Mouse ovarian tissue vitrification on copper electron microscope grids versus slow freezing: a comparative ultrastructural study
Ferda Topal-Celikkan A , Sinan Ozkavukcu B E , Deniz Balci C , Sibel Serin-Kilicoglu D and Esra Atabenli-Erdemli AA Ankara University Faculty of Medicine, Department of Histology and Embryology, 06230 Sihhiye, Ankara ,Turkey.
B Ankara University Faculty of Medicine, Center for Assisted Reproduction, 06100 Dikimevi, Ankara, Turkey.
C Ankara University Biotechnology Institute, 06830 Golbasi, Ankara, Turkey.
D Ufuk University Faculty of Medicine, Department of Histology and Embryology, 06520 Balgat, Ankara, Turkey.
E Corresponding author. Email: sinozk@gmail.com
Reproduction, Fertility and Development 27(7) 1020-1028 https://doi.org/10.1071/RD13262
Submitted: 13 August 2013 Accepted: 19 February 2014 Published: 20 March 2014
Abstract
There are many reasons, including cancer therapy, for premature ovarian failure and infertility. Oocyte, embryo and ovarian cryopreservation are current options for fertility preservation. Ovarian tissue cryopreservation is essential in patients whose cancer therapy cannot be delayed, including prepubertal girls, and is mostly performed using slow freezing. In the present study, mouse ovarian tissues were vitrified on copper electron microscope grids (n = 18) or conventionally slow frozen (n = 18). Post-thaw tissues were examined histologically using light and electron microscopy and compared with the control group. According to light microscopy observations, antral follicles were found to be better preserved with the slow freezing technique rather than vitrification. Electron microscopy revealed swollen mitochondria in the oocyte cytoplasm, condensations in the zona pellucida, breakages in the junctions of granulosa cells and vacuolisation in the extracellular space in pathologic follicles, which were relatively more frequent, in the vitrification group after thawing. These results indicate that ovarian slow freezing is preferable than vitrification on copper electron microscope grids, especially for larger follicles. Conversely, vitrification of ovarian pieces using cooper grids is user-friendly and provided good protection for primordial follicles and stromal cells. There is a need for further studies into advanced tissue vitrification techniques and carriers.
Additional keywords: cryoprotective agents, fertility preservation, follicle, granulosa cells, oocyte, thermal conductivity, ultrastructure.
References
Aerts, J. M., De Clercq, J. B., Andries, S., Leroy, J. L., Van Aelst, S., and Bols, P. E. (2008). Follicle survival and growth to antral stages in short-term murine ovarian cortical transplants after cryologic solid surface vitrification or slow-rate freezing. Cryobiology 57, 163–169.| Follicle survival and growth to antral stages in short-term murine ovarian cortical transplants after cryologic solid surface vitrification or slow-rate freezing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFyltrrE&md5=58de4873fefc16d9a39656413eaf67b6CAS | 18725217PubMed |
Amorim, C. A., Curaba, M., Van Langendonckt, A., Dolmans, M. M., and Donnez, J. (2011a). Vitrification as an alternative means of cryopreserving ovarian tissue. Reprod. Biomed. Online 23, 160–186.
| Vitrification as an alternative means of cryopreserving ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 21676653PubMed |
Amorim, C. A., David, A., Van Langendonckt, A., Dolmans, M. M., and Donnez, J. (2011b). Vitrification of human ovarian tissue: effect of different solutions and procedures. Fertil. Steril. 95, 1094–1097.
| Vitrification of human ovarian tissue: effect of different solutions and procedures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitFGlsbc%3D&md5=160d78309f35b18a9c8f524ab6a5a4e5CAS | 21168134PubMed |
Bagis, H., Akkoc, T., Tass, A., and 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, 608–613.
| Cryogenic effect of antifreeze protein on transgenic mouse ovaries and the production of live offspring by orthotopic transplantation of cryopreserved mouse ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtFClurc%3D&md5=167c0eac5a250934ef5d0c5b4144b548CAS | 17874447PubMed |
Balci, D., and Can, A. (2013). The assessment of cryopreservation conditions for human umbilical cord stroma-derived mesenchymal stem cells towards a potential use for stem cell banking. Curr. Stem Cell Res. Ther. 8, 60–72.
| The assessment of cryopreservation conditions for human umbilical cord stroma-derived mesenchymal stem cells towards a potential use for stem cell banking.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlt1GnurY%3D&md5=fbf27374f61bb69bdda5210cff4203a8CAS | 23270628PubMed |
Blatt, J. (1999). Pregnancy outcome in long-term survivors of childhood cancer. Med. Pediatr. Oncol. 33, 29–33.
| Pregnancy outcome in long-term survivors of childhood cancer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzivFOgtQ%3D%3D&md5=12f7395396530ec75a1c12ff12ebb906CAS | 10401494PubMed |
Choi, W. J., Yeo, H. J., Shin, J. K., Lee, S. A., Lee, J. H., and Paik, W. Y. (2007). Effect of vitrification method on survivability, follicular growth and ovulation of preantral follicles in mice. J. Obstet. Gynaecol. Res. 33, 128–133.
| Effect of vitrification method on survivability, follicular growth and ovulation of preantral follicles in mice.Crossref | GoogleScholarGoogle Scholar | 17441883PubMed |
Comboni, A., Martinez-Madrid, B., Dolmans, M. M., Amorim, C. A., Nottola, S. A., Donnez, J., and Van Langendonckt, A. (2008). Preservation of fertility in young cancer patient: contribution of transmission electron microscopy. Reprod. Biomed. Online 17, 136–150.
| Preservation of fertility in young cancer patient: contribution of transmission electron microscopy.Crossref | GoogleScholarGoogle Scholar |
Courbiere, B., Odagescu, V., Baudot, A., Massardier, J., Mazoyer, C., Salle, B., and Lornage, J. (2006). Cryopreservation of the ovary by vitrification as an alternative to slow-cooling protocols. Fertil. Steril. 86, 1243–1251.
| Cryopreservation of the ovary by vitrification as an alternative to slow-cooling protocols.Crossref | GoogleScholarGoogle Scholar | 16978623PubMed |
Desai, N., AbdelHafez, F., Ali, M. Y., Sayed, E. H., Abu-Alhassan, A. M., Falcone, T., and Goldfarb, J. (2011). Mouse ovarian follicle cryopreservation using vitrification or slow programmed cooling: assessment of in vitro development, maturation, ultra-structure and meiotic spindle organization. J. Obstet. Gynaecol. Res. 37, 1–12.
| Mouse ovarian follicle cryopreservation using vitrification or slow programmed cooling: assessment of in vitro development, maturation, ultra-structure and meiotic spindle organization.Crossref | GoogleScholarGoogle Scholar | 20731766PubMed |
Fabbri, R., Bracone, G., Iannascoli, C., and Venturoli, S. (2003). Cryopreservation of ovarian tissue. In ‘Biotechnology of Human Reproduction’. (Eds A. Revelli, I. Tur-Kaspa, J. G. Holte and M. Massobrio.) pp. 225–237. (The Parthenon Publishing Group: New York.)
Fuller, B., and Paynter, S. (2004). Fundamentals of cryobiology in reproductive medicine. Reprod. Biomed. Online 9, 680–691.
| Fundamentals of cryobiology in reproductive medicine.Crossref | GoogleScholarGoogle Scholar | 15670420PubMed |
Gandolfi, F., Paffoni, A., Papasso Brambilla, E., Bonetti, S., Brevini, T. A., and 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, 1150–1156.
| Efficiency of equilibrium cooling and vitrification procedures for the cryopreservation of ovarian tissue: comparative analysis between human and animal models.Crossref | GoogleScholarGoogle Scholar | 16616087PubMed |
Gosden, R. G., Yin, H., Bodine, R. J., and Morris, G. J. (2010). Character, distribution and biological implications of ice crystallization in cryopreserved rabbit ovarian tissue revealed by cryo-scanning electron microscopy. Hum. Reprod. 25, 470–478.
| Character, distribution and biological implications of ice crystallization in cryopreserved rabbit ovarian tissue revealed by cryo-scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar | 19933523PubMed |
Hashimoto, S., Suzuki, N., Amo, A., Yamochi, T., Hosoi, Y., and Morimoto, Y. (2013). Good thermally conducting material supports follicle morphologies of porcine ovaries cryopreserved with ultrarapid vitrification. J. Reprod. Dev. 59, 496–499.
| Good thermally conducting material supports follicle morphologies of porcine ovaries cryopreserved with ultrarapid vitrification.Crossref | GoogleScholarGoogle Scholar | 23774861PubMed |
Huang, J. Y., Tulandi, T., Holzer, H., Lau, N. M., Macdonald, S., Tan, S. L., and Chian, R. C. (2008). Cryopreservation of ovarian tissue and in vitro matured oocytes in a female with mosaic Turner syndrome: case report. Hum. Reprod. 23, 336–339.
| Cryopreservation of ovarian tissue and in vitro matured oocytes in a female with mosaic Turner syndrome: case report.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2FksFarsQ%3D%3D&md5=4fd21ed56ff6c07616972315501d9996CAS | 18056118PubMed |
Isachenko, V., Lapidus, I., Isachenko, E., Krivokharchenko, A., Kreienberg, R., Woriedh, M., Bader, M., and Weiss, J. M. (2009). Human ovarian tissue vitrification versus conventional freezing: morphological, endocrinological, and molecular biological evaluation. Reproduction 138, 319–327.
| Human ovarian tissue vitrification versus conventional freezing: morphological, endocrinological, and molecular biological evaluation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptlemtL8%3D&md5=01b7a198bbc5c35c4e4aacf6426ec87eCAS | 19439559PubMed |
Kagawa, N., Kuwayama, M., Nakata, K., Vajta, G., Silber, S., Manabe, N., and 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, 693–699.
| Production of the first offspring from oocytes derived from fresh and cryopreserved pre-antral follicles of adult mice.Crossref | GoogleScholarGoogle Scholar | 17579980PubMed |
Kagawa, N., Silber, S., and Kuwayama, M. (2009). Successful vitrification of bovine and human ovarian tissue. Reprod. Biomed. Online 18, 568–577.
| Successful vitrification of bovine and human ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 19401001PubMed |
Keros, V., Xella, S., Hultenby, K., Pettersson, K., Sheikhi, M., Volpe, A., Hreinsson, J., and Hovatta, O. (2009). Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue. Hum. Reprod. 24, 1670–1683.
| Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnslGkurg%3D&md5=bdadb64435100c4880fa7279ca47c01bCAS | 19359339PubMed |
Kim, S. S. (2006). Fertility preservation in female cancer patients: current developments and future directions. Fertil. Steril. 85, 1–11.
| Fertility preservation in female cancer patients: current developments and future directions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvVGhu7k%3D&md5=df1f71e1f2d2323ce6542e65d7cb960eCAS | 16412718PubMed |
Kim, S. S., Battaglia, D. E., and Soules, M. R. (2001). The future of human ovarian cryopreservation and transplantation: fertility and beyond. Fertil. Steril. 75, 1049–1056.
| The future of human ovarian cryopreservation and transplantation: fertility and beyond.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzhtFyguw%3D%3D&md5=af4a0675d038db0494189c461d786c71CAS | 11384626PubMed |
Kim, G. A., Kim, H. Y., Kim, J. W., Lee, G., Lee, E., Ahn, J. Y., Park, J. H., and Lim, J. M. (2011). Effectiveness of slow freezing and vitrification for long-term preservation of mouse ovarian tissue. Theriogenology 75, 1045–1051.
| Effectiveness of slow freezing and vitrification for long-term preservation of mouse ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3jt1Snsw%3D%3D&md5=a181e2fa7c92b7436e459d60401c2465CAS | 21220167PubMed |
Kuwayama, M., Vajta, G., Kato, O., and Leibo, S. P. (2005). Highly efficient vitrification method for cryopreservation of human oocytes. Reprod. Biomed. Online 11, 300–308.
| Highly efficient vitrification method for cryopreservation of human oocytes.Crossref | GoogleScholarGoogle Scholar | 16176668PubMed |
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., and Rodrigues, A. P. R. (2009). Dimethyl sulfoxide perfusion in caprine ovarian tissue and its relationship with follicular viability after cryopreservation. Fertil. Steril. 91, 1513–1515.
| Dimethyl sulfoxide perfusion in caprine ovarian tissue and its relationship with follicular viability after cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsF2nsr8%3D&md5=eb56ca5e4fc01ae4cdfa26a581d02483CAS | 18930196PubMed |
Meirow, D., and Nugent, D. (2001). The effects of radiotherapy and chemotherapy on female reproduction. Hum. Reprod. Update 7, 535–543.
| The effects of radiotherapy and chemotherapy on female reproduction.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnotFKisQ%3D%3D&md5=de18760844cc2e6c249ffc5324bf0147CAS | 11727861PubMed |
Oktem, O., Sonmezer, M., and Oktay, K. H. (2004). Ovarian tissue cryopreservation and other fertility preservation strategies. In ‘Textbook of Assisted Reproductive Techniques: Laboratory and Clinical Perspectives’. 2nd edn. (Eds D. K. Gardner, A. Weissman, C. M. Howles and Z. Shoham.) pp. 315–329. (Taylor & Francis Group: London.)
Oktem, O., Alper, E., Balaban, B., Palaoglu, E., Peker, K., Karakaya, C., and Urman, B. (2011). Vitrified human ovaries have fewer primordial follicles and produce less antimullerian hormone than slow-frozen ovaries. Fertil. Steril. 95, 2661–4 e1.
| Vitrified human ovaries have fewer primordial follicles and produce less antimullerian hormone than slow-frozen ovaries.Crossref | GoogleScholarGoogle Scholar | 21300348PubMed |
Partridge, A. H., Gelber, S., Peppercorn, J., Sampson, E., Knudsen, K., Laufer, M., Rosenberg, R., Przypyszny, M., Rein, A., and Winer, E. P. (2004). Web-based survey of fertility issues in young women with breast cancer. J. Clin. Oncol. 22, 4174–4183.
| Web-based survey of fertility issues in young women with breast cancer.Crossref | GoogleScholarGoogle Scholar | 15483028PubMed |
Powell, R., Ho, C. Y., and Liley, P. E. (1966). Thermal conductivity of selected materials. (Eds R. Powell, C. Y. Ho and P. E. Liley) pp. 5–6. (No. NSRDS-NBS-8. National Standard Reference Data System: Washington, USA.)
Prasath, E. B. (2008). Ovarian tissue cryopreservation: an update. J. Hum. Reprod. Sci. 1, 50–55.
| Ovarian tissue cryopreservation: an update.Crossref | GoogleScholarGoogle Scholar | 19562046PubMed |
Revel, A., Safron, A., Benshushan, A., Shushan, A., Laufer, M., and Simon, A. (2004). In vitro maturation and fertilization oocyte from an intact ovary of surgically treated patient with endometrial carcinoma: a case report. Hum. Reprod. 19, 1608–1611.
| In vitro maturation and fertilization oocyte from an intact ovary of surgically treated patient with endometrial carcinoma: a case report.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2czhvVOqsQ%3D%3D&md5=cf6e19dc45d73f22798ca2ce1bac5bafCAS | 15166126PubMed |
Rho, G. J., Kim, S., Yoo, J. G., Balasubramanian, S., Lee, H. J., and Choe, S. Y. (2002). Microtubulin configuration and mitochondrial distribution after ultra-rapid cooling of bovine oocytes. Mol. Reprod. Dev. 63, 464–470.
| Microtubulin configuration and mitochondrial distribution after ultra-rapid cooling of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotlCgtrs%3D&md5=80a8eb57413414ff2148b362a4c54128CAS | 12412049PubMed |
Ross, M., and Pawlina, W. (2011). Female reproductive system. In ‘Histology, A Text and Atlas’. (Eds M. Ross, W. Pawlina.) pp. 833–837. (Lippincott Williams & Wilkins: Baltimore.)
Salehnia, M., Abbasian Moghadam, E., and Rezazadeh Velojerdi, M. (2002). Ultrastructure of follicles after vitrification of mouse ovarian tissue. Fertil. Steril. 78, 644–645.
| Ultrastructure of follicles after vitrification of mouse ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 12215351PubMed |
Siegel, R., Naishadham, D., and Jemal, A. (2013). Cancer statistics, 2013. CA Cancer J. Clin. 63, 11–30.
| Cancer statistics, 2013.Crossref | GoogleScholarGoogle Scholar | 23335087PubMed |
Ting, A. Y., Yeoman, R. R., Lawson, M. S., and 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, 2461–2472.
| In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification.Crossref | GoogleScholarGoogle Scholar | 21705370PubMed |
Ting, A. Y., Yeoman, R. R., Campos, J. R., Lawson, M. S., Mullen, S. F., Fahy, G. M., and Zelinski, M. B. (2013). Morphological and functional preservation of pre-antral follicles after vitrification of macaque ovarian tissue in a closed system. Hum. Reprod. 28, 1267–1279.
| Morphological and functional preservation of pre-antral follicles after vitrification of macaque ovarian tissue in a closed system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlagsLw%3D&md5=7fe329d78f81e4abceebacde26e5fd57CAS | 23427232PubMed |
Tulandi, T., and Al-Took, S. (1998). Laparoscopic ovarian suspension before irradiation. Fertil. Steril. 70, 381–383.
| Laparoscopic ovarian suspension before irradiation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czlvFCgsA%3D%3D&md5=a999453b99f399d6cc6edac4217e20c2CAS | 9696243PubMed |
Visser, J. A., de Jong, F. H., Laven, J. S., and Themmen, A. P. (2006). Anti-Mullerian hormone: a new marker for ovarian function. Reproduction 131, 1–9.
| Anti-Mullerian hormone: a new marker for ovarian function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFehu7o%3D&md5=3685de73f76c6532d652a0760b82941eCAS | 16388003PubMed |
Wang, Y., Xiao, Z., Li, L., Fan, W., and Li, S. W. (2008). Novel needle immersed vitrification: a practical and convenient method with potential advantages in mouse and human ovarian tissue cryopreservation. Hum. Reprod. 23, 2256–2265.
| Novel needle immersed vitrification: a practical and convenient method with potential advantages in mouse and human ovarian tissue cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFCiu7fJ&md5=64ef1d992869b427ea63a0d4418ca35cCAS | 18614614PubMed |