{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,31]],"date-time":"2026-07-31T01:57:06Z","timestamp":1785463026305,"version":"3.56.0"},"reference-count":47,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2023,8,1]],"date-time":"2023-08-01T00:00:00Z","timestamp":1690848000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/501100000024","name":"Gouvernement du Canada | Canadian Institutes of Health Research","doi-asserted-by":"publisher","award":["VR-1 172 711"],"award-info":[{"award-number":["VR-1 172 711"]}],"id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100011094","name":"Public Health Agency of Canada","doi-asserted-by":"publisher","award":["n\/a"],"award-info":[{"award-number":["n\/a"]}],"id":[{"id":"10.13039\/100011094","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,8,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Previous studies have reported impaired humoral responses after SARS-CoV-2 mRNA vaccination in patients with immune-mediated inflammatory diseases (IMIDs), particularly those treated with anti-TNF biologics. We previously reported that IMID patients diagnosed with inflammatory bowel disease, psoriasis, psoriatic arthritis, ankylosing spondylitis, or rheumatoid arthritis exhibited greater waning of Ab and T cell responses than healthy control subjects after SARS-CoV-2 vaccine dose 2. Fewer data are available on the effects of third and fourth doses. This observational cohort study collected plasma and PBMCs from healthy control subjects and untreated or treated patients with IMIDs prevaccination and after one to four doses of SARS-CoV-2 mRNA vaccine (BNT162b2 or mRNA-1273). SARS-CoV-2\u2013specific Ab levels, neutralization, and T cell cytokine release were measured against wild-type and Omicron BA.1 and BA.5 variants of concern. Third vaccine doses substantially restored and prolonged Ab and T cell responses in patients with IMIDs and broadened responses against variants of concern. Fourth-dose effects were subtle but also prolonged Ab responses. However, patients with IMIDs treated with anti-TNF, especially patients with inflammatory bowel disease, exhibited lower Ab responses even after the fourth dose. Although T cell IFN-\u03b3 responses were maximal after one dose, IL-2 and IL-4 production increased with successive doses, and early production of these cytokines was predictive of neutralization responses at 3\u20134 mo postvaccination. Our study demonstrates that third and fourth doses of the SARS-CoV-2 mRNA vaccines sustain and broaden immune responses to SARS-CoV-2, supporting the recommendation for three- and four-dose vaccination regimens in patients with IMIDs.<\/jats:p>","DOI":"10.4049\/jimmunol.2300190","type":"journal-article","created":{"date-parts":[[2023,6,16]],"date-time":"2023-06-16T09:45:39Z","timestamp":1686908739000},"page":"351-364","source":"Crossref","is-referenced-by-count":24,"title":["Third and Fourth Vaccine Doses Broaden and Prolong Immunity to SARS-CoV-2 in Adult Patients with Immune-Mediated Inflammatory Diseases"],"prefix":"10.1093","volume":"211","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4147-9914","authenticated-orcid":false,"given":"Michelle W","family":"Cheung","sequence":"first","affiliation":[{"name":"Department of Immunology, University of Toronto , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roya M","family":"Dayam","sequence":"additional","affiliation":[{"name":"Lunenfeld-Tanenbaum Research Institute at Mount Sinai Hospital, Sinai Health , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8088-2506","authenticated-orcid":false,"given":"Janna R","family":"Shapiro","sequence":"additional","affiliation":[{"name":"Department of Immunology, University of Toronto , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jaclyn C","family":"Law","sequence":"additional","affiliation":[{"name":"Department of Immunology, University of Toronto , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5054-4685","authenticated-orcid":false,"given":"Gary Y C","family":"Chao","sequence":"additional","affiliation":[{"name":"Department of Immunology, University of Toronto , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Pereira","sequence":"additional","affiliation":[{"name":"Schroeder Arthritis Institute, Krembil Research Institute, University Health Network , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1349-9501","authenticated-orcid":false,"given":"Rogier L","family":"Goetgebuer","sequence":"additional","affiliation":[{"name":"Zane Cohen Centre for Digestive Diseases, Division of Gastroenterology, Mount Sinai Hospital, Sinai Health , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Croitoru","sequence":"additional","affiliation":[{"name":"Division of Dermatology, Department of Medicine, University of Toronto , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-6510-8608","authenticated-orcid":false,"given":"Joanne M","family":"Stempak","sequence":"additional","affiliation":[{"name":"Zane Cohen Centre for Digestive Diseases, Division of Gastroenterology, Mount Sinai Hospital, Sinai Health , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lily","family":"Acheampong","sequence":"additional","affiliation":[{"name":"Division of Dermatology, Department of Medicine, Women\u2019s College Hospital , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Saima","family":"Rizwan","sequence":"additional","affiliation":[{"name":"Zane Cohen Centre for Digestive Diseases, Division of Gastroenterology, Mount Sinai Hospital, Sinai Health , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-6944-2213","authenticated-orcid":false,"given":"Jenny D","family":"Lee","sequence":"additional","affiliation":[{"name":"Zane Cohen Centre for Digestive Diseases, Division of Gastroenterology, Mount Sinai Hospital, Sinai Health , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liz","family":"Jacob","sequence":"additional","affiliation":[{"name":"Zane Cohen Centre for Digestive Diseases, Division of Gastroenterology, Mount Sinai Hospital, Sinai Health , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Darshini","family":"Ganatra","sequence":"additional","affiliation":[{"name":"Schroeder Arthritis Institute, Krembil Research Institute, University Health Network , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryan","family":"Law","sequence":"additional","affiliation":[{"name":"Department of Immunology, University of Toronto , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2298-1818","authenticated-orcid":false,"given":"Victoria E","family":"Rodriguez-Castellanos","sequence":"additional","affiliation":[{"name":"Department of Immunology, University of Toronto , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-7093-9699","authenticated-orcid":false,"given":"Madeline","family":"Kern-Smith","sequence":"additional","affiliation":[{"name":"Department of Immunology, University of Toronto , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melanie","family":"Delgado-Brand","sequence":"additional","affiliation":[{"name":"Lunenfeld-Tanenbaum Research Institute at Mount Sinai Hospital, Sinai Health , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Genevieve","family":"Mailhot","sequence":"additional","affiliation":[{"name":"Lunenfeld-Tanenbaum Research Institute at Mount Sinai Hospital, Sinai Health , Toronto, Ontario ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3210-4771","authenticated-orcid":false,"given":"Nigil","family":"Haroon","sequence":"additional","affiliation":[{"name":"Schroeder Arthritis Institute, Krembil Research Institute, University Health Network , Toronto, Ontario ,","place":["Canada"]},{"name":"Division of Rheumatology, Department of Medicine, University of Toronto , Toronto, Ontario 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,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,8,1]]},"reference":[{"key":"2025020406035130600_r1","article-title":"Statement on the fourteenth meeting of the International Health Regulations (2005) Emergency Committee regarding the coronavirus disease (COVID-19) pandemic","author":"World Health Organization"},{"key":"2025020406035130600_r2","doi-asserted-by":"crossref","first-page":"e490","DOI":"10.1016\/S2665-9913(22)00098-4","article-title":"Risk of severe COVID-19 outcomes associated with immune-mediated inflammatory diseases and immune-modifying therapies: a nationwide cohort study in the OpenSAFELY platform","volume":"4","author":"MacKenna","year":"2022","journal-title":"Lancet Rheumatol."},{"key":"2025020406035130600_r3","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1136\/annrheumdis-2020-218946","article-title":"Prevalence and clinical outcomes of COVID-19 in patients with autoimmune diseases: a systematic review and meta-analysis","volume":"80","author":"Akiyama","year":"2021","journal-title":"Ann. Rheum. Dis."},{"key":"2025020406035130600_r4","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1056\/NEJMoa2035389","article-title":"Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine","volume":"384","author":"Baden","year":"2021","journal-title":"N. Engl. J. Med."},{"key":"2025020406035130600_r5","doi-asserted-by":"crossref","first-page":"2603","DOI":"10.1056\/NEJMoa2034577","article-title":"Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine","volume":"383","author":"Polack","year":"2020","journal-title":"N. Engl. J. Med."},{"key":"2025020406035130600_r6","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1016\/S2468-1253(22)00274-6","article-title":"COVID-19 vaccine-induced antibody and T-cell responses in immunosuppressed patients with inflammatory bowel disease after the third vaccine dose (VIP): a multicentre, prospective, case-control study","volume":"7","author":"Alexander","year":"2022","journal-title":"Lancet Gastroenterol. Hepatol."},{"key":"2025020406035130600_r7","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1053\/j.gastro.2021.10.029","article-title":"Lower serologic response to COVID-19 mRNA vaccine in patients with inflammatory bowel diseases treated with anti-TNF\u03b1","volume":"162","author":"Edelman-Klapper","year":"2022","journal-title":"Gastroenterology"},{"key":"2025020406035130600_r8","doi-asserted-by":"crossref","first-page":"1330","DOI":"10.1136\/annrheumdis-2021-220647","article-title":"Immunogenicity and safety of the BNT162b2 mRNA COVID-19 vaccine in adult patients with autoimmune inflammatory rheumatic diseases and in the general population: a multicentre study. [Published erratum appears in 2022 Ann. Rheum. Dis. 81: e133.]","volume":"80","author":"Furer","year":"2021","journal-title":"Ann. Rheum. 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