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International recommendations for screening and preventative practices for long-term survivors of transplantation and cellular therapy: a 2023 update

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Abstract

As hematopoietic cell transplantation (HCT) and cellular therapy expand to new indications and international access improves, the volume of HCT performed annually continues to rise. Parallel improvements in HCT techniques and supportive care entails more patients surviving long-term, creating further emphasis on survivorship needs. Survivors are at risk for developing late complications secondary to pre-, peri- and post-transplant exposures and other underlying risk-factors. Guidelines for screening and preventive practices for HCT survivors were originally published in 2006 and updated in 2012. To review contemporary literature and update the recommendations while considering the changing practice of HCT and cellular therapy, an international group of experts was again convened. This review provides updated pediatric and adult survivorship guidelines for HCT and cellular therapy. The contributory role of chronic graft-versus-host disease (cGVHD) to the development of late effects is discussed but cGVHD management is not covered in detail. These guidelines emphasize special needs of patients with distinct underlying HCT indications or comorbidities (e.g., hemoglobinopathies, older adults) but do not replace more detailed group, disease, or condition specific guidelines. Although these recommendations should be applicable to the vast majority of HCT recipients, resource constraints may limit their implementation in some settings.

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Fig. 1: International Societies Represented.

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Acknowledgements

We would like to thank the following individuals: Dr. Shigeru Kusumoto (Department of Hematology and Oncology, Nagoya City University Graduate School of Medical Sciences) for his expert review and commentary of management of Hepatitis B; Dr. Mehdi Hamadani (Medical College of Wisconsin), Ms. Jessica Scott (ASTCT), and Mr. Haedyn Smith for their work in reviewing the overall approach and coordinating with the ASTCT guidelines committee; Dr. Miguel-Angel Perales (Memorial Sloan Kettering Cancer Center), Dr. Corey Cutler (Dana Farber Cancer Center), Dr. David Porter (University of Pennsylvania), Dr. Brenda Sandmaier (Fred Hutchinson Cancer Center), Dr. Uday Popat (MD Anderson Cancer Center) for their work in reviewing the guidelines with the ASTCT Executive Committee.

Funding

Supported in part by a grant from NCATS (2KL2TR002547 to SJR.) Supported in part by a grant from NCI (R01CA215134 to KSB, NSM). The CIBMTR is supported primarily by Public Health Service U24CA076518 from the National Cancer Institute (NCI), the National Heart, Lung and Blood Institute (NHLBI) and the National Institute of Allergy and Infectious Diseases (NIAID); 75R60222C00011 from the Health Resources and Services Administration (HRSA); N00014-21-1-2954 and N00014-23-1-2057 from the Office of Naval Research; Support is also provided by Be the Match Foundation, the Medical College of Wisconsin, the National Marrow Donor Program, Gateway for Cancer Research, Pediatric Transplantation and Cellular Therapy Consortium and from the following commercial entities: AbbVie; Actinium Pharmaceuticals, Inc.; Adaptimmune; Adaptive Biotechnologies Corporation; ADC Therapeutics; Adienne SA; Allogene; Allovir, Inc.; Amgen, Inc.; Angiocrine; Anthem; Astellas Pharma US; Atara Biotherapeutics; BeiGene; bluebird bio, inc.; Bristol Myers Squibb Co.; CareDx Inc.; CRISPR; CSL Behring; CytoSen Therapeutics, Inc.; Elevance Health; Eurofins Viracor, DBA Eurofins Transplant Diagnostics; Gamida-Cell, Ltd.; GlaxoSmithKline; HistoGenetics; Incyte Corporation; Janssen Research & Development, LLC; Janssen/Johnson & Johnson; Jasper Therapeutics; Jazz Pharmaceuticals, Inc.; Karius; Kiadis Pharma; Kite, a Gilead Company; Kyowa Kirin; Legend Biotech; Magenta Therapeutics; Mallinckrodt Pharmaceuticals; Medexus Pharma; Merck & Co.; Mesoblast; Millennium, the Takeda Oncology Co.; Miltenyi Biotec, Inc.; MorphoSys; Novartis Pharmaceuticals Corporation; Omeros Corporation; Orca Biosystems, Inc.; Ossium Health, Inc.; Pfizer, Inc.; Pharmacyclics, LLC, An AbbVie Company; Pluristem; PPD Development, LP; Regimmune; Sanofi; Sanofi-Aventis U.S. Inc.; Sobi, Inc.; Stemcyte; Takeda Pharmaceuticals; Talaris Therapeutics; Vertex Pharmaceuticals; Vor Biopharma Inc.; Xenikos BV. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Author notes

  1. These authors contributed equally: Seth J. Rotz, Neel S. Bhatt.

Authors and Affiliations

  1. Division of Pediatric Hematology, Oncology, and Blood and Marrow Transplantation, Pediatric Institute, Cleveland Clinic Foundation, Cleveland, OH, USA

    Seth J. Rotz

  2. Blood and Marrow Transplant Program, Department of Hematology and Oncology, Taussig Cancer Institute, Cleveland Clinic Foundation, Cleveland, OH, USA

    Seth J. Rotz & Betty K. Hamilton

  3. Fred Hutchinson Cancer Center, Seattle, WA, USA

    Neel S. Bhatt, Paul A. Carpenter & K. Scott Baker

  4. Dana Farber/Boston Children’s Cancer and Blood Disorders Center, Harvard University, Boston, MA, USA

    Christine Duncan

  5. King Faisal Specialist Hospital & Research Center, Riyadh, Saudi Arabia

    Mahmoud Aljurf & Naeem Chaudhri

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

    Yoshiko Atsuta

  7. Japanese Data Center for Hematopoietic Cell Transplantation, Nagakute, Japan

    Yoshiko Atsuta

  8. Phoenix Children’s Hospital and Mayo Clinic Arizona, Phoenix, AZ, USA

    Kristen Beebe

  9. Division of Hematology, Children’s Hospital of Orange County, Orange, CA, USA

    David Buchbinder

  10. National Bone Marrow Transplant Link, Southfield, MI, USA

    Peggy Burkhard

  11. Hematology and BMT, University of Saskatchewan, Saskatoon, SK, Canada

    Mohamed Elemary

  12. Division of Hematology, Dalhousie University, Halifax, NS, Canada

    Mahmoud Elsawy

  13. QEII Health Sciences Center, Halifax, NS, Canada

    Mahmoud Elsawy

  14. Section of Pediatric Oncology/Transplant and Cellular Therapy, Alberta Children’s Hospital, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada

    Gregory M. T. Guilcher

  15. Department of Haematology, St Vincent’s Hospital Sydney, Sydney, NSW, Australia

    Nada Hamad

  16. St Vincent’s Clinical School Sydney, University of New South Wales, Sydney, NSW, Australia

    Nada Hamad

  17. School of Medicine Sydney, University of Notre Dame Australia, Sydney, WA, Australia

    Nada Hamad

  18. Bone Marrow Transplant Program, Clinica las Americas, Medellin, Colombia

    Amado Karduss

  19. BMT Unit, Department of Hematology, University Hospital Centre Zagreb and School of Medicine, University of Zagreb, Zagreb, Croatia

    Zinaida Peric

  20. Fiona Stanley Hospital, Murdoch, WA, Australia

    Duncan Purtill

  21. PathWest Laboratory Medicine, Nedlands, WA, Australia

    Duncan Purtill

  22. Medical College of Wisconsin, Milwaukee, WI, USA

    Douglas Rizzo

  23. Center for International Blood and Marrow Transplant Research, Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, USA

    Douglas Rizzo & Rachel Phelan

  24. Israelita Albert Einstein Hospital, São Paulo, Brazil

    Morgani Rodrigues

  25. Division of hematology and bone marrow transplantation, Instituto de trasplante y alta complejidad (ITAC), Buenos Aires, Argentina

    Maria Belén Rosales Ostriz

  26. Centre for Haematology, Imperial College London, London, UK

    Nina Salooja

  27. Department of Hematology, University Hospitals Leuven, Leuven, Belgium

    Helene Schoemans

  28. Department of Public Health and Primary Care, ACCENT VV, KU Leuven—University of Leuven, Leuven, Belgium

    Helene Schoemans

  29. Hospital Samaritano, Sao Paulo, Brazil

    Adriana Seber

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

    Akshay Sharma

  31. Department of Haematology, Christian Medical College, Vellore, India

    Alok Srivastava

  32. Blood & Marrow Transplant Information Network, Highland Park, IL, 60035, USA

    Susan K. Stewart

  33. Sarah Cannon Transplant and Cellular Therapy Network, Nashville, TN, USA

    Navneet S. Majhail

  34. Division of Pediatric Hematology/Oncology/Blood and Marrow Transplant, Department of Pediatrics, Medical College of Wisconsin, Milwaukee, WI, USA

    Rachel Phelan

Authors
  1. Seth J. Rotz
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  2. Neel S. Bhatt
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  3. Betty K. Hamilton
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  4. Christine Duncan
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  5. Mahmoud Aljurf
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  6. Yoshiko Atsuta
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  7. Kristen Beebe
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  8. David Buchbinder
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  9. Peggy Burkhard
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  10. Paul A. Carpenter
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  11. Naeem Chaudhri
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  12. Mohamed Elemary
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  13. Mahmoud Elsawy
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  14. Gregory M. T. Guilcher
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  15. Nada Hamad
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  16. Amado Karduss
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  17. Zinaida Peric
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  18. Duncan Purtill
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  19. Douglas Rizzo
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  20. Morgani Rodrigues
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  21. Maria Belén Rosales Ostriz
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  22. Nina Salooja
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  23. Helene Schoemans
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  24. Adriana Seber
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  25. Akshay Sharma
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  26. Alok Srivastava
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  27. Susan K. Stewart
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  28. K. Scott Baker
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  29. Navneet S. Majhail
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  30. Rachel Phelan
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Contributions

SJR and NSB contributed equally to this work and should be listed as co-first authors; SJR and NSM- conceived of the project, SJR, NSB, BKH, CD, NSM, RP, KSB served as steering committee to guide the project, SJR, NSB, BKH, CD, MJ, YA, KB, DB, NC, ME, ME, GMTG, NH, AK, ZP, DP, DR, MR, MBRO, NS, HS, AS, AS, AS, RP drafted initial sections, SJR, NSB, RP wrote the first draft of the manuscript, all co-authors voted on recommendations, commented on manuscript, and approved final version of manuscript.

Corresponding author

Correspondence to Seth J. Rotz.

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Competing interests

The authors report no conflicts of interest relevant to this work. The authors report the following financial relationships. YA: Lecture fee: Otsuka Pharmaceutical Co., Ltd; CHUGAI PHARMACEUTICAL CO., LTD.; Novartis Pharma KK; AbbVie GK; Honorarium: Meiji Seika Pharma Co, Ltd.; Consultant fee: JCR Pharmaceuticals Co., Ltd.; Kyowa Kirin Co., Ltd. GG: Principal Investigator of Project Sickle Cure, a Sickle Cell Transplant Advocacy and Research Alliance Study partially funded by bluebirdbio. I serve on the steering committee of a STAR clinical trial for which Bristol Myers Squibb has provided funding. NM: Consultant for Anthem, Inc; Stock in HCA Healthcare. Rachel Phelan: Bluebirdbio: advisory board. Amgen: research funding. SR: Medical Monitor for Resource for Clinical Investigation in Blood and Marrow Transplantation (RCI BMT). HS: personal fees: Incyte, Janssen, Novartis, Sanofi and from the Belgian Hematological Society (BHS); research grants from Novartis and the BHS. non-financial support from Gilead, Pfizer, the EBMT (European Society for Blood and Marrow transplantation) and the CIBMTR (Center for International Bone Marrow Transplantation Research). AS: consultant fee from Spotlight Therapeutics, Medexus Inc., Vertex Pharmaceuticals, Sangamo Therapeutics and Editas Medicine. Medical Monitor for Resource for Clinical Investigation in Blood and Marrow Transplantation (RCI BMT). Research funding from CRISPR Therapeutics and honoraria from Vindico Medical Education. AS is the St. Jude Children’s Research Hospital site principal investigator of clinical trials for genome editing of sickle cell disease sponsored by Vertex Pharmaceuticals/CRISPR Therapeutics (NCT03745287), Novartis Pharmaceuticals (NCT04443907) and Beam Therapeutics (NCT05456880). The industry sponsors provide funding for the clinical trial, which includes salary support paid to Dr Sharma’s institution.

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This article is co-published in the journals Bone Marrow Transplantation and Transplantation and Cellular Therapy https://doi.org/10.1038/s41409-023-02190-2 and https://doi.org/10.1016/j.jtct.2023.12.001

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Rotz, S.J., Bhatt, N.S., Hamilton, B.K. et al. International recommendations for screening and preventative practices for long-term survivors of transplantation and cellular therapy: a 2023 update. Bone Marrow Transplant (2024). https://doi.org/10.1038/s41409-023-02190-2

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  • DOI: https://doi.org/10.1038/s41409-023-02190-2

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