European LeukemiaNet laboratory recommendations for the diagnosis and management of chronic myeloid leukemia.


Journal

Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895

Informations de publication

Date de publication:
Nov 2023
Historique:
received: 29 08 2023
accepted: 20 09 2023
revised: 13 09 2023
medline: 6 11 2023
pubmed: 5 10 2023
entrez: 4 10 2023
Statut: ppublish

Résumé

From the laboratory perspective, effective management of patients with chronic myeloid leukemia (CML) requires accurate diagnosis, assessment of prognostic markers, sequential assessment of levels of residual disease and investigation of possible reasons for resistance, relapse or progression. Our scientific and clinical knowledge underpinning these requirements continues to evolve, as do laboratory methods and technologies. The European LeukemiaNet convened an expert panel to critically consider the current status of genetic laboratory approaches to help diagnose and manage CML patients. Our recommendations focus on current best practice and highlight the strengths and pitfalls of commonly used laboratory tests.

Identifiants

pubmed: 37794101
doi: 10.1038/s41375-023-02048-y
pii: 10.1038/s41375-023-02048-y
pmc: PMC10624636
doi:

Substances chimiques

Protein Kinase Inhibitors 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

2150-2167

Informations de copyright

© 2023. The Author(s).

Références

Nowell PC, Hungerford DA. A Minute Chromosome in Human Chronic Granulocytic Leukemia. Science. 1960;132:1497.
Rowley JD. Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature. 1973;243:290–3.
pubmed: 4126434 doi: 10.1038/243290a0
Shtivelman E, Lifshitz B, Gale RP, Canaani E. Fused transcript of abl and bcr genes in chronic myelogenous leukaemia. Nature. 1985;315:550–4.
pubmed: 2989692 doi: 10.1038/315550a0
Daley GQ, Van Etten RA, Baltimore D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science. 1990;247:824–30.
pubmed: 2406902 doi: 10.1126/science.2406902
Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S, et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med. 1996;2:561–6.
pubmed: 8616716 doi: 10.1038/nm0596-561
O’Brien SG, Guilhot F, Larson RA, Gathmann I, Baccarani M, Cervantes F, et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N. Engl J Med. 2003;348:994–1004.
pubmed: 12637609 doi: 10.1056/NEJMoa022457
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;34:2851–7.
pubmed: 27325849 doi: 10.1200/JCO.2015.66.2866
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;31:2398–406.
pubmed: 28804124 pmcid: 5668495 doi: 10.1038/leu.2017.253
Malhotra H, Radich J, Garcia-Gonzalez P. Meeting the needs of CML patients in resource-poor countries. Hematol Am Soc Hematol Educ Program. 2019;2019:433–42.
doi: 10.1182/hematology.2019000050
Mahon FX, Rea D, Guilhot J, Guilhot F, Huguet F, Nicolini F, et al. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. Lancet Oncol. 2010;11:1029–35.
pubmed: 20965785 doi: 10.1016/S1470-2045(10)70233-3
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;36:1703–19.
pubmed: 35732831 pmcid: 9252913 doi: 10.1038/s41375-022-01613-1
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;140:1200–28.
pubmed: 35767897 pmcid: 9479031 doi: 10.1182/blood.2022015850
Rassool F, Martiat P, Taj A, Klisak I, Goldman J. Interstitial insertion of varying amounts of ABL-containing genetic material into chromosome 22 in Ph-negative CML. Leukemia. 1990;4:273–7.
pubmed: 2164119
Lazaridou A, Chase A, Melo J, Garicochea B, Diamond J, Goldman J. Lack of reciprocal translocation in BCR-ABL positive Ph-negative chronic myeloid leukaemia. Leukemia. 1994;8:454–7.
pubmed: 8127150
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;36:2544–7.
pubmed: 35999258 pmcid: 9522580 doi: 10.1038/s41375-022-01681-3
Mitelman F, Levan G, Nilsson PG, Brandt L. Non-random karyotypic evolution in chronic myeloid leukemia. Int J Cancer. 1976;18:24–30.
pubmed: 1065618 doi: 10.1002/ijc.2910180105
Fabarius A, Leitner A, Hochhaus A, Muller MC, Hanfstein B, Haferlach C, et al. Impact of additional cytogenetic aberrations at diagnosis on prognosis of CML: long-term observation of 1151 patients from the randomized CML Study IV. Blood. 2011;118:6760–8.
pubmed: 22039253 doi: 10.1182/blood-2011-08-373902
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;127:2742–50.
pubmed: 27006386 pmcid: 4915795 doi: 10.1182/blood-2016-01-690230
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;34:2074–86.
pubmed: 32382082 pmcid: 7387244 doi: 10.1038/s41375-020-0826-9
Fabarius A, Kalmanti L, Dietz CT, Lauseker M, Rinaldetti S, Haferlach C, et al. Impact of unbalanced minor route versus major route karyotypes at diagnosis on prognosis of CML. Ann Hematol. 2015;94:2015–24.
pubmed: 26385387 doi: 10.1007/s00277-015-2494-9
Gong Z, Medeiros LJ, Cortes JE, Chen Z, Zheng L, Li Y, et al. Cytogenetics-based risk prediction of blastic transformation of chronic myeloid leukemia in the era of TKI therapy. Blood Adv. 2017;1:2541–52.
pubmed: 29296906 pmcid: 5728641 doi: 10.1182/bloodadvances.2017011858
Kockerols CCB, Geelen IGP, Levin MD, Janssen J, BHB, Dinmohamed AG, et al. High-risk additional cytogenetic aberrations in a Dutch chronic phase chronic myeloid leukemia patient population. Haematologica. 2023. https://doi.org/10.3324/haematol.2022.282447 . Online ahead of print.
Deininger MW, Cortes J, Paquette R, Park B, Hochhaus A, Baccarani M, et al. The prognosis for patients with chronic myeloid leukemia who have clonal cytogenetic abnormalities in philadelphia chromosome-negative cells. Cancer. 2007;110:1509–19.
pubmed: 17702093 doi: 10.1002/cncr.22936
Bidet A, Dulucq S, Smol T, Marceau-Renaut A, Morisset S, Coiteux V, et al. Poor prognosis of chromosome 7 clonal aberrations in Philadelphia-negative metaphases and relevance of potential underlying myelodysplastic features in chronic myeloid leukemia. Haematologica. 2019;104:1150–5.
pubmed: 30573507 pmcid: 6545846 doi: 10.3324/haematol.2018.208801
Issa GC, Kantarjian HM, Gonzalez GN, Borthakur G, Tang G, Wierda W, et al. Clonal chromosomal abnormalities appearing in Philadelphia chromosome-negative metaphases during CML treatment. Blood. 2017;130:2084–91.
pubmed: 28835440 pmcid: 5680612 doi: 10.1182/blood-2017-07-792143
ISCN 2020: An International System for Human Cytogenomic Nomenclature (2020). Basel: Karger; 2020.
Bruford EA, Antonescu CR, Carroll AJ, Chinnaiyan A, Cree IA, Cross NCP, et al. HUGO Gene Nomenclature Committee (HGNC) recommendations for the designation of gene fusions. Leukemia. 2021;35:3040–3.
pubmed: 34615987 pmcid: 8550944 doi: 10.1038/s41375-021-01436-6
May PC, Reid AG, Robinson ME, Khorashad JS, Milojkovic D, Claudiani S, et al. FISH-negative BCR::ABL1-positive e19a2 chronic myeloid leukaemia: the most cryptic of insertions. BMC Med Genomics. 2023;16:172.
pubmed: 37496024 pmcid: 10369825 doi: 10.1186/s12920-023-01607-7
Melo JV. BCR-ABL gene variants. Baillieres Clin Haematol. 1997;10:203–22.
pubmed: 9376660 doi: 10.1016/S0950-3536(97)80003-0
Groffen J, Stephenson JR, Heisterkamp N, de Klein A, Bartram CR, Grosveld G. Philadelphia chromosomal breakpoints are clustered within a limited region, bcr, on chromosome 22. Cell. 1984;36:93–9.
pubmed: 6319012 doi: 10.1016/0092-8674(84)90077-1
Baccarani M, Castagnetti F, Gugliotta G, Rosti G, Soverini S, Albeer A, et al. The proportion of different BCR-ABL1 transcript types in chronic myeloid leukemia. An international overview. Leukemia. 2019;33:1173–83.
pubmed: 30675008 doi: 10.1038/s41375-018-0341-4
Hanfstein B, Lauseker M, Hehlmann R, Saussele S, Erben P, Dietz C, et al. Distinct characteristics of e13a2 versus e14a2 BCR-ABL1 driven chronic myeloid leukemia under first-line therapy with imatinib. Haematologica. 2014;99:1441–7.
pubmed: 24837466 pmcid: 4562532 doi: 10.3324/haematol.2013.096537
Jain P, Kantarjian H, Patel KP, Gonzalez GN, Luthra R, Kanagal Shamanna R, et al. Impact of BCR-ABL transcript type on outcome in patients with chronic-phase CML treated with tyrosine kinase inhibitors. Blood. 2016;127:1269–75.
pubmed: 26729897 pmcid: 4786836 doi: 10.1182/blood-2015-10-674242
Castagnetti F, Gugliotta G, Breccia M, Iurlo A, Levato L, Albano F, et al. The BCR-ABL1 transcript type influences response and outcome in Philadelphia chromosome-positive chronic myeloid leukemia patients treated frontline with imatinib. Am J Hematol. 2017;92:797–805.
pubmed: 28466557 doi: 10.1002/ajh.24774
Melo JV, Gordon DE, Cross NC, Goldman JM. The ABL-BCR fusion gene is expressed in chronic myeloid leukemia. Blood. 1993;81:158–65.
pubmed: 8417787 doi: 10.1182/blood.V81.1.158.158
de la Fuente J, Merx K, Steer EJ, Muller M, Szydlo RM, Maywald O, et al. ABL-BCR expression does not correlate with deletions on the derivative chromosome 9 or survival in chronic myeloid leukemia. Blood. 2001;98:2879–80.
pubmed: 11697340 doi: 10.1182/blood.V98.9.2879
Grand F, Kulkarni S, Chase A, Goldman JM, Gordon M, Cross NC. Frequent deletion of hSNF5/INI1, a component of the SWI/SNF complex, in chronic myeloid leukemia. Cancer Res. 1999;59:3870–4.
pubmed: 10463572
Huntly BJ, Guilhot F, Reid AG, Vassiliou G, Hennig E, Franke C, et al. Imatinib improves but may not fully reverse the poor prognosis of patients with CML with derivative chromosome 9 deletions. Blood. 2003;102:2205–12.
pubmed: 12750153 doi: 10.1182/blood-2002-09-2763
Kreil S, Pfirrmann M, Haferlach C, Waghorn K, Chase A, Hehlmann R, et al. Heterogeneous prognostic impact of derivative chromosome 9 deletions in chronic myelogenous leukemia. Blood. 2007;110:1283–90.
pubmed: 17456720 doi: 10.1182/blood-2007-02-074252
Hanfstein B, Shlyakhto V, Lauseker M, Hehlmann R, Saussele S, Dietz C, et al. Velocity of early BCR-ABL transcript elimination as an optimized predictor of outcome in chronic myeloid leukemia (CML) patients in chronic phase on treatment with imatinib. Leukemia. 2014;28:1988–92.
pubmed: 24798484 doi: 10.1038/leu.2014.153
Branford S, Yeung DT, Parker WT, Roberts ND, Purins L, Braley JA, et al. Prognosis for patients with CML and >10% BCR-ABL1 after 3 months of imatinib depends on the rate of BCR-ABL1 decline. Blood. 2014;124:511–8.
pubmed: 24859364 doi: 10.1182/blood-2014-03-566323
Shanmuganathan N, Pagani IS, Ross DM, Park S, Yong ASM, Braley JA, et al. Early BCR-ABL1 kinetics are predictive of subsequent achievement of treatment-free remission in chronic myeloid leukemia. Blood. 2021;137:1196–207.
pubmed: 32871588 doi: 10.1182/blood.2020005514
Cross NC, Melo JV, Feng L, Goldman JM. An optimized multiplex polymerase chain reaction (PCR) for detection of BCR-ABL fusion mRNAs in haematological disorders. Leukemia. 1994;8:186–9.
pubmed: 8289486
Verma D, Kantarjian HM, Jones D, Luthra R, Borthakur G, Verstovsek S, et al. Chronic myeloid leukemia (CML) with P190 BCR-ABL: analysis of characteristics, outcomes, and prognostic significance. Blood. 2009;114:2232–5.
pubmed: 19531657 pmcid: 4828071 doi: 10.1182/blood-2009-02-204693
Gong Z, Medeiros LJ, Cortes JE, Zheng L, Khoury JD, Wang W, et al. Clinical and prognostic significance of e1a2 BCR-ABL1 transcript subtype in chronic myeloid leukemia. Blood Cancer J. 2017;7:e583.
pubmed: 28708130 pmcid: 5549254 doi: 10.1038/bcj.2017.62
Adnan-Awad S, Kim D, Hohtari H, Javarappa KK, Brandstoetter T, Mayer I, et al. Characterization of p190-Bcr-Abl chronic myeloid leukemia reveals specific signaling pathways and therapeutic targets. Leukemia. 2021;35:1964–75.
pubmed: 33168949 doi: 10.1038/s41375-020-01082-4
Abdelmagid MG, Litzow MR, McCullough KB, Gangat N, Pardanani A, Murthy HS, et al. Chronic phase CML with sole P190 (e1a2) BCR::ABL1: long-term outcome among ten consecutive cases. Blood Cancer J. 2022;12:103.
pubmed: 35794090 pmcid: 9259673 doi: 10.1038/s41408-022-00696-4
van Rhee F, Hochhaus A, Lin F, Melo JV, Goldman JM, Cross NC. p190 BCR-ABL mRNA is expressed at low levels in p210-positive chronic myeloid and acute lymphoblastic leukemias. Blood. 1996;87:5213–7.
pubmed: 8652835 doi: 10.1182/blood.V87.12.5213.bloodjournal87125213
Molica M, Zacheo I, Diverio D, Alimena G, Breccia M. Long-term outcome of chronic myeloid leukaemia patients with p210 and p190 co-expression at baseline. Br J Haematol. 2015;169:148–50.
pubmed: 25296902 doi: 10.1111/bjh.13184
Smith BM, Brewer D, Druker BJ, Braun TP. Navigating Challenges in Monitoring Chronic Myeloid Leukemia with Multiple BCR-ABL1 Transcripts. Case Rep Oncol. 2021;14:1707–11.
pubmed: 35082629 pmcid: 8740187 doi: 10.1159/000520400
Branford S, Kim DDH, Apperley JF, Eide CA, Mustjoki S, Ong ST, et al. Laying the foundation for genomically-based risk assessment in chronic myeloid leukemia. Leukemia. 2019;33:1835–50.
pubmed: 31209280 pmcid: 6893870 doi: 10.1038/s41375-019-0512-y
Adnan-Awad S, Kankainen M, Mustjoki S. Mutational landscape of chronic myeloid leukemia: more than a single oncogene leukemia. Leuk Lymphoma. 2021;62:2064–78.
pubmed: 33944660 doi: 10.1080/10428194.2021.1894652
Ernst T, Busch M, Rinke J, Ernst J, Haferlach C, Beck JF, et al. Frequent ASXL1 mutations in children and young adults with chronic myeloid leukemia. Leukemia. 2018;32:2046–9.
pubmed: 29899367 doi: 10.1038/s41375-018-0157-2
Kim T, Tyndel MS, Kim HJ, Ahn JS, Choi SH, Park HJ, et al. Spectrum of somatic mutation dynamics in chronic myeloid leukemia following tyrosine kinase inhibitor therapy. Blood. 2017;129:38–47.
pubmed: 27733357 doi: 10.1182/blood-2016-04-708560
Schonfeld L, Rinke J, Hinze A, Nagel SN, Schafer V, Schenk T, et al. ASXL1 mutations predict inferior molecular response to nilotinib treatment in chronic myeloid leukemia. Leukemia. 2022;36:2242–9.
pubmed: 35902731 pmcid: 9417980 doi: 10.1038/s41375-022-01648-4
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;12:144.
pubmed: 36307398 pmcid: 9616867 doi: 10.1038/s41408-022-00742-1
Adnan Awad S, Kankainen M, Ojala T, Koskenvesa P, Eldfors S, Ghimire B, et al. Mutation accumulation in cancer genes relates to nonoptimal outcome in chronic myeloid leukemia. Blood Adv. 2020;4:546–59.
pubmed: 32045476 pmcid: 7013270 doi: 10.1182/bloodadvances.2019000943
Ng KP, Hillmer AM, Chuah CT, Juan WC, Ko TK, Teo AS, et al. A common BIM deletion polymorphism mediates intrinsic resistance and inferior responses to tyrosine kinase inhibitors in cancer. Nat Med. 2012;18:521–8.
pubmed: 22426421 doi: 10.1038/nm.2713
Marin D, Gabriel IH, Ahmad S, Foroni L, de Lavallade H, Clark R, et al. KIR2DS1 genotype predicts for complete cytogenetic response and survival in newly diagnosed chronic myeloid leukemia patients treated with imatinib. Leukemia. 2012;26:296–302.
pubmed: 21844874 doi: 10.1038/leu.2011.180
Kreutzman A, Jaatinen T, Greco D, Vakkila E, Richter J, Ekblom M, et al. Killer-cell immunoglobulin-like receptor gene profile predicts good molecular response to dasatinib therapy in chronic myeloid leukemia. Exp Hematol. 2012;40:906–13.e1.
pubmed: 22842045 doi: 10.1016/j.exphem.2012.07.007
Yeung DT, Tang C, Vidovic L, White DL, Branford S, Hughes TP, et al. KIR2DL5B genotype predicts outcomes in CML patients treated with response-directed sequential imatinib/nilotinib strategy. Blood. 2015;126:2720–3.
pubmed: 26500342 doi: 10.1182/blood-2015-07-655589
Marum JE, Yeung DT, Purins L, Reynolds J, Parker WT, Stangl D, et al. ASXL1 and BIM germ line variants predict response and identify CML patients with the greatest risk of imatinib failure. Blood Adv. 2017;1:1369–81.
pubmed: 29296778 pmcid: 5727850 doi: 10.1182/bloodadvances.2017006825
Park JH, Woo YM, Youm EM, Hamad N, Won HH, Naka K, et al. HMGCLL1 is a predictive biomarker for deep molecular response to imatinib therapy in chronic myeloid leukemia. Leukemia. 2019;33:1439–50.
pubmed: 30555164 doi: 10.1038/s41375-018-0321-8
Nteliopoulos G, Bazeos A, Claudiani S, Gerrard G, Curry E, Szydlo R, et al. Somatic variants in epigenetic modifiers can predict failure of response to imatinib but not to second-generation tyrosine kinase inhibitors. Haematologica. 2019;104:2400–9.
pubmed: 31073075 pmcid: 6959189 doi: 10.3324/haematol.2018.200220
Thomson DW, Shahrin NH, Wang PPS, Wadham C, Shanmuganathan N, Scott HS, et al. Aberrant RAG-mediated recombination contributes to multiple structural rearrangements in lymphoid blast crisis of chronic myeloid leukemia. Leukemia. 2020;34:2051–63.
pubmed: 32076119 doi: 10.1038/s41375-020-0751-y
Ochi Y, Yoshida K, Huang YJ, Kuo MC, Nannya Y, Sasaki K, et al. Clonal evolution and clinical implications of genetic abnormalities in blastic transformation of chronic myeloid leukaemia. Nat Commun. 2021;12:2833.
pubmed: 33990592 pmcid: 8121838 doi: 10.1038/s41467-021-23097-w
Branford S, Wang P, Yeung DT, Thomson D, Purins A, Wadham C, et al. Integrative genomic analysis reveals cancer-associated mutations at diagnosis of CML in patients with high-risk disease. Blood. 2018;132:948–61.
pubmed: 29967129 doi: 10.1182/blood-2018-02-832253
Senapati J, Jabbour E, Kantarjian H, Short NJ. Pathogenesis and management of accelerated and blast phases of chronic myeloid leukemia. Leukemia. 2023;37:5–17.
pubmed: 36309558 doi: 10.1038/s41375-022-01736-5
Shanmuganathan N, Wadham C, Thomson D, Shahrin NH, Vignaud C, Obourn V, et al. RNA-Based Targeted Gene Sequencing Improves the Diagnostic Yield of Mutant Detection in Chronic Myeloid Leukemia. J Mol Diagn. 2022;24:803–22.
pubmed: 35550185 doi: 10.1016/j.jmoldx.2022.04.004
Yannakou CK, Jones K, McBean M, Thompson ER, Ryland GL, Doig K, et al. ASXL1 c.1934dup;p.Gly646Trpfs*12-a true somatic alteration requiring a new approach. Blood Cancer J. 2017;7:656.
pubmed: 29242575 pmcid: 5802455 doi: 10.1038/s41408-017-0025-8
Alberti MO, Srivatsan SN, Shao J, McNulty SN, Chang GS, Miller CA, et al. Discriminating a common somatic ASXL1 mutation (c.1934dup; p.G646Wfs*12) from artifact in myeloid malignancies using NGS. Leukemia. 2018;32:1874–8.
pubmed: 29959414 pmcid: 6402595 doi: 10.1038/s41375-018-0193-y
Jennings LJ, Arcila ME, Corless C, Kamel-Reid S, Lubin IM, Pfeifer J, et al. Guidelines for Validation of Next-Generation Sequencing-Based Oncology Panels: A Joint Consensus Recommendation of the Association for Molecular Pathology and College of American Pathologists. J Mol Diagn. 2017;19:341–65.
pubmed: 28341590 doi: 10.1016/j.jmoldx.2017.01.011
Thomas M, Sukhai MA, Zhang T, Dolatshahi R, Harbi D, Garg S, et al. Integration of Technical, Bioinformatic, and Variant Assessment Approaches in the Validation of a Targeted Next-Generation Sequencing Panel for Myeloid Malignancies. Arch Pathol Lab Med. 2017;141:759–75.
pubmed: 28557600 doi: 10.5858/arpa.2016-0547-RA
Li MM, Datto M, Duncavage EJ, Kulkarni S, Lindeman NI, Roy S, et al. Standards and Guidelines for the Interpretation and Reporting of Sequence Variants in Cancer: A Joint Consensus Recommendation of the Association for Molecular Pathology, American Society of Clinical Oncology, and College of American Pathologists. J Mol Diagn. 2017;19:4–23.
pubmed: 27993330 pmcid: 5707196 doi: 10.1016/j.jmoldx.2016.10.002
Mateo J, Chakravarty D, Dienstmann R, Jezdic S, Gonzalez-Perez A, Lopez-Bigas N, et al. A framework to rank genomic alterations as targets for cancer precision medicine: the ESMO Scale for Clinical Actionability of molecular Targets (ESCAT). Ann Oncol. 2018;29:1895–902.
pubmed: 30137196 pmcid: 6158764 doi: 10.1093/annonc/mdy263
Horak P, Griffith M, Danos AM, Pitel BA, Madhavan S, Liu X, et al. Standards for the classification of pathogenicity of somatic variants in cancer (oncogenicity): Joint recommendations of Clinical Genome Resource (ClinGen), Cancer Genomics Consortium (CGC), and Variant Interpretation for Cancer Consortium (VICC). Genet Med. 2022;24:986–98.
pubmed: 35101336 pmcid: 9081216 doi: 10.1016/j.gim.2022.01.001
Radich JP, Dai H, Mao M, Oehler V, Schelter J, Druker B, et al. Gene expression changes associated with progression and response in chronic myeloid leukemia. Proc Natl Acad Sci USA. 2006;103:2794–9.
pubmed: 16477019 pmcid: 1413797 doi: 10.1073/pnas.0510423103
Ko TK, Javed A, Lee KL, Pathiraja TN, Liu X, Malik S, et al. An integrative model of pathway convergence in genetically heterogeneous blast crisis chronic myeloid leukemia. Blood. 2020;135:2337–53.
pubmed: 32157296 doi: 10.1182/blood.2020004834
Giustacchini A, Thongjuea S, Barkas N, Woll PS, Povinelli BJ, Booth CAG, et al. Single-cell transcriptomics uncovers distinct molecular signatures of stem cells in chronic myeloid leukemia. Nat Med. 2017;23:692–702.
pubmed: 28504724 doi: 10.1038/nm.4336
Branford S, Apperley JF. Measurable residual disease in chronic myeloid leukemia. Haematologica. 2022;107:2794–809.
pubmed: 36453517 pmcid: 9713565 doi: 10.3324/haematol.2022.281493
Scott S, Cartwright A, Francis S, Whitby L, Sanzone AP, Mulder A, et al. Assessment of droplet digital polymerase chain reaction for measuring BCR-ABL1 in chronic myeloid leukaemia in an international interlaboratory study. Br J Haematol. 2021;194:53–60.
pubmed: 34114218 doi: 10.1111/bjh.17521
Hailu S, Kinde S, Cross M, Tsegaye A, Kelemu T, Seifu D, et al. Estimating prognostic relevant cutoff values for a multiplex PCR detecting BCR::ABL1 in chronic myeloid leukemia patients on tyrosine kinase inhibitor therapy in resource-limited settings. Ann Hematol. 2023;102:1723–9.
pubmed: 37212909 pmcid: 10261237 doi: 10.1007/s00277-023-05254-x
Hughes T, Deininger M, Hochhaus A, Branford S, Radich J, Kaeda J, et al. Monitoring CML patients responding to treatment with tyrosine kinase inhibitors: review and recommendations for harmonizing current methodology for detecting BCR-ABL transcripts and kinase domain mutations and for expressing results. Blood. 2006;108:28–37.
pubmed: 16522812 pmcid: 1895821 doi: 10.1182/blood-2006-01-0092
White HE, Matejtschuk P, Rigsby P, Gabert J, Lin F, Lynn Wang Y, et al. Establishment of the first World Health Organization International Genetic Reference Panel for quantitation of BCR-ABL mRNA. Blood. 2010;116:e111–7.
pubmed: 20720184 doi: 10.1182/blood-2010-06-291641
Branford S, Cross NC, Hochhaus A, Radich J, Saglio G, Kaeda J, et al. Rationale for the recommendations for harmonizing current methodology for detecting BCR-ABL transcripts in patients with chronic myeloid leukaemia. Leukemia. 2006;20:1925–30.
pubmed: 16990771 doi: 10.1038/sj.leu.2404388
Lauseker M, Hanfstein B, Haferlach C, Schnittger S, Pfirrmann M, Fabarius A, et al. Equivalence of BCR-ABL transcript levels with complete cytogenetic remission in patients with chronic myeloid leukemia in chronic phase. J Cancer Res Clin Oncol. 2014;140:1965–9.
pubmed: 24952896 doi: 10.1007/s00432-014-1746-8
Branford S, Fletcher L, Cross NC, Muller MC, Hochhaus A, Kim DW, et al. Desirable performance characteristics for BCR-ABL measurement on an international reporting scale to allow consistent interpretation of individual patient response and comparison of response rates between clinical trials. Blood. 2008;112:3330–8.
pubmed: 18684859 doi: 10.1182/blood-2008-04-150680
Muller MC, Cross NC, Erben P, Schenk T, Hanfstein B, Ernst T, et al. Harmonization of molecular monitoring of CML therapy in Europe. Leukemia. 2009;23:1957–63.
pubmed: 19710700 doi: 10.1038/leu.2009.168
Cross NC, White HE, Ernst T, Welden L, Dietz C, Saglio G, et al. Development and evaluation of a secondary reference panel for BCR-ABL1 quantification on the International Scale. Leukemia. 2016;30:1844–52.
pubmed: 27109508 pmcid: 5240017 doi: 10.1038/leu.2016.90
Cross NC, White HE, Colomer D, Ehrencrona H, Foroni L, Gottardi E, et al. Laboratory recommendations for scoring deep molecular responses following treatment for chronic myeloid leukemia. Leukemia. 2015;29:999–1003.
pubmed: 25652737 pmcid: 4430701 doi: 10.1038/leu.2015.29
White HE, Salmon M, Albano F, Andersen CSA, Balabanov S, Balatzenko G, et al. Standardization of molecular monitoring of CML: results and recommendations from the European treatment and outcome study. Leukemia. 2022;36:1834–42.
pubmed: 35614319 pmcid: 9252906 doi: 10.1038/s41375-022-01607-z
Brown JT, Beldorth IJ, Laosinchai-Wolf W, Fahey ME, Jefferson KL, Ruskin AK, et al. Analytical Validation of a Highly Sensitive, Multiplexed Chronic Myeloid Leukemia Monitoring System Targeting BCR-ABL1 RNA. J Mol Diagn. 2019;21:718–33.
pubmed: 31026597 pmcid: 6626993 doi: 10.1016/j.jmoldx.2019.03.002
Chung HJ, Hur M, Yoon S, Hwang K, Lim HS, Kim H, et al. Performance Evaluation of the QXDx BCR-ABL %IS Droplet Digital PCR Assay. Ann Lab Med. 2020;40:72–5.
pubmed: 31432643 doi: 10.3343/alm.2020.40.1.72
Nasser A, Hussein A, Chamba C, Yonazi M, Mushi R, Schuh A, et al. Molecular response to imatinib in patients with chronic myeloid leukemia in Tanzania. Blood Adv. 2021;5:1403–11.
pubmed: 33666650 pmcid: 7948290 doi: 10.1182/bloodadvances.2020002973
Scott S, Travis D, Whitby L, Bainbridge J, Cross NCP, Barnett D. Measurement of BCR-ABL1 by RT-qPCR in chronic myeloid leukaemia: findings from an International EQA Programme. Br J Haematol. 2017;177:414–22.
pubmed: 28295199 doi: 10.1111/bjh.14557
Garcia-Gutierrez V, Gomez-Casares MT, Puerta JM, Alonso-Dominguez JM, Osorio S, Hernandez-Boluda JC, et al. A BCR-ABL1 cutoff of 1.5% at 3 months, determined by the GeneXpert system, predicts an optimal response in patients with chronic myeloid leukemia. PLoS One. 2017;12:e0173532.
pubmed: 28278193 pmcid: 5344481 doi: 10.1371/journal.pone.0173532
Sala Torra O, Beppu L, Smith JL, Welden L, Georgievski J, Gupta K, et al. Paper or plastic? BCR-ABL1 quantitation and mutation detection from dried blood spots. Blood. 2016;127:2773–4.
pubmed: 27076173 pmcid: 4891957 doi: 10.1182/blood-2015-12-689059
Branford S, Hughes T. Diagnosis and monitoring of chronic myeloid leukemia by qualitative and quantitative RT-PCR. Methods Mol Med. 2006;125:69–92.
pubmed: 16502578
Spiess B, Naumann N, Galuschek N, Rinaldetti S, Kossak-Roth U, Tarnopolscaia I, et al. The benefit of quality control charts (QCC) for routine quantitative BCR-ABL1 monitoring in chronic myeloid leukemia. PLoS One. 2018;13:e0196326.
pubmed: 29689094 pmcid: 5916859 doi: 10.1371/journal.pone.0196326
White H, Deprez L, Corbisier P, Hall V, Lin F, Mazoua S, et al. A certified plasmid reference material for the standardisation of BCR-ABL1 mRNA quantification by real-time quantitative PCR. Leukemia. 2015;29:369–76.
pubmed: 25036192 doi: 10.1038/leu.2014.217
Alikian M, Whale AS, Akiki S, Piechocki K, Torrado C, Myint T, et al. RT-qPCR and RT-Digital PCR: A Comparison of Different Platforms for the Evaluation of Residual Disease in Chronic Myeloid Leukemia. Clin Chem. 2017;63:525–31.
pubmed: 27979961 doi: 10.1373/clinchem.2016.262824
Berdeja JG, Heinrich MC, Dakhil SR, Goldberg SL, Wadleigh M, Kuriakose P, et al. Rates of deep molecular response by digital and conventional PCR with frontline nilotinib in newly diagnosed chronic myeloid leukemia: a landmark analysis. Leuk Lymphoma. 2019;60:2384–93.
pubmed: 30912699 doi: 10.1080/10428194.2019.1590569
Nicolini FE, Dulucq S, Boureau L, Cony-Makhoul P, Charbonnier A, Escoffre-Barbe M, et al. Evaluation of Residual Disease and TKI Duration Are Critical Predictive Factors for Molecular Recurrence after Stopping Imatinib First-line in Chronic Phase CML Patients. Clin Cancer Res. 2019;25:6606–13.
pubmed: 31292142 doi: 10.1158/1078-0432.CCR-18-3373
Kockerols CCB, Valk PJM, Levin MD, Pallisgaard N, Cornelissen JJ, Westerweel PE. Digital PCR for BCR-ABL1 Quantification in CML: Current Applications in Clinical Practice. Hemasphere. 2020;4:e496.
pubmed: 33283168 pmcid: 7710259 doi: 10.1097/HS9.0000000000000496
Machova Polakova K, Zizkova H, Zuna J, Motlova E, Hovorkova L, Gottschalk A, et al. Analysis of chronic myeloid leukaemia during deep molecular response by genomic PCR: a traffic light stratification model with impact on treatment-free remission. Leukemia. 2020;34:2113–24.
pubmed: 32472084 doi: 10.1038/s41375-020-0882-1
Jennings LJ, Smith FA, Halling KC, Persons DL, Kamel-Reid S, Molecular Oncology Resource Committee of the College of American P. Design and analytic validation of BCR-ABL1 quantitative reverse transcription polymerase chain reaction assay for monitoring minimal residual disease. Arch Pathol Lab Med. 2012;136:33–40.
pubmed: 22208485 doi: 10.5858/arpa.2011-0136-OA
Cross NCP, White HE, Evans PAS, Hancock J, Copland M, Milojkovic D, et al. Consensus on BCR-ABL1 reporting in chronic myeloid leukaemia in the UK. Br J Haematol. 2018;182:777–88.
pubmed: 30125955 pmcid: 6175193 doi: 10.1111/bjh.15542
Schafer V, White HE, Gerrard G, Mobius S, Saussele S, Franke GN, et al. Assessment of individual molecular response in chronic myeloid leukemia patients with atypical BCR-ABL1 fusion transcripts: recommendations by the EUTOS cooperative network. J Cancer Res Clin Oncol. 2021;147:3081–9.
pubmed: 33677711 pmcid: 8397658 doi: 10.1007/s00432-021-03569-8
Kjaer L, Skov V, Andersen MT, Aggerholm A, Clair P, Gniot M, et al. Variant-specific discrepancy when quantitating BCR-ABL1 e13a2 and e14a2 transcripts using the Europe Against Cancer qPCR assay. Eur J Haematol. 2019;103:26–34.
pubmed: 30985947 doi: 10.1111/ejh.13238
Dominy KM, Claudiani S, O’Hare M, Szydlo R, Gerrard G, Foskett P, et al. Assessment of quantitative polymerase chain reaction for BCR-ABL1 transcripts in chronic myeloid leukaemia: Are improved outcomes in patients with e14a2 transcripts an artefact of technology? Br J Haematol. 2022;197:52–62.
pubmed: 34997766 doi: 10.1111/bjh.18026
Salmon M, White HE, Zizkova H, Gottschalk A, Motlova E, Cerveira N, et al. Impact of BCR::ABL1 transcript type on RT-qPCR amplification performance and molecular response to therapy. Leukemia. 2022;36:1879–86.
pubmed: 35676453 pmcid: 9252903 doi: 10.1038/s41375-022-01612-2
Pfirrmann M, Evtimova D, Saussele S, Castagnetti F, Cervantes F, Janssen J, et al. No influence of BCR-ABL1 transcript types e13a2 and e14a2 on long-term survival: results in 1494 patients with chronic myeloid leukemia treated with imatinib. J Cancer Res Clin Oncol. 2017;143:843–50.
pubmed: 28083711 doi: 10.1007/s00432-016-2321-2
Claudiani S, Apperley JF, Gale RP, Clark R, Szydlo R, Deplano S, et al. E14a2 BCR-ABL1 transcript is associated with a higher rate of treatment-free remission in individuals with chronic myeloid leukemia after stopping tyrosine kinase inhibitor therapy. Haematologica. 2017;102:e297–e9.
pubmed: 28495914 pmcid: 5541883 doi: 10.3324/haematol.2017.168740
D’Adda M, Farina M, Schieppati F, Borlenghi E, Bottelli C, Cerqui E, et al. The e13a2 BCR-ABL transcript negatively affects sustained deep molecular response and the achievement of treatment-free remission in patients with chronic myeloid leukemia who receive tyrosine kinase inhibitors. Cancer. 2019;125:1674–82.
pubmed: 30707758 doi: 10.1002/cncr.31977
Pagani IS, Dang P, Saunders VA, Grose R, Shanmuganathan N, Kok CH, et al. Lineage of measurable residual disease in patients with chronic myeloid leukemia in treatment-free remission. Leukemia. 2020;34:1052–61.
pubmed: 31768016 doi: 10.1038/s41375-019-0647-x
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;34:966–84.
pubmed: 32127639 pmcid: 7214240 doi: 10.1038/s41375-020-0776-2
Zabriskie MS, Eide CA, Tantravahi SK, Vellore NA, Estrada J, Nicolini FE, et al. BCR-ABL1 compound mutations combining key kinase domain positions confer clinical resistance to ponatinib in Ph chromosome-positive leukemia. Cancer Cell. 2014;26:428–42.
pubmed: 25132497 pmcid: 4160372 doi: 10.1016/j.ccr.2014.07.006
Gibbons DL, Pricl S, Posocco P, Laurini E, Fermeglia M, Sun H, et al. Molecular dynamics reveal BCR-ABL1 polymutants as a unique mechanism of resistance to PAN-BCR-ABL1 kinase inhibitor therapy. Proc Natl Acad Sci USA. 2014;111:3550–5.
pubmed: 24550512 pmcid: 3948238 doi: 10.1073/pnas.1321173111
Byrgazov K, Lucini CB, Valent P, Hantschel O, Lion T. BCR-ABL1 compound mutants display differential and dose-dependent responses to ponatinib. Haematologica. 2018;103:e10–e2.
pubmed: 28983061 pmcid: 5777206 doi: 10.3324/haematol.2017.176347
Soverini S, Martelli M, Bavaro L, De Benedittis C, Sica S, Sora F, et al. BCR-ABL1 compound mutants: prevalence, spectrum and correlation with tyrosine kinase inhibitor resistance in a consecutive series of Philadelphia chromosome-positive leukemia patients analyzed by NGS. Leukemia. 2021;35:2102–7.
pubmed: 33262525 doi: 10.1038/s41375-020-01098-w
Kang KH, Kim SH, Choi SY, Yoo HL, Lee MY, Song HY, et al. Compound mutations involving T315I and P-loop mutations are the major components of multiple mutations detected in tyrosine kinase inhibitor resistant chronic myeloid leukemia. Leuk Res. 2019;76:87–93.
pubmed: 30503643 doi: 10.1016/j.leukres.2018.10.019
Soverini S, Hochhaus A, Nicolini FE, Gruber F, Lange T, Saglio G, et al. BCR-ABL kinase domain mutation analysis in chronic myeloid leukemia patients treated with tyrosine kinase inhibitors: recommendations from an expert panel on behalf of European LeukemiaNet. Blood. 2011;118:1208–15.
pubmed: 21562040 doi: 10.1182/blood-2010-12-326405
Kizilors A, Crisa E, Lea N, Passera R, Mian S, Anwar J, et al. Effect of low-level BCR-ABL1 kinase domain mutations identified by next-generation sequencing in patients with chronic myeloid leukaemia: a population-based study. Lancet Haematol. 2019;6:e276–e84.
pubmed: 31036317 doi: 10.1016/S2352-3026(19)30027-4
Soverini S, Abruzzese E, Bocchia M, Bonifacio M, Galimberti S, Gozzini A, et al. Next-generation sequencing for BCR-ABL1 kinase domain mutation testing in patients with chronic myeloid leukemia: a position paper. J Hematol Oncol. 2019;12:131.
pubmed: 31801582 pmcid: 6894351 doi: 10.1186/s13045-019-0815-5
Soverini S, De Santis S, Martelli M, Monaldi C, Castagnetti F, Gugliotta G, et al. Droplet digital PCR for the detection of second-generation tyrosine kinase inhibitor-resistant BCR::ABL1 kinase domain mutations in chronic myeloid leukemia. Leukemia. 2022;36:2250–60.
pubmed: 35908105 doi: 10.1038/s41375-022-01660-8
Machova Polakova K, Kulvait V, Benesova A, Linhartova J, Klamova H, Jaruskova M, et al. Next-generation deep sequencing improves detection of BCR-ABL1 kinase domain mutations emerging under tyrosine kinase inhibitor treatment of chronic myeloid leukemia patients in chronic phase. J Cancer Res Clin Oncol. 2015;141:887–99.
pubmed: 25367136 doi: 10.1007/s00432-014-1845-6
Soverini S, De Benedittis C, Machova Polakova K, Brouckova A, Horner D, Iacono M, et al. Unraveling the complexity of tyrosine kinase inhibitor-resistant populations by ultra-deep sequencing of the BCR-ABL kinase domain. Blood. 2013;122:1634–48.
pubmed: 23794064 doi: 10.1182/blood-2013-03-487728
Soverini S, De Benedittis C, Castagnetti F, Gugliotta G, Mancini M, Bavaro L, et al. In chronic myeloid leukemia patients on second-line tyrosine kinase inhibitor therapy, deep sequencing of BCR-ABL1 at the time of warning may allow sensitive detection of emerging drug-resistant mutants. BMC Cancer. 2016;16:572.
pubmed: 27485109 pmcid: 4970247 doi: 10.1186/s12885-016-2635-0
Baer C, Kern W, Koch S, Nadarajah N, Schindela S, Meggendorfer M, et al. Ultra-deep sequencing leads to earlier and more sensitive detection of the tyrosine kinase inhibitor resistance mutation T315I in chronic myeloid leukemia. Haematologica. 2016;101:830–8.
pubmed: 27102501 pmcid: 5004462 doi: 10.3324/haematol.2016.145888
Soverini S, Bavaro L, De Benedittis C, Martelli M, Iurlo A, Orofino N, et al. Prospective assessment of NGS-detectable mutations in CML patients with nonoptimal response: the NEXT-in-CML study. Blood. 2020;135:534–41.
pubmed: 31877211 doi: 10.1182/blood.2019002969
Morales J, Pujar S, Loveland JE, Astashyn A, Bennett R, Berry A, et al. A joint NCBI and EMBL-EBI transcript set for clinical genomics and research. Nature. 2022;604:310–5.
pubmed: 35388217 pmcid: 9007741 doi: 10.1038/s41586-022-04558-8
Deininger MW, Hodgson JG, Shah NP, Cortes JE, Kim DW, Nicolini FE, et al. Compound mutations in BCR-ABL1 are not major drivers of primary or secondary resistance to ponatinib in CP-CML patients. Blood. 2016;127:703–12.
pubmed: 26603839 pmcid: 4760131 doi: 10.1182/blood-2015-08-660977
Wang D, Pan H, Wang Y. T315L: a novel mutation within BCR-ABL kinase domain confers resistance against ponatinib. Leuk Lymphoma. 2017;58:1733–5.
pubmed: 27813432 doi: 10.1080/10428194.2016.1251591
Zhang J, Adrian FJ, Jahnke W, Cowan-Jacob SW, Li AG, Iacob RE, et al. Targeting Bcr-Abl by combining allosteric with ATP-binding-site inhibitors. Nature. 2010;463:501–6.
pubmed: 20072125 pmcid: 2901986 doi: 10.1038/nature08675
Wylie AA, Schoepfer J, Jahnke W, Cowan-Jacob SW, Loo A, Furet P, et al. The allosteric inhibitor ABL001 enables dual targeting of BCR-ABL1. Nature. 2017;543:733–7.
pubmed: 28329763 doi: 10.1038/nature21702
Hughes TP, Mauro MJ, Cortes JE, Minami H, Rea D, DeAngelo DJ, et al. Asciminib in Chronic Myeloid Leukemia after ABL Kinase Inhibitor Failure. N. Engl J Med. 2019;381:2315–26.
pubmed: 31826340 pmcid: 7724923 doi: 10.1056/NEJMoa1902328
Eide CA, Zabriskie MS, Savage Stevens SL, Antelope O, Vellore NA, Than H, et al. Combining the Allosteric Inhibitor Asciminib with Ponatinib Suppresses Emergence of and Restores Efficacy against Highly Resistant BCR-ABL1 Mutants. Cancer Cell. 2019;36:431–43 e5.
pubmed: 31543464 pmcid: 6893878 doi: 10.1016/j.ccell.2019.08.004
Mauro MJ, Hughes TP, Kim DW, Rea D, Cortes JE, Hochhaus A, et al. Asciminib monotherapy in patients with CML-CP without BCR::ABL1 T315I mutations treated with at least two prior TKIs: 4-year phase 1 safety and efficacy results. Leukemia. 2023;37:1048–59.
pubmed: 36949155 pmcid: 10169635 doi: 10.1038/s41375-023-01860-w
Hochhaus A, Rea D, Boquimpani C, Minami Y, Cortes JE, Hughes TP, et al. Asciminib vs bosutinib in chronic-phase chronic myeloid leukemia previously treated with at least two tyrosine kinase inhibitors: longer-term follow-up of ASCEMBL. Leukemia. 2023;37:617–26.
pubmed: 36717654 pmcid: 9991909 doi: 10.1038/s41375-023-01829-9
Cortes JE, Hughes TP, Mauro MJ, Hochhaus A, Rea D, Goh YT, et al. Asciminib, a First-in-Class STAMP Inhibitor, Provides Durable Molecular Response in Patients (pts) with Chronic Myeloid Leukemia (CML) Harboring the T315I Mutation: Primary Efficacy and Safety Results from a Phase 1 Trial. Blood. 2020;136:47–50.
doi: 10.1182/blood-2020-139677
Parker WT, Phillis SR, Yeung DT, Hughes TP, Scott HS, Branford S. Many BCR-ABL1 compound mutations reported in chronic myeloid leukemia patients may actually be artifacts due to PCR-mediated recombination. Blood. 2014;124:153–5.
pubmed: 24993880 doi: 10.1182/blood-2014-05-573485
Parker WT, Lawrence RM, Ho M, Irwin DL, Scott HS, Hughes TP, et al. Sensitive detection of BCR-ABL1 mutations in patients with chronic myeloid leukemia after imatinib resistance is predictive of outcome during subsequent therapy. J Clin Oncol. 2011;29:4250–9.
pubmed: 21990409 doi: 10.1200/JCO.2011.35.0934
Parker WT, Ho M, Scott HS, Hughes TP, Branford S. Poor response to second-line kinase inhibitors in chronic myeloid leukemia patients with multiple low-level mutations, irrespective of their resistance profile. Blood. 2012;119:2234–8.
pubmed: 22210874 doi: 10.1182/blood-2011-08-375535
Sanchez R, Dorado S, Ruiz-Heredia Y, Martin-Munoz A, Rosa-Rosa JM, Ribera J, et al. Detection of kinase domain mutations in BCR::ABL1 leukemia by ultra-deep sequencing of genomic DNA. Sci Rep. 2022;12:13057.
pubmed: 35906470 pmcid: 9338264 doi: 10.1038/s41598-022-17271-3
Polivkova V, Benesova A, Zizkova H, Koblihova J, Curik N, Motlova E, et al. Sensitivity and reliability of DNA-based mutation analysis by allele-specific digital PCR to follow resistant BCR-ABL1-positive cells. Leukemia. 2021;35:2419–23.
pubmed: 33772144 doi: 10.1038/s41375-021-01226-0
Minervini CF, Cumbo C, Orsini P, Anelli L, Zagaria A, Impera L, et al. Mutational analysis in BCR-ABL1 positive leukemia by deep sequencing based on nanopore MinION technology. Exp Mol Pathol. 2017;103:33–7.
pubmed: 28663031 doi: 10.1016/j.yexmp.2017.06.007
Cavelier L, Ameur A, Haggqvist S, Hoijer I, Cahill N, Olsson-Stromberg U, et al. Clonal distribution of BCR-ABL1 mutations and splice isoforms by single-molecule long-read RNA sequencing. BMC Cancer. 2015;15:45.
pubmed: 25880391 pmcid: 4335374 doi: 10.1186/s12885-015-1046-y
Kang HY, Hwang JY, Kim SH, Goh HG, Kim M, Kim DW. Comparison of allele specific oligonucleotide-polymerase chain reaction and direct sequencing for high throughput screening of ABL kinase domain mutations in chronic myeloid leukemia resistant to imatinib. Haematologica. 2006;91:659–62.
pubmed: 16627254
Ernst T, Hoffmann J, Erben P, Hanfstein B, Leitner A, Hehlmann R, et al. ABL single nucleotide polymorphisms may masquerade as BCR-ABL mutations associated with resistance to tyrosine kinase inhibitors in patients with chronic myeloid leukemia. Haematologica. 2008;93:1389–93.
pubmed: 18603549 doi: 10.3324/haematol.12964
Lee TS, Ma W, Zhang X, Giles F, Cortes J, Kantarjian H, et al. BCR-ABL alternative splicing as a common mechanism for imatinib resistance: evidence from molecular dynamics simulations. Mol Cancer Ther. 2008;7:3834–41.
pubmed: 19056677 doi: 10.1158/1535-7163.MCT-08-0482
Laudadio J, Deininger MW, Mauro MJ, Druker BJ, Press RD. An intron-derived insertion/truncation mutation in the BCR-ABL kinase domain in chronic myeloid leukemia patients undergoing kinase inhibitor therapy. J Mol Diagn. 2008;10:177–80.
pubmed: 18276770 pmcid: 2259473 doi: 10.2353/jmoldx.2008.070128
Marce S, Cortes M, Zamora L, Cabezon M, Grau J, Milla F, et al. A thirty-five nucleotides BCR-ABL1 insertion mutation of controversial significance confers resistance to imatinib in a patient with chronic myeloid leukemia (CML). Exp Mol Pathol. 2015;99:16–8.
pubmed: 25913326 doi: 10.1016/j.yexmp.2015.04.007
O’Hare T, Zabriskie MS, Eide CA, Agarwal A, Adrian LT, You H, et al. The BCR-ABL35INS insertion/truncation mutant is kinase-inactive and does not contribute to tyrosine kinase inhibitor resistance in chronic myeloid leukemia. Blood. 2011;118:5250–4.
pubmed: 21908430 pmcid: 3217407 doi: 10.1182/blood-2011-05-349191
Marin D, Bazeos A, Mahon FX, Eliasson L, Milojkovic D, Bua M, et al. Adherence is the critical factor for achieving molecular responses in patients with chronic myeloid leukemia who achieve complete cytogenetic responses on imatinib. J Clin Oncol. 2010;28:2381–8.
pubmed: 20385986 pmcid: 6366340 doi: 10.1200/JCO.2009.26.3087
Barnes EJ, Eide CA, Kaempf A, Bottomly D, Romine KA, Wilmot B, et al. Secondary fusion proteins as a mechanism of BCR::ABL1 kinase-independent resistance in chronic myeloid leukaemia. Br J Haematol. 2023;200:323–8.
pubmed: 36264026 doi: 10.1111/bjh.18515
Martin-Cabrera P, Haferlach C, Kern W, Schnittger S, Haferlach T. BCR-ABL1-positive and JAK2 V617F-positive clones in 23 patients with both aberrations reveal biologic and clinical importance. Br J Haematol. 2017;176:135–9.
pubmed: 26847954 doi: 10.1111/bjh.13932
Wasilewska EM, Panasiuk B, Gniot M, Sawicka A, Kozlowska K, Lewandowski K, et al. Clonal chromosomal aberrations in Philadelphia negative cells such as monosomy 7 and trisomy 8 may persist for years with no impact on the long term outcome in patients with chronic myeloid leukemia. Cancer Genet. 2017;216-217:1–9.
pubmed: 29025581 doi: 10.1016/j.cancergen.2017.04.066

Auteurs

Nicholas C P Cross (NCP)

Faculty of Medicine, University of Southampton, Southampton, UK. ncpc@soton.ac.uk.

Thomas Ernst (T)

Klinik für Innere Medizin II, Universitätsklinikum Jena, Jena, Germany.

Susan Branford (S)

Centre for Cancer Biology and SA Pathology, Adelaide, SA, Australia.

Jean-Michel Cayuela (JM)

Laboratory of Hematology, University Hospital Saint-Louis, AP-HP and EA3518, Université Paris Cité, Paris, France.

Michael Deininger (M)

Huntsman Cancer Center Salt Lake City, Salt Lake City, UT, USA.

Alice Fabarius (A)

III. Medizinische Klinik, Medizinische Fakultät Mannheim, Universität Heidelberg, Mannheim, Germany.

Dennis Dong Hwan Kim (DDH)

Department of Medical Oncology and Hematology, Princess Margaret Cancer Centre, University Health Network, University of Toronto, Toronto, Canada.

Katerina Machova Polakova (K)

Institute of Hematology and Blood Transfusion, Prague, Czech Republic.

Jerald P Radich (JP)

Fred Hutchinson Cancer Center, Seattle, WA, USA.

Rüdiger Hehlmann (R)

III. Medizinische Klinik, Medizinische Fakultät Mannheim, Universität Heidelberg, Mannheim, Germany.
ELN Foundation, Weinheim, Germany.

Andreas Hochhaus (A)

Klinik für Innere Medizin II, Universitätsklinikum Jena, Jena, Germany.

Jane F Apperley (JF)

Centre for Haematology, Imperial College London, London, UK.
Department of Clinical Haematology, Imperial College Healthcare NHS Trust, London, UK.

Simona Soverini (S)

Department of Medical and Surgical Sciences, Institute of Hematology "Lorenzo e Ariosto Seràgnoli", University of Bologna, Bologna, Italy.

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