Skip to main content
Top

21-02-2024 | Endometriosis | REVIEW

Endometrial Determinism of Endometriosis: An Unnecessary Adjunct to Retrograde Menstruation

Authors: Marwan Habiba, Sun-Wei Guo, Giuseppe Benagiano

Published in: Current Obstetrics and Gynecology Reports

Login to get access

Abstract

Purpose of Review

The observation that retrograde menstruation is almost universal while only a small proportion of women suffer with endometriosis is among the most quoted challenges to Sampson’s hypothesis. Addressing this challenge has focused on identifying unique features in the endometrium of affected women. The assumption that endometriosis develops from an aberrant endometrium forms the cornerstone of “endometrial determinism.” This review appraises the evidence for endometrial aberrations starting with an appraisal of retrograde menstruation.

Recent Findings

The quantity of endometrial tissue in retrograde menstruation is not well defined and is probably small, variable and its characteristics remain largely unknown. There are well documented differences between the eutopic endometrium in the presence and absence of endometriosis. On the other hand, at least some of the endometrial aberrations in endometriosis are the result of the disease and similar “defects” have been identified in the absence of endometriosis.

Summary

The evidence provided here challenges endometrial determinism as the primum movens in endometriosis. Indeed, it is unclear that the theory is a necessary adjunct to Sampson’s hypothesis. Further research is needed that can further our understanding of the natural history or endometriosis and that can enable the development of novel theories of its pathogenesis.
Literature
1.
go back to reference Sampson JA. The development of the implantation theory for the origin of peritoneal endometriosis. Am J Obstet Gynecol. 1940;40:549–57.CrossRef Sampson JA. The development of the implantation theory for the origin of peritoneal endometriosis. Am J Obstet Gynecol. 1940;40:549–57.CrossRef
2.
go back to reference Ulukus M, Cakmak H, Arici A. The role of endometrium in endometriosis. J Soc Gynecol Investig. 2006;13(7):467–76.PubMedCrossRef Ulukus M, Cakmak H, Arici A. The role of endometrium in endometriosis. J Soc Gynecol Investig. 2006;13(7):467–76.PubMedCrossRef
3.
go back to reference Lang JH. Cornerstone of study on endometriosis. Zhonghua Fu Chan Ke Za Zhi. 2005;40:3–4.PubMed Lang JH. Cornerstone of study on endometriosis. Zhonghua Fu Chan Ke Za Zhi. 2005;40:3–4.PubMed
4.
go back to reference Liang Y, Li Y, Liu K, Chen P, Wang D. Expression and significance of WNT4 in ectopic and eutopic endometrium of human endometriosis. Reprod Sci. 2016;23(3):379–85.PubMedCrossRef Liang Y, Li Y, Liu K, Chen P, Wang D. Expression and significance of WNT4 in ectopic and eutopic endometrium of human endometriosis. Reprod Sci. 2016;23(3):379–85.PubMedCrossRef
5.
go back to reference Guo SW, Habiba M, Benagiano G. From retrograde menstruation to endometrial determinism and a brave new world of “root treatment” of endometriosis: destiny or a fanciful utopia? Biomolecules. 2023;13(2):336.PubMedPubMedCentralCrossRef Guo SW, Habiba M, Benagiano G. From retrograde menstruation to endometrial determinism and a brave new world of “root treatment” of endometriosis: destiny or a fanciful utopia? Biomolecules. 2023;13(2):336.PubMedPubMedCentralCrossRef
6.
go back to reference Blumenkrantz MJ, Gallagher N, Bashore RA, Tenckhoff H. Retrograde menstruation in women undergoing chronic peritoneal dialysis. Obstet Gynecol. 1981;57(5):667–70.PubMed Blumenkrantz MJ, Gallagher N, Bashore RA, Tenckhoff H. Retrograde menstruation in women undergoing chronic peritoneal dialysis. Obstet Gynecol. 1981;57(5):667–70.PubMed
7.
go back to reference Halme J, Hammond MG, Hulka JF, Raj SG, Talbert LM. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol. 1984;64(2):151–4.PubMed Halme J, Hammond MG, Hulka JF, Raj SG, Talbert LM. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol. 1984;64(2):151–4.PubMed
8.
go back to reference Liu DT, Hitchcock A. Endometriosis: its association with retrograde menstruation, dysmenorrhoea and tubal pathology. Br J Obstet Gynaecol. 1986;93(8):859–62.PubMedCrossRef Liu DT, Hitchcock A. Endometriosis: its association with retrograde menstruation, dysmenorrhoea and tubal pathology. Br J Obstet Gynaecol. 1986;93(8):859–62.PubMedCrossRef
9.
go back to reference Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am. 1997;24(2):235–58.PubMedCrossRef Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am. 1997;24(2):235–58.PubMedCrossRef
10.
go back to reference Moradi Y, Shams-Beyranvand M, Khateri S, Gharahjeh S, Tehrani S, Varse F, Tiyuri A, Najmi Z. A systematic review on the prevalence of endometriosis in women. Indian J Med Res. 2021;154(3):446–54.PubMedPubMedCentralCrossRef Moradi Y, Shams-Beyranvand M, Khateri S, Gharahjeh S, Tehrani S, Varse F, Tiyuri A, Najmi Z. A systematic review on the prevalence of endometriosis in women. Indian J Med Res. 2021;154(3):446–54.PubMedPubMedCentralCrossRef
11.
go back to reference Leyendecker G, Herbertz M, Kunz G, Mall G. Endometriosis results from the dislocation of basal endometrium. Hum Reprod. 2002;17(10):2725–36.PubMedCrossRef Leyendecker G, Herbertz M, Kunz G, Mall G. Endometriosis results from the dislocation of basal endometrium. Hum Reprod. 2002;17(10):2725–36.PubMedCrossRef
12.
go back to reference D’Hooghe TM, Debrock S. Evidence that endometriosis results from the dislocation of basal endometrium? Hum Reprod. 2003;18(5):1130–1.PubMedCrossRef D’Hooghe TM, Debrock S. Evidence that endometriosis results from the dislocation of basal endometrium? Hum Reprod. 2003;18(5):1130–1.PubMedCrossRef
13.
go back to reference Dorning A, Dhami P, Panir K, Hogg C, Park E, Ferguson GD, Hargrove D, Karras J, Horne AW, Greaves E. Bioluminescent imaging in induced mouse models of endometriosis reveals differences in four model variations. Dis Model Mech. 2021;14(8):dmm.049070. https://doi.org/10.1242/dmm.049070.CrossRef Dorning A, Dhami P, Panir K, Hogg C, Park E, Ferguson GD, Hargrove D, Karras J, Horne AW, Greaves E. Bioluminescent imaging in induced mouse models of endometriosis reveals differences in four model variations. Dis Model Mech. 2021;14(8):dmm.049070. https://​doi.​org/​10.​1242/​dmm.​049070.CrossRef
14.
go back to reference Donnez O, Van Langendonckt A, Defrère S, Colette S, Van Kerk O, Dehoux JP, Squifflet J, Donnez J. Induction of endometriotic nodules in an experimental baboon model mimicking human deep nodular lesions. Fertil Steril. 2013;99(3):783–9.PubMedCrossRef Donnez O, Van Langendonckt A, Defrère S, Colette S, Van Kerk O, Dehoux JP, Squifflet J, Donnez J. Induction of endometriotic nodules in an experimental baboon model mimicking human deep nodular lesions. Fertil Steril. 2013;99(3):783–9.PubMedCrossRef
15.
go back to reference Donnez O, Soares M, Defrère S, Dehoux JP, van Langendonckt A, Donnez J, Dolmans MM, Colette S. Nerve fiber density in deep nodular endometriotic lesions induced in a baboon experimental model. Fertil Steril. 2013;100(4):1144–50.PubMedCrossRef Donnez O, Soares M, Defrère S, Dehoux JP, van Langendonckt A, Donnez J, Dolmans MM, Colette S. Nerve fiber density in deep nodular endometriotic lesions induced in a baboon experimental model. Fertil Steril. 2013;100(4):1144–50.PubMedCrossRef
16.
go back to reference Orellana R, García-Solares J, Donnez J, van Kerk O, Dolmans MM, Donnez O. Important role of collective cell migration and nerve fiber density in the development of deep nodular endometriosis. Fertil Steril. 2017;107(4):987–95.PubMedCrossRef Orellana R, García-Solares J, Donnez J, van Kerk O, Dolmans MM, Donnez O. Important role of collective cell migration and nerve fiber density in the development of deep nodular endometriosis. Fertil Steril. 2017;107(4):987–95.PubMedCrossRef
17.
go back to reference D’Hooghe TM, Debrock S. Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons. Hum Reprod Update. 2002;8(1):84–8.PubMedCrossRef D’Hooghe TM, Debrock S. Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons. Hum Reprod Update. 2002;8(1):84–8.PubMedCrossRef
18.
go back to reference D’Hooghe TM, Bambra CS, Raeymaekers BM, Koninckx PR. Increased prevalence and recurrence of retrograde menstruation in baboons with spontaneous endometriosis. Hum Reprod. 1996;11(9):2022–5.PubMedCrossRef D’Hooghe TM, Bambra CS, Raeymaekers BM, Koninckx PR. Increased prevalence and recurrence of retrograde menstruation in baboons with spontaneous endometriosis. Hum Reprod. 1996;11(9):2022–5.PubMedCrossRef
20.
go back to reference Scheenjes E, te Velde ER, Kremer J. Inspection of the ovaries and steroids in serum and peritoneal fluid at various time intervals after ovulation in fertile women: implications for the luteinized unruptured follicle syndrome. Fertil Steril. 1990;54(1):38–41.PubMedCrossRef Scheenjes E, te Velde ER, Kremer J. Inspection of the ovaries and steroids in serum and peritoneal fluid at various time intervals after ovulation in fertile women: implications for the luteinized unruptured follicle syndrome. Fertil Steril. 1990;54(1):38–41.PubMedCrossRef
21.
go back to reference Koninckx PR, Ide P, Vandenbroucke W, Brosens IA. New aspects of the pathophysiology of endometriosis and associated infertility. J Reprod Med. 1980;24(6):257–60.PubMed Koninckx PR, Ide P, Vandenbroucke W, Brosens IA. New aspects of the pathophysiology of endometriosis and associated infertility. J Reprod Med. 1980;24(6):257–60.PubMed
22.
go back to reference Bartosik D, Jacobs SL, Kelly LJ. Endometrial tissue in peritoneal fluid. Fertil Steril. 1986;46(5):796–800.PubMedCrossRef Bartosik D, Jacobs SL, Kelly LJ. Endometrial tissue in peritoneal fluid. Fertil Steril. 1986;46(5):796–800.PubMedCrossRef
23.
go back to reference Beyth Y, Yaffe H, Levij ISh, Sadovsky E. Retrograde seeding of endometrium: sequela of tubal flushing. Fertil Steril. 1975;26:1094–7.PubMedCrossRef Beyth Y, Yaffe H, Levij ISh, Sadovsky E. Retrograde seeding of endometrium: sequela of tubal flushing. Fertil Steril. 1975;26:1094–7.PubMedCrossRef
24.
go back to reference Nagele F, Wieser F, Deery A, Hart R, Magos A. Endometrial cell dissemination at diagnostic hysteroscopy: a prospective randomized cross-over comparison of normal saline and carbon dioxide uterine distension. Hum Reprod. 1999;14(11):2739–42.PubMedCrossRef Nagele F, Wieser F, Deery A, Hart R, Magos A. Endometrial cell dissemination at diagnostic hysteroscopy: a prospective randomized cross-over comparison of normal saline and carbon dioxide uterine distension. Hum Reprod. 1999;14(11):2739–42.PubMedCrossRef
25.
go back to reference van der Linden PJ, Dunselman GA, de Goeij AF, van der Linden EP, Evers JL, Ramaekers FC. Epithelial cells in peritoneal fluid - of endometrial origin? Am J Obstet Gynecol. 1995;173(2):566–70.PubMedCrossRef van der Linden PJ, Dunselman GA, de Goeij AF, van der Linden EP, Evers JL, Ramaekers FC. Epithelial cells in peritoneal fluid - of endometrial origin? Am J Obstet Gynecol. 1995;173(2):566–70.PubMedCrossRef
26.
go back to reference Portuondo JA, Herrán C, Echanojauregui AD, Riego AG. Peritoneal flushing and biopsy in laparoscopically diagnosed endometriosis. Fertil Steril. 1982;38(5):538–41.PubMedCrossRef Portuondo JA, Herrán C, Echanojauregui AD, Riego AG. Peritoneal flushing and biopsy in laparoscopically diagnosed endometriosis. Fertil Steril. 1982;38(5):538–41.PubMedCrossRef
27.
go back to reference Badawy SZ, Cuenca V, Marshall L, Munchback R, Rinas AC, Coble DA. Cellular components in peritoneal fluid in infertile patients with and without endometriosis. Fertil Steril. 1984;42(5):704–8.PubMedCrossRef Badawy SZ, Cuenca V, Marshall L, Munchback R, Rinas AC, Coble DA. Cellular components in peritoneal fluid in infertile patients with and without endometriosis. Fertil Steril. 1984;42(5):704–8.PubMedCrossRef
28.
go back to reference Goldstein DP, De Cholnoky C, Emans SJ. Adolescent endometriosis. J Adolesc Health Care. 1980;1(1):37–41.PubMedCrossRef Goldstein DP, De Cholnoky C, Emans SJ. Adolescent endometriosis. J Adolesc Health Care. 1980;1(1):37–41.PubMedCrossRef
29.
go back to reference Bokor A, Debrock S, Drijkoningen M, Goossens W, Fülöp V, D’Hooghe T. Quantity and quality of retrograde menstruation: a case control study. Reprod Biol Endocrinol. 2009;7:123.PubMedPubMedCentralCrossRef Bokor A, Debrock S, Drijkoningen M, Goossens W, Fülöp V, D’Hooghe T. Quantity and quality of retrograde menstruation: a case control study. Reprod Biol Endocrinol. 2009;7:123.PubMedPubMedCentralCrossRef
30.
go back to reference Sharpe-Timms KL. Haptoglobin expression by shed endometrial tissue fragments found in peritoneal fluid. Fertil Steril. 2005;84(1):22–30.PubMedCrossRef Sharpe-Timms KL. Haptoglobin expression by shed endometrial tissue fragments found in peritoneal fluid. Fertil Steril. 2005;84(1):22–30.PubMedCrossRef
31.
go back to reference Kruitwagen RF, Poels LG, Willemsen WN, Jap PH, de Ronde IJ, Hanselaar TG, Rolland R. Immunocytochemical markerprofile of endometriotic epithelial, endometrial epithelial, and mesothelial cells: a comparative study. Eur J Obstet Gynecol Reprod Biol. 1991;41:215–23.PubMedCrossRef Kruitwagen RF, Poels LG, Willemsen WN, Jap PH, de Ronde IJ, Hanselaar TG, Rolland R. Immunocytochemical markerprofile of endometriotic epithelial, endometrial epithelial, and mesothelial cells: a comparative study. Eur J Obstet Gynecol Reprod Biol. 1991;41:215–23.PubMedCrossRef
32.
go back to reference Willemsen WN, Mungyer G, Smets H, Rolland R, Vemer H, Jap P. Behavior of cultured glandular cells obtained by flushing of the uterine cavity. Fertil Steril. 1985;44(1):92–5.PubMedCrossRef Willemsen WN, Mungyer G, Smets H, Rolland R, Vemer H, Jap P. Behavior of cultured glandular cells obtained by flushing of the uterine cavity. Fertil Steril. 1985;44(1):92–5.PubMedCrossRef
33.
go back to reference Kruitwagen RF, Poels LG, Willemsen WN, de Ronde IJ, Jap PH, Rolland R. Endometrial epithelial cells in peritoneal fluid during the early follicular phase. Fertil Steril. 1991;55(2):297–303.PubMedCrossRef Kruitwagen RF, Poels LG, Willemsen WN, de Ronde IJ, Jap PH, Rolland R. Endometrial epithelial cells in peritoneal fluid during the early follicular phase. Fertil Steril. 1991;55(2):297–303.PubMedCrossRef
34.
go back to reference D’Hooghe TM, Bambra CS, De Jonge I, Lauweryns JM, Koninckx PR. The prevalence of spontaneous endometriosis in the baboon (Papio anubis, Papio cynocephalus) increases with the duration of captivity. Acta Obstet Gynecol Scand. 1996;75(2):98–101.PubMedCrossRef D’Hooghe TM, Bambra CS, De Jonge I, Lauweryns JM, Koninckx PR. The prevalence of spontaneous endometriosis in the baboon (Papio anubis, Papio cynocephalus) increases with the duration of captivity. Acta Obstet Gynecol Scand. 1996;75(2):98–101.PubMedCrossRef
35.
go back to reference D’Hooghe TM, Bambra CS, Raeymaekers BM, Koninckx PR. Development of spontaneous endometriosis in baboons. Obstet Gynecol. 1996;88(3):462–6.PubMedCrossRef D’Hooghe TM, Bambra CS, Raeymaekers BM, Koninckx PR. Development of spontaneous endometriosis in baboons. Obstet Gynecol. 1996;88(3):462–6.PubMedCrossRef
36.
go back to reference D’Hooghe TM. Clinical relevance of the baboon as a model for the study of endometriosis. Fertil Steril. 1997;68(4):613–25.PubMedCrossRef D’Hooghe TM. Clinical relevance of the baboon as a model for the study of endometriosis. Fertil Steril. 1997;68(4):613–25.PubMedCrossRef
37.
go back to reference Liu X, Long Q, Guo SW. Surgical history and the risk of endometriosis: a hospital-based case-control study. Reprod Sci. 2016;23(9):1217–24.PubMedCrossRef Liu X, Long Q, Guo SW. Surgical history and the risk of endometriosis: a hospital-based case-control study. Reprod Sci. 2016;23(9):1217–24.PubMedCrossRef
38.
go back to reference Long Q, Liu X, Guo SW. Surgery accelerates the development of endometriosis in mice. Am J Obstet Gynecol. 2016;215(3):320.e1-320.PubMedCrossRef Long Q, Liu X, Guo SW. Surgery accelerates the development of endometriosis in mice. Am J Obstet Gynecol. 2016;215(3):320.e1-320.PubMedCrossRef
39.
go back to reference Dehoux JP, Defrère S, Squifflet J, Donnez O, Polet R, Mestdagt M, Foidart JM, Van Langendonckt A, Donnez J. Is the baboon model appropriate for endometriosis studies? Fertil Steril. 2011;96(3):728–33.PubMedCrossRef Dehoux JP, Defrère S, Squifflet J, Donnez O, Polet R, Mestdagt M, Foidart JM, Van Langendonckt A, Donnez J. Is the baboon model appropriate for endometriosis studies? Fertil Steril. 2011;96(3):728–33.PubMedCrossRef
40.
go back to reference te Linde RW, Scott RB. Experimental endometriosis. Am J Obstet Gynecol. 1950;60(5):1147–73.CrossRef te Linde RW, Scott RB. Experimental endometriosis. Am J Obstet Gynecol. 1950;60(5):1147–73.CrossRef
41.
go back to reference D’Hooghe TM, Bambra CS, Raeymaekers BM, De Jonge I, Lauweryns JM, Koninckx PR. Intrapelvic injection of menstrual endometrium causes endometriosis in baboons (Papio cynocephalus and Papio anubis). Am J Obstet Gynecol. 1995;173(1):125–34.PubMedCrossRef D’Hooghe TM, Bambra CS, Raeymaekers BM, De Jonge I, Lauweryns JM, Koninckx PR. Intrapelvic injection of menstrual endometrium causes endometriosis in baboons (Papio cynocephalus and Papio anubis). Am J Obstet Gynecol. 1995;173(1):125–34.PubMedCrossRef
42.
go back to reference Harirchian P, Gashaw I, Lipskind ST, Braundmeier AG, Hastings JM, Olson MR, Fazleabas AT. Lesion kinetics in a non-human primate model of endometriosis. Hum Reprod. 2012;27(8):2341–51.PubMedPubMedCentralCrossRef Harirchian P, Gashaw I, Lipskind ST, Braundmeier AG, Hastings JM, Olson MR, Fazleabas AT. Lesion kinetics in a non-human primate model of endometriosis. Hum Reprod. 2012;27(8):2341–51.PubMedPubMedCentralCrossRef
43.
go back to reference Slayden OD, Luo F, Martin DVMLD. A protocol for creating endometriosis in rhesus macaques (Macaca mulatta). J Med Primatol. 2023;52(6):405–13.PubMedCrossRef Slayden OD, Luo F, Martin DVMLD. A protocol for creating endometriosis in rhesus macaques (Macaca mulatta). J Med Primatol. 2023;52(6):405–13.PubMedCrossRef
44.
go back to reference Vercellini P, Bandini V, Viganò P, Ambruoso D, Cetera GE, Somigliana E. Proposal for targeted, neo-evolutionary-oriented secondary prevention of early-onset endometriosis and adenomyosis. Part II: medical interventions Hum Reprod. 2024;39(1):18–34.PubMed Vercellini P, Bandini V, Viganò P, Ambruoso D, Cetera GE, Somigliana E. Proposal for targeted, neo-evolutionary-oriented secondary prevention of early-onset endometriosis and adenomyosis. Part II: medical interventions Hum Reprod. 2024;39(1):18–34.PubMed
45.
go back to reference Olive DL, Henderson DY. Endometriosis and Müllerian anomalies. Obstet Gynecol. 1987;69(3 Pt 1):412–5.PubMed Olive DL, Henderson DY. Endometriosis and Müllerian anomalies. Obstet Gynecol. 1987;69(3 Pt 1):412–5.PubMed
46.
go back to reference Matalliotakis M, Goulielmos GN, Matalliotaki C, Trivli A, Matalliotakis I, Arici A. Endometriosis in adolescent and young girls: report on a series of 55 cases. J Pediatr Adolesc Gynecol. 2017;30(5):568–70.PubMedCrossRef Matalliotakis M, Goulielmos GN, Matalliotaki C, Trivli A, Matalliotakis I, Arici A. Endometriosis in adolescent and young girls: report on a series of 55 cases. J Pediatr Adolesc Gynecol. 2017;30(5):568–70.PubMedCrossRef
47.
go back to reference Fedele L, Bianchi S, Di Nola G, Franchi D, Candiani GB. Endometriosis and nonobstructive müllerian anomalies. Obstet Gynecol. 1992;79(4):515–7.PubMed Fedele L, Bianchi S, Di Nola G, Franchi D, Candiani GB. Endometriosis and nonobstructive müllerian anomalies. Obstet Gynecol. 1992;79(4):515–7.PubMed
48.
go back to reference Uğur M, Turan C, Mungan T, Kuşçu E, Senöz S, Ağiş HT, Gökmen O. Endometriosis in association with Müllerian anomalies. Gynecol Obstet Invest. 1995;40(4):261–4.PubMedCrossRef Uğur M, Turan C, Mungan T, Kuşçu E, Senöz S, Ağiş HT, Gökmen O. Endometriosis in association with Müllerian anomalies. Gynecol Obstet Invest. 1995;40(4):261–4.PubMedCrossRef
49.
go back to reference Pitot MA, Bookwalter CA, Dudiak KM. Müllerian duct anomalies coincident with endometriosis: a review. Abdom Radiol (NY). 2020;45(6):1723–40.PubMedCrossRef Pitot MA, Bookwalter CA, Dudiak KM. Müllerian duct anomalies coincident with endometriosis: a review. Abdom Radiol (NY). 2020;45(6):1723–40.PubMedCrossRef
50.
go back to reference Barbieri RL. Stenosis of the external cervical os: an association with endometriosis in women with chronic pelvic pain. Fertil Steril. 1998;70(3):571–3.PubMedCrossRef Barbieri RL. Stenosis of the external cervical os: an association with endometriosis in women with chronic pelvic pain. Fertil Steril. 1998;70(3):571–3.PubMedCrossRef
51.
go back to reference Spechler S, Nieman LK, Premkumar A, Stratton P. The Keeper, a menstrual collection device, as a potential cause of endometriosis and adenomyosis. Gynecol Obstet Invest. 2003;56(1):35–7.PubMedCrossRef Spechler S, Nieman LK, Premkumar A, Stratton P. The Keeper, a menstrual collection device, as a potential cause of endometriosis and adenomyosis. Gynecol Obstet Invest. 2003;56(1):35–7.PubMedCrossRef
52.
go back to reference Mollazadeh S, Sadeghzadeh Oskouei B, Kamalifard M, Mirghafourvand M, Aminisani N, Jafari SM. Association between sexual activity during menstruation and endometriosis: a case-control study. Int J Fertil Steril. 2019;13(3):230–5.PubMedPubMedCentral Mollazadeh S, Sadeghzadeh Oskouei B, Kamalifard M, Mirghafourvand M, Aminisani N, Jafari SM. Association between sexual activity during menstruation and endometriosis: a case-control study. Int J Fertil Steril. 2019;13(3):230–5.PubMedPubMedCentral
53.
go back to reference Filer RB, Wu CH. Coitus during menses. Its effect on endometriosis and pelvic inflammatory disease. J Reprod Med. 1989;34(11):887–90.PubMed Filer RB, Wu CH. Coitus during menses. Its effect on endometriosis and pelvic inflammatory disease. J Reprod Med. 1989;34(11):887–90.PubMed
54.
go back to reference Meaddough EL, Olive DL, Gallup P, Perlin M, Kliman HJ. Sexual activity, orgasm and tampon use are associated with a decreased risk for endometriosis. Gynecol Obstet Invest. 2002;53(3):163–9.PubMedCrossRef Meaddough EL, Olive DL, Gallup P, Perlin M, Kliman HJ. Sexual activity, orgasm and tampon use are associated with a decreased risk for endometriosis. Gynecol Obstet Invest. 2002;53(3):163–9.PubMedCrossRef
55.
go back to reference Arumugam K, Lim JM. Menstrual characteristics associated with endometriosis. Br J Obstet Gynaecol. 1997;104(8):948–50.PubMedCrossRef Arumugam K, Lim JM. Menstrual characteristics associated with endometriosis. Br J Obstet Gynaecol. 1997;104(8):948–50.PubMedCrossRef
56.
go back to reference Mahmood TA, Templeton AA, Thomson L, Fraser C. Menstrual symptoms in women with pelvic endometriosis. Br J Obstet Gynaecol. 1991;98(6):558–63.PubMedCrossRef Mahmood TA, Templeton AA, Thomson L, Fraser C. Menstrual symptoms in women with pelvic endometriosis. Br J Obstet Gynaecol. 1991;98(6):558–63.PubMedCrossRef
57.
go back to reference Vercellini P, De Giorgi O, Aimi G, Panazza S, Uglietti A, Crosignani PG. Menstrual characteristics in women with and without endometriosis. Obstet Gynecol. 1997;90(2):264–8.PubMedCrossRef Vercellini P, De Giorgi O, Aimi G, Panazza S, Uglietti A, Crosignani PG. Menstrual characteristics in women with and without endometriosis. Obstet Gynecol. 1997;90(2):264–8.PubMedCrossRef
58.
go back to reference Cramer DW, Wilson E, Stillman RJ, Berger MJ, Belisle S, Schiff I, Albrecht B, Gibson M, Stadel BV, Schoenbaum SC. The relation of endometriosis to menstrual characteristics, smoking, and exercise. JAMA. 1986;255(14):1904–8.PubMedCrossRef Cramer DW, Wilson E, Stillman RJ, Berger MJ, Belisle S, Schiff I, Albrecht B, Gibson M, Stadel BV, Schoenbaum SC. The relation of endometriosis to menstrual characteristics, smoking, and exercise. JAMA. 1986;255(14):1904–8.PubMedCrossRef
59.
go back to reference Treloar SA, Bell TA, Nagle CM, Purdie DM, Green AC. Early menstrual characteristics associated with subsequent diagnosis of endometriosis. Am J Obstet Gynecol. 2010;202(6):534.e1-534.e5346.PubMedCrossRef Treloar SA, Bell TA, Nagle CM, Purdie DM, Green AC. Early menstrual characteristics associated with subsequent diagnosis of endometriosis. Am J Obstet Gynecol. 2010;202(6):534.e1-534.e5346.PubMedCrossRef
60.
go back to reference Smolarz B, Szyłło K, Romanowicz H. Endometriosis: epidemiology, classification, pathogenesis, treatment and genetics (review of literature). Int J Mol Sci. 2021;22(19):10554.PubMedPubMedCentralCrossRef Smolarz B, Szyłło K, Romanowicz H. Endometriosis: epidemiology, classification, pathogenesis, treatment and genetics (review of literature). Int J Mol Sci. 2021;22(19):10554.PubMedPubMedCentralCrossRef
61.
go back to reference Evers JL. Endometriosis does not exist; all women have endometriosis. Hum Reprod. 1994;9(12):2206–9.PubMedCrossRef Evers JL. Endometriosis does not exist; all women have endometriosis. Hum Reprod. 1994;9(12):2206–9.PubMedCrossRef
63.
go back to reference Murphy AA, Green WR, Bobbie D, dela Cruz ZC, Rock JA. Unsuspected endometriosis documented by scanning electron microscopy in visually normal peritoneum. Fertil Steril. 1986;46(3):522–4.PubMedCrossRef Murphy AA, Green WR, Bobbie D, dela Cruz ZC, Rock JA. Unsuspected endometriosis documented by scanning electron microscopy in visually normal peritoneum. Fertil Steril. 1986;46(3):522–4.PubMedCrossRef
64.
go back to reference Redwine DB. Is “microscopic” peritoneal endometriosis invisible? Fertil Steril. 1988;50(4):665–6.PubMedCrossRef Redwine DB. Is “microscopic” peritoneal endometriosis invisible? Fertil Steril. 1988;50(4):665–6.PubMedCrossRef
65.
go back to reference Nezhat F, Allan CJ, Nezhat C, Martin DC. Nonvisualized endometriosis at laparoscopy. Int J Fertil. 1991;36(6):340–3.PubMed Nezhat F, Allan CJ, Nezhat C, Martin DC. Nonvisualized endometriosis at laparoscopy. Int J Fertil. 1991;36(6):340–3.PubMed
66.
go back to reference Hopton EN, Redwine DB. Eyes wide shut: the illusory tale of ‘occult’ microscopic endometriosis. Hum Reprod. 2014;29(3):384–7.PubMedCrossRef Hopton EN, Redwine DB. Eyes wide shut: the illusory tale of ‘occult’ microscopic endometriosis. Hum Reprod. 2014;29(3):384–7.PubMedCrossRef
67.
go back to reference Khan KN, Fujishita A, Kitajima M, Hiraki K, Nakashima M, Masuzaki H. Occult microscopic endometriosis: undetectable by laparoscopy in normal peritoneum. Hum Reprod. 2014;29(3):462–72.PubMedCrossRef Khan KN, Fujishita A, Kitajima M, Hiraki K, Nakashima M, Masuzaki H. Occult microscopic endometriosis: undetectable by laparoscopy in normal peritoneum. Hum Reprod. 2014;29(3):462–72.PubMedCrossRef
68.
go back to reference Chopyak VV, Koval HD, Havrylyuk AM, Lishchuk-Yakymovych KA, Potomkina HA, Kurpisz MK. Immunopathogenesis of endometriosis - a novel look at an old problem. Cent Eur J Immunol. 2022;47(1):109–16.PubMedPubMedCentralCrossRef Chopyak VV, Koval HD, Havrylyuk AM, Lishchuk-Yakymovych KA, Potomkina HA, Kurpisz MK. Immunopathogenesis of endometriosis - a novel look at an old problem. Cent Eur J Immunol. 2022;47(1):109–16.PubMedPubMedCentralCrossRef
69.
go back to reference Villanacci R, Bandini V, Ottolina J, Pagliardini L, Candiani M, Viganò P. The pathogenesis of endometriosis: clues from the immunological evidence. Minerva Obstet Gynecol. 2021;73(3):275–82.PubMedCrossRef Villanacci R, Bandini V, Ottolina J, Pagliardini L, Candiani M, Viganò P. The pathogenesis of endometriosis: clues from the immunological evidence. Minerva Obstet Gynecol. 2021;73(3):275–82.PubMedCrossRef
70.
go back to reference Anderson G. Endometriosis pathoetiology and pathophysiology: roles of vitamin A, estrogen, immunity, adipocytes, gut microbiome and melatonergic pathway on mitochondria regulation. Biomol Concepts. 2019;10(1):133–49.PubMedCrossRef Anderson G. Endometriosis pathoetiology and pathophysiology: roles of vitamin A, estrogen, immunity, adipocytes, gut microbiome and melatonergic pathway on mitochondria regulation. Biomol Concepts. 2019;10(1):133–49.PubMedCrossRef
71.
go back to reference Yamaguchi M, Yoshihara K, Yachida N, Suda K, Tamura R, Ishiguro T, Enomoto T. The new era of three-dimensional histoarchitecture of the human endometrium. J Pers Med. 2021;11(8):713.PubMedPubMedCentralCrossRef Yamaguchi M, Yoshihara K, Yachida N, Suda K, Tamura R, Ishiguro T, Enomoto T. The new era of three-dimensional histoarchitecture of the human endometrium. J Pers Med. 2021;11(8):713.PubMedPubMedCentralCrossRef
72.
go back to reference Schmidt WA, Karon M. Three-dimensional subgross morphology of the human endometrium. Diagn Gynecol Obstet. 1981;3(3):193–203.PubMed Schmidt WA, Karon M. Three-dimensional subgross morphology of the human endometrium. Diagn Gynecol Obstet. 1981;3(3):193–203.PubMed
73.
go back to reference Donnez J, Nisolle M, Casanas-Roux F. Three-dimensional architectures of peritoneal endometriosis. Fertil Steril. 1992;57(5):980–3.PubMedCrossRef Donnez J, Nisolle M, Casanas-Roux F. Three-dimensional architectures of peritoneal endometriosis. Fertil Steril. 1992;57(5):980–3.PubMedCrossRef
74.
go back to reference Yamaguchi M, Yoshihara K, Suda K, Nakaoka H, Yachida N, Ueda H, Sugino K, Mori Y, Yamawaki K, Tamura R, Ishiguro T, Motoyama T, Watanabe Y, Okuda S, Tainaka K, Enomoto T. Three-dimensional understanding of the morphological complexity of the human uterine endometrium. iScience. 2021;24(4):102258.ADSPubMedPubMedCentralCrossRef Yamaguchi M, Yoshihara K, Suda K, Nakaoka H, Yachida N, Ueda H, Sugino K, Mori Y, Yamawaki K, Tamura R, Ishiguro T, Motoyama T, Watanabe Y, Okuda S, Tainaka K, Enomoto T. Three-dimensional understanding of the morphological complexity of the human uterine endometrium. iScience. 2021;24(4):102258.ADSPubMedPubMedCentralCrossRef
75.
go back to reference Yamaguchi M, Nakaoka H, Suda K, et al. Spatiotemporal dynamics of clonal selection and diversification in normal endometrial epithelium. Nat Commun. 2022;13(1):943.ADSPubMedPubMedCentralCrossRef Yamaguchi M, Nakaoka H, Suda K, et al. Spatiotemporal dynamics of clonal selection and diversification in normal endometrial epithelium. Nat Commun. 2022;13(1):943.ADSPubMedPubMedCentralCrossRef
76.
go back to reference Fasciani A, Bocci G, Xu J, Bielecki R, Greenblatt E, Leyland N, Casper RF. Three-dimensional in vitro culture of endometrial explants mimics the early stages of endometriosis. Fertil Steril. 2003;80(5):1137–43.PubMedCrossRef Fasciani A, Bocci G, Xu J, Bielecki R, Greenblatt E, Leyland N, Casper RF. Three-dimensional in vitro culture of endometrial explants mimics the early stages of endometriosis. Fertil Steril. 2003;80(5):1137–43.PubMedCrossRef
77.
go back to reference Dundon M, Madden O, Comizzoli P. Three-dimensional culture of endometrial cells from domestic cats: a new in vitro platform for assessing plastic toxicity. PLoS ONE. 2019;14(5):e0217365.PubMedPubMedCentralCrossRef Dundon M, Madden O, Comizzoli P. Three-dimensional culture of endometrial cells from domestic cats: a new in vitro platform for assessing plastic toxicity. PLoS ONE. 2019;14(5):e0217365.PubMedPubMedCentralCrossRef
78.
go back to reference Abbas Y, Brunel LG, Hollinshead MS, Fernando RC, Gardner L, Duncan I, Moffett A, Best S, Turco MY, Burton GJ, Cameron RE. Generation of a three-dimensional collagen scaffold-based model of the human endometrium. Interface Focus. 2020;10(2):20190079.PubMedPubMedCentralCrossRef Abbas Y, Brunel LG, Hollinshead MS, Fernando RC, Gardner L, Duncan I, Moffett A, Best S, Turco MY, Burton GJ, Cameron RE. Generation of a three-dimensional collagen scaffold-based model of the human endometrium. Interface Focus. 2020;10(2):20190079.PubMedPubMedCentralCrossRef
79.
go back to reference Ahn J, Yoon MJ, Hong SH, Cha H, Lee D, Koo HS, Ko JE, Lee J, Oh S, Jeon NL, Kang YJ. Three-dimensional microengineered vascularised endometrium-on-a-chip. Hum Reprod. 2021;36(10):2720–31.PubMedPubMedCentralCrossRef Ahn J, Yoon MJ, Hong SH, Cha H, Lee D, Koo HS, Ko JE, Lee J, Oh S, Jeon NL, Kang YJ. Three-dimensional microengineered vascularised endometrium-on-a-chip. Hum Reprod. 2021;36(10):2720–31.PubMedPubMedCentralCrossRef
80.
go back to reference Wu Y, Basir Z, Kajdacsy-Balla A, Strawn E, Macias V, Montgomery K, Guo SW. Resolution of clonal origins for endometriotic lesions using laser capture microdissection and the human androgen receptor (HUMARA) assay. Fertil Steril. 2003;79(Suppl 1):710–7.PubMedCrossRef Wu Y, Basir Z, Kajdacsy-Balla A, Strawn E, Macias V, Montgomery K, Guo SW. Resolution of clonal origins for endometriotic lesions using laser capture microdissection and the human androgen receptor (HUMARA) assay. Fertil Steril. 2003;79(Suppl 1):710–7.PubMedCrossRef
81.
go back to reference Li L, Antero MF, Zhang M, Chu T, Seckin T, Ayhan A, Pisanic T, Wang TL, Cope L, Segars J, Shih IM. Mutation and methylation profiles of ectopic and eutopic endometrial tissues. J Pathol. 2021;255(4):387–98.PubMedPubMedCentralCrossRef Li L, Antero MF, Zhang M, Chu T, Seckin T, Ayhan A, Pisanic T, Wang TL, Cope L, Segars J, Shih IM. Mutation and methylation profiles of ectopic and eutopic endometrial tissues. J Pathol. 2021;255(4):387–98.PubMedPubMedCentralCrossRef
82.
go back to reference Yi D, Lang J, Zhu L, Leng J. The present and future of diagnosis and treatment of endometriosis (in Chinese). Sci Sin Vitae. 2021;51:1017–23.CrossRef Yi D, Lang J, Zhu L, Leng J. The present and future of diagnosis and treatment of endometriosis (in Chinese). Sci Sin Vitae. 2021;51:1017–23.CrossRef
83.
go back to reference Benagiano G, Brosens I, Habiba M. Structural and molecular features of the endomyometrium in endometriosis and adenomyosis. Hum Reprod Update. 2014;20(3):386–402.PubMedCrossRef Benagiano G, Brosens I, Habiba M. Structural and molecular features of the endomyometrium in endometriosis and adenomyosis. Hum Reprod Update. 2014;20(3):386–402.PubMedCrossRef
84.
go back to reference Lawson C, Bourcier N, Al-Akoum M, Maheux R, Naud F, Akoum A. Abnormal interleukin 1 receptor types I and II gene expression in eutopic and ectopic endometrial tissues of women with endometriosis. J Reprod Immunol. 2008;77(1):75–84.PubMedCrossRef Lawson C, Bourcier N, Al-Akoum M, Maheux R, Naud F, Akoum A. Abnormal interleukin 1 receptor types I and II gene expression in eutopic and ectopic endometrial tissues of women with endometriosis. J Reprod Immunol. 2008;77(1):75–84.PubMedCrossRef
86.
88.
go back to reference Laganà AS, Garzon S, Götte M, Viganò P, Franchi M, Ghezzi F, Martin DC. The pathogenesis of endometriosis: molecular and cell biology insights. Int J Mol Sci. 2019;20(22):5615.PubMedPubMedCentralCrossRef Laganà AS, Garzon S, Götte M, Viganò P, Franchi M, Ghezzi F, Martin DC. The pathogenesis of endometriosis: molecular and cell biology insights. Int J Mol Sci. 2019;20(22):5615.PubMedPubMedCentralCrossRef
89.
go back to reference Patel BG, Rudnicki M, Yu J, Shu Y, Taylor RN. Progesterone resistance in endometriosis: origins, consequences and interventions. Acta Obstet Gynecol Scand. 2017;96(6):623–32.PubMedCrossRef Patel BG, Rudnicki M, Yu J, Shu Y, Taylor RN. Progesterone resistance in endometriosis: origins, consequences and interventions. Acta Obstet Gynecol Scand. 2017;96(6):623–32.PubMedCrossRef
90.
go back to reference Zhang X, Lu B, Huang X, Xu H, Zhou C, Lin J. Innervation of endometrium and myometrium in women with painful adenomyosis and uterine fibroids. Fertil Steril. 2010;94(2):730–7.PubMedCrossRef Zhang X, Lu B, Huang X, Xu H, Zhou C, Lin J. Innervation of endometrium and myometrium in women with painful adenomyosis and uterine fibroids. Fertil Steril. 2010;94(2):730–7.PubMedCrossRef
91.
go back to reference Miller EJ, Fraser IS. The importance of pelvic nerve fibers in endometriosis. Womens Health (Lond). 2015;11(5):611–8.PubMedCrossRef Miller EJ, Fraser IS. The importance of pelvic nerve fibers in endometriosis. Womens Health (Lond). 2015;11(5):611–8.PubMedCrossRef
92.
go back to reference Yadav G, Rao M, Gothwal M, Singh P, Kathuria P, Sharma PP. Detection of nerve fibers in the eutopic endometrium of women with endometriosis, uterine fibroids and adenomyosis. Obstet Gynecol Sci. 2021;64(5):454–61.PubMedPubMedCentralCrossRef Yadav G, Rao M, Gothwal M, Singh P, Kathuria P, Sharma PP. Detection of nerve fibers in the eutopic endometrium of women with endometriosis, uterine fibroids and adenomyosis. Obstet Gynecol Sci. 2021;64(5):454–61.PubMedPubMedCentralCrossRef
93.
go back to reference Scutiero G, Iannone P, Bernardi G, Bonaccorsi G, Spadaro S, Volta CA, Greco P, Nappi L. Oxidative stress and endometriosis: a systematic review of the literature. Oxid Med Cell Longev. 2017;2017:7265238.PubMedPubMedCentralCrossRef Scutiero G, Iannone P, Bernardi G, Bonaccorsi G, Spadaro S, Volta CA, Greco P, Nappi L. Oxidative stress and endometriosis: a systematic review of the literature. Oxid Med Cell Longev. 2017;2017:7265238.PubMedPubMedCentralCrossRef
94.
go back to reference Carvalho LF, Abrão MS, Biscotti C, Sharma R, Nutter B, Falcone T. Oxidative cell injury as a predictor of endometriosis progression. Reprod Sci. 2013;20(6):688–98.PubMedCrossRef Carvalho LF, Abrão MS, Biscotti C, Sharma R, Nutter B, Falcone T. Oxidative cell injury as a predictor of endometriosis progression. Reprod Sci. 2013;20(6):688–98.PubMedCrossRef
95.
go back to reference Laschke MW, Menger MD. Basic mechanisms of vascularization in endometriosis and their clinical implications. Hum Reprod Update. 2018;24(2):207–24.PubMedCrossRef Laschke MW, Menger MD. Basic mechanisms of vascularization in endometriosis and their clinical implications. Hum Reprod Update. 2018;24(2):207–24.PubMedCrossRef
96.
go back to reference • Walker ER, McGrane M, Aplin JD, Brison DR, Ruane PT. A systematic review of transcriptomic studies of the human endometrium reveals inconsistently reported differentially expressed genes. Reprod Fertil. Published online June 1, 2023. https://doi.org/10.1530/RAF-22-0115. The review reveals important limitations that hinder collation of results of published studies of transcriptomes obtained from the endometrium in endometriosis. • Walker ER, McGrane M, Aplin JD, Brison DR, Ruane PT. A systematic review of transcriptomic studies of the human endometrium reveals inconsistently reported differentially expressed genes. Reprod Fertil. Published online June 1, 2023. https://​doi.​org/​10.​1530/​RAF-22-0115. The review reveals important limitations that hinder collation of results of published studies of transcriptomes obtained from the endometrium in endometriosis.
97.
go back to reference Prašnikar E, Knez J, Kovačič B, Kunej T. Molecular signature of eutopic endometrium in endometriosis based on the multi-omics integrative synthesis. J Assist Reprod Genet. 2020;37(7):1593–611.PubMedPubMedCentralCrossRef Prašnikar E, Knez J, Kovačič B, Kunej T. Molecular signature of eutopic endometrium in endometriosis based on the multi-omics integrative synthesis. J Assist Reprod Genet. 2020;37(7):1593–611.PubMedPubMedCentralCrossRef
98.
go back to reference Barlow DH, Kennedy S. Endometriosis: new genetic approaches and therapy. Annu Rev Med. 2005;56:345–56.PubMedCrossRef Barlow DH, Kennedy S. Endometriosis: new genetic approaches and therapy. Annu Rev Med. 2005;56:345–56.PubMedCrossRef
99.
go back to reference Di W, Guo SW. The search for genetic variants predisposing women to endometriosis. Curr Opin Obstet Gynecol. 2007;19(4):395–401.PubMedCrossRef Di W, Guo SW. The search for genetic variants predisposing women to endometriosis. Curr Opin Obstet Gynecol. 2007;19(4):395–401.PubMedCrossRef
101.
go back to reference Dyson MT, Roqueiro D, Monsivais D, Ercan CM, Pavone ME, Brooks DC, Kakinuma T, Ono M, Jafari N, Dai Y, Bulun SE. Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis. PLoS Genet. 2014;10(3):e1004158.PubMedPubMedCentralCrossRef Dyson MT, Roqueiro D, Monsivais D, Ercan CM, Pavone ME, Brooks DC, Kakinuma T, Ono M, Jafari N, Dai Y, Bulun SE. Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis. PLoS Genet. 2014;10(3):e1004158.PubMedPubMedCentralCrossRef
104.
go back to reference •• Marquardt RM, Tran DN, Lessey BA, Rahman MS, Jeong JW. Epigenetic dysregulation in endometriosis: implications for pathophysiology and therapeutics. Endocr Rev. 2023;44(6):1074–95. https://doi.org/10.1210/endrev/bnad020. PMID:37409951;PMCID:PMC10638603. This review analyzes the recent evidence of epigenetic contributions to the pathophysiology of endometriosis and how this may impact developments in therapeutics.CrossRefPubMed •• Marquardt RM, Tran DN, Lessey BA, Rahman MS, Jeong JW. Epigenetic dysregulation in endometriosis: implications for pathophysiology and therapeutics. Endocr Rev. 2023;44(6):1074–95. https://​doi.​org/​10.​1210/​endrev/​bnad020. PMID:37409951;PMCID:PMC10638603. This review analyzes the recent evidence of epigenetic contributions to the pathophysiology of endometriosis and how this may impact developments in therapeutics.CrossRefPubMed
105.
go back to reference Wu Y, Strawn E, Basir Z, Halverson G, Guo SW. Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis. Fertil Steril. 2007;87(1):24–32.PubMedCrossRef Wu Y, Strawn E, Basir Z, Halverson G, Guo SW. Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis. Fertil Steril. 2007;87(1):24–32.PubMedCrossRef
106.
go back to reference Szczepanska M, Wirstlein P, Skrzypczak J, Jagodzinski PP. Expression of HOXA11 in the mid-luteal endometrium from women with endometriosis-associated infertility. Reprod Biol Endocrinol. 2012;10(1):1.PubMedPubMedCentralCrossRef Szczepanska M, Wirstlein P, Skrzypczak J, Jagodzinski PP. Expression of HOXA11 in the mid-luteal endometrium from women with endometriosis-associated infertility. Reprod Biol Endocrinol. 2012;10(1):1.PubMedPubMedCentralCrossRef
107.
go back to reference van Kaam KJ, Delvoux B, Romano A, D’Hooghe T, Dunselman GA, Groothuis PG. Deoxyribonucleic acid methyltransferases and methyl-CpG-binding domain proteins in human endometrium and endometriosis. Fertil Steril. 2011;95(4):1421–7.PubMedCrossRef van Kaam KJ, Delvoux B, Romano A, D’Hooghe T, Dunselman GA, Groothuis PG. Deoxyribonucleic acid methyltransferases and methyl-CpG-binding domain proteins in human endometrium and endometriosis. Fertil Steril. 2011;95(4):1421–7.PubMedCrossRef
108.
go back to reference Roca FJ, Loomans HA, Wittman AT, Creighton CJ, Hawkins SM. Ten-eleven translocation genes are downregulated in endometriosis. Curr Mol Med. 2016;16(3):288–98.PubMedCrossRef Roca FJ, Loomans HA, Wittman AT, Creighton CJ, Hawkins SM. Ten-eleven translocation genes are downregulated in endometriosis. Curr Mol Med. 2016;16(3):288–98.PubMedCrossRef
109.
go back to reference Huang Q, Liu X, Critchley H, Fu Z, Guo SW. How does the extent of fibrosis in adenomyosis lesions contribute to heavy menstrual bleeding? Reprod Med Biol. 2022;21(1):e12442.PubMedPubMedCentralCrossRef Huang Q, Liu X, Critchley H, Fu Z, Guo SW. How does the extent of fibrosis in adenomyosis lesions contribute to heavy menstrual bleeding? Reprod Med Biol. 2022;21(1):e12442.PubMedPubMedCentralCrossRef
110.
go back to reference Naqvi H, Mamillapalli R, Krikun G, Taylor HS. Endometriosis located proximal to or remote from the uterus differentially affects uterine gene expression. Reprod Sci. 2016;23(2):186–91.PubMedPubMedCentralCrossRef Naqvi H, Mamillapalli R, Krikun G, Taylor HS. Endometriosis located proximal to or remote from the uterus differentially affects uterine gene expression. Reprod Sci. 2016;23(2):186–91.PubMedPubMedCentralCrossRef
111.
go back to reference Szczepanska M, Wirstlein P, Zawadzka M, Wender-Ozegowska E, Jagodzinski PP. Alternation of ten-eleven translocation 1, 2, and 3 expression in eutopic endometrium of women with endometriosis-associated infertility. Gynecol Endocrinol. 2018;34(12):1084–90.PubMedCrossRef Szczepanska M, Wirstlein P, Zawadzka M, Wender-Ozegowska E, Jagodzinski PP. Alternation of ten-eleven translocation 1, 2, and 3 expression in eutopic endometrium of women with endometriosis-associated infertility. Gynecol Endocrinol. 2018;34(12):1084–90.PubMedCrossRef
113.
114.
go back to reference Xiaomeng X, Ming Z, Jiezhi M, Xiaoling F. Aberrant histone acetylation and methylation levels in woman with endometriosis. Arch Gynecol Obstet. 2013;287(3):487–94.PubMedCrossRef Xiaomeng X, Ming Z, Jiezhi M, Xiaoling F. Aberrant histone acetylation and methylation levels in woman with endometriosis. Arch Gynecol Obstet. 2013;287(3):487–94.PubMedCrossRef
115.
go back to reference Colón-Díaz M, Baez-Vega P, Garcia M, Ruiz A, Monteiro JB, Fourquet J, Bayona M, Alvarez-Garriga C, Achille A, Seto E, Flores I. HDAC1 and HDAC2 are differentially expressed in endometriosis. Reprod Sci. 2012;19(5):483–92.PubMedPubMedCentralCrossRef Colón-Díaz M, Baez-Vega P, Garcia M, Ruiz A, Monteiro JB, Fourquet J, Bayona M, Alvarez-Garriga C, Achille A, Seto E, Flores I. HDAC1 and HDAC2 are differentially expressed in endometriosis. Reprod Sci. 2012;19(5):483–92.PubMedPubMedCentralCrossRef
117.
go back to reference Yoo JY, Kim TH, Fazleabas AT, Palomino WA, Ahn SH, Tayade C, Schammel DP, Young SL, Jeong JW, Lessey BA. KRAS activation and over- expression of SIRT1/BCL6 contributes to the pathogenesis of endometriosis and progesterone resistance. Sci Rep. 2017;7(1):6765.ADSPubMedPubMedCentralCrossRef Yoo JY, Kim TH, Fazleabas AT, Palomino WA, Ahn SH, Tayade C, Schammel DP, Young SL, Jeong JW, Lessey BA. KRAS activation and over- expression of SIRT1/BCL6 contributes to the pathogenesis of endometriosis and progesterone resistance. Sci Rep. 2017;7(1):6765.ADSPubMedPubMedCentralCrossRef
118.
go back to reference Zhang Q, Dong P, Liu X, Sakuragi N, Guo SW. Enhancer of zeste homolog 2 (EZH2) induces epithelial-mesenchymal transition in endometriosis. Sci Rep. 2017;7(1):6804.ADSPubMedPubMedCentralCrossRef Zhang Q, Dong P, Liu X, Sakuragi N, Guo SW. Enhancer of zeste homolog 2 (EZH2) induces epithelial-mesenchymal transition in endometriosis. Sci Rep. 2017;7(1):6804.ADSPubMedPubMedCentralCrossRef
119.
go back to reference Colón-Caraballo M, Torres-Reveron A, Soto-Vargas JL, Young SL, Lessey B, Mendoza A, Urrutia R, Flores I. Effects of histone methyltransferase inhibition in endometriosis. Biol Reprod. 2018;99(2):293–307.PubMedPubMedCentralCrossRef Colón-Caraballo M, Torres-Reveron A, Soto-Vargas JL, Young SL, Lessey B, Mendoza A, Urrutia R, Flores I. Effects of histone methyltransferase inhibition in endometriosis. Biol Reprod. 2018;99(2):293–307.PubMedPubMedCentralCrossRef
120.
go back to reference Wen X, Xiong Y, Liu H, Geng T, Jin L, Zhang M, Ma L, Zhang Y. Decreased mixed lineage leukemia 1 is involved in endometriosis-related infertility. J Mol Endocrinol. 2021;66(1):45–57.PubMedCrossRef Wen X, Xiong Y, Liu H, Geng T, Jin L, Zhang M, Ma L, Zhang Y. Decreased mixed lineage leukemia 1 is involved in endometriosis-related infertility. J Mol Endocrinol. 2021;66(1):45–57.PubMedCrossRef
121.
go back to reference Kim TH, Yoo JY, Wang Z, Lydon JP, Khatri S, Hawkins SM, Leach RE, Fazleabas AT, Young SL, Lessey BA, Ku BJ, Jeong JW. ARID1A is essential for endometrial function during early pregnancy. PLoS Genet. 2015;11(9):e1005537.PubMedPubMedCentralCrossRef Kim TH, Yoo JY, Wang Z, Lydon JP, Khatri S, Hawkins SM, Leach RE, Fazleabas AT, Young SL, Lessey BA, Ku BJ, Jeong JW. ARID1A is essential for endometrial function during early pregnancy. PLoS Genet. 2015;11(9):e1005537.PubMedPubMedCentralCrossRef
122.
go back to reference Rocha-Junior CV, Da Broi MG, Miranda-Furtado CL, Navarro PA, Ferriani RA, Meola J. Progesterone receptor B (PGR-B) is partially methylated in eutopic endometrium from infertile women with endometriosis. Reprod Sci. 2019;26(12):1568–74.PubMedCrossRef Rocha-Junior CV, Da Broi MG, Miranda-Furtado CL, Navarro PA, Ferriani RA, Meola J. Progesterone receptor B (PGR-B) is partially methylated in eutopic endometrium from infertile women with endometriosis. Reprod Sci. 2019;26(12):1568–74.PubMedCrossRef
123.
go back to reference Samadieh Y, Favaedi R, Ramezanali F, Afsharian P, Aflatoonian R, Shahhoseini M. Epigenetic dynamics of HOXA10 gene in infertile women with endometriosis. Reprod Sci. 2019;26(1):88–96.PubMedCrossRef Samadieh Y, Favaedi R, Ramezanali F, Afsharian P, Aflatoonian R, Shahhoseini M. Epigenetic dynamics of HOXA10 gene in infertile women with endometriosis. Reprod Sci. 2019;26(1):88–96.PubMedCrossRef
126.
go back to reference Li Y, An D, Guan YX, Kang S. Aberrant methylation of the E-cadherin gene promoter region in endometrium and ovarian endometriotic cysts of patients with ovarian endometriosis. Gynecol Obstet Invest. 2017;82(1):78–85.PubMedCrossRef Li Y, An D, Guan YX, Kang S. Aberrant methylation of the E-cadherin gene promoter region in endometrium and ovarian endometriotic cysts of patients with ovarian endometriosis. Gynecol Obstet Invest. 2017;82(1):78–85.PubMedCrossRef
127.
go back to reference Xue Q, Zhou YF, Zhu SN, Bulun SE. Hypermethylation of the CpG island spanning from exon II to intron III is associated with steroidogenic factor 1 expression in stromal cells of endometriosis. Reprod Sci. 2011;18(11):1080–4.PubMedPubMedCentralCrossRef Xue Q, Zhou YF, Zhu SN, Bulun SE. Hypermethylation of the CpG island spanning from exon II to intron III is associated with steroidogenic factor 1 expression in stromal cells of endometriosis. Reprod Sci. 2011;18(11):1080–4.PubMedPubMedCentralCrossRef
128.
go back to reference Xue Q, Xu Y, Yang H, Zhang L, Shang J, Zeng C, Yin P, Bulun SE. Methylation of a novel CpG island of intron 1 is associated with steroidogenic factor 1 expression in endometriotic stromal cells. Reprod Sci. 2014;21(3):395–400.PubMedPubMedCentralCrossRef Xue Q, Xu Y, Yang H, Zhang L, Shang J, Zeng C, Yin P, Bulun SE. Methylation of a novel CpG island of intron 1 is associated with steroidogenic factor 1 expression in endometriotic stromal cells. Reprod Sci. 2014;21(3):395–400.PubMedPubMedCentralCrossRef
135.
go back to reference Tanaka M, Kyo S, Kanaya T, Yatabe N, Nakamura M, Maida Y, Okabe M, Inoue M. Evidence of the monoclonal composition of human endometrial epithelial glands and mosaic pattern of clonal distribution in luminal epithelium. Am J Pathol. 2003;163(1):295–301.PubMedPubMedCentralCrossRef Tanaka M, Kyo S, Kanaya T, Yatabe N, Nakamura M, Maida Y, Okabe M, Inoue M. Evidence of the monoclonal composition of human endometrial epithelial glands and mosaic pattern of clonal distribution in luminal epithelium. Am J Pathol. 2003;163(1):295–301.PubMedPubMedCentralCrossRef
136.
go back to reference Wu Y, Guo SW. Reconstructing cellular lineages in endometrial cells. Fertil Steril. 2008;89(2):481–4.PubMedCrossRef Wu Y, Guo SW. Reconstructing cellular lineages in endometrial cells. Fertil Steril. 2008;89(2):481–4.PubMedCrossRef
137.
go back to reference Suda K, Nakaoka H, Yoshihara K, Ishiguro T, Tamura R, Mori Y, Yamawaki K, Adachi S, Takahashi T, Kase H, Tanaka K, Yamamoto T, Motoyama T, Inoue I, Enomoto T. Clonal expansion and diversification of cancer-associated mutations in endometriosis and normal endometrium. Cell Rep. 2018;24(7):1777–89.PubMedCrossRef Suda K, Nakaoka H, Yoshihara K, Ishiguro T, Tamura R, Mori Y, Yamawaki K, Adachi S, Takahashi T, Kase H, Tanaka K, Yamamoto T, Motoyama T, Inoue I, Enomoto T. Clonal expansion and diversification of cancer-associated mutations in endometriosis and normal endometrium. Cell Rep. 2018;24(7):1777–89.PubMedCrossRef
138.
go back to reference Moore L, Leongamornlert D, Coorens THH, et al. The mutational landscape of normal human endometrial epithelium. Nature. 2020;580(7805):640–6.ADSPubMedCrossRef Moore L, Leongamornlert D, Coorens THH, et al. The mutational landscape of normal human endometrial epithelium. Nature. 2020;580(7805):640–6.ADSPubMedCrossRef
139.
go back to reference Takeda T, Banno K, Kobayashi Y, Adachi M, Yanokura M, Tominaga E, Kosaki K, Aoki D. Mutations of RAS genes in endometrial polyps. Oncol Rep. 2019;42(6):2303–8.PubMedPubMedCentral Takeda T, Banno K, Kobayashi Y, Adachi M, Yanokura M, Tominaga E, Kosaki K, Aoki D. Mutations of RAS genes in endometrial polyps. Oncol Rep. 2019;42(6):2303–8.PubMedPubMedCentral
140.
go back to reference Hoshiai H, Ishikawa M, Sawatari Y, Noda K, Fukaya T. Laparoscopic evaluation of the onset and progression of endometriosis. Am J Obstet Gynecol. 1993;169(3):714–9.PubMedCrossRef Hoshiai H, Ishikawa M, Sawatari Y, Noda K, Fukaya T. Laparoscopic evaluation of the onset and progression of endometriosis. Am J Obstet Gynecol. 1993;169(3):714–9.PubMedCrossRef
141.
go back to reference Thomas EJ, Cooke ID. Impact of gestrinone on the course of asymptomatic endometriosis. Br Med J. 1987;294:272–4.CrossRef Thomas EJ, Cooke ID. Impact of gestrinone on the course of asymptomatic endometriosis. Br Med J. 1987;294:272–4.CrossRef
142.
go back to reference Mahmood TA, Templeton A. The impact of treatment on the natural history of endometriosis. Human Reprod. 1990;5:965–70.CrossRef Mahmood TA, Templeton A. The impact of treatment on the natural history of endometriosis. Human Reprod. 1990;5:965–70.CrossRef
143.
go back to reference Telimaa S, Puolakka J, Ronnberg L, Kauppila A. Placebo controlled comparison of danazol and high-dose medroxyprogesterone acetate in the treatment of endometriosis. Gynecol Endocrinol. 1987;1:13–23.PubMedCrossRef Telimaa S, Puolakka J, Ronnberg L, Kauppila A. Placebo controlled comparison of danazol and high-dose medroxyprogesterone acetate in the treatment of endometriosis. Gynecol Endocrinol. 1987;1:13–23.PubMedCrossRef
144.
go back to reference Kim JJ, Taylor HS, Lu Z, Ladhani O, Hastings JM, Jackson KS, Wu Y, Guo SW, Fazleabas AT. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol Hum Reprod. 2007;13(5):323–32.PubMedCrossRef Kim JJ, Taylor HS, Lu Z, Ladhani O, Hastings JM, Jackson KS, Wu Y, Guo SW, Fazleabas AT. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol Hum Reprod. 2007;13(5):323–32.PubMedCrossRef
145.
go back to reference Lee B, Du H, Taylor HS. Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod. 2009;80(1):79–85.PubMedPubMedCentralCrossRef Lee B, Du H, Taylor HS. Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod. 2009;80(1):79–85.PubMedPubMedCentralCrossRef
146.
go back to reference Kim TH, Yoo JY, Choi KC, Shin JH, Leach RE, Fazleabas AT, Young SL, Lessey BA, Yoon HG, Jeong JW. Loss of HDAC3 results in nonreceptive endometrium and female infertility. Sci Transl Med. 2019;11(474):eaaf7533.PubMedPubMedCentralCrossRef Kim TH, Yoo JY, Choi KC, Shin JH, Leach RE, Fazleabas AT, Young SL, Lessey BA, Yoon HG, Jeong JW. Loss of HDAC3 results in nonreceptive endometrium and female infertility. Sci Transl Med. 2019;11(474):eaaf7533.PubMedPubMedCentralCrossRef
147.
go back to reference Sherwin JR, Hastings JM, Jackson KS, Mavrogianis PA, Sharkey AM, Fazleabas AT. The endometrial response to chorionic gonadotropin is blunted in a baboon model of endometriosis. Endocrinology. 2010;151(10):4982–93.PubMedPubMedCentralCrossRef Sherwin JR, Hastings JM, Jackson KS, Mavrogianis PA, Sharkey AM, Fazleabas AT. The endometrial response to chorionic gonadotropin is blunted in a baboon model of endometriosis. Endocrinology. 2010;151(10):4982–93.PubMedPubMedCentralCrossRef
148.
go back to reference • Afshar Y, Hastings J, Roqueiro D, Jeong JW, Giudice LC, Fazleabas AT. Changes in eutopic endometrial gene expression during the progression of experimental endometriosis in the baboon, Papio anubis. Biol Reprod. 2013;88(2):44 This article and others cited provides strong evidence that endometriosis rather than inherent defects in the endometrium is the cause of aberrant gene expression in the eutopic endometrium.PubMedPubMedCentralCrossRef • Afshar Y, Hastings J, Roqueiro D, Jeong JW, Giudice LC, Fazleabas AT. Changes in eutopic endometrial gene expression during the progression of experimental endometriosis in the baboon, Papio anubis. Biol Reprod. 2013;88(2):44 This article and others cited provides strong evidence that endometriosis rather than inherent defects in the endometrium is the cause of aberrant gene expression in the eutopic endometrium.PubMedPubMedCentralCrossRef
149.
go back to reference Bashir ST, Redden CR, Raj K, Arcanjo RB, Stasiak S, Li Q, Steelman AJ, Nowak RA. Endometriosis leads to central nervous system-wide glial activation in a mouse model of endometriosis. J Neuroinflammation. 2023;20(1):59.PubMedPubMedCentralCrossRef Bashir ST, Redden CR, Raj K, Arcanjo RB, Stasiak S, Li Q, Steelman AJ, Nowak RA. Endometriosis leads to central nervous system-wide glial activation in a mouse model of endometriosis. J Neuroinflammation. 2023;20(1):59.PubMedPubMedCentralCrossRef
Metadata
Title
Endometrial Determinism of Endometriosis: An Unnecessary Adjunct to Retrograde Menstruation
Authors
Marwan Habiba
Sun-Wei Guo
Giuseppe Benagiano
Publication date
21-02-2024
Publisher
Springer US
Keyword
Endometriosis
Published in
Current Obstetrics and Gynecology Reports
Electronic ISSN: 2161-3303
DOI
https://doi.org/10.1007/s13669-024-00378-x