Rituximab purging and maintenance combined with auto-SCT: Long-term molecular remissions and prolonged hypogammaglobulinemia in relapsed follicular lymphoma

Bone Marrow Transplantation

Volumn 43, Issue 9, 2009, Pages 701-708

  Hicks, L K ^a   Woods, A ^b   Buckstein, R ^c   Mangel, J ^d   Pennell, N ^c   Zhang, L ^c   Imrie, K ^c   Spaner, D ^c   Cheung, M C ^c   Boudreau, A ^c   Reis, M ^c   Crump, M ^e   Berinstein, N L ^c  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c DEPARTMENT OF RADIATION ONCOLOGY   (Canada)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

^e PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; ARABINOSIDE; CISPLATIN; CYCLOPHOSPHAMIDE; CYTARABINE; CYTOSINE; DEXAMETHASONE; DOXORUBICIN; ETOPOSIDE; GRANULOCYTE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN G; MELPHALAN; PREDNISONE; RITUXIMAB; VINCRISTINE;

ACUTE KIDNEY FAILURE; ADULT; AGED; ARTICLE; ATYPICAL MYCOBACTERIOSIS; AUTOLOGOUS STEM CELL TRANSPLANTATION; BACTERIAL INFECTION; BRONCHOSCOPY; CANCER CHEMOTHERAPY; CANCER REGRESSION; CANCER RELAPSE; CANCER SURVIVAL; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; COUGHING; DRUG MEGADOSE; DYSPNEA; FEMALE; FOLLICULAR LYMPHOMA; HERPES ZOSTER; HUMAN; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN DEFICIENCY; LUNG CARCINOMA; LUNG NODULE; MAINTENANCE THERAPY; MALE; MULTIPLE CYCLE TREATMENT; NEUTROPENIA; OPTIC NEURITIS; OVERALL SURVIVAL; PNEUMONIA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; SALVAGE THERAPY; SECOND CANCER; SINUSITIS; SURVIVAL TIME; THERAPY DELAY; THROMBOTIC THROMBOCYTOPENIC PURPURA; TREATMENT RESPONSE;

ADULT; AGAMMAGLOBULINEMIA; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; FEMALE; FOLLOW-UP STUDIES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; LYMPHOMA, FOLLICULAR; MALE; MIDDLE AGED; NEOPLASM, RESIDUAL; POLYMERASE CHAIN REACTION; REMISSION INDUCTION; SALVAGE THERAPY; SURVIVAL ANALYSIS; TRANSPLANTATION, AUTOLOGOUS;

EID: 67349249726     PISSN: 02683369     EISSN: 14765365     Source Type: Journal    
DOI: 10.1038/bmt.2008.382     Document Type: Article

References (61)

1. Fisher RI, LeBlanc M, Press OW, Maloney DG, Unger JM, Miller TP. New treatment options have changed the survival of patients withfollicular lymphoma. J Clin Oncol 2005; 23: 8447-8452.
2. Weaver CH, Schwartzberg L, Rhinehart S, West J, Zhen B, West WH et al High-dose chemotherapy with BUCY or BEAC and unpurged peripheral blood stem cell infusion in patients withlow-grade non-Hodgkin's lymphoma. Bone Marrow Transplant 1998; 21: 383-389.
3. Bastion Y, Brice P, Haioun C, Sonet A, Salles G, Marolleau JP et al Intensive therapy with peripheral blood progenitor cell transplantation in 60 patients withpoor-prognosis follicular lymphoma. Blood 1995; 86: 3257-3262.
4. Berglund A, Enblad G, Carlson K, Glimelius B, Hagberg H. Long-term follow-up of autologous stem-cell transplantation for follicular and transformed follicular lymphoma. Eur J Haematol 2000; 65: 17-22.
5. Bierman PJ, Vose JM, Anderson JR, Bishop MR, Kessinger A, Armitage JO. High-dose therapy with autologous hematopoietic rescue for follicular low-grade non-Hodgkin's lymphoma. J Clin Oncol 1997; 15: 445-450.
6. Brice P, Simon D, Bouabdallah R, Belanger C, Haioun C, Thieblemont C et al. High-dose therapy with autologous stem-cell transplantation (ASCT) after first progression prolonged survival of follicular lymphoma patients included in the prospective GELF 86 protocol. Ann Oncol 2000; 11: 1585-1590.
7. Cao TM, Horning S, Negrin RS, Hu WW, Johnston LJ, Taylor TL et al. High-dose therapy and autologous hematopoietic-cell transplantation for follicular lymphoma beyond first remission: The Stanford University experience. Biol Blood Marrow Transplant 2001; 7: 294-301.
8. Colombat P, Donadio D, Fouillard L, Milpied N, Tilly H, Pico J et al Value of autologous bone marrow transplantation in follicular lymphoma: A France Autogreffe retrospective study of 42 patients. Bone Marrow Transplant 1994; 13: 157-162.
9. Freedman AS, Neuberg D, Mauch P, Soiffer RJ, Anderson KC, Fisher DC et al. Long-term follow-up of autologous bone marrow transplantation in patients with relapsed follicular lymphoma. Blood 1999; 94 3325-3333.
10. Lopez R, Martino R, Sureda A, Nomdedeu J, Briones J, Martin-Henao G et al. Autologous stem cell transplantation in advanced follicular lymphoma. A single center experience. Haematologica 1999; 84 350-355.
11. Molina A, Nademanee A, O'Donnell M. Long-term follow-up and analysis of prognostic factors after high-dose therapy and peripheral blood stem cell autografting in 58 patients with a history of low grade follicular lymphoma. Blood 1999; 94: 171a.
12. Verdonck LF. Allogeneic versus autologous bone marrow transplantation for refractory and recurrent low-grade non-Hodgkin's lymphoma: Updated results of the Utrecht experience. Leuk Lymphoma 1999; 34: 129-136.
13. Verdonck LF, Dekker AW, Lokhorst HM, Petersen EJ, Nieuwenhuis HK. Allogeneic versus autologous bone marrow transplantation for refractory and recurrent low-grade non-Hodgkin's lymphoma. Blood 1997; 90 4201-4205.
14. Voso MT, Martin S, Hohaus S, Abdallah A, Schlenk RF, Ho AD et al. Prognostic factors for the clinical outcome of patients with follicular lymphoma following high-dose therapy and peripheral blood stem cell transplantation (PBSCT). Bone Marrow Transplant 2000; 25: 957-964.
15. Apostolidis J, Gupta RK, Grenzelias D, Johnson PW, Pappa VI, Summers KE et al. High-dose therapy with autologous bone marrow support as consolidation of remission in follicular lymphoma: Long-term clinical and molecular follow-up. J Clin Oncol 2000; 18: 527-536.
16. Schouten HC, Qian W, Kvaloy S, Porcellini A, Hagberg H, Johnson HE 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. J Clin Oncol 2003; 21: 3918-3927.
17. Apostolidis J, Foran JM, Johnson PW, Norton A, Amess J, Matthews J et al. Patterns of outcome following recurrence after myeloablative therapy with autologous bone marrow transplantation for follicular lymphoma. J Clin Oncol 1999; 17: 216-221.
18. Bachier CR, Giles RE, Ellerson D, Hanania EG, Garcia-Sanchez F, Andreeff M et al. Hematopoietic retroviral gene marking in patients with follicular non-Hodgkin's lymphoma. Leuk Lymphoma 1999; 32: 279-288.
19. Leonard BM, Hetu F, Busque L, Gyger M, Belanger R, Perreault C et al Lymphoma cell burden in progenitor cell grafts measured by competitive polymerase chain reaction: Less than one log difference between bone marrow and peripheral blood sources. Blood 1998; 91: 331-339.
20. Jacquy C, Soree A, Lambert F, Bosly A, Ferrant A, Andre M et al. A quantitative study of peripheral blood stem cell contamination in diffuse large-cell non-Hodgkin's lymphoma: One-half of patients significantly mobilize malignant cells. Br J Haematol 2000; 110 631-637.
21. Moos M, Schulz R, Cremer F, Sucker C, Schmohl D, Dohner H et al. Detection of minimal residual disease by polymerase chain reaction in B cell malignancies. Stem Cells 1995; 13 (Suppl 3): 42-51.
22. Deisseroth AB, Zu Z, Claxton D, Hanania EG, Fu S, Ellerson D et al Genetic marking shows that Ph+ cells present in autologous transplants of chronic myelogenous leukemia (CML) contribute to relapse after autologous bone marrow in CML. Blood 1994; 83: 3068-3076.
23. Brenner MK, Rill DR, Moen RC, Krance RA, Mirro Jr J, Anderson WF et al. Gene-marking to trace origin of relapse after autologous bone-marrow transplantation. Lancet 1993; 341: 85-86.
24. Marcus R, Imrie K, BelchA, Cunningham D, Flores E, Catalano J et al CVP chemotherapy plus rituximab compared with CVP chemotherapy as first-line treatment for advanced follicular lymphoma. Blood 2005; 105: 1417-1423.
25. 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: 2825-2833.
26. Galimberti S, Guerrini F, Morabito F, Palumbo GA, Di Raimondo F, Papineschi F et al. Quantitative molecular evaluation in autotransplant programs for follicular lymphoma: Efficacy of in vivo purging by rituximab. Bone Marrow Transplant 2003; 32: 57-63.
27. Jacobsen E, Freedman A. B-cell purging in autologous stem-cell transplantation for non-Hodgkin lymphoma. Lancet Oncol 2004; 5 711-717.
28. Belhadj K, Delfau-Larue MH, Elgnaoui T, Beaujean F, Beaumont JL, Pautas C et al. Efficiency of in vivo purging withrituximab prior to autologous peripheral blood progenitor cell transplantation in B-cell non-Hodgkin's lymphoma: A single institution study. Ann Oncol 2004; 15: 504-510.
29. Arcaini L, Orlandi E, Alessandrino EP, Iacona I, Brusamolino E, Bonfichi M et al. A model of in vivo purging withrituximab and high-dose AraC in follicular and mantle cell lymphoma. Bone Marrow Transplant 2004; 34: 175-179.
30. Brugger W, Hirsch J, Grunebach F, Repp R, Brossart P, Vogel W et al Rituximab consolidation after high-dose chemotherapy and autologous blood stem cell transplantation in follicular and mantle cell lymphoma: a prospective, multicenter phase II study. Ann Oncol 2004; 15 1691-1698.
31. Pennell N, Woods A, Reis M, Buckstein R, Spaner D, Imrie K et al. Association of clinical status of follicular lymphoma patients after autologous stem cell transplant and quantitative assessment of lymphoma in blood and bone marrow as measured by SYBR Green I polymerase chain reaction. J Mol Diagn 2006; 8: 40-50.
32. Corradini P, Ladetto M, Pileri A, Tarella C. Clinical relevance of minimal residual disease monitoring in non-Hodgkin's lymphomas: A critical reappraisal of molecular strategies. Leukemia 1999; 13 1691-1695.
33. Corradini P, Ladetto M, Zallio F, Astolfi M, Rizzo E, Sametti S et al Long-term follow-up of indolent lymphoma patients treated with high-dose sequential chemotherapy and autografting: Evidence that durable molecular and clinical remission frequently can be attained only in follicular subtypes. J Clin Oncol 2004; 22: 1460-1468.
34. Moos M, Schulz R, Martin S, Benner A, Haas R. The remission status before and the PCR status after high-dose therapy with peripheral blood stem cell support are prognostic factors for relapse-free survival in patients with follicular non-Hodgkin's lymphoma. Leukemia 1998; 12: 1971-1976.
35. Gribben JG, Neuberg D, Freedman AS, Gimmi CD, Pesek KW, Barber M et al. Detection by polymerase chain reaction of residual cells with the bcl-2 translocation is associated with increased risk of relapse after autologous bone marrow transplantation for B-cell lymphoma. Blood 1993; 81: 3449-3457.
36. Jones SE, Grozea PN, Metz EN, Haut A, Stephens RL, Morrison FS et al Superiority of adriamycin-containing combination chemotherapy in the treatment of diffuse lymphoma: A Southwest Oncology Group study. Cancer 1979; 43: 417-425.
37. Velasquez WS, Cabanillas F, Salvador P, McLaughlin P, Fridrik M, Tucker S et al. Effective salvage therapy for lymphoma with cisplatin in combination with high-dose Ara-C and dexamethasone (DHAP). Blood 1988; 1: 117-122.
38. Girouard C, Dufresne J, Imrie K, Stewart AK, Brandwein J, Prince HM et al. Salvage chemotherapy with mini-BEAM for relapsed or refractory non-Hodgkin's lymphoma prior to autologous bone marrow transplantation. Ann Oncol 1997; 8: 675-680.
39. Jagannath S, Dicke KA, Armitage JO, Cabanillas FF, Horwitz LJ, Vellekoop L et al. High-dose cyclophosphamide, carmustine, and etoposide and autologous bone marrow transplantation for relapsed Hodgkin's disease. Ann Intern Med 1986; 104: 163-168.
40. 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: 1244.
41. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc 1958; 53: 457-481.
42. Solal-Celigny P, Roy P, Colombat P, White J, Armitage JO, Arranz-Saez R et al. Follicular lymphoma international prognostic index. Blood 2004; 104: 1258-1265.
43. Ault KA, Antin JH, Ginsburg D, Orkin SH, Rappeport JM, Keohan ML et al. Phenotype of recovering lymphoid cell populations after marrow transplantation. J Exp Med 1985; 161: 1483-1502.
44. Kiesel S, Pezzutto A, Moldenhauer G, Haas R, Korbling M, Hunstein W et al. B-cell proliferative and differentiative responses after autologous peripheral blood stem cell or bone marrow transplantation. Blood 1988; 72: 672-678.
45. Lim SH, Zhang Y, Wang Z, Esler WV, Beggs D, Pruitt B et al. Maintenance rituximab after autologous stem cell transplant for high-risk B-cell lymphoma induces prolonged and severe hypogammaglobulinemia. Bone Marrow Transplant 2005; 35: 207-208.
46. Hess G, Flohr T, Huber C, Kolbe K, Derigs HG, Fischer T. Safety and feasibility of CHOP/rituximab induction treatment followed by high-dose chemo/radiotherapy and autologous PBSC-transplantation in patients with previously untreated mantle cell or indolent B-cell-non-Hodgkin's lymphoma. Bone Marrow Transplant 2003; 31: 775-782.
47. Horwitz SM, Negrin RS, Blume KG, Breslin S, Stuart MJ, Stockerl-Goldstein KE 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. Shortt J, Spencer A. Adjuvant rituximab causes prolonged hypogammaglobulinaemia following autologous stem cell transplant for non-Hodgkin's lymphoma. Bone Marrow Transplant 2006; 38: 433-436.
49. Lim SH, Esler WV, Zhang Y, Zhang J, Periman PO, Burris C et al. B-cell depletion for 2 years after autologous stem cell transplant for NHL induces prolonged hypogammaglobulinemia beyond the rituximab maintenance period. Leuk Lymphoma 2008; 49: 152-153.
50. Van Der Kolk LE, Baars JW, Prins MH, Van Oers MH. Rituximab treatment results in impaired secondary humoral immune responsiveness. Blood 2002; 100: 2257-2259.
51. Ladetto M, Corradini P, Vallet S, Benedetti F, Vitolo U, Martelli M et al. High rate of clinical and molecular remissions in follicular lymphoma patients receiving high-dose sequential chemotherapy and autografting at diagnosis: A multicenter, prospective study by the Gruppo Italiano Trapianto Midollo Osseo (GITMO). Blood 2002; 100: 1559-1565.
52. Goldberg SL, Pecora AL, Alter RS, Kroll MS, Rowley SD, Waintraub SE et al. Unusual viral infections (progressive multifocal leukoencephalopathy and cytomegalovirus disease) after high-dose chemotherapy with autologous blood stem cell rescue and peritransplantation rituximab. Blood 2002; 99: 1486-1488.
53. Bierman PJ, Sweetenham JW, Loberiza Jr FR, Taghipour G, Lazarus HM, Rizzo JD et al. Syngeneic hematopoietic stem-cell transplantation for non-Hodgkin's lymphoma: A comparison witha llogeneic and autologous transplantation - The Lymphoma Working Committee of the International Bone Marrow Transplant Registry and the European Group for Blood and Marrow Transplantation. J Clin Oncol 2003; 21: 3744-3753.
54. 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: 3064-3071.
55. 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: 3725-3732.
56. 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: 3295-3301.
57. 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: 3135-3143.
58. 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: 1088-1095.
59. Carlotti E, Palumbo GA, Oldani E, Tibullo D, Salmoiraghi S, Rossi A et al. FcgammaRIIIA and FcgammaRIIA polymorphisms do not predict clinical outcome of follicular non-Hodgkin's lymphoma patients treated with sequential CHOP and rituximab. Haematologica 2007; 92: 1127-1130.
60. Burton C, Kaczmarski R, Jan-Mohamed R. Interstitial pneumonitis related to rituximab therapy. N Engl J Med 2003; 348: 2690-2691; discussion 2690-2691.
61. Cairoli R, Grillo G, Tedeschi A, D'Avanzo G, Marenco P, Morra E. High incidence of neutropenia in patients treated with rituximab after autologous stem cell transplantation. Haematologica 2004; 89 361-363.