Therapy-related myelodysplastic syndromes deserve specific diagnostic sub-classification and risk-stratification-an approach to classification of patients with t-MDS.
Journal
Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
15
05
2020
accepted:
05
06
2020
revised:
23
05
2020
pubmed:
1
7
2020
medline:
23
3
2021
entrez:
30
6
2020
Statut:
ppublish
Résumé
In the current World Health Organization (WHO)-classification, therapy-related myelodysplastic syndromes (t-MDS) are categorized together with therapy-related acute myeloid leukemia (AML) and t-myelodysplastic/myeloproliferative neoplasms into one subgroup independent of morphologic or prognostic features. Analyzing data of 2087 t-MDS patients from different international MDS groups to evaluate classification and prognostication tools we found that applying the WHO classification for p-MDS successfully predicts time to transformation and survival (both p < 0.001). The results regarding carefully reviewed cytogenetic data, classifications, and prognostic scores confirmed that t-MDS are similarly heterogeneous as p-MDS and therefore deserve the same careful differentiation regarding risk. As reference, these results were compared with 4593 primary MDS (p-MDS) patients represented in the International Working Group for Prognosis in MDS database (IWG-PM). Although a less favorable clinical outcome occurred in each t-MDS subset compared with p-MDS subgroups, FAB and WHO-classification, IPSS-R, and WPSS-R separated t-MDS patients into differing risk groups effectively, indicating that all established risk factors for p-MDS maintained relevance in t-MDS, with cytogenetic features having enhanced predictive power. These data strongly argue to classify t-MDS as a separate entity distinct from other WHO-classified t-myeloid neoplasms, which would enhance treatment decisions and facilitate the inclusion of t-MDS patients into clinical studies.
Identifiants
pubmed: 32595214
doi: 10.1038/s41375-020-0917-7
pii: 10.1038/s41375-020-0917-7
pmc: PMC7932916
doi:
Substances chimiques
Biomarkers, Tumor
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
835-849Références
Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, Le Beau MM, et al. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 2016;127:2391–405.
pubmed: 27069254
pmcid: 27069254
doi: 10.1182/blood-2016-03-643544
Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al. (eds). WHO classification of tumours of haematopoietic and lymphoid tissues. 4th ed. Lyon, France: International Agency for Research on Cancer; 2017.
Vardiman JW, Harris NL, Brunning RD. The World Health Organization (WHO) classification of the myeloid neoplasms. Blood. 2002;100:2292–302.
pubmed: 12239137
doi: 10.1182/blood-2002-04-1199
Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, Porwit A, et al. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009;114:937–51.
pubmed: 19357394
doi: 10.1182/blood-2009-03-209262
Greenberg P, Cox C, LeBeau MM, Fenaux P, Morel P, Sanz G, et al. International scoring system for evaluating prognosis in myelodysplastic syndromes. Blood. 1997;89:2079–88.
pubmed: 9058730
doi: 10.1182/blood.V89.6.2079
Greenberg PL, Tuechler H, Schanz J, Sanz G, Garcia-Manero G, Sole F, et al. Revised international prognostic scoring system for myelodysplastic syndromes. Blood. 2012;120:2454–65.
pubmed: 22740453
pmcid: 4425443
doi: 10.1182/blood-2012-03-420489
Malcovati L, Germing U, Kuendgen A, Della Porta MG, Pascutto C, Invernizzi R, et al. Time-dependent prognostic scoring system for predicting survival and leukemic evolution in myelodysplastic syndromes. J Clin Oncol. 2007;25:3503–10.
pubmed: 17687155
doi: 10.1200/JCO.2006.08.5696
Kantarjian H, O’Brien S, Ravandi F, Cortes J, Shan J, Bennett JM, et al. Proposal for a new risk model in myelodysplastic syndrome that accounts for events not considered in the original International Prognostic Scoring System. Cancer. 2008;113:1351–61.
pubmed: 18618511
pmcid: 4188533
doi: 10.1002/cncr.23697
Smith SM, Le Beau MM, Huo D, Karrison T, Sobecks RM, Anastasi J, et al. Clinical-cytogenetic associations in 306 patients with therapy-related myelodysplasia and myeloid leukemia: the University of Chicago series. Blood. 2003;102:43–52.
pubmed: 12623843
doi: 10.1182/blood-2002-11-3343
Kim SA, Hong J, Park WC, Shin DY, Koh Y, Kim I, et al. Better treatment outcomes in patients with actively treated therapy-related myeloid neoplasms harboring a normal karyotype. PLoS ONE. 2018;13:e0209800.
pubmed: 30596716
pmcid: 6312245
doi: 10.1371/journal.pone.0209800
Ok CY, Patel KP, Garcia-Manero G, Routbort MJ, Fu B, Tang G, et al. Mutational profiling of therapy-related myelodysplastic syndromes and acute myeloid leukemia by next generation sequencing, a comparison with de novo diseases. Leuk Res. 2015;39:348–54.
pubmed: 25573287
doi: 10.1016/j.leukres.2014.12.006
pmcid: 25573287
Hartmann L, Nadarajah N, Meggendorfer M, Höllein A, Vetro C, Kern W, et al. Molecular characterization of a second myeloid neoplasm developing after treatment for acute myeloid leukemia. Leukemia. 2019. https://doi.org/10.1038/s41375-019-0633-3 .
Kuzmanovic T, Patel BJ, Sanikommu SR, Nagata Y, Awada H, Kerr CM, et al. Genomics of therapy-related myeloid neoplasms. Haematologica. 2019. https://doi.org/10.3324/haematol.2019.219352 .
Guru Murthy GS, Hamadani M, Dhakal B, Hari P, Atallah E. Incidence and survival of therapy related myeloid neoplasm in United States. Leuk Res. 2018;71:95–9.
pubmed: 30048839
doi: 10.1016/j.leukres.2018.07.013
pmcid: 30048839
Shih AH, Chung SS, Dolezal EK, Zhang SJ, Abdel-Wahab OI, Park CY, et al. Mutational analysis of therapy-related myelodysplastic syndromes and acute myelogenous leukemia. Haematologica. 2013;98:908–12.
pubmed: 23349305
pmcid: 3669447
doi: 10.3324/haematol.2012.076729
Gillis NK, Ball M, Zhang Q, Ma Z, Zhao Y, Yoder SJ, et al. Clonal haemopoiesis and therapy-related myeloid malignancies in elderly patients: a proof-of-concept, case-control study. Lancet Oncol. 2017;18:112–21.
pubmed: 27927582
doi: 10.1016/S1470-2045(16)30627-1
pmcid: 27927582
Schroeder T, Kuendgen A, Kayser S, Kröger N, Braulke F, Platzbecker U, et al. Therapy-related myeloid neoplasms following treatment with radioiodine. Haematologica. 2012;97:206–12.
pubmed: 21993688
pmcid: 3269479
doi: 10.3324/haematol.2011.049114
Kern W, Haferlach T, Schnittger S, Hiddemann W, Schoch C. Prognosis in therapy-related acute myeloid leukemia and impact of karyotype. J Clin Oncol. 2004;22:2510–1.
pubmed: 15197216
doi: 10.1200/JCO.2004.99.301
pmcid: 15197216
Kayser S, Döhner K, Krauter J, Köhne CH, Horst HA, Held G, et al. The impact of therapy-related acute myeloid leukemia (AML) on outcome in 2853 adult patients with newly diagnosed AML. Blood. 2011;117:2137–45.
pubmed: 21127174
doi: 10.1182/blood-2010-08-301713
pmcid: 21127174
Lindsley RC, Mar BG, Mazzola E, Grauman PV, Shareef S, Allen SL, et al. Acute myeloid leukemia ontogeny is defined by distinct somatic mutations. Blood. 2015;125:1367–76.
pubmed: 25550361
pmcid: 4342352
doi: 10.1182/blood-2014-11-610543
Singh ZN, Huo D, Anastasi J, Smith SM, Karrison T, Le Beau MM, et al. Therapy-related myelodysplastic syndrome: morphologic subclassification may not be clinically relevant. Am J Clin Pathol. 2007;127:197–205.
pubmed: 17210514
doi: 10.1309/NQ3PMV4U8YV39JWJ
pmcid: 17210514
Zeidan AM, Al Ali N, Barnard J, Padron E, Lancet JE, Sekeres MA, et al. Comparison of clinical outcomes and prognostic utility of risk stratification tools in patients with therapy-related vs de novo myelodysplastic syndromes: a report on behalf of the MDS Clinical Research Consortium. Leukemia. 2017;31:1391–7.
pubmed: 28111463
doi: 10.1038/leu.2017.33
pmcid: 28111463
Quintás-Cardama A, Daver N, Kim H, Dinardo C, Jabbour E, Kadia T, et al. A prognostic model of therapy-related myelodysplastic syndrome for predicting survival and transformation to acute myeloid leukemia. Clin Lymphoma Myeloma Leuk. 2014;14:401–10.
pubmed: 24875590
pmcid: 4167474
doi: 10.1016/j.clml.2014.03.001
Borate U, Norris BA, Statler A, Fu R, Bucy T, Sekeres MA. Representation of therapy-related myelodysplastic syndrome in clinical trials over the past 20 years. Blood Adv. 2019;3:2738–47.
pubmed: 31537526
pmcid: 6759730
doi: 10.1182/bloodadvances.2019000293
Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick HR, et al. Proposals for the classification of the myelodysplastic syndromes. Br J Haematol. 1982;51:189–99.
pubmed: 6952920
doi: 10.1111/j.1365-2141.1982.tb08475.x
pmcid: 6952920
Valent P, Orazi A, Steensma DP, Ebert BL, Haase D, Malcovati L, et al. Proposed minimal diagnostic criteria for myelodysplastic syndromes (MDS) and potential pre-MDS conditions. Oncotarget 2017;43:73483–500.
doi: 10.18632/oncotarget.19008
McGowan-Jordan J, Schmid M. ISCN 2016: An international system for human cytogenomic nomenclature. S. Karger, Basel, 2016.
Harrell FE, Lee KL, Mark DB. Multivariable prognostic models: Issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996;15:361–87.
pubmed: 8668867
doi: 10.1002/(SICI)1097-0258(19960229)15:4<361::AID-SIM168>3.0.CO;2-4
pmcid: 8668867
Core Team, R: a Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, 2018, https://www.R-project.org/ .
Therneau T, A Package for Survival Analysis in S. Version 2.38, 2015, http://CRAN.R-project.org/package=survival .
Le Beau MM, Albain KS, Larson RA, Vardiman JW, Davis EM, Blough RR, et al. Clinical and cytogenetic correlations in 63 patients with therapy-related myelodysplastic syndromes and acute nonlymphocytic leukemia: further evidence for characteristic abnormalities of chromosomes no. 5 and 7. J Clin Oncol. 1986;4:325–45.
pubmed: 3950675
doi: 10.1200/JCO.1986.4.3.325
Pedersen-Bjergaard J, Philip P, Larsen SO, Andersson M, Daugaard G, Ersbøll J, et al. Therapy-related myelodysplasia and acute myeloid leukemia. Cytogenetic characteristics of 115 consecutive cases and risk in seven cohorts of patients treated intensively for malignant diseases in the Copenhagen series. Leukemia. 1993;7:1975–86.
pubmed: 8255096
Kuendgen A, Tuechler H, Nomdedeu M, Haase D, Garcia-Manero G, Komrokij RS, et al. Frequency and prognostic significance of cytogenetic abnormalities in 1269 patients with therapy-related myelodysplastic syndrome - a study of the international working group (IWG-PM) for myelodysplastic syndromes (MDS). Blood. 2016;128:112.
doi: 10.1182/blood.V128.22.112.112
Pui CH, Relling MV, Rivera GK, Hancock ML, Raimondi SC, Heslop HE, et al. Epipodophyllotoxin-related acute myeloid leukemia: a study of 35 cases. Leukemia. 1995;9:1990–6.
pubmed: 8609707
pmcid: 8609707
Andersen MK, Johansson B, Larsen SO, Pedersen-Bjergaard J. Chromosomal abnormalities in secondary MDS and AML. Relationship to drugs and radiation with specific emphasis on the balanced rearrangements. Haematologica. 1998;83:483–8.
pubmed: 9676019
pmcid: 9676019
Zhang Y, Poetsch M, Weber-Matthiesen K, Rohde K, Winkemann M, Haferlach T, Gassmann W, et al. Secondary acute leukaemias with 11q23 rearrangement: clinical, cytogenetic, FISH and FICTION studies. Br J Haematol. 1996;92:673–80.
pubmed: 8616034
doi: 10.1046/j.1365-2141.1996.00399.x
pmcid: 8616034
Bloomfield CD, Archer KJ, Mrózek K, et al. 11q23 balanced chromosome aberrations in treatment-related myelodysplastic syndromes and acute leukemia: report from an international workshop. Genes Chromosomes Cancer. 2002;33:362–78.
pubmed: 11921271
doi: 10.1002/gcc.10046
pmcid: 11921271
Ok CY, Hasserjian RP, Fox PS, Stingo F, Zuo Z, Young KH, et al. Application of the international prognostic scoring system-revised in therapy-related myelodysplastic syndromes and oligoblastic acute myeloid leukemia. Leukemia. 2014;28:185–9.
pubmed: 23787392
doi: 10.1038/leu.2013.191
pmcid: 23787392
Nazha A, Seastone DP, Keng M, Hobson S, Kalaycio M, Maciejewski JP, et al. The revised international prognostic scoring system (IPSS-R) is not predictive of survival in patients with secondary myelodysplastic syndromes. Leuk Lymphoma. 2015;56:3437–9.
pubmed: 25907427
doi: 10.3109/10428194.2015.1041391
pmcid: 25907427
Ganser A, Heuser M. Therapy-related myeloid neoplasms. Curr Opin Hematol. 2017;24:152–8.
pubmed: 27930389
doi: 10.1097/MOH.0000000000000316
Singhal D, Wee LYA, Kutyna MM, Chhetri R, Geoghegan J, Schreiber AW, et al. The mutational burden of therapy-related myeloid neoplasms is similar to primary myelodysplastic syndrome but has a distinctive distribution. Leukemia. 2019;33:2842–53.
pubmed: 31089247
doi: 10.1038/s41375-019-0479-8
Katagir S, Makishima H, Azuma K, Nannya Y, Saitoh Y, Yoshizawa S, et al. Predisposed genomic instability in pre-treatment bone marrow evolves to therapy-related myeloid neoplasms in malignant lymphoma. Haematologica 2019. https://doi.org/10.3324/haematol.2019.229856 .
Gibson CJ, Lindsley RC, Tchekmedyian V, Mar BG, Shi J, Jaiswal S, et al. Clonal hematopoiesis associated with adverse outcomes after autologous stem-cell transplantation for lymphoma. J Clin Oncol. 2017;35:1598–605.
pubmed: 28068180
pmcid: 5455707
doi: 10.1200/JCO.2016.71.6712
Schulz E, Valentin A, Ulz P, Beham-Schmid C, Lind K, Rupp V, et al. Germline mutations in the DNA damage response genes BRCA1, BRCA2, BARD1 and TP53 in patients with therapy related myeloid neoplasms. J Med Genet. 2012;49:422–8.
pubmed: 22652532
doi: 10.1136/jmedgenet-2011-100674
Furutani E, Shimamura A. Genetic predisposition to MDS: diagnosis and management. Hematol Am Soc Hematol Educ Program. 2019;2019:110–9.
doi: 10.1182/hematology.2019000021
Genovese G, Kähler AK, Handsaker RE, Lindberg J, Rose SA, Bakhoum SF, et al. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N. Engl J Med. 2014;371:2477–87.
pubmed: 25426838
pmcid: 4290021
doi: 10.1056/NEJMoa1409405
Genovese G, Jaiswal S, Ebert BL, McCarroll SA. Clonal hematopoiesis and blood-cancer risk. N. Engl J Med. 2015;372:1071–2.
pubmed: 25760361
doi: 10.1056/NEJMc1500684
Sperling AS, Gibson CJ, Ebert BL. The genetics of myelodysplastic syndrome: from clonal haematopoiesis to secondary leukaemia. Nat Rev Cancer. 2017;17:5–19.
pubmed: 27834397
doi: 10.1038/nrc.2016.112
Jaiswal S, Fontanillas P, Flannick J, Manning A, Grauman PV, Mar BG, et al. Age-related clonal hematopoiesis associated with adverse outcomes. N Engl J Med. 2014;371:2488–98.
pubmed: 25426837
pmcid: 4306669
doi: 10.1056/NEJMoa1408617
Pedersen-Bjergaard J, Pedersen M, Roulston D, Philip P. Different genetic pathways in leukemogenesis for patients presenting with therapy-related myelodysplasia and therapy-related acute myeloid leukemia. Blood. 1995;86:3542–52.
pubmed: 7579462
doi: 10.1182/blood.V86.9.3542.bloodjournal8693542
pmcid: 7579462
Bacher U, Haferlach C, Alpermann T, Schnittger S, Kern W, Haferlach T. Patients with therapy-related myelodysplastic syndromes and acute myeloid leukemia share genetic features but can be separated by blast counts and cytogenetic risk profiles into prognostically relevant subgroups. Leuk Lymphoma. 2013;54:639–42.
pubmed: 22853779
doi: 10.3109/10428194.2012.717275
pmcid: 22853779
Zhang L, Wang SA. A focused review of hematopoietic neoplasms occurring in the therapy-related setting. Int J Clin Exp Pathol. 2014;7:3512–23.
pubmed: 25120730
pmcid: 4128965
Kayser S, Krzykalla J, Elliott MA, Norsworthy K, Gonzales P, Hills RK, et al. Characteristics and outcome of patients with therapy-related acute promyelocytic leukemia front-line treated with or without arsenic trioxide. Leukemia. 2017;31:2347–54.
pubmed: 28322237
pmcid: 6037311
doi: 10.1038/leu.2017.92
Pulsoni A, Pagano L, Lo Coco F, Avvisati G, Mele L, Di Bona E, et al. Clinicobiological features and outcome of acute promyelocytic leukemia occurring as a second tumor: the GIMEMA experience. Blood. 2002;100:1972–6.
pubmed: 12200354
doi: 10.1182/blood-2001-12-0312
pmcid: 12200354
Ornstein MC, Mukherjee S, Mohan S, Elson P, Tiu RV, Saunthararajah Y, et al. Predictive factors for latency period and a prognostic model for survival in patients with therapy-related acute myeloid leukemia. Am J Hematol. 2014;89:168–73.
pubmed: 24123154
doi: 10.1002/ajh.23605
pmcid: 24123154
Aldoss I, Pullarkat V. Therapy-related acute myeloid leukemia with favorable cytogenetics: still favorable? Leuk Res. 2012;36:1547–51.
pubmed: 23031555
doi: 10.1016/j.leukres.2012.09.008
pmcid: 23031555
Patnaik MM, Vallapureddy R, Yalniz FF, Hanson CA, Ketterling RP, Lasho TL, et al. Therapy related-chronic myelomonocytic leukemia (CMML): Molecular, cytogenetic, and clinical distinctions from de novo CMML. Am J Hematol. 2018;93:65–73.
doi: 10.1002/ajh.24939