Oocyte cryopreservation is a promising adjunct to human assisted reproductive technology. Slow rate freezing has been the cryopreservation standard for storage of sperm, embryos and, subsequently, oocytes. However, earlier concerns regarding damage to the meiotic spindle, loss of cortical granules and the low success rates as compared to the relative success of embryo cryopreservation caused little interest until the 1990s. Interest increased when many studies indicated that acceptable oocyte survival, in vitro fertilization, normal embryos and adequate blastocyst development can be achieved with oocyte cryopreservation. Recently introduced oocyte vitrification techniques are proving to be more efficient. Survival rates are close to 100% and developmental rates are similar to those achieved with fresh oocytes. This efficiency opens the way to the widespread application of the technique in various medical, legal, and social situations, even to replace embryo cryopreservation with the oocyte cryopreservation. Oocyte vitrification has dominated slow freezing to such an extent that it may soon become the exclusive cryopreservation choice, especially considering that potential disease transmission problems commonly associated with vitrification due to direct exposure of oocytes to liquid nitrogen can be eliminated by using the proper techniques and devices. Furthermore, cryopreservation of immature oocytes, ovarian follicles, ovarian tissue and whole ovary are other emerging technologies. Oocyte cryopreservation has tremendous opportunity for preserving fertility in cancer patients, for those who may not have sperm following oocyte retrieval and for those women who wish to delay their motherhood. The purpose of this article is to review the history of oocyte cryopreservation, its applications, current cryopreservation techniques and future trends for fertility cryopreservation, to determine if oocyte cryopreservation is proceeding in the right direction.
Al-HasaniSDiedrichKvan der VenHKrebsD. Preliminary results of cryopreservation of human oocytes. Geburtshilfe Frauenheilkd. 1986; 46:643–4.
2.
Al-HasaniSDiedrichKvan der VenHReineckeAHartjeMKrebsD. Cryopreservation of human oocytes. Hum Reprod. 1987; 2:695–700.
3.
Al-KhtibMPerretAKhoueiryRIbala-RomdhaneSBlachèreTGrezeCLornageJLefèvreA. Vitrification at the germinal vesicle stage does not affect the methylation profile of H19 and KCNQ1OT1 imprinting centers in human oocytes subsequently matured in vitro. Fertil Steril. 2011; 95:1955–60. Epub 2011 Mar 21.
4.
AmorimCADavidAVan LangendoncktADolmansMMDonnezJ. Vitrification of human ovarian tissue: effect of different solutions and procedures. Fertil Steril. 2011; 95:1094–7. Epub 2010 Dec 18.
5.
AntinoriMLicataEDaniGCerusicoFVersaciCAntinoriS. Cryotop vitrification of human oocytes results in high survival rate and healthy deliveries. Reprod Biomed Online. 2007; 14:72–9.
6.
BarrettSLSheaLDWoodruffTK. Noninvasive index of cryorecovery and growth potential for human follicles in vitro. Biol Reprod. 2010; 82:1180–9. Epub 2010 Mar 3.
BernardAHunterJEFullerBJImoedemeDCurtisPJacksonA. Fertilization and embryonic development of human oocytes after cooling. Hum Reprod. 1992; 7:1447–50.
9.
BianchiVCottichioGDistratisVDi GiustoNFlamigniCBoriniA. Differential sucrose concentration during dehydration (0.2 Mol/L) and rehydration (0.3 Mol/L) increases theimplantation rate of frozen human oocytes. Reprod Biomed Online. 2007; 14:64–71.
10.
BielanskiAVajtaG. Risk of contamination of germplasm during cryopreservation and cryobanking in IVF units. Hum Reprod. 2009; 24:2457–67.
11.
BloemersMCPortelanceLLeglerCRenaudMCTanSL. Preservation of ovarian function by ovarian transposition prior to concurrent chemotherapy and pelvic radiation for cervical cancer. A case report and review of the literature. Eur J Gynaecol Oncol. 2010; 31:194–7.
12.
BoisoIMartiMSantalóJPonsáMBarriPNVeigaA. 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; 17:1885–91.
13.
BoldtJClineDMcLaughlinD. Human oocyte cryopreservation as an adjunct to IVF-embryo transfer cycles. Hum Reprod. 1993; 18:1250–5.
14.
BoldtJTidswellNSayersAKilaniRClineD. Human oocyte cryopreservation: 5-year experience with a sodium depleted slow freezing method. Reprod Biomed Online. 2006; 13:96–100.
15.
BonettiACerviMTomeiFMarchiniMOrtolaniFMannoM. Ultrastructural evaluation of human metaphase II oocytes after vitrification: closed versus open devices. Fertil Steril. 2011; 95:928–35.
16.
BoriniABonuMACoticchioGBianchiVCattoliMFlamigniC. Pregnancies and births after oocyte cryopreservation. Fertil Steril. 2004; 82:601–605.
17.
BoriniACoticchioG: The efficacy and safety of human oocyte cryopreservation by slow cooling. Semin Reprod Med.2009; 27:443–449.
18.
BromerJGPatrizioP. Fertility preservation: the rationale for cryopreservation of the whole ovary. Semin Reprod Med.2009; 27:465–471. Epub 2009 Oct 5. Review
19.
ChaKYHanSYChungHMChoiDHLimJMLeeWSKoJJYoonTK. Pregnancies and deliveries after in vitro maturation culture followed by in vitro fertilization and embryo transfer without stimulation in women with polycystic ovary syndrome. Fertil Steril. 2000; 73:978–83.
20.
ChenC. Pregnancy after human oocyte cryopreservation. The Lancet. 1986; 327(8486), 884–886.
21.
ChungHMHongSWLimJMLeeSHChaWTKoJJHanSYChoiDHChaKY. In vitro blastocyst formation of human oocytes obtained from unstimulated and stimulated cycles after vitrification at various maturational stages. Fertil Steril. 2000; 73:545–51.
22.
CobanOHacifazliogluOCirayHNUlugUTekinHIBahceciM. Birth after 12 hours of oocyte refrigeration. Fertil Steril. 2010; 94:2769.e5–7. Epub 2010 Jun 9.
23.
CoboAKuwayamaMPe'rezSRuizAPellicerARemohı'J. Comparison of concomitant outcome achieved with fresh and cryopreserved donor oocytes vitrified by the Cryotop method. Fertil Steril. 2008; 89:1657–64.
24.
CoboARubioCGerliSRuizAPellicerARemohiJ. Use of fluorescence in situ hybridization to assess the chromosomal status of embryos obtained from cryopreserved oocytes. Fertil Steril. 2001; 75:354–60.
25.
CoticchioGGarettiSBonuMABoriniA. Cryopreservation of human oocytes. Hum Fertil. 2001; 4:152–7.
26.
CriadoEAlbaniENovaraPVSmeraldiACesanaAPariniVLevi-SettiPE. Human oocyte ultravitrification with a low concentration of cryoprotectants by ultrafast cooling: a new protocol. Fertil Steril. 2011; 95:1101–3. Epub 2010 Dec 3.
27.
De SantisLCinoIRabellotiEPapaleoECalziFFusiFBriganteCFerrariA. Oocyte cryopreservation: clinical outcome of slow-cooling protocols differing in sucrose concentration. Reprod Biomed Online. 2007a;14:57–63.
28.
De SantisLCoticchioGPaynterSAlbertiniDHuttKCinoIIaccarinoMGambardellaAFlamigniCBoriniA. Permeability of human oocytes to ethylene glycol and their survival and spindle configurations after slow cooling cryopreservation. Hum Reprod. 2007b;22:2776–83.
29.
DursunPAyhanAYanikFBKuscuE. Ovarian transposition for the preservation of ovarian function in young patients with cervical carcinoma. Eur J Gynaecol Oncol. 2009; 30:13–15.
30.
EdgarDHKaraniJGookDA. Increasing dehydration of human cleavage-stage embryos prior to slow cooling significantly increases cryosurvival. Reprod Biomed Online. 2009; 19, 521–525.
31.
ElizurSEChianRCHolzerHEGidoniYTulandiTTanSL. Cryopreservation of oocytes in a young woman with severe and symptomatic endometriosis: a new indication for fertility preservation. Fertil Steril. 2009; 91:293e1–3. Epub 2007 Oct 24.
32.
EsfandiariNJavedMNazemianZCasperR. Fertilization and embryo development of fresh and cryopreserved sibling oocytes. Int J Fert Steril. 2010; 4:98–103.
33.
FabbriRPorcuEMarsellaTRocchettaGVenturoliSFlamigniC. Human oocyte cryopreservation: new perspectives regarding oocyte survival. Hum Reprod. 2001; 16:411–6.
34.
FineschiVNeriMTurillazziE. The new Italian law on assisted reproduction technology (Law 40/2004). J Med Ethics2005; 31:536–539.
35.
GaoSLiYGaoXHuJYangHChenZJ. Spindle and chromosome changes of human MII oocytes during incubation after slow freezing/fast thawing procedures. Reprod Sci.2009; 16:391–6.
36.
GilchristRB. Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod Fertil Dev.2011; 23:23–31. Review
37.
GookDAOsbornSMJohnstonW. Cryopreservation of mouse and human oocytes using 1,2 propanediol and the configuration of the meiotic spindle. Hum Reprod. 1993; 8:1101–9.
38.
GookDASchieweMOsbornSMAschRHJansenRPJohnstonWI. Intracytoplasmic sperm injection and embryo development of human oocytes cryopreserved using 1, 2-propanediol. Hum Reprod. 1995; 10:2637–41.
39.
GosdenR. Cryopreservation: a cold look at technology for fertility preservation. Fertil Steril. 2011; 96:264–8. Epub 2011 Jun 30.
40.
GualtieriRMolloVBarbatoVFiorentinoIIaccarinoMTaleviR. Ultrastructure and intracellular calcium response during activation in vitrified and slow-frozen human oocytes. Hum Reprod. 2011; 26:2452–2460. Epub 2011 June 29.
41.
HeXParkEYHFowlerAYarmushMLTonerM. Vitrification by ultra-fast cooling at a low concentration of cryoprotectants in a quartz micro-capillary: a study using murine embryonic stem cells. Cryobiology. 2008; 56:223–32.
42.
HovattaO. Methods for cryopreservation of human ovarian tissue. Reprod Biomed Online. 2005; 10:729–34.
43.
HuangJYTulandiTHolzerHTanSLChianRC. Combining ovarian tissue cryobanking with retrieval of immature oocytes followed by in vitro maturation and vitrification: an additional strategy of fertility preservation. Fertil Steril. 2008; 89:567–72.
44.
JemalASiegelRWardEHaoYXuJMurrayTThunMJ. Cancer statistics, 2008. CA Cancer J Clin. 2008; 58(2):71–96. Epub 2008 Feb 20.
45.
JohnsonJPatrizioP. Ovarian cryopreservation strategies and the fine control of ovarian follicle development in vitro. Ann N Y Acad Sci.2011; 1221:40–6.
46.
KimSS. Time to re-think: ovarian tissue transplantation versus whole ovary transplantation. Reprod Biomed Online. 2010; 20:171–4. Epub 2009 Nov 29.
47.
KuleshovaLGianaroliLMagliCFerrarettiATrounsonA. Birth following vitrification of a small number of human oocytes: case report. Hum Reprod. 2002; 14:3077–9.
48.
KuwayamaMVajtaGKatoOLeiboSP. Highly efficient vitrification method for cryopreservation of human oocytes. Reprod Biomed Online. 2005; 11:300–8.
49.
LeeHElmoazzenHWrightDBiggersJRuedaBRHeoYSTonerMTothTL. Ultra-rapid vitrification of mouse oocytes in low cryoprotectant concentrations. Reprod Biomed Online. 2010; 20:201–8.
50.
LiYBZhouCQYangGFWangQDongY. Modified vitrification method for cryopreservation of human ovarian tissue. Chin Med J.2007; 120:110–4.
51.
LucenaEBernalDPLucenaCRojasAMoranALucenaA. Successful ongoing pregnancies after vitrification of oocytes. Fertil Steril. 2006; 85:108–11.
52.
Martinez-MadridBDolmansMMVan LangendoncktADefrèreSDonnezJ. Freeze-thawing intact human ovary with its vascular pedicle with a passive cooling device. Fertil Steril. 2004; 82:1390–1394.
53.
MazurPSekiS. Survival of mouse oocytes after being cooled in a vitrification solution to −196°C at 95° to 70,000°C/min and warmed at 610° to 118,000°C/min: A new paradigm for cryopreservation by vitrification. Cryobiology. 2011; 62:1–7. Epub 2010 Nov 3.
54.
MullenSFFahyGM. Fundamental aspects of vitrification as a method of reproductive cell, tissue and organ cryopreservation. In: DonnezJKimSS, editors. Principles and practice of fertility preservation. Cambridge, UK: Cambridge University Press; 2011: 145–63.
55.
NagyZPChangCCShapiroDBBernalDPKortHIVajtaG. The efficacy and safety of human oocyte vitrification. Semin Reprod Med.2009; 27:450–5. Epub 2009 Oct 5. Review
56.
NoyesNBoldtJNagyZP. Oocyte cryopreservation: is it time to remove its experimental label?J Assist Reprod Genet. 2010; 27:69–74. Epub 2010 Feb 6.
57.
NoyesNPorcuEBoriniA. Over 900 oocyte cryopreservation babies born with no apparent increase in congenital anomalies. Reprod Biomed Online. 2009; 18:769–76.
58.
O'NeilLPaynterSJFullerBLShawRW. Vitrification of mature mouse oocytes: improved results following addition of polyethylene glycol to a dimethyl sulfoxide solution. Cryobiology. 1997; 34:295–301.
59.
OakesMBGomesCMFioraventiJSerafiniPMottaELSmithGD. A case of oocyte and embryo vitrification resulting in clinical pregnancy. Fertil Steril. 2008; 90:(2013). e5–8.
60.
OktayKCilAPBangH. Efficiency of oocyte cryopreservation: a meta-analysis. Fertil Steril. 2006; 86:70–80.
61.
OktemOAlperEBalabanBPalaogluEPekerKKarakayaCUrmanB. Vitrified human ovaries have fewer primordial follicles and produce less antimüllerian hormone than slow-frozen ovaries. Fertil Steril. 2011; 95:2661–4.e1. Epub 2011 Feb 5.
62.
ParmegianiLBertocciFGarelloCSalvaraniMCTambuscioGFabbriR. Efficiency of human oocyte slow freezing: results from five assisted reproduction centers. Reprod Biomed Online. 2009; 18:352–9.
63.
PickeringSJBraudeRPJohnstonMHCantACurrieJ. Transient cooling to room temperature can cause irreversible disruption of the meiotic spindle in the human oocyte. Fertil Steril. 1990; 54:102–8.
64.
PomeroyKOHarrisSConaghanJPapadakisMCentolaGBasurayRBattagliaD. Storage of cryopreserved reproductive tissues: evidence that cross-contamination of infectious agents is a negligible risk. Fertil Steril. 2010; 94:1181–8. Epub 2009 May 29.
65.
PorcuEFabbriRDamianoGGiunchiSFarttoRCiottiPVenturoliSFlamigniC. Clinical experience and applications of oocyte cryopreservation. Mol Cell Endocrinol. 2000; 169:33–7.
66.
PorcuEFabbriRSeracchioliRCiottiPMMagriniOFlamigniC. Birth of a healthy female after intracytoplasmic sperm injection of cryopreserved human oocytes. Fertil Steril. 1997; 68:724–6.
67.
Practice Committee of the American Society for Reproductive Medicine and Practice Committee of the Society for Assisted Reproductive Technology. Ovarian tissue and oocyte cryopreservation. Fertile Steril2006; 86 (Suppl 5): S142–47.
68.
RahimiGIsachenkoESauerHIsachenkoVWartenbergMHeschelerJMallmannPNawrothF. Effect of different vitrification protocols for human ovarian tissue on reactive oxygen species and apoptosis. Reprod Fertil Dev.2003; 15:343–9.
69.
RallWFFahyGM. Ice-free cryopreservation of mouse embryos at −196 degrees C by vitrification. Nature. 1985; 313(6003): 573–575.
70.
RehAOktemOOktayK. Impact of breast cancer chemotherapy on ovarian reserve: a prospective observational analysis by menstrual history and ovarian reserve markers. Fertil. Steril. 2008; 90:1635–1639.
71.
RiscoRElmoazzenHDoughtyMHeXTonerM. Thermal performance of quartz capillaries for vitrification. Cryobiology2007; 55:222–9.
72.
Rodriguez-WallbergKAOktayK. Fertility preservation in women with breast cancer. Clin Obstet Gynecol. 2010; 53:753–62.
73.
RudickBOpperNPaulsonRBendiksonKChungK. The status of oocyte cryopreservation in the United States. Fertil Steril. 2010; 94:2642–6. Epub 2010 Jun 18.
74.
SakuraiTKimuraMSatoM. Temporary developmental arrest after storage of fertilized mouse oocytes at 4 degrees C: effects on embryonic development, maternal mRNA processing and cell cycle. Mol Hum Reprod. 2005; 11:325–33.
75.
SaragustyJAravA. Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction. 2011; 141:1–19.
76.
ScaravelliGVigilianoVMayorgaJMBolliSDe LucaRD'AlojaP. Analysis of oocyte cryopreservation in assisted reproduction: the Italian National Register data from 2005 to 2007. Reprod Biomed Online. 2010; 21:496–500.
77.
SchalkoffMEOskowitzSPPowersRD. Ultrastructural observations of human and mouse oocytes treated with cryoprotectants. Biol Reprod. 1989; 40:379–93.
78.
ShermanJKLinTP. Effect of glycerol and low temperature on survival of unfertilized mouse eggs. Nature. 1958; 181:785–6.
79.
SirardMA. Follicle environment and quality of in vitro matured oocytes. J Assist Reprod Genet. 2011. Epub 2011 Mar 11.
80.
SmitzJEThompsonJGGilchristRB. The promise of in vitro maturation in assisted reproduction and fertility preservation. Semin Reprod Med.2011; 29:24–37. Epub 2011 Jan 4. Review
81.
StacheckiJJGarrisiJSabinoSCaetanoJPWiemerKECohenJ. A new safe, simple and successful vitrification method for bovine and human blastocysts. Reprod Biomed Online. 2008; 17:360–7.
82.
SteponkusPLMyersSPLynchDVGardnerLBronstheynVLeiboSPRallWFPittRELinTTMacIntyreRJ. Cryopreservation of Drosophila melanogaster embryos. Nature. 1990; 345:170–2.
83.
TodorowSJSiebzehnrüblERSpitzerMKochRWildtLLangN. Comparative results on survival of human and animal eggs using different cryoprotectants and freeze-thawing regimens. II. Human. Hum Reprod. 1989; 4:812–6.
84.
VajtaGNagyZP. Are programmable freezers still needed in the embryo laboratory? Review on vitrification. Reprod Biomed Online. 2006; 12, 779–796.
85.
VincentCPickeringSJJohnsonMH. The hardening effect of dimethylsulphoxide on the mouse zona pellucida requires the presence of an oocyte and is associated with a reduction in the number of cortical granules present. J Reprod Fertil. 1990; 89:253–9.
86.
WhittinghamDG. Fertilization in vitro and development to term of unfertilized mouse oocytes previously stored at −196 degrees C. J Reprod Fertil. 1977; 49:89–94.
87.
WoJYViswanathanAN. Impact of radiotherapy on fertility, pregnancy, and neonatal outcomes in female cancer patients. Int J Radiat Oncol Biol Phys. 2009; 73:1304–1312.
88.
WuJZhangLWangX. In vitro maturation, fertilization and embryo development after ultrarapid freezing of immature human oocytes. Reproduction. 2001; 121:389–93.
89.
YoonTKChungHMLimJMHanSYKoJJChaEY. Pregnancy and delivery of healthy infants developed from vitrified oocytes in a stimulated in vitro fertilization-embryo transfer program. Fertil Steril. 2000; 74:180–1.
90.
YoonTKLeeDRChaSKChungHMLeeWSChaKY. Survival rate of human oocytes and pregnancy outcome after vitrification using slush nitrogen in assisted reproductive technologies. Fertil Steril. 2007; 88:952–6.
