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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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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
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 805
Factors that affect outcome of in-vitro fertilisation treatment
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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
“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
“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
“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 403
Kunz, G., Beil, D., Huppert, P., Noe, M., Kissler, S., & Leyendecker, G. (2005) · Human Reproduction · doi:10.1093/humrep/dei021 · Cited by 377
“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 376
“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
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 388
Lessey, B. A., & Kim, J. J. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.05.031 · Cited by 286
“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 283
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 269
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
“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
“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].”
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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
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
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
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 209
“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
“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 223
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
“We retrospectively analysed the results of our oocyte donation programme (Simón et al., 1994).”
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Miller, J. E., Ahn, S. H., Monsanto, S. P., Khalaj, K., Koti, M., & Tayade, C. (2016) · Oncotarget · doi:10.18632/oncotarget.12577 · Cited by 195
“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 192
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 180
“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 173
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
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
Epithelial-to-mesenchymal transition in the development of endometriosis
Yang, Y., & Yang, W. (2017) · Oncotarget · doi:10.18632/oncotarget.16472 · Cited by 171
“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 164
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 177
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
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 158
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
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
“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 151
“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
A new concept of endometriosis and adenomyosis, tissue injury and repair (TIAR)
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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
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
Self-citationTubal transport of gametes and embryos: a review of physiology and pathophysiology
Ezzati, M., Djahanbakhch, O., Arian, S. E., & Carr, B. R. (2014) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-014-0309-x · Cited by 142
“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 136
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
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
“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 125
“, in a retrospective study, observed a significantly lower implantation rate (IR) in recipients without endometriosis who received egg from women with endometriosis [64].”
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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
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
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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
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
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
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
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Broi, M. G. D., & Navarro, P. A. (2015) · Cell and Tissue Research · doi:10.1007/s00441-015-2339-9 · Cited by 104
“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
“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
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
“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 101
Pituitary-ovarian dysfunction and endometriosis
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Endometriosis is not detrimental to embryo implantation in oocyte recipients
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“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
“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
“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
“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
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 93
“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
“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
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
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 86
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 84
“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
“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
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
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 77
“[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
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
“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
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
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
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
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
Somigliana, E. (1999) · Human Reproduction Update · doi:10.1093/humupd/5.1.40 · Cited by 66
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
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
Self-citationKumbak, B., Kahraman, S., Karlikaya, G., Laçin, S., & Guney, A. (2007) · Gynecologic and Obstetric Investigation · doi:10.1159/000112310 · Cited by 60
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
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
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 59
“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
“…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 57
“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 59
“Several mechanisms that account for subfertility in women with endometriosis have been suggested [2,6,7].”
Background
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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