{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:02:23Z","timestamp":1760144543919,"version":"build-2065373602"},"reference-count":50,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2024,4,25]],"date-time":"2024-04-25T00:00:00Z","timestamp":1714003200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100005888","name":"Medical University of Lodz","doi-asserted-by":"publisher","award":["503\/1-000-01\/503-11-001-19-00"],"award-info":[{"award-number":["503\/1-000-01\/503-11-001-19-00"]}],"id":[{"id":"10.13039\/501100005888","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Background: As the SARS-CoV-2 virus remains one of the main causes of severe respiratory system infections, the Food and Drug Administration strongly advises the continuation of current vaccination programs, including the distribution of updated boosters, especially in high-risk groups of patients. Therefore, there is an unceasing need for further research on the safety and, no less importantly, the clinical effectivity of the vaccines, with an extra focus on cohorts of patients with underlying health problems. This study aimed to assess the efficacy of the SARS-CoV-2 vaccine in possibly immunocompromised children with rheumatic disease while utilizing the interferon-gamma release assay (IGRA) as a marker for COVID-19 immunity in the study follow-up. Methods: This prospective study was performed in a group of 55 pediatric patients diagnosed with juvenile idiopathic arthritis. Eight participants were immunized with the Comirnaty mRNA vaccine before the research commenced, while the rest of the group (n = 47) had not been vaccinated against SARS-CoV-2. At the study baseline, the cellular response to the virus antigen was measured using a specific quantitative IGRA in whole blood; subsequently, the anti-SARS-CoV-2 test was performed, marking the antibodies\u2019 levels in serum. Around four months after the enrollment of the last patient in the study, a follow-up survey regarding the events of COVID-19 infection within the cohort was conducted. Results: The study confirmed that all the vaccinated children developed specific T-cell (p = 0.0016) and humoral (p = 0.001 for IgA antibodies, p = 0.008 for IgG antibodies) responses to the inoculation, including those receiving biological treatment and those on conventional disease-modifying anti-rheumatic drugs. The study also showed the different patterns of immunity elicited both after infection and post-vaccination, with higher levels of antibodies and T-cell response after inoculation than after natural exposure to the pathogen. According to the follow-up survey, six children developed PCR-confirmed SARS-CoV-2 infection, whereas the additional 10 patients admitted to having COVID-like symptoms with no laboratory verification. Conclusions: SARS-CoV-2 vaccinations elicit valid immune responses in pediatric rheumatic patients. Including the assessment of T-cell immunity in the evaluation of inoculation-induced immunization can enhance the accuracy of sole humoral response assays.<\/jats:p>","DOI":"10.3390\/jcm13092523","type":"journal-article","created":{"date-parts":[[2024,4,25]],"date-time":"2024-04-25T08:08:32Z","timestamp":1714032512000},"page":"2523","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Interferon-\u03b3 Release Assay in the Assessment of Cellular Immunity\u2014A Single-Centre Experience with mRNA SARS-CoV-2 Vaccine in Patients with Juvenile Idiopathic Arthritis"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5676-7233","authenticated-orcid":false,"given":"Katarzyna","family":"Kapten","sequence":"first","affiliation":[{"name":"Department of Pediatric Cardiology and Rheumatology, Medical University of Lodz, 91-738 Lodz, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7294-1676","authenticated-orcid":false,"given":"Krzysztof","family":"Orczyk","sequence":"additional","affiliation":[{"name":"Department of Pediatric Infectious Diseases, Medical University of Lodz, 91-347 Lodz, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna","family":"Maeser","sequence":"additional","affiliation":[{"name":"Department of Pediatric Cardiology and Rheumatology, Central Teaching Hospital of Medical University of Lodz, 91-738 Lodz, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8421-0448","authenticated-orcid":false,"given":"Elzbieta","family":"Smolewska","sequence":"additional","affiliation":[{"name":"Department of Pediatric Cardiology and Rheumatology, Medical University of Lodz, 91-738 Lodz, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,4,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Sayeed, M.A., Shalim, E., Farooqui, F., Farman, S., Khan, M., Iqbal, A., Ahmed, I., Rajput, A.W., Razzaque, A., and Quraishy, S. (2023). Comparison of the Disease Severity and Outcome of Vaccinated COVID-19 Patients with Unvaccinated Patients in a Specialized COVID-19 Facility: A Retrospective Cohort Study from Karachi, Pakistan. Vaccines, 11.","DOI":"10.3390\/vaccines11071178"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Wang, D., Yuan, Y., Liu, B., Epstein, N.D., and Yang, Y. (2023). Protein-based nano-vaccines against SARS-CoV-2: Current design strategies and advances of candidate vaccines. Int. J. Biol. Macromol., 236.","DOI":"10.1016\/j.ijbiomac.2023.123979"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1111\/bcp.15552","article-title":"COVID-19: Clinical status of vaccine development to date","volume":"89","author":"Kumar","year":"2023","journal-title":"Br. J. Clin. Pharmacol."},{"key":"ref_4","unstructured":"(2023, September 01). Updated COVID-19 Vaccines for Use in the United States Beginning in Fall 2023, Available online: https:\/\/www.fda.gov\/vaccines-blood-biologics\/updated-covid-19-vaccines-use-united-states-beginning-fall-2023."},{"key":"ref_5","unstructured":"(2023, September 30). Stay Up to Date with COVID-19 Vaccines, Available online: https:\/\/www.cdc.gov\/coronavirus\/2019-ncov\/vaccines\/stay-up-to-date.html."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1136\/annrheumdis-2021-221575","article-title":"Risk and prognosis of SARS-CoV-2 infection and vaccination against SARS-CoV-2 in rheumatic and musculoskeletal diseases: A systematic literature review to inform EULAR recommendations","volume":"81","author":"Kroon","year":"2022","journal-title":"Ann. Rheum. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1038\/s41584-020-00562-2","article-title":"Rheumatic disease and COVID-19: Epidemiology and outcomes","volume":"17","author":"Hyrich","year":"2021","journal-title":"Nat. Rev. Rheumatol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1002\/art.42030","article-title":"SARS-CoV-2 Infection and COVID-19 Outcomes in Rheumatic Diseases: A Systematic Literature Review and Meta-Analysis","volume":"74","author":"Conway","year":"2022","journal-title":"Arthritis Rheumatol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"197","DOI":"10.5114\/reum.2021.107590","article-title":"COVID-19 in patients with juvenile idiopathic arthritis: Frequency and severity","volume":"59","author":"Boyarchuk","year":"2021","journal-title":"Reumatologia"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1007\/s00296-020-04645-x","article-title":"Management of childhood-onset autoinflammatory diseases during the COVID-19 pandemic","volume":"40","author":"Haslak","year":"2020","journal-title":"Rheumatol. Int."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Liu, J., Wu, H., and Xia, S.L. (2023). New-Onset Arthritis Following COVID-19 Vaccination: A Systematic Review of Case Reports. Vaccines, 11.","DOI":"10.3390\/vaccines11030665"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2761","DOI":"10.1007\/s10067-023-06694-6","article-title":"New-onset systemic vasculitis following SARS-CoV-2 infection and vaccination: The trigger, phenotype, and outcome","volume":"42","author":"Mv","year":"2023","journal-title":"Clin. Rheumatol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e32","DOI":"10.3346\/jkms.2022.37.e32","article-title":"Dermatomyositis Following BNT162b2 mRNA COVID-19 Vaccination","volume":"37","author":"Gouda","year":"2022","journal-title":"J. Korean Med. Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1007\/s10067-022-06065-7","article-title":"New-onset Adult-onset Still\u2019s disease-like syndrome after ChAdOx1 nCoV-19 vaccination-a case series with review of literature","volume":"41","author":"Padiyar","year":"2022","journal-title":"Clin. Rheumatol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"4482","DOI":"10.1093\/rheumatology\/keac140","article-title":"Humoral response and safety of BNT162b2 mRNA vaccine in children with rheumatic diseases","volume":"61","author":"Guliyeva","year":"2022","journal-title":"Rheumatology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4263","DOI":"10.1093\/rheumatology\/keac103","article-title":"Safety and immunogenicity of BNT162b2 mRNA COVID-19 vaccine in adolescents with rheumatic diseases treated with immunomodulatory medications","volume":"61","author":"Ziv","year":"2022","journal-title":"Rheumatology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4229","DOI":"10.1093\/rheumatology\/keac431","article-title":"SARS-CoV-2 vaccinations in children and adolescents with rheumatic diseases","volume":"61","author":"Sen","year":"2022","journal-title":"Rheumatology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e236","DOI":"10.1016\/S2666-5247(22)00390-1","article-title":"Efficacy of SARS-CoV-2 vaccines and the dose-response relationship with three major antibodies: A systematic review and meta-analysis of randomised controlled trials","volume":"4","author":"Yang","year":"2023","journal-title":"Lancet Microbe"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1016\/j.cell.2022.01.015","article-title":"SARS-CoV-2 vaccination induces immunological T cell memory able to cross-recognize variants from Alpha to Omicron","volume":"185","author":"Tarke","year":"2022","journal-title":"Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"eabo2202","DOI":"10.1126\/sciimmunol.abo2202","article-title":"Divergent SARS-CoV-2 Omicron-reactive T and B cell responses in COVID-19 vaccine recipients","volume":"7","author":"GeurtsvanKessel","year":"2022","journal-title":"Sci. Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"S12","DOI":"10.1016\/j.ijid.2022.02.047","article-title":"The role of IGRA in the diagnosis of tuberculosis infection, differentiating from active tuberculosis, and decision making for initiating treatment or preventive therapy of tuberculosis infection","volume":"124","author":"Goletti","year":"2022","journal-title":"Int. J. Infect. Dis."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1007\/s00296-022-05091-7","article-title":"Interferon-gamma release assays outcomes in healthy subjects following BNT162b2 mRNA COVID-19 vaccination","volume":"42","author":"Kurteva","year":"2022","journal-title":"Rheumatol. Int."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e42","DOI":"10.1016\/S2665-9913(21)00333-7","article-title":"Humoral and cellular immunogenicity to a second dose of COVID-19 vaccine BNT162b2 in people receiving methotrexate or targeted immunosuppression: A longitudinal cohort study","volume":"4","author":"Mahil","year":"2022","journal-title":"Lancet Rheumatol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e541","DOI":"10.1212\/WNL.0000000000013108","article-title":"Humoral- and T-Cell-Specific Immune Responses to SARS-CoV-2 mRNA Vaccination in Patients with MS Using Different Disease-Modifying Therapies","volume":"98","author":"Tortorella","year":"2022","journal-title":"Neurology"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1347","DOI":"10.1093\/ecco-jcc\/jjac048","article-title":"Cellular and Humoral Immune Responses to SARS-CoV-2 Vaccination in Inflammatory Bowel Disease Patients","volume":"16","author":"Cerna","year":"2022","journal-title":"J. Crohn\u2019s Colitis"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Standardization of Uveitis Nomenclature (SUN) Working Group (2021). Classification Criteria for Juvenile Idiopathic Arthritis-Associated Chronic Anterior Uveitis. Am. J. Ophthalmol., 228, 192\u2013197.","DOI":"10.1016\/j.ajo.2021.03.055"},{"key":"ref_27","unstructured":"(2024, April 12). STROBE Checklists. Available online: https:\/\/www.strobe-statement.org\/checklists\/."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1007\/s00005-023-00673-0","article-title":"Immunity in SARS-CoV-2 Infection: Clarity or Mystery? A Broader Perspective in the Third Year of a Worldwide Pandemic","volume":"71","author":"Kapten","year":"2023","journal-title":"Arch. Immunol. Ther. Exp."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2434","DOI":"10.1016\/j.cell.2022.05.022","article-title":"Humoral and cellular immune memory to four COVID-19 vaccines","volume":"185","author":"Zhang","year":"2022","journal-title":"Cell"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1016\/j.cell.2021.01.007","article-title":"Adaptive immunity to SARS-CoV-2 and COVID-19","volume":"184","author":"Sette","year":"2021","journal-title":"Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"100562","DOI":"10.1016\/j.xcrm.2022.100562","article-title":"Count on us: T cells in SARS-CoV-2 infection and vaccination","volume":"3","author":"Kedzierska","year":"2022","journal-title":"Cell Rep. Med."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Primorac, D., Brlek, P., Mati\u0161i\u0107, V., Molnar, V., Vrdoljak, K., Zadro, R., and Par\u010dina, M. (2022). Cellular Immunity-The Key to Long-Term Protection in Individuals Recovered from SARS-CoV-2 and after Vaccination. Vaccines, 10.","DOI":"10.3390\/vaccines10030442"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1038\/s41586-020-2814-7","article-title":"COVID-19 vaccine BNT162b1 elicits human antibody and TH1 T cell responses","volume":"586","author":"Sahin","year":"2020","journal-title":"Nature"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"6687","DOI":"10.1038\/s41598-022-07741-z","article-title":"Persistent Spike-specific T cell immunity despite antibody reduction after 3 months from SARS-CoV-2 BNT162b2-mRNA vaccine","volume":"12","author":"Agrati","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Masi\u00e1, M., de la Rica, A., Fern\u00e1ndez-Gonz\u00e1lez, M., Garc\u00eda, J.A., Padilla, S., Garc\u00eda-Abell\u00e1n, J., Botella, \u00c1., Mascarell, P., and Guti\u00e9rrez, F. (2023). Integrating SARS-CoV-2-specific interferon-\u03b3 release assay testing in the evaluation of patients hospitalized with COVID-19. Microbiol. Spectr., 11.","DOI":"10.1128\/spectrum.02419-23"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"732787","DOI":"10.3389\/fpubh.2021.732787","article-title":"Long-Term Course of Humoral and Cellular Immune Responses in Outpatients After SARS-CoV-2 Infection","volume":"9","author":"Schiffner","year":"2021","journal-title":"Front. Public Health"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"105098","DOI":"10.1016\/j.jcv.2022.105098","article-title":"Accuracy and real life performance of a novel interferon-\u03b3 release assay for the detection of SARS-CoV2 specific T cell response","volume":"148","author":"Huzly","year":"2022","journal-title":"J. Clin. Virol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1258","DOI":"10.1016\/j.semarthrit.2021.10.006","article-title":"SARS-CoV-2-specific T-cell responses after COVID-19 recovery in patients with rheumatic diseases on immunosuppressive therapy","volume":"51","author":"Retuerto","year":"2021","journal-title":"Semin. Arthritis Rheum."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1038\/s41392-022-01282-7","article-title":"Antibody and T cell responses against wild-type and Omicron SARS-CoV-2 after third-dose BNT162b2 in adolescents","volume":"7","author":"Mu","year":"2022","journal-title":"Signal Transduct. Target. Ther."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"11756","DOI":"10.1128\/JVI.01460-06","article-title":"Cellular immune responses in children and adults receiving inactivated or live attenuated influenza vaccines","volume":"80","author":"He","year":"2006","journal-title":"J. Virol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"498","DOI":"10.3389\/fimmu.2018.00498","article-title":"Differences Between Pediatric and Adult T Cell Responses to In Vitro Staphylococcal Enterotoxin B Stimulation","volume":"9","author":"Rudolph","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1007\/s11596-021-2318-1","article-title":"Differences in Immune Responses between Children and Adults with COVID-19","volume":"41","author":"Yuan","year":"2021","journal-title":"Curr. Med. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1306","DOI":"10.1136\/annrheumdis-2021-220272","article-title":"Immunogenicity and safety of anti-SARS-CoV-2 mRNA vaccines in patients with chronic inflammatory conditions and immunosuppressive therapy in a monocentric cohort","volume":"80","author":"Geisen","year":"2021","journal-title":"Ann. Rheum. Dis."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1136\/annrheumdis-2021-220461","article-title":"SARS-CoV-2 vaccination responses in untreated, conventionally treated and anticytokine-treated patients with immune-mediated inflammatory diseases","volume":"80","author":"Simon","year":"2021","journal-title":"Ann. Rheum. Dis."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"858399","DOI":"10.3389\/fimmu.2022.858399","article-title":"Evaluation of Humoral and Cellular Responses in SARS-CoV-2 mRNA Vaccinated Immunocompromised Patients","volume":"13","author":"Oyaert","year":"2022","journal-title":"Front. Immunol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Calcoen, B., Callewaert, N., Vandenbulcke, A., Kerstens, W., Imbrechts, M., Vercruysse, T., Dallmeier, K., Van Weyenbergh, J., Maes, P., and Bossuyt, X. (2022). High Incidence of SARS-CoV-2 Variant of Concern Breakthrough Infections Despite Residual Humoral and Cellular Immunity Induced by BNT162b2 Vaccination in Healthcare Workers: A Long-Term Follow-Up Study in Belgium. Viruses, 14.","DOI":"10.3390\/v14061257"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1007\/s10875-022-01354-x","article-title":"Monitoring of Both Humoral and Cellular Immunities Could Early Predict COVID-19 Vaccine Efficacy against the Different SARS-CoV2 Variants","volume":"43","author":"Vogrig","year":"2023","journal-title":"J. Clin. Immunol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1136\/annrheumdis-2021-221922","article-title":"Postvaccination antibody titres predict protection against COVID-19 in patients with autoimmune diseases: Survival analysis in a prospective cohort","volume":"81","author":"Ahmed","year":"2022","journal-title":"Ann. Rheum. Dis."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"3936","DOI":"10.1016\/j.cell.2021.06.005","article-title":"SARS-CoV-2 mRNA vaccination induces functionally diverse antibodies to NTD, RBD, and S2","volume":"184","author":"Amanat","year":"2021","journal-title":"Cell"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e153201","DOI":"10.1172\/jci.insight.153201","article-title":"Single-cell profiling of T and B cell repertoires following SARS-CoV-2 mRNA vaccine","volume":"6","author":"Sureshchandra","year":"2021","journal-title":"JCI Insight"}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/9\/2523\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:33:53Z","timestamp":1760106833000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/9\/2523"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,25]]},"references-count":50,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2024,5]]}},"alternative-id":["jcm13092523"],"URL":"https:\/\/doi.org\/10.3390\/jcm13092523","relation":{},"ISSN":["2077-0383"],"issn-type":[{"type":"electronic","value":"2077-0383"}],"subject":[],"published":{"date-parts":[[2024,4,25]]}}}