (8.8%). CONCLUSION: IMID patients using ISPs showed reduced long-term humoral immune responses after primary SARS-CoV-2 infection, which was mainly attributed to treatment with anti-CD20 and anti-TNF agents. Increased disease activity after SARS-CoV-2 infection was reported commonly, but was mostly mild. TRIAL REGISTRATION: NL74974.018.20, Trial ID: NL8900. Registered on 9 September 2020. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12879-023-08298-6.
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spelling pubmed-101892162023-05-18 Primary SARS-CoV-2 infection in patients with immune-mediated inflammatory diseases: long-term humoral immune responses and effects on disease activity van Dam, Koos P. J. Volkers, Adriaan G. Wieske, Luuk Stalman, Eileen W. Kummer, Laura Y. L. van Kempen, Zoé L. E. Killestein, Joep Tas, Sander W. Boekel, Laura Wolbink, Gerrit J. van der Kooi, Anneke J. Raaphorst, Joost Takkenberg, R. Bart D’Haens, Geert R. A. M. Spuls, Phyllis I. Bekkenk, Marcel W. Musters, Annelie H. Post, Nicoline F. Bosma, Angela L. Hilhorst, Marc L. Vegting, Yosta Bemelman, Frederike J. Voskuyl, Alexandre E. Broens, Bo Sanchez, Agner Parra van Els, Cécile A. C. M. de Wit, Jelle Rutgers, Abraham de Leeuw, Karina Horváth, Barbara Verschuuren, Jan J. G. M. Ruiter, Annabel M. van Ouwerkerk, Lotte van der Woude, Diane Allaart, Renée C. F. Teng, Y. K. Onno van Paassen, Pieter Busch, Matthias H. Jallah, Papay B. P. Brusse, Esther van Doorn, Pieter A. Baars, Adája E. Hijnen, Dirk Jan Schreurs, Corine R. G. van der Pol, W. Ludo Goedee, H. Stephan Steenhuis, Maurice Keijzer, Sofie Keijser, Jim B. D. Cristianawati, Olvi ten Brinke, Anja Verstegen, Niels J. M. van Ham, S. Marieke Rispens, Theo Kuijpers, Taco W. Löwenberg, Mark Eftimov, Filip BMC Infect Dis Research Article BACKGROUND: Patients with immune-mediated inflammatory diseases (IMIDs) on immunosuppressants (ISPs) may have impaired long-term humoral immune responses and increased disease activity after SARS-CoV-2 infection. We aimed to investigate long-term humoral immune responses against SARS-CoV-2 and increased disease activity after a primary SARS-CoV-2 infection in unvaccinated IMID patients on ISPs. METHODS: IMID patients on active treatment with ISPs and controls (i.e. IMID patients not on ISP and healthy controls) with a confirmed SARS-CoV-2 infection before first vaccination were included from an ongoing prospective cohort study (T2B! study). Clinical data on infections and increased disease activity were registered using electronic surveys and health records. A serum sample was collected before first vaccination to measure SARS-CoV-2 anti-receptor-binding domain (RBD) antibodies. RESULTS: In total, 193 IMID patients on ISP and 113 controls were included. Serum samples from 185 participants were available, with a median time of 173 days between infection and sample collection. The rate of seropositive IMID patients on ISPs was 78% compared to 100% in controls (p < 0.001). Seropositivity rates were lowest in patients on anti-CD20 (40.0%) and anti-tumor necrosis factor (TNF) agents (60.5%), as compared to other ISPs (p < 0.001 and p < 0.001, respectively). Increased disease activity after infection was reported by 68 of 260 patients (26.2%; 95% CI 21.2–31.8%), leading to ISP intensification in 6 out of these 68 patients (8.8%). CONCLUSION: IMID patients using ISPs showed reduced long-term humoral immune responses after primary SARS-CoV-2 infection, which was mainly attributed to treatment with anti-CD20 and anti-TNF agents. Increased disease activity after SARS-CoV-2 infection was reported commonly, but was mostly mild. TRIAL REGISTRATION: NL74974.018.20, Trial ID: NL8900. Registered on 9 September 2020. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12879-023-08298-6. BioMed Central 2023-05-17 /pmc/articles/PMC10189216/ /pubmed/37198536 http://dx.doi.org/10.1186/s12879-023-08298-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
van Dam, Koos P. J.
Volkers, Adriaan G.
Wieske, Luuk
Stalman, Eileen W.
Kummer, Laura Y. L.
van Kempen, Zoé L. E.
Killestein, Joep
Tas, Sander W.
Boekel, Laura
Wolbink, Gerrit J.
van der Kooi, Anneke J.
Raaphorst, Joost
Takkenberg, R. Bart
D’Haens, Geert R. A. M.
Spuls, Phyllis I.
Bekkenk, Marcel W.
Musters, Annelie H.
Post, Nicoline F.
Bosma, Angela L.
Hilhorst, Marc L.
Vegting, Yosta
Bemelman, Frederike J.
Voskuyl, Alexandre E.
Broens, Bo
Sanchez, Agner Parra
van Els, Cécile A. C. M.
de Wit, Jelle
Rutgers, Abraham
de Leeuw, Karina
Horváth, Barbara
Verschuuren, Jan J. G. M.
Ruiter, Annabel M.
van Ouwerkerk, Lotte
van der Woude, Diane
Allaart, Renée C. F.
Teng, Y. K. Onno
van Paassen, Pieter
Busch, Matthias H.
Jallah, Papay B. P.
Brusse, Esther
van Doorn, Pieter A.
Baars, Adája E.
Hijnen, Dirk Jan
Schreurs, Corine R. G.
van der Pol, W. Ludo
Goedee, H. Stephan
Steenhuis, Maurice
Keijzer, Sofie
Keijser, Jim B. D.
Cristianawati, Olvi
ten Brinke, Anja
Verstegen, Niels J. M.
van Ham, S. Marieke
Rispens, Theo
Kuijpers, Taco W.
Löwenberg, Mark
Eftimov, Filip
Primary SARS-CoV-2 infection in patients with immune-mediated inflammatory diseases: long-term humoral immune responses and effects on disease activity
title Primary SARS-CoV-2 infection in patients with immune-mediated inflammatory diseases: long-term humoral immune responses and effects on disease activity
title_full Primary SARS-CoV-2 infection in patients with immune-mediated inflammatory diseases: long-term humoral immune responses and effects on disease activity
title_fullStr Primary SARS-CoV-2 infection in patients with immune-mediated inflammatory diseases: long-term humoral immune responses and effects on disease activity
title_full_unstemmed Primary SARS-CoV-2 infection in patients with immune-mediated inflammatory diseases: long-term humoral immune responses and effects on disease activity
title_short Primary SARS-CoV-2 infection in patients with immune-mediated inflammatory diseases: long-term humoral immune responses and effects on disease activity
title_sort primary sars-cov-2 infection in patients with immune-mediated inflammatory diseases: long-term humoral immune responses and effects on disease activity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10189216/
https://www.ncbi.nlm.nih.gov/pubmed/37198536
http://dx.doi.org/10.1186/s12879-023-08298-6
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