Semin Reprod Med 2005; 23(3): 266-276
DOI: 10.1055/s-2005-872455
Copyright © 2005 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA.

Oocyte and Ovarian Tissue Cryopreservation: Indications, Techniques, and Applications

Mousa Issa Shamonki1 , 3 , Kutluk Oktay2 , 3
  • 1Fellow in Reproductive Endocrinology, The Weill Medical College of Cornell University, New York, New York
  • 2Associate Professor, The Weill Medical College of Cornell University, New York, New York
  • 3The Center for Reproductive Medicine and Infertility, The Weill Medical College of Cornell University, New York, New York
Further Information

Publication History

Publication Date:
01 August 2005 (online)

ABSTRACT

With recent advances in cryobiology, cryopreservation of the oocyte and ovarian tissue is rapidly becoming an important service provided by medical centers throughout the world. The general indication for oocyte or ovarian tissue cryopreservation is to retain future fertility potential for women who face the possibility of premature or imminent ovarian failure resulting from treatments for various disease states including cancer. Considering limitations imposed by age, lack of a partner, or sufficient time to undergo embryo cryopreservation, these patients have few options if they desire preservation of their fertility. The objective of this manuscript is to review the basic aspects of oocyte and ovarian tissue cryopreservation, and to discuss the current and future applications of these technologies in fertility preservation.

REFERENCES

  • 1 Deanesly R. Immature rat ovaries grafted after freezing and thawing.  J Endocrinol. 1954;  11 197-200
  • 2 Green S H, Smith A U, Zuckerman S. The numbers of oocytes in ovarian autografts after freezing and thawing.  J Endocrinol. 1956;  13 330-334
  • 3 Parks A S. Factors affecting the viability of frozen ovarian tissue.  J Endocrinol. 1960;  17 337-343
  • 4 Parrott D MV. The fertility of mice with orthotopic ovarian grafts derived from frozen tissue.  J Reprod Fertil. 1960;  1 230-241
  • 5 Gosden R G, Baird D T, Wade J C et al.. Restoration of fertility to oophorectomized sheep by ovarian autografts stored at -196°C.  Hum Reprod. 1994;  9 597-603
  • 6 Gunasena K T, Villines P M, Critser E S et al.. Live births after autologous transplant of cryopreserved mouse ovaries.  Hum Reprod. 1997;  12 101-106
  • 7 Sztein J, Sweet H, Farley J et al.. Cryopreservation and orthotopic transplantation of mouse ovaries: new approach in gamete banking.  Biol Reprod. 1998;  58 1071-1074
  • 8 Candy C J, Wood M J, Whittingham D G. Restoration of normal reproductive lifespan after grafting of cryopreserved mouse ovaries.  Hum Reprod. 2000;  15 1300-1304
  • 9 Shaw J M, Cox S L, Trounson A O et al.. Evaluation of the long-term function of cryopreserved ovarian grafts in the mouse, implications for human applications.  Mol Cell Endocrinol. 2000;  161 103-110
  • 10 American Cancer Society .Cancer Facts and Figures-2001. Atlanta, GA; American Cancer Society 2001
  • 11 National Cancer Institute .SEER*Stat software, version 2.0 SEER cancer incidence public-use database, 1973-1996, August 1998 submission Bethesda, MD; National Cancer Institute 1999
  • 12 Reis L AG, Percy C L, Bunin G R. Introduction. In: Reis LAG, Smith MA, Gurney JG, et al. Cancer Incidence and Survival among Children and Adolescents: United States SEER Program 1975-1995. NIH Pub. No. 99-4649 Bethesda, MD; National Cancer Institute 1999: 1-15
  • 13 Meirow D, Epstein M, Lewis H et al.. Administration of cyclophosphamide at different stages of follicular maturation in mice: effects on reproductive performance and fetal malformations.  Hum Reprod. 2001;  16 632-637
  • 14 Meirow D. Reproduction post-chemotherapy in young cancer patients.  Mol Cell Endocrinol. 2000;  169 123-131
  • 15 Practice Committee . Ovarian tissue and oocyte cryopreservation.  Fertil Steril. 2004;  82 993-998
  • 16 Porcu E, Fabbri R, Seracchiolli R et al.. Birth of a healthy female after intracytoplasmic sperm injection of cryopreserved human oocytes.  Fertil Steril. 1997;  68 724-726
  • 17 Porcu E, Fabbri R, Seracchiolli R et al.. Birth of six healthy children after intracytoplasmic sperm injection of cryopreserved human oocytes.  Hum Reprod. 1998;  13 124 , (abst)
  • 18 Antinori S, Dani G, Selman H A et al.. Pregnancies after sperm injection into cryopreserved oocytes.  Hum Reprod. 1998;  13 (suppl) 157-158 , (abst)
  • 19 Borini A, Bafaro M G, Bonu M A et al.. Pregnancies after freezing and thawing human oocytes. Preliminary data.  Hum Reprod. 1998;  13 124-125
  • 20 Polak de Fried E, Notrica J, Rubinstein M et al.. Oocyte cryopreservation program: removal vs. non removal of cumulus corona complex.  Fertil Steril. 1998;  70 S148
  • 21 Porcu E, Fabbri R, Ciotti P et al.. Four healthy children from frozen human oocytes and frozen human sperms.  Fertil Steril. 2001;  76 S76
  • 22 Winslow K, Yang D, Blohm P et al.. Oocyte cryopreservation: a three year follow up of sixteen births.  Fertil Steril. 2001;  76 S120
  • 23 Bahadur G, Steele S J. Ovarian tissue cryopreservation for patients.  Hum Reprod. 1996;  11 2215-2216
  • 24 Oktay K, Buyuk E, Veeck L et al.. Embryo development after heterotopic transplantation of cryopreserved ovarian tissue.  Lancet. 2004;  363 837-840
  • 25 Oktay K, Karlikaya G. Ovarian function after transplantation of frozen, banked autologous ovarian tissue.  N Engl J Med. 2000;  342 1919
  • 26 Poirot C, Vacher-Lavenu M C, Helardot P et al.. Human ovarian tissue cryopreservation: indications and feasibility.  Hum Reprod. 2002;  17 1447-1452
  • 27 Trounson A, Mohr L. Human pregnancy following cryopreservation, thawing and transfer of an eight-cell embryo.  Nature. 1983;  305 707-709
  • 28 Chen C. Pregnancy after human oocyte cryopreservation.  Lancet. 1986;  1 884-886
  • 29 Van Uem J FHM, Siebzehnruebl E R, Schuh B et al.. Birth after cryopreservation of unfertilized oocytes.  Lancet. 1987;  1 752-753
  • 30 Chen C. Pregnancies after human oocyte cryopreservation.  Ann N Y Acad Sci. 1988;  541 541-549
  • 31 Chian R C, Buckett W M, Tan S L. In vitro maturation of human oocytes.  Reprod Biomed Online. 2004;  8 148-166
  • 32 Chian R C, Kuwayama M, Tan L et al.. High survival rates of bovine and human oocytes matured in vitro following vitrification [abstract]. 49th Annual Meeting of the Canadian Fertility and Andrology Society. November 5-8, 2003 Victoria, British Columbia TP-23;
  • 33 Durga Rao G, Chian R C, Son W S et al.. Fertility preservation in women undergoing cancer treatment [letter].  Lancet. 2004;  363 1829-1830
  • 34 Hankey B F, Miller B, Curtis R et al.. Trends in breast cancer in younger women in contrast to older women.  J Natl Cancer Inst Monogr. 1994;  16 7-14
  • 35 Higgins S, Hafftey B G. Pregnancy and lactation after breast-conserving therapy for early stage breast cancer.  Cancer. 1994;  73 2175-2180
  • 36 Bines J, Oleske D M, Cobleigh M A. Ovarian function in premenopausal women treated with adjuvant chemotherapy for breast cancer.  J Clin Oncol. 1996;  14 1718-1729
  • 37 Hortobagyi G N. Progress in systemic chemotherapy of primary breast cancer: an overview.  J Natl Cancer Inst Monogr. 2001;  30 72-79
  • 38 National Institutes of Health Consensus Development Panel . National Institutes of Health Consensus Development Conference statement: adjuvant therapy for breast cancer; November 1-3, 2000.  J Natl Cancer Inst Monogr. 2001;  30 5-15
  • 39 Oktay K H, Buyuk E, Davis O et al.. Fertility preservation in breast cancer patients: in vitro fertilization and embryo cryopreservation after ovarian stimulation with tamoxifen.  Hum Reprod. 2003;  18 90-95
  • 40 Allred C D, Allred K F, Ju Y H et al.. Soy diets containing varying amounts of genistein stimulate growth of estrogen-dependant (MCF-7) tumors in a dose-dependent manner.  Cancer Res. 2001;  61 5045-5050
  • 41 Prest S J, May F E, Westly B R. The estrogen-regulated protein, TFF1, stimulated migration of human breast cancer cells.  FASEB J. 2002;  16 592-594
  • 42 Omland A K, Fedorcsak P, Storeng R et al.. Natural cycle IVF in unexplained, endometriosis-associated and tubal factor infertility.  Hum Reprod. 2001;  16 2587-2592
  • 43 Mitwally M F, Casper R F. Use of an aromatase inhibitor for induction of ovulation in patients with an inadequate response to clomiphene citrate.  Fertil Steril. 2001;  75 305-309
  • 44 Mitwally M F, Casper R F. Aromatase inhibition improves ovarian response to follicle-stimulating hormone in poor responders.  Fertil Steril. 2002;  77 776-780
  • 45 Mitwally M F, Casper R F. Aromatase inhibition reduces gonadotrophin dose required for controlled ovarian stimulation in women with unexplained infertility.  Hum Reprod. 2003;  18 1588-1597
  • 46 Oktay K, Buyuk E, Libertella N et al.. Fertility preservation in breast cancer patients: a prospective controlled comparison of ovarian stimulation with tamoxifen and letrozole for embryo cryopreservation.  J Clin Oncol. , In press
  • 47 Sonmezer M, Oktay K. Fertility preservation in female cancer patients: a comprehensive approach. In: Gosden RG, Tulandi T Text Book of Fertility Preservation London; Taylor and Francis 2004: 177-190
  • 48 Sonmezer M, Oktay K. Fertility preservation in female patients.  Hum Reprod Update. 2004;  10 251-266
  • 49 Oktay K, Sonmezer M. Debate - ovarian tissue banking for cancer patients: Fertility preservation, not just ovarian cryopreservation.  Human Reprod. 2004;  19 447-480
  • 50 Oktay K, Buyuk E, Rosenwaks Z. Novel use of an aromatase inhibitor for fertility preservation via embryo cryopreservation in endometrial cancer: a case report.  Fertil Steril. 2003;  80(suppl) 144 , (abst)
  • 51 Klopper A, Hall M. New synthetic agent for the induction of ovulation: preliminary trials in women.  BMJ. 1971;  1 152-154
  • 52 Jordan V C. Effect of tamoxifen (ICI 46 474) on initiation and growth of DMBA-induced rat mammary carcinomata.  Eur J Cancer. 1976;  12 419-424
  • 53 Early Breast Cancer Trialists’ Collaborative Group . Systematic treatment of early breast cancer by hormonal, cytotoxic, or immune therapy. 133 randomised trials involving 31 000 recurrences and 24 000 deaths among 75 000 women.  Lancet. 1992;  339 71-85
  • 54 Mourits M J, De Vries E G, Willemse P H et al.. Tamoxifen treatment and gynecologic side effects: a review.  Obstet Gynecol. 2001;  97 855-866
  • 55 Oktay K. Ovarian cryopreservation and transplantation: preliminary findings and implications for cancer patients.  Hum Reprod Update. 2001;  7 526-534
  • 56 Tucker M, Morton P, Liebermann J. Human oocyte cryopreservation: a valid alternative to embryo cryopreservation?.  Eur J Obstet Gynecol Reprod Biol. 2004;  113(suppl) S24-S27
  • 57 Ludwig M, Schopper B, Al-Hasani S et al.. Clinical use of a pronuclear stage score following intracytoplasmic sperm injection: impact on pregnancy rates under the conditions of the German embryo protection law.  Hum Reprod. 2000;  15 325-329
  • 58 Zollner K P, Zollner U, Steck T et al.. First experiences with human blastocyst culture after IVF/ICSI under the conditions of the German embryo protection law.  Zentralbl Gynakol. 2002;  124 164-169
  • 59 Ludwig M, Diedrich K. Regulation of assisted reproductive technology: the German experience. In: Brinsden PR A Textbook of In Vitro Fertilization and Assisted Reproduction New York; Parthenon 1999: 431-434
  • 60 Mandelbaum J, Anastasiou O, Levy R et al.. Effects of cryopreservation on the meiotic spindle of human oocytes.  Eur J Obstet Gynecol Reprod Biol. 2004;  113(suppl) S17-S23
  • 61 Wang W H, Meg L, Hackett R J et al.. Limited recovery of meiotic spindles in living human oocytes after cooling-rewarming observed using polarized light microscopy.  Hum Reprod. 2001;  16 2374-2378
  • 62 Kim N H, Chung H M, Cha K Y et al.. Microtubule and microfilament organization in maturing human oocytes.  Hum Reprod. 1998;  13 2217-2222
  • 63 Sathananthan A H, Trounson A, Freeman L et al.. The effects of cooling human oocytes.  Hum Reprod. 1988;  3 968-977
  • 64 Pickering S J, Braude P R, Johnson M H et al.. Transient cooling to room temperature can cause irreversible disruption to the meiotic spindle in human oocytes.  Fertil Steril. 1990;  54 102-108
  • 65 Almeida P A, Bolton V N. The effect of temperature fluctuations on the cytoskeletal organization and chromosomal constitution of the human oocyte.  Zygote. 1995;  3 357-365
  • 66 George M A, Pickering S J, Braude P R et al.. The distribution of α- and γ-tubulin in fresh and aged mouse and human oocytes exposed to cryoprotectant.  Mol Hum Reprod. 1996;  2 445-456
  • 67 Zenzes M T, Bielecki R, Casper R F et al.. Effects of chilling to 0 °C on the morphology of meiotic spindles in human metaphase II oocytes.  Fertil Steril. 2001;  75 769-777
  • 68 Bernard A, Fuller B J. Cryopreservation of human oocytes: a review of current problems and perspectives.  Hum Reprod Update. 1996;  2 193-207
  • 69 Aigner S, Van der Elst J, Siebzehnrubl E et al.. The influence of slow and ultra-rapid freezing on the organization of the meiotic spindle in the mouse oocyte.  Hum Reprod. 1992;  7 857-864
  • 70 Joly C, Bchini O, Boulekbache H et al.. Effects of 1,2-propanediol on the cytoskeletal organisation of the mouse oocyte.  Hum Reprod. 1992;  7 374-378
  • 71 George M A, Johnson M H. Use of fetal bovine serum substitutes for the protection of mouse zona pellucida against hardening during cryoprotectant addition.  Hum Reprod. 1993;  8 1898-1900
  • 72 Shaw J M, Oranratnachai A, Trounson A O. Fundamental cryobiology of mammalian oocytes and ovarian tissue.  Theriogenology. 2000;  53 59-72
  • 73 Baka S G, Toth T L, Veeck L L et al.. Evaluation of the spindle apparatus of in-vitro matured human oocytes following cryopreservation.  Hum Reprod. 1995;  10 1816-1820
  • 74 Matson P L, Graefling J, Junk S M et al.. Cryopreservation of oocytes and embryos: use of the mouse model to investigate effects upon zona hardness and formulate treatment strategies in an in-vitro fertilization programme.  Hum Reprod. 1997;  12 1550-1553
  • 75 Palermo G, Joris H, Devroey P et al.. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte.  Lancet. 1992;  340 17-18
  • 76 Boiso I, Marti M, Santalo J et al.. A confocal microscopy analysis of the spindle and chromosome configurations of human oocytes cryopreserved at the germinal vesicle and metaphase II stage.  Hum Reprod. 2002;  17 1885-1891
  • 77 Lucifero D, Mertineit C, Clarke H J et al.. Methylation dynamics of imprinted genes in mouse germ cells.  Genomics. 2002;  79 530-538
  • 78 Vincent C, Garnier V, Heyman Y et al.. Solvent effects on cytoskeletal organization and in-vivo survival after freezing of rabbit oocytes.  J Reprod Fertil. 1989;  87 809-820
  • 79 Eroglu A, Toth T L, Toner M. Alterations of the cytoskeleton and polyploidy induced by cryopreservation of metaphase II mouse oocytes.  Fertil Steril. 1998;  69 944-957
  • 80 Chen S U, Lien Y L, Chen H F et al.. Open pulled straws for vitrification of mature mouse oocytes preserve patterns of meiotic spindles and chromosomes better than conventional straws.  Hum Reprod. 2000;  15 2598-2603
  • 81 Park S E, Chung H M, Cha K Y, Hwang W S, Lee E S, Lim J M. Cryopreservation of ICR mouse oocytes: improved post-thawed preimplantation development after vitrification using Taxol, a cytoskeletal stabilizer.  Fertil Steril. 2001;  75 1171-1184
  • 82 Chen S U, Lien Y L, Cheng Y Y et al.. Vitrification of mouse oocytes using closed pulled straws (CPS) achieves a high survival and preserves good patterns of meiotic spindles, compared with conventional straws, open pulled straws (OPS) and grids.  Hum Reprod. 2001;  16 2350-2356
  • 83 Chen S U, Lien Y L, Chao H N et al.. Effects of cryopreservation on meiotic spindles of oocytes and its dynamics after thawing: clinical implications in oocyte freezing-a review article.  Mol Cell Endocrinol. 2003;  202 101-107
  • 84 Vincent C, Johnson M H. Cooling, cryoprotectants, and the cytoskeleton on the mammalian oocyte.  Oxf Rev Reprod Biol. 1992;  14 73-100
  • 85 Stachecki J J, Munne S, Cohen J. Spindle organization after cryopreservation of mouse, human, and bovine oocytes.  Reprod Biomed Online. 2004;  8 664-672
  • 86 Stachecki J J, Cohen J, Willadsen S M. Cryopreservation of unfertilized mouse oocytes: the effect of replacing sodium with choline in the freezing medium.  Cryobiology. 1998;  37 346-354
  • 87 Stachecki J J, Cohen J, Schimmel T et al.. Fetal development of mouse oocytes and zygotes cryopreserved in a nonconventional freezing medium.  Cryobiology. 2002;  44 5-13
  • 88 Stachecki J J, Willadsen S M. Cryopreservation of mouse oocytes using a medium with low sodium content: effect of low plunge temperature.  Cryobiology. 2000;  40 4-12
  • 89 Fahy G M, McFarlane D R, Angell C A et al.. Vitrification as an approach to cryopreservation.  Cryobiology. 1984;  21 407-426
  • 90 Kola I, Kirby C, Shaw J et al.. Vitrification of mouse oocytes results in aneuploid zygotes and malformed fetuses.  Teratology. 1988;  38 467-474
  • 91 Nakagata N. High survival rate of unfertilized mouse oocytes after vitrification.  J Reprod Fertil. 1989;  87 479-483
  • 92 Aono N, Naganuma T, Abe Y et al.. Successful production of blastocysts following ultrarapid vitrification with step-wise equilibration of germinal vesicle-stage mouse oocytes.  J Reprod Dev. 2003;  49 501-506
  • 93 Begin I, Bhatia B, Baldassarre H et al.. Cryopreservation of goat oocytes and in vivo derived 2- to 4-cell embryos using the cryoloop (CLV) and solid-surface vitrification (SSV) methods.  Theriogenology. 2003;  59 1839-1850
  • 94 Viera A D, Mezzalira A, Barbieri D P et al.. Calves born after open pulled straw vitrification of immature bovine oocytes.  Cryobiology. 2002;  45 91-94
  • 95 Kuleshova L L, Lopata A. Vitrification can be more favorable than slow cooling.  Fertil Steril. 2002;  78 449-454
  • 96 Borini A, Coticchio G, Flamigni C. Oocyte freezing: a positive comment based on our experience.  Reprod Biomed Online. 2003;  7 120
  • 97 Porcu E, Fabbri R, Ciotti P et al.. Cycles of human oocyte cryopreservation and intracytoplasmic sperm injection: results of 112 cycles.  Fertil Steril. 1999;  72 S2
  • 98 Marina F, Marina S. Comments on oocyte cryopreservation.  Reprod Biomed Online. 2003;  6 401-402
  • 99 Yoon T K, Chung H M, Lim J M et al.. Pregnancy and delivery of healthy infants developed from vitrified oocytes in a stimulated in vitro fertilization-embryo transfer program.  Fertil Steril. 2000;  74 180-181
  • 100 Yoon T K, Kim T J, Park S E et al.. Live births after vitrification of oocytes in a stimulated in vitro fertilization-embryo transfer program.  Fertil Steril. 2003;  79 1323-1326
  • 101 Kuleshova L, Gianaroli L, Magli C et al.. Birth following vitrification of a small number of human oocytes: case report.  Hum Reprod. 1999;  14 3077-3079
  • 102 Katayama K P, Stehlik J, Kuwayama M et al.. High survival rate of vitrified human oocytes results in clinical pregnancy.  Fertil Steril. 2003;  80 223-224
  • 103 Kazem R, Thompson L A, Srikantharajah A et al.. Cryopreservation of human oocytes and fertilization by two techniques: in-vitro fertilization and intracytoplasmic sperm injection.  Hum Reprod. 1995;  10 2650-2654
  • 104 Tucker M, Wright G, Morton P et al.. Preliminary experience with human oocyte cryopreservation using 1,2-propanediol and sucrose.  Hum Reprod. 1996;  11 1513-1515
  • 105 Gook D A, Schiewe M C, Osborn S M et al.. Intracytoplasmic sperm injection and embryo development of human oocytes cryopreserved using 1,2-propanediol.  Hum Reprod. 1995;  10 2637-2641
  • 106 Porcu E, Fabbri R, Damiano G et al.. Oocyte cryopreservation in oncological patients.  Eur J Obstet Gynecol Reprod Biol. 2004;  113S S14-S16
  • 107 Eroglu A, Toner M, Toth T L. Beneficial effect of microinjected trehalose on the cryosurvival of human oocytes.  Fertil Steril. 2002;  77 152-158
  • 108 Gook D A, Osborne S M, Bourne H et al.. Fertilization of human oocytes following cryopreservation: normal karyotypes and absence of stray chromosomes.  Hum Reprod. 1994;  9 684-691
  • 109 Cobo A, Rubio C, Gerli S et al.. Use of fluorescence in situ hybridization to assess the chromosomal status of embryos obtained from cryopreserved oocytes.  Fertil Steril. 2001;  75 354-360
  • 110 Porcu E, Fabbri R, Seracchioli R et al.. Obstetric, perinatal outcome and follow up of children conceived from cryopreserved oocytes.  Fertil Steril. 2000;  74 S48
  • 111 Tucker M J, Wright G, Morton P C et al.. Birth after cryopreservation of immature oocytes with subsequent in vitro maturation.  Fertil Steril. 1998;  70 578-579
  • 112 Wu J, Zhang L, Wang X. In vitro maturation, fertilization and embryo development after ultrarapid freezing of immature human oocytes.  Reproduction. 2001;  121 389-393
  • 113 Newton H, Aubard Y, Rutherford A et al.. Low temperature storage and grafting of human ovarian tissue.  Hum Reprod. 1996;  11 1487-1491
  • 114 Hovatta O, Silye R, Krausz T et al.. Cryopreservation of human ovarian tissue using dimethylsulphoxide and propanediol-sucrose as cryoprotectants.  Hum Reprod. 1996;  11 1268-1272
  • 115 Oktay K, Nugent D, Newton H et al.. Isolation and characterization of primordial follicles from fresh and cryopreserved human ovarian tissue.  Fertil Steril. 1997;  67 481-486
  • 116 Jemel A, Murray T, Samuels A et al.. Cancer statistics, 2003.  CA Cancer J Clin. 2003;  53 5-26
  • 117 Oktay K H, Yih M. Preliminary experience with orthotopic and heterotopic transplantation of ovarian cortical strips.  Semin Reprod Med. 2002;  20 63-74
  • 118 Brenner H, Kaatsch P, Burkhardt-Hammer T et al.. Long-term survival of children with leukemia achieved at the end of the millennium.  Cancer. 2001;  92 1977-1983
  • 119 Pui C H, Cheng C, Leung W et al.. Extended follow-up of long-term survivors of acute lymphoblastic leukemia.  N Engl J Med. 2003;  349 640-649
  • 120 Robison L L, Bhatia S. Late-effects among survivors of leukaemia and lymphoma during childhood and adolescence.  Br J Haematol. 2003;  122 345-359
  • 121 Michet Jr C J, McKenna C H, Elveback L R et al.. Epidemiology of systemic lupus erythematosus and other connective tissue diseases in Rochester, Minnesota, 1950 through 1979.  Mayo Clin Proc. 1985;  60 105-113
  • 122 Russell A I, Lawson W A, Haskard D O. Potential new therapeutic options in Behcet’s syndrome.  Biodrugs. 2001;  15 25-35
  • 123 Gladstone D E, Prestrud A A, Pradhan A et al.. High-dose cyclophosphamide for severe systemic lupus erythematosus.  Lupus. 2002;  11 405-410
  • 124 Langford C A, Talar-Williams C, Barron K S et al.. Use of a cyclophosphamide-induction methotrexate-maintenance regimen for the treatment of Wegener’s granulomatosis: extended follow-up and rate of relapse.  Am J Med. 2003;  114 463-469
  • 125 Nousari C H, Brodsky R, Anhalt G J. Evaluating the role of immunoablative high-dose cyclophosphamide therapy in pemphigus vulgaris.  J Am Acad Dermatol. 2003;  49 148-150
  • 126 Stallmach A, Wittig B M, Moser C et al.. Safety and efficacy of intravenous pulse cyclophosphamide in acute steroid refractory inflammatory bowel disease.  Gut. 2003;  52 377-382
  • 127 Chu J Y, Craddock T V, Danis R K et al.. Ovarian tumor as manifestation of relapse in acute lymphoblastic leukemia.  Cancer. 1981;  48 377-379
  • 128 Wyld P J, Lilleyman J S. Ovarian disease in childhood lymphoblastic leukemia.  Acta Haematol. 1983;  69 278-280
  • 129 Yada-Hashimoto N, Yamamoto T, Kamiura S et al.. Metastatic ovarian tumors: a review of 64 cases.  Gynecol Oncol. 2003;  89 314-317
  • 130 McCarville M B, Hill D A, Miller B E et al.. Secondary ovarian neoplasms in children: imaging features with histopathologic correlation.  Pediatr Radiol. 2001;  31 358-364
  • 131 Oktay K, Kan M T, Rosenwaks Z. Recent progress in oocyte and ovarian tissue cryopreservation and transplantation.  Curr Opin Obstet Gynecol. 2001;  13 263-268
  • 132 Struewing J P, Abeliovich D, Peretz T et al.. The carrier frequency of the BRCA1 185delAG mutation is approximately 1 percent in Ashkenazi Jewish individuals.  Nat Genet. 1995;  11 198-200
  • 133 Struewing J P, Hartge P, Wacholder S et al.. The risk of cancer associated with specific mutations of BRCA1 and BRCA2 among Ashkenazi Jews.  N Engl J Med. 1997;  336 1401-1408
  • 134 Liede A, Narod S A. Hereditary breast and ovarian cancer in Asia: genetic epidemiology of BRCA1 and BRCA2.  Hum Mutat. 2002;  20 413-424
  • 135 Kauff N D, Satagopan J M, Robson M E et al.. Risk-reducing salpingo-oophorectomy in women with a BRCA1 or BRCA2 mutation.  N Engl J Med. 2002;  346 1609-1615
  • 136 Rebbeck T R, Lynch H T, Neuhausen S L et al.. Prophylactic oophorectomy in carriers of BRCA1 and BRCA2 mutations.  N Engl J Med. 2002;  346 1616-1622
  • 137 Yin H, Wang X, Kim S S et al.. Transplantation of intact rat gonads using vascular anastamosis: effects of cryopreservation, ischaemia and genotype.  Hum Reprod. 2003;  18 1165-1172
  • 138 Baird D T, Campbell B, de Souza C et al.. Long-term ovarian function in sheep after ovariectomy and autotransplantation of cryopreserved ovarian strips.  Eur J Obstet Gynecol Reprod Biol. 2004;  113 S55-S59
  • 139 Almodin C G, Minguetti-Camara V C, Meister H et al.. Recovery of natural fertility after grafting of cryopreserved germinative tissue in ewes subjected to radiotherapy.  Fertil Steril. 2004;  81 160-164
  • 140 Lee D M, Yeoman R R, Battaglia D E et al.. Live birth after ovarian tissue transplant.  Nature. 2004;  428 137-138
  • 141 Segino M, Ikeda M, Aoki S et al.. In vitro culture of mouse GV oocytes and preantral follicles isolated from ovarian tissues cryopreserved by vitrification.  Hum Cell. 2003;  16 109-116
  • 142 Migishima F, Suzuki-Migishima R, Song S Y et al.. Successful cryopreservation of mouse ovaries by vitrification.  Biol Reprod. 2003;  68 881-887
  • 143 Hasegawa A, Hamada Y, Mehandjiev T et al.. In vitro growth and maturation as well as fertilization of mouse preantral oocytes from vitrified ovaries.  Fertil Steril. 2004;  81 824-830
  • 144 Gosden R, Boulton M, Grant K et al.. Follicular development from ovarian xenografts in SCID mice.  J Reprod Fertil. 1994;  101 619-623
  • 145 Oktay K, Newton H, Mullan J et al.. Development of human primordial follicles to antral stages in SCID/hpg mice stimulated with follicle stimulating hormone.  Hum Reprod. 1998;  13 1133-1138
  • 146 Oktay K, Newton H, Gosden R G. Transplantation of cryopreserved human ovarian tissue results in follicle growth initiation in SCID mice.  Fertil Steril. 2000;  73 599-603
  • 147 Gook D A, McCully B A, Edgar D H et al.. Development of antral follicles in human cryopreserved ovarian tissue following xenografting.  Hum Reprod. 2001;  16 417-422
  • 148 Van den Broecke R, Liu J, Handyside A et al.. Follicular growth in fresh and cryopreserved human ovarian cortical grafts transplanted to immunodeficient mice.  Eur J Obstet Gynecol Reprod Biol. 2001;  97 193-201
  • 149 Kim S S, Soules M R, Battaglia D E. Follicular development, ovulation, and corpus luteum formation in cryopreserved human ovarian tissue after xenotransplantation.  Fertil Steril. 2002;  78 77-82
  • 150 Gook D A, Edgar D H, Borg J et al.. Oocyte maturation follicle rupture and luteinization in human cryopreserved ovarian tissue following xenografting.  Hum Reprod. 2003;  18 1772-1781
  • 151 Gook D A, Osborn S M, Archer J et al.. Follicle development following cryopreservation of human ovarian tissue.  Eur J Obstet Gynecol Reprod Biol. 2004;  113S S60-S62
  • 152 Morris R T. The ovarian graft.  N Y Med J. 1895;  62 436
  • 153 Frank R T. Ueber Transplantation der ovarien.  Zentralbl Gynakol. 1898;  22 436-437
  • 154 Morris R T. A case of heteroplastic ovarian grafting followed by pregnancy, and the delivery of a living child.  Med Rec. 1906;  69 697-698
  • 155 Donnez J, Dolmans M M, Demylle D et al.. Live birth after orthotopic transplantation of cryopreserved ovarian tissue.  Lancet. 2004;  364 1405-1410
  • 156 Schilsky R L, Sherin R J, Hubbard S M et al.. Long-term follow up of ovarian function in women treated with MOPP chemotherapy for Hodgkin’s disease.  Am J Med. 1981;  71 552-556
  • 157 Baird D T, Web R, Campbell B K et al.. Long-term ovarian function in sheep after ovariectomy and transplantation of autografts stored at -196°C.  Endocrinology. 1999;  140 462-471
  • 158 Gook D A, Edgar D H, Stern C. Cryopreservation of human ovarian tissue.  Eur J Obstet Gynecol Reprod Biol. 2004;  S113 S41-S44
  • 159 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 2061-2068
  • 160 Isachenko E, Isachenko V, Rahimi G et al.. Cryopreservation of human ovarian tissue by direct plunging into liquid nitrogen.  Eur J Obstet Gynecol Reprod Biol. 2003;  108 186-193
  • 161 Dudzinski D M. Ethical issues in fertility preservation for adolescent cancer survivors: oocyte and ovarian cryopreservation.  J Pediatr Adolesc Gynecol. 2004;  17 97-102

Kutluk OktayM.D. 

Associate Professor, The Center for Reproductive Medicine and Infertility

The Weill Medical College of Cornell University, 505 East 70th Street

HT-340, New York, NY 10021

Email: kuo9001@med.cornell.edu