Skip to main content
Key Specialties
Anesthesiology Cardiology Dermatology Diabetology Endocrinology Gastroenterology and Hepatology General Medicine Geriatrics Hematology Infectious Diseases Internal Medicine Nephrology Neurology Obstetrics and Gynecology Oncology Ophthalmology Pediatrics Psychiatry Radiology Respiratory Medicine Rheumatology Surgery Urology
Congress Coverage
ASH 2024 Annual Meeting 2024 ESMO Congress 2024 ERS Congress 2024 EASD Congress 2024 ESC Congress 2024 EAN Congress 2024 ASCO Annual Meeting 2024 ACC Congress
Clinical Collections
Advances in Alzheimer’s

Podcast | Sexual health in older age

Dr Holly Thomas helps us unpack the needlessly taboo subject of sex and sexual health in women of older age.

Listen now
ADVANCED SEARCH
Log in
Top
Annals of Hematology

Open Access 12-03-2025 | Obinutuzumab | Research

Anti-CD20 maintenance strategies to face the challenge of COVID-19 pandemic in follicular lymphoma: results from the R-FolSTOP multicentre Italian study

Authors: Alessia Castellino, Lorenzo Comba, Laura Bertolotti, Carola Boccomini, Michele Clerico, Paolo Nicoli, Anna Vanazzi, Fulvia Fanelli, Tommasina Perrone, Francesco Marchesi, Federica Cocito, Michele Merli, Sara Bigliardi, Bianca Mecacci, Valentina Bozzoli, Gloria Margiotta-Casaluci, Erika Meli, Antonella Anastasia, Lucia Farina, Ombretta Annibali, Annarita Conconi, Sara Ratotti, Sara Galimberti, Claudia Castellino, Massimo Massaia

Published in: Annals of Hematology

Login to get access

Abstract

The SARS-CoV2 pandemic has posed unprecedented challenges between temporary or permanent discontinuation of immunosuppressive treatment to protect patients, or disease control prioritization by not interrupting treatment. Maintenance treatment with anti-CD20 monoclonal antibodies (MoAbs) improves progression-free survival (PFS) in follicular lymphoma (FL), but also impairs anti-SARS-CoV2 immune response. This challenge has been addressed in Italy by temporary, definitive or no discontinuation of anti-CD20 treatment. We report the outcome of 539 FL patients receiving anti-CD20 MoAbs (rituximab in 431, obinutuzumab in 108), which were temporarily discontinued in 150 patients (group A), definitively discontinued in 166 (group B), or uninterrupted in 223 (group C). In the overall cohort, the 3-year progression-free survival (3y PFS) and 3-year overall survival (3y OS) rates were 80% and 88%. PFS and OS were significantly better in group A compared to group B and C (p = 0.01). Induction chemoimmunotherapy significantly influenced OS: the 3y OS was 91% vs 85% in CHOP vs bendamustine treated patients (p = 0.04), while the 3y OS was 90% vs 77% in rituximab vs obinutuzumab treated patients (p = 0.002). SARS-Cov2 infection was the main cause of death (67% of cases). Vaccination with multiple doses demonstrated to be clinically helpful, with impact on OS.
Appendix
Available only for authorised users
Literature
1.
Freedman A, Jacobsen E (2020) Follicular lymphoma: 2020 update on diagnosis and management. Am J Hematol 95(3):316–327CrossRefPubMed
2.
Bachy E, Seymour JF, Feugier P, Offner F, López-Guillermo A, Belada D et al (2019) Sustained progression-free survival benefit of rituximab maintenance in patients with follicular lymphoma: long-term results of the PRIMA study. J Clin Oncol 37(31):2815–2824CrossRefPubMedPubMedCentral
3.
Salles G, Seymour JF, Offner F, López-Guillermo A, Belada D, Xerri L et al (2011) Rituximab maintenance for 2 years in patients with high tumour burden follicular lymphoma responding to rituximab plus chemotherapy (PRIMA): a phase 3, randomised controlled trial. Lancet 377(9759):42–51CrossRefPubMed
4.
Vitolo U, Ladetto M, Boccomini C, Baldini L, De Angelis F, Tucci A et al (2013) Rituximab maintenance compared with observation after brief first-line R-FND chemoimmunotherapy with rituximab consolidation in patients age older than 60 years with advanced follicular lymphoma: a phase III randomized study by the Fondazione Italiana Linfomi. J Clin Oncol 31(27):3351–3359CrossRefPubMed
5.
Hill BT, Nastoupil L, Winter AM, Becnel MR, Cerhan JR, Habermann TM et al (2019) Maintenance rituximab or observation after frontline treatment with bendamustine-rituximab for follicular lymphoma. Br J Haematol 184(4):524–535CrossRefPubMed
6.
Hiddemann W, Barbui AM, Canales MA, Cannell PK, Collins GP, Dürig J et al (2018) Immunochemotherapy With obinutuzumab or rituximab for previously untreated follicular lymphoma in the GALLIUM study: Influence of chemotherapy on efficacy and safety. J Clin Oncol 36(23):2395–2404CrossRefPubMed
7.
Nazi I, Kelton JG, Larché M, Snider DP, Heddle NM, Crowther MA et al (2013) The effect of rituximab on vaccine responses in patients with immune thrombocytopenia. Blood 122(11):1946–1953CrossRefPubMed
8.
Yasuda H, Tsukune Y, Watanabe N, Sugimoto K, Uchimura A, Tateyama M et al (2020) Persistent COVID-19 pneumonia and failure to develop anti-SARS-CoV-2 antibodies during rituximab maintenance therapy for Follicular Lymphoma. Clin Lymphoma Myeloma Leuk 20(11):774–776CrossRefPubMedPubMedCentral
9.
Wright Z, Bersabe A, Eden R, Bradley J, Cap A (2021) Successful use of COVID-19 convalescent plasma in a patient recently treated for Follicular Lymphoma. Clin Lymphoma Myeloma Leuk 21(1):66–68CrossRefPubMed
10.
Shah V, Ko Ko T, Zuckerman M, Vidler J, Sharif S, Mehra V et al (2020) Poor outcome and prolonged persistence of SARS-CoV-2 RNA in COVID-19 patients with haematological malignancies; King’s College Hospital experience. Br J Haematol 190(5):e279–e282CrossRefPubMedPubMedCentral
11.
Schiavetti I, Ponzano M, Signori A, Bovis F, Carmisciano L, Sormani MP (2022) Severe outcomes of COVID-19 among patients with multiple sclerosis under anti-CD-20 therapies: A systematic review and meta-analysis. Mult Scler Relat Disord 57(103358):5
12.
Barzegar M, Houshi S, Sadeghi E, Hashemi MS, Pishgahi G, Bagherieh S et al (2022) Association of disease-modifying therapies with COVID-19 susceptibility and severity in patients with multiple sclerosis: a systematic review and network meta-analysis. Mult Scler Int 21:9388813
13.
Galusic D, Basic-Kinda S, Pijuk A, Milunovic V, Dreta B, Franjic N et al (2022) Efficacy and safety of obinutuzumab-chemotherapy combinations in front-line treatment of follicular non-hodgkin lymphoma during the COVID-19 pandemic: A Study of KROHEM, the croatian cooperative group for hematologic diseases. Hemasphere 6(12):e807CrossRefPubMedPubMedCentral
14.
Serna Á, Navarro V, Iacoboni G, López L, Sancho JM, González-Barca E et al (2025) Rituximab maintenance after bendamustine-based treatment for follicular lymphoma and mantle cell lymphoma may exert a negative influence on SARS-CoV-2 infection outcomes. Haematologica 110(1):173–178PubMed
15.
Pinto A, Caltagirone M, Battista M, Gazzoli GC, Patti C, Pennese E et al (2024) Exposure to obinutuzumab does not affect outcomes of SARS-CoV-2 infection in vaccinated patients with newly diagnosed advanced-stage follicular lymphoma. Br J Haematol. 205:2219–2219CrossRefPubMedPubMedCentral
16.
Gong IY, Prica A, Ante Z, Calzavara A, Krzyzanowska MK, Singh S et al (2024) Indolent lymphoma care delivery and outcomes during the COVID-19 pandemic in Ontario. Canada Br J Haematol 204(3):805–814CrossRefPubMed
17.
Passamonti F, Cattaneo C, Arcaini L, Bruna R, Cavo M, Merli F et al (2020) Clinical characteristics and risk factors associated with COVID-19 severity in patients with haematological malignancies in Italy: a retrospective, multicentre, cohort study. Lancet Haematol 7(10):e737–e745CrossRefPubMedPubMedCentral
18.
Łyżwa E, Sobiecka M, Lewandowska K, Siemion-Szcześniak I, Barańska I, Klatt M et al (2023) Prolonged SARS-CoV-2 Infection and Organizing Pneumonia in a Patient with Follicular Lymphoma, Treated with Obinutuzumab-Challenging Recognition and Treatment. Viruses. 15:693 (Switzerland)CrossRefPubMedPubMedCentral
19.
Huang L, Tong X, Cui J, Du X, Liao Y, Tan X et al (2024) Recurrent and persistent fever after SARS-CoV-2 infection in patients with follicular lymphoma: A case series. Int J Infect Dis 141:106973CrossRefPubMed
20.
Martínez-Barranco P, García-Roa M, Trelles-Martínez R, Arribalzaga K, Velasco M, Guijarro C et al (2022) Management of persistent SARS-CoV-2 infection in patients with follicular Lymphoma. Acta Haematol 145(4):384–393CrossRefPubMed
21.
Maruyama S, Wada D, Kanayama S, Shimazu H, Miyano Y, Inoue A et al (2024) The evaluation of risk factors for prolonged viral shedding during anti-SARS-CoV-2 monoclonal antibodies and long-term administration of antivirals in COVID-19 patients with B-cell lymphoma treated by anti-CD20 antibody. BMC Infect Dis 24(1):715CrossRefPubMedPubMedCentral
22.
Luminari S, Manni M, Galimberti S, Versari A, Tucci A, Boccomini C et al (2022) Response-adapted postinduction strategy in patients with advanced-stage Follicular Lymphoma: The FOLL12 study. J Clin Oncol 40(7):729–739CrossRefPubMed
23.
Rajamäki A, Hujo M, Sund R, Prusila REI, Kuusisto MEL, Kuitunen H et al (2022) Mortality among patients with low-grade follicular lymphoma: A binational retrospective analysis. Cancer 128(13):2474–2482CrossRefPubMed
24.
Lim YJ, Ward V, Brown A, Phillips E, Kronsteiner B, Malone T et al (2024) Immunogenicity of COVID-19 vaccines in patients with follicular lymphoma receiving frontline chemoimmunotherapy. Br J Haematol 205(2):440–451CrossRefPubMed
25.
Chong EA, Kumashie KG, Chong ER, Fabrizio J, Gupta A, Svoboda J et al (2024) Immunologic predictors of vaccine responsiveness in patients with lymphoma and chronic lymphocytic leukemia. J Infect Dis 230(1):15–27CrossRefPubMedPubMedCentral
26.
Spanjaart AM, Ljungman P, Tridello G, Schwartz J, Martinez-Cibrián N, Barba P et al (2024) Improved outcome of COVID-19 over time in patients treated with CAR T-cell therapy: Update of the European COVID-19 multicenter study on behalf of the European Society for Blood and Marrow Transplantation (EBMT) Infectious Diseases Working Party (IDWP) and the European Hematology Association (EHA) Lymphoma Group. Leukemia 38(9):1985–1991CrossRefPubMedPubMedCentral
27.
Lori LA, Falchi L, Vermaat JSP (2024) Epcoritamab with rituximab + lenalidomide (R2) in previously untreated (1L) follicular lymphoma (FL) and epcoritamab maintenance in FL: EPCORE NHL-2 arms 6 and 7. J Clin Oncol 42(16):suppl.70
Metadata
Title
Anti-CD20 maintenance strategies to face the challenge of COVID-19 pandemic in follicular lymphoma: results from the R-FolSTOP multicentre Italian study
Authors
Alessia Castellino
Lorenzo Comba
Laura Bertolotti
Carola Boccomini
Michele Clerico
Paolo Nicoli
Anna Vanazzi
Fulvia Fanelli
Tommasina Perrone
Francesco Marchesi
Federica Cocito
Michele Merli
Sara Bigliardi
Bianca Mecacci
Valentina Bozzoli
Gloria Margiotta-Casaluci
Erika Meli
Antonella Anastasia
Lucia Farina
Ombretta Annibali
Annarita Conconi
Sara Ratotti
Sara Galimberti
Claudia Castellino
Massimo Massaia
Publication date
12-03-2025
Publisher
Springer Berlin Heidelberg
Published in
Annals of Hematology
Print ISSN: 0939-5555
Electronic ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-025-06295-0

Elevate your expertise in aplastic anemia (Link opens in a new window)

Transform the way you care for your patients with aplastic anemia with our 3-module series using real-world case studies and expert insights. Discover why early diagnosis matters, explore the benefits and risks of current treatments, and develop tailored approaches for complex cases. 

Supported by:
  • Pfizer
Developed by: Springer Healthcare IME
Learn more

Keynote series | Spotlight on menopause

Menopause can have a significant impact on the body, with effects ranging beyond the endocrine and reproductive systems. Learn about the systemic effects of menopause, so you can help patients in your clinics through the transition.   

Prof. Martha Hickey
Dr. Claudia Barth
Dr. Samar El Khoudary
Developed by: Springer Medicine
Watch now
Video
Image Credits