163
Views
0
CrossRef citations to date
0
Altmetric
Review Articles

Stem cell allografting for chronic Myeloid leukemia in the tyrosine kinase era – forgotten but not gone

&
Pages 705-714 | Received 02 Nov 2023, Accepted 29 Jan 2024, Published online: 09 Feb 2024

References

  • Hochhaus A, Baccarani M, Silver RT, et al. European LeukemiaNet 2020 recommendations for treating chronic myeloid leukemia. Leukemia. 2020;34(4):966–984. doi:10.1038/s41375-020-0776-2
  • Jabbour E, Kantarjian H. Chronic myeloid leukemia: 2020 update on diagnosis, therapy and monitoring. Am J Hematol. 2020;95(6):691–709. doi:10.1002/ajh.25792
  • Barrett AJ, Ito S. The role of stem cell transplantation for chronic myelogenous leukemia in the 21st century. Blood. 2015;125(21):3230–3235. doi:10.1182/blood-2014-10-567784
  • Gratwohl A, Brand R, Apperley J, et al. Allogeneic hematopoietic stem cell transplantation for chronic myeloid leukemia in Europe 2006: transplant activity, long-term data and current results. An analysis by the chronic leukemia working party of the european group for blood and marrow transplantation (EBMT). Haematologica. 2006;91(4):513–521.
  • Jabbour E, Cortes J, Kantarjian HM, et al. Allogeneic stem cell transplantation for patients with chronic myeloid leukemia and acute lymphocytic leukemia after bcr-abl kinase mutation–related imatinib failure. Blood. 2006;108(4):1421–1423. doi:10.1182/blood-2006-02-001933
  • Craddock CF. We do still transplant CML, don’t we? Hematology Am Soc Hematol Educ Program. 2018;2018(1):177–184. doi:10.1182/asheducation-2018.1.177
  • Kantarjian H, O’Brien S, Jabbour E, et al. Improved survival in chronic myeloid leukemia since the introduction of imatinib therapy: a single-institution historical experience. Blood. 2012;119(9):1981–1987. doi:10.1182/blood-2011-08-358135
  • Goldman J, McCarthy D, Hows J, et al. Marrow transplantation for patients in the chronic phase of chronic granulocytic leukaemia. Lancet. 1982;2(8299):623–625. doi:10.1016/s0140-6736(82)92736-2
  • Mcglave P, Kim T, Hurd D, et al. Successful allogeneic bone-marrow transplantation for patients in the accelerated phase of chronic granulocytic leukaemia. Lancet. 1982;2(8299):625–627. doi:10.1016/s0140-6736(82)92737-4
  • Clift R, Thomas E, Fefer A, et al. Treatment of chronic granulocytic leukaemia in chronic phase by allogeneic marrow transplantation. Lancet. 1982;2(8299):621–623. doi:10.1016/s0140-6736(82)92735-0
  • Goldman JM, Gale RP, Horowitz MM, et al. Bone marrow transplantation for chronic myelogenous leukemia in chronic phase. Increased risk for relapse associated with T-cell depletion. Ann Intern Med. 1988;108(6):806–814. doi:10.7326/0003-4819-108-6-806
  • Pavlu J, Szydlo RM, Goldman JM, et al. Three decades of transplantation for chronic myeloid leukemia: what have we learned? Blood. 2011;117(3):755–763. doi:10.1182/blood-2010-08-301341
  • Goldman JM. Allogeneic stem cell transplantation for chronic myeloid leukemia–status in 2007. Bone Marrow Transplant. 2008;42 Suppl 1(S1):S11–S13. doi:10.1038/bmt.2008.105
  • Horowitz MM, Gale RP, Sondel PM, et al. Graft-versus-leukemia reactions after. Bone Marrow Transplant. 1990;6 Suppl 1:94–97.
  • Kolb H, Schattenberg A, Goldman J, et al. Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients. European group for blood and marrow transplantation working party chronic leukemia [see comments]. Blood. 1995;86(5):2041–2050. doi:10.1182/blood.V86.5.2041.bloodjournal8652041
  • McSweeney PA, Niederwieser D, Shizuru JA, et al. Hematopoietic cell transplantation in older patients with hematologic malignancies: replacing high-dose cytotoxic therapy with graft-versus-tumor effects. Blood. 2001;97(11):3390–3400. doi:10.1182/blood.v97.11.3390
  • Chhabra S, Ahn KW, Hu ZH, et al. Myeloablative vs reduced-intensity conditioning allogeneic hematopoietic cell transplantation for chronic myeloid leukemia. Blood Adv. 2018;2(21):2922–2936. doi:10.1182/bloodadvances.2018024844
  • Kantarjian H, Pasquini R, Hamerschlak N, et al. Dasatinib or high-dose imatinib for chronic-phase chronic myeloid leukemia after failure of first-line imatinib: a randomized phase 2 trial. Blood. 2007;109(12):5143–5150. doi:10.1182/blood-2006-11-056028
  • Kantarjian HM, Giles FJ, Bhalla KN, et al. Nilotinib is effective in patients with chronic myeloid leukemia in chronic phase after imatinib resistance or intolerance: 24-month follow-up results. Blood. 2011;117(4):1141–1145. doi:10.1182/blood-2010-03-277152
  • Kantarjian HM, Cortes JE, Kim DW, et al. Bosutinib safety and management of toxicity in leukemia patients with resistance or intolerance to imatinib and other tyrosine kinase inhibitors. Blood. 2014;123(9):1309–1318. doi:10.1182/blood-2013-07-513937
  • Hughes TP, Mauro MJ, Cortes JE, et al. Asciminib in chronic myeloid leukemia after ABL kinase inhibitor failure. N Engl J Med. 2019;381(24):2315–2326. doi:10.1056/NEJMoa1902328
  • Nicolini FE, Basak GW, Kim DW, et al. Overall survival with ponatinib versus allogeneic stem cell transplantation in philadelphia chromosome-positive leukemias with the T315I mutation. Cancer. 2017;123(15):2875–2880. doi:10.1002/cncr.30558
  • Cortes JE, Kim DW, Pinilla-Ibarz J, et al. Ponatinib efficacy and safety in philadelphia chromosome-positive leukemia: final 5-year results of the phase 2 PACE trial. Blood. 2018;132(4):393–404. doi:10.1182/blood-2016-09-739086
  • Lokeshwar N, Kumar L, Kumari M. Severe bone marrow aplasia following imatinib mesylate in a patient with chronic myelogenous leukemia. Leuk Lymphoma. 2005;46(5):781–784. doi:10.1080/10428190500046778
  • Song M-K, Choi Y-J, Seol Y-M, et al. Nilotinib-induced bone marrow aplasia. Eur J Haematol. 2009;83(2):161–162. doi:10.1111/j.1600-0609.2009.01269.x
  • Saussele S, Lauseker M, Gratwohl A, et al. Allogeneic hematopoietic stem cell transplantation (allo SCT) for chronic myeloid leukemia in the imatinib era: evaluation of its impact within a subgroup of the randomized german CML study IV. Blood. 2010;115(10):1880–1885. doi:10.1182/blood-2009-08-237115
  • Crawley C, Szydlo R, Lalancette M, et al. Outcomes of reduced-intensity transplantation for chronic myeloid leukemia: an analysis of prognostic factors from the chronic leukemia working party of the EBMT. Blood. 2005;106(9):2969–2976. doi:10.1182/blood-2004-09-3544
  • Warlick E, Ahn KW, Pedersen TL, et al. Reduced intensity conditioning is superior to nonmyeloablative conditioning for older chronic myelogenous leukemia patients undergoing hematopoietic cell transplant during the tyrosine kinase inhibitor era. Blood. 2012;119(17):4083–4090. doi:10.1182/blood-2012-02-409763
  • Palandri F, Castagnetti F, Testoni N, et al. Chronic myeloid leukemia in blast crisis treated with imatinib 600 mg: outcome of the patients alive after a 6-year follow-up. Haematologica. 2008;93(12):1792–1796. doi:10.3324/haematol.13068
  • Nicolini FE, Masszi T, Shen Z, et al. Expanding nilotinib access in clinical trials (ENACT), an open-label multicenter study of oral nilotinib in adult patients with imatinib-resistant or -intolerant chronic myeloid leukemia in accelerated phase or blast crisis. Leuk Lymphoma. 2012;53(5):907–914. doi:10.3109/10428194.2011.627480
  • Saglio G, Hochhaus A, Goh YT, et al. Dasatinib in imatinib‐resistant or imatinib‐intolerant chronic myeloid leukemia in blast phase after 2 years of follow‐up in a phase 3 study: efficacy and tolerability of 140 milligrams once daily and 70 milligrams twice daily. Cancer. 2010;116(16):3852–3861. doi:10.1002/cncr.25123
  • Giles F, Kantarjian H, Le Coutre P, et al. Nilotinib is effective in imatinib-resistant or-intolerant patients with chronic myeloid leukemia in blastic phase. Leukemia. 2012;26(5):959–962. doi:10.1038/leu.2011.355
  • Jiang Q, Xu L-P, Liu D-H, et al. Imatinib mesylate versus allogeneic hematopoietic stem cell transplantation for patients with chronic myelogenous leukemia in the accelerated phase. Blood. 2011;117(11):3032–3040. doi:10.1182/blood-2010-09-308510
  • Silver RT, Cortes J, Waltzman R, et al. Sustained durability of responses and improved progression-free and overall survival with imatinib treatment for accelerated phase and blast crisis chronic myeloid leukemia: long-term follow-up of the STI571 0102 and 0109 trials. Haematologica. 2009;94(5):743–744. doi:10.3324/haematol.2009.006999
  • Phelan R, Arora M, Chen M. Current use and outcome of hematopoietic stem cell transplantation: CIBMTR US summary slides. 2020.
  • Hehlmann R, Saußele S, Voskanyan A, et al. Management of CML-blast crisis. Best Pract Res Clin Haematol. 2016;29(3):295–307. doi:10.1016/j.beha.2016.10.005
  • Milojkovic D, Ibrahim A, Reid A, et al. Efficacy of combining dasatinib and FLAG-IDA for patients with chronic myeloid leukemia in blastic transformation. Haematologica. 2012;97(3):473–474. doi:10.3324/haematol.2011.057513
  • Jain P, Kantarjian HM, Ghorab A, et al. Prognostic factors and survival outcomes in patients with chronic myeloid leukemia in blast phase in the tyrosine kinase inhibitor era: Cohort study of 477 patients. Cancer. 2017;123(22):4391–4402. doi:10.1002/cncr.30864
  • Rea D, Legros L, Raffoux E, et al. High-dose imatinib mesylate combined with vincristine and dexamethasone (DIV regimen) as induction therapy in patients with resistant philadelphia-positive acute lymphoblastic leukemia and lymphoid blast crisis of chronic myeloid leukemia. Leukemia. 2006;20(3):400–403. doi:10.1038/sj.leu.2404115
  • Strati P, Kantarjian H, Thomas D, et al. HCVAD plus imatinib or dasatinib in lymphoid blastic phase chronic myeloid leukemia. Cancer. 2014;120(3):373–380. doi:10.1002/cncr.28433
  • Sasaki K, Jabbour EJ, Ravandi F, et al. Hyper-CVAD plus ponatinib versus hyper-CVAD plus dasatinib as frontline therapy for patients with philadelphia chromosome-positive acute lymphoblastic leukemia: a propensity score analysis. Cancer. 2016;122(23):3650–3656. doi:10.1002/cncr.30231
  • Jiang H, Xu LP, Liu DH, et al. Allogeneic hematopoietic SCT in combination with tyrosine kinase inhibitor treatment compared with TKI treatment alone in CML blast crisis. Bone Marrow Transplant. 2014;49(9):1146–1154. doi:10.1038/bmt.2014.146
  • Hochhaus A, Breccia M, Saglio G, et al. Expert opinion-management of chronic myeloid leukemia after resistance to second-generation tyrosine kinase inhibitors. Leukemia. 2020;34(6):1495–1502. doi:10.1038/s41375-020-0842-9
  • Ohanian M, Kantarjian HM, Quintas-Cardama A, et al. Tyrosine kinase inhibitors as initial therapy for patients with chronic myeloid leukemia in accelerated phase. Clin Lymphoma Myeloma Leuk. 2014;14(2):155–162.e1. doi:10.1016/j.clml.2013.08.008
  • Sorror ML, Maris MB, Storb R, et al. Hematopoietic cell transplantation (HCT)-specific comorbidity index: a new tool for risk assessment before allogeneic HCT. Blood. 2005;106(8):2912–2919. doi:10.1182/blood-2005-05-2004
  • Shimazu Y, Murata M, Kondo T, et al. The new generation tyrosine kinase inhibitor improves the survival of chronic myeloid leukemia patients after allogeneic stem cell transplantation. Hematol Oncol. 2022;40(3):442–456. doi:10.1002/hon.3000
  • Oehler VG, Gooley T, Snyder DS, et al. The effects of imatinib mesylate treatment before allogeneic transplantation for chronic myeloid leukemia. Blood. 2007;109(4):1782–1789. doi:10.1182/blood-2006-06-031682
  • Deininger M, Schleuning M, Greinix H, et al. The effect of prior exposure to imatinib on transplant-related mortality. Haematologica. 2006;91(4):452–459.
  • Lee SJ, Kukreja M, Wang T, et al. Impact of prior imatinib mesylate on the outcome of hematopoietic cell transplantation for chronic myeloid leukemia. Blood. 2008;112(8):3500–3507. doi:10.1182/blood-2008-02-141689
  • Khoury HJ, Kukreja M, Goldman JM, et al. Prognostic factors for outcomes in allogeneic transplantation for CML in the imatinib era: a CIBMTR analysis. Bone Marrow Transplant. 2012;47(6):810–816. doi:10.1038/bmt.2011.194
  • Breccia M, Palandri F, Iori AP, et al. Second-generation tyrosine kinase inhibitors before allogeneic stem cell transplantation in patients with chronic myeloid leukemia resistant to imatinib. Leuk Res. 2010;34(2):143–147. doi:10.1016/j.leukres.2009.04.036
  • Innes AJ, Milojkovic D, Apperley JF. Allogeneic transplantation for CML in the TKI era: striking the right balance. Nat Rev Clin Oncol. 2016;13(2):79–91. doi:10.1038/nrclinonc.2015.193
  • Or R, Shapira MY, Resnick I, et al. Nonmyeloablative allogeneic stem cell transplantation for the treatment of chronic myeloid leukemia in first chronic phase. Blood. 2003;101(2):441–445. doi:10.1182/blood-2002-02-0535
  • Kerbauy FR, Storb R, Hegenbart U, et al. Hematopoietic cell transplantation from HLA-identical sibling donors after low-dose radiation-based conditioning for treatment of CML. Leukemia. 2005;19(6):990–997. doi:10.1038/sj.leu.2403730
  • Kebriaei P, Detry MA, Giralt S, et al. Long-term follow-up of allogeneic hematopoietic stem-cell transplantation with reduced-intensity conditioning for patients with chronic myeloid leukemia. Blood. 2007;110(9):3456–3462. doi:10.1182/blood-2007-04-085969
  • Das M, Saikia TK, Advani SH, et al. Use of a reduced-intensity conditioning regimen for allogeneic transplantation in patients with chronic myeloid leukemia. Bone Marrow Transplant. 2003;32(2):125–129. doi:10.1038/sj.bmt.1704107
  • Negrin RS. Graft-versus-host disease versus graft-versus-leukemia. Hematology Am Soc Hematol Educ Program. 2015;2015(1):225–230. doi:10.1182/asheducation-2015.1.225
  • Soiffer RJ, Kim HT, McGuirk J, et al. Prospective, randomized, Double-Blind, phase III clinical trial of anti-T-lymphocyte globulin to assess impact on chronic graft-versus-Host disease-free survival in patients undergoing HLA-Matched unrelated myeloablative hematopoietic cell transplantation. J Clin Oncol. 2017;35(36):4003–4011. doi:10.1200/JCO.2017.75.8177
  • Poiré X, Artz A, Larson RA, et al. Allogeneic stem cell transplantation with alemtuzumab-based conditioning for patients with advanced chronic myelogenous leukemia. Leuk Lymphoma. 2009;50(1):85–91. doi:10.1080/10428190802626624
  • Dazzi F, Szydlo RM, Craddock C, et al. Comparison of single-dose and escalating-dose regimens of donor lymphocyte infusion for relapse after allografting for chronic myeloid leukemia. Blood. 2000;95(1):67–71. doi:10.1182/blood.V95.1.67
  • Olavarria E, Ottmann OG, Deininger M, et al. Response to imatinib in patients who relapse after allogeneic stem cell transplantation for chronic myeloid leukemia. Leukemia. 2003;17(9):1707–1712. doi:10.1038/sj.leu.2403068
  • Weisser M, Tischer J, Schnittger S, et al. A comparison of donor lymphocyte infusions or imatinib mesylate for patients with chronic myelogenous leukemia who have relapsed after allogeneic stem cell transplantation. Haematologica. 2006;91(5):663–666.
  • Kanakry CG, Tsai H-L, Bolaños-Meade J, et al. Single-agent GVHD prophylaxis with posttransplantation cyclophosphamide after myeloablative, HLA-matched BMT for AML, ALL, and MDS. Blood. 2014;124(25):3817–3827. doi:10.1182/blood-2014-07-587477
  • Luznik L, O'Donnell PV, Symons HJ, et al. HLA-haploidentical bone marrow transplantation for hematologic malignancies using nonmyeloablative conditioning and high-dose, posttransplantation cyclophosphamide. Biol Blood Marrow Transplant. 2008;14(6):641–650. doi:10.1016/j.bbmt.2008.03.005
  • Solomon SR, Solh M, Morris LE, et al. Myeloablative conditioning with PBSC grafts for T cell-Replete haploidentical donor transplantation using posttransplant cyclophosphamide. Adv Hematol. 2016;2016:9736564–9736567. doi:10.1155/2016/9736564
  • Kaeda J, O'Shea D, Szydlo RM, et al. Serial measurement of BCR-ABL transcripts in the peripheral blood after allogeneic stem cell transplantation for chronic myeloid leukemia: an attempt to define patients who may not require further therapy. Blood. 2006;107(10):4171–4176. doi:10.1182/blood-2005-08-3320
  • Arpinati M, Tolomelli G, Bochicchio MT, et al. Molecular monitoring of BCR-ABL transcripts after allogeneic stem cell transplantation for chronic myeloid leukemia. Biol Blood Marrow Transplant. 2013;19(5):735–740. doi:10.1016/j.bbmt.2013.01.007
  • Goldman JM, Majhail NS, Klein JP, et al. Relapse and late mortality in 5-year survivors of myeloablative allogeneic hematopoietic cell transplantation for chronic myeloid leukemia in first chronic phase. J Clin Oncol. 2010;28(11):1888–1895. doi:10.1200/JCO.2009.26.7757
  • Dazzi F, Szydlo RM, Cross NC, et al. Durability of responses following donor lymphocyte infusions for patients who relapse after allogeneic stem cell transplantation for chronic myeloid leukemia. Blood. 2000;96(8):2712–2716. doi:10.1182/blood.V96.8.2712
  • Chalandon Y, Passweg JR, Schmid C, et al. Outcome of patients developing GVHD after DLI given to treat CML relapse: a study by the chronic leukemia working party of the EBMT. Bone Marrow Transplant. 2010;45(3):558–564. doi:10.1038/bmt.2009.177
  • Savani BN, Montero A, Kurlander R, et al. Imatinib synergizes with donor lymphocyte infusions to achieve rapid molecular remission of CML relapsing after allogeneic stem cell transplantation. Bone Marrow Transplant. 2005;36(11):1009–1015. doi:10.1038/sj.bmt.1705167
  • Olavarria E, Siddique S, Griffiths MJ, et al. Posttransplantation imatinib as a strategy to postpone the requirement for immunotherapy in patients undergoing reduced-intensity allografts for chronic myeloid leukemia. Blood. 2007;110(13):4614–4617. doi:10.1182/blood-2007-04-082990
  • Carpenter PA, Snyder DS, Flowers ME, et al. Prophylactic administration of imatinib after hematopoietic cell transplantation for high-risk philadelphia chromosome-positive leukemia. Blood. 2007;109(7):2791–2793. doi:10.1182/blood-2006-04-019836
  • Nakasone H, Kanda Y, Takasaki H, et al. Prophylactic impact of imatinib administration after allogeneic stem cell transplantation on the incidence and severity of chronic graft versus host disease in patients with philadelphia chromosome-positive leukemia. Leukemia. 2010;24(6):1236–1239. doi:10.1038/leu.2010.83
  • DeFilipp Z, Ancheta R, Liu Y, et al. Maintenance tyrosine kinase inhibitors following allogeneic hematopoietic stem cell transplantation for chronic myelogenous leukemia: a center for international blood and marrow transplant research study. Biol Blood Marrow Transplant. 2020;26(3):472–479. doi:10.1016/j.bbmt.2019.10.017
  • Brissot E, Labopin M, Beckers MM, et al. Tyrosine kinase inhibitors improve long-term outcome of allogeneic hematopoietic stem cell transplantation for adult patients with philadelphia chromosome positive acute lymphoblastic leukemia. Haematologica. 2015;100(3):392–399. doi:10.3324/haematol.2014.116954
  • Saini N, Marin D, Ledesma C, et al. Impact of TKIs post–allogeneic hematopoietic cell transplantation in philadelphia chromosome–positive ALL. Blood. 2020;136(15):1786–1789. doi:10.1182/blood.2019004685
  • Warraich Z, Tenneti P, Thai T, et al. Relapse prevention with tyrosine kinase inhibitors after allogeneic transplantation for philadelphia chromosome–positive acute lymphoblast leukemia: a systematic review. Biol Blood Marrow Transplant. 2020;26(3):e55–e64. doi:10.1016/j.bbmt.2019.09.022
  • Lipton JH. The expanding CML treatment landscape: an introspective commentary. Blood Cancer J. 2023;13(1):145. doi:10.1038/s41408-023-00918-3
  • Godara A, Siddiqui NS, Munigala S, et al. Length of stay and hospital costs for patients undergoing allogeneic stem-cell transplantation. J Clin Oncol Oncol Pract. 2021;17(3):e355–e68. doi:10.1200/OP.20.00170
  • Ruiz-Argüelles GJ, Tarin-Arzaga LC, Gonzalez-Carrillo ML, et al. Therapeutic choices in patients with Ph-positive CML living in Mexico in the tyrosine kinase inhibitor era: SCT or TKIs? Bone Marrow Transplant. 2008;42(1):23–28. doi:10.1038/bmt.2008.90

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.