Persistence of minimal residual disease in bone marrow predicts outcome in follicular lymphomas treated with a rituximab-intensive program

Blood

Volumn 122, Issue 23, 2013, Pages 3759-3766

  Ladetto, Marco ^a   Lobetti Bodoni, Chiara ^a   Mantoan, Barbara ^a   Ceccarelli, Manuela ^b   Boccomini, Carola ^b   Genuardi, Elisa ^a   Chiappella, Annalisa ^b   Baldini, Luca ^c   Rossi, Giuseppe ^d   Pulsoni, Alessandro ^e   Di Raimondo, Francesco ^f   Rigacci, Luigi ^g   Pinto, Antonello ^h   Galimberti, Sara ⁱ   Bari, Alessia ^j   Rota Scalabrini, Delia ^k   Ferrari, Angela ^l   Zaja, Francesco ^m   Gallamini, Andrea ⁿ   Specchia, Giorgina ^o   Musto, Pellegrino ^p   Rossi, Francesca Gaia ^c   Gamba, Enrica ^q   Evangelista, Andrea ^b   Vitolo, Umberto ^b   more..

^a UNIVERSITY OF TURIN   (Italy)

^b Azienda Ospedaliera Città della Salute e della Scienza   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF BRESCIA   (Italy)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f UNIVERSITY OF CATANIA   (Italy)

^g CAREGGI UNIVERSITY HOSPITAL   (Italy)

^h NATIONAL CANCER INSTITUTE   (Italy)

ⁱ UNIVERSITY OF PISA   (Italy)

^j UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^k CANDIOLO CANCER INSTITUTE   (Italy)

^l S MARIA NUOVA HOSPITAL   (Italy)

^m UNIVERSITY HOSPITAL OF UDINE   (Italy)

ⁿ S CROCE E CARLE HOSPITAL   (Italy)

^o UNIVERSITY OF BARI   (Italy)

^p Direzione Scientifica   (Italy)

^q ROCHE MILANO RICERCHE   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; FLUDARABINE; MITOXANTRONE; MOLECULAR MARKER; PROTEIN BCL 2; RITUXIMAB;

AGED; ARTICLE; BONE MARROW CELL; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CANCER SURVIVAL; FOLLICULAR LYMPHOMA; FOLLOW UP; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MINIMAL RESIDUAL DISEASE; MULTICENTER STUDY (TOPIC); OUTCOME ASSESSMENT; PHASE 3 CLINICAL TRIAL (TOPIC); POLYMERASE CHAIN REACTION; POST TREATMENT SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REAL TIME POLYMERASE CHAIN REACTION; RELAPSE;

EID: 84891043722     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-06-507319     Document Type: Article

References (52)

1. Freedman A. Follicular lymphoma: 2011 update on diagnosis and management. Am J Hematol. 2011;86(9):768-775.
2. Fisher RI, LeBlanc M, Press OW, Maloney DG, Unger JM, Miller TP. New treatment options have changed the survival of patients with follicular lymphoma. J Clin Oncol. 2005;23(33):8447-8452.
3. Liu Q, Fayad L, Cabanillas F, et al. Improvement of overall and failure-free survival in stage IV follicular lymphoma: 25 years of treatment experience at The University of Texas M.D. Anderson Cancer Center. J Clin Oncol. 2006; 24(10):1582-1589.
4. Griffiths RI, Gleeson ML, Mikhael J, et al. Impact on Medical Cost, Cumulative Survival, and Cost- Effectiveness of Adding Rituximab to First-Line Chemotherapy for Follicular Lymphoma in Elderly Patients: An Observational Cohort Study Based on SEER-Medicare. J Cancer Epidemiol. 2012; 2012:978391.
5. Gribben JG, Freedman A, Woo SD, et al. All advanced stage non-Hodgkin's lymphomas with a polymerase chain reaction amplifiable breakpoint of bcl-2 have residual cells containing the bcl-2 rearrangement at evaluation and after treatment. Blood. 1991;78(12):3275-3280.
6. Gribben JG, Freedman AS, Neuberg D, et al. Immunologic purging of marrow assessed by PCR before autologous bone marrow transplantation for B-cell lymphoma. N Engl J Med. 1991;325(22): 1525-1533.
7. Gribben JG, Saporito L, Barber M, et al. Bone marrows of non-Hodgkin's lymphoma patients with a bcl-2 translocation can be purged of polymerase chain reaction-detectable lymphoma cells using monoclonal antibodies and immunomagnetic bead depletion. Blood. 1992; 80(4):1083-1089.
8. Hardingham JE, Kotasek D, Sage RE, et al. Significance of molecular marker-positive cells after autologous peripheral-blood stem-cell transplantation for non-Hodgkin's lymphoma. J Clin Oncol. 1995;13(5):1073-1079.
9. Corradini P, Astolfi M, Cherasco C, et al. Molecular monitoring of minimal residual disease in follicular and mantle cell non-Hodgkin's lymphomas treated with high-dose chemotherapy and peripheral blood progenitor cell autografting. Blood. 1997;89(2):724-731.
10. 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(12):1971-1976.
11. Freedman AS, Neuberg D, Mauch P, et al. Longterm follow-up of autologous bone marrow transplantation in patients with relapsed follicular lymphoma. Blood. 1999;94(10):3325-3333.
12. L'opez-Guillermo A, Cabanillas F, McLaughlin P, et al. The clinical significance of molecular response in indolent follicular lymphomas. Blood. 1998;91(8):2955-2960.
13. Apostolidis J, Gupta RK, Grenzelias D, et al. Highdose 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(3):527-536.
14. Rambaldi A, Lazzari M, Manzoni C, et al. Monitoring of minimal residual disease after CHOP and rituximab in previously untreated patients with follicular lymphoma. Blood. 2002; 99(3):856-862.
15. Ladetto M, Corradini P, Vallet S, 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(5):1559-1565.
16. Corradini P, Ladetto M, Zallio F, 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(8): 1460-1468.
17. Ghielmini M, Schmitz SF, Cogliatti SB, et al. Prolonged treatment with rituximab in patients with follicular lymphoma significantly increases event-free survival and response duration compared with the standard weekly x 4 schedule. Blood. 2004;103(12):4416-4423.
18. Rambaldi A, Carlotti E, Oldani E, et al. Quantitative PCR of bone marrow BCL2/IgH1 cells at diagnosis predicts treatment response and long-term outcome in follicular non-Hodgkin lymphoma. Blood. 2005;105(9):3428-3433.
19. Ladetto M, Vallet S, Benedetti F, et al. Prolonged survival and low incidence of late toxic sequelae in advanced follicular lymphoma treated with a TBIfree autografting program: updated results of the multicenter consecutive GITMO trial. Leukemia. 2006;20(10):1840-1847.
20. Brown JR, Feng Y, Gribben JG, et al. Long-term survival after autologous bone marrow transplantation for follicular lymphoma in first remission. Biol Blood Marrow Transplant. 2007; 13(9):1057-1065.
21. Hirt C, Schüler F, Kiefer T, et al. Rapid and sustained clearance of circulating lymphoma cells after chemotherapy plus rituximab: clinical significance of quantitative t(14;18) PCR monitoring in advanced stage follicular lymphoma patients. Br J Haematol. 2008;141(5):631-640.
22. Ladetto M, De Marco F, Benedetti F, et al; GruppoItaliano Trapianto di Midollo Osseo (GITMO); Intergruppo Italiano Linfomi (IIL). 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. 2008; 111(8):4004-4013.
23. Goff L, Summers K, Iqbal S, et al. Quantitative PCR analysis for Bcl-2/IgH in a phase III study of Yttrium-90 Ibritumomab Tiuxetan as consolidation of first remission in patients with follicular lymphoma. J Clin Oncol. 2009;27(36):6094-6100.
24. Morschhauser F, Recher C, Milpied N, et al. A 4-weekly course of rituximab is safe and improves tumor control for patients with minimal residual disease persisting 3 months after autologous hematopoietic stem-cell transplantation: results of a prospective multicenter phase II study in patients with follicular lymphoma. Ann Oncol. 2012;23(10):2687-2695.
25. Mandigers CM, Meijerink JP, Mensink EJ, et al Interzol (South-East Netherlands Comprehensive Cancer Centers Cooperative Group). Lack of correlation between numbers of circulating t(14;18)-positive cells and response to first-line treatment in follicular lymphoma. Blood. 2001; 98(4):940-944.
26. Schmitt C, Grundt A, Buchholtz C, et al. One single dose of rituximab added to a standard regimen of CHOP in primary treatment of follicular lymphoma appears to result in a high clearance rate from circulating bcl-2/IgH positive cells: Is the end of molecular monitoring near? Leuk Res. 2006;30(12):1563-1568.
27. Paszkiewicz-Kozik E, Kulik J, Fabisiewicz A, et al. Presence of t(14;18) positive cells in blood and bone marrow does not predict outcome in follicular lymphoma. Med Oncol. 2009;26(1): 16-21.
28. van Oers MH, Tönnissen E, Van Glabbeke M, et al. BCL-2/IgH polymerase chain reaction status at the end of induction treatment is not predictive for progression-free survival in relapsed/resistant follicular lymphoma: results of a prospective randomized EORTC 20981 phase III intergroup study. J Clin Oncol. 2010;28(13):2246-2252.
29. Vitolo U, Ladetto M, Boccomini C, et al. Rituximab maintenance compared with observation after brief first-line R-FND chemoimmunotherapy with rituximab consolidation in patients age older than 60 years with advanced follicular lymphoma: a phase III randomized study by the Fondazione Italiana Linfomi. J Clin Oncol. 2013;31(27): 3351-3359.
30. Cheson BD, Horning SJ, Coiffier B, et al NCI Sponsored International Working Group. Report of an international workshop to standardize response criteria for non-Hodgkin's lymphomas. J Clin Oncol. 1999;17(4):1244.
31. Voena C, Ladetto M, Astolfi M, et al. A novel nested-PCR strategy for the detection of rearranged immunoglobulin heavy-chain genes in B cell tumors. Leukemia. 1997;11(10):1793-1798.
32. Ladetto M, Sametti S, Donovan JW, et al. A validated real-time quantitative PCR approach shows a correlation between tumor burden and successful ex vivo purging in follicular lymphoma patients. Exp Hematol. 2001;29(2):183-193.
33. Ladetto M, Omedé P, Sametti S, et al. Real-time polymerase chain reaction in multiple myeloma: quantitative analysis of tumor contamination of stem cell harvests. Exp Hematol. 2002;30(6): 529-536.
34. Kluin-Nelemans HC, Limpens J, Meerabux J, et al. A new non-Hodgkin's B-cell line (DoHH2) with a chromosomal translocation t(14;18)(q32; q21). Leukemia. 1991;5(3):221-224.
35. Ladetto M, Drandi D, Compagno M, et al. PCR-detectable nonneoplastic Bcl-2/IgH rearrangements are common in normal subjects and cancer patients at diagnosis but rare in subjects treated with chemotherapy. J Clin Oncol. 2003;21(7):1398-1403.
36. Ladetto M, Mantoan B, Ricca I, et al. Recurrence of Bcl-2/IgH polymerase chain reaction positivity following a prolonged molecular remission can be unrelated to the original follicular lymphoma clone. Exp Hematol. 2003;31(9):784-788.
37. Ladetto M, Mantoan B, De Marco F, et al. Cells carrying nonlymphoma-associated bcl-2/IgH rearrangements (NLABR) are phenotypically related to follicular lymphoma and can establish as long-term persisting clonal populations. Exp Hematol. 2006;34(12):1680-1686.
38. Ladetto M, Magni M, Pagliano G, et al. Rituximab induces effective clearance of minimal residual disease in molecular relapses of mantle cell lymphoma. Biol Blood Marrow Transplant. 2006; 12(12):1270-1276.
39. van der Velden VH, Cazzaniga G, Schrauder A, et al; European Study Group on MRD detection in ALL (ESG-MRD-ALL). Analysis of minimal residual disease by Ig/TCR gene rearrangements: guidelines for interpretation of real-time quantitative PCR data. Leukemia. 2007;21(4): 604-611.
40. Royston P. Multiple imputation of missing values: update of ice. Stata J. 2005;5(4):527-536.
41. Rubin DB. Multiple Imputation for Non-Response in Surveys. New York, NY: John Wiley & Sons; 1987.
42. Boccomini C, Ladetto M, Rigacci L, et al. Brief rituximab, bendamustine, mitoxantrone (R-BM) induction followed by rituximab consolidation in elderly de novo advanced stage follicular lymphoma (FL) patients: a study by Fondazione Italiana Linfomi (FIL). In: 12th International Conference on Malignant Lymphoma, Palazzo dei Congressi; June 19-22, 2013; Lugano, Switzerland. Abstract 104.
43. Pott C, Brüggemann M, Ritgen M, van der Velden VH, van Dongen JJ, Kneba M. MRD detection in B-cell non-Hodgkin lymphomas using Ig gene rearrangements and chromosomal translocations as targets for real-time quantitative PCR. Methods Mol Biol. 2013;971:175-200.
44. Morice WG, Hanson CA, Kumar S, Frederick LA, Lesnick CE, Greipp PR. Novel multi-parameter flow cytometry sensitively detects phenotypically distinct plasma cell subsets in plasma cell proliferative disorders. Leukemia. 2007;21(9): 2043-2046.
45. Rawstron AC, Orfao A, Beksac M, et al European Myeloma Network. Report of the European Myeloma Network on multiparametric flow cytometry in multiple myeloma and related disorders. Haematologica. 2008;93(3):431-438.
46. Böttcher S, Ritgen M, Buske S, et al; EU MCL MRD Group. Minimal residual disease detection in mantle cell lymphoma: methods and significance of four-color flow cytometry compared to consensus IGH-polymerase chain reaction at initial staging and for follow-up examinations. Haematologica. 2008;93(4):551-559.
47. Faham M, Zheng J, Moorhead M, et al. Deepsequencing approach for minimal residual disease detection in acute lymphoblastic leukemia. Blood. 2012;120(26):5173-5180.
48. Ladetto M, Bruggemann M, Ferrero S, et al. Nextgeneration sequencing and real-time quantitative PCR for minimal residual disease (MRD) detection using the immunoglobulin heavy chain variable region: a methodical comparison in acute lymphoblastic leukemia (ALL), mantle cell lymphoma (MCL) and multiple myeloma (MM). ASH Annual Meeting Abstracts. 2012;120:788.
49. Trotman J, Fournier M, Lamy T, et al. Positron emission tomography-computed tomography (PET-CT) after induction therapy is highly predictive of patient outcome in follicular lymphoma: analysis of PET-CT in a subset of PRIMA trial participants. J Clin Oncol. 2011; 29(23):3194-3200.
50. Dupuis J, Berriolo-Riedinger A, Julian A, et al. Impact of [(18)F]fluorodeoxyglucose positron emission tomography response evaluation in patients with high-tumor burden follicular lymphoma treated with immunochemotherapy: a prospective study from the Groupe d'Etudes des Lymphomes de l'Adulte and GOELAMS. J Clin Oncol. 2012;30(35):4317-4322.
51. Mattsson S, Söderberg M. Radiation dose management in CT, SPECT/CT and PET/CT techniques. Radiat Prot Dosimetry. 2011; 147(1-2):13-21.
52. Eckert C, von Stackelberg A, Seeger K, et al. Minimal residual disease after induction is the strongest predictor of prognosis in intermediate risk relapsed acute lymphoblastic leukaemia - long-term results of trial ALL-REZ BFM P95/96. Eur J Cancer. 2013;49(6):1346-1355.