Originally published as JCO Early Release 10.1200/JCO.2002.11.076 on April 22 2002
Journal of Clinical Oncology, Vol 20, Issue 10
(May), 2002: 2453-2463
© 2002 American Society for Clinical Oncology
Randomized Controlled Trial of Yttrium-90Labeled Ibritumomab Tiuxetan Radioimmunotherapy Versus Rituximab Immunotherapy for Patients With Relapsed or Refractory Low-Grade, Follicular, or Transformed B-Cell Non-Hodgkins Lymphoma
By Thomas E. Witzig,
Leo I. Gordon,
Fernando Cabanillas,
Myron S. Czuczman,
Christos Emmanouilides,
Robin Joyce,
Brad L. Pohlman,
Nancy L. Bartlett,
Gregory A. Wiseman,
Norman Padre,
Antonio J. Grillo-López,
Pratik Multani,
Christine A. White
From the Division of Internal Medicine and Hematology and Department of Radiology, Nuclear Medicine, Mayo Clinic and Mayo Foundation, Rochester, MN; Division of Hematology/Oncology and The Robert H. Lurie Comprehensive Cancer Center of Northwestern University, Chicago, IL; M.D. Anderson Cancer Center, Houston, TX; Roswell Park Cancer Center, Buffalo, NY; University of California Los Angeles Medical Center, Los Angeles, IDEC Pharmaceuticals Corporation, San Diego, and Clinical Research and Regulatory Strategy, Rancho Santa Fe, CA; Beth Israel Deaconess Medical Center, Boston, MA; The Cleveland Clinic Foundation, Cleveland, OH; and Washington University School of Medicine, St Louis, MO.
Address reprint requests to Thomas E. Witzig, MD, Mayo Clinic, 620 Stabile Building, Rochester, MN 55905; email: witzig{at}mayo.eduThis article was published online ahead of print at www.jco.org.
PURPOSE: Radioimmunotherapy combines biologic and radiolytic mechanisms to target and destroy tumor cells, thus offering a needed therapeutic alternative for refractory non-Hodgkins lymphoma (NHL) patients. This phase III randomized study compares the novel radioimmunotherapy yttrium-90 (90Y) ibritumomab tiuxetan with a control immunotherapy, rituximab, in 143 patients with relapsed or refractory low-grade, follicular, or transformed CD20+ transformed NHL.
PATIENTS AND METHODS: Patients received either a single intravenous (IV) dose of 90Y ibritumomab tiuxetan 0.4 mCi/kg (n = 73) or rituximab 375 mg/m2 IV weekly for four doses (n = 70). The radioimmunotherapy group was pretreated with two rituximab doses (250 mg/m2) to improve biodistribution and one dose of indium-111 ibritumomab tiuxetan for imaging and dosimetry. The primary end point, overall response rate (ORR), was assessed by an independent, blinded, lymphoma expert panel.
RESULTS: ORR was 80% for the 90Y ibritumomab tiuxetan group versus 56% for the rituximab group (P = .002). Complete response (CR) rates were 30% and 16% in the 90Y ibritumomab tiuxetan and rituximab groups, respectively (P = .04). An additional 4% achieved an unconfirmed CR in each group. Kaplan-Meier estimated median duration of response was 14.2 months in the 90Y ibritumomab tiuxetan group versus 12.1 months in the control group (P = .6), and time to progression was 11.2 versus 10.1 months (P = .173) in all patients. Durable responses of 6 months were 64% versus 47% (P = .030). Reversible myelosuppression was the primary toxicity noted with 90Y ibritumomab tiuxetan.
CONCLUSION: Radioimmunotherapy with 90Y ibritumomab tiuxetan is well tolerated and produces statistically and clinically significant higher ORR and CR compared with rituximab alone.

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J. Nucl. Med.,
February 1, 2006;
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S. M. Glaser, I. E. Hughes, J. R. Hopp, K. Hathaway, D. Perret, and M. E. Reff
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W. Hiddemann, M. Kneba, M. Dreyling, N. Schmitz, E. Lengfelder, R. Schmits, M. Reiser, B. Metzner, H. Harder, S. Hegewisch-Becker, et al.
Frontline therapy with rituximab added to the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) significantly improves the outcome for patients with advanced-stage follicular lymphoma compared with therapy with CHOP alone: results of a prospective randomized study of the German Low-Grade Lymphoma Study Group
Blood,
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P. S. Conti, C. White, P. Pieslor, A. Molina, J. Aussie, and P. Foster
The Role of Imaging with 111In-Ibritumomab Tiuxetan in the Ibritumomab Tiuxetan (Zevalin) Regimen: Results from a Zevalin Imaging Registry
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M. S. Kaminski, J. A. Radford, S. A. Gregory, J. P. Leonard, S. J. Knox, S. Kroll, and R. L. Wahl
Re-Treatment With I-131 Tositumomab in Patients With Non-Hodgkin's Lymphoma Who Had Previously Responded to I-131 Tositumomab
J. Clin. Oncol.,
November 1, 2005;
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R. I. Fisher, M. S. Kaminski, R. L. Wahl, S. J. Knox, A. D. Zelenetz, J. M. Vose, J. P. Leonard, S. Kroll, S. J. Goldsmith, and M. Coleman
Tositumomab and Iodine-131 Tositumomab Produces Durable Complete Remissions in a Subset of Heavily Pretreated Patients With Low-Grade and Transformed Non-Hodgkin's Lymphomas
J. Clin. Oncol.,
October 20, 2005;
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A. Nademanee, S. Forman, A. Molina, H. Fung, D. Smith, A. Dagis, C. Kwok, D. Yamauchi, A.-L. Anderson, P. Falk, et al.
A phase 1/2 trial of high-dose yttrium-90-ibritumomab tiuxetan in combination with high-dose etoposide and cyclophosphamide followed by autologous stem cell transplantation in patients with poor-risk or relapsed non-Hodgkin lymphoma
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P. F. Ferrucci, A. Vanazzi, G. Tesoriere, M. Ferrari, M. Bartolomei, P. Rocca, M. Cremonesi, G. Paganelli, and G. Martinelli
Cerebrospinal fluid diffusion of Zevalin(R) after high-activity treatment and stem cell support in a patient affected by diffuse large B-cell non-Hodgkin's lymphoma with central nervous system involvement
Ann. Onc.,
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D. M. Goldenberg
Introduction to the Tenth Conference on Cancer Therapy with Antibodies and Immunoconjugates
Clin. Cancer Res.,
October 1, 2005;
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G. L. DeNardo, E. Tobin, K. Chan, B. M. Bradt, and S. J. DeNardo
Direct Antilymphoma Effects on Human Lymphoma Cells of Monotherapy and Combination Therapy with CD20 and HLA-DR Antibodies and 90Y-Labeled HLA-DR Antibodies
Clin. Cancer Res.,
October 1, 2005;
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S. A. Jacobs, N. Vidnovic, J. Joyce, B. McCook, F. Torok, and N. Avril
Full-Dose 90Y Ibritumomab Tiuxetan Therapy Is Safe in Patients with Prior Myeloablative Chemotherapy
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W. Hiddemann, C. Buske, M. Dreyling, O. Weigert, G. Lenz, R. Forstpointner, C. Nickenig, and M. Unterhalt
Treatment Strategies in Follicular Lymphomas: Current Status and Future Perspectives
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J. P. Leonard, M. Coleman, L. Kostakoglu, A. Chadburn, E. Cesarman, R. R. Furman, M. W. Schuster, R. Niesvizky, D. Muss, J. Fiore, et al.
Abbreviated Chemotherapy With Fludarabine Followed by Tositumomab and Iodine I 131 Tositumomab for Untreated Follicular Lymphoma
J. Clin. Oncol.,
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J. P. Leonard, M. Coleman, J. Ketas, M. Ashe, J. M. Fiore, R. R. Furman, R. Niesvizky, T. Shore, A. Chadburn, H. Horne, et al.
Combination Antibody Therapy With Epratuzumab and Rituximab in Relapsed or Refractory Non-Hodgkin's Lymphoma
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A. V. Rao, G. Akabani, and D. A. Rizzieri
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O. Linden, C. Hindorf, E. Cavallin-Stahl, W. A. Wegener, D. M. Goldenberg, H. Horne, T. Ohlsson, L. Stenberg, S.-E. Strand, and J. Tennvall
Dose-Fractionated Radioimmunotherapy in Non-Hodgkin's Lymphoma Using DOTA-Conjugated, 90Y-Radiolabeled, Humanized Anti-CD22 Monoclonal Antibody, Epratuzumab
Clin. Cancer Res.,
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J. M. Bennett, M. S. Kaminski, J. P. Leonard, J. M. Vose, A. D. Zelenetz, S. J. Knox, S. Horning, O. W. Press, J. A. Radford, S. M. Kroll, et al.
Assessment of treatment-related myelodysplastic syndromes and acute myeloid leukemia in patients with non-Hodgkin lymphoma treated with tositumomab and iodine I131 tositumomab
Blood,
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A. Hagenbeek and V. Lewington
Report of a European consensus workshop to develop recommendations for the optimal use of 90Y-ibritumomab tiuxetan (Zevalin(R)) in lymphoma
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A. P Levene, G. Singh, and C. Palmieri
Therapeutic monoclonal antibodies in oncology
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J. D. Hainsworth, S. Litchy, D. W. Shaffer, V. L. Lackey, M. Grimaldi, and F. A. Greco
Maximizing Therapeutic Benefit of Rituximab: Maintenance Therapy Versus Re-Treatment at Progression in Patients With Indolent Non-Hodgkin's Lymphoma--A Randomized Phase II Trial of the Minnie Pearl Cancer Research Network
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February 20, 2005;
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J. M. Connors
Radioimmunotherapy -- Hot New Treatment for Lymphoma
N. Engl. J. Med.,
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D. M. Goldenberg and R. M. Sharkey
Radioimmunotherapy of Non-Hodgkin's Lymphoma Revisited
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S. J. Horning, A. Younes, V. Jain, S. Kroll, J. Lucas, D. Podoloff, and M. Goris
Efficacy and Safety of Tositumomab and Iodine-131 Tositumomab (Bexxar) in B-Cell Lymphoma, Progressive After Rituximab
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February 1, 2005;
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M. Ginj, J. Chen, M. A. Walter, V. Eltschinger, J. C. Reubi, and H. R. Maecke
Preclinical Evaluation of New and Highly Potent Analogues of Octreotide for Predictive Imaging and Targeted Radiotherapy
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E. R. Nemecek, D. K. Hamlin, D. R. Fisher, K. A. Krohn, J. M. Pagel, F. R. Appelbaum, O. W. Press, and D. C. Matthews
Biodistribution of Yttrium-90-Labeled Anti-CD45 Antibody in a Nonhuman Primate Model
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M. Z. Lin, M. A. Teitell, and G. J. Schiller
The Evolution of Antibodies into Versatile Tumor-Targeting Agents
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A. S. Freedman
Biology and Management of Histologic Transformation of Indolent Lymphoma
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L. S. Shahied, Y. Tang, R. K. Alpaugh, R. Somer, D. Greenspon, and L. M. Weiner
Bispecific Minibodies Targeting HER2/neu and CD16 Exhibit Improved Tumor Lysis When Placed in a Divalent Tumor Antigen Binding Format
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J. W. Friedberg
Radioimmunotherapy for Non-Hodgkin's Lymphoma
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T. A. Davis, M. S. Kaminski, J. P. Leonard, F. J. Hsu, M. Wilkinson, A. Zelenetz, R. L. Wahl, S. Kroll, M. Coleman, M. Goris, et al.
The Radioisotope Contributes Significantly to the Activity of Radioimmunotherapy
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C.-L. Law, C. G. Cerveny, K. A. Gordon, K. Klussman, B. J. Mixan, D. F. Chace, D. L. Meyer, S. O. Doronina, C. B. Siegall, J. A. Francisco, et al.
Efficient Elimination of B-Lineage Lymphomas by Anti-CD20-Auristatin Conjugates
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S. S. Dave, G. Wright, B. Tan, A. Rosenwald, R. D. Gascoyne, W. C. Chan, R. I. Fisher, R. M. Braziel, L. M. Rimsza, T. M. Grogan, et al.
Prediction of Survival in Follicular Lymphoma Based on Molecular Features of Tumor-Infiltrating Immune Cells
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J. Christiansen and A. K. Rajasekaran
Biological impediments to monoclonal antibody-based cancer immunotherapy
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S. Hallmeyer and D. Peace
Integrative Tumor Board: Recurrent Lymphoma
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J. P. Leonard, M. Coleman, J. C. Ketas, A. Chadburn, R. Furman, M. W. Schuster, E. J. Feldman, M. Ashe, S. J. Schuster, W. A. Wegener, et al.
Epratuzumab, a Humanized Anti-CD22 Antibody, in Aggressive Non-Hodgkin's Lymphoma: Phase I/II Clinical Trial Results
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A. Forero, P. L. Weiden, J. M. Vose, S. J. Knox, A. F. LoBuglio, J. Hankins, M. L. Goris, V. J. Picozzi, D. B. Axworthy, H. B. Breitz, et al.
Phase 1 trial of a novel anti-CD20 fusion protein in pretargeted radioimmunotherapy for B-cell non-Hodgkin lymphoma
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L. I. Gordon, A. Molina, T. Witzig, C. Emmanouilides, A. Raubtischek, M. Darif, R. J. Schilder, G. Wiseman, and C. A. White
Durable responses after ibritumomab tiuxetan radioimmunotherapy for CD20+ B-cell lymphoma: long-term follow-up of a phase 1/2 study
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M. Bendandi, S. A. Pileri, and P. L. Zinzani
Challenging paradigms in lymphoma treatment
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A.J. Davies, A.Z.S. Rohatiner, S. Howell, K.E. Britton, S.E. Owens, I.N. Micallef, D.P. Deakin, B.M. Carrington, J.A. Lawrance, S. Vinnicombe, et al.
Tositumomab and Iodine I 131 Tositumomab for Recurrent Indolent and Transformed B-Cell Non-Hodgkin's Lymphoma
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Y. Du, J. Honeychurch, M. S. Cragg, M. Bayne, M. J. Glennie, P. W. M. Johnson, and T. M. Illidge
Antibody-induced intracellular signaling works in combination with radiation to eradicate lymphoma in radioimmunotherapy
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J. N. Winter, R. D. Gascoyne, and K. Van Besien
Low-Grade Lymphoma
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R. M. Sharkey, A. Brenner, J. Burton, G. Hajjar, S. P. Toder, A. Alavi, A. Matthies, D. E. Tsai, S. J. Schuster, E. A. Stadtmauer, et al.
Radioimmunotherapy of Non-Hodgkin's Lymphoma with 90Y-DOTA Humanized Anti-CD22 IgG (90Y-Epratuzumab): Do Tumor Targeting and Dosimetry Predict Therapeutic Response?
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J. Y. C. Wong, S. Shibata, L. E. Williams, C. S. Kwok, A. Liu, D. Z. Chu, D. M. Yamauchi, S. Wilczynski, D. N. Ikle, A. M. Wu, et al.
A Phase I Trial of 90Y-Anti-Carcinoembryonic Antigen Chimeric T84.66 Radioimmunotherapy with 5-Fluorouracil in Patients with Metastatic Colorectal Cancer
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T. A. Lister
High-Dose Therapy for Follicular Lymphoma Revisited: Not If, but When?
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V. Bhaskar, D. A. Law, E. Ibsen, D. Breinberg, K. M. Cass, R. B. DuBridge, F. Evangelista, S. M. Henshall, P. Hevezi, J. C. Miller, et al.
E-Selectin Up-Regulation Allows for Targeted Drug Delivery in Prostate Cancer
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A. K. Gopal, T. A. Gooley, D. G. Maloney, S. H. Petersdorf, J. F. Eary, J. G. Rajendran, S. A. Bush, L. D. Durack, J. Golden, P. J. Martin, et al.
High-dose radioimmunotherapy versus conventional high-dose therapy and autologous hematopoietic stem cell transplantation for relapsed follicular non-Hodgkin lymphoma: a multivariable cohort analysis
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P. K. E. Borjesson, E. J. Postema, J. C. Roos, D. R. Colnot, H. A. M. Marres, M. H. van Schie, G. Stehle, R. de Bree, G. B. Snow, W. J. G. Oyen, et al.
Phase I Therapy Study with 186Re-labeled Humanized Monoclonal Antibody BIWA 4 (Bivatuzumab) in Patients with Head and Neck Squamous Cell Carcinoma
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