Longitudinal Postvaccine SARS-CoV-2 Immunoglobulin G Titers, Memory B-Cell Responses, and Risk of COVID-19 in Multiple Sclerosis Over 1 Year.

Humans SARS-CoV-2 COVID-19 / prevention & control Multiple Sclerosis Immunoglobulin G Cladribine Leukocytes, Mononuclear Prospective Studies Antigens, CD20 RNA, Messenger

Journal

Neurology(R) neuroimmunology & neuroinflammation
ISSN: 2332-7812
Titre abrégé: Neurol Neuroimmunol Neuroinflamm
Pays: United States
ID NLM: 101636388

Informations de publication

Date de publication:
01 2023
Historique:
received: 08 06 2022
accepted: 29 08 2022
entrez: 17 11 2022
pubmed: 18 11 2022
medline: 22 11 2022
Statut: epublish

Résumé

Some disease-modifying treatments impair response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccines in multiple sclerosis (MS), potentially increasing the risk of breakthrough infections. We aimed to investigate longitudinal SARS-CoV-2 antibody dynamics and memory B cells after 2 and 3 messenger RNA (mRNA) vaccine doses and their association with the risk of COVID-19 in patients with MS on different treatments over 1 year. Prospective observational cohort study in patients with MS undergoing SARS-CoV-2 mRNA vaccinations. Antispike (anti-S) immunoglobulin G (IgG) titers were measured by chemiluminescence microparticle immunoassay. Frequencies of spike-specific memory B cells were measured on polyclonal stimulation of peripheral blood mononuclear cells and screening of secreted antibodies by ELISA. We recruited 120 patients with MS (58 on anti-CD20 antibodies, 9 on sphingosine 1-phosphate (S1P) receptor modulators, 15 on cladribine, 24 on teriflunomide (TFL), and 14 untreated) and collected 392 samples up to 10.8 months after 2 vaccine doses. When compared with untreated patients, anti-CD20 antibodies (β = -2.07, Postvaccine anti-S IgG titers decrease over time regardless of MS treatment and are associated with breakthrough COVID-19. Both humoral and specific memory B-cell responses are diminished on S1P modulators. Within anti-CD20-treated patients, B-cell count at first vaccine determines anti-S IgG production, whereas postvaccine anti-CD20 infusions negatively affect spike-specific memory B cells.

Sections du résumé

BACKGROUND AND OBJECTIVES
Some disease-modifying treatments impair response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccines in multiple sclerosis (MS), potentially increasing the risk of breakthrough infections. We aimed to investigate longitudinal SARS-CoV-2 antibody dynamics and memory B cells after 2 and 3 messenger RNA (mRNA) vaccine doses and their association with the risk of COVID-19 in patients with MS on different treatments over 1 year.
METHODS
Prospective observational cohort study in patients with MS undergoing SARS-CoV-2 mRNA vaccinations. Antispike (anti-S) immunoglobulin G (IgG) titers were measured by chemiluminescence microparticle immunoassay. Frequencies of spike-specific memory B cells were measured on polyclonal stimulation of peripheral blood mononuclear cells and screening of secreted antibodies by ELISA.
RESULTS
We recruited 120 patients with MS (58 on anti-CD20 antibodies, 9 on sphingosine 1-phosphate (S1P) receptor modulators, 15 on cladribine, 24 on teriflunomide (TFL), and 14 untreated) and collected 392 samples up to 10.8 months after 2 vaccine doses. When compared with untreated patients, anti-CD20 antibodies (β = -2.07,
DISCUSSION
Postvaccine anti-S IgG titers decrease over time regardless of MS treatment and are associated with breakthrough COVID-19. Both humoral and specific memory B-cell responses are diminished on S1P modulators. Within anti-CD20-treated patients, B-cell count at first vaccine determines anti-S IgG production, whereas postvaccine anti-CD20 infusions negatively affect spike-specific memory B cells.

Identifiants

DOI: 10.1212/NXI.0000000000200043 PMID: 36396447 PMC: PMC9747147
pubmed: 36396447
pii: 10/1/e200043
doi: 10.1212/NXI.0000000000200043
pmc: PMC9747147
pii:
doi:

Substances chimiques

Immunoglobulin G 0
Cladribine 47M74X9YT5
Antigens, CD20 0
RNA, Messenger 0

Types de publication

Observational Study Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

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Auteurs

Giulio Disanto (G)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Alice Galante (A)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Marco Cantu' (M)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Rosaria Sacco (R)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Federico Mele (F)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Jennifer Jessica Eisler (JJ)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Franco Keller (F)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Enos Bernasconi (E)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Federica Sallusto (F)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Chiara Zecca (C)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland.

Claudio Gobbi (C)

From the Multiple Sclerosis Center (G.D., R.S., J.J.E., C.Z., C.G.), Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano; Institute for Research in Biomedicine (A.G., F.M., F.S.), Università Della Svizzera Italiana, Bellinzona; Institute of Laboratory Medicine (M.C., F.K.), Ente Ospedaliero Cantonale, Bellinzona; Department of Medicine (E.B.), Ente Ospedaliero Cantonale, Lugano; Faculty of Biomedical Sciences (E.B., F.S., C.Z., C.G.), Università Della Svizzera Italiana, Lugano; and Institute of Microbiology (F.S.), ETH Zurich, Switzerland. claudio.gobbi@eoc.ch.

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