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1 This article was downloaded by:[heal-link Consortium] On: 27 July 2008 Access Details: [subscription number ] Publisher: Informa Healthcare Informa Ltd Registered in England and Wales Registered Number: Registered office: Mortimer House, Mortimer Street, London W1T 3JH, UK Leukemia and Lymphoma Publication details, including instructions for authors and subscription information: Phase II study of low-grade non-hodgkin lymphomas with fludarabine and mitoxantrone followed by rituximab consolidation: Promising results in marginal zone lymphoma Theofanis Economopoulos a ; Amanda Psyrri a ; George Fountzilas b ; Constantinos Tsatalas c ; Athanasios Anagnostopoulos d ; Sotirios Papageorgiou a ; Nikolaos Xiros a ; Meletios Athanasios Dimopoulos d a Second Department of Internal Medicine, Attikon University Hospital, Athens, Greece b Department of Medicinal Oncology, Papageorgiou University Hospital, Thessaloniki, Greece c Department of Hematology, University Hospital of Alexandroupolis, Alexandroupolis, Greece d Department of Clinical Therapeutics, Alexandra University Hospital, Athens, Greece Online Publication Date: 01 January 2008 To cite this Article: Economopoulos, Theofanis, Psyrri, Amanda, Fountzilas, George, Tsatalas, Constantinos, Anagnostopoulos, Athanasios, Papageorgiou, Sotirios, Xiros, Nikolaos and Dimopoulos, Meletios Athanasios (2008) 'Phase II study of low-grade non-hodgkin lymphomas with fludarabine and mitoxantrone followed by rituximab consolidation: Promising results in marginal zone lymphoma', Leukemia and Lymphoma, 49:1, To link to this article: DOI: / URL: PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: This article maybe used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.
2 Leukemia & Lymphoma, January 2008; 49(1): ORIGINAL ARTICLE: CLINICAL Phase II study of low-grade non-hodgkin lymphomas with fludarabine and mitoxantrone followed by rituximab consolidation: Promising results in marginal zone lymphoma THEOFANIS ECONOMOPOULOS 1, AMANDA PSYRRI 1, GEORGE FOUNTZILAS 2, CONSTANTINOS TSATALAS 3, ATHANASIOS ANAGNOSTOPOULOS 4, SOTIRIOS PAPAGEORGIOU 1, NIKOLAOS XIROS 1,& MELETIOS ATHANASIOS DIMOPOULOS 4 1 Second Department of Internal Medicine, Attikon University Hospital, Athens, Greece, 2 Department of Medicinal Oncology, Papageorgiou University Hospital, Thessaloniki, Greece, 3 Department of Hematology, University Hospital of Alexandroupolis, Alexandroupolis, Greece, and 4 Department of Clinical Therapeutics, Alexandra University Hospital, Athens, Greece (Received 22 May 2007; revised 26 October 2007; accepted 2 November 2007) Abstract The majority of patients with indolent lymphomas relapse due to minimal residual disease (MRD). In the present study, we sought to determine whether by using rituximab consolidation, for eradication of MRD, following induction chemotherapy with fludarabine and mitoxantrone (FN) combination could improve the outcome of indolent lymphomas. Patients with indolent lymphoma received fludarabine 25 mg/m 2 Day 1 3 and mitoxantrone 10 mg/m 2 on Day 1 every 28 days. Patients who attained a response (complete response, CR or partial response, PR) received four weekly doses of Rituximab 375 mg/m 2 1 month and 3 months after completion of treatment. Forty-five patients were entered into this Phase II trial. The median follow-up time was 39 months. The median number of delivered cycles was 6. Fifty-three percent of patients attained a CR and 38% a PR for an overall response rate of 91%. One patient had stable disease, one had progression of the disease, whereas 2 were non-evaluable. After a median follow-up of 39 months, 32 of 46 patients (74%) are alive and disease-free. Grade III and IV toxicities included leucopenia (37%), neutropenia (28%), thrombocytopenia (7%), anemia (4%), and diarrhea (2%). Grade V toxicities included septic death in one patient and death due to hepatititis B reactivation 6 months after the last Rituximab dose in another patient. FN followed by R consolidation is a well-tolerated and active regimen in the treatment of patients with indolent lymphomas. Further follow-up is required to determine if these remissions are maintained. Keywords: Low-grade NHL, chemotherapy, rituximab Introduction Indolent lymphomas usually lack disease-related symptoms and are diagnosed at advanced stage (III or IV). Most patients with indolent lymphomas attain a complete response (CR) after treatment, but eventually most of them are destined to relapse [1]. Until the introduction of the anti-cd20 antibody rituximab in the treatment of B-cell lymphomas [2,3], survival data for indolent lymphoma had essentially remained unchanged for several decades, with a median survival time of approximately 7 years [4,5]. The standard treatment options for patients with indolent lymphomas have been careful observation or chemotherapy [5]. Radiotherapy is a consideration for the rare patient with stage I disease or for patients with bulky disease and compromise of vital organs. The results of these strategies have been suboptimal and, despite the long course, most patients relapse, probably due to minimal residual disease (MRD) [6]. Correspondence: Amanda Psyrri, MD, Second Department of Internal Medicine, Attikon University Hospital, Rimini 1, Haidari, Athens, Greece. diamando.psyrri@yale.edu ISSN print/issn online Ó 2008 Informa UK Ltd. DOI: /
3 Increase in cure rate is a major therapeutic goal in low-grade lymphomas since, despite the long course, the majority of patients will eventually succumb to the disease. It is known that even complete clinical responders with indolent lymphomas often have MRD. Molecular remission (MR) is a sign of major cytoreduction, although it is not always translated to disease eradication. It has been shown that patients attaining a molecular remission may sustain a durable clinical remission, suggesting that increase in survival is a reasonable treatment goal for a proportion of patients. Rituximab, a human chimeric monoclonal antibody to the CD20 antigen was approved in 1998 and it has since been introduced in the treatment of B-cell lymphomas [7]. The addition of Rituximab to chemotherapy regimens in patients with B-cell lymphomas has dramatically improved patient outcome [8]. Rituximab combined with chemotherapy significantly improves response rates, response duration and overall survival in low-grade lymphomas at first and second line settings [2,9 15]. Rituximab (Mabthera) was originally tested in patients with recurrent indolent non-hodgkin lymphomas (NHL) and demonstrated consistent results across numerous studies. Specifically, Rituximab therapy in indolent lymphomas induces a durable response in approximately 50% of patients with refractory or recurrent disease and in up to 73% in patients with untreated disease [16]. Rituximab can also induce molecular remissions in cases harbouring minimal residual disease after chemotherapy [17]. We [18], along with others [19,20], had previously reported excellent results with the combination of fludarabine and mitoxantrone (FN) in the treatment of indolent lymphomas. The regimen is well tolerated and at least as effective as older anthracycline-containing regimens [21]. We conducted a Phase II trial in patients with indolent lymphoma using the FN combination for remission induction. Patients who attained a complete or partial response received Rituximab consolidation. The current study was conducted to assess the safety profile and clinical activity of rituximab in combination with fludarabine and mitoxantrone in patients with indolent lymphomas. Materials and methods Study design An open Phase II trial was conducted at four institutions in Greece.The primary objective was to assess the efficacy of the regimen, with response rates (overall response (OR), complete response (CR), and partial remission (PR)) determined according to FN plus rituximab in low-grade NHL 69 International Workshop of Standardized Response Criteria for NHL [22]. Secondary objectives were to assess the duration of remission, overall survival and safety. The study was conducted with local ethics committee approval, and all patients gave written informed consent prior to enrollment. Toxicity was graded according to the WHO criteria. Patients Patients were entered into the study after written informed consent was obtained according to institutional guidelines. Entry criteria included (1) Patients with previously untreated low-grade lymphoma who required treatment; (2) confirmation of the histologic diagnosis of low-grade lymphoma according to WHO classification; (3) adequate renal function (creatinine levels 52 mg/dl) and hepatic function (bilirubin levels 52 mg/dl), unless these abnormalities were due to organ infiltration by lymphocytes; (4) a life expectancy of at least 12 weeks (5) Eastern Cooperative Oncology Group Performance Status (ECOG-PS) 2; (6) age 416 years. Exclusion criteria were active infection, human immunodeficiency virus-positive disease, Grade III or IV heart failure, according to the New York Heart Association functional classification and arrhythmias. Patients who had positive direct antiglobulin (Coombs) test results were not excluded from the trial. Therapy The regimen of fludarabine and mitoxantrone (FN) included intravenous fludarabine 25 mg/m 2 over 30 min on Days 1 3 and intravenous mitoxantrone 10 mg/m 2 over 15 min on Day 1 administered 4 h after completion of the first dose of fludarabine. FN therapy was repeated every 4 weeks for a maximum of 6 courses. Patients who did not achieve at least stable disease after three cycles of FN were withdrawn from the study. Patients who attained a response (CR or PR) received 4 weekly doses of consolidation Rituximab 1 month and 3 months after completion of treatment. Gastrointestinal lymphomas received the protocol treatment regardless of the type and extent of surgical intervention. If grade 3 or 4 neutropenia and/or thrombocytopenia occurred, treatment was delayed by one week. In cases of persistent neutropenia, G-CSF was administered with the next chemotherapy cycle. Monitoring At enrollment, a pretreatment evaluation was performed. This included acquisition of medical history,
4 70 T. Economopoulos et al. physical examination with assessment of lymph node, liver, and spleen size, a computed tomography (CT) scan of the thorax and abdomen, and full laboratory analysis of blood parameters including LDH, b2 microglobulin and serum immunoglobulins. Bone marrow aspiration and biopsy were performed and immunophenotyping of lymphoma cells in blood or bone marrow was carried out by flow cytometry. Patients were re-evaluated after 3 courses and at the end of chemotherapy. Restaging evaluation included CBC, full chemistry panel, bone marrow biopsy and CT chest/abdomen/pelvis. One month after completion of rituximab consolidation all the above tests were repeated. Patients with bone marrow involvement or monoclonal gammopathy underwent repeat bone marrow biopsy and serum immunoelectrophoresis 1 month after completion of therapy. During treatment, blood counts and a differential were analyzed once weekly. During follow-up, physical examination was performed monthly between months 2 and 6 and quarterly thereafter. A chest and abdominal CT scan was performed twice yearly to a maximum of 2 years. Follow-up examinations were stopped if patients were diagnosed with PD. Response criteria The response criteria were those defined by the International Workshop of Standardized Response Criteria for NHL [22] with the modification that CR had to be confirmed by the first follow-up examination 3 months after restaging. Death without progression during treatment, or within 4 weeks of the end of therapy from causes other than lymphoma was designated as treatment-related death. No bone marrow evaluation was required for determinations of PR. Toxicities were graded according to the WHO Criteria. Statistical considerations The primary endpoint of this study was to evaluate the response of chemotherapy and the secondary were survival and toxicity. Sample size was based on overall response rate. According to Simon s two stage minimax design, assuming that the expected overall response rate will be at least 85% and the minimum acceptable response rate 70%, a sample of 23 patients would be required in the first step. Since more than 17 responses were observed, a total of 49 patients were needed to be accrued. Thereby, if than 40 responses occurred, the probability of accepting a treatment with a real response rate of less than 70% would be 5%. On the other hand, the risk of rejecting a treatment (at the second stage) with a response rate of more than 85% would be 20%. Overall survival (OS) and time to disease progression (TTP) were estimated using the Kaplan Meier method. OS was estimated from the date of initial diagnosis until the date of last follow-up or death. TTP was defined as the time between date of initial diagnosis and the date of documented recurrence or last follow up. Deaths due to disease-related factors without previous documentation of disease progression were considered as events for the evaluation of TTP. Univariate Cox regression analysis was performed in order to evaluate the effect of age (as a continuous variable), gender (male versus female), performance status (1 or 2 versus 0) and LDH (abnormal versus normal). In case of TTP, stage (III, IV versus I, II) was included in a univariate Cox model, while for the overall survival, stage was not included in this analysis since all deaths were observed in the group of stage IV patients. Results Patient characteristics Fifty-two patients were enrolled, 45 were evaluable for toxicity and response. Seven patients were registered but were ineligible and never received treatment because two had aggressive lymphoma and five had received prior treatment. Patient characteristics are detailed in Table I. The median age was 63 years (range, years). Six patients (13%) had Stage I, 7 (16%) Stage II, 3 Stage III (7%) and 29 (64%) Stage IV disease. All patients with Stage I had gastric lymphoma. Thirty-six (80%) of 45 patients had PS 0. Eleven patients (24%) had elevated LDH. Histology was distributed as follows: small lymphocytic lymphoma/chronic lymphocytic leukemia (SLL/CLL) 15 patients (33%), splenic marginal zone lymphoma 2 (4%), lymphoplasmocytic lymphoma 1 patient (2%), marginal zone B-cell lymphoma 15 (33%) (extranodal 11 and nodal 4), follicular Grade I 6 (13%) and follicular Grade II 5 (11%) patients. One patient had both splenic marginal zone and extranodal lymphoma (2%). Sixty-four percent of patients had 2 or more negative prognostic factors. Toxicity A total of 249 courses were administered with a median of 6(1 8) courses (Table II). The treatment was well tolerated and the intended dose-intensity was delivered.
5 Table I. Patient and disease characteristics (N ¼ 45). Age Median 63 Range Age group (44)* 60 25(56) Sex Male 23(51) Female 22(49) PS 0 36(80) 1 6(13) 2 3(7) LDH Normal 33(73) Abnormal 11(24) Unknown 1(2) Extra nodal sites 0 27(60) 1 16(36) 2 2(4) Stage I { 6(13) II 7(16) III 3(7) IV 29(64) Histology { SLL 15(33) Lymphoplasmacytic lymphoma 1(2) Marginal zone B-cell Extranodal 12(26) Nodal 4(9) Splenic 3(7) Follicular Grade I 6(13) Follicular Grade II 5(11) FN plus rituximab in low-grade NHL 71 Table II. Treatment characteristics (N ¼ 45). Number of cycles per patient N % Total number of cycles delivered 249 Median (range) 6 (1 8) DI of Fludarabine (mg/m 2 /wk) Median delivered Range 7 27 Relative DI of Fludarabine Median delivered 1.01 Range DI of Mitoxantrone (mg/m 2 /wk) Median delivered 2.47 Range 2 3 Relative DI of Mitoxantrone Median delivered 0.99 Range DI of Rituximab (mg/m 2 /wk)* Median delivered Range Relative DI of Rituximab Median delivered 0.91 Range *Three patients did not receive mabthera (1 died during treatment, 1 had a disease progression and discontinued treatment and 1 had an allergic reaction on the first infusion and did not receive mabthera). Table III. Incidence of toxicity. *Values in parentheses indicate percentages. { Stage I gastric lymphoma. { Total number of histologic types is 46 because one patient had both splenic marginal zone lymphoma and extranodal Marginal zone B-cell. Table III shows toxicity data for the FN regimen. The main toxicity was myelosuppresion. Grade 3/4 leukocytopenia, neutropenia, anaemia and thrombocytopenia were developed in 17 (37%), 13 (29%), 3 (7%) and 2 (4%) patients, respectively. Four patients (9%) developed febrile neutropenia. Overall the treatment was well tolerated. Three of 45 patients did not receive rituximab: one died during treatment (septic shock), one had disease progression and discontinued treatment and one had an allergic reaction on the first infusion and did not receive rituximab. Grade V toxicities included septic death in one patient and death due to hepatititis B reactivation 6 months after the last Mabthera dose in another patient. N ¼ 45 Grade 1 Grade 2 Grade 3 Grade 4 Grade 5 Leucopenia 10 (22) 11 (24) 15 (33) 2 (4) Neutropenia 6 (13) 10 (22) 7 (16) 6 (13) Febrile 4 (9) Neutropenia Thrombocytopenia 4 (9) 2 (4) 3 (7) Anaemia 9 (20) 5 (11) 2 (4) Nausea/vomiting 6 (13) 2 (4) Allergic reaction 1 (2) Mucositis 1 (2) 1 (2) Diarrhea 2 (4) 1 (2) Infection 2 (4) 1 (2) Alopecia 3 (7) 3 (7) 3 (7) Neurotoxicity 1 (2) Fatigue 2 (4) 1 (2) Fever 5 (11) 5 (11) Cough 1 (2) Arthalgia/myalgia 1 (2) 1 (2) Anorexia 1 (2) Headache 1 (2) Septic death 1 (2%) Death due to 1 (2%) hepatitis
6 72 T. Economopoulos et al. Response The median follow-up time was 39 (range: 35 43) months. Twenty-four (53%) patients attained a complete response (CR/Cru) and 17 (38%) a partial response for an overall response rate of 91% (Table IV). One patient had stable disease and one developed disease progression. Patients with gastric lymphoma are still on complete remission. Survival, TTP for the entire cohort and duration of response (for complete responders only) curves are shown in Figure 1. At a median follow-up of 39 months, 13 patients relapsed and 5 died (3 from the disease, 1 from hepatic and renal failure due to reactivation of Hepatitis B six months after the last dose of Rituximab, 1 toxic death due to septic shock). For the entire cohort, 1-year OS rate was 93% and 1-year progression-free rate was 89% (Table V). Responses per stage and histology are listed in Table VI. Twenty-two of 24 complete responders remain in remission. Median OS, Table IV. Best response (N ¼ 45). Response N % 95% CI CR PR ORR SD PD N.E TTP and remission duration (for complete responders) rates for the entire cohort have not been reached. Discussion In the present study, our goal was to assess the safety profile and clinical activity of rituximab in combination with fludarabine and mitoxantrone in patients with indolent lymphomas. At a median follow-up of 39 months, median OS and TTP parameters have not yet been reached. Twenty-two of 24 complete responders remain in remission. The 3-year PFS rate of our regimen was 65% whereas FN combination alone has been associated with 3-year PFS rates of approximately 50% and 4-year PFS rates ranging between 38 and 43% [23,24]. Table V. Survival, TTP and remission duration (N ¼ 45). Survival Events 5/45 Range (months) year survival rate 87% Median Not reached yet 95% C.I. TTP Events* 13/45 Range (months) year progression-free rate 65% Median Not reached yet 95% C.I. Remission duration (for pts with CR) Events* 2/24 Range (months) Median Not reached yet 95% C.I. Follow-up Median 39 Range *Disease progression or death from disease related reasons. Figure 1. Kaplan Meier curves for patients survival ( ), TTP ( ) and duration of response (, complete responders only). Table VI. Response per stage and histology. CR (%) Other (%) Stage I 5 (83) 1 (17) II 4 (57) 3 (43) III 2 (67) 1 (33) IV 13 (45) 16 (55) Histology SLL 5 (33) 10 (67) Lymphoplasmocytic 0 (0) 1 (100) Marginal zone Extranodal 9 (82) 2 (18) Nodal 2 (50) 2 (50) Splenic 3 (100) 0 (0) Follicular 5 (45) 6 (55)
7 These results appear promising. However, we noted that marginal zone lymphomas had the higher complete response rates whereas follicular or small lymphocytic lymphomas displayed lower CR rates. One of the limitations of the present study is that it included patients with different histologic subtypes. The heterogeneity of the patient population combined with the small number of patients included in each histologic subtype limits our ability to derive definitive conclusions regarding efficacy of therapy per histological subtype. It appears that our regimen was effective in marginal zone lymphomas while it resulted in modest CR rates in follicular and small lymphocytic lymphomas. However, this regimen should be tested in homogeneous, in terms of histology, populations of indolent lymphomas before definitive conclusions are made. Furthermore, lowgrade lymphomas tend to have long natural history with a median survival of 8 10 years and further follow-up is required to determine if these remissions are maintained. Five randomized studies [25 29] have evaluated the role of Rituximab as consolidation therapy in patients with indolent B-cell lymphomas. These studies were conducted mainly in patients with follicular lymphomas. The incorporation of consolidation rituximab has been tested in the following settings: (1) following rituximab monotherapy; (2) following initial combination chemotherapy; and (3) following second-line or subsequent combination chemotherapy. In addition to the present study, only one other trial has studied the use of consolidation Rituximab, following initial combination chemotherapy. Hochster et al. [26] found a significant prolongation of response duration and survival by rituximab consolidation in patients with advanced-stage previously untreated follicular lymphoma responding to induction therapy with cyclophosphamide, vincristine, prednisone (CVP). Different schedules of Rituximab consolidation are applied in remission across different studies. While in the present study Rituximab was administered once a week for four consecutive weeks given at 1 and 3 months after entering remission, Hainsworth et al. [27] and Hochster et al. [26] used the 4 doses every 6 months schedule in their studies and Ghielmini et al. [25] administered infusions of Rituximab every 2 months, a total of 4 times. It still remains unclear which is the most effective dose and schedule of Rituximab for consolidation. The present study demonstrates that Rituximab consolidation following first-line FN induction chemotherapy yields promising results in marginal zone lymphomas. The Phase III trial conducted by Hochster et al. [26] also showed that Rituximab consolidation after CVP induction chemotherapy improves survival and prolongs remission duration in follicular lymphomas. The PRIMA study, a multicentre, Phase III randomized study in patients with advanced follicular lymphoma evaluating the benefit of consolidation therapy with Rituximab after induction of response with chemotherapy plus Rituximab in comparison with no consolidation therapy recently completed accrual and we are awaiting for the results. References FN plus rituximab in low-grade NHL Horning SJ. Natural history of and therapy for the indolent non-hodgkin s lymphomas. Semin Oncol 1993;20: Forstpointner R, Dreyling M, Repp R, Hermann S, Hanel A, Metzner B, et al. The addition of rituximab to a combination of fludarabine, cyclophosphamide, mitoxantrone (FCM) significantly increases the response rate and prolongs survival as compared with FCM alone in patients with relapsed and refractory follicular and mantle cell lymphomas: results of a prospective randomized study of the German Low- Grade Lymphoma Study Group. Blood 2004;104: Herold M, Haas A, Srock S, Neser S, Al-Aki KH, Neubauer A, et al. Rituximab added to first-line mitoxantrone, chlorambucil, and prednisolone chemotherapy followed by interferon maintenance prolongs survival in patients with advanced follicular lymphoma: an East German Study Group Hematology and Oncology Study. J Clin Oncol 2007;25: Horning SJ. Follicular lymphoma: have we made any progress? Ann Oncol 2000;11(Suppl 1): Lister TA. The management of follicular lymphoma. Ann Oncol 1991;2(Suppl 2): Rambaldi A, Lazzari M, Manzoni C, Carlotti E, Arcaini L, Baccarani, et al. Monitoring of minimal residual disease after CHOP and rituximab in previously untreated patients with follicular lymphoma. Blood 2002;99: McLaughlin P, Grillo-Lopez AJ, Link BK, Levy R, Czuczman MS, Williams ME, et al. Rituximab chimeric anti-cd20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program. J Clin Oncol 1998;16: Colombat P, Salles G, Brousse N, Eftekhari P, Soubeyran P, Delwail V, et al. Rituximab (anti-cd20 monoclonal antibody) as single first-line therapy for patients with follicular lymphoma with a low tumor burden: clinical and molecular evaluation. Blood 2001;97: Economopoulos T, Fountzilas G, Pavlidis N, Kalantzis D, Papageorgiou E, Christodoulou C, et al. Rituximab in combination with CNOP chemotherapy in patients with previously untreated indolent non-hodgkin s lymphoma. Hematol J 2003;4: Czuczman MS, Grillo-Lopez AJ, White CA, Saleh M, Gordon L, LoBuglio AF, et al. Treatment of patients with low-grade B-cell lymphoma with the combination of chimeric anti-cd20 monoclonal antibody and CHOP chemotherapy. J Clin Oncol 1999;17: Davis TA, Grillo-Lopez AJ, White CA, McLaughlin P, Czuczman MS, Link BK, et al. Rituximab anti-cd20 monoclonal antibody therapy in non-hodgkin s lymphoma: safety and efficacy of re-treatment. J Clin Oncol 2000; 18:
8 74 T. Economopoulos et al. 12. Hiddemann W, Kneba M, Dreyling M, Schmitz N, Lengfelder E, Schmits R, 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 2005; 106: Marcus R, Imrie K, Belch A, Cunningham D, Flores E, Catalano J, et al. CVP chemotherapy plus rituximab compared with CVP as first-line treatment for advanced follicular lymphoma. Blood 2005;105: Herold M, Dolken G, Fiedler F, Franke A, Freund M, Helbig W, et al. Randomized phase III study for the treatment of advanced indolent non-hodgkin s lymphomas (NHL) and mantle cell lymphoma: chemotherapy versus chemotherapy plus rituximab. Ann Hematol 2003;82: Lenz G, Dreyling M, Hoster E, Wormann B, Duhrsen U, Metzner B, et al. Immunochemotherapy with rituximab and cyclophosphamide, doxorubicin, vincristine, and prednisone significantly improves response and time to treatment failure, but not long-term outcome in patients with previously untreated mantle cell lymphoma: results of a prospective randomized trial of the German Low Grade Lymphoma Study Group (GLSG). J Clin Oncol 2005;23: Schulz H, Skoetz N, Bohlius J, Treller S, Kober T, Greb A, et al. Does combined immunochemotherapy with the monoclonal antibody rituximab improve overall survival in the treatment of patients with indolent non-hodgkin lymphoma? Preliminary results of a comprehensive meta-analysis. Blood 2005;(ed 11): Schmitt C, Grundt A, Buchholtz C, Scheuer L, Benner A, Hensel M, et al. One single dose of rituximab added to a standard regimen of CHOP in primary treatment of follicular lymphoma appears to result in a high clearance rate from circulating bcl-2/igh positive cells: is the end of molecular monitoring near? Leuk Res 2006;30: Dimopoulos MA, Fountzilas G, Papageorgiou E, Kiamouris C, Mantzios G, Anagnostopoulos A, et al. Primary treatment of low-grade non-hodgkin s lymphoma with the combination of fludarabine and mitoxantrone: a phase II study of the Hellenic Cooperative Oncology Group. Leuk Lymphoma 2002;43: Seymour JF, Grigg AP, Szer J, Fox RM. Fludarabine and mitoxantrone: effective and well-tolerated salvage therapy in relapsed indolent lymphoproliferative disorders. Ann Oncol 2001;12: Zinzani PL, Magagnoli M, Bendandi M, Gherlinzoni F, Orcioni GF, Cellini C, et al. Efficacy of fludarabine and mitoxantrone (FN) combination regimen in untreated indolent non-hodgkin s lymphomas. Ann Oncol 2000;11: Zinzani PL, Pulsoni A, Perrotti A, Soverini S, Zaja F, De Renzo A, et al. Fludarabine plus mitoxantrone with and without rituximab versus CHOP with and without rituximab as front-line treatment for patients with follicular lymphoma. J Clin Oncol 2004;22: Cheson BD, Horning SJ, Coiffier B, Shipp MA, Fisher RI, Connors JM, et al. Report of an international workshop to standardize response criteria for non-hodgkin s lymphomas. NCI Sponsored International Working Group. J Clin Oncol 1999;17: Hagemeister F, Cabanillas F, Coleman M, Grecory SA, Zinzani PL. The role of mitoxantrone in the treatment of indolent lymphomas. Oncologist 2005;10: Foussard C, Colombat P, Maisonneuve H, Berthou C, Gressin R, Rousselet MC, et al. Long-term follow-up of a randomized trial of fludarabine-mitoxantrone, compared with cyclophosphamide, doxorubicin, vindesine, prednisone (CHVP), as first-line treatment of elderly patients with advanced, low-grade non-hodgkin s lymphoma before the era of monoclonal antibodies. Ann Oncol 2005;16: Ghielmini M, Schmitz SF, Cogliatti SB, Pichert G, Hummerjohann J, Waltzer U, et al. Prolonged treatment with rituximab in patients with follicular lymphoma significantly increases event-free survival and response duration compared with the standard weekly64 schedule. Blood 2004;103: Hochster HS, Weller E, Gascoyne R, Teodorovic I, Rosewics C, Klasa R, et al. Maintenance rituximab after CVP results in superior clinical outcome in advanced follicular lymphoma (FL): results of the E1496 phase III trial from the Eastern Cooperative Oncology Group and the Cancer and Leukemia Group B. Blood 2005;(ed 11): Hainsworth JD, Litchy S, Shaffer DW, Lackey VL, Grimaldi M, Greco FA. 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. J Clin Oncol 2005;23: van Oers MH, Klasa R, Marcus RE, Wolf M, Kimby E, Gascoyne RD, et al. Rituximab maintenance improves clinical outcome of relapsed/resistant follicular non-hodgkin lymphoma in patients both with and without rituximab during induction: results of a prospective randomized phase 3 intergroup trial. Blood 2006;108: Forstpointner R, Unterhalt M, Dreyling M, Bock HP, Repp R, Wandt H, et al. Maintenance therapy with rituximab leads to a significant prolongation of response duration after salvage therapy with a combination of rituximab, fludarabine, cyclophosphamide, and mitoxantrone (R-FCM) in patients with recurring and refractory follicular and mantle cell lymphomas: results of a prospective randomized study of the German Low Grade Lymphoma Study Group (GLSG). Blood 2006;108:
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