Abstract
This study is aimed at identifying variations in the effect of endometriosis on fecundity in a mouse model based on prior pregnancy experience. Endometriosis is one of the most prevalent gynecological diseases and is known to impact female fecundity adversely. In this study, an endometriosis mouse model was established by allografting uterine horn tissue using Pelch’s method. The effect of endometriosis on fecundity was confirmed in primiparous and multiparous female mice. As fecundity indicators, the pregnancy rate, number of litters, pregnancy period, and survival rate of the pups were investigated. As a result of the experiment, the pregnancy rate decreased, and the pregnancy period tended to be shorter in primiparous female mice. However, there was no significant change in the multiparous mice. In addition, it has been established that correlations exist between the size of lesions and certain fecundity indicators of the lesion, even among primiparous and multiparous females with endometriosis. The study attempted to demonstrate a link between pregnancy experience and fecundity changes caused by endometriosis by experimentally reproducing clinical results using mouse models. These results suggest strategies for identifying several pathophysiological characteristics of endometriosis.
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References
Chauhan S, More A, Chauhan V, Kathane A. Endometriosis: A review of clinical diagnosis, treatment, and pathogenesis. Cureus. 2022;14:e28864.
WHO (World Health Organization). Endometriosis. 2023. [7 August 2023]. Available from https://www.who.int/news-room/fact-sheets/detail/endometriosis
Kuan KKW, Gibson DA, Whitaker LHR, Horne AW. Menstruation dysregulation and endometriosis development. Front Reprod Health. 2021;3:756704.
Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 1927;3(93–110):143.
Pedrassani M, Guerriero S, Pascual MA, Ajossa S, Graupera B, Pagliuca M, Podgaec S, Camargos E, Vieira de Oliveira Y, Alcázar JL. Superficial endometriosis at ultrasound examination-A diagnostic criteria proposal. Diagnostics (Basel) 2023;13(11):1876.
Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril. 2012;98:511–9.
Horne AW, Daniels J, Hummelshoj L, Cox E, Cooper KG. Surgical removal of superficial peritoneal endometriosis for managing women with chronic pelvic pain: Time for a rethink? BJOG. 2019;126:1414–6.
Lebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil Steril. 2001;75:1–10.
de Ziegler D, Borghese B, Chapron C. Endometriosis and infertility: Pathophysiology and management. Lancet. 2010;376:730–8.
Haas D, Chvatal R, Reichert B, Renner S, Shebl O, Binder H, Wurm P, Oppelt P. Endometriosis: A premenopausal disease? Age pattern in 42,079 patients with endometriosis. Arch Gynecol Obstet. 2012;286:667–70.
Bulletti C, Coccia ME, Battistoni S, Borini A. Endometriosis and infertility. J Assist Reprod Genet. 2010;27:441–7.
Farland LV, Prescott J, Sasamoto N, Tobias DK, Gaskins AJ, Stuart JJ, Carusi DA, Chavarro JE, Horne AW, Rich-Edwards JW, Missmer SA. Endometriosis and risk of adverse pregnancy outcomes. Obstet Gynecol. 2019;134:527–36.
Vannuccini S, Clifton VL, Fraser IS, Taylor HS, Critchley H, Giudice LC, Petraglia F. Infertility and reproductive disorders: Impact of hormonal and inflammatory mechanisms on pregnancy outcome. Hum Reprod Update. 2016;22:104–15.
Horton J, Sterrenburg M, Lane S, Maheshwari A, Li TC, Cheong Y. Reproductive, obstetric, and perinatal outcomes of women with adenomyosis and endometriosis: A systematic review and meta-analysis. Hum Reprod Update. 2019;25:592–632.
Mavrelos D, Saridogan E. Treatment of endometriosis in women desiring fertility. J Obstet Gynaecol India. 2015;65:11–6.
Leone Roberti Maggiore U, Ferrero S, Mangili G, Bergamini A, Inversetti A, Giorgione V, Vigano P, Candiani M. A systematic review on endometriosis during pregnancy: Diagnosis, misdiagnosis, complications and outcomes. Hum Reprod Update. 2016;22:70–103.
Vercellini P, Buggio L, Berlanda N, Barbara G, Somigliana E, Bosari S. Estrogen-progestins and progestins for the management of endometriosis. Fertil Steril. 2016;106(1552–1571):e1552.
Sri Ranjan Y, Ziauddeen N, Stuart B, Alwan NA, Cheong Y. The role of parity in the relationship between endometriosis and pregnancy outcomes: A systematic review and meta-analysis. Reprod Fertil 2023;4(1):e220070.
Lagana AS, Garzon S, Franchi M, Casarin J, Gullo G, Ghezzi F. Translational animal models for endometriosis research: A long and windy road. Ann Transl Med. 2018;6:431.
Sharpe-Timms KL. Using rats as a research model for the study of endometriosis. Ann N Y Acad Sci 2002; 955:318–327; discussion 340–342, 396–406.
Pelch KE, Sharpe-Timms KL, Nagel SC. Mouse model of surgically-induced endometriosis by auto-transplantation of uterine tissue. J Vis Exp 2012;(59):e3396.
Park S, Lim W, You S, Song G. Ameliorative effects of luteolin against endometriosis progression in vitro and in vivo. J Nutr Biochem. 2019;67:161–72.
Adamson GD, Pasta DJ. Endometriosis fertility index: The new, validated endometriosis staging system. Fertil Steril. 2010;94:1609–15.
Bonuccelli GA, Negrini R, da Silva Ferreira RD. Premature birth in women with endometriosis: A systematic review and meta-analysis. Reprod Sci. 2022;29:250–9.
Jeljeli M, Riccio LGC, Chouzenoux S, Moresi F, Toullec L, Doridot L, Nicco C, Bourdon M, Marcellin L, Santulli P, Abrao MS, Chapron C, et al. Macrophage immune memory controls endometriosis in mice and humans. Cell Rep. 2020;33:108325.
Chen S, Liu Y, Zhong Z, Wei C, Liu Y, Zhu X. Peritoneal immune microenvironment of endometriosis: Role and therapeutic perspectives. Front Immunol. 2023;14:1134663.
Hogg C, Horne AW, Greaves E. Endometriosis-associated macrophages: Origin, phenotype, and function. Front Endocrinol (Lausanne). 2020;11:7.
Hamilton S, Oomomian Y, Stephen G, Shynlova O, Tower CL, Garrod A, Lye SJ, Jones RL. Macrophages infiltrate the human and rat decidua during term and preterm labor: Evidence that decidual inflammation precedes labor. Biol Reprod. 2012;86:39.
Shan Y, Shen S, Long J, Tang Z, Wu C, Ni X. Term and preterm birth initiation is associated with the macrophages shifting to M1 polarization in gestational tissues in mice. Biology (Basel) 2022;11(12):1759.
Frincu F, Carp-Veliscu A, Petca A, Badiu DC, Bratila E, Cirstoiu M, Mehedintu C. Maternal-fetal outcomes in women with endometriosis and shared pathogenic mechanisms. Medicina (Kaunas) 2021;57(11):1258.
Salmeri N, Li Piani L, Cavoretto PI, Somigliana E, Vigano P, Candiani M. Endometriosis increases the risk of gestational diabetes: A meta-analysis stratified by mode of conception, disease localization and severity. Sci Rep. 2023;13:8099.
Bilotas MA, Olivares CN, Ricci AG, Baston JI, Bengochea TS, Meresman GF, Baranao RI. Interplay between endometriosis and pregnancy in a mouse model. PLoS ONE. 2015;10:e0124900.
Chantalat E, Valera MC, Vaysse C, Noirrit E, Rusidze M, Weyl A, Vergriete K, Buscail E, Lluel P, Fontaine C, Arnal JF, Lenfant F. Estrogen receptors and endometriosis. Int J Mol Sci 2020;21(8):2815.
Marquardt RM, Kim TH, Shin JH, Jeong JW. Progesterone and estrogen signaling in the endometrium: What goes wrong in endometriosis? Int J Mol Sci 2019;20(15):3822.
Puri CP, Garfield RE. Changes in hormone levels and gap junctions in the rat uterus during pregnancy and parturition. Biol Reprod. 1982;27:967–75.
Funding
This research was supported by a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (grant number: HI22C1424). And this work was supported by Commercializations Promotion Agency for R&D Outcomes grant funded by the Korea government (the Ministry of Science and ICT) (Project No. 1711177795).
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SJP, WL, and SP designed the study. WP and MK conducted experiments and analyzed the data, and HK and GS interpreted the data. WL and SP provided reagents. WP and MK wrote the original draft of the manuscript, and SJP, WL, and SP reviewed the draft of the manuscript. All authors have read and approved the manuscript.
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Park, W., Kim, M., Kim, H.S. et al. Alteration in Effects of Endometriosis on Fecundity According to Pregnancy Experience in Mouse Model. Reprod. Sci. 31, 404–412 (2024). https://doi.org/10.1007/s43032-023-01426-2
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DOI: https://doi.org/10.1007/s43032-023-01426-2