The Graduated Embryo Score of Embryos from Infertile Women with and without Peritoneal Endometriosis

Abstract

Objective To determine embryo quality (mean graduated embryo score [GES]) in infertile patients with endometriosis undergoing in vitro fertilization with embryo transfer (IVF-ET) compared with infertile patients without endometriosis.

Methods A case-control study was performed comparing 706 embryos (162 patients) divided into 2 groups: 472 embryos derived from patients without endometriosis (n = 109, infertile patients with tubal infertility) and 234 embryos from patients in the study group (n = 53, infertile patients with peritoneal endometriosis). All patients were subjected to IVF using an oestradiol-antagonist-recombinant follicle-stimulating hormone (FSH) protocol for ovarian stimulation. The mean GES was performed to evaluate all embryos at 3 points in time: 16 to 18 hours, 25 to 27 hours, and 64 to 67 hours. Embryo evaluation was performed according to the following parameters: fragmentation, nucleolar alignment, polar body apposition, blastomere number/morphology, and symmetry. The primary outcome measure was the mean GES score. We also compared fertilization, implantation, and pregnancy rates.

Results Although the number of embryos transferred was greater in patients with endometriosis than in the control group (2.38 ± 0.66 versus 2.15 ± 0.54; p = 0.001), the mean GES was similar in both groups (71 ± 19.8 versus 71.9 ± 23.5; p = 0.881). Likewise, the fertilization rate was similar in all groups, being 61% in patients with endometriosis and 59% in the control group (p = 0.511). No significant differences were observed in the implantation (21% versus 22%; [p = 0.989]) and pregnancy rates (26.4% versus 28.4%; p = 0.989).

Conclusion Embryo quality measured by the mean GES was not influenced by peritoneal endometriosis. Likewise, the evaluated reproductive outcomes were similar between infertile patients with and without endometriosis.

Resumo

Objetivo Determinar a qualidade do embrião (média de escore embrionário graduado [EEG]) em pacientes inférteis com endometriose submetidas à fertilização in vitro com transferência de embrião (FIV-TE) em comparação com pacientes inférteis sem endometriose.

Métodos Realizamos um estudo de caso-controle comparando 706 embriões (162 pacientes) divididos em dois grupos: 472 embriões derivados de pacientes sem endometriose (n = 109, pacientes inférteis com infertilidade tubária) e 234 embriões de pacientes do grupo de estudo (n = 53, inférteis pacientes com endometriose peritoneal). Todos os pacientes foram submetidos à fertilização in vitro usando um protocolo follicle-stimulating hormone (FSH) recombinante de estradiol-antagonista para estimulação ovariana. A média do EEG foi realizada para avaliar todos os embriões em três momentos: de 16 a 18 horas, 25 a 27 horas e 64 a 67 horas. A avaliação embrionária foi realizada de acordo com os seguintes parâmetros: fragmentação, alinhamento nucleolar, aposição do corpo polar, número de blastômeros/morfologia e simetria. A medida de desfecho primário foi o escore médios embrionário (EEG). Também avaliamos como desfechos secundários as taxas de fertilização, implantação e gravidez.

Resultados Embora o número de embriões transferidos tenha sido maior em pacientes com endometriose do que no grupo controle (2,38 ± 0,66 versus 2,15 ± 0,54; p = 0,001), o EEG médio foi semelhante nos dois grupos (71 ± 19,8 versus 71,9 ± 23,5; p = 0,881). Da mesma forma, a taxa de fertilização foi semelhante em todos os grupos, sendo 61% nos pacientes com endometriose e 59% no grupo controle (p = 0,511). Não foram observadas diferenças significativas nas taxas de implantação (21% versus 22%; [p = 0,989]) e nas taxas de gravidez (26,4% versus 28,4%; p = 0,989).

Conclusão A qualidade embrionária medida pelo EEG médio não foi influenciada pela endometriose peritoneal. Da mesma forma, os resultados reprodutivos avaliados foram semelhantes entre pacientes inférteis com e sem endometriose.

Keywords

endometriosis - in vitro fertilization - graduated embryo score - infertility

Palavras-chave

endometriose - fertilização in vitro - escore do embrião - infertilidade

Contributions

According to the criteria for scientific authorship of the International Committee of Medical Journal Editors (ICMJE), authorship credit was based on three conditions met in full: 1. Substantial contributions to conception and design, data collection or analysis, and interpretation of data; 2. Writing of the article or critical review of the intellectual content; and 3. Final approval of the version to be published.

Publikationsverlauf

Eingereicht: 15. April 2020

Angenommen: 23. Oktober 2020

Artikel online veröffentlicht:
29. Januar 2021

• References

• 1 Falconer H, Sundqvist J, Gemzell-Danielsson K, von Schoultz B, D'Hooghe TM, Fried G. IVF outcome in women with endometriosis in relation to tumour necrosis factor and anti-Müllerian hormone. Reprod Biomed Online 2009; 18 (04) 582-588
• 2 Mekaru K, Yagi C, Asato K, Masamoto H, Sakumoto K, Aoki Y. Effects of early endometriosis on IVF-ET outcomes. Front Biosci (Elite Ed) 2013; 5: 720-724
• 3 González-Comadran M, Schwarze JE, Zegers-Hochschild F, Souza MD, Carreras R, Checa MA. The impact of endometriosis on the outcome of Assisted Reproductive Technology. Reprod Biol Endocrinol 2017; 15 (01) 8
• 4 Hu Y, Maxson WS, Hoffman DI, Ory SJ, Eager S, Dupre J, Lu C. Maximizing pregnancy rates and limiting higher-order multiple conceptions by determining the optimal number of embryos to transfer based on quality. Fertil Steril 1998; 69 (04) 650-657
• 5 Coccia ME, Rizzello F, Mariani G, Bulletti C, Palagiano A, Scarselli G. Impact of endometriosis on in vitro fertilization and embryo transfer cycles in young women: a stage-dependent interference. Acta Obstet Gynecol Scand 2011; 90 (11) 1232-1238
• 6 De Conto E, Matte U, Cunha-Filho JS. BMP-6 and SMAD4 gene expression is altered in cumulus cells from women with endometriosis-associated infertility. Acta Obstet Gynecol Scand 2020; ••• [ahead of print]
• 7 De Conto E, Matte Ú, Bilibio JP, Genro VK, Souza CA, Leão DP, Cunha-Filho JS. Endometriosis-associated infertility: GDF-9, AMH, and AMHR2 genes polymorphisms. J Assist Reprod Genet 2017; 34 (12) 1667-1672
• 8 Lemos NA, Arbo E, Scalco R, Weiler E, Rosa V, Cunha-Filho JS. Decreased anti-Müllerian hormone and altered ovarian follicular cohort in infertile patients with mild/minimal endometriosis. Fertil Steril 2008; 89 (05) 1064-1068
• 9 Barbosa MAP, Teixeira DM, Navarro PA, Ferriani RA, Nastri CO, Martins WP. Impact of endometriosis and its staging on assisted reproduction outcome: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2014; 44 (03) 261-278
• 10 Yang X, Huang R, Cai M, Liang X. Endometriosis has no negative impact on outcomes of in vitro fertilisation in women with poor ovarian response. BJOG 2016; 123 (Suppl. 03) 76-81
• 11 Genro V, Souza C, Guedes da Luz L, Silva D, Andreoli C, Cunha-Filho J. The graduated embryo score (GES) and total graduated embryo score (TGES) were not associated to endometriosis. Fertil Steril 2009; 92 (03) S112-S113
• 12 Fisch JD, Rodriguez H, Ross R, Overby G, Sher G. The Graduated Embryo Score (GES) predicts blastocyst formation and pregnancy rate from cleavage-stage embryos. Hum Reprod 2001; 16 (09) 1970-1975
• 13 Garrido N, Navarro J, García-Velasco J, Remoh J, Pellice A, Simón C. The endometrium versus embryonic quality in endometriosis-related infertility. Hum Reprod Update 2002; 8 (01) 95-103
• 14 Simón C, Gutiérrez A, Vidal A, de los Santos MJ, Tarín JJ, Remohí J, Pellicer A. Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod 1994; 9 (04) 725-729
• 15 Cohen J, Ziyyat A, Naoura I, Chabbert-Buffet N, Aractingi S, Darai E, Lefevre B. Effect of induced peritoneal endometriosis on oocyte and embryo quality in a mouse model. J Assist Reprod Genet 2015; 32 (02) 263-270
• 16 Shebl O, Sifferlinger I, Habelsberger A, Oppelt P, Mayer RB, Petek E, Ebner T. Oocyte competence in in vitro fertilization and intracytoplasmic sperm injection patients suffering from endometriosis and its possible association with subsequent treatment outcome: a matched case-control study. Acta Obstet Gynecol Scand 2017; 96 (06) 736-744
• 17 Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 1997; 67 (05) 817-821
• 18 Julious SA. Sample sizes for clinical trials with normal data. Stat Med 2004; 23 (12) 1921-1986
• 19 von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol 2008; 61 (04) 344-349
• 20 Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A. Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril 2008; 90 (02) 247-257
• 21 Brizek CL, Schlaff S, Pellegrini VA, Frank JB, Worrilow KC. Increased incidence of aberrant morphological phenotypes in human embryogenesis--an association with endometriosis. J Assist Reprod Genet 1995; 12 (02) 106-112
• 22 Pellicer A, Valbuena D, Bauset C, Albert C, Bonilla-Musoles F, Remohí J, Simón C. The follicular endocrine environment in stimulated cycles of women with endometriosis: steroid levels and embryo quality. Fertil Steril 1998; 69 (06) 1135-1141
• 23 Sjöblom P, Menezes J, Cummins L, Mathiyalagan B, Costello MF. Prediction of embryo developmental potential and pregnancy based on early stage morphological characteristics. Fertil Steril 2006; 86 (04) 848-861
• 24 Terriou P, Sapin C, Giorgetti C, Hans E, Spach JL, Roulier R. Embryo score is a better predictor of pregnancy than the number of transferred embryos or female age. Fertil Steril 2001; 75 (03) 525-531
• 25 Luna M, Copperman AB, Duke M, Ezcurra D, Sandler B, Barritt J. Human blastocyst morphological quality is significantly improved in embryos classified as fast on day 3 (>or=10 cells), bringing into question current embryological dogma. Fertil Steril 2008; 89 (02) 358-363
• 26 Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil Steril 2002; 77 (06) 1148-1155