Seminars in Oncology
Volume 35, Issue 4 , Pages 388-400 , August 2008

Development of Minimal Residual Disease–Directed Therapy in Acute Myeloid Leukemia

  • Sylvie D. Freeman

      Affiliations

    • Departments of Immunology and Haematology, University of Birmingham, Birmingham, UK.
    • ,
  • Jelena V. Jovanovic

      Affiliations

    • Division of Genetics and Molecular Medicine, King's College, London, UK.
    • ,
  • David Grimwade

      Affiliations

    • Division of Genetics and Molecular Medicine, King's College, London, UK.
    • Corresponding Author InformationAddress correspondence to David Grimwade, PhD, Cancer Genetics Lab, Department of Medical and Molecular Genetics, 8th Floor, Tower Wing, Guy's Hospital, London SE1 9RT, UK.

References 

  1. Wheatley K, Burnett AK, Goldstone AH, et al. A simple, robust, validated and highly predictive index for the determination of risk-directed therapy in acute myeloid leukaemia derived from the MRC AML 10 trial (United Kingdom Medical Research Council's Adult and Childhood Leukaemia Working Parties). Br J Haematol. 1999;107:69–79
  2. Cheson BD, Bennett JM, Kopecky KJ, et al. Revised recommendations of the International Working Group for Diagnosis, Standardization of Response Criteria, Treatment Outcomes, and Reporting Standards for Therapeutic Trials in Acute Myeloid Leukemia. J Clin Oncol. 2003;21:4642–4649
  3. Lo-Coco F, Ammatuna E. The biology of acute promyelocytic leukemia and its impact on diagnosis and treatment. Hematology Am Soc Hematol Educ Program. 2006;156–161
  4. Reiter A, Lengfelder E, Grimwade D. Pathogenesis, diagnosis and monitoring of residual disease in acute promyelocytic leukaemia. Acta Haematol. 2004;112:55–67
  5. Lo Coco F, Diverio D, Avvisati G, et al. Therapy of molecular relapse in acute promyelocytic leukemia. Blood. 1999;94:2225–2229
  6. Esteve J, Escoda L, Martín G, et al. Outcome of patients with acute promyelocytic leukemia failing to front-line treatment with all-trans retinoic acid and anthracycline-based chemotherapy (PETHEMA protocols LPA96 and LPA99): benefit of an early intervention. Leukemia. 2007;21:446–452
  7. Yin JA, Grimwade D. Minimal residual disease evaluation in acute myeloid leukaemia. Lancet. 2002;360:160–162
  8. Miyamoto T, Weissman IL, Akashi K. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc Natl Acad Sci U S A. 2000;97:7521–7526
  9. Gabert J, Beillard E, van der Velden VHJ, et al. Standardization and quality control studies of ‘real-time' quantitative reverse transcriptase polymerase chain reaction of fusion gene transcripts for residual disease detection in leukemia—a Europe Against Cancer Program. Leukemia. 2003;17:2318–2357
  10. van der Velden VHJ, Hochhaus A, Cazzaniga G, et al. Detection of minimal residual disease in hematologic malignancies by real-time quantitative PCR: principles, approaches, and laboratory aspects. Leukemia. 2003;17:1013–1034
  11. Beillard E, Pallisgaard N, van der Velden VH, et al. Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using ‘real-time' quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR)—a Europe Against Cancer Program. Leukemia. 2003;17:2474–2486
  12. van der Velden VH, Boeckx N, Gonzalez M, et al. Differential stability of control gene and fusion gene transcripts over time may hamper accurate quantification of minimal residual disease—a study within the Europe Against Cancer Program. Leukemia. 2004;18:884–886
  13. Santamaría C, Chillón MC, Fernández C, et al. Using quantification of the PML-RARα transcript to stratify the risk of relapse in patients with acute promyelocytic leukemia. Haematologica. 2007;92:315–322
  14. Stock W, Harvey R, Moser B, et al. Minimal residual disease (MRD) and risk of relapse in acute promyelocytic leukemia (APL): insights from the North American Intergroup phase III trial C9710 [abstract]. Blood. 2006;108:150a
  15. Grimwade DJ, Jovanovic J, Hills R, et al. Evaluation of prospective detection of PML-RARA and RARA-PML fusion transcripts by real-time quantitative PCR (RQ-PCR) to direct pre-emptive therapy with arsenic trioxide (ATO) in acute promyelocytic leukemia (APL) patients treated in the UK MRC AML15 trial [abstract]. Blood. 2007;110:167a
  16. Krauter J, Gorlich K, Ottmann O, et al. Prognostic value of minimal residual disease quantification by real-time reverse transcriptase polymerase chain reaction in patients with core binding factor leukemias. J Clin Oncol. 2003;21:4413–4422
  17. Leroy H, de Botton S, Grardel-Duflos N, et al. Prognostic value of real-time quantitative PCR (RQ-PCR) in AML with t(8;21). Leukemia. 2005;19:367–372
  18. Stentoft J, Hokland P, Østergaard M, et al. Minimal residual core binding factor AMLs by real time quantitative PCR—initial response to chemotherapy predicts event free survival and close monitoring of peripheral blood unravels the kinetics of relapse. Leuk Res. 2006;30:389–395
  19. Perea G, Lasa A, Aventín A, et al. Prognostic value of minimal residual disease (MRD) in acute myeloid leukemia (AML) with favorable cytogenetics [t(8;21) and inv(16)]. Leukemia. 2006;20:87–94
  20. Weisser M, Haferlach C, Hiddemann W, et al. The quality of molecular response to chemotherapy is predictive for the outcome of AML1-ETO-positive AML and is independent of pretreatment risk factors. Leukemia. 2007;21:1177–1182
  21. Martinelli G, Rondoni M, Buonamici S, et al. Molecular monitoring to identify a threshold of CBFβ/MYH11 transcript below which continuous complete remission of acute myeloid leukemia inv16 is likely. Haematologica. 2004;89:495–497
  22. Scholl C, Schlenk RF, Eiwen K, et al. The prognostic value of MLL-AF9 detection in patients with t(9;11)(p22;q23)-positive acute myeloid leukemia. Haematologica. 2005;90:1626–1634
  23. Tobal K, Frost L, Liu Yin JA. Quantification of DEK-CAN fusion transcript by real-time reverse transcription polymerase reaction in patients with t(6;9) acute myeloid leukemia. Haematologica. 2004;89:1267–1269
  24. Østergaard M, Stentoft J, Hokland P. A real-time quantitative RT-PCR assay for monitoring DEK-CAN fusion transcripts arising from translocation t(6;9) in acute myeloid leukemia. Leuk Res. 2004;28:1213–1215
  25. Garçon L, Libura M, Delabesse E, et al. DEK-CAN molecular monitoring of myeloid malignancies could aid therapeutic stratification. Leukemia. 2005;19:1338–1344
  26. Baldus CD, Mrózek K, Marcucci G, et al. Clinical outcome of de novo acute myeloid leukaemia patients with normal cytogenetics is affected by molecular genetic alterations: a concise review. Br J Haematol. 2007;137:387–400
  27. Falini B, Nicoletti I, Martelli MF, et al. Acute myeloid leukemia carrying cytoplasmic/mutated nucleophosmin (NPMc+ AML): biologic and clinical features. Blood. 2007;109:874–885
  28. Gorello P, Cazzaniga G, Alberti F, et al. Quantitative assessment of minimal residual disease in acute myeloid leukemia carrying nucleophosmin (NPM1) gene mutations. Leukemia. 2006;20:1103–1108
  29. Chou WC, Tang JL, Wu SJ, et al. Clinical implications of minimal residual disease monitoring by quantitative polymerase chain reaction in acute myeloid leukemia patients bearing nucleophosmin (NPM1) mutations. Leukemia. 2007;21:998–1004
  30. Schnittger S, Kern W, Haferlach C, et al. PCR-based MRD detection in NPM1 mutated AML: a prospective follow-up study in 97 patients [abstract]. Haematologica. 2007;92(Suppl 1):147
  31. Grimwade D. NPM1 mutation in AML: WHO and why?. Blood. 2006;108:3965
  32. Palmisano M, Grafone T, Ottaviani E, et al. NPM1 mutations are more stable than FLT3 mutations during the course of disease in patients with acute myeloid leukemia. Haematologica. 2007;92:1268–1269
  33. Beretta C, Gaipa G, Rossi V, et al. Development of a quantitative-PCR method for specific FLT3/ITD monitoring in acute myeloid leukemia. Leukemia. 2004;18:1441–1444
  34. Schnittger S, Schoch C, Kern W, et al. FLT3 length mutations as marker for follow-up studies in acute myeloid leukaemia. Acta Haematol. 2004;112:68–78
  35. Scholl S, Loncarevic IF, Krause C, et al. Minimal residual disease based on patient specific Flt3-ITD and -ITT mutations in acute myeloid leukemia. Leuk Res. 2005;29:849–853
  36. Kottaridis PD, Gale RE, Langabeer SE, et al. Studies of FLT3 mutations in paired presentation and relapse samples from patients with acute myeloid leukemia: implications for the role of FLT3 mutations in leukemogenesis, minimal residual disease detection, and possible therapy with FLT3 inhibitors. Blood. 2002;100:2393–2398
  37. Shih LY, Huang CF, Wu JH, et al. Internal tandem duplication of FLT3 in relapsed acute myeloid leukemia: a comparative analysis of bone marrow samples from 108 adult patients at diagnosis and relapse. Blood. 2002;100:2387–2392
  38. Cloos J, Goemans BF, Hess CJ, et al. Stability and prognostic influence of FLT3 mutations in paired initial and relapsed AML samples. Leukemia. 2006;20:1217–1220
  39. Smith LL, Pearce D, Smith ML, et al. Development of a quantitative real-time polymerase chain reaction method for monitoring CEBPA mutations in normal karyotype acute myeloid leukaemia. Br J Haematol. 2006;133:103–105
  40. Weisser M, Kern W, Schoch C, et al. Risk assessment by monitoring expression levels of partial tandem duplications in the MLL gene in acute myeloid leukemia during therapy. Haematologica. 2005;90:881–889
  41. Steinbach D, Schramm A, Eggert A, et al. Identification of a set of seven genes for the monitoring of minimal residual disease in pediatric acute myeloid leukemia. Clin Cancer Res. 2006;12:2434–2441
  42. Cilloni D, Renneville A, Hermitte F, et al. Real-time quantitative PCR (RQ-PCR) detection of minimal residual disease (MRD) by optimized WT1 assay to enhance risk stratification in acute myeloid leukemia (AML): a European LeukemiaNet study [abstract]. Blood. 2007;110:167a
  43. Lapillonne H, Renneville A, Auvrignon A, et al. High WT1 expression after induction therapy predicts high risk of relapse and death in pediatric acute myeloid leukemia. J Clin Oncol. 2006;24:1507–1515
  44. Coustan-Smith E, Ribeiro RC, Rubnitz JE, et al. Clinical significance of residual disease during treatment in childhood acute myeloid leukaemia. Br J Haematol. 2003;123:243–252
  45. Feller N, van der Pol MA, van Stijn A, et al. MRD parameters using immunophenotypic detection methods are highly reliable in predicting survival in acute myeloid leukaemia. Leukemia. 2004;18:1380–1390
  46. Kern W, Voskova D, Schoch C, et al. Determination of relapse risk based on assessment of minimal residual disease during complete remission by multiparameter flow cytometry in unselected patients with acute myeloid leukemia. Blood. 2004;104:3078–3085
  47. San Miguel JF, Vidriales MB, López-Berges C, et al. Early immunophenotypical evaluation of minimal residual disease in acute myeloid leukemia identifies different patient risk groups and may contribute to postinduction treatment stratification. Blood. 2001;98:1746–1751
  48. Sievers EL, Lange BJ, Alonzo TA, et al. Immunophenotypic evidence of leukemia after induction therapy predicts relapse: results from a prospective Children's Cancer Group study of 252 patients with acute myeloid leukemia. Blood. 2003;101:3398–3406
  49. Venditti A, Buccisano F, Del Poeta G, et al. Level of minimal residual disease after consolidation therapy predicts outcome in acute myeloid leukemia. Blood. 2000;96:3948–3952
  50. Buccisano F, Maurillo L, Gattei V, et al. The kinetics of reduction of minimal residual disease impacts on duration of response and survival of patients with acute myeloid leukemia. Leukemia. 2006;20:1783–1789
  51. Langebrake C, Creutzig U, Dworzak M, et al. Residual disease monitoring in childhood acute myeloid leukemia by multiparameter flow cytometry: the MRD-AML-BFM Study Group. J Clin Oncol. 2006;24:3686–3692
  52. Laane E, Derolf AR, Bjorklund E, et al. The effect of allogeneic stem cell transplantation on outcome in younger acute myeloid leukemia patients with minimal residual disease detected by flow cytometry at the end of post-remission chemotherapy. Haematologica. 2006;91:833–836
  53. Baer MR, Stewart CC, Dodge RK, et al. High frequency of immunophenotype changes in acute myeloid leukemia at relapse: implications for residual disease detection (Cancer and Leukemia Group B Study 8361). Blood. 2001;97:3574–3580
  54. Langebrake C, Brinkmann I, Teigler-Schlegel A, et al. Immunophenotypic differences between diagnosis and relapse in childhood AML: implications for MRD monitoring. Cytometry B Clin Cytom. 2005;63:1–9
  55. Elliott MA, Litzow MR, Letendre LL, et al. Early peripheral blood blast clearance during induction chemotherapy for acute myeloid leukemia predicts superior relapse-free survival. Blood. 2007;110:4172-4.
  56. van Rhenen A, van Dongen GA, Kelder A, et al. The novel AML stem cell associated antigen CLL-1 aids in discrimination between normal and leukemic stem cells. Blood. 2007;110:2659–2666
  57. van Rhenen A, Moshaver B, Kelder A, et al. Aberrant marker expression patterns on the CD34+CD38- stem cell compartment in acute myeloid leukemia allows to distinguish the malignant from the normal stem cell compartment both at diagnosis and in remission. Leukemia. 2007;21:1700–1707
  58. Pallisgaard N, Clausen N, Schroder H, et al. Rapid and sensitive minimal residual disease detection in acute leukemia by quantitative real-time RT-PCR exemplified by t(12;21) TEL-AML1 fusion transcript. Genes Chromosomes Cancer. 1999;26:355–365
  59. Gallagher RE, Yeap BY, Bi W, et al. Quantitative real-time RT-PCR analysis of PML-RARα mRNA in acute promyelocytic leukemia: assessment of prognostic significance in adult patients from Intergroup protocol 0129. Blood. 2003;101:2521–2528
  60. Hughes T, Deininger M, Hochhaus A, et al. Monitoring CML patients responding to treatment with tyrosine kinase inhibitors: review and recommendations for harmonizing current methodology for detecting BCR-ABL transcripts and kinase domain mutations and for expressing results. Blood. 2006;108:28–37

PII: S0093-7754(08)00119-X

doi: 10.1053/j.seminoncol.2008.04.009

Seminars in Oncology
Volume 35, Issue 4 , Pages 388-400 , August 2008

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