BAALC-Expressing Leukemia Hematopoietic Stem Cells and Their Place in the Study of CBF-Positive Acute Myeloid Leukemias in Children and Adults

MM Kanunnikov, NN Mamaev, TL Gindina, AI Shakirova, AM Sadykov, SV Razumova, SN Bondarenko, LS Zubarovskaya

RM Gorbacheva Scientific Research Institute of Pediatric Oncology, Hematology and Transplantation; IP Pavlov First Saint Petersburg State Medical University, 6/8 L’va Tolstogo ul., Saint Petersburg, Russian Federation, 197022

For correspondence: Prof. Nikolai Nikolaevich Mamaev, MD, PhD, 6/8 L’va Tolstogo ul., Saint Petersburg, Russian Federation, 197022; e-mail: nikmamaev524@gmail.com

For citation: Kanunnikov MM, Mamaev NN, Gindina TL, et al. BAALC-Expressing Leukemia Hematopoietic Stem Cells and Their Place in the Study of CBF-Positive Acute Myeloid Leukemias in Children and Adults. Clinical oncohematology. 2023;16(4):387–98. (In Russ).

DOI: 10.21320/2500-2139-2023-16-4-387-398


ABSTRACT

Background. Due to changing views on pathogenesis, risk factors and therapy strategies in prognostically favorable CBF-positive acute myeloid leukemias[1] (AML), the expression monitoring of RUNX1/RUNX1T1 or CBFB/MYH11 fusion genes, as an additional evaluation of treatment outcomes, appears to be insufficient. This indicates the need to improve the monitoring of the CBF+ AML course by means of parallel measurements of BAALC expression levels which roughly correlate with the mass of BAALC-expressing leukemia hematopoietic stem cells (BAALC-e LHSC).

Aim. To improve the quality of assessing treatment outcomes with due account for expression levels of RUNX1/RUNX1T1 or CBFB/MYH11 fusion genes and the mass of BAALC-e LHSC and on this basis to pave the way for personalized CBF+ AML treatment.

Materials & Methods. This study enrolled 39 adult patients aged 20–81 years (median 32 years) and 8 children aged 2–18 years (median 12 years). Among them there were 20 females and 27 males. AML with inv(16)(p13;q22)/t(16;16) was identified in 19 patients, t(8;21)(q22;q22) was detected in 28 patients. BAALC, WT1, RUNX1/RUNX1T1, CBFB/MYH11 expression levels were measured by quantitative real-time PCR and related to the expression of the ABL1 expert gene.

Results. In 23 patients, inv(16) and t(8;21) appeared to be isolated. Additional multidirectional chromosomal changes were observed in 24 patients with inv(16) and in 18 patients with t(8;21). All enrolled patients showed increased BAALC expression. In the course of therapy, it was decreasing to the threshold value in 16/18 (89 %) patients. The evaluation of the mean BAALC expression levels in the pooled groups of children and adults with isolated findings of either inv(16) or t(8;21) showed the decrease of the BAALC-e LHSC mass only in children (= 0.049). The comparison of the mean WT1 expression levels in the pooled groups of children and adults with isolated and additional chromosomal abnormalities revealed their significant decrease in patients with complicated variants (= 0.023).

Conclusion. The case reports provided in this paper show that the molecular monitoring with serial measurements of fusion genes and BAALC gene expression levels in CBF+ AML patients can lay the basis for further improvement of personalized treatment strategies for these patients. In all likelihood, parallel measurements of the above gene expression levels will allow to establish the framework for decision-making concerning treatment extent and timely HSC transplantation.


[1] NOTE. CBF-positive acute myeloid leukemias are characterized by the presence of inv(16)(p13;q22)/t(16;16) or t(8;21)(q22;q22) in blast cells, incidence of 12–15 %, and favorable prognosis. (Scientific editor.)


Keywords: CBF+ AML, BAALC, WT1, RUNX1/RUNX1T1, and CBFB/MYH11 genes, molecular monitoring, chemotherapy, HSCT.

Received: March 15, 2023

Accepted: September 7, 2023

Read in PDF

Статистика Plumx английский

REFERENCES

  1. Sangle NA, Perkins S. Core-Binding Factor Acute Myeloid Leukemia. Arch Pathol. Lab Med. 2011;135(11):1504–9. doi: 10.5868/arpa.2010-0482-RS.
  2. Byrd JC, Dodge RK, Carroll A, et al. Patients with t(8;21)(q22;q22) and acute myeloid leukemia have superior failure-free and overall survival when repetitive cycles of high-dose cytarabine are administered. J Clin Oncol. 1999;17(12):3767–75. doi: 1200/jco.1999.17.12.3767.
  3. Byrd JC, Ruppert AS, Mrozek K, et al. Repetitive cycles of high-dose cytarabine benefit patients with acute myeloid leukemia and inv(16)(p13;q22) or t(16;16)(p13;q22): results from CALGB 8461. J Clin Oncol. 2004;22(6):1087–94. doi: 10.1200/JCO.2004.07.012.
  4. Begna KH, Xu X, Gangatet N, et al. Core-binding factor acute myeloid leukemia: Long-term outcome of 70 patients uniformly treated with “7+3”. Blood Cancer J. 2022;12(4):55. doi: 10.1038/s41408-022-00654-0.
  5. Schlenk RF, Benner A, Krauter J, et al. Individual Patient Data-Based Meta Analysis of Patients aged 16 to 60 Years with Core Binding Factor Acute Myeloid Leukemia: A Survey the German Acute Myeloid Leukemia Intergroup. J Clin Oncol. 2004;22(18):3741–50. doi: 10.1200/JCO.2004.03.012.
  6. Reikvam H, Hatfield KJ, Kittang AO, et al. Acute myeloid leukemia with the t(8;21) translocation: Clinical consequences and biological implications. J Biomed Biotechnol. 2011;2011:104631. doi: 10.1155/2011/104631.
  7. Goyama S, Mulloy JC. Molecular pathogenesis of core binding factor leukemia: current knowledge and future prospects. Int J Hematol. 2011;94(2):126–33. doi: 10.1007/s12185-011-0858-z.
  8. Lam K, Zhang D-E. RUNX1 and RUNX1-ETO: roles in hematopoiesis and leukemogenesis. Front Biosci. 2012;17(3):1120–39. doi: 10.2741/3977.
  9. Han C, Gao X, Li Y, et al. Characteristics of Cohesin Mutation in Acute Myeloid Leukemia and Its Clinical Significance. Front Oncol. 2021;11:579881. doi: 10.3389/fonc.2021.579881.
  10. Solh M, Yohe S, Weisdorf D, et al. Core-binding factor acute myeloid leukemia: Heterogeneity, monitoring, and therapy. Am J Hematol. 2014;89(12):1121–9. doi: 10.1002/ajh.23821.
  11. Paschka p, Du J, Schlenk RF, et al. Secondary Genetic Lesions in Acute Myeloid Leukemia with Inv(16) or t(16;16): A study of the German-Austrian AML Study Group (AMLSG). Blood. 2013;121(1):170–7. doi: 10.1182/blood-2012-05-431486.
  12. Krauth MT, Eder C, Alpermann T, et al. High number of additional genetic lesions in acute myeloid leukemia with t(8;21)/RUNX1-RUNX1T1: frequency and impact on clinical outcome. Leukemia. 2014;28(7):1449–58. doi: 10.1038/leu.2014.4.
  13. Гиндина Т.Л., Мамаев Н.Н., Бондаренко С.Н. и др. Результаты аллогенной трансплантации гемопоэтических стволовых клеток у больных острым миелоидным лейкозом c t(8;21)(q22;q22)/RUNX1-RUNX1T1 и дополнительными цитогенетическими аномалиями. Клиническая онкогематология. 2016;9(2):148–54. doi: 10.21320/2500-2139-2016-9-2-148-154.
    [Gindina TL, Mamaev NN, Bondarenko SN, et al. Results of Allogeneic Hematopoietic Stem Cell Transplantation in Patients with Acute Myeloid Leukemia with t(8;21)(q22;q22)/RUNX1-RUNX1T1 and Additional Cytogenetic Abnormalities. Clinical oncohematology. 2016;9(2):148–54. doi: 10.21320/2500-2139-2016-9-2-148-154. (In Russ)]
  14. Christen F, Hoyer K, Yoshida K, et al. Genomic landscape and clonal evolution of acute myeloid leukemia with t(8;21): an international study on 331 patients. Blood. 2019;133(10):1140–51. doi: 10.1182/blood-2018-05-852822.
  15. Allen C, Hills RK, Lamb R, et al. The importance of Relative Mutant Level for Evaluation Impact on Outcome of KIT, FLT3 and CBL Mutations in Core-Binding Factor Acute Myeloid Leukemia. 2013;27(9):1891–901. doi: 10.1038/leu.2013.186.
  16. Sood R, Hansen NF, Donovan FX, et al. Somatic mutational landscape of AML with inv(16) or t(8;21) identifies patterns of clonal evolution in relapse leukemia. Leukemia. 2016;30(2):501–4. doi: 10.1038/leu.2015.141.
  17. Ishikawa Y, Kawashima N, Atsuta Y, et al. Prospective Evaluation of Prognostic Impact of Kit Mutations on Acute Myeloid Leukemia with RUNX1-RUNX1T1 and CBFB-MYH11. Blood Adv. 2020;4(1):66–75. doi: 10.1182/bloodadvances.2019000709.
  18. Jahn N, Terzer T, Strang Str E. et al. Genomic Heterogeneity in Core-Binding Factor Acute Myeloid Leukemia and its Clinical Implications. Blood Adv. 2020;4(21):6342–52. doi: 10.1182/bloodadvances.2020002673.
  19. Opatz S, Bamopoulos SA, Metzeler KH, et al. The Clinical Mutatome of Core Binding Factor Leukemia. 2020;34(6):1553–62. doi: 10.1038/s41375-019-0697-0.
  20. Zhen T, Cao Y, Ren G. et al. RUNX1 and CBFβ-SMMHC transactive target genes together in abnormal myeloid progenitors for leukemia development. Blood. 2020;136(21):2373–85. doi: 10.1182/blood.2020007747.
  21. Al-Harbi S, Aljurf M, Mothy M, et al. An update on the molecular pathogenesis and potential therapeutic targeting of AML with t(8;21)(q22;q22.1); RUNX1-RUNX1T1. Blood Adv. 2020;4(1):229–38. doi: 10.1182/bloodadvances.2019000168.
  22. Mao X, Yin R, Liu L, et al. Clinical impact of c-KIT and CEBPA mutations in 33 patients with corebinding factor (Non-M3) acute myeloid leukemia. Pediatr Neonatol. 2022;64(4):435–41. doi: 10.1016/j.pedneo.2022.05.020.
  23. Kayser S, Kramer M, Martinez-Cuadron D, et al. Characteristics and outcome of patients with core-binding factor acute myeloid leukemia and FLT3-ITD: results from an international collaborative study. Haematologica. 2022;107(4):836–43. doi: 10.3324/haematol.2021.278645.
  24. Rege K, Swansbury GJ, Atra AA, et al. Disease features in acute myeloid leukemia with t(8;21)(q22;q22). Influence of age, secondary karyotype abnormalities, CD19 status, and extramedullary leukemia on survival. Leuk Lymphoma. 2000;40(1–2):67–77. doi: 10.3109/10428190009054882.
  25. Marcucci G, Mrozek K, Ruppert AS, et al. Prognostic factors and Outcome of Core Binding Factor Acute Myeloid Leukemia Patients with t(8;21) Differ from those of Patients with inv(16): A Cancer and Leukemia Group B Study. J Clin Oncol. 2005;23(24):5705–17. doi: 10.1200/JCO.2005.15.610.
  26. Mosna F, Papayannidis C, Martinelli G, et al. Complex karyotype, older age, and reduced first-line dose intensity determine poor survival in core binding factor acute myeloid leukemia patients with long-term follow-up. Am J Hematol. 2015;90(6):515–23. doi: 10.1002/ajh.24000.
  27. Ustun C, Morgan EA, Ritz EM, et al. Core-binding factor acute myeloid leukemia with inv(16): Older age and high white blood cell count are risk factors for treatment failure. Int J Lab Hematol. 2021;43(1):e19-e25. doi: 10.1111/ijlh.13338.
  28. Marcault C, Boissel N, Haferlach C, et al. Prognostic of Core Binding Factor (CBF) Acute myeloid Leukemia with Complex Karyotype. Clin Lymphoma Myeloma Leuk. 2021;22(3):e199–e205. doi: 10.1016/j.clml.2021.09.007.
  29. Wei H, Wang Y, Gale RB, et al. Randomized Trial of Intermediate-dose Cytarabine in Induction and Consolidation Therapy in Adults with Acute Myeloid Leukemia. Clin Cancer Res. 2020;26(13):3154–61. doi: 10.1158/1078-0432.CCR-19-3433.
  30. Chen G, Yang J, Cao F, et al. The prognostic benefit from intermediate-dose cytarabine as consolidation therapy varies by cytogenetic subtype in t(8;21) acute myeloid leukemia: a retrospective cohort study. Ann Transl Med. 2022;10(16):858. doi: 10.21037/atm-22-2965.
  31. Shen Y, Zhang Y, Chang J, et al. CAG (cytarabine, aclarubicine and granulocytic colony-stimulating factor) regimen for core binding acute myeloid leukemia with measurable residual disease. Res Square. 2022; doi: 10.21203/rs.3.rs-2234776/v1.
  32. Yoon JH, Kim HJ, Kim JW, et al. Identification of Molecular and Cytogenetic Risk Factors for Unfavorable Core-Binding-Factor- Positive Adult AML with Post-Remission Treatment Outcome Analysis Including Transplantation. Bone Marrow Transplant. 2014;49(12):1466–74. doi: 10.1038/bmt.2014.180.
  33. Xiaosu Z, Leqing C, Yazhen Q, et al. Classifying AML Patients with inv(16) into high-risk and low-risk relapsed patients based on peritransplantation minimal residual disease determined by CBFβ/MYH11 gene expression. Ann Hematol. 2019;98(1):73–81. doi: 10.1007/s00277-018-3480-9.
  34. Kuwatsuka S, Miyamura K, Suzuki R, et al, Hematopoietic stem cell transplantation for core binding factor acute myeloid leukemia t(8;21) and inv(16) represent different clinical outcomes. 2009;113(9):2096–103. doi: 10.1182/blood-2008-03-145862.
  35. Mizutani M, Hara M, Fujita H, et al. Comparable outcomes between autologous and allogeneic transplant for adult acute myeloid leukemia in first CR. Bone Marrow Transplant. 2016;51(5):645–53. doi: 10.1038/bmt.2015.349.
  36. Byun JM, Shin D-Y, Koh Y, et al. Survival disparities in patients with relapsed core-binding factor acute myeloid leukemia following allogeneic hematopoietic stem cell transplantation. Int J Clin Exp Med. 2016;9(12):23285–93.
  37. Beyar-Katz O, Lavi N, Ringelstein-Harlev S, et al. Superior outcome of patients with favorable-risk acute myeloid leukemia using consolidation with autologous stem cell transplantation. Leuk Lymphoma. 2019;60(10):2449–56. doi: 10.1080/10428194.2019.1594214.
  38. Hu GH, Chemg YE, Lu AD, et al. Allogeneic hematopoietic stem cell transplantation can improve the prognosis of high-risk pediatric t(8;21) acute myeloid leukemia in first remission based on MRD-guided treatment. BMC Cancer. 2020;20(1):553. doi: 10.1186/s12885-020-07043-5.
  39. Choi EJ, Lee JH, Kim H, et al. Autologous hematopoietic cell transplantation following high-dose cytarabine consolidation for core-binding factor acute myeloid leukemia in first complete remission: a phase 2 prospective trial. Int J Hematol. 2021;113(6):851–60. doi: 10.1007/s12185-021-03099-6.
  40. Capria S, Trisolini SM, Diverio D, et al. Autologous stem cell transplantation in favorable-risk acute myeloid leukemia: single-center experience and current challenges. Int J Hematol. 2022;116(4):586–93. doi: 10.1007/s12185-022-03370-4.
  41. Sula M, Bacher U, Leibundgut EO, et al. Excellent outcome after consolidation with autologous transplantation in patients with core binding factor acute myeloid leukemia. Bone Marrow Transplant. 2020;55(8):1690–3. doi: 10.1038/s41409-019-0762-3.
  42. Halaburda K, Labopin M, Mailhol A, et al. Allogeneic stem cell transplantation in second complete remission for core binding factor acute myeloid leukemia: a study from the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation. Haematologica. 2020;105(6):1723–30. doi: 10.3324/haematol.2019.222810.
  43. Wang T, Chen S, Chen J, et al. Allogeneic Hematopoietic Stem Cell Transplantation Improved Survival for Adult Core Binding Factor Acute Myelogenous Leukemia Patients with Intermediate- and Adverse-Risk Genetics in the 2017 European LeukemiaNet. Transplant Cell Ther. 2021;27(2):173.e1–173.e9. doi: 10.1016/j.jtct.2020.10.010.
  44. Ustun C, Morgan E, Moodie EEM, et al. Core-binding factor acute myeloid leukemia with t(8;21): Risk factors and a novel scoring system (I-CBFit). Cancer Med. 2018;7(9):4447–55. doi: 10.1002/cam4.1733.
  45. Martin G, Barragan E, Bolufer P, et al. Relevance of Presenting White Blood Cells Count and Kinetic of Molecular Remission in the Prognosis of Acute Myeloid Leukemia with CBFbeta/MYH11 Rearrangements. Haematologica. 2000;85(7):699–703.
  46. Delaunay J, Vey N, Leblanc T, et al. Prognosis of inv(16)/t(16;16) Acute Myeloid Leukemia (AML): A Survey of 110 Cases from the French AML Intergroup. Blood. 2003;102(2):462–9. doi: 10.1182/blood-2002-11-3527.
  47. Appelbaum FR, Kopecky KI, Tallman MS, et al. The clinical spectrum of adult acute myeloid leukemia associated with core binding factor translocations. Br J Haematol. 2006;135(2):165–73. doi: 10.1111/j.1365-2141.2006.06276.x
  48. Jourdan E, Boissel N, Chevret S, et al. Prospective evaluation of gene mutations and minimal residual disease in patients with core binding factor acute myeloid leukemia. Blood. 2013;121(12):2213–23. doi: 10.1182/blood-2012-10-462879.
  49. Hoyos M, Nomdedeu JF, Esteve J, et al. Core Binding Factor Acute Myeloid Leukemia: The impact of Age, Leukocyte Count, Molecular Findings and Minimal Residual Disease. Eur J Haematol. 2013;91(3):209–18. doi: 10.1111/ejh.12130.
  50. Brunner AM, Blonquist TM, Sadrzadeh H, et al. Population-Based Disparities in Survival Among Patients with Core-Binding Factor Acute Myeloid Leukemia: A SEEP Database Analyze. Leuk Res. 2014:38(7):773–80. doi: 10.1016/j.leukres. 2014.04.001.
  51. Jung HAE, Maeng CH, Park S, et al. Prognostic Factor Analysis in Core-Binding Factor-positive Acute Myeloid Leukemia. Anticancer Res. 2014;34(2):1037–45.
  52. Duployez N, Willekens C, Marceau-Renout A, et al. Prognosis and monitoring of core-binding factor acute myeloid leukemia: current and emerging factors. Exp Rev Hematol. 2015;8(1):43–56. doi: 10.1586/17474086.2014.976551.
  53. Talami A, Bettelli F, Pioli V, et al. How to improve Prognostification in Acute Myeloid Leukemia with CBFB-MYH11 Fusion Transcript: Focus on the Role of Molecular Measurable Residual Disease (MRD) Monitoring. 2021;9(8):958. doi: 10.3390/biomedicines9089953.
  54. Tobal K, Newton J, Macheta M, et al. Molecular quantitation of minimal residual disease in acute myeloid leukemia with t(8;21) can identify patients in durable remission and predict clinical relapse. Blood. 2000;95(3):815–9.
  55. Corbaciouglu A, Scholl C, Schlenk RF, et al. Prognostic impact of minimal residual disease in CBF-MYH11-positive acute myeloid leukemia. J Clin Oncol. 2010;28(23):3724–9. doi: 10.1200/JCO.2010.28.6468.
  56. Wang Y, Wu DP, Liu QF, et al. In adults with t(8;21)AML posttransplant RUNX1/RUNX1T1-based MRD monitoring, rather than c-KIT mutations, allows further risk stratification. Blood. 2014;124(12):1880–6. doi: 10.1182/blood-2014-03-563403.
  57. Wang T, Zhou B, Zhang J, et al. Allogeneic hematopoietic stem cell transplantation could improve survival for pure CBF-AML patients with minimal residual disease positive after the second consolidation. Leuk Lymphoma. 2021;62(4):995–8. doi: 10.1080/10428194.2020.1846736.
  58. Konuma T, Kondo T, Masuko M, et al. Prognostic value of measurable residual disease at allogeneic transplantation for adults with core binding factor acute myeloid leukemia in complete remission. Bone Marrow Transplant. 2021;56(11):2779–87. doi: 10.1038/s41409-021-01409-4.
  59. Duan W, Liu X, Jia J, et al. The loss of absence of minimal residual disease of < 0.1% at any time after two cycles of consolidation chemotherapy in CBFB-MYH11-positive acute myeloid leukemia indicates poor prognosis. Br J Haematol. 2021;192(2):265–71. doi: 10.1111/bjh.16745.
  60. Duan W, Liu X, Zhao X, et al. Both the Subtypes of KIT Mutation and Minimal Residual Disease Are Associated with Prognosis in Core Binding Factor Acute Myeloid Leukemia: A Retrospective Clinical Cohort Study in Single Center. Ann Hematol. 2021;100(5):1203–12. doi: 10.1007/s00277-021-04432-z.
  61. Kurosawa S, Miyawaki S, Yamaguchi T, et al. Prognosis of patients with core and minimal residual disease. Eur J Haematol. 2013;91(3):209–18. doi: 10.1111/ejh.12130.
  62. Rucker F, Agrawal M, Corbaciouglu A, et al. Measurable Residual Disease Monitoring in Acute Myeloid Leukemia with t(8;21)(q22;q22.1): Results of the AML Study Group. Blood. 2019;134(19):1608–18. doi: 10.1182/blood.2019001425.
  63. Yalniz FE, Patel KP, Bashir Q, et al. Significance of Minimal Residual Disease Monitoring by Real-Time Quantitative Polymerase Chain Reaction in Core Binding Factor Acute Myeloid Leukemia for Transplantation Outcomes. Cancer. 2020;126(10):2183–92. doi: 10.1002/cncr.32769.
  64. Rotchanapanya W, Hokland P, Tunsing P, et al. Clinical Outcomes Based on Measurable Residual Disease Status in Patients with Core-Binding Factor Acute Myeloid Leukemia: A Systematic Review and Meta-Analysis. J Pers Med. 2020;10(4):250. doi: 10.3390/jpm.10040250.
  65. Wiemels JL, Xiao Z, Buffler PA, et al. In utero origin of t(8;21) AML-ETO translocations in childhood acute myeloid leukemia. B 2002;99(10):3801–5. doi: 10.1182/blood.v99.10.3801.
  66. Nicifora G, Larson RA, Rowley JD. Persistence of the 8;21 translocation in patients with acute myeloid leukemia type M2 in long-term remission. 1993;82(3):712–5.
  67. Yoon J-H, Kim H-J, Shin S-H, et al. BAALC and WT1 expressions from diagnosis to hematopoietic stem cell transplantation: consecutive monitoring in adult patients with core-binding-factor-positive AML. Eur J Haematol. 2013;91(2):112–21. doi: 10.1111/ejh.12142.
  68. Mamaev NN, Shakirova AI, Barkhatov IM, et al. Crucial role of BAALC-expressing leukemic precursors in origin and development of posttransplant relapses in patients with acute myeloid leukemias. Hematol Transfus Int J. 2020;8(6):127–31. doi: 10.15406/htij.2020.08.00240.
  69. Mamaev NN, Shakirova AI, Kanunnikov MM. BAALC-expressing Cells in Acute Leukemia and Myelodysplastic Syndromes: Present and Future. Generis Publishing; 2022. 98 p.
  70. McGowan-Jordan J, Hastings RJ, Moore S, eds. An International System for Human Cytogenomic Nomenclature (2020). Basel; 2020. 170 p. doi: 10.1159/isbn.978-3-318-06867-2.
  71. Shakirova AI, Mamaev NN, Barkhatov IM, et al. Clinical significance of BAALC overexpression for prediction post-transplant relapses in acute myeloid leukemia. Cell Ther Transplant. 2019;8(2):45–57. doi: 10.18620/ctt-1866-8836-02019-8-2-45-57.
  72. Гудожникова Я.В., Мамаев Н.Н., Бархатов И.М. и др. Результаты молекулярного мониторинга в посттрансплантационный период с помощью серийного исследования уровня экспрессии гена WT1 у больных острыми миелоидными лейкозами. Клиническая онкогематология. 2018;11(3):241–51. doi: 10.21320/2500-2139-2018-11-3-241-251.
    [Gudozhnikova YaV, Mamaev NN, Barkhatov IM, et al. Results of Molecular Monitoring in Posttransplant Period by Means of Series Investigation of WT1 Gene Expression in Patients with Acute Myeloid Leukemia. Clinical oncohematology. 2018;11(3):241–51. doi: 10.21320/2500-2139-2018-11-3-241-251. (In Russ)]
  73. Gottardi M, Mosna F, De Angeli S, et al. Clinical and Experimental Efficacy of Gemtuzumab Ozogamicin in Core Binding Factor Acute Myeloid Leukemia. Hematol Rep. 2017;9(3):87–90. doi: 10.4081/hr.2017.7028.
  74. Mansoor N, Jabbar N, Arshed U, et al. Outcome of Core Binding Factor Acute Leukemia in Children: A Single-Center Experience. J Pediatr Hematol Oncol. 2020;42(6):e423–e427. doi: 10.1097/MPH.0000000000001853.
  75. Baul SN, Baveja A, Kumar P, et al. A glimpse into translocation (8;21) in acute myeloid leukemia: Profile and therapeutic outcomes from a tertiary care hematology center from East India. J Hematol Allied Sci. 2022;2(3):85–90. doi: 10.25259/JHAS_1_2022.
  76. Borthakur G, Kantarjian H. Core binding factor acute myelogenous leukemia-2021 treatment algorithm. Blood Cancer. 2021;11(6):114. doi: 10.1038/s31408-021-00503-06.
  77. Surapally S, Tanen DG, Pullkan AA. Emerging therapies for inv(16) AML. Blood. 2021;137(9):2579–84. doi: 10.1182/blood.2020008971.
  78. Fan S, Shen MZ, Zhang XH, et al. Preemptive Immunotherapy for Minimal Residual Disease in Patients With t(8;21) Acute Myeloid Leukemia after Allogeneic Hematopoietic Stem Cell Transplantation. Front Oncol. 2022;11(10):773394. doi: 3389/fonc.2021.773394.
  79. Cooperrider JH, Shukla N, Nawas MT, Patel AA. The Cup Runneth Over: Treatment Strategies for Newly Diagnosed Acute Myeloid Leukemia. JCO Oncol Pract. 2023;19(2):74–85. doi: 10.1200/OP.22.00342.