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Total body irradiation + fludarabine compared to busulfan + fludarabine as “reduced-toxicity conditioning” for patients with acute myeloid leukemia treated with allogeneic hematopoietic cell transplantation in first complete remission: a study by the Acute Leukemia Working Party of the EBMT

Bone Marrow Transplantation volume 56, pages 481–491 (2021)Cite this article

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Abstract

The optimal conditioning for patients with acute myeloid leukemia in first complete remission treated with allogeneic hematopoietic cell transplantation (allo-HCT) has not been defined so far. In this retrospective study, we compared two “reduced-toxicity” regimens: intravenous busulfan at a total dose of 9.6 mg/kg (3 days) + fludarabine (Bu3/Flu) and total body irradiation at a dose of 8 Gy + fludarabine (TBI8Gy/Flu). In the entire study cohort (n = 518), the probabilities of overall survival (OS), leukemia-free survival (LFS), relapse and non-relapse mortality (NRM) at 2 years for Bu3/Flu and TBI8Gy/Flu were 62% vs. 72.5% (p = 0.051), 59.5% vs. 65% (p = 0.15), 30% vs. 20% (p = 0.01), and 10% vs. 14% (p = 0.18), respectively. In multivariate model for patients <50 years old, TBI8Gy/Flu was associated with improved LFS (hazard ratio (HR) = 0.5, p = 0.04), OS (HR = 0.31, p = 0.004), and survival free from both graft-versus-host disease and relapse (HR = 0.55, p = 0.03), as well as tendency to reduced risk of relapse (HR = 0.53, p = 0.08). Among patients aged 50 years or older the use of TBI8Gy/Flu was associated with increased incidence of NRM (HR = 3.9, p = 0.0009), with no significant impact on other outcome measures. We conclude that the use of TBI8Gy/Flu as “reduced-toxicity” regimen may be advised in younger patients with AML referred for allo-HCT.

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Fig. 1: Comparison of Bu3/Flu and TBI8Gy/Flu for patients <50 years old.
Fig. 2: Comparison of Bu3/Flu and TBI8Gy/Flu for patients aged 50 years or older.

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Acknowledgements

We sincerely thank the centers of the EBMT for contributing patient information and data collection. Principal investigators of the contributing institutions are listed below.

Principle investigators of the contributing institutions

Sonja Martin15, Patrice Chevallier16, Andreas Neubauer17, Gandhi Damaj18, Yener Koc19, Arnold Ganser20, Matthew Collin21, Ibrahim Yakoub-Agha22, Hakan Ozdogu23, Mercedes Colorado Araujo24, Maija Itäla-Remes25, Kim Orchard26, Cecilia Isaksson27, Wolfgang Bethge28, Hans Martin29, Mahmoud Aljurf30, Edgar Faber31, Dolores Caballero32, Pavel Zák33, Xavier Leleu34, Jacques-Olivier Bay35, Pierre-Simon Rohrlich36, Nicolaus Kröger37, Anne Huynh38, Kerstin Schäfer-Eckart39, Noel Milpied40, Stig Lenhoff41, Aloysius Ho42, Jose Luis Bello López43, Nicola Mordini44, Bruno Lioure45, Kazimierz Halaburda46, Attilio Olivieri47, Tobias Gedde-Dahl48, Rachel Protheroe49, Johanna Tischer50, Matthias Klammer51, Johannes Clausen52, Victoria Potter53, Marco Ladetto54, Herve Tilly55, Eric Deconinck56, Arne Brecht57, Lutz Peter Müller58, Thomas Heinicke59, Juan Pio Torres Carrete60, Ali Bazarbachi61, Péter Reményi62, Marie Thérèse Rubio63, Renato Fanin64, Jose Antonio Pérez-Simón65, Murawski Niels66, J. L. Diez-Martin67, Mutlu Arat68, Olivier Hermine69, Gerard Socié70, Jan J. Cornelissen71, Stella Santarone72, Denis Guyotat73, Claude Eric Bulabois74, Paolo Bernasconi75, Jan-Erik Johansson76, Radovan Vrhovac77, Hildegard Greinix78, José Luis López Lorenzo79, Shashikant Apte80, Charles Craddock81, Guido Kobbe82, Mohsen Al Zahrani83, Peter Dreger84, Andrzej Lange85, Abdelghani Tbakhi86, Ellen Meijer87, Carlos Vallejo Llamas88, Josep Maria Ribera Santasusana89, Paolo Corradini90, Fabio Benedetti91, Alessandro Rambaldi92, Virginie Gandemer93, Jean-Valère Malfuson94, Ain Kaare95, Antonio Risitano96, Mario Petrini97, Carmine Selleri98, Depei Wu99.

Author information

Authors and Affiliations

  1. Department of Bone Marrow Transplantation and Onco-Hematology, Maria Sklodowska-Curie National Research Institute of Oncology, Gliwice Branch, Gliwice, Poland

    Sebastian Giebel & Malgorzata Sobczyk-Kruszelnicka

  2. European Society for Blood and Marrow Transplantation Paris Study Office/CEREST-TC, Paris, France

    Myriam Labopin

  3. Department of Hematology and Oncology, University Hospital of Münster, University of Münster, Münster, Germany

    Matthias Stelljes

  4. Faculty of Medicine and Health Sciences, University of Nottingham, Nottingham, UK

    Jenny L. Byrne

  5. Department of Hematology, CHU Lapeyronie, Montpellier, France

    Nathalie Fegueux

  6. Department of Bone Marrow Transplantation, West German Cancer Centre, University Hospital of Essen, University of Duisburg, Essen, Germany

    Dietrich W. Beelen

  7. HSCT Unit, Hematology Department, Hospital Clínic de Barcelona, University of Barcelona, Barcelona, Catalunya, Spain

    Montserrat Rovira

  8. Department of Internal Medicine, Bone Marrow Transplantation Unit, University Hospital of Patras, Patras, Greece

    Alexandros Spyridonidis

  9. Programme de Transplantation & Therapie Cellulaire, Centre de Recherche en Cancérologie de Marseille, Institut Paoli Calmettes, Marseille, France

    Didier Blaise

  10. Department of Internal Medicine I, University Hospital Carl Gustav Carus, Dresden, Germany

    Martin Bornhäuser

  11. Division of Hematology, Antalya Medstar Hospital, Antalya, Turkey

    Ihsan Karadogan

  12. Division of Hematology and Oncology, Vanderbilt University Medical Center, Nashville, TN, USA

    Bipin N. Savani

  13. Hematology Division, Chaim Sheba Medical Center, Tel-Hashomer, Israel

    Arnon Nagler

  14. Department of Hematology, Hospital Saint Antoine, Paris, France

    Mohamad Mohty

  15. Robert_Bosch_Krankenhaus, Abt. Hämatologie/Onkologie, Stuttgart, Germany

    Sonja Martin

  16. CHU Nantes, Dept. D’Hematologie, Nantes, France

    Patrice Chevallier

  17. Philipps Universitaet Marburg, University Hospital Giessen and Marburg, Marburg, Germany

    Andreas Neubauer

  18. CHU CAEN, Institut d’hématologie de Basse-Normandie, Caen, France

    Gandhi Damaj

  19. Medical Park Hospitals, Stem Cell Transplant Unit, Antalya, Turkey

    Yener Koc

  20. Hannover Medical School, Department of Haematology, Hemostasis, Oncology, and Stem Cell Transplantation, Hannover, Germany

    Arnold Ganser

  21. Adult HSCT unit, Northern Centre for Bone Marrow Transplantation, Freeman Hospital, Newcastle Tyne, UK

    Matthew Collin

  22. CHU de Lille, LIRIC, INSERM U995, Université de Lille, Lille, France

    Ibrahim Yakoub-Agha

  23. Baskent University Hospital, Haematology Division, BMT Unit, Haemaology Reserach Laboratory, Training & Medical, Adana, Turkey

    Hakan Ozdogu

  24. Hospital U. Marqués de Valdecilla, Servicio de Hematología-Hemoterapia, Santander, Spain

    Mercedes Colorado Araujo

  25. Turku University Hospital, TD7 (Stem Cell Transplant Unit), Turku, Finland

    Maija Itäla-Remes

  26. Southampton General Hospital, Haematology, Oncology, & Paediatrics, Dept. of Haematology, Southampton, UK

    Kim Orchard

  27. Umea University Hospital, Hematology, Umea, Sweden

    Cecilia Isaksson

  28. Universitaet Tuebingen, Medizinische Klinik, Tuebingen, Germany

    Wolfgang Bethge

  29. Goethe-Universitaet, Medizinische Klinik II, Hämatologie, Medizinische Onkologie, Frankfurt Main, Germany

    Hans Martin

  30. King Faisal Specialist Hospital & Research Centre, Oncology (Section of Adult Haematolgy/BMT), Riyadh, Saudi Arabia

    Mahmoud Aljurf

  31. NADACE HAIMOM, University Hospital, Department of Haemato-Oncology, Olomouc, Czech Republic

    Edgar Faber

  32. Hospital Clínico, Servicio de Hematología, Salamanca, Spain

    Dolores Caballero

  33. Charles University Hospital, Department of Internal Medicine-Hematology, Hradec Kralove, Czech Republic

    Pavel Zák

  34. Hopital La Miletrie, Head of the Bone Marrow TransplantUnit, Clinical Hematology, Poitiers, France

    Xavier Leleu

  35. CHU ESTAING, Service d’hématologie clinique Adulte et pédiatrie, Clermont Ferrant, France

    Jacques-Olivier Bay

  36. CHU Nice - Hôpital de l’ARCHET I, Hematologie Clinique, Nice, France

    Pierre-Simon Rohrlich

  37. University Hospital Eppendorf, Bone Marrow Transplantation Centre, Hamburg, Germany

    Nicolaus Kröger

  38. CHU - Institut Universitaire du Cancer Toulouse, Oncopole, Toulouse, France

    Anne Huynh

  39. Klinikum Nuernberg, 5. Medizinische Klinik, BMT-Unit, Nuernberg, Germany

    Kerstin Schäfer-Eckart

  40. CHU Bordeaux, Hôpital Haut-leveque, Pessac, France

    Noel Milpied

  41. Skanes University Hospital, Dept. of Hematology, Lund, Sweden

    Stig Lenhoff

  42. Singapore General Hospital, 20 College Road, Singapore, Singapore

    Aloysius Ho

  43. Hospital Clinico Universitario, Servicio de Hematología, S de Compostela, Spain

    Jose Luis Bello López

  44. Az. Ospedaliera S. Croce e Carle, Division of Hematology, Cuneo, Italy

    Nicola Mordini

  45. Techniciens d’Etude Clinique suivi de patients greffes, Nouvel Hopital Civil, Strasbourg, France

    Bruno Lioure

  46. Institute of Hematology and Transfusion Medicine, I. Gandhi 14 str, Warsaw, Poland

    Kazimierz Halaburda

  47. Azienda Ospedali Riuniti di Ancona, Department of Hematology, Ancona University, Ancona, Italy

    Attilio Olivieri

  48. Oslo University Hospital, Rikshospitalet, Clinic for Cancer Medicine, Hematology Dept., Section for Stem Cell Transplantation, Oslo, Norway

    Tobias Gedde-Dahl

  49. Bristol Royal Hospital for Children, Dept, of Paediatric Oncology/BMT, Upper Maudlin Street, Bristol, UK

    Rachel Protheroe

  50. Klinikum Grosshadern, Med. Klinik III, Munich, Germany

    Johanna Tischer

  51. St. George’s Hospital, Department of Haematology, London, UK

    Matthias Klammer

  52. Elisabethinen-Hospital, I. Internal Department, Linz, Austria; Mathilde Hunault-Berger, CHRU, Service des Maladies du Sang, Angers, France

    Johannes Clausen

  53. Kings College Hospital, Dept, of Haematological Medicine, London, UK

    Victoria Potter

  54. H SS. Antonio e Biagio, Haematology Department, Alessandria, Italy

    Marco Ladetto

  55. Centre Henri Becquerel, Hematology, Rouen, France

    Herve Tilly

  56. Hopital Jean Minjoz, Service d’Hématologie, Besancon, France

    Eric Deconinck

  57. Deutsche Klinik fuer Diagnostik, KMT Zentrum, Wiesbaden, Germany

    Arne Brecht

  58. Martin-Luther-Universitaet Halle-Wittenberg, Klinik für Innere Medizin IV, Halle, Germany

    Lutz Peter Müller

  59. Universitaetsklinium Magdeburg, Med, Fakultät d., Klin.f.Hämatol./Onkologie, Magdeburg, Germany

    Thomas Heinicke

  60. Complejo Hospitalario de A Coruña, Hematologia, La Coruna, Spain

    Juan Pio Torres Carrete

  61. Department of Internal Medicine, American University of Beirut Medical Center, Beirut, Lebanon

    Ali Bazarbachi

  62. Dél-pesti Centrumkórház –, Országos Hematológiai és Infektológiai Intézet, Department of Haematology and Stem Cell Transplant, Budapest, Hungary

    Péter Reményi

  63. CHRU BRABOIS, Service Hématologie, Vandoeuvre Nancy, France

    Marie Thérèse Rubio

  64. Azienda Ospedaliero Universitaria di Udine, Division of Hematology, Udine, Italy

    Renato Fanin

  65. Hospital Universitario Virgen del Rocío, Servicio de Hematologia y Hemoterapia, Servicio Andaluz de Salud, Sevilla, Spain

    Jose Antonio Pérez-Simón

  66. University of Saarland, University Hospital, Department of Internal Med., BMT Unit, Homburg, Germany

    Murawski Niels

  67. Hospital Gregorio Marañón, Sección de Trasplante de Medula Osea, Madrid, Spain

    J. L. Diez-Martin

  68. Florence Nightingale Sisli Hospital, Hematopoietic SCT Unit, Istanbul, Turkey

    Mutlu Arat

  69. Hôpital Necker, Service Hematologie Adulte, Paris, France

    Olivier Hermine

  70. Hopital St. Louis, Dept. of Hematology-BMT, Paris, France

    Gerard Socié

  71. Erasmus MC Cancer Institute, University Medical Center Rotterdam, Department of Hematology, Rotterdam, The Netherlands

    Jan J. Cornelissen

  72. Ospedale Civile, Dipartimento Oncologico Ematologico, Pescara, Italy

    Stella Santarone

  73. Institut de Cancerologie Lucien Neuwirth, 108 B avenue Albert Raimond, Service d’Hematologie Clinique, Saint Etienne, France

    Denis Guyotat

  74. CHU Grenoble Alpes-Université Grenoble Alpes, Service d’Hématologie, Grenoble, France

    Claude Eric Bulabois

  75. BMT unit, Clinica Ematologica, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy

    Paolo Bernasconi

  76. Sahlgrenska University Hospital, Center for Hematopoietic Cell Transplantation, Hematology Section, Goeteborg, Sweden

    Jan-Erik Johansson

  77. University Hospital Center Rebro, Kispaticeva 12, Zagreb, Croatia

    Radovan Vrhovac

  78. Medical University Graz, LKH - University Hospital Graz, Division of Haematology, Graz, Austria

    Hildegard Greinix

  79. Fundación Jiménez Díaz, Hematología, Madrid, Spain

    José Luis López Lorenzo

  80. Sahyadri Speciality Hospital, Department of Haematology & BMT, Pune, India

    Shashikant Apte

  81. University Hospital Birmingham NHSTrust, Queen Elizabeth Medical Centre, Edgbaston, Dept. of Haematology, Birmingham, UK

    Charles Craddock

  82. Heinrich Heine Universitaet, Klinik für Hämat, Onkol, Klin. Immun, Duesseldorf, Germany

    Guido Kobbe

  83. King Abdul-Aziz Medical City, Riyadh, Saudi Arabia

    Mohsen Al Zahrani

  84. University of Heidelberg, Medizinische Klinik u. Poliklinik V, Heidelberg, Germany

    Peter Dreger

  85. DCTK, ul. Grabiszynska 105, Marrow Donor Registry, Wroclaw, Poland

    Andrzej Lange

  86. King Hussein Cancer Centre, Queen Rania Street - Aljubiha, Amman, Jordan

    Abdelghani Tbakhi

  87. VU University Medical Center, Department of Hematology (Br 250), Amsterdam, The Netherlands

    Ellen Meijer

  88. Hospital Universitario Donostia, Paseo Dr Beguiristain 107-116, San Sebastian, Spain

    Carlos Vallejo Llamas

  89. ICO-Hospital Universitari Germans Trias i Pujol, Cattedra e Servizio di Ematologia, Badalona, Spain

    Josep Maria Ribera Santasusana

  90. University of Milano, Istituto Nazionale dei Tumori, Hematology - Bone Marrow Transplantation Unit, Milano, Italy

    Paolo Corradini

  91. Policlinico G.B. Rossi, Divisione di Ematologia, Unità di TMO, Verona, Italy

    Fabio Benedetti

  92. ASST Papa Giovanni XXIII, Hematology and Bone Marrow Transplant Unit, Bergamo, Italy

    Alessandro Rambaldi

  93. Centre Hospitalier Universitaire de Rennes, Service d’Hematologie Clinique Adulte, Rennes, France

    Virginie Gandemer

  94. Hôpital Percy, Hematology Department, Clamart, France

    Jean-Valère Malfuson

  95. Tartu University Hospital, Clinic of Hematology and Oncology, Tartu, Estonia

    Ain Kaare

  96. University of Napoli, ‘Federico II‘ Medical School, Division of Hematology, Napoli, Italy

    Antonio Risitano

  97. Azienda Ospedaliero Universitaria Pisana, Unità Operativa Ematologia, Pisa, Italy

    Mario Petrini

  98. Medical School University of Salerno, AOU San Giovanni di Dio e Ruggi D´Aragona Hospital, Hematology and Hematopoietic SCT Center, Salerno, Italy

    Carmine Selleri

  99. First Affiliated Hospital of Soochow University, Department of Hematology, Suzhou, China

    Depei Wu

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  1. Sebastian Giebel
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  2. Myriam Labopin
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  3. Malgorzata Sobczyk-Kruszelnicka
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  4. Matthias Stelljes
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  5. Jenny L. Byrne
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  6. Nathalie Fegueux
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  7. Dietrich W. Beelen
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  8. Montserrat Rovira
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  9. Alexandros Spyridonidis
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  10. Didier Blaise
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  11. Martin Bornhäuser
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  13. Bipin N. Savani
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Consortia

Principal investigators of the contributing institutions

  • Sonja Martin
  • , Patrice Chevallier
  • , Andreas Neubauer
  • , Gandhi Damaj
  • , Yener Koc
  • , Arnold Ganser
  • , Matthew Collin
  • , Ibrahim Yakoub-Agha
  • , Hakan Ozdogu
  • , Mercedes Colorado Araujo
  • , Maija Itäla-Remes
  • , Kim Orchard
  • , Cecilia Isaksson
  • , Wolfgang Bethge
  • , Hans Martin
  • , Mahmoud Aljurf
  • , Edgar Faber
  • , Dolores Caballero
  • , Pavel Zák
  • , Xavier Leleu
  • , Jacques-Olivier Bay
  • , Pierre-Simon Rohrlich
  • , Nicolaus Kröger
  • , Anne Huynh
  • , Kerstin Schäfer-Eckart
  • , Noel Milpied
  • , Stig Lenhoff
  • , Aloysius Ho
  • , Jose Luis Bello López
  • , Nicola Mordini
  • , Bruno Lioure
  • , Kazimierz Halaburda
  • , Attilio Olivieri
  • , Tobias Gedde-Dahl
  • , Rachel Protheroe
  • , Johanna Tischer
  • , Matthias Klammer
  • , Johannes Clausen
  • , Victoria Potter
  • , Marco Ladetto
  • , Herve Tilly
  • , Eric Deconinck
  • , Arne Brecht
  • , Lutz Peter Müller
  • , Thomas Heinicke
  • , Juan Pio Torres Carrete
  • , Ali Bazarbachi
  • , Péter Reményi
  • , Marie Thérèse Rubio
  • , Renato Fanin
  • , Jose Antonio Pérez-Simón
  • , Murawski Niels
  • , J. L. Diez-Martin
  • , Mutlu Arat
  • , Olivier Hermine
  • , Gerard Socié
  • , Jan J. Cornelissen
  • , Stella Santarone
  • , Denis Guyotat
  • , Claude Eric Bulabois
  • , Paolo Bernasconi
  • , Jan-Erik Johansson
  • , Radovan Vrhovac
  • , Hildegard Greinix
  • , José Luis López Lorenzo
  • , Shashikant Apte
  • , Charles Craddock
  • , Guido Kobbe
  • , Mohsen Al Zahrani
  • , Peter Dreger
  • , Andrzej Lange
  • , Abdelghani Tbakhi
  • , Ellen Meijer
  • , Carlos Vallejo Llamas
  • , Josep Maria Ribera Santasusana
  • , Paolo Corradini
  • , Fabio Benedetti
  • , Alessandro Rambaldi
  • , Virginie Gandemer
  • , Jean-Valère Malfuson
  • , Ain Kaare
  • , Antonio Risitano
  • , Mario Petrini
  • , Carmine Selleri
  •  & Depei Wu

Corresponding author

Correspondence to Sebastian Giebel.

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The authors declare that they have no conflict of interest.

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Members of the contributing institutions are listed below Acknowledgements.

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Giebel, S., Labopin, M., Sobczyk-Kruszelnicka, M. et al. Total body irradiation + fludarabine compared to busulfan + fludarabine as “reduced-toxicity conditioning” for patients with acute myeloid leukemia treated with allogeneic hematopoietic cell transplantation in first complete remission: a study by the Acute Leukemia Working Party of the EBMT. Bone Marrow Transplant 56, 481–491 (2021). https://doi.org/10.1038/s41409-020-01050-7

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