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Female fertility preservation strategies: cryopreservation and ovarian tissue in vitro culture, current state of the art and future perspectives

Published online by Cambridge University Press:  04 May 2016

M.A. Filatov ,
Y.V. Khramova ,
M.V. Kiseleva ,
I.V. Malinova ,
E.V. Komarova  and
M.L. Semenova
M.A. Filatov*
Affiliation:
Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory 1, bld. 12, Moscow 119991, Russia.
Y.V. Khramova
Affiliation:
Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory 1, bld. 12, Moscow 119991, Russia.
M.V. Kiseleva
Affiliation:
Medical Radiological Research Centre, Ministry of Health of the Russian Federation (MMRC), Koroleva st. 4, Obninsk 249036, Russia.
I.V. Malinova
Affiliation:
Medical Radiological Research Centre, Ministry of Health of the Russian Federation (MMRC), Koroleva st. 4, Obninsk 249036, Russia.
E.V. Komarova
Affiliation:
Medical Radiological Research Centre, Ministry of Health of the Russian Federation (MMRC), Koroleva st. 4, Obninsk 249036, Russia.
M.L. Semenova
Affiliation:
Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory 1, bld. 12, Moscow 119991, Russia.
*
All correspondence to: M.A. Filatov. Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory 1, bld. 12, Moscow 119991, Russia. Tel: +7 495 939 39 00. E-mail: maxfilat@yandex.ru
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Summary

In the present review, the main strategies of female fertility preservation are covered. Procedures of fertility preservation are necessary for women who suffer from diseases whose treatment requires the use of aggressive therapies, such as chemotherapy and radiotherapy. These kinds of therapy negatively influence the health of gametes and their progenitors. The most commonly used method of female fertility preservation is ovarian tissue cryopreservation, followed by the retransplantation of thawed tissue. Another approach to female fertility preservation that has been actively developed lately is the ovarian tissue in vitro culture. The principal methods, advantages and drawbacks of these two strategies are discussed in this article.

Keywords

CryopreservationIn vitroOncologyOvaryTissue
Type
Research Article
Information
Zygote , Volume 24 , Issue 5 , October 2016 , pp. 635 - 653
Copyright
Copyright © Cambridge University Press 2016 

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References

Abedellhafez, F., Desai, N., Abou-Setta, A., Falcone, T. & Goldfarb, J. (2010). Slow freezing, vitrification and ultra-rapid freezing of human embryos; a systematic review and meta-analysis. Reprod. Biomed. Online 2, 209–22.Google Scholar
Abir, R., Franks, S., Mobberley, M.A., Moore, P.A., Margara, R.A. & Winston, R.M. (1997). Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertil. Steril. 68, 682–8.Google Scholar
Abir, R., Roizman, P., Fisch, B., Nitke, S., Okon, E., Orvieto, R. & Ben Rafael, Z. (1999). Pilot study of isolated early human follicles cultured in collagen gels for 24 hours. Hum. Reprod. 14, 1299–301.CrossRefGoogle ScholarPubMed
Abir, R., Fisch, B., Nitke, S., Okon, E., Raz, A. & Ben Rafael, Z. (2001). Morphological study of fully and partially isolated early human follicles. Fertil. Steril. 75, 141–6.Google Scholar
Amorim, C.A., Van Langendonckt, A., David, A., Dolmans, M.M. & 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.Google Scholar
Amorim, C.A., David, A., Van Langendonckt, A., Dolmans, M.M. & Donnez, J. (2011). Vitrification of human ovarian tissue: effect of different solutions and procedures. Fertil. Steril. 95, 1094–7.CrossRefGoogle ScholarPubMed
Andersen, C.Y., Rosendahl, M., Byskov, A.G., Loft, A., Ottosen, C., Dueholm, M., Schmidt, K.L., Andersen, A.N. & Ernst, E. (2008). Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Hum. Reprod. 23, 2266–72.CrossRefGoogle ScholarPubMed
Aubard, Y., Teissier, M.P. & Baudet, J.H. (1994). Cryopreservation of the ovary and ovarian tissue. Rev. Fr. Gynecol. Obstet. 89, 192–7.Google Scholar
Andersen, C., Silber, S., Berghold, S., Jorgensen, J. & Ernst, E. (2012). Long-term duration of function of ovarian tissue transplants: case reports. Reprod. Biomed. Online 25, 128–32.CrossRefGoogle ScholarPubMed
Behringer, K., Breuer, K., Reineke, T., May, M., Nogova, L., Klimm, B., Schmitz, T., Wildt, L., Diehl, V. & Engert, A. (2005). German Hodgkin's Lymphoma Study Group. Secondary amenorrhea after Hodgkin's lymphoma is influenced by age at treatment, stage of disease, chemotherapy regimen, and the use of oral contraceptives during therapy: a report from the German Hodgkin's Lymphoma Study Group. J. Clin. Oncol. 23, 7555–64.Google Scholar
Bokemeyer, C., Schmoll, H.J., van Rhee, J., Kuczyk, M., Schuppert, F. & Poliwoda, H. (1994). Long-term gonadal toxicity after therapy for Hodgkin's and non-Hodgkin's lymphoma. Ann. Hematol. 68, 105–10.Google Scholar
Bolla, D., Deseö, N., Sturm, A., Schöning, A. & Leimgruber, C. (2012). Minilaparotomy a good option in specific cases: a case report of bilateral ovarian germ cell tumor. Case Rep. Obstet. Gynecol. 2012, 589568.Google Scholar
Bosma, G.C., Custer, R.P. & Bosma, M.J. (1983). A severe combined immunodeficiency mutation in the mouse. Nature 301, 527–30.Google Scholar
Callejo, J., Salvador, C., Miralles, A., Vilaseca, S., Lailla, J.M. & Balasch, J. (2001). Long-term ovarian function evaluation after autografting by implantation with fresh and frozen-thawed human ovarian tissue. J. Clin. Endocrinol. Metab. 86, 4489–94.CrossRefGoogle ScholarPubMed
Callejo, J., Salvador, C., González-Nuñez, S., Almeida, L., Rodriguez, L., Marqués, L., Valls, A. & Lailla, J.M. (2013). Live birth in a woman without ovaries after autograft of frozen-thawed ovarian tissue combined with growth factors. J. Ovarian. Res. 6, 33.Google Scholar
Cardozo, E.R., Thomson, A.P., Karmon, A.E., Dickinson, K.A., Wright, D.L. & Sabatini, M.E. (2015). Ovarian stimulation and in-vitro fertilization outcomes of cancer patients undergoing fertility preservation compared to age matched controls: a 17-year experience. J. Assist. Reprod. Genet. 32, 587–96.Google Scholar
Chao, L., Jiang, A.F., Deng, X.H., Yu, H.L. & Zhen, J.H. (2008). Capability of oocyte maturation in human cryopreserved ovarian tissue following xenografting. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 30, 583–8.Google Scholar
Choi, J.K., Agarwal, P., Huang, H., Zhao, S. & He, X. (2014). The crucial role of mechanical heterogeneity in regulating follicle development and ovulation with engineered ovarian microtissue. Biomaterials 35, 5122–8.Google Scholar
Chung, K., Donnez, J., Ginsburg, E. & Meirow, D. (2013). Emergency IVF versus ovarian tissue cryopreservation: decision making in fertility preservation for female cancer patients. Fertil. Steril. 6, 1534–42.CrossRefGoogle Scholar
Cobo, A., Domingo, J., Perez, S., Crespo, J., Remohi, J. & Pellicer, A. (2009). Vitrification: an effective new approach to oocyte banking and preserving fertility in cancer patients. Clin. Transl. Oncol. 5, 268–73.Google Scholar
Cobo, A., Meseguer, M., Remohi, J. & Pellicer, A. (2010). Use of cryo-banked oocytes in an ovum donation program: a prospective randomized, controlled, clinical trial. Hum. Reprod. 9, 2239–46.Google Scholar
Courbiere, B., Caquant, L., Mazoyer, C., Franck, M., Lornage, J. & Salle, B. (2009). Difficulties improving ovarian functional recovery by microvascular transplantation and whole ovary vitrification. Fertil. Steril. 91, 2697–706.Google Scholar
Demeestere, I., Simon, P., Buxant, F., Robin, V., Fernandez, S.A., Centner, J., Delbaere, A. & Englert, Y. (2006). Ovarian function and spontaneous pregnancy after combined heterotopic and orthotopic cryopreserved ovarian tissue transplantation in a patient previously treated with bone marrow transplantation: case report. Hum. Reprod. 21, 2010–4.Google Scholar
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.Google Scholar
Demeestere, I., Simon, P., Moffa, F., Delbaere, A. & Englert, Y. (2010). Birth of a second healthy girl more than 3 years after cryopreserved ovarian graft. Hum. Reprod. 25, 1590–1.Google Scholar
Di Leva, Gianpiero, Piovan, Claudia, Gasparini, Pierluigi, Ngankeu, Apollinaire, Taccioli, Cristian, Briskin, Daniel, Cheung, Douglas G., Bolon, Brad, Anderlucci, Laura, Alder, Hansjuerg, Nuovo, Gerard, Li, Meng, Iorio, Marilena V., Galasso, Marco, Ramasamy, Santhanam, Marcucci, Guido, Perrotti, Danilo, Powell, Kimerly A., Bratasz, Anna, Garofalo, Michela, Nephew, Kenneth P. & Croce, Carlo M.. (2013). Estrogen mediated-activation of miR-191/425 cluster modulates tumorigenicity of breast cancer cells depending on estrogen receptor status. PLoS Genet. 9, e1003311.CrossRefGoogle ScholarPubMed
Dittrich, R., Hackl, J., Lotz, L., Hoffmann, I. & Beckmann, M.W. (2015). Pregnancies and live births after 20 transplantations of cryopreserved ovarian tissue in a single center. Fertil. Steril. 103, 462–8.Google Scholar
Donnez, J. & Dolmans, M.M. (2013). Fertility preservation in women. Nat. Rev. Endocrinol. 9, 735–49.Google Scholar
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.Google Scholar
Donnez, J., Squifflet, J., Dolmans, M.M., Martinez-Madrid, B., Jadoul, P. & van Langendonckt, A. (2005). Orthotopic transplantation of fresh ovarian cortex: a report of two cases. Fertil. Steril. 84, 1018.Google Scholar
Donnez, J., Dolmans, M.M., Demylle, D., Jadoul, P., Pirard, C., Squifflet, J., Martinez-Madrid, B. & Van Langendonckt, A. (2006b). Restoration of ovarian function after orthotopic (intraovarian and periovarian). transplantation of cryopreserved ovarian tissue in a woman treated by bone marrow transplantation for sickle cell anaemia: case report. Hum. Reprod. 21, 183–8.Google Scholar
Donnez, J., Martinez-Madrid, B., Jadoul, P., Van Langendonckt, A., Demylle, D. & Dolmans, M.M. (2006a). Ovarian tissue cryopreservation and transplantation: a review. Hum. Reprod. Update 12, 519–35.Google Scholar
Donnez, J., Jadoul, P., Squifflet, J., Van Langendonckt, A., Donnez, O., Van Eyck, A.S., Marinescu, C. & Dolmans, M.M. (2010a). Ovarian tissue cryopreservation and transplantation in cancer patients. Best. Pract. Res. Clin. Obstet. Gynaecol. 24, 87–100.Google Scholar
Donnez, J., Squifflet, J., Jadoul, P., Demylle, D., Cheron, A.C., Van Langendonckt, A. & Dolmans, M.M. (2010b). 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, 1787.e1–4.Google Scholar
Donnez, J., Silber, S., Andersen, C.Y., Demeestere, I., Piver, P., Meirow, D., Pellicer, A. & Dolmans, M.M. (2011). Children born after autotransplantation of cryopreserved ovarian tissue: a review of 13 live births. Ann. Med. 43, 437–50.Google Scholar
Donnez, J., Jadoul, P., Pirard, C., Hutchings, G., Demylle, D., Squifflet, J., Smitz, J. & Dolmans, M.M. (2012). Live birth after transplantation of frozen-thawed ovarian tissue after bilateral oophorectomy for benign disease. Fertil. Steril. 98, 720–5.Google Scholar
Donnez, J., Dolmans, M.M., Pellicer, A., Diaz-Garcia, C., Sanchez Serrano, M., Schmidt, K.T., Ernst, E., Luyckx, V. & Andersen, C.Y. (2013). Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertil. Steril. 99, 1503–13.Google Scholar
Edgar, D.H. & Gook, D.A. (2012). A critical appraisal of cryopreservation (slow cooling versus vitrification). of human oocytes and embryos. Hum. Reprod. Update 18, 536–54.Google Scholar
Ernst, E., Bergholdt, S., Jørgensen, 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.Google Scholar
Fahy, G.M., MacFarlane, D.R., Angell, C.A. & Meryman, H.T. (1984). Vitrification as an approach to cryopreservation. Cryobiology 21, 407–26.CrossRefGoogle ScholarPubMed
Fahy, G., Lilley, T.H., Linsdell, H., Douglas, M.S. & Meryman, H.T. (1990). Cryoprotectant toxicity and cryoprotectant toxicity reduction: in search of molecular mechanisms. Cryobiology 3, 247–68.CrossRefGoogle Scholar
Familiari, G., Caggiati, A., Nottola, S.A., Ermini, M., Di Benedetto, M.R. & Motta, P.M. (1993). Ultrastructure of human ovarian primordial follicles after combination chemotherapy for Hodgkin's disease. Hum. Reprod. 8, 2080–7.Google Scholar
Fauque, P., Ben Amor, A., Joanne, C., Agnani, G., Bresson, J.L. & Roux, C. (2007). Use of trypan blue staining to assess the quality of ovarian cryopreservation. Fertil. Steril. 87, 1200–7.Google Scholar
Ferreira, M., Bos-Mikich, A., Frantz, N., Rodrigues, J.L., Brunetto, A.L. & Schwartsmann, G. (2010). The effects of sample size on the outcome of ovarian tissue cryopreservation. Reprod. Domest. Anim. 45, 99–102.Google Scholar
Filatov, M.A., Khramova, Y.V. & Semenova, M.L. (2015). In vitro mouse ovarian follicle growth and maturation in alginate hydrogel: current state of the art. Acta Naturae 7, 48–56.Google Scholar
Fujihara, M., Comizzoli, P., Wildt, D.E. & Songsasen, N. (2012). Cat and dog primordial follicles enclosed in ovarian cortex sustain viability after in vitro culture on agarose gel in a protein-free medium. Reprod. Domest. Anim. 6, 102–8.Google Scholar
Fuller, B. & Paynter, S. (2004). Fundamentals of cryobiology in reproductive medicine. Reprod. Biomed. Online 9, 680–91.Google Scholar
Gandolfi, F., Paffoni, A., Papasso Brambilla, E., Bonetti, S., Brevini, T.A. & Ragni, G. (2006). Efficiency of equilibrium cooling and vitrification procedures for the cryopreservation of ovarian tissue: comparative analysis between human and animal models. Fertil. Steril. 85, 1150–6.Google Scholar
Gook, D.A., Edgar, D.H. & Stern, C. (1999). Effect of cooling rate and dehydration regimen on the histological appearance of human ovarian cortex following cryopreservation in 1, 2-propanediol. Hum. Reprod. 14, 2061–8.CrossRefGoogle ScholarPubMed
Gook, D.A., Edgar, D.H., Borg, J., Archer, J. & McBain, J.C. (2005). Diagnostic assessment of the developmental potential of human cryopreserved ovarian tissue from multiple patients using xenografting. Hum. Reprod. 20, 72–8.Google Scholar
Grynberg, M., Poulain, M., Sebag-Peyrelevade, S., le Parco, S., Fanchin, R. & Frydman, N. (2012). Ovarian tissue and follicle transplantation as an option for fertility preservation. Fertil. Steril. 97, 1260–8.Google Scholar
Guzel, Y., Nur Şahin, G., Sekeroglu, M. & Deniz, A. (2014). Recombinant activin A enhances the growth and survival of isolated preantral follicles cultured three-dimensionally in extracellular basement matrix protein (matrigel). under serum-free conditions. Gynecol Endocrinol. 30, 388–91.Google Scholar
Harel, S., Ferme, C. & Poirot, C. (2011). Management of fertility in patients treated for Hodgkin's lymphoma. Haematologica 96, 1692–9.Google Scholar
Harp, R., Leibach, J., Black, J., Keldahl, C & Karow, A. (1994). Cryopreservation of murine ovarian tissue. Cryobiology 31, 336–43.Google Scholar
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.Google Scholar
Higuchi, C.M., Maeda, Y., Horiuchi, T., Yamazaki, Y. (2015). A Simplified method for three-dimensional (3-D) ovarian tissue culture yielding oocytes competent to produce full-term offspring in mice. PLoS One 16, e0143114.Google Scholar
Hilders, C.G., Baranski, A.G., Peters, L., Ramkhelawan, A. & Trimbos, J.B. (2004). Successful human ovarian autotransplantation to the upper arm. Cancer 101, 2771–8.Google Scholar
Hirao, Y. (2012). Isolation of ovarian components essential for growth and development of mammalian oocytes in vitro . J. Reprod. Dev. 58, 167–74.Google Scholar
Hornick, J.E., Duncan, F.E., Shea, L.D. & Woodruff, T.K. (2012). Isolated primate primordial follicles require a rigid physical environment to survive and grow in vitro . Hum. Reprod. 27, 1801–10.Google Scholar
Hovatta, O. (2005). Methods for cryopreservation of human ovarian tissue. Reprod. Biomed. Online 10, 729–34.Google Scholar
Hovatta, O., Silye, R., Krausz, T., Abir, R., Margara, R., Trew, G., Lass, A. & Winston, R.M. (1996). Cryopreservation of human ovarian tissue using dimethylsulphoxide and propanediol–sucrose as cryoprotectants. Hum. Reprod. 11, 1268–72.Google Scholar
Hovatta, O., Silye, R., Abir, R., Krausz, T. & Winston, R.M. (1997). Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum. Reprod. 12, 1032–6.Google Scholar
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.Google Scholar
Isachenko, E., Isachenko, V., Rahimi, G. & Nawroth, F. (2003). Cryopreservation of human ovarian tissue by direct plunging into liquid nitrogen. Eur. J. Obstet. Gynecol. Reprod. Biol. 108, 186–93.Google Scholar
Isachenko, V., Isachenko, E., Reinsberg, J., Montag, M., van der Ven, K., Dorn, C., Roesing, B. & van der Ven, H. (2007). Cryopreservation of human ovarian tissue: comparison of rapid and conventional freezing. Cryobiology 55, 261–8.Google Scholar
Itami, S., Yasuda, K., Yoshida, Y., Matsui, C., Hashiura, S., Sakai, A. & Tamotsu, S. (2011). Co-culturing of follicles with interstitial cells in collagen gel reproduce follicular development accompanied with theca cell layer formation. Reprod. Biol. Endocrinol. 17, 159.Google Scholar
Jagarlamudi, K., Liu, L., Adhikari, D., Reddy, P., Idahl, A., Ottander, U., Lundin, E., Liu, K. (2009). Oocyte-specific deletion of Pten in mice reveals a stage-specific function of PTEN/PI3K signaling in oocytes in controlling follicular activation. PLoS One 4, e6186.Google Scholar
Jemal, A., Siegel, R., Xu, J. & Ward, E. (2010). Cancer statistics, 2010 CA Cancer J Clin. 5, 277–300.Google Scholar
Jin, S.Y., Lei, L., Shikanov, A., Shea, L.D. & Woodruff, T.K. (2010). A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil. Steril. 93, 2633–9.CrossRefGoogle ScholarPubMed
Kagawa, N., Silber, S. & Kuwayama, M. (2009). Successful vitrification of bovine and human ovarian tissue. Reprod. Biomed. Online 18, 568–77.Google Scholar
Kawamura, K., Cheng, Y., Suzuki, N., Deguchi, M., Sato, Y., Takae, S., Ho, C.H., Kawamura, N., Tamura, M., Hashimoto, S., Sugishita, Y., Morimoto, Y., Hosoi, Y., Yoshioka, N., Ishizuka, B. & Hsueh, A.J. (2013). Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc. Natl. Acad. Sci. USA 110, 17474–9.Google Scholar
Keros, V., Xella, S., Hultenby, K., Pettersson, K., Sheikhi, M., Volpe, A., Hreinsson, J. & Hovatta, O. (2009). Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue. Hum. Reprod. 24, 1670–83.Google Scholar
Kim, S.S., Lee, W.S., Chung, M.K., Lee, H.C., Lee, H.H. & Hill, D. (2009). Long-term ovarian function and fertility after heterotopic autotransplantation of cryobanked human ovarian tissue: 8-year experience in cancer patients. Fertil. Steril. 91, 2349.Google Scholar
Kiseleva, M., Malinova, I., Komarova, E., Shvedova, T. & Chudakov, K. (2014). The Russian experience of autotransplantation of vitrified ovarian tissue to cancer patient. Gynecol. Endocrinol. 30, 30–1.Google Scholar
Kuwayama, M., Vajta, G., Kato, O. & Leibo, S.P. (2005). Highly efficient vitrification method for cryopreservation of human oocytes. Reprod. Biomed. Online 3, 300–8.CrossRefGoogle Scholar
Lan, C., Xiao, W., Xiao-Hui, D., Chun-Yan, H. & Hong-Ling, Y. (2010). Tissue culture before transplantation of frozen-thawed human fetal ovarian tissue into immunodeficient mice. Fertil. Steril. 93, 913–9.Google Scholar
Laronda, M.M., Duncan, F.E., Hornick, J.E., Xu, M., Pahnke, J.E., Whelan, K.A., Shea, L.D., Woodruff, T.K. (2014). Alginate encapsulation supports the growth and differentiation of human primordial follicles within ovarian cortical tissue. J. Assist. Reprod. Genet. 31, 1013–28.Google Scholar
Leporrier, M., von Theobald, P., Roffe, J.L. & Muller, G. (1987). A new technique to protect ovarian function before pelvic irradiation. Heterotopic ovarian autotransplantation. Cancer 60, 2201–4.Google Scholar
Luyckx, V., Dolmans, M.M., Vanacker, J., Scalercio, S.R., Donnez, J., Amorim, C.A. (2013). First step in developing a 3D biodegradable fibrin scaffold for an artificial ovary. J. Ovarian Res. 6, 83.Google Scholar
Mahajan, N. (2015). Fertility preservation in female cancer patients: an overview. J. Hum. Reprod. Sci. 8, 3–13.Google Scholar
Martinez-Madrid, B., Dolmans, M.M., van Langendonckt, A., Defrere, S. & Donnez, J. (2004). Freeze thawing intact human ovary with its vascular pedicle with a passive cooling device. Fertil. Steril. 82, 1390–4.Google Scholar
McLaughlin, M., Kinnell, H.L., Anderson, R.A., Telfer, E.E. (2014). Inhibition of phosphatase and tensin homologue (PTEN) in human ovary in vitro results in increased activation of primordial follicles but compromises development of growing follicles. Mol. Hum. Reprod. 20, 736–44.Google Scholar
Meirow, D. (1999). Ovarian injury and modern options to preserve fertility in female cancer patients treated with high dose radio-chemotherapy for hemato-oncological neoplasias and other cancers. Leuk. Lymphoma 33, 65–76.Google Scholar
Meirow, D., Fasouliotis, S.J., Nugent, D., Schenker, J.G., Gosden, R.G. & Rutherford, A.J. (1999). A laparoscopic technique for obtaining ovarian cortical biopsy specimens for fertility conservation in patients with cancer. Fertil. Steril. 71, 948–51.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. N. Engl. J. Med. 353, 318–21.Google Scholar
Meirow, D., Baum, M., Yaron, R., Levron, J., Hardan, I., Schiff, E., Nagler, A., Yehuda, D.B., Raanani, H., Hourvitz, A. & Dor, J. (2007). Ovarian tissue cryopreservation in hematologic malignancy: ten years’ experience. Leuk. Lymphoma 48, 1569–76.CrossRefGoogle ScholarPubMed
Mhatre, P., Mhatre, J. & Magotra, R. (2005). Ovarian transplant: a new frontier. Transplant. Proc. 37, 1396–8.Google Scholar
Mochida, N., Akatani-Hasegawa, A., Saka, K., Ogino, M., Hosoda, Y., Wada, R., Sawai, H. & Shibahara, H. (2013). Live births from isolated primary/early secondary follicles following a multistep culture without organ culture in mice. Reproduction 146, 37–47.Google Scholar
Nayudu, P.L., Wu, J. & Michelmann, H.W. (2003). In vitro development of marmoset monkey oocytes by pre-antral follicle culture. Reprod. Domest. Anim. 38, 90–6.Google Scholar
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
Newton, H., Fisher, J., Arnold, J.R., Pegg, D.E., Faddy, M.J. & Gosden, R.G. (1998). Permeation of human ovarian tissue with cryoprotective agents in preparation for cryopreservation. Hum. Reprod. 13, 376–80.Google Scholar
Oktay, K. & Karlikaya, G. (2000). Ovarian function after transplantation of frozen, banked autologous ovarian tissue. N. Engl. J. Med. 342, 1919.Google Scholar
Oktay, K., Nugent, D., Newton, H., Salha, O., Chatterjee, P. & Gosden, R.G. (1997). Isolation and characterization of primordial follicles from fresh and cryopreserved human ovarian tissue. Fertil. Steril. 67, 481–6.Google Scholar
Oktay, K., Economos, K., Kan, M., Rucinski, J., Veek, L. & Rosenwaks, Z. (2001). Endocrine function and oocyte retrieval after autologous transplantation of ovarian cortical strips to the forearm. JAMA 286, 1490–3.Google Scholar
Oktay, K., Buyuk, E., Veeck, L., Zaninovic, N., Xu, K., Takeuchi, T., Opsahl, M. & Rosenwaks, Z. (2004). Embryo development after heterotopic transplantation of cryopreserved ovarian tissue. Lancet 363, 837–40.Google Scholar
Oktem, O. & Oktay, K. (2007a). Quantitative assessment of the impact of chemotherapy on ovarian follicle reserve and stromal function. Cancer 110, 2222–9.Google Scholar
Oktem, O. & Oktay, K. (2007b). A novel ovarian xenografting model to characterize the impact of chemotherapy agents on human primordial follicle reserve. Cancer Res. V, 10159–62.CrossRefGoogle Scholar
Oktem, O. & Oktay, K. (2007c). The role of extracellular matrix and activin-A in in vitro growth and survival of murine preantral follicles. Reprod. Sci. 14, 358–66.Google Scholar
Oktem, O., Buyuk, E. & Oktay, K. (2011). Preantral follicle growth is regulated by c-Jun-N-terminal kinase (JNK). pathway. Reprod. Sci. 18, 269–76.Google Scholar
Partridge, A.H. & Winer, E.P. (2004). Long-term complications of adjuvant chemotherapy for early stage breast cancer. Breast Dis. 21, 55–64.Google Scholar
Radford, J.A., Lieberman, B.A., Brison, D.R., Smith, A.R., Critchlow, J.D., Russell, S.A., Watson, A.J., Clayton, J.A., Harris, M., Gosden, R.G. & Shalet, S.M. (2001). Orthotopic reimplantation of cryopreserved ovarian cortical strips after high-dose chemotherapy for Hodgkin's lymphoma. Lancet 357, 1172–5.Google Scholar
Revel, A., Revel-Vilk, S., Aizenman, E., Porat-Katz, A., Safran, A., Ben-Meir, A., Weintraub, M., Shapira, M., Achache, H. & Laufer, N. (2009). At what age can human oocytes be obtained? Fertil. Steril. 92, 458–63.Google Scholar
Revel, A., Laufer, N., Ben Meir, A., Lebovich, M. & Mitrani, E. (2011). Micro-organ ovarian transplantation enables pregnancy: a case report. Hum. Reprod. 26, 1097–103.Google Scholar
Revelli, A., Marchino, G., Dolfin, E., Molinari, E., Delle Piane, L., Salvagno, F. & Benedetto, C. (2013). Live birth after orthotopic grafting of autologous cryopreserved ovarian tissue and spontaneous conception in Italy. Fertil. Steril. 99, 227–30.Google Scholar
Rodriguez-Wallberg, K.A., Karlström, P.O., Rezapour, M., Castellanos, E., Hreinsson, J., Rasmussen, C., Sheikhi, M., Ouvrier, B., Bozóky, B., Olofsson, J.I., Lundqvist, M. & Hovatta, O. (2015). Full-term newborn after repeated ovarian tissue transplants in a patient treated for Ewing sarcoma by sterilizing pelvic irradiation and chemotherapy. Acta Obstet. Gynecol. Scand. 94, 324–8.Google Scholar
Rosendahl, M., Loft, A., Byskov, A.G. Ziebe, S., Schmidt, K.T., Andersen, A.N., Ottosen, C. & Andersen, C.Y. (2006). Biochemical pregnancy after fertilization of an oocyte aspirated from a heterotopic autotransplant of cryopreserved ovarian tissue: case report. Hum. Reprod. 8, 2006–9.Google Scholar
Rosendahl, M., Andersen, C.Y., Ernst, E., Westergaard, L.G., Rasmussen, P.E., Loft, A. & Andersen, A.N. (2008). Ovarian function after removal of an entire ovary for cryopreservation of pieces of cortex prior to gonadotoxic treatment: a follow-up study. Hum. Reprod. 23, 2475–83.Google Scholar
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, 2413.e15–9.CrossRefGoogle Scholar
Roy, S.K. & Treacy, B.J. (1993). Isolation and long-term culture of human preantral follicles. Fertil. Steril. 59, 783–90.Google Scholar
Sanchez, M., Novella-Maestre, E., Teruel, J., Ortiz, E. & Pellicer, A. (2008). The Valencia programme for fertility preservation. Clin. Transl. Oncol. 10, 433–438.Google Scholar
Sánchez-Serrano, M., Crespo, J., Mirabet, V., Cobo, A.C., Escribá, M.J., Simón, C. & Pellicer, A. (2010). Twins born after transplantation of ovarian cortical tissue and oocyte vitrification. Fertil. Steril. 93, 268.e11–3.Google Scholar
Schmidt, K.L., Byskov, A.G., Nyboe Andersen, A., Müller, J. & Yding Andersen, C. (2003). Density and distribution of primordial follicles in single pieces of cortex from 21 patients and in individual pieces of cortex from three entire human ovaries. Hum. Reprod. 18, 1158–64.Google Scholar
Schmidt, K.L., Andersen, C.Y., Loft, A., Byskov, A.G., Ernst, E. & Andersen, A. (2005). Followup of ovarian function post chemotherapy following ovarian cryopreservation and transplantation. Hum. Reprod. 20, 3539–46.Google Scholar
Schmidt, K.T., Rosendahl, M., Ernst, E., Loft, A., Andersen, A.N., Dueholm, M., Ottosen, C. & Andersen, C.Y. (2011). Autotransplantation of cryopreserved ovarian tissue in 12 women with chemotherapy-induced premature ovarian failure: the Danish experience. Fertil. Steril. 95, 695–701.Google Scholar
Seli, E. & Tangir, J. (2005). Fertility preservation options for female patients with malignancies. Curr. Opin. Obstet. Gynecol. 17, 299–308.Google Scholar
Sharma, G.T., Dubey, P.K. & Meur, S.K. (2009). Survival and developmental competence of buffalo preantral follicles using three-dimensional collagen gel culture system. Anim. Reprod. Sci. 114, 115–24.CrossRefGoogle ScholarPubMed
Shikanov, A., Xu, M., Woodruff, T.K. & Shea, L.D. (2009). Interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials 30, 5476–85.Google Scholar
Shikanov, A., Xu, M., Woodruff, T.K. & Shea, L.D. (2011). A method for ovarian follicle encapsulation and culture in a proteolytically degradable 3 dimensional system. J. Vis. Exp. 15, 2695.Google Scholar
Sigismondi, C., Papaleo, E., Viganò, P., Vailati, S., Candiani, M., Ottolina, J., Di Mattei, V.E. & Mangili, G. (2015). Fertility preservation in female cancer patients: a single center experience. Chin. J. Cancer 34, 56–60.Google Scholar
Silber, S. (2011). Ovary cryopreservation and transplantation for fertility preservation. Mol. Hum. Reprod. 18, 59–67.Google Scholar
Silber, S. & Barbey, N. (2012). Scientific molecular basis for treatment of reproductive failure in the human: an insight into the future. Biochim. Biophys. Acta 1822, 1981–96.Google Scholar
Silber, S.J., Lenahan, K.M., Levine, D.J., Pineda, J.A., Gorman, K.S., Friez, M.J., Crawford, E.C. & Gosden, R.G. (2005). Ovarian transplantation between monozygotic twins discordant for premature ovarian failure. N. Engl. J. Med. 353, 58–63.Google Scholar
Silber, S.J., DeRosa, M., Pineda, J., Lenahan, K., Grenia, D., Gorman, K. & Gosden, R.G. (2008a). A series of monozygotic twins discordant for ovarian failure: ovary transplantation (cortical versus microvascular). and cryopreservation. Hum. Reprod. 23, 1531–7.Google Scholar
Silber, S.J., Grudzinskas, G. & Gosden, R.G. (2008b). Successful pregnancy after microsurgical transplantation of an intact ovary. N. Engl. J. Med. 359, 2617–8.CrossRefGoogle ScholarPubMed
Skory, R.M., Xu, Y., Shea, L.D. & Woodruff, T.K. (2015). Engineering the ovarian cycle using in vitro follicle culture. Hum. Reprod. 30, 1386–95.Google Scholar
Sonmezer, M. & Oktay, K. (2004). Fertility preservation in female patients. Hum. Reprod. Update 10, 251–66.Google Scholar
Stern, C.J., Gook, D., Hale, L.G., Agresta, F., Oldham, J., Rozen, G. & Jobling, T. (2013). First reported clinical pregnancy following heterotopic grafting of cryopreserved ovarian tissue in a woman after a bilateral oophorectomy. Hum. Reprod. 28, 2996–9.Google Scholar
Streets, A.M. & Huang, Y. (2014). Microfluidics for biological measurements with single-molecule resolution. Curr. Opin. Biotechnol. 25, 69–77.Google Scholar
Suzuki, N., Hashimoto, S., Igarashi, S., Takae, S., Yamanaka, M., Yamochi, T., Takenoshita, M., Hosoi, Y., Morimoto, Y. & Ishizuka, B. (2012). Assessment of long-term function of heterotopic transplants of vitrified ovarian tissue in cynomolgus monkeys. Hum. Reprod. 27, 2420–9.Google Scholar
Suzuki, N., Yoshioka, N., Takae, S., Sugishita, Y., Tamura, M., Hashimoto, S., Morimoto, Y., Kawamura, K. (2015). Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum. Reprod. 30, 608–15.Google Scholar
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.Google Scholar
Thomson, A.B., Critchley, H.O. & Wallace, W.H. (2002). Fertility and progeny. Eur. J. Cancer 38, 1634–44.Google Scholar
Vanacker, J., Luyckx, V., Dolmans, M.M., Des Rieux, A., Jaeger, J., Van Langendonckt, A., Donnez, J., Amorim, C.A. (2012). Transplantation of an alginate-matrigel matrix containing isolated ovarian cells: first step in developing a biodegradable scaffold to transplant isolated preantral follicles and ovarian cells. Biomaterials 33, 6079–85.Google Scholar
Verga Falzacappa, C., Timperi, E., Bucci, B., Amendola, D., Piergrossi, P., D'Amico, D., Santaguida, M.G., Centanni, M. & Misiti, S. (2012). T(3). preserves ovarian granulosa cells from chemotherapy-induced apoptosis. J. Endocrinol. 215, 281–9.Google Scholar
Wallace, W.H. & Kelsey, T.W. (2010). Human ovarian reserve from conception to the menopause. PLoS One 5, e8772.CrossRefGoogle Scholar
Wallace, W.H., Anderson, R.A. & Irvine, D.S. (2005). Fertility preservation for young patients with cancer: who is at risk and what can be offered? The Lancet Oncology 6, 209–18.Google Scholar
Wang, Z., Chen, H., Yin, H., Kim, S.S., Lin Tan, S. & Gosden, R.G. (2002). Fertility after intact ovary transplantation. Nature 415, 385.Google Scholar
Xu, M., West, E., Shea, L.D. & Woodruff, T.K. (2006a). Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol. Reprod. 75, 916–23.Google Scholar
Xu, M., Kreeger, P.K., Shea, L.D. & Woodruff, T.K. (2006b). Tissue-engineered follicles produce live, fertile offspring. Tissue Eng. 12, 2739–46.Google Scholar
Xu, M., Barrett, S.L., West-Farrell, E., Kondapalli, L.A., Kiesewetter, S.E., Shea, L.D. & Woodruff, T.K. (2009). In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum. Reprod. 24, 2531–40.Google Scholar
Xu, J., Lawson, M.S., Yeoman, R.R., Pau, K.Y., Barrett, S.L., Zelinski, M.B. & Stouffer, R.L. (2011a). Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys: effects of gonadotrophins, oxygen and fetuin. Hum. Reprod. 5, 1061–72.Google Scholar
Xu, M., Fazleabas, A.T., Shikanov, A., Jackson, E., Barrett, S.L., Hirshfeld-Cytron, J., Kiesewetter, S.E., Shea, L.D. & Woodruff, T.K. (2011b). In vitro oocyte maturation and preantral follicle culture from the luteal-phase baboon ovary produce mature oocytes. Biol. Reprod. 84, 689–97.Google Scholar
Xu, J., Lawson, M.S., Yeoman, R.R., Molskness, T.A., Ting, A.Y., Stouffer, R.L. & Zelinski, M.B. (2013). Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum. Reprod. 2013. 28, 2187–200.Google Scholar
Yamamoto, K., Otoi, T., Koyama, N., Horikita, N., Tachikawa, S. & Miyano, T. (1999). Development to live young from bovine small oocytes after growth, maturation and fertilization in vitro . Theriogenology 52, 81–9.Google Scholar