Should evaluation for minimal residual disease be routine in acute myeloid leukemia?

Current Opinion in Hematology

Volumn 20, Issue 2, 2013, Pages 86-92

  Coustan Smith, Elaine ^a   Campana, Dario ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

acute myeloblastic leukemia; flow cytometry; minimal residual disease; polymerase chain reaction; prognosis; remission

Indexed keywords

CD135 ANTIGEN; MIXED LINEAGE LEUKEMIA PROTEIN; NUCLEOPHOSMIN; TRANSCRIPTION FACTOR RUNX1;

ACUTE GRANULOCYTIC LEUKEMIA; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER REGRESSION; CANCER SURVIVAL; CONSOLIDATION CHEMOTHERAPY; FLOW CYTOMETRY; GENE EXPRESSION; GENE MUTATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOPHENOTYPING; MINIMAL RESIDUAL DISEASE; MOLECULAR GENETICS; OVERALL SURVIVAL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RECURRENCE FREE SURVIVAL; REVIEW; TREATMENT OUTCOME; TREATMENT RESPONSE;

FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; LEUKEMIA, MYELOID, ACUTE; NEOPLASM, RESIDUAL;

EID: 84873341730     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/MOH.0b013e32835dd90a     Document Type: Review

References (67)

1. Chen Y, Cortes J, Estrov Z, et al. Persistence of cytogenetic abnormalities at complete remission after induction in patients with acute myeloid leukemia: prognostic significance and the potential role of allogeneic stem-cell transplantation. J Clin Oncol 2011; 29:2507-2513.
2. Bacher U, Kern W, Schoch C, et al. Evaluation of complete disease remission in acute myeloid leukemia: a prospective study based on cytomorphology, interphase fluorescence in situ hybridization, and immunophenotyping during follow-up in patients with acute myeloid leukemia. Cancer 2006; 106:839-847.
3. Shook D, Coustan-Smith E, Ribeiro RC, et al. Minimal residual disease quantitation in acute myeloid leukemia. Clin Lymphoma Myeloma 2009; 9 (Suppl. 3):S281-S285.
4. Grimwade D, Vyas P, Freeman S. Assessment of minimal residual disease in acute myeloid leukemia. Curr Opin Oncol 2010; 22:656-663.
5. Buccisano F, Maurillo L, Del Principe MI, et al. Prognostic and therapeutic implications of minimal residual disease detection in acute myeloid leukemia. Blood 2012; 119:332-341.
6. Sanz MA, Lo-Coco F. Modern approaches to treating acute promyelocytic leukemia. J Clin Oncol 2011; 29:495-503.
7. Grimwade D, Tallman MS. Should minimal residual disease monitoring be the standard of care for all patients with acute promyelocytic leukemia? Leuk Res 2011; 35:3-7.
8. Grimwade D, Hills RK, Moorman AV, et al. Refinement of cytogenetic classification in acute myeloid leukemia: determination of prognostic significance of rare recurring chromosomal abnormalities among 5876 younger adult patients treated in the United Kingdom Medical Research Council trials. Blood 2010; 116:354-365.
9. Harrison CJ, Hills RK, Moorman AV, et al. Cytogenetics of childhood acute myeloid leukemia: United Kingdom Medical Research Council Treatment trials AML 10 and 12. J Clin Oncol 2010; 28:2674-2681.
10. Falini B, Martelli MP, Bolli N, et al. Acute myeloid leukemia with mutated nucleophosmin (NPM1): is it a distinct entity? Blood 2010; 117:1109-1120.
11. Hollink IH, Zwaan CM, Zimmermann M, et al. Favorable prognostic impact of NPM1 gene mutations in childhood acute myeloid leukemia, with emphasis on cytogenetically normal AML. Leukemia 2009; 23:262-270.
12. Ley TJ, Ding L, Walter MJ, et al. DNMT3A mutations in acute myeloid leukemia. N Engl J Med 2010; 363:2424-2433.
13. Hollink IH, Feng Q, Danen-van Oorschot AA, et al. Low frequency of DNMT3A mutations in pediatric AML, and the identification of the OCI-AML3 cell line as an in vitro model. Leukemia 2012; 26:371-373.
14. Hou HA, Kuo YY, Liu CY, et al. DNMT3A mutations in acute myeloid leukemia: stability during disease evolution and clinical implications. Blood 2012; 119:559-568.
15. Kottaridis PD, Gale RE, Frew ME, et al. The presence of a FLT3 internal tandem duplication in patients with acute myeloid leukemia (AML) adds important prognostic information to cytogenetic risk group and response to the first cycle of chemotherapy: analysis of 854 patients from the United Kingdom Medical Research Council AML 10 and 12 trials. Blood 2001; 98:1752-1759.
16. Meshinchi S, Woods WG, Stirewalt DL, et al. Prevalence and prognostic significance of Flt3 internal tandem duplication in pediatric acute myeloid leukemia. Blood 2001; 97:89-94.
17. 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.
18. 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.
19. Chou WC, Hou HA, Liu CY, et al. Sensitive measurement of quantity dynamics of FLT3 internal tandem duplication at early time points provides prognostic information. Ann Oncol 2011; 22:696-704.
20. Schiller J, Praulich I, Krings Rocha C, Kreuzer KA. Patient-specific analysis of FLT3 internal tandem duplications for the prognostication and monitoring of acute myeloid leukemia. Eur J Haematol 2012; 89:53-62.
21. Abdelhamid E, Preudhomme C, Helevaut N, et al. Minimal residual disease monitoring based on FLT3 internal tandem duplication in adult acute myeloid leukemia. Leuk Res 2012; 36:316-323.
22. 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.
23. Van der Velden V, 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.
24. Gabert J, Beillard E, van der Velden V, 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.
25. Varella-Garcia M, Hogan CJ, Odom LF, et al. Minimal residual disease (MRD) in remission t(8;21) AML and in vivo differentiation detected by FISH and CD34\+ cell sorting. Leukemia 2001; 15:1408-1414.
26. Sexauer A, Perl A, Yang X, et al. Terminal myeloid differentiation in vivo is induced by FLT3 inhibition in FLT3/ITD AML. Blood 2012; 120:4205-4214.
27. Suzuki T, Kiyoi H, Ozeki K, et al. Clinical characteristics and prognostic implications of NPM1 mutations in acute myeloid leukemia. Blood 2005; 106:2854-2861.
28. Papadaki C, Dufour A, Seibl M, et al. Monitoring minimal residual disease in acute myeloid leukaemia with NPM1 mutations by quantitative PCR: clonal evolution is a limiting factor. Br J Haematol 2009; 144:517-523.
29. Kronke J, Schlenk RF, Jensen KO, et al. Monitoring of minimal residual disease in NPM1-mutated acute myeloid leukemia: a study from the German-Austrian acute myeloid leukemia study group. J Clin Oncol 2011; 29:2709-2716.
30. Cilloni D, Renneville A, Hermitte F, et al. Real-time quantitative polymerase chain reaction detection of minimal residual disease by standardized WT1 assay to enhance risk stratification in acute myeloid leukemia: a European LeukemiaNet study. J Clin Oncol 2009; 27:5195-5201.
31. Willasch AM, Gruhn B, Coliva T, et al. Standardization of WT1 mRNA quantitation for minimal residual disease monitoring in childhood AML and implications of WT1 gene mutations: a European multicenter study. Leukemia 2009; 23:1472-1479.
32. Kristensen T, Moller MB, Friis L, et al. NPM1 mutation is a stable marker for minimal residual disease monitoring in acute myeloid leukaemia patients with increased sensitivity compared to WT1 expression. Eur J Haematol 2011; 87:400-408.
33. Corbacioglu A, Scholl C, Schlenk RF, et al. Prognostic impact of minimal residual disease in CBFB-MYH11-positive acute myeloid leukemia. J Clin Oncol 2010; 28:3724-3729.
34. Lane S, Saal R, Mollee P, et al. A-1 log rise in RQ-PCR transcript levels defines molecular relapse in core binding factor acute myeloid leukemia and predicts subsequent morphologic relapse. Leuk Lymphoma 2008; 49:517-523.
35. Yin JA, O'Brien MA, Hills RK, et al. Minimal residual disease monitoring by quantitative RT-PCR in core binding factor AML allows risk stratification and predicts relapse: results of the United Kingdom MRC AML-15 trial. Blood 2012; 120:2826-2835.
36. Viehmann S, Teigler-Schlegel A, Bruch J, et al. Monitoring of minimal residual disease (MRD) by real-time quantitative reverse transcription PCR (RQ-RTPCR) in childhood acute myeloid leukemia with AML1/ETO rearrangement. Leukemia 2003; 17:1130-1136.
37. Inaba H, Coustan-Smith E, Cao X, et al. Comparative analysis of different approaches to measure treatment response in acute myeloid leukemia. J Clin Oncol 2012; 30:3625-3632.
38. 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.
39. 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.
40. Barragan E, Pajuelo JC, Ballester S, et al. Minimal residual disease detection in acute myeloid leukemia by mutant nucleophosmin (NPM1): comparison with WT1 gene expression. Clin Chim Acta 2008; 395:120-123.
41. Schnittger S, Kern W, Tschulik C, et al. Minimal residual disease levels assessed by NPM1 mutation-specific RQ-PCR provide important prognostic information in AML. Blood 2009; 114:2220-2231.
42. Stahl T, Badbaran A, Kroger N, et al. Minimal residual disease diagnostics in patients with acute myeloid leukemia in the posttransplant period: comparison of peripheral blood and bone marrow analysis. Leuk Lymphoma 2010; 51:1837-1843.
43. Miglino M, Colombo N, Grasso R, et al. Nucleophosmin gene-based monitoring in de novo cytogenetically normal acute myeloid leukemia with nucleophosmin gene mutations: comparison with cytofluorimetric analysis and study of Wilms tumor gene 1 expression. Leuk Lymphoma 2012; 53:2214-2217.
44. Inoue K, Ogawa H, Yamagami T, et al. Long-term follow-up of minimal residual disease in leukemia patients by monitoring WT1 (Wilms tumor gene) expression levels. Blood 1996; 88:2267-2278.
45. Trka J, Kalinova M, Hrusak O, et al. Real-time quantitative PCR detection of WT1 gene expression in children with AML: prognostic significance, correlation with disease status and residual disease detection by flow cytometry. Leukemia 2002; 16:1381-1389.
46. Ostergaard M, Olesen LH, Hasle H, et al. WT1 gene expression: an excellent tool for monitoring minimal residual disease in 70% of acute myeloid leukaemia patients-results from a single-centre study. Br J Haematol 2004; 125:590-600.
47. Weisser M, Kern W, Rauhut S, et al. Prognostic impact of RT-PCRbased quantification of WT1 gene expression during MRD monitoring of acute myeloid leukemia. Leukemia 2005; 19:1416-1423.
48. 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.
49. Jacobsohn DA, Tse WT, Chaleff S, et al. High WT1 gene expression before haematopoietic stem cell transplant in children with acute myeloid leukaemia predicts poor event-free survival. Br J Haematol 2009; 146:669-674.
50. Buccisano F, Maurillo L, Spagnoli A, et al. Cytogenetic and molecular diagnostic characterization combined to postconsolidation minimal residual disease assessment by flow cytometry improves risk stratification in adult acute myeloid leukemia. Blood 2010; 116:2295-2303.
51. Coustan-Smith E, Ribeiro RC, Rubnitz JE, et al. Clinical significance of residual disease during treatment in childhood acute myeloid leukemia. Br J Haematol 2003; 123:243-252.
52. Rubnitz JE, Inaba H, Dahl GV, et al. Minimal residual disease-directed therapy for childhood acute myeloid leukemia: results of the AML02 multicenter trial. Lancet Oncol 2010; 11:543-552.
53. Van der Velden VH, Sluijs-Geling A, Gibson BE, et al. Clinical significance of flowcytometric minimal residual disease detection in pediatric acute myeloid leukemia patients treated according to the DCOG ANLL97/MRC AML12 protocol. Leukemia 2010; 24:1599-1606.
54. Bjorklund E, Gruber A, Mazur J, et al. CD34\+ cell subpopulations detected by 8-color flow cytometry in bone marrow and in peripheral blood stem cell collections: application for MRD detection in leukemia patients. Int J Hematol 2009; 90:292-302.
55. Coustan-Smith E, Song G, Clark C, et al. New markers for minimal residual disease detection in acute lymphoblastic leukemia. Blood 2011; 117:6267-6276.
56. Gruszka AM, Lavorgna S, Consalvo MI, et al. A monoclonal antibody against mutated nucleophosmin 1 for the molecular diagnosis of acute myeloid leukemias. Blood 2010; 116:2096-2102.
57. Grimwade L, Gudgin E, Bloxham D, et al. Detection of cytoplasmic nucleophosmin expression by imaging flow cytometry. Cytometry A 2012; 81:896-900.
58. Fiser K, Sieger T, Schumich A, et al. Detection and monitoring of normal and leukemic cell populations with hierarchical clustering of flow cytometry data. Cytometry A 2012; 81:25-34.
59. Van Dongen JJ, Lhermitte L, Bottcher S, et al. EuroFlow antibody panels for standardized n-dimensional flow cytometric immunophenotyping of normal, reactive and malignant leukocytes. Leukemia 2012; 26:1908-1975.
60. Inaba H, Rubnitz JE, Coustan-Smith E, et al. Phase I pharmacokinetic and pharmacodynamic study of the multikinase inhibitor sorafenib in combination with clofarabine and cytarabine in pediatric relapsed/refractory leukemia. J Clin Oncol 2011; 29:3293-3300.
61. Walter RB, Gooley TA, Wood BL, et al. Impact of pretransplantation minimal residual disease, as detected by multiparametric flow cytometry, on outcome of myeloablative hematopoietic cell transplantation for acute myeloid leukemia. J Clin Oncol 2011; 29:1190-1197.
62. 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 acute myeloid leukemia patients. Blood 2003; 101:3398-3406.
63. 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.
64. Loken MR, Alonzo TA, Pardo L, et al. Residual disease detected by multidimensional flow cytometry signifies high relapse risk in patients with de novo acute myeloid leukemia: a report from Children's Oncology Group. Blood 2012; 120:1581-1588.
65. Leung W, Pui CH, Coustan-Smith E, et al. Detectable minimal residual disease before hematopoietic cell transplantation is prognostic but does not preclude cure for children with very-high-risk leukemia. Blood 2012; 120:468-472.
66. Bruggemann M, Schrauder A, Raff T, et al. Standardized MRD quantification in European ALL trials: proceedings of the Second International Symposium on MRD assessment in Kiel, Germany, 18-20 September. Leukemia 2010; 24:521-535.
67. Ommen HB, Schnittger S, Jovanovic JV, et al. Strikingly different molecular relapse kinetics in NPM1c, PML-RARA, RUNX1-RUNX1T1, and CBFB-MYH11 acute myeloid leukemias. Blood 2010; 115:198-205.