Top

Reproductive Biology and Endocrinology

Published in:

Open Access 01-12-2021 | ICSI | Review

Effect of the time interval between oocyte retrieval and ICSI on embryo development and reproductive outcomes: a systematic review

Authors: Xue Wang, YaLing Xiao, ZhengYi Sun, JingRan Zhen, Qi Yu

Published in: Reproductive Biology and Endocrinology | Issue 1/2021

Abstract

Background

Intra-cytoplasmic sperm injection (ICSI) is used in assisted reproductive technology (ART) laboratories. However, there is no consensus regarding the precise time intervals within ICSI cycles [oocyte pick up (OPU), oocyte denudation (DN), and ICSI], and results are inconsistent and contradictory. Thus, we aim to evaluate whether there is a concordance regarding the time intervals used in different laboratories and a concrete time that gives better laboratory and reproductive results.

Methods

A systematic review of the literature until July 25, 2020, was performed with the keywords “Oocyte Denudation/Denudation/Oocyte,” “Intra-cytoplasmic Sperm Injection/ICSI,” “Oocyte/Oocyte maturation/ cumulus,” and “Cumulus removal/ removal.” Articles and abstracts in English and involving human subjects referring to the effects of oocyte DN time on embryo development and clinical outcomes were included.

Results

Of the 294 evaluated articles, 24 (including 20 full articles and 4 abstracts) were included in this review. Eighteen studies analysed the effect of OPU-DN time on embryo development and clinical outcomes. Most of these studies concluded that OPU-DN time did not influence ICSI outcomes, but some suggested that oocytes should be incubated for a short time before DN to improve oocyte maturity and enhance ICSI outcomes. In addition to reports on positive or negligible effects, adverse effects were reported in 12 studies on DN-ICSI timing. Neither OPU-DN nor DN-ICSI time could improve live birth rate.

Conclusions

Oocytes should be pre-incubated for a short duration (preferably < 4 h) before DN according to the ART laboratory schedule. More randomised controlled trials are warranted to clarify the effect of DN-ICSI timing on ICSI outcomes.

Palermo G, Joris H, Devroey P, Van Steirteghem AC. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet. 1992;340(8810):17–8.

Hassan HA. Cumulus cell contribution to cytoplasmic maturation and oocyte developmental competence in vitro. J Assist Reprod Genet. 2001;18(10):539–43.PubMedPubMedCentralCrossRef

Falcone P, Gambera L, Pisoni M, et al. Correlation between oocyte preincubation time and pregnancy rate after intracytoplasmic sperm injection. Gynecol Endocrinol. 2008;24(6):295–9.PubMedCrossRef

Aletebi F. Denudation and sperm injection interval timing: impact on outcome of intracytoplasmic sperm injection. Int J Women's Health. 2011;3:99–103.CrossRef

Garor R, Shufaro Y, Kotler N, 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):72–5.PubMedCrossRef

Kimura N, Hoshino Y, Totsukawa K, Sato E. Cellular and molecular events during oocyte maturation in mammals: molecules of cumulus-oocyte complex matrix and signalling pathways regulating meiotic progression. Soc Reprod Fertil Suppl. 2007;63:327–42.PubMed

Richani D, Gilchrist RB. The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update. 2018;24(1):1–14.PubMedCrossRef

Mao L, Lou H, Lou Y, Wang N, Jin F. Behaviour of cytoplasmic organelles and cytoskeleton during oocyte maturation. Reprod BioMed Online. 2014;28(3):284–99.PubMedCrossRef

Watson AJ. Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J Anim Sci. 2007;85(13 Suppl):E1–3.PubMedCrossRef

10.

Kidder GM, Vanderhyden BC. Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can J Physiol Pharmacol. 2010;88(4):399–413.

11.

Scarica C, Cimadomo D, Dovere L, et al. An integrated investigation of oocyte developmental competence: expression of key genes in human cumulus cells, morphokinetics of early divisions, blastulation, and euploidy. J Assist Reprod Genet. 2019;36(5):875–87.PubMedPubMedCentralCrossRef

12.

Dumesic DA, Meldrum DR, Katz-Jaffe MG, Krisher RL, Schoolcraft WB. Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health. Fertil Steril. 2015;103(2):303–16.PubMedCrossRef

13.

Richard S, Baltz JM. Prophase I arrest of mouse oocytes mediated by natriuretic peptide precursor C requires GJA1 (connexin-43) and GJA4 (connexin-37) gap junctions in the antral follicle and cumulus-oocyte complex. Biol Reprod. 2014;90(6):137.PubMedCrossRef

14.

Rubino P, Viganò P, Luddi A, Piomboni P. The ICSI procedure from past to future: a systematic review of the more controversial aspects. Hum Reprod Update. 2016;22(2):194–227.

15.

Isiklar A, Mercan R, Balaban B, Alatas C, Aksoy S, Urman B. Impact of oocyte pre-incubation time on fertilization, embryo quality and pregnancy rate after intracytoplasmic sperm injection. Reprod BioMed Online. 2004;8(6):682–6.PubMedCrossRef

16.

Mizuno S, Ishikawa Y, Matsumoto H, et al. The timing of cumulus cell removal for intracytoplasmic sperm injection influences the capability of embryonic development. Reprod Med Biol. 2019;18(1):111–7.PubMedCrossRef

17.

Patrat C, Kaffel A, Delaroche L, et al. Optimal timing for oocyte denudation and intracytoplasmic sperm injection. Obstet Gynecol Int. 2012;2012:403531.PubMedPubMedCentralCrossRef

18.

Zhu J, Zhang J, Li H, et al. Cumulus cells accelerate oocyte aging by releasing soluble Fas ligand in mice. Sci Rep. 2015;5:8683.PubMedPubMedCentralCrossRef

19.

Bárcena P, Rodríguez M, Obradors A, Vernaeve V, Vassena R. Should we worry about the clock? Relationship between time to ICSI and reproductive outcomes in cycles with fresh and vitrified oocytes. Hum Reprod. 2016;31(6):1182–91.PubMedCrossRef

20.

Pujol A, García D, Obradors A, Rodríguez A, Vassena R. Is there a relation between the time to ICSI and the reproductive outcomes. Hum Reprod. 2018;33(5):797–806.PubMedCrossRef

21.

Van de Velde H, De Vos A, Joris H, Nagy ZP, Van Steirteghem AC. Effect of timing of oocyte denudation and micro-injection on survival, fertilization and embryo quality after intracytoplasmic sperm injection. Hum Reprod. 1998;13(11):3160–4.PubMedCrossRef

22.

Yanagida K, Yazawa H, Katayose H, Suzuki K, Hoshi K, Sato A. Influence of oocyte preincubation time on fertilization after intracytoplasmic sperm injection. Hum Reprod. 1998;13(8):2223–6.PubMedCrossRef

23.

Rienzi L, Ubaldi F, Anniballo R, Cerulo G, Greco E. Preincubation of human oocytes may improve fertilization and embryo quality after intracytoplasmic sperm injection. Hum Reprod. 1998;13(4):1014–9.PubMedCrossRef

24.

Andrews MM, Fishel SB, Rowe PH, Berry JA, Lisi F, Rinaldi L. Analysis of intracytoplasmic sperm injection procedures related to delayed insemination and ejaculated, epididymal and testicular spermatozoa. Reprod BioMed Online. 2001;2(2):89–97.PubMedCrossRef

25.

Jacobs M, Stolwijk AM, Wetzels AM. The effect of insemination/injection time on the results of IVF and ICSI. Hum Reprod. 2001;16(8):1708-13.

26.

Ho JY, Chen MJ, Yi YC, Guu HF, Ho ES. The effect of preincubation period of oocytes on nuclear maturity, fertilization rate, embryo quality, and pregnancy outcome in IVF and ICSI. J Assist Reprod Genet. 2003;20(9):358–64.

27.

Boldi CP, Colasante C, Perego L, De Lauretis L. Effect of early and late oocyte denudation on ICSI outcome. Human Reprod. 2010;25(SUPPL. 1):i180.

28.

Esbert M, Florensa M, Riqueros M, Teruel J, Ballesteros A. Effect of oocyte denudation timing on clinical outcomes in 1212 oocyte recipients. Fertility and Sterility. 2013;100(3 SUPPL):1 S482-.

29.

Terasawa H, Ueno S, Uchiyama K, Yabuuchi A, Okuno T, Kobayashi T, Kato K. Effect of timing of oocyte denudation after oocyte retrieval on fertilization and pregnancy outcome following cleavage stage single embryo transfer. Human Reprod. 2016;31(Supplement 1):i202.

30.

Ishikawa Y, Inaba M, Matsumoto H, Mizuno S, Mori R, Ida M, Fukuda A, Morimoto Y. Influence of the duration between removal of cumulus cells and oocyte retrieval on fertilization and embryonic development. Human Reprod. 2016;31(Supplement 1):i1–2.

31.

Pereira N, Neri QV, Lekovich JP, Palermo GD, Rosenwaks Z. The role of in-vivo and in-vitro maturation time on ooplasmic dysmaturity. Reprod BioMed Online. 2016;32(4):401–6.PubMedCrossRef

32.

Naji O, Moska N, Dajani Y, et al. Early oocyte denudation does not compromise ICSI cycle outcome: a large retrospective cohort study. Reprod BioMed Online. 2018;37(1):18–24.PubMedCrossRef

33.

Zhang Y, Ma Y, Fang Z, et al. Performing ICSI within 4 hours after denudation optimizes clinical outcomes in ICSI cycles. Reprod Biol Endocrinol. 2020;18(1):27.PubMedPubMedCentralCrossRef

34.

Azizi E, Naji M, Nazarian H, et al. Does timing in ICSI cycle affect oocyte quality and reproductive outcomes? A prospective study. Arch Gynecol Obstet. 2020;302(2):505–13.PubMedCrossRef

35.

Maggiulli R, Cimadomo D, Fabozzi G, et al. The effect of ICSI-related procedural timings and operators on the outcome. Hum Reprod. 2020;35(1):32–43.PubMedCrossRef

36.

Eppig JJ, Schultz RM, O'Brien M, Chesnel F. Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Dev Biol. 1994;164(1):1–9.PubMedCrossRef

37.

Raziel A, Schachter M, Strassburger D, Kasterstein E, Ron-El R, Friedler S. In vivo maturation of oocytes by extending the interval between human chorionic gonadotropin administration and oocyte retrieval. Fertil Steril. 2006;86(3):583–7.

38.

Son WY, Chung JT, Chian RC, Herrero B, Demirtas E, Elizur S, Gidoni Y, Sylvestre C, Dean N, Tan SL. A 38 h interval between hCG priming and oocyte retrieval increases in vivo and in vitro oocyte maturation rate in programmed IVM cycles. Hum Reprod. 2008;23(9):2010–6.

39.

Gilchrist RB, Ritter LJ, Armstrong DT. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci. 2004;82-83:431–46.PubMedCrossRef

40.

Schramm RD, Bavister BD. Granulosa cells from follicle stimulating hormone-primed monkeys enhance the development competence of in-vitro-matured oocytes from non-stimulated rhesus monkeys. Hum Reprod. 1996;11(8):1698–702.PubMedCrossRef

41.

Zhao X, Du F, Liu X, et al. Brain-derived neurotrophic factor (BDNF) is expressed in buffalo (Bubalus bubalis) ovarian follicles and promotes oocyte maturation and early embryonic development. Theriogenology. 2019;130:79–88.PubMedCrossRef

42.

Martini E, Flaherty SP, Swann NJ, Payne D, Matthews CD. Analysis of unfertilized oocytes subjected to intracytoplasmic sperm injection using two rounds of fluorescence in-situ hybridization and probes to five chromosomes. Hum Reprod. 1997;12(9):2011–8.PubMedCrossRef

43.

Jiang GJ, Wang K, Miao DQ, et al. Protein profile changes during porcine oocyte aging and effects of caffeine on protein expression patterns. PLoS One. 2011;6(12):e28996.PubMedPubMedCentralCrossRef

44.

Ebeling S, Labudda A, Meinecke B. In vitro ageing of porcine oocytes: changes in phosphorylation of the mitogen-activated protein kinase (MAPK) and parthenogenetic activability. Reprod Domest Anim. 2010;45(6):e398–404.PubMedCrossRef

45.

Combelles CM, Kearns WG, Fox JH, Racowsky C. Cellular and genetic analysis of oocytes and embryos in a human case of spontaneous oocyte activation. Hum Reprod. 2011;26(3):545–52.

46.

Cui W, Zhang J, Lian HY, Wang HL, Miao DQ, Zhang CX, Luo MJ, Tan JH. Roles of MAPK and spindle assembly checkpoint in spontaneous activation and MIII arrest of rat oocytes. PLoS One. 2012;7(2):e32044.

47.

Madgwick S, Jones KT. How eggs arrest at metaphase II: MPF stabilisation plus APC/C inhibition equals cytostatic factor. Cell Div. 2007;2:4.PubMedPubMedCentralCrossRef

48.

Vogt E, Kirsch-Volders M, Parry J, Eichenlaub-Ritter U. Spindle formation, chromosome segregation and the spindle checkpoint in mammalian oocytes and susceptibility to meiotic error. Mutat Res. 2008;651(1-2):14–29.

49.

Muechler EK, Graham MC, Huang KE, Partridge AB, Jones K. Parthenogenesis of human oocytes as a function of vacuum pressure. J In Vitro Fert Embryo Transf. 1989;6(6):335–7.

50.

Grigoryan H, Levkov L, Sciorio R, Hambartsoumian E. Unexplained total abnormal fertilization of donor oocytes in ICSI with using spermatozoa from different patients. Gynecol Endocrinol. 2019;35(Sup 1):60–2.

51.

Ye Y, Li N, Yan X, Wu R, Zhou W, Cheng L, Li Y. Genetic analysis of embryo in a human case of spontaneous oocyte activation: a case report. Gynecol Endocrinol. 2020;36(4):294–6.

52.

Cui W, Zhang J, Zhang CX, Jiao GZ, Zhang M, Wang TY, Luo MJ, Tan JH. Control of spontaneous activation of rat oocytes by regulating plasma membrane Na+/Ca2+ exchanger activities. Biol Reprod. 2013;88(6):160.

53.

Socolov R, Ebner T, Gorduza V, Martiniuc V, Angioni S, Socolov D. Self-oocyte activation and parthenogenesis: an unusual outcome of a misconducted IVF cycle. Gynecol Endocrinol. 2015;31(7):529–30.

54.

Dai J, Leng LZ, Lu CF, Gong F, Zhang SP, Zheng W, Lu GX, Lin G. Time-lapse observation and transcriptome analysis of a case with repeated multiple pronuclei after IVF/ICSI. J Assist Reprod Genet. 2017;34(9):1189–97.

55.

Lian HY, Gao Y, Jiao GZ, Sun MJ, Wu XF, Wang TY, Li H, Tan JH. Antioxidant supplementation overcomes the deleterious effects of maternal restraint stress-induced oxidative stress on mouse oocytes. Reproduction. 2013;146(6):559–68.

56.

Belli M, Zhang L, Liu X, Donjacour A, Ruggeri E, Palmerini MG, Nottola SA, Macchiarelli G, Rinaudo P. Oxygen concentration alters mitochondrial structure and function in in vitro fertilized preimplantation mouse embryos. Hum Reprod. 2020;35(6):1476.

57.

Al-Gubory KH, Fowler PA, Garrel C. The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int J Biochem Cell Biol. 2010;42(10):1634–50.PubMedCrossRef

58.

Guérin P, El MS, Ménézo Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update. 2001;7(2):175–89.PubMedCrossRef

59.

Adeoye O, Olawumi J, Opeyemi A, Christiania O. Review on the role of glutathione on oxidative stress and infertility. JBRA Assist Reprod. 2018;22(1):61–6.PubMedPubMedCentral

60.

Takahashi T, Igarashi H, Amita M, Hara S, Matsuo K, Kurachi H. Molecular mechanism of poor embryo development in postovulatory aged oocytes: mini review. J Obstet Gynaecol Res. 2013;39(10):1431–9.PubMedCrossRef

61.

Takahashi T, Igarashi H, Kawagoe J, Amita M, Hara S, Kurachi H. Poor embryo development in mouse oocytes aged in vitro is associated with impaired calcium homeostasis. Biol Reprod. 2009;80(3):493–502.PubMedCrossRef

62.

Bontekoe S, Mantikou E, van Wely M, Seshadri S, Repping S, Mastenbroek S. Low oxygen concentrations for embryo culture in assisted reproductive technologies. Cochrane Database Syst Rev. 2012;11(7):CD008950.

63.

Bianchi S, Macchiarelli G, Micara G, et al. Ultrastructural markers of quality are impaired in human metaphase II aged oocytes: a comparison between reproductive and in vitro aging. J Assist Reprod Genet. 2015;32(9):1343–58.PubMedPubMedCentralCrossRef

64.

García-Oro S, Rey MI, Rodríguez M, Durán Á, Devesa R, Valverde D. Predictive value of spindle retardance in embryo implantation rate. J Assist Reprod Genet. 2017;34(5):617–25.PubMedPubMedCentralCrossRef

65.

Trapphoff T, Heiligentag M, Dankert D, et al. Postovulatory aging affects dynamics of mRNA, expression and localization of maternal effect proteins, spindle integrity and pericentromeric proteins in mouse oocytes. Hum Reprod. 2016;31(1):133–49.PubMedCrossRef

Title: Effect of the time interval between oocyte retrieval and ICSI on embryo development and reproductive outcomes: a systematic review
Authors: Xue Wang
YaLing Xiao
ZhengYi Sun
JingRan Zhen
Qi Yu
Publication date: 01-12-2021
Publisher: BioMed Central
Keyword: ICSI
Published in: Reproductive Biology and Endocrinology / Issue 1/2021
Electronic ISSN: 1477-7827
DOI: https://doi.org/10.1186/s12958-021-00717-0

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Effect of the time interval between oocyte retrieval and ICSI on embryo development and reproductive outcomes: a systematic review

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2021

Exploration of the value of progesterone and progesterone/estradiol ratio on the hCG trigger day in predicting pregnancy outcomes of PCOS patients undergoing IVF/ICSI: a retrospective cohort study

5-aza-2′-deoxycitidine inhibits cell proliferation, extracellular matrix formation and Wnt/β-catenin pathway in human uterine leiomyomas

The cannabinoid receptor CB1 affects the proliferation and apoptosis of adenomyotic human uterine smooth muscle cells of the junctional zone: a mechanism study

Corpus luteum number and the maternal renin-angiotensin-aldosterone system as determinants of utero-placental (vascular) development: the Rotterdam Periconceptional Cohort

Downregulation of decidual SKP2 is associated with human recurrent miscarriage

Evaluation of intra-ovarian platelet-rich plasma administration on oocytes-dependent variables in patients with poor ovarian response: A retrospective study according to the POSEIDON criteria