{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,23]],"date-time":"2026-01-23T13:14:00Z","timestamp":1769174040453,"version":"3.49.0"},"reference-count":64,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,11,1]],"date-time":"2021-11-01T00:00:00Z","timestamp":1635724800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,11,1]],"date-time":"2021-11-01T00:00:00Z","timestamp":1635724800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Centro Hospitalar e Universit\u00e1rio de Coimbra, Coimbra"},{"name":"Sociedade Portuguesa de Ginecologia"},{"DOI":"10.13039\/100004334","name":"Merck\u00ae","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100004334","id-type":"DOI","asserted-by":"crossref"}]},{"name":"National Funds via FCT"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Ovarian Res"],"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>Cryopreservation of ovarian tissue is a powerful technique for preserving female fertility, as it can restore fertility and endocrine function. To increase the longevity of the transplant and decrease the risk of reimplantation of neoplastic cells, several studies have been carried out with culture of ovarian tissue. The aim of this study was to compare a conventional (2D) culture with an alginate matrix three-dimensional (3D) model for ovarian tissue culture.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>The ovarian tissue culture within the alginate matrix (3D) was similar to 2D culture, regarding follicular density and cell apoptosis in follicles and stroma. The proliferation rate remained stable in both models for follicles, but for stromal cell proliferation it decreased only in 3D culture (<jats:italic>p<\/jats:italic>\u00a0=\u20090.001). At 24\u2009h of culture, cytotoxicity was lower in the 3D model (<jats:italic>p<\/jats:italic>\u00a0=\u20090.006). As culture time increased, cytotoxicity seemed similar. Degradation of the tissue was suggested by the histological score analysis of tissue morphology after 72\u2009h of culture. Tissue injury was greater (<jats:italic>p<\/jats:italic>\u00a0=\u20090.01) in 3D culture due to higher interstitial oedema (<jats:italic>p<\/jats:italic>\u00a0=\u20090.017) and tissue necrosis (<jats:italic>p<\/jats:italic>\u00a0=\u20090.035).<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusion<\/jats:title>\n                <jats:p>According to our results, 3D culture of ovarian tissue has no advantage over 2Dculture; it is more time consuming and difficult to perform and has worse reproducibility.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s13048-021-00892-z","type":"journal-article","created":{"date-parts":[[2021,11,1]],"date-time":"2021-11-01T19:02:37Z","timestamp":1635793357000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["The challenge of ovarian tissue culture: 2D versus 3D culture"],"prefix":"10.1186","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1977-5258","authenticated-orcid":false,"given":"Ana Sofia","family":"Pais","sequence":"first","affiliation":[]},{"given":"Sandra","family":"Reis","sequence":"additional","affiliation":[]},{"given":"Mafalda","family":"Laranjo","sequence":"additional","affiliation":[]},{"given":"Francisco","family":"Caramelo","sequence":"additional","affiliation":[]},{"given":"F\u00e1tima","family":"Silva","sequence":"additional","affiliation":[]},{"given":"Maria Filomena","family":"Botelho","sequence":"additional","affiliation":[]},{"given":"Teresa","family":"Almeida-Santos","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2021,11,1]]},"reference":[{"issue":"1","key":"892_CR1","doi-asserted-by":"publisher","first-page":"7","DOI":"10.3322\/caac.21590","volume":"70","author":"RL Siegel","year":"2020","unstructured":"Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70(1):7\u201330.","journal-title":"CA Cancer J Clin"},{"issue":"11","key":"892_CR2","doi-asserted-by":"publisher","first-page":"1493","DOI":"10.1016\/S1470-2045(19)30456-5","volume":"20","author":"M Arnold","year":"2019","unstructured":"Arnold M, Rutherford MJ, Bardot A, Ferlay J, Andersson TML, Myklebust T\u00c5, et al. Progress in cancer survival, mortality, and incidence in seven high-income countries 1995\u20132014 (ICBP SURVMARK-2): a population-based study. Lancet Oncol. 2019;20(11):1493\u2013505.","journal-title":"Lancet Oncol"},{"key":"892_CR3","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1016\/B978-0-12-813209-8.00031-5","volume-title":"The ovary","author":"AM Akasha","year":"2019","unstructured":"Akasha AM, Woodruff TK. Oncofertility: preservation of ovarian function after a cancer diagnosis. In:  The ovary. 3rd ed: Elsevier Inc.; 2019. p. 501\u20138. https:\/\/doi.org\/10.1016\/B978-0-12-813209-8.00031-5.","edition":"3"},{"issue":"4","key":"892_CR4","first-page":"1","volume":"2020","author":"RA Anderson","year":"2020","unstructured":"Anderson RA, Amant F, Braat D, D\u2019Angelo A, Chuva de Sousa Lopes SM, Demeestere I, et al. ESHRE guideline: female fertility preservation. Hum Reprod Open. 2020;2020(4):1\u201317.","journal-title":"Hum Reprod Open"},{"key":"892_CR5","doi-asserted-by":"publisher","first-page":"857","DOI":"10.1016\/B978-0-323-47912-7.00033-0","volume-title":"Yen & Jaffe\u2019s reproductive endocrinology: physiology, pathophysiology, and clinical management: eighth edition","author":"FE Duncan","year":"2019","unstructured":"Duncan FE, Feinberg E, Brannigan RE, Edmonds M, Ataman L, Woodruff TK. Fertility preservation. In:  Yen & Jaffe\u2019s reproductive endocrinology: physiology, pathophysiology, and clinical management: eighth edition. 8th ed: Elsevier Inc.; 2019. p. 857\u2013886.e6. https:\/\/doi.org\/10.1016\/B978-0-323-47912-7.00033-0.","edition":"8"},{"issue":"6","key":"892_CR6","doi-asserted-by":"publisher","first-page":"1022","DOI":"10.1016\/j.fertnstert.2019.09.013","volume":"112","author":"Practice Commitee of the American Society for Reproductive Medicine","year":"2019","unstructured":"Practice Commitee of the American Society for Reproductive Medicine. Fertility preservation in patients undergoing gonadotoxic therapy or gonadectomy: a committee opinion. Fertil Steril. 2019;112(6):1022\u201333. https:\/\/doi.org\/10.1016\/j.fertnstert.2019.09.013.","journal-title":"Fertil Steril"},{"issue":"1","key":"892_CR7","doi-asserted-by":"publisher","first-page":"214","DOI":"10.1097\/01.AOG.0000150288.43243.34","volume":"105","author":"J Donnez","year":"2005","unstructured":"Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Obstet Gynecol. 2005;105(1):214.","journal-title":"Obstet Gynecol"},{"key":"892_CR8","first-page":"1","volume":"1","author":"J Chen","year":"2021","unstructured":"Chen J, Todorov P, Isachenko E, Rahimi G, Mallmann P, Isachenko V. Construction and cryopreservation of an artificial ovary in cancer patients as an element of cancer therapy and a promising approach to fertility restoration. Hum Fertil. 2021;1:1\u201321.","journal-title":"Hum Fertil"},{"issue":"6","key":"892_CR9","doi-asserted-by":"publisher","first-page":"1746","DOI":"10.1007\/s43032-021-00517-2","volume":"28","author":"S Lee","year":"2021","unstructured":"Lee S, Ozkavukcu S, Ku SY. Current and future perspectives for improving ovarian tissue cryopreservation and transplantation outcomes for cancer patients. Reprod Sci. 2021;28(6):1746\u201358.","journal-title":"Reprod Sci"},{"key":"892_CR10","doi-asserted-by":"publisher","unstructured":"Terren C, Nisolle M, Munaut C. Pharmacological inhibition of the PI3K \/ PTEN \/ Akt and mTOR signalling pathways limits follicle activation induced by ovarian cryopreservation and in vitro culture. J Ovarian Res. 2021:1\u201315. https:\/\/doi.org\/10.1186\/s13048-021-00846-5.","DOI":"10.1186\/s13048-021-00846-5"},{"issue":"10\u201312","key":"892_CR11","doi-asserted-by":"publisher","first-page":"931","DOI":"10.1387\/ijdb.120175mz","volume":"56","author":"M Belli","year":"2012","unstructured":"Belli M, Vigone G, Merico V, Redi CA, Zuccotti M, Garagna S. Towards a 3D culture of mouse ovarian follicles. Int J Dev Biol. 2012;56(10\u201312):931\u20137.","journal-title":"Int J Dev Biol"},{"key":"892_CR12","doi-asserted-by":"publisher","unstructured":"Monniaux D, Cadoret V, Cl\u00e9ment F, Dalbies-Tran R, Elis S, Fabre S, et al. Folliculogenesis. In: Huhtaniemi I, Martini L, editors. Encyclopedia of Endocrine Diseases (Second Edition),  vol. 2. Oxford: Academic Press; 2019. p. 377\u201398. https:\/\/doi.org\/10.1016\/B978-0-12-801238-3.64550-6.","DOI":"10.1016\/B978-0-12-801238-3.64550-6"},{"issue":"4","key":"892_CR13","first-page":"910","volume":"14","author":"M Kapa\u0142czy\u0144ska","year":"2018","unstructured":"Kapa\u0142czy\u0144ska M, Kolenda T, Przyby\u0142a W, Zaj\u0105czkowska M, Teresiak A, Filas V, et al. State of the art paper 2D and 3D cell cultures \u2013 a comparison of different types of cancer cell cultures. Arch Med Sci. 2018;14(4):910\u20139.","journal-title":"Arch Med Sci"},{"issue":"March","key":"892_CR14","first-page":"1","volume":"7","author":"C Jensen","year":"2020","unstructured":"Jensen C, Teng Y. Is it time to start transitioning from 2D to 3D cell culture? Front Mol Biosci. 2020;7(March):1\u201315.","journal-title":"Front Mol Biosci"},{"issue":"3","key":"892_CR15","doi-asserted-by":"publisher","first-page":"R25","DOI":"10.1530\/REP-19-0501","volume":"160","author":"HM Kinnear","year":"2020","unstructured":"Kinnear HM, Tomaszewski CE, Chang FL, Moravek MB, Xu M, Padmanabhan V, et al. The ovarian stroma as a new frontier. Reproduction. 2020;160(3):R25\u201339.","journal-title":"Reproduction"},{"issue":"3","key":"892_CR16","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1016\/S1472-6483(10)62143-8","volume":"9","author":"J Scott","year":"2004","unstructured":"Scott J, Carlsson IB, Bavister BD, Hovatta O. Human ovarian tissue cultures: extracellular matrix composition , coating density and tissue dimensions. Reprod Biomed Online. 2004;9(3):287\u201393. https:\/\/doi.org\/10.1016\/S1472-6483(10)62143-8.","journal-title":"Reprod Biomed Online"},{"issue":"June","key":"892_CR17","first-page":"4","volume":"52","author":"SM King","year":"2011","unstructured":"King SM, Quartuccio S, Hilliard TS, Inoue K, Burdette JE. Alginate hydrogels for three-dimensional organ culture of ovaries and oviducts. J Vis Exp. 2011;52(June):4\u20139.","journal-title":"J Vis Exp"},{"issue":"8","key":"892_CR18","doi-asserted-by":"publisher","first-page":"3921","DOI":"10.1210\/en.2008-1674","volume":"150","author":"KS Jackson","year":"2009","unstructured":"Jackson KS, Inoue K, Davis DA, Hilliard TS, Burdette JE. Three-dimensional ovarian organ culture as a tool to study normal ovarian surface epithelial wound repair. Endocrinology. 2009;150(8):3921\u20136.","journal-title":"Endocrinology"},{"issue":"3","key":"892_CR19","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1159\/000499054","volume":"46","author":"EC Rivas Leonel","year":"2019","unstructured":"Rivas Leonel EC, Lucci CM, Amorim CA. Cryopreservation of human ovarian tissue: a review. Transfus Med Hemother. 2019;46(3):173\u201381.","journal-title":"Transfus Med Hemother"},{"issue":"7","key":"892_CR20","doi-asserted-by":"publisher","first-page":"1531","DOI":"10.1093\/humrep\/dew049","volume":"31","author":"H Yin","year":"2016","unstructured":"Yin H, Kristensen SG, Jiang H, Rasmussen A, Andersen CY. Survival and growth of isolated pre-antral follicles from human ovarian medulla tissue during long-term 3D culture. Hum Reprod. 2016;31(7):1531\u20139.","journal-title":"Hum Reprod"},{"issue":"1","key":"892_CR21","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1093\/humrep\/12.1.101","volume":"12","author":"KT Gunasena","year":"1997","unstructured":"Gunasena KT, Villines PM, Critser ES, Critser JK. Live births after autologous transplant of cryopreserved mouse ovaries. Hum Reprod. 1997;12(1):101\u20136.","journal-title":"Hum Reprod"},{"issue":"1","key":"892_CR22","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1095\/biolreprod54.1.197","volume":"54","author":"JJ Eppig","year":"1996","unstructured":"Eppig JJ, O\u2019Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod. 1996;54(1):197\u2013207.","journal-title":"Biol Reprod"},{"issue":"4","key":"892_CR23","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1093\/humupd\/dmp056","volume":"16","author":"J Smitz","year":"2010","unstructured":"Smitz J, Dolmans MM, Donnez J, Fortune JE, Hovatta O, Jewgenow K, et al. Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation. Hum Reprod Update. 2010;16(4):395\u2013414.","journal-title":"Hum Reprod Update"},{"issue":"1","key":"892_CR24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-020-14936-3","volume":"11","author":"M Wagner","year":"2020","unstructured":"Wagner M, Yoshihara M, Douagi I, Damdimopoulos A, Panula S, Petropoulos S, et al. Single-cell analysis of human ovarian cortex identifies distinct cell populations but no oogonial stem cells. Nat Commun. 2020;11(1):1\u201315. https:\/\/doi.org\/10.1038\/s41467-020-14936-3.","journal-title":"Nat Commun"},{"issue":"7","key":"892_CR25","doi-asserted-by":"publisher","first-page":"1633","DOI":"10.1007\/s10439-017-1816-6","volume":"45","author":"J Vanacker","year":"2017","unstructured":"Vanacker J, Amorim CA. Alginate: a versatile biomaterial to encapsulate isolated ovarian follicles. Ann Biomed Eng. 2017;45(7):1633\u201349.","journal-title":"Ann Biomed Eng"},{"issue":"1","key":"892_CR26","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1186\/1477-7827-8-119","volume":"8","author":"N Desai","year":"2010","unstructured":"Desai N, Alex A, AbdelHafez F, Calabro A, Goldfarb J, Fleischman A, et al. Three-dimensional in vitro follicle growth: overview of culture models, biomaterials, design parameters and future directions. Reprod Biol Endocrinol. 2010;8(1):119 Available from: http:\/\/www.rbej.com\/content\/8\/1\/119.","journal-title":"Reprod Biol Endocrinol"},{"issue":"10","key":"892_CR27","first-page":"173","volume":"19","author":"R Fathi","year":"2017","unstructured":"Fathi R, Valojerdi MR, Ebrahimi B, Eivazkhani F, Akbarpour M, Tahaei LS, et al. Fertility preservation in cancer patients: in vivo and in vitro options. Cell J. 2017;19(10):173\u201383 Available from: https:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC5412777\/pdf\/Cell-J-19-173.pdf.","journal-title":"Cell J"},{"key":"892_CR28","doi-asserted-by":"publisher","unstructured":"Higuchi CM, Maeda Y, Horiuchi T, Yamazaki Y. A simplified method for three-dimensional ( 3-D) ovarian tissue culture yielding oocytes competent to produce full-term offspring in mice. PLoS One. 2015;10(11). https:\/\/doi.org\/10.1371\/journal.pone.0143114.","DOI":"10.1371\/journal.pone.0143114"},{"issue":"5","key":"892_CR29","doi-asserted-by":"publisher","first-page":"1013","DOI":"10.1089\/107632703322495655","volume":"9","author":"SA Pangas","year":"2003","unstructured":"Pangas SA, Saudye H, Shea LD, Woodruff TK. Novel approach for the three-dimensional culture of granulosa cell-oocyte complexes. Tissue Eng. 2003;9(5):1013\u201321.","journal-title":"Tissue Eng"},{"issue":"6","key":"892_CR30","doi-asserted-by":"publisher","first-page":"916","DOI":"10.1095\/biolreprod.106.054833","volume":"75","author":"M Xu","year":"2006","unstructured":"Xu M, West E, Shea LD, Woodruff TK. Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol Reprod. 2006;75(6):916\u201323.","journal-title":"Biol Reprod"},{"key":"892_CR31","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1477-7827-3-47","volume":"3","author":"M Heise","year":"2005","unstructured":"Heise M, Koepsel R, Russell AJ, McGee EA. Calcium alginate microencapsulation of ovarian follicles impacts FSH delivery and follicle morphology. Reprod Biol Endocrinol. 2005;3:1\u20138.","journal-title":"Reprod Biol Endocrinol"},{"issue":"1","key":"892_CR32","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1093\/humrep\/den343","volume":"24","author":"CA Amorim","year":"2009","unstructured":"Amorim CA, Van Langendonckt A, David A, Dolmans MM, Donnez J. Survival of human pre-antral follicles after cryopreservation of ovarian tissue, follicular isolation and in vitro culture in a calcium alginate matrix. Hum Reprod. 2009;24(1):92\u20139.","journal-title":"Hum Reprod"},{"issue":"2","key":"892_CR33","doi-asserted-by":"publisher","first-page":"133","DOI":"10.3390\/microarrays4020133","volume":"4","author":"T Andersen","year":"2015","unstructured":"Andersen T, Auk-Emblem P, Dornish M. 3D cell culture in alginate hydrogels. Microarrays. 2015;4(2):133\u201361.","journal-title":"Microarrays"},{"issue":"30","key":"892_CR34","doi-asserted-by":"publisher","first-page":"6076","DOI":"10.1016\/j.biomaterials.2009.07.054","volume":"30","author":"L Gurski","year":"2009","unstructured":"Gurski L, Jha A, Zhang C, Jia X, Farach-Carson M. Hyaluronic acid-based hydrogels as 3D matrices for in vitro evaluation of chemotherapeutic drugs using poorly adherent prostate cancer cells. Biomaterials. 2009;30(30):6076\u201385 Available from: https:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC3624763\/pdf\/nihms412728.pdf.","journal-title":"Biomaterials"},{"issue":"1","key":"892_CR35","doi-asserted-by":"publisher","first-page":"181","DOI":"10.3390\/ijms19010181","volume":"19","author":"J Hoarau-V\u00e9chot","year":"2018","unstructured":"Hoarau-V\u00e9chot J, Rafii A, Touboul C, Pasquier J. Halfway between 2D and animal models: are 3D cultures the ideal tool to study cancer-microenvironment interactions? Int J Mol Sci. 2018;19(1):181.","journal-title":"Int J Mol Sci"},{"issue":"4","key":"892_CR36","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1089\/adt.2014.573","volume":"12","author":"R Edmondson","year":"2014","unstructured":"Edmondson R, Broglie JJ, Adcock AF, Yang L. Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev Technol. 2014;12(4):207\u201318.","journal-title":"Assay Drug Dev Technol"},{"issue":"17","key":"892_CR37","doi-asserted-by":"publisher","first-page":"1361","DOI":"10.1007\/s10529-006-9104-9","volume":"28","author":"SF Khattak","year":"2006","unstructured":"Khattak SF, Spatara M, Roberts L, Roberts SC. Application of colorimetric assays to assess viability, growth and metabolism of hydrogel-encapsulated cells. Biotechnol Lett. 2006;28(17):1361\u201370.","journal-title":"Biotechnol Lett"},{"key":"892_CR38","doi-asserted-by":"publisher","first-page":"915","DOI":"10.1071\/RD12401","volume":"26","author":"IR Brito","year":"2014","unstructured":"Brito IR, Lima IMT, Xu M, Shea LD. Three-dimensional systems for in vitro follicular culture\u00a0: overview of alginate-based matrices. Reprod Fertil Dev. 2014;26:915\u201330.","journal-title":"Reprod Fertil Dev"},{"issue":"1","key":"892_CR39","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1038\/emm.1997.4","volume":"29","author":"MH Javed","year":"1997","unstructured":"Javed MH, Azimuddin SMI, Hussain AN, Ahmed A, Ishaq M. Purification and characterization of lactate dehydrogenase from Varanus liver. Exp Mol Med. 1997;29(1):25\u201330.","journal-title":"Exp Mol Med"},{"issue":"2","key":"892_CR40","doi-asserted-by":"publisher","first-page":"34","DOI":"10.15761\/COGRM.1000110","volume":"1","author":"V Asfour","year":"2015","unstructured":"Asfour V, Polson A, Varma R, Menon P. Evaluating ovarian preservation after ovarian torsion using the ovarian preservation score and tissue necrosis score. Clin Obstet Gynecol Reprod Med. 2015;1(2):34\u20139.","journal-title":"Clin Obstet Gynecol Reprod Med"},{"issue":"4","key":"892_CR41","doi-asserted-by":"publisher","first-page":"1327","DOI":"10.1016\/j.fertnstert.2008.10.053","volume":"93","author":"S Guven","year":"2010","unstructured":"Guven S, Muci E, Unsal MA, Yulug E, Alver A, Duman MK, et al. The effects of carbon dioxide pneumoperitoneum on ovarian blood flow, oxidative stress markers, and morphology during laparoscopy: a rabbit model. Fertil Steril. 2010;93(4):1327\u201332. https:\/\/doi.org\/10.1016\/j.fertnstert.2008.10.053.","journal-title":"Fertil Steril"},{"issue":"6","key":"892_CR42","doi-asserted-by":"publisher","first-page":"807","DOI":"10.3892\/br.2015.515","volume":"3","author":"A Eser","year":"2015","unstructured":"Eser A, Hizli D, Haltas H, Namuslu M, Kosus A, Kosus N, et al. Effects of curcumin on ovarian ischemia-reperfusion injury in a rat model. Biomed Rep. 2015;3(6):807\u201313.","journal-title":"Biomed Rep"},{"key":"892_CR43","doi-asserted-by":"publisher","first-page":"3537471","DOI":"10.1155\/2018\/3537471","volume":"2018","author":"SY Lee","year":"2018","unstructured":"Lee SY, Ju MK, Jeon HM, Jeong EK, Lee YJ, Kim CH, et al. Regulation of tumor progression by programmed necrosis. Oxidative Med Cell Longev. 2018;2018:3537471.","journal-title":"Oxidative Med Cell Longev"},{"issue":"3","key":"892_CR44","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1093\/molehr\/8.3.228","volume":"8","author":"M Otala","year":"2002","unstructured":"Otala M, Erkkil\u00e4 K, Tuuri T, Sj\u00f6berg J, Suomalainen L, Suikkari AM, et al. Cell death and its suppression in human ovarian tissue culture. Mol Hum Reprod. 2002;8(3):228\u201336.","journal-title":"Mol Hum Reprod"},{"issue":"18","key":"892_CR45","doi-asserted-by":"publisher","first-page":"3825","DOI":"10.1016\/S0142-9612(02)00118-7","volume":"23","author":"G Orive","year":"2002","unstructured":"Orive G, Ponce S, Hern\u00e1ndez RM, Gasc\u00f3n AR, Igartua M, Pedraz JL. Biocompatibility of microcapsules for cell immobilization elaborated with different type of alginates. Biomaterials. 2002;23(18):3825\u201331.","journal-title":"Biomaterials"},{"issue":"1","key":"892_CR46","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1016\/j.progpolymsci.2011.06.003","volume":"37","author":"KY Lee","year":"2012","unstructured":"Lee KY, Mooney DJ. Alginate: properties and biomedical applications. Prog Polym Sci. 2012;37(1):106\u201326.","journal-title":"Prog Polym Sci"},{"issue":"2","key":"892_CR47","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1093\/humupd\/dmi001","volume":"11","author":"MR Hussein","year":"2005","unstructured":"Hussein MR. Apoptosis in the ovary: molecular mechanisms. Hum Reprod Update. 2005;11(2):161\u201377.","journal-title":"Hum Reprod Update"},{"key":"892_CR48","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1042\/bj3260001","volume":"326","author":"GM Cohen","year":"1997","unstructured":"Cohen GM. Caspases: executioners of apoptosis. Biochem J. 1997;326:1\u201316.","journal-title":"Biochem J"},{"issue":"3","key":"892_CR49","doi-asserted-by":"publisher","first-page":"549","DOI":"10.1016\/S0015-0282(98)00194-0","volume":"70","author":"M Izawa","year":"1998","unstructured":"Izawa M, Nguyen PH, Kim HH, Yeh J. Expression of the apoptosis-related genes, caspase-1, caspase-3, DNA fragmentation factor, and apoptotic protease activating factor-1, in human granulosa cells. Fertil Steril. 1998;70(3):549\u201352.","journal-title":"Fertil Steril"},{"issue":"8","key":"892_CR50","first-page":"1605","volume":"57","author":"M Krajewska","year":"1997","unstructured":"Krajewska M, Wang HG, Krajewski S, Zapata JM, Shabaik A, Gascoyne R, et al. Immunohistochemical analysis of in vivo patterns of expression of CPP32 (Caspase-3), a cell death protease. Cancer Res. 1997;57(8):1605\u201313.","journal-title":"Cancer Res"},{"issue":"5","key":"892_CR51","doi-asserted-by":"publisher","first-page":"1176","DOI":"10.1016\/j.fertnstert.2012.01.123","volume":"97","author":"M Milenkovic","year":"2012","unstructured":"Milenkovic M, Diaz-Garcia C, Wallin A, Br\u00e4nnstr\u00f6m M. Viability and function of the cryopreserved whole rat ovary: comparison between slow-freezing and vitrification. Fertil Steril. 2012;97(5):1176\u201382.","journal-title":"Fertil Steril"},{"key":"892_CR52","first-page":"149","volume-title":"Experimental surgical models in the laboratory rat","author":"VE Di Loreto","year":"2009","unstructured":"Di Loreto VE, Pera LI, Rigalli A. In: Rigalli A, Di Loreto V, editors. Experimental surgical models in the laboratory rat. 1st ed; 2009. p. 149\u201351.","edition":"1"},{"issue":"3","key":"892_CR53","first-page":"462","volume":"52","author":"DK Khajuria","year":"2012","unstructured":"Khajuria DK, Razdan R, Mahapatra DR. Descri\u00e7\u00e3o de um novo m\u00e9todo de ooforectomia em ratas. Rev Bras Reum. 2012;52(3):462\u201370 Available from: http:\/\/www.scielo.br\/pdf\/rbr\/v52n3\/v52n3a16.pdf.","journal-title":"Rev Bras Reum"},{"issue":"2","key":"892_CR54","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1016\/j.rbmo.2010.10.015","volume":"22","author":"M Rosendahl","year":"2011","unstructured":"Rosendahl M, Schmidt KT, Ernst E, Rasmussen PE, Loft A, Byskov AG, et al. Cryopreservation of ovarian tissue for a decade in Denmark: a view of the technique. Reprod Biomed Online. 2011;22(2):162\u201371. https:\/\/doi.org\/10.1016\/j.rbmo.2010.10.015.","journal-title":"Reprod Biomed Online"},{"key":"892_CR55","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12958-015-0015-2","volume":"13","author":"L Henry","year":"2015","unstructured":"Henry L, Labied S, Fransolet M, Kirschvink N, Blacher S, Noel A, et al. Isoform 165 of vascular endothelial growth factor in collagen matrix improves ovine cryopreserved ovarian tissue revascularisation after xenotransplantation in mice. Reprod Biol Endocrinol. 2015;13:1\u201310.","journal-title":"Reprod Biol Endocrinol"},{"issue":"10","key":"892_CR56","doi-asserted-by":"publisher","first-page":"1591","DOI":"10.1111\/jog.12770","volume":"41","author":"N Yildirim","year":"2015","unstructured":"Yildirim N, Yigitturk G, Sahingoz Yildirim AG, Akdemir A, Ilgen O, Yeniel O, et al. Octreotide protects ovary against ischemia-reperfusion injury in rats: evaluation of histological and biochemical parameters. J Obstet Gynaecol Res. 2015;41(10):1591\u20137.","journal-title":"J Obstet Gynaecol Res"},{"key":"892_CR57","unstructured":"Brown K, Awan NA, Le PH, Wilson AM. Histology, Cell Death. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2021. Available at: http:\/\/www.ncbi.nlm.nih.gov\/books\/NBK526045\/.\u00a0[cited April 24, 2021]"},{"issue":"2","key":"892_CR58","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1210\/edrv-17-2-121","volume":"17","author":"A Gougeon","year":"1996","unstructured":"Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev. 1996;17(2):121\u201355.","journal-title":"Endocr Rev"},{"issue":"3","key":"892_CR59","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0091073","volume":"9","author":"M Fransolet","year":"2014","unstructured":"Fransolet M, Labied S, Henry L, Masereel MC, Rozet E, Kirschvink N, et al. Strategies for using the sheep ovarian cortex as a model in reproductive medicine. PLoS One. 2014;9(3):1\u20137.","journal-title":"PLoS One"},{"issue":"5","key":"892_CR60","doi-asserted-by":"publisher","first-page":"1350","DOI":"10.1016\/j.fertnstert.2013.07.202","volume":"100","author":"V Luyckx","year":"2013","unstructured":"Luyckx V, Scalercio S, Jadoul P, Amorim CA, Soares M, Donnez J, et al. Evaluation of cryopreserved ovarian tissue from prepubertal patients after long-term xenografting and exogenous stimulation. Fertil Steril. 2013;100(5):1350\u20137.","journal-title":"Fertil Steril"},{"issue":"8","key":"892_CR61","doi-asserted-by":"publisher","first-page":"1251","DOI":"10.1007\/s10815-015-0542-y","volume":"32","author":"MM Dolmans","year":"2015","unstructured":"Dolmans MM, Binda MM, Jacobs S, Dehoux JP, Squifflet JL, Ambroise J, et al. Impact of the cryopreservation technique and vascular bed on ovarian tissue transplantation in cynomolgus monkeys. J Assist Reprod Genet. 2015;32(8):1251\u201362.","journal-title":"J Assist Reprod Genet"},{"issue":"3","key":"892_CR62","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/0022-1759(83)90438-6","volume":"64","author":"C Korzeniewski","year":"1983","unstructured":"Korzeniewski C, Callewaert DM. An enzyme-release assay for natural cytotoxicity. J Immunol Methods. 1983;64(3):313\u201320.","journal-title":"J Immunol Methods"},{"issue":"1","key":"892_CR63","first-page":"32","volume":"32","author":"F De Michele","year":"2017","unstructured":"De Michele F, Poels J, Weerens L, Petit C, Evrard Z, Ambroise J, et al. Preserved seminiferous tubule integrity with spermatogonial survival and induction of Sertoli and Leydig cell maturation after long-term organotypic culture of prepubertal human testicular tissue. Hum Reprod. 2017;32(1):32\u201345.","journal-title":"Hum Reprod"},{"issue":"19","key":"892_CR64","doi-asserted-by":"publisher","first-page":"4171","DOI":"10.1016\/j.biomaterials.2004.10.021","volume":"26","author":"H Keshaw","year":"2005","unstructured":"Keshaw H, Forbes A, Day RM. Release of angiogenic growth factors from cells encapsulated in alginate beads with bioactive glass. Biomaterials. 2005;26(19):4171\u20139.","journal-title":"Biomaterials"}],"container-title":["Journal of Ovarian Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13048-021-00892-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13048-021-00892-z\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13048-021-00892-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,2,8]],"date-time":"2023-02-08T07:05:58Z","timestamp":1675839958000},"score":1,"resource":{"primary":{"URL":"https:\/\/ovarianresearch.biomedcentral.com\/articles\/10.1186\/s13048-021-00892-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,1]]},"references-count":64,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["892"],"URL":"https:\/\/doi.org\/10.1186\/s13048-021-00892-z","relation":{},"ISSN":["1757-2215"],"issn-type":[{"value":"1757-2215","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,1]]},"assertion":[{"value":"24 April 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 October 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 November 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The present study was approved by the Ethics Committee for Animal Experimentation (ORBEA Authorization number 11060495\/23-11-2016) of the Faculty of Medicine of the University of Coimbra and performed according to the European Guidelines and Portuguese Law.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"None.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"147"}}