Single-agent lenalidomide is active in patients with relapsed or refractory aggressive non-Hodgkin lymphoma who received prior stem cell transplantation

British Journal of Haematology

Volumn 162, Issue 5, 2013, Pages 639-647

  Vose, Julie M ^a   Habermann, Thomas M ^b   Czuczman, Myron S ^c   Zinzani, Pier Luigi ^d   Reeder, Craig B ^e   Tuscano, Joseph M ^f   Lossos, Izidore S ^g   Li, Ju ^h   Pietronigro, Dennis ^h   Witzig, Thomas E ^b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b MAYO CLINIC   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d UNIVERSITY OF BOLOGNA   (Italy)

^e MAYO CLINIC   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^h CELGENE CORPORATION   (United States)

Author keywords

Autologous stem cell transplantation; Lenalidomide; Non Hodgkin lymphoma

Indexed keywords

LENALIDOMIDE;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; AGED; ANEMIA; ARTICLE; ASTHENIA; AUTOLOGOUS STEM CELL TRANSPLANTATION; CANCER CHEMOTHERAPY; CANCER RECURRENCE; CANCER SURVIVAL; CONTROLLED STUDY; DEEP VEIN THROMBOSIS; DRUG DOSE REDUCTION; DRUG EFFICACY; DRUG INDUCED CANCER; DRUG SAFETY; DYSPNEA; FATIGUE; FEBRILE NEUTROPENIA; FEMALE; HUMAN; LARGE CELL LYMPHOMA; LEUKOPENIA; LUNG EMBOLISM; MAJOR CLINICAL STUDY; MALE; MANTLE CELL LYMPHOMA; MONOTHERAPY; NAUSEA; NEUTROPENIA; NONHODGKIN LYMPHOMA; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; SKIN CANCER; SOLID TUMOR; SURVIVAL TIME; THROMBOCYTOPENIA; TUMOR FLARE;

AUTOLOGOUS STEM CELL TRANSPLANTATION; LENALIDOMIDE; NON-HODGKIN LYMPHOMA;

ADULT; AGED; ANGIOGENESIS INHIBITORS; COMBINED MODALITY THERAPY; DISEASE PROGRESSION; DRUG EVALUATION; FEMALE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; LYMPHOMA, NON-HODGKIN; MALE; MIDDLE AGED; RECURRENCE; RETROSPECTIVE STUDIES; THALIDOMIDE; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84881664038     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12449     Document Type: Article

References (40)

1. Calvo-Villas, J.M., Martin, A., Conde, E., Pascual, A., Heras, I., Varela, R., de la Rubia, J., Ramirez, M.J., Diez-Martin, J.L., Panizo, C., Rodriguez-Salazar, M.J., Pascual, M.J., Donato, E.M., Gonzalez-Barca, E. & Caballero, M.D. (2010) Effect of addition of rituximab to salvage chemotherapy on outcome of patients with diffuse large B-cell lymphoma relapsing after an autologous stem-cell transplantation. Annals of Oncology, 21, 1891-1897.
2. Cheson, B.D., Horning, S.J., Coiffier, B., Shipp, M.A., Fisher, R.I., Connors, J.M., Lister, T.A., Vose, J., Grillo-Lopez, A., Hagenbeek, A., Cabanillas, F., Klippensten, D., Hiddemann, W., Castellino, R., Harris, N.L., Armitage, J.O., Carter, W., Hoppe, R. & Canellos, G.P. (1999) Report of an international workshop to standardize response criteria for non-Hodgkin's lymphomas. NCI Sponsored International Working Group. Journal of Clinical Oncology, 17, 1244.
3. Coiffier, B., Thieblemont, C., Van Den Neste, E., Lepeu, G., Plantier, I., Castaigne, S., Lefort, S., Marit, G., Macro, M., Sebban, C., Belhadj, K., Bordessoule, D., Ferme, C. & Tilly, H. (2010) Long-term outcome of patients in the LNH-98·5 trial, the first randomized study comparing rituximab-CHOP to standard CHOP chemotherapy in DLBCL patients: a study by the Groupe d'Etudes des Lymphomes de l'Adulte. Blood, 116, 2040-2045.
4. Copelan, E.A. (2006) Hematopoietic stem-cell transplantation. New England Journal of Medicine, 354, 1813-1826.
5. Czuczman, M.S. & Rummel, M.J. (2010) Clinical Roundtable Monograph: recent advances in NHL. Highlights from the 51st ASH Annual Meeting and Exposition, December 5-8, 2009, New Orleans, Louisiana. Clinical Advances in Hematology and Oncology, 8, A1-A11.
6. Dutia, M., DeRoock, I., Chee, K., O'Donnell, R.T., Quirch, C., Reed-Pease, C. & Tuscano, J.M. (2009) R2: Preliminary results of a phase II study of lenalidomide and rituximab in relapsed/ refractory indolent non-Hodgkin's lymphoma. Blood (ASH Annual Meeting Abstracts), 114, 1679.
7. Freytes, C.O., Loberiza, F.R., Rizzo, J.D., Bashey, A., Bredeson, C.N., Cairo, M.S., Gale, R.P., Horowitz, M.M., Klumpp, T.R., Martino, R., McCarthy, P.L., Molina, A., Pavlovsky, S., Pecora, A.L., Serna, D.S., Tsai, T., Zhang, M.J., Vose, J.M., Lazarus, H.M. & van Besien, K. (2004) Myeloablative allogeneic hematopoietic stem cell transplantation in patients who experience relapse after autologous stem cell transplantation for lymphoma: a report of the International Bone Marrow Transplant Registry. Blood, 104, 3797-3803.
8. Gaidarova, S., Li, J., Corral, L.G., Glezer, E., Schafer, P.H., Xie, W., Lopez-Girona, A., Cheson, B.D. & Bennett, B. (2009) Lenalidomide alone and in combination with rituximab enhances NK cell immune synapse formation in chronic lymphocytic leukemia (CLL) cells in vitro through activation of Rho and Rac1 GTPases. ASH Annual Meeting Abstracts, 114, 3441.
9. Gandhi, A.K., Kang, J., Naziruddin, S., Parton, A., Schafer, P.H. & Stirling, D.I. (2006) Lenalidomide inhibits proliferation of Namalwa CSN.70 cells and interferes with Gab1 phosphorylation and adaptor protein complex assembly. Leukemia Research, 30, 849-858.
10. Gisselbrecht, C., Glass, B., Mounier, N., Singh Gill, D., Linch, D.C., Trneny, M., Bosly, A., Ketterer, N., Shpilberg, O., Hagberg, H., Ma, D., Briere, J., Moskowitz, C.H. & Schmitz, N. (2010) Salvage regimens with autologous transplantation for relapsed large B-cell lymphoma in the rituximab era. Journal of Clinical Oncology, 28, 4184-4190.
11. Gorgun, G., Ramsay, A.G., Holderried, T.A., Zahrieh, D., Le Dieu, R., Liu, F., Quackenbush, J., Croce, C.M. & Gribben, J.G. (2009) E(mu)-TCL1 mice represent a model for immunotherapeutic reversal of chronic lymphocytic leukemia-induced T-cell dysfunction. Proceedings of the National Academy of Sciences of the United States of America, 106, 6250-6255.
12. Habermann, T.M., Weller, E.A., Morrison, V.A., Gascoyne, R.D., Cassileth, P.A., Cohn, J.B., Dakhil, S.R., Woda, B., Fisher, R.I., Peterson, B.A. & Horning, S.J. (2006) Rituximab-CHOP versus CHOP alone or with maintenance rituximab in older patients with diffuse large B-cell lymphoma. Journal of Clinical Oncology, 24, 3121-3127.
13. Habermann, T.M., Lossos, I.S., Justice, G., Vose, J.M., Wiernik, P.H., McBride, K., Wride, K., Ervin-Haynes, A., Takeshita, K., Pietronigro, D., Zeldis, J.B. & Tuscano, J.M. (2009) Lenalidomide oral monotherapy produces a high response rate in patients with relapsed or refractory mantle cell lymphoma. British Journal of Haematology, 145, 344-349.
14. Hagberg, H. & Gisselbrecht, C. (2006) Randomised phase III study of R-ICE versus R-DHAP in relapsed patients with CD20 diffuse large B-cell lymphoma (DLBCL) followed by high-dose therapy and a second randomisation to maintenance treatment with rituximab or not: an update of the CORAL study. Annals of Oncology, 17(Suppl. 4), iv31-iv32.
15. Hernandez-Ilizaliturri, F.J., Reddy, N., Holkova, B., Ottman, E. & Czuczman, M.S. (2005) Immunomodulatory drug CC-5013 or CC-4047 and rituximab enhance antitumor activity in a severe combined immunodeficient mouse lymphoma model. Clinical Cancer Research, 11, 5984-5992.
16. Kaplan, E.L. & Meier, P. (1958) Nonparametric estimation from incomplete observations. Journal of the American Statistical Association, 53, 457-481.
17. Kewalramani, T., Nimer, S.D., Zelenetz, A.D., Malhotra, S., Qin, J., Yahalom, J. & Moskowitz, C.H. (2003) Progressive disease following autologous transplantation in patients with chemosensitive relapsed or primary refractory Hodgkin's disease or aggressive non-Hodgkin's lymphoma. Bone Marrow Transplantation, 32, 673-679.
18. Kim, J.W., Kim, B.S., Bang, S.M., Kim, I., Kim, D.H., Kim, W.S., Yang, D.H., Lee, J.J., Lee, J.H., Kim, J.S., Sohn, S.K., Yhim, H.Y., Kwak, J.Y., Yoon, S.S., Lee, J.S., Park, S. & Kim, B.K. (2011) Allogeneic stem cell transplantation in patients with non-Hodgkin lymphoma who experienced relapse or progression after autologous stem cell transplantation. Annals of Hematology, 90, 1409-1418.
19. Mantel, N. (1966) Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemotherapy Reports, 50, 163-170.
20. Nagler, A., Berger, R., Ackerstein, A., Czyz, J.A., Diez-Martin, J.L., Naparstek, E., Or, R., Gan, S., Shimoni, A. & Slavin, S. (2010) A randomized controlled multicenter study comparing recombinant interleukin 2 (rIL-2) in conjunction with recombinant interferon alpha (IFN-alpha) versus no immunotherapy for patients with malignant lymphoma postautologous stem cell transplantation. Journal of Immunotherapy, 33, 326-333.
21. Nowakowski, G.S., LaPlant, B., Habermann, T.M., Rivera, C.E., Macon, W.R., Inwards, D.J., Micallef, I.N., Johnston, P.B., Porrata, L.F., Ansell, S.M., Klebig, R.R., Reeder, C.B. & Witzig, T.E. (2011) Lenalidomide can be safely combined with R-CHOP (R2CHOP) in the initial chemotherapy for aggressive B-cell lymphomas: phase I study. Leukemia, 25, 1877-1881.
22. Nowakowski, G.S., LaPlant, B.R., Reeder, C., Foran, J.M., Porrata, L.F., Macon, W.R., Johnston, P.B., Rivera, C.E., Habermann, T.M., Inwards, D.J., Micallef, I.N., Nelson, G.D., Ansell, S.M. & Witzig, T.E. (2012) Combination of lenalidomide with R-CHOP (R2CHOP) is well-tolerated and effective as initial therapy for aggressive B-cell lymphomas - A phase II study. Blood (ASH Annual Meeting Abstracts), 120, Abstract 689.
23. Paltiel, O., Rubinstein, C., Or, R., Nagler, A., Gordon, L., Deutsch, L., Polliack, A. & Naparstek, E. (2003) Factors associated with survival in patients with progressive disease following autologous transplant for lymphoma. Bone Marrow Transplantation, 31, 565-569.
24. Pan, D., Moskowitz, C.H., Zelenetz, A.D., Straus, D., Kewalaramani, T., Noy, A., Qin, J., Teruya-Feldstein, J. & Portlock, C.S. (2002) Rituximab for aggressive non-Hodgkin's lymphomas relapsing after or refractory to autologous stem cell transplantation. Cancer Journal, 8, 371-376.
25. Pfreundschuh, M., Schubert, J., Ziepert, M., Schmits, R., Mohren, M., Lengfelder, E., Reiser, M., Nickenig, C., Clemens, M., Peter, N., Bokemeyer, C., Eimermacher, H., Ho, A., Hoffmann, M., Mertelsmann, R., Trumper, L., Balleisen, L., Liersch, R., Metzner, B., Hartmann, F., Glass, B., Poeschel, V., Schmitz, N., Ruebe, C., Feller, A.C. & Loeffler, M. (2008) Six versus eight cycles of bi-weekly CHOP-14 with or without rituximab in elderly patients with aggressive CD20+ B-cell lymphomas: a randomised controlled trial (RICOVER-60). The Lancet Oncology, 9, 105-116.
26. Pfreundschuh, M., Kuhnt, E., Trumper, L., Osterborg, A., Trneny, M., Shepherd, L., Gill, D.S., Walewski, J., Pettengell, R., Jaeger, U., Zinzani, P.L., Shpilberg, O., Kvaloy, S., de Nully Brown, P., Stahel, R., Milpied, N., Lopez-Guillermo, A., Poeschel, V., Grass, S., Loeffler, M. & Murawski, N. (2011) CHOP-like chemotherapy with or without rituximab in young patients with good-prognosis diffuse large-B-cell lymphoma: 6-year results of an open-label randomised study of the MabThera International Trial (MInT) Group. The Lancet Oncology, 12, 1013-1022.
27. Ramsay, A.G., Clear, A.J., Kelly, G., Fatah, R., Matthews, J., Macdougall, F., Lister, T.A., Lee, A.M., Calaminici, M. & Gribben, J.G. (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, 4713-4720.
28. Reddy, N., Hernandez-Ilizaliturri, F.J., Deeb, G., Roth, M., Vaughn, M., Knight, J., Wallace, P. & Czuczman, M.S. (2008) Immunomodulatory drugs stimulate natural killer-cell function, alter cytokine production by dendritic cells, and inhibit angiogenesis enhancing the anti-tumour activity of rituximab in vivo. British Journal of Haematology, 140, 36-45.
29. Thompson, J.A., Fisher, R.I., Leblanc, M., Forman, S.J., Press, O.W., Unger, J.M., Nademanee, A.P., Stiff, P.J., Petersdorf, S.H. & Fefer, A. (2008) Total body irradiation, etoposide, cyclophosphamide, and autologous peripheral blood stem-cell transplantation followed by randomization to therapy with interleukin-2 versus observation for patients with non-Hodgkin lymphoma: results of a phase 3 randomized trial by the Southwest Oncology Group (SWOG 9438). Blood, 111, 4048-4054.
30. Tsai, D., Moore, H., Hardy, C., Porter, D., Loh, E., Vaughn, D., Luger, S., Schuster, S. & Stadtmauer, E. (1999) Rituximab (anti-CD20 monoclonal antibody) therapy for progressive intermediate-grade non-Hodgkin's lymphoma after high-dose therapy and autologous peripheral stem cell transplantation. Bone Marrow Transplantation, 24, 521-526.
31. Tsirigotis, P., Dray, L., Resnick, I.B., Ackerstein, A., Gesundheit, B., Elad, S., Or, R. & Shapira, M.Y. (2010) Post-autologous stem cell transplantation administration of rituximab improves the outcome of patients with aggressive B cell non-Hodgkin's lymphoma. Annals of Hematology, 89, 263-272.
32. Verhelle, D., Corral, L.G., Wong, K., Mueller, J.H., Moutouh-de Parseval, L., Jensen-Pergakes, K., Schafer, P.H., Chen, R., Glezer, E., Ferguson, G.D., Lopez-Girona, A., Muller, G.W., Brady, H.A. & Chan, K.W. (2007) Lenalidomide and CC-4047 inhibit the proliferation of malignant B cells while expanding normal CD34+ progenitor cells. Cancer Research, 67, 746-755.
33. Vose, J.M., Bierman, P.J., Anderson, J.R., Kessinger, A., Pierson, J., Nelson, J., Frappier, B., Schmit-Pokorny, K., Weisenburger, D.D. & Armitage, J.O. (1992) Progressive disease after high-dose therapy and autologous transplantation for lymphoid malignancy: clinical course and patient follow-up. Blood, 80, 2142-2148.
34. Vose, J.M., Rizzo, D.J., Tao-Wu, J., Armitage, J.O., Bashey, A., Burns, L.J., Christiansen, N.P., Freytes, C.O., Gale, R.P., Gibson, J., Giralt, S.A., Herzig, R.H., Lemaistre, C.F., McCarthy, P.L. Jr, Nimer, S.D., Petersen, F.B., Schenkein, D.P., Wiernik, P.H., Wiley, J.M., Loberiza, F.R., Lazarus, H.M., van Biesen, K. & Horowitz, M.M. (2004) Autologous transplantation for diffuse aggressive non-Hodgkin lymphoma in first relapse or second remission. Biology of Blood and Marrow Transplantation, 10, 116-127.
35. Wiernik, P.H., Lossos, I.S., Tuscano, J.M., Justice, G., Vose, J.M., Cole, C.E., Lam, W., McBride, K., Wride, K., Pietronigro, D., Takeshita, K., Ervin-Haynes, A., Zeldis, J.B. & Habermann, T.M. (2008) Lenalidomide monotherapy in relapsed or refractory aggressive non-Hodgkin's lymphoma. Journal of Clinical Oncology, 26, 4952-4957.
36. Witzig, T.E., Wiernik, P.H., Moore, T., Reeder, C., Cole, C., Justice, G., Kaplan, H., Voralia, M., Pietronigro, D., Takeshita, K., Ervin-Haynes, A., Zeldis, J.B. & Vose, J.M. (2009) Lenalidomide oral monotherapy produces durable responses in relapsed or refractory indolent non-Hodgkin's Lymphoma. Journal of Clinical Oncology, 27, 5404-5409.
37. Witzig, T.E., Vose, J.M., Zinzani, P.L., Reeder, C.B., Buckstein, R., Polikoff, J.A., Bouabdallah, R., Haioun, C., Tilly, H., Guo, P., Pietronigro, D., Ervin-Haynes, A.L. & Czuczman, M.S. (2011) An international phase II trial of single-agent lenalidomide for relapsed or refractory aggressive B-cell non-Hodgkin's lymphoma. Annals of Oncology, 22, 1622-1627.
38. Wu, L., Adams, M., Carter, T., Chen, R., Muller, G., Stirling, D., Schafer, P. & Bartlett, J.B. (2008) Lenalidomide enhances natural killer cell and monocyte-mediated antibody-dependent cellular cytotoxicity of rituximab-treated CD20+ tumor cells. Clinical Cancer Research, 14, 4650-4657.
39. Zhu, D., Corral, L.G., Fleming, Y.W. & Stein, B. (2008) Immunomodulatory drugs Revlimid (lenalidomide) and CC-4047 induce apoptosis of both hematological and solid tumor cells through NK cell activation. Cancer Immunology, Immunotherapy, 57, 1849-1859.
40. Zinzani, P.L., Vose, J.M., Czuczman, M.S., Reeder, C., Haioun, C., Polikoff, J., Tilly, H., Pietronigro, D., Ervin-Haynes, A., Li, J. & Witzig, T.E. (2012) Phase II multicenter study of the safety and efficacy of single-agent lenalidomide in subjects with relapsed/refractory mantle cell lymphoma: Long-term follow-up analysis of the NHL-003 study. Blood (ASH Annual Meeting Abstracts), 120, 2738.