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Outcomes of pediatric patients with therapy-related myeloid neoplasms

Bone Marrow Transplantation volume 56, pages 2997–3007 (2021)Cite this article

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Abstract

Long-term outcomes after allogeneic hematopoietic cell transplantation (HCT) for therapy-related myeloid neoplasms (tMNs) are dismal. There are few multicenter studies defining prognostic factors in pediatric patients with tMNs. We have accumulated the largest cohort of pediatric patients who have undergone HCT for a tMN to perform a multivariate analysis defining factors predictive of long-term survival. Sixty-eight percent of the 401 patients underwent HCT using a myeloablative conditioning (MAC) regimen, but there were no statistically significant differences in the overall survival (OS), event-free survival (EFS), or cumulative incidence of relapse and non-relapse mortality based on the conditioning intensity. Among the recipients of MAC regimens, 38.4% of deaths were from treatment-related causes, especially acute graft versus host disease (GVHD) and end-organ failure, as compared to only 20.9% of deaths in the reduced-intensity conditioning (RIC) cohort. Exposure to total body irradiation (TBI) during conditioning and experiencing grade III/IV acute GVHD was associated with worse OS. In addition, a diagnosis of therapy-related myelodysplastic syndrome and having a structurally complex karyotype at tMN diagnosis were associated with worse EFS. Reduced-toxicity (but not reduced-intensity) regimens might help to decrease relapse while limiting mortality associated with TBI-based HCT conditioning in pediatric patients with tMNs.

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Fig. 1: Outcomes following HCT for tMN.
Fig. 2: Multivariable analysis of risk factors associated with overall survival after HCT for tMN.
Fig. 3: Multivariable analysis of risk factors associated with event-free survival after HCT for tMN.
Fig. 4: Multivariable analysis of risk factors associated with relapse after HCT for tMN.
Fig. 5: Multivariable analysis of risk factors associated with non-relapse mortality after HCT for tMN.

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Acknowledgements

We would like to thank Keith A. Laycock, PhD, ELS for the scientific editing of the manuscript. We thank Dr. Stephen Gottschalk for helpful comments on the manuscript. We would like to thank our colleagues, advanced practice providers, nurses, data managers and other healthcare professional who participated in patient care and data collection. We also would like to thank the parents, who entrusted the care of our children to us. This work was supported by the American Society of Hematology (Scholar Award to AS) and the American Lebanese Syrian Associated Charities (ALSAC).

Author information

Authors and Affiliations

  1. Bone Marrow Transplantation and Cellular Therapy, St. Jude Children’s Research Hospital, Memphis, TN, USA

    Akshay Sharma, Ying Li & Brandon M. Triplett

  2. Biostatistics, St. Jude Children’s Research Hospital, Memphis, TN, USA

    Sujuan Huang, Russell J. Brooke & Cheng Cheng

  3. Pediatric Hematology, Oncology and BMT, Children’s Mercy Hospital Kansas City, Kansas City, MO, USA

    Ibrahim Ahmed & Mohamed Radhi

  4. Pediatric Hematology Oncology, AdventHealth for Children, Orlando, FL, USA

    Heather B. Allewelt

  5. Department of Bone Marrow Transplant, Great Ormond St Children’s Hospital, London, UK

    Persis Amrolia

  6. Hematology, Oncology, Stem Cell Transplantation and Regenerative Medicine, Department of Pediatrics, Stanford School of Medicine, Stanford, CA, USA

    Alice Bertaina

  7. Clinical Research Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA

    Neel S. Bhatt & Ann Dahlberg

  8. Stem cell transplantation, Princess Maxima Centre for Pediatric Oncology, Utrecht, Netherlands

    Marc B. Bierings & Birgitta Versluys

  9. Pediatrics, University of North Carolina, Chapel Hill, NC, USA

    Joshua Bies & Kimberly A. Kasow

  10. Hemato-immunology Department, Robert Debré Hospital, GHU APHP Nord—Université de Paris, Paris, France

    Claire Brisset, Jean-Hugues Dalle, Mony Fahd & Marie de Tersant

  11. Pediatric Transplant and Cellular Therapy, Duke University School of Medicine, Durham, NC, USA

    Jennifer E. Brondon, Erika S. Goeckerman & Paul L. Martin

  12. Blood and Marrow Transplant and Cellular Therapeutics, Center for Cancer and Blood Disorders, Children’s Hospital Colorado, Aurora, CO, USA

    Hesham Eissa

  13. Department of Haematology and Oncology, Royal Hospital for Children, Bristol, UK

    Adam Gassas

  14. Pediatrics, University of California San Diego, Rady Children’s Hospital San Diego, San Diego, CA, USA

    Nicholas J. Gloude & Colette R. Lauhan

  15. Pediatrics, Riley Hospital for Children at IU Health, Indiana University School of Medicine, Indianapolis, IN, USA

    W. Scott Goebel & Jodi L. Skiles

  16. Blood and Marrow Transplantation, Children’s National Hospital, Washington, DC, USA

    Katherine Harris & David Jacobsohn

  17. Pediatric Hematology, Oncology and BMT, Vanderbilt University Medical Center, Nashville, TN, USA

    Richard Ho & Saara Kaviany

  18. Pediatric Hematology and Oncology, Medical University of South Carolina, Charleston, SC, USA

    Michelle P. Hudspeth & Allison N. Uber

  19. Pediatric Cellular Therapies, Cancer and Blood Disorders, Atrium Health Levine Children’s Hospital, Charlotte, NC, USA

    Jeffrey S. Huo & Philip A. Roehrs

  20. Department of Pediatrics, University of Arizona, Tucson, AZ, USA

    Emmanuel Katsanis & Kristie Ramos

  21. Department of Pediatrics, University of Colorado School of Medicine, Aurora, CO, USA

    Amy K. Keating

  22. Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York City, NY, USA

    Nancy A. Kernan

  23. Pediatric Oncology, Sidney Kimmel Cancer Center, Johns Hopkins University, Baltimore, MD, USA

    Yiouli P. Ktena & Heather J. Symons

  24. Bone Marrow Transplant and Cell therapy Department, National Institute of Pediatrics, Ciudad de Mexico, Mexico

    Gerardo López-Hernandez & Alberto Olaya-Vargas

  25. Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    Kasiani C. Myers & Megan E. Sampson

  26. Division of Bone Marrow Transplantation and Immune Deficiency, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Kasiani C. Myers & Megan E. Sampson

  27. Center for Cell and Gene Therapy, Texas Children’s Hospital, Baylor College of Medicine, Houston, TX, USA

    Swati Naik & Toshihiro Onishi

  28. Oncology, Haematology, Blood and Marrow Transplantation, Child and Adolescent Health Services, Perth Children’s Hospital, Nedlands, WA, Australia

    Shanti Ramachandran

  29. Hematology, Oncology, Blood and Marrow Transplant, Nationwide Children’s Hospital, Columbus, OH, USA

    Hemalatha G. Rangarajan & Katherine Somers

  30. Children’s Hospital at Westmead, Westmead, NSW, Australia

    Peter J. Shaw

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  1. Akshay Sharma
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  54. Brandon M. Triplett
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Contributions

AS, SH, CC, and BMT designed the study. AS, YL, IA, HBA, PA, AB, NSB, MBB, JB, CB, JEB, AD, J-HD, HE, MF, AG, NJG, WSG, ESG, KH, RH, MPH, JSH, DJ, KAK, EK, SK, AKK, NAK, YPK, CRL, GL-H, PM, KCM, SN, AO-V, TO, MR, SR, KR, HGR, PAR, MES, PJS, JLS, KS, HJS, MdT, ANU, and BV acquired the data and verified it. AS, SH, RJB, CC, and BMT analyzed the data. AS and BMT wrote the manuscript, and YL, IA, HBA, PA, AB, NSB, MBB, JB, CB, JEB, AD, J-HD, HE, MF, AG, NJG, WSG, ESG, KH, RH, MPH, JSH, DJ, KAK, EK, SK, AKK, NAK, YPK, CRL, GL-H, PM, KCM, SN, AO-V, TO, MR, SR, KR, HGR, PAR, MES, PJS, JLS, KS, HJS, MdT, ANU, and BV critically reviewed the manuscript. All authors agree with and take full responsibility for the content of this manuscript.

Corresponding author

Correspondence to Akshay Sharma.

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Competing interests

AS’s institution receives support for the conduct of industry sponsored trials from Vertex Pharmaceuticals, CRISPR Therapeutics and Novartis. AS has received consulting fee from Spotlight Therapeutics and Medexus Inc, and honoraria from Vindico Medical Education. HBA reports that she is an employee of BeiGene Ltd and began her employment after the contribution of any clinical data. RJB reports that he currently is an employee of Smith & Nephew, a position that he transitioned to while this project was ongoing. J-HD reports receiving honoraria from blue bird bio, Orchard, Jazz Pharmaceuticals, Novartis, Sanofi Genzyme and Gilead. MPH serves on the advisory board for Mesoblast. NAK has equity interest in Amgen, Johnson and Johnson, Merck and Pfizer and has received financial support for research from Jazz Pharmaceuticals. HJS reports receiving honoraria from Jazz Pharmaceuticals and has a patent US-2020-0163997-A1 with royalties paid. BMT has received financial support for research and travel from Miltenyi Biotec. Remaining authors do not have any conflicts of interest to disclose.

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Sharma, A., Huang, S., Li, Y. et al. Outcomes of pediatric patients with therapy-related myeloid neoplasms. Bone Marrow Transplant 56, 2997–3007 (2021). https://doi.org/10.1038/s41409-021-01448-x

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