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CC BY 4.0 · Indian J Med Paediatr Oncol 2023; 44(06): 554-565
DOI: 10.1055/s-0043-1772203
DOI: 10.1055/s-0043-1772203
Review Article
Monitoring Measurable/Minimal Residual Disease in Acute Myeloid Leukemia: Multiparametric Flow Cytometry-Based Approach
Autoren
Funding None declared.
Abstract
Measurable/minimal residual disease (MRD) status is the most relevant predictor of clinical outcome in hematolymphoid neoplasms, including acute myeloid leukemia (AML). In contrast to acute lymphoblastic leukemia, multiple myeloma, or chronic lymphocytic leukemia, etc., AML is a widely heterogeneous neoplasm with poor clinical outcomes. Multicolor flow cytometry (MFC) is a powerful technology with high sensitivity, rapid results, cost-effectiveness, and easy availability. It is routinely used for diagnosing and MRD monitoring in many hematological neoplasms. However, MFC-based MRD monitoring in AML is complex and challenging. It requires a refined approach, a wide panel of markers, and adequate training and experience. This review focuses on the panel design, processing details, template design, analysis approach, and recent updates in MFC-based MRD monitoring in AML. It further describes the normal distribution and maturation patterns of various sublineages among hematological progenitors and their utility in studying AML MRD.
Publikationsverlauf
Artikel online veröffentlicht:
27. November 2023
© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)
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References
- 1 Döhner H, Weisdorf DJ, Bloomfield CD. Acute myeloid leukemia. N Engl J Med 2015; 373 (12) 1136-1152
- 2 Pessach I, Spyropoulos T, Lamprianidou E, Kotsianidis I. MRD monitoring by multiparametric flow cytometry in AML: is it time to incorporate immune parameters?. Cancers (Basel) 2022; 14 (17) 4294
- 3 Pratz KW, Jonas BA, Pullarkat V. et al. Measurable residual disease response and prognosis in treatment-naïve acute myeloid leukemia with venetoclax and azacitidine. J Clin Oncol 2022; 40 (08) 855-865
- 4 Rossi G, Giambra V, Minervini MM. et al. Leukemia-associated immunophenotypes subdivided in “categories of specificity” improve the sensitivity of minimal residual disease in predicting relapse in acute myeloid leukemia. Cytometry B Clin Cytom 2020; 98 (03) 216-225
- 5 Khoury JD, Solary E, Abla O. et al. The 5th edition of the World Health Organization Classification of Haematolymphoid Tumours: myeloid and histiocytic/dendritic neoplasms. Leukemia 2022; 36 (07) 1703-1719
- 6 Cheson BD, Cassileth PA, Head DR. et al. Report of the National Cancer Institute-sponsored workshop on definitions of diagnosis and response in acute myeloid leukemia. J Clin Oncol 1990; 8 (05) 813-819
- 7 O'Donnell MR, Appelbaum F, Bishop M, Estey EH, Grever M, Maslak P. The National Comprehensive Cancer Network. NCCN acute leukemia practice guidelines. Oncology (Williston Park) 1996; 10 (11, Suppl): 205-221
- 8 Appelbaum FR, Baer MR, Carabasi MH. et al; National Comprehensive Cancer Network. NCCN Practice Guidelines for acute myelogenous leukemia. Oncology (Williston Park) 2000; 14 (11A): 53-61
- 9 Cheson BD, Bennett JM, Kopecky KJ. et al; International Working Group for Diagnosis, Standardization of Response Criteria, Treatment Outcomes, and Reporting Standards for Therapeutic Trials in Acute Myeloid Leukemia. 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 (24) 4642-4649
- 10 Creutzig U, Kaspers GJ. 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 2004; 22 (16) 3432-3433
- 11 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 (29) 3625-3632
- 12 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 (08) 1581-1588
- 13 Brodersen LE, Gerbing RB, Pardo ML. et al. Morphologic remission status is limited compared to ΔN flow cytometry: a Children's Oncology Group AAML0531 report. Blood Adv 2020; 4 (20) 5050-5061
- 14 Chen X, Cherian S. Role of minimal residual disease testing in acute myeloid leukemia. Clin Lab Med 2021; 41 (03) 467-483
- 15 Shook D, Coustan-Smith E, Ribeiro RC, Rubnitz JE, Campana D. Minimal residual disease quantitation in acute myeloid leukemia. Clin Lymphoma Myeloma 2009; 9 (Suppl 3): S281-S285
- 16 Vedula RS, Lindsley RC. Measurement of residual disease in acute myeloid leukemia. Curr Hematol Malig Rep 2017; 12 (06) 574-581
- 17 Freeman SD, Jovanovic JV, Grimwade D. Development of minimal residual disease-directed therapy in acute myeloid leukemia. Semin Oncol 2008; 35 (04) 388-400
- 18 Grimwade D, Vyas P, Freeman S. Assessment of minimal residual disease in acute myeloid leukemia. Curr Opin Oncol 2010; 22 (06) 656-663
- 19 Freeman SD, Virgo P, Couzens S. et al. Prognostic relevance of treatment response measured by flow cytometric residual disease detection in older patients with acute myeloid leukemia. J Clin Oncol 2013; 31 (32) 4123-4131
- 20 Grimwade D, Freeman SD. Defining minimal residual disease in acute myeloid leukemia: which platforms are ready for “prime time”?. Blood 2014; 124 (23) 3345-3355
- 21 Buccisano F, Dillon R, Freeman SD, Venditti A. Role of minimal (measurable) residual disease assessment in older patients with acute myeloid leukemia. Cancers (Basel) 2018; 10 (07) 215
- 22 Freeman SD, Hills RK, Virgo P. et al. Measurable residual disease at induction redefines partial response in acute myeloid leukemia and stratifies outcomes in patients at standard risk without NPM1 mutations. J Clin Oncol 2018; 36 (15) 1486-1497
- 23 Hourigan CS, Gale RP, Gormley NJ, Ossenkoppele GJ, Walter RB. Measurable residual disease testing in acute myeloid leukaemia. Leukemia 2017; 31 (07) 1482-1490
- 24 Paterno G, Del Principe MI, Venditti A. Detection and management of acute myeloid leukemia measurable residual disease: is it standard of care?. Curr Opin Hematol 2020; 27 (02) 81-87
- 25 Schuurhuis GJ, Heuser M, Freeman S. et al. Minimal/measurable residual disease in AML: a consensus document from the European LeukemiaNet MRD Working Party. Blood 2018; 131 (12) 1275-1291
- 26 DiNardo CD, Luger SM. Beyond morphology: minimal residual disease detection in acute myeloid leukemia. Curr Opin Hematol 2012; 19 (02) 82-88
- 27 Jacobsohn DA, Loken MR, Fei M. et al. Outcomes of measurable residual disease in pediatric acute myeloid leukemia before and after hematopoietic stem cell transplant: validation of difference from normal flow cytometry with chimerism studies and Wilms tumor 1 gene expression. Biol Blood Marrow Transplant 2018; 24 (10) 2040-2046
- 28 Freeman SD, Hills RK, Russell NH. et al; UK NCRI AML Trial Group; HOVON AML Trial Group. Induction response criteria in acute myeloid leukaemia: implications of a flow cytometric measurable residual disease negative test in refractory adults. Br J Haematol 2019; 186 (01) 130-133
- 29 Heuser M, Freeman SD, Ossenkoppele GJ. et al. 2021 Update on MRD in acute myeloid leukemia: a consensus document from the European LeukemiaNet MRD Working Party. Blood 2021; 138 (26) 2753-2767
- 30 Chen X, Wood BL. Monitoring minimal residual disease in acute leukemia: technical challenges and interpretive complexities. Blood Rev 2017; 31 (02) 63-75
- 31 Thol F, Gabdoulline R, Liebich A. et al. Measurable residual disease monitoring by NGS before allogeneic hematopoietic cell transplantation in AML. Blood 2018; 132 (16) 1703-1713
- 32 Heuser M, Heida B, Büttner K. et al. Posttransplantation MRD monitoring in patients with AML by next-generation sequencing using DTA and non-DTA mutations. Blood Adv 2021; 5 (09) 2294-2304
- 33 Simoes C, Paiva B, Martínez-Cuadrón D. et al. Measurable residual disease in elderly acute myeloid leukemia: results from the PETHEMA-FLUGAZA phase 3 clinical trial. Blood Adv 2021; 5 (03) 760-770
- 34 Caballero-Velázquez T, Pérez-López O, Yeguas Bermejo A. et al. Prognostic value of measurable residual disease in patients with AML undergoing HSCT: a multicenter study. Cancers (Basel) 2023; 15 (05) 1609
- 35 Fuda F, Chen W. Minimal/measurable residual disease detection in acute leukemias by multiparameter flow cytometry. Curr Hematol Malig Rep 2018; 13 (06) 455-466
- 36 Zhou Y, Othus M, Walter RB, Estey EH, Wu D, Wood BL. Deep NPM1 sequencing following allogeneic hematopoietic cell transplantation improves risk assessment in adults with NPM1-mutated AML. Biol Blood Marrow Transplant 2018; 24 (08) 1615-1620
- 37 Roloff GW, Lai C, Hourigan CS, Dillon LW. Technical Advances in the Measurement of Residual Disease in Acute Myeloid Leukemia. J Clin Med 2017; 6 (09) 87
- 38 Tettero JM, Freeman S, Buecklein V. et al. Technical aspects of flow cytometry-based measurable residual disease quantification in acute myeloid leukemia: experience of the European LeukemiaNet MRD working party. HemaSphere 2021; 6 (01) e676
- 39 Juul-Dam KL, Ommen HB, Nyvold CG. et al. Measurable residual disease assessment by qPCR in peripheral blood is an informative tool for disease surveillance in childhood acute myeloid leukaemia. Br J Haematol 2020; 190 (02) 198-208
- 40 Zhang YW, Su L, Tan YH. et al. Measurable residual disease detected by flow cytometry independently predicts prognoses of NPM1-mutated acute myeloid leukemia. Ann Hematol 2023; 102 (02) 337-347
- 41 McGowan F P, Hyter D S, Cui W, Plummer RM, Godwin AK, Zhang D. P FM. Comparison of flow cytometry and next-generation sequencing in minimal residual disease monitoring of acute myeloid leukemia: one institute's practical clinical experience. Int J Lab Hematol 2022; 44 (01) 118-126
- 42 Patkar N, Kakirde C, Shaikh AF. et al. Clinical impact of panel-based error-corrected next generation sequencing versus flow cytometry to detect measurable residual disease (MRD) in acute myeloid leukemia (AML). Leukemia 2021; 35 (05) 1392-1404
- 43 Fajtova M, Babusikova O. Immunophenotype characterization of hematopoietic stem cells, progenitor cells restricted to myeloid lineage and their leukemia counterparts. Neoplasma 2010; 57 (05) 392-400
- 44 Pettit K, Stock W, Walter RB. Incorporating measurable (“minimal”) residual disease-directed treatment strategies to optimize outcomes in adults with acute myeloid leukemia. Leuk Lymphoma 2016; 57 (07) 1527-1533
- 45 Wouters R, Cucchi D, Kaspers GJ, Schuurhuis GJ, Cloos J. Relevance of leukemic stem cells in acute myeloid leukemia: heterogeneity and influence on disease monitoring, prognosis and treatment design. Expert Rev Hematol 2014; 7 (06) 791-805
- 46 Farge T, Saland E, de Toni F. et al. Chemotherapy-resistant human acute myeloid leukemia cells are not enriched for leukemic stem cells but require oxidative metabolism. Cancer Discov 2017; 7 (07) 716-735
- 47 Cloos J, Harris JR, Janssen JJWM. et al. Comprehensive protocol to sample and process bone marrow for measuring measurable residual disease and leukemic stem cells in acute myeloid leukemia. J Vis Exp 2018; ;( (133) 56386
- 48 Jaddaoui S, Bencharef H, Lamchahab M, Quessar A, Oukkache B. Prognostic impact and phenotype of residual acute myeloid leukemia stem cells. Clin Lab 2022;68(06):
- 49 Khaldoyanidi SK, Hindoyan A, Stein A, Subklewe M. Leukemic stem cells as a target for eliminating acute myeloid leukemia: gaps in translational research. Crit Rev Oncol Hematol 2022; 175: 103710
- 50 Röhnert MA, Kramer M, Schadt J. et al. Reproducible measurable residual disease detection by multiparametric flow cytometry in acute myeloid leukemia. Leukemia 2022; 36 (09) 2208-2217
- 51 Kalina T, Flores-Montero J, van der Velden VH. et al; EuroFlow Consortium (EU-FP6, LSHB-CT-2006-018708). EuroFlow standardization of flow cytometer instrument settings and immunophenotyping protocols. Leukemia 2012; 26 (09) 1986-2010
- 52 Kern W, Bacher U, Haferlach C, Schnittger S, Haferlach T. The role of multiparameter flow cytometry for disease monitoring in AML. Best Pract Res Clin Haematol 2010; 23 (03) 379-390
- 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 (11) 3574-3580
- 54 Voskova D, Schoch C, Schnittger S, Hiddemann W, Haferlach T, Kern W. Stability of leukemia-associated aberrant immunophenotypes in patients with acute myeloid leukemia between diagnosis and relapse: comparison with cytomorphologic, cytogenetic, and molecular genetic findings. Cytometry B Clin Cytom 2004; 62 (01) 25-38
- 55 Zelezníková T, Babusíková O. The impact of cell heterogeneity and immunophenotypic changes on monitoring minimal residual disease in acute myeloid leukemia. Neoplasma 2006; 53 (06) 500-506
- 56 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 (01) 1-9
- 57 Xiao W, Petrova-Drus K, Roshal M. Optimal measurable residual disease testing for acute myeloid leukemia. Surg Pathol Clin 2019; 12 (03) 671-686
- 58 Wood BL. Acute myeloid leukemia minimal residual disease detection: the difference from normal approach. Curr Protoc Cytom 2020; 93 (01) e73
- 59 Wood BL. Flow cytometric monitoring of residual disease in acute leukemia. Methods Mol Biol 2013; 999: 123-136
- 60 Zhou Y, Wood BL. Methods of detection of measurable residual disease in AML. Curr Hematol Malig Rep 2017; 12 (06) 557-567
- 61 Bruserud Ø, Aasebø E, Hernandez-Valladares M, Tsykunova G, Reikvam H. Therapeutic targeting of leukemic stem cells in acute myeloid leukemia: the biological background for possible strategies. Expert Opin Drug Discov 2017; 12 (10) 1053-1065
- 62 Canali A, Vergnolle I, Bertoli S. et al. Prognostic impact of unsupervised early assessment of bulk and leukemic stem cell measurable residual disease in acute myeloid leukemia. Clin Cancer Res 2023; 29 (01) 134-142
- 63 Tembhare PR, Subramanian Pg Bertolli, Ghogale S. et al. A high-sensitivity 10-color flow cytometric minimal residual disease assay in B-lymphoblastic leukemia/lymphoma can easily achieve the sensitivity of 2-in-106 and is superior to standard minimal residual disease assay: a study of 622 patients. Cytometry B Clin Cytom 2020; 98 (01) 57-67
- 64 Tembhare PR, Chatterjee G, Khanka T. et al. Eleven-marker 10-color flow cytometric assessment of measurable residual disease for T-cell acute lymphoblastic leukemia using an approach of exclusion. Cytometry B Clin Cytom 2021; 100 (04) 421-433
- 65 Aanei CM, Veyrat-Masson R, Selicean C. et al. Database-guided analysis for immunophenotypic diagnosis and follow-up of acute myeloid leukemia with recurrent genetic abnormalities. Front Oncol 2021; 11: 746951
- 66 Piñero P, Morillas M, Gutierrez N. et al. Identification of leukemia-associated immunophenotypes by databaseguided flow cytometry provides a highly sensitive and reproducible strategy for the study of measurable residual disease in acute myeloblastic leukemia. Cancers (Basel) 2022; 14 (16) 4010
- 67 Zeijlemaker W, Kelder A, Cloos J, Schuurhuis GJ. Immunophenotypic detection of measurable residual (stem cell) disease using LAIP approach in acute myeloid leukemia. Curr Protoc Cytom 2019; 91 (01) e66
- 68 Buccisano F, Palmieri R, Piciocchi A. et al. Clinical relevance of an objective flow cytometry approach based on limit of detection and limit of quantification for measurable residual disease assessment in acute myeloid leukemia. A post-hoc analysis of the GIMEMA AML1310 trial. Haematologica 2022; 107 (12) 2823-2833
- 69 Paras G, Morsink LM, Othus M. et al. Conditioning intensity and peritransplant flow cytometric MRD dynamics in adult AML. Blood 2022; 139 (11) 1694-1706
- 70 Walter RB, Buckley SA, Pagel JM. et al. Significance of minimal residual disease before myeloablative allogeneic hematopoietic cell transplantation for AML in first and second complete remission. Blood 2013; 122 (10) 1813-1821
- 71 Norkin M, Katragadda L, Zou F. et al. Minimal residual disease by either flow cytometry or cytogenetics prior to an allogeneic hematopoietic stem cell transplant is associated with poor outcome in acute myeloid leukemia. Blood Cancer J 2017; 7 (12) 634
- 72 Liu J, Ma R, Liu YR. et al. The significance of peri-transplantation minimal residual disease assessed by multiparameter flow cytometry on outcomes for adult AML patients receiving haploidentical allografts. Bone Marrow Transplant 2019; 54 (04) 567-577
- 73 Nagler A, Baron F, Labopin M. et al. Measurable residual disease (MRD) testing for acute leukemia in EBMT transplant centers: a survey on behalf of the ALWP of the EBMT. Bone Marrow Transplant 2021; 56 (01) 218-224
- 74 Fasan O. Using minimal (measurable) residual disease assessments to guide decision-making for timing of allogeneic transplantation in acute myeloid leukemia. Curr Opin Hematol 2019; 26 (06) 413-420
- 75 Guolo F, Di Grazia C, Minetto P. et al. Pre-transplant minimal residual disease assessment and transplant-related factors predict the outcome of acute myeloid leukemia patients undergoing allogeneic stem cell transplantation. Eur J Haematol 2021; 107 (05) 573-582
- 76 Klyuchnikov E, Christopeit M, Badbaran A. et al. Role of pre-transplant MRD level detected by flow cytometry in recipients of allogeneic stem cell transplantation with AML. Eur J Haematol 2021; 106 (05) 606-615
- 77 Oran B, Jorgensen JL, Marin D. et al. Pre-transplantation minimal residual disease with cytogenetic and molecular diagnostic features improves risk stratification in acute myeloid leukemia. Haematologica 2017; 102 (01) 110-117
- 78 Shen X, Pan J, Qi C. et al. Impact of pre-transplantation minimal residual disease (MRD) on the outcome of Allogeneic hematopoietic stem cell transplantation for acute leukemia. Hematology 2021; 26 (01) 295-300
- 79 Rossi G, Carella AM, Minervini MM. et al. Optimal time-points for minimal residual disease monitoring change on the basis of the method used in patients with acute myeloid leukemia who underwent allogeneic stem cell transplantation: a comparison between multiparameter flow cytometry and Wilms' tumor 1 expression. Leuk Res 2015; 39 (02) 138-143
- 80 Zhou Y, Othus M, Araki D. et al. Pre- and post-transplant quantification of measurable (“minimal”) residual disease via multiparameter flow cytometry in adult acute myeloid leukemia. Leukemia 2016; 30 (07) 1456-1464
- 81 Klyuchnikov E, Badbaran A, Massoud R. et al. Post-transplantation day +100 minimal residual disease detection rather than mixed chimerism predicts relapses after allogeneic stem cell transplantation for intermediate-risk acute myelogenous leukemia patients undergoing transplantation in complete remission. Transplant Cell Ther 2022; 28 (07) 374.e1-374.e9
- 82 Meur GL, Plesa A, Larcher MV. et al. Impact on outcome of minimal residual disease after hematopoietic stem cell transplantation with fludarabine, amsacrine, and cytosine arabinoside-busulfan conditioning: a retrospective monocentric study. Transplant Cell Ther 2023; 29 (01) 38.e1-38.e9
- 83 Winters AC, Bosma G, Abbott D. et al. Outcomes are similar after allogeneic hematopoietic stem cell transplant for newly diagnosed acute myeloid leukemia patients who received venetoclax + azacitidine versus intensive chemotherapy. Transplant Cell Ther 2022; 28 (10) 694.e1-694.e9
- 84 Soh KT, Conway A, Liu X, Wallace PK. Development of a 27-color panel for the detection of measurable residual disease in patients diagnosed with acute myeloid leukemia. Cytometry A 2022; 101 (11) 970-983
- 85 Maag AH, Swanton H, Kull M, Vegi NM, Feuring M. Immunophenotypical profiling of myeloid neoplasms with erythroid predominance using mass cytometry (CyTOF). Cytometry A 2023; 1003 (07) 551-562