A Phase II study of a nonmyeloablative allogeneic stem cell transplant with peritransplant rituximab in patients with BCell lymphoid malignancies: Favorably durable event-free survival in chemosensitive patients

Biology of Blood and Marrow Transplantation

Volumn 20, Issue 3, 2014, Pages 354-360

  Sauter, Craig S ^a,b   Barker, Juliet N ^a,b   Lechner, Lauren ^a   Zheng, Junting ^a   Devlin, Sean M ^a   Papadopoulos, Esperanza B ^a,b   Perales, Miguel Angel ^a,b   Jakubowski, Ann A ^a,b   Goldberg, Jenna D ^a,b   Koehne, Guenther ^a,b   Ceberio, Izaskun ^a,c   Giralt, Sergio ^a,b   Zelenetz, Andrew D ^a,b   Moskowitz, Craig H ^a,b   Castro Malaspina, Hugo ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c Universidad Pública de Navarra   (Spain)

Author keywords

Allogeneic stem cell transplant; Non Hodgkin lymphoma; Nonmyeloablative; Rituximab

Indexed keywords

ALANINE AMINOTRANSFERASE; CYCLOPHOSPHAMIDE; CYCLOSPORIN; FLUDARABINE; GANCICLOVIR; METHOTREXATE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; RAPAMYCIN; RECOMBINANT GRANULOCYTE COLONY STIMULATING FACTOR; RITUXIMAB; TACROLIMUS; THYMOCYTE ANTIBODY; VALGANCICLOVIR;

ACUTE GRAFT VERSUS HOST DISEASE; ADULT; AGED; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ARTICLE; B CELL LYMPHOMA; BONE MARROW; CD4 LYMPHOCYTE COUNT; CHEMOSENSITIVITY; CHIMERA; CHRONIC GRAFT VERSUS HOST DISEASE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; DONOR LYMPHOCYTE INFUSION; ENGRAFTMENT; EVENT FREE SURVIVAL; FEMALE; FEVER; FOLLOW UP; HUMAN; LARGE CELL LYMPHOMA; MAJOR CLINICAL STUDY; MALE; NEUTROPENIA; NONMYELOABLATIVE CONDITIONING; NONMYELOABLATIVE STEM CELL TRANSPLANTATION; OVERALL SURVIVAL; PATIENT SAFETY; PHASE 2 CLINICAL TRIAL; PROPHYLAXIS; PROSPECTIVE STUDY; STEVENS JOHNSON SYNDROME; T LYMPHOCYTE; THROMBOCYTOPENIA; TREATMENT DURATION; UNRELATED DONORS; WHOLE BODY RADIATION;

ALLOGENEIC STEM CELL TRANSPLANT; NON-HODGKIN LYMPHOMA; NONMYELOABLATIVE; RITUXIMAB;

ADULT; AGED; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTINEOPLASTIC AGENTS; CYCLOPHOSPHAMIDE; FEMALE; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; LYMPHOMA, B-CELL; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; SURVIVAL ANALYSIS; TRANSPLANTATION CHIMERA; TRANSPLANTATION CONDITIONING; TRANSPLANTATION, HOMOLOGOUS; TREATMENT OUTCOME; UNRELATED DONORS; VIDARABINE; WHOLE-BODY IRRADIATION;

EID: 84896846970     PISSN: 10838791     EISSN: 15236536     Source Type: Journal    
DOI: 10.1016/j.bbmt.2013.11.029     Document Type: Article

References (63)

1. Fisher R.I., LeBlanc M., Press O.W., et al. New treatment options have changed the survival of patients with follicular lymphoma. JClin Oncol 2005, 23:8447-8452.
2. Keegan T.H., Moy L.M., Foran J.M., et al. Rituximab use and survival after diffuse large B-cell or follicular lymphoma: a population-based study. Leuk Lymph 2013, 54:743-751.
3. Kluin-Nelemans H.C., Hoster E., Hermine O., et al. Treatment of older patients with mantle-cell lymphoma. NEngl J Med 2012, 367:520-531.
4. Robak T., Lech-Maranda E., Robak P. Rituximab plus fludarabine and cyclophosphamide or other agents in chronic lymphocytic leukemia. Exp Rev Anticancer Ther 2010, 10:1529-1543.
5. Philip T., Guglielmi C., Hagenbeek A., et al. Autologous bone marrow transplantation as compared with salvage chemotherapy in relapses of chemotherapy-sensitive non-Hodgkin's lymphoma. NEngl J Med 1995, 333:1540-1545.
6. Gisselbrecht C., Glass B., Mounier N., et al. Salvage regimens with autologous transplantation for relapsed large B-cell lymphoma in the rituximab era. JClin Oncol 2010, 28:4184-4190.
7. Geisler C.H., Kolstad A., Laurell A., et al. Long-term progression-free survival of mantle cell lymphoma after intensive front-line immunochemotherapy with invivo-purged stem cell rescue: a nonrandomized phase 2 multicenter study by the Nordic Lymphoma Group. Blood 2008, 112:2687-2693.
8. Schaffel R., Hedvat C.V., Teruya-Feldstein J., et al. Prognostic impact of proliferative index determined by quantitative image analysis and the International Prognostic Index in patients with mantle cell lymphoma. Ann Oncol 2010, 21:133-139.
9. Schouten H.C., Qian W., Kvaloy S., et al. High-dose therapy improves progression-free survival and survival in relapsed follicular non-Hodgkin's lymphoma: results from the randomized European CUP trial. JClin Oncol 2003, 21:3918-3927.
10. Lenz G., Dreyling M., Schiegnitz E., et al. 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 2004, 104:2667-2674.
11. van Besien K., Sobocinski K.A., Rowlings P.A., et al. Allogeneic bone marrow transplantation for low-grade lymphoma. Blood 1998, 92:1832-1836.
12. Bacher U., Klyuchnikov E., Le-Rademacher J., et al. Conditioning regimens for allotransplants for diffuse large B-cell lymphoma: myeloablative or reduced intensity?. Blood 2012, 120:4256-4262.
13. Khouri I.F., Keating M., Korbling M., et al. Transplant-lite: induction of graft-versus-malignancy using fludarabine-based nonablative chemotherapy and allogeneic blood progenitor-cell transplantation as treatment for lymphoid malignancies. JClin Oncol 1998, 16:2817-2824.
14. van Besien K.W., de Lima M., Giralt S.A., et al. Management of lymphoma recurrence after allogeneic transplantation: the relevance of graft-versus-lymphoma effect. Bone Marrow Transplant 1997, 19:977-982.
15. van Kampen R.J., Canals C., Schouten H.C., et al. Allogeneic stem-cell transplantation as salvage therapy for patients with diffuse large B-cell non-Hodgkin's lymphoma relapsing after an autologous stem-cell transplantation: an analysis of the European Group for Blood and Marrow Transplantation Registry. JClin Oncol 2011, 29:1342-1348.
16. Rezvani A.R., Norasetthada L., Gooley T., et al. Non-myeloablative allogeneic haematopoietic cell transplantation for relapsed diffuse large B-cell lymphoma: a multicentre experience. Br J Haematol 2008, 143:395-403.
17. Rezvani A.R., Storer B., Maris M., et al. Nonmyeloablative allogeneic hematopoietic cell transplantation in relapsed, refractory, and transformed indolent non-Hodgkin's lymphoma. JClin Oncol 2008, 26:211-217.
18. Thomson K.J., Morris E.C., Milligan D., et al. T-cell-depleted reduced-intensity transplantation followed by donor leukocyte infusions to promote graft-versus-lymphoma activity results in excellent long-term survival in patients with multiply relapsed follicular lymphoma. JClin Oncol 2010, 28:3695-3700.
19. Khouri I.F., McLaughlin P., Saliba R.M., et al. Eight-year experience with allogeneic stem cell transplantation for relapsed follicular lymphoma after nonmyeloablative conditioning with fludarabine, cyclophosphamide, and rituximab. Blood 2008, 111:5530-5536.
20. Dreger P., Dohner H., Ritgen M., et al. Allogeneic stem cell transplantation provides durable disease control in poor-risk chronic lymphocytic leukemia: long-term clinical and MRD results of the German CLL Study Group CLL3X trial. Blood 2010, 116:2438-2447.
21. Corradini P., Dodero A., Farina L., et al. Allogeneic stem cell transplantation following reduced-intensity conditioning can induce durable clinical and molecular remissions in relapsed lymphomas: pre-transplant disease status and histotype heavily influence outcome. Leukemia 2007, 21:2316-2323.
22. Morris E., Thomson K., Craddock C., et al. Outcomes after alemtuzumab-containing reduced-intensity allogeneic transplantation regimen for relapsed and refractory non-Hodgkin lymphoma. Blood 2004, 104:3865-3871.
23. Cook G., Smith G.M., Kirkland K., et al. Outcome following reduced-intensity allogeneic stem cell transplantation (RIC AlloSCT) for relapsed and refractory mantle cell lymphoma (MCL): a study of the British Society for Blood and Marrow Transplantation. Biol Blood Marrow Transplant 2010, 16:1419-1427.
24. Cheson B.D., Horning S.J., Coiffier B., et al. Report of an international workshop to standardize response criteria for non-Hodgkin's lymphomas. NCI Sponsored International Working Group. JClin Oncol 1999, 17:1244.
25. Hallek M., Cheson B.D., Catovsky D., et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood 2008, 111:5446-5456.
26. Sorror M.L., Maris M.B., Storb R., et al. Hematopoietic cell transplantation (HCT)-specific comorbidity index: a new tool for risk assessment before allogeneic HCT. Blood 2005, 106:2912-2919.
27. Jazirehi A.R., Huerta-Yepez S., Cheng G., Bonavida B. Rituximab (chimeric anti-CD20 monoclonal antibody) inhibits the constitutive nuclear factor-{kappa}B signaling pathway in non-Hodgkin's lymphoma B-cell lines: role in sensitization to chemotherapeutic drug-induced apoptosis. Cancer Res 2005, 65:264-276.
28. Bonavida B. Rituximab-induced inhibition of antiapoptotic cell survival pathways: implications in chemo/immunoresistance, rituximab unresponsiveness, prognostic and novel therapeutic interventions. Oncogene 2007, 26:3629-3636.
29. van Oers M.H., Klasa R., Marcus R.E., 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, 108:3295-3301.
30. Forstpointner R., Unterhalt M., Dreyling M., 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, 108:4003-4008.
31. Peggs K.S. Immune reconstitution following stem cell transplantation. Leuk Lymph 2004, 45:1093-1101.
32. Dall'Ozzo S., Tartas S., Paintaud G., et al. Rituximab-dependent cytotoxicity by natural killer cells: influence of FCGR3A polymorphism on the concentration-effect relationship. Cancer Res 2004, 64:4664-4669.
33. Ponce D.M., Sauter C., Devlin S., et al. Anovel reduced intensity conditioning regimen induces a high incidence of sustained donor-derived neutrophil and platelet engraftment after double-unit cord blood transplantation. Biol Blood Marrow Transplant 2013, 19:799-803.
34. Alyea E.P., Li S., Kim H.T., et al. Sirolimus, tacrolimus, and low-dose methotrexate as graft-versus-host disease prophylaxis in related and unrelated donor reduced-intensity conditioning allogeneic peripheral blood stem cell transplantation. Biol Blood Marrow Transplant 2008, 14:920-926.
35. Copelan E., Casper J.T., Carter S.L., et al. Ascheme for defining cause of death and its application in the T cell depletion trial. Biol Blood Marrow Transplant 2007, 13:1469-1476.
36. http://www.acrin.org/Portals/0/Administration/Regulatory/CTCAE_4.02_2009-09-15_QuickReference_5x7.pdf.
37. Rowlings P.A., Przepiorka D., Klein J.P., et al. IBMTR Severity Index for grading acute graft-versus-host disease: retrospective comparison with Glucksberg grade. Br J Haematol 1997, 97:855-864.
38. Filipovich A.H., Weisdorf D., Pavletic S., et al. National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-Versus-Host Disease. I. Diagnosis and Staging Working Group Report. Biol Blood Marrow Transplant 2005, 11:945-956.
39. Gray R.J. A class of k-sample tests for comparing the cumulative incidence of a competing risk. Ann Stat 1988, 16:1141-1154.
40. Avivi I., Montoto S., Canals C., et al. Matched unrelated donor stem cell transplant in 131 patients with follicular lymphoma: an analysis from the Lymphoma Working Party of the European Group for Blood and Marrow Transplantation. Br J Haematol 2009, 147:719-728.
41. Vigouroux S., Michallet M., Porcher R., et al. Long-term outcomes after reduced-intensity conditioning allogeneic stem cell transplantation for low-grade lymphoma: a survey by the French Society of Bone Marrow Graft Transplantation and Cellular Therapy (SFGM-TC). Haematologica 2007, 92:627-634.
42. Thomson K.J., Morris E.C., Bloor A., et al. Favorable long-term survival after reduced-intensity allogeneic transplantation for multiple-relapse aggressive non-Hodgkin's lymphoma. JClin Oncol 2009, 27:426-432.
43. Robinson S.P., Goldstone A.H., Mackinnon S., et al. Chemoresistant or aggressive lymphoma predicts for a poor outcome following reduced-intensity allogeneic progenitor cell transplantation: an analysis from the Lymphoma Working Party of the European Group for Blood and Bone Marrow Transplantation. Blood 2002, 100:4310-4316.
44. Pinana J.L., Martino R., Gayoso J., et al. Reduced intensity conditioning HLA identical sibling donor allogeneic stem cell transplantation for patients with follicular lymphoma: long-term follow-up from two prospective multicenter trials. Haematologica 2010, 95:1176-1182.
45. Castillo J.J., Furman M., Winer E.S. CAL-101: a phosphatidylinositol-3-kinase p110-delta inhibitor for the treatment of lymphoid malignancies. Exp Opin Invest Drugs 2012, 21:15-22.
46. Advani R.H., Buggy J.J., Sharman J.P., et al. Bruton tyrosine kinase inhibitor ibrutinib (PCI-32765) has significant activity in patients with relapsed/refractory B-cell malignancies. JClin Oncol 2013, 31:88-94.
47. Horwitz S.M., Negrin R.S., Blume K.G., et al. Rituximab as adjuvant to high-dose therapy and autologous hematopoietic cell transplantation for aggressive non-Hodgkin lymphoma. Blood 2004, 103:777-783.
48. Cattaneo C., Spedini P., Casari S., et al. Delayed-onset peripheral blood cytopenia after rituximab: frequency and risk factor assessment in a consecutive series of 77 treatments. Leuk Lymph 2006, 47:1013-1017.
49. Auer R.L., MacDougall F., Oakervee H.E., et al. T-cell replete fludarabine/cyclophosphamide reduced intensity allogeneic stem cell transplantation for lymphoid malignancies. Br J Haematol 2012, 157:580-585.
50. Freytes C.O., Zhang M.J., Carreras J., et al. Outcome of lower-intensity allogeneic transplantation in non-Hodgkin lymphoma after autologous transplantation failure. Biol Blood Marrow Transplant 2012, 18:1255-1264.
51. Arai S., Sahaf B., Narasimhan B., et al. Prophylactic rituximab after allogeneic transplantation decreases B-cell alloimmunity with low chronic GVHD incidence. Blood 2012, 119:6145-6154.
52. Cutler C., Kim H.T., Bindra B., et al. Rituximab prophylaxis prevents corticosteroid-requiring chronic GVHD after allogeneic peripheral blood stem cell transplantation: results of a phase II trial. Blood 2013, 122:1510-1517.
53. Ho V.T., Aldridge J., Kim H.T., et al. Comparison of tacrolimus and sirolimus (Tac/Sir) versus tacrolimus, sirolimus, and mini-methotrexate (Tac/Sir/MTX) as acute graft-versus-host disease prophylaxis after reduced-intensity conditioning allogeneic peripheral blood stem cell transplantation. Biol Blood Marrow Transplant 2009, 15:844-850.
54. Griffith M.L., Savani B.N., Boord J.B. Dyslipidemia after allogeneic hematopoietic stem cell transplantation: evaluation and management. Blood 2010, 116:1197-1204.
55. Laskin B.L., Goebel J., Davies S.M., Jodele S. Small vessels, big trouble in the kidneys and beyond: hematopoietic stem cell transplantation-associated thrombotic microangiopathy. Blood 2011, 118:1452-1462.
56. Pidala J., Kim J., Jim H., et al. Arandomized phase II study to evaluate tacrolimus in combination with sirolimus or methotrexate after allogeneic hematopoietic cell transplantation. Haematologica 2012, 97:1882-1889.
57. Cutler C, Nakamura R, Johnston L, et al. Tacrolimus/sirolimus vs. tacrolimus/methotrexate for graft-vs.-host disease prophylaxis after HLA-matched, related donor hematopoietic stem cell transplantation: results of Blood and Marrow Transplant Clinical Trials Network Trial 0402. Blood. Abstract #739 Blood (ASH Annual Meeting Abstracts), Nov 2012; 120: 739.
58. Schatz J.H. Targeting the PI3K/AKT/mTOR pathway in non-Hodgkin's lymphoma: results, biology, and development strategies. Curr Oncol Rep 2011, 13:398-406.
59. Armand P., Gannamaneni S., Kim H.T., et al. Improved survival in lymphoma patients receiving sirolimus for graft-versus-host disease prophylaxis after allogeneic hematopoietic stem-cell transplantation with reduced-intensity conditioning. JClin Oncol 2008, 26:5767-5774.
60. Socie G., Schmoor C., Bethge W.A., et al. Chronic graft-versus-host disease: long-term results from a randomized trial on graft-versus-host disease prophylaxis with or without anti-T-cell globulin ATG-Fresenius. Blood 2011, 117:6375-6382.
61. Malard F., Cahu X., Clavert A., et al. Fludarabine, antithymocyte globulin, and very low-dose busulfan for reduced-intensity conditioning before allogeneic stem cell transplantation in patients with lymphoid malignancies. Biol Blood Marrow Transplant 2011, 17:1698-1703.
62. Soiffer R.J., Lerademacher J., Ho V., et al. Impact of immune modulation with anti-T-cell antibodies on the outcome of reduced-intensity allogeneic hematopoietic stem cell transplantation for hematologic malignancies. Blood 2011, 117:6963-6970.
63. Koreth J., Stevenson K.E., Kim H.T., et al. Bortezomib-based graft-versus-host disease prophylaxis in HLA-mismatched unrelated donor transplantation. JClin Oncol 2012, 30:3202-3208.