Cytogenetic abnormalities predict survival after allogeneic hematopoietic stem cell transplantation for pediatric acute myeloid leukemia: a PDWP/EBMT study.

Journal

Bone marrow transplantation

ISSN: 1476-5365

Titre abrégé: Bone Marrow Transplant

Pays: England

ID NLM: 8702459

Informations de publication

Date de publication:
15 Jan 2024

Historique:

received: 29 10 2023

accepted: 02 01 2024

revised: 14 12 2023

medline: 16 1 2024

pubmed: 16 1 2024

entrez: 15 1 2024

Statut: aheadofprint

Résumé

Poor-risk (PR) cytogenetic/molecular abnormalities generally direct pediatric patients with acute myeloid leukemia (AML) to allogeneic hematopoietic stem cell transplant (HSCT). We assessed the predictive value of cytogenetic risk classification at diagnosis with respect to post-HSCT outcomes in pediatric patients. Patients younger than 18 years at the time of their first allogeneic HSCT for AML in CR1 between 2005 and 2022 who were reported to the European Society for Blood and Marrow Transplantation registry were subgrouped into four categories. Of the 845 pediatric patients included in this study, 36% had an 11q23 abnormality, 24% had monosomy 7/del7q or monosomy 5/del5q, 24% had a complex or monosomal karyotype, and 16% had other PR cytogenetic abnormalities. In a multivariable model, 11q23 (hazard ratio [HR] = 0.66, P = 0.03) and other PR cytogenetic abnormalities (HR = 0.55, P = 0.02) were associated with significantly better overall survival when compared with monosomy 7/del7q or monosomy 5/del5q. Patients with other PR cytogenetic abnormalities had a lower risk of disease relapse after HSCT (HR = 0.49, P = 0.01) and, hence, better leukemia-free survival (HR = 0.55, P = 0.01). Therefore, we conclude that PR cytogenetic abnormalities at diagnosis predict overall survival after HSCT for AML in pediatric patients.

Identifiants

DOI: 10.1038/s41409-024-02197-3 PMID: 38225386

pubmed: 38225386

doi: 10.1038/s41409-024-02197-3

pii: 10.1038/s41409-024-02197-3

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Subventions

Organisme : U.S. Department of Health & Human Services | NIH | National Cancer Institute (NCI)

ID : P30CA021765

Organisme : American Lebanese Syrian Associated Charities (ALSAC)

ID : NA

Informations de copyright

Références

Rubnitz JE, Kaspers GJL. How I treat pediatric acute myeloid leukemia. Blood. 2021;138:1009–18.

doi: 10.1182/blood.2021011694 pubmed: 34115839

Loken MR, Alonzo TA, Pardo L, Gerbing RB, Raimondi SC, Hirsch BA, et al. Residual disease detected by multidimensional flow cytometry signifies high relapse risk in patients with de novo acute myeloid leukemia: a report from Children’s Oncology Group. Blood. 2012;120:1581–8.

doi: 10.1182/blood-2012-02-408336 pubmed: 22649108 pmcid: 3429302

Pui CH, Carroll WL, Meshinchi S, Arceci RJ. Biology, risk stratification, and therapy of pediatric acute leukemias: an update. J Clin Oncol. 2011;29:551–65.

doi: 10.1200/JCO.2010.30.7405 pubmed: 21220611

Rubnitz JE. Current management of childhood acute myeloid leukemia. Paediatr Drugs. 2017;19:1–10.

doi: 10.1007/s40272-016-0200-6 pubmed: 27785777

Balgobind BV, Raimondi SC, Harbott J, Zimmermann M, Alonzo TA, Auvrignon A, et al. Novel prognostic subgroups in childhood 11q23/MLL-rearranged acute myeloid leukemia: results of an international retrospective study. Blood. 2009;114:2489–96.

doi: 10.1182/blood-2009-04-215152 pubmed: 19528532 pmcid: 2927031

Horan JT, Alonzo TA, Lyman GH, Gerbing RB, Lange BJ, Ravindranath Y, et al. Impact of disease risk on efficacy of matched related bone marrow transplantation for pediatric acute myeloid leukemia: the Children’s Oncology Group. J Clin Oncol. 2008;26:5797–801.

doi: 10.1200/JCO.2007.13.5244 pubmed: 18955460 pmcid: 2645105

Pollard JA, Guest E, Alonzo TA, Gerbing RB, Loken MR, Brodersen LE, et al. Gemtuzumab Ozogamicin improves event-free survival and reduces relapse in pediatric KMT2A-rearranged AML: results from the Phase III children’s oncology group trial AAML0531. J Clin Oncol. 2021;39:3149–60.

doi: 10.1200/JCO.20.03048 pubmed: 34048275 pmcid: 8478392

van Weelderen RE, Klein K, Harrison CJ, Jiang Y, Abrahamsson J, Arad-Cohen N, et al. Measurable residual disease and fusion partner independently predict survival and relapse risk in childhood KMT2A-rearranged acute myeloid leukemia: a study by the international Berlin-Frankfurt-Munster Study Group. J Clin Oncol. 2023;41:2963–74.

doi: 10.1200/JCO.22.02120 pubmed: 36996387 pmcid: 10414713

Coenen EA, Zwaan CM, Reinhardt D, Harrison CJ, Haas OA, de Haas V, et al. Pediatric acute myeloid leukemia with t(8;16)(p11;p13), a distinct clinical and biological entity: a collaborative study by the International-Berlin-Frankfurt-Munster AML-study group. Blood. 2013;122:2704–13.

doi: 10.1182/blood-2013-02-485524 pubmed: 23974201 pmcid: 4314534

Harrison CJ, Hills RK, Moorman AV, Grimwade DJ, Hann I, Webb DK, et al. Cytogenetics of childhood acute myeloid leukemia: United Kingdom Medical Research Council Treatment trials AML 10 and 12. J Clin Oncol. 2010;28:2674–81.

doi: 10.1200/JCO.2009.24.8997 pubmed: 20439644

Marceau-Renaut A, Duployez N, Ducourneau B, Labopin M, Petit A, Rousseau A, et al. Molecular profiling defines distinct prognostic subgroups in childhood AML: a report from the french ELAM02 Study Group. Hemasphere. 2018;2:e31.

doi: 10.1097/HS9.0000000000000031 pubmed: 31723759 pmcid: 6745946

Masetti R, Pigazzi M, Togni M, Astolfi A, Indio V, Manara E, et al. CBFA2T3-GLIS2 fusion transcript is a novel common feature in pediatric, cytogenetically normal AML, not restricted to FAB M7 subtype. Blood. 2013;121:3469–72.

doi: 10.1182/blood-2012-11-469825 pubmed: 23407549

von Neuhoff C, Reinhardt D, Sander A, Zimmermann M, Bradtke J, Betts DR, et al. Prognostic impact of specific chromosomal aberrations in a large group of pediatric patients with acute myeloid leukemia treated uniformly according to trial AML-BFM 98. J Clin Oncol. 2010;28:2682–9.

doi: 10.1200/JCO.2009.25.6321

Armand P, Kim HT, DeAngelo DJ, Ho VT, Cutler CS, Stone RM, et al. Impact of cytogenetics on outcome of de novo and therapy-related AML and MDS after allogeneic transplantation. Biol Blood Marrow Transplant. 2007;13:655–64.

doi: 10.1016/j.bbmt.2007.01.079 pubmed: 17531775 pmcid: 2743535

Armand P, Kim HT, Zhang MJ, Perez WS, Dal Cin PS, Klumpp TR, et al. Classifying cytogenetics in patients with acute myelogenous leukemia in complete remission undergoing allogeneic transplantation: a Center for International Blood and Marrow Transplant Research study. Biol Blood Marrow Transplant. 2012;18:280–8.

doi: 10.1016/j.bbmt.2011.07.024 pubmed: 21810400

Chevallier P, Labopin M, Milpied N, Cornelissen JJ, Blaise D, Petersen E, et al. Impact of cytogenetics risk on outcome after reduced intensity conditioning allo-SCT from an HLA-identical sibling for patients with AML in first CR: a report from the acute leukemia working party of EBMT. Bone Marrow Transplant. 2012;47:1442–7.

doi: 10.1038/bmt.2012.55 pubmed: 22504932

Ferrant A, Labopin M, Frassoni F, Prentice HG, Cahn JY, Blaise D, et al. Karyotype in acute myeloblastic leukemia: prognostic significance for bone marrow transplantation in first remission: a European Group for Blood and Marrow Transplantation study. Acute Leukemia Working Party of the European Group for Blood and Marrow Transplantation (EBMT). Blood. 1997;90:2931–8.

pubmed: 9376573

Ogawa H, Ikegame K, Kawakami M, Takahashi S, Sakamaki H, Karasuno T, et al. Impact of cytogenetics on outcome of stem cell transplantation for acute myeloid leukemia in first remission: a large-scale retrospective analysis of data from the Japan Society for Hematopoietic Cell Transplantation. Int J Hematol. 2004;79:495–500.

doi: 10.1532/IJH97.03166 pubmed: 15239403

Alloin AL, Leverger G, Dalle JH, Galambrun C, Bertrand Y, Baruchel A, et al. Cytogenetics and outcome of allogeneic transplantation in first remission of acute myeloid leukemia: the French pediatric experience. Bone Marrow Transplant. 2017;52:516–21.

doi: 10.1038/bmt.2016.293 pubmed: 27941778

Chalandon Y, Barnett MJ, Horsman DE, Conneally EA, Nantel SH, Nevill TJ, et al. Influence of cytogenetic abnormalities on outcome after allogeneic bone marrow transplantation for acute myeloid leukemia in first complete remission. Biol Blood Marrow Transplant. 2002;8:435–43.

doi: 10.1053/bbmt.2002.v8.pm12234169 pubmed: 12234169

Gupta V, Tallman MS, He W, Logan BR, Copelan E, Gale RP, et al. Comparable survival after HLA-well-matched unrelated or matched sibling donor transplantation for acute myeloid leukemia in first remission with unfavorable cytogenetics at diagnosis. Blood. 2010;116:1839–48.

doi: 10.1182/blood-2010-04-278317 pubmed: 20538804 pmcid: 3173984

Schetelig J, Bornhauser M, Schmid C, Hertenstein B, Schwerdtfeger R, Martin H, et al. Matched unrelated or matched sibling donors result in comparable survival after allogeneic stem-cell transplantation in elderly patients with acute myeloid leukemia: a report from the cooperative German Transplant Study Group. J Clin Oncol. 2008;26:5183–91.

doi: 10.1200/JCO.2007.15.5184 pubmed: 18768435

Walter RB, Pagel JM, Gooley TA, Petersdorf EW, Sorror ML, Woolfrey AE, et al. Comparison of matched unrelated and matched related donor myeloablative hematopoietic cell transplantation for adults with acute myeloid leukemia in first remission. Leukemia. 2010;24:1276–82.

doi: 10.1038/leu.2010.102 pubmed: 20485378 pmcid: 3001162

Yanada M, Kurosawa S, Yamaguchi T, Uchida N, Miyawaki S, Kanamori H, et al. Effect of related donor availability on outcome of AML in the context of related and unrelated hematopoietic cell transplantation. Bone Marrow Transplant. 2013;48:390–5.

doi: 10.1038/bmt.2012.159 pubmed: 22941379

Bashey A, Zhang X, Sizemore CA, Manion K, Brown S, Holland HK, et al. T-cell-replete HLA-haploidentical hematopoietic transplantation for hematologic malignancies using post-transplantation cyclophosphamide results in outcomes equivalent to those of contemporaneous HLA-matched related and unrelated donor transplantation. J Clin Oncol. 2013;31:1310–6.

doi: 10.1200/JCO.2012.44.3523 pubmed: 23423745

Bertaina A, Zecca M, Buldini B, Sacchi N, Algeri M, Saglio F, et al. Unrelated donor vs HLA-haploidentical alpha/beta T-cell- and B-cell-depleted HSCT in children with acute leukemia. Blood. 2018;132:2594–607.

doi: 10.1182/blood-2018-07-861575 pubmed: 30348653

Ciurea SO, Zhang MJ, Bacigalupo AA, Bashey A, Appelbaum FR, Aljitawi OS, et al. Haploidentical transplant with posttransplant cyclophosphamide vs matched unrelated donor transplant for acute myeloid leukemia. Blood. 2015;126:1033–40.

doi: 10.1182/blood-2015-04-639831 pubmed: 26130705 pmcid: 4543223

Berger M, Lanino E, Cesaro S, Zecca M, Vassallo E, Faraci M, et al. Feasibility and outcome of haploidentical hematopoietic stem cell transplantation with post-transplant high-dose cyclophosphamide for children and adolescents with hematologic malignancies: an AIEOP-GITMO retrospective multicenter study. Biol Blood Marrow Transplant. 2016;22:902–9.

doi: 10.1016/j.bbmt.2016.02.002 pubmed: 26860636

Locatelli F, Merli P, Pagliara D, Li Pira G, Falco M, Pende D, et al. Outcome of children with acute leukemia given HLA-haploidentical HSCT after alphabeta T-cell and B-cell depletion. Blood. 2017;130:677–85.

doi: 10.1182/blood-2017-04-779769 pubmed: 28588018

Mrozek K, Marcucci G, Nicolet D, Maharry KS, Becker H, Whitman SP, et al. Prognostic significance of the European LeukemiaNet standardized system for reporting cytogenetic and molecular alterations in adults with acute myeloid leukemia. J Clin Oncol. 2012;30:4515–23.

doi: 10.1200/JCO.2012.43.4738 pubmed: 22987078 pmcid: 3518729

Patel JP, Gonen M, Figueroa ME, Fernandez H, Sun Z, Racevskis J, et al. Prognostic relevance of integrated genetic profiling in acute myeloid leukemia. N Engl J Med. 2012;366:1079–89.

doi: 10.1056/NEJMoa1112304 pubmed: 22417203 pmcid: 3545649

Rollig C, Bornhauser M, Thiede C, Taube F, Kramer M, Mohr B, et al. Long-term prognosis of acute myeloid leukemia according to the new genetic risk classification of the European LeukemiaNet recommendations: evaluation of the proposed reporting system. J Clin Oncol. 2011;29:2758–65.

doi: 10.1200/JCO.2010.32.8500 pubmed: 21632498

Sharma A, Huang S, Li Y, Brooke RJ, Ahmed I, Allewelt HB, et al. Outcomes of pediatric patients with therapy-related myeloid neoplasms. Bone Marrow Transplant. 2021;56:2997–3007.

doi: 10.1038/s41409-021-01448-x pubmed: 34480120 pmcid: 9260859

Bitan M, He W, Zhang MJ, Abdel-Azim H, Ayas MF, Bielorai B, et al. Transplantation for children with acute myeloid leukemia: a comparison of outcomes with reduced intensity and myeloablative regimens. Blood. 2014;123:1615–20.

doi: 10.1182/blood-2013-10-535716 pubmed: 24435046 pmcid: 3945869