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Transplantation of frozen-thawed ovarian tissue: an update on worldwide activity published in peer-reviewed papers and on the Danish cohort

  • Fertility Preservation
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

The purpose of the study is to review all peer-reviewed published reports of women receiving ovarian tissue transplantation (OTT) with frozen/thawed tissue (OTC) with respect to age, diagnosis, transplantation site, fertility outcome, and potential side effects, including data from all women in the Danish program.

Methods

A systematic review of the literature was performed in PubMed combined with results from all patients who had received OTT in Denmark up to December 2017.

Results

OTT has been reported from 21 different countries comprising a total of 360 OTT procedures in 318 women. In nine women, malignancy was diagnosed after OTT; none were considered to be directly caused by the OTT. Despite a potential under reporting of cancer recurrence, there is currently no evidence to suggest that OTT causes reseeding of the original cancer. Renewed ovarian endocrine function was reported in 95% of the women. Half of all children born following OTT resulted from natural conception, and newborns were reported to be healthy except for one neonate with a chromosome anomaly with a family disposition. Women who conceived after OTT were significantly younger than those who failed.

Conclusion

This study found no indications of sufficient numbers of malignant cells present in the ovarian tissue to cause recurrence of cancer after OTT. Further, it is unlikely that OTC affects the well-being of children born. OTC is now an established method of fertility preservation in Denmark with public reimbursement. The current data encourage that women who require gonadotoxic treatment should be offered an individual evaluation considering fertility preservation.

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References

  1. Jensen AK, Macklon KT, Fedder J, Ernst E, Humaidan P, Andersen CY. 86 successful births and 9 ongoing pregnancies worldwide in women transplanted with frozen-thawed ovarian tissue: focus on birth and perinatal outcome in 40 of these children. J Assist Reprod Genet. 2017;34(3):325–36.

    Article  PubMed  Google Scholar 

  2. Donnez J, Dolmans MM. Fertility preservation in women. N Engl J Med. 2017;377(17):1657–65.

    Article  PubMed  Google Scholar 

  3. Rosendahl M, Greve T, Andersen CY. The safety of transplanting cryopreserved ovarian tissue in cancer patients: a review of the literature. J Assist Reprod Genet. 2013;30(1):11–24.

    Article  PubMed  Google Scholar 

  4. Kim SS, Donnez J, Barri P, Pellicer A, Patrizio P, Rosenwaks Z, et al. Recommendations for fertility preservation in patients with lymphoma, leukemia, and breast cancer. J Assist Reprod Genet. 2012;29(6):465–8.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Schmidt KT, Andersen CY. Recommendations for fertility preservation in patients with lymphomas. J Assist Reprod Genet. 2012;29(6):473–7.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Greve T, Wielenga VT, Grauslund M, Sorensen N, Christiansen DB, Rosendahl M, et al. Ovarian tissue cryopreserved for fertility preservation from patients with Ewing or other sarcomas appear to have no tumour cell contamination. Eur J Cancer (Oxf, Engl: 1990). 2013;49(8):1932–8.

    Article  Google Scholar 

  7. Greve T, Clasen-Linde E, Andersen MT, Andersen MK, Sorensen SD, Rosendahl M, et al. Cryopreserved ovarian cortex from patients with leukemia in complete remission contains no apparent viable malignant cells. Blood. 2012;120(22):4311–6.

    Article  CAS  PubMed  Google Scholar 

  8. Dolmans MM, Luyckx V, Donnez J, Andersen CY, Greve T. Risk of transferring malignant cells with transplanted frozen-thawed ovarian tissue. Fertil Steril. 2013;99(6):1514–22.

    Article  PubMed  Google Scholar 

  9. Soares M, Saussoy P, Sahrari K, Amorim CA, Donnez J, Dolmans MM. Is transplantation of a few leukemic cells inside an artificial ovary able to induce leukemia in an experimental model? J Assist Reprod Genet. 2015;32(4):597–606.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Shapira M, Raanani H, Barshack I, Amariglio N, Derech-Haim S, Marciano MN, et al. First delivery in a leukemia survivor after transplantation of cryopreserved ovarian tissue, evaluated for leukemia cells contamination. Fertil Steril. 2017;

  11. Silber S. How ovarian transplantation works and how resting follicle recruitment occurs: a review of results reported from one center. Women's Health (Lond Engl). 2016;12(2):217–27.

    Article  CAS  Google Scholar 

  12. Dittrich R, Hackl J, Lotz L, Hoffmann I, Beckmann MW. Pregnancies and live births after 20 transplantations of cryopreserved ovarian tissue in a single center. Fertil Steril. 2015;103(2):462–8.

    Article  PubMed  Google Scholar 

  13. Schmidt KT, Rosendahl M, Ernst E, Loft A, Andersen AN, Dueholm M, et al. Autotransplantation of cryopreserved ovarian tissue in 12 women with chemotherapy-induced premature ovarian failure: the Danish experience. Fertil Steril. 2011;95(2):695–701.

    Article  PubMed  Google Scholar 

  14. 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(2):467–74.

    Article  PubMed  Google Scholar 

  15. Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S, et al. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci U S A. 2013;110(43):17474–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Suzuki N, Yoshioka N, Takae S, Sugishita Y, Tamura M, Hashimoto S, et al. Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod (Oxf, Engl). 2015;30(3):608–15.

    Article  Google Scholar 

  17. Zhai J, Yao G, Dong F, Bu Z, Cheng Y, Sato Y, et al. In vitro activation of follicles and fresh tissue auto-transplantation in primary ovarian insufficiency patients. J Clin Endocrinol Metab. 2016;101(11):4405–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lorenzo FVM, Buzzi PJ, Marconi G, Tiberon M, Young ET. Live birth with intrauterine insemination (IUH) after orthotopic transplantation of cryopreserved ovarian tissue in a young patient previously treated with chemotherapy for a skin’s disease. Argentina e160 ASRM Abstracts. Fertil Steril. 2014;102(3 Suppl):64.

    Google Scholar 

  19. Lorenzo FVM, Viola J, Tiveron M, Young E. Second children born after autotransplantation of cryopreserved ovarian tissue in a young patient previously treated with chemotherapy for Askin’s disease. The successful of fertility preservation program. Fertil Steril. 2016;106(suppl 3):e29.

    Article  Google Scholar 

  20. Stern CJ, Gook D, Hale LG, Agresta F, Oldham J, Rozen G, et al. Delivery of twins following heterotopic grafting of frozen-thawed ovarian tissue. Hum Reprod (Oxf Engl). 2014;29(8):1828.

    Article  CAS  Google Scholar 

  21. Stern CJ, Gook D, Hale LG, Agresta F, Oldham J, Rozen G, et al. First reported clinical pregnancy following heterotopic grafting of cryopreserved ovarian tissue in a woman after a bilateral oophorectomy. Hum Reprod (Oxf Engl). 2013;28(11):2996–9.

    Article  CAS  Google Scholar 

  22. Burmeister L, Kovacs GT, Osianlis T. First Australian pregnancy after ovarian tissue cryopreservation and subsequent autotransplantation. Med J Aust. 2013;198(3):158–9.

    Article  PubMed  Google Scholar 

  23. Stern CJ, Toledo MG, Hale LG, Gook DA, Edgar DH. The first Australian experience of heterotopic grafting of cryopreserved ovarian tissue: evidence of establishment of normal ovarian function. Aust N Z J Obstet Gynaecol. 2011;51(3):268–75.

    Article  PubMed  Google Scholar 

  24. Rozen G, Agresta F, Gook D, Braat D, Stern CJ. Success and challenges in fertility preservation after ovarian tissue grafting. Lancet (Lond, Engl). 2015;385(9981):1947.

    Article  Google Scholar 

  25. Stern K RG, Gook D, Agresta F, Braat D, Hale L. Are there factors which predict the success of ovarian tissue grafting in oncofertility patients? Abstract presented at: 32nd Annual Meeting of the European Society of Human Reproduction and Embryology.3–6 July, 2016; Helsinki, Finland.

  26. Donnez J, Dolmans MM, Pellicer A, Diaz-Garcia C, Sanchez Serrano M, Schmidt KT, et al. Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertil Steril. 2013;99(6):1503–13.

    Article  PubMed  Google Scholar 

  27. Imbert R, Moffa F, Tsepelidis S, Simon P, Delbaere A, Devreker F, et al. Safety and usefulness of cryopreservation of ovarian tissue to preserve fertility: a 12-year retrospective analysis. Hum Reprod (Oxf Engl). 2014;29(9):1931–40.

    Article  CAS  Google Scholar 

  28. Donnez J, Dolmans MM, Diaz C, Pellicer A. Ovarian cortex transplantation: time to move on from experimental studies to open clinical application. Fertil Steril. 2015;104(5):1097–8.

    Article  PubMed  Google Scholar 

  29. Lambertini M, Goldrat O, Ferreira AR, Dechene J, Azim HA Jr, Desir J, et al. Reproductive potential and performance of fertility preservation strategies in BRCA-mutated breast cancer patients. Ann Oncol: Off J Eur Soc Med Oncol. 2017;29(1):237–43.

    Article  Google Scholar 

  30. Donnez J, Jadoul P, Pirard C, Hutchings G, Demylle D, Squifflet J, et al. Live birth after transplantation of frozen-thawed ovarian tissue after bilateral oophorectomy for benign disease. Fertil Steril. 2012;98(3):720–5.

    Article  PubMed  Google Scholar 

  31. Donnez J, Silber S, Andersen CY, Demeestere I, Piver P, Meirow D, et al. Children born after autotransplantation of cryopreserved ovarian tissue. A review of 13 live births. Ann Med. 2011;43(6):437–50.

    Article  PubMed  Google Scholar 

  32. 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 (Oxf, Engl). 2015;30(9):2107–9.

    Article  Google Scholar 

  33. Demeestere I, Simon P, Buxant F, Robin V, Fernandez SA, Centner J, et al. Ovarian function and spontaneous pregnancy after combined heterotopic and orthotopic cryopreserved ovarian tissue transplantation in a patient previously treated with bone marrow transplantation: case report. Hum Reprod (Oxf Engl). 2006;21(8):2010–4.

    Article  Google Scholar 

  34. Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Fertility preservation: successful transplantation of cryopreserved ovarian tissue in a young patient previously treated for Hodgkin’s disease. Oncologist. 2007;12(12):1437–42.

    Article  PubMed  Google Scholar 

  35. Demeestere I, Simon P, Moffa F, Delbaere A, Englert Y. Birth of a second healthy girl more than 3 years after cryopreserved ovarian graft. Hum Reprod (Oxf, Engl). 2010;25(6):1590–1.

    Article  CAS  Google Scholar 

  36. Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet (Lond Engl). 2004;364(9443):1405–10.

    Article  CAS  Google Scholar 

  37. Jadoul P, Guilmain A, Squifflet J, Luyckx M, Votino R, Wyns C, et al. Efficacy of ovarian tissue cryopreservation for fertility preservation: lessons learned from 545 cases. Hum Reprod (Oxf Engl). 2017;32(5):1046–54.

    Article  CAS  Google Scholar 

  38. Donnez J, Squifflet J, Jadoul P, Demylle D, Cheron AC, Van Langendonckt A, et al. Pregnancy and live birth after autotransplantation of frozen-thawed ovarian tissue in a patient with metastatic disease undergoing chemotherapy and hematopoietic stem cell transplantation. Fertil Steril. 2011;95(5):1787.e1–4.

    Article  Google Scholar 

  39. Donnez J, Martinez-Madrid B, Jadoul P, Van Langendonckt A, Demylle D, Dolmans MM. Ovarian tissue cryopreservation and transplantation: a review. Hum Reprod Update. 2006;12(5):519–35.

    Article  PubMed  Google Scholar 

  40. Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Restoration of ovarian function after orthotopic (intraovarian and periovarian) transplantation of cryopreserved ovarian tissue in a woman treated by bone marrow transplantation for sickle cell anaemia: case report. Hum Reprod (Oxf Engl). 2006;21(1):183–8.

    Article  CAS  Google Scholar 

  41. Donnez J, Squifflet J, Van Eyck AS, Demylle D, Jadoul P, Van Langendonckt A, et al. Restoration of ovarian function in orthotopically transplanted cryopreserved ovarian tissue: a pilot experience. Reprod BioMed Online. 2008;16(5):694–704.

    Article  CAS  PubMed  Google Scholar 

  42. Janse F, Donnez J, Anckaert E, de Jong FH, Fauser BC, Dolmans MM. Limited value of ovarian function markers following orthotopic transplantation of ovarian tissue after gonadotoxic treatment. J Clin Endocrinol Metab. 2011;96(4):1136–44.

    Article  CAS  PubMed  Google Scholar 

  43. Dolmans MM, Donnez J, Camboni A, Demylle D, Amorim C, Van Langendonckt A, et al. IVF outcome in patients with orthotopically transplanted ovarian tissue. Hum Reprod (Oxf Engl). 2009;24(11):2778–87.

    Article  Google Scholar 

  44. Hulsbosch S, Koskas M, Tomassetti C, De Sutter P, Wildiers H, Neven P, et al. A real-life analysis of reproductive outcome after fertility preservation in female cancer patients. Gynecol Obstet Investig. 2017.

  45. Donnez J, Dolmans MM, Pellicer A, Diaz-Garcia C, Ernst E, Macklon KT, et al. Fertility preservation for age-related fertility decline. Lancet (Lond Engl). 2015;385(9967):506–7.

    Article  Google Scholar 

  46. 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 ReProduct (Oxf Engl). 2015;30(12):2838–45.

    Article  CAS  Google Scholar 

  47. Ernst EH, Offersen BV, Andersen CY, Ernst E. Legal termination of a pregnancy resulting from transplanted cryopreserved ovarian tissue due to cancer recurrence. J Assist Reprod Genet. 2013;30(7):975–8.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Ernst E, Kjaersgaard M, Birkebaek NH, Clausen N, Andersen CY. Case report: stimulation of puberty in a girl with chemo- and radiation therapy induced ovarian failure by transplantation of a small part of her frozen/thawed ovarian tissue. Eur J Cancer (Oxf Engl: 1990). 2013;49(4):911–4.

    Article  Google Scholar 

  49. Yding Andersen C, Ernst E, Baerentzen S, Birkebaek NH, Clausen N. No malignancy detected in surplus ovarian tissue from a former Ewing sarcoma patient who experienced relapse four years after being grafted with frozen/thawed ovarian tissue. J Assist Reprod Genet. 2014;31(11):1567–8.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Andersen CY, Silber SJ, Bergholdt SH, Jorgensen JS, Ernst E. Long-term duration of function of ovarian tissue transplants: case reports. Reprod BioMed Online. 2012;25(2):128–32.

    Article  PubMed  Google Scholar 

  51. Greve T, Ernst E, Markholt S, Schmidt KT, Andersen CY. Legal termination of a pregnancy resulting from transplanted cryopreserved ovarian tissue. Acta Obstet Gynecol Scand. 2010;89(12):1589–91.

    Article  PubMed  Google Scholar 

  52. Schmidt KL, Andersen CY, Loft A, Byskov AG, Ernst E, Andersen AN. Follow-up of ovarian function post-chemotherapy following ovarian cryopreservation and transplantation. Hum Reprod (Oxf Engl). 2005;20(12):3539–46.

    Article  CAS  Google Scholar 

  53. Rosendahl M, Loft A, Byskov AG, Ziebe S, Schmidt KT, Andersen AN, et al. Biochemical pregnancy after fertilization of an oocyte aspirated from a heterotopic autotransplant of cryopreserved ovarian tissue: case report. Hum Reprod (Oxf Engl). 2006;21(8):2006–9.

    Article  CAS  Google Scholar 

  54. Andersen CY, Rosendahl M, Byskov AG, Loft A, Ottosen C, Dueholm M, et al. Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Hum Reprod (Oxf Engl). 2008;23(10):2266–72.

    Article  Google Scholar 

  55. Macklon KT, Jensen AK, Loft A, Ernst E, Andersen CY. Treatment history and outcome of 24 deliveries worldwide after autotransplantation of cryopreserved ovarian tissue, including two new Danish deliveries years after autotransplantation. J Assist Reprod Genet. 2014;31(11):1557–64.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Ernst E, Bergholdt S, Jorgensen JS, Andersen CY. The first woman to give birth to two children following transplantation of frozen/thawed ovarian tissue. Hum Reproduct (Oxf Engl). 2010;25(5):1280–1.

    Article  Google Scholar 

  57. Rodriguez-Wallberg KA, Tanbo T, Tinkanen H, Thurin-Kjellberg A, Nedstrand E, Kitlinski ML, et al. Ovarian tissue cryopreservation and transplantation among alternatives for fertility preservation in the Nordic countries—compilation of 20 years of multicenter experience. Acta Obstet Gynecol Scand. 2016;95(9):1015–26.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Fajau-Prevot C, Le Gac YT, Chevreau C, Cohade C, Gatimel N, Parinaud J, et al. Ovarian mucinous cystadenoma after ovarian graft. Obstet Gynecol. 2017;129(6):1035–6.

    Article  PubMed  Google Scholar 

  59. Poirot C, Abirached F, Prades M, Coussieu C, Bernaudin F, Piver P. Induction of puberty by autograft of cryopreserved ovarian tissue. Lancet (Lond Engl). 2012;379(9815):588.

    Article  Google Scholar 

  60. Roux C, Amiot C, Agnani G, Aubard Y, Rohrlich PS, Piver P. Live birth after ovarian tissue autograft in a patient with sickle cell disease treated by allogeneic bone marrow transplantation. Fertil Steril. 2010;93(7):2413.e15–9.

    Article  Google Scholar 

  61. Dittrich R, Mueller A, Maltaris T, Hoffmann I, Magener A, Oppelt PG, et al. Hormonal and histologic findings in human cryopreserved ovarian autografts. Fertil Steril. 2009;91(4 Suppl):1503–6.

    Article  PubMed  Google Scholar 

  62. Dittrich R, Mueller A, Binder H, Oppelt PG, Renner SP, Goecke T, et al. First retransplantation of cryopreserved ovarian tissue following cancer therapy in Germany. Deutsch Arztebl Int. 2008;105(15):274–8.

    Google Scholar 

  63. Muller A, Keller K, Wacker J, Dittrich R, Keck G, Montag M, et al. Retransplantation of cryopreserved ovarian tissue: the first live birth in Germany. Deutsch Arztebl Int. 2012;109(1–2):8–13.

    Google Scholar 

  64. Van der Ven H, Liebenthron J, Beckmann M, Toth B, Korell M, Krussel 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 (Oxf Engl). 2016;31(9):2031–41.

    Article  Google Scholar 

  65. Isachenko V, Orth I, Isachenko E, Mallmann P, Peters D, Schmidt T, et al. Viability of human ovarian tissue confirmed 5 years after freezing with spontaneous ice-formation by autografting and chorio-allantoic membrane culture. Cryobiology. 2013;66(3):233–8.

    Article  PubMed  Google Scholar 

  66. Meirow D, Levron J, Eldar-Geva T, Hardan I, Fridman E, Yemini Z, et al. Monitoring the ovaries after autotransplantation of cryopreserved ovarian tissue: endocrine studies, in vitro fertilization cycles, and live birth. Fertil Steril. 2007;87(2):418.e7–e15.

    Article  Google Scholar 

  67. Meirow D, Levron J, Eldar-Geva T, Hardan I, Fridman E, Zalel Y, et al. Pregnancy after transplantation of cryopreserved ovarian tissue in a patient with ovarian failure after chemotherapy. N Engl J Med. 2005;353(3):318–21.

    Article  CAS  PubMed  Google Scholar 

  68. Revel A, Laufer N, Ben Meir A, Lebovich M, Mitrani E. Micro-organ ovarian transplantation enables pregnancy: a case report. Hum Reprod (Oxf Engl). 2011;26(5):1097–103.

    Article  Google Scholar 

  69. Azem FAA, Vagman I, Mey Raz N, Ben-Yosef D, Lessing J. Successful pregnancy and birth following avascular micro ovarian tissue orthotopic transplantation in a patient with Hodgkin disease. Scientific Congress Supplement: oral and poster abstracts. Fertil Steril. 2012;98(3):S95–6.

    Article  Google Scholar 

  70. Fabbri R, Pasquinelli G, Magnani V, Macciocca M, Vicenti R, Parazza I, et al. Autotransplantation of cryopreserved ovarian tissue in oncological patients: recovery of ovarian function. Future Oncol (Lond Engl). 2014;10(4):549–61.

    Article  CAS  Google Scholar 

  71. Revelli A, Marchino G, Dolfin E, Molinari E, Delle Piane L, Salvagno F, et al. Live birth after orthotopic grafting of autologous cryopreserved ovarian tissue and spontaneous conception in Italy. Fertil Steril. 2013;99(1):227–30.

    Article  PubMed  Google Scholar 

  72. Tanbo T, Greggains G, Storeng R, Busund B, Langebrekke A, Fedorcsak P. Autotransplantation of cryopreserved ovarian tissue after treatment for malignant disease—the first Norwegian results. Acta Obstet Gynecol Scand. 2015;94(9):937–41.

    Article  PubMed  Google Scholar 

  73. Radwan P, Abramik A, Wilczynski J, Radwan M. Successful autotransplantation of cryopreserved ovarian tissue with recovery of the ovarian function. Ginekol Pol. 2016;87(3):235–40.

    Article  PubMed  Google Scholar 

  74. Povoa A, Xavier P, Calejo L, Soares S, Sousa M, Silva J, et al. First transplantation of cryopreserved ovarian tissue in Portugal, stored for 10 years: an unexpected indication. Reprod BioMed Online. 2016;32(3):334–6.

    Article  PubMed  Google Scholar 

  75. Kiseleva M, Malinova I, Komarova E, Shvedova T, Chudakov K. The Russian experience of autotransplantation of vitrified ovarian tissue to a cancer patient. Gynecological Endocrinol. 2014;30(Suppl 1):30–1.

    Article  Google Scholar 

  76. Filatov MA, Khramova YV, Kiseleva MV, Malinova IV, Komarova EV, Semenova ML. Female fertility preservation strategies: cryopreservation and ovarian tissue in vitro culture, current state of the art and future perspectives. Zygote (Cambridge, England). 2016;24(5):635–53.

    Article  CAS  Google Scholar 

  77. Kim SS, Hwang IT, Lee HC. Heterotopic autotransplantation of cryobanked human ovarian tissue as a strategy to restore ovarian function. Fertil Steril. 2004;82(4):930–2.

    Article  PubMed  Google Scholar 

  78. Sanchez-Serrano M, Crespo J, Mirabet V, Cobo AC, Escriba MJ, Simon C, et al. Twins born after transplantation of ovarian cortical tissue and oocyte vitrification. Fertil Steril. 2010;93(1):268.e11–3.

    Article  Google Scholar 

  79. Callejo J, Salvador C, Gonzalez-Nunez S, Almeida L, Rodriguez L, Marques L, et al. Live birth in a woman without ovaries after autograft of frozen-thawed ovarian tissue combined with growth factors. J Ovarian Res. 2013;6(1):33.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Sanchez M, Novella-Maestre E, Teruel J, Ortiz E, Pellicer A. The Valencia Programme for fertility preservation. Clin Transl Oncol. 2008;10(7):433–8.

    Article  CAS  PubMed  Google Scholar 

  81. Callejo J, Salvador C, Miralles A, Vilaseca S, Lailla JM, Balasch J. Long-term ovarian function evaluation after autografting by implantation with fresh and frozen-thawed human ovarian tissue. J Clin Endocrinol Metab. 2001;86(9):4489–94.

    Article  CAS  PubMed  Google Scholar 

  82. Rodriguez-Wallberg KA, Karlstrom PO, Rezapour M, Castellanos E, Hreinsson J, Rasmussen C, et al. Full-term newborn after repeated ovarian tissue transplants in a patient treated for Ewing sarcoma by sterilizing pelvic irradiation and chemotherapy. Acta Obstet Gynecol Scand. 2015;94(3):324–8.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Milenkovic M, Brannstrom M, Diaz-Garcia C, Lundin K, Selleskog U, Soderlund B, et al. Spontaneous twin pregnancy with live births after cryopreservation and re-implantation of ovarian tissue. Gynecol Surg. 2017;14(1):9.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Wolner-Hanssen P, Hagglund L, Ploman F, Ramirez A, Manthorpe R, Thuring A. Autotransplantation of cryopreserved ovarian tissue to the right forearm 4(1/2) years after autologous stem cell transplantation. Acta Obstet Gynecol Scand. 2005;84(7):695–8.

    PubMed  Google Scholar 

  85. Akar ME, Carrillo AJ, Jennell JL, Yalcinkaya TM. Robotic-assisted laparoscopic ovarian tissue transplantation. Fertil Steril. 2011;95(3):1120.e5–8.

    Article  Google Scholar 

  86. Dunlop CE, Brady BM, McLaughlin M, Telfer EE, White J, Cowie F, et al. Re-implantation of cryopreserved ovarian cortex resulting in restoration of ovarian function, natural conception and successful pregnancy after haematopoietic stem cell transplantation for Wilms tumour. J Assist Reprod Genet. 2016;33(12):1615–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Radford JA, Lieberman BA, Brison DR, Smith AR, Critchlow JD, Russell SA, et al. Orthotopic reimplantation of cryopreserved ovarian cortical strips after high-dose chemotherapy for Hodgkin’s lymphoma. Lancet (Lond Engl). 2001;357(9263):1172–5.

    Article  CAS  Google Scholar 

  88. Kim SS. Assessment of long term endocrine function after transplantation of frozen-thawed human ovarian tissue to the heterotopic site: 10 year longitudinal follow-up study. J Assist Reprod Genet. 2012;29(6):489–93.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Oktay K, Karlikaya G. Ovarian function after transplantation of frozen, banked autologous ovarian tissue. N Engl J Med. 2000;342(25):1919.

    Article  CAS  PubMed  Google Scholar 

  90. Oktay K, Oktem O. Ovarian cryopreservation and transplantation for fertility preservation for medical indications: report of an ongoing experience. Fertil Steril. 2010;93(3):762–8.

    Article  PubMed  Google Scholar 

  91. Pacheco F, Oktay K. Current success and efficiency of autologous ovarian transplantation: a meta-analysis. Reprod Sci (Thousand Oaks, Calif). 2017;24(8):1111–20.

    Article  Google Scholar 

  92. Oktay K, Buyuk E, Veeck L, Zaninovic N, Xu K, Takeuchi T, et al. Embryo development after heterotopic transplantation of cryopreserved ovarian tissue. Lancet (Lond Engl). 2004;363(9412):837–40.

    Article  Google Scholar 

  93. Oktay K. Spontaneous conceptions and live birth after heterotopic ovarian transplantation: is there a germline stem cell connection? Hum Reprod (Oxf Engl). 2006;21(6):1345–8.

    Article  Google Scholar 

  94. Oktay K, Bedoschi G, Pacheco F, Turan V, Emirdar V. First pregnancies, live birth, and in vitro fertilization outcomes after transplantation of frozen-banked ovarian tissue with a human extracellular matrix scaffold using robot-assisted minimally invasive surgery. Am J Obstet Gynecol. 2016;214(1):94.e1–9.

    Article  Google Scholar 

  95. Oktay K, Taylan E, Sugishita Y, Goldberg GM. Robot-assisted laparoscopic transplantation of frozen-thawed ovarian tissue. J Minim Invasive Gynecol. 2017;24(6):897–8.

    Article  PubMed  Google Scholar 

  96. Silber S, Pineda J, Lenahan K, DeRosa M, Melnick J. Fresh and cryopreserved ovary transplantation and resting follicle recruitment. Reprod BioMed Online. 2015;30(6):643–50.

    Article  PubMed  Google Scholar 

  97. Silber S. Chapter 13 human ovarian tissue vitrification. Methods Mol Biol (Clifton, NJ). 2017;1568:177–94.

    Article  Google Scholar 

  98. Silber S, Kagawa N, Kuwayama M, Gosden R. Duration of fertility after fresh and frozen ovary transplantation. Fertil Steril. 2010;94(6):2191–6.

    Article  PubMed  Google Scholar 

  99. Silber S. Ovarian tissue cryopreservation and transplantation: scientific implications. J Assist Reprod Genet. 2016;33(12):1595–603.

    Article  PubMed  PubMed Central  Google Scholar 

  100. Kim SS, Lee WS, Chung MK, Lee HC, Lee HH, Hill D. Long-term ovarian function and fertility after heterotopic autotransplantation of cryobanked human ovarian tissue: 8-year experience in cancer patients. Fertil Steril. 2009;91(6):2349–54.

    Article  PubMed  Google Scholar 

  101. Greve T, Schmidt KT, Kristensen SG, Ernst E, Andersen CY. Evaluation of the ovarian reserve in women transplanted with frozen and thawed ovarian cortical tissue. Fertil Steril. 2012;97(6):1394–8.e1.

    Article  PubMed  Google Scholar 

  102. 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 

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Acknowledgements

All personnel including the clinical activities in fertility preservation are thanked for their passionate work.

Funding

The University Hospital of Copenhagen, the EU interregional project ReproUnion, and Vera and Carl Johan Michaelsens Legat are gratefully acknowledged for financial support.

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Author notes

  1. E. Ernst

    Present address: The Fertility Clinic, Horsens Regional Hospital, 8700, Horsens, Denmark

Authors and Affiliations

  1. Laboratory of Reproductive Biology, Section 5712, The Juliane Marie Centre for Women, Children and Reproduction, University Hospital of Copenhagen, Faculty of Health and Medicine, University of Copenhagen, Blegdamsvej 9, Rigshospitalet, DK-2100, Copenhagen, Denmark

    S. E. Gellert, S. E. Pors, S. G. Kristensen & C. Yding Andersen

  2. The Fertility Clinic, Aarhus University Hospital, Skejby, 8200, Aarhus, Denmark

    A. M. Bay-Bjørn & E. Ernst

Authors
  1. S. E. Gellert
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  2. S. E. Pors
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  3. S. G. Kristensen
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  4. A. M. Bay-Bjørn
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  5. E. Ernst
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  6. C. Yding Andersen
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Corresponding author

Correspondence to C. Yding Andersen.

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Gellert, S.E., Pors, S.E., Kristensen, S.G. et al. Transplantation of frozen-thawed ovarian tissue: an update on worldwide activity published in peer-reviewed papers and on the Danish cohort. J Assist Reprod Genet 35, 561–570 (2018). https://doi.org/10.1007/s10815-018-1144-2

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  • DOI: https://doi.org/10.1007/s10815-018-1144-2

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