Skip to main content

Ovarian Tissue Cryopreservation: Slow Freezing

  • Chapter
  • First Online:
Gonadal Tissue Cryopreservation in Fertility Preservation

Abstract

The needs for fertility preservation (FP) have substantially increased due to improvements in early diagnosis and survival of many malignancies experienced during the last decades. Different FP options can be offered nowadays, but ovarian tissue cryopreservation and retransplantation is the preferred option in prepubertal girls or when there is an urgent need to start the treatment (no time for ovarian stimulation). In this chapter, the basic principles of cryopreservation will be reviewed. A comprehensive and clinical practice-oriented description of the retrieval, preparation, and slow-freezing procedure of the tissue will be provided, together with a summary of the cryopreservation protocols that have been proven to be effective by obtaining live births.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Linabery AM, Ross JA (2008) Childhood and adolescent cancer survival in the US by race and ethnicity for the diagnostic period 1975–1999. Cancer 113(9):2575–2596

    Article  PubMed  PubMed Central  Google Scholar 

  2. Gnerlich JL, Deshpande AD, Jeffe DB, Sweet A, White N, Margenthaler JA (2009) Elevated breast cancer mortality in women younger than age 40 years compared with older women is attributed to poorer survival in early-stage disease. J Am Coll Surg 208(3):341–347

    Article  PubMed  PubMed Central  Google Scholar 

  3. Jemal A, Clegg LX, Ward E, Ries LA, Wu X, Jamison PM et al (2004) Annual report to the nation on the status of cancer, 1975–2001, with a special feature regarding survival. Cancer 101(1):3–27

    Article  PubMed  Google Scholar 

  4. Marhhom E, Cohen I (2007) Fertility preservation options for women with malignancies. Obstet Gynecol Surv 62(1):58–72

    Article  PubMed  Google Scholar 

  5. Bleyer WA (1990) The impact of childhood cancer on the United States and the world. CA Cancer J Clin 40(6):355–367

    Article  CAS  PubMed  Google Scholar 

  6. Meirow D, Dor J, Kaufman B, Shrim A, Rabinovici J, Schiff E et al (2007) Cortical fibrosis and blood-vessels damage in human ovaries exposed to chemotherapy. Potential mechanisms of ovarian injury. Hum Reprod 22(6):1626–1633

    Article  CAS  PubMed  Google Scholar 

  7. Kiserud CE, Fossa A, Holte H, Fossa SD (2007) Post-treatment parenthood in Hodgkin’s lymphoma survivors. Br J Cancer 96(9):1442–1449

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Familiari G, Caggiati A, Nottola SA, Ermini M, Di Benedetto MR, Motta PM (1993) Ultrastructure of human ovarian primordial follicles after combination chemotherapy for Hodgkin’s disease. Hum Reprod 8(12):2080–2087

    CAS  PubMed  Google Scholar 

  9. Kalich-Philosoph L, Roness H, Carmely A, Fishel-Bartal M, Ligumsky H, Paglin S et al (2013) Cyclophosphamide triggers follicle activation and “burnout”; AS101 prevents follicle loss and preserves fertility. Sci Transl Med [Research Support, Non-US Gov’t] 5(185):185ra62

    Google Scholar 

  10. Meirow D, Baum M, Yaron R, Levron J, Hardan I, Schiff E et al (2007) Ovarian tissue cryopreservation in hematologic malignancy: ten years’ experience. Leuk Lymphoma 48(8):1569–1576

    Article  PubMed  Google Scholar 

  11. Chiarelli AM, Marrett LD, Darlington G (1999) Early menopause and infertility in females after treatment for childhood cancer diagnosed in 1964–1988 in Ontario Canada. Am J Epidemiol 150(3):245–254

    Article  CAS  PubMed  Google Scholar 

  12. Wallace WH, Thomson AB, Kelsey TW (2003) The radiosensitivity of the human oocyte. Hum Reprod 18(1):117–121

    Article  CAS  PubMed  Google Scholar 

  13. Grigsby PW, Herzog TJ (2001) Current management of patients with invasive cervical carcinoma. Clin Obstet Gynecol 44(3):531–537

    Article  CAS  PubMed  Google Scholar 

  14. Gill S, Blackstock AW, Goldberg RM (2007) Colorectal cancer. Mayo Clin Proc 82(1):114–129

    Article  CAS  PubMed  Google Scholar 

  15. Tauchmanova L, Selleri C, Rosa GD, Pagano L, Orio F, Lombardi G et al (2002) High prevalence of endocrine dysfunction in long-term survivors after allogeneic bone marrow transplantation for hematologic diseases. Cancer 95(5):1076–1084

    Article  PubMed  Google Scholar 

  16. Linch DC, Gosden RG, Tulandi T, Tan SL, Hancock SL (2000) Hodgkin’s lymphoma: choice of therapy and late complications. Hematol Am Soc Hematol Educ Program 205–221

    Google Scholar 

  17. Burdach S, van Kaick B, Laws HJ, Ahrens S, Haase R, Korholz D et al (2000) Allogeneic and autologous stem-cell transplantation in advanced Ewing tumors. An update after long-term follow-up from two centers of the European Intergroup study EICESS. Stem-Cell Transplant Programs at Dusseldorf University Medical Center, Germany and St. Anna Kinderspital, Vienna, Austria. Ann Oncol 11(11):1451–1462

    Article  CAS  PubMed  Google Scholar 

  18. Wu HY, Snyder HM 3rd, D’Angio GJ (2005) Wilms’ tumor management. Curr Opin Urol 15(4):273–276

    Article  PubMed  Google Scholar 

  19. Spreafico F, Bellani FF (2006) Wilms’ tumor: past, present and (possibly) future. Expert Rev Anticancer Ther 6(2):249–258

    Article  PubMed  Google Scholar 

  20. Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y (2009) Orthotopic and heterotopic ovarian tissue transplantation. Hum Reprod Update [Research Support, Non-US Gov’t Review] 15(6):649–665

    Article  CAS  Google Scholar 

  21. Practice Committee of American Society for Reproductive M (2013) Fertility preservation in patients undergoing gonadotoxic therapy or gonadectomy: a committee opinion. Fertil Steril [Practice Guideline] 100(5):1214–1223

    Article  Google Scholar 

  22. von Wolff M, Thaler CJ, Frambach T, Zeeb C, Lawrenz B, Popovici RM et al. (2009) Ovarian stimulation to cryopreserve fertilized oocytes in cancer patients can be started in the luteal phase. Fertil Steril 92(4):1360–1365

    Google Scholar 

  23. Maman E, Meirow D, Brengauz M, Raanani H, Dor J, Hourvitz A (2011) Luteal phase oocyte retrieval and in vitro maturation is an optional procedure for urgent fertility preservation. Fertil Steril 95(1):64–67

    Article  PubMed  Google Scholar 

  24. Fadini R, Mignini Renzini M, Dal Canto M, Epis A, Crippa M, Caliari I et al (2013) Oocyte in vitro maturation in normo-ovulatory women. Fertil Steril [Review] 99(5):1162–1169

    Article  Google Scholar 

  25. Shaw JM, Jones GM (2003) Terminology associated with vitrification and other cryopreservation procedures for oocytes and embryos. Hum Reprod Update 9(6):583–605

    Article  CAS  PubMed  Google Scholar 

  26. Kuwayama M (2007) Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method. Theriogenology 67(1):73–80

    Article  CAS  PubMed  Google Scholar 

  27. Mazur P (1970) Cryobiology: the freezing of biological systems. Science 168(3934):939–949

    Article  CAS  PubMed  Google Scholar 

  28. Sun WQ (1999) State and phase transition behaviors of Quercus rubra seed axes and cotyledonary tissues: relevance to the desiccation sensitivity and cryopreservation of recalcitrant seeds. Cryobiology 38(4):372–385

    Article  PubMed  Google Scholar 

  29. Liebermann J (2002) Potential importance of vitrification in reproductive medicine. Biol Reprod 67(6):1671–1680

    Article  CAS  PubMed  Google Scholar 

  30. Muldrew K, McGann LE (1990) Mechanisms of intracellular ice formation. Biophys J 57(3):525–532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Mazur P (1990) Equilibrium, quasi-equilibrium, and nonequilibrium freezing of mammalian embryos. Cell Biophys 17(1):53–92

    Article  CAS  PubMed  Google Scholar 

  32. Shaw JM, Oranratnachai A, Trounson AO (2000) Fundamental cryobiology of mammalian oocytes and ovarian tissue. Theriogenology 53(1):59–72

    Article  CAS  PubMed  Google Scholar 

  33. Whittingham DG, Leibo SP, Mazur P (1972) Survival of mouse embryos frozen to −196 and −269 C. Science 178(4059):411–414

    Article  CAS  PubMed  Google Scholar 

  34. Demeestere I, Simon P, Buxant F, Robin V, Fernandez SA, Centner J et al (2006) 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 21(8):2010–2014

    Article  PubMed  Google Scholar 

  35. Shaw JM, Kola I, MacFarlane DR, Trounson AO (1991) An association between chromosomal abnormalities in rapidly frozen 2-cell mouse embryos and the ice-forming properties of the cryoprotective solution. Reproduction 91(1):9–18

    Article  CAS  Google Scholar 

  36. Arav A, Natan Y (2009) Directional freezing: a solution to the methodological challenges to preserve large organs. Semin Reprod Med 27(06):438–442

    Article  PubMed  Google Scholar 

  37. Wowk B (2010) Thermodynamic aspects of vitrification. Cryobiology 60(1):11–22

    Article  CAS  PubMed  Google Scholar 

  38. Fahy GM (2010) Cryoprotectant toxicity neutralization. Cryobiology 60(3):S45–S53

    Article  CAS  PubMed  Google Scholar 

  39. Karlsson JOM, Toner M (1996) Long-term storage of tissues by cryopreservation: critical issues. Biomaterials 17(3):243–256

    Article  CAS  PubMed  Google Scholar 

  40. Acker JP, Elliott JAW, McGann LE (2001) Intercellular ice propagation: experimental evidence for ice growth through membrane pores. Biophys J 81(3):1389–1397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Beckmann J, Körber C, Rau G, Hubel A, Cravalho EG (1990) Redefining cooling rate in terms of ice front velocity and thermal gradient: first evidence of relevance to freezing injury of lymphocytes. Cryobiology 27(3):279–287

    Article  CAS  PubMed  Google Scholar 

  42. Hubel A, Cravalho EG, Nunner B, Körber C (1992) Survival of directionally solidified B-lymphoblasts under various crystal growth conditions. Cryobiology 29(2):183–198

    Article  CAS  PubMed  Google Scholar 

  43. Rall WF, Reid DS, Polge C (1984) Analysis of slow-warming injury of mouse embryos by cryomicroscopical and physiochemical methods. Cryobiology 21(1):106–121

    Article  CAS  PubMed  Google Scholar 

  44. Gougeon A (1996) Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev 17(2):121–155

    Article  CAS  PubMed  Google Scholar 

  45. Qu J, Godin PA, Nisolle M, Donnez J (2000) Distribution and epidermal growth factor receptor expression of primordial follicles in human ovarian tissue before and after cryopreservation. Hum Reprod 15(2):302–310

    Article  CAS  PubMed  Google Scholar 

  46. Picton HM, Harris SE, Muruvi W, Chambers EL (2008) The in vitro growth and maturation of follicles. Reproduction 136(6):703–715

    Article  CAS  PubMed  Google Scholar 

  47. Thomas FH, Walters KA, Telfer EE (2003) How to make a good oocyte: an update on in-vitro models to study follicle regulation. Hum Reprod Update 9(6):541–555

    Article  PubMed  Google Scholar 

  48. Zuckerman S (1951) The number of oocytes in the mature ovary. Recent Prog Horm Res 6:63–108

    Google Scholar 

  49. Tingen CM, Bristol-Gould SK, Kiesewetter SE, Wellington JT, Shea L, Woodruff TK (2009) Prepubertal primordial follicle loss in mice is not due to classical apoptotic pathways. Biol Reprod 81(1):16–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Hardy K, Wright CS, Franks S, Winston RM (2000) In vitro maturation of oocytes. Br Med Bull 56(3):588–602

    Article  CAS  PubMed  Google Scholar 

  51. Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR, Klein NA (2008) A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod 23(3):699–708

    Article  PubMed  Google Scholar 

  52. Macklon NS, Fauser BC (1999) Aspects of ovarian follicle development throughout life. Horm Res 52(4):161–170

    Article  CAS  PubMed  Google Scholar 

  53. Greenwald GS (1972) Of eggs and follicles. Am J Anat 135(1):1–3

    Article  CAS  PubMed  Google Scholar 

  54. Lass A (2004) Assessment of ovarian reserve: is there still a role for ovarian biopsy in the light of new data? Hum Reprod [Review] 19(3):467–469

    Article  Google Scholar 

  55. Kohl J, Dittrich R, Siebzehnrübl E, Wildt L (2000) Determination of follicle numbers in human ovarian biopsies—a method for estimation of outcome of ovarian cryopreservation? Fertil Steril 74(3):1

    Article  Google Scholar 

  56. Poirot C, Vacher-Lavenu MC, Helardot P, Guibert J, Brugieres L, Jouannet P (2002) Human ovarian tissue cryopreservation: indications and feasibility. Hum Reprod 17(6):1447–1452

    Article  PubMed  Google Scholar 

  57. Schmidt KL, Byskov AG, Nyboe Andersen A, Muller J, Yding Andersen C (2003) Density and distribution of primordial follicles in single pieces of cortex from 21 patients and in individual pieces of cortex from three entire human ovaries. Hum Reprod 18(6):1158–1164

    Article  CAS  PubMed  Google Scholar 

  58. Kristensen SG, Rasmussen A, Byskov AG, Andersen CY (2011) Isolation of pre-antral follicles from human ovarian medulla tissue. Hum Reprod [Research Support, Non-US Gov’t] 26(1):157–166

    Google Scholar 

  59. Kagawa N, Kuwayama M, Nakata K, Vajta G, Silber S, Manabe N et al (2007) Production of the first offspring from oocytes derived from fresh and cryopreserved pre-antral follicles of adult mice. Reprod Biomed Online 14(6):693–699

    Article  PubMed  Google Scholar 

  60. Shimizu T, Jiang JY, Iijima K, Miyabayashi K, Ogawa Y, Sasada H et al (2003) Induction of follicular development by direct single injection of vascular endothelial growth factor gene fragments into the ovary of miniature gilts. Biol Reprod 69(4):1388–1393

    Article  CAS  PubMed  Google Scholar 

  61. Nunez Valera MJ, Padilla Iserte P, Higueras Garcia G, Herraiz S, Rubio JM, Romeu Villarroya M et al (2015) Single site laparoscopy for fertility preservation: a cohort study. J Minim Invasive Gynecol 22(2):291–296

    Article  PubMed  Google Scholar 

  62. Rosendahl M, Schmidt KT, Ernst E, Rasmussen PE, Loft A, Byskov AG et al (2011) Cryopreservation of ovarian tissue for a decade in Denmark: a view of the technique. Reprod Biomed Online [Historical Article Research Support, Non-US Gov’t] 22(2):162–171

    Google Scholar 

  63. Silber S, Kagawa N, Kuwayama M, Gosden R (2010) Duration of fertility after fresh and frozen ovary transplantation. Fertil Steril 94(6):2191–2196

    Article  PubMed  Google Scholar 

  64. Donnez J, Dolmans MM, Pellicer A, Diaz-Garcia C, Sanchez Serrano M, Schmidt KT et al (2013) Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertil Steril 99(6):1503–1513

    Article  PubMed  Google Scholar 

  65. Jadoul P, Dolmans MM, Donnez J (2010) Fertility preservation in girls during childhood: is it feasible, efficient and safe and to whom should it be proposed? Hum Reprod Update [Research Support, Non-US Gov’t Review] 16(6):617–630

    Article  Google Scholar 

  66. Rosendahl M, Andersen CY, Ernst E, Westergaard LG, Rasmussen PE, Loft A et al (2008) Ovarian function after removal of an entire ovary for cryopreservation of pieces of cortex prior to gonadotoxic treatment: a follow-up study. Hum Reprod 23(11):2475–2483

    Article  PubMed  Google Scholar 

  67. Cursio R, Colosetti P (2015) Autophagy and liver ischemia-reperfusion injury. Biomed Res Int 2015:417590

    Google Scholar 

  68. Gonzalez LM, Moeser AJ, Blikslager AT (2015) Animal models of ischemia-reperfusion-induced intestinal injury: progress and promise for translational research. Am J Physiol Gastrointest Liver Physiol 308(2):G63–G75

    Article  CAS  PubMed  Google Scholar 

  69. Hilbert T, Klaschik S (2015) The angiopoietin/TIE receptor system: focusing its role for ischemia-reperfusion injury. Cytokine Growth Factor Rev 26(3):281–291

    Article  CAS  PubMed  Google Scholar 

  70. Ibanez B, Heusch G, Ovize M, Van de Werf F (2015) Evolving therapies for myocardial ischemia/reperfusion injury. BioMed Res Int 65(14):1454–1471

    Google Scholar 

  71. Salvadori M, Rosso G, Bertoni E (2015) Update on ischemia-reperfusion injury in kidney transplantation: pathogenesis and treatment. World J Trans 5(2):52–67

    Google Scholar 

  72. Donnez J, Dolmans MM, Pellicer A, Diaz-Garcia C, Ernst E, Macklon KT et al (2015) Fertility preservation for age-related fertility decline. Lancet [Comment Letter] 385(9967):506–507

    Article  Google Scholar 

  73. Dittrich R, Lotz L, Keck G, Hoffmann I, Mueller A, Beckmann MW et al (2012) Live birth after ovarian tissue autotransplantation following overnight transportation before cryopreservation. Fertil Steril 97(2):387–390

    Article  PubMed  Google Scholar 

  74. Baird DT, Webb R, Campbell BK, Harkness LM, Gosden RG (1999) Long-term ovarian function in sheep after ovariectomy and transplantation of autografts stored at -196 C. Endocrinology 140(1):462–471

    CAS  PubMed  Google Scholar 

  75. Gavish Z, Ben-Haim M, Arav A (2008) Cryopreservation of whole murine and porcine livers. Rejuvenation Res 11(4):765–772

    Article  PubMed  Google Scholar 

  76. Gavish Z, Peer G, Roness H, Cohen Y, Meirow D (2014) Follicle activation and ‘burn-out’ contribute to post-transplantation follicle loss in ovarian tissue grafts: the effect of graft thickness. Hum Reprod [Research Support, Non-US Gov’t] 29(5):989–996

    Google Scholar 

  77. Kagawa N, Silber S, Kuwayama M (2009) Successful vitrification of bovine and human ovarian tissue. Reprod Biomed Online 18(4):568–577

    Article  PubMed  Google Scholar 

  78. Gosden RG, Baird DT, Wade JC, Webb R (1994) Restoration of fertility to oophorectomized sheep by ovarian autografts stored at -196 degrees C. Hum Reprod 9(4):597–603

    CAS  PubMed  Google Scholar 

  79. Silber SJ, DeRosa M, Pineda J, Lenahan K, Grenia D, Gorman K et al (2008) A series of monozygotic twins discordant for ovarian failure: ovary transplantation (cortical versus microvascular) and cryopreservation. Hum Reprod 23(7):1531–1537

    Article  CAS  PubMed  Google Scholar 

  80. Arav A, Zeron Y, Leslie SB, Behboodi E, Anderson GB, Crowe JH (1996) Phase transition temperature and chilling sensitivity of bovine oocytes. Cryobiology 33(6):589–599

    Article  CAS  PubMed  Google Scholar 

  81. Silber SJ, Grudzinskas G, Gosden RG (2008) Successful pregnancy after microsurgical transplantation of an intact ovary. N Engl J Med 359(24):2617–2618

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  83. Callejo J, Salvador C, Miralles A, Vilaseca S, Lailla JM, Balasch J (2001) Long-term ovarian function evaluation after autografting by implantation with fresh and frozen-thawed human ovarian tissue. J Clin Endocrinol Metab 86(9):4489–4494

    Article  CAS  PubMed  Google Scholar 

  84. Gook DA, McCully BA, Edgar DH, McBain JC (2001) Development of antral follicles in human cryopreserved ovarian tissue following xenografting. Hum Reprod 16(3):417–422

    Article  CAS  PubMed  Google Scholar 

  85. Oktay K, Buyuk E, Veeck L, Zaninovic N, Xu K, Takeuchi T et al (2004) Embryo development after heterotopic transplantation of cryopreserved ovarian tissue. Lancet 363(9412):837–840

    Article  PubMed  Google Scholar 

  86. Meirow D, Levron J, Eldar-Geva T, Hardan I, Fridman E, Zalel Y et al (2005) Pregnancy after transplantation of cryopreserved ovarian tissue in a patient with ovarian failure after chemotherapy. N Engl J Med 353(3):318–321

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  88. Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S et al (2013) Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci U S A 110(43):17474–17479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Parkes AS (1953) Conservation of gonadal tissue for transplantation. Acta Physiol Lat Am 3(2–3):158–161

    CAS  PubMed  Google Scholar 

  90. Parkes AS (1956) Grafting of mouse ovarian tissue after freezing and thawing. J Endocrinol 14(3):xxx-–xxxi

    CAS  PubMed  Google Scholar 

  91. Parkes AS (1956) Survival time of ovarian homografts in two strains of rats. J Endocrinol 13(2):201–210

    Article  CAS  PubMed  Google Scholar 

  92. Parkes AS (1957) Viability of ovarian tissue after freezing. Proc R Soc Lond Ser B Biol Sci 147(929):520–528

    Article  CAS  Google Scholar 

  93. Parkes AS, Smith AU (1953) Regeneration of rat ovarian tissue grafted after exposure to low temperatures. Proc R Soc Lond Ser B Biol Sci 140(901):455–470

    Article  CAS  Google Scholar 

  94. Baird DT, Campbell B, de Souza C, Telfer E (2004) Long-term ovarian function in sheep after ovariectomy and autotransplantation of cryopreserved cortical strips. Eur J Obstet Gynecol Reprod Biol 113(Suppl 1):S55–S59

    Article  PubMed  Google Scholar 

  95. Radford JA, Lieberman BA, Brison DR, Smith AR, Critchlow JD, Russell SA et al (2001) Orthotopic reimplantation of cryopreserved ovarian cortical strips after high-dose chemotherapy for Hodgkin’s lymphoma. Lancet 357(9263):1172–1175

    Article  CAS  PubMed  Google Scholar 

  96. Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J et al (2004) Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet 364(9443):1405–1410

    Article  CAS  PubMed  Google Scholar 

  97. Donnez J, Dolmans MM (2015) Ovarian cortex transplantation: 60 reported live births brings the success and worldwide expansion of the technique towards routine clinical practice. J Assist Reprod Genet 32:1167–1170. doi:10.1007/s10815-015-0544-9

    Google Scholar 

  98. Ashwood-Smith MJ (1986) The cryopreservation of human embryos. Hum Reprod 1(5):319–332

    CAS  PubMed  Google Scholar 

  99. Hovatta O (2005) Methods for cryopreservation of human ovarian tissue. Reprod Biomed Online 10(6):729–734

    Article  PubMed  Google Scholar 

  100. Gandolfi F, Paffoni A, Papasso Brambilla E, Bonetti S, Brevini TA, Ragni G (2006) Efficiency of equilibrium cooling and vitrification procedures for the cryopreservation of ovarian tissue: comparative analysis between human and animal models. Fertil Steril 85(Suppl 1):1150–1156

    Article  PubMed  Google Scholar 

  101. Huang L, Mo Y, Wang W, Li Y, Zhang Q, Yang D (2008) Cryopreservation of human ovarian tissue by solid-surface vitrification. Eur J Obstet Gynecol Reprod Biol 139(2):193–198

    Article  CAS  PubMed  Google Scholar 

  102. Isachenko V, Isachenko E, Rahimi G, Krivokharchenko A, Alabart JL, Nawroth F (2002) Cryopreservation of human ovarian tissue by direct plunging into liquid nitrogen: negative effect of disaccharides in vitrification solution. Cryo Lett 23(5):333–344

    CAS  Google Scholar 

  103. Isachenko E, Isachenko V, Rahimi G, Nawroth F (2003) Cryopreservation of human ovarian tissue by direct plunging into liquid nitrogen. Eur J Obstet Gynecol Reprod Biol 108(2):186–193

    Article  CAS  PubMed  Google Scholar 

  104. Rahimi G, Isachenko E, Sauer H, Isachenko V, Wartenberg M, Hescheler J et al (2003) Effect of different vitrification protocols for human ovarian tissue on reactive oxygen species and apoptosis. Reprod Fertil Dev 15(6):343–349

    Article  PubMed  Google Scholar 

  105. Isachenko V, Isachenko E, Reinsberg J, Montag M, van der Ven K, Dorn C et al (2007) Cryopreservation of human ovarian tissue: comparison of rapid and conventional freezing. Cryobiology 55(3):261–268

    Article  CAS  PubMed  Google Scholar 

  106. Isachenko V, Isachenko E, Reinsberg J, Montag M, Weiss J, Braun F et al (2008) Simplified technique of human ovarian tissue freezing: quick cooling from -36 degree C. Cryo Lett 29(3):261–268

    CAS  Google Scholar 

  107. Isachenko V, Isachenko E, Reinsberg J, Montag M, Braun F, van der Ven H (2008) Cryopreservation of human ovarian tissue: effect of spontaneous and initiated ice formation. Reprod Biomed Online 16(3):336–345

    Article  PubMed  Google Scholar 

  108. Newton H, Aubard Y, Rutherford A, Sharma V, Gosden R (1996) Low temperature storage and grafting of human ovarian tissue. Hum Reprod 11(7):1487–1491

    Article  CAS  PubMed  Google Scholar 

  109. Newton H, Fisher J, Arnold JR, Pegg DE, Faddy MJ, Gosden RG (1998) Permeation of human ovarian tissue with cryoprotective agents in preparation for cryopreservation. Hum Reprod 13(2):376–380

    Article  CAS  PubMed  Google Scholar 

  110. Candy CJ, Wood MJ, Whittingham DG (1997) Effect of cryoprotectants on the survival of follicles in frozen mouse ovaries. J Reprod Fertil 110(1):11–19

    Article  CAS  PubMed  Google Scholar 

  111. Herraiz S, Novella-Maestre E, Rodriguez B, Diaz C, Sanchez-Serrano M, Mirabet V et al (2014) Improving ovarian tissue cryopreservation for oncologic patients: slow freezing versus vitrification, effect of different procedures and devices. Fertil Steril 101(3):775–784

    Article  CAS  PubMed  Google Scholar 

  112. Sanchez M, Novella-Maestre E, Teruel J, Ortiz E, Pellicer A (2008) The Valencia Programme for fertility preservation. Clin Trans Oncol: Off Publ Fed Span Oncol Soc Natl Cancer Inst Mex 10(7):433–438

    Article  CAS  Google Scholar 

  113. Amorim CA, David A, Van Langendonckt A, Dolmans MM, Donnez J (2011) Vitrification of human ovarian tissue: effect of different solutions and procedures. Fertil Steril 95(3):1094–1097

    Article  CAS  PubMed  Google Scholar 

  114. Fahy GM, Wowk B, Wu J, Paynter S (2004) Improved vitrification solutions based on the predictability of vitrification solution toxicity. Cryobiology 48(1):22–35

    Article  CAS  PubMed  Google Scholar 

  115. Gook DA, Edgar DH, Stern C (2004) Cryopreservation of human ovarian tissue. Eur J Obstet Gynecol Reprod Biol 113(Suppl 1):S41–S44

    Article  CAS  PubMed  Google Scholar 

  116. Gook DA, Edgar DH, Stern C (2000) The effects of cryopreservation regimens on the morphology of human ovarian tissue. Mol Cell Endocrinol 169(1–2):99–103

    Article  CAS  PubMed  Google Scholar 

  117. Keros V, Xella S, Hultenby K, Pettersson K, Sheikhi M, Volpe A et al (2009) Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue. Hum Reprod 24(7):1670–1683

    Article  CAS  PubMed  Google Scholar 

  118. Hovatta O, Silye R, Krausz T, Abir R, Margara R, Trew G et al (1996) Cryopreservation of human ovarian tissue using dimethylsulphoxide and propanediol-sucrose as cryoprotectants. Hum Reprod 11(6):1268–1272

    Article  CAS  PubMed  Google Scholar 

  119. Maltaris T, Koelbl H, Fischl F, Seufert R, Schmidt M, Kohl J et al (2006) Xenotransplantation of human ovarian tissue pieces in gonadotropin-stimulated SCID mice: the effect of ovariectomy. Anticancer Res 26(6B):4171–4176

    PubMed  Google Scholar 

  120. Chen SU, Chien CL, Wu MY, Chen TH, Lai SM, Lin CW et al (2006) Novel direct cover vitrification for cryopreservation of ovarian tissues increases follicle viability and pregnancy capability in mice. Hum Reprod 21(11):2794–2800

    Article  PubMed  Google Scholar 

  121. Oktem O, Alper E, Balaban B, Palaoglu E, Peker K, Karakaya C et al (2011) Vitrified human ovaries have fewer primordial follicles and produce less antimullerian hormone than slow-frozen ovaries. Fertil Steril 95(8):2661–2664, e1

    Article  PubMed  Google Scholar 

  122. Sheikhi M, Hultenby K, Niklasson B, Lundqvist M, Hovatta O (2011) Clinical grade vitrification of human ovarian tissue: an ultrastructural analysis of follicles and stroma in vitrified tissue. Hum Reprod 26(3):594–603

    Article  PubMed  PubMed Central  Google Scholar 

  123. Zhou XH, Wu YJ, Shi J, Xia YX, Zheng SS (2010) Cryopreservation of human ovarian tissue: comparison of novel direct cover vitrification and conventional vitrification. Cryobiology 60(2):101–105

    Article  CAS  PubMed  Google Scholar 

  124. Mazoochi T, Salehnia M, Valojerdi MR, Mowla SJ (2008) Morphologic, ultrastructural, and biochemical identification of apoptosis in vitrified-warmed mouse ovarian tissue. Fertil Steril 90(4 Suppl):1480–1486

    Article  PubMed  Google Scholar 

  125. Suzuki N, Yoshioka N, Takae S, Sugishita Y, Tamura M, Hashimoto S et al (2015) Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod [Research Support, Non-US Gov’t] 30(3):608–615

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  127. Revel A, Laufer N, Ben Meir A, Lebovich M, Mitrani E (2011) Micro-organ ovarian transplantation enables pregnancy: a case report. Hum Reprod 26(5):1097–1103

    Article  PubMed  Google Scholar 

  128. Andersen CY, Rosendahl M, Byskov AG, Loft A, Ottosen C, Dueholm M et al (2008) Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Hum Reprod 23(10):2266–2272

    Article  PubMed  Google Scholar 

  129. Rodriguez-Wallberg KA, Karlstrom PO, Rezapour M, Castellanos E, Hreinsson J, Rasmussen C et al (2015) 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 [Case Reports Research Support, Non-US Gov’t] 94(3):324–328

    Article  Google Scholar 

  130. Gook DA, Edgar DH, Stern C (1999) Effect of cooling rate and dehydration regimen on the histological appearance of human ovarian cortex following cryopreservation in 1, 2-propanediol. Hum Reprod 14(8):2061–2068

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cesar Diaz-Garcia .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Japan

About this chapter

Cite this chapter

Herraiz, S., Diaz-Garcia, C., Pellicer, A. (2016). Ovarian Tissue Cryopreservation: Slow Freezing. In: Suzuki, N., Donnez, J. (eds) Gonadal Tissue Cryopreservation in Fertility Preservation. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55963-4_4

Download citation

  • DOI: https://doi.org/10.1007/978-4-431-55963-4_4

  • Published:

  • Publisher Name: Springer, Tokyo

  • Print ISBN: 978-4-431-55961-0

  • Online ISBN: 978-4-431-55963-4

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics