{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,8]],"date-time":"2026-01-08T16:49:35Z","timestamp":1767890975542,"version":"3.49.0"},"reference-count":42,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2023,5,30]],"date-time":"2023-05-30T00:00:00Z","timestamp":1685404800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"AbbVie"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cancers"],"abstract":"<jats:p>High morbidity and mortality due to COVID-19 were described in the pre-vaccination era in patients with chronic lymphocytic leukemia (CLL). To evaluate COVID-19 morbidity after the SARS-CoV-2 vaccine, we carried out a prospective study in 200 CLL patients. The median age of patients was 70 years; 35% showed IgG levels \u2264 550 mg\/dL, 61% unmutated IGHV, and 34% showed TP53 disruption. Most patients, 83.5%, were previously treated, including 36% with ibrutinib and 37.5% with venetoclax. The serologic response rates to the second and third dose of the vaccine were 39% and 53%, respectively. With a median follow-up of 23.4 months, 41% of patients experienced COVID-19, 36.5% during the Omicron pandemic, and 10% had subsequent COVID-19 events. Severe COVID-19 requiring hospitalization was recorded in 26% of patients, and 4% died. Significant and independent factors associated with the response to the vaccine and vulnerability to COVID-19 were age (OR: 0.93; HR: 0.97) and less than 18 months between the start of targeted agents and vaccine (OR: 0.17; HR: 0.31). TP53 mutation and \u2265two prior treatments also emerged as significant and independent factors associated with an increased risk of developing COVID-19 (HR: 1.85; HR: 2.08). No statistical difference in COVID-19 morbidity was found in patients with or without antibody response to the vaccine (47.5% vs. 52.5%; p = 0.21). Given the persistent risk of infection due to the continuous emergence of SARS-CoV-2 variants, our results support the importance of new vaccines and protective measures to prevent and mitigate COVID-19 in CLL patients.<\/jats:p>","DOI":"10.3390\/cancers15112993","type":"journal-article","created":{"date-parts":[[2023,5,31]],"date-time":"2023-05-31T02:27:30Z","timestamp":1685500050000},"page":"2993","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Antibody Response to the SARS-CoV-2 Vaccine and COVID-19 Vulnerability during the Omicron Pandemic in Patients with CLL: Two-Year Follow-Up of a Multicenter Study"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2425-9474","authenticated-orcid":false,"given":"Francesca R.","family":"Mauro","sequence":"first","affiliation":[{"name":"Hematology, Department of Translational and Precision Medicine, Sapienza University, 00161 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Diana","family":"Giannarelli","sequence":"additional","affiliation":[{"name":"Design and Analysis of Clinical Trials Unit, Scientific Directorate, IRCS Fondazione Policlinico Universitario A. Gemelli, 00168 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1392-6569","authenticated-orcid":false,"given":"Clementina M.","family":"Galluzzo","sequence":"additional","affiliation":[{"name":"National Center for Global Health, Istituto Superiore di Sanit\u00e0, 00161 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0271-7200","authenticated-orcid":false,"given":"Andrea","family":"Visentin","sequence":"additional","affiliation":[{"name":"Hematology and Clinical Immunology Unit, Department of Medicine, University of Padua, 35122 Padova, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2587-7901","authenticated-orcid":false,"given":"Anna M.","family":"Frustaci","sequence":"additional","affiliation":[{"name":"ASST Grande Ospedale Metropolitano Niguarda, 20162 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5630-9862","authenticated-orcid":false,"given":"Paolo","family":"Sportoletti","sequence":"additional","affiliation":[{"name":"Institute of Hematology and Center for Hemato-Oncology Research, University of Perugia and Santa Maria della Misericordia Hospital, 06129 Perugia, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2592-8724","authenticated-orcid":false,"given":"Candida","family":"Vitale","sequence":"additional","affiliation":[{"name":"Department of Molecular Biotechnology and Health Sciences, University of Torino and Division of Hematology, A.O.U. Citt\u00e0 della Salute e della Scienza di Torino, 10125 Torino, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gianluigi","family":"Reda","sequence":"additional","affiliation":[{"name":"Hematology Unit, Fondazione IRCCS C\u00e0 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5256-0726","authenticated-orcid":false,"given":"Massimo","family":"Gentile","sequence":"additional","affiliation":[{"name":"Hematology Unit AO of Cosenza, Cosenza and Department of Pharmacy, Health and Nutritional Sciences, University of Calabria, 87036 Rende, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Luciano","family":"Levato","sequence":"additional","affiliation":[{"name":"Department Hematology-Oncology, Azienda Ospedaliera Pugliese-Ciaccio, 88100 Catanzaro, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roberta","family":"Murru","sequence":"additional","affiliation":[{"name":"Hematology and Stem Cell Transplantation Unit, Ospedale Oncologico A. Businco, ARNAS \u201cG. Brotzu\u201d, 09134 Cagliari, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniele","family":"Armiento","sequence":"additional","affiliation":[{"name":"Unit of Hematology, Stem Cell Transplantation, University Campus Bio-Medico, 00128 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria C.","family":"Molinari","sequence":"additional","affiliation":[{"name":"Hematology, Department of Translational and Precision Medicine, Sapienza University, 00161 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7827-3696","authenticated-orcid":false,"given":"Giulia","family":"Proietti","sequence":"additional","affiliation":[{"name":"Hematology, Department of Translational and Precision Medicine, Sapienza University, 00161 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sara","family":"Pepe","sequence":"additional","affiliation":[{"name":"Hematology, Department of Translational and Precision Medicine, Sapienza University, 00161 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Filomena","family":"De Falco","sequence":"additional","affiliation":[{"name":"Institute of Hematology and Center for Hemato-Oncology Research, University of Perugia and Santa Maria della Misericordia Hospital, 06129 Perugia, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Veronica","family":"Mattiello","sequence":"additional","affiliation":[{"name":"Hematology Unit, Fondazione IRCCS C\u00e0 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3676-3240","authenticated-orcid":false,"given":"Luca","family":"Barabino","sequence":"additional","affiliation":[{"name":"Department of Medical Sciences and Public Health, University of Cagliari, 09124 Cagliari, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roberta","family":"Amici","sequence":"additional","affiliation":[{"name":"National Center for Global Health, Istituto Superiore di Sanit\u00e0, 00161 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2123-7675","authenticated-orcid":false,"given":"Marta","family":"Coscia","sequence":"additional","affiliation":[{"name":"Department of Molecular Biotechnology and Health Sciences, University of Torino and Division of Hematology, A.O.U. Citt\u00e0 della Salute e della Scienza di Torino, 10125 Torino, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alessandra","family":"Tedeschi","sequence":"additional","affiliation":[{"name":"ASST Grande Ospedale Metropolitano Niguarda, 20162 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Corrado","family":"Girmenia","sequence":"additional","affiliation":[{"name":"Azienda Policlinico Umberto I, 00161 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1222-6149","authenticated-orcid":false,"given":"Livio","family":"Trentin","sequence":"additional","affiliation":[{"name":"Hematology and Clinical Immunology Unit, Department of Medicine, University of Padua, 35122 Padova, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2050-9037","authenticated-orcid":false,"given":"Silvia","family":"Baroncelli","sequence":"additional","affiliation":[{"name":"National Center for Global Health, Istituto Superiore di Sanit\u00e0, 00161 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2881","DOI":"10.1182\/blood.2020008824","article-title":"Outcomes of Patients with Hematologic Malignancies and COVID-19: A Systematic Review and Meta-Analysis of 3377 Patients","volume":"136","author":"Vijenthira","year":"2020","journal-title":"Blood"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e737","DOI":"10.1016\/S2352-3026(20)30251-9","article-title":"ITA-HEMA-COV Investigators. 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Oncol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2354","DOI":"10.1038\/s41375-020-0959-x","article-title":"COVID-19 Severity and Mortality in Patients with Chronic Lymphocytic Leukemia: A Joint Study by ERIC, the European Research Initiative on CLL, and CLL Campus","volume":"34","author":"Chatzikonstantinou","year":"2020","journal-title":"Leukemia"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1134","DOI":"10.1182\/blood.2020006965","article-title":"Outcomes of COVID-19 in Patients with CLL: A Multicenter International Experience","volume":"136","author":"Mato","year":"2020","journal-title":"Blood"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3444","DOI":"10.1038\/s41375-021-01450-8","article-title":"COVID-19 Severity and Mortality in Patients with CLL: An Update of the International ERIC and Campus CLL Study","volume":"35","author":"Chatzikonstantinou","year":"2021","journal-title":"Leukemia"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3047","DOI":"10.1038\/s41375-020-01030-2","article-title":"Anti-SARS-CoV-2 Antibody Response in Patients with Chronic Lymphocytic Leukemia","volume":"34","author":"Roeker","year":"2020","journal-title":"Leukemia"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3165","DOI":"10.1182\/blood.2021011568","article-title":"Efficacy of the BNT162b2 MRNA COVID-19 Vaccine in Patients with Chronic Lymphocytic Leukemia","volume":"137","author":"Herishanu","year":"2021","journal-title":"Blood"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2703","DOI":"10.1038\/s41375-021-01270-w","article-title":"COVID-19 Vaccine Efficacy in Patients with Chronic Lymphocytic Leukemia","volume":"35","author":"Roeker","year":"2021","journal-title":"Leukemia"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1038\/s41408-021-00528-x","article-title":"Antibody Responses after First and Second Covid-19 Vaccination in Patients with Chronic Lymphocytic Leukaemia","volume":"11","author":"Parry","year":"2021","journal-title":"Blood Cancer J."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1182\/bloodadvances.2021006215","article-title":"Humoral Response to MRNA Anti-COVID-19 Vaccines BNT162b2 and MRNA-1273 in Patients with Chronic Lymphocytic Leukemia","volume":"6","author":"Bagacean","year":"2022","journal-title":"Blood Adv."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"625","DOI":"10.3324\/haematol.2021.279196","article-title":"Safety and Efficacy of the BNT162b MRNA COVID-19 Vaccine in Patients with Chronic Lymphocytic Leukemia","volume":"107","author":"Benjamini","year":"2022","journal-title":"Haematologica"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1671","DOI":"10.1182\/bloodadvances.2021006627","article-title":"Humoral and Cellular Immunogenicity of SARS-CoV-2 Vaccines in Chronic Lymphocytic Leukemia: A Prospective Cohort Study","volume":"6","author":"Haydu","year":"2022","journal-title":"Blood Adv."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3020","DOI":"10.1200\/JCO.22.00088","article-title":"Humoral Responses Against SARS-CoV-2 and Variants of Concern After MRNA Vaccines in Patients With Non-Hodgkin Lymphoma and Chronic Lymphocytic Leukemia","volume":"40","author":"Chang","year":"2022","journal-title":"J. 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