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Transplant Toxicities

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

Abstract

Fertility preservation is an urgent challenge in the transplant setting. A panel of transplanters and fertility specialists within the Pediatric Diseases Working Party of the European Society for Blood and Marrow Transplantation (EBMT) and the International BFM Study Group provides specific guidelines. Patients and families should be informed of possible gender- and age-specific cryopreservation strategies that should be tailored according to the underlying disease, clinical condition and previous exposure to chemotherapy. Semen collection should be routinely offered to all postpubertal boys at the diagnosis of any disease requiring therapy that could potentially impair fertility. Testicular tissue collection might be offered to postpubertal boys; nevertheless, its use has been unsuccessful to date. Oocyte collection after hormonal hyperstimulation should be offered to postpubertal girls facing gonadotoxic therapies that could be delayed for the 2 weeks required for the procedure. Ovarian tissue collection could be offered to pre-/post-pubertal girls. Pregnancies have been reported after postpubertal ovarian tissue reimplantation; however, to date, no pregnancy has been reported after the reimplantation of prepubertal ovarian tissue or in vitro maturation of pre-/post-pubertal ovarian tissue. Possible future advances in reproductive medicine could change this scenario. Health authorities should prioritize fertility preservation projects in pediatric transplantation to improve patient care and quality of life.

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References

  1. Passweg JR, Baldomero H, Peters C, Gaspar HB, Cesaro S, Dreger P et al. Hematopoietic SCT in Europe: data and trends in 2012 with special consideration of pediatric transplantation. Bone Marrow Transplant 2014; 49: 744–750.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Lawitschka A, Faraci M, Yaniv I, Veys P, Bader P, Wachowiak J et al. Paediatric reduced intensity conditioning: analysis of centre strategies on regimens and definitions by the EBMT Paediatric Diseases and Complications and Quality of Life WP. Bone Marrow Transplant 2015; 50: 592–597.

    Article  CAS  PubMed  Google Scholar 

  3. Dvorak CC, Gracia CR, Sanders JE, Cheng EY, Scott Baker K, Pulsipher MA et al. NCI, NHLBI/PBMTC first international conference on late effects after pediatric hematopoietic cell transplantation: endocrine challenges-thyroid dysfunction, growth impairment, bone health, & reproductive risks. Biol Blood Marrow Transplant 2011; 17: 1725–1738.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Chow EJ, Stratton KL, Leisenring WM, Oeffinger KC, Sklar CA, Donaldson SS et al. Pregnancy after chemotherapy in male and female survivors of childhood cancer treated between 1970 and 1999: a report from the Childhood Cancer Survivor Study cohort. Lancet Oncol 2016; 17: 567–576.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Vatanen A, Wilhelmsson M, Borgstrom B, Gustafsson B, Taskinen M, Saarinen-Pihkala UM et al. Ovarian function after allogeneic hematopoietic stem cell transplantation in childhood and adolescence. Eur J Endocrinol 2014; 170: 211–218.

    Article  CAS  PubMed  Google Scholar 

  6. Pfizer C, Orawa H, Balcerek M, Langer T, Dirksen U, Keslova P et al. Dynamics of fertility impairment and recovery after allogeneic haematopoietic stem cell transplantation in childhood and adolescence: results from a longitudinal study. J Cancer Res Clin Oncol 2015; 141: 135–142.

    Article  Google Scholar 

  7. Meistricht ML . The effects of chemotherapy and radiotherapy on spermatogenesis in humans. Fertil Steril 2013; 100: 1180–1186.

    Article  CAS  Google Scholar 

  8. Nakagawa K, Kanda Y, Yamashita H, Nakagawa S, Sasano N, Ohtomo K et al. Ovarian shielding allows ovarian recovery and normal birth in female hematopoietic SCT recipients undergoing TBI. Bone Marrow Transplant 2008; 42: 697–699.

    Article  CAS  PubMed  Google Scholar 

  9. 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: 271–276.

    Article  CAS  PubMed  Google Scholar 

  10. Sanders JE, Hawley J, Levy W, Gooley T, Buckner CD, Deeg HJ et al. Pregnancies following high-dose cyclophosphamide with or without high-dose busulfan or total-body irradiation and bone marrow transplantation. Blood 1996; 87: 3045–3052.

    CAS  PubMed  Google Scholar 

  11. 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.

    Article  PubMed  Google Scholar 

  12. Vatanen A, Wilhelmsson M, Borgström B, Gustafsson B, Taskinen M, Saarinen-Pihkala UM et al. Ovarian function after allogeneic hematopoietic stem cell transplantation in childhood and adolescence. Eur J Endocrinol 2013; 170: 211–218.

    Article  CAS  PubMed  Google Scholar 

  13. Assouline E, Crocchiolo R, Prebet T, Broussais F, Coso D, Gamerre M et al. Impact of reduced-intensity conditioning allogeneic stem cell transplantation on women's fertility. Clin Lymphoma Myeloma Leuk 2013; 13: 704–710.

    Article  PubMed  Google Scholar 

  14. 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: 719–726.

    Article  CAS  PubMed  Google Scholar 

  15. Faraci M, Matthes-Martin S, Lanino E, Morreale G, Ferretti M, Giardino S et al. Two pregnancies shortly after transplantation with reduced intensity conditioning in chronic myeloid leukemia. Pediatr Transplant 2016; 20: 158–161.

    Article  CAS  PubMed  Google Scholar 

  16. Lambertini M, Del Mastro L, Pescio MC, Andersen CY, Azim HA Jr, Peccatori FA et al. Cancer and fertility preservation: international recommendations from an expert meeting. BMC Med 2016; 14: 1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ronn R, Holzer HE . Oncofertility in Canada: the impact of cancer on fertility. Curr Oncol 2013; 20: e338–e344.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. McLaren JF, Bates GW . Fertility preservation in women of reproductive age with cancer. Am J Obstet Gynecol 2012; 207: 455–462.

    Article  PubMed  Google Scholar 

  19. Asadi Azarbaijani B, Sheikhi M, Oskam IC, Nurmio M, Laine T, Tinkanen H et al. Effect of previous chemotherapy on the quality of cryopreserved human ovarian tissue in vitro. PLoS ONE 2015; 10: e0133985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. von Wolff M, Dittrich R, Liebenthron J, Nawroth F, Schuring AN, Bruckner T et al. Fertility-preservation counselling and treatment for medical reasons: data from a multinational network of over 5000 women. Reprod Biomed Online 2015; 31: 605–612.

    Article  PubMed  Google Scholar 

  21. Dalle JH, Lucchini G, Balduzzi A, Ifversen M, Jahnukainen K, Macklon KT et al. State-of-the-art fertility preservation in children and adolescents undergoing haematopoietic stem cell transplantation: a report on the expert meeting of the Paediatric Diseases Working Party (PDWP) of the European Society for Blood and Marrow Transplantation (EBMT) in Baden, Austria, 29-30 September 2015. Bone Marrow Transplant 2017; doi:10.1038/bmt.2017.21.

  22. Muller J, Sonksen J, Sommer P, Schmiegelow M, Petersen PM, Heilman C et al. Cryopreservation of semen from pubertal boys with cancer. Med Ped Oncol 2000; 34: 191–194.

    Article  CAS  Google Scholar 

  23. DiNofia AM, Wang X, Yannekis G, Ogle S, Hobbie WL, Carlson CA et al. Analysis of semen parameters in a young cohort of cancer patients. Pediatr Blood Cancer 2017; 64: 381–386.

    Article  PubMed  Google Scholar 

  24. Jahnukainen K, Mitchell RT, Stukenborg JB . Testicular function and fertility preservation after treatment for haematological cancer. Curr Opin Endocrinol Diabetes Obes 2015; 22: 217–223.

    Article  CAS  PubMed  Google Scholar 

  25. Rotgers E, Cisneros-Montalvo S, Jahnukainen K, Sandholm J, Toppari J, Nurmio M . A detailed protocol for a rapid analysis of testicular cell populations using flow cytometry. Andrology 2015; 3: 947–955.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Adank MC, van Dorp W, Smit M, van Casteren NJ, Laven JS, Pieters R et al. Electroejaculation as a method of fertility preservation in boys diagnosed with cancer: a single-center experience and review of the literature. Fertil Steril 2014; 102: 199–205.

    Article  PubMed  Google Scholar 

  27. Calhaz-Jorge C, de Geyter C, Kupka MS, de Mouzon J, Erb K, Mocanu E et al. Assisted reproductive technology in Europe, 2012: results generated from European registers by ESHRE. Hum Reprod 2016; 31: 1638–1652.

    Article  CAS  PubMed  Google Scholar 

  28. Masliukaite I, Hagen JM, Jahnukainen K, Stukenborg JB, Repping S, van der Veen F et al. Establishing reference values for age-related spermatogonial quantity in prepubertal human testes: a systematic review and meta-analysis. Fertil Steril 2016; 106: 1652–1657.e2.

    Article  PubMed  Google Scholar 

  29. Picton HM, Wyns C, Anderson RA, Goossens E, Jahnukainen K, Kliesch S et al. A European perspective on testicular tissue cryopreservation for fertility preservation in prepubertal and adolescent boys. Hum Reprod 2015; 30: 2463–2475.

    Article  PubMed  Google Scholar 

  30. Hermann BP, Sukhwani M, Winkler F, Pascarella JN, Peters KA, Sheng Y et al. Spermatogonial stem cell transplantation into rhesus testes regenerates spermatogenesis producing functional sperm. Cell Stem Cell 2012; 11: 715–726.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Jahnukainen K, Ehmcke J, Nurmio M, Schlatt S . Autologous ectopic grafting of cryopreserved testicular tissue preserves the fertility of prepubescent monkeys which receive a sterilizing cytotoxic therapy. Cancer Res 2012; 72: 5174–5178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Goossens E, Van Saen D, Tournaye H . Spermatogonial stem cell preservation and transplantation: from research to clinic. Hum Reprod 2013; 28: 897–907.

    Article  CAS  PubMed  Google Scholar 

  33. Nurmio M, Keros V, Lähteenmäki P, Salmi T, Kallajoki M, Jahnukainen K . Effect of childhood acute lymphoblastic leukemia therapy on spermatogonia populations and future fertility. J Clin Endocrinol Metab 2009; 94: 2119–2122.

    Article  CAS  PubMed  Google Scholar 

  34. Lawrenz B, Jauckus J, Kupka M, Strowitzki T, von Wolff M . Efficacy and safety of ovarian stimulation before chemotherapy in 205 cases. Fertil Steril 2010; 94: 2871–2873.

    Article  PubMed  Google Scholar 

  35. Lawrenz B, Jauckus J, Kupka MS, Strowitzki T, von Wolff M . Fertility preservation in >1000 patients: patient's characteristics, spectrum, efficacy and risks of applied preservation techniques. Arch Gynecol Obstetr 2011; 283: 651–656.

    Article  Google Scholar 

  36. Schmidt KT, Larsen EC, Andersen CY, Andersen AN . Risk of ovarian failure and fertility preserving methods in girls and adolescents with a malignant disease. BJOG 2010; 117: 163–174.

    Article  CAS  PubMed  Google Scholar 

  37. Cakmak H, Katz A, Cedars MI, Rosen MP . Effective method for emergency fertility preservation: random-start controlled ovarian stimulation. Fertil Steril 2013; 100: 1673–1680.

    Article  PubMed  Google Scholar 

  38. Moffat R, Pirtea P, Gayet V, Wolf JP, Chapron C, de Ziegler D . Dual ovarian stimulation is a new viable option for enhancing the oocyte yield when the time for assisted reproductive technology is limited. Reprod Biomed Online 2014; 29: 659–661.

    Article  PubMed  Google Scholar 

  39. von Wolff M, Thaler CJ, Frambach T, Zeeb C, Lawrenz B, Popovici RM et al. Ovarian stimulation to cryopreserve fertilized oocytes in cancer patients can be started in the luteal phase. Fertil Steril 2009; 92: 1360–1365.

    Article  CAS  PubMed  Google Scholar 

  40. Meistrich ML, Shetty G . Hormonal suppression for fertility preservation in males and females. Reproduction 2008; 136: 691–701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lambertini M, Ceppi M, Poggio F, Peccatori FA, Azim HA Jr, Ugolini D et al. Ovarian suppression using luteinizing hormone-releasing hormone agonists during chemotherapy to preserve ovarian function and fertility of breast cancer patients: a meta-analysis of randomized studies. Ann Oncol 2015; 26: 2408–2419.

    Article  CAS  PubMed  Google Scholar 

  42. Anderson R, Adamson D, Yellowlees A, Dunlop GT, Leonard R . Administration of a GnRH agonist during chemotherapy for breast cancer reduces ovarian toxicity in women aged under 40 years. Hum Reprod 2016; 39: i339.

    Google Scholar 

  43. Elgindy E, Sibai H, Abdelghani A, Mostafa M . Protecting ovaries during chemotherapy through gonad suppression: a systematic review and meta-analysis. Obstet Gynecol 2015; 126: 187–195.

    Article  CAS  PubMed  Google Scholar 

  44. Demeestere I, Brice P, Peccatori FA, Kentos A, Dupuis J, Zachee P et al. No evidence for the benefit of gonadotropin-releasing hormone agonist in preserving ovarian function and fertility in lymphoma survivors treated with chemotherapy: final long-term report of a prospective randomized trial. J Clin Oncol 2016; 34: 2568–2574.

    Article  CAS  PubMed  Google Scholar 

  45. Andersen CY, Kristensen SG, Greve T, Schmidt KT . Cryopreservation of ovarian tissue for fertility preservation in young female oncological patients. Future Oncol 2012; 8: 595–608.

    Article  CAS  PubMed  Google Scholar 

  46. Rosendahl M, Schmidt KT, Ernst E, Rasmussen PE, Loft A, Byskov AG et al. Cryopreservation of ovarian tissue for a decade in Denmark: a view of the technique. Reprod Biomed Online 2011; 22: 162–171.

    Article  PubMed  Google Scholar 

  47. Huober-Zeeb C, Lawrenz B, Popovici RM, Strowitzki T, Germeyer A, Stute P et al. Improving fertility preservation in cancer: ovarian tissue cryobanking followed by ovarian stimulation can be efficiently combined. Fertil Steril 2011; 95: 342–344.

    Article  PubMed  Google Scholar 

  48. Dolmans MM, Marotta ML, Pirard C, Donnez J, Donnez O . Ovarian tissue cryopreservation followed by controlled ovarian stimulation and pick-up of mature oocytes does not impair the number or quality of retrieved oocytes. J Ovarian Res 2014; 7: 80.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Abir R, Ben-Aharon I, Garor R, Yaniv I, Ash S, Stemmer SM et al. Cryopreservation of in vitro matured oocytes in addition to ovarian tissue freezing for fertility preservation in paediatric female cancer patients before and after cancer therapy. Hum Reprod 2016; 31: 750–762.

    Article  CAS  PubMed  Google Scholar 

  50. Jadoul P, Dolmans MM, Donnez J . Fertility preservation in girls during childhood: is it feasible, efficient and safe and to whom should it be proposed? Human Reprod Update 2010; 16: 617–630.

    Article  Google Scholar 

  51. Poirot CJ, Martelli H, Genestie C, Golmard JL, Valteau-Couanet D, Helardot P et al. Feasibility of ovarian tissue cryopreservation for prepubertal females with cancer. Pediatr Blood Cancer 2007; 49: 74–78.

    Article  PubMed  Google Scholar 

  52. Knight S, Lorenzo A, Maloney AM, Srikanthan A, Donen R, Greenblatt E et al. An approach to fertility preservation in prepubertal and postpubertal females: a critical review of current literature. Pediatr Blood Cancer 2015; 62: 935–939.

    Article  PubMed  Google Scholar 

  53. Luyckx V, Scalercio S, Jadoul P, Amorim CA, Soares M, Donnez J et al. Evaluation of cryopreserved ovarian tissue from prepubertal patients after long-term xenografting and exogenous stimulation. Fertile Steril 2013; 100: 1350–1357.

    Article  CAS  Google Scholar 

  54. Anderson RA, McLaughlin M, Wallace WHB, Albertini DF, Telfer EE . The immature human ovary shows loss of abnormal follicles and increasing follicle developmental competence through childhood and adolescence. Hum Reprod 2014; 29: 97–106.

    Article  CAS  PubMed  Google Scholar 

  55. Westergaard CG, Byskov AG, Andersen CY . Morphometric characteristics of the primordial to primary follicle transition in the human ovary in relation to age. Hum Reprod 2007; 22: 2225–2231.

    Article  PubMed  Google Scholar 

  56. Donnez J, Dolmans MM . Ovarian cortex transplantation: 60 reported live births brings the success and worldwide expansion of the technique towards routine clinical practice. J Assist Reprod Gen 2015; 32: 1167–1170.

    Article  Google Scholar 

  57. Jensen AK, Kristensen SG, Macklon KT, Jeppesen JV, Fedder J, Ernst E et al. Outcomes of transplantations of cryopreserved ovarian tissue to 41 women in Denmark. Hum Reprod 2015; 30: 2838–2845.

    Article  CAS  PubMed  Google Scholar 

  58. Meirow D, Ra'anani H, Shapira M, Brenghausen M, Derech Chaim S, Aviel-Ronen S et al. Transplantations of frozen-thawed ovarian tissue demonstrate high reproductive performance and the need to revise restrictive criteria. Fertil Steril 2016; 106: 467–474.

    Article  PubMed  Google Scholar 

  59. Van der Ven H, Liebenthron J, Beckmann M, Toth B, Korell M, Krüssel J et al. Ninety-five orthotopic transplantations in 74 women of ovarian tissue after cytotoxic treatment in a fertility preservation network: tissue activity, pregnancy and delivery rates. Hum Reprod 2016; 31: 2031–2041.

    Article  CAS  PubMed  Google Scholar 

  60. Liebenthron J, Dittrich R, Toth B, Korell M, Krüssel J, Van der Ven K et al. Orthotopic ovarian tissue transplantation - results in relation to experience of the transplanting centers, overnight tissue transportation and transplantation into the peritoneum. Hum Reprod 2015; 30 (Suppl 1): i97–i98.

    Google Scholar 

  61. Demeestere I, Simon P, Dedeken L, Moffa F, Tsepelidis S, Brachet C et al. Live birth after autograft of ovarian tissue cryopreserved during childhood. Hum Reprod 2015; 30: 2107–2109.

    Article  PubMed  Google Scholar 

  62. Asadi-Azarbaijani B, Sheikhi M, Nurmio M, Tinkanen H, Juvonen V, Dunkel L et al. Minimal residual disease of leukemia and the quality of cryopreserved human ovarian tissue in vitro. Leuk Lymphoma 2016; 57: 700–707.

    Article  CAS  PubMed  Google Scholar 

  63. Dolmans MM, Marinescu C, Saussoy P, Van Langendonckt A, Amorim C, Donnez J . Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood 2010; 116: 2908–2914.

    Article  CAS  PubMed  Google Scholar 

  64. Abir R, Feinmesser M, Yaniv I, Fisch B, Cohen IJ, Ben-Haroush A et al. Occasional involvement of the ovary in Ewing sarcoma. Hum Reprod 2010; 25: 1708–1712.

    Article  CAS  PubMed  Google Scholar 

  65. Abir R, Aviram A, Feinmesser M, Stein J, Yaniv I, Parnes D et al. Ovarian minimal residual disease in chronic myeloid leukaemia. Reprod Biomed Online 2014; 28: 255–260.

    Article  CAS  PubMed  Google Scholar 

  66. Ben-Aharon I, Abir R, Perl G, Stein J, Gilad G, Toledano H et al. Optimizing the process of fertility preservation in pediatric female cancer patients - a multidisciplinary program. BMC Cancer 2016; 16: 620.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Jensen AK, Rechnitzer C, Macklon KT, Ifversen MR, Birkebæk N, Clausen N et al. Cryopreservation of ovarian tissue for fertility preservation in a large cohort of young girls: focus on pubertal development. Hum Reprod 2017; 32: 154–164.

    CAS  PubMed  Google Scholar 

  68. Poirot C, Abirached F, Prades M, Coussieu C, Bernaudin F, Piver P . Induction of puberty by autograft of cryopreserved ovarian tissue. Lancet 2012; 379: 588.

    Article  PubMed  Google Scholar 

  69. von Wolff M, Stute P, Flück C . Autologous transplantation of cryopreserved ovarian tissue to induce puberty-the endocrinologists' view. Eur J Pediatr 2016; 175: 2007–2010.

    Article  CAS  PubMed  Google Scholar 

  70. Rovó 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: 1100–1105.

    Article  CAS  PubMed  Google Scholar 

  71. Wilhelmsson M, Vatanen A, Borgström 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.

    Article  CAS  PubMed  Google Scholar 

  72. Frey Tirri B, Häusermann P, Bertz H, Greinix H, Lawitschka A, Schwarze C-P et al. Clinical guidelines for gynecologic care after hematopoietic SCT. Report from the international consensus project on clinical practice in chronic GVHD. Bone Marrow Transplant 2015; 50: 3–9.

    Article  CAS  PubMed  Google Scholar 

  73. Salooja N, Szydlo RM, Socié G, Rio B, Chatterjee R, Ljungman P et al. Pregnancy outcomes after peripheral blood or bone marrow transplantation: a retrospective survey. Lancet 2001; 358: 271–276.

    Article  CAS  PubMed  Google Scholar 

  74. 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: 157–166.

    Article  PubMed  Google Scholar 

  75. van Dorp W, Mulder RL, Kremer LC, Hudson MM, van den Heuvel-Eibrink MM, van den Berg MH et al. Recommendations for Premature Ovarian Insufficiency Surveillance for Female Survivors of Childhood, Adolescent, and Young Adult Cancer: A Report From the International Late Effects of Childhood Cancer Guideline Harmonization Group in Collaboration With the PanCareSurFup Consortium. J Clin Oncol 2016; 34: 3440–3450.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Cui L, Gao X, Lu J, Geng L, Ding L, Qu Z et al. Anti-Müllerian hormone: correlation with age and androgenic and metabolic factors in women from birth to postmenopause. Fertil Steril 2016; 105: 481–485.

    Article  CAS  PubMed  Google Scholar 

  77. Hagen CP, Aksglaede L, Sørensen K, Main KM, Boas M, Cleemann L et al. Serum levels of anti-Müllerian hormone as a marker of ovarian function in 926 healthy females from birth to adulthood and in 172 Turner syndrome patients. J Clin Endocrinol Metab 2010; 95: 5003–5010.

    Article  CAS  PubMed  Google Scholar 

  78. Kelsey TW, Anderson RA, Wright P, Nelson SM, Wallace WH . Data-driven assessment of the human ovarian reserve. Mol Hum Reprod 2012; 18: 79–87.

    Article  CAS  PubMed  Google Scholar 

  79. Jeffery A, Streeter AJ, Hosking J, Wilkin TJ, Nelson SM . Anti-Müllerian hormone in children: a ten-year prospective longitudinal study (EarlyBird 39). J Pediatr Endocrinol Metab 2015; 28: 1153–1162.

    Article  CAS  PubMed  Google Scholar 

  80. Brougham MF, Crofton PM, Johnson EJ, Evans N, Anderson RA, Wallace WH . Anti-Müllerian hormone is a marker of gonadotoxicity in pre- and post-pubertal girls treated for cancer: a prospective study. J Clin Endocrinol Metab 2012; 97: 2059–2067.

    Article  CAS  PubMed  Google Scholar 

  81. Maheshwari A, McLernon D, Bhattacharya S . Cumulative live birth rate: time for a consensus? Hum Reprod 2015; 30: 2703–2707.

    PubMed  Google Scholar 

  82. Provoost V, Tilleman K, D'Angelo A, De Sutter P, de Wert G, Nelen W et al. Beyond the dicotomy: a tool for distinguishing between experimental, innovative and established treatment. Hum Reprod 2014; 29: 413–417.

    Article  PubMed  Google Scholar 

  83. Woodward B, Tomlinson M, Kirkman-Brown J . Replacing IUI with IVF for initial treatment of unexplained infertility: why this NICE recommendation is cause for concern. Hum Fertil (Camb) 2016; 19: 80–84.

    Article  Google Scholar 

  84. Rienzi L, Romano S, Albricci L, Maggiulli R, Capalbo A, Baroni E et al. Embryo development of fresh 'versus' vitrified metaphase II oocytes after ICSI: a prospective randomized sibling-oocyte study. Hum Reprod 2010; 25: 66–73.

    Article  PubMed  Google Scholar 

  85. Perrard MH, Sereni N, Schluth-Bolard C, Blondet A, D Estaing SG, Plotton I et al. Complete human and rat ex vivo spermatogenesis from fresh or frozen testicular tissue. Biol Reprod 2016; 95: 89.

    Article  CAS  PubMed  Google Scholar 

  86. Paramanantham J, Talmor AJ, Osianlis T, Weston GC . Cryopreserved oocytes: update on clinical applications and success rates. Obstet Gynecol Surv 2015; 70: 97–114.

    Article  PubMed  Google Scholar 

  87. Diesch T, Rovo A, von der Weid N, Faraci M, Pillon M, Dalissier A et al. Fertility preservation practices in pediatric and adolescent cancer patients undergoing HSCT in Europe: a population-based survey. Biol Reprod 2016; 89: 1–10.

    Google Scholar 

  88. von Wolff M, Dian D . Fertility preservation in women with malignant tumors and gonadotoxic treatments. Dtsch Arztebl Int 2012; 109: 220–226.

    PubMed  PubMed Central  Google Scholar 

  89. Alvarez RM, Ramanathan P . Fertility preservation in female oncology patients: the influence of the type of cancer on ovarian stimulation response. Hum Reprod (e-pub ahead of print 1 July 2016; pii: dew158).

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We thank Francesca Fossati and Andreina di Palma for secretarial support.

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Balduzzi, A., Dalle, JH., Jahnukainen, K. 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 52, 1406–1415 (2017). https://doi.org/10.1038/bmt.2017.147

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