Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-27T19:47:41.093Z Has data issue: false hasContentIssue false
  • English
  • Français

Restoring fertility after ovarian tissue cryopreservation: a half century of research

Published online by Cambridge University Press:  31 October 2012

Franciele Osmarini Lunardi ,
Valdevane Rocha Araújo ,
Marcelo Picinin Bernuci ,
Luciane Osmarini Lunardi ,
Raphael Fernando Braga Gonçalves ,
Adeline de Andrade Carvalho ,
José Ricardo de Figueiredo  and
Ana Paula Ribeiro Rodrigues
Franciele Osmarini Lunardi*
Affiliation:
Laboratory of Manipulation of Oocytes and Ovarian Pre-antral Follicles (LAMOFOPA), Faculty of Veterinary of Ceará State University, Fortaleza, CE, Brazil.
Valdevane Rocha Araújo
Affiliation:
Laboratory of Manipulation of Oocytes and Ovarian Pre-antral Follicles (LAMOFOPA), Veterinary Faculty of Ceará State University, Fortaleza, CE, Brazil.
Marcelo Picinin Bernuci
Affiliation:
Department of Gynecology and Obstetrics, Clinical Hospital of the Faculty of Medicine of Ribeirao Preto of Sao Paulo University, Ribeirao Preto, SP, Brazil.
Luciane Osmarini Lunardi
Affiliation:
Faculty of Biosciences of Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, RS, Brazil.
Raphael Fernando Braga Gonçalves
Affiliation:
Laboratory of Manipulation of Oocytes and Ovarian Pre-antral Follicles (LAMOFOPA), Veterinary Faculty of Ceará State University, Fortaleza, CE, Brazil.
Adeline de Andrade Carvalho
Affiliation:
Laboratory of Manipulation of Oocytes and Ovarian Pre-antral Follicles (LAMOFOPA), Veterinary Faculty of Ceará State University, Fortaleza, CE, Brazil.
José Ricardo de Figueiredo
Affiliation:
Laboratory of Manipulation of Oocytes and Ovarian Pre-antral Follicles (LAMOFOPA), Veterinary Faculty of Ceará State University, Fortaleza, CE, Brazil.
Ana Paula Ribeiro Rodrigues
Affiliation:
Laboratory of Manipulation of Oocytes and Ovarian Pre-antral Follicles (LAMOFOPA), Veterinary Faculty of Ceará State University, Fortaleza, CE, Brazil.
*
All correspondence to: Franciele Osmarini Lunardi. Laboratory of Manipulation of Oocytes and Ovarian Pre-antral Follicles (LAMOFOPA), Faculty of Veterinary of Ceará State University, Fortaleza, CE, Brazil. Tel: + 55 85 3101 9852. Fax: + 55 85 3101 9840. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Tissue transplantation and in vitro ovarian follicle culture have been investigated as alternative techniques to restore fertility in young women who are facing fertility-threatening diseases or treatments following ovarian tissue cryopreservation. Although transplants of fresh or frozen ovarian tissue have successfully yielded healthy live births in different species including humans, the risks of reintroducing cancer cells back into the patient, post treatment, have limited its clinical purpose. The in vitro ovarian follicle culture minimizes these risks and provides a way to harvest more mature oocytes, however its clinical translation has yet to be determined. Not only is it possible for tissue cryopreservation to safeguard fertility in cancer patients, this technique also allows the maintenance of germplasm banks for animals of high commercial value or for those animals that are at risk of extinction. Given the importance of managing female genetic material, this paper reviews the progress of the methods used to preserve and restore female fertility in different species to demonstrate the results obtained in the past 50 years of research, the current achievements and the future directions on this field.

Keywords

Fertility preservationIn vitro follicle cultureOvarian tissue transplantSlow freezingVitrification
Type
Research Article
Information
Zygote , Volume 21 , Issue 4 , November 2013 , pp. 394 - 405
Copyright
Copyright © Cambridge University Press 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abir, R., Franks, S., Mobberley, M.A., Moore, P.A., Margara, R.A. & Winston, R.M.L. (1997). Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertil. Steril. 68, 682–8.CrossRefGoogle ScholarPubMed
Almodin, C.G., Minguetti-Camara, V.C., Meister, H., Ceschin, A.P., Kriger, E. & Ferreira, J. (2004a). Recovery of natural fertility after grafting of cryopreserved germinative tissue in ewes subjected to radiotherapy. Fertil. Steril. 81, 160–4.CrossRefGoogle ScholarPubMed
Almodin, C.G., Minguetti-Camara, V.C., Meister, H., Ferreira, J., Franco, R.L., Cavalcante, A.A., Radaelli, M.R.M., Bahls, A.S., Moron, A.F. & Murta, C.G.V. (2004b). Recovery of fertility after grafting of cryopreserved germinative tissue in female rabbits following radiotherapy. Hum. Reprod. 19, 1287–93.CrossRefGoogle ScholarPubMed
Amorim, C.A., Rondina, D., Rodrigues, A.P.R., Goncalves, P.B.D., de Figueiredo, J.R. & Giorgetti, A. (2004). Cryopreservation of isolated ovine primordial follicles with propylene glycol and glycerol. Fertil. Steril. 81, 735–40.CrossRefGoogle ScholarPubMed
Amorim, C.A., Van Langendonckt, A., David, A., Dolmans, M.M. and 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. Hum. Reprod. 24, 92–9.CrossRefGoogle Scholar
Andersen, C.Y., Rosendahl, M., Byskov, A.G., Loft, A., Ottosen, C., Dueholm, M., Schmidt, K.L.T., Andersen, A.N. & Ernst, E. (2008). Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Hum. Reprod. 23, 2266–72.CrossRefGoogle ScholarPubMed
Arunakumari, G., Shanmugasundaram, N. & Rao, V.H. (2010). Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74, 884–94.CrossRefGoogle ScholarPubMed
Aubard, Y., Piver, P., Pech, J.C., Galinat, S. & Teissier, M.P. (2001). Ovarian tissue cryopreservation and gynecologic oncology: a review. Eur. J. Obstet. Gynecol. Reprod. Biol. 97, 5–14.CrossRefGoogle ScholarPubMed
Bagchi, A., Woods, E.J. & Critser, J.K. (2008). Cryopreservation and vitrification: recent advances in fertility preservation technologies. Expert Rev. Med. Devices 5, 359–70.CrossRefGoogle ScholarPubMed
Bagis, H., Akkoq, T., Tas, A. & Aktoprakligil, D. (2008). Cryogenic effect of antifreeze protein on transgenic mouse ovaries and the production of live offspring by orthotopic transplantation of cryopreserved mouse ovaries. Mol. Reprod. Dev. 75, 608–13.CrossRefGoogle ScholarPubMed
Bordes, A., Lornage, J., Demirci, B., Franck, M., Courbiere, B., Guerin, J.F. & Salle, B. (2005). Normal gestations and live births after orthotopic autograft of vitrified-warmed hemi-ovaries into ewes. Hum. Reprod. 20, 2745–8.CrossRefGoogle ScholarPubMed
Borges, E.N., Silva, R.C., Futino, D.O., Rocha, C.M.C., Amorim, C.A., Bao, S.N. & Lucci, C.M. (2009). Cryopreservation of swine ovarian tissue: Effect of different cryoprotectants on the structural preservation of preantral follicle oocytes. Cryobiology 59, 195–200.CrossRefGoogle ScholarPubMed
Candy, C.J., Wood, M.J. & Whittingham, D.G. (1997). Effect of cryoprotectants on the survival of follicles in frozen mouse ovaries. J. Reprod. Fertil. 110, 11–9.CrossRefGoogle ScholarPubMed
Candy, C.J., Wood, M.J. & Whittingham, D.G. (2000). Restoration of a normal reproductive lifespan after grafting of cryopreserved mouse ovaries. Hum. Reprod. 15, 1300–4.CrossRefGoogle ScholarPubMed
Carvalho, A.A., Faustino, L.R., Silva, C.M.G., Castro, S.V., Luz, H.K.M., Rossetto, R., Lopes, C.A.P., Campello, C.C., Figueiredo, J.R., Rodrigues, A.P.R. & Costa, A.P.R. (2011). Influence of vitrification techniques and solutions on the morphology and survival of preantral follicles after in vitro culture of caprine ovarian tissue. Theriogenology 76, 933–41.CrossRefGoogle ScholarPubMed
Castro, S.V., Carvalho, A.D., da Silva, C.M.G., Faustino, L.R., de Figueiredo, J.R. & Rodrigues, A.P.R. (2011). Intracellular cryoprotectant agents: characteristics and use of ovarian tissue and oocyte cryopreservation. Acta Scientiae Veterinariae 39.Google Scholar
Celestino, J.J.D., dos Santos, R.R., Lopes, C.A.P., Martins, F.S., Matos, M.H.T., Melo, M.A.P., Bao, S.N., Rodrigues, A.P.R., Silva, J.R.V. & de Figueiredo, J.R. (2008). Preservation of bovine preantral follicle viability and ultra-structure after cooling and freezing of ovarian tissue. Anim. Reprod. Sci. 108, 309–18.CrossRefGoogle ScholarPubMed
Chen, S.U., Chien, C.L., Wu, M.Y., Chen, T.H., Lai, S.M., Lin, C.W. & Yang, Y.S. (2006). Novel direct cover vitrification for cryopreservation of ovarian tissues increases follicle viability and pregnancy capability in mice. Hum. Reprod. 21, 2794–800.CrossRefGoogle ScholarPubMed
Cox, S.L., Shaw, J. & Jenkin, G. (1996). Transplantation of cryopreserved fetal ovarian tissue to adult recipients in mice. J. Reprod. Fertil. 107, 315–22.CrossRefGoogle ScholarPubMed
Demeestere, I., Simon, P., Emiliani, S., Delbaere, A. & Englert, Y. (2006). Options to preserve fertility before oncological treatment: Cryopreservation of ovarian tissue and its clinical application. Acta Clinica Belgica 61, 259–63.CrossRefGoogle ScholarPubMed
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, 1437–42.CrossRefGoogle Scholar
Demirci, B., Lornage, J., Salle, B., Poirel, M.T., Guerin, J.F. & Franck, M. (2003). The cryopreservation of ovarian tissue: uses and indications in veterinary medicine. Theriogenology 60, 999–1010.CrossRefGoogle ScholarPubMed
Donnez, J. & Dolmans, M.M. (2010). Cryopreservation and transplantation of ovarian tissue. Clin. Obstet. Gynecol. 53, 787–96.CrossRefGoogle ScholarPubMed
Donnez, J., Dolmans, M.M., Demylle, D., Jadoul, P., Pirard, C., Squifflet, J., Martinez-Madrid, B. & Van Langendonckt, A. (2004). Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet 364, 1405–10.CrossRefGoogle ScholarPubMed
Donnez, J., Squifflet, J., Jadoul, P., Demylle, D., Cheron, A.C., Van Langendonckt, A. & Dolmans, M.M. (2011). Pregnancy and live birth after autotransplantation of frozen–thawed ovarian tissue in a patient with metastatic disease undergoing chemotherapy and hematopoietic stem cell transplantation. Fertil. Steril. 95.CrossRefGoogle Scholar
Eppig, J.J. & O'Brien, M.J. (1996). Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54, 197–207.CrossRefGoogle ScholarPubMed
Ernst, E., Bergholdt, S., Jorgensen, J.S. & Andersen, C.Y. (2010). The first woman to give birth to two children following transplantation of frozen/thawed ovarian tissue. Hum. Reprod. 25, 1280–1.CrossRefGoogle ScholarPubMed
Faustino, L.R., Santos, R.R., Silva, C.M.G., Pinto, L.C., Celestino, J.J.H., Campello, C.C., Figueiredo, J.R. & Rodrigues, A.P.R. (2010). Goat and sheep ovarian tissue cryopreservation: effects on the morphology and development of primordial follicles and density of stromal cell. Anim. Reprod. Sci. 122, 90–7.CrossRefGoogle ScholarPubMed
Gosden, R.G., Baird, D.T., Wade, J.C. & Webb, R. (1994). Restoration of fertility to oophorectomized sheep by ovarian autografts stored at –196°C. Hum. Reprod. 9, 597–603.CrossRefGoogle Scholar
Gunasena, K.T., Villines, P.M., Critser, E.S. & Critser, J.K. (1997). Live births after autologous transplant of cryopreserved mouse ovaries. Hum. Reprod. 12, 101–6.CrossRefGoogle ScholarPubMed
Gutierrez, C.G., Ralph, J.H., Telfer, E.E., Wilmut, I. & Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod. 62, 1322–8.CrossRefGoogle ScholarPubMed
Hani, T., Tachibe, T., Shingai, S., Kamada, N., Ueda, O. & Jishage, K. (2006). Fertility of mice receiving vitrified adult mouse ovaries. Reproduction 131, 681–7.CrossRefGoogle ScholarPubMed
Hasegawa, A., Mochida, N., Ogasawara, T. & Koyama, K. (2006). Pup birth from mouse oocytes in preantral follicles derived from vitrified and warmed ovaries followed by in vitro growth, in vitro maturation, and in vitro fertilization. Fertil. Steril. 86, 1182–92.CrossRefGoogle ScholarPubMed
Hovatta, O., Silye, R., Krausz, T., Abir, R., Margara, R., Trew, G., Lass, A. & Winston, R.M.L. (1996). Cryopreservation of human ovarian tissue using dimethylsulphoxide and propanediol-sucrose as cryoprotectants. Hum. Reprod. 11, 1268–72.CrossRefGoogle ScholarPubMed
Imhof, M., Bergmeister, H., Lipovac, M., Rudas, M., Hofstetter, G. & Huber, J. (2006). Orthotopic microvascular reanastomosis of whole cryopreserved ovine ovaries resulting in pregnancy and live birth. Fertil. Steril. 85, 1208–15.CrossRefGoogle ScholarPubMed
Kagawa, N., Kuwayama, M., Nakata, K., Vajta, G., Silber, S., Manabe, N. & Kato, O. (2007). Production of the first offspring from oocytes derived from fresh and cryopreserved pre-antral follicles of adult mice. Reprod. Biomed. Online 14, 693–9.CrossRefGoogle ScholarPubMed
Liu, L.J., Xie, X.Y., Zhang, R.Z., Xu, P., Bujard, H. & Jun, M. (2008a). Reproduction and fertility in wild-type and transgenic mice after orthotopic transplantation of cryopreserved ovaries from 10-d-old mice. Lab. Anim. 37, 353–7.CrossRefGoogle Scholar
Liu, L., Wood, G.A., Morikawa, L., Ayearst, R., Fleming, C. & McKerlie, C. (2008b). Restoration of fertility by orthotopic transplantation of frozen adult mouse ovaries. Hum. Reprod. 23, 122–8.CrossRefGoogle ScholarPubMed
Lornage, J., Courbière, B., Mazoyer, C., Odagescu, V., Baudot, A., Bordes, A., Poirel, M.T., Franck, M. & Salle, B. (2006). Ovarian tissue vitrification: cortex and whole ovary in sheep. Gynecol. Obstet. Fertil. 34, 746–53.CrossRefGoogle ScholarPubMed
Lovelock, J.E. (1953). Het mechanism of the protective action of glycerol against haemolysis by freezing and thawing. Biochim. Biophys. Acta 11, 28–36.CrossRefGoogle Scholar
Lovelock, J.E. (1954). The protective action of neutral solutes against haemolysis by freezing and thawing. Biochem. J. 56, 265–70.CrossRefGoogle ScholarPubMed
Luyet, B. & Hodapp, E.L. (1938). Revival of frog's spermatozoa vitrified in liquid air. Proc. Soc. Exp. Biol. Med. 39, 433–5.CrossRefGoogle Scholar
Luz, V.B., Santos, R.R., Pinto, L.C., Soares, A.A.X., Celestino, J.J.H., Mafezoli, J., Campello, C.C., Figueiredo, J.R. & Rodrigues, A.P.R. (2009). Dimethyl sulfoxide perfusion in caprine ovarian tissue and its relationship with follicular viability after cryopreservation. Fertil. Steril. 91, 1513–5.CrossRefGoogle ScholarPubMed
Magalhães, D.M., Duarte, A.B.G., Araujo, V.R., Brito, I.R., Soares, T.G., Lima, I.M.T., Lopes, C.A.P., Campello, C.C., Rodrigues, A.P.R. & Figueiredo, J.R. (2011). In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology 75, 182–8.CrossRefGoogle ScholarPubMed
Matzuk, M.M., Burns, K.H., Vivieros, M.M. & Eppig, J.J. (2002). Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178–80.CrossRefGoogle ScholarPubMed
Meirow, D., Lewis, H., Nugent, D. & Epstein, M. (1999). Subclinical depletion of primordial follicular reserve in mice treated with cyclophosphamide: clinical importance and proposed accurate investigative tool. Hum. Reprod. 14, 1903–7.CrossRefGoogle ScholarPubMed
Meirow, D., Levron, J., Eldar-Geva, T., Hardan, I., Fridman, E., Zalel, Y., Schiff, E. & Dor, J. (2005). Pregnancy after transplantation of cryopreserved ovarian tissue in a patient with ovarian failure after chemotherapy. New Eng. J. Med. 353, 318–21.CrossRefGoogle Scholar
Migishima, F., Suzuki-Migishima, R., Song, S. Y., Kuramochi, T., Azuma, S., Nishijima, M. & Yokoyama, M. (2003). Successful cryopreservation of mouse ovaries by vitrification. Biol. Reprod. 68, 881–7.CrossRefGoogle ScholarPubMed
Newton, H. & Illingworth, P. (2001). In-vitro growth of murine pre-antral follicles after isolation from cryopreserved ovarian tissue. Hum. Reprod. 16, 423–9.CrossRefGoogle ScholarPubMed
Newton, H., Aubard, Y., Rutherford, A., Sharma, V. & Gosden, R. (1996). Low temperature storage and grafting of human ovarian tissue. Hum. Reprod. 11, 1487–91.CrossRefGoogle ScholarPubMed
Nisolle, M., Casanas-Roux, F., Qu, J.P., Motta, P. & Donnez, J. (2000). Histologic and ultrastructural evaluation of fresh and frozen-thawed human ovarian xenografts in nude mice. Fertil. Steril. 74, 122–9.CrossRefGoogle ScholarPubMed
O'Brien, M.J., Pendola, J.K. & Eppig, J.J. (2003). A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod. 68, 1682–6.CrossRefGoogle ScholarPubMed
Oktay, K., Buyuk, E., Veeck, L., Zaninovic, N., Xu, K.P., Takeuchi, T., Opsahl, M. & Rosenwaks, Z. (2004). Embryo development after heterotopic transplantation of cryopreserved ovarian tissue. Lancet 363, 837–40.CrossRefGoogle ScholarPubMed
Oktay, K., Turkcuoglu, I. & Rodriguez-Wallberg, K.A. (2011). Four spontaneous pregnancies and three live births following subcutaneous transplantation of frozen banked ovarian tissue: What is the explanation? Fertil. Steril. 95.CrossRefGoogle ScholarPubMed
Parkes, A.S. (1955). Radiation sensitivity of ovarian tissue at –79°C. Nature 176, 1216–7.CrossRefGoogle Scholar
Parkes, A.S. (1956). Grafting of mouse ovarian tissue after freezing and thawing. Journal of Endocrinology 14, R30–1.Google ScholarPubMed
Parkes, A.S. (1957). Viability of ovarian tissue after freezing. Proc. Roy. Soc. Lond. Series B – Biol. Sci. 147, 520–8.Google ScholarPubMed
Parkes, A.S. & Smith, A.U. (1953). Regeneration of rat ovarian tissue grafted after exposure to low temperatures. Proc. Roy. Soc. Lond. Series B – Biol. Sci. 140, 455–70.Google ScholarPubMed
Parrott, D.M.V. (1960). The fertility of mice with orthotopic ovarian grafts derived from frozen tissue. J. Reprod. Fertil. 1, 230–41.CrossRefGoogle Scholar
Picton, H.M., Danfour, M.A., Harris, S.E., Chambers, E.L. & Huntriss, J. (2002). Growth and maturation of oocytes in vitro. Reproduction 61, 445–62.Google Scholar
Polge, C., Smith, A.U. & Parkes, A.S. (1949). Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature 164, 666.CrossRefGoogle ScholarPubMed
Rodrigues, A.P.R., Amorim, C.A., Costa, S.H.F., Matos, M.H.T., Santos, R.R., Lucci, C.M., Bao, S.N., Ohashi, O.M. & Figueiredo, J.R. (2004a). Cryopreservation of caprine ovarian tissue using dimethylsulphoxide and propanediol. Anim. Reprod. Sci. 84, 211–27.CrossRefGoogle ScholarPubMed
Rodrigues, A.P.R., Amorim, C.A., Costa, S.H.F., Matos, M.H.T., Santos, R.R., Lucci, C.M., Bao, S.N., Ohashi, O.M. & Figueiredo, J.R. (2004b). Cryopreservation of caprine ovarian tissue using glycerol and ethylene glycol. Theriogenology 61, 1009–24.CrossRefGoogle ScholarPubMed
Roux, C., Amiot, C., Agnani, G., Aubard, Y., Rohrlich, P.S. & 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.CrossRefGoogle Scholar
Rowley, J.A., Madlambayan, G. & Mooney, D.J. (1999). Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 20, 45–53.CrossRefGoogle ScholarPubMed
Salle, B., Demirci, B., Franck, M., Rudigoz, R.C., Guerin, J.F. & Lornage, J. (2002). Normal pregnancies and live births after autograft of frozen–thawed hemi-ovaries into ewes. Fertil. Steril. 77, 403–8.CrossRefGoogle ScholarPubMed
Salle, B., Demirci, B., Franck, M., Berthollet, C. & Lornage, J. (2003). Long-term follow-up of cryopreserved hemi-ovary autografts in ewes: pregnancies, births, and histologic assessment. Fertil. Steril. 80, 172–7.CrossRefGoogle ScholarPubMed
Shea, L.D., Woodruff, T.K., Lowe, M.P. (2008). Perspectives on oncofertility: preserving fertility for young cancer patients. Endocrine News 33 14–19.Google Scholar
Silber, S.J., DeRosa, M., Pineda, J., Lenahan, K., Grenia, D., Gorman, K. & Gosden, R.G. (2008). A series of monozygotic twins discordant for ovarian failure: ovary transplantation (cortical versus microvascular) and cryopreservation. Hum. Reprod. 23, 1531–7.CrossRefGoogle ScholarPubMed
Silber, S., Kagawa, N., Kuwayama, M. & Gosden, R. (2010). Duration of fertility after fresh and frozen ovary transplantation. Fertil. Steril. 94, 2191–6.CrossRefGoogle ScholarPubMed
Smith, A.U. (1950). Prevention of haemolysis during freezing and thawing of red blood-cells. Lancet 259, 910–1.CrossRefGoogle Scholar
Smitz, J, Dolmans, M.M., Donnez, J., Fortune, J.E., Hovatta, O., Jewgenow, K., Picton, H.M., Plancha, C., Shea, L.D., Stouffer, R.L., Telfer, E.E., Woodruff, T.K., Zelinski, M. B. (2010). Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation. Hum. Reprod. Update 16, 395–414.CrossRefGoogle ScholarPubMed
Snow, M., Cox, S.L., Jenkin, G. & Shaw, J. (2003). Fertility of mice following receipt of ovaries slow cooled in dimethyl sulphoxide or ethylene glycol is largely independent of cryopreservation equilibration time and temperature. Reprod. Fertil. Dev. 15, 407–14.CrossRefGoogle ScholarPubMed
Sonmezer, M. & Oktay, K. (2004). Fertility preservation in female patients. Hum. Reprod. Update 10, 251–66.CrossRefGoogle ScholarPubMed
Sonmezer, M. & Oktay, K. (2010). Orthotopic and heterotopic ovarian tissue transplantation. Best Prac. Res. Clin. Obstet. Gynaecol. 24, 113–26.CrossRefGoogle ScholarPubMed
Sztein, J., Sweet, H., Farley, J. & Mobraaten, L. (1998). Cryopreservation and orthotopic transplantation of mouse ovaries: new approach in gamete banking. Biol. Reprod. 58, 1071–4.CrossRefGoogle ScholarPubMed
Takahashi, E., Miyoshi, I. & Nagasu, T. (2001). Rescue of a transgenic mouse line by transplantation of a frozen-thawed ovary obtained postmortem. Contemp. Top. Lab. Anim. Sci. 40, 28–31.Google ScholarPubMed
Tambe, S.S. & Nandedkar, T.D. (1993). Steroidogenesis in sheep ovarian antral follicles in culture – time-course study and supplementation with a precursor. Steroids 58, 379–83.CrossRefGoogle ScholarPubMed
Telfer, E.E., McLaughlin, M., Ding, C. & Thong, K.J. (2008). A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum. Reprod. 23, 1151–8.CrossRefGoogle ScholarPubMed
Ting, A.Y., Yeoman, R.R., Lawson, M.S., Zelinski, M.B. (2011). In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Hum. Reprod. 26, 2461–72.CrossRefGoogle ScholarPubMed
Vajta, G., Holm, P., Kuwayama, M., Booth, P.J., Jacobsen, H., Greve, T. & Callesen, H. (1998). Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol. Reprod. Dev. 51, 53–8.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Wallace, W.H.B., Anderson, R.A. & Irvine, D.S. (2005). Fertility preservation for young patients with cancer: who is at risk and what can be offered? Lancet Oncol. 6, 209–18.CrossRefGoogle ScholarPubMed
Wang, X.Q., Catt, S., Pangestu, M. & Temple-Smith, P. (2009). Live offspring from vitrified blastocysts derived from fresh and cryopreserved ovarian tissue grafts of adult mice. Reproduction 138, 527–35.CrossRefGoogle ScholarPubMed
Wang, X.Q., Catt, S., Pangestu, M. & Temple-Smith, P. (2011). Successful in vitro culture of pre-antral follicles derived from vitrified murine ovarian tissue: oocyte maturation, fertilization, and live births. Reproduction 141, 183–91.CrossRefGoogle ScholarPubMed
West, E.R., Xu, M., Woodruff, T.K. & Shea, L.D. (2007). Physical properties of alginate hydrogels and their effects on in vitro follicle development. Biomaterials 28, 4439–48.CrossRefGoogle ScholarPubMed
West, E.R., Zelinski, M.B., Kondapalli, L.A., Gracia, C., Chang, J., Coutifaris, C., Critser, J., Stouffer, R.L., Shea, L.D. & Woodruff, T.K. (2009). Preserving female fertility following cancer treatment: current options and future possibilities. Ped. Blood Cancer 53, 289–95.CrossRefGoogle ScholarPubMed
Woodruff, T.K. & Snyder, K.A. (2008). Oncofertility Fertility Preservation for Cancer Survivors Series: Cancer Treatment and Research. New York: Springer, Vol. 138.Google Scholar
Xu, J., Bernuci, M.P., Lawson, M.S., Yeoman, R.R., Fisher, T.E., Zelinski, M.B. & Stouffer, R L. (2010). Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotropins and insulin. Reproduction 140, 685–97.CrossRefGoogle Scholar
Xu, J., Lawson, M.S., Yeoman, R.R., Pau, K.Y., Barrett, S.L., Zelinski, M.B. & Stouffer, R.L. (2011). Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys: effects of gonadotrophins, oxygen and fetuin. Hum. Reprod. 26, 1061–72.CrossRefGoogle ScholarPubMed
Xu, M., Kreeger, P.K., Shea, L.D. & Woodruff, T.K. (2006). Tissue-engineered follicles produce live, fertile offspring. Tissue Eng. 12, 2739–46.CrossRefGoogle ScholarPubMed
Xu, M., West-Farrell, E.R., Stouffer, R.L., Shea, L.D., Woodruff, T.K. & Zelinski, M.B. (2009a). Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol. Reprod. 81, 587–94.CrossRefGoogle ScholarPubMed
Xu, M., Barrett, S.L., West-Farrell, E., Kondapalli, L.A., Kiesewetter, S.E., Shea, L.D. & Woodruff, T.K. (2009b). In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum. Reprod. 24, 2531–40.CrossRefGoogle ScholarPubMed
Zhang, J.M., Sheng, Y., Cao, Y.Z., Wang, H.Y. & Chen, Z.J. (2011). Effects of cooling rates and ice-seeding temperatures on the cryopreservation of whole ovaries. J. Ass. Reprod. Genet. 28, 627–33.CrossRefGoogle ScholarPubMed