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Decitabine improves progression-free survival in older high-risk MDS patients with multiple autosomal monosomies: results of a subgroup analysis of the randomized phase III study 06011 of the EORTC Leukemia Cooperative Group and German MDS Study Group

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Abstract

In a study of elderly AML patients treated with the hypomethylating agent decitabine (DAC), we noted a surprisingly favorable outcome in the (usually very unfavorable) subgroup with two or more autosomal monosomies (MK2+) within a complex karyotype (Lübbert et al., Haematologica 97:393-401, 2012). We now analyzed 206 myelodysplastic syndrome (MDS) patients (88 % of 233 patients randomized in the EORTC/GMDSSG phase III trial 06011, 61 of them with RAEBt, i.e. AML by WHO) with cytogenetics informative for MK status.. Endpoints are the following: complete/partial (CR/PR) and overall response rate (ORR) and progression-free (PFS) and overall survival (OS). Cytogenetic subgroups are the following: 63 cytogenetically normal (CN) patients, 143 with cytogenetic abnormalities, 73 of them MK-negative (MK−), and 70 MK-positive (MK+). These MK+ patients could be divided into 17 with a single autosomal monosomy (MK1) and 53 with at least two monosomies (MK2+). ORR with DAC in CN patients: 36.1 %, in MK− patients: 16.7 %, in MK+ patients: 43.6 % (MK1: 44.4 %, MK2+ 43.3 %). PFS was prolonged by DAC compared to best supportive care (BSC) in the CN (hazard ratio (HR) 0.55, 99 % confidence interval (CI), 0.26; 1.15, p = 0.03) and MK2+ (HR 0.50; 99 % CI, 0.23; 1.06, p = 0.016) but not in the MK−, MK+, and MK1 subgroups. OS was not improved by DAC in any subgroup. In conclusion, we demonstrate for the first time in a randomized phase III trial that high-risk MDS patients with complex karyotypes harboring two or more autosomal monosomies attain encouraging responses and have improved PFS with DAC treatment compared to BSC.

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Acknowledgments

The authors thank Philipp Sander and Margit Sauer for the editorial assistance and Claudia Schmoor for the helpful discussions. This publication was supported by the EORTC Charitable Trust; the 06011 trial was supported by an educational grant from MGI Pharma and Janssen Research and Development. Survival data of the PCH phase II studies were kindly provided by Janssen Research and Development. M.L. is supported by DFG (SFB 992/Medep).

Authors’ contributions

M.L., S. S., A. H., B. R., P. M., L. B., G. H., T. de W., and P. W. W. contributed to the conception and design. M. L., B. R., U. P., A. G., D. S., U. G., B. L, K.-H. P., H.-E. Sch., H. R. S., P. M., G. H., L. van der H., E. V., F. B., J.-P. M., A. G., C. A., T. de W., and P. W. W. contributed to the provision of study materials or patients. M.L., S. S., A. H., L. van der H., and G. H. contributed to the collection and assembly of data. M.L., S. S., and L. B. contributed to the data analyses and interpretation. M.L., S.S., and L. B. contributed to the manuscript writing. All authors have read and approved the final manuscript.

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Authors and Affiliations

  1. Division of Hematology, Oncology and Stem Cell Transplantation, University of Freiburg Medical Center, Freiburg, Germany

    Michael Lübbert, Björn Rüter, Lioudmila Bogatyreva & Heiko Becker

  2. European Organisation for Research and Treatment of Cancer Headquarters, Brussels, Belgium

    Stefan Suciu

  3. Department of Human Genetics, University Hospital, University of Leuven, Leuven, Belgium

    Anne Hagemeijer

  4. Department of Hematology and Oncology, University of Dresden, Dresden, Germany

    Uwe Platzbecker

  5. Department of Hematology and Oncology, Marienhospital, Düsseldorf, Germany

    Aristoteles Giagounidis

  6. Department of Hematology, AZ Sint-Jan Brugge-Oostende, Brugge, Belgium

    Dominik Selleslag

  7. University Hospital Center Rebro, Zagreb, Croatia

    Boris Labar

  8. Department of Hematology, Oncology and Clinical Immunology, Heinrich-Heine-University, Düsseldorf, Germany

    Ulrich Germing

  9. Department of Hematology/Oncology, Eberhard Karls University, Tübingen, Germany

    Helmut R. Salih

  10. Department of Hematology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands

    Petra Muus & Gerwin Huls

  11. Department of Medicine II, DIAKO Bremen, Bremen, Germany

    Karl-Heinz Pflüger

  12. Institute of Pathology, University of Freiburg, Freiburg, Germany

    Hans-Eckart Schaefer

  13. Institute for Medical Biometry and Medical Informatics, University of Freiburg, Freiburg, Germany

    Lioudmila Bogatyreva

  14. Hematology, Oncology, and Clinical Immunology, St Johannes Hospital, Duisburg, Germany

    Carlo Aul

  15. Department of Tumor Immunology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands

    Theo de Witte

  16. Department of Hematology, Hemostasis, Oncology, and Stem Cell Transplantation, Hannover Medical School, Hannover, Germany

    Arnold Ganser

  17. Department of Hematology, University Medical Center Groningen, Groningen, The Netherlands

    Gerwin Huls, Lieke van der Helm & Edo Vellenga

  18. C.H.U. Sart-Tilman, Liège, Belgium

    Frédéric Baron

  19. UPMC, UMRS 872 and Saint-Antoine Hospital, AP-HP, Paris, France

    Jean-Pierre Marie

  20. Department of Hematology, Haga Hospital, The Hague, The Netherlands

    Pierre W. Wijermans

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  1. Michael Lübbert
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on behalf of the EORTC Leukemia Group and the German MDS Study Group

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Correspondence to Michael Lübbert.

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Conflict of interest

The authors declare no competing financial conflict of interests except for the following authors (U, no compensation was received; C, compensation was received): Consultant or Advisory Role: Uwe Platzbecker, Celgene (C), Amgen (C), and Novartis (C); Aristoteles Giagounidis, Celgene (C); Dominik Selleslag, Celgene (C), Novartis (C), and Amgen (C); Arnold Ganser, Celgene (C) and Novartis (C); and Michael Lübbert, Johnson & Johnson (C); and Petra Muus, Alexion (U). Honoraria: Uwe Platzbecker, Celgene, Novartis, and Amgen; Aristoteles Giagounidis, Celgene; Dominik Selleslag, Celgene, Novartis, and Amgen; Ulrich Germing, Johnson & Johnson; and Arnold Ganser, Genzyme. Research Funding: Michael Lübbert, Johnson & Johnson; Uwe Platzbecker, Celgene and Novartis; and Ulrich Germing, MDS Registry Düsseldorf.

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Lübbert, M., Suciu, S., Hagemeijer, A. et al. Decitabine improves progression-free survival in older high-risk MDS patients with multiple autosomal monosomies: results of a subgroup analysis of the randomized phase III study 06011 of the EORTC Leukemia Cooperative Group and German MDS Study Group. Ann Hematol 95, 191–199 (2016). https://doi.org/10.1007/s00277-015-2547-0

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