Implications of disease-modifying therapies for multiple sclerosis on immune cells and response to COVID-19 vaccination

Front Immunol. 2024 Jul 15:15:1416464. doi: 10.3389/fimmu.2024.1416464. eCollection 2024.

Abstract

Introduction: Disease-modifying therapies (DMTs) have been shown to improve disease outcomes in multiple sclerosis (MS) patients. They may also impair the immune response to vaccines, including the SARS-CoV-2 vaccine. However, available data on both the intrinsic immune effects of DMTs and their influence on cellular response to the SARS-CoV-2 vaccine are still incomplete.

Methods: Here, we evaluated the immune cell effects of 3 DMTs on the response to mRNA SARS-CoV-2 vaccination by comparing MS patients treated with one specific therapy (fingolimod, dimethyl fumarate, or natalizumab) with both healthy controls and untreated patients. We profiled 23 B-cell traits, 57 T-cell traits, and 10 cytokines, both at basal level and after stimulation with a pool of SARS-CoV-2 spike peptides, in 79 MS patients, treated with DMTs or untreated, and 32 healthy controls. Measurements were made before vaccination and at three time points after immunization.

Results and discussion: MS patients treated with fingolimod showed the strongest immune cell dysregulation characterized by a reduction in all measured lymphocyte cell classes; the patients also had increased immune cell activation at baseline, accompanied by reduced specific immune cell response to the SARS-CoV-2 vaccine. Also, anti-spike specific B cells progressively increased over the three time points after vaccination, even when antibodies measured from the same samples instead showed a decline. Our findings demonstrate that repeated booster vaccinations in MS patients are crucial to overcoming the immune cell impairment caused by DMTs and achieving an immune response to the SARS-CoV-2 vaccine comparable to that of healthy controls.

Keywords: SARS-CoV-2; disease-modifying therapy; immune response; immune-phenotyping; multiple sclerosis.

MeSH terms

  • Adult
  • B-Lymphocytes / immunology
  • COVID-19 Vaccines* / immunology
  • COVID-19* / immunology
  • COVID-19* / prevention & control
  • Cytokines / metabolism
  • Dimethyl Fumarate* / pharmacology
  • Dimethyl Fumarate* / therapeutic use
  • Female
  • Fingolimod Hydrochloride* / pharmacology
  • Fingolimod Hydrochloride* / therapeutic use
  • Humans
  • Immunosuppressive Agents / therapeutic use
  • Male
  • Middle Aged
  • Multiple Sclerosis* / drug therapy
  • Multiple Sclerosis* / immunology
  • Natalizumab / therapeutic use
  • SARS-CoV-2* / immunology
  • T-Lymphocytes / immunology
  • Vaccination

Substances

  • COVID-19 Vaccines
  • Fingolimod Hydrochloride
  • Dimethyl Fumarate
  • Immunosuppressive Agents
  • Natalizumab
  • Cytokines

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The study was supported by the Italian Foundation for Multiple Sclerosis- FISM (Grant N. 22021/Special/002 and 2021/C19-R-Single/010) and by the Intramural Research Program of the US National Institutes of Health, National Institute on Aging (No. HHSN271201600005C).