Current therapeutic strategies and new treatment paradigms for follicular lymphoma

Cancer Treatment and Research

Volumn 165, Issue , 2015, Pages 197-226

  Kritharis, Athena ^a   Sharma, Jaya ^a   Evens, Andrew M ^a  

^a TUFTS MEDICAL CENTER   (United States)

Author keywords

Antibody; Cancer; Follicular; Non hodgkin lymphoma; Rituximab; Treatment

Indexed keywords

BENDAMUSTINE; BORTEZOMIB; CD20 ANTIBODY; CD22 ANTIGEN; CHLORAMBUCIL; CYCLOPHOSPHAMIDE; DOXORUBICIN; ETOPOSIDE; FLUDARABINE; GEMCITABINE; HISTONE DEACETYLASE INHIBITOR; IBRITUMOMAB TIUXETAN; IDELALISIB; IMMUNOMODULATING AGENT; INOTUZUMAB OZOGAMICIN; INTERFERON; LENALIDOMIDE; MITOXANTRONE; MONOCLONAL ANTIBODY; OBINUTUZUMAB; OFATUMUMAB; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PREDNISONE; PROTEASOME INHIBITOR; RITUXIMAB; TEMSIROLIMUS; TOSITUMOMAB I 131; UNINDEXED DRUG; VELTUZUMAB; VINCRISTINE; ANTINEOPLASTIC AGENT; IMMUNOLOGIC FACTOR;

ADVANCED CANCER; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CANCER CLASSIFICATION; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER MORTALITY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER STAGING; CHRONIC LYMPHATIC LEUKEMIA; COMPARATIVE EFFECTIVENESS; DIARRHEA; DRUG CONTRAINDICATION; DRUG CYTOTOXICITY; DRUG PROTEIN BINDING; DRUG TOLERABILITY; EVENT FREE SURVIVAL; FOLLICULAR LYMPHOMA; FOLLICULAR LYMPHOMA INTERNATIONAL PROGNOSTIC INDEX; GROUPE D ETUDE DES LYMPHOMES FOLLICULAIRES SCORE; HUMAN; HYPERTRANSAMINASEMIA; INFECTION; MAINTENANCE THERAPY; MANTLE CELL LYMPHOMA; MONOTHERAPY; MULTIPLE CYCLE TREATMENT; NEUROTOXICITY; NEUTROPENIA; NONHODGKIN LYMPHOMA; ONCOLOGICAL PARAMETERS; OVERALL SURVIVAL; PARESTHESIA; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PNEUMONIA; PRACTICE GUIDELINE; PROGRESSION FREE SURVIVAL; QUALITY OF LIFE; RADIATION DOSE; RANDOMIZED CONTROLLED TRIAL (TOPIC); RATING SCALE; REFRACTORY PERIOD; STOMATITIS; SYMPTOMATOLOGY; THROMBOCYTOPENIA; TRANSPLANT RELATED MORTALITY; TREATMENT DURATION; TREATMENT FAILURE; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR VOLUME; UNSPECIFIED SIDE EFFECT; WATCHFUL WAITING; AUTOTRANSPLANTATION; IMMUNOTHERAPY; LYMPHOMA, FOLLICULAR; PATHOLOGY; PROCEDURES; PROGNOSIS; RADIOIMMUNOTHERAPY; STEM CELL TRANSPLANTATION;

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; HUMANS; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; LYMPHOMA, FOLLICULAR; PROGNOSIS; PROTEASOME INHIBITORS; RADIOIMMUNOTHERAPY; STEM CELL TRANSPLANTATION; TRANSPLANTATION, AUTOLOGOUS;

EID: 84922348765     PISSN: 09273042     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-3-319-13150-4_8     Document Type: Article

References (91)

1. Chan WC, Armitage JO, Gascoyne R et al (1997) A clinical evaluation of the international lymphoma study group classification of non-Hodgkin’s lymphoma. The non-Hodgkin’s lymphoma classification project. Blood 89(11):3909–3918
2. Morton LM, Wang SS, Devesa SS, Hartge P, Weisenburger DD, Linet MS (2006) Lymphoma incidence patterns by WHO subtype in the United States, 1992–2001. Blood 107(1):265–276
3. Link BK, Maurer MJ, Nowakowski GS et al (2013) Rates and outcomes of follicular lymphoma transformation in the immunochemotherapy era: a report from the University of Iowa/MayoClinic specialized program of research excellence molecular epidemiology resource. J Clin Oncol 31(26):3272–3278
4. Tan D, Horning SJ, Hoppe RT et al (2013) Improvements in observed and relative survival in follicular grade 1-2 lymphoma during 4 decades: the Stanford University experience. Blood 122(6):981–987
5. Nabhan C, Aschebrook-Kilfoy B, Chiu BC, Kruczek K, Smith SM, Evens AM (2014) The impact of race, age, and sex in follicular lymphoma: a comprehensive SEER analysis across consecutive treatment eras. Am J Hematol 89(6):633–638
6. Federico M, Luminari S, Dondi A et al (2013) 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. J Clin Oncol 31(12):1506–1513
7. Brice P, Bastion Y, Lepage E et al (1997) Comparison in low-tumor-burden follicular lymphomas between an initial no-treatment policy, prednimustine, or interferon alfa: a randomized study from the Groupe d’Etude des Lymphomes Folliculaires. Groupe d’Etude des Lymphomes de l’Adulte. J Clin Oncol 15(3):1110–1117
8. Solal-Celigny P, Lepage E, Brousse N et al (1998) Doxorubicin-containing regimen with or without interferon alfa-2b for advanced follicular lymphomas: final analysis of survival and toxicity in the Groupe d’Etude des Lymphomes Folliculaires 86 Trial. J Clin Oncol 16 (7):2332–2338
9. Ardeshna KM, Qian W, Smith P et al (2014) Rituximab versus a watch-and-wait approach in patients with advanced-stage, asymptomatic, non-bulky follicular lymphoma: an open-label randomised phase 3 trial. Lancet Oncol 15(4):424–435
10. Ardeshna KM, Smith P, Norton A et al (2003) Long-term effect of a watch and wait policy versus immediate systemic treatment for asymptomatic advanced-stage non-Hodgkin lymphoma: a randomised controlled trial. Lancet 362(9383):516–522
11. Buske C, Hoster E, Dreyling M, Hasford J, Unterhalt M, Hiddemann W (2006) The follicular lymphoma international prognostic index (FLIPI) separates high-risk from intermediate- or low-risk patients with advanced-stage follicular lymphoma treated front-line with rituximab and the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (R-CHOP) with respect to treatment outcome. Blood 108(5):1504–1508
12. Colombat P, Salles G, Brousse N et al (2001) 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 97(1):101–106
13. Hiddemann W, Kneba M, Dreyling M et al (2005) 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 106(12):3725–3732
14. Romaguera JE, McLaughlin P, North L et al (1991) Multivariate analysis of prognostic factors in stage IV follicular low-grade lymphoma: a risk model. J Clin Oncol 9(5):762–769
15. Salles G, Mounier N, de Guibert S et al (2008) Rituximab combined with chemotherapy and interferon in follicular lymphoma patients: results of the GELA-GOELAMS FL2000 study. Blood 112(13):4824–4831
16. Salles G, Seymour JF, Offner F 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):42–51
17. Herold M, Haas A, Srock S et al (2007) 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 25(15):1986–1992
18. Kahl BS (2006) Eastern Cooperative Oncology Group 4402: rituximab extended schedule or retreatment trial (RESORT). Clin Lymphoma Myeloma. 6(5):423–426
19. Solal-Celigny P, Roy P, Colombat P et al (2004) Follicular lymphoma international prognostic index. Blood 104(5):1258–1265
20. Plancarte F, Lopez-Guillermo A, Arenillas L et al (2006) Follicular lymphoma in early stages: high risk of relapse and usefulness of the follicular lymphoma international prognostic index to predict the outcome of patients. Eur J Haematol 76(1):58–63
21. Montoto S, Lopez-Guillermo A, Altes A et al (2004) Predictive value of follicular lymphoma international prognostic index (FLIPI) in patients with follicular lymphoma at first progression. Ann Oncol 15(10):1484–1489
22. Friedberg JW, Taylor MD, Cerhan JR et al (2009) Follicular lymphoma in the United States: first report of the national LymphoCare study. J Clin Oncol 27(8):1202–1208
23. Mac Manus MP, Hoppe RT (1996) Is radiotherapy curative for stage I and II low-grade follicular lymphoma? Results of a long-term follow-up study of patients treated at Stanford University. J Clin Oncol 14(4):1282–1290
24. Tsang RW, Gospodarowicz MK (2005) Radiation therapy for localized low-grade non-Hodgkin’s lymphomas. Hematol Oncol 23(1):10–17
25. Seymour JF, Pro B, Fuller LM et al (2003) Long-term follow-up of a prospective study of combined modality therapy for stage I-II indolent non-Hodgkin’s lymphoma. J Clin Oncol 21 (11):2115–2122
26. Advani R, Rosenberg SA, Horning SJ (2004) Stage I and II follicular non-Hodgkin’s lymphoma: long-term follow-up of no initial therapy. J Clin Oncol 22(8):1454–1459
27. Solal-Celigny P, Bellei M, Marcheselli L et al (2012) Watchful waiting in low-tumor burden follicular lymphoma in the rituximab era: results of an F2-study database. J Clin Oncol 30 (31):3848–3853
28. Li ZM, Ghielmini M, Moccia AA (2013) Managing newly diagnosed follicular lymphoma: state of the art and future perspectives. Expert Rev Anticancer Ther 13(3):313–325
29. Forstpointner R, Dreyling M, Repp R et al (2004) 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 104(10):3064–3071
30. Foussard C, Colombat P, Maisonneuve H et al (2005) 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 16(3):466–472
31. Hochster H, Weller E, Gascoyne RD et al (2009) Maintenance rituximab after cyclophosphamide, vincristine, and prednisone prolongs progression-free survival in advanced indolent lymphoma: results of the randomized phase III ECOG1496 study. J Clin Oncol 27(10):1607–1614
32. Marcus R, Imrie K, Belch A et al (2005) CVP chemotherapy plus rituximab compared with CVP as first-line treatment for advanced follicular lymphoma. Blood 105(4):1417–1423
33. Rummel MJ, Al-Batran SE, Kim SZ et al (2005) Bendamustine plus rituximab is effective and has a favorable toxicity profile in the treatment of mantle cell and low-grade non-Hodgkin’s lymphoma. J Clin Oncol 23(15):3383–3389
34. Rummel MJ, Niederle N, Maschmeyer G et al (2013) 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 381 (9873):1203–1210
35. Flinn IW, van der Jagt R, Kahl BS et al (2014) Randomized trial of bendamustine-rituximab or R-CHOP/R-CVP in first-line treatment of indolent NHL or MCL: the BRIGHT study. Blood 123(19):2944–2952
36. Baum E, Sather H, Nachman J et al (1979) Relapse rates following cessation of chemotherapy during complete remission of acute lymphocytic leukemia. Med Pediatr Oncol 7(1):25–34
37. Jacobson CA, Freedman AS (2013) One size does not fit all in follicular lymphoma. J Clin Oncol 31(27):3307–3308
38. Kaminski MS, Tuck M, Estes J et al (2005) 131I-tositumomab therapy as initial treatment for follicular lymphoma. N Engl J Med 52(5):441–449
39. Oliansky DM, Gordon LI, King J et al (2010) The role of cytotoxic therapy with hematopoietic stem cell transplantation in the treatment of follicular lymphoma: an evidence-based review. Biol Blood Marrow Transplant 16(4):443–468
40. Schaaf M, Reiser M, Borchmann P, Engert A, Skoetz N (2012) High-dose therapy with autologous stem cell transplantation versus chemotherapy or immuno-chemotherapy for follicular lymphoma in adults. Cochrane Database Syst Rev 1:CD007678
41. Cheson BD, Leonard JP (2008) Monoclonal antibody therapy for B-cell non-Hodgkin’s lymphoma. N Engl J Med 359(6):613–626
42. Davis TA, Grillo-Lopez AJ, White CA et al (2000) Rituximab anti-CD20 monoclonal antibody therapy in non-Hodgkin’s lymphoma: safety and efficacy of re-treatment. J Clin Oncol 18(17):3135–3143
43. Friedberg JW, Cohen P, Chen L et al (2008) Bendamustine in patients with rituximab-refractory indolent and transformed non-Hodgkin’s lymphoma: results from a phase II multicenter, single-agent study. J Clin Oncol 26(2):204–210
44. Sacchi S, Pozzi S, Marcheselli R et al (2007) Rituximab in combination with fludarabine and cyclophosphamide in the treatment of patients with recurrent follicular lymphoma. Cancer 110 (1):121–128
45. Tam CS, Wolf M, Prince HM et al (2006) Fludarabine, cyclophosphamide, and rituximab for the treatment of patients with chronic lymphocytic leukemia or indolent non-Hodgkin lymphoma. Cancer 106(11):2412–2420
46. Al-Tourah AJ, Gill KK, Chhanabhai M et al (2008) Population-based analysis of incidence and outcome of transformed non-Hodgkin’s lymphoma. J Clin Oncol 26(32):5165–5169
47. Carney DA, Westerman DA, Tam CS et al (2010) Therapy-related myelodysplastic syndrome and acute myeloid leukemia following fludarabine combination chemotherapy. Leukemia 24 (12):2056–2062
48. Waterman J, Rybicki L, Bolwell B et al (2012) Fludarabine as a risk factor for poor stem cell harvest, treatment-related MDS and AML in follicular lymphoma patients after autologous hematopoietic cell transplantation. Bone Marrow Transplant 47(4):488–493
49. Janikova A, Koristek Z, Vinklarkova J et al (2009) Efficacious but insidious: a retrospective analysis of fludarabine-induced myelotoxicity using long-term culture-initiating cells in 100 follicular lymphoma patients. Exp Hematol 37(11):1266–1273
50. Lanza F, Lemoli RM, Olivieri A et al (2014) Factors affecting successful mobilization with plerixafor: an Italian prospective survey in 215 patients with multiple myeloma and lymphoma. Transfusion. 54(2):331–339
51. Wiseman GA, Gordon LI, Multani PS et al (2002) Ibritumomab tiuxetan radioimmunotherapy for patients with relapsed or refractory non-Hodgkin lymphoma and mild thrombocytopenia: a phase II multicenter trial. Blood 99(12):4336–4342
52. Fisher RI, Kaminski MS, Wahl RL et al (2005) 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 23(30):7565–7573
53. Derenzini E, Stefoni V, Maglie R et al (2013) Collection of hematopoietic stem cells after previous radioimmunotherapy is feasible and does not impair engraftment after autologous stem cell transplantation in follicular lymphoma. Biol Blood Marrow Transplant 19(12):1695–1701
54. Czuczman MS, Emmanouilides C, Darif M et al (2007) Treatment-related myelodysplastic syndrome and acute myelogenous leukemia in patients treated with ibritumomab tiuxetan radioimmunotherapy. J Clin Oncol 25(27):4285–4292
55. Chan EK, Fung S, Gospodarowicz M et al (2011) Palliation by low-dose local radiation therapy for indolent non-Hodgkin lymphoma. Int J Radiat Oncol Biol Phys 81(5):e781–786
56. Montoto S, Corradini P, Dreyling M et al (2013) Indications for hematopoietic stem cell transplantation in patients with follicular lymphoma: a consensus project of the EBMT-lymphoma working party. Haematologica 98(7):1014–1021
57. Oliansky DM, Gordon LI, King J et al (2010) The role of cytotoxic therapy with hematopoietic stem cell transplantation in the treatment of follicular lymphoma: an evidence-based review. Biol Blood Marrow Transplant 16(4):443–468
58. Rohatiner AZ, Nadler L, Davies AJ et al (2007) Myeloablative therapy with autologous bone marrow transplantation for follicular lymphoma at the time of second or subsequent remission: long-term follow-up. J Clin Oncol 25(18):2554–2559
59. Evens AM, Vanderplas A, LaCasce AS et al (2013) Stem cell transplantation for follicular lymphoma relapsed/refractory after prior rituximab: a comprehensive analysis from the NCCN lymphoma outcomes project. Cancer 119(20):3662–3671
60. Khouri IF, McLaughlin P, Saliba RM et al (2008) Eight-year experience with allogeneic stem cell transplantation for relapsed follicular lymphoma after nonmyeloablative conditioning with fludarabine, cyclophosphamide, and rituximab. Blood 111(12):5530–5536
61. Morschhauser FA, Cartron G, Thieblemont C et al (2013) Obinutuzumab (GA101) monotherapy in relapsed/refractory diffuse large b-cell lymphoma or mantle-cell lymphoma: results from the phase II GAUGUIN study. J Clin Oncol 31(23):2912–2919
62. Radford J, Davies A, Cartron G, et al (2013) Obinutuzumab (GA101) plus CHOP or FC in relapsed/refractory follicular lymphoma: results of the GAUDI study (BO21000). Blood 122 (7):1137–1143
63. Advani A, Coiffier B, Czuczman MS et al (2010) Safety, pharmacokinetics, and preliminary clinical activity of inotuzumab ozogamicin, a novel immunoconjugate for the treatment of B-cell non-Hodgkin’s lymphoma: results of a phase I study. J Clin Oncol 28(12):2085–2093
64. Negrea GO, Elstrom R, Allen SL et al (2011) Subcutaneous injections of low-dose veltuzumab (humanized anti-CD20 antibody) are safe and active in patients with indolent non-Hodgkin’s lymphoma. Haematologica 96(4):567–573
65. Genovese MC, Kaine JL, Lowenstein MB et al (2008) Ocrelizumab, a humanized anti-CD20 monoclonal antibody, in the treatment of patients with rheumatoid arthritis: a phase I/II randomized, blinded, placebo-controlled, dose-ranging study. Arthritis Rheum 58(9):2652– 2661
66. Morschhauser F, Marlton P, Vitolo U et al (2010) Results of a phase I/II study of ocrelizumab, a fully humanized anti-CD20 mAb, in patients with relapsed/refractory follicular lymphoma. Ann Oncol 21(9):1870–1876
67. Casulo C, Vose JM, Ho WY et al (2014) A phase I study of PRO131921, a novel anti-CD20 monoclonal antibody in patients with relapsed/refractory CD20 + indolent NHL: correlation between clinical responses and AUC pharmacokinetics. Clin Immunol 154(1):37–46
68. Leonard JP, Schuster SJ, Emmanouilides C et al (2008) Durable complete responses from therapy with combined epratuzumab and rituximab: final results from an international multicenter, phase 2 study in recurrent, indolent, non-Hodgkin lymphoma. Cancer 113 (10):2714–2723
69. Younes A, Kim S, Romaguera J et al (2012) Phase I multidose-escalation study of the anti-CD19 maytansinoid immunoconjugate SAR3419 administered by intravenous infusion every 3 weeks to patients with relapsed/refractory B-cell lymphoma. J Clin Oncol 30(22):2776–2782
70. Fayad L, Offner F, Smith MR et al (2013) Safety and clinical activity of a combination therapy comprising two antibody-based targeting agents for the treatment of non-Hodgkin lymphoma: results of a phase I/II study evaluating the immunoconjugate inotuzumab ozogamicin with rituximab. J Clin Oncol 31(5):573–583
71. Flinn IW, Kahl BS, Leonard JP et al (2014) Idelalisib, a selective inhibitor of phosphatidylinositol 3-kinase-delta, as therapy for previously treated indolent non-Hodgkin lymphoma. Blood 123(22):3406–3413
72. Gopal AK, Kahl BS, de Vos S et al (2014) PI3Kdelta inhibition by idelalisib in patients with relapsed indolent lymphoma. N Engl J Med 370(11):1008-1018
73. Wang M, Fowler N, Wagner-Bartak N et al (2013) Oral lenalidomide with rituximab in relapsed or refractory diffuse large cell, follicular and transformed lymphoma: a phase II clinical trial. Leukemia 27(9):1902–1909
74. Friedberg JW, Vose JM, Kelly JL et al (2011) The combination of bendamustine, bortezomib, and rituximab for patients with relapsed/refractory indolent and mantle cell non-Hodgkin lymphoma. Blood 117(10):2807–2812
75. Coiffier B, Li W, Henitz ED et al (2013) Prespecified candidate biomarkers identify follicular lymphoma patients who achieved longer progression-free survival with bortezomib-rituximab versus rituximab. Clin Cancer Res 19(9):2551–2561
76. Zinzani PL, Khuageva NK, Wang H et al (2012) Bortezomib plus rituximab versus rituximab in patients with high-risk, relapsed, rituximab-naive or rituximab-sensitive follicular lymphoma: subgroup analysis of a randomized phase 3 trial. J Hematol Oncol 5:67
77. Ramsay AG, Clear AJ, Kelly G et al (2009) Follicular lymphoma cells induce T-cell immunologic synapse dysfunction that can be repaired with lenalidomide: implications for the tumor microenvironment and immunotherapy. Blood 114(21):4713–4720
78. Fowler NH, Davis RE, Rawal S et al (2014) Safety and activity of lenalidomide and rituximab in untreated indolent lymphoma: an open-label, phase 2 trial. Lancet Oncol 15(12):1311–1318
79. Evens AM, Smith MR, Lossos IS et al (2014) Frontline bortezomib and rituximab for the treatment of newly diagnosed high tumour burden indolent non-Hodgkin lymphoma: a multicentre phase II study. Br J Haematol 166(4):514–520
80. Witzig TE, Wiernik PH, Moore T et al (2009) Lenalidomide oral monotherapy produces durable responses in relapsed or refractory indolent non-Hodgkin’s lymphoma. J Clin Oncol 27(32):5404–5409
81. Kirschbaum M, Frankel P, Popplewell L et al (2011) Phase II study of vorinostat for treatment of relapsed or refractory indolent non-Hodgkin’s lymphoma and mantle cell lymphoma. J Clin Oncol 29(9):1198–1203
82. Smith SM, van Besien K, Karrison T et al (2010) Temsirolimus has activity in non-mantle cell non-Hodgkin’s lymphoma subtypes: the University of Chicago phase II consortium. J Clin Oncol 28(31):4740–4746
83. Westin JR, Chu F, Zhang M et al (2014) Safety and activity of PD1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: a single group, open-label, phase 2 trial. Lancet Oncol 15(1):69–77
84. van Oers MH, Klasa R, Marcus RE et al (2006) 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 108(10):3295–3301
85. Horning SJ, Negrin RS, Hoppe RT et al (2001) High-dose therapy and autologous bone marrow transplantation for follicular lymphoma in first complete or partial remission: results of a phase II clinical trial. Blood 97(2):404–409
86. Lenz G, Dreyling M, Schiegnitz E et al (2004) Myeloablative radiochemotherapy followed by autologous stem cell transplantation in first remission prolongs progression-free survival in follicular lymphoma: results of a prospective, randomized trial of the German Low-Grade Lymphoma Study Group. Blood 104(9):2667–2674
87. Lenz G, Dreyling M, Schiegnitz E et al (2004) Moderate increase of secondary hematologic malignancies after myeloablative radiochemotherapy and autologous stem-cell transplantation in patients with indolent lymphoma: results of a prospective randomized trial of the German Low Grade Lymphoma Study Group. J Clin Oncol 22(24):4926–4933
88. Sebban C, Mounier N, Brousse N et al (2006) Standard chemotherapy with interferon compared with CHOP followed by high-dose therapy with autologous stem cell transplantation in untreated patients with advanced follicular lymphoma: the GELF-94 randomized study from the Groupe d’Etude des Lymphomes de l’Adulte (GELA). Blood 108 (8):2540–2544
89. Ladetto M, De Marco F, Benedetti F et al (2008) Prospective, multicenter randomized GITMO/IIL trial comparing intensive (R-HDS) versus conventional (CHOP-R) chemoimmunotherapy in high-risk follicular lymphoma at diagnosis: the superior disease control of R-HDS does not translate into an overall survival advantage. Blood 111(8):4004– 4013
90. Gyan E, Foussard C, Bertrand P et al (2009) High-dose therapy followed by autologous purged stem cell transplantation and doxorubicin-based chemotherapy in patients with advanced follicular lymphoma: a randomized multicenter study by the GOELAMS with final results after a median follow-up of 9 years. Blood 113(5):995–1001
91. Federico M et al (2009) Follicular lymphoma international prognostic index 2: a new prognostic index for follicular lymphoma developed by the international follicular lymphoma prognostic factor project. J Clin Oncol 27:1–9