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March 2022; 9 (2) ArticleOpen Access

Humoral and Cellular Responses to SARS-CoV-2 in Convalescent COVID-19 Patients With Multiple Sclerosis

View ORCID ProfileAna Zabalza, View ORCID ProfileGeorgina Arrambide, View ORCID ProfilePaula Tagliani, View ORCID ProfileSimón Cárdenas-Robledo, View ORCID ProfileSusana Otero-Romero, View ORCID ProfileJuliana Esperalba, View ORCID ProfileCandela Fernandez-Naval, Jesus Trocoli Campuzano, View ORCID ProfileMónica Martínez Gallo, View ORCID ProfileMireia Castillo, Mercè Bonastre, View ORCID ProfileMireia Resina Sallés, Jordina Beltran, Pere Carbonell-Mirabent, View ORCID ProfileMarta Rodríguez-Barranco, Samuel López-Maza, Pedro José Melgarejo Otálora, View ORCID ProfileMariano Ruiz-Ortiz, View ORCID ProfileAgustin Pappolla, View ORCID ProfileBreogán Rodríguez Acevedo, View ORCID ProfileLuciana Midaglia, View ORCID ProfileAngela Vidal-Jordana, View ORCID ProfileAlvaro Cobo-Calvo, View ORCID ProfileCarmen Tur, View ORCID ProfileIngrid Galán, View ORCID ProfileJoaquín Castilló, View ORCID ProfileJordi Río, View ORCID ProfileCarmen Espejo, View ORCID ProfileManuel Comabella, View ORCID ProfileCarlos Nos, View ORCID ProfileJaume Sastre-Garriga, View ORCID ProfileMar Tintore, View ORCID ProfileXavier Montalban
First published February 1, 2022, DOI: https://doi.org/10.1212/NXI.0000000000001143
Ana Zabalza
From the Servei de Neurologia-Neuroimmunologia (A.Z., G.A., P.T., S.C.-R., S.O.-R., M. Castillo, M.B., M.R.S., J.B., P.C.-M., M.R.-B., S.L.-M., A.P., B.R.A., L.M., A.V.-J., A.C.-C., C.T., I.G., J.C., J.R., C.E., M. Comabella, C.N., J.S.-G., M.T., X.M.), and Preventive Medicine and Epidemiology Department (S.O.-R.), Centre d'Esclerosi Múltiple de Catalunya (Cemcat), Vall d'Hebron Institut de Recerca, Hospital Universitari Vall d'Hebron, Departament de Medicina, Universitat Autònoma de Barcelona; Microbiology Department (J.E., C.F.-N., J.T.C.), Vall d'Hebron University Hospital, Vall d'Hebron Barcelona Hospital Campus, Universitat Autònoma de Barcelona; Immunology Division (M.M.G.), Hospital Universitari Vall d'Hebron and Diagnostic Immunology Research Group, Vall d'Hebron Research Institute (VHIR), Barcelona; Department of Neurology (P.J.M.O.), Hospital General Universitario Gregorio Marañón, Madrid; and Department of Neurology (M.R.-O.), Hospital Universitario 12 de Octubre, Madrid, Spain.
MD
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Georgina Arrambide
MD, PhD
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  • For correspondence: garrambide@cem-cat.org
Paula Tagliani
MD
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Simón Cárdenas-Robledo
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Susana Otero-Romero
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Juliana Esperalba
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Candela Fernandez-Naval
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Jesus Trocoli Campuzano
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Mónica Martínez Gallo
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Mireia Castillo
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Mercè Bonastre
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Mireia Resina Sallés
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Jordina Beltran
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Pere Carbonell-Mirabent
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Marta Rodríguez-Barranco
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Samuel López-Maza
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Pedro José Melgarejo Otálora
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Mariano Ruiz-Ortiz
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Agustin Pappolla
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Breogán Rodríguez Acevedo
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Luciana Midaglia
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Angela Vidal-Jordana
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Alvaro Cobo-Calvo
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Carmen Tur
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Ingrid Galán
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Joaquín Castilló
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Jordi Río
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Carmen Espejo
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Manuel Comabella
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Carlos Nos
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Jaume Sastre-Garriga
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Mar Tintore
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Xavier Montalban
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Full PDF
Citation
Humoral and Cellular Responses to SARS-CoV-2 in Convalescent COVID-19 Patients With Multiple Sclerosis
Ana Zabalza, Georgina Arrambide, Paula Tagliani, Simón Cárdenas-Robledo, Susana Otero-Romero, Juliana Esperalba, Candela Fernandez-Naval, Jesus Trocoli Campuzano, Mónica Martínez Gallo, Mireia Castillo, Mercè Bonastre, Mireia Resina Sallés, Jordina Beltran, Pere Carbonell-Mirabent, Marta Rodríguez-Barranco, Samuel López-Maza, Pedro José Melgarejo Otálora, Mariano Ruiz-Ortiz, Agustin Pappolla, Breogán Rodríguez Acevedo, Luciana Midaglia, Angela Vidal-Jordana, Alvaro Cobo-Calvo, Carmen Tur, Ingrid Galán, Joaquín Castilló, Jordi Río, Carmen Espejo, Manuel Comabella, Carlos Nos, Jaume Sastre-Garriga, Mar Tintore, Xavier Montalban
Neurol Neuroimmunol Neuroinflamm Mar 2022, 9 (2) e1143; DOI: 10.1212/NXI.0000000000001143

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Abstract

Background and Objectives Information about humoral and cellular responses to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and antibody persistence in convalescent (COVID-19) patients with multiple sclerosis (PwMS) is scarce. The objectives of this study were to investigate factors influencing humoral and cellular responses to SARS-CoV-2 and its persistence in convalescent COVID-19 PwMS.

Methods This is a retrospective study of confirmed COVID-19 convalescent PwMS identified between February 2020 and May 2021 by SARS-CoV-2 antibody testing. We examined relationships between demographics, MS characteristics, disease-modifying therapy (DMT), and humoral (immunoglobulin G against spike and nucleocapsid proteins) and cellular (interferon-gamma [IFN-γ]) responses to SARS-CoV-2.

Results A total of 121 (83.45%) of 145 PwMS were seropositive, and 25/42 (59.5%) presented a cellular response up to 13.1 months after COVID-19. Anti–CD20-treated patients had lower antibody titers than those under other DMTs (p < 0.001), but severe COVID-19 and a longer time from last infusion increased the likelihood of producing a humoral response. IFN-γ levels did not differ among DMT. Five of 7 (71.4%) anti-–CD20-treated seronegative patients had a cellular response. The humoral response persisted for more than 6 months in 41/56(81.13%) PwMS. In multivariate analysis, seropositivity decreased due to anti-CD20 therapy (OR 0.08 [95% CI 0.01–0.55]) and increased in males (OR 3.59 [1.02–12.68]), whereas the cellular response decreased in those with progressive disease (OR 0.04 [0.001–0.88]). No factors were associated with antibody persistence.

Discussion Humoral and cellular responses to SARS-CoV-2 are present in COVID-19 convalescent PwMS up to 13.10 months after COVID-19. The humoral response decreases under anti-CD20 treatment, although the cellular response can be detected in anti–CD20-treated patients, even in the absence of antibodies.

Glossary

CIS=
clinically isolated syndrome;
CLIA=
chemiluminescence immunoassay;
COVID-19=
coronavirus disease 2019;
DMT=
disease-modifying therapy;
EDSS=
Expanded Disability Status Scale;
IFN=
interferon;
Ig=
immunoglobulin;
IGRA=
interferon-gamma release immunoassay;
IQR=
interquartile range;
MS=
multiple sclerosis;
PwMS=
patients with MS;
RRMS=
relapsing-remitting MS;
RT-PCR=
reverse transcription–PCR;
SARS-CoV-2=
severe acute respiratory syndrome coronavirus 2

Footnotes

  • Go to Neurology.org/NN for full disclosures. Funding information is provided at the end of the article.

  • ↵* These authors contributed equally to this work (co–senior authors).

  • The Article Processing Charge was funded by the authors.

  • Received August 20, 2021.
  • Accepted in final form December 21, 2021.
  • Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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