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Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation
Abstract
A retrospective analysis of our in-vitro fertilization (IVF) and oocyte donation programmes was carried out in order to gain clinical knowledge of the factors involved in the aetiology of the endometriosis-associated infertility. Comparison between the IVF outcomes from 96 cycles in 78 patients with tubal infertility and from 96 cycles in 59 women with endometriosis indicates that endometriosis patients have a poor IVF outcome in terms of reduced pregnancy rate per cycle (P < 0.0004), reduced pregnancy rate per transfer (P < 0.002), and reduced implantation rate (P < 0.003). The analysis of patients undergoing oocyte donation for different reasons, including low response with or without endometriosis, showed that patients with this disease have the same chances of implantation and pregnancy as other recipients when the oocytes came from donors without known endometriosis. However, when the results of oocyte donation were classified according to the origin of the oocytes donated, patients who received embryos derived from endometriotic ovaries showed a significantly (P < 0.05) reduced implantation rate as compared to the remaining groups. Taken together, all these observations suggest that infertility in endometriosis patients may be related to alterations within the oocyte, which in turn result in embryos with decreased ability to implant.
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“Moreover, clinical studies with oocyte donation do not support a generally impeded implantation in women with endometriosis [84].”
From The pathophysiology of endometriosis and adenomyosis, tissue injury and repair (2009) · cites this paper as [84]
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The sensitivity of the DNA damage checkpoint prevents oocyte maturation in endometriosis
Hamdan, M., Jones, K. T., Cheong, Y. C., & Lane, S. I. R. (2016) · Scientific Reports · doi:10.1038/srep36994 · Cited by 57
Prapas, Y., Goudakou, M., Matalliotakis, I., Kalogeraki, A. M., Matalliotaki, C., Panagiotidis, Y., Ravanos, K., & Prapas, N. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.07.020 · Cited by 58
“In oocyte donation programmes, it has been reported that patients with endometriosis had the same chances of implantation and pregnancy as other recipients (Simon et al., 1994; Sung et al., 1997).”
BackgroundHsu, A. L., Townsend, P. M., Oehninger, S., & Castora, F. J. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.11.002 · Cited by 56
Pelvic endometriosis and natural killer cell immunity
Fukui, A., Mai, C., Saeki, S., Yamamoto, M., Takeyama, R., Kato, T., Ukita, Y., Wakimoto, Y., Yamaya, A., & Shibahara, H. (2020) · American Journal of Reproductive Immunology · doi:10.1111/aji.13342 · Cited by 55
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HOXA10 expression in ectopic endometrial tissue
Browne, H. N., & Taylor, H. S. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.10.072 · Cited by 54
Managing Endometriosis-associated Infertility
Senapati, S., & Barnhart, K. T. (2011) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3182353e06 · Cited by 54
“Specifically, in a retrospective analysis women who received embryos from endometriotic ovaries had significantly reduced implantation rates.(7) Medical Management for Endometriosis-related Infertility Medical management has been demonstrated to improve the quality of life for many patients with endometriosis.”
BackgroundMorin, M., Bellehumeur, C., Therriault, M., Metz, C. N., Maheux, R., & Akoum, A. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.10.039 · Cited by 53
Do endometriomas induce an inflammatory reaction in nearby follicles?
Opøien, H. K., Fedorcsák, P., Polec, A., Stensen, M. H., Åbyholm, T., & Tanbo, T. G. (2013) · Human Reproduction · doi:10.1093/humrep/det087 · Cited by 52
“were observed when solely the recipients had endometriosis (Simon et al., 1994).”
BackgroundIncreased ENA‐78 in the follicular fluid of patients with endometriosis
Wunder, D. M., Mueller, M. D., Birkhäuser, M., & Bersinger, N. A. (2006) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1080/00016340500501715 · Cited by 53
“Endometriosis is associated with a dysfunction of the pituitary / ovarian axis (8) and a reduced pregnancy rate per embryo after treatment by in vitro fertilization (IVF) by reduced fertilization and oocyte cleavage rates (9 /12), reduced implantation rates (9,13), and impaired quality of the embryos (9,14).”
BackgroundEndometriosis and Infertility: Is There a Cause and Effect Relationship?
Witz, C. A., & Burns, W. N. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000049418 · Cited by 51
Giorgi, V. S. I., Broi, M. G. D., de Paz, C. C. P., et al. (2015) · Reproductive Sciences · doi:10.1177/1933719115602772 · Cited by 51
“Although controversial, studies have suggested worsening of oocyte quality as one of the events responsible for the infertility related to endometriosis,(8-11) but the mechanisms leading to this impairment is unknown.(12,13) However, human oocytes are extremely rare for study, and their use in invasive studies usually…”
BackgroundDysregulation of Lysyl Oxidase Expression in Lesions and Endometrium of Women With Endometriosis
Ruiz, L. A., Báez, P., Ruiz, A., Peterse, D., Monteiro, J. B., Bracero, N. J., Beauchamp, P. J., Fazleabas, A. T., & Flores, I. (2015) · Reproductive Sciences · doi:10.1177/1933719115585144 · Cited by 49
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Oocyte Donation and Endometriosis: What Are the Lessons?
Hauzman, E. E., Pellicer, A., & García-Velasco, J. A. (2013) · Seminars in Reproductive Medicine · doi:10.1055/s-0032-1333483 · Cited by 48
Self-citationWunder, D. M., Mueller, M. D., Birkhäuser, M., & Bersinger, N. A. (2005) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-005-5149-2 · Cited by 47
“It was shown that oocytes of women with endometriosis are of inferior quality and have lower implantation rates in IVF than oocytes from women with other origins of infertility (12).”
BackgroundBoucret, L., Bouet, P., Riou, J., Legendre, G., Delbos, L., Hachem, H. E., Descamps, P., Reynier, P., & May‐Panloup, P. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9082478 · Cited by 48
“Furthermore, in oocyte donation programs, recipients without endometriosis using oocytes from donors with endometriosis had significantly lower implantation rates when compared with recipients from donors without endometriosis [48,49].”
ResultSimopoulou, M., Rapani, A., Grigoriadis, S., Pantou, A., Tsioulou, P., Maziotis, E., Tzanakaki, D., Triantafyllidou, O., Kalampokas, T., Siristatidis, C. S., et al. (2021) · Biomedicines · doi:10.3390/biomedicines9030273 · Cited by 50
“Along these lines, it was further documented that receiving oo‐ cytes originating from patients with endometriosis results in reduced implantation rate, suggesting the detrimental effect of endometriosis on oocyte and embryo quality more so than on endometrial receptivity [8].”
BackgroundImplantation Failure in Endometriosis Patients: Etiopathogenesis
Boucher, A., Brichant, G., Gridelet, V., Nisolle, M., Ravet, S., Timmermans, M., & Henry, L. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11185366 · Cited by 46
“Endometriotic patients with oocyte donation from healthy donors had the same implantation and pregnancy rate as women without endometriosis, suggesting that oocytes from affected patients may compromise fertility [10].”
BackgroundInfluentialThe Effect of Surgery for Endometriomas on Fertility
(2017) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.14834 · Cited by 49
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“However, when the results were classified by donor factors, the eggs from women with endometriosis led to a statistically significant decrease in pregnancy rate regardless of recipient status [14].”
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“Possible causes of the infertility include poor quality of oocytes and embryos [3], impaired fertilization [4,5], and impaired implantation [6], each of which can be induced by inflammation and”
BackgroundCobo, A. C., Coello, A., Santos, M. J. D. L., Gilés, J., Pellicer, A., Remohi, J. A., & García-Velasco, J. A. (2021) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2020.12.013 · Cited by 43
Self-citationHow does endometriosis affect infertility?
Navarro, J., Garrido, N., Remohi, J., Sr., & Pellicer, A. (2003) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(02)00060-8 · Cited by 41
“The authors’ studies obviate this criticism and support the observations of Simón et al [11], because recipients were allocated oocytes provided by the same donor.”
BackgroundResultInfluentialSelf-citationWu, Y., Yang, R., Lan, J., Lin, H., Jiao, X., & Zhang, Q. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.739228 · Cited by 42
“Ovarian endometrioma is one of the most common forms of EMS, present in up to 30%–40% of women with EMS (1).”
ResultInfluentialFertility Preservation in Women with Endometriosis
Rangi, S. K., Hur, C. E., Richards, E. G., & Falcone, T. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12134331 · Cited by 45
Evidence-based management of endometrioma
Gelbaya, T. A., & Nardo, L. G. (2011) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2010.11.013 · Cited by 42
Kolanska, K., Cohen, J., Bendifallah, S., Selleret, L., Antoine, J.-M., Chabbert-Buffet, N., Darai, E., & d’Argent, E.-M. (2017) · Journal of Gynecology Obstetrics and Human Reproduction · doi:10.1016/j.jogoh.2017.09.007 · Cited by 42
Chen, S.-F., Zhang, J., Huang, C., Lu, W. Z., Liang, Y., & Wan, X. (2012) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-10-34 · Cited by 41
“The combination of these factors leads to poor oocyte quality and impaired fertilization and implantation [2,3].”
BackgroundEndometriosis and Assisted Reproductive Technologies: Maximizing Outcomes
Surrey, E. S. (2013) · Seminars in Reproductive Medicine · doi:10.1055/s-0032-1333481 · Cited by 41
Vaporisation laser des endométriomes ovariens : impact sur la réponse aux gonadotrophines
Wyns, C., & Donnez, J. (2003) · Gynécologie Obstétrique & Fertilité · doi:10.1016/s1297-9589(03)00069-9 · Cited by 39
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“Our studies of in-vitro fertilization (IVF) and oocyte donation programmes (Simo´n et al., 1994) showed that the oocyte quality in endometriosis patients may be impaired, resulting in embryos of reduced ability to implant.”
BackgroundMethodInfluentialSelf-citationAn Estrogen–NK Cells Regulatory Axis in Endometriosis, Related Infertility, and Miscarriage
Yang, S., Wang, H., Li, D., & Li, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25063362 · Cited by 44
“Tolerant NK cells should possess potent cytokine secretion capabilities; however, relevant research relating to the regulatory effect of NK cells on surrounding cells is lacking, and the underlying molecular basis has yet to be revealed.”
BackgroundYland, J. J., Carvalho, L. F. P., Beste, M. T., Bailey, A. P., Thomas, C., Abrão, M. S., Racowsky, C., Griffith, L. G., & Missmer, S. A. (2019) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2019.12.005 · Cited by 37
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Kamath, M. S., Subramanian, V., Antonisamy, B., & Sunkara, S. K. (2022) · Human Reproduction Open · doi:10.1093/hropen/hoac025 · Cited by 39
“In a study by Simon et al. (1994), the treatment outcomes following oocyte donation according to origin of the oocyte (n¼ 141) was evaluated.”
BackgroundResultInfluentialDonabela, F. C., Meola, J., Padovan, C. C., et al. (2015) · Reproductive Sciences · doi:10.1177/1933719115585146 · Cited by 35
The Role of Fertility Preservation in Women with Endometriosis: A Systematic Review
Lantsberg, D., Fernando, S., Cohen, Y., & Rombauts, L. J. F. (2019) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2019.09.780 · Cited by 35
Xu, H., Schultze-Mosgau, A., Agic, A., Diedrich, K., Taylor, R. N., & Hornung, D. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.05.043 · Cited by 37
Secretion of inhibin B during ovarian stimulation is decreased in infertile women with endometriosis
Dokras, A., Habana, A. E., Giraldo, J. L., & Jones, E. E. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)00568-9 · Cited by 35
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“(37) compared oocyte donors who had endometriosis with recipients who had endometriosis and found reduced pregnancy and implantation rates when the oocytes came from donors with endometriosis, but normal rates when only the recipients had endometriosis.”
BackgroundÇelik, Ö., Çelik, E., Türkçüoğlu, İ., Yılmaz, E., Ulaş, M., Şimşek, Y., Karaer, A., Çelik, N., Aydın, N. E., Özerol, İ. H., et al. (2012) · Reproductive Sciences · doi:10.1177/1933719112466307 · Cited by 34
PTGS2 down-regulation in cumulus cells of infertile women with endometriosis
da Luz, C. M., Broi, M. G. D., Donabela, F. C., de Paz, C. C. P., Meola, J., & Navarro, P. A. (2017) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2017.06.021 · Cited by 34
“…in these women, and some studies suggest a significant role of oocyte quality in this condition (Andrade et al., 2010; Barcelos et al., 2009, 2015; Da Broi and Navarro, 2016; Da Broi et al., 2014; Donabela et al., 2015; 2016; Garcia-Velasco and Arici, 1999; Simon et al., 1994; Sung et al., 1997).”
BackgroundMurta, M., Machado, R. C., Zegers-Hochschild, F., Checa, M. Á., Sampaio, M., & Geber, S. (2018) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-018-1214-5 · Cited by 33
Implantation markers and endometriosis
Bulletti, C., Flamigni, C., & de Ziegler, D. (2005) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61142-x · Cited by 31
Endometriosis, Oocyte, and Embryo Quality
Latif, S., & Sarıdoğan, E. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12134186 · Cited by 33
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Relatively poor oocyte quality is an indication for intracytoplasmic sperm injection
Saito, H., Saito, T., Kaneko-Tarui, T., et al. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00547-6 · Cited by 31
Endometriosis and assisted reproductive technologies: are outcomes affected?
MAHUTTE, N. G., & Arici, A. M. (2001) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-200106000-00005 · Cited by 30
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Choi, Y. S., Park, J. H., Lee, J. H., Yoon, J., Yun, B. H., Park, J. H., Seo, S. K., Sung, H., Kim, H. S., Cho, S., et al. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00772 · Cited by 29
“Studies from oocyte donation–in vitro fertilization and embryo transfer, which may exclude the impact of endometrial receptivity, suggest that subfertility in endometriosis is attributed to quality of oocytes rather than endometrial receptivity (4).”
BackgroundSukhikh, G. T., Adamyan, L. V., Олеговна, Д. С., Baranov, I. I., Bezhenar, V. F., Kozachenko, A. V., Radzinsky, V. E., Orazov, M. R., Yarmolinskaya, M. I., & Olofsson, J. I. (2021) · Fertility and Sterility · doi:10.1016/j.fertnstert.2021.07.1194 · Cited by 32
Down-regulation of the CYP19A1 gene in cumulus cells of infertile women with endometriosis
Barcelos, I. D. E. S., Donabela, F. C., Ribas, C. P., Meola, J., Ferriani, R. A., de Paz, C. C. P., & Navarro, P. A. (2015) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2015.01.012 · Cited by 30
“in part, to lower oocyte quality (Díaz et al., 2000; Simón et al., 1994).”
BackgroundÖzcan, C., Özdamar, Ö., Gökbayrak, M. E., Döğer, E., Çakıroğlu, Y., & Çine, N. (2018) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2018.11.027 · Cited by 30
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“Several lines of evidence suggest that infertility associated with endometriosis, even minimal-to-mild disease, may be related to decreased oocyte quality [20,38,42,43].”
BackgroundResultEndometriosis and infertility: The debate continues
Trinder, J., & Cahill, D. J. (2002) · Human Fertility · doi:10.1080/1464727022000199871 · Cited by 28
Impact of assisted hatching on ART outcome in women with endometriosis
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“Normal endometrial receptivity has been reported in women with moderate to severe endometriosis who received donor oocytes from women without endometriosis (Simon et al., 1994; Sung et al., 1997; Garcia-Velasco and Arici, 1999; Garrido et al., 2000, 2002).”
BackgroundResultInfluentialAlkudmani, B., Gat, I., Buell, D., Salman, J., Zohni, K., Librach, C., & Sharma, P. (2018) · Journal of minimally invasive gynecology · doi:10.1016/j.jmig.2017.08.641 · Cited by 25
Garrido, N., Albert, C., Krüssel, J.-S., O’Connor, J., Remohi, J. A., Simón, C., & Pellicer, A. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01961-6 · Cited by 27
“those with tubal infertility (2), whereas the”
Self-citationCahill, D. J. (2002) · Human Reproduction · doi:10.1093/humrep/17.5.1135 · Cited by 25
“…minor) compared with controls (tubal and/or unexplained infertility) Gonadotrophin-stimulated cycles Yovich et al., 1988 110 9 (8) 116 1 (1) Simon et al., 1994 329 44 (13) 275 16 (6) Geber et al., 1995 a – – (23) – – (22) Arici et al., 1996 531 43 (8) 180 5 (3) 0.013 Hull et al., 1998 2328…”
InfluentialLive Birth After Oocyte Donation In Vitro Fertilization Cycles in Women With Endometriosis
Paffoni, A., Casalechi, M., de Ziegler, D., Cicinelli, E., Somigliana, E., Viganò, P., & Vitagliano, A. (2024) · JAMA Network Open · doi:10.1001/jamanetworkopen.2023.54249 · Cited by 31
Lü, X., Wu, Y. R., Gao, X., Wang, Y., Wang, L., & Sun, X. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.03.055 · Cited by 26
Endometriosis and Assisted Reproductive Technologies
Dokras, A., & Olive, D. L. (1999) · Clinical Obstetrics & Gynecology · doi:10.1097/00003081-199909000-00020 · Cited by 26
Management of endometriosis-associated infertility
Surrey, E. S., & Schoolcraft, W. B. (2003) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(02)00061-x · Cited by 26
Kligman, I., GRIFO, J. A., & Witkin, S. S. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019200 · Cited by 26
Characterizing the endometrial fluid cytokine profile in women with endometriosis
Llarena, N. C., Richards, E. G., Priyadarshini, A., Fletcher, D., Bonfield, T. L., & Flyckt, R. L. (2020) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-020-01989-y · Cited by 25
“Additionally, data from infertility patients shows that the endometrial cytokine profile is altered by ovarian stimulation for IVF [37], suggesting the potential for modulation of the endometrial environment through medical or surgical treatment of endometriosis.”
BackgroundLong-term use of gonadotropin-releasing hormone analogues before IVF in women with endometriosis
Tavmergen, E., Ulukuş, M., & Göker, E. N. T. (2007) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e3281053a52 · Cited by 21
Tabatabaei, F., Tahernia, H., Ghaedi, A., Bazrgar, A., & Khanzadeh, S. (2023) · BMC Women s Health · doi:10.1186/s12905-023-02692-7 · Cited by 26
“Research on oocyte donation indicates a negative impact on oocytes rather than endometrial receptivity [51].”
BackgroundOmland, A. K., Bjercke, S., Ertzeid, G., et al. (2006) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-006-9060-2 · Cited by 24
Carvalho, L. F. P., Rossener, R., Azeem, A., Malvezzi, H., Abrão, M. S., & Agarwal, A. K. (2013) · PubMed · Cited by 25
The Endometrioma Treatment Paradigm when Fertility Is Desired: A Systematic Review
Miller, C. E. (2020) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2020.11.020 · Cited by 23
Assisted reproductive technology for women with endometriosis, a clinically oriented review
Ata, B., & Telek, S. B. (2021) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000710 · Cited by 24
“Although early studies using oocyte donation model [2] suggested that oocytes can be affected rather than endometrial receptivity, more recent observations yielded contradictory results.”
ResultCould surgical management improve the IVF outcomes in infertile women with endometrioma?: a review
Park, H. J., Kim, H. H., Lee, G. H., Yoon, T. K., & Lee, W. S. (2019) · Obstetrics & Gynecology Science · doi:10.5468/ogs.2019.62.1.1 · Cited by 23
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Yamashita, Y., Ueda, M., Takehara, M., Yamashita, H., Suzuki, Y., Hung, Y., Terai, Y., & Ueki, M. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03339-3 · Cited by 22
Polymorphic variants of CYP 17 and CYP 19A and risk of infertility in endometriosis
Szczepańska, M., Wirstlein, P. K., Skrzypczak, J., & Jagodziński, P. P. (2013) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.12210 · Cited by 21
“women with endometriosis due to a disturbance in folliculogenesis, decreased fertilization, implantation defects, and poor oocyte quality with decreased blastocyst implantation ability (25,26).”
BackgroundJianini, B. T. G. M., Giorgi, V. S. I., Broi, M. G. D., de Paz, C. C. P., Silva, J. C. R. E., Ferriani, R. A., & Navarro, P. A. (2017) · Reproductive Sciences · doi:10.1177/1933719116687658 · Cited by 22
Neto, M. A. C., Martins, W. P., da Luz, C. M., Jianini, B. T. G. M., Ferriani, R. A., & Navarro, P. A. (2016) · Revista Brasileira Ginecologia e Obstetrícia · doi:10.1055/s-0036-1584126 · Cited by 20
Caccavo, D., Pellegrino, N. M., Totaro, I., Vacca, M. P., Selvaggi, L. E., & Depalo, R. (2011) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463201102400221 · Cited by 20
“Concerning the relationship between oocyte quality and endometriosis-associated infertility, alterations within oocyte, resulting in embryos with decreased ability to implant has been suggested as a possible cause of reproductive failure (23).”
BackgroundThe relevance of the peritoneal fluid in endometriosis-associated infertility
Mülayim, N., & Arici, A. M. (1999) · Human Reproduction · doi:10.1093/humrep/14.suppl_2.67 · Cited by 20
“…the oocytes of endometriosis patients (Wardle et al., 1985, 1986), more recent studies have found that endometriosis has no effect on oocyte quality, fertilization, and pregnancy rates in patients undergoing assisted reproduction (Braeckmans et al., 1987; Simon et al., 1994; Arici et al., 1996a).”
BackgroundInfluentialDaniilidis, A., Balaouras, D., Chitzios, D., et al. (2017) · Journal of Obstetrics and Gynaecology · doi:10.1080/01443615.2017.1287685 · Cited by 19
“…tubal factor infertility Several studies have indicated that embryo quality and implantation rate were decreased in infertile women with endometriosis undergoing IVF, however, endometrial receptivity appeared not to be affected (Simon et al. 1994; Garcia-Velasco et al. 2001; Garrido et al. 2002).”
BackgroundOocyte Cryopreservation in Patients with Endometriosis: Current Knowledge and Number Needed to Treat
Henry, L., Vervier, J., Boucher, A., Brichant, G., Gaspard, O., Labied, S., Munaut, C., Ravet, S., & Nisolle, M. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11154559 · Cited by 20
Mao, J., Zhang, J., Cai, L., et al. (2022) · Molecular Human Reproduction · doi:10.1093/molehr/gaac018 · Cited by 18
Embryo quality before and after surgical treatment of endometriosis in infertile patients
Shahine, L. K., Burney, R. O., Behr, B. R., Milki, A. A., Westphal, L. M., & Lathi, R. B. (2009) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-008-9287-1 · Cited by 18
“Though lower implantation rates in the setting of endometriosis have been reported in multiple clinical studies [13, 14], the relative contribution of embryo quality and endometrial receptivity to this finding can be debated.”
BackgroundTan, J., Cerrillo, M., Cruz, M., Cecchino, G. N., & García-Velasco, J. A. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10020344 · Cited by 19
“Indeed, [25] observed that women with endometriosis who received donor oocytes achieved similar pregnancy outcomes compared to women with other causes of infertility, while donor recipients who received oocytes from women with endometriosis experienced significantly lower implantation rates (p < 0.”
ResultCampos, C. S., Vaamonde, D., Andreoli, C., Martins, A. C., Genro, V. K., de Souza, C. A. B., Chapon, R. D. C. B., & Cunha‐Filho, J. S. (2010) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2010.05.007 · Cited by 18
“Studies on oocyte donation have demonstrated that embryos from patients with endometriosis had lower implantation rates (Simon et al., 1994).”
BackgroundZhou, L., Wang, Y., & Kuang, Y. (2020) · Drug Design Development and Therapy · doi:10.2147/dddt.s263138 · Cited by 18
Xiao, L. Y., Pei, T., Huang, W., Zhou, M., Fu, J., Tan, J., Liu, T., Song, Y., & Yang, S. (2020) · PLoS ONE · doi:10.1371/journal.pone.0234086 · Cited by 17
da Luz, C. M., Broi, M. G. D., Koopman, L. D. O., Plaça, J. R., Silva, W. A., Ferriani, R. A., Meola, J., & Navarro, P. A. (2022) · Scientific Reports · doi:10.1038/s41598-022-09386-4 · Cited by 16
Diagnosis and treatment of endometriosis
Frackiewicz, E. J., & Zarotsky, V. (2003) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.4.1.67 · Cited by 18
Endometriosis and In Vitro Fertilization
Latif, S., Khanjani, S., & Sarıdoğan, E. (2024) · Medicina · doi:10.3390/medicina60081358 · Cited by 22
Hox Genes in Adult Tissues and Their Role in Endothelial Cell Differentiation and Angiogenesis
Nova‐Lamperti, E., Aguilera, V., Oporto, K., Guzman, P. C. C., Ormazábal, V., Zuñiga, F. A., Escudero, C., & Aguayo, C. R. (2018) · InTech eBooks · doi:10.5772/intechopen.76745 · Cited by 16
The gene expression profile of cumulus cells reveals altered pathways in patients with endometriosis
Allegra, A., Raimondo, S., Volpes, A., Fanale, D., Marino, A. A., Cicero, G., Leo, G. D., Sammartano, F., Allegra, G., & Alessandro, R. (2014) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-014-0305-1 · Cited by 15
“On the contrary, the oocytes retrieved by donors with endometriosis led to a statistically significant decrease in pregnancy rates in recipients, thereby demonstrating a direct effect of endometriosis on oocyte and embryo quality rather than on endometrial receptivity [7].”
BackgroundLaparoscopic Treatment of Endometrioma-Associated Infertility and Pregnancy Outcome
Takuma, N., Sengoku, K., Pan, B., Wada, K., Yamauchi, T., Miyamoto, T., Ohsumi, D., & Ishikawa, M. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000066292 · Cited by 15
The Effect of Surgery on Endometriomas on Fertility (2025 Second Edition)
Supramaniam, P. R., Mittal, M., Becker, C. M., & Jayaprakasan, K. (2025) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.18221 · Cited by 14
“Nevertheless, the European Society of Human Reproduction and Embryology (ESHRE) guideline for the management of endometriosis [29], published 20 years after Simón et al. [52], has not identified such differences.”
Metadata
- Authors
- Simón, C., Gutiérrez, A., Vidal, A., de los Santos, M. J., Tarín, J. J., Remohí, J., & Pellicer, A.
- Affiliations
- Universitat de València (ES)
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 1994-04
- Volume
- 9
- Issue
- 4
- Pages
- 725-729
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2151618269
- Cited by
- 374
- References
- 0
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 14 · 2023: 18 · 2022: 12 · 2021: 14 · 2020: 14 · 2019: 17 · 2018: 11 · 2017: 18 · 2016: 12 · 2015: 14 · 2014: 13 · 2013: 14 · 2012: 19
- FWCI
- 7.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Health and Technologies
- Keywords
- endometriosis, endometriosis-associated infertility, IVF outcomes, oocyte donation, tubal infertility, implantation rate, oocyte quality
- MeSH terms
- Adult, Embryo Transfer, Endometriosis, Female, Fertilization in Vitro, Humans, Infertility, Female, Oocytes, Embryo Implantation, Pregnancy, Retrospective Studies, Tissue Donors
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