Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Journal of Ovarian Research
Published in: Journal of Ovarian Research 1/2017

Open Access 01-12-2017 | Research

Impact of oocytes with CLCG on ICSI outcomes and their potential relation to pesticide exposure

Authors: Philippe Merviel, Rosalie Cabry, Karen Chardon, Elodie Haraux, Florence Scheffler, Naima-belhadri Mansouri, Aviva Devaux, Hikmat Chahine, Véronique Bach, Henri Copin, Moncef Benkhalifa

Published in: Journal of Ovarian Research | Issue 1/2017

Login to get access

Abstract

Background

Oocyte quality is a key limiting factor in female fertility which is primarily reflected in morphological features. Centrally located cytoplasm granulation (CLCG) is one type of cytoplasmic dimorphism exhibited by oocytes that could be linked to pesticide exposure with a significant risk of decreased ICSI outcomes.

Methods

This retrospective study included 633 women who were part of an intracytoplasmic spermatozoa injection (ICSI) program between 2009 and 2011. The participants lived in the Picardy region of France and had been exposed to pesticides. The participants were divided in two groups based on prevalence of oocytes with CLCG (LCLCG [n = 83]: low prevalence of oocytes with CLCG under 25%. HCLCG [n = 68]: high prevalence of CLCG over 75%). The embryological and clinical outcomes were analysed for both groups and were calculated using the difference between the two values.

Results

Results for couples with HCLCG compared to LCLCG showed a decrease in embryo cleavage, ongoing pregnancy, and live birth rates (82%, 14%, 13% vs 99%, 32%, 30%, respectively).The early miscarriage rate was increased (47% vs 11%), with an OR of 3.1 (95%CI [2.1–4.1]). Due to high pesticide exposure (over 3000 g/ha), there is a higher risk of a resulting disturbed oocyte cohort with a high prevalence of CLCG over 75%.

Conclusion

The high prevalence of oocytes with CLCG over 75% has a negative effect on embryos and the general ICSI clinical outcomes. Furthermore, a putative association between pesticide exposure and risk of CLCG was identified, justifying the need for further research and a potential need to find alternative assisted reproductive technologies for these couples.

Trial registration

Tabacfertimasc. ID number: ID2011-A00634–37; registered 2011/2/8
Literature
1.
Van Blerkom J. Occurrence and developmental consequences of aberrant cellular organization in meiotically mature human oocytes after exogenous ovarian hyperstimulation. J Electron Microsc Tech. 1990;16:324–46.CrossRefPubMed
2.
Veeck LL. Oocyte quality and assisted conception. ActaEurFertil. 1992; 23: 275–288.
3.
Rienzi L, Vajta G, Ubaldi F. Predictive value of oocyte morphology in human IVF: a systematic review of the literature. Hum Reprod Update. 2010;17:34–45.CrossRefPubMedPubMedCentral
4.
De Sutter P, Dozortsev D, Qian C, Dhont M. Oocyte morphology does not correlate with fertilization rate and embryo quality after intracytoplasmic sperm injection. Hum Reprod. 1996;11:595–7.CrossRefPubMed
5.
Ebner T, Moser M, Tews G. Is oocyte morphology prognostic of embryo developmental potential after ICSI ?RBM. Online. 2006;12:507–12.
6.
Rienzi L, Ubaldi FM, Iacobelli M, Minasi MG, Romano S, et al. Significance of metaphase II human oocyte morphology on ICSI outcome. FertilSteril. 2008;90:1692–700.
7.
8.
Serhal PF, Ranieri DM, Kinis A, Marchant S, Davies M, et al. Oocyte morphology predicts outcome of intracytoplasmic sperm injection. Hum Reprod. 1997;12:1267–70.CrossRefPubMed
9.
Balaban B, Urman B, Sertac A, Alatas C, Aksoy S, et al. Oocyte morphology does not affect fertilization rate, embryo quality and implantation rate after intracytoplasmic sperm injection. Hum Reprod. 1998;13:3431–3.CrossRefPubMed
10.
Ebner T, Yaman C, Moser M, Sommergruber M, Feichtinger O, et al. Prognostic value of first polar body morphology on fertilization rate and embryo quality in intracytoplasmic sperm injection. Hum Reprod. 2000;15:427–30.CrossRefPubMed
11.
Otsuki J, Okada A, Morimoto K, Nagai Y, Kubo H. The relationship between pregnancy outcome and smooth endoplasmic reticulum clusters in MII human oocytes. Hum Reprod. 2004;19:1591–7.CrossRefPubMed
12.
Sa R, Cunha M, Silva J, Luis A, Oliveira C, et al. Ultrastructure of tubular smooth endoplasmic reticulum aggregates in human metaphase II oocytes and clinical implications. FertilSteril. 2011;96:143–9.
13.
14.
Kahraman S, Yakin K, Donmez E, Samli H, Bahce M, et al. Relationship between granular cytoplasm of oocytes and pregnancy outcome following intracytoplasmic sperm injection. Hum Reprod. 2000;15:2390–3.CrossRefPubMed
15.
Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update. 2008;14:159–77.CrossRefPubMed
16.
Kahraman S, Benkhalifa M, Donmez E, Biricik A, Sertyel S, et al. The results of aneuploidy screening in 276 couples undergoing assisted reproductive techniques. Prenat Diagn. 2004;24:307–11.CrossRefPubMed
17.
Van Blerkom J, Henry G. Oocyte dysmorphism and aneuploidy in meiotically mature human oocytes after ovarian stimulation. Hum Reprod. 1992;7:379–90.CrossRefPubMed
18.
Plachot M. Chromosomal abnormalities in oocytes. Mol Cell Endocrinol. 2001;183:59–63.CrossRef
19.
Xia P. Intracytoplasmic sperm injection: correlation of oocyte grade based on polar body, perivitelline space and cytoplasmic inclusions with fertilization rate and embryo quality. Hum Reprod. 1997;12:1750–5.CrossRefPubMed
20.
Wilding M, Di ML, D’Andretti S, Montanaro N, Capobianco C, Dale B. An oocyte score for use in assisted reproduction. J Assist Reprod Genet. 2007;24:350–8.CrossRefPubMedPubMedCentral
21.
22.
Alikani M, Palermo G, Adler A, Bertoli M, Blake M, et al. Intracytoplasmic sperm injection in dysporphic human oocytes. Zygote. 1995;3:283–8.CrossRefPubMed
23.
Schmutzler AG, Acar-Perk B, Weimer J, Salmassi A, Sievers K, et al. Oocyte morphology on day 0 correlates with aneuploidy as detected by polar body biopsy and FISH. Arch Gynecol Obstet. 2014;289:445–50.CrossRefPubMed
24.
Pocar P, Brevini TA, Fischer B, Gandolfi F. The impact of endocrine disruptors on oocyte competence. Reproduction. 2003;125:313–25.CrossRefPubMed
25.
Terriou P, Sapin C, Giorgetti C, Hans E, Spach JL, et al. Embryo score is a better predictor of pregnancy than the number of transferred embryos or female age. FertilSteril. 2001;75:525–31.
26.
Benkhalifa M, Madkour A, Louanjli N, Bouamoud N, Saadani B, et al. From global proteome profiling to single targeted molecules of follicular fluid and oocyte: contribution to embryo development and IVF outcome. Exp Rev Proteom. 2015;12:407–23.CrossRef
27.
World Health Organization. WHO laboratory manual for the examination and processing of human semen. 2010.
28.
Madkour A, Bouamoud N, Louanjli N, Kaarouch I, Copin H, et al. Intrauterine insemination of cultured peripheral blood mononuclear cells prior to embryo transfer improves clinical outcome for patients with repeated implantation failures. Zygote. 2016;24:58–69.CrossRefPubMed
29.
Balaban B, Urman B. Effect of oocyte morphology on embryo development and implantation. RBM Online. 2006;12:608–15.PubMed
30.
Figueira RC, Braga DP, Semiao-Francisco L, Iaconelli A Jr, Borges E Jr. Oocyte yield and dysmorphisms as indicators of biological efficiency in intracytoplasmic sperm injection cycles. Hum Fertil (Camb). 2011;14:41–7.CrossRef
31.
Ten J, Mendiola J, Vioque J, de Juan J, Bernabeu R. Donor oocyte dysmorphisms and their influence on fertilization and embryo quality. RBM Online. 2007;14:40–8.PubMed
32.
Yakin K, Balaban B, Isiklar A, Urman B. Oocyte dysmorphism is not associated with aneuploidy in the developing embryo. FertilSteril. 2007;88:811–6.
33.
Setti AS, Figueira RC, Braga DP, Colturato SS, Iaconelli A Jr, et al. Relationship between oocyte abnormal morphology and intracytoplasmic sperm injection outcomes : a meta-analysis. Eur J ObstetGynecolReprod Biol. 2011;159:364–70.
34.
Sousa M, Cunha M, Silva J, Oliveira E, Pinho MJ, et al. Ultrastructural and cytogenetic analyses of mature human oocyte dysmorphisms with respect to clinical outcomes. J Assist Reprod Genet. 2016:1–7.
35.
Seidler EA, Moley KH. Metabolic determinants of mitochondrial function in oocytes. In seminars in reproductive medicine. Thieme Medical Publishers. 2015;33:396–400.
36.
Kovalskaya EV, Makarova NP, Syrkasheva AG, Dolgushina NV, Kurilo LF. Mechanisms of smooth endoplasmic reticulum aggregates creation in oocyte's cytoplasm in IVF cycles and its clinical relevance. Tsitologiia. 2015;57:129–34.PubMed
37.
Balaban B, Ata B, Isiklar A, Yakin K, Urman B. Severe cytoplasmic abnormalities of the oocyte decrease cryosurvival and subsequent embryonic development of cryopreserved embryos. Hum Reprod. 2008;23:1778–5.CrossRefPubMed
38.
Ebner T, Moser M, Shebl O, Sommergruber M, Yaman C, et al. Blood clots in the cumulus–oocyte complex predict poor oocyte quality and post-fertilization development. RBM Online. 2008;16:801–7.PubMed
39.
Chamayou S, Ragolia C, Alecci C, Storaci G, Maglia E, et al. Meiotic spindle presence and oocyte morphology do not predict clinical ICSI outcomes: a study of 967 transferred embryos. RBM Online. 2006;13:661–7.PubMed
40.
Ashrafi M, Karimian L, Eftekhari-Yazdi P, Hasani F, Arabipoor A, et al. Effect of oocyte dysmorphisms on intracytoplasmic sperm injection cycle outcomes in normal ovarian responders. J ObstGyn Res. 2015;41:1912–20.
41.
Yu EJ, Ahn H, Lee JM, Jee BC, Kim SH. Fertilization and embryo quality of mature oocytes with specific morphological abnormalities. ClinExperReprod Med. 2015;42:156–62.
42.
Baart EB, Martini E, Eijkemans MJ, Van Opstal D, Beckers NG, et al. Milder ovarian stimulation for in-vitro fertilization reduces aneuploidy in the human preimplantation embryo: a randomized controlled trial. Hum Reprod. 2007;22:980–8.CrossRefPubMed
43.
Dolgushina NV, Syrkasheva AG, Makarova NP, Kovalskaya EV, Kalinina EA, et al. Correlation between oocyte morphology and the embryo aneuploidy rate in IVF cycles. GynecolEndocrin. 2015;31:61–4.
44.
Loutradis D, Drakakis P, Kallianidis K, Milingos S, Dendrinos S, et al. Oocyte morphology correlates with embryo quality and pregnancy rate after intracytoplasmic sperm injection. FertilSteril. 1999;72:240–4.
45.
Maranghi F, Tassinari R, Moracci G, Macrì C, Mantovani A. Effects of a low oral dose of diethylstilbestrol (DES) on reproductive tract development in F1 female CD-1 mice. ReprodToxicol. 2008;26:146–50.
46.
Stoop D, Ermini B, Polyzos NP, Haentjens P, De Vos M, et al. Reproductive potential of a metaphase II oocyte retrieved after ovarian stimulation: an analysis of 23 354 ICSI cycles. Hum Reprod. 2012;27:2030–5.CrossRefPubMed
47.
Munné S, Ary J, Zouves C, Escudero T, Barnes F, et al. Wide range of chromosome abnormalities in the embryos of young egg donors. RBM Online. 2006;12:340–6.PubMed
48.
Dominguez MA, Sadeu JC, Guerra MT, Furlong HC, Baines S, et al. Ovarian toxicity of environmental contaminants: 50 shades of Grey. In TranslatToxicol Springer International Publishing. 2016:215–44.
49.
Fujimoto VY, Kim D, vom Saal FS, Lamb JD, Taylor JA et al. Serum unconjugated bisphenol a concentrations in women may adversely influence oocyte quality during in vitro fertilization. Fert Steril 2011;95:1816–1819.
50.
Newbold R. Cellular and molecular effects of developmental exposure to diethylstilbestrol: implications for other environmental estrogens. Environ Health Perspect. 1995;103:83–7.CrossRefPubMedPubMedCentral
51.
Kelce WR, Stone CR, Laws SC, Gray LE, Kemppainen JA, et al. Persistent DDT metabolite p, p'DDE is a potent androgen receptor antagonist. Nature. 1995;375:581–5.CrossRefPubMed
52.
Kelce WR, Monosson E, Gamcsik MP, Laws SC, Gray LE. Environmental hormone disruptors: evidence that vinclozolin developmental toxicity is mediated by antiandrogenic metabolites. ToxicolApplPharmacol. 1994;126:276–85.
53.
Chedrese PJ, Feyles F. The diverse mechanism of action of dichlorodiphenyldichloroethylene (DDE) and methoxychlor in ovarian cells in vitro. ReprodToxicol. 2001;15:693–8.
54.
Holloway AC, Petrik JJ, Younglai EV. Influence of dichlorodiphenylchloroethylene on vascular endothelial growth factor and insulin-like growth factor in human and rat ovarian cells. ReprodToxicol. 2007;24:359–64.
55.
Hall DL, Payne LA, Putnam JM, Huet-Hudson YM. Effect of methoxychlor on implantation and embryo development in the mouse. ReprodToxicol. 1997;11:703–8.
56.
Arbuckle TE, Lin Z, Mery LS. An exploratory analysis of the effect of pesticide exposure on the risk of spontaneous abortion in an Ontario farm population. Environ HealthPerspect. 2001;109:851–7.
57.
Willis WO, de Peyster A, Molgaard CA, Walker C, MacKendrick T. Pregnancy outcome among women exposed to pesticides through work or residence in an agricultural area. J Occup Med. 1993;35:943–9.CrossRefPubMed
Metadata
Title
Impact of oocytes with CLCG on ICSI outcomes and their potential relation to pesticide exposure
Authors
Philippe Merviel
Rosalie Cabry
Karen Chardon
Elodie Haraux
Florence Scheffler
Naima-belhadri Mansouri
Aviva Devaux
Hikmat Chahine
Véronique Bach
Henri Copin
Moncef Benkhalifa
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of Ovarian Research / Issue 1/2017
Electronic ISSN: 1757-2215
DOI
https://doi.org/10.1186/s13048-017-0335-2

Other articles of this Issue 1/2017

Journal of Ovarian Research 1/2017 Go to the issue

Research

The value of dynamic contrast–enhanced MRI in characterizing complex ovarian tumors

Research

MiR-1307 promotes ovarian cancer cell chemoresistance by targeting the ING5 expression

Research

Plasma levels of MMP-7 and TIMP-1 in laboratory diagnostics and differentiation of selected histological types of epithelial ovarian cancers

Research

A retrospective study of reproductive outcomes after fertility-sparing surgery and postoperative adjuvant chemotherapy in malignant ovarian germ cell tumors and sex cord-stromal tumors

Review

Racial health disparities in ovarian cancer: not just black and white

Research

Intravenous neutralization of vascular endothelial growth factor reduces vascular function/permeability of the ovary and prevents development of OHSS-like symptoms in rhesus monkeys