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Article

Dynamic Evolution of Humoral and T-Cell Specific Immune Response to COVID-19 mRNA Vaccine in Patients with Multiple Sclerosis Followed until the Booster Dose

by
Serena Ruggieri
1,2,†,
Alessandra Aiello
3,†,
Carla Tortorella
1,
Assunta Navarra
4,
Valentina Vanini
3,5,
Silvia Meschi
6,
Daniele Lapa
6,
Shalom Haggiag
1,
Luca Prosperini
1,
Gilda Cuzzi
3,
Andrea Salmi
3,
Maria Esmeralda Quartuccio
1,
Anna Maria Gerarda Altera
3,
Anna Rosa Garbuglia
6,
Tommaso Ascoli Bartoli
7,
Simonetta Galgani
1,
Stefania Notari
8,
Chiara Agrati
8,9,
Vincenzo Puro
10,
Emanuele Nicastri
7,
Claudio Gasperini
1 and
Delia Goletti
3,*add Show full author list remove Hide full author list
1
Department of Neurosciences, San Camillo Forlanini Hospital, 00152 Rome, Italy
2
Department of Human Neurosciences, Sapienza University of Rome, 00185 Rome, Italy
3
Translational Research Unit, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS, 00149 Rome, Italy
4
Clinical Epidemiology Unit, National Institute for Infectious Disease Lazzaro Spallanzani-IRCCS, 00149 Rome, Italy
5
UOS Professioni Sanitarie Tecniche, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS, 00149 Rome, Italy
6
Laboratory of Virology, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS, 00149 Rome, Italy
7
Clinical Division of Infectious Diseases, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS, 00149 Rome, Italy
8
Cellular Immunology Laboratory, National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS, 00149 Rome, Italy
9
Department of Pediatric Hematology and Oncology, IRCCS Bambino Gesù Children’s Hospital, 00146 Rome, Italy
10
UOC Emerging Infections and Centro di Riferimento AIDS (CRAIDS), National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS, 00149 Rome, Italy
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work and shared the first authorship.
Int. J. Mol. Sci. 2023, 24(10), 8525; https://doi.org/10.3390/ijms24108525
Submission received: 20 April 2023 / Revised: 5 May 2023 / Accepted: 8 May 2023 / Published: 10 May 2023
(This article belongs to the Special Issue COVID-19 Pandemic: Therapeutic Strategies and Vaccines)
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Abstract

This study characterizes antibody and T-cell immune responses over time until the booster dose of COronaVIrus Disease 2019 (COVID-19) vaccines in patients with multiple sclerosis (PwMS) undergoing different disease-modifying treatments (DMTs). We prospectively enrolled 134 PwMS and 99 health care workers (HCWs) having completed the two-dose schedule of a COVID-19 mRNA vaccine within the last 2–4 weeks (T0) and followed them 24 weeks after the first dose (T1) and 4–6 weeks after the booster (T2). PwMS presented a significant reduction in the seroconversion rate and anti-receptor-binding domain (RBD)-Immunoglobulin (IgG) titers from T0 to T1 (p < 0.0001) and a significant increase from T1 to T2 (p < 0.0001). The booster dose in PwMS showed a good improvement in the serologic response, even greater than HCWs, as it promoted a significant five-fold increase of anti-RBD-IgG titers compared with T0 (p < 0.0001). Similarly, the T-cell response showed a significant 1.5- and 3.8-fold increase in PwMS at T2 compared with T0 (p = 0.013) and T1 (p < 0.0001), respectively, without significant modulation in the number of responders. Regardless of the time elapsed since vaccination, most ocrelizumab- (77.3%) and fingolimod-treated patients (93.3%) showed only a T-cell-specific or humoral-specific response, respectively. The booster dose reinforces humoral- and cell-mediated-specific immune responses and highlights specific DMT-induced immune frailties, suggesting the need for specifically tailored strategies for immune-compromised patients to provide primary prophylaxis, early SARS-CoV-2 detection and the timely management of COVID-19 antiviral treatments.
Keywords: SARS-CoV-2; COVID-19; mRNA vaccines; multiple sclerosis; antibody response; T-cell response SARS-CoV-2; COVID-19; mRNA vaccines; multiple sclerosis; antibody response; T-cell response

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MDPI and ACS Style

Ruggieri, S.; Aiello, A.; Tortorella, C.; Navarra, A.; Vanini, V.; Meschi, S.; Lapa, D.; Haggiag, S.; Prosperini, L.; Cuzzi, G.; et al. Dynamic Evolution of Humoral and T-Cell Specific Immune Response to COVID-19 mRNA Vaccine in Patients with Multiple Sclerosis Followed until the Booster Dose. Int. J. Mol. Sci. 2023, 24, 8525. https://doi.org/10.3390/ijms24108525

AMA Style

Ruggieri S, Aiello A, Tortorella C, Navarra A, Vanini V, Meschi S, Lapa D, Haggiag S, Prosperini L, Cuzzi G, et al. Dynamic Evolution of Humoral and T-Cell Specific Immune Response to COVID-19 mRNA Vaccine in Patients with Multiple Sclerosis Followed until the Booster Dose. International Journal of Molecular Sciences. 2023; 24(10):8525. https://doi.org/10.3390/ijms24108525

Chicago/Turabian Style

Ruggieri, Serena, Alessandra Aiello, Carla Tortorella, Assunta Navarra, Valentina Vanini, Silvia Meschi, Daniele Lapa, Shalom Haggiag, Luca Prosperini, Gilda Cuzzi, and et al. 2023. "Dynamic Evolution of Humoral and T-Cell Specific Immune Response to COVID-19 mRNA Vaccine in Patients with Multiple Sclerosis Followed until the Booster Dose" International Journal of Molecular Sciences 24, no. 10: 8525. https://doi.org/10.3390/ijms24108525

APA Style

Ruggieri, S., Aiello, A., Tortorella, C., Navarra, A., Vanini, V., Meschi, S., Lapa, D., Haggiag, S., Prosperini, L., Cuzzi, G., Salmi, A., Quartuccio, M. E., Altera, A. M. G., Garbuglia, A. R., Ascoli Bartoli, T., Galgani, S., Notari, S., Agrati, C., Puro, V., ... Goletti, D. (2023). Dynamic Evolution of Humoral and T-Cell Specific Immune Response to COVID-19 mRNA Vaccine in Patients with Multiple Sclerosis Followed until the Booster Dose. International Journal of Molecular Sciences, 24(10), 8525. https://doi.org/10.3390/ijms24108525

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