Hostname: page-component-848d4c4894-8kt4b Total loading time: 0 Render date: 2024-07-04T01:16:40.881Z Has data issue: false hasContentIssue false

In vitro maturation of oocytes in light of ovarian mitochondrial improvement: effectiveness and safety

Published online by Cambridge University Press:  02 July 2024

Nikos Petrogiannis
Affiliation:
ART Unit, Naval Hospital of Athens, Athens, Greece
Kalliopi Chatzovoulou*
Affiliation:
ART Unit, Naval Hospital of Athens, Athens, Greece
Maria Filippa
Affiliation:
ART Unit, Naval Hospital of Athens, Athens, Greece
Grigoris Grimbizis
Affiliation:
Unit for Human Reproduction, 1st Department of Obstetrics and Gynaecology, Aristotle University Medical School, Papageorgiou General Hospital, Thessaloniki, Greece
Efstratios Kolibianakis
Affiliation:
Unit for Human Reproduction, 1st Department of Obstetrics and Gynaecology, Aristotle University Medical School, Papageorgiou General Hospital, Thessaloniki, Greece
Katerina Chatzimeletiou
Affiliation:
Unit for Human Reproduction, 1st Department of Obstetrics and Gynaecology, Aristotle University Medical School, Papageorgiou General Hospital, Thessaloniki, Greece
*
Corresponding author: Kalliopi Chatzovoulou; Email: kchatzovoulou@icloud.com

Summary

In vitro maturation of oocytes (IVM) represents an assisted reproductive technique that involves the minimal or absence of ovarian stimulation and is beneficial to specific groups of patients. These may include women with polycystic ovarian syndrome and/or patients who need a fertility preservation option before undergoing gonadotoxic treatment. However, when IVM is applied in cases where it is not recommended, it can be considered as an add-on technique, as described by the ESHRE Guideline Group on Female Fertility Preservation. Interestingly, IVM has not been proven yet to be as effective as conventional IVF in the laboratory, in terms of clinical pregnancy and live birth rates, while concerns have been raised for its long-term safety. As a result, both safety and efficacy of IVM remain still questionable and additional data are needed to draw conclusions.

Type
Review Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdulhasan, M.K., Li, Q., Dai, J., Abu-Soud, H.M., Puscheck, E.E. and Rappolee, D.A. (2017) CoQ10 increases mitochondrial mass and polarization, ATP and Oct4 potency levels, and bovine oocyte MII during IVM while decreasing AMPK activity and oocyte death. Journal of Assisted Reproduction and Genetics 34, 15951607.CrossRefGoogle ScholarPubMed
Al-Sunaidi, M., Tulandi, T., Holzer, H., Sylvestre, C., Chian, R.C. and Tan, S.L. (2007) Repeated pregnancies and live births after in vitro maturation treatment. Fertility and Sterility 87, 1212.e9–12.CrossRefGoogle ScholarPubMed
Bao, S., Obata, Y., Carroll, J., Domeki, I and Kono, T. (2000) Epigenetic modifications necessary for normal development are established during oocyte growth in mice. Biology of Reproduction 62, 616621.CrossRefGoogle ScholarPubMed
Beilby, K.H., Kneebone, E., Roseboom, T.J., van Marrewijk, I.M., Thompson, J.G., Norman, R.J., Robker, R.L., Mol, B.W.J. and Wang, R. (2023) Offspring physiology following the use of IVM, IVF and ICSI: a systematic review and meta-analysis of animal studies. Human Reproduction Update 29, 272290.CrossRefGoogle ScholarPubMed
Belva, F., Roelants, M., Vermaning, S., Desmyttere, S., De Schepper, J., Bonduelle, M., Tournaye, H., Hes, F. and De Vos, M. (2020) Growth and other health outcomes of 2-year-old singletons born after IVM versus controlled ovarian stimulation in mothers with polycystic ovary syndrome. Human Reproduction Open 2020, hoz043.Google ScholarPubMed
Bertolini, M., Mason, J.B., Beam, S.W., Carneiro, G.F., Sween, M.L., Kominek, D.J., Moyer, A.L., Famula, T.R., Sainz, R.D. and Anderson, G.B. (2002) Morphology and morphometry of in vivo- and in vitro-produced bovine concepti from early pregnancy to term and association with high birth weights. Theriogenology 58, 973994.CrossRefGoogle ScholarPubMed
Bock, F.J. and Tait, S.W.G. (2020) Mitochondria as multifaceted regulators of cell death. Nature Reviews Molecular Cell Biology 21, 85100.CrossRefGoogle ScholarPubMed
Boyman, L., Karbowski, M. and Lederer, W.J. (2020) Regulation of Mitochondrial ATP production: Ca2+ signaling and quality control. Trends in Molecular Medicine 26, 2139.CrossRefGoogle ScholarPubMed
Braam, S.C., Ho, V.N.A., Pham, T.D., Mol, B.W, Van Wely, M. and Vuong, L.N. (2021) In-vitro maturation versus IVF: a cost-effectiveness analysis. Reproductive Biomedicine Online 42, 143149.CrossRefGoogle ScholarPubMed
Braga, D.P.D.A.F., Figueira, R.D.C.S., Ferreira, R.C., Pasqualotto, F.F., Iaconelli, A. and Borges, E. (2010) Contribution of in-vitro maturation in ovarian stimulation cycles of poor-responder patients. Reproductive Biomedicine Online 20, 335340.CrossRefGoogle ScholarPubMed
Buckett, W.M., Chian, R.C., Holzer, H., Dean, N., Usher, R. and Tan, S.L. (2007) Obstetric outcomes and congenital abnormalities after in vitro maturation, in vitro fertilization, and intracytoplasmic sperm injection. Obstet Gynecol 110, 885891.CrossRefGoogle ScholarPubMed
Buckett, W.M., Chian, R.C. and Tan, S.L. (2004) Human chorionic gonadotropin for in vitro oocyte maturation: does it improve the endometrium or implantation? The Journal of Reproductive Medicine 49, 9398.Google ScholarPubMed
Cao, Y., Zhao, H., Wang, Z., Zhang, C., Bian, Y., Liu, X., Zhang, C., Zhang, X. and Zhao, Y. (2020) Quercetin promotes in vitro maturation of oocytes from humans and aged mice. Cell Death & Disease 11, 965.CrossRefGoogle ScholarPubMed
Casper, R.F. (2015). Basic understanding of gonadotropin-releasing hormone–agonist triggering. Fertility and sterility 103, 867869.CrossRefGoogle ScholarPubMed
Cha, K.Y., Chung, H.M., Lee, D.R., Kwon, H., Chung, M.K., Park, L.S., Choi, D.H. and Yoon, T.K. (2005) Obstetric outcome of patients with polycystic ovary syndrome treated by in vitro maturation and in vitro fertilization-embryo transfer. Fertility and sterility 83, 14611465.CrossRefGoogle ScholarPubMed
Cha, K.Y., Han, S.Y., Chung, H.M., Choi, D.H., Lim, J.M., Lee, W.S., Ko, J.J. and Yoon, T.K. (2000) Pregnancies and deliveries after in vitro maturation culture followed by in vitro fertilization and embryo transfer without stimulation in women with polycystic ovary syndrome. Fertility and sterility 73, 978983.CrossRefGoogle ScholarPubMed
Cha, K.Y., Koo, J.J., Ko, J.J., Choi, D.H., Han, S.Y. and Yoon, T.K. (1991) Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertility and sterility 55, 109113.CrossRefGoogle Scholar
Chang, E.M., Song, H.S., Lee, D.R., Lee, W.S. and Yoon, T.K. (2014) In vitro maturation of human oocytes: its role in infertility treatment and new possibilities. Clinical and Experimental Reproductive Medicine 41, 4146.CrossRefGoogle ScholarPubMed
Child, T.J, Abdul-Jalil, A.K., Gulekli, B. and Tan, S.L. (2001) In vitro maturation and fertilization of oocytes from unstimulated normal ovaries, polycystic ovaries, and women with polycystic ovary syndrome. Fertility and sterility 76, 936942.CrossRefGoogle ScholarPubMed
Cobley, J.N. (2020) Mechanisms of mitochondrial ROS production in assisted reproduction: the known, the unknown, and the intriguing. Antioxidants 9, 933.CrossRefGoogle ScholarPubMed
Coticchio, G., Dal Canto, M., Fadini, R., Mignini Renzini, M., Guglielmo, M.C., Miglietta, S., Palmerini, M.G., Macchiarelli, G. and Nottola, S.A. (2016) Ultrastructure of human oocytes after in vitro maturation. Molecular Human Reproduction 22, 110118.CrossRefGoogle ScholarPubMed
De Vos, A., Van de Velde, H., Joris, H. and Van Steirteghem, A. (1999) In-vitro matured metaphase-I oocytes have a lower fertilization rate but similar embryo quality as mature metaphase-II oocytes after intracytoplasmic sperm injection. Human Reproduction 14, 18591863.CrossRefGoogle ScholarPubMed
De Vos, M., Grynberg, M., Ho, T.M., Yuan, Y., Albertini, D.F. and Gilchrist, R.B. (2021) Perspectives on the development and future of oocyte IVM in clinical practice. Journal of Assisted Reproduction and Genetics 38, 12651280.CrossRefGoogle ScholarPubMed
De Vos, M., Ortega-Hrepich, C., Albuz, F.K., Guzman, L., Polyzos, N.P., Smitz, J. and Devroey, P. (2011) Clinical outcome of non-hCG-primed oocyte in vitro maturation treatment in patients with polycystic ovaries and polycystic ovary syndrome. Fertility and sterility 96, 860864.CrossRefGoogle ScholarPubMed
De Vos, M., Smitz, J., Thompson, J.G. and Gilchrist, R.B. (2016) The definition of IVM is clear-variations need defining. Human Reproduction 31, 24112415.CrossRefGoogle ScholarPubMed
Dumollard, R., Campbell, K., Halet, G., Carroll, J. and Swann, K. (2008) Regulation of cytosolic and mitochondrial ATP levels in mouse eggs and zygotes. Developmental Biology 316, 431440.CrossRefGoogle ScholarPubMed
Edwards, R.G. (1962) Meiosis in ovarian oocytes of adult mammals. Nature 196, 446450.CrossRefGoogle Scholar
Edwards, R.G. (1965) Maturation in vitro of human ovarian oöcytes. Lancet 2, 926929.CrossRefGoogle ScholarPubMed
Edwards, R.G., Bavister, B.D. and Steptoe, P.C. (1969) Early stages of fertilization in vitro of human oocytes matured in vitro. Nature 221, 632635.CrossRefGoogle ScholarPubMed
ESHRE Add-ons working group, Lundin, K., Bentzen, J.G., Bozdag, G., Ebner, T., Harper, J., Le Clef, N., Moffett, A., Norcross, S., Polyzos, N.P. and Rautakallio-Hokkanen, S. (2023) Good practice recommendations on add-ons in reproductive medicine†. Human Reproduction 38, 20622104.Google ScholarPubMed
ESHRE Guideline Group on Female Fertility Preservation, Anderson, R.A., Amant, F., Braat, D., D’Angelo, A., Chuva de Sousa Lopes, S.M., Demeestere, I., Dwek, S., Frith, L., Lambertini, M. and Maslin, C. (2020) ESHRE guideline: female fertility preservation. Human Reproduction Open 2020, hoaa052.Google ScholarPubMed
Fadini, R., Comi, R., Mignini Renzini, M., Coticchio, G., Crippa, M., De Ponti, E. and Dal Canto, M. (2011) Anti-mullerian hormone as a predictive marker for the selection of women for oocyte in vitro maturation treatment. Journal of Assisted Reproduction and Genetics 28, 501508.CrossRefGoogle ScholarPubMed
Galvão, A., Segers, I., Smitz, J., Tournaye, H. and De Vos, M. (2018) In vitro maturation (IVM) of oocytes in patients with resistant ovary syndrome and in patients with repeated deficient oocyte maturation. Journal of Assisted Reproduction and Genetics 35, 21612171.CrossRefGoogle ScholarPubMed
Ge, H., Tollner, T.L., Hu, Z., Da, M., Li, X., Guan, H., Shan, D., Lu, J., Huang, C. and Dong, Q. (2012) Impaired mitochondrial function in murine oocytes is associated with controlled ovarian hyperstimulation and in vitro maturation. Reproduction, Fertility and Development 24, 945952.CrossRefGoogle ScholarPubMed
Gilchrist, R.B. (2011) Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reproduction, Fertility and Development 23, 2331.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Luciano, A.M., Richani, D., Zeng, H.T., Wang, X., De Vos, M., … and Thompson, J.G. (2016) Oocyte maturation and quality: role of cyclic nucleotides. Reproduction 152, R143R157.CrossRefGoogle ScholarPubMed
Gilchrist, R.B. and Smitz, J. (2023) Oocyte in vitro maturation: physiological basis and application to clinical practice. Fertility and sterility 119, 524539.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Ho, T.M., De Vos, M., Sanchez, F., Romero, S., Ledger, W.L., Anckaert, E., Vuong, L.N. and Smitz, J. (2024) A fresh start for IVM: capacitating the oocyte for development using pre-IVM. Human Reproduction Update 30, 325.CrossRefGoogle ScholarPubMed
Gonen, Y.A.E.L., Balakier, H., Powell, W. and Casper, R.F. (1990) Use of gonadotropin-releasing hormone agonist to trigger follicular maturation for in vitro fertilization. The Journal of Clinical Endocrinology & Metabolism 71, 918922.CrossRefGoogle ScholarPubMed
Hao, Y., Zhang, Z., Han, D., Cao, Y., Zhou, P., Wei, Z., Lv, M. and Chen, D. (2017) Gene expression profiling of human blastocysts from in vivo and ‘rescue IVM’ with or without melatonin treatment. Molecular Medicine Reports 16, 12781288.CrossRefGoogle ScholarPubMed
El Hachem, H., Sonigo, C., Benard, J., Presse, M., Sifer, C., Sermondade, N. and Grynberg, M. (2018) Comparison of GnRH agonist and hCG for priming in vitro maturation cycles in cancer patients undergoing urgent fertility preservation. PLoS One 13, e0208576.CrossRefGoogle ScholarPubMed
Heydarnejad, A., Ostadhosseini, S., Varnosfaderani, S.R., Jafarpour, F., Moghimi, A. and Nasr-Esfahani, M.H. (2019) Supplementation of maturation medium with CoQ10 enhances developmental competence of ovine oocytes through improvement of mitochondrial function. Molecular Reproduction and Development 86, 812824.CrossRefGoogle ScholarPubMed
Hourvitz, A., Maman, E., Brengauz, M., Machtinger, R. and Dor, J. (2010) In vitro maturation for patients with repeated in vitro fertilization failure due to “oocyte maturation abnormalities.” Fertility and sterility 94, 496501.CrossRefGoogle ScholarPubMed
Huhtaniemi, I. and Alevizaki, M. (2006) Gonadotrophin resistance. Best Pract Res Clin Endocrinol Metab 20, 561576.CrossRefGoogle ScholarPubMed
Jacobsen, H., Schmidt, M., Hom, P., Sangild, P.T., Greve, T. and Callesen, H. (2000) Ease of calving, blood chemistry, insulin and bovine growth hormone of newborn calves derived from embryos produced in vitro in culture systems with serum and co-culture or with PVA. Theriogenology 54, 147158.CrossRefGoogle ScholarPubMed
Jansen, R.P. and De Boer, K. (1998) The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Molecular and Cellular Endocrinology 145, 8188.CrossRefGoogle ScholarPubMed
Kang, J.T., Kwon, D.K., Park, S.J., Kim, S.J., Moon, J.H., Koo, O.J., Jang, G. and Lee, B.C. (2013) Quercetin improves the in vitro development of porcine oocytes by decreasing reactive oxygen species levels. Journal of Veterinary Science 14, 1520.CrossRefGoogle ScholarPubMed
Khoueiry, R., Ibala-Rhomdane, S., Méry, L., Blachère, T., Guérin, J.F., Lornage, J. and Lefèvre, A. (2008) Dynamic CpG methylation of the KCNQ1OT1 gene during maturation of human oocytes. Journal of Medical Genetics 45, 583588.CrossRefGoogle ScholarPubMed
Kim, M.K., Park, E.A., Kim, H.J., Choi, W.Y., Cho, J.H., Lee, W.S., Cha, K.Y., Kim, Y.S., Lee, D.R. and Yoon, T.K. (2013) Does supplementation of in-vitro culture medium with melatonin improve IVF outcome in PCOS? Reprod Biomed Online 26, 2229.CrossRefGoogle ScholarPubMed
Krisher, R.L. (2022) Present state and future outlook for the application of in vitro oocyte maturation in human infertility treatment. Biology of Reproduction 106, 235242.CrossRefGoogle ScholarPubMed
Kuhtz, J., Romero, S., De Vos, M., Smitz, J., Haaf, T. and Anckaert, E. (2014) Human in vitro oocyte maturation is not associated with increased imprinting error rates at LIT1, SNRPN, PEG3 and GTL2. Human Reproduction 29, 19952005.CrossRefGoogle Scholar
Li, J., Chen, J., Sun, T., Zhang, S., Jiao, T., Chian, R.C., Li, Y. and Xu, Y. (2021) Chromosome aneuploidy analysis in embryos derived from in vivo and in vitro matured human oocytes. Journal of Translational Medicine 19, 416.CrossRefGoogle ScholarPubMed
Li, Y., Jin, L., Tian, W., Yan, E., Li, Y., Ren, X. and Guo, N. (2024) The ploidy of blastocysts from in-vitro-matured metaphase I oocytes. Reproductive BioMedicine Online 48, 103571.CrossRefGoogle Scholar
Le, F., Lou, H.Y., Wang, Q.J., Wang, N., Wang, L.Y., Li, L.J., Yang, X.Y., Zhan, Q.T., Lou, Y.Y. and Jin, F. (2019) Increased hepatic INSIG-SCAP-SREBP expression is associated with cholesterol metabolism disorder in assisted reproductive technology-conceived aged mice. Reproductive Toxicology 84, 917.CrossRefGoogle ScholarPubMed
Lill, R. and Freibert, S.A. (2020) Mechanisms of mitochondrial iron-sulfur protein biogenesis. Annual Review of Biochemistry 89, 471499.CrossRefGoogle ScholarPubMed
Liu, M.J., Sun, A.G., Zhao, S.G., Liu, H., Ma, S.Y., Li, M., Huai, Y.X., Zhao, H. and Liu, H.B. (2018) Resveratrol improves in vitro maturation of oocytes in aged mice and humans. Fertility and sterility 109, 900907.CrossRefGoogle ScholarPubMed
Liu, S., Li, Y., Gao, X., Yan, J.H. and Chen, Z.J. (2010) Changes in the distribution of mitochondria before and after in vitro maturation of human oocytes and the effect of in vitro maturation on mitochondria distribution. Fertility and sterility 93, 15501555.CrossRefGoogle ScholarPubMed
Ma, L., Cai, L., Hu, M., Wang, J., Xie, J., Xing, Y., Shen, J., Cui, Y., Liu, X.J. and Liu, J. (2020) Coenzyme Q10 supplementation of human oocyte in vitro maturation reduces postmeiotic aneuploidies. Fertility and sterility 114, 331337.CrossRefGoogle ScholarPubMed
Market-Velker, B.A., Zhang, L., Magri, L.S., Bonvissuto, A.C. and Mann, M.R.W. (2010) Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Human Molecular Genetics 19, 3651.CrossRefGoogle ScholarPubMed
May-Panloup, P., Chrétien, M.F., Jacques, C., Vasseur, C., Malthièry, Y. and Reynier, P. (2005) Low oocyte mitochondrial DNA content in ovarian insufficiency. Human Reproduction 20, 593597.CrossRefGoogle ScholarPubMed
Menkin, M.F. and Rock, J. (1948) In vitro fertilization and cleavage of human ovarian eggs. American Journal of Obstetrics and Gynecology 55, 440452.CrossRefGoogle ScholarPubMed
Mikkelsen, A.L., Smith, S.D. and Lindenberg, S. (1999) In-vitro maturation of human oocytes from regularly menstruating women may be successful without follicle stimulating hormone priming. Human Reproduction 14, 18471851.CrossRefGoogle ScholarPubMed
Mostinckx, L., Segers, I., Belva, F., Buyl, R., Santos-Ribeiro, S., Blockeel, C., Smitz, J., Anckaert, E., Tournaye, H. and De Vos, M.0020(2019) Obstetric and neonatal outcome of ART in patients with polycystic ovary syndrome: IVM of oocytes versus controlled ovarian stimulation. Human Reproduction 34, 15951607.CrossRefGoogle ScholarPubMed
Mostinckx, L., Goyens, E., Mackens, S., Roelens, C., Boudry, L., Uvin, V., Segers, I., Schoemans, C., Drakopoulos, P., Blockeel, C. and De Vos, M. (2024) Clinical outcomes from ART in predicted hyperresponders: in vitro maturation of oocytes versus conventional ovarian stimulation for IVF/ICSI. Human Reproduction 39, 586594.CrossRefGoogle ScholarPubMed
Ortega-Hrepich, C., Drakopoulos, P., Bourgain, C., Van Vaerenbergh, I., Guzman, L., Tournaye, H., Smitz, J. and De Vos, M. (2019) Aberrant endometrial steroid receptor expression in in-vitro maturation cycles despite hormonal luteal support: A pilot study. Reprod Biol 19, 210217.CrossRefGoogle ScholarPubMed
Pincus, G. and Enzmann, E.V. (1935) The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs. The Journal of Experimental Medicine 62, 665675.CrossRefGoogle ScholarPubMed
Pinyopummintr, T. and Bavister, B.D. (1995) Optimum gas atmosphere for in vitro maturation and in vitro fertilization of bovine oocytes. Theriogenology 44, 471477.CrossRefGoogle ScholarPubMed
Pliushch, G., Schneider, E., Schneider, T., El Hajj, N., Rösner, S., Strowitzki, T. and Haaf, T. (2015) In vitro maturation of oocytes is not associated with altered deoxyribonucleic acid methylation patterns in children from in vitro fertilization or intracytoplasmic sperm injection. Fertility and sterility 103, 720727.e1.CrossRefGoogle ScholarPubMed
Practice Committees of the American Society for Reproductive Medicine, the Society of Reproductive Biologists and Technologists, and the Society for Assisted Reproductive Technology. (2021) Electronic address: . In vitro maturation: a committee opinion. Fertility and sterility 115, 298304.Google Scholar
Reynier, P., May-Panloup, P., Chrétien, M.F., Morgan, C.J., Jean, M., Savagner, F., Barrière, P. and Malthièry, Y. (2001) Mitochondrial DNA content affects the fertilizability of human oocytes. Molecular Human Reproduction 7, 425429.CrossRefGoogle ScholarPubMed
Richani, D. and Gilchrist, R.B. (2022) Approaches to oocyte meiotic arrest in vitro and impact on oocyte developmental competence. Biology of Reproduction 106, 243252.CrossRefGoogle ScholarPubMed
Rock, J. and Menkin, M.F. (1944) In vitro fertilization and cleavage of human ovarian eggs. Science 100, 105107.CrossRefGoogle ScholarPubMed
Rossi, A., Pizzo, P. and Filadi, R. (2019) Calcium, mitochondria and cell metabolism: A functional triangle in bioenergetics. Biochimica et Biophysica Acta, Molecular Cell Research 1866, 10681078.CrossRefGoogle ScholarPubMed
, N.A.R., Vieira, L.A., Ferreira, A.C.A., Cadenas, J., Bruno, J.B., Maside, C., Sousa, F.G.C., Cibin, F.W.S., Alves, B.G., Rodrigues, A.P.R. and Leal-Cardoso, J.H. (2019) Anethole supplementation during oocyte maturation improves in vitro production of bovine embryos. Reproductive Sciences. doi: 10.1177/1933719119831783.CrossRefGoogle ScholarPubMed
Saenz-de-Juano, M.D., Ivanova, E., Romero, S., Lolicato, F., Sánchez, F., Van Ranst, H., Krueger, F., Segonds-Pichon, A., De Vos, M., Andrews, S. and Smitz, J. (2019) DNA methylation and mRNA expression of imprinted genes in blastocysts derived from an improved in vitro maturation method for oocytes from small antral follicles in polycystic ovary syndrome patients. Human Reproduction 34, 16401649.CrossRefGoogle ScholarPubMed
Sánchez, F., Romero, S., De Vos, M., Verheyen, G. and Smitz, J. (2015) Human cumulus-enclosed germinal vesicle oocytes from early antral follicles reveal heterogeneous cellular and molecular features associated with in vitro maturation capacity. Human Reproduction 30, 13961409.CrossRefGoogle ScholarPubMed
Sangild, P.T., Schmidt, M., Jacobsen, H., Fowden, A.L., Forhead, A., Avery, B. and Greve, T. (2000) Blood chemistry, nutrient metabolism, and organ weights in fetal and newborn calves derived from in vitro-produced bovine embryos. Biology of Reproduction 62, 14951504.CrossRefGoogle ScholarPubMed
Silva, A.A.A., Silva, M.N.P., Figueiredo, L.B.F., Gonçalves, J.D., Silva, M.J.S., Loiola, M.L.G., Bastos, B.D.M., Oliveira, R.A., Ribeiro, L.G.M., Barberino, R.S. and Gouveia, B.B. (2018) Quercetin influences in vitro maturation, apoptosis and metabolically active mitochondria of goat oocytes. Zygote 26, 465470.CrossRefGoogle ScholarPubMed
Söderström-Anttila, V., Mäkinen, S., Tuuri, T. and Suikkari, A.M. (2005) Favourable pregnancy results with insemination of in vitro matured oocytes from unstimulated patients. Human Reproduction 20, 15341540.CrossRefGoogle ScholarPubMed
Söderström-Anttila, V., Salokorpi, T., Pihlaja, M., Serenius-Sirve, S. and Suikkari, A.M. (2006) Obstetric and perinatal outcome and preliminary results of development of children born after in vitro maturation of oocytes. Human Reproduction 21, 15081513.CrossRefGoogle ScholarPubMed
Son, W.Y., Chung, J.T., Chian, R.C., Herrero, B., Demirtas, E., Elizur, S., Gidoni, Y., Sylvestre, C., Dean, N. and Tan, S.L. (2008) A 38 h interval between hCG priming and oocyte retrieval increases in vivo and in vitro oocyte maturation rate in programmed IVM cycles. Human Reproduction 23, 20102016.CrossRefGoogle ScholarPubMed
Spinelli, J.B., Haigis, M.C. (2018) The multifaceted contributions of mitochondria to cellular metabolism. Nature Cell Biology 20, 745754.CrossRefGoogle ScholarPubMed
Strowitzki, T., Bruckner, T. and Roesner, S. (2021) Maternal and neonatal outcome and children’s development after medically assisted reproduction with in-vitro matured oocytes-a systematic review and meta-analysis. Human Reproduction Update 27, 460473.CrossRefGoogle ScholarPubMed
Takahashi, Y., Hashimoto, S., Yamochi, T., Goto, H., Yamanaka, M., Amo, A., Matsumoto, H., Inoue, M., Ito, K., Nakaoka, Y. and Suzuki, N. (2016) Dynamic changes in mitochondrial distribution in human oocytes during meiotic maturation. Journal of Assisted Reproduction and Genetics 33, 929938.CrossRefGoogle ScholarPubMed
Talbert, L.M., Raj, M.H., Hammond, M.G. and Greer, T. (1984) Endocrine and immunologic studies in a patient with resistant ovary syndrome. Fertility and sterility 42, 741744.CrossRefGoogle Scholar
Tao, X., Landis, J.N., Krisher, R.L., Duncan, F.E., Silva, E., Lonczak, A., Scott, R.T., Zhan, Y., Chu, T., Scott, R.T. and Treff, N.R. (2017) Mitochondrial DNA content is associated with ploidy status, maternal age, and oocyte maturation methods in mouse blastocysts. Journal of Assisted Reproduction and Genetics 34, 15871594.CrossRefGoogle ScholarPubMed
Thompson, J. and Gilchrist, R. Improving oocyte maturation in vitro. 2013; Cambridge University Press Available from: https://digital.library.adelaide.edu.au/dspace/handle/2440/81932.CrossRefGoogle Scholar
Trebichalská, Z., Kyjovská, D., Kloudová, S., Otevřel, P., Hampl, A. and Holubcová, Z. (2021) Cytoplasmic maturation in human oocytes: an ultrastructural study †. Biology of Reproduction 104, 106116.CrossRefGoogle ScholarPubMed
Walls, M.L., Hunter, T., Ryan, J.P., Keelan, J.A., Nathan, E. and Hart, R.J. (2015) In vitro maturation as an alternative to standard in vitro fertilization for patients diagnosed with polycystic ovaries: a comparative analysis of fresh, frozen and cumulative cycle outcomes. Human Reproduction 30, 8896.CrossRefGoogle ScholarPubMed
Van Wagtendonk-de Leeuw, A.M., Mullaart, E., De Roos, A.P., Merton, J.S., den Daas, J.H., Kemp, B. and De Ruigh, L. (2000) Effects of different reproduction techniques: AI MOET or IVP, on health and welfare of bovine offspring. Theriogenology 53, 575597.CrossRefGoogle ScholarPubMed
Whitty, A., Kind, K.L., Dunning, K.R. and Thompson, J.G. (2021) Effect of oxygen and glucose availability during in vitro maturation of bovine oocytes on development and gene expression. Journal of Assisted Reproduction and Genetics 38, 13491362.CrossRefGoogle ScholarPubMed
Vuong, L.N., Ho, V.N.A., Ho, T.M., Dang, V.Q., Phung, T.H., Giang, N.H., Le, A.H., Pham, T.D., Wang, R., Smitz, J. and Gilchrist, R.B. (2020) In-vitro maturation of oocytes versus conventional IVF in women with infertility and a high antral follicle count: a randomized non-inferiority controlled trial. Human Reproduction 35, 25372547.CrossRefGoogle Scholar
Vuong, L.N., Nguyen, L.K., Le, A.H., Pham, H.H., Ho, V.N., Le, H.L., Pham, T.D., Dang, V.Q., Phung, T.H., Smitz, J. and Ho, T.M. (2021) Fresh embryo transfer versus freeze-only after in vitro maturation with a pre-maturation step in women with high antral follicle count: a randomized controlled pilot study. Journal of Assisted Reproduction and Genetics 38, 12931302.CrossRefGoogle Scholar
Vuong, L.N., Nguyen, M.H.N., Nguyen, N.A., Ly, T.T., Tran, V.T.T., Nguyen, N.T., Hoang, H.L.T., Le, X.T.H., Pham, T.D., Smitz, J.E.J. and Mol, B.W. (2022) Development of children born from IVM versus IVF: 2-year follow-up of a randomized controlled trial. Human Reproduction 37, 18711879.CrossRefGoogle ScholarPubMed
Vuong, L.N., Pham, T.D., Ho, T.M. and De Vos, M. (2023). Outcomes of clinical in vitro maturation programs for treating infertility in hyper responders:a systematic review. Fertility and Sterility 119, 540549.CrossRefGoogle ScholarPubMed
Yang, S.H., Patrizio, P., Yoon, S.H., Lim, J.H. and Chian, R.C. (2012) Comparison of pregnancy outcomes in natural cycle IVF/M treatment with or without mature oocytes retrieved at time of egg collection. Systems Biology in Reproductive Medicine 58, 154159.CrossRefGoogle ScholarPubMed
Zhao, H., Li, T., Zhao, Y., Tan, T., Liu, C., Liu, Y., Chang, L., Huang, N., Li, C., Fan, Y. and Yu, Y. (2019) Single-Cell Transcriptomics of Human Oocytes: Environment-Driven Metabolic Competition and Compensatory Mechanisms During Oocyte Maturation. Antioxidants & Redox Signaling 30, 542559.CrossRefGoogle ScholarPubMed
Zou, H., Chen, B., Ding, D., Gao, M., Chen, D., Liu, Y., Hao, Y., Zou, W., Ji, D., Zhou, P. and Wei, Z. (2020) Melatonin promotes the development of immature oocytes from the COH cycle into healthy offspring by protecting mitochondrial function. Journal of Pineal Research 68, e12621.CrossRefGoogle ScholarPubMed