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Acute myeloid leukemia

Lomustine is beneficial to older AML with ELN2017 adverse risk profile and intermediate karyotype: a FILO study

Leukemia volume 35, pages 1291–1300 (2021)Cite this article

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Abstract

We previously reported the benefit of lomustine addition to conventional chemotherapy in older acute myeloid leukemias with nonadverse chromosomal aberrations in the LAM-SA 2007 randomized clinical trial (NCT00590837). A molecular analysis of 52 genes performed in 330 patients included in this trial, 163 patients being treated with lomustine in combination with idarubicin and cytarabine and 167 without lomustine, identified 1088 mutations with an average of 3.3 mutations per patient. NPM1, FLT3, and DNMT3A were the most frequently mutated genes. A putative therapeutic target was identified in 178 patients (54%). Among five molecular classifications analyzed, the ELN2017 risk classification has the stronger association with the clinical evolution. Patients not treated with lomustine have an expected survival prognosis in agreement with this classification regarding the overall and event-free survivals. In strong contrast, lomustine erased the ELN2017 classification prognosis. The benefit of lomustine in nonadverse chromosomal aberrations was restricted to patients with RUNX1, ASXL1, TP53, and FLT3-ITDhigh/NPM1WT mutations in contrast to the intermediate and favorable ELN2017 patients. This post-hoc analysis identified a subgroup of fit elderly AML patients with intermediate cytogenetics and molecular markers who may benefit from lomustine addition to intensive chemotherapy.

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Fig. 1: LAM-SA 2007 molecular workflow.
Fig. 2: LAM-SA 2007 mutation pattern.
Fig. 3: Mutations associations classified as gene categories as defined by Bullinger et al. [16], NPM1, signalization, DNA methylation, splicing, chromatin, transcription factors, cohesin, and antioncogenes.
Fig. 4: Circos plots of gene categories showing the profiles of co-mutations.
Fig. 5: Clinical responses (OS and EFS) to lomustine (lomustine) according to the ELN2017 risk classification.

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Acknowledgements

We thank physicians from participating centers as well as central and local data managers for collecting and monitoring patients’ data. We thank Filothèque members for the conservation of patients samples; Catherine Lacombe, Rachid Boulghana, Laure Cabaret, Ségolène Diry, Krishshanthi Sinnadurai, and Shari Dini Mohamed.

French Innovative Leukemia Organization

J.-P. Marolleau26, A. Aleme26, F. Orsini-Piocelle27, N. Cadoux27, N. Ifrah28, M. Hunault28, C. Marie28, A. Al Jijakli29, G. Lepeu30, H. Zerazhi30, M. Beyrne30, A. Banos31, S. Labarrere31, E. Deconinck32, M. Peria32, A. El Yamani33, O. Kadiri33, B. Choufi34, M. Brument34, A. Pigneux35, T. Leguay35, P.-Y. Dumas35, C. Berthou36, G. Guillerm36, G. Drugmanne36, O. Tournilhac37, G. Roy37, B. Audhuy38, S. Camara38, D. Caillot39, M. Grandjean39, J.-Y. Cahn40, C.-E. Bulabois40, B. Fief40, N. Vey41, C. Ladraa41, V. Dorvaux42, M. Hagopian42, N. Fegueux43, C. Fenoll43, V. Sabadash43, M. Ojeda44, C. Haby44, F. Witz45, C. Bonmati45, M. Lhuire45, J. Delaunay46, P. Peterlin46, L. Airiau46, L. Mannone47, I. Touitou47, E. Jourdan48, D. Umuhire48, M. Alexis49, O. Michel49, F. Dreyfus50, D. Bouscary50, A. Cheung50, L. Sanhes51, F. Touhami51, E. Ribas51, M. Puyade52, M.-P. Gallego-Hernanz52, N. Hugon52, C. Himberlin53, L. Maggi53, T. Lamy54, A. Testu54, E. Tavernier55, S. Marchand55, B. Lioure56, C. Kravanja56, L. Benboubker57, D. Nollet57, M. Attal58, C. Recher58, A. Sarry58, A. Lhermitte59, G. Yrica59, D. Schwartz59, N. Le Montagner59, C. Fenoll59, V. Sabadash59, D. Nollet59, L. Auvray59, R. Delepine59, A. Fayault59

Author information

Author notes

  1. These authors contributed equally: Laetitia Largeaud, Pascale Cornillet-Lefebvre, Jean-François Hamel, Christian Récher, Arnaud Pigneux, Eric Delabesse

Authors and Affiliations

  1. Hematology Biology, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse Oncopôle, Université Toulouse III Paul Sabatier, Toulouse, France

    Laetitia Largeaud, Naïs Prade, Stéphanie Dufrechou, Isabelle Luquet & Eric Delabesse

  2. Hematology Biology, Reims University Hospital, Reims, France

    Pascale Cornillet-Lefebvre

  3. Department of Statistics, Angers University Hospital, Angers, France

    Jean-François Hamel

  4. Clinical Hematology, Bordeaux University Hospital, Bordeaux University, Inserm 1035, Bordeaux, France

    Pierre-Yves Dumas & Arnaud Pigneux

  5. Bioinformatic Department, Claudius Regaud Institute, Institut Universitaire du Cancer de Toulouse Oncopôle, Toulouse, France

    Julien Plenecassagnes

  6. Hematology Biology, Angers University Hospital, Angers University, Inserm, CRCINA, Angers, France

    Odile Blanchet

  7. Clinical Hematology, Cote Basque General Hospital, Bayonne, France

    Anne Banos

  8. Hematology Biology, Nantes University Hospital, Nantes, France

    Marie C. Béné

  9. Clinical Hematology, Rennes University Hospital, Rennes, France

    Marc Bernard

  10. Clinical Hematology, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse Oncopôle, Université Toulouse III Paul Sabatier, Toulouse, France

    Sarah Bertoli & Christian Récher

  11. Clinical Hematology, Nancy University Hospital, Nancy, France

    Caroline Bonmati

  12. Clinical Hematology, Strasbourg University Hospital, Strasbourg, France

    Luc Matthieu Fornecker

  13. Clinical Hematology, Clermont-Ferrand University Hospital, Clermont-Ferrand, France

    Romain Guièze

  14. FILO Tumor Bank, Pitié-Salpêtrière Hospital, Paris, France

    Lamya Haddaoui

  15. Clinical Hematology, Angers University Hospital, INSERM U 892/CNRS 6299, Angers, France

    Mathilde Hunault & Norbert Ifrah

  16. Clinical Hematology, Institute of Oncology and Hematology, Brest University Hospital, Brest, France

    Jean Christophe Ianotto

  17. Clinical Hematology, Nîmes University Hospital, Nîmes, France

    Eric Jourdan

  18. Clinical Hematology, GHRMSA, Hôpital E Muller, Mulhouse, France

    Mario Ojeda

  19. Clinical Hematology, Nantes University Hospital, Nantes, France

    Pierre Peterlin

  20. Clinical Hematology, Aix-Marseille University, Inserm, CNRS, Institut Paoli-Calmettes, CRCM, Marseille, France

    Norbert Vey & Hicheri Yosr

  21. Clinical Hematology, Avignon General Hospital, Avignon, France

    Hacene Zerazhi

  22. Clinical Hematology, Montpellier University Hospital, Montpellier, France

    Hicheri Yosr

  23. Clinical Research Unit, Bordeaux University Hospital, Bordeaux, France

    Ariane Mineur

  24. FILO, Tours University Hospital, Tours, France

    Ariane Mineur

  25. Clinical Hematology, Grenoble University Hospital, Grenoble, France

    Jean-Yves Cahn

  26. Hematology Department, CHU Amiens, Amiens, France

    J.-P. Marolleau & A. Aleme

  27. Hematology Department, CH Annecy-Genevois, Annecy, France

    F. Orsini-Piocelle & N. Cadoux

  28. Hematology Department, CHU Angers, Angers, France

    N. Ifrah, M. Hunault & C. Marie

  29. Hematology Department, CH Argenteuil, Argenteuil, France

    A. Al Jijakli

  30. Hematology Department, CH Avignon, Avignon, France

    G. Lepeu, H. Zerazhi & M. Beyrne

  31. Hematology Department, CH Côte Basque, Bayonne, France

    A. Banos & S. Labarrere

  32. Hematology Department, CHU Besancon, Besancon, France

    E. Deconinck & M. Peria

  33. Hematology Department, CH Simone Veil, Blois, France

    A. El Yamani & O. Kadiri

  34. Hematology Department, CH Boulogne sur Mer, Boulogne sur Mer, France

    B. Choufi & M. Brument

  35. Hematology Department, CHU Bordeaux, Bordeaux, France

    A. Pigneux, T. Leguay & P.-Y. Dumas

  36. Hematology Department, CHU Brest, Brest, France

    C. Berthou, G. Guillerm & G. Drugmanne

  37. Hematology Department, CHU Clermont-Ferrand, Clermont-Ferrand, France

    O. Tournilhac & G. Roy

  38. Hematology Department, Hôpitaux Civils de Colmar, Colmar, France

    B. Audhuy & S. Camara

  39. Hematology Department, CHU Dijon, Dijon, France

    D. Caillot & M. Grandjean

  40. Hematology Department, CHU Grenoble-Alpes, Grenoble, France

    J.-Y. Cahn, C.-E. Bulabois & B. Fief

  41. Hematology Department, Institut Paoli-Calmettes, Marseille, France

    N. Vey & C. Ladraa

  42. Hematology Department, CHR Metz-Thionville, Metz, France

    V. Dorvaux & M. Hagopian

  43. Hematology Department, CHU Montpellier, Montpellier, France

    N. Fegueux, C. Fenoll & V. Sabadash

  44. Hematology Department, CH Emile-Muller, Mulhouse, France

    M. Ojeda & C. Haby

  45. Hematology Department, CHRU Nancy, Nancy, France

    F. Witz, C. Bonmati & M. Lhuire

  46. Hematology Department, CHU Nantes, Nantes, France

    J. Delaunay, P. Peterlin & L. Airiau

  47. Hematology Department, CHU Nice, Nice, France

    L. Mannone & I. Touitou

  48. Hematology Department, CHU Nimes, Nimes, France

    E. Jourdan & D. Umuhire

  49. Hematology Department, CHR Orléans, Orleans, France

    M. Alexis & O. Michel

  50. Hematology Department, CHU Cochin, Paris, France

    F. Dreyfus, D. Bouscary & A. Cheung

  51. Hematology Department, CH Perpignan, Perpignan, France

    L. Sanhes, F. Touhami & E. Ribas

  52. Hematology Department, CHU Poitiers, Poitiers, France

    M. Puyade, M.-P. Gallego-Hernanz & N. Hugon

  53. Hematology Department, CHU Reims, Reims, France

    C. Himberlin & L. Maggi

  54. Hematology Department, CHU Rennes, Rennes, France

    T. Lamy & A. Testu

  55. Hematology Department, CHU Saint-Etienne, Saint Priest En Jarez, France

    E. Tavernier & S. Marchand

  56. Hematology Department, CHU Strasbourg, Strasbourg, France

    B. Lioure & C. Kravanja

  57. Hematology Department, CHU Tours, Tours, France

    L. Benboubker & D. Nollet

  58. Hematology Department, CHU Toulouse, Toulouse, France

    M. Attal, C. Recher & A. Sarry

  59. Filo Central Office, Tours, France

    A. Lhermitte, G. Yrica, D. Schwartz, N. Le Montagner, C. Fenoll, V. Sabadash, D. Nollet, L. Auvray, R. Delepine & A. Fayault

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  1. Laetitia Largeaud
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Consortia

on behalf of the French Innovative Leukemia Organization (FILO)

  • J.-P. Marolleau
  • , A. Aleme
  • , F. Orsini-Piocelle
  • , N. Cadoux
  • , N. Ifrah
  • , M. Hunault
  • , C. Marie
  • , A. Al Jijakli
  • , G. Lepeu
  • , H. Zerazhi
  • , M. Beyrne
  • , A. Banos
  • , S. Labarrere
  • , E. Deconinck
  • , M. Peria
  • , A. El Yamani
  • , O. Kadiri
  • , B. Choufi
  • , M. Brument
  • , A. Pigneux
  • , T. Leguay
  • , P.-Y. Dumas
  • , C. Berthou
  • , G. Guillerm
  • , G. Drugmanne
  • , O. Tournilhac
  • , G. Roy
  • , B. Audhuy
  • , S. Camara
  • , D. Caillot
  • , M. Grandjean
  • , J.-Y. Cahn
  • , C.-E. Bulabois
  • , B. Fief
  • , N. Vey
  • , C. Ladraa
  • , V. Dorvaux
  • , M. Hagopian
  • , N. Fegueux
  • , C. Fenoll
  • , V. Sabadash
  • , M. Ojeda
  • , C. Haby
  • , F. Witz
  • , C. Bonmati
  • , M. Lhuire
  • , J. Delaunay
  • , P. Peterlin
  • , L. Airiau
  • , L. Mannone
  • , I. Touitou
  • , E. Jourdan
  • , D. Umuhire
  • , M. Alexis
  • , O. Michel
  • , F. Dreyfus
  • , D. Bouscary
  • , A. Cheung
  • , L. Sanhes
  • , F. Touhami
  • , E. Ribas
  • , M. Puyade
  • , M.-P. Gallego-Hernanz
  • , N. Hugon
  • , C. Himberlin
  • , L. Maggi
  • , T. Lamy
  • , A. Testu
  • , E. Tavernier
  • , S. Marchand
  • , B. Lioure
  • , C. Kravanja
  • , L. Benboubker
  • , D. Nollet
  • , M. Attal
  • , C. Recher
  • , A. Sarry
  • , A. Lhermitte
  • , G. Yrica
  • , D. Schwartz
  • , N. Le Montagner
  • , C. Fenoll
  • , V. Sabadash
  • , D. Nollet
  • , L. Auvray
  • , R. Delepine
  •  & A. Fayault

Corresponding author

Correspondence to Eric Delabesse.

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Members of the French Innovative Leukemia Organization (FILO) are listed below Acknowledgements.

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Largeaud, L., Cornillet-Lefebvre, P., Hamel, JF. et al. Lomustine is beneficial to older AML with ELN2017 adverse risk profile and intermediate karyotype: a FILO study. Leukemia 35, 1291–1300 (2021). https://doi.org/10.1038/s41375-020-01031-1

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  • DOI: https://doi.org/10.1038/s41375-020-01031-1

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