Three decades of transplantation for chronic myeloid leukemia: what have we learned?

Last year marked 30 years of hematopoietic stem cell transplantation as a curative treatment of chronic myeloid leukemia (CML). Initially studies used stem cells from identical twins but techniques rapidly developed to use cells first from HLA-identical siblings and later unrelated donors. During the 1990s CML became the most frequent indication for allogeneic transplantation worldwide. This, together with the relative biologic homogeneity of CML in chronic phase, its responsiveness to graft-versus-leukemia effect and the ability to monitor low level residual disease placed CML at the forefront of research into different strategies of stem cell transplantation. The introduction of BCR-ABL1 tyrosine kinase inhibitors during the last decade resulted in long-term disease control in the majority of patients with CML. In those who fail to respond and/or develop intolerance to these agents, transplantation remains an effective therapeutic solution. The combination of tyrosine kinase inhibitors with transplantation is an exciting new strategy and it provides inspiration for similar approaches in other malignancies.

[1]  Krishna Komanduri,et al.  Maintenance therapy with low‐dose azacitidine after allogeneic hematopoietic stem cell transplantation for recurrent acute myelogenous leukemia or myelodysplastic syndrome , 2010, Cancer.

[2]  M. Brenner,et al.  Cellular immunotherapy of cancer. , 2010, Methods in molecular biology.

[3]  M. Sanz,et al.  Single-unit umbilical cord blood transplantation from unrelated donors in adult patients with chronic myelogenous leukemia. , 2010, Biology of blood and marrow transplantation : journal of the American Society for Blood and Marrow Transplantation.

[4]  J. Sanz,et al.  Umbilical cord blood transplantation from unrelated donors in adult patients with chronic myeloid leukaemia. , 2010, Best practice & research. Clinical haematology.

[5]  Katayoun Rezvani,et al.  Optimizing patient selection for myeloablative allogeneic hematopoietic cell transplantation in chronic myeloid leukemia in chronic phase. , 2010, Blood.

[6]  J. Klein,et al.  Relapse and late mortality in 5-year survivors of myeloablative allogeneic hematopoietic cell transplantation for chronic myeloid leukemia in first chronic phase. , 2010, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[7]  Martin C. Müller,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. , 2010, Blood.

[8]  S. Iacobelli,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 , 2010, Bone Marrow Transplantation.

[9]  D. Marin,et al.  Early prediction of success or failure of treatment with second-generation tyrosine kinase inhibitors in patients with chronic myeloid leukemia , 2010, Haematologica.

[10]  J. Radich,et al.  Chronic myeloid leukemia: an update of concepts and management recommendations of European LeukemiaNet. , 2009, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[11]  Z. Estrov,et al.  The use of nilotinib or dasatinib after failure to 2 prior tyrosine kinase inhibitors: long-term follow-up. , 2009, Blood.

[12]  R. Brand,et al.  Risk score for outcome after allogeneic hematopoietic stem cell transplantation , 2009, Cancer.

[13]  N. Cross Standardisation of molecular monitoring for chronic myeloid leukaemia. , 2009, Best practice & research. Clinical haematology.

[14]  R. Silver The blast phase of chronic myeloid leukaemia. , 2009, Best practice & research. Clinical haematology.

[15]  K. Rezvani,et al.  Immunotherapy: Can we include vaccines with stem-cell transplantation? , 2009, Nature Reviews Clinical Oncology.

[16]  J. Cayuela,et al.  Sustained major molecular response in the absence of any antileukaemic therapy after dasatinib treatment and autologous peripheral blood stem cell transplantation in a patient with imatinib-resistant myeloblastic-phase chronic myeloid leukaemia , 2009, Leukemia.

[17]  K. Rezvani,et al.  European LeukemiaNet criteria for failure or suboptimal response reliably identify patients with CML in early chronic phase treated with imatinib whose eventual outcome is poor. , 2008, Blood.

[18]  A. Zander,et al.  Impact of prior imatinib mesylate on the outcome of hematopoietic cell transplantation for chronic myeloid leukemia. , 2008, Blood.

[19]  H. Kantarjian,et al.  Failure to achieve a major cytogenetic response by 12 months defines inadequate response in patients receiving nilotinib or dasatinib as second or subsequent line therapy for chronic myeloid leukemia. , 2008, Blood.

[20]  Jaspal Kaeda,et al.  Imatinib for newly diagnosed patients with chronic myeloid leukemia: incidence of sustained responses in an intention-to-treat analysis. , 2008, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[21]  H. Azuma,et al.  Unrelated cord blood transplantation in CML: Japan Cord Blood Bank Network analysis , 2008, Bone Marrow Transplantation.

[22]  C. Craddock,et al.  Posttransplantation imatinib as a strategy to postpone the requirement for immunotherapy in patients undergoing reduced-intensity allografts for chronic myeloid leukemia. , 2007, Blood.

[23]  Francisco Cervantes,et al.  Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. , 2006, The New England journal of medicine.

[24]  M. Copland,et al.  Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. , 2006, Blood.

[25]  D. Marin,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. , 2006, Blood.

[26]  A. Barrett,et al.  Imatinib synergizes with donor lymphocyte infusions to achieve rapid molecular remission of CML relapsing after allogeneic stem cell transplantation , 2005, Bone Marrow Transplantation.

[27]  J. Sierra,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. , 2005, Blood.

[28]  M. Sorror,et al.  Hematopoietic cell transplantation (HCT)-specific comorbidity index: a new tool for risk assessment before allogeneic HCT. , 2005, Blood.

[29]  J. Cahn Clinical bone marrow and blood stem cell transplantation , 2004, Leukemia.

[30]  John P Klein,et al.  Validation and extension of the EBMT Risk Score for patients with chronic myeloid leukaemia (CML) receiving allogeneic haematopoietic stem cell transplants , 2004, British journal of haematology.

[31]  D. Zahrieh,et al.  Comparison of T-cell-depleted and non-T-cell-depleted unrelated donor transplantation for hematologic diseases: clinical outcomes, quality of life, and costs. , 2002, Blood.

[32]  B. Horisberger,et al.  Current trends in hematopoietic stem cell transplantation in Europe. , 2002, Blood.

[33]  J. Wagner,et al.  Equivalent outcomes in patients with chronic myelogenous leukemia after early transplantation of phenotypically matched bone marrow from related or unrelated donors. , 2001, The American journal of medicine.

[34]  C. Craddock,et al.  Early detection of BCR-ABL transcripts by quantitative reverse transcriptase-polymerase chain reaction predicts outcome after allogeneic stem cell transplantation for chronic myeloid leukemia. , 2001, Blood.

[35]  C. Craddock,et al.  Cytomegalovirus seropositivity adversely influences outcome after T‐depleted unrelated donor transplant in patients with chronic myeloid leukaemia: the case for tailored graft‐versus‐host disease prophylaxis , 2001, British journal of haematology.

[36]  Mark M. Davis,et al.  Evidence that specific T lymphocytes may participate in the elimination of chronic myelogenous leukemia , 2000, Nature Medicine.

[37]  C. Geary The story of chronic myeloid leukaemia , 2000, British journal of haematology.

[38]  P. Piccaluga,et al.  Second chronic phase before transplantation is crucial for improving survival of blastic phase chronic myeloid leukaemia , 2000, British journal of haematology.

[39]  W. M. Smit,et al.  Complete remission of accelerated phase chronic myeloid leukemia by treatment with leukemia-reactive cytotoxic T lymphocytes. , 1999, Blood.

[40]  J. Ritz,et al.  Comparative outcomes of T-cell-depleted and non-T-cell-depleted allogeneic bone marrow transplantation for chronic myelogenous leukemia: impact of donor lymphocyte infusion. , 1999, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[41]  J Hermans,et al.  Risk assessment for patients with chronic myeloid leukaemia before allogeneic blood or marrow transplantation , 1998, The Lancet.

[42]  Schaap,et al.  Quantitation of minimal residual disease in Philadelphia chromosome positive chronic myeloid leukaemia patients using real‐time quantitative RT‐PCR , 1998, British journal of haematology.

[43]  E. Estey,et al.  Engraftment of allogeneic hematopoietic progenitor cells with purine analog-containing chemotherapy: harnessing graft-versus-leukemia without myeloablative therapy. , 1997, Blood.

[44]  B. Bär,et al.  Survival in first or second remission after lymphocyte-depleted transplantation for Philadelphia chromosome-positive CML in first chronic phase , 1997, Bone Marrow Transplantation.

[45]  C. Dunbar,et al.  CD34+ cell dose predicts survival, posttransplant morbidity, and rate of hematologic recovery after allogeneic marrow transplants for hematologic malignancies , 1996 .

[46]  K. Parker,et al.  Targeted T-cell therapy for human leukemia: cytotoxic T lymphocytes specific for a peptide derived from proteinase 3 preferentially lyse human myeloid leukemia cells. , 1996, Blood.

[47]  V. Barbu,et al.  Cord-blood transplantation from an unrelated donor in an adult with chronic myelogenous leukemia. , 1996, The New England journal of medicine.

[48]  S. Mackinnon,et al.  Adoptive immunotherapy evaluating escalating doses of donor leukocytes for relapse of chronic myeloid leukemia after bone marrow transplantation: separation of graft-versus-leukemia responses from graft-versus-host disease. , 1995, Blood.

[49]  A. Deisseroth,et al.  Autologous transplants for chronic myelogenous leukaemia: results from eight transplant groups , 1994, The Lancet.

[50]  G. Hale,et al.  Control of graft-versus-host disease and graft rejection by T cell depletion of donor and recipient with Campath-1 antibodies. Results of matched sibling transplants for malignant diseases. , 1994, Bone marrow transplantation.

[51]  A. Chase,et al.  Competitive polymerase chain reaction to estimate the number of BCR-ABL transcripts in chronic myeloid leukemia patients after bone marrow transplantation. , 1993, Blood.

[52]  P. Riches,et al.  Who pioneered the use of alternative donors (and stem cells from peripheral blood) in bone marrow transplantation? , 1991, Archives of disease in childhood.

[53]  G. Saglio,et al.  Therapy of acute phase chronic myelogenous leukemia with intensive chemotherapy, blood cell autotransplant and cyclosporine A. , 1991, Leukemia.

[54]  G. Morgan,et al.  Detection of residual leukemia after bone marrow transplant for chronic myeloid leukemia: role of polymerase chain reaction in predicting relapse. , 1991, Blood.

[55]  S. Mackinnon,et al.  Bone marrow transplantation for chronic myeloid leukemia: the use of histocompatible unrelated volunteer donors. , 1990, Experimental hematology.

[56]  A. Rimm,et al.  Graft-versus-leukemia reactions after bone marrow transplantation. , 1990, Blood.

[57]  H. Deeg,et al.  Methotrexate and cyclosporine versus cyclosporine alone for prophylaxis of graft-versus-host disease in patients given HLA-identical marrow grafts for leukemia: long-term follow-up of a controlled trial. , 1989, Blood.

[58]  S. Smith,et al.  Diagnosis of chronic myeloid and acute lymphocytic leukemias by detection of leukemia-specific mRNA sequences amplified in vitro. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[59]  E. Scott,et al.  Unrelated donor bone marrow transplantation therapy for chronic myelogenous leukemia. , 1987, Blood.

[60]  A. Gratwohl,et al.  European experience of bone marrow transplantation for leukemia. , 1987, Transplantation proceedings.

[61]  Apperley,et al.  Histocompatible unrelated volunteer donors compared with HLA nonidentical family donors in marrow transplantation for aplastic anemia and leukemia. , 1986, Blood.

[62]  R. Marcus,et al.  Bone marrow transplantation for patients with chronic myeloid leukaemia: T-cell depletion with Campath-1 reduces the incidence of graft-versus-host disease but may increase the risk of leukaemic relapse. , 1986, Bone marrow transplantation.

[63]  N. Wareham,et al.  Chemotherapy and autografting for chronic granulocytic leukaemia in transformation: probable prolongation of survival for some patients , 1984, British journal of haematology.

[64]  G. Hale,et al.  ELIMINATION OF GRAFT-VERSUS-HOST DISEASE BY IN-VITRO DEPLETION OF ALLOREACTIVE LYMPHOCYTES WITH A MONOCLONAL RAT ANTI-HUMAN LYMPHOCYTE ANTIBODY (CAMPATH-1) , 1984, The Lancet.

[65]  C. Eaves,et al.  Cytogenetic studies of early myeloid progenitor compartments in Ph1- positive chronic myeloid leukemia. II. Long-term culture reveals the persistence of Ph1-negative progenitors in treated as well as newly diagnosed patients , 1984 .

[66]  A. Rimm,et al.  ALLOGENEIC BONE-MARROW TRANSPLANTATION FOR CHRONIC MYELOGENOUS LEUKAEMIA , 1984, The Lancet.

[67]  A. Gratwohl,et al.  Allogeneic marrow transplantation for chronic granulocytic leukemia , 1982, Blut.

[68]  R. Gale,et al.  Allogeneic bone marrow transplantation for chronic myelogenous leukemia in chronic or accelerated phase , 1982 .

[69]  E. Gordon-Smith,et al.  Bone-marrow transplantation for severe aplastic anaemia using histocompatible unrelated volunteer donors. , 1982, British medical journal.

[70]  D. Catovsky,et al.  MARROW TRANSPLANTATION FOR PATIENTS IN THE CHRONIC PHASE OF CHRONIC GRANULOCYTIC LEUKAEMIA , 1982, The Lancet.

[71]  D. Arthur,et al.  SUCCESSFUL ALLOGENEIC BONE-MARROW TRANSPLANTATION FOR PATIENTS IN THE ACCELERATED PHASE OF CHRONIC GRANULOCYTIC LEUKAEMIA , 1982, The Lancet.

[72]  P. Neiman,et al.  TREATMENT OF CHRONIC GRANULOCYTIC LEUKAEMIA IN CHRONIC PHASE BY ALLOGENEIC MARROW TRANSPLANTATION , 1982, The Lancet.

[73]  G. Janossy,et al.  USE OF ANTI-T-CELL MONOCLONAL ANTIBODY OKT3 TO PREVENT ACUTE GRAFT-VERSUS-HOST DISEASE IN ALLOGENEIC BONE-MARROW TRANSPLANTATION FOR ACUTE LEUKAEMIA , 1982, The Lancet.

[74]  R. Storb,et al.  Allogeneic bone marrow transplantation for chronic granulocytic leukemia. , 1981, Experimental hematology.

[75]  P. Burke,et al.  Successful engraftment of blood derived normal hemopoietic stem cells in chronic myelogenous leukemia. , 1981, Experimental hematology.

[76]  C. Scaroni,et al.  ADDITION OF HEPATITIS-B IMMUNOGLOBULIN TO CLOTTING FACTORS , 1980, The Lancet.

[77]  R. Storb,et al.  Transplantation of marrow from an unrelated donor to a patient with acute leukemia. , 1980, The New England journal of medicine.

[78]  D. Catovsky,et al.  Cryopreserved peripheral blood cells functioning as autografts in patients with chronic granulocytic leukaemia in transformation. , 1979, British medical journal.

[79]  R. Storb,et al.  Antileukemic effect of graft-versus-host disease in human recipients of allogeneic-marrow grafts. , 1979, The New England journal of medicine.

[80]  R. Chaganti,et al.  Results of treatment of Ph'+ chronic myelogenous leukemia with an intensive treatment regimen (L-5 protocol). , 1979, Blood.

[81]  R. Storb,et al.  Disappearance of Ph1-positive cells in four patients with chronic granulocytic leukemia after chemotherapy, irradiation and marrow transplantation from an identical twin. , 1979, The New England journal of medicine.

[82]  G. Sale,et al.  Treatment of chronic granulocytic leukemia by chemotherapy, total body irradiation and allogeneic bone marrow transplantation. , 1978, Experimental hematology.

[83]  T. Ruutu,et al.  Collection, Cryopreservation and Subsequent Viability of Haemopoietic Stem Cells Intended for Treatment of Chronic Granulocytic Leukaemia in Blast‐Cell Transformation , 1978, British journal of haematology.

[84]  D. Peakman,et al.  REMISSION OF RELAPSED LEUKÆMIA DURING A GRAFT-VERSUS-HOST REACTION A "GRAFT-VERSUS-LEUKÆMIA REACTION" IN MAN? , 1978, The Lancet.

[85]  N. Bersch,et al.  Chromosomal mosaicism associated with prolonged remission in chronic myelogenous leukemia , 1976, Cancer.

[86]  J. Goldman,et al.  In vitro Colony Forming Cells and Colony Stimulating Factor in Chronic Granulocytic Leukaemia , 1974, British Journal of Cancer.

[87]  J. Adamson,et al.  THE PROLIFERATIVE POTENTIAL OF FROZEN STORED HUMAN MARROW CELLS , 1972, Transplantation.

[88]  P. Chervenick,et al.  Human Leukemic Cells: In vitro Growth of Colonies Containing the Philadelphia (Ph1) Chromosome , 1971, Science.

[89]  P. Neiman,et al.  Allogeneic marrow grafting for hematologic malignancy using HL-A matched donor-recipient sibling pairs. , 1971, Blood.

[90]  E. Henderson,et al.  Complication of bone-marrow transplantation. Graft-versus-host disease resulting from chronic-myelogenous-leukaemia leucocyte transfusions. , 1970, Lancet.

[91]  K. A. AHLQUIST,et al.  Chronic granulocytic leukaemia: comparison of radiotherapy and busulphan therapy. Report of the Medical Research Council's working party for therapeutic trials in leukaemia. , 1968, British medical journal.

[92]  G. Mathé,et al.  Study of factors determining the usefulness and complications of leukocyte transfusions. , 1967, The American journal of medicine.

[93]  C. Symons,et al.  Measurement of A.D.P.-induced platelet aggregation and A.D.P.-splitting enzymes in plasma. , 1966, Lancet.

[94]  Williams Ja SKIN LESIONS AS RESERVOIRS OF HOSPITAL INFECTION. , 1965 .

[95]  W. Quinton,et al.  PROLONGED PERITONEAL DIALYSIS FOR CHRONIC RENAL FAILURE. , 1964, Lancet.

[96]  M. Mcginniss,et al.  HEMATOPOIETIC GRAFT DETECTED BY A CHANGE IN ABO GROUP. , 1964, Blood.

[97]  R. H. Levin,et al.  Persistent Mitosis of Transfused Homologous Leukocytes in Children Receiving Antileukemic Therapy , 1963, Science.

[98]  W. Dameshek,et al.  Autologous bone marrow infusion as an adjunct in therapy of malignant disease. , 1959, Blood.

[99]  J. Loutit,et al.  Treatment of Murine Leukaemia with X Rays and Homologous Bone Marrow , 1956, British medical journal.

[100]  K. Keyvanfar,et al.  Hematopoietic stem cells and progenitors of chronic myeloid leukemia express leukemia-associated antigens: implications for the graft-versus-leukemia effect and peptide vaccine-based immunotherapy , 2008, Leukemia.

[101]  R. Brand,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). , 2006, Haematologica.

[102]  É.,et al.  Allogeneic Marrow Grafting for Hematologic Malignancy Using HLA Matched Donor-Recipient Sibling Pairs , 2005 .

[103]  T. Holyoake,et al.  Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. , 2002, Blood.

[104]  C. Craddock,et al.  Comparison of single-dose and escalating-dose regimens of donor lymphocyte infusion for relapse after allografting for chronic myeloid leukemia. , 2000, Blood.

[105]  K. Atkinson Clinical bone marrow and blood stem cell transplantation , 2000 .

[106]  J. Epstein,et al.  Patient reports of complications of bone marrow transplantation , 2000, Supportive Care in Cancer.

[107]  J P Klein,et al.  Estimating leukemia-free survival after allografting for chronic myeloid leukemia: a new method that takes into account patients who relapse and are restored to complete remission. , 2000, Blood.

[108]  J Hermans,et al.  Risk assessment for patients with chronic myeloid leukaemia before allogeneic blood or marrow transplantation. Chronic Leukemia Working Party of the European Group for Blood and Marrow Transplantation. , 1998, Lancet.

[109]  M. Horowitz,et al.  Choice of pretransplant treatment and timing of transplants for chronic myelogenous leukemia in chronic phase. , 1993, Blood.

[110]  I. Macdonald,et al.  Poor prognosis acute myeloid leukaemia treated by matched unrelated donor marrow transplant without preceding total body irradiation. , 1992, Bone marrow transplantation.

[111]  W. Wilmanns,et al.  Donor leukocyte transfusions for treatment of recurrent chronic myelogenous leukemia in marrow transplant patients. , 1990, Blood.

[112]  K. Sullivan,et al.  Graft versus leukemia effect in man: the relapse rate of acute leukemia is lower after allogeneic than after syngeneic marrow transplantation. , 1987, Progress in clinical and biological research.

[113]  H. Deeg,et al.  Effects of in vitro depletion of T cells in HLA-identical allogeneic marrow grafts. , 1985, Blood.

[114]  R. Champlin,et al.  Allogeneic bone marrow transplantation for chronic myelogenous leukemia in chronic or accelerated phase. , 1982, Blood.

[115]  D. Arthur,et al.  Cytogenetic conversion following allogeneic bone marrow transplantation for advanced chronic myelogenous leukemia. , 1981, Blood.

[116]  D. Peakman,et al.  Remission of relapsed leukaemia during a graft-versus-host reaction. A "graft-versus-leukaemia reaction" in man? , 1978, Lancet.

[117]  P. Neiman,et al.  Treatment of blastic transformation of chronic granulocytic leukemia by chemotherapy, total body irradiation and infusion of cryopreserved autologous marrow. , 1978, Experimental hematology.

[118]  P. Neiman,et al.  Treatment of blastic transformation of chronic granulocytic leukemia by high dose cyclophosphamide, total body irradiation and infusion of cryopreserved autologous marrow. , 1974, Experimental hematology.

[119]  M. Scanlon,et al.  Letter: X long-arm deletion with features of Turner's syndrome. , 1974, Lancet.

[120]  A. De vries,et al.  Prolonged remission in chronic myeloid leukemia after one course of busulfan. , 1966, Blood.