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Male-specific late effects in adult hematopoietic cell transplantation recipients: a systematic review from the Late Effects and Quality of Life Working Committee of the Center for International Blood and Marrow Transplant Research and Transplant Complications Working Party of the European Society of Blood and Marrow Transplantation

Bone Marrow Transplantation volume 57, pages 1150–1163 (2022)Cite this article

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Abstract

Male-specific late effects after hematopoietic cell transplantation (HCT) include genital chronic graft-versus-host disease (GvHD), hypogonadism, sexual dysfunction, infertility, and subsequent malignancies. They may be closely intertwined and cause prolonged morbidity and decreased quality of life after HCT. We provide a systematic review of male-specific late effects in a collaboration between transplant physicians, endocrinologists, urologists, dermatologists, and sexual health professionals through the Late Effects and Quality of Life Working Committee of the Center for International Blood and Marrow Transplant Research, and the Transplant Complications Working Party of the European Society of Blood and Marrow Transplantation. The systematic review summarizes incidence, risk factors, screening, prevention and treatment of these complications and provides consensus evidence-based recommendations for clinical practice and future research.

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Fig. 1: PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses) flowcharts for the five different subgroup analysis.
Fig. 2: From Müller et al. 2013 [27].

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Acknowledgements

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); HHSH250201700006C from the Health Resources and Services Administration (HRSA); and N00014-20-1-2705 and N00014-20-1-2832 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, and from the following commercial entities: AbbVie; Accenture; Actinium Pharmaceuticals, Inc.; Adaptive Biotechnologies Corporation; Adienne SA; Allovir, Inc.; Amgen, Inc.; Astellas Pharma US; bluebird bio, inc.; Bristol Myers Squibb Co.; CareDx; CSL Behring; CytoSen Therapeutics, Inc.; Daiichi SankyoCo., Ltd; Eurofins Viracor; ExcellThera; Fate Therapeutics; Gamida-Cell, Ltd; Genentech Inc; Gilead; GlaxoSmithKline; Incyte Corporation; Janssen/Johnson & Johnson; Jasper Therapeutics; Jazz Pharmaceuticals, Inc.; Karyopharm Therapeutics; Kiadis Pharma; Kite, a Gilead Company; Kyowa Kirin; Magenta Therapeutics; Medac GmbH; Merck & Co.; Millennium, the Takeda Oncology Co.; Miltenyi Biotec, Inc.; MorphoSys; Novartis Pharmaceuticals Corporation; Omeros Corporation; Oncopeptides, Inc.; Orca Biosystems, Inc.; Pfizer, Inc.; Pharmacyclics, LLC; Sanofi Genzyme; Seagen, Inc.; Stemcyte; Takeda Pharmaceuticals; Tscan; Vertex; Vor Biopharma; Xenikos BV.

Author information

Author notes

  1. These authors contributed equally: Rachel Phelan, Annie Im, Hélène Schoemans and André Tichelli

Authors and Affiliations

  1. CIBMTR® (Center for International Blood and Marrow Transplant Research), Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, USA

    Rachel Phelan & Linda Burns

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

    Rachel Phelan

  3. University of Pittsburgh/UPMC Hillman Cancer Center, Pittsburgh, PA, USA

    Annie Im

  4. Division of Hematology, University of Colorado Anschutz Medical Center, Aurora, CO, USA

    Rebecca L. Hunter

  5. Division of Hematopoietic Stem Cell Transplantation, National Cancer Center Hospital, Tokyo, Japan

    Yoshihiro Inamoto

  6. Hematology and Bone Marrow Transplantation Unit, IRCC San Raffaele Scientific Institute, Milano, Italy

    Maria Teresa Lupo-Stanghellini

  7. Department of Hematology and Central Hematology Laboratory, Inselspital Bern University Hospital, University of Bern, Bern, Switzerland

    Alicia Rovo

  8. Division of Hematology, Oncology and Stem Cell Transplant, Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL, USA

    Sherif M. Badawy

  9. Department of Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

    Sherif M. Badawy

  10. Department of Pediatrics, Center for Cancer and Blood Disorders, University of Colorado School of Medicine, Aurora, CO, USA

    Hesham Eissa

  11. Division of Hematology-Oncology, Blood and Marrow Transplantation Program, Mayo Clinic, Jacksonville, FL, USA

    Hemant S. Murthy

  12. Louisiana State University Health Sciences Center/Children’s Hospital of New Orleans, Department of Pediatrics, New Orleans, LA, USA

    Pinki Prasad

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

    Akshay Sharma

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

    Elizabeth Suelzer

  15. Division of Leukemia, Department of Hematology & Hematopoietic Cell Transplantation, City of Hope National Medical Center, Duarte, CA, USA

    Vaibhav Agrawal

  16. Department of Oncology, King Faisal Specialist Hospital Center & Research, Riyadh, Saudi Arabia

    Mahmoud Aljurf

  17. Duke University Medical Center, Durham, NC, USA

    Karen Baker

  18. University Clinical Centre, Medical University of Warsaw, Warsaw, Poland

    Grzegorz W. Basak

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

    David Buchbinder

  20. Hematopoietic Cell Transplant and Cellular Therapy Program, Massachusetts General Hospital, Boston, MA, USA

    Zachariah DeFilipp

  21. University Hospital Centre Zagreb, Zagreb, Croatia

    Lana Desnica Grkovic

  22. Beth Israel Deaconess Medical Center, Boston, MA, USA

    Ajoy Dias

  23. Universitätsklinikum Würzburg, Department of Internal Medicine II, Würzburg, Germany

    Hermann Einsele

  24. Department of Urology, Stanford University School of Medicine, Stanford, CA, USA

    Michael L. Eisenberg

  25. Division of Hematology, Department of Medicine, The James Cancer Hospital and Solove Research Institute, The Ohio State University, Columbus, Ohio, USA

    Narendranath Epperla

  26. Division of Hematology/Oncology, University of Florida College of Medicine, Gainesville, FL, USA

    Nosha Farhadfar

  27. Association of Cancer Online Resources, Association of Cancer Online Resources, Austin, TX, USA

    Arthur Flatau

  28. Haematology Research Centre, Department of Immunology and Inflammation, Imperial College London, London, UK

    Robert Peter Gale

  29. Medical University Graz, Division of Hematology, Graz, Austria

    Hildegard Greinix

  30. Blood & Marrow Transplant Program, Cleveland Clinic Taussig Cancer Institute, Cleveland, OH, USA

    Betty K. Hamilton

  31. Department of Internal Medicine, Mayo Clinic, Rochester, MN, USA

    Shahrukh Hashmi

  32. Department of Medicine, Sheikh Shakhbout Medical City, Abu Dhabi, UAE

    Shahrukh Hashmi

  33. Division of Hematology/Oncology/Bone Marrow Transplantation, Department of Medicine, University of Wisconsin, Madison, WI, USA

    Peiman Hematti

  34. Tom Baker Cancer Centre, University of Calgary, Calgary, AB, Canada

    Kareem Jamani

  35. South Florida Bone Marrow Stem Cell Transplant Institute, Boynton Beach, FL, USA

    Dipnarine Maharaj

  36. The Christie NHS Foundation Trust, Manchester, UK

    John Murray

  37. Division Hematology and Oncology, Department of Medicine, Penn State Cancer Institute, Milton Hershey Medical Center, Hershey, PA, USA

    Seema Naik

  38. Section of Bone Marrow Transplant and Cell Therapy, Rush University Medical Center, Chicago, IL, USA

    Sunita Nathan

  39. Immune Deficiency Cellular Therapy Program, Center for Cancer Research, National Cancer Institute, Bethesda, MD, USA

    Steven Pavletic

  40. University Hospital Centre Zagreb and Medical School University of Zagreb, Zagreb, Croatia

    Zinaida Peric & Drazen Pulanic

  41. The University of Sheffield, Sheffield, UK

    Richard Ross & John A. Snowden

  42. University Vita-Salute San Raffaele, Milan, Italy

    Andrea Salonia

  43. Division of Experimental Oncology/Unit of Urology; URI; IRCCS Ospedale San Raffaele, Milan, Italy

    Andrea Salonia

  44. Institut Catala d’Oncologia, Barcelona, Spain

    Isabel Sanchez-Ortega

  45. Division of Hematology/Oncology, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA

    Bipin N. Savani

  46. Division of Pediatric Hematology/Oncology, The Hospital for Sick Children, University of Toronto, Toronto, ON, Canada

    Tal Schechter

  47. Division of Hematology/ Oncology/ Stem Cell Transplantation and Regenerative Medicine, Lucile Packard Children’s Hospital, Stanford School of Medicine, Palo Alto, CA, USA

    Ami J. Shah

  48. Division of Hematology/Oncology, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA, USA

    Stephanie M. Smith

  49. Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield, UK

    John A. Snowden

  50. Westchester Medical Center, Valhalla, NY, USA

    Amir Steinberg

  51. Division of Hematology/Oncology, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Douglas Tremblay

  52. Department of Urology, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, OH, USA

    Sarah C. Vij

  53. Department of Oncology, Tom Baker Cancer Centre, Calgary, AB, Canada

    Lauren Walker

  54. Department of Internal Medicine III, University Hospital Regensburg, Regensburg, Germany

    Daniel Wolff

  55. Blood & Marrow Transplantation Program, Division of Hematology/Oncology, Department of Medicine, Greenebaum Comprehensive Cancer Center, University of Maryland, Baltimore, MD, USA

    Jean A. Yared

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

    Hélène Schoemans

  57. Department of Public Health and Primary Care, ACCENT VV, KU Leuven – University of Leuven, Leuven, Belgium

    Hélène Schoemans

  58. University Hospital Basel, Basel, Switzerland

    André Tichelli

Authors
  1. Rachel Phelan
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  2. Annie Im
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  3. Rebecca L. Hunter
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  4. Yoshihiro Inamoto
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  55. André Tichelli
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Contributions

RP and HS. designed and directed the study plan and contributed to manuscript writing and revision. AT, AI, and RLH served as study co-leaders and contributed to manuscript writing and revision. YI, DB, MTL-S, SP, AR, and LB served as section subgroup leaders and contributed to manuscript writing and revision; ES performed the literature search and contributed to manuscript writing and revision. SMB, HE, HSM, PP, AS, MA, KB, GWB, ZD, LDG, AD, HE, MLE, NF, AF, RPG, HG, BKH, SH, PH, KJ, DM, JM, SN, SN, SP, ZP, DP, RR, Amir S, ISO, BNS, JAS, Akshay S, DT, SCV, LW, DW, JAY, VA, NE, AJS, and SMS contributed to manuscript writing and revision. All authors critically reviewed the data and approved the final manuscript before it was submitted.

Corresponding author

Correspondence to Rachel Phelan.

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Competing interests

HE reports grants and other from BMS/Celgene, grants and other from Janssen, grants and other from Amgen, other from Takeda, grants and other from Sanofi, grants and other from GSK, during the conduct of the study. SH reports other from Pfizer, other from Novartis, other from Therakos, other from Janssen, other from MSD, outside the submitted work. YI reports personal fees from Novartis, personal fees from Janssen, personal fees from Meiji Seika Pharma, outside the submitted work. RP reports research funding from Amgen. RR reports other from Diurnal Plc, during the conduct of the study. HS reports participation in advisory boards for Janssen & Novartis; speaker’s fees from Incyte, Jazz Pharmaceuticals, Takeda, Novartis and the BHS (Belgian Hematological Society); travel grants from EBMT, CIBMTR, Incyte & Gilead and research funding from Novartis & the BHS, outside of the submitted work. AR reports grants from Novartis, grants from CSL Behring, grants from Alexion, personal fees from Novartis, personal fees from BMS, personal fees from OrPha Swiss GmbH, other from Amgen, other from AstraZeneca, other from Sanofi, other from Celgene, outside the submitted work. ASharma reports clinical trial salary support from Vertex Pharmaceuticals, CRISPR Therapeutics, Novartis paid to his institution, and personal consultancy fees from Spotlight Therapeutics, outside the submitted work. JAS reports personal fees from MEDAC, personal fees from KIADIS, personal fees from GILEAD, personal fees from JANSSEN, personal fees from MALLINCKRODT, personal fees from JAZZ, personal fees from ACTELION, outside the submitted work. DW reports grants and personal fees from Novartis, personal fees from Mallinckrodt, personal fees from Behring, outside the submitted work. PG is a consultant to Ascenage Pharma, BeiGene Ltd, Kite Pharma Inc., Fusion Pharma LLC, LaJolla NanoMedical Inc., Mingsight Parmaceuticals Inc. and CStone Pharmaceuticals; Medical Director, FFF Enterprises Inc.; Partner, AZCA Inc.; Board of Directors, RakFond Foundation for Cancer Research Support; Scientific Advisory Board, Antegene Biotech LLC and StemRad Ltd.

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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/s41409-022-01591-z and https://doi.org/10.1016/j.jtct.2021.10.013

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Phelan, R., Im, A., Hunter, R.L. et al. Male-specific late effects in adult hematopoietic cell transplantation recipients: a systematic review from the Late Effects and Quality of Life Working Committee of the Center for International Blood and Marrow Transplant Research and Transplant Complications Working Party of the European Society of Blood and Marrow Transplantation. Bone Marrow Transplant 57, 1150–1163 (2022). https://doi.org/10.1038/s41409-022-01591-z

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