Fresh Ovarian Tissue and Whole Ovary Transplantation

ABSTRACT

A series of monozygotic (MZ) twin pairs discordant for premature ovarian failure presented an unusual opportunity to study ovarian transplantation. Ten MZ twin pairs requested ovarian transplantation and nine have undergone transplantation with cryopreservation of spare tissue. Eight had a fresh cortical tissue transplant, one of whom received a second frozen-thawed transplant after the first ceased functioning at 3 years. One had a fresh microvascular transplant. All recipients reinitiated ovulatory menstrual cycles and normal day 3 serum follicle-stimulating hormone levels by 77 to 142 days. Seven have already conceived naturally (three twice). Currently, seven healthy infants have been delivered out of 10 pregnancies. The oldest transplant ceased functioning by 3 years, but then she conceived again after a frozen-thawed secondary transplant. There was no apparent difference in return of ovarian function between the nine fresh ovarian grafts and the one frozen graft. Ovarian transplantation appears to restore ovulatory function robustly. Ten pregnancies, leading to seven healthy infants, including one after cryopreservation, bode well for application to fertility preservation.

KEYWORDS

Cryopreservation - fertility - menopause - monozygotic twins - ovary transplantation

REFERENCES

• 1 Silber S J, Lenahan K M, Levine D J et al.. Ovarian transplantation between monozygotic twins discordant for premature ovarian failure.  N Engl J Med. 2005;  353(1) 58-63
• 2 Gosden R G, Baird D T, Wade J C, Webb R. Restoration of fertility to oophorectomized sheep by ovarian autografts stored at −196 degrees C.  Hum Reprod. 1994;  9(4) 597-603
• 3 Silber S J, Gosden R G. Ovarian transplantation in a series of monozygotic twins discordant for ovarian failure.  N Engl J Med. 2007;  356(13) 1382-1384
• 4 Silber S J, DeRosa M, Pineda J et al.. A series of monozygotic twins discordant for ovarian failure: ovary transplantation (cortical versus microvascular) and cryopreservation.  Hum Reprod. 2008;  23(7) 1531-1537
• 5 Silber S J, Grudzinskas G, Gosden R G. Successful pregnancy after microsurgical transplantation of an intact ovary.  N Engl J Med. 2008;  359(24) 2617-2618
• 6 Coulam C B, Adamson S C, Annegers J F. Incidence of premature ovarian failure.  Obstet Gynecol. 1986;  67(4) 604-606
• 7 Riboli E, Hunt K J, Slimani N et al.. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection.  Public Health Nutr. 2002;  5(6B) 1113-1124
• 8 Luborsky J L, Meyer P, Sowers M F, Gold E B, Santoro N. Premature menopause in a multi-ethnic population study of the menopause transition.  Hum Reprod. 2003;  18(1) 199-206
• 9 Goswami D, Conway G S. Premature ovarian failure.  Hum Reprod Update. 2005;  11(4) 391-410
• 10 Snieder H, MacGregor A J, Spector T D. Genes control the cessation of a woman's reproductive life: a twin study of hysterectomy and age at menopause.  J Clin Endocrinol Metab. 1998;  83(6) 1875-1880
• 11 de Bruin J P, Bovenhuis H, van Noord P A et al.. The role of genetic factors in age at natural menopause.  Hum Reprod. 2001;  16(9) 2014-2018
• 12 van Asselt K M, Kok H S, Pearson P L et al.. Heritability of menopausal age in mothers and daughters.  Fertil Steril. 2004;  82(5) 1348-1351
• 13 Bedaiwy M A, Falcone T. Harvesting and autotransplantation of vascularized ovarian grafts: approaches and techniques.  Reprod Biomed Online. 2007;  14(3) 360-371
• 14 Silber S J. Transplantation of a human testis for anorchia.  Fertil Steril. 1978;  30(2) 181-187
• 15 Gosden R G, Telfer E, Faddy M J, Brook D J. Ovarian cyclicity and follicular recruitment in unilaterally ovariectomized mice.  J Reprod Fertil. 1989;  87(1) 257-264
• 16 Faddy M J, Gosden R G, Gougeon A, Richardson S J, Nelson J F. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause.  Hum Reprod. 1992;  7(10) 1342-1346
• 17 Newton H, Aubard Y, Rutherford A, Sharma V, Gosden R. Low temperature storage and grafting of human ovarian tissue.  Hum Reprod. 1996;  11(7) 1487-1491
• 18 Gook D A, Edgar D H, Stern C. Effect of cooling rate and dehydration regimen on the histological appearance of human ovarian cortex following cryopreservation in 1, 2-propanediol.  Hum Reprod. 1999;  14(8) 2061-2068
• 19 Gosden R G, Treloar S A, Martin N G et al.. Prevalence of premature ovarian failure in monozygotic and dizygotic twins.  Hum Reprod. 2007;  22(2) 610-615
• 20 Dueck A, Poenaru D, Jamieson M A, Kamal I K. Unilateral ovarian agenesis and fallopian tube maldescent.  Pediatr Surg Int. 2001;  17(2-3) 228-229
• 21 Su L L. Monoamniotic twins: diagnosis and management.  Acta Obstet Gynecol Scand. 2002;  81(11) 995-1000
• 22 Weksberg R, Shuman C, Caluseriu O et al.. Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith-Wiedemann syndrome.  Hum Mol Genet. 2002;  11(11) 1317-1325
• 23 Oktay K, Economos K, Kan M, Rucinski J, Veeck L, Rosenwaks Z. Endocrine function and oocyte retrieval after autologous transplantation of ovarian cortical strips to the forearm.  JAMA. 2001;  286(12) 1490-1493
• 24 Salle B, Demirci B, Franck M, Rudigoz R C, Guerin J F, Lornage J. Normal pregnancies and live births after autograft of frozen-thawed hemi-ovaries into ewes.  Fertil Steril. 2002;  77(2) 403-408
• 25 Donnez J, Dolmans M M, Demylle D et al.. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue.  Lancet. 2004;  364(9443) 1405-1410
• 26 Meirow D, Levron J, Eldar-Geva T et al.. Pregnancy after transplantation of cryopreserved ovarian tissue in a patient with ovarian failure after chemotherapy.  N Engl J Med. 2005;  353(3) 318-321
• 27 Kagawa N, Silber S, Kuwayama M. Successful vitrification of bovine and human ovarian tissue.  Reprod Biomed Online. 2009;  18 568-577
• 28 Hilders C G, Baranski A G, Peters L, Ramkhelawan A, Trimbos J B. Successful human ovarian autotransplantation to the upper arm.  Cancer. 2004;  101(12) 2771-2778
• 29 Kim S S, Hwang I T, Lee H C. Heterotopic autotransplantation of cryobanked human ovarian tissue as a strategy to restore ovarian function.  Fertil Steril. 2004;  82(4) 930-932
• 30 Oktay K, Buyuk E, Veeck L et al.. Embryo development after heterotopic transplantation of cryopreserved ovarian tissue.  Lancet. 2004;  363(9412) 837-840
• 31 Rosendahl M, Loft A, Byskov A G et al.. Biochemical pregnancy after fertilization of an oocyte aspirated from a heterotopic autotransplant of cryopreserved ovarian tissue: case report.  Hum Reprod. 2006;  21(8) 2006-2009
• 32 Wang X, Chen H, Yin H, Kim S S, Lin Tan S, Gosden R G. Fertility after intact ovary transplantation.  Nature. 2002;  415(6870) 385
• 33 Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results.  Hum Reprod. 1986;  1(2) 81-87
• 34 Donnez J, Martinez-Madrid B, Jadoul P, Van Langendonckt A, Demylle D, Dolmans M M. Ovarian tissue cryopreservation and transplantation: a review.  Hum Reprod Update. 2006;  12(5) 519-535
• 35 Donnez J, Dolmans M M, Pirard C et al.. Allograft of ovarian cortex between two genetically non-identical sisters: case report.  Hum Reprod. 2007;  22(10) 2653-2659
• 36 Mhatre P, Mhatre J, Magotra R. Ovarian transplant: a new frontier.  Transplant Proc. 2005;  37(2) 1396-1398
• 37 Armenti V T, Radomski J S, Moritz M J, Philips L Z, McGrory C H, Coscia L A. Report from the National Transplantation Pregnancy Registry (NTPR): outcomes of pregnancy after transplantation.  Clin Transpl. 2000;  123-134
• 38 Andersen C Y, Rosendahl M, Byskov A G et al.. Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue.  Hum Reprod. 2008;  23(10) 2266-2272
• 39 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) 1437-1442