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Allogeneic transplantation of bone marrow versus peripheral blood stem cells from HLA-identical relatives in patients with myelodysplastic syndromes and oligoblastic acute myeloid leukemia: a propensity score analysis of a nationwide database

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Abstract

Bone marrow (BM) and granulocyte colony-stimulating factor-mobilized peripheral blood stem cells (PBSC) are used as grafts from HLA-identical-related donors for adults with myelodysplastic syndrome (MDS). To assess the impact of graft sources on post-transplant outcomes in MDS patients, we conducted a retrospective analysis of a nationwide database. A total of 247 and 280 patients underwent transplantation with BM and PBSC, respectively. The inverse probability of treatment weighting (IPTW) methods revealed that overall survival (OS) was comparable between BM and PBSC (P = .129), but PBSC transplantation was associated with worse graft-versus-host disease (GVHD)-free/relapse-free survival (GRFS) (hazard rate [HR], 1.24; 95% confidence intervals [CIs], 1.00–1.53; P = 0.049) and chronic GVHD-free and relapse-free survival (CRFS) (HR, 1.29; 95% CIs, 1.13–1.73; P = 0.002) than BM transplantation. In the propensity score matched cohort (BM, n = 216; PBSC, n = 216), no significant differences were observed in OS and relapse; 3-year OS rates were 64.7% and 60.0% (P = 0.107), while 3-year relapse rates were 27.1% and 23.5% (P = 0.255) in BM and PBSC, respectively. Three-year GRFS rates (36.6% vs. 29.2%; P = 0.006), CRFS rate (37.7% vs. 32.5%; P = 0.003), and non-relapse mortality rates (13.9% vs. 21.1%; P = 0.020) were better in BM than in PBSC. The present study showed that BM transplantation provides a comparable survival benefit with PBSC transplantation and did not identify an enhanced graft-versus-MDS effect to reduce the incidence of relapse in PBSC transplantation.

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Acknowledgements

This work was supported in part by the Takeda Science Foundation.

The authors would like to thank all the physicians and data managers at the various institutes who contributed valuable data on transplantation to the Japanese Society for Transplantation and Cellular Therapy (JSTCT), all the members of the data management committees of JSTCT, and all the members of the “Adult Myelodysplastic Syndromes Working Group of the JSTCT.”

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Authors and Affiliations

  1. Department of Hematology, Nagasaki University Hospital, Nagasaki, Japan

    Hidehiro Itonaga & Yasushi Miyazaki

  2. Department of Hematology, Atomic Bomb Disease and Hibakusha Medicine Unit, Atomic Bomb Disease Institute, Nagasaki University, Nagasaki, Japan

    Yasushi Miyazaki

  3. Laboratory of Stem Cell Genetics, Institute for Life and Medical Sciences, Kyoto University, Kyoto, Japan

    Kazunari Aoki

  4. Hematology Division, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, Tokyo, Japan

    Naoki Shingai

  5. Department of Hematology, Japanese Red Cross Aichi Medical Center Nagoya Daiichi Hospital, Nagoya, Aichi, Japan

    Yukiyasu Ozawa

  6. Department of Hematopoietic Stem Cell Transplantation, National Cancer Center Hospital, Tokyo, Japan

    Takahiro Fukuda

  7. Division of Hematology, Department of Medicine, Keio University School of Medicine, Tokyo, Japan

    Keisuke Kataoka

  8. Division of Molecular Oncology, National Cancer Center Research Institute, Tokyo, Japan

    Keisuke Kataoka

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

    Toshiro Kawakita

  10. Department of Hematology/Oncology and Transfusion and Hemapheresis Center, Kurashiki Central Hospital, Okayama, Japan

    Yasunori Ueda

  11. Department of Hematology, Hokkaido University Hospital, Sapporo, Hokkaido, Japan

    Takahide Ara

  12. Department of Hematology, Kanagawa Cancer Center, Kanagawa, Japan

    Masatsugu Tanaka

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

    Yuta Katayama

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

    Masashi Sawa

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

    Tetsuya Eto

  16. Department of Hematology and Oncology, Graduate School of Medicine, Kyoto University, Kyoto, Japan

    Junya Kanda

  17. Japanese Data Center for Hematopoietic Cell Transplantation, Aichi, Japan

    Yoshiko Atsuta

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

    Yoshiko Atsuta

  19. Department of Hematology, Kanazawa University Hospital, Kanazawa, Japan

    Ken Ishiyama

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  1. Hidehiro Itonaga
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  2. Yasushi Miyazaki
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Contributions

H.I. and Y.M. designed the research, organized the project, analyzed the data, and wrote the manuscript. H.I., Y.M., and K.I. collected data from TRUMP. H.I., Y.M., K.A., N.S., Y.O., T.F., K.K., T.K., Y.U., T.A., M.T., Y.K., M.S., T.E., J.K., Y.A., and K.I. interpreted data and reviewed and approved the final manuscript.

Corresponding author

Correspondence to Hidehiro Itonaga.

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Figure S1. Transplant outcomes in the entire subset. (A) The 3-year probabilities of overall survival (OS) were 66.1% (95% CI, 59.6-71.8%) and 57.6% (95% CI, 51.4-63.2%) in the bone marrow (BM) and peripheral blood stem cell (PBSC) groups, respectively. (B) The 3-year probabilities of graft-versus-host disease (GVHD)-free and relapse-free survival (GRFS) were 38.3% (95% CI, 32.1-44.5%) and 28.4% (95% CI, 23.1-33.9%) in the BM and PBSC groups, respectively. (C) The 3-year probabilities of chronic GVHD-free and relapse-free survival (CRFS) were 40.5% (95% CI, 34.2-46.7%) and 31.2% (95% CI, 25.8-36.8%) in the BM and PBSC groups, respectively. (D) The 3-year cumulative incidences of relapse (CIR) were 23.7% (95% CI, 18.5-29.2%) and 24.7% (95% CI, 19.8-30.0%) in the BM and PBSC groups, respectively. (E) The 3-year non-relapse mortalities (NRM) were 15.2% (95% CI, 10.9-20.1%) and 22.2% (95% CI, 17.5-27.2%) in the BM and PBSC groups, respectively. Figure S2. Histogram of the propensity score distribution in the entire subset. Propensity score distributions represented a better overlap in the post-inverse probability of treatment weighting (IPTW) adjustment (left) than the pre-IPTW adjustment (right). Figure S3. Box-plot of the propensity score distribution in the PSM population. Propensity score distributions represented a better overlap in the post-propensity score matching (PSM) subset (left) than the pre-PSM subset (right). Figure S4. Transplant outcomes in the PSM population. The estimated cumulative incidence curves of neutrophil engraftment (A), platelet recovery (B), acute GVHD development (C), and chronic GVHD development (D). (A) The median times of neutrophil engraftment were days 17 and 14 in the BM and PBSC groups, respectively. The rate of neutrophil engraftment was 90.7% (95% CI, 86.0-93.9%) and 96.3% (95% CI, 92.7-98.1%) at day 28 after HSCT in BM and PBSC groups, respectively; and 95.4% (95% CI, 91.6-97.5%) and 96.3% (95% CI, 92.7-98.1%) at day 100 after HSCT in BM and PBSC groups, respectively. (B) The median times of platelet recovery were days 30 and 24 in the BM and PBSC groups, respectively. The rate of platelet recovery was 71.7% (95% CI, 65.2-77.3%) and 78.6% (95% CI, 72.5-83.5%) at day 45 after HSCT in BM and PBSC groups, respectively; and 78.2% (95% CI, 72.1-83.2%) and 82.7% (95% CI, 77.0-87.2%) at day 100 after HSCT in BM and PBSC groups, respectively. (C) The cumulative incidence of acute GVHD on day 100 were 49.3% (95% CI, 42.5-55.8%) and 58.9% (95% CI, 51.9-65.3%) in the BM and PBSC groups, respectively. (D) The cumulative incidence of chronic GVHD at 3 years were 41.5% (95% CI, 34.4-48.3%) and 55.8% (95% CI, 48.2-62.8%) in the BM and PBSC groups, respectively. Figure S5. A forest plot of transplant outcomes. Hazard ratios (HRs) from the subgroup analysis of NRM (A) and CIR (B) between BM and PBSC transplantation. HRs <1.00 indicate a better outcome after BM transplantation than after PBSC transplantation. (1.07 MB)

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Itonaga, H., Miyazaki, Y., Aoki, K. et al. Allogeneic transplantation of bone marrow versus peripheral blood stem cells from HLA-identical relatives in patients with myelodysplastic syndromes and oligoblastic acute myeloid leukemia: a propensity score analysis of a nationwide database. Ann Hematol 102, 1215–1227 (2023). https://doi.org/10.1007/s00277-023-05167-9

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