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Testicular Tissue Vitrification: a Promising Strategy for Male Fertility Preservation

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Abstract

Destruction of spermatogonial stem cells in juvenile men survivors of pediatric cancers leads to infertility as a side effect of gonadotoxic therapies. Sperm freezing before cancer treatment is commonly used in the clinic for fertility preservation, but this method is not applicable for prepubertal boys due to the lack of mature sperm. In these cases, cryopreservation of testicular tissues is the only option for fertility preservation. Although controlled slow freezing (CSF) is the most common procedure for testicular tissue cryopreservation, vitrification can be used as an alternative method. Controlled vitrification has prevented cell damage and formation of ice crystals. Procedures were done easily and quickly with a brief exposure time to high concentration of cryoprotectants without expensive equipment. Different studies used vitrification of testicular tissues and they assessed the morphology of seminiferous tubules, apoptosis, and viability of spermatogonial cells. Transplantation of vitrified testicular tissue into infertile recipient mice as well as in vitro culture of vitrified tissues was done in previous studies and their findings showed complete spermatogenesis and production of mature sperm. Review articles usually have compared controlled slow freezing with vitrification. In this review, we focused only on the vitrification method and its results. Despite promising results, many studies have been done for finding an optimal cryopreservation protocol in order to successfully preserve fertility in prepubertal boys.

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References

  1. Jang TH, et al. Cryopreservation and its clinical applications. Integr Med Res. 2017;6(1):12–8.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Liu X, et al. Male cancer patient sperm cryopreservation for fertility preservation: 10-year monocentric experience. Basic Clin Androl. 2021;31(1):1–9.

    Article  Google Scholar 

  3. Aslam I, et al. Fertility preservation of boys undergoing anti-cancer therapy: A review of the existing situation and prospects for the future. Hum Reprod. 2000;15(10):2154–9.

    Article  CAS  PubMed  Google Scholar 

  4. Brenner H, Steliarova-Foucher E, Arndt V. Up-to-date monitoring of childhood cancer long-term survival in Europe: methodology and application to all forms of cancer combined. Ann Oncol. 2007;18(9):1561–8.

    Article  PubMed  Google Scholar 

  5. Benvenutti L, et al. Wistar rats immature testicular tissue vitrification and heterotopic grafting. JBRA Assist Reprod. 2018;22(3):167–73.

    PubMed  PubMed Central  Google Scholar 

  6. Trottmann M, et al. Semen quality in men with malignant diseases before and after therapy and the role of cryopreservation. Eur Urol. 2007;52(2):355–67.

    Article  PubMed  Google Scholar 

  7. Radaelli MRM, et al. A comparison between a new vitrification protocol and the slow freezing method in the cryopreservation of prepubertal testicular tissue. JBRA Assist Reprod. 2017;21(3):188–95.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Di Santo M, et al. Human sperm cryopreservation: update on techniques, effect on DNA integrity, and implications for ART. Adv Urol. 2012.

  9. Brinster RL. Male germline stem cells: from mice to men. Science. 2007;316(5823):404–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Yango P, et al. Optimizing cryopreservation of human spermatogonial stem cells: comparing the effectiveness of testicular tissue and single cell suspension cryopreservation. Fertil Steril. 2014;102(5):1491-1498.e1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ogawa T, Ohmura M, Ohbo K. The niche for spermatogonial stem cells in the mammalian testis. Int J Hematol. 2005;82(5):381–8.

    Article  CAS  PubMed  Google Scholar 

  12. Spradling A, Drummond-Barbosa D, Kai T. Stem cells find their niche. Nature. 2001;414(6859):98–104.

    Article  CAS  PubMed  Google Scholar 

  13. Gouk SS, et al. Cryopreservation of mouse testicular tissue: prospect for harvesting spermatogonial stem cells for fertility preservation. Fertil Steril. 2011;95(7):2399–403.

    Article  PubMed  Google Scholar 

  14. Keros V, et al. Methods of cryopreservation of testicular tissue with viable spermatogonia in pre-pubertal boys undergoing gonadotoxic cancer treatment. Hum Reprod. 2007;22(5):1384–95.

    Article  CAS  PubMed  Google Scholar 

  15. Wyns C, et al. Management of fertility preservation in prepubertal patients: 5 years’ experience at the Catholic University of Louvain. Hum Reprod. 2011;26(4):737–47.

    Article  CAS  PubMed  Google Scholar 

  16. Dumont L, et al. Assessment of the optimal vitrification protocol for pre-pubertal mice testes leading to successful in vitro production of flagellated spermatozoa. Andrology. 2015;3(3):611–25.

    Article  CAS  PubMed  Google Scholar 

  17. Keros V, et al. Optimizing cryopreservation of human testicular tissue: comparison of protocols with glycerol, propanediol and dimethylsulphoxide as cryoprotectants. Hum Reprod. 2005;20(6):1676–87.

    Article  CAS  PubMed  Google Scholar 

  18. Kvist K, et al. Cryopreservation of intact testicular tissue from boys with cryptorchidism. Hum Reprod. 2006;21(2):484–91.

    Article  CAS  PubMed  Google Scholar 

  19. Wyns C, et al. Spermatogonial survival after cryopreservation and short-term orthotopic immature human cryptorchid testicular tissue grafting to immunodeficient mice. Hum Reprod. 2007;22(6):1603–11.

    Article  PubMed  Google Scholar 

  20. Milazzo JP, et al. Comparison of conditions for cryopreservation of testicular tissue from immature mice. Hum Reprod. 2008;23(1):17–28.

    Article  CAS  PubMed  Google Scholar 

  21. Slabbert M. Investigating alternative sperm preservation methods for assisted reproductive technologies. 2013, University of Pretoria.

  22. Pomeroy KO, et al. The ART of cryopreservation and its changing landscape. Fertil Steril. 2022;117(3):469–76.

    Article  CAS  PubMed  Google Scholar 

  23. Yokota Y, et al. Successful pregnancy following blastocyst vitrification: case report. Hum Reprod. 2000;15(8):1802–3.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  25. Heo YS, et al. “Universal” vitrification of cells by ultra-fast cooling. Technology. 2015;3(01):64–71.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Yavin S, Arav A. Measurement of essential physical properties of vitrification solutions. Theriogenology. 2007;67(1):81–9.

    Article  CAS  PubMed  Google Scholar 

  27. Karlsson JO, Toner M. Long-term storage of tissues by cryopreservation: critical issues. Biomaterials. 1996;17(3):243–56.

    Article  CAS  PubMed  Google Scholar 

  28. Zhang X, et al. Emerging technologies in medical applications of minimum volume vitrification. Nanomedicine (Lond). 2011;6(6):1115–29.

    Article  PubMed  Google Scholar 

  29. Sambu S. A Bayesian approach to optimizing cryopreservation protocols. PeerJ. 2015;3:e1039–e1039.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Shaw JM, Jones GM. Terminology associated with vitrification and other cryopreservation procedures for oocytes and embryos. Hum Reprod Update. 2003;9(6):583–605.

    Article  CAS  PubMed  Google Scholar 

  31. Karlsson JO. Cryopreservation: freezing and vitrification. Science. 2002;296(5568):655–6.

    Article  CAS  PubMed  Google Scholar 

  32. Yong KW, et al. Review of non-permeating cryoprotectants as supplements for vitrification of mammalian tissues. Cryobiology. 2020;96:1–11.

    Article  CAS  PubMed  Google Scholar 

  33. Ali J, Shelton JN. Design of vitrification solutions for the cryopreservation of embryos. J Reprod Fertil. 1993;99(2):471–7.

    Article  CAS  PubMed  Google Scholar 

  34. Fahy GM, et al. Vitrification as an approach to cryopreservation. Cryobiology. 1984;21(4):407–26.

    Article  CAS  PubMed  Google Scholar 

  35. Wusteman M, Robinson M, Pegg D. Vitrification of large tissues with dielectric warming: biological problems and some approaches to their solution. Cryobiology. 2004;48(2):179–89.

    Article  CAS  PubMed  Google Scholar 

  36. Baril G, et al. Successful direct transfer of vitrified sheep embryos. Theriogenology. 2001;56(2):299–305.

    Article  CAS  PubMed  Google Scholar 

  37. Song YC, et al. Vitreous preservation of articular cartilage grafts. J Invest Surg. 2004;17(2):65–70.

    Article  PubMed  Google Scholar 

  38. 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.

    Article  PubMed  Google Scholar 

  39. Curaba M, et al. Cryopreservation of prepubertal mouse testicular tissue by vitrification. Fertil Steril. 2011;95(4):1229-34 e1.

    Article  CAS  PubMed  Google Scholar 

  40. Amorim CA, et al. Vitrification as an alternative means of cryopreserving ovarian tissue. Reprod Biomed Online. 2011;23(2):160–86.

    Article  PubMed  Google Scholar 

  41. Quan GB, et al. Comparison of the effect of various disaccharides on frozen goat spermatozoa. Biopreserv Biobank. 2012;10(5):439–45.

    Article  CAS  PubMed  Google Scholar 

  42. Gosden RG. Gonadal tissue cryopreservation and transplantation. Reprod Biomed Online. 2002;4:64–7.

    Article  PubMed  Google Scholar 

  43. Hovatta O. Cryopreservation and culture of human ovarian cortical tissue containing early follicles. Eur J Obstet Gynecol Reprod Biol. 2004;113(Suppl 1):S50–4.

    Article  PubMed  Google Scholar 

  44. Fuller B, Paynter S. Fundamentals of cryobiology in reproductive medicine. Reprod Biomed Online. 2004;9(6):680–91.

    Article  PubMed  Google Scholar 

  45. Luyet BJ. The vitrification of organic colloids and of protoplasm. Biodynamica. 1937;29:1–14.

    Google Scholar 

  46. Gonzales F, Luyet B. Resumption of heart-beat in chick embryo frozen in liquid nitrogen. Biodynamica. 1950;7(126–128):1–5.

    CAS  PubMed  Google Scholar 

  47. Farrant J. Mechanism of cell damage during freezing and thawing and its prevention. Nature. 1965;205(4978):1284–7.

    Article  CAS  Google Scholar 

  48. Schiewe M, Anderson R. Vitrification: the pioneering past to current trends and perspectives of cryopreserving human embryos, gametes and reproductive tissue. J Biorepository Sci Appl Med. 2017;5:57–68.

    Article  Google Scholar 

  49. Rapatz G, Luyet B. Electron microscope study of erythrocytes in rapidly cooled suspensions containing various concentrations of glycerol. Biodynamica. 1968;10(210):193–210.

    CAS  PubMed  Google Scholar 

  50. Boutron P, Kaufmann A. Stability of the amorphous state in the system water-glycerol-dimethylsulfoxide. Cryobiology. 1978;15(1):93–108.

    Article  CAS  PubMed  Google Scholar 

  51. Fahy GM, et al. Physical and biological aspects of renal vitrification. Organogenesis. 2009;5(3):167–75.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Finger EB, Bischof JC. Cryopreservation by vitrification: a promising approach for transplant organ banking. Curr Opin Organ Transplant. 2018;23(3):353–60.

    Article  CAS  PubMed  Google Scholar 

  53. Shaw JM, Diotallevi L, Trounson AO. A simple rapid 4–5 m dimethyl-sulfoxide freezing technique for the cryopreservation of one-cell to blastocyst stage preimplantation mouse embryos. Reprod Fertil Dev. 1991;3(5):621–6.

    Article  CAS  PubMed  Google Scholar 

  54. Shaw JM, et al. Vitrification properties of solutions of ethylene glycol in saline containing PVP, Ficoll, or dextran. Cryobiology. 1997;35(3):219–29.

    Article  CAS  PubMed  Google Scholar 

  55. Mukaida T, et al. Vitrification of human embryos based on the assessment of suitable conditions for 8-cell mouse embryos. Hum Reprod. 1998;13(10):2874–9.

    Article  CAS  PubMed  Google Scholar 

  56. Vajta G, et al. Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol Reprod Dev:Inc Gamete Res. 1998;51(1):53–8.

    Article  CAS  Google Scholar 

  57. Kuleshova L, et al. Birth following vitrification of a small number of human oocytes. Hum Reprod. 1999;14(12):3077–9.

    Article  CAS  PubMed  Google Scholar 

  58. Cobo A, et al. Use of cryo-banked oocytes in an ovum donation programme: a prospective, randomized, controlled, clinical trial. Hum Reprod. 2010;25(9):2239–46.

    Article  PubMed  Google Scholar 

  59. Zhu D, et al. Vitrified-warmed blastocyst transfer cycles yield higher pregnancy and implantation rates compared with fresh blastocyst transfer cycles - time for a new embryo transfer strategy? Fertil Steril. 2011;95(5):1691–5.

    Article  PubMed  Google Scholar 

  60. Chang C-C, Huang J-C, Shen P-C. Method for microdrop vitrification of cells. 2006, Google Patents.

  61. Xing W, et al. Solid-surface vitrification is an appropriate and convenient method for cryopreservation of isolated rat follicles. Reprod Biol Endocrinol. 2010;8(1):1–9.

    Article  Google Scholar 

  62. Seki S, Mazur P. Ultra-rapid warming yields high survival of mouse oocytes cooled to -196°c in dilutions of a standard vitrification solution. PLoS One. 2012;7(4).

  63. Mazur P, Seki S. Survival of mouse oocytes after being cooled in a vitrification solution to -196°C at 95° to 70,000°C/min and warmed at 610° to 118,000°C/min: a new paradigm for cryopreservation by vitrification. Cryobiology. 2011;62(1):1–7.

    Article  CAS  PubMed  Google Scholar 

  64. Gutnisky C, et al. Evaluation of the Cryotech Vitrification Kit for bovine embryos. Cryobiology. 2013;67(3):391–3.

    Article  CAS  PubMed  Google Scholar 

  65. Allahbadia GN, Gandhi G. Vitrification in assisted reproduction. 2016: Springer.

  66. Fahy GM, et al. Cryopreservation of organs by vitrification: perspectives and recent advances. Cryobiology. 2004;48(2):157–78.

    Article  CAS  PubMed  Google Scholar 

  67. Armstrong AG, et al. Ovarian tissue cryopreservation in young females through the Oncofertility Consortium’s National Physicians Cooperative. Future Oncol. 2018;14(4):363–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Liebermann J, et al. Potential importance of vitrification in reproductive medicine. Biol Reprod. 2002;67(6):1671–80.

    Article  CAS  PubMed  Google Scholar 

  69. Kader AA, et al. Factors affecting the outcome of human blastocyst vitrification. Reprod Biol Endocrinol. 2009;7:99.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Cho HJ, et al. An improved protocol for dilution of cryoprotectants from vitrified human blastocysts. Hum Reprod. 2002;17(9):2419–22.

    Article  CAS  PubMed  Google Scholar 

  71. Poels J, et al. Vitrification of non-human primate immature testicular tissue allows maintenance of proliferating spermatogonial cells after xenografting to recipient mice. Theriogenology. 2012;77(5):1008–13.

    Article  CAS  PubMed  Google Scholar 

  72. Baert Y, et al. Orthotopic grafting of cryopreserved prepubertal testicular tissue: in search of a simple yet effective cryopreservation protocol. Fertil Steril. 2012;97(5):1152-1157.e2.

    Article  PubMed  Google Scholar 

  73. Liu I, Cheng KM, Silversides FG. Production of live offspring from testicular tissue cryopreserved by vitrification procedures in Japanese quail (Coturnix japonica). Biol Reprod. 2013;88(5).

  74. Chatdarong K, Thuwanut P, Morrell JM. The development of cat testicular sperm cryopreservation protocols: effects of tissue fragments or sperm cell suspension. Theriogenology. 2016;85(2):200–6.

    Article  CAS  PubMed  Google Scholar 

  75. Curaba M, et al. Can prepubertal human testicular tissue be cryopreserved by vitrification? Fertil Steril. 2011;95(6):2123 e9–12.

  76. Baert Y, et al. What is the best cryopreservation protocol for human testicular tissue banking? Hum Reprod. 2013;28(7):1816–26.

    Article  CAS  PubMed  Google Scholar 

  77. Poels J, et al. Vitrification preserves proliferation capacity in human spermatogonia. Hum Reprod. 2013;28(3):578–89.

    Article  CAS  PubMed  Google Scholar 

  78. Sa R, et al. Cryopreservation of human testicular diploid germ cell suspensions. Andrologia. 2012;44(6):366–72.

    Article  CAS  PubMed  Google Scholar 

  79. Pegg DE. The role of vitrification techniques of cryopreservation in reproductive medicine. Hum Fertil. 2005;8(4):231–9.

    Article  CAS  Google Scholar 

  80. Abrishami M, et al. Cryopreservation of immature porcine testis tissue to maintain its developmental potential after xenografting into recipient mice. Theriogenology. 2010;73(1):86–96.

    Article  CAS  PubMed  Google Scholar 

  81. Kaneko H, et al. Generation of live piglets for the first time using sperm retrieved from immature testicular tissue cryopreserved and grafted into nude mice. PLoS One. 2013;8(7):e70989.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Yokonishi T, et al. Offspring production with sperm grown in vitro from cryopreserved testis tissues. Nat Commun. 2014;5:4320.

    Article  CAS  PubMed  Google Scholar 

  83. Bhakta G, et al. Cryoreservation of alginate-fibrin beads involving bone marrow derived mesenchymal stromal cells by vitrification. Biomaterials. 2009;30(3):336–43.

    Article  CAS  PubMed  Google Scholar 

  84. Kuleshova LL, et al. Vitrification of encapsulated hepatocytes with reduced cooling/warming rates. Cryo-Letters. 2004;25(4):241–54.

    CAS  PubMed  Google Scholar 

  85. Tan FCK, et al. Optimization of cryopreservation of stem cells cultured as neurospheres: comparison between vitrification, slow-cooling and raped cooling “freezing” protocols. Cryo-Letters. 2007;28(6):445–60.

    PubMed  Google Scholar 

  86. Wen F, et al. Vitreous cryopreservation of nanofibrous tissue-engineered constructs generated using mesenchymal stromal cells. Tissue Eng-Part C: Methods. 2009;15(1):105–14.

    Article  CAS  PubMed  Google Scholar 

  87. Martincic DS, et al. Germ cell apoptosis in the human testis. Pflugers Arch. 2001;442(6 Suppl 1):R159–60.

    Article  CAS  PubMed  Google Scholar 

  88. Aggarwal A, et al. Adverse effects associated with persistent stimulation of Leydig cells with hCG in vitro. Mol Reprod Dev. 2009;76(11):1076–83.

    Article  CAS  PubMed  Google Scholar 

  89. Nagata S, Golstein P. The Fas death factor. Science. 1995;267(5203):1449–56.

    Article  CAS  PubMed  Google Scholar 

  90. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer. 2002;2(9):647–56.

    Article  CAS  PubMed  Google Scholar 

  91. Shaha C, Tripathi R, Mishra DP. Male germ cell apoptosis: regulation and biology. Philos Trans R Soc Lond B Biol Sci. 2010;365(1546):1501–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer. 2002;2(4):277–88.

    Article  CAS  PubMed  Google Scholar 

  93. Majno G, Joris I. Apoptosis, oncosis, and necrosis an overview of cell death. Am J Pathol. 1995;146(1):3–15.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Papaliagkas V, et al. The proteins and the mechanisms of apoptosis: a mini-review of the fundamentals. Hippokratia. 2007;11(3):108–13.

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Fadok VA, et al. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol. 1992;148(7):2207–16.

    Article  CAS  PubMed  Google Scholar 

  96. Aitken RJ, et al. Apoptosis in the germ line. Reproduction. 2011;141(2):139–50.

    Article  CAS  PubMed  Google Scholar 

  97. Soussi T, Caron de Fromentel C, May P. Structural aspects of the p53 protein in relation to gene evolution. Oncogene, 1990;5(7):945–52.

  98. Hemadi M, et al. Assessment of morphological and functional changes in neonate vitrified testis grafts after host treatment with melatonin. Folia Morphol (Warsz). 2011;70(2):95–102.

    CAS  PubMed  Google Scholar 

  99. Hemadi M, et al. Potential use of melatonin supplementation to protect vitrified testicular grafts from hypoxic-ischaemic damage. Andrologia. 2014;46(5):513–21.

    Article  CAS  PubMed  Google Scholar 

  100. Gholami M, et al. Does prepubertal testicular tissue vitrification influence spermatogonial stem cells (SSCs) viability? J Assist Reprod Genet. 2013;30(10):1271–7.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Hajiaghalou S, et al. Comparison of apoptosis pathway following the use of two protocols for vitrification of immature mouse testicular tissue. Theriogenology. 2016;86(8):2073–82.

    Article  PubMed  Google Scholar 

  102. Dumont L, et al. Evaluation of apoptotic- and autophagic-related protein expressions before and after IVM of fresh, slow-frozen and vitrified pre-pubertal mouse testicular tissue. Mol Hum Reprod. 2017;23(11):738–54.

    Article  CAS  PubMed  Google Scholar 

  103. Orrenius S, Nicotera P, Zhivotovsky B. Cell death mechanisms and their implications in toxicology. Toxicol Sci. 2011;119(1):3–19.

    Article  CAS  PubMed  Google Scholar 

  104. Bebbere D, et al. Gene expression analysis of ovine prepubertal testicular tissue vitrified with a novel cryodevice (E.Vit). J Assist Reprod Genet. 2019;36(10):2145–54.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Oblette A, et al. DNA methylation and histone post-translational modifications in the mouse germline following in-vitro maturation of fresh or cryopreserved prepubertal testicular tissue. Reprod Biomed Online. 2019;39(3):383–401.

    Article  CAS  PubMed  Google Scholar 

  106. Jahnukainen K, Mitchell RT, Stukenborg JB. Testicular function and fertility preservation after treatment for haematological cancer. Curr Opin Endocrinol Diabetes Obes. 2015;22(3):217–23.

    Article  CAS  PubMed  Google Scholar 

  107. Patience C, Takeuchi Y, Weiss RA. Zoonosis in xenotransplantation. Curr Opin Immunol. 1998;10(5):539–42.

    Article  CAS  PubMed  Google Scholar 

  108. Abu Elhija M, et al. Differentiation of murine male germ cells to spermatozoa in a soft agar culture system. Asian J Androl. 2012;14(2):285–93.

    Article  CAS  PubMed  Google Scholar 

  109. Arkoun B, et al. Does soaking temperature during controlled slow freezing of pre-pubertal mouse testes influence course of in vitro spermatogenesis? Cell Tissue Res. 2016;364(3):661–74.

    Article  CAS  PubMed  Google Scholar 

  110. Dumont L, et al. Vitamin A prevents round spermatid nuclear damage and promotes the production of motile sperm during in vitro maturation of vitrified pre-pubertal mouse testicular tissue. Mol Hum Reprod. 2016;22(12):819–32.

    CAS  PubMed  Google Scholar 

  111. Rondanino C, et al. Establishment, maintenance and functional integrity of the blood-testis barrier in organotypic cultures of fresh and frozen/thawed prepubertal mouse testes. Mol Hum Reprod. 2017;23(5):304–20.

    Article  CAS  PubMed  Google Scholar 

  112. Sato T, et al. In vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011;471(7339):504–7.

    Article  CAS  PubMed  Google Scholar 

  113. Lima DBC, Silva L, Comizzoli P. Influence of warming and reanimation conditions on seminiferous tubule morphology, mitochondrial activity, and cell composition of vitrified testicular tissues in the domestic cat model. PLoS One. 2018;13(11):e0207317.

    Article  PubMed  PubMed Central  Google Scholar 

  114. Woods EJ, et al. Fundamental cryobiology of reproductive cells and tissues. Cryobiology. 2004;48(2):146–56.

    Article  CAS  PubMed  Google Scholar 

  115. Yildiz C, et al. Comparison of cryosurvival and spermatogenesis efficiency of cryopreserved neonatal mouse testicular tissue between three vitrification protocols and controlled-rate freezing. Cryobiology. 2018;84:4–9.

    Article  PubMed  Google Scholar 

  116. Kimura Y, Yanagimachi R. Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development. 1995;121(8):2397–405.

    Article  CAS  PubMed  Google Scholar 

  117. Gilmore JA, et al. Determination of optimal cryoprotectants and procedures for their addition and removal from human spermatozoa. Hum Reprod. 1997;12(1):112–8.

    Article  CAS  PubMed  Google Scholar 

  118. Kaneko H, et al. Production of sperm from porcine fetal testicular tissue after cryopreservation and grafting into nude mice. Theriogenology. 2017;91:154–62.

    Article  PubMed  Google Scholar 

  119. Pukazhenthi BS, et al. Slow freezing, but not vitrification supports complete spermatogenesis in cryopreserved, neonatal sheep testicular xenografts. PLoS One. 2015;10(4):e0123957.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Yamini N, et al. Developmental potential of vitrified mouse testicular tissue after ectopic transplantation. Cell J. 2016;18(1):74–82.

    PubMed  PubMed Central  Google Scholar 

  121. Poels J, et al. In search of better spermatogonial preservation by supplementation of cryopreserved human immature testicular tissue xenografts with N-acetylcysteine and testosterone. Front Surg. 2014;1:47.

    Article  PubMed  PubMed Central  Google Scholar 

  122. Wu B, et al. iNOS enhances rat intestinal apoptosis after ischemia-reperfusion. Free Radic Biol Med. 2002;33(5):649–58.

    Article  CAS  PubMed  Google Scholar 

  123. Frederickx V, et al. Recovery, survival and functional evaluation by transplantation of frozen–thawed mouse germ cells. Hum Reprod. 2004;19(4):948–53.

    Article  CAS  PubMed  Google Scholar 

  124. Israely T, et al. Reducing ischaemic damage in rodent ovarian xenografts transplanted into granulation tissue. Hum Reprod. 2006;21(6):1368–79.

    Article  PubMed  Google Scholar 

  125. Wyns C, et al. Long-term spermatogonial survival in cryopreserved and xenografted immature human testicular tissue. Hum Reprod. 2008;23(11):2402–14.

    Article  PubMed  Google Scholar 

  126. Rathi R, et al. Maturation of testicular tissue from infant monkeys after xenografting into mice. Endocrinology. 2008;149(10):5288–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Schlatt S, et al. Modulating testicular mass in xenografting: a model to explore testis development and endocrine function. Endocrinology. 2010;151(8):4018–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Zeng W, et al. The length of the spermatogenic cycle is conserved in porcine and ovine testis xenografts. J Androl. 2006;27(4):527–33.

    Article  PubMed  Google Scholar 

  129. Pietzak EJ 3rd, et al. Histology of testicular biopsies obtained for experimental fertility preservation protocol in boys with cancer. J Urol. 2015;194(5):1420–4.

    Article  PubMed  PubMed Central  Google Scholar 

  130. Kilcoyne KR, Mitchell RT. Fertility preservation: testicular transplantation for fertility preservation: clinical potential and current challenges. Reproduction. 2019;158(5):F1-f14.

    Article  CAS  PubMed  Google Scholar 

  131. Onofre J, et al. Cryopreservation of testicular tissue or testicular cell suspensions: a pivotal step in fertility preservation. Hum Reprod Update. 2016;22(6):744–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Tang W, et al. Up-regulation of heme oxygenase-1 expression modulates reactive oxygen species level during the cryopreservation of human seminiferous tubules. Fertil Steril. 2014;102(4):974-980 e4.

    Article  CAS  PubMed  Google Scholar 

  133. Nagy ZP, Shapiro D, Chang CC. Vitrification of the human embryo: a more efficient and safer in vitro fertilization treatment. Fertil Steril. 2020;113(2):241–7.

    Article  CAS  PubMed  Google Scholar 

  134. Yokonishi T, et al. Offspring production with sperm grown in vitro from cryopreserved testis tissues. Nat Commun. 2014;5(1):1–6.

    Article  Google Scholar 

  135. Shinohara T, et al. Birth of offspring following transplantation of cryopreserved immature testicular pieces and in-vitro microinsemination. Hum Reprod. 2002;17(12):3039–45.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the Anatomical Department of Tehran University of Medical Sciences.

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Authors and Affiliations

  1. Department of Anatomy, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

    Aghbibi Nikmahzar, Mehdi Abbasi & Forough Mahdavinezhad

  2. Department of Anatomy, School of Medicine, Shahrekord University of Medical Sciences, Shahrekord, Iran

    Farnaz Khadivi

  3. School of Dentistry, Tehran University of Medical Sciences, Tehran, Iran

    Yasaman Abbasi

  4. Department of Anatomy, School of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran

    Erfan Daneshi

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  1. Aghbibi Nikmahzar
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  2. Farnaz Khadivi
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  3. Mehdi Abbasi
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  4. Forough Mahdavinezhad
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  5. Yasaman Abbasi
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  6. Erfan Daneshi
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Correspondence to Farnaz Khadivi.

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Nikmahzar, A., Khadivi, F., Abbasi, M. et al. Testicular Tissue Vitrification: a Promising Strategy for Male Fertility Preservation. Reprod. Sci. 30, 1687–1700 (2023). https://doi.org/10.1007/s43032-022-01113-8

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