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Efficacy and safety of allogeneic hematopoietic cell transplantation in acute myeloid leukemia patients aged > 65 years with unfavorable cytogenetics

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Abstract

Unrelated donor bone marrow transplantation (UR-BMT), unrelated donor cord blood stem cell transplantation (UR-CBT), and haploidentical peripheral blood stem cell transplantation (Haplo-PBSCT) are the main alternative stem cell sources for allogeneic hematopoietic cell transplantation (HCT) in Japan. The present study aimed to identify factors associated with the outcomes of UR-BMT, UR-CBT, and Haplo-PBSCT in older patients with acute myeloid leukemia (AML) and intermediate- or poor-risk cytogenetics to improve the clinical efficacy and safety of allogeneic HCT. We retrospectively analyzed data for 448 AML patients aged > 65 years who received UR-BMT (n = 102), UR-CBT (n = 250), or Haplo-PBSCT (n = 96) between 2014 and 2020. Overall survival (OS) in the UR-BMT group was superior (P = 0.033) to that in the other groups. However, all patients without complete remission (non-CR) who had Karnofsky performance status (KPS) < 80 at HCT and poor-risk cytogenetics died within 1 year after HCT. Multivariate Cox regression analysis identified KPS <80 at HCT and poor-risk cytogenetics as independent predictors of worse OS in non-CR patients. KPS < 80 may be an alternative indicator for non-CR AML patients with poor-risk cytogenetics during the selection of HCT, alternative treatments, or best supportive therapy, and the optimal KPS is important for the success of HCT.

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Acknowledgements

We thank the patients and clinical staff for their participation in the study. We are grateful to the Japanese Data Center for Hematopoietic Cell Transplantation for data management. The article processing charges were funded by the authors. The work was supported by JSPS KAKENHI Grant Number 22K12887. We thank Alison Sherwin, PhD, from Edanz (https://jp.edanz.com/ac), for editing a draft of this manuscript. The authors also thank Takahiko Horiuchi (Kyushu University Beppu Hospital) for editorial support.

Funding

The study was supported by The Practical Research Project for Allergic Diseases and Immunology (Research Technology of Medical Transplantation) of the Japan Agency for Medical Research and Development (AMED).

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Kyushu University Beppu Hospital, 4546 Tsurumihara, Tsurumi, Beppu, Oita, 874-0838, Japan

    Satoshi Yamasaki

  2. Division of Hematology, Department of Internal Medicine, Aichi Medical University, Nagakute, Japan

    Shohei Mizuno

  3. Department of Hematology, Kyoto University Hospital, Kyoto, Japan

    Makoto Iwasaki & Junya Kanda

  4. Department of Hematology and Oncology, Dokkyo Medical University, Mibu, Japan

    Sachiko Seo

  5. Department of Hematology, Federation of National Public Service Personnel Mutual Aid Associations Toranomon Hospital, Tokyo, Japan

    Naoyuki Uchida

  6. Department of Hematology, Tokyo, Metropolitan Geriatric Hospital, Tokyo, Japan

    Miyakoshi Shigesaburo

  7. Department of Hematology, Imamura General Hospital, Kagoshima, Japan

    Nobuaki Nakano

  8. Department of Hematology, Federation of National Public Service Personnel Mutual Aid Associations, Toranomon Hospital, Kawasaki, Japan

    Kazuya Ishiwata

  9. Department of Hematology, Kitakyushu City Hospital Organization, Kitakyushu Municipal Medical Center, Kitakyushu, Japan

    Yasufumi Uehara

  10. Department of Hematology, Hamanomachi Hospital, Fukuoka, Japan

    Tetsuya Eto

  11. Department of Hematology, National Hospital Organization Kyusyu Medical Center, Fukuoka, Japan

    Ken Takase

  12. Department of Hematology, National Hospital Organization Kumamoto Medical Center, Kumamoto, Japan

    Toshiro Kawakita

  13. Department of Hematology, Kanagawa Cancer Center, Yokohama, Japan

    Masatsugu Tanaka

  14. Department of Hematology and Oncology, Anjo Kosei Hospital, Anjo, Japan

    Masashi Sawa

  15. Department of Hematology, Hiroshima Red Cross Hospital & Atomic-bomb Survivors Hospital, Hiroshima, Japan

    Yuta Katayama

  16. Department of Hematology, Ehime Prefectural Central Hospital, Matsuyama, Japan

    Yuichiro Nawa

  17. Department of Hematology and Oncology, Tokai University School of Medicine, Isehara, Japan

    Onizuka Makoto

  18. Department of Hematology, Research Institute for Radiation Biology and Medicine, Hiroshima University, Hiroshima, Japan

    Tatsuo Ichinohe

  19. Department of Registry Science for Transplant and Cellular Therapy, Aichi Medical University School of Medicine, Nagakute, Japan

    Yoshiko Atsuta

  20. Japanese Data Center for Hematopoietic Cell Transplantation, Nagoya, Japan

    Yoshiko Atsuta

  21. Department of Hematology and Cell Therapy, Aichi Cancer Center, Nagoya, Japan

    Masamitsu Yanada

Authors
  1. Satoshi Yamasaki
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  2. Shohei Mizuno
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  3. Makoto Iwasaki
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  4. Sachiko Seo
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  7. Nobuaki Nakano
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  9. Yasufumi Uehara
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  21. Masamitsu Yanada
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Contributions

S. Y. contributed to the study design, data analysis, and manuscript preparation. S. M., M. I., S. S., J. K., and M. Y. contributed to the manuscript preparation. N. U., MShigesaburo, N. N., K. I., Y. U., T. E., K. T., T. K., M. T., MSawa, Y. K., Y. N., and O. M. provided the clinical data. T. I. and Y. A. managed the clinical data. All authors reviewed the manuscript.

Corresponding author

Correspondence to Satoshi Yamasaki.

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Ethics statement

The study was approved by the Data Management Committee of the Japanese Society for Hematopoietic Cell Transplantation and the Institutional Review Board of Kyushu University Hospital.

Informed consent

The Transplant Registry Unified Management Program database contains physician-reviewed data. Observational studies based on the Transplant Registry Unified Management Program database are performed with informed consent.

Competing interests

The authors declare no competing interests.

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Supplementary information

ESM 1

Supplementary Figure 1. (A–C) Cumulative incidences of TRM (A) and Kaplan–Meier estimates of GRFS (B) and CRFS (C) in the AML patients with intermediate- or poor-risk cytogenetics who underwent UR-BMT, UR-CBT, or Haplo-PBSCT. TRM, transplant-related mortality; GVHD, graft-versus-host disease; GRFS, GVHD-free, relapse-free survival; CRFS, chronic GVHD-free, relapse-free survival; AML, acute myeloid leukemia; UR-BMT, unrelated donor bone marrow transplantation; UR-CBT, unrelated donor cord blood transplantation; Haplo-PBSCT, haploidentical peripheral blood stem cell transplantation; HCT, hematopoietic cell transplantation.

ESM 2

Supplementary Figure 2. (A–F) Cumulative incidences of TRM (A) and relapse (B) and Kaplan–Meier estimates of DFS (C), GRFS (D), CRFS (E), and OS (F) in the CR AML patients with intermediate- or poor-risk cytogenetics who underwent UR-BMT, UR-CBT, or Haplo-PBSCT. TRM, transplant-related mortality; DFS, disease-free survival; GVHD, graft-versus-host disease; GRFS, GVHD-free, relapse-free survival; CRFS, chronic GVHD-free, relapse-free survival; OS, overall survival; CR, complete remission; AML, acute myeloid leukemia; UR-BMT, unrelated donor bone marrow transplantation; UR-CBT, unrelated donor cord blood transplantation; Haplo-PBSCT, haploidentical peripheral blood stem cell transplantation; HCT, hematopoietic cell transplantation.

ESM 3

Supplementary Figure 3. (A–F) Cumulative incidences of TRM (A) and relapse (B) and Kaplan–Meier estimates of DFS (C), GRFS (D), CRFS (E), and OS (F) in the non-CR AML patients with intermediate- or poor-risk cytogenetics who underwent UR-BMT, UR-CBT, or Haplo-PBSCT. TRM, transplant-related mortality; DFS, disease-free survival; GVHD, graft-versus-host disease; GRFS, GVHD-free, relapse-free survival; CRFS, chronic GVHD-free, relapse-free survival; OS, overall survival; CR, complete remission; AML, acute myeloid leukemia; UR-BMT, unrelated donor bone marrow transplantation; UR-CBT, unrelated donor cord blood transplantation; Haplo-PBSCT, haploidentical peripheral blood stem cell transplantation; HCT, hematopoietic cell transplantation.

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Yamasaki, S., Mizuno, S., Iwasaki, M. et al. Efficacy and safety of allogeneic hematopoietic cell transplantation in acute myeloid leukemia patients aged > 65 years with unfavorable cytogenetics. Ann Hematol 102, 1549–1559 (2023). https://doi.org/10.1007/s00277-023-05243-0

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