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Effects of Supplementation of Human Endometriotic Fluids on In Vitro Mouse Preantral Follicle Culture

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Abstract

This study aimed to investigate the potential detrimental effect of human endometriotic fluids (EFs) on in vitro growth of mouse preantral follicles. Preantral follicles (isolated from ovaries of 7- to 8-week-old mice) were cultured in growth medium for 10 days and then in maturation medium for 2 days. During in vitro culture, EF supernatants (0%, 2.5%, 5%, and 10%) were supplemented. Meiotic spindle integrity of metaphase II (Mil) oocytes was analyzed. Hormone (l7(3-estradiol and anti-Mullerian hormone [AMH]) levels in the final spent media were measured by enzyme-linked immunosorbent assay. The survival rates offolliclesatday 10 were significantly lower in 3 EF-supplemented groups (56.1%, 30.6%, and 6.2%; 83.6% in the nonsupplemented group). The production of total oocytes per initiated follicle was also significantly lower in the 3 EF-supplemented groups (34.7%, 18.4%, and 4.1 %; 68.1 % in the nonsupplemented group). Proportions of the oocyte with normal spindles were significantly lower in the 3 EF-supplemented groups (10%, 0% and 0%; 52% in the nonsupplemented group). In the final spent media, the level of 17(3-estradiol was significantly lower only in the 10% EF-supplemented group, and the level of AMH was significantly lower in all 3 EF-supplemented groups, when compared with the nonsupplemented group. During in vitro culture of mouse preantral follicles, the survival rate, oocyte acquisition, spindle integrity of Mil oocytes, and AMH production were greatly affected by EF supplementation. These findings suggest a possibility of detrimental effects of endometriotic cysts on folliculogenesis in adjacent ovarian tissues.

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References

  1. Redwine DB. Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril. 1999;72(2):310–315.

    CAS  PubMed  Google Scholar 

  2. Sanchez AM, Vigano P, Somigliana E, Panina-Bordignon P, Vercellini P, Candiani M. The distinguishing cellular and molecular features of the endometriotic ovarian cyst: from pathophysiology to the potential endometrioma-mediated damage to the ovary. Hum Reprod Update. 2014;20(2):217–230.

    CAS  PubMed  Google Scholar 

  3. Kim JY, Jee BC, Suh CS, Kim SH. Preoperative serum anti-mullerian hormone level in women with ovarian endometrioma and mature cystic teratoma. Yonsei Med J. 2013;54(4):921–926.

    PubMed  PubMed Central  Google Scholar 

  4. Uncu G, Kasapoglu I, Ozerkan K, Seyhan A, Oral Yilmaztepe A, Ata B. Prospective assessment of the impact of endometriomas and their removal on ovarian reserve and determinants of the rate of decline in ovarian reserve. Hum Reprod. 2013;28(8): 2140–2145.

    CAS  PubMed  Google Scholar 

  5. Benaglia L, Somigliana E, Vercellini P, Abbiati A, Ragni G, Fedele L. Endometriotic ovarian cysts negatively affect the rate of spontaneous ovulation. Hum Reprod. 2009;24(9):2183–2186.

    PubMed  Google Scholar 

  6. Benaglia L, Bermejo A, Somigliana E, et al. In vitro fertilization outcome in women with unoperated bilateral endometriomas. Fertil Steril. 2013;99(6): 1714–1719.

    PubMed  Google Scholar 

  7. Matsuzaki S, Schubert B. Oxidative stress status in normal ovar-ian cortex surrounding ovarian endometriosis. Fertil Steril. 2010; 93(7):2431–2432.

    PubMed  Google Scholar 

  8. Schubert B, Canis M, Darcha C, et al. Human ovarian tissue from cortex surrounding benign cysts: a model to study ovarian tissue cryopreservation. Hum Reprod. 2005;20(7): 1786–1792.

    PubMed  Google Scholar 

  9. Kitajima M, Defrere S, Dolmans MM, et al. Endometriomas as a possible cause of reduced ovarian reserve in women with endometriosis. Fertil Steril. 2011;96(3):685–691.

    PubMed  Google Scholar 

  10. Maneschi F, Marasa L, Incandela S, Mazzarese M, Zupi E. Ovarian cortex surrounding benign neoplasms: a histologic study. Am J Obstet Gynecol. 1993;169(2 pt 1):388–393.

    CAS  PubMed  Google Scholar 

  11. Muzii L, Bianchi A, Croce C, Manci N, Panici PB. Laparoscopic excision of ovarian cysts: is the stripping technique a tissue-sparing procedure? Fertil Steril. 2002;77(3):609–614.

    PubMed  Google Scholar 

  12. Kuroda M, Kuroda K, Arakawa A, et al. Histological assessment of impact of ovarian endometrioma and laparoscopic cystectomy on ovarian reserve. J Obstet Gynaecol Res. 2012;38(9): 1187–1193.

    PubMed  Google Scholar 

  13. Fasciani A, D’Ambrogio G, Bocci G, Luisi S, Artini PG, Genazzani AR. Vascular endothelial growth factor and interleukin-8 in ovarian cystic pathology. Fertil Steril. 2001;75(6):1218–1221.

    CAS  PubMed  Google Scholar 

  14. Boss EA, Massuger LF, Thomas CM, et al. Clinical value of components of the plasminogen activation system in ovarian cyst fluid. Anticancer Res. 2002;22(1 A):275–282.

    CAS  PubMed  Google Scholar 

  15. Darai E, Detchev R, Hugol D, Quang NT. Serum and cyst fluid levels of interleukin (IL) -6, IL-8 and tumour necrosis factor-alpha in women with endometriomas and benign and malignant cystic ovarian tumours. Hum Reprod. 2003;18(8):1681–1685.

    CAS  PubMed  Google Scholar 

  16. Velasco I, Acien P, Campos A, Acien MI, Ruiz-Macia E. Interleukin-6 and other soluble factors in peritoneal fluid and endometriomas and their relation to pain and aromatase expression. J Reprod Immunol. 2010;84(2):199–205.

    CAS  PubMed  Google Scholar 

  17. Yamaguchi K, Mandai M, Toyokuni S, et al. Contents of endometriotic cysts, especially the high concentration of free iron, are a possible cause of carcinogenesis in the cysts through the iron-induced persistent oxidative stress. Clin Cancer Res. 2008; 14(1): 32–40.

    CAS  PubMed  Google Scholar 

  18. Donnez J, Nisolle M, Gillet N, Smets M, Bassil S, Casanas-Roux F. Large ovarian endometriomas. Hum Reprod. 1996; 11(3): 641–646.

    CAS  PubMed  Google Scholar 

  19. Muzii L, Bianchi A, Bellati F, et al. Histologic analysis of endometriomas: what the surgeon needs to know. Fertil Steril. 2007; 87(2):362–366.

    PubMed  Google Scholar 

  20. Bedaiwy M, Shahin AY, AbulHassan AM, et al. Differential expression of follicular fluid cytokines: relationship to subsequent pregnancy in IVF cycles. Reprod Biomed Online. 2007;15(3): 321–325.

    CAS  PubMed  Google Scholar 

  21. Opoien HK, Fedorcsak P, Polec A, Stensen MH, Abyholm T, Tanbo T. Do endometriomas induce an inflammatory reaction in nearby follicles? Hum Reprod. 2013;28(7): 1837–1845.

    CAS  PubMed  Google Scholar 

  22. Kitajima M, Dolmans MM, Donnez O, Masuzaki H, Soares M, Donnez J. Enhanced follicular recruitment and atresia in cortex derived from ovaries with endometriomas. Fertil Steril. 2014; 101(4):1031–1037.

    PubMed  Google Scholar 

  23. Jee BC, Kim JH, Park da H, Youm H, Suh CS, Kim SH. In vitro growth of mouse preantral follicles: effect of animal age and stem cell factor/insulin-like growth factor supplementation. Clin Exp Reprod Med. 2012;39(3): 107–113.

    PubMed  PubMed Central  Google Scholar 

  24. Chun EK, Jee BC, Kim JY, Kim SH, Moon SY. Effect of imatinib coadministration on in vitro oocyte acquisition and subsequent embryo development in cyclophosphamide-treated mice [published online January 8, 2014]. Reprod Sci. 21(7):906–914.

    PubMed  PubMed Central  Google Scholar 

  25. Leone Roberti Maggiore U, Scala C, Venturini PL, Remorgida V, Ferrero S. Endometriotic ovarian cysts do not negatively affect the rate of spontaneous ovulation. Hum Reprod. 2015;30(2):299–307.

    CAS  PubMed  Google Scholar 

  26. Shebl O, Sifferlinger I, Habelsberger A, et al. Oocyte competence in in vitro fertilization and intracytoplasmic sperm injection patients suffering from endometriosis and its possible association with subsequent treatment outcome: a matched case-control study [published online June 18, 2016]. Acta Obstet Gynecol Scand.

    Google Scholar 

  27. Desai N, AbdelHafez F, Ali MY, et al. Mouse ovarian follicle cryopreservation using vitrification or slow programmed cooling: assessment of in vitro development, maturation, ultra-structure and meiotic spindle organization. J Obstet Gynaecol Res. 2011; 37(1):1–12.

    PubMed  Google Scholar 

  28. Somigliana E, Infantino M, Benedetti F, Arnoldi M, Calanna G, Ragni G. The presence of ovarian endometriomas is associated with a reduced responsiveness to gonadotropins. Fertil Steril. 2006;86(1):192–196.

    CAS  PubMed  Google Scholar 

  29. Almog B, Shehata F, Sheizaf B, Tan SL, Tulandi T. Effects of ovarian endometrioma on the number of oocytes retrieved for in vitro fertilization. Fertil Steril. 2011;95(2):525–527.

    PubMed  Google Scholar 

  30. Benaglia L, Pasin R, Somigliana E, Vercellini P, Ragni G, Fedele L. Unoperated ovarian endometriomas and responsiveness to hyperstimulation. Hum Reprod. 2011;26(6):1356–1361.

    PubMed  Google Scholar 

  31. Esinler I, Bozdag G, Arikan I, Demir B, Yarali H. Endometrioma ≤3 cm in diameter per se does not affect ovarian reserve in intracytoplasmic sperm injection cycles. Gynecol Obstet Invest. 2012;74(4):261–264.

    PubMed  Google Scholar 

  32. Ashrafi M, Fakheri T, Kiani K, Sadeghi M, Akhoond MR. Impact of the endometrioma on ovarian response and pregnancy rate in in vitro fertilization cycles. Int J Fertil Steril. 2014;8(1):29–34.

    PubMed  PubMed Central  Google Scholar 

  33. Coccia ME, Rizzello F, Barone S, et al. Is there a critical endometrioma size associated with reduced ovarian responsiveness in assisted reproduction techniques? Reprod Biomed Online. 2014; 29(2):259–266.

    PubMed  Google Scholar 

  34. Filippi F, Benaglia L, Paffoni A, et al. Ovarian endometriomas and oocyte quality: insights from in vitro fertilization cycles. Fertil Steril. 2014;101(4):988–993.e1.

    PubMed  Google Scholar 

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Correspondence to Seok Hyun Kim MD PhD.

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Kim, S.K., Jee, B.C. & Kim, S.H. Effects of Supplementation of Human Endometriotic Fluids on In Vitro Mouse Preantral Follicle Culture. Reprod. Sci. 25, 683–689 (2018). https://doi.org/10.1177/1933719116678687

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