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Anthracycline-containing regimens for treatment of follicular lymphoma in adults

  1. Gilad Itchaki1,*,
  2. Anat Gafter-Gvili2,
  3. Meir Lahav3,
  4. Liat Vidal2,
  5. Pia Raanani1,
  6. Ofer Shpilberg1,
  7. Mical Paul4

Editorial Group: Cochrane Haematological Malignancies Group

Published Online: 7 JUL 2013

Assessed as up-to-date: 17 APR 2013

DOI: 10.1002/14651858.CD008909.pub2

How to Cite

Itchaki G, Gafter-Gvili A, Lahav M, Vidal L, Raanani P, Shpilberg O, Paul M. Anthracycline-containing regimens for treatment of follicular lymphoma in adults. Cochrane Database of Systematic Reviews 2013, Issue 7. Art. No.: CD008909. DOI: 10.1002/14651858.CD008909.pub2.

Author Information

  1. 1

    Beilinson Hospital, Rabin Medical Center, Institute of Hematology, Davidoff Center, Petah Tikva, Israel

  2. 2

    Beilinson Hospital, Rabin Medical Center, Department of Medicine E, Petah Tikva, Israel

  3. 3

    Beilinson Hospital, Rabin Medical Center, Department of Medicine A, Petah Tikva, Israel

  4. 4

    Rambam Health Care Center. Haifa, Israel and Sackler Faculty of Medicine, Unit of Infectious Diseases, Tel Aviv, Israel

*Gilad Itchaki, Institute of Hematology, Davidoff Center, Beilinson Hospital, Rabin Medical Center, 39 Jabotinski Street, Petah Tikva, 49100, Israel.

Publication History

  1. Publication Status: New
  2. Published Online: 7 JUL 2013



References to studies included in this review

  1. References to studies included in this review
  2. References to studies excluded from this review
  3. References to ongoing studies
  4. Additional references
Federico 2013 {published and unpublished data}
  • Federico M, Luminari S, Dondi A, Tucci A, Vitolo U, Rigacci L, et al. R-CVP versus R-CHOP versus R-FM for the initial treatment of patients with advanced-stage follicular lymphoma: results of the FOLL05 trial conducted by the Fondazione Italiana Linfomi. Journal of Clinical Oncology 2013;31(12):1506-13.
Jones 1983 {published data only}
  • Jones SE, Grozea PN, Metz EN, Haut A, Stephens RL, Morrison FS, et al. Improved complete remission rates and survival for patients with large cell lymphoma treated with chemoimmunotherapy. A Southwest Oncology Group Study. Cancer 1983;51(6):1083-90.
Kimby 1994 {published data only}
  • Kimby E, Bjorkholm M, Gahrton G, Glimelius B, Hagberg H, Johansson B, et al. Chlorambucil/prednisone vs. CHOP in symptomatic low-grade non-Hodgkin's lymphomas: a randomized trial from the Lymphoma Group of Central Sweden. Annals of Oncology 1994;5 Suppl 2:67-71.
Lepage 1990 {published data only}
Peterson 2003 {published data only}
  • Peterson BA, Petroni GR, Frizzera G, Barcos M, Bloomfield CD, Nissen NI, et al. Prolonged single-agent versus combination chemotherapy in indolent follicular lymphomas: a study of the cancer and leukemia group B. Journal of Clinical Oncology 2003;21(1):5-15.
Taylor 2006 {published data only}
  • Taylor PR, White JM, Prescott RJ, Angus B, Galloway MJ, Jackson GH, et al. The addition of oral idarubicin to a chlorambucil/dexamethasone combination has a significant impact on time to treatment failure but none on overall survival in patients with low grade non-Hodgkin's lymphoma: results of the Scotland and Newcastle Lymphoma Group randomized NHL VIII trial. Leukemia & Lymphoma 2006;47(11):2321-30.
Unterhalt 1996 {published data only}
  • Unterhalt M, Herrmann R, Tiemann M, Parwaresch R, Stein H, Trumper L, et al. Prednimustine, mitoxantrone (PmM) vs cyclophosphamide, vincristine, prednisone (COP) for the treatment of advanced low-grade non-Hodgkin's lymphoma. German Low-Grade Lymphoma Study Group. Leukemia 1996;10(5):836-43.
Zinzani 2000 {published data only}
  • Zinzani PL, Magagnoli M, Moretti L, De Renzo A, Battista R, Zaccaria A, et al. Randomized trial of fludarabine versus fludarabine and idarubicin as frontline treatment in patients with indolent or mantle-cell lymphoma. Journal of Clinical Oncology 2000;18(4):773-9.

References to studies excluded from this review

  1. References to studies included in this review
  2. References to studies excluded from this review
  3. References to ongoing studies
  4. Additional references
Acker 1983 {published data only}
  • Acker B, Hoppe RT, Colby TV, Cox RS, Kaplan HS, Rosenberg SA. Histologic conversion in the non-Hodgkin's lymphomas. Journal of Clinical Oncology 1983;1(1):11-6.
Al-Ismail 1987 {published data only}
  • Al-Ismail SA, Whittaker JA, Gough J. Combination chemotherapy including epirubicin for the management of non-Hodgkin's lymphoma. European Journal of Cancer & Clinical Oncology 1987;23(9):1379-84.
Andersen 1990 {published data only}
  • Andersen J, Thorling K, Bentzen SM, Brincker H, Christensen BE, Pedersen M. Phase III trial of cyclophosphamide, doxorubicin, vincristine and prednisone (CHOP) versus cisplatin, etoposide, bleomycin and prednisone (CisEBP) for the treatment of advanced non-Hodgkin's lymphoma of high grade malignancy. The Danish Lymphoma Study Group. Acta Oncologica 1990;29(8):995-9.
Ben-Shahar 1998 {published data only}
  • Ben-Shahar M, Gepstein R, Haim R, Polliack A. Phase III trial of a combination of chlorambucil (L) and prednisone (P) with or without mitoxantrone (M) in advanced low grade non-Hodgkin's lymphoma (NHL) and CLL. Proceedings of the American Society of Clinical Oncology (Annual Meeting of the American Society of Clinical Oncology). Los Angeles, CA: Annual Meeting of the American Society of Clinical Oncology, 1998; Vol. 17:20a Abstract No 75.
Bonadonna 1975 {published data only}
  • Bonadonna G, De Lena M, Lattuada A, Milani F, Monfardini S, Beretta G. Combination chemotherapy and radiotherapy in non-Hodgkin's lymphomata. The British Journal Cancer. Supplement 1975;2:481-8.
Cabanillas 1978 {published data only}
Coiffier 1999 {published data only}
  • Coiffier B, Neidhardt-Berard EM, Tilly H, Belanger C, Bouabdallah R, Haioun C, et al. Fludarabine alone compared to CHVP plus interferon in elderly patients with follicular lymphoma and adverse prognostic parameters: a GELA study. Groupe d'Etudes des Lymphomes de l'Adulte. Annals of Oncology 1999;10(10):1191-7.
Engelhard 1986 {published data only}
  • Engelhard M, Bartels H, Binder T, Fulle HH, Gunzer U, Havemann K, et al. Multicenter randomized trial of the polychemotherapy of advanced centrocytic lymphoma: no prognostic advantage by anthracycline. Blut 1986;53(3):220.
Flinn 2012 {published data only}
  • Flinn EW, Van der Jagt RH, Kahl BS, Wood P, Hawkins TE, MacDonald D, et al. An open-label, randomized study of bendamustine and rituximab (BR) compared with rituximab, cyclophosphamide, vincristine, and prednisone (R-CVP) or rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisone (R-CHOP) in first-line treatment of patients with advanced indolent non-Hodgkin’s lymphoma (NHL) or mantle cell lymphoma (MCL): The BRIGHT Study. Blood (ASH Annual Meeting Abstracts) 2012;120(21):Abstract No 902.
Gad 1976 {published data only}
  • Gad EMN. Chemotherapeutic management of non Hodgkin's lymphoma: comparative study of various combinations. Chemotherapy - Proceedings of the 9th International Congress of Chemotherapy. New York: Plenum press, 1976; Vol. 2:581-3.
Gams 1985 {published data only}
  • Gams RA, Rainey M, Dandy M, Bartolucci AA, Silberman H, Omura G. Phase III study of BCOP v CHOP in unfavorable categories of malignant lymphoma: a Southeastern Cancer Study Group trial. Journal of Clinical Oncology 1985;3(9):1188-95.
Gisselbrecht 1987 {published data only}
  • Gisselbrecht C, Lepage E, Sebban C, Coiffier B. Low-grade non-Hodgkin's lymphoma in the adult: new therapeutic approaches [Lymphome non hodgkinien de l'adulte de faible evolutivite: nouvelles approches therapeutiques]. Nouvelle Revue Francaise d'Hematologie 1987;29(1):77-81.
Ha 2005 {published data only}
  • Ha CS, Cabanillas F, Lee MS, Tucker SL, McLaughlin P, Rodriguez MA, et al. A prospective randomized study to compare the molecular response rates between central lymphatic irradiation and intensive alternating triple chemotherapy in the treatment of stage I-III follicular lymphoma. International Journal of Radiation Oncology, Biology, Physics 2005;63(1):188-93.
Hainsworth 2005 {published data only}
  • Hainsworth JD, Litchy S, Morrissey LH, Andrews MB, Grimaldi M, McCarty M, et al. Rituximab plus short-duration chemotherapy as first-line treatment for follicular non-Hodgkin's lymphoma: a phase II trial of the Minnie Pearl Cancer Research Network. Journal of Clinical Oncology 2005;23(7):1500-6.
Hiddemann 1994 {published data only}
  • Hiddemann W, Unterhalt M, Koch P, Nahler M, Herrmann R. New aspects in the treatment of advanced low-grade non-Hodgkin's lymphomas: prednimustine/mitoxantrone versus cyclophosphamide/vincristine/prednisone followed by interferon alfa versus observation only - a preliminary update of the German Low-Grade Lymphoma Study Group. Seminars in Hematology 1994;31 Suppl 3(2):32-5.
Hiddemann 1998 {published data only}
  • Hiddemann W, Unterhalt M, Herrmann R, Woltjen HH, Kreuser ED, Trumper L, et al. Mantle-cell lymphomas have more widespread disease and a slower response to chemotherapy compared with follicle-center lymphomas: results of a prospective comparative analysis of the German Low-Grade Lymphoma Study Group. Journal of Clinical Oncology 1998;16(5):1922-30.
Inoue 1993 {published data only}
  • Inoue T, Fujiyama Y, Kitoh K, Niwakawa M, Andoh A, Hodohara K, et al. Effect of combination chemotherapy for elderly patients with malignant lymphoma. Nippon Ronen Igakkai Zasshi 1993;30(10):864-8.
Jones 1979 {published data only}
Junmin 2005 {published data only}
  • Junmin L. Fludarabine-based regimens in the treatment of indolent non-Hodgkin’s lymphoma patients: a clinical study of the Fludarabine Cooperation Group in 16 hospitals in Eastern China. Blood (ASH Annual Meeting Abstracts) 2005;106:Abstract No 4753.
Meerwaldt 1991 {published data only}
  • Meerwaldt JH, Carde P, Burgers JM, Monconduit M, Thomas J, Somers R, et al. Low-dose total body irradiation versus combination chemotherapy for lymphomas with follicular growth pattern. International Journal of Radiation Oncology, Biology, Physics 1991;21(5):1167-72.
Meusers 1989 {published data only}
Mukherji 2009 {published and unpublished data}
Niitsu 1997 {published data only}
  • Niitsu N, Umeda M. Prognostic factors of follicular lymphoma treated with combination chemotherapy. Rinsho Ketsueki [The Japanese Journal of Clinical Hematology] 1997;38(6):496-504.
Parlier 1981 {published data only}
  • Parlier Y, Gorin NC, Stachowiak J, Najman A, Duhamel G. Adriamycin for the treatment of non Hodgkin's lymphomas [Interet de l'adriamycine dans le traitement des lymphomes non Hodgkiniens]. La Seminae de Hospitaux 1981;57(41-42):1685-90.
Parlier 1982 {published data only}
  • Parlier Y, Gorin NC, Najman A, Stachowiak J, Duhamel G. Combination chemotherapy with cyclophosphamide, vincristine, prednisone and the contribution of adriamycin in the treatment of adult non-Hodgkin's lymphomas a report of 131 cases. Cancer 1982;50(3):401-9.
Peterson 1985 {published and unpublished data}
  • Peterson BA, Anderson JR, Frizzera G, Bloomfield CD, Gottlieb AJ, Holland JF. Nodular mixed lymphoma (NML): a comparative trial of cyclophosphamide adriamycin vincristine prednisone and bleomycin (CAVPB). Blood 1985;5 Suppl 1:216a.
Pettengell 2009 {published data only}
  • Pettengell R, Narayanan G, Mendoza FH, Digumarti R, Gomez H, Cernohous P, et al. Randomized phase III trial of pixantrone compared with other chemotherapeutic agents for third-line single-agent treatment of relapsed aggressive non-Hodgkin's lymphoma. Journal of Clinical Oncology (ASCO Annual Meeting) 2009;27(15s):Abstract No 8523.
Pott 1994 {published data only}
  • Pott C, Unterhalt M, Sandford D, Markert H, Freund M, Engert A, et al. Fludarabine as single agent and in combination with mitoxantrone and dexamethasone in relapsed and refractory low-grade non-Hodgkin-lymphoma. Annals of Hematology 1994;68 Suppl 1:A2.
Prentice 1996 {published data only}
  • Prentice AG, Johnson SAN, Harper M, Hewins P, Tyrrell CJ, Copplestone JA, et al. A randomised, prospective trial of chlorambucil and prednisolone (CP) v mitozantrone, chlorambucil and prednisolone (MCP) in de novo, stage II or more advanced, low-grade non-Hodgkins lymphoma (LG-NHL). British Journal of Haematology (Annual Meeting of the British Society for Haematology) 1996;93 Suppl 1:74 Abstract No 286.
Robak 2000 {published data only}
  • Robak T, Gora-Tybor J, Chojnowski K. Cladribine as monotherapy or combined with dexamethasone and idarubicin or mitoxantrone in previously treated patients with low-grade lymphoid malignancies. Haematologica 2000;85(2):215-6.
Rummel 2008 {published and unpublished data}
Rummel 2009 {published and unpublished data}
  • Rummel MJ, von Gruenhagen U, Niederle N, Ballo H, Weidmann E, Welslau M, et al. Bendamustine plus rituximab versus CHOP plus rituximab in the first-Line-treatment of patients with follicular, indolent and mantle cell lymphomas: results of a randomized phase III study of the Study Group Indolent Lymphomas (StiL). Blood (ASH Annual Meeting Abstracts) 2008;112:Abstract No 2596.
Rummel 2013 {published and unpublished data}
  • Rummel MJ, Niederle N, Maschmeyer G, Banat GA, von Grünhagen U, Losem C, et al. Bendamustine plus rituximab versus CHOP plus rituximab as first-line treatment for patients with indolent and mantle-cell lymphomas: an open-label, multicentre,randomised, phase 3 non-inferiority trial. Lancet 2013;381:1203-10.
Santini 2001 {published data only}
  • Santini G, Nati S, Spriano M, Gallamini A, Pierluigi D, Congiu AM, et al. Fludarabine in combination with cyclophosphamide or with cyclophosphamide plus mitoxantrone for relapsed or refractory low-grade non-Hodgkin's lymphoma. Haematologica 2001;86(3):282-6.
Santoro 2006 {published data only}
  • Santoro A, Voglova J, Gabrail N, Ciuleanu T, Liberati M, Hancock BW, et al. Comparative trial of BBR 2778 (pixantrone) + rituximab vs single agent rituximab in the treatment of relapsed/refractory indolent non-Hodgkin's lymphoma (NHL). Journal of Clinical Oncology (ASCO Annual Meeting Proceedings) 2006;24 Suppl(18):Abstract No 7578.
Somers 1987 {published data only}
Unterhalt 1994 {published data only}
  • Unterhalt M, Koch P, Pfreundschuh M, Maschmeyer G, Freund M, Thiel F, et al. Prednimustine, mitoxantrone (PMM) versus cyclophosphamide, vincristine, prednisone (COP) for the treatment of advanced low grade non-Hodgkin's lymphoma. Blood 1994;84 Suppl 1:Abstract No 656.
Yahalom 1993 {published data only}
  • Yahalom J, Varsos G, Fuks Z, Myers J, Clarkson BD, Straus DJ. Adjuvant cyclophosphamide, doxorubicin, vincristine, and prednisone chemotherapy after radiation therapy in stage I low-grade and intermediate-grade non-Hodgkin lymphoma. Results of a prospective randomized study. Cancer 1993;71(7):2342-50.
Young 1977 {published data only}
  • Young RC, Johnson RE, Canellos GP, Chabner BA, Brereton HD, Berard CW, et al. Advanced lymphocytic lymphoma: randomized comparisons of chemotherapy and radiotherapy, alone or in combination. Cancer Treatment Reports 1977;61(6):1153-9.

References to ongoing studies

  1. References to studies included in this review
  2. References to studies excluded from this review
  3. References to ongoing studies
  4. Additional references
NCT00551239 {published and unpublished data}
  • NCT00551239. Fludarabine and rituximab with or without pixantrone in treating patients with relapsed or refractory indolent non-Hodgkin lymphoma. (accessed 17 April 2013).
NCT00801281 {published and unpublished data}
  • NCT00801281. First-line R-CVP vs R-CHOP induction immunochemotherapy for indolent lymphoma and R maintenance (PLRG4). (accessed 17 April 2013).

Additional references

  1. References to studies included in this review
  2. References to studies excluded from this review
  3. References to ongoing studies
  4. Additional references
Bartlett 1994
  • Bartlett NL, Rizeq M, Dorfman RF, Halpern J, Horning SJ. Follicular large-cell lymphoma: intermediate or low grade?. Journal of Clinical Oncology 1994;12(7):1349-57.
Bendandi 2008
Billingham 1978
  • Billingham ME, Mason JW, Bristow MR, Daniels JR. Anthracycline cardiomyopathy monitored by morphologic changes. Cancer Treatments Reports 1978;62(6):865-72.
Brandt 2001
Buske 2008
Chau 2003
  • Chau I, Jones R, Cunningham D, Wotherspoon A, Maisey N, Norman AR, et al. Outcome of follicular lymphoma grade 3: is anthracycline necessary as front-line therapy?. British Journal of Cancer 2003;89(1):36-42.
Cheson 1999
  • 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. Journal of Clinical Oncology 1999;17(4):1244.
Cheson 2007
Dana 1993
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Federico 2000
  • Federico M, Vitolo U, Zinzani PL, Chisesi T, Clo V, Bellesi G, et al. Prognosis of follicular lymphoma: a predictive model based on a retrospective analysis of 987 cases. Intergruppo Italiano Linfomi. Blood 2000;95(3):783-9.
Federico 2009
  • Federico M, Bellei M, Marcheselli L, Luminari S, Lopez-Guillermo A, Vitolo U, et al. Follicular Lymphoma International Prognostic Index 2: a new prognostic index for follicular lymphoma developed by the international follicular lymphoma prognostic factor project. Journal of Clinical Oncology 2009;27(27):4555-62.
Friedberg 2009
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Ganti 2006
  • Ganti AK, Weisenburger DD, Smith LM, Hans CP, Bociek RG, Bierman PJ, et al. Patients with grade 3 follicular lymphoma have prolonged relapse-free survival following anthracycline-based chemotherapy: the Nebraska Lymphoma Study Group Experience. Annals of Oncology 2006;17(6):920-7.
Goodman 2006
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Lister 1978
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Liu 2006
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Mann 1983
Miller 1981
Montoto 2007
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Morton 2006
Nabhan 2007
NHLCP 1997
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Schulz 2007
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Solal-Celigny 1993
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Solal-Celigny 2004
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Tierney 2007
Tilly 2008
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Williamson 2002
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Zinzani 2004
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