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Journal of Ovarian Research

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Open Access 01-12-2018 | Research

Innovative multi-protectoral approach increases survival rate after vitrification of ovarian tissue and isolated follicles with improved results in comparison with conventional method

Authors: Dmitry Nikiforov, Valentina Russo, Delia Nardinocchi, Nicola Bernabò, Mauro Mattioli, Barbara Barboni

Published in: Journal of Ovarian Research | Issue 1/2018

Abstract

Background

In recent years, autotransplantation of cryopreserved ovarian tissue became a promising approach to preserve female fertility. The slow freezing is the most effective technique which resulted in greater live birth incidence so far. Despite that, interest to vitrification of the ovarian tissue is swiftly growing, thereby undermining the necessity for further improvements in the technique. In present study, we evaluated possibilities to increase follicle survival rates adopting innovative multi-protectoral vitrification protocols, applied to the slivers of ovarian cortex or isolated early-antral follicles, frozen individually. These experimental protocols have been compared with with validated vitrification and slow freezing ones, clinically used for female fertility preservation.

Results

The results showed that third tested variation of experimental vitrification protocol, with four cryoprotectants in relatively low concentrations and applied to pieces of ovarian tissue at 0 °C during equilibration, increased survival rate of ovine ovarian tissue and improved results in comparison with conventional vitrification method. This variation of experimental protocol showed significant increase in percentage of follicles with good morphology (69,3%) in comparison with only commercially available vitrification protocol for ovarian tissue (62,1%). Morphology results were confirmed by TUNEL assay. Analysis of estradiol and progesterone production by cultured individual follicles after freezing/thawing revealed that steroids secretion remained significantly higher after multi-protectoral vitrification and slow freezing protocol, when follicles after standard vitrification protocol demonstrated decline in steroidogenic activity.

Conclusions

The multi-protectoral approach represents a workable solution to improve vitrification outcome on ovarian tissue and isolated follicles. The reduction of individual cryoprotectants concentrations, while maintaining their sufficient cumulative level in the final freezing solution, helps to increase efficiency of the procedure. Moreover, equilibration with lower temperatures helped to decrease even further the toxic effects of cryoprotectants and preserve original quality of ovarian tissue. Therefore, multi-protectoral vitrification can be suggested as an improved method for the clinical cryopreservation of ovarian tissue.

Oktay K, Oktem O. Ovarian cryopreservation and transplantation for fertility preservation for medical indications: report of an ongoing experience. Fertil Steril. 2010;93(3):762–8.CrossRefPubMed

Stoop D, Cobo A, Silber S. Fertility preservation for age-related fertility decline. Lancet. 2014;4(384(9950)):1311–9.CrossRef

Donnez J, Dolmans MM. Fertility Preservation in Women. N Engl J Med. 2017;26(377(17)):1657–65.CrossRef

Ata B, Chian RC, Tan SL. Cryopreservation of oocytes and embryos for fertility preservation for female cancer patients. Best Pract Res Clin Obstet Gynaecol. 2010;24(1):101–12.CrossRefPubMed

Anderson RA, Wallace WH. Chemotherapy risks to fertility of childhood cancer survivors. Lancet Oncol. 2016;17(5):540–1.CrossRefPubMed

Jensen AK, Rechnitzer C, Macklon KT, Ifversen MR, Birkebæk N, Clausen N, et al. Cryopreservation of ovarian tissue for fertility preservation in a large cohort of young girls: focus on pubertal development. Hum Reprod. 2017;32(1):154–64.PubMed

Gellert SE, Pors SE, Kristensen SG, Bay-Bjørn AM, Ernst E, Yding AC. Transplantation of frozen-thawed ovarian tissue: an update on worldwide activity published in peer-reviewed papers and on the Danish cohort. J Assist Reprod Genet. 2018; https://doi.org/10.1007/s10815-018-1144-2.

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.CrossRefPubMedPubMedCentral

Kelly SM, Buckett WM, Abdul-Jalil AK, Tan SL. The cryobiology of assisted reproduction. Minerva Ginecol. 2003;55(5):389–98.PubMed

10.

AbdelHafez FF, Desai N, Abou-Setta AM, Falcone T, Goldfarb J. Slow freezing, vitrification and ultra-rapid freezing of human embryos: a systematic review and meta-analysis. Reprod BioMed Online. 2010;20(2):209–22.CrossRefPubMed

11.

Boldt J. Current results with slow freezing and vitrification of the human oocyte. Reprod BioMed Online. 2011;23(3):314–22.CrossRefPubMed

12.

Hovatta O, Silye R, Krausz T, Abir R, Margara R, Trew G, et al. Cryopreservation of human ovarian tissue using dimethylsulphoxide and propanediol-sucrose as cryoprotectants. Hum Reprod. 1996;11(6):1268–72.CrossRefPubMed

13.

Hovatta O. Cryobiology of ovarian and testicular tissue. Best Pract Res Clin Obstet Gynaecol. 2003;17(2):331–42.CrossRefPubMed

14.

Klocke S, Bündgen N, Köster F, Eichenlaub-Ritter U, Griesinger G. Slow-freezing versus vitrification for human ovarian tissue cryopreservation. Arch Gynecol Obstet. 2015;291(2):419–26.CrossRefPubMed

15.

Sanfilippo S, Canis M, Smitz J, Sion B, Darcha C, Janny L. Vitrification of human ovarian tissue: a practical and relevant alternative to slow freezing. Reprod Biol Endocrinol. 2015;13:67.CrossRefPubMedPubMedCentral

16.

Amorim CA, Curaba M, Van Langendonckt A, Dolmans MM, Donnez J. Vitrification as an alternative means of cryopreserving ovarian tissue. Reprod BioMed Online. 2011;23(2):160–86.CrossRefPubMed

17.

Jensen AK, Macklon KT, Fedder J, Ernst E, Humaidan P, Andersen CY. 86 successful births and 9 ongoing pregnancies worldwide in women transplanted with frozen-thawed ovarian tissue: focus on birth and perinatal outcome in 40 of these children. J Assist Reprod Genet. 2017;34(3):325–36.CrossRefPubMed

18.

Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S, et al. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci U S A. 2013;110:17474–9.CrossRefPubMedPubMedCentral

19.

Suzuki N, Yoshioka N, Takae S, Sugishita Y, Tamura M, Hashimoto S, et al. Successful fertility preservation following Ovar- ian tissue vitrification in patients with primary ovarian insufficien- cy. Hum Reprod. 2015;30:608–15.CrossRefPubMed

20.

Silber S. Ovarian tissue cryopreservation and transplantation: scientific implications. J Assist Reprod Genet. 2016;33(12):1595–603.CrossRefPubMedPubMedCentral

21.

Whittingham DG. Survival of mouse embryos after freezing and thawing. Nature. 1971;233(5315):125–6.CrossRefPubMed

22.

Rall WF, Fahy GM. Ice-free cryopreservation of mouse embryos at −196 degrees C by vitrification. Nature. 1985;20(313(6003)):573–5.CrossRef

23.

Ishijima T, Kobayashi Y, Lee DS, Ueta YY, Matsui M, Lee JY, et al. Cryopreservation of canine ovaries by vitrification. J Reprod Dev. 2006;52(2):293–9.CrossRefPubMed

24.

Kagabu S, Umezu M. Transplantation of cryopreserved mouse, Chinese hamster, rabbit, Japanese monkey and rat ovaries into rat recipients. Exp Anim. 2000;49(1):17–21.CrossRefPubMed

25.

Santos RR, Tharasanit T, Van Haeften T, Figueiredo JR, Silva JR, Van den Hurk R. Vitrification of goat preantral follicles enclosed in ovarian tissue by using conventional and solid-surface vitrification methods. Cell Tissue Res. 2007;327(1):167–76.CrossRefPubMed

26.

Yeoman RR, Wolf DP, Lee DM. Coculture of monkey ovarian tissue increases survival after vitrification and slow-rate freezing. Fertil Steril. 2005;83(Suppl 1):1248–54.CrossRefPubMed

27.

Nagano M, Atabay EP, Atabay EC, Hishinuma M, Katagiri S, Takahashi Y. Effects of isolation method and pre-treatment with ethylene glycol or raffinose before vitrification on in vitro viability of mouse preantral follicles. Biomed Res. 2007;28(3):153–60.CrossRefPubMed

28.

Sugimoto M, Maeda S, Manabe N, Miyamoto H. Development of infantile rat ovaries autotransplanted after cryopreservation by vitrification. Theriogenology. 2000;53(5):1093–103.CrossRefPubMed

29.

Courbiere B, Odagescu V, Baudot A, Massardier J, Mazoyer C, Salle B, et al. Cryopreservation of the ovary by vitrification as an alternative to slow-cooling protocols. Fertil Steril. 2006;86(4 Suppl):1243–51.CrossRefPubMed

30.

Schmidt KL, Byskov AG, Nyboe Andersen A, Muller J, Yding AC. 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. 2003;18:1158–64.CrossRefPubMed

31.

Kagawa N, Kuwayama M, Nakata K, Vajta G, Silber S, Manabe N, et al. Production of the first offspring from oocytes derived from fresh and cryopreserved pre-antral follicles of adult mice. Reprod BioMed Online. 2007;14(6):693–9.CrossRefPubMed

32.

Kagawa N, Silber S, Kuwayama M. Successful vitrification of bovine and human ovarian tissue. Reprod BioMed Online. 2009;18(4):568–77.CrossRefPubMed

33.

Cecconi S, Capacchietti G, Russo V, Berardinelli P, Mattioli M, Barboni B. In vitro growth of Preantral follicles isolated from cryopreserved ovine ovarian tissue. Biol Reprod. 2004;70:12–7.CrossRefPubMed

34.

Barboni B, Russo V, Cecconi S, Curini V, Colosimo A, Garofalo MLA, et al. In vitro grown sheep Preantral follicles yield oocytes with normal nuclear-epigenetic maturation. PLoS One. 2011;6(11):e27550.CrossRefPubMedPubMedCentral

35.

Klocke S, Bündgen N, Köster F, Eichenlaub-Ritter U, Griesinger G. Slow-freezing versus vitrification for human ovarian tissue cryopreservation. Arch Gynecol Obstet. 2015 Feb;291(2):419–26.CrossRefPubMed

36.

Gook DA. Chapter 12 human ovarian tissue slow freezing. Methods Mol Biol. 2017;1568:161–76.CrossRefPubMed

37.

Dalman A, Deheshkar Gooneh Farahani NS, Totonchi M, Pirjani R, Ebrahimi B. 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.CrossRefPubMed

38.

Fauque P, Ben Amor A, Joanne C, Agnani G, Bresson JL, et al. Use of trypan blue staining to assess the quality of ovarian cryopreservation. Fertil Steril. 2007;87(5):1200–7.CrossRefPubMed

39.

Isachenko V, Lapidus I, Isachenko E, Krivokharchenko A, Kreienberg R, Woriedh M. Human ovarian tissue vitrification versus conventional freezing: morphological, endocrinological, and molecular biological evaluation. Reproduction. 2009 Aug;138(2):319–27.CrossRefPubMed

40.

Makabe S, Naguro T, Stallone T. Oocyte-follicle cell interactions during ovarian follicle development, as seen by high resolution scanning and transmission electron microscopy in humans. Microsc Res Tech. 2006;69(6):436–49.CrossRefPubMed

41.

Santos RR, van den Hurk R, Rodrigues AP, Costa SH, Martins FS, Matos MH. Effect of cryopreservation on viability, activation and growth of in situ and isolated ovine early-stage follicles. Anim Reprod Sci. 2007;99(1–2):53–64.CrossRefPubMed

42.

Lunardi FO, de Aguiar FL, Duarte AB, Araújo VR, de Lima LF. Ribeiro de Sá NA et al. ovine secondary follicles vitrified out the ovarian tissue grow and develop in vitro better than those vitrified into the ovarian fragments. Theriogenology. 2016;85(7):1203–10.CrossRefPubMed

43.

Lu XL, Yu J, Zhang G, Wei ZT, Li JT, Zhang JM. Effects of varying tissue sizes on the efficiency of baboon ovarian tissue vitrification. Cryobiology. 2014;69(1):79–83.CrossRefPubMed

44.

Gioia L, Saponaro I, Bernabò N, Tettamanti E, Mattioli M, Barboni B. Chronic exposure to a 2 mT static magnetic field affects the morphology, the metabolism and the function of in vitro cultured swine granulosa cells. Electromagn Biol Med. 2013;32(4):536–50.CrossRefPubMed

45.

Bafrani HH, Salsabil N, Pasbakhsh P, Hassani H, Movahedin M, Al-tarihi T. Comparison of 1,2-propanediol and ethylene glycol for cryopreservation of slow-cooled mouse zygotes and their subsequent development. J Assist Reprod Genet. 2003;20(6):234–40.CrossRefPubMedPubMedCentral

46.

Emiliani S, Van den Bergh M, Vannin AS, Biramane J, Englert Y. Comparison of ethylene glycol, 1,2-propanediol and glycerol for cryopreservation of slow-cooled mouse zygotes, 4-cell embryos and blastocysts. Hum Reprod. 2000;15(4):905–10.CrossRefPubMed

47.

Gook DA, Edgar DH. Human oocyte cryopreservation. Hum Reprod Update. 2007;13(6):591–605.CrossRefPubMed

48.

Iwatani M, Ikegami K, Kremenska Y, Hattori N, Tanaka S, Yagi S, et al. Dimethyl sulfoxide has an impact on epigenetic profile in mouse embryoid body. Stem Cells. 2006;24:2549–56.CrossRefPubMed

49.

Tsuribe PM, Gobbo CA, Landim-Alvarenga FC. Viability of primordial follicles derived from cryopreserved ovine ovarian cortex tissue. Fertil Steril. 2009;91(5 Suppl):1976–83.CrossRefPubMed

50.

Sheikhi M, Hultenby K, Niklasson B, Lundqvist M, Hovatta O. Preservation of human ovarian follicles within tissue frozen by vitrification in a xeno-free closed system using only ethylene glycol as a permeating cryoprotectant. Fertil Steril. 2013;100(1):170–7.e1–2.CrossRefPubMed

51.

Gastal GDA, Aguiar FLN, Alves BG, Alves KA, de Tarso SGS, Ishak GM, et al. Equine ovarian tissue viability after cryopreservation and in vitro culture. Theriogenology. 2017;97:139–47.CrossRefPubMed

52.

Crowe JH, Crowe LM, Chapman D. Infrared spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Arch Biochem Biophys. 1984;232(1):400–7.CrossRefPubMed

53.

Tanpradit N, Comizzoli P, Srisuwatanasagul S, Chatdarong K. Positive impact of sucrose supplementation during slow freezing of cat ovarian tissues on cellular viability, follicle morphology, and DNA integrity. Theriogenology. 2015;83(9):1553–61.CrossRefPubMed

54.

Fabbri R, Pasquinelli G, Keane D, Magnani V, Paradisi R, Venturoli S. Optimization of protocols for human ovarian tissue cryopreservation with sucrose, 1,2-propanediol and human serum. Reprod BioMed Online. 2010;21(6):819–28.CrossRefPubMed

55.

Marsella T, Sena P, Xella S, La Marca A, Giulini S, De Pol A. Human ovarian tissue cryopreservation: effect of sucrose concentration on morphological features after thawing. Reprod BioMed Online. 2008;16(2):257–67.CrossRefPubMed

56.

Kuleshowa LL, Shaw JM, Trounson AO. Studies on replacing most of the penetrating cryoprotectant by polymers for embryo cryopreservation. Cryobiology. 2001;43:21–5.CrossRef

57.

Kasai M, Komi JH, Takakamo A, Tsudera H, Sakurai T, Machida T. A simple method for mouse embryo cryopreservation in a low toxicity vitrification solution, without appreciable loss of viability. J Reprod Fertil. 1990;89(1):91–7.CrossRefPubMed

58.

Nikseresht M, Toori MA, Rasti T, Kashani IR, Mahmoudi R. The nuclear maturation and embryo development of mice germinal vesicle oocytes with and without cumulus cell after Vitrification. Clin Diagn Res. 2015;9(1):AF01–4.

59.

Mochida K, Hasegawa A, Li MW, Fray MD, Kito S, Vallelunga JM, et al. High osmolality vitrification: a new method for the simple and temperature-permissive cryopreservation of mouse embryos. PLoS One. 2013;8(1):e49316.CrossRefPubMedPubMedCentral

60.

Lee JR, Youm HW, Lee HJ, Jee BC, Suh CS, Kim SH. Effect of antifreeze protein on mouse ovarian tissue cryopreservation and transplantation. Yonsei Med J. 2015;56(3):778–84.CrossRefPubMedPubMedCentral

Title: Innovative multi-protectoral approach increases survival rate after vitrification of ovarian tissue and isolated follicles with improved results in comparison with conventional method
Authors: Dmitry Nikiforov
Valentina Russo
Delia Nardinocchi
Nicola Bernabò
Mauro Mattioli
Barbara Barboni
Publication date: 01-12-2018
Publisher: BioMed Central
Published in: Journal of Ovarian Research / Issue 1/2018
Electronic ISSN: 1757-2215
DOI: https://doi.org/10.1186/s13048-018-0437-5

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Innovative multi-protectoral approach increases survival rate after vitrification of ovarian tissue and isolated follicles with improved results in comparison with conventional method

Abstract

Background

Results

Conclusions

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Results

Conclusions

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