Top

Journal of Assisted Reproduction and Genetics

Published in:

Open Access 16-02-2024 | Progesterone | Gamete Biology

Mature oocyte dysmorphisms may be associated with progesterone levels, mitochondrial DNA content, and vitality in luteal granulosa cells

Authors: Georges Raad, Judy Tanios, Munevver Serdarogullari, Marwa Bazzi, Youmna Mourad, Joseph Azoury, Zalihe Yarkiner, Georgios Liperis, Fadi Fakih, Chadi Fakih

Published in: Journal of Assisted Reproduction and Genetics | Issue 3/2024

Abstract

Purpose

To identify whether follicular environment parameters are associated with mature oocyte quality, embryological and clinical outcomes.

Methods

This retrospective study examined 303 mature oocytes from 51 infertile women undergoing ICSI cycles between May 2018 and June 2021. Exclusion criteria consisted of advanced maternal age (> 36 years old), premature ovarian failure, obesity in women, or use of frozen gametes. Luteal granulosa cells (LGCs) were analyzed for mitochondrial DNA/genomic (g) DNA ratio and vitality. The relationships between hormone levels in the follicular fluid and oocyte features were assessed. Quantitative morphometric measurements of mature oocytes were assessed, and the association of LGC parameters and oocyte features on live birth rate after single embryo transfer was examined.

Results

Results indicated an inverse correlation between the mtDNA/gDNA ratio of LGCs and the size of polar body I (PBI). A 4.0% decrease in PBI size was observed with each one-unit increase in the ratio (p = 0.04). Furthermore, a 1% increase in LGC vitality was linked to a 1.3% decrease in fragmented PBI (p = 0.03), and a 1 ng/mL increase in progesterone levels was associated with a 0.1% rise in oocytes with small inclusions (p = 0.015). Associations were drawn among LGC characteristics, perivitelline space (PVS) debris, cytoplasmic inclusions, PBI integrity, and progesterone levels. Certain dysmorphisms in mature oocytes were associated with embryo morphokinetics; however, live birth rates were not associated with follicular parameters and oocyte quality characteristics.

Conclusion

Follicular markers may be associated with mature oocyte quality features.

Available only for authorised users

Wyns C, Bergh C, Calhaz-Jorge C, De Geyter C, Kupka MS, Motrenko T, et al. ART in Europe, 2016: results generated from European registries by ESHRE†. Hum Reprod Open. 2020;2020:hoaa032. https://doi.org/10.1093/hropen/hoaa032

Zagadailov P, Hsu A, Seifer DB, Stern JE. Differences in utilization of Intracytoplasmic sperm injection (ICSI) within human services (HHS) regions and metropolitan megaregions in the U.S. Reprod Biol Endocrinol. 2017;15:45. https://doi.org/10.1186/s12958-017-0263-4

Setti AS, Figueira RCS, Braga DPAF, Colturato SS, Iaconelli A, Borges E. Relationship between oocyte abnormal morphology and intracytoplasmic sperm injection outcomes: a meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2011;159:364–70.CrossRefPubMed

Bartolacci A, Intra G, Coticchio G, dell’Aquila M, Patria G, Borini A. Does morphological assessment predict oocyte developmental competence? A systematic review and proposed score. J Assist Reprod Genet. 2022;39:3–17. https://doi.org/10.1007/s10815-021-02370-3.CrossRefPubMedPubMedCentral

Nikiforov D, Grøndahl ML, Hreinsson J, Andersen CY. Human oocyte morphology and outcomes of infertility treatment: a systematic review. Reprod Sci. 2022;29:2768–85. https://doi.org/10.1007/s43032-021-00723-y.CrossRefPubMed

Magli MC, Jones GM, Lundin K, van den Abbeel E. Atlas of human embryology: from oocytes to preimplantation embryos. Preface Hum Reprod. 2012;27(Suppl):1.

Uyar A, Torrealday S, Seli E. Cumulus and granulosa cell markers of oocyte and embryo quality. Fertil Steril Am Soc Reproductive Med. 2013;99:979–97. https://doi.org/10.1016/j.fertnstert.2013.01.129.CrossRef

Dompe C, Kulus M, Stefańska K, Kranc W, Chermuła B, Bryl R, et al. Human granulosa cells—stemness properties, molecular cross-talk and follicular angiogenesis. Cells. 2021;10.

Sutton-McDowall ML, Gilchrist RB, Thompson JG. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction. 2010;139:685–95.CrossRefPubMed

10.

Sutton-McDowall ML, Mottershead DG, Gardner DK, Gilchrist RB, Thompson JG. Metabolic differences in bovine cumulus-oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 151. Biol Reprod. 2012;87(1–8):87. https://doi.org/10.1095/biolreprod.112.102061.CrossRefPubMed

11.

Turathum B, Gao EM, Chian RC. The function of cumulus cells in oocyte growth and maturation and in subsequent ovulation and fertilization. Cells. 2021;10:1–18.CrossRef

12.

Richani D, Gilchrist RB. The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update. 2018;24:1–14. https://doi.org/10.1093/humupd/dmx029.CrossRefPubMed

13.

Tesarik JAN, Biology R, Hospital A, Mbdicale R, Biology M, Faculty G. Oocytes : relationship to oocyte developmental. J Clin Endocrinol Metab. 1995;03:1438–43.

14.

Tesarik J, Mendoza C. Direct non-genomic effects of follicular steroids on maturing human oocytes: oestrogen versus androgen antagonism. Hum Reprod Update. 1997;3:95–100. https://doi.org/10.1093/humupd/3.2.95.CrossRefPubMed

15.

Hasegawa J, Yanaihara A, Iwasaki S, Otsuka Y, Negishi M, Akahane T, et al. Reduction of progesterone receptor expression in human cumulus cells at the time of oocyte collection during IVF is associated with good embryo quality. Hum Reprod. 2005;20:2194–200. https://doi.org/10.1093/humrep/dei005.CrossRefPubMed

16.

Hu J, Zhang Z, Shen W-J, Azhar S. Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones. Nutr Metab (Lond). 2010;7:47. https://doi.org/10.1186/1743-7075-7-47.CrossRefPubMed

17.

Dai Q, Likes CE III, Luz AL, Mao L, Yeh JS, Wei Z, et al. A mitochondrial progesterone receptor increases cardiac beta-oxidation and remodeling. J Endocr Soc. 2019;3:446–67. https://doi.org/10.1210/js.2018-00219.CrossRefPubMedPubMedCentral

18.

Behera MA, Dai Q, Garde R, Saner C, Jungheim E, Price TM. Progesterone stimulates mitochondrial activity with subsequent inhibition of apoptosis in MCF-10A benign breast epithelial cells. Am J Physiol Metab. Am Physiol Soc. 2009;297:E1089-96. https://doi.org/10.1152/ajpendo.00209.2009.CrossRef

19.

Klinge CM. Estrogenic control of mitochondrial function. Redox Biol . Elsevier B.V.; 2020;31:101435. https://doi.org/10.1016/j.redox.2020.101435

20.

Yager JD, Chen JQ. Mitochondrial estrogen receptors - new insights into specific functions. Trends Endocrinol Metab . Elsevier; 2007;18:89–91. https://doi.org/10.1016/j.tem.2007.02.006

21.

Liu Y, Han M, Li X, Wang H, Ma M, Zhang S, et al. Age-related changes in the mitochondria of human mural granulosa cells. Hum Reprod. 2017;32:2465–73.CrossRefPubMed

22.

Zhang Q, Ren J, Wang F, Pan M, Cui L, Li M, et al. Mitochondrial and glucose metabolic dysfunctions in granulosa cells induce impaired oocytes of polycystic ovary syndrome through Sirtuin 3. Free Radic Biol Med Pergamon. 2022;187:1–16.CrossRef

23.

Bhargava D, Urs S, Wu W, Komrskova K, Postlerova P, Lin Y, et al. Mitochondrial function in modulating human granulosa cell steroidogenesis and female fertility. Int J Mol Sci. 2020;

24.

Lamas-toranzo I, Gonz L, Alvarez PB-, Gonz P. The human cumulus cell transcriptome provides poor predictive value for embryo transfer outcome. Reprod Biomed Online. 2023;46:783–91.CrossRefPubMed

25.

Mantovani C, Luz D, Gomes M, Broi D, Koopman LDO, Plaça JR, et al. Transcriptomic analysis of cumulus cells shows altered pathways in patients with minimal and mild endometriosis. Sci Rep . Nature Publishing Group UK; 2022;1–9. https://doi.org/10.1038/s41598-022-09386-4

26.

Meseguer M, Rubio I, Cruz M, Basile N, Marcos J, Requena A. Embryo incubation and selection in a time-lapse monitoring system improves pregnancy outcome compared with a standard incubator: a retrospective cohort study. Fertil Steril Elsevier. 2012;98:1481-1489.e10.CrossRef

27.

Bamford T, Barrie A, Montgomery S, Dhillon-Smith R, Campbell A, Easter C, et al. Morphological and morphokinetic associations with aneuploidy: a systematic review and meta-analysis. Hum Reprod Update. 2022;28:656–86. https://doi.org/10.1093/humupd/dmac022.CrossRefPubMed

28.

Meng Q, Xu Y, Zheng A, Li H, Ph D, Ding J. Noninvasive embryo evaluation and selection by time-lapse monitoring vs. conventional morphologic assessment in women undergoing in vitro fertilization / intracytoplasmic sperm injection : a single-center randomized controlled study. Fertil Steril. Am Soc Reproductive Med. 2023;117:1203–12. https://doi.org/10.1016/j.fertnstert.2022.02.015.CrossRef

29.

Xin B, Hang M, Lei Z, Bo J. Neonatal outcomes of embryos cultured in a time ‑ lapse incubation system : an analysis of more than 15 , 000 fresh transfer cycles. Reprod Sci . Springer International Publishing; 2021;1–7. https://doi.org/10.1007/s43032-021-00714-z

30.

Tabibnejad N, Sheikhha MH, Ghasemi N, Fesahat F, Soleimani M, Aflatoonian A. Association between early embryo morphokinetics plus cumulus cell gene expression and assisted reproduction outcomes in polycystic ovary syndrome women. Reprod Biomed Online . Elsevier Ltd; 2019;38:139–51. https://doi.org/10.1016/j.rbmo.2018.10.010

31.

Raad G, Tanios J, Kerbaj S, Mourad Y, Fakih F, Shamas F, et al. Stress management during the intracytoplasmic sperm injection cycle may slow down first embryo cleavage and accelerate embryo compaction: a pilot randomized controlled trial. Psychother Psychosom. 2021;90:119–26.CrossRefPubMed

32.

Bakos HW, Henshaw RC, Mitchell M, Lane M. Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology. Fertil Steril . Elsevier Ltd; 2011;95:1700–4. https://doi.org/10.1016/j.fertnstert.2010.11.044

33.

Bellver J, Mifsud A, Grau N, Privitera L, Meseguer M. Similar morphokinetic patterns in embryos derived from obese and normoweight infertile women: a time-lapse study. Hum Reprod. 2013;28:794–800.CrossRefPubMed

34.

Feil D, Henshaw RC, Lane M. Day 4 embryo selection is equal to Day 5 using a new embryo scoring system validated in single embryo transfers. Hum Reprod. 2008;23:1505–10. https://doi.org/10.1093/humrep/dem419.CrossRefPubMed

35.

Yu L, Liu M, Wang Z, Liu T, Liu S, Wang B, et al. Correlation between steroid levels in follicular fluid and hormone synthesis related substances in its exosomes and embryo quality in patients with polycystic ovary syndrome. Reprod Biol Endocrinol. 2021;19:74. https://doi.org/10.1186/s12958-021-00749-6.CrossRefPubMedPubMedCentral

36.

Floehr J, Dietzel E, Neulen J, Rösing B, Weissenborn U, Jahnen-Dechent W. Association of high fetuin-B concentrations in serum with fertilization rate in IVF: a cross-sectional pilot study. Hum Reprod. 2016;31:630–7. https://doi.org/10.1093/humrep/dev340.CrossRefPubMed

37.

Qu F, Wang F-F, Lu X-E, Dong M-Y, Sheng J-Z, Lv P-P, et al. Altered aquaporin expression in women with polycystic ovary syndrome: hyperandrogenism in follicular fluid inhibits aquaporin-9 in granulosa cells through the phosphatidylinositol 3-kinase pathway. Hum Reprod. 2010;25:1441–50. https://doi.org/10.1093/humrep/deq078.CrossRefPubMed

38.

Scalici E, Traver S, Molinari N, Mullet T, Monforte M, Vintejoux E, et al. Cell-free DNA in human follicular fluid as a biomarker of embryo quality. Hum Reprod. 2014;29:2661–9.CrossRefPubMed

39.

Raad G, Bazzi M, Tanios J, Mourad Y, Azouri J, Azouri J, et al. Optimization of the cell aggregates method for isolation and purification of human granulosa cells from follicular fluid. Int J Fertil Steril. 2020;13:339–45.PubMed

40.

Wells D, Kaur K, Grifo J, Glassner M, Taylor JC, Fragouli E, et al. Clinical utilisation of a rapid low-pass whole genome sequencing technique for the diagnosis of aneuploidy in human embryos prior to implantation. J Med Genet. 2014;51:553–62.CrossRefPubMed

41.

Fragouli E, Spath K, Alfarawati S, Kaper F, Craig A, Michel CE, et al. Altered levels of mitochondrial DNA are associated with female age, aneuploidy, and provide an independent measure of embryonic implantation potential. PLoS Genet. 2015;11:1–18.CrossRef

42.

Shenoy CC, Khan Z, Coddington CC, Stewart EA, Morbeck DE. Symmetry at the 4-cell stage is associated with embryo aneuploidy. Reprod Sci . Springer International Publishing; 2021;28:3473–9. https://doi.org/10.1007/s43032-021-00758-1

43.

Coello A, Meseguer M, Galán A, Alegre L, Remohí J, Cobo A. Analysis of the morphological dynamics of blastocysts after vitrification/warming: defining new predictive variables of implantation. Fertil Steril. 2017;108:659-666.e4.CrossRefPubMed

44.

Park JK, Ahn S-Y, Seok SH, Park SY, Bang S, Eum JH, et al. Clinical usability of embryo development using a combined qualitative and quantitative approach in a single vitrified-warmed blastocyst transfer: assessment of pre-vitrified blastocyst diameter and post-warmed blastocyst re-expansion speed. J. Clin. Med. 2022.

45.

Ebner T, Ph D, Moser M, Ph D, Sommergruber M. Occurrence and developmental consequences of vacuoles throughout preimplantation development. Fertil Steril. 2005;83.

46.

Balaban B, Brison D, Calderón G, Catt J, Conaghan J, Cowan L, et al. The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod. 2011;26:1270–83.CrossRef

47.

Lainas GT, Lainas TG, Sfontouris IA, Chatzimeletiou K, Venetis CA, Bosdou JK, et al. Is oocyte maturation rate associated with triptorelin dose used for triggering final oocyte maturation in patients at high risk for severe ovarian hyperstimulation syndrome. Hum Reprod. 2019;34:1770–7.CrossRefPubMed

48.

Apter S, Ebner T, Freour T, Guns Y, Kovacic B, Le Clef N, et al. Good practice recommendations for the use of time-lapse technology†. Hum Reprod Open. 2020;2020:hoaa008. https://doi.org/10.1093/hropen/hoaa008.CrossRefPubMedPubMedCentral

49.

Meseguer M, Herrero J, Tejera A, Hilligsøe KM, Ramsing NB, Remohı J. The use of morphokinetics as a predictor of embryo implantation. Hum Reprod. 2011;26:2658–71.CrossRefPubMed

50.

Marklund A, Eloranta S, Wikander I, Kitlinski ML, Lood M, Nedstrand E, et al. Efficacy and safety of controlled ovarian stimulation using GnRH antagonist protocols for emergency fertility preservation in young women with breast cancer - a prospective nationwide Swedish multicenter study. Hum Reprod. 2020;35:929–38.CrossRefPubMedPubMedCentral

51.

Geber S, Brandão AHF, Sampaio M. Effects of estradiol and FSH on leptin levels in women with suppressed pituitary. Reprod Biol Endocrinol. 2012;10:45. https://doi.org/10.1186/1477-7827-10-45.CrossRefPubMedPubMedCentral

52.

Linting M, Van Der Kooij A. Nonlinear principal components analysis with CATPCA: a tutorial. J Pers Assess. 2012;94:12–25.CrossRefPubMed

53.

Vidal AF, Cruz AMP, Magalhães L, Pereira AL, Anaissi AKM, Alves NCF, et al. Hsa-miR-29c and hsa-miR-135b differential expression as potential biomarker of gastric carcinogenesis. World J Gastroenterol. 2016;22:2060–70.CrossRefPubMedPubMedCentral

54.

PENG X-R, HSUEH AJW, LAPOLT PS, BJERSING L, NY T. Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation*. Endocrinology . 1991;129:3200–7. https://doi.org/10.1210/endo-129-6-3200

55.

Jamnongjit Stephen R MH. Oocyte maturation: the coming of age of a germ cell. Semin Reprod Med . 2005;23:234–41. Available from: http://www.thieme-connect.com/products/ejournals/abstract/https://doi.org/10.1055/s-2005-872451

56.

Swain JE, Pool TB. ART failure: oocyte contributions to unsuccessful fertilization. Hum Reprod Update. 2008;14:431–46. https://doi.org/10.1093/humupd/dmn025.CrossRefPubMed

57.

Mao L, Lou H, Lou Y, Wang N, Jin F. Behaviour of cytoplasmic organelles and cytoskeleton during oocyte maturation. Reprod Biomed Online . Reproductive Healthcare Ltd.; 2014;28:284–99. https://doi.org/10.1016/j.rbmo.2013.10.016

58.

Reader KL, Stanton JAL, Juengel JL. The role of oocyte organelles in determining developmental competence. Biology (Basel). 2017;6:1–22.

59.

Coticchio G, Dal Canto M, Mignini Renzini M, Guglielmo MC, Brambillasca F, Turchi D, et al. Oocyte maturation: gamete-somatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum Reprod Update. 2015;21:427–54. https://doi.org/10.1093/humupd/dmv011.CrossRefPubMed

60.

Sousa M, Cunha M, Silva J, Oliveira E, Pinho MJ, Almeida C, et al. Ultrastructural and cytogenetic analyses of mature human oocyte dysmorphisms with respect to clinical outcomes. J Assist Reprod Genet. J Ass Reproduction Gen. 2016;33:1041–57. https://doi.org/10.1007/s10815-016-0739-8.CrossRef

61.

Kahraman S, Yakın K, Dönmez E, Şamlı H, Bahçe M, Cengiz G, et al. Relationship between granular cytoplasm of oocytes and pregnancy outcome following intracytoplasmic sperm injection. Hum Reprod. 2000;15:2390–3. https://doi.org/10.1093/humrep/15.11.2390.CrossRefPubMed

62.

Ebner T. Extracytoplasmic markers of human oocyte quality. J Mamm Ova Res. 2009;26:18–25.CrossRef

63.

Miao YL, Kikuchi K, Sun QY, Schatten H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update. 2009;15:573–85.CrossRefPubMed

64.

Huang Z, Wells D. The human oocyte and cumulus cells relationship : new insights from the cumulus cell transcriptome. 2010;16:715–25.

65.

Revelli A, Piane LD, Casano S, Molinari E, Massobrio M, Rinaudo P. Follicular fluid content and oocyte quality : from single biochemical markers to metabolomics. Reprod Biol Endocrinol. 2009;13:1–13.

66.

Eppig JJ. Reproduction: oocytes call, granulosa cells connect. Curr Biol . Elsevier Ltd; 2018;28:R354–6. https://doi.org/10.1016/j.cub.2018.03.005

67.

Jaffe LA, Egbert JR. Regulation of mammalian oocyte meiosis by intercellular communication within the ovarian follicle. Rev Adv. 2017;1–24.

68.

Tatone C, Ph D, Amicarelli F, Ph D. The aging ovary — the poor granulosa cells. Fertil Steril . Elsevier Inc.; 2013;99:12–7. https://doi.org/10.1016/j.fertnstert.2012.11.029

69.

Adhikari D, Lee I, Yuen WS, Carroll J. Oocyte mitochondria — key regulators of oocyte function and potential therapeutic targets for improving fertility. Biol Reprod. 2022;106:366–77.CrossRefPubMed

70.

Richani D, Dunning KR, Thompson JG, Gilchrist RB. Metabolic co-dependence of the oocyte and cumulus cells: essential role in determining oocyte developmental competence. Hum Reprod Update. 2021;27:27–47.CrossRefPubMed

71.

Chien Y, Rosal K, Chung BC. Function of CYP11A1 in the mitochondria. Mol Cell Endocrinol. 2017;441:55–61. https://doi.org/10.1016/j.mce.2016.10.030.CrossRefPubMed

72.

Kauppila TES, Kauppila ohanna HK, Larsson N-G. Review mammalian mitochondria and aging : an update. Cell Metab 2017;25:1–15

73.

Mao J, Zhang J, Cai L, Cui Y, Liu J, Mao Y. Elevated prohibitin 1 expression mitigates glucose metabolism defects in granulosa cells of infertile patients with endometriosis. Mol Hum Reprod. 2022;28:gaac018. https://doi.org/10.1093/molehr/gaac018.CrossRefPubMed

74.

Li D, Wang X, Li G, Dang Y, Zhao S, Qin Y. LncRNA ZNF674-AS1 regulates granulosa cell glycolysis and proliferation by interacting with ALDOA. Cell Death Discov. 2021;7(1):107. https://doi.org/10.1038/s41420-021-00493-1.CrossRefPubMedPubMedCentral

75.

Wang J, Wu J, Zhang Y, Zhang J, Xu W, Wu C, Zhou P. Growth hormone protects against ovarian granulosa cell apoptosis: Alleviation oxidative stress and enhancement mitochondrial function. Reprod Biol. 2021;21(2):100504. https://doi.org/10.1016/j.repbio.2021.100504

76.

Gu L, Liu H, Gu X, Boots C, Moley KH, Wang Q. Metabolic control of oocyte development: linking maternal nutrition and reproductive outcomes. Cellular and molecular life sciences : CMLS. 2015;72(2):251–71. https://doi.org/10.1007/s00018-014-1739-4.CrossRefPubMed

77.

Kirillova A, Smitz JEJ, Sukhikh GT, Mazunin I. The role of mitochondria in oocyte maturation. Cells. 2021;10:1–17.CrossRef

78.

Liu S, Li Y, Gao X, Yan JH, Chen ZJ. 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. Fertil Steril. 2010;93(5):1550–5. https://doi.org/10.1016/j.fertnstert.2009.03.050.CrossRefPubMed

79.

Babayev E, Seli E. Oocyte mitochondrial function and reproduction. Curr Opin Gynecol Obstet. 2015;27(3):175–81. https://doi.org/10.1097/GCO.0000000000000164.

80.

Rose BI, Laky D. Polar body fragmentation in IVM oocytes is associated with impaired fertilization and embryo development. J Assist Reprod Genet. 2013;30:679–82. https://doi.org/10.1007/s10815-013-9982-4.CrossRefPubMedPubMedCentral

81.

Wu FJ, Wang YW, Luo CW. Human bone morphogenetic protein 8A promotes expansion and prevents apoptosis of cumulus cells in vitro. Mol Cell Endocrinol. 2021;522:111121. https://doi.org/10.1016/j.mce.2020.111121

82.

Lu X, Liu Y, Xu J, Cao X, Zhang D, Liu M, Liu S, Dong X, Shi H. Mitochondrial dysfunction in cumulus cells is related to decreased reproductive capacity in advanced-age women. Fertil Steril. 2022;118(2):393–404. https://doi.org/10.1016/j.fertnstert.2022.04.019.CrossRefPubMed

83.

Ferrero H, Delgado-Rosas F, Garcia-Pascual CM, Monterde M, Zimmermann RC, Simón C, Pellicer A, Gómez R. Efficiency and purity provided by the existing methods for the isolation of luteinized granulosa cells: a comparative study. Hum Reprod (Oxford, England). 2012;27(6):1781–9. https://doi.org/10.1093/humrep/des096.CrossRef

84.

Nagy B, Poto L, Farkas N, Koppan M, Varnagy A, Kovacs K, Papp S, Bohonyi N, Bodis J. Follicular fluid progesterone concentration is associated with fertilization outcome after IVF: a systematic review and meta-analysis. Reprod Biomed Online. 2019;38(6):871–82. https://doi.org/10.1016/j.rbmo.2018.12.045.CrossRefPubMed

85.

Sun Z, Song J, Zhang X, Wang A, Guo Y, Yang Y, Wang X, Xu K, Deng J. SWATHHM-Based Metabolomics of Follicular Fluid in Patients Shows That Progesterone Adversely Affects Oocyte Quality. Biomed Res Int. 2018;2018:1780391. https://doi.org/10.1155/2018/1780391.CrossRefPubMedPubMedCentral

86.

Sousa M, Cunha M, Silva J, Oliveira E, Pinho MJ, Almeida C, Sá R, da Silva JT, Oliveira C, Barros A. Ultrastructural and cytogenetic analyses of mature human oocyte dysmorphisms with respect to clinical outcomes. J Assist Reprod Genet. 2016;33(8):1041–57. https://doi.org/10.1007/s10815-016-0739-8.CrossRefPubMedPubMedCentral

87.

Armstrong S, Bhide P, Jordan V, Pacey A, Farquhar C Time-lapse systems for embryo incubation and assessment in assisted reproduction. Cochrane Database Syst Rev. 2018;5(5):CD011320. https://doi.org/10.1002/14651858.CD011320.pub3

88.

Kieslinger DC, Vergouw CG, Ramos L, Arends B, Curfs MHJM, Slappendel E, Kostelijk EH, Pieters MHEC, Consten D, Verhoeven MO, Besselink DE, Broekmans F, Cohlen BJ, Smeenk JMJ, Mastenbroek S, de Koning CH, van Kasteren YM, Moll E, van Disseldorp J, Brinkhuis EA, Lambalk CB. Clinical outcomes of uninterrupted embryo culture with or without time-lapse-based embryo selection versus interrupted standard culture (SelecTIMO): a three-armed, multicentre, double-blind, randomised controlled trial. Lancet (London, England). 2023;401(10386):1438–46. https://doi.org/10.1016/S0140-6736(23)00168-X.CrossRefPubMed

89.

Meriano JS, Alexis J, Visram-Zaver S, Cruz M, Casper RF. Tracking of oocyte dysmorphisms for ICSI patients may prove relevant to the outcome in subsequent patient cycles. Hum Reprod. 2001;16:2118–23. https://doi.org/10.1093/humrep/16.10.2118.CrossRefPubMed

90.

Merviel P, Cabry R, Chardon K, Haraux E, Scheffler F, Mansouri NB, Devaux A, Chahine H, Bach V, Copin H, Benkhalifa M. Impact of oocytes with CLCG on ICSI outcomes and their potential relation to pesticide exposure. J Ovarian Res. 2017;10(1):42. https://doi.org/10.1186/s13048-017-0335-2.CrossRefPubMedPubMedCentral

91.

Yu EJ, Ahn H, Lee JM, Jee BC, Kim SH. Fertilization and embryo quality of mature oocytes with specific morphological abnormalities. Clin Exp Reprod Med Korea (South). 2015;42:156–62.CrossRef

Title: Mature oocyte dysmorphisms may be associated with progesterone levels, mitochondrial DNA content, and vitality in luteal granulosa cells
Authors: Georges Raad
Judy Tanios
Munevver Serdarogullari
Marwa Bazzi
Youmna Mourad
Joseph Azoury
Zalihe Yarkiner
Georgios Liperis
Fadi Fakih
Chadi Fakih
Publication date: 16-02-2024
Publisher: Springer US
Keywords: Progesterone
Estradiol
Published in: Journal of Assisted Reproduction and Genetics / Issue 3/2024
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI: https://doi.org/10.1007/s10815-024-03053-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Mature oocyte dysmorphisms may be associated with progesterone levels, mitochondrial DNA content, and vitality in luteal granulosa cells

Abstract

Purpose

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 3/2024

A report of two homozygous TERB1 protein-truncating variants in two unrelated women with primary infertility

Long-term health risk of offspring born from assisted reproductive technologies

Do IVF culture conditions have an impact on neonatal outcomes? A systematic review and meta-analysis

Mosaic embryo transfer versus additional IVF with PGT-A Cycle: a decision model comparing live birth rate and cost

Maternal and neonatal outcomes of dichorionic twin pregnancies achieved with assisted reproductive technology: meta-analysis of contemporary data

Impact of mildly evaluated thyroid-stimulating hormone levels on in vitro fertilization or intracytoplasmic sperm injection outcomes in women with the first fresh embryo transfer: a large study from China