Developmental Status of Human Oocytes that Fail to Cleave After Intracytoplasmic Sperm Injection

Ali Mohsin Alwaeli; Maan Hamad Al-Khalisy; Shatha Sadiq Al-Marayaty

doi:10.54133/ajms.v9i1.2276

Authors

Ali Mohsin Alwaeli Department of Human Anatomy, College of Medicine, Mustansiriyah University, Baghdad, Iraq https://orcid.org/0000-0001-9345-6717
Maan Hamad Al-Khalisy Department of Anatomy, College of Medicine, University of Baghdad, Baghdad, Iraq
Shatha Sadiq Al-Marayaty Department of Physiology, Al-Rafidain University College, Baghdad, Iraq

DOI:

https://doi.org/10.54133/ajms.v9i1.2276

Keywords:

Chromatin, Cleavage failure, Fertilization failure, ICSI, Oocyte, Meiotic spindle

Abstract

Background: Oocyte maturity is crucial for the success of intracytoplasmic sperm injection (ICSI). However, the oocyte appearance under a light microscope is the only indicator of maturity. Examining the chromatin status of the oocytes that fail to fertilize after ICSI may enrich the knowledge about maturity and possible causes of fertilization failure. Objectives: To investigate the developmental progress of human oocytes that fail to cleave after ICSI, and the stages at which the progress has been arrested. Methods: An observational study of human oocytes from women having ICSI cycles. Oocytes that failed to cleave after ICSI were collected and immunostained to visualize the meiotic spindles and chromatin using immunofluorescence microscopy. Results: 100 failed oocytes were successfully immunostained. Oocytes showed the following developmental stages: anaphase-I (4%), telophase-I (9%), prometaphase-II (14%), metaphase-II (24%), anaphase-II (33%), one pronucleus (6%), two pronuclei (9%), and syngamy (1%). The meiotic spindle was seen in most of the prometaphase-II and metaphase-II oocytes. Sperm chromatin showed different levels of decondensation in the oocytes. Meiotic spindles were absent in MII oocytes that showed condensed sperm chromatin. At least one polar body was identifiable in all of the oocytes studied. Many apparently MII oocytes haven’t reached the MII stage at ICSI time, despite having a visible first polar body. Conclusions: The appearance of a polar body in the oocyte doesn’t guarantee that the oocyte has reached the MII stage. Oocyte cleavage may be arrested at any developmental stage from sperm injection to syngamy.

Downloads

Download data is not yet available.

References

Palermo GD, O'Neill CL, Chow S, Cheung S, Parrella A, Pereira N, et al. Intracytoplasmic sperm injection: state of the art in humans. Reproduction. 2017;154(6):F93-F110. doi: 10.1530/REP-17-0374. DOI: https://doi.org/10.1530/REP-17-0374

Esterhuizen AD, Franken DR, Becker PJ, Lourens JG, Müller II, van Rooyen LH. Defective sperm decondensation: a cause for fertilization failure. Andrologia. 2002;34(1):1-7. doi: 10.1046/j.0303-4569.2001.00423.x. DOI: https://doi.org/10.1046/j.0303-4569.2001.00423.x

Terada Y, Nakamura S, Simerly C, Hewitson L, Murakami T, Yaegashi N, et al. Centrosomal function assessment in human sperm using heterologous ICSI with rabbit eggs: a new male factor infertility assay. Mol Reprod Dev. 2004;67(3):360-365. doi: 10.1002/mrd.20024. DOI: https://doi.org/10.1002/mrd.20024

Swain JE, Pool TB. ART failure: oocyte contributions to unsuccessful fertilization. Hum Reprod Update. 2008;14(5):431-446. doi: 10.1093/humupd/dmn025. DOI: https://doi.org/10.1093/humupd/dmn025

Combelles CM, Morozumi K, Yanagimachi R, Zhu L, Fox JH, Racowsky C. Diagnosing cellular defects in an unexplained case of total fertilization failure. Hum Reprod. 2010;25(7):1666-1671. doi: 10.1093/humrep/deq064. DOI: https://doi.org/10.1093/humrep/deq064

Kashir J, Heindryckx B, Jones C, De Sutter P, Parrington J, Coward K. Oocyte activation, phospholipase C zeta and human infertility. Hum Reprod Update. 2010;16(6):690-703. doi: 10.1093/humupd/dmq018. DOI: https://doi.org/10.1093/humupd/dmq018

Yeste M, Jones C, Amdani SN, Patel S, Coward K. Oocyte activation deficiency: a role for an oocyte contribution? Hum Reprod Update. 2016;22(1):23-47. doi: 10.1093/humupd/dmv040. DOI: https://doi.org/10.1093/humupd/dmv040

Watson AJ. Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J Anim Sci. 2007;85(13 Suppl):E1-3. doi: 10.2527/jas.2006-432. DOI: https://doi.org/10.2527/jas.2006-432

Rienzi LF, Ubaldi FM. Oocyte retrieval and selection. In: Gardner DK, Weissman A, Howles CM, Shoham Z, (Eds.), Textbook of Assisted Reproductive Techniques, Volume1: Laboratory Perspectives, (5th ed.) CRC Press, Taylor and Francis group; 2018. P. 89-107.

Ferrer-Vaquer A, Barragán M, Rodríguez A, Vassena R. Altered cytoplasmic maturation in rescued in vitro matured oocytes. Hum Reprod. 2019;34(6):1095-1105. doi: 10.1093/humrep/dez052. DOI: https://doi.org/10.1093/humrep/dez052

Al Rahwanji MJ, Abouras H, Shammout MS, Altalla R, Al Sakaan R, Alhalabi N, et al. The optimal period for oocyte retrieval after the administration of recombinant human chorionic gonadotropin in in vitro fertilization. BMC Pregnancy Childbirth. 2022;22(1):184. doi: 10.1186/s12884-022-04412-9. DOI: https://doi.org/10.1186/s12884-022-04412-9

Garor R, Shufaro Y, Kotler N, Shefer D, Krasilnikov N, Ben-Haroush A, et al. Prolonging oocyte in vitro culture and handling time does not compensate for a shorter interval from human chorionic gonadotropin administration to oocyte pickup. Fertil Steril. 2015;103(1):72-75. doi: 10.1016/j.fertnstert.2014.09.022. DOI: https://doi.org/10.1016/j.fertnstert.2014.09.022

Rienzi L, Ubaldi F, Iacobelli M, Minasi MG, Romano S, Greco E. Meiotic spindle visualization in living human oocytes. Reprod Biomed Online. 2005;10(2):192-198. doi: 10.1016/s1472-6483(10)60940-6. DOI: https://doi.org/10.1016/S1472-6483(10)60940-6

De Santis L, Cino I, Rabellotti E, Calzi F, Persico P, Borini A, et al. Polar body morphology and spindle imaging as predictors of oocyte quality. Reprod Biomed Online. 2005;11(1):36-42. doi: 10.1016/s1472-6483(10)61296-5. DOI: https://doi.org/10.1016/S1472-6483(10)61296-5

Montag M, Schimming T, van der Ven H. Spindle imaging in human oocytes: the impact of the meiotic cell cycle. Reprod Biomed Online. 2006;12(4):442-446. doi: 10.1016/s1472-6483(10)61996-7. DOI: https://doi.org/10.1016/S1472-6483(10)61996-7

Holubcová Z, Kyjovská D, Martonová M, Páralová D, Klenková T, Kloudová S. Human egg maturity assessment and its clinical application. J Vis Exp. 2019;(150). doi: 10.3791/60058. DOI: https://doi.org/10.3791/60058-v

Granot I, Dekel N. Preparation and evaluation of oocytes for intracytoplasmic sperm injection. In: Gardner DK, Weissman A, Howles CM, Shoham Z, (Eds.), Textbook of Assisted Reproductive Techniques, Volume1: Laboratory Perspectives, (5th ed.) CRC Press, Taylor and Francis group; 2018. P. 108-116.

Rienzi L, Maggiulli R, Ubaldi F. Oocyte denuding. In: Nagy ZP, Varghese AC, Agarwal A, (Eds.), In Vitro Fertilization, A Textbook of Current and Emerging Methods and Devices, (2nd ed.) Springer Nature Switzerland AG; 2019. P. 133-145. DOI: https://doi.org/10.1007/978-3-319-43011-9_14

Falcone P, Gambera L, Pisoni M, Lofiego V, De Leo V, Mencaglia L, et al. Correlation between oocyte preincubation time and pregnancy rate after intracytoplasmic sperm injection. Gynecol Endocrinol. 2008;24(6):295-299. doi: 10.1080/09513590802095613. DOI: https://doi.org/10.1080/09513590802095613

Wang WH, Meng L, Hackett RJ, Odenbourg R, Keefe DL. Limited recovery of meiotic spindles in living human oocytes after cooling-rewarming observed using polarized light microscopy. Hum Reprod. 2001;16(11):2374-2378. doi: 10.1093/humrep/16.11.2374. DOI: https://doi.org/10.1093/humrep/16.11.2374

Moon JH, Hyun CS, Lee SW, Son WY, Yoon SH, Lim JH. Visualization of the metaphase II meiotic spindle in living human oocytes using the Polscope enables the prediction of embryonic developmental competence after ICSI. Hum Reprod. 2003;18(4):817-820. doi: 10.1093/humrep/deg165. DOI: https://doi.org/10.1093/humrep/deg165

Rienzi L, Ubaldi F, Martinez F, Iacobelli M, Minasi MG, Ferrero S, et al. Relationship between meiotic spindle location with regard to the polar body position and oocyte developmental potential after ICSI. Hum Reprod. 2003;18(6):1289-1293. doi: 10.1093/humrep/deg274. DOI: https://doi.org/10.1093/humrep/deg274

Cohen Y, Malcov M, Schwartz T, Mey-Raz N, Carmon A, Cohen T, et al. Spindle imaging: a new marker for optimal timing of ICSI? Hum Reprod. 2004;19(3):649-654. doi: 10.1093/humrep/deh113. DOI: https://doi.org/10.1093/humrep/deh113

Thanh Hoa N, Thanh Hoa N, Khanh Trang HN, Minh Duc N, Manh Ha N. Characteristics of oocytes that failed to fertilize after intracytoplasmic sperm injection. Clin Ter. 2023;174(2):189-194. doi: 10.7417/CT.2023.2518.

Hondo S, Arichi A, Muramatsu H, Omura N, Ito K, Komine H, et al. Clinical outcomes of transfer of frozen and thawed single blastocysts derived from nonpronuclear and monopronuclear zygotes. Reprod Med Biol. 2019;18(3):278-283. doi: 10.1002/rmb2.12275. DOI: https://doi.org/10.1002/rmb2.12275

Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, Matzuk MM. Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet. 2003;33(2):187-191. doi: 10.1038/ng1079. DOI: https://doi.org/10.1038/ng1079

Li L, Zheng P, Dean J. Maternal control of early mouse development. Development. 2010;137(6):859-870. doi: 10.1242/dev.039487. DOI: https://doi.org/10.1242/dev.039487

Ma T, Zhang Ch, Zhou S, Xie X, Chen J, Wang J, et al. RGS12 as a novel maternal-effect gene causes arrest at the pronuclear stage of human zygote. Res Square. 2021. doi: 10.21203/rs.3.rs-140375/v1. DOI: https://doi.org/10.21203/rs.3.rs-140375/v1

Pitsos MA, Nicolopoulou-Stamati P. DNA spatial distribution in unfertilized human oocytes by confocal laser scanning microscope. Mol Reprod Dev. 2002;62(3):368-374. doi: 10.1002/mrd.10095. DOI: https://doi.org/10.1002/mrd.10095

Galotto C, Cambiasso MY, Julianelli VL, Valzacchi GJR, Rolando RN, Rodriguez ML, et al. Human sperm decondensation in vitro is related to cleavage rate and embryo quality in IVF. J Assist Reprod Genet. 2019;36(11):2345-2355. doi: 10.1007/s10815-019-01590-y. DOI: https://doi.org/10.1007/s10815-019-01590-y

Sadeghi MR, Hodjat M, Lakpour N, Arefi S, Amirjannati N, Modarresi T, et al. Effects of sperm chromatin integrity on fertilization rate and embryo quality following intracytoplasmic sperm injection. Avicenna J Med Biotechnol. 2009;1(3):173-180. PMID: 23408716.

Bichara C, Berby B, Rives A, Jumeau F, Letailleur M, Setif V, et al. Sperm chromatin condensation defects, but neither DNA fragmentation nor aneuploidy, are an independent predictor of clinical pregnancy after intracytoplasmic sperm injection. J Assist Reprod Genet. 2019 Jul;36(7):1387-1399. doi: 10.1007/s10815-019-01471-4. DOI: https://doi.org/10.1007/s10815-019-01471-4