Acute Myeloid Leukemias After the Treatment of Classical Hodgkin’s Lymphoma: A Literature Review

AUTOIMMUNE THROMBOCYTOPENIA

AA Danilenko, SV Shakhtarina, NA Falaleeva

AF Tsyb Medical Radiological Research Centre, branch of the NMRC of Radiology, 4 Koroleva ul., Obninsk, Kaluga Region, Russian Federation, 249036

For correspondence: Anatolii Aleksandrovich Danilenko, MD, PhD, 4 Koroleva ul., Obninsk, Kaluga Region, Russian Federation, 249036; Tel.: +7(909)250-18-10; e-mail: danilenkoanatol@mail.ru

For citation: Danilenko AA, Shakhtarina SV, Falaleeva NA. Acute Myeloid Leukemias After the Treatment of Classical Hodgkin’s Lymphoma: A Literature Review. Clinical oncohematology. 2022;15(4):414–23. (In Russ).

DOI: 10.21320/2500-2139-2022-15-4-414-423

ABSTRACT

Second malignant tumors occurring in classical Hodgkin’s lymphoma (cHL) patients after treatment include mainly solid neoplasms and far more rarely acute myeloid leukemias (AML). At the same time, a relative risk of developing secondary AML substantially exceeds the risks of second (solid) tumors, and the efficacy of secondary AML treatment is considerably lower compared to the outcomes of primary AML treatment. All that implies the importance and relevance of this issue. The present literature review discusses the epidemiology of developing secondary AMLs in patents after cHL treatment. In addition to that, it focuses on modern drugs and technologies for effective treatment of secondary AMLs.

Keywords: classical Hodgkin’s lymphoma, secondary acute myeloid leukemias.

Received: April 15, 2022

Accepted: August 28, 2022

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Статистика Plumx английский

REFERENCES

  1. Kanzler H, Kuppers R, Hansmann ML, Rajewsky K. Hodgkin and Reed-Sternberg cells in Hodgkin’s disease represent the outgrowth of a dominant tumor clone derived from (crippled) germinal center B cells. J Exp Med. 1996;184(4):1495–505. doi: 10.1084/jem.184.4.1495.
  2. Devita VT, Serpick AA, Carbone PP. Combination chemotherapy in the treatment of advanced Hodgkin’s disease. Ann Intern Med. 1970;73(6):881–95. doi: 10.7326/0003-4819-73-6-881.
  3. Donaldson SS, Hancock SL, Hoppe RT. The Janeway lecture. Hodgkin’s disease—finding the balance between cure and late effects. Cancer J Sci Am. 1999;5:325–33.
  4. Borchmann P, Eichenauer DA, Engert A. State of the art in the treatment of Hodgkin lymphoma. Nat Rev Clin Oncol. 2012;9(8):450–9. doi: 10.1038/nrclinonc.2012.91.
  5. Federico M, Luminari S, Iannitto E, et al. ABVD compared with BEACOPP compared with CEC for the initial treatment of patients with advanced Hodgkin’s lymphoma: results from the HD2000 Gruppo Italiano per lo Studio dei Linfomi Trial. J Clin Oncol. 2009;27(5):805–11. doi: 10.1200/JCO.2008.17.0910.
  6. Sasse S, Brockelmann PJ, Georgen H, et al. Long-term follow-up of contemporary treatment in early-stage Hodgkin lymphoma: Updated analyses of the German Hodgkin Study Group HD7, HD8, HD10 and HD11 trials. J Clin Oncol. 2017;35(18):1999–2007. doi: 10.1200/JCO.2016.70.9410.
  7. Henry-Amar M, Joly F. Late complications after Hodgkin’s disease. Ann Oncol. 1996;7(Suppl 4):115–26. doi: 10.1093/annonc/7.suppl_4.s115.
  8. Hoppe RT. Hodgkin’s disease: complications of therapy and excess mortality. Ann Oncol. 1997;8(Suppl 1):115–8. doi: 10.1093/annonc/8.suppl_1.s115.
  9. Merli F, Luminari S, Gobbi PG, et al. Long-term results of the HD2000 Trial comparing ABVD versus BEACOPP versus COPP-EBV-CAD in untreated patients with advanced Hodgkin lymphoma: a study by Fondazione Italiana Linfomi. J Clin Oncol. 2016;34(11):1175–81. doi: 10.1200/jco.2015.62.4817.
  10. Hancock SL, Hoppe RT. Long-term complications of treatment and causes of mortality after Hodgkin’s disease. Semin Radiat 1996;6(3):225–42. doi: 10.1053/SRAO00600225.
  11. Dorr FA, Coltman CA Jr. Second cancers following antineoplastic therapy. Curr Probl Cancer. 1985;9(2):1–43. doi: 10.1016/s0147-0272(85)80033-7.
  12. Arseneau JC, Sponzo RW, Levin DL, et al. Nonlymphomatous malignant tumors complicating Hodgkin’s disease: possible association with intensive therapy. N Engl J Med. 1972;287(22):1119–22. doi: 10.1056/NEJM197211302872204.
  13. Brunning RD, Matutes E, Harris NL, et al. Acute myeloid leukemia. World Health Organization of Tumors Pathology and Genetics, Tumors of Haematopoietic and Lymphoid Tissues. Lyon: IARC Press; 2001. рр. 75–108. doi: 10.1182/blood-2002-04-1199.
  14. Shulman LN. The biology of alkylating-agent cellular injury. Hematol Oncol Clin North Am. 1993;7(2):325–35. doi: 10.1016/s0889-8588(18)30243-0.
  15. Tucker MA, Coleman CN, Cox RS, et al. Risk of second cancers after treatment for Hodgkin’s disease. N Engl J Med. 1988;318(2):76–81. doi: 10.1056/nejm198801143180203.
  16. van Leeuwen FE, Chorus AM, van den Belt-Dusebout AW, et al. Leukemia risk following Hodgkin’s disease: relation to cumulative dose of alkylating agents, treatment with teniposide combinations, number of episodes of chemotherapy, and bone marrow damage. J Clin Oncol. 1994;12(5):1063–73. doi: 10.1200/jco.1994.12.5.1063.
  17. Cosset JM, Henry-Amar M, Meerwaldt JH. Long-term toxicity of early stages of Hodgkin’s disease therapy: the EORTC experience. EORTC Lymphoma Cooperative Group. Ann Oncol. 1991;2(Suppl 2):77–82. doi: 10.1007/978-1-4899-7305-4_13.
  18. Park DJ, Koeffler HP. Therapy-related myelodysplastic syndromes. Semin Hematol. 1996;33(3):256–73.
  19. Abrahamsen JF, Andersen A, Hannisdal E, et al. Second malignancies after treatment of Hodgkin’s disease: the influence of treatment, follow-up time, and age. J Clin Oncol. 1993;11(2):255–61. doi: 10.1200/jco.1993.11.2.255.
  20. Glicksman AS, Pajak TF, Gottlieb A, et al. Second malignant neoplasms in patients successfully treated for Hodgkin’s disease: a Cancer and Leukemia Group B study. Cancer Treat Rep. 1982;66(4):1035–44.
  21. Delwail V, Jais JP, Colonna P, Andrieu JM. Fifteen-year secondary leukaemia risk observed in 761 patients with Hodgkin’s disease prospectively treated by MOPP or ABVD chemotherapy plus high-dose irradiation. Br J Haematol. 2002;118(1):189–94. doi: 10.1046/j.1365-2141.2002.03564.x.
  22. Coltman C, Dixon D. Second malignancies complicating Hodgkin’s disease: a Southwest Oncology Group 10-year follow-up. Cancer Treat Rep. 1982;66(4):1023–33.
  23. Aisenberg AC. Acute nonlymphocytic leukemia after treatment for Hodgkin’s disease. Am J Med. 1983;75(3):449–54. doi: 10.1016/0002-9343(83)90348-0.
  24. Coleman CN, Williams CJ, Flint AS, et al. Hematologic neoplasia in patients treated for Hodgkin’s disease. N Engl J Med. 1977;97(23):1249–52. doi: 10.1056/NEJM197712082972303.
  25. Holtzman AL, Stahl JM, Zhu S, et al. Does the Incidence of Treatment-Related Toxicity Plateau After Radiatio Therapy: The Long-Term Impact of Integral Dose in Hodgkin’s Lymphoma Survivors. Adv Radiat Oncol. 2019;4(4):699–705. doi: 10.1016/j.adro.2019.07.010.
  26. Henry-Amar M. Second cancer after the treatment of Hodgkin’s disease: a report from the International Database on Hodgkin’s disease. Ann Oncol. 1992;3(Suppl 4):117–28. doi: 10.1093/annonc/3.suppl_4.s117.
  27. Kaldor JM, Day NE, Clarke EA, et al. Leukemia following Hodgkin’s disease. N Engl J Med. 1990;322(1):7–13. doi: 10.1056/NEJM199001043220102.
  28. Brusamolino E, Anselmo AP, Klersy C, et al. The risk of acute leukemia in patients treated for Hodgkin’s disease is significantly higher after combined modality programs than after chemotherapy alone and is correlated with the extent of radiotherapy and type and duration of chemotherapy: a case-control study. Haematologica. 1998;83(9):812–23.
  29. Swerdlow AJ, Douglas AJ, Vaughan-Hudson G, et al. Risk of second primary cancers after Hodgkin’s disease by type of treatment: analysis of 2846 patients in the British National Lymphoma Investigation. Br J Med. 1992;304(6835):1137–43. doi: 10.1136/bmj.304.6835.1137.
  30. Schonfeld SJ, Gilbert ES, Dores GM, et al. Acute myeloid leukemia following Hodgkin lymphoma: a population-based study of 35,511 patients. J Natl Cancer Inst. 2006;98(3):215–8. doi: 10.1093/jnci/djj017.
  31. Pedersen-Bjergaard J, Specht L, Larsen SO, et al. Risk of therapy-related leukemia and preleukemia after Hodgkin’s disease. Lancet. 1987;2(8550):83–8. doi: 10.1016/s0140-6736(87)92744-9.
  32. Leone G, Voso MT, Sica S, et al. Therapy related leukemias: susceptibility, prevention and treatment. Leuk Lymphoma. 2001;41(3–4):255–76. doi: 10.3109/10428190109057981.
  33. Koontz MZ, Horning SJ, Balise R, et al. Risk of therapy-related secondary leukemia in Hodgkin lymphoma: the Stanford University experience over three generations of clinical trials. J Clin Oncol. 2013;31(5):592–8. doi: 10.1200/JCO.2012.44.5791.
  34. Andre MPE, Carde P, Viviani S, et al. Long-term overall survival and toxicities of ABVD vs BEACOPP in advanced Hodgkin lymphoma: A pooled analysis of four randomized trials. Cancer Med. 2020;9(18):6565–75. doi: 10.1002/cam4.3298.
  35. Skoetz N, Will A, Monsef I, et al. Comparison of first-line chemotherapy including escalated BEACOPP versus chemotherapy including ABVD for people with early unfavourable or advanced stage Hodgkin lymphoma. Cohrane Database Syst Rev. 2017;5(5):CD007941. doi: 10.1002/14651858.CD007941.pub3.
  36. Schaapveld M, Aleman BMP, van Eggermond AM, et al. Second Cancer Risk Up to 40 Years after Treatment for Hodgkin’s Lymphoma. N Engl J Med. 2015;373(26):2499–511. doi: 10.1056/NEJMoa1505949.
  37. Eichenauer DA, Thielen I, Haverkamp H, et al. Therapy-related acute myeloid leukemia and myelodysplastic syndromes in patients with Hodgkin lymphoma: a report from the German Hodgkin Study Group. Blood. 2014;123(11):1658–64. doi: 10.1182/blood-2013-07-512657.
  38. Eichenauer DA, Becker I, Monsef I, et al. Secondary malignant neoplasms, progression-free survival and overall survival in patients treated for Hodgkin lymphoma: a systematic review and meta-analysis of randomized clinical trials. Haematologica. 2017;102(10):1748–57. doi: 10.3324/haematol.2017.167478.
  39. Franklin J, Eichenauer DA, Becker I, et al. Optimisation of chemotherapy and radiotherapy for untreated Hodgkin lymphoma patients with respect to second malignant neoplasms, overall and progression-free survival: individual participant data analysis. Cohrane Database Syst Rev. 2017;9(9):CD008814. doi: 10.1002/14651858.CD008814.pub2.
  40. Scholz M, Engert A, Franklin J, et al. Impact of first- and second-line treatment for Hodgkin’s lymphoma on the incidence of AML/MDS and NHL – experience of the German Hodgkin’s Lymphoma Study Group analyzed by a parametric model of carcinogenesis. Ann Oncol. 2011;22(3):681–8. doi: 10.1093/annonc/mdq408.
  41. Leone G, Fianchi L, Voso MT. Therapy-related myeloid neoplasms. Curr Opin Oncol. 2011;23(6):672–80. doi: 10.1097/CCO.0b013e32834bcc2a.
  42. Kumar V, Garg M, Chandra AB, et al. Trends in the Risks of Secondary Cancers in Patients With Hodgkin Lymphoma. Clin Lymphoma Myeloma Leuk. 2018;18(9):576–89. doi: 10.1016/j.clml.2018.05.021.
  43. Baker KS, DeFor TE, Burns LJ, et al. New malignancies after blood or marrow stem-cell transplantation in children and adults: incidence and risk factors. J Clin Oncol. 2003;21(7):1352–8. doi: 10.1200/jco.2003.05.108.
  44. Bilmon IA, Ashton LJ, Le Marsney RE, et al. Second cancer risk in adults receiving autologous haematopoietic SCT for cancer: a population-based cohort study. Bone Marrow Transplant. 2014;49(5):691–8. doi: 10.1038/bmt.2014.13.
  45. Hodgson DC. Long-term toxicity of chemotherapy and radiotherapy in lymphoma survivors: optimizing treatment for individual patients. Clin Adv Hematol Oncol. 2015;13(2):103–12.
  46. Howe R, Micallef IN, Inwards DJ, et al. Secondary myelodysplastic syndrome and acute myelogenous leukemia are significant complications following autologous stem cell transplantation for lymphoma. Bone Marrow Transplant. 2003;32(3):317–24. doi: 10.1038/sj.bmt.1704124.
  47. Stone RM, Neuberg D, Soiffer R, et al. Myelodysplastic syndrome as a late complication following autologous bone marrow transplantation for non-Hodgkin’s lymphoma. J Clin Oncol. 1994;12(12):2535–42. doi: 10.1200/jco.1994.12.12.2535.
  48. Bhatia S. Therapy-related myelodysplasia and acute myeloid leukemia. Semin Oncol. 2013;40(6):666–75. doi: 10.1053/j.seminoncol.2013.09.013.
  49. Morton LM, Dores GM, Tucker MA, et al. Evolving risk of therapy-related acute myeloid leukemia following cancer chemotherapy among adults in the United States, 1975–2008. Blood. 2013;121(15):2996–3004. doi: 10.1182/blood-2012-08-448068.
  50. Krishnan A, Bhatia S, Slovak ML, et al. Predictors of therapy-related leukemia and myelodysplasia following autologous transplantation for lymphoma: an assessment of risk factors. Blood. 2000;95(5):1588–93. doi: 10.1182/blood.v95.5.1588.005k38_1588_1593.
  51. Pedersen-Bjergaard J, Andersen MK, Christiansen DH. Therapy-related acute myeloid leukemia and myelodysplasia after high-dose chemotherapy and autologous stem cell transplantation. Blood. 2000;95(11):3273–9. doi: 10.1182/blood.v95.11.3273.011k15_3273_3279.
  52. Andre M, Henry-Amar M, Blaise D, et al. Treatment-related deaths and second cancer risk after autologous stem cell transplantation for Hodgkin’s disease. Blood. 1998;92(6):1933–40. doi: 10.1182/blood.V92.6.1933.
  53. Hosing C, Munsell M, Yazji S, et al. Risk of therapy-related myelodysplastic syndrome/acute leukemia following high-dose therapy and autologous bone marrow transplantation for non-Hodgkin’s lymphoma. Ann Oncol. 2002;13(3):450–9. doi: 10.1093/annonc/mdf109.
  54. Kalaycio M, Rybicki L, Pohlman B, et al. Risk factors before autologous stem-cell transplantation for lymphoma predict for secondary myelodysplasia and acute myelogenous leukemia. J Clin Oncol. 2006;24(22):3604–10. doi: 10.1200/jco.2006.06.0673.
  55. Metayer C, Curtis RE, Vose J, et al. Myelodysplastic syndrome and acute myeloid leukemia after autotransplantation for lymphoma: a multicenter case–control study. Blood. 2003;101(5):2015–23. doi: 10.1182/blood-2002-04-1261.
  56. Miller JS, Arthur DC, Litz CE, et al. Myelodysplastic syndrome after autologous bone marrow transplantation: an additional late complication of curative cancer therapy. Blood. 1994;83(12):3780–6. doi: 10.1182/blood.v83.12.3780.3780.
  57. Yamasaki S, Suzuki R, Hatano K, et al. Therapy-related acute myeloid leukemia and myelodysplastic syndrome after hematopoietic cell transplantation for lymphoma. Bone Marrow Transplant. 2017;52(7):969–76. doi: 10.1038/bmt.2017.52.
  58. Ge I, Saliba RM, Maadani F. Age and number of apheresis days may predict for development of Secondary Myelodysplastic Syndrome and Acute Myelogenous Leukemia after transplantation for lymphomas. Transfusion. 2017;57(4):1052–7. doi: 10.1111/trf.14016.
  59. Josting A, Wiedenmann S, Franklin J, et al. Secondary myeloid leukemia and myelodysplastic syndromes in patients treated for Hodgkin’s disease: a report from the German Hodgkin’s Lymphoma Study Group. J Clin Oncol. 2003;21(18):3440–6. doi: 10.1200/JCO.2003.07.160.
  60. Hake CR, Graubert TA, Fenske TS. Does autologous transplantation directly increase the risk of secondary leukemia in lymphoma patients? Bone Marrow Transplant. 2007;39(2):59–70. doi: 10.1038/sj.bmt.1705547.
  61. Wong TN, Miller CA, Jotte MRM, et al. Cellular stressors contribute to the expansion of hematopoietic clones of varying leukemic potential. Nat Commun. 2018;9(1):455. doi: 10.1038/s41467-018-02858-0.
  62. Sharpless NE, DePinho RA. Telomeres, stem cells, senescence, and cancer. J Clin Invest. 2004;113(2):160–8. doi: 10.1172/JCI200420761.
  63. Forrest DL, Hogge DE, Nevill TJ, et al. High-dose therapy and autologous hematopoietic stem-cell transplantation does not increase the risk of second neoplasms for patients with Hodgkin’s lymphoma: a comparison of conventional therapy alone versus conventional therapy followed by autologous hematopoietic stem-cell transplantation. J Clin Oncol. 2005;23(31):7994–8002. doi: 10.1200/JCO.2005.01.9083.
  64. Arber DA, Orazi A, Hasserjian R, et al. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 2016;127(20):2391–405. doi: 10.1182/blood-2016-03-643544.
  65. Leone G, Fianchi L, Pagano L, Voso MT. Incidence and susceptibility to therapy-related myeloid neoplasms. Chem Biol Interact. 2010;184(1–2):39–45. doi: 10.1016/j.cbi.2009.12.013.
  66. Pedersen-Bjergaard J, Andersen MK, Andersen MT, Christiansen DH. Genetics of therapy-related myelodysplasia and acute myeloid leukemia. Leukemia. 2008;22(2):240–8. doi: 10.1038/sj.leu.2405078.
  67. Cowell IG, Austin CA. Mechanism of generation of therapy related leukemia in response to anti-topoisomerase II agents. Int J Environ Res Public Health. 2012;9(6):2075–91. doi: 10.3390/ijerph9062075.
  68. Kayser S, Dohner K, Krauter J, et al. The impact of therapy-related acute myeloid leukemia (AML) on outcome in 2853 adult patients with newly diagnosed AML. Blood. 2011;117(7):2137–45. doi: 10.1182/blood-2010-08-301713.
  69. Shea LK, Uy GL. Choosing induction chemotherapy in therapy-related acute myeloid leukemia. Best Pract Res Clin Haematol. 2019;32(1):89–97. doi: 10.1016/j.beha.2019.02.013.
  70. Ostgard BC, Medeiros H, Sengelov LS, et al Epidemiology and clinical significance of secondary and therapy-related acute myeloid leukemia: a national population-based cohort study. J Clin Oncol. 2015;33(31):3641–9. doi: 10.1200/jco.2014.60.0890.
  71. Boddu P, Kantarjian HM, Garcia-Manero G, et al. Treated secondary acute myeloid leukemia: a distinct high-risk subset of AML with adverse prognosis. Blood Adv. 2017;1(17):1312–23. doi: 10.1182/bloodadvances.2017008227.
  72. Lowenberg B, Pabst T, Vellenga E, et al. Cytarabine dose for acute myeloid leukemia. N Engl J Med. 2011;364(11):1027–36. doi: 10.1056/NEJMoa1010222.
  73. Lee J-H, Joo Y-D, Kim H, et al. A randomized trial comparing standard versus high-dose daunorubicin induction in patients with acute myeloid leukemia. Blood. 2011;118(14):3832–41. doi: 10.1182/blood-2011-06-361410.
  74. Lancet JE, Uy GL, Cortes JE. CPX-351 (cytarabine and daunorubicin) Liposome for Injection Versus Conventional Cytarabine Plus Daunorubicin in Older Patients With Newly Diagnosed Secondary Acute Myeloid Leukemia. J Clin Oncol. 2018;36(26):2684–92. doi: 10.1200/JCO.2017.77.6112.
  75. Walter RB, Othus M, Orlowski KF, et al. Unsatisfactory efficacy in randomized study of reduced-dose CPX-351 for medically less fit adults with newly diagnosed acute myeloid leukemia or other high-grade myeloid neoplasm. Haematologica. 2018;103(3):e106–e109. doi: 10.3324/haematol.2017.182642.
  76. Willemze R, Suciu S, Meloni G, et al. High-dose cytarabine in induction treatment improves the outcome of adult patients younger than age 46 years with acute myeloid leukemia: results of the EORTC-GIMEMA AML-12 trial. J Clin Oncol. 2014;32(3):219–28. doi: 10.1200/JCO.2013.51.8571.
  77. Theyab A, Algahtani M, Alsharif KF, et al. New insight into the mechanism of granulocyte colony-stimulating factor (G-CSF) that induces the mobilization of neutrophils. J Hematol. 2021;26(1):628–36. doi: 10.1080/16078454.2021.1965725.
  78. Leith CP, Kopecky KJ, Chen JM, et al. Frequency and clinical significance of the expression of the multidrug resistance proteins MDR1/P-glycoprotein, MRP1, and LRP in acute myeloid leukemia: a Southwest Oncology Group Study. Blood. 1999;94(3):1086–99.
  79. Becker PS, Medeiros BC, Stein AS, et al. G-CSF priming, clofarabine, and high dose cytarabine (GCLAC) for upfront treatment of acute myeloid leukemia, advanced myelodysplastic syndrome or advanced myeloproliferative neoplasm. Am J Hematol. 2015;90(4):295–300. doi: 10.1002/ajh.23927.
  80. Vulaj V, Perissinotti AJ, Uebel JR, et al. The FOSSIL Study: FLAG or standard 7+3 induction therapy in secondary acute myeloid leukemia. Leuk Res. 2018;70:91–6. doi: 10.1016/j.leukres.2018.05.011.
  81. Richardson DR, Green SD, Foster MC, Zeidner JF. Secondary AML Emerging After Therapy with Hypomethylating Agents: Outcomes, Prognostic Factors, and Treatment Options. Curr Hematol Malig Rep. 2021;16(1):97–111. doi: 10.1007/s11899-021-00608-6.
  82. 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.
  83. Cortes JE, Heidel FH, Heuser M, et al. A Phase 2 Randomized Study of Low Dose Ara-C with or without Glasdegib (PF-04449913) in Untreated Patients with Acute Myeloid Leukemia or High-Risk Myelodysplastic Syndrome. Blood. 2016;128(22):99. doi: 10.1182/blood.V128.22.99.99.
  84. Sengsayadeth S, Labopin M, Boumendil A. Transplant Outcomes for Secondary Acute Myeloid Leukemia: Acute Leukemia Working Party of the European Society for Blood and Bone Marrow Transplantation Study. Biol Blood Marrow Transplant. 2018l;24(7):1406–14. doi: 10.1016/j.bbmt.2018.04.008.
  85. Tang F-F, Huang X-J, Zhang X-H, et al. Allogeneic hematopoietic cell transplantation for adult patients with treatment-related acute myeloid leukemia during first remission: Comparable to de novo acute myeloid leukemia. Leuk Res. 2016;47:8–15. doi: 10.1016/j.leukres.2016.05.005.
  86. Michelis FV, Atenafu EG, Gupta V, et al. Comparable outcomes post allogeneic hematopoietic cell transplant for patients with de novo or secondary acute myeloid leukemia in first remission. Bone Marrow Transplant. 2015;50(7):907–13. doi: 10.1038/bmt.2015.59.
  87. Nilsson C, Hulegardh E, Garelius H, et al. Secondary Acute Myeloid Leukemia and the Role of Allogeneic Stem Cell Transplantation in a Population-Based Setting. Biol Blood Marrow Transplant. 2019;25(9):1770–8. doi: 10.1016/j.bbmt.2019.05.038.
  88. Oliai С, Schiller G. How to address second and therapy-related acute myelogenous leukaemia. Br J Haematol. 2020;188(1):116–28. doi: 10.1111/bjh.16354.