Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

Subjects

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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].

Data availability

CIBMTR supports accessibility of research in accord with the National Institutes of Health (NIH) Data Sharing Policy and the National Cancer Institute (NCI) Cancer Moonshot Public Access and Data Sharing Policy. The CIBMTR only releases de-identified datasets that comply with all relevant global regulations regarding privacy and confidentiality.

References

  1. Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med. 2006;354:1813–26. https://doi.org/10.1056/NEJMra052638.

    Article  CAS  PubMed  Google Scholar 

  2. Singh AK, McGuirk JP. Allogeneic stem cell transplantation: a historical and scientific overview. Cancer Res. 2016;76:6445–51. https://doi.org/10.1158/0008-5472.CAN-16-1311.

    Article  CAS  PubMed  Google Scholar 

  3. Bhatia S, Armenian SH, Landier W. How I monitor long-term and late effects after blood or marrow transplantation. Blood. 2017;130:1302–14. https://doi.org/10.1182/blood-2017-03-725671

    Article  CAS  PubMed  Google Scholar 

  4. Inamoto Y, Lee SJ. Late effects of blood and marrow transplantation. Haematologica. 2017;102:614–25. https://doi.org/10.3324/haematol.2016.150250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Tichelli A, Rovo A, Passweg J, Schwarze CP, Van Lint MT, Arat M, et al. Late complications after hematopoietic stem cell transplantation. Expert Rev Hematol. 2009;2:583–601. https://doi.org/10.1586/ehm.09.48

    Article  PubMed  Google Scholar 

  6. Hamilton BK, Goje O, Savani BN, Majhail NS, Stratton P. Clinical management of genital chronic GvHD. Bone Marrow Transpl. 2017;52:803–10. https://doi.org/10.1038/bmt.2016.315

    Article  CAS  Google Scholar 

  7. Murphy J, McKenna M, Abdelazim S, Battiwalla M, Stratton P. A practical guide to gynecologic and reproductive health in women undergoing hematopoietic stem cell transplant. Blood Marrow Transplant. 2019;25:e331–e343. https://doi.org/10.1016/j.bbmt.2019.07.038.

    Article  CAS  Google Scholar 

  8. Stratton P. Gynecologic care after hematopoietic cell transplantation: a call to action to include 646 gynecologists in the transplant team. Bone Marrow Transplant. 2015;50:1–2. https://doi.org/10.1038/bmt.2014.247.

    Article  CAS  PubMed  Google Scholar 

  9. Chow EJ, Anderson L, Baker KS, Bhatia S, Guilcher GM, Huang JT, et al. Late effects surveillance recommendations among survivors of childhood hematopoietic cell transplantation: a Children’s Oncology Group Report. Biol Blood Marrow Transplant. 2016;22:782–95. https://doi.org/10.1016/j.bbmt.2016.01.023.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Sharma A, Badawy S, Suelzer E, Eissa H, Murthy H, Prasad P, et al. Male-specific late effects after hematopoietic cell transplantation. In: PROSPERO 2020 CRD42020147640; 2020.

  11. Sharma A, Badawy S, Suelzer E, Murphy E, Prasad P, Eissa H, et al. Systematic reviews in hematopoietic cell transplantation and cellular therapy: considerations and guidance from the American Society for Transplantation and Cellular Therapy, European Society for Blood and Marrow Transplantation, and Center for International Blood and Marrow Transplant Research Late Effects and Quality of Life Working Committee. Transplant Cell Ther. 2021;27:380–8. https://doi.org/10.1016/j.jtct.2020.12.002.

  12. Sharma A, Badawy SM, Suelzer EM, Murthy HS, Prasad P, Eissa H, et al. Systematic reviews in hematopoietic cell transplantation and cellular therapy: considerations and guidance from the American Society for Transplantation and Cellular Therapy, European Society for Blood and Marrow Transplantation, and the Center for International Blood and Marrow Transplant Research late effects and quality of life working committee. Bone Marrow Transplant 2022. https://doi.org/10.1038/s41409-020-01199-1.

  13. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336:924–6. https://doi.org/10.1136/bmj.39489.470347.AD.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4:1 https://doi.org/10.1186/2046-4053-4-1.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Au WY, Yeung CK, Cheung MC, Trendell-Smith NJ. Penile lichen sclerosus after allogeneic stem cell transplantation. Br J Dermatol. 2008;159:470–2. https://doi.org/10.1111/j.1365-2133.2008.08645.x

    Article  PubMed  Google Scholar 

  16. Grigg AP, Underhill C, Russell J, Sale G. Peyronie’s disease as a complication of chronic graft versus host disease. Hematology. 2002;7:165–8. https://doi.org/10.1080/1024533021000008182.

    Article  CAS  PubMed  Google Scholar 

  17. Jain NA, Venkatesan K, Anandi P, Ito S, Kumar D, Lu K, et al. A rare consequence of chronic graft versus host disease-Peyronie’s disease. Arch Cancer Res. 2015;3:18. https://doi.org/10.21767/2254-6081.100018.

  18. Kami M, Kanda Y, Sasaki M, Takeda N, Tanaka Y, Saito T, et al. Phimosis as a manifestation of chronic graft-versus-host disease after allogeneic bone marrow transplantation. Bone Marrow Transplant. 1998;21:721–3. https://doi.org/10.1038/sj.bmt.1701159.

    Article  CAS  PubMed  Google Scholar 

  19. Lara LA, De Andrade JM, Mauad LM, Ferrarese SR, Marana HR, Tiezzi DG, et al. Genital manifestation of graft-vs.-host disease: a series of case reports. J Sex Med. 2010;7:3216–25. https://doi.org/10.1111/j.1743-6109.2010.01885.x.

    Article  PubMed  Google Scholar 

  20. Nylander E, Wahlin YB, Lundskog B, Wahlin A. Genital graft-versus-host disease in a male following allogeneic stem cell transplantation. Acta Derm Venereol. 2007;87:367–8. https://doi.org/10.2340/00015555-0226.

    Article  PubMed  Google Scholar 

  21. Odorici G, Baraldi C, Loi C, Bardazzi F. Chronic graft-versus-host disease of the male genitalia: an underrecognized manifestation. J Dtsch Dermatol Ges. 2017;15:746–8. https://doi.org/10.1111/ddg.13281.

    Article  PubMed  Google Scholar 

  22. Tauchmanova L, Alviggi C, Foresta C, Strina I, Garolla A, Colao A, et al. Cryptozoospermia with normal testicular function after allogeneic stem cell transplantation: a case report. Hum Reprod. 2007;22:495–9. https://doi.org/10.1093/humrep/del376.

    Article  CAS  PubMed  Google Scholar 

  23. Thomas LJ, Shim TN, Borysiewicz C, Dinneen M, Fawcett H, Roy A, et al. Male genital lichen sclerosus in recipients of bone marrow transplants. Clin Exp Dermatol. 2016;41:495–7. https://doi.org/10.1111/ced.12812

    Article  CAS  PubMed  Google Scholar 

  24. Yared J, Gojo I, Akpek G. Glans penis involvement: an under-recognized manifestation of chronic GVHD. Bone Marrow Transpl. 2012;47:1006–7. https://doi.org/10.1038/bmt.2011.209.

    Article  CAS  Google Scholar 

  25. Andreini A, Zampieri N, Costantini C, Malerba G, Bruno C, Salvagno G, et al. Chronic graft versus host disease is associated with erectile dysfunction in allogeneic hematopoietic stem cell transplant patients: a single-center experience. Leuk Lymphoma. 2018;59:2719–22. https://doi.org/10.1080/10428194.2018.1443338.

    Article  CAS  PubMed  Google Scholar 

  26. Dyer G, Gilroy N, Bradford J, Brice L, Kabir M, Greenwood M, et al. A survey of fertility and sexual health following allogeneic haematopoietic stem cell transplantation in New South Wales, Australia. Br J Haematol. 2016;172:592–601. https://doi.org/10.1111/bjh.13872.

    Article  PubMed  Google Scholar 

  27. Mueller SM, Haeusermann P, Rovo A, Halter JP, Passweg J, Itin P, et al. Genital chronic GVHD in men after hematopoietic stem cell transplantation: a single-center cross-sectional analysis of 155 patients. Biol Blood Marrow Transplant. 2013;19:1574–80. https://doi.org/10.1016/j.bbmt.2013.07.010

    Article  PubMed  Google Scholar 

  28. Wong FL, Francisco L, Togawa K, Kim H, Bosworth A, Atencio L, et al. Longitudinal trajectory of sexual functioning after hematopoietic cell transplantation: impact of chronic graft-versus-host disease and total body irradiation. Blood. 2013;122:3973–81. https://doi.org/10.1182/blood-2013-05-499806.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jagasia MH, Greinix HT, Arora M, Williams KM, Wolff D, Cowen EW, et al. National institutes of health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. The 2014 Diagnosis and Staging Working Group Report. Biol Blood Marrow Transplant. 2015;21:389–401. https://doi.org/10.1016/j.bbmt.2014.12.001

    Article  PubMed  Google Scholar 

  30. Eeltink CM, Witte BI, Stringer J, Liptrott S, Babic A, Greenfield DM, et al. Health-care professionals’ perspective on discussing sexual issues in adult patients after haematopoietic cell transplantation. Bone Marrow Transpl. 2018;53:235–45. https://doi.org/10.1038/s41409-017-0027-y.

    Article  Google Scholar 

  31. Majhail NS, Rizzo JD, Lee SJ, Aljurf M, Atsuta Y, Bonfim C, et al. Recommended screening and preventive practices for long-term survivors after hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2012;18:348–71. https://doi.org/10.1016/j.bbmt.2011.12.519

    Article  PubMed  Google Scholar 

  32. Greenfield DM, Walters SJ, Coleman RE, Hancock BW, Eastell R, Davies HA, et al. Prevalence and consequences of androgen deficiency in young male cancer survivors in a controlled cross- sectional study. J Clin Endocrinol Metab. 2007;92:3476–82. https://doi.org/10.1210/jc.2006-2744.

    Article  CAS  PubMed  Google Scholar 

  33. Gebauer J, Higham C, Langer T, Denzer C, Brabant G. Long-term endocrine and metabolic consequences of cancer treatment: a systematic review. Endocr Rev. 2019;40:711–67. https://doi.org/10.1210/er.2018-00092.

    Article  PubMed  Google Scholar 

  34. Chatterjee R, Kottaridis PD, McGarrigle HH, Eliahoo J, McKeag N, Mackinnon S, et al. Patterns of Leydig cell insufficiency in adult males following bone marrow transplantation for haematological malignancies. Bone Marrow Transplant. 2001;28:497–502. https://doi.org/10.1038/sj.bmt.1703160.

    Article  CAS  PubMed  Google Scholar 

  35. Chatterjee R, Andrews HO, McGarrigle HH, Kottaridis PD, Lees WR, Mackinnon S, et al. Cavernosal arterial insufficiency is a major component of erectile dysfunction in some recipients of high-dose chemotherapy/chemo-radiotherapy for haematological malignancies. Bone Marrow Transplant. 2000;25:1185–9. https://doi.org/10.1038/sj.bmt.1702391.

    Article  CAS  PubMed  Google Scholar 

  36. Greenfield DM, Boland E, Ezaydi Y, Ross RJ, Ahmedzai SH, Snowden JA, et al. Endocrine, metabolic, nutritional and body composition abnormalities are common in advanced intensively-treated (transplanted) multiple myeloma. Bone Marrow Transplant. 2014;49:907–12. https://doi.org/10.1038/bmt.2014.63.

    Article  CAS  PubMed  Google Scholar 

  37. Gundgurthi A, Garg MK, Nair V, Pakhetra R, Das S, Sharma S, et al. Endocrine complications after busulphan and cyclophosphamide based hematopoietic stem cell transplant: a single tertiary care centre experience. Indian J Endocrinol Metab. 2013;17:855–63. https://doi.org/10.4103/2230-8210.117248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Schimmer AD, Ali V, Stewart AK, Imrie K, Keating A. Male sexual function after autologous blood or marrow transplantation. Biol Blood Marrow Transplant. 2001;7:279–83. https://doi.org/10.1053/bbmt.2001.v7.pm11400950.

    Article  CAS  PubMed  Google Scholar 

  39. Schneidewind L, Neumann T, Probst KA, Schmidt CA, Kruger W. Recovery from hypogonadism and male health in adult allogeneic stem cell transplantation. Eur J Haematol. 2018;100:584–91. https://doi.org/10.1111/ejh.13052

    Article  CAS  PubMed  Google Scholar 

  40. Sirmatel P, Yilmaz H, Gündüz E. Non-malignant late effects in lymphoma patients treated with autologous hematopoietic stem cell transplantation. Eur J Ther. 2017;23:106–10.

    Article  Google Scholar 

  41. Tauchmanova L, Selleri C, De Rosa G, Esposito M, Di Somma C, Orio F, et al. Endocrine disorders during the first year after autologous stem-cell transplant. Am J Med. 2005;118:664–70. https://doi.org/10.1016/j.amjmed.2005.02.009.

    Article  CAS  PubMed  Google Scholar 

  42. Tauchmanova L, Selleri C, Rosa GD, Pagano L, Orio F, Lombardi G, et al. High prevalence of endocrine dysfunction in long-term survivors after allogeneic bone marrow transplantation for hematologic diseases. Cancer. 2002;95:1076–84. https://doi.org/10.1002/cncr.10773.

    Article  PubMed  Google Scholar 

  43. Vaezi M, Gharib C, Souri M, Ghavamzadeh A. Late complications in acute Leukemia patients following HSCT: a single center experience. Int J Hematol Oncol Stem Cell Res. 2016;10:1–6.

    PubMed  PubMed Central  Google Scholar 

  44. Bhasin S, Brito JP, Cunningham GR, Hayes FJ, Hodis HN, Matsumoto AM, et al. Testosterone therapy in men with hypogonadism: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2018;103:1715–44. https://doi.org/10.1210/jc.2018-00229.

    Article  PubMed  Google Scholar 

  45. Taskinen M, Kananen K, Valimaki M, Loyttyniemi E, Hovi L, Saarinen-Pihkala U, et al. Risk factors for reduced areal bone mineral density in young adults with stem cell transplantation in childhood. Pediatr Transplant. 2006;10:90–97. https://doi.org/10.1111/j.1399-3046.2005.00405.x.

    Article  CAS  PubMed  Google Scholar 

  46. Anandi P, Jain NA, Tian X, Wu CO, Pophali PA, Koklanaris E, et al. Factors influencing the late phase of recovery after bone mineral density loss in allogeneic stem cell transplantation survivors. Bone Marrow Transplant. 2016;51:1101–6. https://doi.org/10.1038/bmt.2016.85.

    Article  CAS  PubMed  Google Scholar 

  47. Orio F, Muscogiuri G, Palomba S, Serio B, Sessa M, Giudice V, et al. Endocrinopathies after allogeneic and autologous transplantation of hematopoietic stem cells. ScientificWorldJournal. 2014;2014:282147 https://doi.org/10.1155/2014/282147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Li Z, Mewawalla P, Stratton P, Yong AS, Shaw BE, Hashmi S, et al. Sexual health in hematopoietic stem cell transplant recipients. Cancer. 2015;121:4124–31. https://doi.org/10.1002/cncr.29675

    Article  PubMed  Google Scholar 

  49. Ponce OJ, Spencer-Bonilla G, Alvarez-Villalobos N, Serrano V, Singh-Ospina N, Rodriguez- Gutierrez R, et al. The efficacy and adverse events of testosterone replacement therapy in hypogonadal men: a systematic review and meta-analysis of randomized, placebo-controlled trials. J Clin Endocrinol Metab. 2018. https://doi.org/10.1210/jc.2018-00404

  50. Mulhall JP, Trost LW, Brannigan RE, Kurtz EG, Redmon JB, Chiles KA, et al. Evaluation and management of testosterone deficiency: AUA guideline. J Urol. 2018;200:423–32. https://doi.org/10.1016/j.juro.2018.03.115.

    Article  PubMed  Google Scholar 

  51. Walsh JS, Marshall H, Smith IL, Greenfield DM, Swain J, Best E, et al. Testosterone replacement in young male cancer survivors: a 6-month double-blind randomised placebo-controlled trial. PLoS Med. 2019;16:e1002960 https://doi.org/10.1371/journal.pmed.1002960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Howell SJ, Radford JA, Adams JE, Smets EM, Warburton R, Shalet SM. Randomized placebo- controlled trial of testosterone replacement in men with mild Leydig cell insufficiency following cytotoxic chemotherapy. Clin Endocrinol. 2001;55:315–24. https://doi.org/10.1046/j.1365-2265.2001.01297.x.

    Article  CAS  Google Scholar 

  53. Chatterjee R, Kottaridis PD, McGarrigle HH, Linch DC. Management of erectile dysfunction by combination therapy with testosterone and sildenafil in recipients of high-dose therapy for haematological malignancies. Bone Marrow Transplant. 2002;29:607–10. https://doi.org/10.1038/sj.bmt.1703421

    Article  CAS  PubMed  Google Scholar 

  54. Kananen K, Volin L, Laitinen K, Alfthan H, Ruutu T, Valimaki MJ. Prevention of bone loss after allogeneic stem cell transplantation by calcium, vitamin D, and sex hormone replacement with or without pamidronate. J Clin Endocrinol Metab. 2005;90:3877–85. https://doi.org/10.1210/jc.2004-2161.

    Article  CAS  PubMed  Google Scholar 

  55. Bar M, Ott SM, Lewiecki EM, Sarafoglou K, Wu JY, Thompson MJ, et al. Bone health management after hematopoietic cell transplantation: an expert panel opinion from the American Society for Transplantation and Cellular Therapy. Biol Blood Marrow Transplant. 2020;26:1784–802. https://doi.org/10.1016/j.bbmt.2020.07.001.

    Article  CAS  PubMed  Google Scholar 

  56. Boquiren VM, Esplen MJ, Wong J, Toner B, Warner E, Malik N. Sexual functioning in breast cancer survivors experiencing body image disturbance. Psychooncology. 2016;25:66–76. https://doi.org/10.1002/pon.3819.

    Article  PubMed  Google Scholar 

  57. Knoepp LR, Shippey SH, Chen CC, Cundiff GW, Derogatis LR, Handa VL. Sexual complaints, pelvic floor symptoms, and sexual distress in women over forty. J Sex Med. 2010;7:3675–82. https://doi.org/10.1111/j.1743-6109.2010.01955.x.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Thygesen KH, Schjodt I, Jarden M. The impact of hematopoietic stem cell transplantation on sexuality: a systematic review of the literature. Bone Marrow Transpl. 2012;47:716–24. https://doi.org/10.1038/bmt.2011.169.

    Article  CAS  Google Scholar 

  59. Syrjala KL, Langer SL, Abrams JR, Storer BE, Martin PJ. Late effects of hematopoietic cell transplantation among 10-year adult survivors compared with case-matched controls. J Clin Oncol. 2005;23:6596–606. https://doi.org/10.1200/JCO.2005.12.674.

    Article  PubMed  Google Scholar 

  60. Watson M, Buck G, Wheatley K, Homewood JR, Goldstone AH, Rees JK, et al. Adverse impact of bone marrow transplantation on quality of life in acute myeloid leukaemia patients; analysis of the UK Medical Research Council AML 10 Trial. Eur J Cancer. 2004;40:971–8. https://doi.org/10.1016/S0959-8049(03)00628-2.

    Article  CAS  PubMed  Google Scholar 

  61. Messerer D, Engel J, Hasford J, Schaich M, Ehninger G, Sauerland C, et al. Impact of different post-remission strategies on quality of life in patients with acute myeloid leukemia. Haematologica. 2008;93:826–33. https://doi.org/10.3324/haematol.11987.

    Article  PubMed  Google Scholar 

  62. Lee SJ, Fairclough D, Parsons SK, Soiffer RJ, Fisher DC, Schlossman RL, et al. Recovery after stem-cell transplantation for hematologic diseases. J Clin Oncol. 2001;19:242–52. https://doi.org/10.1200/JCO.2001.19.1.242.

    Article  CAS  PubMed  Google Scholar 

  63. Hjermstad MJ, Evensen SA, Kvaloy SO, Loge JH, Fayers PM, Kaasa S. The CARES-SF used for prospective assessment of health-related quality of life after stem cell transplantation. Psychooncology. 2003;12:803–13. https://doi.org/10.1002/pon.708.

    Article  PubMed  Google Scholar 

  64. Gruber U, Fegg M, Buchmann M, Kolb HJ, Hiddemann W. The long-term psychosocial effects of haematopoetic stem cell transplantation. Eur J Cancer Care. 2003;12:249–56.

    CAS  Google Scholar 

  65. Lee HG, Park EY, Kim HM, Kim K, Kim WS, Yoon SS, et al. Sexuality and quality of life after hematopoietic stem cell transplantation. Korean J Intern Med. 2002;17:19–23. https://doi.org/10.3904/kjim.2002.17.1.19.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Gifford G, Gilroy N, Dyer G, Brice L, Kabir M, Greenwood M, et al. The experience of survival following allogeneic haematopoietic stem cell transplantation in New South Wales, Australia. Bone Marrow Transplant. 2016;51:1361–8. https://doi.org/10.1038/bmt.2016.135.

    Article  CAS  PubMed  Google Scholar 

  67. Bersvendsen HS, Haugnes HS, Dahl AA, Fagerli UM, Fluge O, Holte H, et al. Sexual function in long-term male lymphoma survivors after high-dose therapy with autologous stem-cell transplantation. Bone Marrow Transplant. 2020;55:891–905. https://doi.org/10.1038/s41409-019-0745-4.

    Article  PubMed  Google Scholar 

  68. Syrjala KL, Schoemans H, Yi JC, Langer SL, Mukherjee A, Onstad L, et al. Sexual functioning in long-term survivors of hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2020. https://doi.org/10.1016/j.bbmt.2020.09.027.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Socie G, Mary JY, Esperou H, Robert DV, Aractingi S, Ribaud P, et al. Health and functional status of adult recipients 1 year after allogeneic haematopoietic stem cell transplantation. Br J Haematol. 2001;113:194–201. https://doi.org/10.1046/j.1365-2141.2001.02678.x.

    Article  CAS  PubMed  Google Scholar 

  70. Heinonen H, Volin L, Uutela A, Zevon M, Barrick C, Ruutu T. Gender-associated differences in the quality of life after allogeneic BMT. Bone Marrow Transpl. 2001;28:503–9. https://doi.org/10.1038/sj.bmt.1703158.

    Article  CAS  Google Scholar 

  71. Noerskov KH, Schjodt I, Syrjala KL, Jarden M. Sexual function 1-year after allogeneic hematopoietic stem cell transplantation. Bone Marrow Transpl. 2016;51:833–40. https://doi.org/10.1038/bmt.2015.342.

    Article  CAS  Google Scholar 

  72. Chiodi S, Spinelli S, Ravera G, Petti AR, Van Lint MT, Lamparelli T, et al. Quality of life in 244 recipients of allogeneic bone marrow transplantation. Br J Haematol. 2000;110:614–9. https://doi.org/10.1046/j.1365-2141.2000.02053.x.

    Article  CAS  PubMed  Google Scholar 

  73. Humphreys CT, Tallman B, Altmaier EM, Barnette V. Sexual functioning in patients undergoing bone marrow transplantation: a longitudinal study. Bone Marrow Transplant. 2007;39:491–6. https://doi.org/10.1038/sj.bmt.1705613.

    Article  CAS  PubMed  Google Scholar 

  74. Mosher CE, DuHamel KN, Rini C, Corner G, Lam J, Redd WH. Quality of life concerns and depression among hematopoietic stem cell transplant survivors. Support Care Cancer. 2011;19:1357–65. https://doi.org/10.1007/s00520-010-0958-y.

    Article  PubMed  Google Scholar 

  75. Syrjala KL, Kurland BF, Abrams JR, Sanders JE, Heiman JR. Sexual function changes during the 5 years after high-dose treatment and hematopoietic cell transplantation for malignancy, with case-matched controls at 5 years. Blood. 2008;111:989–96. https://doi.org/10.1182/blood-2007-06-096594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Norskov KH, Schmidt M, Jarden M. Patients’ experience of sexuality 1-year after allogeneic Haematopoietic Stem Cell Transplantation. Eur J Oncol Nurs. 2015;19:419–26. https://doi.org/10.1016/j.ejon.2014.12.005.

    Article  PubMed  Google Scholar 

  77. Yoo KH, Kang D, Kim IR, Choi EK, Kim JS, Yoon SS, et al. Satisfaction with sexual activity and sexual dysfunction in hematopoietic stem cell transplantation survivors and their partners: a couple study. Bone Marrow Transpl. 2018;53:967–76. https://doi.org/10.1038/s41409-018-0097-5.

    Article  Google Scholar 

  78. Case P. The impact of gender role on recovery from bone marrow transplantation. Illn Crisis Loss. 2002;10:344–55.

    Article  Google Scholar 

  79. Polomeni A, Lapusan S, Bompoint C, Rubio MT, Mohty M. The impact of allogeneic- hematopoietic stem cell transplantation on patients’ and close relatives’ quality of life and relationships. Eur J Oncol Nurs. 2016;21:248–56. https://doi.org/10.1016/j.ejon.2015.10.011.

    Article  CAS  PubMed  Google Scholar 

  80. Bishop MM, Beaumont JL, Hahn EA, Cella D, Andrykowski MA, Brady MJ, et al. Late effects of cancer and hematopoietic stem-cell transplantation on spouses or partners compared with survivors and survivor-matched controls. J Clin Oncol. 2007;25:1403–11. https://doi.org/10.1200/JCO.2006.07.5705.

    Article  PubMed  Google Scholar 

  81. Langer S, Abrams J, Syrjala K. Caregiver and patient marital satisfaction and affect following hematopoietic stem cell transplantation: a prospective, longitudinal investigation. Psychooncology. 2003;12:239–53. https://doi.org/10.1002/pon.633.

    Article  PubMed  Google Scholar 

  82. Booker R, Walker L, Raffin Bouchal S. Sexuality after hematopoietic stem cell transplantation: a mixed methods study. Eur J Oncol Nurs. 2019;39:10–20. https://doi.org/10.1016/j.ejon.2019.01.001.

    Article  PubMed  Google Scholar 

  83. Kim IR, Jang SY, Shin HS, Choi HJ, Jung CW, Yoon SS, et al. Association between sexuality knowledge and sexual dysfunction in hematopoietic stem cell transplantation patients and their partners. Patient Educ Couns. 2020;103:1630–6. https://doi.org/10.1016/j.pec.2020.03.007.

    Article  PubMed  Google Scholar 

  84. Russell C, Harcourt D, Henderson L, Marks DI. Patients’ experiences of appearance changes following allogeneic bone marrow transplantation. Cancer Nurs. 2011;34:315–21. https://doi.org/10.1097/NCC.0b013e3181f8f884.

    Article  PubMed  Google Scholar 

  85. Carter J, Lacchetti C, Andersen BL, Barton DL, Bolte S, Damast S, et al. Interventions to Address Sexual Problems in People With Cancer: American Society of Clinical Oncology Clinical Practice Guideline Adaptation of Cancer Care Ontario Guideline. J Clin Oncol. 2018;36:492–511. https://doi.org/10.1200/JCO.2017.75.8995.

    Article  PubMed  Google Scholar 

  86. El-Jawahri A, Fishman SR, Vanderklish J, Dizon DS, Pensak N, Traeger L, et al. Pilot study of a multimodal intervention to enhance sexual function in survivors of hematopoietic stem cell transplantation. Cancer. 2018;124:2438–46. https://doi.org/10.1002/cncr.31333.

    Article  PubMed  Google Scholar 

  87. Burnett AL, Nehra A, Breau RH, Culkin DJ, Faraday MM, Hakim LS, et al. Erectile dysfunction: AUA guideline. J Urol. 2018;200:633–41. https://doi.org/10.1016/j.juro.2018.05.004.

    Article  PubMed  Google Scholar 

  88. Tichelli A, Rovo A. Fertility issues following hematopoietic stem cell transplantation. Expert Rev Hematol. 2013;6:375–88. https://doi.org/10.1586/17474086.2013.816507

    Article  CAS  PubMed  Google Scholar 

  89. Anserini P, Chiodi S, Spinelli S, Costa M, Conte N, Copello F, et al. Semen analysis following allogeneic bone marrow transplantation. Additional data for evidence-based counselling. Bone Marrow Transplant. 2002;30:447–51. https://doi.org/10.1038/sj.bmt.1703651.

    Article  CAS  PubMed  Google Scholar 

  90. Rovo A, Aljurf M, Chiodi S, Spinelli S, Salooja N, Sucak G, et al. Ongoing graft-versus-host disease is a risk factor for azoospermia after allogeneic hematopoietic stem cell transplantation: a survey of the Late Effects Working Party of the European Group for Blood and Marrow Transplantation. Haematologica. 2013;98:339–45. https://doi.org/10.3324/haematol.2012.071944

    Article  PubMed  PubMed Central  Google Scholar 

  91. Rovo A, Tichelli A, Passweg JR, Heim D, Meyer-Monard S, Holzgreve W, et al. Spermatogenesis in long-term survivors after allogeneic hematopoietic stem cell transplantation is associated with age, time interval since transplantation, and apparently absence of chronic GvHD. Blood. 2006;108:1100–5. https://doi.org/10.1182/blood-2006-01-0176

    Article  CAS  PubMed  Google Scholar 

  92. Joshi S, Savani BN, Chow EJ, Gilleece MH, Halter J, Jacobsohn DA, et al. Clinical guide to fertility preservation in hematopoietic cell transplant recipients. Bone Marrow Transplant. 2014;49:477–84. https://doi.org/10.1038/bmt.2013.211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Logan S, Perz J, Ussher JM, Peate M, Anazodo A. Systematic review of fertility-related psychological distress in cancer patients: Informing on an improved model of care. Psychooncology. 2019;28:22–30. https://doi.org/10.1002/pon.4927.

    Article  PubMed  Google Scholar 

  94. Ussher JM, Perz J, Australian C. Threat of biographical disruption: the gendered construction and experience of infertility following cancer for women and men. BMC Cancer. 2018;18:250 https://doi.org/10.1186/s12885-018-4172-5.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Borgmann-Staudt A, Rendtorff R, Reinmuth S, Hohmann C, Keil T, Schuster FR, et al. Fertility after allogeneic haematopoietic stem cell transplantation in childhood and adolescence. Bone Marrow Transplant. 2012;47:271–6. https://doi.org/10.1038/bmt.2011.78.

    Article  CAS  PubMed  Google Scholar 

  96. Grigg AP, McLachlan R, Zaja J, Szer J. Reproductive status in long-term bone marrow transplant survivors receiving busulfan-cyclophosphamide (120 mg/kg). Bone Marrow Transplant. 2000;26:1089–95. https://doi.org/10.1038/sj.bmt.1702695.

    Article  CAS  PubMed  Google Scholar 

  97. Lukusa AK, Vermylen C, Vanabelle B, Curaba M, Brichard B, Chantrain C, et al. Bone marrow transplantation or hydroxyurea for sickle cell anemia: long-term effects on semen variables and hormone profiles. Pediatr Hematol Oncol. 2009;26:186–94. https://doi.org/10.1080/07357900902892780.

    Article  CAS  PubMed  Google Scholar 

  98. Panasiuk A, Nussey S, Veys P, Amrolia P, Rao K, Krawczuk-Rybak M, et al. Gonadal function and fertility after stem cell transplantation in childhood: comparison of a reduced intensity conditioning regimen containing melphalan with a myeloablative regimen containing busulfan. Br J Haematol. 2015;170:719–26. https://doi.org/10.1111/bjh.13497.

    Article  CAS  PubMed  Google Scholar 

  99. Savani BN, Kozanas E, Shenoy A, Barrett AJ. Recovery of spermatogenesis after total-body irradiation. Blood. 2006;108:4292–3. https://doi.org/10.1182/blood-2006-08-044289.

    Article  CAS  PubMed  Google Scholar 

  100. Wilhelmsson M, Vatanen A, Borgstrom B, Gustafsson B, Taskinen M, Saarinen-Pihkala UM, et al. Adult testicular volume predicts spermatogenetic recovery after allogeneic HSCT in childhood and adolescence. Pediatr Blood Cancer. 2014;61:1094–1100. https://doi.org/10.1002/pbc.24970.

    Article  CAS  PubMed  Google Scholar 

  101. Mathiesen S, Sorensen K, Nielsen MM, Suominen A, Ifversen M, Grell K, et al. Male gonadal function after allogeneic hematopoietic stem cell transplantation in childhood: a cross-sectional, population-based study. Biol Blood Marrow Transpl. 2020;26:1635–45. https://doi.org/10.1016/j.bbmt.2020.05.009.

    Article  CAS  Google Scholar 

  102. Kerbauy MN, Mariano L, Seber A, Rocha V. The impact of low dose busulfan on gonodal function after allogeneic hematopoietic stem cell transplantation for aplastic anemia. Bone Marrow Transplant. 2020;55:1169–71. https://doi.org/10.1038/s41409-019-0639-5.

    Article  PubMed  Google Scholar 

  103. Wagner AM, Beier K, Christen E, Hollander GA, Krenger W. Leydig cell injury as a consequence of an acute graft-versus-host reaction. Blood. 2005;105:2988–90. https://doi.org/10.1182/blood-2004-07-2646.

    Article  CAS  PubMed  Google Scholar 

  104. Babb A, Farah N, Lyons C, Lindsay K, Reddy N, Goldman J, et al. Uptake and outcome of assisted reproductive techniques in long-term survivors of SCT. Bone Marrow Transplant. 2012;47:568–73. https://doi.org/10.1038/bmt.2011.134.

    Article  CAS  PubMed  Google Scholar 

  105. Branvall E, Derolf AR, Johansson E, Hultcrantz M, Bergmark K, Bjorkholm M. Self-reported fertility in long-term survivors of acute myeloid leukemia. Ann Hematol. 2014;93:1491–8. https://doi.org/10.1007/s00277-014-2088-y.

    Article  CAS  PubMed  Google Scholar 

  106. Carter A, Robison LL, Francisco L, Smith D, Grant M, Baker KS, et al. Prevalence of conception and pregnancy outcomes after hematopoietic cell transplantation: report from the Bone Marrow Transplant Survivor Study. Bone Marrow Transpl. 2006;37:1023–9. https://doi.org/10.1038/sj.bmt.1705364.

    Article  CAS  Google Scholar 

  107. Hammond C, Abrams JR, Syrjala KL. Fertility and risk factors for elevated infertility concern in 10-year hematopoietic cell transplant survivors and case-matched controls. J Clin Oncol. 2007;25:3511–7. https://doi.org/10.1200/JCO.2007.10.8993

    Article  PubMed  Google Scholar 

  108. Hayden PJ, Keogh F, Ni Conghaile M, Carroll M, Crowley M, Fitzsimon N, et al. A single-centre assessment of long-term quality-of-life status after sibling allogeneic stem cell transplantation for chronic myeloid leukaemia in first chronic phase. Bone Marrow Transplant. 2004;34:545–56. https://doi.org/10.1038/sj.bmt.1704638.

    Article  CAS  PubMed  Google Scholar 

  109. Ishiguro H, Yasuda Y, Tomita Y, Shinagawa T, Shimizu T, Morimoto T, et al. Gonadal shielding to irradiation is effective in protecting testicular growth and function in long-term survivors of bone marrow transplantation during childhood or adolescence. Bone Marrow Transplant. 2007;39:483–90. https://doi.org/10.1038/sj.bmt.1705612.

    Article  CAS  PubMed  Google Scholar 

  110. Loren AW, Chow E, Jacobsohn DA, Gilleece M, Halter J, Joshi S, et al. Pregnancy after hematopoietic cell transplantation: a report from the late effects working committee of the Center for International Blood and Marrow Transplant Research (CIBMTR). Biol Blood Marrow Transplant. 2011;17:157–66. https://doi.org/10.1016/j.bbmt.2010.07.009.

    Article  PubMed  Google Scholar 

  111. Rahal I, Galambrun C, Bertrand Y, Garnier N, Paillard C, Frange P, et al. Late effects after hematopoietic stem cell transplantation for beta-thalassemia major: the French national experience. Haematologica. 2018;103:1143–9. https://doi.org/10.3324/haematol.2017.183467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Salooja N, Szydlo RM, Socie G, Rio B, Chatterjee R, Ljungman P, et al. Pregnancy outcomes after peripheral blood or bone marrow transplantation: a retrospective survey. Lancet. 2001;358:271–6. https://doi.org/10.1016/s0140-6736(01)05482-4.

    Article  CAS  PubMed  Google Scholar 

  113. Wilhelmsson M, Glosli H, Ifversen M, Abrahamsson J, Winiarski J, Jahnukainen K, et al. Long- term health outcomes in survivors of childhood AML treated with allogeneic HSCT: a NOPHO- AML Study. Bone Marrow Transpl. 2019;54:726–36. https://doi.org/10.1038/s41409-018-0337-8.

    Article  Google Scholar 

  114. Rovo A, Aljurf M, Chiodi S, Spinelli S, Salooja N, Sucak G, et al. Paternity wishes in long-term survivors after allogeneic hematopoietic SCT. A study of the late effects working party of the EBMT. Bone Marrow Transplant. 2013;48:878–9. https://doi.org/10.1038/bmt.2012.255

    Article  CAS  PubMed  Google Scholar 

  115. Balduzzi A, Dalle JH, Jahnukainen K, von Wolff M, Lucchini G, Ifversen M, et al. Fertility preservation issues in pediatric hematopoietic stem cell transplantation: practical approaches from the consensus of the Pediatric Diseases Working Party of the EBMT and the International BFM Study Group. Bone Marrow Transplant. 2017;52:1406–15. https://doi.org/10.1038/bmt.2017.147

    Article  CAS  PubMed  Google Scholar 

  116. Nahata L, Cohen LE, Lehmann LE, Yu RN. Semen analysis in adolescent cancer patients prior to bone marrow transplantation: when is it too late for fertility preservation? Pediatr Blood Cancer. 2013;60:129–32. https://doi.org/10.1002/pbc.24172.

    Article  PubMed  Google Scholar 

  117. Schlegel PN, Sigman M, Collura B, De Jonge CJ, Eisenberg ML, Lamb DJ, et al. Diagnosis and treatment of infertility in men: AUA/ASRM guideline part II. Fertil Steril. 2020. https://doi.org/10.1016/j.fertnstert.2020.11.016.

    Article  PubMed  Google Scholar 

  118. Borgstrom B, Fridstrom M, Gustafsson B, Ljungman P, Rodriguez-Wallberg KA. A prospective study on the long-term outcome of prepubertal and pubertal boys undergoing testicular biopsy for fertility preservation prior to hematologic stem cell transplantation. Pediatr Blood Cancer. 2020;67:e28507 https://doi.org/10.1002/pbc.28507.

    Article  CAS  PubMed  Google Scholar 

  119. Bernaudin F, Dalle JH, Bories D, de Latour RP, Robin M, Bertrand Y, et al. Long-term event-free survival, chimerism and fertility outcomes in 234 patients with sickle-cell anemia younger than 30 years after myeloablative conditioning and matched-sibling transplantation in France. Haematologica. 2020;105:91–101. https://doi.org/10.3324/haematol.2018.213207.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Abdelaal O, Barber H, Atala A, Sadri-Ardekani H. Purging of malignant cell contamination prior to spermatogonia stem cell autotransplantation to preserve fertility: progress & prospects. Curr Opin Endocrinol Diabetes Obes. 2019;26:166–74. https://doi.org/10.1097/MED.0000000000000481.

    Article  PubMed  Google Scholar 

  121. Syrjala KL, Martin PJ, Lee SJ. Delivering care to long-term adult survivors of hematopoietic cell transplantation. J Clin Oncol. 2012;30:3746–51. https://doi.org/10.1200/JCO.2012.42.3038

    Article  PubMed  PubMed Central  Google Scholar 

  122. Bilmon IA, Ashton LJ, Le Marsney RE, Dodds AJ, O’Brien TA, Wilcox L, et al. Second cancer risk in adults receiving autologous haematopoietic SCT for cancer: a population-based cohort study. Bone Marrow Transpl. 2014;49:691–8. https://doi.org/10.1038/bmt.2014.13.

    Article  Google Scholar 

  123. Gallagher G, Forrest DL. Second solid cancers after allogeneic hematopoietic stem cell transplantation. Cancer. 2007;109:84–92. https://doi.org/10.1002/cncr.22375.

    Article  PubMed  Google Scholar 

  124. Rizzo JD, Curtis RE, Socie G, Sobocinski KA, Gilbert E, Landgren O, et al. Solid cancers after allogeneic hematopoietic cell transplantation. Blood. 2009;113:1175–83. https://doi.org/10.1182/blood-2008-05-158782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Mahindra A, Raval G, Mehta P, Brazauskas R, Zhang MJ, Zhong X, et al. New cancers after autotransplantations for multiple myeloma. Biol Blood Marrow Transplant. 2015;21:738–45. https://doi.org/10.1016/j.bbmt.2014.12.028.

    Article  PubMed  Google Scholar 

  126. Baker KS, Leisenring WM, Goodman PJ, Ermoian RP, Flowers ME, Schoch G, et al. Total body irradiation dose and risk of subsequent neoplasms following allogeneic hematopoietic cell transplantation. Blood. 2019;133:2790–9. https://doi.org/10.1182/blood.2018874115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Wu PA, Stern RS, Huang V, Liu KX, Chen CA, Tzachanis D, et al. Reduced-Intensity conditioning regimens, prior chronic lymphocytic leukemia, and graft-versus-host disease are associated with higher rates of skin cancer after allogeneic hematopoietic stem cell transplantation. J Investig Dermatol. 2019;139:591–9. https://doi.org/10.1016/j.jid.2018.08.025.

    Article  CAS  PubMed  Google Scholar 

  128. Inamoto Y, Matsuda T, Tabuchi K, Kurosawa S, Nakasone H, Nishimori H, et al. Outcomes of patients who developed subsequent solid cancer after hematopoietic cell transplantation. Blood Adv. 2018;2:1901–13. https://doi.org/10.1182/bloodadvances.2018020966

    Article  PubMed  PubMed Central  Google Scholar 

  129. Bhatia S, Louie AD, Bhatia R, O’Donnell MR, Fung H, Kashyap A, et al. Solid cancers after bone marrow transplantation. J Clin Oncol. 2001;19:464–71. https://doi.org/10.1200/JCO.2001.19.2.464.

    Article  CAS  PubMed  Google Scholar 

  130. Leisenring W, Friedman DL, Flowers ME, Schwartz JL, Deeg HJ. Nonmelanoma skin and mucosal cancers after hematopoietic cell transplantation. J Clin Oncol. 2006;24:1119–26. https://doi.org/10.1200/JCO.2005.02.7052

    Article  PubMed  Google Scholar 

  131. Tichelli A, Beohou E, Labopin M, Socie G, Rovo A, Badoglio M, et al. Evaluation of second solid cancers after hematopoietic stem cell transplantation in European patients. JAMA Oncol. 2019;5:229–35. https://doi.org/10.1001/jamaoncol.2018.4934.

    Article  PubMed  Google Scholar 

  132. Atsuta Y, Suzuki R, Yamashita T, Fukuda T, Miyamura K, Taniguchi S, et al. Continuing increased risk of oral/esophageal cancer after allogeneic hematopoietic stem cell transplantation in adults in association with chronic graft-versus-host disease. Ann Oncol. 2014;25:435–41. https://doi.org/10.1093/annonc/mdt558.

    Article  CAS  PubMed  Google Scholar 

  133. Baker KS, DeFor TE, Burns LJ, Ramsay NK, Neglia JP, Robison LL. New malignancies after blood or marrow stem-cell transplantation in children and adults: incidence and risk factors. J Clin Oncol. 2003;21:1352–8. https://doi.org/10.1200/JCO.2003.05.108

    Article  PubMed  Google Scholar 

  134. Majhail NS, Brazauskas R, Rizzo JD, Sobecks RM, Wang Z, Horowitz MM, et al. Secondary solid cancers after allogeneic hematopoietic cell transplantation using busulfan-cyclophosphamide conditioning. Blood. 2011;117:316–22. https://doi.org/10.1182/blood-2010-07-294629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Ringden O, Brazauskas R, Wang Z, Ahmed I, Atsuta Y, Buchbinder D, et al. Second solid cancers after allogeneic hematopoietic cell transplantation using reduced-intensity conditioning. Biol Blood Marrow Transplant. 2014;20:1777–84. https://doi.org/10.1016/j.bbmt.2014.07.009

    Article  PubMed  PubMed Central  Google Scholar 

  136. Vajdic CM, Mayson E, Dodds AJ, O’Brien T, Wilcox L, Nivison-Smith I, et al. Second cancer risk and late mortality in adult Australians receiving allogeneic hematopoietic stem cell transplantation: a population-based cohort study. Biol Blood Marrow Transplant. 2016;22:949–56. https://doi.org/10.1016/j.bbmt.2016.01.027.

    Article  PubMed  Google Scholar 

  137. Yokota A, Ozawa S, Masanori T, Akiyama H, Ohshima K, Kanda Y, et al. Secondary solid tumors after allogeneic hematopoietic SCT in Japan. Bone Marrow Transplant. 2012;47:95–100. https://doi.org/10.1038/bmt.2011.23.

    Article  CAS  PubMed  Google Scholar 

  138. Danner-Koptik KE, Majhail NS, Brazauskas R, Wang Z, Buchbinder D, Cahn JY, et al. Second malignancies after autologous hematopoietic cell transplantation in children. Bone Marrow Transplant. 2013;48:363–8. https://doi.org/10.1038/bmt.2012.166.

    Article  CAS  PubMed  Google Scholar 

  139. Shimoni A, Shem-Tov N, Chetrit A, Volchek Y, Tallis E, Avigdor A, et al. Secondary malignancies after allogeneic stem-cell transplantation in the era of reduced-intensity conditioning; the incidence is not reduced. Leukemia. 2013;27:829–35. https://doi.org/10.1038/leu.2012.299

    Article  CAS  PubMed  Google Scholar 

  140. Gutierrez-Pascual M, Vicente-Martin FJ, Lopez-Estebaranz JL. Lichen sclerosus and squamous cell carcinoma. Actas Dermosifiliogr. 2012;103:21–28. https://doi.org/10.1016/j.adengl.2011.05.004.

    Article  PubMed  Google Scholar 

  141. Snowden JA, McGrath E, Duarte RF, Saccardi R, Orchard K, Worel N, et al. JACIE accreditation for blood and marrow transplantation: past, present and future directions of an international model for healthcare quality improvement. Bone Marrow Transplant. 2017;52:1367–71. https://doi.org/10.1038/bmt.2017.54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

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
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Annie Im
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rebecca L. Hunter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoshihiro Inamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Teresa Lupo-Stanghellini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alicia Rovo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sherif M. Badawy
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Linda Burns
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hesham Eissa
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hemant S. Murthy
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Pinki Prasad
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Akshay Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Elizabeth Suelzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Vaibhav Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Mahmoud Aljurf
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Karen Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Grzegorz W. Basak
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. David Buchbinder
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Zachariah DeFilipp
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Lana Desnica Grkovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Ajoy Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Hermann Einsele
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Michael L. Eisenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Narendranath Epperla
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Nosha Farhadfar
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Arthur Flatau
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. Robert Peter Gale
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. Hildegard Greinix
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. Betty K. Hamilton
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. Shahrukh Hashmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. Peiman Hematti
    View author publications

    You can also search for this author in PubMed Google Scholar

  32. Kareem Jamani
    View author publications

    You can also search for this author in PubMed Google Scholar

  33. Dipnarine Maharaj
    View author publications

    You can also search for this author in PubMed Google Scholar

  34. John Murray
    View author publications

    You can also search for this author in PubMed Google Scholar

  35. Seema Naik
    View author publications

    You can also search for this author in PubMed Google Scholar

  36. Sunita Nathan
    View author publications

    You can also search for this author in PubMed Google Scholar

  37. Steven Pavletic
    View author publications

    You can also search for this author in PubMed Google Scholar

  38. Zinaida Peric
    View author publications

    You can also search for this author in PubMed Google Scholar

  39. Drazen Pulanic
    View author publications

    You can also search for this author in PubMed Google Scholar

  40. Richard Ross
    View author publications

    You can also search for this author in PubMed Google Scholar

  41. Andrea Salonia
    View author publications

    You can also search for this author in PubMed Google Scholar

  42. Isabel Sanchez-Ortega
    View author publications

    You can also search for this author in PubMed Google Scholar

  43. Bipin N. Savani
    View author publications

    You can also search for this author in PubMed Google Scholar

  44. Tal Schechter
    View author publications

    You can also search for this author in PubMed Google Scholar

  45. Ami J. Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  46. Stephanie M. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  47. John A. Snowden
    View author publications

    You can also search for this author in PubMed Google Scholar

  48. Amir Steinberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  49. Douglas Tremblay
    View author publications

    You can also search for this author in PubMed Google Scholar

  50. Sarah C. Vij
    View author publications

    You can also search for this author in PubMed Google Scholar

  51. Lauren Walker
    View author publications

    You can also search for this author in PubMed Google Scholar

  52. Daniel Wolff
    View author publications

    You can also search for this author in PubMed Google Scholar

  53. Jean A. Yared
    View author publications

    You can also search for this author in PubMed Google Scholar

  54. Hélène Schoemans
    View author publications

    You can also search for this author in PubMed Google Scholar

  55. André Tichelli
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Ethics declarations

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.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41409-022-01591-z

This article is cited by

Search

Advanced search

Quick links