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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Clinical studies with oocyte donation do not support a generally impeded implantation in women with endometriosis.
“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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Zondervan, K. T., Becker, C. M., Koga, K., Missmer, S. A., Taylor, R. N., & Viganò, P. (2018) · Nature Reviews Disease Primers · doi:10.1038/s41572-018-0008-5 · Cited by 1,257 · see citing works
Effect of endometriosis on in vitro fertilization
Barnhart, K. T., Dunsmoor-Su, R. F., & Coutifaris, C. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03112-6 · Cited by 798 · see citing works
Factors that affect outcome of in-vitro fertilisation treatment
Templeton, A. A., Morris, J. K., & Parslow, W. (1996) · The Lancet · doi:10.1016/s0140-6736(96)05291-9 · Cited by 709 · see citing works
Pathogenic mechanisms in endometriosis-associated infertility
Gupta, S., Goldberg, J. M., Aziz, N., Goldberg, E., Krajcir, N., & Agarwal, A. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.02.093 · Cited by 409 · see citing works
“Endometriosis and infertility oocyte donors with endometriosis establish pregnancies at lower rates than normal donors (83, 89).”
BackgroundThe pathophysiology of endometriosis and adenomyosis, tissue injury and repair
Leyendecker, G., Wildt, L., & Mall, G. (2009) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-009-1191-0 · Cited by 418 · see citing works
“Moreover, clinical studies with oocyte donation do not support a generally impeded implantation in women with endometriosis [84].”
BackgroundImplantation failure: molecular mechanisms and clinical treatment
Çakmak, H., & Taylor, H. S. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmq037 · Cited by 396 · see citing works
“In women with endometriosis, donor oocytes obtained from women without the disease implant as efficiently as in other recipients (Simon et al., 1994).”
BackgroundResultHorton, J., Sterrenburg, M. D., Lane, S. I. R., Maheshwari, A., Li, T. C., & Cheong, Y. C. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz012 · Cited by 387 · see citing works
Kunz, G., Beil, D., Huppert, P., Noe, M., Kissler, S., & Leyendecker, G. (2005) · Human Reproduction · doi:10.1093/humrep/dei021 · Cited by 377 · see citing works
“A number of studies demonstrated a diminished ovarian reserve, an impaired granulosa cell–oocyte environment and impaired oocyte quality and fertilization rates in patients with endometriosis (Simon et al., 1994; Hull et al., 1998; Pal et al., 1998; Azem et al., 1999).”
BackgroundInfluentialHOX gene expression is altered in the endometrium of women with endometriosis
Taylor, H. S. (1999) · Human Reproduction · doi:10.1093/humrep/14.5.1328 · Cited by 372 · see citing works
“Reports from several in-vitro fertilization (IVF)/ embryo transfer programmes indicate patients with endometriosis have decreased implantation rates (Hahn et al., 1986; Simón et al., 1994; Arici et al., 1996).”
BackgroundLong-term pituitary down-regulation before in vitro fertilization (IVF) for women with endometriosis
Sallam, H. N., Garcia-Velasco, J. A., Dias, S., Arici, A., Abou-Setta, A. M., & Jaafar, S. H. (2006) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd004635.pub2 · Cited by 349 · see citing works
Endometriosis-associated infertility: From pathophysiology to tailored treatment
Bonavina, G., & Taylor, H. S. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1020827 · Cited by 359 · see citing works
Lessey, B. A., & Kim, J. J. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.05.031 · Cited by 286 · see citing works
“While early studies on donor oocytes has suggested the primary defect associated with endometriosis may reside in the ovary and oocyte quality (29), larger and more recent studies have documented that defective implantation is also likely involved (30).”
Bazot, M., Fiori, O., & Daraï, É. (2006) · Human Reproduction · doi:10.1093/humrep/dei448 · Cited by 282 · see citing works
The effect of endometriosis on in vitro fertilisation outcome: a systematic review and meta‐analysis
Harb, H., Gallos, I. D., Chu, J., HARB, M. D. D. Y. M. H., & Coomarasamy, A. (2013) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.12366 · Cited by 261 · see citing works
Structural and molecular features of the endomyometrium in endometriosis and adenomyosis
Benagiano, G., Brosens, I., & Habiba, M. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmt052 · Cited by 246 · see citing works
“For instance, Simon et al. (1994) compared the outcome of IVF in 78 women with tubal infertility and patients with endometriosis and found a statistically significant reduced pregnancy rate per cycle and per transfer and a reduced implantation rate.”
ResultIs the oocyte quality affected by endometriosis? A review of the literature
Sanchez, A. M., Vanni, V. S., Bartiromo, L., Papaleo, E., Zilberberg, E., Candiani, M., Orvieto, R., & Viganò, P. (2017) · Journal of Ovarian Research · doi:10.1186/s13048-017-0341-4 · Cited by 257 · see citing works
“One of the first studies that tried to gain clinical knowledge of the factors involved in the aetiology of the endometriosis-associated infertility was the study by Simon and colleagues [76].”
BackgroundBerkkanoğlu, M., & Arici, A. M. (2003) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2003.00042.x · Cited by 240 · see citing works
Impact of stage iii–iv endometriosis on recipients of sibling oocytes: matched case-control study
Dı́az, I., Dı́az, I., Navarro, J., Blasco, L., Simón, C., Pellicer, A., & Remohi, J., Sr. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)00570-7 · Cited by 220 · see citing works
Self-citationArici, A. M., Oral, E., Bükülmez, O., Dulęba, A. J., Olive, D. L., & Jones, E. E. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58162-x · Cited by 219 · see citing works
Garcia-Velasco, J. A., Mahutte, N. G., Corona, J., Zúñiga, V., Gilés, J., Arici, A., & Pellicer, A. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.04.006 · Cited by 214 · see citing works
Self-citationZanatta, A., da Rocha, A. M., Carvalho, F. M., Pereira, R., Taylor, H. S., Motta, E. L. A., Baracat, E. C., & Serafini, P. C. (2010) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-010-9471-y · Cited by 206 · see citing works
“Several studies have suggested an impairment of implantation in patients with endometriosis, but the mechanisms underlying it are not well understood [16–18].”
BackgroundPellicer, A., Albert, C., Mercader, A., Bonilla-Musoles, F. M., Remohi, J., Sr., & Simón, C. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00204-0 · Cited by 192 · see citing works
“The patients were divided into two groups according to the laparoscopic findings: [1] the control group was composed of 7 patients who underwent laparoscopy on day 11.”
BackgroundSelf-citationOrisaka, M., Mizutani, T., Miyazaki, Y., Shirafuji, A., Tamamura, C., Fujita, M., Tsuyoshi, H., & Yoshida, Y. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1324429 · Cited by 215 · see citing works
Follicular hormonal environment and embryo quality in women with endometriosis
Garrido, N. (2000) · Human Reproduction Update · doi:10.1093/humupd/6.1.67 · Cited by 186 · see citing works
“We retrospectively analysed the results of our oocyte donation programme (Simón et al., 1994).”
BackgroundMethodResultInfluentialLin, Y.-H., Chen, Y.-H., Chang, H.-Y., Au, H., Tzeng, C., & Huang, Y. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082385 · Cited by 187 · see citing works
Implications of immune dysfunction on endometriosis associated infertility
Miller, J., Ahn, S., Monsanto, S. P., Khalaj, K., Koti, M., & Tayade, C. (2016) · OncoTarget · doi:10.18632/oncotarget.12577 · Cited by 157 · see citing works
“They also find that healthy ovum donation to endometriosis patients produces the same rate of implantation and pregnancy compared to controls [62-64].”
BackgroundResultPeter, A. W., Adamson, G. D., Al‐Jefout, M., Becker, C. M., D’Hooghe, T. M., Dunselman, G. A. J., Fazleabas, A. T., Giudice, L. C., Horne, A. W., Hull, M. L., et al. (2016) · Reproductive Sciences · doi:10.1177/1933719116654991 · Cited by 188 · see citing works
Senapati, S., Sammel, M. D., Morse, C. B., & Barnhart, K. T. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.03.037 · Cited by 179 · see citing works
“0003) compared with tubal factor infertility (11).”
The Role of Endometrium in Endometriosis
Ulukuş, M., Çakmak, H., & Arici, A. M. (2006) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2006.07.005 · Cited by 171 · see citing works
Seino, T., Saito, H., Kaneko-Tarui, T., Takahashi, T., Kawachiya, S., & Kurachi, H. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03103-5 · Cited by 167 · see citing works
The endometrium versus embryonic quality in endometriosis-related infertility
Garrido, N. (2002) · Human Reproduction Update · doi:10.1093/humupd/8.1.95 · Cited by 166 · see citing works
Epithelial-to-mesenchymal transition in the development of endometriosis
Yang, Y., & Yang, W. (2017) · Oncotarget · doi:10.18632/oncotarget.16472 · Cited by 167 · see citing works
“Besides, significantly reduced implantation rates are shown in women who received embryos from endometriotic ovaries [82].”
BackgroundEndometriosis and Inflammation in Infertility
Halis, G., & Arici, A. M. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1335.032 · Cited by 163 · see citing works
Influence of Endometriosis on Assisted Reproductive Technology Outcomes
Hamdan, M., Omar, S. Z., Dunselman, G. A. J., & Cheong, Y. C. (2014) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000000592 · Cited by 168 · see citing works
Does ovarian surgery for endometriomas impair the ovarian response to gonadotropin?
Donnez, J., Wyns, C., & Nisolle, M. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)02011-8 · Cited by 162 · see citing works
In vitro fertilization is a successful treatment in endometriosis-associated infertility
Opøien, H. K., Fedorcsák, P., Omland, A. K., Åbyholm, T., Bjercke, S., Ertzeid, G., Oldereid, N. B., Mellembakken, J. R., & Tanbo, T. G. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.01.112 · Cited by 154 · see citing works
Engmann, L., Sladkevicius, P., Agrawal, R., Bekir, J. S., Campbell, S. C., & Tan, S. L. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00406-3 · Cited by 156 · see citing works
Cellular and molecular basis for endometriosis-associated infertility
Stilley, J. A. W., Birt, J. A., & Sharpe-Timms, K. L. (2012) · Cell and Tissue Research · doi:10.1007/s00441-011-1309-0 · Cited by 151 · see citing works
“Women with endometriosis are reported to experience implantation failure more often than controls (Arici et al. 1996; Cahill and Hull 2000; Simon et al. 1994).”
BackgroundSzczepańska, M., Wirstlein, P. K., Skrzypczak, J., & Jagodziński, P. P. (2012) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-10-1 · Cited by 150 · see citing works
“It has been suggested that endometriosis-associated infertility may be due to disorders of folliculogenesis, decreased fertilization, defective implantation, and reduced oocyte quality with low capacity of blastocyst implantation [6,7].”
BackgroundImpact of ovarian endometrioma on assisted reproduction outcomes
Gupta, S., Agarwal, A. K., Agarwal, R., & de Mola, J. R. L. (2006) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61439-3 · Cited by 148 · see citing works
A new concept of endometriosis and adenomyosis, tissue injury and repair (TIAR)
Leyendecker, G., & Wildt, L. (2011) · hmbci · doi:10.1515/hmbci.2011.002 · Cited by 147 · see citing works
Impact of ovarian endometrioma on oocytes and pregnancy outcome in in vitro fertilization
Suzuki, T., Izumi, S., Matsubayashi, H., Awaji, H., Yoshikata, K., & Makino, T. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.11.028 · Cited by 138 · see citing works
Effect of age on sperm fertility potential: oocyte donation as a model
Gallardo, E., Simón, C., Levy, M., Guanes, P. P., Remohi, J. A., & Pellicer, A. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58450-7 · Cited by 136 · see citing works
Self-citationTubal transport of gametes and embryos: a review of physiology and pathophysiology
Ezzati, M., Djahanbakhch, O., Arian, S. E., et al. (2014) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-014-0309-x · Cited by 131 · see citing works
“At a clinical level, this hypothesis is further supported by studies demonstrating a decreased pregnancy rates when IVF-ET treatment is performed using donated oocytes obtained from women with endometriosis as compared to when oocyte donors did not have endometriosis [90].”
ResultGoud, P. T., Goud, A. P., Joshi, N., Puscheck, E. E., Diamond, M. P., & Abu‐Soud, H. M. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.03.053 · Cited by 129 · see citing works
Oocyte vitrification for fertility preservation in women with endometriosis: an observational study
Cobo, A., Giles, J., Paolelli, S., Pellicer, A., Remohí, J., & García-Velasco, J. A. (2020) · Fertility and Sterility · doi:10.1016/j.fertnstert.2019.11.017 · Cited by 127 · see citing works
Self-citationOpøien, H. K., Fedorcsak, P., Åbyholm, T., & Tanbo, T. (2011) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2011.06.002 · Cited by 120 · see citing works
“Oocytes donated by women with endometriosis lead to decreased pregnancy rates regardless of recipient status (Simon et al., 1994), indicative of a potential unfavourable effect in oocyte development, but that conclusion should be viewed in the light of small sample size mostly limited to a group of patients with ASRM…”
BackgroundVitale, S. G., Capriglione, S., Peterlunger, I., Rosa, V. L. L., Vitagliano, A., Noventa, M., Valenti, G., Sapia, F., Angioli, R., Lopez, S., et al. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/7924021 · Cited by 121 · see citing works
“, in a retrospective study, observed a significantly lower implantation rate (IR) in recipients without endometriosis who received egg from women with endometriosis [64].”
BackgroundCano, F., Simón, C., Remohí, J., & Pellicer, A. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57797-8 · Cited by 118 · see citing works
Self-citationCarlberg, M., Nejaty, J., Fröysa, B., Guan, Y.-M., Söder, O., & Bergqvist, A. (2000) · Human Reproduction · doi:10.1093/humrep/15.6.1250 · Cited by 132 · see citing works
Pregnancy and birth rates after oocyte donation
Remohi, J. A., Gartner, B., Gallardo, E., et al. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81372-6 · Cited by 117 · see citing works
Self-citationEutopic endometrium in women with endometriosis: ground zero for the study of implantation defects
Lessey, B., Lebovic, D., & Taylor, R. (2013) · Seminars in Reproductive Medicine · doi:10.1055/s-0032-1333476 · Cited by 113 · see citing works
Toya, M., Saito, H., Ohta, N., Saito, T., Kaneko-Tarui, T., & Hiroi, M. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00507-5 · Cited by 115 · see citing works
Barbosa, M. A. P., Teixeira, D. M., Navarro, P. A., Ferriani, R. A., Nastri, C. O., & Martins, W. P. (2014) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.13366 · Cited by 115 · see citing works
Angiogenesis and Macrophage Activation in Endometriosis
TAYLOR, R. N., RYAN, S. P., MOORE, E. S., HORNUNG, D., SHIFREN, J. L., & TSENG, J. F. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48540.x · Cited by 113 · see citing works
Georgiou, E. X., Melo, P., Baker, P. E., Sallam, H. N., Arici, A., Garcia-Velasco, J. A., Abou-Setta, A. M., Becker, C., & Granne, I. E. (2019) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd013240.pub2 · Cited by 113 · see citing works
Endometriosis, recurrent miscarriage and implantation failure: is there an immunological link?
Tomassetti, C., Meuleman, C., Pexsters, A., Mihalyi, A., Kyama, C., Simsa, P., & D'Hooghe, T. (2006) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)62016-0 · Cited by 106 · see citing works
Cakmak, H., & Taylor, H. (2010) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1242996 · Cited by 105 · see citing works
Matalliotakis, I., Çakmak, H., MAHUTTE, N. G., Fragouli, Y. G., Arici, A. M., & Sakkas, D. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.01.037 · Cited by 103 · see citing works
Broi, M. D. D., & Navarro, P. (2016) · Cell and Tissue Research · doi:10.1007/s00441-015-2339-9 · Cited by 94 · see citing works
“In a retrospective study, Simon et al. (1994) assessed outcomes of ovodonation cycles and observed similar implantation and pregnancy rates in women who presented with and without endometriosis and who received oocytes from donors without the disease.”
BackgroundUrman, B., Yakın, K., & Balaban, B. (2005) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60846-2 · Cited by 101 · see citing works
“former group (Simon et al., 1994).”
BackgroundAzem, F., Lessing, J. B., Geva, E., Shahar, A., Lerner‐Geva, L., Yovel, I., & Amit, A. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00392-1 · Cited by 100 · see citing works
Ferrero, H., Corachán, A., Aguilar, A., Quiñonero, A., Carbajo‐García, M. C., Alamá, P., Tejera, A., Taboas, E., Muñoz, E., Pellicer, A., et al. (2019) · Human Reproduction · doi:10.1093/humrep/dez053 · Cited by 100 · see citing works
“patients who receive embryos derived from endometriotic ovaries had a significantly reduced implantation rate, indicating reduced quality of oocytes produced by affected ovaries (Simón et al., 1994).”
BackgroundSelf-citationSubfertility: causes, treatment and outcome
Adamson, G. D., & Baker, V. L. (2003) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/s1521-6934(02)00146-3 · Cited by 100 · see citing works
Pituitary-ovarian dysfunction and endometriosis
Cahill, D. J. (2000) · Human Reproduction Update · doi:10.1093/humupd/6.1.56 · Cited by 98 · see citing works
Endometriosis is not detrimental to embryo implantation in oocyte recipients
Sung, L., Mukherjee, T., Takeshige, T., Bustillo, M., & Copperman, A. B. (1997) · Journal of Assisted Reproduction and Genetics · doi:10.1007/bf02766132 · Cited by 98 · see citing works
Hull, M. G. R., Williams, J. A., Ray, B. D., McLaughlin, E. A., Akande, V. A., & Ford, W. C. (1998) · Human Reproduction · doi:10.1093/humrep/13.7.1825 · Cited by 97 · see citing works
Leyendecker, G., Kunz, G., Kissler, S., & Wildt, L. (2006) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2006.01.008 · Cited by 94 · see citing works
Implications of Sperm Chromosome Abnormalities in Recurrent Miscarriage
Rubio, C., Simón, C., Blanco, J., Vidal, F., Mı́nguez, Y., Egozcue, J., Crespo, J., Remohi, J., Sr., & Pellicer, A. (1999) · Journal of Assisted Reproduction and Genetics · doi:10.1023/a:1020315529090 · Cited by 94 · see citing works
“Protocols for oocyte donation and in vitro fertilization were carried out as described previously (20,21).”
MethodSelf-citationImpact of Varying Stages of Endometriosis on the Outcome of In Vitro Fertilization–Embryo Transfer
Pal, L., Shifren, J. L., Isaacson, K., Chang, Y., Leykin, L., & Toth, T. L. (1998) · Journal of Assisted Reproduction and Genetics · doi:10.1023/a:1022574221115 · Cited by 95 · see citing works
“The exists limited data suggesting impaired implantation in patients with endometriosis, regardless of the severity of the disease (3,10).”
BackgroundMáté, G., Bernstein, L. R., & Török, Á. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00725 · Cited by 93 · see citing works
“reported that donor egg recipients with endometriosis receiving eggs from fertile donors had the same rates of implantation and pregnancy as recipients without endometriosis (37).”
BackgroundFISH Preimplantation Diagnosis of Chromosome Aneuploidy in Recurrent Pregnancy Wastage
Vidal, F., Giménez-Rodríguez, C., Rubio, C., et al. (1998) · Journal of Assisted Reproduction and Genetics · doi:10.1023/a:1022552713015 · Cited by 92 · see citing works
“based on the elimination of some of the risk factors, has been reported to improve pregnancy rates (3,4).”
BackgroundSelf-citationBudak, E., Garrido, N., Soares, S. R., de Melo, M. A. B., Meseguer, M., Pellicer, A., & Remohi, J. A. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.11.118 · Cited by 90 · see citing works
Self-citationOmland, A. K., Åbyholm, T., Fedorcsák, P., Ertzeid, G., Oldereid, N. B., Bjercke, S., & Tanbo, T. G. (2005) · Human Reproduction · doi:10.1093/humrep/deh664 · Cited by 91 · see citing works
“Indeed, previous studies have shown that embryo quality and implantation rate are reduced in infertile women with endometriosis undergoing IVF, whereas endometrial receptivity seems to be unaffected (Simón et al., 1994; Garcia-Velasco et al., 2001; Garrido et al., 2002).”
BackgroundOutcome of IVF in Patients with Endometriosis in Comparison with Tubal-Factor Infertility
Bergendal, A., Naffah, S., Nagy, C., Bergqvist, A., Sjöblom, P., & Hillensjø, T. (1998) · Journal of Assisted Reproduction and Genetics · doi:10.1023/a:1022526002421 · Cited by 86 · see citing works
“compared with oocytes donated from women without endometriosis (30).”
Brizek, C. L., Schlaff, S., Pellegrini, V. A., Frank, J. B., & Worrilow, K. C. (1995) · Journal of Assisted Reproduction and Genetics · doi:10.1007/bf02211378 · Cited by 86 · see citing works
Endometrial Quality in Infertile Women with Endometriosis
Pellicer, A., NAVARRO, J., Bosch, E., Garrido, N., García-Velasco, J. A., Remohi, J. A., & Simón, C. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb03796.x · Cited by 83 · see citing works
Self-citationEndometrial Receptivity Analysis (ERA): data versus opinions
Ruíz-Alonso, M., Valbuena, D., Gómez, C., Cuzzi, J., & Simón, C. (2021) · Human Reproduction Open · doi:10.1093/hropen/hoab011 · Cited by 82 · see citing works
Self-citationAn evidence-based evaluation of endometriosis-associated infertility
Pritts, E. A., & Taylor, R. N. (2003) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(03)00045-8 · Cited by 82 · see citing works
“Some investigators found that embryos derived from oocytes of women with endometriosis had a lower likelihood of implantation when transferred to women with or without endometriosis [62].”
BackgroundLong oestradiol replacement in an oocyte donation programme
Remohi, J. A., Gutierrez, A. M., Cano, F., et al. (1995) · Human Reproduction · doi:10.1093/humrep/10.6.1387 · Cited by 80 · see citing works
“Furthermore, we recently described the low performance of embryos derived from ovaries with endometriosis (Simon et al., 1994).”
BackgroundSelf-citationRole of Laparoscopy in the Treatment of Endometriosis-Associated Infertility
Osuga, Y., Koga, K., Tsutsumi, O., Yano, T., Maruyama, M., Kugu, K., Momoeda, M., & Taketani, Y. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000049422 · Cited by 80 · see citing works
Endometriosis and Oocyte Quality
Saito, H., Seino, T., Kaneko-Tarui, T., Nakahara, K., Toya, M., & Kurachi, H. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000049424 · Cited by 74 · see citing works
The impact of endometriosis on the outcome of Assisted Reproductive Technology
González-Comadran, M., Schwarze, J.-E., Zegers-Hochschild, F., de Souza, M. D. C. B., Carreras, R., & Checa, M. Á. (2017) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-016-0217-2 · Cited by 74 · see citing works
“[33], reported a significantly reduced pregnancy and implantation rates when oocytes came from donors with endometriosis, although implantation rates among women with and without endometriosis were comparable when oocytes came from donors without endometriosis.”
ResultPellicer, A., Valbuena, D., Bauset, C., Albert, C., Bonilla-Musoles, F., Remohı́, J., & Simón, C. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00085-5 · Cited by 73 · see citing works
Self-citationNew advances in the understanding of endometriosis related infertility
MAHUTTE, N. G., & Arici, A. M. (2002) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(01)00130-9 · Cited by 69 · see citing works
“Several studies have suggested an impairment of implantation in patients with endometriosis (Simon et al., 1994; Arici et al., 1996; Pellicer et al., 1998).”
BackgroundResultCorachán, A., Pellicer, N., Pellicer, A., & Ferrero, H. (2021) · Human Reproduction Update · doi:10.1093/humupd/dmab014 · Cited by 70 · see citing works
Self-citationMiravet-Valenciano, J., Ruiz-Alonso, M., Gómez, E., & Garcia-Velasco, J. A. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.06.002 · Cited by 69 · see citing works
Is endometrial receptivity transcriptomics affected in women with endometriosis? A pilot study
Garcia-Velasco, J. A., Fassbender, A., Ruiz-Alonso, M., Blesa, D., D‘Hooghe, T., & Simon, C. (2015) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2015.07.014 · Cited by 70 · see citing works
Self-citationEgg-sharing in assisted conception: ethical and practical considerations
Ahuja, K. K., Simons, E. G., Fiamanya, W., et al. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019310 · Cited by 69 · see citing works
Nakahara, K., Saito, H., Saito, T., Ito, M., Ohta, N., Takahashi, T., & Hiroi, M. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00038-7 · Cited by 67 · see citing works
Somigliana, E. (1999) · Human Reproduction Update · doi:10.1093/humupd/5.1.40 · Cited by 66 · see citing works
Fertility Preservation in Women With Endometriosis
Llarena, N. C., Falcone, T., & Flyckt, R. L. (2019) · Clinical Medicine Insights Reproductive Health · doi:10.1177/1179558119873386 · Cited by 69 · see citing works
Clinical factors affecting endometrial receptiveness in oocyte donation cycles
Soares, S. R., García-Velasco, J. A., Sánchez, M. F., Bosch, E., Remohi, J. A., Pellicer, A., & Simón, C. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.01.080 · Cited by 61 · see citing works
Self-citationKumbak, B., Kahraman, S., Karlikaya, G., Laçin, S., & Guney, A. (2007) · Gynecologic and Obstetric Investigation · doi:10.1159/000112310 · Cited by 60 · see citing works
Obstetric Outcome in Women with Endometriosis – A Matched Case-Control Study
Kortelahti, M., Anttila, M. A., Hippeläinen, M. I., & Heinonen, S. T. (2003) · Gynecologic and Obstetric Investigation · doi:10.1159/000074815 · Cited by 59 · see citing works
Involvement of catalase in the endometrium of patients with endometriosis and adenomyosis
Ota, H., Igarashi, S., Sato, N., Tanaka, H., & Tanaka, T. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03344-7 · Cited by 56 · see citing works
Hosseini, E., Mehraein, F., Shahhoseini, M., Karimian, L., Nikmard, F., Ashrafi, M., Afsharian, P., & Aflatoonian, R. (2016) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-016-0727-z · Cited by 58 · see citing works
“low rate of pregnancy in endometriosis patients [48, 49].”
BackgroundNatural cycle IVF in unexplained, endometriosis-associated and tubal factor infertility
Omland, A. K., Fedorcsák, P., Storeng, R., Dale, P. O., Åbyholm, T., & Tanbo, T. G. (2001) · Human Reproduction · doi:10.1093/humrep/16.12.2587 · Cited by 58 · see citing works
“…implantation rates than tubal factor controls, and as oocytes from women without endometriosis donated to women with endometriosis showed the same implantation ability as tubal factor controls, more advanced stages of endometriosis could be responsible for poor oocyte quality (Simón et al., 1994).”
BackgroundPapaleo, E., Ottolina, J., Viganò, P., Brigante, C., Marsiglio, E., de Michele, F., & Candiani, M. (2011) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/j.1600-0412.2011.01161.x · Cited by 56 · see citing works
“It has been suggested that endometriosis may affect almost any step of reproduction, including altered folliculogenesis (24), ovulatory dysfunction (25), reduced preovulatory steroidogenesis of granulosa cells (26), sperm phagocytosis (27), impaired fertilization (28,29), toxicity against early embryonic development (…”
BackgroundSzczepańska, M., Wirstlein, P. K., Łuczak, M. W., Jagodziński, P. P., & Skrzypczak, J. (2010) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2010.09.012 · Cited by 57 · see citing works
“Several mechanisms that account for subfertility in women with endometriosis have been suggested [2,6,7].”
Background
- 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 › Public Health, Environmental and Occupational Health › 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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