Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2023-0065
Animal Reproduction (AR)
REVIEW ARTICLE

Systematic review and meta-analysis on patented and non-patented vitrification processes to ovarian tissue reported between 2000 and 2021

Éverton Pimentel Ferreira Lopes; Gildas Mbemya Tetaping; Marco Aurélio Schiavo Novaes; Regiane Rodrigues dos Santos; Ana Paula Ribeiro Rodrigues

Downloads: 0
Views: 151

Abstract

Due to the great interest in ovarian cryopreservation and, consequently conservation and restoration of female fertility in the last decades, different vitrification procedures (vitrification devices or solutions) have been developed, patented, and used both for academic research purposes and for clinical use. Therefore, the present study aimed to provide a systematic review and meta-analysis of data obtained from the application of different patented and non-patented vitrification devices and solutions in different countries. For this purpose, relevant observational studies published between the years 2000 to 2021 were selected to verify the efficiency of ovarian vitrification processes on parameters such as morphology, viability, and apoptosis in preantral ovarian follicles after transplantation or in vitro culture. Our research revealed that, although several countries were considered in the study, the United States and Japan were the countries that registered the most processes, and 22 and 16 vitrification devices and solutions out of a total of 51, respectively were patented. Sixty-two non-patented processes were also considered in the study in all countries. We also observed that transplantation and in vitro ovarian culture were the techniques predominantly used to evaluate the efficiency of the devices and vitrification solutions, respectively. In conclusion, this review showed that patented or non-patented protocols available in the literature are able to successfully preserve preantral follicles present in ovarian tissue. Despite the satisfactory results reported so far, adjustments in ovarian vitrification protocols in order to minimize cryoinjuries to the follicles remain one of the goals of cryopreservation and preservation of the female reproductive function. We found that vitrification alters the morphology and viability, and offers risks leading in some cases to follicular apoptosis. However, adjustments to current protocols to develop an optimal procedure can minimize damage by not compromising follicular development after vitrification/warming.

Keywords

intellectual property, cryopreservation, ovarian follicles, fertility preservation

References

Abir R, Ben-Aharon I, Garor R, Yaniv I, Ash S, Stemmer SM, Ben-Haroush A, Freud E, Kravarusic D, Sapir O, Fisch B. Cryopreservation of in vitro matured oocytes in addition to ovarian tissue freezing for fertility preservation in paediatric female cancer patients before and after cancer therapy. Hum Reprod. 2016;31(4):750-62. http://dx.doi.org/10.1093/humrep/dew007. PMid:26848188.

Amorim CA, David A, van Langendonckt A, Dolmans MM, Donnez J. Vitrification of human ovarian tissue: effect of different solutions and procedures. Fertil Steril. 2011;95(3):1094-7. http://dx.doi.org/10.1016/j.fertnstert.2010.11.046. PMid:21168134.

Bandeira FT, Carvalho AA, Castro SV, Lima LF, Viana DA, Evangelista JSAM, Pereira MJS, Campello CC, Figueiredo JR, Rodrigues APR. Two methods of vitrification followed by in vitro culture of the ovine ovary: evaluation of the follicular development and ovarian extracellular matrix. Reprod Domest Anim. 2015;50(2):177-85. http://dx.doi.org/10.1111/rda.12463. PMid:25545956.

Barbato V, Gualtieri R, Capriglione T, Pallotta MM, Braun S, Di Nardo M, Costanzo V, Ferraro R, Catapano G, Talevi R. Slush nitrogen vitrification of human ovarian tissue does not alter gene expression and improves follicle health and progression in long-term in vitro culture. Fertil Steril. 2018;110(7):1356-66. http://dx.doi.org/10.1016/j.fertnstert.2018.08.020. PMid:30503135.

Bordes A, Lornage J, Demirci B, Franck M, Courbiere B, Guerin JF, Salle B. Normal gestations and live births after orthotopic autograft of vitrified-warmed hemi-ovaries into ewes. Hum Reprod. 2005;20(10):2745-8. http://dx.doi.org/10.1093/humrep/dei155. PMid:15980012.

Brito DCC, Domingues SFS, Rodrigues APR, Maside C, Lunardi FO, Wu X, Figueiredo JR, Pieczarka JC, Santos RR. Cryopreservation of domestic cat (Felis catus) ovarian tissue: comparison of two vitrification methods. Theriogenology. 2018;111:69-77. http://dx.doi.org/10.1016/j.theriogenology.2018.01.015. PMid:29428847.

Carvalho AA, Faustino LR, Silva CMG, Castro SV, Lobo CH, Santos FW, Santos RR, Campello CC, Bordignon V, Figueiredo JR, Rodrigues AP. Catalase addition to vitrification solutions maintains goat ovarian preantral follicles stability. Res Vet Sci. 2014;97(1):140-7. http://dx.doi.org/10.1016/j.rvsc.2014.05.006. PMid:24972862.

Carvalho AA, Faustino LR, Silva CMG, Castro SV, Lopes CAP, Santos RR, Báo SM, Figueiredo JR, Rodrigues APR. Novel wide-capacity method for vitrification of caprine ovaries: Ovarian Tissue Cryosystem (OTC). Anim Reprod Sci. 2013;138(3-4):220-7. http://dx.doi.org/10.1016/j.anireprosci.2013.02.015. PMid:23522695.

Chang HJ, Moon JH, Lee JR, Jee BC, Suh CS, Kim SH. Optimal condition of vitrification method for cryopreservation of human ovarian cortical tissues. J Obstet Gynaecol Res. 2011;37(8):1092-101. http://dx.doi.org/10.1111/j.1447-0756.2010.01496.x. PMid:21501331.

Chitale S, Lawler C, Macfarlane S. Understanding the basics of patenting. Nat Biotechnol. 2020;38(3):263-70. http://dx.doi.org/10.1038/s41587-020-0447-x. PMid:32132682.

Comizzoli P. Biobanking and fertility preservation for rare and endangered species. Anim Reprod. 2017;14(1):30-3. http://dx.doi.org/10.21451/1984-3143-AR889.

El Cury-Silva T, Nunes MEG, Casalechi M, Comim FV, Rodrigues JK, Reis FM. Cryoprotectant agents for ovarian tissue vitrification: systematic review. Cryobiology. 2021;103:7-14. http://dx.doi.org/10.1016/j.cryobiol.2021.08.001. PMid:34370991.

Dalman A, Deheshkar Gooneh Farahani NS, Totonchi M, Pirjani R, Ebrahimi B, Rezazadeh Valojerdi M. Slow freezing versus vitrification technique for human ovarian tissue cryopreservation: an evaluation of histological changes, WNT signaling pathway and apoptotic genes expression. Cryobiology. 2017;79:29-36. http://dx.doi.org/10.1016/j.cryobiol.2017.09.007. PMid:28987775.

Deller RC, Congdon T, Sahid MA, Morgan M, Vatish M, Mitchell DA, Notman R, Gibson MI. Ice recrystallisation inhibition by polyols: comparison of molecular and macromolecular inhibitors and role of hydrophobic units. Biomater Sci. 2013;1(5):478-85. http://dx.doi.org/10.1039/c3bm00194f. PMid:32482011.

Dolmans MM, Donnez J, Cacciottola L. Fertility preservation: the challenge of freezing and transplanting ovarian tissue. Trends Mol Med. 2021;27(8):777-91. http://dx.doi.org/10.1016/j.molmed.2020.11.003. PMid:33309205.

Dolmans MM, Falcone T, Patrizio P. Importance of patient selection to analyze in vitro fertilization outcome with transplanted cryopreserved ovarian tissue. Fertil Steril. 2020;114(2):279-80. http://dx.doi.org/10.1016/j.fertnstert.2020.04.050. PMid:32741467.

Dolmans MM, Luyckx V, Donnez J, Andersen CY, Greve T. Risk of transferring malignant cells with transplanted frozen-thawed ovarian tissue. Fertil Steril. 2013;99(6):1514-22. http://dx.doi.org/10.1016/j.fertnstert.2013.03.027. PMid:23541406.

Donfack NJ, Alves KA, Alves BG, Rocha RMP, Bruno JB, Bertolini M, Santos RR, Domingues SFS, Figueiredo JR, Smitz J, Rodrigues APR. Stroma cell-derived factor 1 and connexins (37 and 43) are preserved after vitrification and in vitro culture of goat ovarian cortex. Theriogenology. 2018;116:83-8. http://dx.doi.org/10.1016/j.theriogenology.2018.05.001. PMid:29783047.

Fabbri R, Vicenti R, Macciocca M, Pasquinelli G, Paradisi R, Battaglia C, Martino NA, Venturoli S. Good preservation of stromal cells and no apoptosis in human ovarian tissue after vitrification. BioMed Res Int. 2014;2014:673537. http://dx.doi.org/10.1155/2014/673537. PMid:24804230.

Faustino LR, Carvalho AA, Silva CMG, Rossetto R, Lopes CAP, van Tilburg MF, Carneiro PBM, Báo SN, Moura AAA, Bordignon V, Figueiredo JR, Rodrigues APR. Assessment of DNA damage in goat preantral follicles after vitrification of the ovarian cortex. Reprod Fertil Dev. 2015;27(3):440-8. http://dx.doi.org/10.1071/RD13164. PMid:25481978.

Fujihara M, Kaneko T, Inoue-Murayama M. Vitrification of canine ovarian tissues with polyvinylpyrrolidone preserves the survival and developmental capacity of primordial follicles. Sci Rep. 2019;9(1):3970. http://dx.doi.org/10.1038/s41598-019-40711-6. PMid:30850725.

Fuller B, Paynter S. Fundamentals of cryobiology in reproductive medicine. Reprod Biomed Online. 2004;9(6):680-91. http://dx.doi.org/10.1016/S1472-6483(10)61780-4. PMid:15670420.

Gandolfi F, Paffoni A, Papasso Brambilla E, Bonetti S, Brevini TAL, Ragni G. Efficiency of equilibrium cooling and vitrification procedures for the cryopreservation of ovarian tissue: comparative analysis between human and animal models. Fertil Steril. 2006;85(Suppl 1):1150-6. http://dx.doi.org/10.1016/j.fertnstert.2005.08.062. PMid:16616087.

Gastal GDA, Aguiar FLN, Rodrigues APR, Scimeca JM, Apgar GA, Banz WJ, Feugang JM, Gastal EL. Cryopreservation and in vitro culture of white-tailed deer ovarian tissue. Theriogenology. 2018;113:253-60. http://dx.doi.org/10.1016/j.theriogenology.2018.03.003. PMid:29574135.

Gupta PSP, Kaushik K, Johnson P, Krishna K, Nandi S, Mondal S, Tej JNK, Somoskoi B, Cseh S. Effect of different vitrification protocols on post thaw viability and gene expression of ovine preantral follicles. Theriogenology. 2022;178:1-7. http://dx.doi.org/10.1016/j.theriogenology.2021.10.024. PMid:34735977.

Haino T, Tarumi W, Kawamura K, Harada T, Sugimoto K, Okamoto A, Ikegami M, Suzuki N. Determination of follicular localization in human ovarian cortex for vitrification. J Adolesc Young Adult Oncol. 2018;7(1):46-53. http://dx.doi.org/10.1089/jayao.2017.0028. PMid:28846463.

Etzkowitz H, Zhou C. Innovation incommensurability and the science park. R & D Manag. 2017;53:73-87.

Herraiz S, Novella-Maestre E, Rodríguez B, Díaz C, Sánchez-Serrano M, Mirabet V, Pellicer A. Improving ovarian tissue cryopreservation for oncologic patients: slow freezing versus vitrification, effect of different procedures and devices. Fertil Steril. 2014;101(3):775-84. http://dx.doi.org/10.1016/j.fertnstert.2013.11.016. PMid:24359888.

Hickman C, Rogers S, Huang G, MacArthur S, Meseguer M, Nogueira D, Portela R, Rienzi L, Sharp T, Ye H. Managing the IVF laboratory during a pandemic: international perspectives from laboratory managers. Reprod Biomed Online. 2020;41(2):141-50. http://dx.doi.org/10.1016/j.rbmo.2020.05.006. PMid:32622702.

Higgins JPT, Lane PW, Anagnostelis B, Anzures-Cabrera J, Baker NF, Cappelleri JC, Haughie S, Hollis S, Lewis SC, Moneuse P, Whitehead A. A tool to assess the quality of a meta-analysis. Res Synth Methods. 2013;4(4):351-66. http://dx.doi.org/10.1002/jrsm.1092. PMid:26053948.

Huang S, Siah KW, Vasileva D, Chen S, Nelsen L, Lo AW. Life sciences intellectual property licensing at the Massachusetts Institute of Technology. Nat Biotechnol. 2021;39(3):293-301. http://dx.doi.org/10.1038/s41587-021-00843-5. PMid:33692518.

Jafarabadi M, Abdollahi M, Salehnia M. Assessment of vitrification outcome by xenotransplantation of ovarian cortex pieces in γ-irradiated mice: morphological and molecular analyses of apoptosis. J Assist Reprod Genet. 2015;32(2):195-205. http://dx.doi.org/10.1007/s10815-014-0382-1. PMid:25392074.

Donfack NJ, Alves KA, Alves BG, Pedrosa Rocha RM, Bruno JB, Lobo CH, Bertolini M, Santos RR, Taumaturgo MO, Raposo RS, Figueiredo JR, Smitz J, Rodrigues APR. Xenotransplantation of goat ovary as an alternative to analyse follicles after vitrification. Reprod Domest Anim. 2019;54(2):216-24. http://dx.doi.org/10.1111/rda.13340. PMid:30203872.

Kagawa N, Silber S, Kuwayama M. Successful vitrification of bovine and human ovarian tissue. Reprod Biomed Online. 2009;18(4):568-77. http://dx.doi.org/10.1016/S1472-6483(10)60136-8. PMid:19401001.

Keros V, Xella S, Hultenby K, Pettersson K, Sheikhi M, Volpe A, Hreinsson J, Hovatta O. Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue. Hum Reprod. 2009;24(7):1670-83. http://dx.doi.org/10.1093/humrep/dep079. PMid:19359339.

Kevles DJ. Patents, protections, and privileges the establishment of intellectual property in animals and plants. Isis. 2007;98(2):323-31. http://dx.doi.org/10.1086/518192.

Khosravi F, Reid RL, Moini A, Abolhassani F, Valojerdi MR, Kan FWK. In vitro development of human primordial follicles to preantral stage after vitrification. J Assist Reprod Genet. 2013;30(11):1397-406. http://dx.doi.org/10.1007/s10815-013-0105-z. PMid:24254400.

Klocke S, Tappehorn C, Griesinger G. Effects of supra-zero storage on human ovarian cortex prior to vitrification-warming. Reprod Biomed Online. 2014;29(2):251-8. http://dx.doi.org/10.1016/j.rbmo.2014.03.025. PMid:24953192.

Kong HS, Hong YH, Lee J, Youm HW, Lee JR, Suh CS, Kim SH. Antifreeze protein supplementation during the warming of vitrified bovine ovarian tissue can improve the ovarian tissue quality after xenotransplantation. Front Endocrinol (Lausanne). 2021;12:672619. http://dx.doi.org/10.3389/fendo.2021.672619. PMid:34122348.

Kong HS, Kim EJ, Youm HW, Kim SK, Lee JR, Suh CS, Kim SH. Improvement in ovarian tissue quality with supplementation of antifreeze protein during warming of vitrified mouse ovarian tissue. Yonsei Med J. 2018;59(2):331-6. http://dx.doi.org/10.3349/ymj.2018.59.2.331. PMid:29436204.

Kristensen SG, Andersen CY. Cryopreservation of ovarian tissue: opportunities beyond fertility preservation and a positive view into the future. Front Endocrinol (Lausanne). 2018;9:347. http://dx.doi.org/10.3389/fendo.2018.00347. PMid:30002647.

Lee HH, Lee HJ, Kim HJ, Lee JH, Ko Y, Kim SM, Lee JR, Suh CS, Kim SH. Effects of antifreeze proteins on the vitrification of mouse oocytes: comparison of three different antifreeze proteins. Hum Reprod. 2015;30(9):2110-9. http://dx.doi.org/10.1093/humrep/dev170. PMid:26202918.

Lee J, Kim EJ, Kong HS, Youm HW, Kim SK, Lee JR, Suh CS, Kim SH. Establishment of an improved vitrification protocol by combinations of vitrification medium for isolated mouse ovarian follicles. Theriogenology. 2018;121:97-103. http://dx.doi.org/10.1016/j.theriogenology.2018.07.022. PMid:30144737.

Lee S, Ryu KJ, Kim B, Kang D, Kim YY, Kim T. Comparison between slow freezing and vitrification for human ovarian tissue cryopreservation and xenotransplantation. Int J Mol Sci. 2019;20(13):3346. http://dx.doi.org/10.3390/ijms20133346. PMid:31288388.

Lee SG, Lee JH, Kang S-H, Kim HJ. Marine antifreeze proteins: types, functions and applications. In: Kim SK, editor. Marine proteins and peptides: biological activities and applications. New York: Wiley;2013. p. 667-94.

Leonel ECR, Corral A, Risco R, Camboni A, Taboga SR, Kilbride P, Vazquez M, Morris J, Dolmans MM, Amorim CA. Stepped vitrification technique for human ovarian tissue cryopreservation. Sci Rep. 2019;9(1):20008. http://dx.doi.org/10.1038/s41598-019-56585-7. PMid:31882972.

Locatelli Y, Calais L, Duffard N, Lardic L, Monniaux D, Piver P, Mermillod P, Bertoldo MJ. In vitro survival of follicles in prepubertal ewe ovarian cortex cryopreserved by slow freezing or non-equilibrium vitrification. J Assist Reprod Genet. 2019;36(9):1823-35. http://dx.doi.org/10.1007/s10815-019-01532-8. PMid:31376104.

Lopes EPF, Rodrigues GQ, de Brito DCC, Rocha RMP, Ferreira ACA, Sá NAR, Silva RF, Alcântara GLH, Alves BG, Figueiredo JR, Rodrigues APR. Vitrification of caprine secondary and early antral follicles as a perspective to preserve fertility function. Reprod Biol. 2020;20(3):371-8. http://dx.doi.org/10.1016/j.repbio.2020.05.001. PMid:32418820.

Luyet BJ, Hodapp EL. Revival of Frog’s Spermatozoa Vitrified in Liquid Air. Exp Biol Med. 1938;39(3):433-4. http://dx.doi.org/10.3181/00379727-39-10229P.

Marin L, Bedoschi G, Kawahara T, Oktay KH. History, Evolution and Current State of Ovarian Tissue Auto-Transplantation with Cryopreserved Tissue: a Successful Translational Research Journey from 1999 to 2020. Reprod Sci. 2020;27(4):955-62. http://dx.doi.org/10.1007/s43032-019-00066-9. PMid:32046442.

Marschalek J, Egarter C, Nouri K, Dekan S, Ott J, Frank M, Pietrowski D. The effect of different vitrification protocols on cell survival in human ovarian tissue: a pilot study. J Ovarian Res. 2021;14(1):170. http://dx.doi.org/10.1186/s13048-021-00924-8. PMid:34872604.

McGee EA, Hsueh AJW. Initial and Cyclic Recruitment of Ovarian Follicles*. Endocr Rev. 2000;21(2):200-14. PMid:10782364.

Mofarahe ZS, Novin MG, Jafarabadi M, Salehnia M, Noroozian M, Ghorbanmehr N. Effect of human ovarian tissue vitrification/warming on the expression of genes related to folliculogenesis. Iran Biomed J. 2015;19(4):220-5. http://dx.doi.org/10.7508/ibj.2015.04.005. PMid:26175108.

Vizcarra DAM, Silva YP, Bruno JB, Brito DCC, Berrocal DD, Silva LM, Morais MLGS, Alves BG, Alves KA, Cibin FWS, Figueiredo JR, Zelinski MB, Rodrigues APR. Use of synthetic polymers improves the quality of vitrified caprine preantral follicles in the ovarian tissue. Acta Histochem. 2020;122(2):151484. http://dx.doi.org/10.1016/j.acthis.2019.151484. PMid:31902536.

Okamoto N, Nakajima M, Sugishita Y, Suzuki N. Effect of mouse ovarian tissue cryopreservation by vitrification with Rapid-i closed system. J Assist Reprod Genet. 2018;35(4):607-13. http://dx.doi.org/10.1007/s10815-018-1121-9. PMid:29357026.

Porcu E, Tranquillo ML, Notarangelo L, Ciotti PM, Calza N, Zuffa S, Mori L, Nardi E, Dirodi M, Cipriani L, Labriola FS, Damiano G. High-security closed devices are efficient and safe to protect human oocytes from potential risk of viral contamination during vitrification and storage especially in the COVID-19 pandemic. J Assist Reprod Genet. 2021;38(3):681-8. http://dx.doi.org/10.1007/s10815-021-02062-y. PMid:33432422.

Ramezani M, Salehnia M, Jafarabadi M. Vitrification and in vitro culture had no adverse effect on the follicular development and gene expression of stimulated human ovarian tissue. J Obstet Gynaecol Res. 2018;44(3):474-87. http://dx.doi.org/10.1111/jog.13530. PMid:29316020.

Ramos L, Galbinski S, Nacul A, Jiménez MF, Frantz N, Bos-Mikich A. Detailed morphological analysis of cryoinjury in human ovarian tissue following vitrification or slow freezing. Reprod Sci. 2022;29(8):2374-81. http://dx.doi.org/10.1007/s43032-021-00716-x. PMid:34398410.

Sanfilippo S, Canis M, Smitz J, Sion B, Darcha C, Janny L, Brugnon F. Vitrification of human ovarian tissue: a practical and relevant alternative to slow freezing. Reprod Biol Endocrinol. 2015;13(1):67. http://dx.doi.org/10.1186/s12958-015-0065-5. PMid:26109179.

Morais MLGS, Brito DCC, Pinto Y, Silva LM, Vizcarra DM, Silva RF, Cibin FWS, Campello CC, Alves BG, Araújo VR, Pinto FC, Pessoa ODL, Figueiredo JR, Rodrigues APR. Natural antioxidants in the vitrification solution improve the ovine ovarian tissue preservation. Reprod Biol. 2019;19(3):270-8. http://dx.doi.org/10.1016/j.repbio.2019.07.008. PMid:31466906.

Santos RR, Amorim C, Cecconi S, Fassbender M, Imhof M, Lornage J, Paris M, Schoenfeldt V, Martinez-Madrid B. Cryopreservation of ovarian tissue: an emerging technology for female germline preservation of endangered species and breeds. Anim Reprod Sci. 2010;122(3-4):151-63. http://dx.doi.org/10.1016/j.anireprosci.2010.08.010. PMid:20832203.

Shahsavari MH, Alves KA, Alves BG, de Lima LF, Vizcarra DAM, Berrocal DJD, Silva LM, Silva YP, Zelinski MB, Figueiredo JR, Moghaddam G, Rodrigues APR. Impacts of different synthetic polymers on vitrification of ovarian tissue. Cryobiology. 2020;94:66-72. http://dx.doi.org/10.1016/j.cryobiol.2020.04.007. PMid:32339491.

Shahsavari MH, Moghaddam G, Kia HD, Rodrigues APR. Effects of new synthetic cryoprotectant agents on histological characteristics of various classes of vitrified bovine pre-antral follicles. Vet Res Forum. 2019;10(1):9-16. http://dx.doi.org/10.30466/vrf.2019.34306. PMid:31183010.

Sheikhi M, Hultenby K, Niklasson B, Lundqvist M, Hovatta O. Clinical grade vitrification of human ovarian tissue: an ultrastructural analysis of follicles and stroma in vitrified tissue. Hum Reprod. 2011;26(3):594-603. http://dx.doi.org/10.1093/humrep/deq357. PMid:21217141.

Shi Q, Xie Y, Wang Y, Li S. Vitrification versus slow freezing for human ovarian tissue cryopreservation: A systematic review and meta-anlaysis. Sci Rep. 2017;7(1):8538. http://dx.doi.org/10.1038/s41598-017-09005-7. PMid:28819292.

Silva LM, Mbemya GT, Guerreiro DD, Brito DCC, Donfack NJ, Morais MLGS, Rodrigues GQ, Bruno JB, Rocha RMP, Alves BG, Apgar GA, Cibin FWS, Figueiredo JR, Rodrigues APR. Effect of catalase or alpha lipoic acid supplementation in the vitrification solution of ovine ovarian tissue. Biopreserv Biobank. 2018;16(4):258-69. http://dx.doi.org/10.1089/bio.2017.0122. PMid:29957024.

Sugishita Y, Okamoto N, Uekawa A, Yamochi T, Nakajima M, Namba C, Igarashi S, Sato T, Ohta S, Takenoshita M, Hashimoto S, Tozawa A, Morimoto Y, Suzuki N. Oocyte retrieval after heterotopic transplantation of ovarian tissue cryopreserved by closed vitrification protocol. J Assist Reprod Genet. 2018;35(11):2037-48. http://dx.doi.org/10.1007/s10815-018-1298-y. PMid:30173352.

Sugishita Y, Taylan E, Kawahara T, Shahmurzada B, Suzuki N, Oktay K. Comparison of open and a novel closed vitrification system with slow freezing for human ovarian tissue cryopreservation. J Assist Reprod Genet. 2021;38(10):2723-33. http://dx.doi.org/10.1007/s10815-021-02297-9. PMid:34398400.

Suzuki N, Hashimoto S, Igarashi S, Takae S, Yamanaka M, Yamochi T, Takenoshita M, Hosoi Y, Morimoto Y, Ishizuka B. Assessment of long-term function of heterotopic transplants of vitrified ovarian tissue in cynomolgus monkeys. Hum Reprod. 2012;27(8):2420-9. http://dx.doi.org/10.1093/humrep/des178. PMid:22647449.

Suzuki N, Yoshioka N, Takae S, Sugishita Y, Tamura M, Hashimoto S, Morimoto Y, Kawamura K. Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod. 2015;30(3):608-15. http://dx.doi.org/10.1093/humrep/deu353. PMid:25567618.

Tian T, Zhao G, Han D, Zhu K, Chen D, Zhang Z, Wei Z, Cao Y, Zhou P. Effects of vitrification cryopreservation on follicular morphology and stress relaxation behaviors of human ovarian tissues: sucrose versus trehalose as the non-permeable protective agent. Hum Reprod. 2015;30(4):877-83. http://dx.doi.org/10.1093/humrep/dev012. PMid:25662812.

Ting AY, Yeoman RR, Campos JR, Lawson MS, Mullen SF, Fahy GM, Zelinski MB. Morphological and functional preservation of pre-antral follicles after vitrification of macaque ovarian tissue in a closed system. Hum Reprod. 2013;28(5):1267-79. http://dx.doi.org/10.1093/humrep/det032. PMid:23427232.

Ting AY, Yeoman RR, Lawson MS, Zelinski MB. Synthetic polymers improve vitrification outcomes of macaque ovarian tissue as assessed by histological integrity and the in vitro development of secondary follicles. Cryobiology. 2012;65(1):1-11. http://dx.doi.org/10.1016/j.cryobiol.2012.04.005. PMid:22569078.

Ñaupas LVS, Brito DCC, Souza SS, Brandão FAS, Silva RF, Raposo RS, Oliveira ACOM, Araújo AA, Alves BG, Guedes MIF, Silva JYG, Cordova A, Figueiredo JR, Rodrigues APR. Alpha lipoic acid supplementation improves ovarian tissue vitrification outcome: an alternative to preserve the ovarian function of Morada Nova Ewe. Reprod Sci. 2021;28(11):3109-22. http://dx.doi.org/10.1007/s43032-021-00593-4. PMid:34008154.

Wall MA, Padmanabhan V, Shikanov A. Hormonal stimulation of human ovarian xenografts in mice: studying folliculogenesis, activation, and oocyte maturation. Endocrinology. 2020;161(12):bqaa194. http://dx.doi.org/10.1210/endocr/bqaa194. PMid:33099627.

Wang TR, Yan J, Lu CL, Xia X, Yin TL, Zhi X, Zhu X, Ding T, Hu W, Guo H, Li R, Yan L, Qiao J. Human single follicle growth in vitro from cryopreserved ovarian tissue after slow freezing or vitrification. Hum Reprod. 2016;31(4):763-73. http://dx.doi.org/10.1093/humrep/dew005. PMid:26851603.

Wowk B. Anomalous high activity of a subfraction of polyvinyl alcohol ice blocker. Cryobiology. 2005;50(3):325-31. http://dx.doi.org/10.1016/j.cryobiol.2005.04.001. PMid:15904915.

Xiao Z, Wang Y, Li L, Luo S, Li SW. Needle immersed vitrification can lower the concentration of cryoprotectant in human ovarian tissue cryopreservation. Fertil Steril. 2010;94(6):2323-8. http://dx.doi.org/10.1016/j.fertnstert.2010.01.011. PMid:20189561.

Xiao Z, Zhang Y, Fan W. Cryopreservation of human ovarian tissue using the silver closed vitrification system. J Assist Reprod Genet. 2017;34(11):1435-44. http://dx.doi.org/10.1007/s10815-017-1004-5. PMid:28756496.

Yagoub SH, Lim M, Tan TCY, Chow DJX, Dholakia K, Gibson BC, Thompson JG, Dunning KR. Vitrification within a nanoliter volume: oocyte and embryo cryopreservation within a 3D photopolymerized device. J Assist Reprod Genet. 2022;39(9):1997-2014. http://dx.doi.org/10.1007/s10815-022-02589-8. PMid:35951146.

Yeoman RR, Wolf DP, Lee DM. Coculture of monkey ovarian tissue increases survival after vitrification and slow-rate freezing. Fertil Steril. 2005;83(4, Suppl 1):1248-54. http://dx.doi.org/10.1016/j.fertnstert.2004.11.036. PMid:15831299.

Yong KW, Laouar L, Elliott JAW, Jomha NM. Review of non-permeating cryoprotectants as supplements for vitrification of mammalian tissues. Cryobiology. 2020;96:1-11. http://dx.doi.org/10.1016/j.cryobiol.2020.08.012. PMid:32910946.

Zeng Q, Wang K, He L-B, Wang T-T, Fan X-M, Liu W-X. Cryoprotective effect of antifreeze protein III on the rabbit ovary. Reprod Fertil Dev. 2022;34(9):645-57. http://dx.doi.org/10.1071/RD21324. PMid:35450570.

Zhao Q, Zhang Y, Su K, Wang XW, Hai PP, Han B, Bian A, Guo R. Vitrification freezing of large ovarian tissue in the human body. J Ovarian Res. 2019;12(1):77. http://dx.doi.org/10.1186/s13048-019-0553-x. PMid:31438999.

Zhou XH, Zhang D, Shi J, Wu YJ. Comparison of vitrification and conventional slow freezing for cryopreservation of ovarian tissue with respect to the number of intact primordial follicles. Medicine (United States). 2016;95(39):e4095. http://dx.doi.org/10.1097/MD.0000000000004095. PMid:27684791.
 


Submitted date:
05/12/2023

Accepted date:
09/17/2023

654bd82aa953954ca84c61e2 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections