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Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2024

Open Access 01-12-2024 | Fertility | Review

Advancements in fertility preservation strategies for pediatric male cancer patients: a review of cryopreservation and transplantation of immature testicular tissue

Authors: Zih-Yi Sung, Yong-Qi Liao, Jung-Hsiu Hou, Hong-Hsien Lai, Sung-Ming Weng, Hai-Wei Jao, Buo-Jia Lu, Chi-Huang Chen

Published in: Reproductive Biology and Endocrinology | Issue 1/2024

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Abstract

Recently, there has been increasing emphasis on the gonadotoxic effects of cancer therapy in prepubertal boys. As advances in oncology treatments continue to enhance survival rates for prepubertal boys, the need for preserving their functional testicular tissue for future reproduction becomes increasingly vital. Therefore, we explore cutting-edge strategies in fertility preservation, focusing on the cryopreservation and transplantation of immature testicular tissue as a promising avenue. The evolution of cryopreservation techniques, from controlled slow freezing to more recent advancements in vitrification, with an assessment of their strengths and limitations was exhibited. Detailed analysis of cryoprotectants, exposure times, and protocols underscores their impact on immature testicular tissue viability. In transplantation strategy, studies have revealed that the scrotal site may be the preferred location for immature testicular tissue grafting in both autotransplantation and xenotransplantation scenarios. Moreover, the use of biomaterial scaffolds during graft transplantation has shown promise in enhancing graft survival and stimulating spermatogenesis in immature testicular tissue over time. This comprehensive review provides a holistic approach to optimize the preservation strategy of human immature testicular tissue in the future.
Literature
1.
Fujita K, Tsujimura A, Miyagawa Y, Kiuchi H, Matsuoka Y, Takao T, et al. Isolation of germ cells from leukemia and lymphoma cells in a human in vitro model: potential clinical application for restoring human fertility after anticancer therapy. Cancer Res. 2006;66(23):11166–71.PubMedCrossRef
2.
Howell S, Shalet S. Gonadal damage from chemotherapy and radiotherapy. Endocrinol Metab Clin North Am. 1998;27(4):927–43.PubMedCrossRef
3.
Jahnukainen K, Ehmcke J, Schlatt S. Testicular xenografts: a novel approach to study cytotoxic damage in juvenile primate testis. Cancer Res. 2006;66(7):3813–8.PubMedCrossRef
4.
Howell SJ, Radford JA, Ryder WD, Shalet SM. Testicular function after cytotoxic chemotherapy: evidence of leydig cell insufficiency. J Clin Oncology: Official J Am Soc Clin Oncol. 1999;17(5):1493–8.CrossRef
5.
Fosså SD, Klepp O, Norman N. Lack of gonadal protection by medroxyprogesterone acetate-induced transient medical castration during chemotherapy for testicular cancer. Br J Urol. 1988;62(5):449–53.PubMedCrossRef
6.
Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2021. Cancer J Clin. 2021;71(1):7–33.CrossRef
7.
Stiller CA, Desandes E, Danon SE, Izarzugaza I, Ratiu A, Vassileva-Valerianova Z et al. Cancer incidence and survival in european adolescents (1978–1997). Report from the automated childhood cancer information system project. European journal of cancer (Oxford, England: 1990) 2006; 42(13):2006—18.
8.
9.
Pendergraft SS, Sadri-Ardekani H, Atala A, Bishop CE. Three-dimensional testicular organoid: a novel tool for the study of human spermatogenesis and gonadotoxicity in vitro. Biol Reprod. 2017;96(3):720–32.PubMedCrossRef
10.
Shinohara T, Inoue K, Ogonuki N, Kanatsu-Shinohara M, Miki H, Nakata K, et al. Birth of offspring following transplantation of cryopreserved immature testicular pieces and in-vitro microinsemination. Hum Reprod (Oxford England). 2002;17(12):3039–45.CrossRef
11.
Fayomi AP, Peters K, Sukhwani M, Valli-Pulaski H, Shetty G, Meistrich ML, et al. Autologous grafting of cryopreserved prepubertal rhesus testis produces sperm and offspring. Volume 363. New York, NY: Science; 2019. pp. 1314–19. 6433.
12.
Kaneko H, Kikuchi K, Nakai M, Somfai T, Noguchi J, Tanihara F, 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.PubMedPubMedCentralCrossRef
13.
Lu BJ, Huang YL, Liu YL, Chen BS, Lin BZ, Chen CH. Tracking immature testicular tissue after vitrification in vitro and in vivo for pre-pubertal fertility preservation: a translational transgenic mouse model. Int J Mol Sci 2022; 23(15).
14.
Poels J, Van Langendonckt A, Many MC, Wese FX, Wyns C. Vitrification preserves proliferation capacity in human spermatogonia. Hum Reprod (Oxford England). 2013;28(3):578–89.CrossRef
15.
Benvenutti L, Salvador RA, Til D, Senn AP, Tames DR, Amaral NLL, et al. Wistar rats immature testicular tissue vitrification and heterotopic grafting. JBRA Assist Reprod. 2018;22(3):167–73.PubMedPubMedCentral
16.
Chen CH, Shih TC, Liu YL, Peng YJ, Huang YL, Chen BS et al. Engineered immature testicular tissue by electrospun mats for prepubertal fertility preservation in a bioluminescence imaging transgenic mouse model. Int J Mol Sci 2022; 23(20).
17.
18.
Nicodemus GD, Bryant SJ. Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng Part B Reviews. 2008;14(2):149–65.CrossRef
19.
Bahadur G, Chatterjee R, Ralph D. Testicular tissue cryopreservation in boys. Ethical and legal issues: Case report. Hum Reprod (Oxford England). 2000;15(6):1416–20.
20.
Ginsberg JP, Carlson CA, Lin K, Hobbie WL, Wigo E, Wu X, et al. An experimental protocol for fertility preservation in prepubertal boys recently diagnosed with cancer: a report of acceptability and safety. Hum Reprod (Oxford England). 2010;25(1):37–41.CrossRef
21.
Schlatt S, Honaramooz A, Ehmcke J, Goebell PJ, Rübben H, Dhir R, et al. Limited survival of adult human testicular tissue as ectopic xenograft. Hum Reprod (Oxford England). 2006;21(2):384–9.CrossRef
22.
Wyns C, Curaba M, Martinez-Madrid B, Van Langendonckt A, François-Xavier W, Donnez J. Spermatogonial survival after cryopreservation and short-term orthotopic immature human cryptorchid testicular tissue grafting to immunodeficient mice. Hum Reprod (Oxford England). 2007;22(6):1603–11.CrossRef
23.
Wyns C, Van Langendonckt A, Wese FX, Donnez J, Curaba M. Long-term spermatogonial survival in cryopreserved and xenografted immature human testicular tissue. Hum Reprod (Oxford England). 2008;23(11):2402–14.CrossRef
24.
Abrishami M, Anzar M, Yang Y, Honaramooz A. Cryopreservation of immature porcine testis tissue to maintain its developmental potential after xenografting into recipient mice. Theriogenology. 2010;73(1):86–96.PubMedCrossRef
25.
Oblette A, Rives-Feraille A, Dumont L, Delessard M, Saulnier J, Rives N, et al. Dynamics of epigenetic modifications in icsi embryos from in vitro-produced spermatozoa. Andrology. 2021;9(2):640–56.PubMedCrossRef
26.
Oblette A, Rives N, Dumont L, Rives A, Verhaeghe F, Jumeau F, et al. Assessment of sperm nuclear quality after in vitro maturation of fresh or frozen/thawed mouse pre-pubertal testes. Mol Hum Reprod. 2017;23(10):674–84.PubMedCrossRef
27.
Dumont L, Lopez Maestre H, Chalmel F, Huber L, Rives-Feraille A, Moutard L et al. Throughout in vitro first spermatogenic wave: next-generation sequencing gene expression patterns of fresh and cryopreserved prepubertal mice testicular tissue explants. 2023; 14.
28.
Yokonishi T, Sato T, Komeya M, Katagiri K, Kubota Y, Nakabayashi K, et al. Offspring production with sperm grown in vitro from cryopreserved testis tissues. Nat Commun. 2014;5:4320.PubMedCrossRef
29.
Van Saen D, Goossens E, De Block G, Tournaye H. Regeneration of spermatogenesis by grafting testicular tissue or injecting testicular cells into the testes of sterile mice: a comparative study. Fertil Steril. 2009;91(5 Suppl):2264–72.PubMedCrossRef
30.
Kanatsu-Shinohara M, Ogonuki N, Inoue K, Ogura A, Toyokuni S, Shinohara T. Restoration of fertility in infertile mice by transplantation of cryopreserved male germline stem cells. Hum Reprod (Oxford England). 2003;18(12):2660–7.CrossRef
31.
Rives-Feraille A, Liard A, Bubenheim M, Barbotin AL, Giscard d’Estaing S, Mirallié S, et al. Assessment of the architecture and integrity of frozen-thawed testicular tissue from (pre)pubertal boys with cancer. Andrology. 2022;10(2):279–90.PubMedCrossRef
32.
Poels J, Van Langendonckt A, Dehoux JP, Donnez J, Wyns C. 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.PubMedCrossRef
33.
Radaelli MRM, Almodin CG, Minguetti-Câmara VC, Cerialli PMA, Nassif AE, Gonçalves AJ. 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.PubMedPubMedCentral
34.
Yamini N, Pourmand G, Amidi F, Salehnia M, Ataei Nejad N, Mougahi SM. Developmental potential of vitrified mouse testicular tissue after ectopic transplantation. Cell J. 2016;18(1):74–82.PubMedPubMedCentral
35.
Curaba M, Poels J, van Langendonckt A, Donnez J, Wyns C. Can prepubertal human testicular tissue be cryopreserved by vitrification? Fertil Steril. 2011;95(6):e21239–12.CrossRef
36.
Pukazhenthi BS, Nagashima J, Travis AJ, Costa GM, Escobar EN, França LR, et al. Slow freezing, but not vitrification supports complete spermatogenesis in cryopreserved, neonatal sheep testicular xenografts. PLoS ONE. 2015;10(4):e0123957.PubMedPubMedCentralCrossRef
37.
Baert Y, Van Saen D, Haentjens P, In’t Veld P, Tournaye H, Goossens E. What is the best cryopreservation protocol for human testicular tissue banking? Human reproduction (Oxford. England). 2013;28(7):1816–26.
38.
Gurtovenko AA, Anwar J. Modulating the structure and properties of cell membranes: the molecular mechanism of action of dimethyl sulfoxide. J Phys Chem B. 2007;111(35):10453–60.PubMedCrossRef
39.
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 reproduction. 1990; 89(1):91–7.
40.
Unni S, Kasiviswanathan S, D’Souza S, Khavale S, Mukherjee S, Patwardhan S, et al. Efficient cryopreservation of testicular tissue: Effect of age, sample state, and concentration of cryoprotectant. Fertil Steril. 2012;97(1):200–e81.PubMedCrossRef
41.
Goossens E, Frederickx V, Geens M, De Block G, Tournaye H. Cryosurvival and spermatogenesis after allografting prepubertal mouse tissue: comparison of two cryopreservation protocols. Fertil Steril. 2008;89(3):725–7.PubMedCrossRef
42.
Jahnukainen K, Ehmcke J, Hergenrother SD, Schlatt S. Effect of cold storage and cryopreservation of immature non-human primate testicular tissue on spermatogonial stem cell potential in xenografts. Hum Reprod (Oxford England). 2007;22(4):1060–7.CrossRef
43.
Milazzo JP, Vaudreuil L, Cauliez B, Gruel E, Massé L, Mousset-Siméon N, et al. Comparison of conditions for cryopreservation of testicular tissue from immature mice. Hum Reprod (Oxford England). 2008;23(1):17–28.CrossRef
44.
Jung SE, Ahn JS, Kim YH, Kim BJ, Won JH, Ryu BY. Effective cryopreservation protocol for preservation of male primate (macaca fascicularis) prepubertal fertility. Reprod Biomed Online. 2020;41(6):1070–83.PubMedCrossRef
45.
Wistuba J, Luetjens CM, Wesselmann R, Nieschlag E, Simoni M, Schlatt S. Meiosis in autologous ectopic transplants of immature testicular tissue grafted to callithrix jacchus. Biol Reprod. 2006;74(4):706–13.PubMedCrossRef
46.
Luetjens CM, Stukenborg JB, Nieschlag E, Simoni M, Wistuba J. Complete spermatogenesis in orthotopic but not in ectopic transplants of autologously grafted marmoset testicular tissue. Endocrinology. 2008;149(4):1736–47.PubMedCrossRef
47.
Jahnukainen K, Ehmcke J, Nurmio M, Schlatt S. Autologous ectopic grafting of cryopreserved testicular tissue preserves the fertility of prepubescent monkeys that receive sterilizing cytotoxic therapy. Cancer Res. 2012;72(20):5174–8.PubMedPubMedCentralCrossRef
48.
Mieusset R, Bujan L, Mansat A, Pontonnier F, Grandjean H. Hyperthermia and human spermatogenesis: enhancement of the inhibitory effect obtained by ‘artificial cryptorchidism’. Int J Androl. 1987;10(4):571–80.PubMedCrossRef
49.
Honaramooz A, Snedaker A, Boiani M, Schöler H, Dobrinski I, Schlatt S. Sperm from neonatal mammalian testes grafted in mice. Nature. 2002;418(6899):778–81.PubMedCrossRef
50.
Snedaker AK, Honaramooz A, Dobrinski I. A game of cat and mouse: Xenografting of testis tissue from domestic kittens results in complete cat spermatogenesis in a mouse host. J Androl. 2004;25(6):926–30.PubMedCrossRef
51.
Rathi R, Honaramooz A, Zeng W, Schlatt S, Dobrinski I. Germ cell fate and seminiferous tubule development in bovine testis xenografts. Reproduction. 2005;130(6):923–9.PubMedCrossRef
52.
Rathi R, Honaramooz A, Zeng W, Turner R, Dobrinski I. Germ cell development in equine testis tissue xenografted into mice. Reprod (Cambridge England). 2006;131(6):1091–8.CrossRef
53.
Arregui L, Rathi R, Megee SO, Honaramooz A, Gomendio M, Roldan ER, et al. Xenografting of sheep testis tissue and isolated cells as a model for preservation of genetic material from endangered ungulates. Reprod (Cambridge England). 2008;136(1):85–93.CrossRef
54.
Abrishami M, Abbasi S, Honaramooz A. The effect of donor age on progression of spermatogenesis in canine testicular tissue after xenografting into immunodeficient mice. Theriogenology. 2010;73(4):512–22.PubMedCrossRef
55.
Reddy N, Mahla RS, Thathi R, Suman SK, Jose J, Goel S. Gonadal status of male recipient mice influences germ cell development in immature buffalo testis tissue xenograft. Reprod (Cambridge England). 2012;143(1):59–69.CrossRef
56.
Ntemou E, Kadam P, Van Saen D, Wistuba J, Mitchell RT, Schlatt S, et al. Complete spermatogenesis in intratesticular testis tissue xenotransplants from immature non-human primate. Hum Reprod (Oxford England). 2019;34(3):403–13.CrossRef
57.
Rathi R, Zeng W, Megee S, Conley A, Meyers S, Dobrinski I. Maturation of testicular tissue from infant monkeys after xenografting into mice. Endocrinology. 2008;149(10):5288–96.PubMedPubMedCentralCrossRef
58.
Ehmcke J, Gassei K, Westernströer B, Schlatt S. Immature rhesus monkey (macaca mulatta) testis xenografts show increased growth, but not enhanced seminiferous differentiation, under human chorionic gonadotropin treatment of nude mouse recipients. Int J Androl. 2011;34(5 Pt 2):e459–67.PubMedCrossRef
59.
Poels J, Abou-Ghannam G, Herman S, Van Langendonckt A, Wese FX, Wyns C. 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.PubMedPubMedCentralCrossRef
60.
Hutka M, Kadam P, Van Saen D, Homer NZM, Onofre J, Wallace WHB et al. Fertility preservation in childhood cancer: endocrine activity in prepubertal human testis xenografts exposed to a pubertal hormone environment. Cancers 2020; 12(10).
61.
Tseng H, Liu YL, Lu BJ, Chen CH. Immature testicular tissue engineered from weaned mice to adults for prepubertal fertility preservation-an in vivo translational study. Int J Mol Sci 2022; 23(4).
62.
Lin YH, Yeh YC, Tzeng CR, Shang WJ, Liu JY, Chen CH. Evaluating the effects of immunosuppression by in-vivo bioluminescence imaging after allotransplantation of ovarian grafts. Reprod Biomed Online. 2011;22(2):220–7.PubMedCrossRef
63.
64.
Chen CH, Wang CW, Hsu MI, Huang YH, Lai WF, Tzeng CR. Bioluminescence imaging as a tool to evaluate germ cells in vitro and transplantation in vivo as fertility preservation of prepubertal male mice. Fertil Steril. 2012;97(5):1192–8.PubMedCrossRef
65.
Zinn KR, Chaudhuri TR, Szafran AA, O’Quinn D, Weaver C, Dugger K, et al. Noninvasive bioluminescence imaging in small animals. ILAR J. 2008;49(1):103–15.PubMedCrossRef
66.
Mallick KK, Cox SC. Biomaterial scaffolds for tissue engineering. Front Biosci. 2013;5(1):341–60.CrossRef
67.
Chan BP, Leong KW. Scaffolding in tissue engineering: general approaches and tissue-specific considerations. European spine journal: official publication of the European Spine Society, the European Spinal Deformity Society, and the European section of the cervical. Spine Res Soc. 2008;17(Suppl 4):467–79.
68.
Dong L, Xia S, Wu K, Huang Z, Chen H, Chen J, et al. A ph/enzyme-responsive tumor-specific delivery system for doxorubicin. Biomaterials. 2010;31(24):6309–16.PubMedCrossRef
69.
Kolambkar YM, Dupont KM, Boerckel JD, Huebsch N, Mooney DJ, Hutmacher DW, et al. An alginate-based hybrid system for growth factor delivery in the functional repair of large bone defects. Biomaterials. 2011;32(1):65–74.PubMedCrossRef
70.
Shojarazavi N, Mashayekhan S, Pazooki H, Mohsenifard S, Baniasadi H. Alginate/cartilage extracellular matrix-based injectable interpenetrating polymer network hydrogel for cartilage tissue engineering. J Biomater Appl. 2021;36(5):803–17.PubMedCrossRef
71.
Vermeulen M, Poels J, de Michele F, des Rieux A, Wyns C. Restoring fertility with cryopreserved prepubertal testicular tissue: perspectives with hydrogel encapsulation, nanotechnology, and bioengineered scaffolds. Ann Biomed Eng. 2017;45(7):1770–81.PubMedCrossRef
72.
Catoira MC, Fusaro L, Di Francesco D, Ramella M, Boccafoschi F. Overview of natural hydrogels for regenerative medicine applications. J Mater Sci - Mater Med. 2019;30(10):115.PubMedPubMedCentralCrossRef
73.
74.
Poels J, Abou-Ghannam G, Decamps A, Leyman M, Rieux A, Wyns C. Transplantation of testicular tissue in alginate hydrogel loaded with vegf nanoparticles improves spermatogonial recovery. J Controlled Release: Official J Controlled Release Soc. 2016;234:79–89.CrossRef
75.
Cilia La Corte AL, Philippou H, Ariëns RA. Role of fibrin structure in thrombosis and vascular disease. Adv Protein Chem Struct Biology. 2011;83:75–127.CrossRef
76.
Vedakumari WS, Prabu P, Babu SC, Sastry TP. Fibrin nanoparticles as possible vehicles for drug delivery. Biochim Biophys Acta. 2013;1830(8):4244–53.PubMedCrossRef
77.
78.
Eslahi N, Hadjighassem MR, Joghataei MT, Mirzapour T, Bakhtiyari M, Shakeri M, et al. The effects of poly l-lactic acid nanofiber scaffold on mouse spermatogonial stem cell culture. Int J Nanomed. 2013;8:4563–76.
79.
Byrne AM, Bouchier-Hayes DJ, Harmey JH. Angiogenic and cell survival functions of vascular endothelial growth factor (vegf). J Cell Mol Med. 2005;9(4):777–94.PubMedPubMedCentralCrossRef
80.
Johnson KE, Wilgus TA. Vascular endothelial growth factor and angiogenesis in the regulation of cutaneous wound repair. Adv Wound care. 2014;3(10):647–61.CrossRef
81.
Kang F, Yi Q, Gu P, Dong Y, Zhang Z, Zhang L, et al. Controlled growth factor delivery system with osteogenic-angiogenic coupling effect for bone regeneration. J Orthop Translation. 2021;31:110–25.CrossRef
82.
Losi P, Briganti E, Errico C, Lisella A, Sanguinetti E, Chiellini F, et al. Fibrin-based scaffold incorporating vegf- and bfgf-loaded nanoparticles stimulates wound healing in diabetic mice. Acta Biomater. 2013;9(8):7814–21.PubMedCrossRef
83.
Simón-Yarza T, Formiga FR, Tamayo E, Pelacho B, Prosper F, Blanco-Prieto MJ. Vascular endothelial growth factor-delivery systems for cardiac repair: an overview. Theranostics. 2012;2(6):541–52.PubMedPubMedCentralCrossRef
84.
Gnavi S, di Blasio L, Tonda-Turo C, Mancardi A, Primo L, Ciardelli G, et al. Gelatin-based hydrogel for vascular endothelial growth factor release in peripheral nerve tissue engineering. J Tissue Eng Regen Med. 2017;11(2):459–70.PubMedCrossRef
85.
Li Z, Qu T, Ding C, Ma C, Sun H, Li S, et al. Injectable gelatin derivative hydrogels with sustained vascular endothelial growth factor release for induced angiogenesis. Acta Biomater. 2015;13:88–100.PubMedCrossRef
86.
Chung CW, Marra KG, Li H, Leung AS, Ward DH, Tan H, et al. Vegf microsphere technology to enhance vascularization in fat grafting. Ann Plast Surg. 2012;69(2):213–9.PubMedCrossRef
87.
Lee J, Lee KY. Local and sustained vascular endothelial growth factor delivery for angiogenesis using an injectable system. Pharm Res. 2009;26(7):1739–44.PubMedCrossRef
88.
O’Brien FJ, Harley BA, Yannas IV, Gibson LJ. The effect of pore size on cell adhesion in collagen-gag scaffolds. Biomaterials. 2005;26(4):433–41.PubMedCrossRef
89.
Sellimi S, Younes I, Ayed HB, Maalej H, Montero V, Rinaudo M, et al. Structural, physicochemical and antioxidant properties of sodium alginate isolated from a Tunisian brown seaweed. Int J Biol Macromol. 2015;72:1358–67.PubMedCrossRef
90.
Hellström M, Kalén M, Lindahl P, Abramsson A, Betsholtz C. Role of pdgf-b and pdgfr-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development. 1999;126(14):3047–55.PubMedCrossRef
91.
Del Vento F, Poels J, Vermeulen M, Ucakar B, Giudice MG, Kanbar M et al. Accelerated and improved vascular maturity after transplantation of testicular tissue in hydrogels supplemented with vegf- and pdgf-loaded nanoparticles. Int J Mol Sci 2021; 22(11).
92.
Del Vento F, Vermeulen M, Ucakar B, Poels J, des Rieux A, Wyns C. Significant benefits of nanoparticles containing a necrosis inhibitor on mice testicular tissue autografts outcomes. Int J Mol Sci 2019; 20(23).
93.
Fathi-Achachelouei M, Knopf-Marques H, Ribeiro da Silva CE, Barthès J, Bat E, Tezcaner A, et al. Use of nanoparticles in tissue engineering and regenerative medicine. Front Bioeng Biotechnol. 2019;7:113.PubMedPubMedCentralCrossRef
94.
Monteiro N, Martins A, Reis RL, Neves NM. Nanoparticle-based bioactive agent release systems for bone and cartilage tissue engineering. Regenerative Therapy. 2015;1:109–18.PubMedPubMedCentralCrossRef
95.
Tan HL, Teow SY, Pushpamalar J. Application of metal nanoparticle−hydrogel composites in tissue regeneration. Bioeng (Basel Switzerland) 2019; 6(1).
96.
Hasan A, Morshed M, Memic A, Hassan S, Webster TJ, Marei HE. Nanoparticles in tissue engineering: applications, challenges and prospects. Int J Nanomed. 2018;13:5637–55.CrossRef
97.
Rathi R, Honaramooz A, Zeng W, Schlatt S, Dobrinski I. Germ cell fate and seminiferous tubule development in bovine testis xenografts. Reprod (Cambridge England). 2005;130(6):923–9.CrossRef
Metadata
Title
Advancements in fertility preservation strategies for pediatric male cancer patients: a review of cryopreservation and transplantation of immature testicular tissue
Authors
Zih-Yi Sung
Yong-Qi Liao
Jung-Hsiu Hou
Hong-Hsien Lai
Sung-Ming Weng
Hai-Wei Jao
Buo-Jia Lu
Chi-Huang Chen
Publication date
01-12-2024
Publisher
BioMed Central
Keyword
Fertility
Published in
Reproductive Biology and Endocrinology / Issue 1/2024
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-024-01219-5

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