Outcome of 3q26.2/MECOM rearrangements in chronic myeloid leukemia.

MECOM Chronic myeloid leukemia Stem cell transplant Tyrosine kinase inhibitors

Journal

International journal of hematology
ISSN: 1865-3774
Titre abrégé: Int J Hematol
Pays: Japan
ID NLM: 9111627

Informations de publication

Date de publication:
15 May 2024
Historique:
received: 30 01 2024
accepted: 30 04 2024
revised: 21 04 2024
medline: 15 5 2024
pubmed: 15 5 2024
entrez: 15 5 2024
Statut: aheadofprint

Résumé

To evaluate the outcomes of patients with 3q26.2/MECOM-rearranged chronic myeloid leukemia (CML). We reviewed consecutive adult patients with 3q26.2/MECOM-rearranged CML between January 1, 1998 and February 16, 2023. Rearrangements of 3q26.2/MECOM were confirmed by conventional cytogenetics, and fluorescence in situ hybridization starting in 2015. We identified 55 patients with MECOM-rearranged CML, including 23 in chronic phase (CP) or accelerated phase (AP) and 32 in blast phase (BP). Nine patients (16%) achieved a major cytogenetic response (MCyR) or deeper. At a median follow-up of 89 months, median survival was 14 months. The 5-year survival rate was 19% overall, 23% in CML-CP/AP, and 15% in CML-BP. In the 6-month landmark analysis, the 5-year survival rate was 41% for allogeneic stem cell transplantation (allo-SCT) recipients versus 17% for non-recipients (P = 0.050). Multivariate analysis showed that the percentage of marrow blasts and achievement of MCyR or deeper could predict survival. Outcomes of 3q26.2/MECOM-rearranged CML are poor despite the availability of multiple BCR::ABL1 tyrosine kinase inhibitors (TKIs). Third-generation TKIs in combination with novel agents and possible allo-SCT could be considered given the poor outcomes and resistance to second-generation TKIs.

Identifiants

pubmed: 38748089
doi: 10.1007/s12185-024-03787-z
pii: 10.1007/s12185-024-03787-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : The University of Texas MD Anderson Cancer Center Support Grant
ID : CA016672

Informations de copyright

© 2024. Japanese Society of Hematology.

Références

Kimura S. Evolution of CML treatment. Int J Hematol. 2021;113(5):622–3.
doi: 10.1007/s12185-021-03128-4 pubmed: 33721192
Senapati J, Sasaki K, Issa GC, Lipton JH, Radich JP, Jabbour E, et al. Management of chronic myeloid leukemia in 2023 – common ground and common sense. Blood Cancer J. 2023;13(1):58.
doi: 10.1038/s41408-023-00823-9 pubmed: 37088793 pmcid: 10123066
Hochhaus A, Baccarani M, Silver RT, Schiffer C, Apperley JF, Cervantes F, et al. European LeukemiaNet 2020 recommendations for treating chronic myeloid leukemia. Leukemia. 2020;34(4):966–84.
doi: 10.1038/s41375-020-0776-2 pubmed: 32127639 pmcid: 7214240
Senapati J, Sasaki K, Issa GC, Lipton JH, Radich JP, Jabbour E, et al. Management of chronic myeloid leukemia in 2023 - common ground and common sense. Blood Cancer J. 2023;13(1):58.
doi: 10.1038/s41408-023-00823-9 pubmed: 37088793 pmcid: 10123066
Radich JP, Deininger M, Abboud CN, Altman JK, Berman E, Bhatia R, et al. Chronic myeloid leukemia, version1.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2018;16(9):1108–11035.
doi: 10.6004/jnccn.2018.0071 pubmed: 30181422
Kantarjian H, Paul S, Thakkar J, Jabbour E. The influence of drug prices, new availability of inexpensive generic imatinib, new approvals, and post-marketing research on the treatment of chronic myeloid leukaemia in the USA. The Lancet Haematology. 2022;9(11):e854–61.
doi: 10.1016/S2352-3026(22)00246-0 pubmed: 36174582
Jain P, Kantarjian H, Alattar ML, Jabbour E, Sasaki K, Nogueras Gonzalez G, et al. Long-term molecular and cytogenetic response and survival outcomes with imatinib 400 mg, imatinib 800 mg, dasatinib, and nilotinib in patients with chronic-phase chronic myeloid leukaemia: retrospective analysis of patient data from five clinical trials. Lancet Haematol. 2015;2(3):e118–28.
doi: 10.1016/S2352-3026(15)00021-6 pubmed: 26687797 pmcid: 4854752
Hehlmann R, Lauseker M, Saussele S, Pfirrmann M, Krause S, Kolb HJ, et al. Assessment of imatinib as first-line treatment of chronic myeloid leukemia: 10-year survival results of the randomized CML study IV and impact of non-CML determinants. Leukemia. 2017;31(11):2398–406.
doi: 10.1038/leu.2017.253 pubmed: 28804124 pmcid: 5668495
Kizaki M, Takahashi N, Iriyama N, Okamoto S, Ono T, Usui N, et al. Efficacy and safety of tyrosine kinase inhibitors for newly diagnosed chronic-phase chronic myeloid leukemia over a 5-year period: results from the Japanese registry obtained by the New TARGET system. Int J Hematol. 2019;109(4):426–39.
doi: 10.1007/s12185-019-02613-1 pubmed: 30762219
Morita K, Sasaki K. Current status and novel strategy of CML. Int J Hematol. 2021;113(5):624–31.
doi: 10.1007/s12185-021-03127-5 pubmed: 33782818
Nakamae H, Yamamoto M, Sakaida E, Kanda Y, Ohmine K, Ono T, et al. Nilotinib vs. imatinib in Japanese patients with newly diagnosed chronic myeloid leukemia in chronic phase: 10-year follow‑up of the Japanese subgroup of the randomized ENESTnd trial. Int J Hematol. 2023;115(1):33–42.
doi: 10.1007/s12185-021-03216-5
Sasaki K, Haddad FG, Short NJ, Jain N, Issa G, Jabbour E, et al. Outcome of Philadelphia chromosome-positive chronic myeloid leukemia in the United States since the introduction of imatinib therapy-the surveillance, epidemiology, and end results database, 2000–2019. Cancer. 2023;129(23):3805–14.
doi: 10.1002/cncr.35038 pubmed: 37769040
Sasaki K, Strom SS, O’Brien S, Jabbour E, Ravandi F, Konopleva M, et al. Relative survival in patients with chronic-phase chronic myeloid leukaemia in the tyrosine-kinase inhibitor era: analysis of patient data from six prospective clinical trials. Lancet Haematol. 2015;2(5):e186–93.
doi: 10.1016/S2352-3026(15)00048-4 pubmed: 26688093 pmcid: 4884053
Bower H, Bjorkholm M, Dickman PW, Hoglund M, Lambert PC, Andersson TM. Life expectancy of patients with chronic myeloid leukemia approaches the life expectancy of the general population. J Clin Oncol. 2016;34(24):2851–7.
doi: 10.1200/JCO.2015.66.2866 pubmed: 27325849
Bidikian A, Kantarjian H, Jabbour E, Short NJ, Patel K, Ravandi F, et al. Prognostic impact of ASXL1 mutations in chronic phase chronic myeloid leukemia. Blood Cancer J. 2022;12(10):144.
doi: 10.1038/s41408-022-00742-1 pubmed: 36307398 pmcid: 9616867
Schönfeld L, Rinke J, Hinze A, Nagel SN, Schäfer V, Schenk T, et al. ASXL1 mutations predict inferior molecular response to nilotinib treatment in chronic myeloid leukemia. Leukemia. 2022;36(9):2242–9.
doi: 10.1038/s41375-022-01648-4 pubmed: 35902731 pmcid: 9417980
Bidikian A, Jabbour E, Issa GC, Short NJ, Sasaki K, Kantarjian H. Chronic myeloid leukemia without major molecular response after 2 years of treatment with tyrosine kinase inhibitor. Am J Hematol. 2023;98(4):639–44.
doi: 10.1002/ajh.26836 pubmed: 36606715
Shahrin NH, Wadham C, Branford S. Defining higher-risk chronic myeloid leukemia: risk scores, genomic landscape, and prognostication. Curr Hematol Malig Rep. 2022;17(6):171–80.
doi: 10.1007/s11899-022-00668-2 pubmed: 35932396 pmcid: 9712352
Yoshimaru R, Minami Y. Genetic landscape of chronic myeloid leukemia and a novel targeted drug for overcoming resistance. Int J Mol Sci. 2023;24(18):13806. https://doi.org/10.3390/ijms241813806 .
doi: 10.3390/ijms241813806 pubmed: 37762109 pmcid: 10530602
Wang W, Cortes JE, Tang G, Khoury JD, Wang S, Bueso-Ramos CE, et al. Risk stratification of chromosomal abnormalities in chronic myelogenous leukemia in the era of tyrosine kinase inhibitor therapy. Blood. 2016;127(22):2742–50.
doi: 10.1182/blood-2016-01-690230 pubmed: 27006386 pmcid: 4915795
Hehlmann R, Voskanyan A, Lauseker M, Pfirrmann M, Kalmanti L, Rinaldetti S, et al. High-risk additional chromosomal abnormalities at low blast counts herald death by CML. Leukemia. 2020;34(8):2074–86.
doi: 10.1038/s41375-020-0826-9 pubmed: 32382082 pmcid: 7387244
Hehlmann R, Lauseker M, Voskanyan A, Fabarius A, Haferlach C, Hochhaus A, et al. Impact of emerging ACA on survival in chronic myeloid leukemia (CML). Leukemia. 2022;36(10):2544–7.
doi: 10.1038/s41375-022-01681-3 pubmed: 35999258 pmcid: 9522580
Birdwell C, Fiskus W, Kadia TM, DiNardo CD, Mill CP, Bhalla KN. EVI1 dysregulation: impact on biology and therapy of myeloid malignancies. Blood Cancer J. 2021;11(3):64.
doi: 10.1038/s41408-021-00457-9 pubmed: 33753715 pmcid: 7985498
Sato T, Goyama S, Kataoka K, Nasu R, Tsuruta-Kishino T, Kagoya Y, et al. Evi1 defines leukemia-initiating capacity and tyrosine kinase inhibitor resistance in chronic myeloid leukemia. Oncogene. 2014;33(42):5028–38.
doi: 10.1038/onc.2014.108 pubmed: 24747972 pmcid: 4217142
Vinothkumar K, Chanda S, Singh VK, Biswas S, Mohapatra S, Biswas G, et al. EVI1 upregulates PTGS1 (COX1) and decreases the action of tyrosine kinase inhibitors (TKIs) in chronic myeloid leukemia cells. Int J Hematol. 2023;117(1):110–20.
doi: 10.1007/s12185-022-03465-y pubmed: 36282419
Wang W, Cortes JE, Lin P, Beaty MW, Ai D, Amin HM, et al. Clinical and prognostic significance of 3q26.2 and other chromosome 3 abnormalities in CML in the era of tyrosine kinase inhibitors. Blood. 2015;126(14):1699–706.
doi: 10.1182/blood-2015-05-646489 pubmed: 26243778 pmcid: 4624442
Ogawa S, Kurokawa M, Tanaka T, Tanaka K, Hangaishi A, Mitani K, et al. Increased Evi-1 expression is frequently observed in blastic crisis of chronic myelocytic leukemia. Leukemia. 1996;10(5):788–94.
pubmed: 8656673
Yin CC, Cortes J, Barkoh B, Hayes K, Kantarjian H, Jones D. t(3;21)(q26;q22) in myeloid leukemia: an aggressive syndrome of blast transformation associated with hydroxyurea or antimetabolite therapy. Cancer. 2006;106(8):1730–8.
doi: 10.1002/cncr.21797 pubmed: 16532439
Daghistani M, Marin D, Khorashad JS, Wang L, May PC, Paliompeis C, et al. EVI-1 oncogene expression predicts survival in chronic-phase CML patients resistant to imatinib treated with second-generation tyrosine kinase inhibitors. Blood. 2010;116(26):6014–7.
doi: 10.1182/blood-2010-01-264234 pubmed: 20855863
Paquette RL, Nicoll J, Chalukya M, Elashoff D, Shah NP, Sawyers C, et al. Frequent EVI1 translocations in myeloid blast crisis CML that evolves through tyrosine kinase inhibitors. Cancer Genet. 2011;204(7):392–7.
doi: 10.1016/j.cancergen.2011.06.002 pubmed: 21872826
Khoury JD, Solary E, Abla O, Akkari Y, Alaggio R, Apperley JF, et al. The 5th edition of the World Health Organization Classification of Haematolymphoid Tumours: Myeloid and Histiocytic/Dendritic Neoplasms. Leukemia. 2022;36(7):1703–19.
doi: 10.1038/s41375-022-01613-1 pubmed: 35732831 pmcid: 9252913
Arber DA, Orazi A, Hasserjian RP, Borowitz MJ, Calvo KR, Kvasnicka HM, et al. International consensus classification of myeloid neoplasms and acute Leukemias: integrating morphologic, clinical, and genomic data. Blood. 2022;140(11):1200–28.
doi: 10.1182/blood.2022015850 pubmed: 35767897 pmcid: 9479031
Saxena K, Jabbour E, Issa G, Sasaki K, Ravandi F, Maiti A, et al. Impact of frontline treatment approach on outcomes of myeloid blast phase CML. J Hematol Oncol. 2021;14(1):94.
doi: 10.1186/s13045-021-01106-1 pubmed: 34130720 pmcid: 8204504
Kantarjian HM, O’Brien S, Cortes J, Giles FJ, Faderl S, Issa JP, et al. Results of decitabine (5-aza-2’deoxycytidine) therapy in 130 patients with chronic myelogenous leukemia. Cancer. 2003;98(3):522–8.
doi: 10.1002/cncr.11543 pubmed: 12879469
Senapati J, Ravandi F, DiNardo CD, Issa GC, Sasaki K, Konopleva M, et al. A phase II study of the combination of decitabine, venetoclax and ponatinib in patients with Chronic Myeloid Leukemia (CML) in Myeloid Blast Phase (MBP) or Philadelphia-Chromosome Positive (Ph+) Acute Myeloid Leukemia (AML). Blood. 2022;140(Supplement 1):3880–2.
doi: 10.1182/blood-2022-170773

Auteurs

Hiroki Akiyama (H)

Department of Leukemia, The University of Texas, MD Anderson Cancer Center, 1515 Holcombe Blvd. Unit 428, Houston, TX, 77030, USA.

Hagop Kantarjian (H)

Department of Leukemia, The University of Texas, MD Anderson Cancer Center, 1515 Holcombe Blvd. Unit 428, Houston, TX, 77030, USA.

Elias Jabbour (E)

Department of Leukemia, The University of Texas, MD Anderson Cancer Center, 1515 Holcombe Blvd. Unit 428, Houston, TX, 77030, USA.

Ghayas Issa (G)

Department of Leukemia, The University of Texas, MD Anderson Cancer Center, 1515 Holcombe Blvd. Unit 428, Houston, TX, 77030, USA.

Fadi G Haddad (FG)

Department of Leukemia, The University of Texas, MD Anderson Cancer Center, 1515 Holcombe Blvd. Unit 428, Houston, TX, 77030, USA.

Nicholas J Short (NJ)

Department of Leukemia, The University of Texas, MD Anderson Cancer Center, 1515 Holcombe Blvd. Unit 428, Houston, TX, 77030, USA.

Shimin Hu (S)

Department of Hematopathology, The University of Texas, MD Anderson Cancer Center, Houston, TX, 77030, USA.

Jo Ishizawa (J)

Department of Leukemia, The University of Texas, MD Anderson Cancer Center, 1515 Holcombe Blvd. Unit 428, Houston, TX, 77030, USA.

Michael Andreeff (M)

Department of Leukemia, The University of Texas, MD Anderson Cancer Center, 1515 Holcombe Blvd. Unit 428, Houston, TX, 77030, USA.

Koji Sasaki (K)

Department of Leukemia, The University of Texas, MD Anderson Cancer Center, 1515 Holcombe Blvd. Unit 428, Houston, TX, 77030, USA. ksasaki1@mdanderson.org.

Classifications MeSH