138
Views
0
CrossRef citations to date
0
Altmetric
REVIEW

Role of Measurable Residual Disease in Older Adult Acute Myeloid Leukemia

& ORCID Icon
Pages 921-931 | Received 19 Feb 2023, Accepted 25 May 2023, Published online: 07 Jun 2023

References

  • Jemal A, Tiwari R, Murray T, et al. Cancer statistics, 2004. CA Cancer J Clin. 2004;54(1):8–29. doi:10.3322/canjclin.54.1.8
  • Appelbaum FR, Gundacker H, Head DR, et al. Age and acute myeloid leukemia. Blood. 2006;107(9):3481–3485. doi:10.1182/blood-2005-09-3724
  • Dohner H, Estey EH, Amadori S, et al. Diagnosis and management of acute myeloid leukemia in adults: recommendations from an international expert panel, on behalf of the European LeukemiaNet. Blood. 2010;115(3):453–474. doi:10.1182/blood-2009-07-235358
  • Kantarjian H, Ravandi F, O’Brien S, et al. Intensive chemotherapy does not benefit most older patients (age 70 years or older) with acute myeloid leukemia. Blood. 2010;116(22):4422–4429. doi:10.1182/blood-2010-03-276485
  • Short N, Ravandi F. How close are we to incorporating measurable residual disease into clinical practice for acute myeloid leukemia? Haematologica. 2019;104(8):1532–1541. doi:10.3324/haematol.2018.208454
  • Buccisano F, Dillon R, Freeman SD, Venditti A. Role of minimal (measurable) residual disease assessment in older patients with acute myeloid leukemia. Cancers. 2018;10(7):215. doi:10.3390/cancers10070215
  • Gale RP, Hochhaus A. Therapy of older persons with acute myeloid leukemia. Leukemia. 2015;29(4):759. doi:10.1038/leu.2014.337
  • McClune BL, Weisdorf DJ, Pedersen TL, et al. Effect of age on outcome of reduced-intensity hematopoietic cell transplantation for older patients with acute myeloid leukemia in first complete remission or with myelodysplastic syndrome. J Clin Oncol. 2010;28(11):1878–1887. doi:10.1200/JCO.2009.25.4821
  • Boddu P, Jorgensen J, Kantarjian H, et al. Achievement of a negative minimal residual disease state after hypomethylating agent therapy in older patients with AML reduces the risk of relapse. Leukemia. 2018;32(1):241–244. doi:10.1038/leu.2017.285
  • Foran J. Frontline therapy of AML: should the older patient be treated differently?. Curr Hematol Malig Rep. 2014;9(2):100–108. doi:10.1007/s11899-014-0211-8
  • 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. doi:10.1182/blood-2017-09-801498
  • Hourigan C, Karp J. Minimal residual disease in acute myeloid leukaemia. Nat Rev Clin Oncol. 2013;10(8):460–471. doi:10.1038/nrclinonc.2013.100
  • Hokland P, Ommen H. Towards individualized follow-up in adult acute myeloid leukemia in remission. Blood. 2011;117(9):2577–2584. doi:10.1182/blood-2010-09-303685
  • Buccisano F, Maurillo L, Del Principe M, et al. Prognostic and therapeutic implications of minimal residual disease detection in acute myeloid leukemia. Blood. 2012;119(2):332–341. doi:10.1182/blood-2011-08-363291
  • Fuda F, Chen W. Minimal/measurable residual disease detection in acute leukemias by multiparameter flow cytometry. Curr Hematol Malig Rep. 2018;13(6):455–466. doi:10.1007/s11899-018-0479-1
  • Freeman S, 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. doi:10.1200/jco.2013.49.1753
  • Ravandi F, Walter R, Freeman S. Evaluating measurable residual disease in acute myeloid leukemia. Blood Adv. 2018;2(11):1356–1366. doi:10.1182/bloodadvances.2018016378
  • Zink F, Stacey SN, Norddahl GL, et al. Clonal hematopoiesis, with and without candidate driver mutations, is common in the elderly. Blood. 2017;130(6):742–752. doi:10.1182/blood-2017-02-769869
  • Corces-Zimmerman MR, Majeti R. Pre-leukemic evolution of hematopoietic stem cells: the importance of early mutations in leukemogenesis. Leukemia. 2014;28(12):2276–2282. doi:10.1038/leu.2014.211
  • Amatangelo MD, Quek L, Shih A, et al. Enasidenib induces acute myeloid leukemia cell differentiation to promote clinical response. Blood. 2017;130(6):732–741. doi:10.1182/blood-2017-04-779447
  • Dohner H, Estey E, Grimwade D, et al. Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood. 2017;129(4):424–447. doi:10.1182/blood-2016-08-733196
  • Genovese G, Kahler AK, Handsaker RE, et al. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. New Engl J Med. 2014;371(26):2477–2487. doi:10.1056/NEJMoa1409405
  • 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(11):2220–2231. doi:10.1182/blood-2009-03-213389
  • Pratcorona M, Brunet S, Nomdedeu J, et al. Favorable outcome of patients with acute myeloid leukemia harboring a low-allelic burden FLT3-ITD mutation and concomitant NPM1 mutation: relevance to post-remission therapy. Blood. 2013;121(14):2734–2738. doi:10.1182/blood-2012-06-431122
  • Ostronoff F, Othus M, Lazenby M, Estey E, Appelbaum FR. Prognostic significance of NPM1 mutations in the absence of FLT3-internal tandem duplication in older patients with acute myeloid leukemia: a SWOG and UK national cancer research institute/medical research council report. J Clin Oncol. 2015;33(15):1715. doi:10.1200/Jco.2015.62.4288
  • Prebet T, Boissel N, Reutenauer S, et al. Acute myeloid leukemia with translocation (8;21) or inversion (16) in elderly patients treated with conventional chemotherapy: a collaborative study of the French CBF-AML intergroup. J Clin Oncol. 2009;27(28):4747–4753. doi:10.1200/JCO.2008.21.0674
  • Ossenkoppele G, Schuurhuis G. MRD in AML: does it already guide therapy decision-making? Hematology Am Soc Hematol Educ Program. 2016;2016(1):356–365. doi:10.1182/asheducation-2016.1.356
  • Nomdedéu J, Hoyos M, Carricondo M, et al. Bone marrow WT1 levels at diagnosis, post-induction and post-intensification in adult de novo AML. Leukemia. 2013;27(11):2157–2164. doi:10.1038/leu.2013.111
  • Short N, Rytting M, Cortes J. Acute myeloid leukaemia. Lancet. 2018;392(10147):593–606. doi:10.1016/s0140-6736(18)31041-9
  • Prassek VV, Rothenberg-Thurley M, Sauerland MC, et al. Genetics of acute myeloid leukemia in the elderly: mutation spectrum and clinical impact in intensively treated patients aged 75 years or older. Haematologica. 2018;103(11):1853–1861. doi:10.3324/haematol.2018.191536
  • Aitken M, Ravandi F, Patel K, Short N. Prognostic and therapeutic implications of measurable residual disease in acute myeloid leukemia. J Hematol Oncol. 2021;14(1):137. doi:10.1186/s13045-021-01148-5
  • Smol T, Nibourel O, Marceau-Renaut A, et al. Quantification of EVI1 transcript levels in acute myeloid leukemia by RT-qPCR analysis: a study by the ALFA Group. Leuk Res. 2015;39(12):1443–1447. doi:10.1016/j.leukres.2015.09.021
  • 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(31):5195–5201. doi:10.1200/Jco.2009.22.4865
  • Gianfaldoni G, Mannelli F, Ponziani V, et al. Early reduction of WT1 transcripts during induction chemotherapy predicts for longer disease free and overall survival in acute myeloid leukemia. Haematol Hematol J. 2010;95(5):833–836. doi:10.3324/haematol.2009.011908
  • 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(5):1392–1404. doi:10.1038/s41375-021-01131-6
  • Metzeler KH, Becker H, Maharry K, et al. ASXL1 mutations identify a high-risk subgroup of older patients with primary cytogenetically normal AML within the ELN favorable genetic category. Blood. 2011;118(26):6920–6929. doi:10.1182/blood-2011-08-368225
  • Mendler JH, Maharry K, Radmacher MD, et al. RUNX1 mutations are associated with poor outcome in younger and older patients with cytogenetically normal acute myeloid leukemia and with distinct gene and MicroRNA expression signatures. J Clin Oncol. 2012;30(25):3109–3118. doi:10.1200/JCO.2011.40.6652
  • Gaidzik VI, Paschka P, Spath D, et al. TET2 mutations in acute myeloid leukemia (AML): results from a comprehensive genetic and clinical analysis of the AML study group. J Clin Oncol. 2012;30(12):1350–1357. doi:10.1200/JCO.2011.39.2886
  • Rucker FG, Schlenk RF, Bullinger L, et al. TP53 alterations in acute myeloid leukemia with complex karyotype correlate with specific copy number alterations, monosomal karyotype, and dismal outcome. Blood. 2012;119(9):2114–2121. doi:10.1182/blood-2011-08-375758
  • Young AL, Wong TN, Hughes AE, et al. Quantifying ultra-rare pre-leukemic clones via targeted error-corrected sequencing. Leukemia. 2015;29(7):1608–1611. doi:10.1038/leu.2015.17
  • Hiatt JB, Pritchard CC, Salipante SJ, O’Roak BJ, Shendure J. Single molecule molecular inversion probes for targeted, high-accuracy detection of low-frequency variation. Genome Res. 2013;23(5):843–854. doi:10.1101/gr.147686.112
  • Schmitt MW, Kennedy SR, Salk JJ, Fox EJ, Hiatt JB, Loeb LA. Detection of ultra-rare mutations by next-generation sequencing. Proc Natl Acad Sci U S A. 2012;109(36):14508–14513. doi:10.1073/pnas.1208715109
  • 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. doi:10.1182/blood-2014-05-577593
  • Mrozek K, Marcucci G, Nicolet D, et al. Prognostic significance of the European LeukemiaNet standardized system for reporting cytogenetic and molecular alterations in adults with acute myeloid leukemia. J Clin Oncol. 2012;30(36):4515–4523. doi:10.1200/Jco.2012.43.4738
  • Metzeler KH, Herold T, Rothenberg-Thurley M, et al. Spectrum and prognostic relevance of driver gene mutations in acute myeloid leukemia. Blood. 2016;128(5):686–698. doi:10.1182/blood-2016-01-693879
  • Dombret H, Seymour JF, Butrym A, et al. International phase 3 study of azacitidine vs conventional care regimens in older patients with newly diagnosed AML with >30% blasts. Blood. 2015;126(3):291–299. doi:10.1182/blood-2015-01-621664
  • Kantarjian HM, Thomas XG, Dmoszynska A, et al. Multicenter, randomized, open-label, phase III trial of decitabine versus patient choice, with physician advice, of either supportive care or low-dose cytarabine for the treatment of older patients with newly diagnosed acute myeloid leukemia. J Clin Oncol. 2012;30(21):2670–2677. doi:10.1200/jco.2011.38.9429
  • Schuh AC, Dohner H, Pleyer L, Seymour JF, Fenaux P, Dombret H. Azacitidine in adult patients with acute myeloid leukemia. Crit Rev Oncol Hematol. 2017;116:159–177. doi:10.1016/j.critrevonc.2017.05.010
  • Kadia TM, Cortes J, Ravandi F, et al. Cladribine and low-dose cytarabine alternating with decitabine as front-line therapy for elderly patients with acute myeloid leukaemia: a Phase 2 single-arm trial. Lancet Haematol. 2018;5(9):e411–e421. doi:10.1016/S2352-3026(18)30132-7
  • DiNardo CD, Pratz K, Pullarkat V, et al. Venetoclax combined with decitabine or azacitidine in treatment-naive, elderly patients with acute myeloid leukemia. Blood. 2019;133(1):7–17. doi:10.1182/blood-2018-08-868752
  • DiNardo CD, Jonas BA, Pullarkat V, et al. Azacitidine and venetoclax in previously untreated acute myeloid leukemia. New Engl J Med. 2020;383(7):617–629. doi:10.1056/NEJMoa2012971
  • Maiti A, DiNardo C, Wang S, et al. Prognostic value of measurable residual disease after venetoclax and decitabine in acute myeloid leukemia. Blood Adv. 2021;5(7):1876–1883. doi:10.1182/bloodadvances.2020003717
  • Kadia TM, Reville PK, Wang X, et al. Phase II study of venetoclax added to cladribine plus low-dose cytarabine alternating with 5-azacitidine in older patients with newly diagnosed acute myeloid leukemia. J Clin Oncol. 2022;40(33):3848–3857. doi:10.1200/JCO.21.02823
  • Simoes C, Paiva B, Martinez-Cuadron D, et al. Measurable residual disease in elderly acute myeloid leukemia: results from the PETHEMA-FLUGAZA phase 3 clinical trial. Blood Adv. 2021;5(3):760–770. doi:10.1182/bloodadvances.2020003195
  • Hilberink JR, Morsink LM, van der Velden W, et al. Pretransplantation MRD in older patients with AML after treatment with decitabine or conventional chemotherapy. Transplant Cell Ther. 2021;27(3):246–252. doi:10.1016/j.jtct.2020.12.014
  • Walter RB, Gyurkocza B, Storer BE, et al. Comparison of minimal residual disease as outcome predictor for AML patients in first complete remission undergoing myeloablative or nonmyeloablative allogeneic hematopoietic cell transplantation. Leukemia. 2015;29(1):137–144. doi:10.1038/leu.2014.173
  • Foran JM, Sun ZX, Paietta E, et al. Minimal Residual Disease (MRD) at time of complete remission is commonly detected in Acute Myeloid Leukemia (AML) patients age ≥ 60 years and significantly impacts outcome based on post-remission treatment strategies: prospective analysis of ECOG-ACRIN (E-A) E2906 phase III trial. Blood. 2018;132. doi:10.1182/blood-2018-99-113950
  • Roboz GJ, Ravandi F, Wei AH, et al. Oral azacitidine prolongs survival of patients with AML in remission independently of measurable residual disease status. Blood. 2022;139(14):2145–2155. doi:10.1182/blood.2021013404
  • Oliai C, Schiller G. How to address second and therapy-related acute myelogenous leukaemia. Br J Haematol. 2020;188(1):116–128. doi:10.1111/bjh.16354
  • Walter R, Buckley S, Pagel J, 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. doi:10.1182/blood-2013-06-506725
  • Kharfan-Dabaja M. Guadecitabine for AML and MDS: hype or hope? Lancet Oncol. 2015;16(9):1009–1011. doi:10.1016/s1470-2045(15)00095-9
  • Wei A, Döhner H, Pocock C, et al. Oral azacitidine maintenance therapy for acute myeloid leukemia in first remission. N Engl J Med. 2020;383(26):2526–2537. doi:10.1056/NEJMoa2004444
  • Buccisano F, Maurillo L, Piciocchi A, et al. Minimal residual disease negativity in elderly patients with acute myeloid leukemia may indicate different postremission strategies than in younger patients. Ann Hematol. 2015;94(8):1319–1326. doi:10.1007/s00277-015-2364-5
  • Cornelissen J, Gratwohl A, Schlenk R, et al. The European LeukemiaNet AML working party consensus statement on allogeneic HSCT for patients with AML in remission: an integrated-risk adapted approach. Nat Rev Clin Oncol. 2012;9(10):579–590. doi:10.1038/nrclinonc.2012.150
  • Appelbaum FR. Incorporating hematopoietic cell transplantation (HCT) into the management of adults aged under 60 years with acute myeloid leukemia (AML). Best Pract Res Clin Haematol. 2008;21(1):85–92. doi:10.1016/j.beha.2007.11.013
  • Ustun C, Lazarus H, Weisdorf D. To transplant or not: a dilemma for treatment of elderly AML patients in the twenty-first century. Bone Marrow Transplant. 2013;48(12):1497–1505. doi:10.1038/bmt.2013.67