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Conditioning Regimens

The outcome of reduced intensity allogeneic stem cell transplantation and autologous stem cell transplantation when performed as a first transplant strategy in relapsed follicular lymphoma: an analysis from the Lymphoma Working Party of the EBMT

Bone Marrow Transplantation volume 48, pages 1409–1414 (2013)Cite this article

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Abstract

Both auto-SCT and reduced intensity allo-SCT (RIST) are employed in the treatment of relapsed follicular lymphoma (FL). We have analysed the outcome of these two transplant procedures when used as a first transplant in this setting. We conducted a retrospective comparison of 726 patients who underwent an auto-SCT and 149 who underwent a RIST as a first transplant procedure for relapsed FL as reported to the Lymphoma Working Party of the European Bone Marrow Transplant. The non-relapse mortality (NRM) was significantly worse for patients undergoing a RIST (relative risk (RR) 4.0, P<0.001). The 1-year NRM was 15% for those undergoing a RIST compared with 3% for those undergoing an auto-SCT. Disease relapse or progression were significantly worse for those receiving an auto-SCT (RR 3.1, P<0.001). Patients undergoing a RIST had a 5-year relapse rate of 20% compared with 47% for those undergoing an auto-SCT. The PFS at 5 years was 57% for patients receiving a RIST compared with 48% for those receiving an auto-SCT. There was no significant difference in OS between the two groups. RIST is associated with a higher NRM and lower relapse rate in patients with relapsed FL.

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References

  1. Schouten HC, Qian W, Kvaloy S, Porcellini A, Hagberg H, Johnsen H et al. High dose therapy improves progression-free survival and survival in relapsed follicular non-Hodgkin’s lymphoma: results from the randomised European CUP trial. J Clin Oncol 2003; 21: 3918–3927.

    Article  CAS  PubMed  Google Scholar 

  2. Montoto S, Canals C, Rohatiner AZS, Taghipour G, Sureda A, Schmitz N et al. Long term follow up of of high dose treatment with autologous haematopoietic progenitor cell support in 693 patients with follicular lymphoma: an EBMT registry study. Leukaemia 2007; 21: 2324–2331.

    Article  CAS  Google Scholar 

  3. Rohatiner AZS, Nadler L, Davies AJ, Apostolidis J, Neuberg D, Matthews J et al. Myeloablative therapy with autologous bone marrow transplantation for follicular lymphoma at the time of second or subsequent remisssion: long-term follow-up. J Clin Oncol 2007; 25: 2554–2559.

    Article  PubMed  Google Scholar 

  4. Darrington DL, Vose JM, Anderson JR, Bierman PJ, Bishop MR, Chan WC et al. Incidence and characterisation of secondary myelodysplastic syndrome and acute myelogenous leukemia following high-dosee chemoradiotherapy and autologous stem cell transplantation for lymphoid malignancies. J Clin Oncol 1994; 12: 2527–2534.

    Article  CAS  PubMed  Google Scholar 

  5. Metayer C, Curtis RE, Vose JM, Sobocinski KA, Horowitz MM, Bhatia S et al. Myelodysplastic syndrome and acute myeloid leukemia after autotransplantation for lymphoma: a multicentre case-control study. Blood 2003; 101: 2015–2023.

    Article  CAS  PubMed  Google Scholar 

  6. van Besien K, Sobocinski K, Rowlings P, Murphy SC, Armitage JO, Bishop MR et al. Allogeneic bone marrow transplantation for low grade lymphoma. Blood 1998; 92: 1832–1836.

    CAS  PubMed  Google Scholar 

  7. Peniket AJ, Ruiz de Elvira MC, Taghipour G, Cordonnier C, Gluckman E, de Witte T et al. An EBMT registry matched study of allogeneic stem cell transplants for lymphoma: allogeneic transplantation is associated with a lower relapse rate but a higher procedure-related mortality rate than autologous transplantation. Bone Marrow Transplant 2003; 31: 667–678.

    Article  CAS  PubMed  Google Scholar 

  8. van Besien K, Carreras J, Bierman PJ, Logan B, Molina A, King R et al. Unrelated donor hematopoietic cell transplantation for non-hodgkin lymphoma: long-term outcomes. Biol Blood Marrow Transplant 2009; 15: 554–563.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Khouri IF, Keating M, Korbling M, Przepiorka D, Anderlini P, O’Brien S 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. J Clin Oncol 1998; 16: 2817–2824.

    Article  CAS  PubMed  Google Scholar 

  10. Giralt S, Estey E, Albitar M, van Besien K, Rondon G, Anderlini P et al. Engraftment of allogeneic hematopoietic progenitor cells with purine analog-containing chemotherapy: harnessing graft-versus-leukemia without myeloablative therapy. Blood 1997; 89: 4531–4536.

    CAS  PubMed  Google Scholar 

  11. Khouri IF, McLaughlin P, Saliba RM, Hosing C, Korbling M, Lee MS 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Morris E, Thomson K, Craddock C, Mahendra P, Milligan D, Cook G et al. Outcome following alemtuzumab (CAMPATH-1H)-containing reduced intensity allogeneic transplant regimen for relapsed and refractory non-Hodgkin’s lymphoma (NHL). Blood 2004; 104: 3865–3871.

    Article  CAS  PubMed  Google Scholar 

  13. Rezvani AR, Storer B, Maris M, Sorror ML, Agura E, Maziarz RT et al. Nonmyeloablative allogeneic hematopoietic cell transplantation in relapsed, refractory, and transformed indolent non-Hodgkin’s lymphoma. J Clin Oncol 2008; 26: 211–217.

    Article  PubMed  Google Scholar 

  14. Vigouroux S, Michallet M, Porcher R, Attal M, Ades L, Bernard M 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.

    Article  PubMed  Google Scholar 

  15. Pinana JL, Martino R, Gayoso J, Sureda A, Serna J, Diez-Martin JL 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 multicentre trials. Haematologica 2010; 95: 1176–1182.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Laport G, Bredeson C, Tomblyn MR, Kahl BS, Goodman SA, Ewell M et al. Autologous versus reduced intensity allogeneic hematopoietic cell transplantation for patients with follicular non Hodgkin’s lymphoma beyond first complete response. J Clin Oncol 2008; 26: 15s (suppl; abstr 7041).

    Article  Google Scholar 

  17. European Bone Marrow Transplant Registry. Operational manual. http://www.ebmt.org/4Registry/Registry docs/MEDAB%20Manual.pdf.

  18. Gyan E, Foussard C, Bertrand P, Michenet P, Le Gouill S, Berthou C et al. 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 2009; 113: 995–1001.

    Article  CAS  PubMed  Google Scholar 

  19. Sebban C, Mounier N, Brousse N, Belanger C, Brice P, Haioun C et al. 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 2006; 108: 2540–2544.

    Article  CAS  PubMed  Google Scholar 

  20. Lenz G, Dreyling M, Schiegnitz E, Forstpointner R, Wandt H, Freund M 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.

    Article  CAS  PubMed  Google Scholar 

  21. Armitage JO, Carbone PP, Connors JM, Levine A, Bennett JM, Kroll S et al. Treatment-related myelodysplasia and acute leukemia in non-Hodgkin’s lymphoma patients. J Clin Oncol 2003; 21: 897–906.

    Article  PubMed  Google Scholar 

  22. Sorror ML, Maris MB, Storb R, Baron F, Sandmaier BM, Maloney DG et al. Hematopoietic cell transplantation (HCT)-specific comorbidity index: a new tool for risk assessment before allogeneic HCT. Blood 2005; 106: 2912–2919.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. van Besien K, Loberiza FR, Bajorunaite R, Armitage JO, Bashey A, Burns LJ et al. Comparison of autologous and allogeneic hematopoietic stem cell transplantation for follicular lymphoma. Blood 2003; 102: 3521–3529.

    Article  CAS  PubMed  Google Scholar 

  24. Bierman PJ, Sweetenham JW, Loberiza FM, Fausto R, Taghipour G, Lazarus HM et al. Syngeneic hematopoietic stem cell transplantation for non-Hodgkin’s lymphoma: a comparison with allogeneic and autologous transplantation. J Clin Oncol 2003; 21: 3744–3753.

    Article  PubMed  Google Scholar 

  25. Russell NH, Byrne JL, Faulkner RD, Gilyead M, Das-Gupta EP, Haynes AP . Donor lymphocyte infusions can result in sustained remissions in patients with residual or relapsed lymphoid malignancy following allogeneic haemopoietic stem cell transplantation. Bone Marrow Transplant 2005; 36: 437–441.

    Article  CAS  PubMed  Google Scholar 

  26. Mandigers CM, Verdonck LF, Meijerink JP, Dekker AW, Schaltenberg B, Raemaekers JMM . Graft-versus-lymphoma effect of donor lymphocyte infusion in indolent lymphomas relapsed after allogeneic stem cell transplantation. Bone Marrow Transplant 2003; 32: 1159–1163.

    Article  CAS  PubMed  Google Scholar 

  27. Bloor AJ, Thomson K, Chowdhry N, Verfeuth S, Ings S, Chakraverty R et al. High response rate to donor lymphocyte infusion after allogeneic stem cell transplantation for indolent non-Hodgkin lymphoma. Biol Blood Marrow Transplant 2008; 14: 50–58.

    Article  PubMed  Google Scholar 

  28. Delgado J, Canals C, Attal M, Thomson K, Campos A, Martino R et al. The role of in vivo T-cell depletion on reduced-intensity conditioning allogeneic stem cell transplantation from HLA-identical siblings in patients with follicular lymphoma. Leukemia 2010; 25: 551–555.

    Article  PubMed  Google Scholar 

  29. Branson K, Chopra R, Kottaridis PD, McQuaker G, Parker A, Schey S et al. Role of nonmyeloablative allogeneic stem-cell transplantation after failure of autologous transplantation in patients with lymphoproliferative malignancies. J Clin Oncol 2002; 20: 4022–4031.

    Article  PubMed  Google Scholar 

  30. Thomson K, Morris E, Milligan D, Parker A, Hunter AE, Cook G 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. J Clin Oncol 2010; 28: 3695–3700.

    Article  PubMed  Google Scholar 

  31. Pettengel R, Schmitz N, Gisselbrecht C, Caballero D, Colombat P, Conde E et al. Randomised study of rituximab in patients with relapsed or resistant follicular lymphoma prior to high-dose therapy as in vivo purging and to maintain remission following high-dose therapy. J Clin Oncol 2010; 28: 7s (suppl;abstr 8005).

    Article  Google Scholar 

  32. Marcus R, Imrie K, Belch A, Cunningham D, Flores E, Catalano J et al. CVP chemotherapy plus rituximab compared with CVP as first-line treatment for advanced follicular lymphoma. Blood 2005; 105: 1417–1423.

    Article  CAS  PubMed  Google Scholar 

  33. 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, vincritine, and prednisone (CHOP) significantly improves the outcome for patients with advanced-stage follicular lymphoma compared with therapy with CHOP alone: results of a prospective randomised study of the German Low-Grade Lymphoma Study Group. Blood 2005; 106: 3725–3732.

    Article  CAS  PubMed  Google Scholar 

  34. Salles GA, Seymour JF, Offner F, Lopez-Guillermo A, Belada D, Xerri L et al. Rituximab maintenance for 2 years in patients with untreated high tumour burden follicular lymphoma after response to immunochemotherapy. Lancet 2011; 377: 42–51.

    Article  CAS  PubMed  Google Scholar 

  35. van Oers MHJ, Klasa R, Marcus R, Wolf M, Kimby E, Gascoyne RD et al. Rituximab maintenance improves clinical outcome of relapsed/resistant follicular non-Hodgkin’s lymphoma in patients both with and without rituximab during induction: results of a prospective randomised phase 3 trial. Blood 2006; 108: 3295–3301.

    Article  CAS  PubMed  Google Scholar 

  36. Forstpointner R, Unterhalt M, Dreyling M, Bock H-P, Repp R, Wandt H et al. Maintenance therapy with rituximab leads to 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 study of the German Low Grade Lymphoma Study Group. Blood 2006; 108: 4003–4008.

    Article  CAS  PubMed  Google Scholar 

  37. Horning SJ, Younes A, Jain V, Kroll S, Lucas J, Podoloff D et al. Efficacy and safety of tositumumab and iodine-131 tositumumab (Bexxar) in B-cell lymphoma, progressive after rituximab. J Clin Oncol 2005; 23: 712–719.

    Article  CAS  PubMed  Google Scholar 

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Author information

Authors and Affiliations

  1. BMT Unit, Bristol Children’s Hospital, Bristol, UK

    S P Robinson

  2. Lymphoma Working Party of the EBMT, Barcelona, Spain

    C Canals

  3. Lymphoma Working Party of the EBMT, Paris, France

    J J Luang

  4. Centre Henri Becquerel, Rouen, France

    H Tilly

  5. Addendrokes Hospital, Cambridge, UK

    C Crawley

  6. Hopital A Michallon, Grenoble, France

    J Y Cahn

  7. Charles University Hospital, Prague, Czech Republic

    D Pohlreich

  8. CHU Nantes, Nantes, France

    S Le Gouill

  9. St James’s Institute of Oncology, Leeds, UK

    M Gilleece

  10. CHU Bordeaux, Pessac, France

    N Milpied

  11. Hopital de Purpan, Toulouse, France

    M Attal

  12. Centre Leon Berard, Lyon, France

    P Biron

  13. Hopital Henri Mondor, Creteil, France

    S Maury

  14. Ospedali Riuniti di Bergamo, Bergamo, Italy

    A Rambaldi

  15. University Hospital Gasthuisberg Leuven, Leuven, Belgium

    J Maertens

  16. Department of Haematology, University ‘La Sapienza’, Rome, Italy

    S Capria

  17. Hopital Bretonneau, Tours Cedex, France

    P Colombat

  18. St Bartholemews Hospital, London, UK

    S Montoto

  19. Clinical Hematology Division, Hospital Santa Creu i Sant Pau, Barcelona, Spain

    A Sureda

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Correspondence to S P Robinson.

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This study was presented at the American Society Of Hematology Annual Meeting 2008.

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Robinson, S., Canals, C., Luang, J. et al. The outcome of reduced intensity allogeneic stem cell transplantation and autologous stem cell transplantation when performed as a first transplant strategy in relapsed follicular lymphoma: an analysis from the Lymphoma Working Party of the EBMT. Bone Marrow Transplant 48, 1409–1414 (2013). https://doi.org/10.1038/bmt.2013.83

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