Real-world data on the Immunity Response to the COVID-19 Vaccine among Patients with Central Nervous System Immunological Diseases

Immune Response to COVID-19 Vaccine in CNS Immunological Disease

Authors

  • Punchika Kosiyakul Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand / Siriraj Neuroimmunology Center, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand / Department of Research and Development, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand
  • Jiraporn Jitprapaikulsan Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand / Siriraj Neuroimmunology Center, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Ekdanai Uawithya Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Patimaporn Wongprompitak Department of Immunology, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Chutikarn Chaimayo Department of Microbiology, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Navin Horthongkham Department of Microbiology, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Nasikarn Angkasekwinai Division of Infectious Disease and Tropical Medicine, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Nanthaya Tisavipat Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand / Siriraj Neuroimmunology Center, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Naraporn Prayoonwiwat Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand / Siriraj Neuroimmunology Center, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Natthapon Rattanathamsakul Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand / Siriraj Neuroimmunology Center, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand / Department of Research and Development, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand
  • Kanokwan Boonyapisit Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Theerawat Kumutpongpanich Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Onpawee Sangsai Siriraj Neuroimmunology Center, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Kamonchanok Aueaphatthanawong Siriraj Neuroimmunology Center, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Jirawan Budkum Siriraj Neuroimmunology Center, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand
  • Sasitorn Siritho Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand / Siriraj Neuroimmunology Center, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, 10700, Thailand / Bumrungrad International Hospital, Bangkok 10110, Thailand

DOI:

https://doi.org/10.33192/smj.v76i2.266638

Keywords:

neuromyelitis optica spectrum disorder, multiple sclerosis, COVID-19 vaccine, immunosuppressant, humoral immune response

Abstract

Objective: The effects of immunotherapies on the immune response to various regimens of SARS-CoV-2 vaccines in patients with autoimmune neurological disease have been demonstrated in limited data. Thus, we evaluated the immune responses in each platform of COVID-19 vaccination between patients with autoimmune neurological disease and a healthy population.

Materials and Methods: We conducted a prospective observational study. We collected serum from patients with autoimmune neurological diseases to perform serological methods using anti-RBD IgG assay, neutralizing antibodies assay, and interferon SARS-CoV-2 immunoassay. Serological response level was analyzed by platforms of vaccines and types of immune modifying therapy.

Results: Fifty-eight patients had tested for an anti-RBD IgG response, and those receiving no immunotherapy/ healthy controls had the highest median anti-RBD IgG levels amongst immunotherapy statuses. Rituximab in those who received inactivated or mRNA vaccine regimens had the lowest antibody level compared with other immunotherapies. In vector-based vaccine regimens, significant reductions of anti-RBD IgG response were observed in all other immunotherapy groups except for azathioprine, with the greatest difference seen compared to rituximab. Thirty-five patients with positive anti-RBD responses were further tested for neutralizing antibodies. The mRNA vaccine regimen demonstrated the highest inhibition percentage among the Delta and Omicron variants. Twentytwo patients were tested for T cell responses, with no significant difference in T-cell activity across all groups.

Conclusion: We have demonstrated a significant decrease in antibody response against SARS-CoV-2 in patients with autoimmune neurological diseases receiving immunotherapies compared to a healthy population, especially for patients taking rituximab.

References

Andrews N, Stowe J, Kirsebom F, Toffa S, Rickeard T, Gallagher E, et al. Covid-19 Vaccine Effectiveness against the Omicron (B.1.1.529) Variant. N Engl J Med. 2022;386(16):1532-46.

Jara A, Undurraga EA, Gonzalez C, Paredes F, Fontecilla T, Jara G, et al. Effectiveness of an Inactivated SARS-CoV-2 Vaccine in Chile. N Engl J Med. 2021;385(10):875-84.

Lopez Bernal J, Andrews N, Gower C, Robertson C, Stowe J, Tessier E, et al. Effectiveness of the Pfizer-BioNTech and Oxford-AstraZeneca vaccines on covid-19 related symptoms, hospital admissions, and mortality in older adults in England: test negative case-control study. BMJ. 2021;373:n1088.

Frenck RW, Jr., Klein NP, Kitchin N, Gurtman A, Absalon J, Lockhart S, et al. Safety, Immunogenicity, and Efficacy of the BNT162b2 Covid-19 Vaccine in Adolescents. N Engl J Med. 2021;385(3):239-50.

Tisavipat N, Jitpratoom P, Siritho S, Prayoonwiwat N, Apiwattanakul M, Boonyasiri A, et al. The epidemiology and burden of neuromyelitis optica spectrum disorder, multiple sclerosis, and MOG antibody-associated disease in a province in Thailand: A population-based study. Mult Scler Relat Disord. 2023;70:104511.

Hor JY, Asgari N, Nakashima I, Broadley SA, Leite MI, Kissani N, et al. Epidemiology of Neuromyelitis Optica Spectrum Disorder and Its Prevalence and Incidence Worldwide. Front Neurol. 2020;11:501.

Holroyd K, Vogel A, Lynch K, Gazdag B, Voghel M, Alakel N, et al. Neuromyelitis optica testing and treatment: Availability and affordability in 60 countries. Mult Scler Relat Disord. 2019;33:44-50.

Mathew T, John SK, Kamath V, Murgod U, Thomas K, Baptist AA, et al. Efficacy and safety of rituximab in multiple sclerosis: Experience from a developing country. Mult Scler Relat Disord. 2020;43:102210.

Zheng C, Kar I, Chen CK, Sau C, Woodson S, Serra A, et al. Multiple Sclerosis Disease-Modifying Therapy and the COVID-19 Pandemic: Implications on the Risk of Infection and Future Vaccination. CNS Drugs. 2020;34(9):879-96.

Deepak P, Kim W, Paley MA, Yang M, Carvidi AB, Demissie EG, et al. Effect of Immunosuppression on the Immunogenicity of mRNA Vaccines to SARS-CoV-2: A Prospective Cohort Study. Ann Intern Med. 2021;174(11):1572-85.

Louapre C, Ibrahim M, Maillart E, Abdi B, Papeix C, Stankoff B, et al. Anti-CD20 therapies decrease humoral immune response to SARS-CoV-2 in patients with multiple sclerosis or neuromyelitis optica spectrum disorders. J Neurol Neurosurg Psychiatry. 2022;93(1):24-31.

Angkasekwinai N, Sewatanon J, Niyomnaitham S, Phumiamorn S, Sukapirom K, Sapsutthipas S, et al. Comparison of safety and immunogenicity of CoronaVac and ChAdOx1 against the SARS-CoV-2 circulating variants of concern (Alpha, Delta, Beta) in Thai healthcare workers. Vaccine X. 2022;10:100153.

Angkasekwinai N, Niyomnaitham S, Sewatanon J, Phumiamorn S, Sukapirom K, Senawong S, et al. The immunogenicity and reactogenicity of four COVID-19 booster vaccinations against SARS-CoV-2 variants of concerns (Delta, Beta, and Omicron) following CoronaVac or ChAdOx1 nCoV-19 primary series. 2022.

Department of Disease Control MoPH, Thailand. Guidelines for vaccination against COVID-19 in Thailand - 2021 epidemic situation 2022 [Available from: https://ddc.moph.go.th/vaccine-covid19/getFiles/11/1628849610213.pdf.

Hassold N, Brichler S, Ouedraogo E, Leclerc D, Carroue S, Gater Y, et al. Impaired antibody response to COVID-19 vaccination in advanced HIV infection. AIDS. 2022;36(4):F1-F5.

Company NGB. Instruction for use: cPass™ SARS-CoV-2 Neutralization Antibody Detection Kit 2022 [cited 2022 26 August]. Available from: https://www.genscript.com/gsfiles/techfiles/GS-SOP-CPTS001G-05_L00847-C.pdf?1109908894.

QIAGEN Company. Instructions for use: QuantiFERON SARS-CoV-2 ELISA Kit [Internet]. 2022 [cited 2022 Aug 26]. Available from: https://www.qiagen.com/at/resources/download.aspx?id=3d27842e-c811-442c-bcad-a9d42945e59c&lang=en.

Johnson SA, Phillips E, Adele S, Longet S, Malone T, Mason C, et al. Evaluation of QuantiFERON SARS-CoV-2 interferon- release assay following SARS-CoV-2 infection and vaccination. Clin Exp Immunol. 2023.

GraphPad Software Company. Prism: a statistical analysis software [Internet]. 2022 [cited 2022 Aug 26]. Available from: https://www.graphpad.com/scientific-software/prism.

Coyle PK, Gocke A, Vignos M, Newsome SD. Vaccine Considerations for Multiple Sclerosis in the COVID-19 Era. Adv Ther. 2021;38(7):3550-88.

Buchan SA, Chung H, Brown KA, Austin PC, Fell DB, Gubbay JB, et al. Estimated Effectiveness of COVID-19 Vaccines Against Omicron or Delta Symptomatic Infection and Severe Outcomes. JAMA Netw Open. 2022;5(9):e2232760.

Mariottini A, Bertozzi A, Marchi L, Di Cristinzi M, Mechi C, Barilaro A, et al. Effect of disease-modifying treatments on antibody-mediated response to anti-COVID19 vaccination in people with multiple sclerosis. J Neurol. 2022;269(6):2840-7.

Sormani MP, Inglese M, Schiavetti I, Carmisciano L, Laroni A, Lapucci C, et al. Effect of SARS-CoV-2 mRNA vaccination in MS patients treated with disease modifying therapies. EBioMedicine. 2021;72:103581.

Luo W, Yin Q. B Cell Response to Vaccination. Immunol Invest. 2021;50(7):780-801.

Han S, Zhang X, Wang G, Guan H, Garcia G, Li P, et al. FTY720 suppresses humoral immunity by inhibiting germinal center reaction. Blood. 2004;104(13):4129-33.

Mateen FJ, Rezaei S, Alakel N, Gazdag B, Kumar AR, Vogel A. Impact of COVID-19 on U.S. and Canadian neurologists' therapeutic approach to multiple sclerosis: a survey of knowledge, attitudes, and practices. J Neurol. 2020;267(12):3467-75.

Apostolidis SA, Kakara M, Painter MM, Goel RR, Mathew D, Lenzi K, et al. Cellular and humoral immune responses following SARS-CoV-2 mRNA vaccination in patients with multiple sclerosis on anti-CD20 therapy. Nat Med. 2021;27(11):1990-2001.

Iannetta M, Landi D, Cola G, Malagnino V, Teti E, Fraboni D, et al. T-cell responses to SARS-CoV-2 in multiple sclerosis patients treated with ocrelizumab healed from COVID-19 with absent or low anti-spike antibody titers. Mult Scler Relat Disord. 2021;55:103157.

Peng Y, Mentzer AJ, Liu G, Yao X, Yin Z, Dong D, et al. Broad and strong memory CD4(+) and CD8(+) T cells induced by SARS-CoV-2 in UK convalescent individuals following COVID-19. Nat Immunol. 2020;21(11):1336-45.

Tauzin A, Gendron-Lepage G, Nayrac M, Anand SP, Bourassa C, Medjahed H, et al. Evolution of Anti-RBD IgG Avidity following SARS-CoV-2 Infection. Viruses. 2022;14(3).

Lo Sasso B, Agnello L, Giglio RV, Gambino CM, Ciaccio AM, Vidali M, et al. Longitudinal analysis of anti-SARS-CoV-2 S-RBD IgG antibodies before and after the third dose of the BNT162b2 vaccine. Sci Rep. 2022;12(1):8679.

Pang NY, Pang AS, Chow VT, Wang DY. Understanding neutralising antibodies against SARS-CoV-2 and their implications in clinical practice. Mil Med Res. 2021;8(1):47.

Khoury DS, Cromer D, Reynaldi A, Schlub TE, Wheatley AK, Juno JA, et al. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat Med. 2021;27(7):1205-11.

Published

01-02-2024

How to Cite

Kosiyakul, P., Jitprapaikulsan , J. ., Uawithya, E. ., Wongprompitak , P. ., Chaimayo, C. ., Horthongkham , N. ., Angkasekwinai , N. ., Tisavipat, N. ., Prayoonwiwat , N. ., Rattanathamsakul, N., Boonyapisit , K. ., Kumutpongpanich , T. ., Sangsai , O. ., Aueaphatthanawong, K. ., Budkum , J. ., & Siritho , S. . (2024). Real-world data on the Immunity Response to the COVID-19 Vaccine among Patients with Central Nervous System Immunological Diseases: Immune Response to COVID-19 Vaccine in CNS Immunological Disease. Siriraj Medical Journal, 76(2), 69–79. https://doi.org/10.33192/smj.v76i2.266638

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