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Journal of Clinical Oncology, Vol 17, Issue 1 (January), 1999: 268
© 1999 American Society for Clinical Oncology

Treatment of Patients With Low-Grade B-Cell Lymphoma With the Combination of Chimeric Anti-CD20 Monoclonal Antibody and CHOP Chemotherapy

M. S. Czuczman, A. J. Grillo-López, C. A. White, M. Saleh, L. Gordon, A. F. LoBuglio, C. Jonas, D. Klippenstein, B. Dallaire, C. Varns

From the Roswell Park Cancer Institute, Buffalo, NY; IDEC Pharmaceuticals Corporation, San Diego, CA; Sidney Kimmel Cancer Center, San Diego, CA; University of Alabama, Birmingham, AL; and Northwestern University, Chicago, IL.

Address reprint requests to Myron S. Czuczman, MD, Department of Hematologic Oncology and Bone Marrow Transplantation, Roswell Park Cancer Institute, Elm and Carlton Sts, Buffalo, NY 14263

PURPOSE: To determine the safety and efficacy of the combination of the chimeric anti-CD20 antibody, Rituxan (Rituximab, IDEC-C2B8; IDEC Pharmaceuticals Corporation, San Diego, CA), and cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) chemotherapy.

PATIENTS AND METHODS: Forty patients with low-grade or follicular B-cell non–Hodgkin's lymphoma received six infusions of Rituxan (375 mg/m2 per dose) in combination with six doses of CHOP chemotherapy.

RESULTS: The overall response rate was 95% (38 of 40 patients). Twenty-two patients experienced a complete response (55%), 16 patients had a partial response (40%), and two patients, who received no treatment, were classified as nonresponders. Medians for duration of response and time to progression had not been reached after a median observation time of 29 + months. Twenty-eight of 38 assessable patients (74%) continued in remission during this median follow-up period. The most frequent adverse events attributable to CHOP were alopecia (38 patients), neutropenia (31 patients), and fever (23 patients). The most frequent events attributed to Rituxan were fever and chills, observed primarily with the first infusion. No quantifiable immune response to the chimeric antibody was detected. In a subset of 18 patients, the bcl-2 [t(14;18)] translocation was positive in eight patients; seven of these patients had complete remissions and converted to polymerase chain reaction (PCR) negativity by completion of therapy.

CONCLUSION: This is the first report demonstrating the safety and efficacy of Rituxan anti-CD20 chimeric antibody in combination with standard-dose systemic chemotherapy in the treatment of indolent B-cell lymphoma. The clinical responses suggest an additive therapeutic benefit for the combination with no significant added toxicity. The conversion of bcl-2 from positive to negative by PCR in blood and/or marrow suggests possible clearing of minimal residual disease not previously demonstrated by CHOP chemotherapy alone.


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F. J. Hernandez-Ilizaliturri, V. Jupudy, J. Ostberg, E. Oflazoglu, A. Huberman, E. Repasky, and M. S. Czuczman
Neutrophils Contribute to the Biological Antitumor Activity of Rituximab in a Non-Hodgkin's Lymphoma Severe Combined Immunodeficiency Mouse Model
Clin. Cancer Res., December 1, 2003; 9(16): 5866 - 5873.
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T. A. Lister
High-Dose Therapy for Follicular Lymphoma Revisited: Not If, but When?
J. Clin. Oncol., November 1, 2003; 21(21): 3894 - 3896.
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J. Zhou, J. Chen, M. Mokotoff, R. Zhong, L. D. Shultz, and E. D. Ball
Bombesin/Gastrin-Releasing Peptide Receptor: A Potential Target for Antibody-Mediated Therapy of Small Cell Lung Cancer
Clin. Cancer Res., October 15, 2003; 9(13): 4953 - 4960.
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A. Conconi, G. Martinelli, C. Thieblemont, A. J. M. Ferreri, L. Devizzi, F. Peccatori, M. Ponzoni, E. Pedrinis, S. Dell'Oro, G. Pruneri, et al.
Clinical activity of rituximab in extranodal marginal zone B-cell lymphoma of MALT type
Blood, October 15, 2003; 102(8): 2741 - 2745.
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 LupusHome page
R Weide, J Heymanns, A Pandorf, and H Koppler
Successful long-term treatment of systemic lupus erythematosus with rituximab maintenance therapy
Lupus, October 1, 2003; 12(10): 779 - 782.
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M. Orjuela, T. G. Gross, Y.-K. Cheung, B. Alobeid, E. Morris, and M. S. Cairo
A Pilot Study of Chemoimmunotherapy (Cyclophosphamide, Prednisone, and Rituximab) in Patients with Post-Transplant Lymphoproliferative Disorder following Solid Organ Transplantation
Clin. Cancer Res., September 1, 2003; 9(10): 3945S - 3952.
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T. H. Westhoff, F. Jochimsen, A. Schmittel, M. Stoffler-Meilicke, J. H. Schafer, W. Zidek, W. H. Gerlich, and E. Thiel
Fatal hepatitis B virus reactivation by an escape mutant following rituximab therapy
Blood, September 1, 2003; 102(5): 1930 - 1930.
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O. W. Press, J. M. Unger, R. M. Braziel, D. G. Maloney, T. P. Miller, M. LeBlanc, E. R. Gaynor, S. E. Rivkin, and R. I. Fisher
A phase 2 trial of CHOP chemotherapy followed by tositumomab/iodine I 131 tositumomab for previously untreated follicular non-Hodgkin lymphoma: Southwest Oncology Group Protocol S9911
Blood, September 1, 2003; 102(5): 1606 - 1612.
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D. W. Blayney, M. L. LeBlanc, T. Grogan, E. R. Gaynor, R. A. Chapman, C. H. Spiridonidis, S. A. Taylor, S. I. Bearman, T. P. Miller, and R. I. Fisher
Dose-Intense Chemotherapy Every 2 Weeks With Dose-Intense Cyclophosphamide, Doxorubicin, Vincristine, and Prednisone May Improve Survival in Intermediate- and High-Grade Lymphoma: A Phase II Study of the Southwest Oncology Group (SWOG 9349)
J. Clin. Oncol., July 1, 2003; 21(13): 2466 - 2473.
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E. Voog, F. Morschhauser, P. Solal-Celigny, M. C. Benyunes, P. S. Multani, and A. Saunders
Neutropenia in Patients Treated with Rituximab
N. Engl. J. Med., June 26, 2003; 348(26): 2691 - 2694.
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W. S. Velasquez, D. Lew, T. M. Grogan, C. H. Spiridonidis, S. P. Balcerzak, S. R. Dakhil, T. P. Miller, K. S. Lanier, R. A. Chapman, and R. I. Fisher
Combination of Fludarabine and Mitoxantrone in Untreated Stages III and IV Low-Grade Lymphoma: S9501
J. Clin. Oncol., May 15, 2003; 21(10): 1996 - 2003.
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J. Mangel, R. Buckstein, K. Imrie, D. Spaner, E. Franssen, P. Pavlin, A. Boudreau, N. Pennell, D. Combs, and N. L. Berinstein
Pharmacokinetic study of patients with follicular or mantle cell lymphoma treated with rituximab as 'in vivo purge' and consolidative immunotherapy following autologous stem cell transplantation
Ann. Onc., May 1, 2003; 14(5): 758 - 765.
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S. Faderl, D. A. Thomas, S. O'Brien, G. Garcia-Manero, H. M. Kantarjian, F. J. Giles, C. Koller, A. Ferrajoli, S. Verstovsek, B. Pro, et al.
Experience with alemtuzumab plus rituximab in patients with relapsed and refractory lymphoid malignancies
Blood, May 1, 2003; 101(9): 3413 - 3415.
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J. Boye, T. Elter, and A. Engert
An overview of the current clinical use of the anti-CD20 monoclonal antibody rituximab
Ann. Onc., April 1, 2003; 14(4): 520 - 535.
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 ASH Education BookHome page
S. N. O'Brien, N. M.A. Blijlevens, T. H. Mahfouz, and E. J. Anaissie
Infections in Patients with Hematological Cancer: Recent Developments
Hematology, January 1, 2003; 2003(1): 438 - 472.
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J. C. Byrd, B. L. Peterson, V. A. Morrison, K. Park, R. Jacobson, E. Hoke, J. W. Vardiman, K. Rai, C. A. Schiffer, and R. A. Larson
Randomized phase 2 study of fludarabine with concurrent versus sequential treatment with rituximab in symptomatic, untreated patients with B-cell chronic lymphocytic leukemia: results from Cancer and Leukemia Group B 9712 (CALGB 9712)
Blood, January 1, 2003; 101(1): 6 - 14.
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M. E. Juweid
Radioimmunotherapy of B-Cell Non-Hodgkin's Lymphoma: From Clinical Trials to Clinical Practice
J. Nucl. Med., November 1, 2002; 43(11): 1507 - 1529.
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J. D. Hainsworth, S. Litchy, H. A. Burris III, D. C. Scullin Jr, S. W. Corso, D. A. Yardley, L. Morrissey, and F. A. Greco
Rituximab as First-Line and Maintenance Therapy for Patients With Indolent Non-Hodgkin's Lymphoma
J. Clin. Oncol., October 15, 2002; 20(20): 4261 - 4267.
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R. O. Dillman
Radiolabeled Anti-CD20 Monoclonal Antibodies for the Treatment of B-Cell Lymphoma
J. Clin. Oncol., August 15, 2002; 20(16): 3545 - 3557.
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M. Ladetto, P. Corradini, S. Vallet, F. Benedetti, U. Vitolo, M. Martelli, M. Brugiatelli, P. Coser, A. Perrotti, I. Majolino, et al.
High rate of clinical and molecular remissions in follicular lymphoma patients receiving high-dose sequential chemotherapy and autografting at diagnosis: a multicenter, prospective study by the Gruppo Italiano Trapianto Midollo Osseo (GITMO)
Blood, August 13, 2002; 100(5): 1559 - 1565.
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T. E. Witzig, I. W. Flinn, L. I. Gordon, C. Emmanouilides, M. S. Czuczman, M. N. Saleh, L. Cripe, G. Wiseman, T. Olejnik, P. S. Multani, et al.
Treatment With Ibritumomab Tiuxetan Radioimmunotherapy in Patients With Rituximab-Refractory Follicular Non-Hodgkin's Lymphoma
J. Clin. Oncol., August 1, 2002; 20(15): 3262 - 3269.
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 The OncologistHome page
P. McLaughlin
Progress and Promise in the Treatment of Indolent Lymphomas
Oncologist, June 1, 2002; 7(3): 217 - 225.
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M. A. Dimopoulos, C. Zervas, A. Zomas, C. Kiamouris, N. A. Viniou, V. Grigoraki, C. Karkantaris, C. Mitsouli, D. Gika, J. Christakis, et al.
Treatment of Waldenstrom's Macroglobulinemia With Rituximab
J. Clin. Oncol., May 1, 2002; 20(9): 2327 - 2333.
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 Stem CellsHome page
A. Countouriotis, T. B. Moore, and K. M. Sakamoto
Cell Surface Antigen and Molecular Targeting in the Treatment of Hematologic Malignancies
Stem Cells, May 1, 2002; 20(3): 215 - 229.
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 JCOHome page
O. M. Howard, J. G. Gribben, D. S. Neuberg, M. Grossbard, C. Poor, M. J. Janicek, and M. A. Shipp
Rituximab and CHOP Induction Therapy for Newly Diagnosed Mantle-Cell Lymphoma: Molecular Complete Responses Are Not Predictive of Progression-Free Survival
J. Clin. Oncol., March 1, 2002; 20(5): 1288 - 1294.
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E Drewe and R J Powell
Clinically useful monoclonal antibodies in treatment
J. Clin. Pathol., February 1, 2002; 55(2): 81 - 85.
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A. Rambaldi, M. Lazzari, C. Manzoni, E. Carlotti, L. Arcaini, M. Baccarani, T. Barbui, C. Bernasconi, G. Dastoli, G. Fuga, et al.
Monitoring of minimal residual disease after CHOP and rituximab in previously untreated patients with follicular lymphoma
Blood, February 1, 2002; 99(3): 856 - 862.
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J. C. Byrd, S. Kitada, I. W. Flinn, J. L. Aron, M. Pearson, D. Lucas, and J. C. Reed
The mechanism of tumor cell clearance by rituximab in vivo in patients with B-cell chronic lymphocytic leukemia: evidence of caspase activation and apoptosis induction
Blood, February 1, 2002; 99(3): 1038 - 1043.
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 NEJMHome page
B. Coiffier, E. Lepage, J. Briere, R. Herbrecht, H. Tilly, R. Bouabdallah, P. Morel, E. Van Den Neste, G. Salles, P. Gaulard, et al.
CHOP Chemotherapy plus Rituximab Compared with CHOP Alone in Elderly Patients with Diffuse Large-B-Cell Lymphoma
N. Engl. J. Med., January 24, 2002; 346(4): 235 - 242.
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B. D. Cheson
CHOP plus Rituximab -- Balancing Facts and Opinion
N. Engl. J. Med., January 24, 2002; 346(4): 280 - 282.
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J. M. Vose, B. C.-H. Chiu, B. D. Cheson, J. Dancey, and J. Wright
Update on Epidemiology and Therapeutics for Non-Hodgkin's Lymphoma
Hematology, January 1, 2002; 2002(1): 241 - 262.
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I. F. Khouri, R. M. Saliba, S. A. Giralt, M.-S. Lee, G.-J. Okoroji, F. B. Hagemeister, M. Korbling, A. Younes, C. Ippoliti, J. L. Gajewski, et al.
Nonablative allogeneic hematopoietic transplantation as adoptive immunotherapy for indolent lymphoma: low incidence of toxicity, acute graft-versus-host disease, and treatment-related mortality
Blood, December 15, 2001; 98(13): 3595 - 3599.
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B. Bellosillo, N. Villamor, A. Lopez-Guillermo, S. Marce, J. Esteve, E. Campo, D. Colomer, and E. Montserrat
Complement-mediated cell death induced by rituximab in B-cell lymphoproliferative disorders is mediated in vitro by a caspase-independent mechanism involving the generation of reactive oxygen species
Blood, November 1, 2001; 98(9): 2771 - 2777.
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 NEJMHome page
F. Suzan, M. Ammor, and V. Ribrag
Fatal Reactivation of Cytomegalovirus Infection after Use of Rituximab for a Post-Transplantation Lymphoproliferative Disorder
N. Engl. J. Med., September 27, 2001; 345(13): 1000 - 1000.
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C. L. Perez and S. Rudoy
Anti-CD20 Monoclonal Antibody Treatment of Human Herpesvirus 8-Associated, Body Cavity-Based Lymphoma with an Unusual Phenotype in a Human Immunodeficiency Virus-Negative Patient
Clin. Vaccine Immunol., September 1, 2001; 8(5): 993 - 996.
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D. Huhn, C. von Schilling, M. Wilhelm, A. D. Ho, M. Hallek, R. Kuse, W. Knauf, U. Riedel, A. Hinke, S. Srock, et al.
Rituximab therapy of patients with B-cell chronic lymphocytic leukemia
Blood, September 1, 2001; 98(5): 1326 - 1331.
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A. Renz, W. E. Berdel, M. Kreuter, C. Belka, K. Schulze-Osthoff, and M. Los
Rapid extracellular release of cytochrome c is specific for apoptosis and marks cell death in vivo
Blood, September 1, 2001; 98(5): 1542 - 1548.
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R. Stasi, A. Pagano, E. Stipa, and S. Amadori
Rituximab chimeric anti-CD20 monoclonal antibody treatment for adults with chronic idiopathic thrombocytopenic purpura
Blood, August 15, 2001; 98(4): 952 - 957.
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 Clin. Cancer Res.Home page
D. Shan, A. K. Gopal, and O. W. Press
Synergistic Effects of the Fenretinide (4-HPR) and Anti-CD20 Monoclonal Antibodies on Apoptosis Induction of Malignant Human B Cells
Clin. Cancer Res., August 1, 2001; 7(8): 2490 - 2495.
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M. Petryk and M. L. Grossbard
Hematologic Malignancies
Oncologist, August 1, 2001; 6(4): 317 - 326.
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D. G. Savage and R. Staron
Rituximab for Bone Lymphoma
Ann Intern Med, June 19, 2001; 134(12): 1156 - 1157.
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S. Modak, K. Kramer, S. H. Gultekin, H. F. Guo, and N.-K. V. Cheung
Monoclonal Antibody 8H9 Targets a Novel Cell Surface Antigen Expressed by a Wide Spectrum of Human Solid Tumors
Cancer Res., May 1, 2001; 61(10): 4048 - 4054.
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M.-A. Ghetie, H. Bright, and E. S. Vitetta
Homodimers but not monomers of Rituxan (chimeric anti-CD20) induce apoptosis in human B-lymphoma cells and synergize with a chemotherapeutic agent and an immunotoxin
Blood, March 1, 2001; 97(5): 1392 - 1398.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
R. Marches, E. S. Vitetta, and J. W. Uhr
A role for intracellular pH in membrane IgM-mediated cell death of human B lymphomas
PNAS, February 22, 2001; (2001) 61028998.
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J. M. Vose, B. K. Link, M. L. Grossbard, M. Czuczman, A. Grillo-Lopez, P. Gilman, A. Lowe, L. A. Kunkel, and R. I. Fisher
Phase II Study of Rituximab in Combination With CHOP Chemotherapy in Patients With Previously Untreated, Aggressive Non-Hodgkin's Lymphoma
J. Clin. Oncol., January 15, 2001; 19(2): 389 - 397.
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