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The long term vaccine-induced anti-SARS-CoV-2 immune response is impaired in quantity and quality under TNFα blockade.
J Med Virol. 2022 12; 94(12):5780-5789.JM

Abstract

The humoral immune response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in patients with chronic inflammatory disease (CID) declines more rapidly with tumor necrosis factor-α (TNF-α) inhibition. Furthermore, the efficacy of current vaccines against Omicron variants of concern (VOC) including BA.2 is limited. Alterations within immune cell populations, changes in IgG affinity, and the ability to neutralize a pre-VOC strain and the BA.2 virus were investigated in these at-risk patients. Serum levels of anti-SARS-CoV-2 IgG, IgG avidity, and neutralizing antibodies (NA) were determined in anti-TNF-α patients (n = 10) and controls (n = 24 healthy individuals; n = 12 patients under other disease-modifying antirheumatic drugs, oDMARD) before and after the second and third vaccination by ELISA, immunoblot and live virus neutralization assay. SARS-CoV-2-specific B- and T cell subsets were analysed by multicolor flow cytometry. Six months after the second vaccination, anti-SARS-CoV-2 IgG levels, IgG avidity and anti-pre-VOC NA titres were significantly reduced in anti-TNF-α recipients compared to controls (healthy individuals: avidity: p ≤ 0.0001; NA: p = 0.0347; oDMARDs: avidity: p = 0.0012; NA: p = 0.0293). The number of plasma cells was increased in anti-TNF-α patients (Healthy individuals: p = 0.0344; oDMARDs: p = 0.0254), while the absolute number of SARS-CoV-2-specific plasma cells 7 days after 2nd vaccination were comparable. Even after a third vaccination, these patients had lower anti-BA.2 NA titres compared to both other groups. We show a reduced SARS-CoV-2 neutralizing capacity in patients under TNF-α blockade. In this cohort, the plasma cell response appears to be less specific and shows stronger bystander activation. While these effects were observable after the first two vaccinations and with older VOC, the differences in responses to BA.2 were enhanced.

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Authors+Show Affiliations

Geisen UM
Medical Department I, Rheumatology and Clinical Immunology, University Medical Center Schleswig-Holstein Campus Kiel, Kiel, Germany.
Rose R
Institute for Infection Medicine, Christian-Albrecht University of Kiel and University Medical Center Schleswig-Holstein, Kiel, Germany.
Neumann F
Labor Dr. Krause und Kollegen MVZ GmbH, Kiel, Germany.
Ciripoi M
Medical Department I, Rheumatology and Clinical Immunology, University Medical Center Schleswig-Holstein Campus Kiel, Kiel, Germany.
Vullriede L
Medical Department I, Rheumatology and Clinical Immunology, University Medical Center Schleswig-Holstein Campus Kiel, Kiel, Germany.
Reid HM
Medical Department I, Rheumatology and Clinical Immunology, University Medical Center Schleswig-Holstein Campus Kiel, Kiel, Germany.
Berner DK
Medical Department I, Rheumatology and Clinical Immunology, University Medical Center Schleswig-Holstein Campus Kiel, Kiel, Germany.
Bertoglio F
Department of Biotechnology, Institute of Biochemistry, Biotechnology, and Bioinformatics, Technische Universität Braunschweig, Braunschweig, Germany.
Hoff P
Department of Rheumatology, Endokrinologikum-Gruppe, Berlin, Germany.
Hust M
Department of Biotechnology, Institute of Biochemistry, Biotechnology, and Bioinformatics, Technische Universität Braunschweig, Braunschweig, Germany.
Longardt AC
Department of Pediatrics, University Medical Center Schleswig-Holstein, Kiel, Germany.
Lorentz T
Labor Dr. Krause und Kollegen MVZ GmbH, Kiel, Germany.
Martini GR
Institute of Immunology, University Medical Center Schleswig-Holstein, Kiel, Germany. Department for Dermatology, University Medical Center Schleswig-Holstein, Kiel, Germany.
Saggau C
Institute of Immunology, University Medical Center Schleswig-Holstein, Kiel, Germany.
Schirmer JH
Medical Department I, Rheumatology and Clinical Immunology, University Medical Center Schleswig-Holstein Campus Kiel, Kiel, Germany.
Schubert M
Department of Biotechnology, Institute of Biochemistry, Biotechnology, and Bioinformatics, Technische Universität Braunschweig, Braunschweig, Germany.
Sümbül M
Department for Dermatology, University Medical Center Schleswig-Holstein, Kiel, Germany.
Tran F
Institute of Clinical Molecular Biology, Christian-Albrecht University of Kiel, Kiel, Germany. Department for Internal Medicine I, University Medical Center Schleswig-Holstein, Kiel.
Voβ M
Institute for Infection Medicine, Christian-Albrecht University of Kiel and University Medical Center Schleswig-Holstein, Kiel, Germany.
Zeuner R
Medical Department I, Rheumatology and Clinical Immunology, University Medical Center Schleswig-Holstein Campus Kiel, Kiel, Germany.
Morrison PJ
Department for Dermatology, University Medical Center Schleswig-Holstein, Kiel, Germany.
Bacher P
Institute of Immunology, University Medical Center Schleswig-Holstein, Kiel, Germany. Institute of Clinical Molecular Biology, Christian-Albrecht University of Kiel, Kiel, Germany.
Fickenscher H
Institute for Infection Medicine, Christian-Albrecht University of Kiel and University Medical Center Schleswig-Holstein, Kiel, Germany.
Gerdes S
Department for Dermatology, University Medical Center Schleswig-Holstein, Kiel, Germany.
Peipp M
Department of Internal Medicine II, Division of Antibody-Based Immunotherapy, University Medical Center Schleswig-Holstein, Kiel, Germany.
Schreiber S
Institute of Clinical Molecular Biology, Christian-Albrecht University of Kiel, Kiel, Germany. Department for Internal Medicine I, University Medical Center Schleswig-Holstein, Kiel.
Krumbholz A
Institute for Infection Medicine, Christian-Albrecht University of Kiel and University Medical Center Schleswig-Holstein, Kiel, Germany. Labor Dr. Krause und Kollegen MVZ GmbH, Kiel, Germany.
Hoyer BF
Medical Department I, Rheumatology and Clinical Immunology, University Medical Center Schleswig-Holstein Campus Kiel, Kiel, Germany.

MeSH

AIDS VaccinesAntibodies, NeutralizingAntibodies, ViralAntirheumatic AgentsBCG VaccineCOVID-19Diphtheria-Tetanus VaccineDiphtheria-Tetanus-Pertussis VaccineHumansImmunityImmunoglobulin GInfluenza VaccinesMeasles-Mumps-Rubella VaccinePapillomavirus VaccinesRespiratory Syncytial Virus VaccinesSAIDS VaccinesSARS-CoV-2Tumor Necrosis Factor InhibitorsTumor Necrosis Factor-alphaVaccination

Pub Type(s)

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

Language

eng

PubMed ID

35945627

Citation

Geisen, Ulf Martin, et al. "The Long Term Vaccine-induced anti-SARS-CoV-2 Immune Response Is Impaired in Quantity and Quality Under TNFα Blockade." Journal of Medical Virology, vol. 94, no. 12, 2022, pp. 5780-5789.
Geisen UM, Rose R, Neumann F, et al. The long term vaccine-induced anti-SARS-CoV-2 immune response is impaired in quantity and quality under TNFα blockade. J Med Virol. 2022;94(12):5780-5789.
Geisen, U. M., Rose, R., Neumann, F., Ciripoi, M., Vullriede, L., Reid, H. M., Berner, D. K., Bertoglio, F., Hoff, P., Hust, M., Longardt, A. C., Lorentz, T., Martini, G. R., Saggau, C., Schirmer, J. H., Schubert, M., Sümbül, M., Tran, F., Voβ, M., ... Hoyer, B. F. (2022). The long term vaccine-induced anti-SARS-CoV-2 immune response is impaired in quantity and quality under TNFα blockade. Journal of Medical Virology, 94(12), 5780-5789. https://doi.org/10.1002/jmv.28063
Geisen UM, et al. The Long Term Vaccine-induced anti-SARS-CoV-2 Immune Response Is Impaired in Quantity and Quality Under TNFα Blockade. J Med Virol. 2022;94(12):5780-5789. PubMed PMID: 35945627.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The long term vaccine-induced anti-SARS-CoV-2 immune response is impaired in quantity and quality under TNFα blockade. AU - Geisen,Ulf Martin, AU - Rose,Ruben, AU - Neumann,Franziska, AU - Ciripoi,Maria, AU - Vullriede,Lena, AU - Reid,Hayley M, AU - Berner,Dennis Kristopher, AU - Bertoglio,Federico, AU - Hoff,Paula, AU - Hust,Michael, AU - Longardt,Ann Carolin, AU - Lorentz,Thomas, AU - Martini,Gabriela Rios, AU - Saggau,Carina, AU - Schirmer,Jan Henrik, AU - Schubert,Maren, AU - Sümbül,Melike, AU - Tran,Florian, AU - Voβ,Mathias, AU - Zeuner,Rainald, AU - Morrison,Peter J, AU - Bacher,Petra, AU - Fickenscher,Helmut, AU - Gerdes,Sascha, AU - Peipp,Matthias, AU - Schreiber,Stefan, AU - Krumbholz,Andi, AU - Hoyer,Bimba Franziska, Y1 - 2022/08/19/ PY - 2022/08/03/revised PY - 2022/07/07/received PY - 2022/08/06/accepted PY - 2022/8/10/pubmed PY - 2022/10/18/medline PY - 2022/8/9/entrez KW - COVID-19 KW - autoimmune diseases KW - tumor necrosis factor inhibitors KW - vaccination SP - 5780 EP - 5789 JF - Journal of medical virology JO - J Med Virol VL - 94 IS - 12 N2 - The humoral immune response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in patients with chronic inflammatory disease (CID) declines more rapidly with tumor necrosis factor-α (TNF-α) inhibition. Furthermore, the efficacy of current vaccines against Omicron variants of concern (VOC) including BA.2 is limited. Alterations within immune cell populations, changes in IgG affinity, and the ability to neutralize a pre-VOC strain and the BA.2 virus were investigated in these at-risk patients. Serum levels of anti-SARS-CoV-2 IgG, IgG avidity, and neutralizing antibodies (NA) were determined in anti-TNF-α patients (n = 10) and controls (n = 24 healthy individuals; n = 12 patients under other disease-modifying antirheumatic drugs, oDMARD) before and after the second and third vaccination by ELISA, immunoblot and live virus neutralization assay. SARS-CoV-2-specific B- and T cell subsets were analysed by multicolor flow cytometry. Six months after the second vaccination, anti-SARS-CoV-2 IgG levels, IgG avidity and anti-pre-VOC NA titres were significantly reduced in anti-TNF-α recipients compared to controls (healthy individuals: avidity: p ≤ 0.0001; NA: p = 0.0347; oDMARDs: avidity: p = 0.0012; NA: p = 0.0293). The number of plasma cells was increased in anti-TNF-α patients (Healthy individuals: p = 0.0344; oDMARDs: p = 0.0254), while the absolute number of SARS-CoV-2-specific plasma cells 7 days after 2nd vaccination were comparable. Even after a third vaccination, these patients had lower anti-BA.2 NA titres compared to both other groups. We show a reduced SARS-CoV-2 neutralizing capacity in patients under TNF-α blockade. In this cohort, the plasma cell response appears to be less specific and shows stronger bystander activation. While these effects were observable after the first two vaccinations and with older VOC, the differences in responses to BA.2 were enhanced. SN - 1096-9071 UR - https://www.unboundmedicine.com/medline/citation/35945627/The_long_term_vaccine_induced_anti_SARS_CoV_2_immune_response_is_impaired_in_quantity_and_quality_under_TNFα_blockade_ DB - PRIME DP - Unbound Medicine ER -