Cryopreservation of Gametes and Embryos

Kay Elder; Brian Dale

doi:10.1017/9781108611633.013

The first live births following frozen-thawed embryo transfer were reported in 1984 and 1985 by groups in Australia, the Netherlands and the United Kingdom. Since that time, the original protocols have been modified and simplified such that cryopreservation with successful survival of sperm, oocytes and embryos is now an essential component of every routine IVF program. Pregnancy and live birth rates after frozen embryo transfer contribute significantly to cumulative conception rates after fresh transfer. In recent years, traditional methods of freezing and thawing have been increasingly replaced by protocols for vitrification/warming. For both slow freezing and vitrification, an understanding of the basic principles of cryobiology involved is essential to ensure that the methodology is correctly and successfully applied, in order to minimize cell damage during the processes of freezing/vitrification and thawing/warming.

Fahy, GM, Wowk, B (2015) Principles of cryopreservation by vitrification. In: Wolkers, WF, Oldenhof, H (eds.) Cryopreservation and Freeze-Drying Protocols, Methods in Molecular Biology, vol 1257. Springer Science + Business Media, New York, pp. 21–82.

Fogarty, NM, Maxwell, WM, Eppleston, J, Evans, G (2000) The viability of transferred sheep embryos after long-term cryopreservation. Reproduction, Fertility and Development 12: 31–37.

Fuller, BJ (2003) Gene expression in response to low temperatures in mammalian cells: a review of current ideas. Cryo Letters 24(2): 95–102.

Lasalle, B, Testart, J, Renard, JP (1985) Human embryo features that influence the success of cryopreservation with the use of 1,2 propanediol. Fertility and Sterility 44: 645–651.

Leibo, SP (1976) Freezing damage of bovine erythrocytes: simulation using glycerol concentration changes at sub-zero temperatures. Cryobiology 13: 587–598.

Leibo, SP, Oda, K (1993) High survival of mouse zygotes and embryos cooled rapidly or slowly in ethylene glycol plus polyvinylpyrrolidone. Cryo Letters 14: 133–144.

Leibo, SP, Pool, TB (2011) The principal vairables of cryopreservation: solutions, temperatures, and rate changes. Fertility and Sterility 96(2): 269–275.

Leibo, SP, Semple, ME, Kroetsch, TG (1994) In vitro fertilization of oocytes by 37-year-old bovine spermatozoa. Theriogenology 42: 1257–1262.

Liebermann, J, Nawroth, F, Isachenko, V, et al. (2002) Potential importance of vitrification in reproductive medicine. Biology of Reproduction 67(6): 1671–1680.

Mazur, P (1963) Kinetics of water loss from cells at subzero temperatures and the likelihood of intracellular freezing. Journal of General Physiology 47: 347–369.

Mazur, P (1970) Cryobiology: the freezing of living systems. Science 168: 93–94.

Mazur, P (1984) Freezing of living cells: mechanisms and implications. American Journal of Physiology 247: 125–142.

McWilliams, RB, Gibbons, WE, Leibo, SP (1995) Osmotic and physiological responses of mouse and human ova to mono- and disaccharides. Human Reproduction 10: 1163–1171.

Morató, R, Izquierdo, D, Paramio, MT, Mogas, T (2008) Cryotops versus open-pulled straws (OPS) as carriers for the cryopreservation of bovine oocytes: effects on spindle and chromosome configuration and embryo development. Cryobiology 57(2): 137–141.

Parks, JE (1997) Hypothermia and mammalian gametes. In: Karow, A, Critser, JK (eds.) Reproductive Tissue Banking: Scientific Principles. Academic Press, San Diego, pp. 229–261.

Pegg, DE (1996) Cryopreservation: a perspective. In: Hervé, P, Rifle, G, Vuitton, D, Dureau, G, Bechtel, P, Justrabo, E (eds.) Organ Transplantation and Tissue Grafting. John Libbey, London, pp. 375–378.

Pegg, DE (2002) The history and principles of cryopreservation. Seminars in Reproductive Medicine 20(1): 5–13.

Pegg, DE (2015) Principles of cryopreservation. In: Wolkers, W, Oldenhof, H (eds.) Cryopreservation and Freeze-Drying Protocols, Methods in Molecular Biology (Methods and Protocols), vol 1257. Springer, New York, NY, pp. 3–19.

Pegg, DE, Karow, AM (1987) The Biophysics of Organ Cryopreservation. Plenum, New York.

Smith, AU (1952) Behaviour of fertilized rabbit eggs exposed to glycerol and to low temperatures. Nature 170: 373.

Tucker, MJ, Liebermann, J (2007) Vitrification in Assisted Reproduction: A User’s Manual and Troubleshooting Guide. Informa Healthcare, New York.

Vajta, G, Rienzi, L, Ubaldi, FM (2015) Open versus closed systems for vitrification of human oocytes and embryos. Reproductive BioMedicine Online 30: 325–333.

Watson, PF, Morris, GJ (1987) Cold shock injury in animal cells. In: Bowler, P, Fuller, J (eds.) Temperature and Animal Cells. Symposia of the Society for Experimental Biology no. 41. Company of Biologists, Cambridge, UK, pp. 311–340.

Whittingham, DG (1977) Some factors affecting embryo storage in laboratory animals. Ciba Foundation Symposium 52: 97–127.

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

Bahadur, G, Tedder, RS (1997) Safety during sperm banking. Human Reproduction 12: 198.

British Andrology Society (1993) British Andrology Society guidelines for the screening of semen donors for donor insemination. Human Reproduction 8: 1521–1523.

Department of Health (1997) Guidance on the processing, storage and issue of bone marrow and blood stem cells. NHS Executive, Health Service Guidelines 97(19).

Fountain, D, Ralston, M, Higgins, N, et al. (1997) Liquid nitrogen freezers: potential source of hematopoietic stem cell components. Transfusion 37: 585–591.

Hawkins, AE, Zuckerman, MA, Briggs, M, et al. (1996) Hepatitis B nucleotide sequence analysis – linking an outbreak of acute Hepatitis B to contamination of a cryopreservation tank. Journal of Virological Methods 60: 81–88.

Human Fertilisation and Embryology Authority (1998) Consultation on the Safe Cryopreservation of Gametes and Embryos. HFEA, London.

Hunt, CJ, Pegg, DE (1996) Improved temperature stability in gas phase nitrogen refrigerators: use of a copper heat shunt. Cryobiology 33: 544–551.

McKee, TA, Avery, S, Majid, A, et al. (1996) Risks for transmission of hepatitis C virus during artificial insemination. Fertility and Sterility 66: 161–163.

Pomeroy, KO, Harris, S, Conaghan, J, et al. (2009) Storage of cryopreserved reproductive tissues: evidence that cross-contamination of infectious agents is a negligible risk. Fertility and Sterility 94(4): 1181–1188.

Russell, PH, Lyaruu, VH, Millar, JD, Curry, MR, Watson, PF (1997) The potential transmission of infectious agents by semen packaging during storage for artificial insemination. Animal Reproduction Science 47: 337–342.

Tedder, RS, Zuckerman, AH, Goldstone, AH, et al. Hepatitis B transmission from contaminated cryopreservation tank. Lancet 1995; 346: 137–140.

Tomlinson, M, Sakkas, D (2000) Safe and effective cryopreservation: should sperm banks and fertility centres move toward storage in nitrogen vapour? Human Reproduction 15(12): 2460–2463.

Alteri, A, Vigano, P, Maizar, AA, Jovine, L, Giacomini, E, Rubino, P (2018) Revisiting embryo assisted hatching approaches: a systematic review of the current protocols. Journal of Assisted Reproduction and Genetics 35(3): 367–391.

Ashwood-Smith, MJ (1986) The cryopreservation of human embryos. Human Reproduction 1: 319–332.

Cimadonmo, D, Capalbo, A, Levi-Setti, PE, Soscia, DD, Orland, G (2018) Associations of blastocyst features, trophectoderm biopsy and other laboratory practice with post-warming behavior and implantation. Human Reproduction 33(11): 1992–2001.

Cohen, J, Devane, GW, Elsner, CW, et al. (1988) Cryopreservation of zygotes and early cleaved human embryos. Fertility and Sterility 49: 2.

Cohen, J, Simons, RF, Edwards, RG, Fehilly, CB, Fishel, SB (1985) Pregnancies following the frozen storage of expanding human blastocysts. Journal of In Vitro Fertilization and Embryo Transfer 2: 59–64.

Elder, K, Van den Bergh, M, Woodward, B (2015) Troubleshooting and Problem-Solving in the IVF Laboratory. Cambridge University Press, Cambridge, UK, Chapter 10.

Fehilly, CB, Cohen, J, Simons, RF, Fishel, SB, Edwards, RG (1985) Cryopreservation of cleaving embryos and expanded blastocysts in the human: a comparative study. Fertility and Sterility 44: 638–644.

Givens, C, Markun, L, Chenette, P, et al. (2009) Outcomes of natural cycles versus programmed cycles for 1677 frozen-thawed embryo transfers. Reproductive BioMedicine Online 19(3): 380–384.

Guerif, F, Cadoret, V, Poindron, J, Lansac, J, Royere, D (2003) Overnight incubation improves selection of frozen-thawed blastocysts for transfer: preliminary study using supernumerary embryos. Theriogenology 60(8): 1457–1466.

Hartshorne, GM, Elder, K, Crow, J, Dyson, H, Edwards, RG (1991) The influence of in vitro development upon post-thaw survival and implantation of cryopreserved human blastocysts. Human Reproduction 6: 136–141.

Hartshorne, GM, Wick, K, Elder, K, Dyson, H (1990) Effect of cell number at freezing upon survival and viability of cleaving embryos generated from stimulated IVF cycles. Human Reproduction 5: 857–861.

Jin, B, Kleinhaus, FW, Mazur, P (2014) Survivals of mouse oocytes approach 100% after vitrification in 3-fold diluted media and ultra-raid warming by an IR laser pulse. Cryobiology 68(3): 419–430.

Jin, B, Mazur, P (2015) High survival of mouse oocytes/embryos after vitrification without permeating cryoprotectants followed by ultra-rapid warming with an IR laser pulse. Scientific Reports 5: 9271.

Jones, HW Jr., Veeck, LL, Muasher, SJ (1995) Cryopreservation: the problem of evaluation. Human Reproduction 10: 2136–2138.

Kader, AA, Choi, A, Orief, Y, Agarwal, A (2009) Factors affecting the outcome of human blastocyst vitrification. Reproductive Biology and Endocrinology 7: 99.

Katkov, II, Bolyukh, VF, Sukhikh, GT (2018) KrioBlast^TM as a new technology of ultrafast cryopreservation of cells and tissues. 2. Kinetic vitrification of human pluripotent stem cells and spermatozoa. Bulletins in Experimental Biological Medicine 165: 171.

Kojima, E, Fukunaga, N, Nagai, R, Kitasaka, H, Ohno, H, Asada, Y (2012) The vitrification method is significantly better for thawing of slow-freezing embryos. Fertility and Sterility 98: S124.

Lassalle, B, Testart, J, Renard, JP (1985) Human embryo features that influence the success of cryopreservation with the use of 1, 2, propanediol. Fertility and Sterility 44: 645–651.

Loutradi, KE, Kolibianakis, EM, Venetis, CA, et al. (2008) Cryopreservation of human embryos by vitrification or slow freezing: a systematic review and meta-analysis. Fertility and Sterility 90(1): 186–193.

Magli, MC, Gianaroli, L, Grieco, N, et al. (2006) Cryopreservation of biopsied embryos at the blastocyst stage. Human Reproduction 21(10): 2656–2660.

Martino, A, Songsasen, N, Leibo, SP (1996) Development into blastocysts of bovine oocytes cryopreserved by ultra-rapid cooling. Biology of Reproduction 54: 1059–1069.

Ménézo, Y, Nicollet, B, Herbaut, N, André, D (1992) Freezing cocultured human blastocysts. Fertility and Sterility 58(5): 977–980.

Noyes, N, Reh, A, McCaffrey, C, Tan, O, Krey, L (2009) Impact of developmental stage at cryopreservation and transfer on clinical outcome of frozen embryo cycles. Reproductive BioMedicine Online 19(Suppl. 3): 9–15.

Parmegiani, L, Tatone, C, Cognigni, GE, et al. (2014) Rapid warming increases survival of slow-frozen sibling oocytes: a step towards a single warming procedure irrespective of the freezing protocol? Reproductive BioMedicine Online 28: 614–623.

Pribenszky, C, Losonczi, E, Molnár, M, et al. (2010) Prediction of in-vitro developmental competence of early cleavage-stage mouse embryos with compact time-lapse equipment. Reproductive BioMedicine Online 20(3): 371–379.

Rall, WF (1987) Factors affecting the survival of mouse embryos cryopreserved by vitrification. Cryobiology 24: 387–402.

Rall, WF, Fahy, GM (1985) Ice-free cryopreservation of mouse embryos at –196°C by vitrification. Nature 313: 573–575.

Rama Raju, GA, Jaya Prakash, G, Murali Krishna, K, Madan, K (2009) Neonatal outcome after vitrified day 3 embryo transfers: a preliminary study. Fertility and Sterility 92(1): 143–148.

Riggs, R, Mayer, J, Dowling-Lacey, D, et al. (2010) Does storage time influence post-thaw survival and pregnancy outcome? An analysis of 11,768 cryopreserved human embryos. Fertility and Sterility 93(1): 109–115.

Schmidt, CL, Taney, FH, de Ziegler, D, et al. (1989) Transfer of cryopreserved-thawed embryos: the natural cycle versus controlled preparation of the endometrium with gonadotropin-releasing hormone agonist and exogenous estradiol and progesterone (GEEP). Fertility and Sterility 52: 1609–1616.

Schuster, TG, Hickner-Cruz, K, Ohl, DA, Goldman, E, Smith, GD (2003) Legal considerations for cryopreservation of sperm and embryos. Fertility and Sterility 80(1): 61–66.

Sher, G, Keskintepe, L, Mukaida, T, et al. (2008) Selective vitrification of euploid oocytes markedly improves survival, fertilization and pregnancy-generating potential. Reproductive BioMedicine Online 17(4): 524–529.

Shu, Y, Watt, J, Gebhardt, J, et al. (2009) The value of fast blastocoele re-expansion in the selection of a viable thawed blastocyst for transfer. Fertility and Sterility 91(2): 401–406.

Testart, J, Belaisch Allart, J, Lassalle, B, et al. (1987) Factors influencing the success rate of human embryo freezing in an in vitro fertilization and embryo transfer program. Fertility and Sterility 48: 107–112.

Trounson, A, Mohr, L (1983) Human pregnancy following cryopreservation, thawing, and transfer of an eight-cell embryo. Nature 305: 707–709.

Tucker, MJ, Cohen, J, Massey, JB, et al. (1991) Partial dissection of the zona pellucida of frozen-thawed human embryos may enhance blastocyst hatching, implantation, and pregnancy rates. American Journal of Obstetrics and Gynecology 165(2): 341–344.

Vajta, G, Holm, P, Kuwayama, M, et al. (1998) Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Molecular Reproduction and Development 51: 53–58.

Van den Abbeel, E, Camus, M, Verheyen, G, et al. (2005) Slow controlled-rate freezing of sequentially cultured human blastocysts: an evaluation of two freezing strategies. Human Reproduction 20(10): 2939–2945.

Van den Abbeel, E, Van Steirteghem, A (2000) Zona pellucida damage to human embryos after cryopreservation and the consequences for their blastomere survival and in-vitro viability. Human Reproduction 15(2): 373–378.

Wennerholm, UB, Söderström-Anttila, V, Bergh, C, et al. (2009) Children born after cryopreservation of embryos or oocytes: a systematic review of outcome data. Human Reproduction 24(9): 2158–2172.

Youssry, M, Ozmen, B, Zohni, K, Diedrich, K, Al-Hasani, S (2008) Current aspects of blastocyst cryopreservation. Reproductive BioMedicine Online 16(2): 311–320.

Al-Hasani, S, Diedrich, K, van der Ven, H, et al. (1987) Cryopreservation of human oocytes. Human Reproduction 2: 695–700.

Al-Hasani, S, Ludwig, M, Diedrich, K, et al. (1996) Preliminary results on the incidence of polyploidy in cryopreserved human oocytes after ICSI. Human Reproduction 11: Abstract book 1, 50–51.

Amorim, CA, Gonçalves, PB, Figueiredo, JR (2003) Cryopreservation of oocytes from pre-antral follicles. Human Reproduction Update 9(2): 119–129.

Amorim, CA, Van Langendonckt, A, David, A, Dolmans, MM, Donnez, J (2009) Survival of human pre-antral follicles after cryopreservation of ovarian tissue, follicular isolation and in vitro culture in a calcium alginate matrix. Human Reproduction 24(1): 92–99.

Balkenende, EME, Dahhan, T, van der Veen, F, Repping, S, Goddijn, M (2018). Reproductive outcomes after oocyte banking for fertility preservation. Reproductive BioMedicine Online 37(4):425–433.

Boldt, J, Tidswell, J, Sayer, A, Kilani, R, Cline, D (2006) Human oocyte cryopreservation: Five-year experience with a sodium-depleted slow freezing method. Reproductive BioMedicine Online 13: 96–100.

Cao, YX, Xing, Q, Li, L, et al. (2009) Comparison of survival and embryonic development in human oocytes cryopreserved by slow-freezing and vitrification. Fertility and Sterility 92(4): 1306–1311.

Chen, C (1986) Pregnancy after human oocyte cryopreservation. Lancet 1: 884–886.

Chen, SU, Lien, YR, Chao, KH, et al. (2003) Effects of cryopreservation on meiotic spindles of oocytes and its dynamics after thawing: clinical implications in oocyte freezing – a review article. Molecular and Cellular Endocrinology 202(1–2): 101–107.

Chen, SU, Lien, YR, Chen, HF, et al. (2005) Observational clinical follow-up of oocyte cryopreservation using a slow-freezing method with 1,2-propanediol plus sucrose followed by ICSI. Human Reproduction 20(7): 1975–1980.

Cobo, A, Kuwayama, M, Perez, S, et al. (2008) Comparison of concomitant outcome achieved with fresh and cryopreserved donor oocyte vitrified by the cryotop method. Fertility and Sterility 89(6): 1657–1664.

Coticchio, G, De Santis, L, Rossi, G, et al. (2006) Sucrose concentration influences the rate of human oocytes with normal spindle and chromosome configurations after slow-cooling cryopreservation. Human Reproduction 21(7): 1771–1776.

Edgar, DH, Gook, DA (2007) How should the clinical efficiency of oocyte cryopreservation be measured? Reproductive BioMedicine Online 14(4): 430–435.

Eppig, JJ, O’Brien, MJ, Wigglesworth, K, et al. (2009) Effect of in vitro maturation of mouse oocytes on the health and lifespan of adult offspring. Human Reproduction 24(4): 922–928.

Gook, DA, Osborn, SM, Bourne, H, Johnston, WIH (1994) Fertilization of human oocytes following cryopreservation: normal karyotypes and absence of stray chromosomes. Human Reproduction 9: 684–691.

Gook, DA, Osborn, SM, Johnston, WIH (1993) Cryopreservation of mouse and human oocytes using 1,2-propanediol and the configuration of the meiotic spindle. Human Reproduction 8: 1101–1109.

Gook, DA, Osborn, SM, Johnston, WIH (1995a) Parthenogenetic activation of human oocytes following cryopreservation using 1,2-propanediol. Human Reproduction 10: 654–658.

Gook, DA, Schiewe, MC, Osborn, SM, et al. (1995b) Intracytoplasmic sperm injection and embryo development of human oocytes cryopreserved using 1,2-propanediol. Human Reproduction 10: 2637–2641.

Hong, S, Sepilian, V, Chung, H, Kim, T (2009) Cryopreserved human blastocysts after vitrification result in excellent implantation and clinical pregnancy rates Fertility and Sterility 92(6): 2062–2064.

Huang, J, Chen, H, Tan, S, Chian, R (2007) Effect of choline-supplemented sodium-depleted slow freezing versus vitrification on mouse oocytes meiotic spindles and chromosome abnormalities. Fertility and Sterility 88(2): 1093–1110.

Kuleshova, L, Gianaroli, L, Magli, C, Ferraretti, A, Trounson, A (1999) Birth following vitrification of a small number of human oocytes: case report. Human Reproduction 14: 3077–3079.

Kuwayama, M, Vajta, G, Kato, O, Leibo, SP (2005) Highly efficient vitrification method for cryopreservation of human oocytes. Reproductive BioMedicine Online 11(3): 300–308.

Lane, M, Bavister, BD, Lyons, EA, Forest, KT (1999) Containerless vitrification of mammalian oocytes and embryos: adapting a proven method for flash-cooling protein crystals to the cryopreservation of live cells. Nature Biotechnology 17: 1234–1236.

Nottola, S, Coticchio, G, De Santis, L, et al. (2008) Ultrastructure of human mature oocytes after slow cooling cryopreservation with ethylene glycol. Reproductive BioMedicine Online 17(3): 368–377.

Noyes, N, Porcu, E, Borini, A (2009) Over 900 oocyte cryopreservation babies born with no apparent increase in congenital anomalies. Reproductive BioMedicine Online 18(6): 769–776.

Parmegiani, L, Bertocci, F, Garello, C, Salvarani, MC, Tambuscio, G, Fabbri, R (2009) Efficiency of human oocyte slow freezing: results from five assisted reproduction centres. Reproductive BioMedicine Online 18(3): 352–359.

Parmegiani, L, Cognigni, GE, Bernardi, S, et al. (2008) Freezing within 2 h from oocyte retrieval increases the efficiency of human oocyte cryopreservation when using a slow freezing/rapid thawing protocol with high sucrose concentration. Human Reproduction 23(8): 1771–1777.

Paynter, SJ, Borini, A, Bianchi, V, et al. (2005) Volume changes of mature human oocytes on exposure to cryoprotectant solutions used in slow cooling procedures. Human Reproduction 20(5): 1194–1199.

Pickering, SJ, Braude, PR, Johnson, MH, Cant, A, Currie, J (1990) Transient cooling to room temperature can cause irreversible disruption of the meiotic spindle in the human oocyte. Fertility and Sterility 54: 102–108.

Porcu, E, Fabbri, R, Seracchioli, R, et al. (1997) Birth of a healthy female after intracytoplasmic sperm injection of cryopreserved human oocytes. Fertility and Sterility 68: 724–726.

Rienzi, L, Martinez, F, Ubaldi, F, et al. (2004) Polscope analysis of meiotic spindle changes in living metaphase II human oocytes during the freezing and thawing procedures. Human Reproduction 19(3): 655–659.

Sereni, E, Bonu, M, Borini, A (2000) High survival rates after cryopreservation of human prophase oocytes. Fertility and Sterility 74(Suppl. 1): S161.

Stachecki, JJ, Cohen, J, Willadsen, SM (1999) Cryopreservation of mouse oocytes: the effect of replacing sodium with choline in the freezing medium. Cryobiology 37: 346–354.

Stachecki, J, Cohen, J, Garrisi, J, Munné, S, Willadsen, SM (2006) Cryopreservation of unfertilized human oocytes. Reproductive BioMedicine Online 13(2): 222–227.

Van den Abbeel, E, Schneider, U, Liu, J, et al. (2007) Osmotic responses and tolerance limits to changes in external osmolalities, and oolemma permeability characteristics, of human in vitro matured MII oocytes. Human Reproduction 22(7): 1959–1972.

Yoon, TK, Kim, TJ, Park, SE, et al. (2003) Live births after vitrification of oocytes in a stimulated in vitro fertilization-embryo transfer program. Fertility and Sterility 79(6): 1323–1326.

Amorim, CA, Curaba, M, Van Langendonckt, A, Dolmans, MM, Donnez, J (2011) Vitrification as an alternative means of cryopreserving ovarian tissue. Reproductive BioMedicine Online 23: 160–186.

Amorim, CA, Dolmans, MM, David, A, et al. (2012) Vitrification and xenografting of human ovarian tissue. Fertility and Sterility 98: 1291–1298.e1–2.

Andersen, CY, Rosendahl, M, Byskov, AG, et al. (2008) Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Human Reproduction 23(10): 2266–2272.

Anderson, RA, Wallace, WHB, Telfer, EE (2017) Ovarian tissue cryopreservation for fertility preservation: clinical and research perspectives. Human Reproduction Open 1: hox001, https://doi.org/10.1093/hropen/hox001.

Chen, SU, Chien, CL, Wu, MY, et al. (2006) Novel direct cover vitrification for cryopreservation of ovarian tissues increases follicle viability and pregnancy capability in mice. Human Reproduction 21(11): 2794–2800.

Chian, RC, Uzelac, PS, Nargund, G (2013) In vitro maturation of human immature oocytes for fertility preservation. Fertility and Sterility 99: 1173–1181.

Cox, SL, Shaw, J, Jenkin, G (1996) Transplantation of cryopreserved fetal ovarian tissue to adult recipients in mice. Journal of Reproduction and Fertility 107(2): 315–322.

Demeestere, I, Simon, P, Buxant, F, 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. Human Reproduction 21(8): 2010–2014.

Demeestere, I, Simon, P, Emiliani, S, Delbaere, A, Englert, Y (2007) Fertility preservation: successful transplantation of cryopreserved ovarian tissue in a young patient previously treated for Hodgkin’s disease. Oncologist 12(12): 1437–1442.

Demirci, B, Lornage, J, Salle, B, et al. (2003) The cryopreservation of ovarian tissue: uses and indications in veterinary medicine. Theriogenology 60(6): 999–1010.

Dolmans, MM, Donnez, J, Camboni, A, et al. (2009) IVF outcome in patients with orthotopically transplanted ovarian tissue. Human Reproduction 24(11): 2778–2787.

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. Journal of Assisted Reproduction and Genetics 32: 1167–1170.

Donnez, J, Dolmans, MM (2017) Fertility preservation in women. New England Journal of Medicine 377: 1657–1665.

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

Donnez, J, Dolmans, MM, Pellicer, A, et al. (2013) Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertility and Sterility 99(6): 1503–1513.

Donnez, J, Jadoul, P, Squifflet, J, et al. (2009) Cryopreservation and autotransplantation of human ovarian tissue prior to cytotoxic therapy – a technique in its infancy but already successful in fertility preservation. European Journal of Cancer 45(9): 1547–1553.

Donnez, J, Martinez-Madrid, B, Jadou, Pl, et al. (2006) Ovarian tissue cryopreservation and transplantation: a review. Human Reproduction Update 12: 519–535.

Gellert, SE, Pors, SE, Kristensen, SG, Bay-Bjørn, AM, Ernst, E, Yding Andersen, C. (2018) Transplantation of frozen-thawed ovarian tissue: an update on worldwide activity published in peer-reviewed papers and on the Danish cohort. Journal of Assisted Reproduction and Genetics 35: 561–570.

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. Human Reproduction 14: 2061–2068.

Gosden, RG (2002) Gonadal tissue cryopreservation and transplantation. Reproductive BioMedicine Online 4(Suppl. 1): 64–67.

Gosden, RG, Oktay, K, Radford, JA, et al. (1997) Ovarian tissue banking. Human Reproduction Update 3: CD-ROM, item 1, video.

Hovatta, O (2004) Cryopreservation and culture of human ovarian cortical tissue containing early follicles. European Journal of Obstetrics, Gynecology, and Reproductive Biology 113(Suppl. 1): S50–54.

Huang, L, Mo, Y, Wang, W, Li, Y, Zhang, Q, Yang, D (2008) Cryopreservation of human ovarian tissue by solid-surface vitrification. European Journal of Obstetrics, Gynecology and Reproductive Biology 139(2): 193–198.

Isachenko, V, Isachenko, E, Kreienberg, R, Woriedh, M, Weiss, J (2010) Human ovarian tissue cryopreservation: quality of follicles as a criteria of effectiveness. Reproductive BioMedicine Online 20(4): 441–442.

Isachenko, V, Isachenko, E, Reinsberg, J, et al. (2007) Cryopreservation of human ovarian tissue: comparison of rapid and conventional freezing. Cryobiology 55(3): 261–268.

Isachenko, V, Lapidus, I, Isachenko, E, et al. (2009) Human ovarian tissue vitrification versus conventional freezing: morphological, endocrinological, and molecular biological evaluation. Reproduction 138(2): 319–327.

Kader, A, Biscotti, C, Agarwal, A, Sharma, R, Falcone, T (2008) Comparison of post-warming degeneration and apoptosis of porcine ovarian tissue following vitrification using the Ohio-Cryo device and slow cryopreservation. Fertility and Sterility 90: S288–S288.

Kagawa, N, Kuwayama, M, Silber, S, et al. (2008) Successful vitrification method for bovine and human ovarian tissue: the cryotissue method. Human Reproduction 23(Suppl. 1): 145.

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

Kim, SS, Battaglia, DE, Soules, MR (2001) The future of human ovarian cryopreservation and transplantation. Fertility and Sterility 75: 1049–1056.

Kim, SS, Lee, WS, Chung, MK, et al. (2009) Long-term ovarian function and fertility after heterotopic autotransplantation of cryobanked human ovarian tissue: Eight-year experience in cancer patients. Fertility and Sterility 91(6): 2349–2354.

Li, YB, Zhou, CQ, Yang, GF, Wang, Q, Dong, Y (2007) Modified vitrification method for cryopreservation of human ovarian tissues. Chinese Medical Journal (Engl.) 120(2): 110–114.

Martinez-Madrid, B, Dolmans, MM, Van Langendonckt, A, Defrère, S, Donnez, J (2004) Freeze-thawing intact human ovary with its vascular pedicle with a passive cooling device. Fertility and Sterility 82(5): 1390–1394.

McLaughlin, MM, Albertini, DF, Wallace, DHB, et al. (2018) Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system Molecular Human Reproduction 24(3): 135–142.

Newton, H, Aubard, Y, Rutherford, A, Sharma, V, Gosden, RG (1996) Low temperature storage and grafting of human ovarian tissue. Human Reproduction 11: 487–491.

Newton, H, Fisher, J, Arnold, JR, et al. (1998) Permeation of human ovarian tissue with cryoprotective agents in preparation for cryopreservation. Human Reproduction 13: 376–380.

Nugent, D, Meirow, D, Brook, PF, Aubard, Y, Gosden, RG (1997) Transplantation in reproductive medicine: previous experience, present knowledge, and future prospects. Human Reproduction Update 3: 267–280.

Nugent, D, Newton, H, Gosden, RG, Rutherford, AJ (1998) Investigation of follicle survival after human heterotopic grafting. Human Reproduction 13(1): 22–23.

Oktay, K, Newton, H, Aubard, Y, Salha, O, Gosden, RG (1998) Cryopreservation of immature human oocytes and ovarian tissue: an emerging technology? Fertility and Sterility 69: 1–7.

Oktay, K, Nugent, D, Newton, H (1997) Isolation and characterisation of primordial follicles from fresh and cryopreserved human ovarian tissue. Fertility and Sterility 67: 481–486.

Onions, VJ, Webb, R, McNeilly, AS, Campbell, BK (2009) Ovarian endocrine profile and long-term vascular patency following heterotopic autotransplantation of cryopreserved whole ovine ovaries. Human Reproduction 24(11): 2845–2855.

Picton, HM, Kim, SS, Gosden, RG (2000) Cryopreservation of gonadal tissue and cells. British Medical Bulletin 56: 603–615.

Potdar, N, Gelbaya, TA, Nardo, LG (2014) Oocyte vitrification in the 21st century and post-warming fertility outcomes: a systematic review and meta-analysis. Reproductive Biomedicine Online 29(2): 159–176.

Shaw, J, Trounson, AO (1997) Ovarian banking for cancer patients: oncological implications in the replacement of ovarian tissue. Human Reproduction 12: 403–405.

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

Silber, S, Pineda, J, Lenahan, K, et al. (2015) Fresh and cryopreserved ovary transplantation and resting follicle recruitment. Reproductive Biomedicine Online 30(6): 643–650.

Smitz, J, Dolmans, MM, Donnez, J, et al. (2010) Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation. Human Reproduction Update 16: 395–414.

Tryde Schmidt, KL, Yding Andersen, C, Starup, J, et al. (2004) Orthotopic autotransplantation of cryopreserved ovarian tissue to a woman cured of cancer – follicular growth, steroid production and oocyte retrieval. Reproductive BioMedicine Online 8(4): 448–453.

von Wolff, M, Dittrich, R, Liebenthron, J, et al (2015) Fertility-preservation counselling and treatment for medical reasons: data from a multinational network of over 5000 women. Reproductive BioMedicine Online 31: 605–612.

Agha-Rahimi, A, Khalili, MA, Nabi, A, Ashourzadeh, S (2014) Vitrification is not superior to rapid freezing of normozoospermic spermatozoa: effects on sperm parameters, DNA fragmentation and hyaluron binding. Reproductive BioMedicine Online 28: 352–358.

Gilbert, K, Nangia, AK, Dupree, JM, Smith, JF, Mehta, A (2018) Fertility preservation for men with testicular cancer: is sperm cryopreservation cost effective in the era of assisted reproductive technology? Urological Oncology 36(3): 92e1–92e9.

Gilmore, JA, Liu, J, Gao, DY, Critser, JK (1997) Determination of optimal cryoprotectants and procedures for their addition and removal from human spermatozoa. Human Reproduction 12: 12–18.

Giraud, MN, Motta, C, Boucher, D, Grizard, G (2000) Membrane fluidity predicts the outcome of cryopreservation of human spermatozoa. Human Reproduction 15: 2160–2164.

Hammerstedt, RH, Graham, JK, Nolan, JP (1990) Cryopreservation of human sperm. Journal of Andrology 11(1): 73–88.

Kawai, K, Nishiyama, H (2018) Preservation of fertility of adult male cancer patients treated with chemotherapy. International Journal of Oncology Oct 23. doi: 10.1007/s10147-018-1333-0 [Epub ahead of print].

Leibo, SP, Bradley, L (1999) Comparative cryobiology of mammalian spermatozoa. In: Gagnon, C (ed.) The Male Gamete: From Basic Knowledge to Clinical Applications. Cache River Press, Vienna, IL, pp. 501–516.

Mahadevan, M, Trounson, A (1983) Effects of CPM and dilution methods on the preservation of human spermatozoa. Andrologia 15: 355–366.

McLaughlin, EA, Ford, WCL, Hill, MGR (1990) A comparison of the freezing of human semen in the uncirculated vapour above liquid nitrogen and in a commercial semi-programmable freezer. Human Reproduction 5: 734–738.

Meirow, D, Schenker, JG (1995) Cancer and male infertility. Human Reproduction 10: 2017–2022.

Morris, GJ (2006) Rapidly cooled human sperm: no evidence of intracellular ice formation. Human . Reproduction 21: 2075–2083.

Morris, GJ, Acton, E, Murray, BJ, Fonseca, F (2012) Freezing injury: the special case of the sperm cell. Cryobiology 64: 71–80.

Polge, C, Smith, AU, Parkes, AS (1949) Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature 164: 666–667.

Stanic, P, Tandara, M, Sonicki, Z, et al. (2000) Comparison of protective media and freezing techniques for cryopreservation of human semen. European Journal of Obstetrics, Gynecology and Reproductive Biology 91: 65–70.

Ukita, Y, Wakimoto, Y, Sugiyama, Y, et al. (2018) Fertility preservation and pregnancy outcomes in adolescent and young adult male patients with cancer. Reproductive BioMedicine Online 17(4): 449–453.

Van den Berg, M (1998) Sample preparation. In: Elder, K, Elliott, T (eds.) The Use of Epididymal and Testicular Sperm in IVF. WorldWide Conferences on Reproduction Biology. Ladybrook Publishing, Australia, pp. 51–54.

Walmsley, R, Cohen, J, Ferrara-Congedo, T, Reing, A, Garrisi, J (1999) The first births and ongoing pregnancies associated with sperm cryopreservation within evacuated egg zonae. Human Reproduction 13: 61–70.

Watson, PF (2000) The causes of reduced fertility with cryopreserved semen. Animal Reproduction Science 60: 481–492.

Wyns, C, Curaba, M, Vanabelle, B, Van Langendonckt, A, Donnez, J (2010) Options for fertility preservation in prepubertal boys. Human Reproduction Update 16(3): 312–328.