Endometriozis ve Adenomyozis: Oosit Kalitesine Etkisi
Synopsis
Endometriozis, üreme çağındaki kadınların %10’unu etkileyen kronik ve inflamatuar bir hastalıktır. Bu hastalıkla ilişkili infertilite, kadınların %50'sinde görülmektedir. Endometriozisli hastalarda fertilite kaybı; pelvik yapışıklıklar, inflamasyon, oksidatif stres, bağışıklık sistemi düzensizlikleri ve bozulmuş ovulasyon gibi çeşitli faktörlere bağlanmaktadır. Endometriozis overyan rezervi ve oosit kalitesini pelvik ortamda oluşan toksik mikro çevre ile etkileyebilir. Özellikle endometriomanın oosit kalitesini olumsuz etkileyebileceği ve embriyo gelişimi ile implantasyonu bozabileceği düşünülmektedir. Ancak, mevcut araştırmaların kanıtları kesin değildir. IVF sonuçları üzerine yapılan meta-analizler, endometriozis varlığının olgun oosit sayısını azaltabileceğini, ancak canlı doğum oranlarına etkisinin minimal olduğunu göstermektedir.
Endometriosis is a chronic and inflammatory condition that affects 10% of women of reproductive age. Infertility associated with this disease is observed in 50% of affected women. Fertility decline in women with endometriosis is attributed to several factors, including pelvic adhesions, inflammation, oxidative stress, immune system dysregulation, and impaired ovulation. Endometriosis can impact ovarian reserve and oocyte quality by creating a toxic microenvironment in the pelvic cavity. In particular, endometriomas are thought to affect oocyte quality and disrupt embryo development and implantation negatively. However, current research evidence remains inconclusive. Meta-analyses of IVF outcomes suggest that while endometriosis may reduce the number of mature oocytes retrieved, its impact on live birth rates appears minimal.
References
Chapron C, Marcellin L, Borghese B, et al. Rethinking mechanisms, diagnosis and management of endometriosis. Nature Reviews. Endocrinology. 2019;15(11): 666–682. doi.org/10.1038/s41574-019-0245-z.
Koch J, Rowan K, Rombauts L, et al. Endometriosis and infertility - a consensus statement from ACCEPT (Australasian CREI Consensus Expert Panel on Trial evidence). The Australian & New Zealand Journal of Obstetrics & Gynaecology. 2012;52(6): 513–522. doi.org/10.1111/j.1479-828X.2012.01480.x.
Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: a committee opinion. Fertility and Sterility. 2012;98(3): 591–598. doi.org/10.1016/j.fertnstert.2012.05.031.
Sanchez AM, Viganò P, Somigliana E, et al. The distinguishing cellular and molecular features of the endometriotic ovarian cyst: from pathophysiology to the potential endometrioma-mediated damage to the ovary. Human Reproduction Update. 2014;20(2): 217–230. doi.org/10.1093/humupd/dmt053.
Simopoulou M, Rapani A, Grigoriadis S, et al. Getting to Know Endometriosis-Related Infertility Better: A Review on How Endometriosis Affects Oocyte Quality and Embryo Development. Biomedicines. 2021;9(3). doi.org/10.3390/biomedicines9030273.
Gleicher N, Weghofer A, Barad DH. Defining ovarian reserve to better understand ovarian aging. Reproductive Biology and Endocrinology : RB&E. 2011;9: 23. doi.org/10.1186/1477-7827-9-23.
Nelson SM. Biomarkers of ovarian response: current and future applications. Fertility and Sterility. 2013;99(4): 963–969. doi.org/10.1016/j.fertnstert.2012.11.051.
Sanchez AM, Papaleo E, Corti L, et al. Iron availability is increased in individual human ovarian follicles in close proximity to an endometrioma compared with distal ones. Human Reproduction. 2014;29(3): 577–583. doi.org/10.1093/humrep/det466.
Matsuzaki S, Schubert B. Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis. Fertility and Sterility. 2010;93(7): 2431–2432. doi.org/10.1016/j.fertnstert.2009.08.068.
Maneschi F, Marasá L, Incandela S, et al. Ovarian cortex surrounding benign neoplasms: a histologic study. American Journal of Obstetrics and Gynecology. 1993;169(2 Pt 1): 388–393. doi.org/10.1016/0002-9378(93)90093-x.
Kitajima M, Dolmans MM, Donnez O, et al. Enhanced follicular recruitment and atresia in cortex derived from ovaries with endometriomas. Fertility and Sterility. 2014;101(4): 1031–1037. doi.org/10.1016/j.fertnstert.2013.12.049.
Takeuchi A, Koga K, Satake E, et al. Endometriosis Triggers Excessive Activation of Primordial Follicles via PI3K-PTEN-Akt-Foxo3 Pathway. The Journal of Clinical Endocrinology and Metabolism. 2019;104(11): 5547–5554. doi.org/10.1210/jc.2019-00281.
Di Nisio V, Rossi G, Di Luigi G, et al. Increased levels of proapoptotic markers in normal ovarian cortex surrounding small endometriotic cysts. Reproductive Biology. 2019;19(3): 225–229. doi.org/10.1016/j.repbio.2019.08.002.
Thombre Kulkarni M, Shafrir A, Farland L V, et al. Association Between Laparoscopically Confirmed Endometriosis and Risk of Early Natural Menopause. JAMA. 2022;5(1): e2144391. doi.org/10.1001/jamanetworkopen.2021.44391.
Tian Z, Zhang Y, Zhang C, et al. Antral follicle count is reduced in the presence of endometriosis: a systematic review and meta-analysis. Reproductive Biomedicine Online. 2021;42(1): 237–247. doi.org/10.1016/j.rbmo.2020.09.014.
Kasapoğlu I, Ata B, Uyanıklar O, et al. Endometrioma-related reduction in ovarian reserve (ERROR): a prospective longitudinal study. Fertility and Sterility. 2018;110(1): 122–127. doi.org/10.1016/j.fertnstert.2018.03.015.
Gupta S, Agarwal A, Agarwal R, et al. Impact of ovarian endometrioma on assisted reproduction outcomes. Reproductive Biomedicine Online. 2006;13(3): 349–360. doi.org/10.1016/s1472-6483(10)61439-3.
Hamdan M, Dunselman G, Li TC, et al. The impact of endometrioma on IVF/ICSI outcomes: a systematic review and meta-analysis. Human Reproduction Update. 2015;21(6): 809–825. doi.org/10.1093/humupd/dmv035.
Alshehre SM, Narice BF, Fenwick MA, et al. The impact of endometrioma on in vitro fertilisation/intra-cytoplasmic injection IVF/ICSI reproductive outcomes: a systematic review and meta-analysis. Archives of Gynecology and Obstetrics. 2021;303(1): 3–16. doi.org/10.1007/s00404-020-05796-9.
Yang C, Geng Y, Li Y, et al. Impact of ovarian endometrioma on ovarian responsiveness and IVF: a systematic review and meta-analysis. Reproductive Biomedicine Online. 2015;31(1): 9–19. doi.org/10.1016/j.rbmo.2015.03.005.
González-Fernández R, Peña Ó, Hernández J, Martín-Vasallo P, et al. Patients with endometriosis and patients with poor ovarian reserve have abnormal follicle-stimulating hormone receptor signaling pathways. Fertility and Sterility. 2011;95(7): 2373–2378. doi.org/10.1016/j.fertnstert.2011.03.030.
Sanchez AM, Somigliana E, Vercellini P, et al. Endometriosis as a detrimental condition for granulosa cell steroidogenesis and development: From molecular alterations to clinical impact. The Journal of Steroid Biochemistry and Molecular Biology. 2016;155(Pt A): 35–46. doi.org/10.1016/j.jsbmb.2015.07.023.
Lin X, Tong X, Zhang Y, et al. Decreased Expression of EZH2 in Granulosa Cells Contributes to Endometriosis-Associated Infertility by Targeting IL-1R2. Endocrinology. 2022;164(2). doi.org/10.1210/endocr/bqac210.
Regiani T, Cordeiro FB, da Costa L do VT, et al. Follicular fluid alterations in endometriosis: label-free proteomics by MS(E) as a functional tool for endometriosis. Systems Biology in Reproductive Medicine. 2015;61(5): 263–276. doi.org/10.3109/19396368.2015.1037025.
Gomes FM, Navarro PAAS, de Abreu LG, Ferriani RA, et al. Effect of peritoneal fluid from patients with minimal/mild endometriosis on progesterone release by human granulosa-lutein cells obtained from infertile patients without endometriosis: a pilot study. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2008;138(1): 60–65. doi.org/10.1016/j.ejogrb.2007.12.008.
Du YB, Gao MZ, Shi Y, et al. Endocrine and inflammatory factors and endometriosis-associated infertility in assisted reproduction techniques. Archives of Gynecology and Obstetrics. 2013;287(1): 123–130. doi.org/10.1007/s00404-012-2567-0.
Sreerangaraja Urs DB, Wu WH, Komrskova K, et al. Mitochondrial Function in Modulating Human Granulosa Cell Steroidogenesis and Female Fertility. International Journal of Molecular Sciences. 2020;21(10). doi.org/10.3390/ijms21103592.
Wang J, Shen X xin, Huang X hua, et al. Follicular fluid levels of prostaglandin E2 and the effect of prostaglandin E2 on steroidogenesis in granulosa-lutein cells in women with moderate and severe endometriosis undergoing in vitro fertilization and embryo transfer. Chinese Medical Journal. 2012;125(22): 3985–3990.
Bulun SE, Imir G, Utsunomiya H, et al. Aromatase in endometriosis and uterine leiomyomata. The Journal of Steroid Biochemistry and Molecular Biology. 2005;95(1–5): 57–62. doi.org/10.1016/j.jsbmb.2005.04.012.
Noël JC, Borghese B, Vaiman D, et al. Steroidogenic factor-1 expression in ovarian endometriosis. Applied Immunohistochemistry & Molecular Morphology : AIMM. 2010;18(3): 258–261. doi.org/10.1097/PAI.0b013e3181c06948.
Cordeiro FB, Cataldi TR, Perkel KJ, et al. Lipidomics analysis of follicular fluid by ESI-MS reveals potential biomarkers for ovarian endometriosis. Journal of Assisted Reproduction and Genetics. 2015;32(12): 1817–1825. doi.org/10.1007/s10815-015-0592-1.
Nasiri N, Moini A, Eftekhari-Yazdi P, et al. Oxidative Stress Statues in Serum and Follicular Fluid of Women with Endometriosis. Cell Journal. 2017;18(4): 582–587. doi.org/10.22074/cellj.2016.4724.
Prieto L, Quesada JF, Cambero O, et al. Analysis of follicular fluid and serum markers of oxidative stress in women with infertility related to endometriosis. Fertility and Sterility. 2012;98(1): 126–130. doi.org/10.1016/j.fertnstert.2012.03.052.
Paffoni A, Bolis V, Ferrari S, et al. The Gametotoxic Effects of the Endometrioma Content: Insights From a Parthenogenetic Human Model. Reproductive Sciences. 2019;26(5): 573–579. doi.org/10.1177/1933719118777637.
Gupta RK, Patel AK, Shah N, et al. Oxidative stress and antioxidants in disease and cancer: a review. Asian Pacific Journal of Cancer Prevention : APJCP. 2014;15(11): 4405–4409. doi.org/10.7314/apjcp.2014.15.11.4405.
Behrman HR, Kodaman PH, Preston SL, et al. Oxidative stress and the ovary. Journal of the Society for Gynecologic Investigation. 2001;8(1 Suppl Proceedings): S40-2. doi.org/10.1016/s1071-5576(00)00106-4.
Askoxylaki M, Siristatidis C, Chrelias C, et al. Reactive oxygen species in the follicular fluid of subfertile women undergoing In Vitro Fertilization: a short narrative review. Journal of Endocrinological Investigation. 2013;36(11): 1117–1120. doi.org/10.3275/9097.
Velthut A, Zilmer M, Zilmer K, et al. Elevated blood plasma antioxidant status is favourable for achieving IVF/ICSI pregnancy. Reproductive Biomedicine Online. 2013;26(4): 345–352. doi.org/10.1016/j.rbmo.2012.12.012.
Seino T, Saito H, Kaneko T, et al. Eight-hydroxy-2’-deoxyguanosine in granulosa cells is correlated with the quality of oocytes and embryos in an in vitro fertilization-embryo transfer program. Fertility and Sterility. 2002;77(6): 1184–1190. doi.org/10.1016/s0015-0282(02)03103-5.
Goud PT, Goud AP, Joshi N, et al. Dynamics of nitric oxide, altered follicular microenvironment, and oocyte quality in women with endometriosis. Fertility and Sterility. 2014;102(1): 151-159.e5. doi.org/10.1016/j.fertnstert.2014.03.053.
Jancar N, Kopitar AN, Ihan A, et al. Effect of apoptosis and reactive oxygen species production in human granulosa cells on oocyte fertilization and blastocyst development. Journal of Assisted Reproduction and Genetics. 2007;24(2–3): 91–97. doi.org/10.1007/s10815-006-9103-8.
Russell DL, Robker RL. Molecular mechanisms of ovulation: co-ordination through the cumulus complex. Human Reproduction Update. 2007;13(3): 289–312. doi.org/10.1093/humupd/dml062.
Almeida CP, Ferreira MCF, Silveira CO, et al. Clinical correlation of apoptosis in human granulosa cells-A review. Cell Biology International. 2018;42(10): 1276–1281. doi.org/10.1002/cbin.11036.
Nakahara K, Saito H, Saito T, et al. The incidence of apoptotic bodies in membrana granulosa can predict prognosis of ova from patients participating in in vitro fertilization programs. Fertility and Sterility. 1997;68(2): 312–317. doi.org/10.1016/s0015-0282(97)81521-x.
Regan SLP, Knight PG, Yovich JL, et al. The effect of ovarian reserve and receptor signalling on granulosa cell apoptosis during human follicle development. Molecular and Cellular Endocrinology. 2018;470: 219–227. doi.org/10.1016/j.mce.2017.11.002.
Kunitomi C, Harada M, Takahashi N, et al. Activation of endoplasmic reticulum stress mediates oxidative stress-induced apoptosis of granulosa cells in ovaries affected by endometrioma. Molecular Human Reproduction. 2020;26(1): 40–52. doi.org/10.1093/molehr/gaz066.
Lobach VN, Casalechi M, Dela Cruz C, et al. Caspase-3 gene expression in human luteinized granulosa cells is inversely correlated with the number of oocytes retrieved after controlled ovarian stimulation. Human Fertility. 2019;22(1): 33–38. doi.org/10.1080/14647273.2017.1356474.
Cecchino GN, Seli E, Alves da Motta EL, et al. The role of mitochondrial activity in female fertility and assisted reproductive technologies: overview and current insights. Reproductive Biomedicine Online. 2018;36(6): 686–697. doi.org/10.1016/j.rbmo.2018.02.007.
von Mengden L, Klamt F, Smitz J. Redox Biology of Human Cumulus Cells: Basic Concepts, Impact on Oocyte Quality, and Potential Clinical Use. Antioxidants & Redox Signaling. 2020;32(8): 522–535. doi.org/10.1089/ars.2019.7984.
Yamashita Y, Asano M, Morishima S, et al. Mitochondrial gene expression in granulosa cells of severe endometriosis with in vitro fertilization and embryo transfer. Fertility and Sterility. 2007;88(6): 1703–1705. doi.org/10.1016/j.fertnstert.2007.01.111.
Mao J, Zhang J, Cai L, et al. Elevated prohibitin 1 expression mitigates glucose metabolism defects in granulosa cells of infertile patients with endometriosis. Molecular Human Reproduction. 2022;28(6). doi.org/10.1093/molehr/gaac018.
González-Fernández R, Martín-Ramírez R, Rotoli D, et al. Granulosa-Lutein Cell Sirtuin Gene Expression Profiles Differ between Normal Donors and Infertile Women. International Journal of Molecular Sciences. 2019;21(1). doi.org/10.3390/ijms21010295.
Singh AK, Dutta M, Chattopadhyay R, et al. Intrafollicular interleukin-8, interleukin-12, and adrenomedullin are the promising prognostic markers of oocyte and embryo quality in women with endometriosis. Journal of Assisted Reproduction and Genetics. 2016;33(10): 1363–1372. doi.org/10.1007/s10815-016-0782-5.
Choi YS, Cho S, Seo SK, et al. Alteration in the intrafollicular thiol-redox system in infertile women with endometriosis. Reproduction. 2015;149(2): 155–162. doi.org/10.1530/REP-14-0438.
Xu H, Schultze-Mosgau A, Agic A, et al. Regulated upon activation, normal T cell expressed and secreted (RANTES) and monocyte chemotactic protein 1 in follicular fluid accumulate differentially in patients with and without endometriosis undergoing in vitro fertilization. Fertility and Sterility. 2006;86(6): 1616–1620. doi.org/10.1016/j.fertnstert.2006.05.043.
Hahn DW, Carraher RP, Foldesy RG, et al. Experimental evidence for failure to implant as a mechanism of infertility associated with endometriosis. American Journal of Obstetrics and Gynecology. 1986;155(5): 1109–1113. doi.org/10.1016/0002-9378(86)90360-1.
Illera MJ, Juan L, Stewart CL, et al. Effect of peritoneal fluid from women with endometriosis on implantation in the mouse model. Fertility and Sterility. 2000;74(1): 41–48. doi.org/10.1016/s0015-0282(00)00552-5.
Brizek CL, Schlaff S, Pellegrini VA, et al. Increased incidence of aberrant morphological phenotypes in human embryogenesis--an association with endometriosis. Journal of Assisted Reproduction and Genetics. 1995;12(2): 106–112. doi.org/10.1007/BF02211378.
Schatten G, Simerly C, Schatten H. Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proceedings of the National Academy of Sciences of the United States of America. 1985;82(12): 4152–4156. doi.org/10.1073/pnas.82.12.4152.
Eroğlu A, Toth TL, Toner M. Alterations of the cytoskeleton and polyploidy induced by cryopreservation of metaphase II mouse oocytes. Fertility and Sterility. 1998;69(5): 944–957. doi.org/10.1016/s0015-0282(98)00030-2.
Horton J, Sterrenburg M, Lane S, et al. Reproductive, obstetric, and perinatal outcomes of women with adenomyosis and endometriosis: a systematic review and meta-analysis. Human Reproduction Update. 2019;25(5): 592–632. doi.org/10.1093/humupd/dmz012.
Nirgianakis K, Kalaitzopoulos DR, et al. Fertility, pregnancy and neonatal outcomes of patients with adenomyosis: a systematic review and meta-analysis. Reproductive Biomedicine Online. 2021;42(1): 185–206. doi.org/10.1016/j.rbmo.2020.09.023.
Liang T, Zhang W, Pan N, et al. Reproductive Outcomes of In Vitro Fertilization and Fresh Embryo Transfer in Infertile Women With Adenomyosis: A Retrospective Cohort Study. Frontiers in Endocrinology. 2022;13: 865358. doi.org/10.3389/fendo.2022.865358.
Setti AS, Figueira RCS, Braga DPAF, et al. Relationship between oocyte abnormal morphology and intracytoplasmic sperm injection outcomes: a meta-analysis. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2011;159(2): 364–370. doi.org/10.1016/j.ejogrb.2011.07.031.
Latif S, Saridogan E. Endometriosis, Oocyte, and Embryo Quality. Journal of Clinical Medicine. 2023;12(13). doi.org/10.3390/jcm12134186.
Robin C, Uk A, Decanter C, et al. Impact of endometriosis on oocyte morphology in IVF-ICSI: retrospective study of a cohort of more than 6000 mature oocytes. Reproductive Biology and Endocrinology : RB&E. 2021;19(1): 160. doi.org/10.1186/s12958-021-00798-x.
Metzemaekers J, Lust E, Rhemrev J, et al. Prognosis in fertilisation rate and outcome in IVF cycles in patients with and without endometriosis: a population-based comparative cohort study with controls. Facts, Views & Vision in ObGyn. 2021;13(1): 27–34. doi.org/10.52054/FVVO.13.1.007.
Sanchez AM, Vanni VS, Bartiromo L, et al. Is the oocyte quality affected by endometriosis? A review of the literature. Journal of Ovarian Research. 2017;10(1): 43. doi.org/10.1186/s13048-017-0341-4.
Rossi AC, Prefumo F. The effects of surgery for endometriosis on pregnancy outcomes following in vitro fertilization and embryo transfer: a systematic review and meta-analysis. Archives of Gynecology and Obstetrics. 2016;294(3): 647–655. doi.org/10.1007/s00404-016-4136-4.
Kasapoğlu I, Kuspınar G, Sarıbal S, et al. Detrimental effects of endometriosis on oocyte morphology in intracytoplasmic sperm injection cycles: a retrospective cohort study. Gynecological Endocrinology. 2018;34(3): 206–211. doi.org/10.1080/09513590.2017.1391203.
Boucret L, Bouet PE, Riou J, et al. Endometriosis Lowers the Cumulative Live Birth Rates in IVF by Decreasing the Number of Embryos but Not Their Quality. Journal of Clinical Medicine. 2020;9(8). doi.org/10.3390/jcm9082478.
Ata B, Telek SB. Assisted reproductive technology for women with endometriosis, a clinically oriented review. Current Opinion in Obstetrics & Gynecology. 2021;33(3): 225–231. doi.org/10.1097/GCO.0000000000000710.
Harb HM, Gallos ID, Chu J, et al. The effect of endometriosis on in vitro fertilisation outcome: a systematic review and meta-analysis. BJOG : an International Journal of Obstetrics and Gynaecology. 2013;120(11): 1308–1320. doi.org/10.1111/1471-0528.12366.
Senapati S, Sammel MD, Morse C, et al. Impact of endometriosis on in vitro fertilization outcomes: an evaluation of the Society for Assisted Reproductive Technologies Database. Fertility and Sterility. 2016;106(1): 164-171.e1. doi.org/10.1016/j.fertnstert.2016.03.037.
Kamath MS, Subramanian V, Antonisamy B, et al. Endometriosis and oocyte quality: an analysis of 13 614 donor oocyte recipient and autologous IVF cycles. Human Reproduction Open. 2022;2022(3): hoac025. doi.org/10.1093/hropen/hoac025.
Koch J, Rowan K, Rombauts L, et al. Endometriosis and infertility - a consensus statement from ACCEPT (Australasian CREI Consensus Expert Panel on Trial evidence). The Australian & New Zealand Journal of Obstetrics & Gynaecology. 2012;52(6): 513–522. doi.org/10.1111/j.1479-828X.2012.01480.x.
Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: a committee opinion. Fertility and Sterility. 2012;98(3): 591–598. doi.org/10.1016/j.fertnstert.2012.05.031.
Sanchez AM, Viganò P, Somigliana E, et al. The distinguishing cellular and molecular features of the endometriotic ovarian cyst: from pathophysiology to the potential endometrioma-mediated damage to the ovary. Human Reproduction Update. 2014;20(2): 217–230. doi.org/10.1093/humupd/dmt053.
Simopoulou M, Rapani A, Grigoriadis S, et al. Getting to Know Endometriosis-Related Infertility Better: A Review on How Endometriosis Affects Oocyte Quality and Embryo Development. Biomedicines. 2021;9(3). doi.org/10.3390/biomedicines9030273.
Gleicher N, Weghofer A, Barad DH. Defining ovarian reserve to better understand ovarian aging. Reproductive Biology and Endocrinology : RB&E. 2011;9: 23. doi.org/10.1186/1477-7827-9-23.
Nelson SM. Biomarkers of ovarian response: current and future applications. Fertility and Sterility. 2013;99(4): 963–969. doi.org/10.1016/j.fertnstert.2012.11.051.
Sanchez AM, Papaleo E, Corti L, et al. Iron availability is increased in individual human ovarian follicles in close proximity to an endometrioma compared with distal ones. Human Reproduction. 2014;29(3): 577–583. doi.org/10.1093/humrep/det466.
Matsuzaki S, Schubert B. Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis. Fertility and Sterility. 2010;93(7): 2431–2432. doi.org/10.1016/j.fertnstert.2009.08.068.
Maneschi F, Marasá L, Incandela S, et al. Ovarian cortex surrounding benign neoplasms: a histologic study. American Journal of Obstetrics and Gynecology. 1993;169(2 Pt 1): 388–393. doi.org/10.1016/0002-9378(93)90093-x.
Kitajima M, Dolmans MM, Donnez O, et al. Enhanced follicular recruitment and atresia in cortex derived from ovaries with endometriomas. Fertility and Sterility. 2014;101(4): 1031–1037. doi.org/10.1016/j.fertnstert.2013.12.049.
Takeuchi A, Koga K, Satake E, et al. Endometriosis Triggers Excessive Activation of Primordial Follicles via PI3K-PTEN-Akt-Foxo3 Pathway. The Journal of Clinical Endocrinology and Metabolism. 2019;104(11): 5547–5554. doi.org/10.1210/jc.2019-00281.
Di Nisio V, Rossi G, Di Luigi G, et al. Increased levels of proapoptotic markers in normal ovarian cortex surrounding small endometriotic cysts. Reproductive Biology. 2019;19(3): 225–229. doi.org/10.1016/j.repbio.2019.08.002.
Thombre Kulkarni M, Shafrir A, Farland L V, et al. Association Between Laparoscopically Confirmed Endometriosis and Risk of Early Natural Menopause. JAMA. 2022;5(1): e2144391. doi.org/10.1001/jamanetworkopen.2021.44391.
Tian Z, Zhang Y, Zhang C, et al. Antral follicle count is reduced in the presence of endometriosis: a systematic review and meta-analysis. Reproductive Biomedicine Online. 2021;42(1): 237–247. doi.org/10.1016/j.rbmo.2020.09.014.
Kasapoğlu I, Ata B, Uyanıklar O, et al. Endometrioma-related reduction in ovarian reserve (ERROR): a prospective longitudinal study. Fertility and Sterility. 2018;110(1): 122–127. doi.org/10.1016/j.fertnstert.2018.03.015.
Gupta S, Agarwal A, Agarwal R, et al. Impact of ovarian endometrioma on assisted reproduction outcomes. Reproductive Biomedicine Online. 2006;13(3): 349–360. doi.org/10.1016/s1472-6483(10)61439-3.
Hamdan M, Dunselman G, Li TC, et al. The impact of endometrioma on IVF/ICSI outcomes: a systematic review and meta-analysis. Human Reproduction Update. 2015;21(6): 809–825. doi.org/10.1093/humupd/dmv035.
Alshehre SM, Narice BF, Fenwick MA, et al. The impact of endometrioma on in vitro fertilisation/intra-cytoplasmic injection IVF/ICSI reproductive outcomes: a systematic review and meta-analysis. Archives of Gynecology and Obstetrics. 2021;303(1): 3–16. doi.org/10.1007/s00404-020-05796-9.
Yang C, Geng Y, Li Y, et al. Impact of ovarian endometrioma on ovarian responsiveness and IVF: a systematic review and meta-analysis. Reproductive Biomedicine Online. 2015;31(1): 9–19. doi.org/10.1016/j.rbmo.2015.03.005.
González-Fernández R, Peña Ó, Hernández J, Martín-Vasallo P, et al. Patients with endometriosis and patients with poor ovarian reserve have abnormal follicle-stimulating hormone receptor signaling pathways. Fertility and Sterility. 2011;95(7): 2373–2378. doi.org/10.1016/j.fertnstert.2011.03.030.
Sanchez AM, Somigliana E, Vercellini P, et al. Endometriosis as a detrimental condition for granulosa cell steroidogenesis and development: From molecular alterations to clinical impact. The Journal of Steroid Biochemistry and Molecular Biology. 2016;155(Pt A): 35–46. doi.org/10.1016/j.jsbmb.2015.07.023.
Lin X, Tong X, Zhang Y, et al. Decreased Expression of EZH2 in Granulosa Cells Contributes to Endometriosis-Associated Infertility by Targeting IL-1R2. Endocrinology. 2022;164(2). doi.org/10.1210/endocr/bqac210.
Regiani T, Cordeiro FB, da Costa L do VT, et al. Follicular fluid alterations in endometriosis: label-free proteomics by MS(E) as a functional tool for endometriosis. Systems Biology in Reproductive Medicine. 2015;61(5): 263–276. doi.org/10.3109/19396368.2015.1037025.
Gomes FM, Navarro PAAS, de Abreu LG, Ferriani RA, et al. Effect of peritoneal fluid from patients with minimal/mild endometriosis on progesterone release by human granulosa-lutein cells obtained from infertile patients without endometriosis: a pilot study. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2008;138(1): 60–65. doi.org/10.1016/j.ejogrb.2007.12.008.
Du YB, Gao MZ, Shi Y, et al. Endocrine and inflammatory factors and endometriosis-associated infertility in assisted reproduction techniques. Archives of Gynecology and Obstetrics. 2013;287(1): 123–130. doi.org/10.1007/s00404-012-2567-0.
Sreerangaraja Urs DB, Wu WH, Komrskova K, et al. Mitochondrial Function in Modulating Human Granulosa Cell Steroidogenesis and Female Fertility. International Journal of Molecular Sciences. 2020;21(10). doi.org/10.3390/ijms21103592.
Wang J, Shen X xin, Huang X hua, et al. Follicular fluid levels of prostaglandin E2 and the effect of prostaglandin E2 on steroidogenesis in granulosa-lutein cells in women with moderate and severe endometriosis undergoing in vitro fertilization and embryo transfer. Chinese Medical Journal. 2012;125(22): 3985–3990.
Bulun SE, Imir G, Utsunomiya H, et al. Aromatase in endometriosis and uterine leiomyomata. The Journal of Steroid Biochemistry and Molecular Biology. 2005;95(1–5): 57–62. doi.org/10.1016/j.jsbmb.2005.04.012.
Noël JC, Borghese B, Vaiman D, et al. Steroidogenic factor-1 expression in ovarian endometriosis. Applied Immunohistochemistry & Molecular Morphology : AIMM. 2010;18(3): 258–261. doi.org/10.1097/PAI.0b013e3181c06948.
Cordeiro FB, Cataldi TR, Perkel KJ, et al. Lipidomics analysis of follicular fluid by ESI-MS reveals potential biomarkers for ovarian endometriosis. Journal of Assisted Reproduction and Genetics. 2015;32(12): 1817–1825. doi.org/10.1007/s10815-015-0592-1.
Nasiri N, Moini A, Eftekhari-Yazdi P, et al. Oxidative Stress Statues in Serum and Follicular Fluid of Women with Endometriosis. Cell Journal. 2017;18(4): 582–587. doi.org/10.22074/cellj.2016.4724.
Prieto L, Quesada JF, Cambero O, et al. Analysis of follicular fluid and serum markers of oxidative stress in women with infertility related to endometriosis. Fertility and Sterility. 2012;98(1): 126–130. doi.org/10.1016/j.fertnstert.2012.03.052.
Paffoni A, Bolis V, Ferrari S, et al. The Gametotoxic Effects of the Endometrioma Content: Insights From a Parthenogenetic Human Model. Reproductive Sciences. 2019;26(5): 573–579. doi.org/10.1177/1933719118777637.
Gupta RK, Patel AK, Shah N, et al. Oxidative stress and antioxidants in disease and cancer: a review. Asian Pacific Journal of Cancer Prevention : APJCP. 2014;15(11): 4405–4409. doi.org/10.7314/apjcp.2014.15.11.4405.
Behrman HR, Kodaman PH, Preston SL, et al. Oxidative stress and the ovary. Journal of the Society for Gynecologic Investigation. 2001;8(1 Suppl Proceedings): S40-2. doi.org/10.1016/s1071-5576(00)00106-4.
Askoxylaki M, Siristatidis C, Chrelias C, et al. Reactive oxygen species in the follicular fluid of subfertile women undergoing In Vitro Fertilization: a short narrative review. Journal of Endocrinological Investigation. 2013;36(11): 1117–1120. doi.org/10.3275/9097.
Velthut A, Zilmer M, Zilmer K, et al. Elevated blood plasma antioxidant status is favourable for achieving IVF/ICSI pregnancy. Reproductive Biomedicine Online. 2013;26(4): 345–352. doi.org/10.1016/j.rbmo.2012.12.012.
Seino T, Saito H, Kaneko T, et al. Eight-hydroxy-2’-deoxyguanosine in granulosa cells is correlated with the quality of oocytes and embryos in an in vitro fertilization-embryo transfer program. Fertility and Sterility. 2002;77(6): 1184–1190. doi.org/10.1016/s0015-0282(02)03103-5.
Goud PT, Goud AP, Joshi N, et al. Dynamics of nitric oxide, altered follicular microenvironment, and oocyte quality in women with endometriosis. Fertility and Sterility. 2014;102(1): 151-159.e5. doi.org/10.1016/j.fertnstert.2014.03.053.
Jancar N, Kopitar AN, Ihan A, et al. Effect of apoptosis and reactive oxygen species production in human granulosa cells on oocyte fertilization and blastocyst development. Journal of Assisted Reproduction and Genetics. 2007;24(2–3): 91–97. doi.org/10.1007/s10815-006-9103-8.
Russell DL, Robker RL. Molecular mechanisms of ovulation: co-ordination through the cumulus complex. Human Reproduction Update. 2007;13(3): 289–312. doi.org/10.1093/humupd/dml062.
Almeida CP, Ferreira MCF, Silveira CO, et al. Clinical correlation of apoptosis in human granulosa cells-A review. Cell Biology International. 2018;42(10): 1276–1281. doi.org/10.1002/cbin.11036.
Nakahara K, Saito H, Saito T, et al. The incidence of apoptotic bodies in membrana granulosa can predict prognosis of ova from patients participating in in vitro fertilization programs. Fertility and Sterility. 1997;68(2): 312–317. doi.org/10.1016/s0015-0282(97)81521-x.
Regan SLP, Knight PG, Yovich JL, et al. The effect of ovarian reserve and receptor signalling on granulosa cell apoptosis during human follicle development. Molecular and Cellular Endocrinology. 2018;470: 219–227. doi.org/10.1016/j.mce.2017.11.002.
Kunitomi C, Harada M, Takahashi N, et al. Activation of endoplasmic reticulum stress mediates oxidative stress-induced apoptosis of granulosa cells in ovaries affected by endometrioma. Molecular Human Reproduction. 2020;26(1): 40–52. doi.org/10.1093/molehr/gaz066.
Lobach VN, Casalechi M, Dela Cruz C, et al. Caspase-3 gene expression in human luteinized granulosa cells is inversely correlated with the number of oocytes retrieved after controlled ovarian stimulation. Human Fertility. 2019;22(1): 33–38. doi.org/10.1080/14647273.2017.1356474.
Cecchino GN, Seli E, Alves da Motta EL, et al. The role of mitochondrial activity in female fertility and assisted reproductive technologies: overview and current insights. Reproductive Biomedicine Online. 2018;36(6): 686–697. doi.org/10.1016/j.rbmo.2018.02.007.
von Mengden L, Klamt F, Smitz J. Redox Biology of Human Cumulus Cells: Basic Concepts, Impact on Oocyte Quality, and Potential Clinical Use. Antioxidants & Redox Signaling. 2020;32(8): 522–535. doi.org/10.1089/ars.2019.7984.
Yamashita Y, Asano M, Morishima S, et al. Mitochondrial gene expression in granulosa cells of severe endometriosis with in vitro fertilization and embryo transfer. Fertility and Sterility. 2007;88(6): 1703–1705. doi.org/10.1016/j.fertnstert.2007.01.111.
Mao J, Zhang J, Cai L, et al. Elevated prohibitin 1 expression mitigates glucose metabolism defects in granulosa cells of infertile patients with endometriosis. Molecular Human Reproduction. 2022;28(6). doi.org/10.1093/molehr/gaac018.
González-Fernández R, Martín-Ramírez R, Rotoli D, et al. Granulosa-Lutein Cell Sirtuin Gene Expression Profiles Differ between Normal Donors and Infertile Women. International Journal of Molecular Sciences. 2019;21(1). doi.org/10.3390/ijms21010295.
Singh AK, Dutta M, Chattopadhyay R, et al. Intrafollicular interleukin-8, interleukin-12, and adrenomedullin are the promising prognostic markers of oocyte and embryo quality in women with endometriosis. Journal of Assisted Reproduction and Genetics. 2016;33(10): 1363–1372. doi.org/10.1007/s10815-016-0782-5.
Choi YS, Cho S, Seo SK, et al. Alteration in the intrafollicular thiol-redox system in infertile women with endometriosis. Reproduction. 2015;149(2): 155–162. doi.org/10.1530/REP-14-0438.
Xu H, Schultze-Mosgau A, Agic A, et al. Regulated upon activation, normal T cell expressed and secreted (RANTES) and monocyte chemotactic protein 1 in follicular fluid accumulate differentially in patients with and without endometriosis undergoing in vitro fertilization. Fertility and Sterility. 2006;86(6): 1616–1620. doi.org/10.1016/j.fertnstert.2006.05.043.
Hahn DW, Carraher RP, Foldesy RG, et al. Experimental evidence for failure to implant as a mechanism of infertility associated with endometriosis. American Journal of Obstetrics and Gynecology. 1986;155(5): 1109–1113. doi.org/10.1016/0002-9378(86)90360-1.
Illera MJ, Juan L, Stewart CL, et al. Effect of peritoneal fluid from women with endometriosis on implantation in the mouse model. Fertility and Sterility. 2000;74(1): 41–48. doi.org/10.1016/s0015-0282(00)00552-5.
Brizek CL, Schlaff S, Pellegrini VA, et al. Increased incidence of aberrant morphological phenotypes in human embryogenesis--an association with endometriosis. Journal of Assisted Reproduction and Genetics. 1995;12(2): 106–112. doi.org/10.1007/BF02211378.
Schatten G, Simerly C, Schatten H. Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proceedings of the National Academy of Sciences of the United States of America. 1985;82(12): 4152–4156. doi.org/10.1073/pnas.82.12.4152.
Eroğlu A, Toth TL, Toner M. Alterations of the cytoskeleton and polyploidy induced by cryopreservation of metaphase II mouse oocytes. Fertility and Sterility. 1998;69(5): 944–957. doi.org/10.1016/s0015-0282(98)00030-2.
Horton J, Sterrenburg M, Lane S, et al. Reproductive, obstetric, and perinatal outcomes of women with adenomyosis and endometriosis: a systematic review and meta-analysis. Human Reproduction Update. 2019;25(5): 592–632. doi.org/10.1093/humupd/dmz012.
Nirgianakis K, Kalaitzopoulos DR, et al. Fertility, pregnancy and neonatal outcomes of patients with adenomyosis: a systematic review and meta-analysis. Reproductive Biomedicine Online. 2021;42(1): 185–206. doi.org/10.1016/j.rbmo.2020.09.023.
Liang T, Zhang W, Pan N, et al. Reproductive Outcomes of In Vitro Fertilization and Fresh Embryo Transfer in Infertile Women With Adenomyosis: A Retrospective Cohort Study. Frontiers in Endocrinology. 2022;13: 865358. doi.org/10.3389/fendo.2022.865358.
Setti AS, Figueira RCS, Braga DPAF, et al. Relationship between oocyte abnormal morphology and intracytoplasmic sperm injection outcomes: a meta-analysis. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2011;159(2): 364–370. doi.org/10.1016/j.ejogrb.2011.07.031.
Latif S, Saridogan E. Endometriosis, Oocyte, and Embryo Quality. Journal of Clinical Medicine. 2023;12(13). doi.org/10.3390/jcm12134186.
Robin C, Uk A, Decanter C, et al. Impact of endometriosis on oocyte morphology in IVF-ICSI: retrospective study of a cohort of more than 6000 mature oocytes. Reproductive Biology and Endocrinology : RB&E. 2021;19(1): 160. doi.org/10.1186/s12958-021-00798-x.
Metzemaekers J, Lust E, Rhemrev J, et al. Prognosis in fertilisation rate and outcome in IVF cycles in patients with and without endometriosis: a population-based comparative cohort study with controls. Facts, Views & Vision in ObGyn. 2021;13(1): 27–34. doi.org/10.52054/FVVO.13.1.007.
Sanchez AM, Vanni VS, Bartiromo L, et al. Is the oocyte quality affected by endometriosis? A review of the literature. Journal of Ovarian Research. 2017;10(1): 43. doi.org/10.1186/s13048-017-0341-4.
Rossi AC, Prefumo F. The effects of surgery for endometriosis on pregnancy outcomes following in vitro fertilization and embryo transfer: a systematic review and meta-analysis. Archives of Gynecology and Obstetrics. 2016;294(3): 647–655. doi.org/10.1007/s00404-016-4136-4.
Kasapoğlu I, Kuspınar G, Sarıbal S, et al. Detrimental effects of endometriosis on oocyte morphology in intracytoplasmic sperm injection cycles: a retrospective cohort study. Gynecological Endocrinology. 2018;34(3): 206–211. doi.org/10.1080/09513590.2017.1391203.
Boucret L, Bouet PE, Riou J, et al. Endometriosis Lowers the Cumulative Live Birth Rates in IVF by Decreasing the Number of Embryos but Not Their Quality. Journal of Clinical Medicine. 2020;9(8). doi.org/10.3390/jcm9082478.
Ata B, Telek SB. Assisted reproductive technology for women with endometriosis, a clinically oriented review. Current Opinion in Obstetrics & Gynecology. 2021;33(3): 225–231. doi.org/10.1097/GCO.0000000000000710.
Harb HM, Gallos ID, Chu J, et al. The effect of endometriosis on in vitro fertilisation outcome: a systematic review and meta-analysis. BJOG : an International Journal of Obstetrics and Gynaecology. 2013;120(11): 1308–1320. doi.org/10.1111/1471-0528.12366.
Senapati S, Sammel MD, Morse C, et al. Impact of endometriosis on in vitro fertilization outcomes: an evaluation of the Society for Assisted Reproductive Technologies Database. Fertility and Sterility. 2016;106(1): 164-171.e1. doi.org/10.1016/j.fertnstert.2016.03.037.
Kamath MS, Subramanian V, Antonisamy B, et al. Endometriosis and oocyte quality: an analysis of 13 614 donor oocyte recipient and autologous IVF cycles. Human Reproduction Open. 2022;2022(3): hoac025. doi.org/10.1093/hropen/hoac025.
Pages
193-204
Published
January 21, 2025
Copyright (c) 2025 Academician Publishing Book Portal
