Bilateral Endometrioma Excision: Surgery-Related Damage to Ovarian Reserve

To study whether unoperated ovarian endometrioma(s) or its surgical excision led to a modified pattern of ovarian decay with increasing female age. A sectional analysis of basal follicle stimulating hormone (FSH) and ovarian response to gonadotropins was conducted on women treated with fresh autologous In Vitro Fertilization/Intracytoplasmic sperm injection (IVF/ICSI) cycles. The study group included patients with unoperated ovarian endometrioma(s) (108 cycles); control groups were women with previous surgery for monolateral ovarian endometrioma (101 cycles), surgery for bilateral ovarian endometriomas (39 cycles), and tubal factor infertility (171 cycles). Simple linear regression analyses and the Pearson correlation were used to analyze the correlation between basal FSH, number of dominant follicles, number of retrieved oocytes, and age of patients. The relationship between the variables was significant in case of patients with nonoperated ovarian endometrioma(s) and patients with previous surgery for monolateral endometrioma and tubal factor infertility group. In patients with a history of surgery for bilateral endometriomas, no relationship was found among the variables (basal FSH 95% confidence interval [CI]: −0.475 to 0.319; P =.688; number of dominant follicles 95% CI: −0.484 to 0.382; P =.808; number of retrieved oocytes 95% CI: −0.478 to 0.370, P =.792). In women with unoperated ovarian endometrioma(s) or with a history of surgery for monolateral endometrioma, the remaining ovarian parenchyma maintains the same pattern of ovarian decay as healthy ovaries. Unoperated ovarian endometriotic lesions did not interfere with ovarian reserve and IVF/ICSI cycles’ outcomes and were less injurious than surgery. After surgery for bilateral ovarian endometriomas, a decline in ovarian reserve seems independent from the patient’s age. Similar content being viewed by others

Forabosco A, Sforza C. Establishment of ovarian reserve: a quantitative morphometric study of the developing human ovary. Fertil Steril. 2007;88(3):675–683. McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev. 2000;21(2):200–214. Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum Reprod. 1992;7(10):1342–1346. Faddy MJ, Gosden RG. A mathematical model of follicle dynamics in the human ovary. Hum Reprod. 1995;10(4):770–775. Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR, Klein NA. A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod. 2008;23(3):699–708. Coccia ME, Rizzello F, Mariani G, Bulletti C, Palagiano A, Scarselli G. Ovarian surgery for bilateral endometriomas influences age at menopause. Hum Reprod. 2011;26(11):3000–3007. Kitajima M, Defrère 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. Hudelist G, Ballard K, English J, et al. Transvaginal sonography vs. clinical examination in the preoperative diagnosis of deep infiltrating endometriosis. Ultrasound Obstet Gynecol. 2011;37(4):480–487. 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. Da Broi MG, Navarro PA. Oxidative stress and oocyte quality: ethiopathogenic mechanisms of minimal/mild endometriosis-related infertility. Cell Tissue Res. 2016;364(1):1–7. Nasiri N, Moini A, Eftekhari-Yazdi P, Karimian L, Salman-Yazdi R, Arabipoor A. Oxidative stress statues in serum and follicular fluid of women with endometriosis. Cell J. 2017;18(4):582–587. Becatti M, Fucci R, Mannucci A, et al. A biochemical approach to detect oxidative stress in infertile women undergoing assisted reproductive technology procedures. Int J Mol Sci. 2018:16;19(2). 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. Ferrero S, Scala C, Tafi E, Racca A, Venturini PL, Leone Roberti Maggiore U. Impact of large ovarian endometriomas on the response to superovulation for in vitro fertilization: a retrospective study. Eur J Obstet Gynecol Reprod Biol. 2017;213:17–21. Hamdan M, Dunselman G, Li TC, Cheong Y. The impact of endometrioma on IVF/ICSI outcomes: a systematic review and meta-analysis. Hum Reprod Update. 2015;21(6):809–825. Raffi F, Metwally M, Amer S. The impact of excision of ovarian endometrioma on ovarian reserve: a systematic review and meta-analysis. J Clin Endocrinol Metab. 2012;97(9):3146–3154. Somigliana E, Berlanda N, Benaglia L, Viganò P, Vercellini P, Fedele L. Surgical excision of endometriomas and ovarian reserve: a systematic review on serum antimüllerian hormone level modifications. Fertil Steril. 2012;98(6):1531–1538. Muzii L, Di Tucci C, Di Feliciantonio M, Marchetti C, Perniola G, Panici PB. The effect of surgery for endometrioma on ovarian reserve evaluated by antral follicle count: a systematic review and meta-analysis. Hum Reprod. 2014;29(10):2190–2198. 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. Muzii L, Marana R, Angioli R, et al. Histologic analysis of specimens from laparoscopic endometrioma excision performed by different surgeons: does the surgeon matter? Fertil Steril. 2011;95(6):2116–2119. Hachisuga T, Kawarabayashi T. Histopathological analysis of laparoscopically treated ovarian endometriotic cysts with special reference to loss of follicles. Hum Reprod. 2002;17(2):432–435. Alborzi S, Foroughinia L, Kumar PV, Asadi N, Alborzi S. A comparison of histopathologic findings of ovarian tissue inadvertently excised with endometrioma and other kinds of benign ovarian cyst in patients undergoing laparoscopy versus laparotomy. Fertil Steril. 2009;92(6):2004–2007. Chang HJ, Han SH, Lee JR, et al. Impact of laparoscopic cystectomy on ovarian reserve: serial changes of serum anti-Müllerian hormone levels. Fertil Steril. 2010;94(1):343–349. Ferrero S, Scala C, Racca A, et al. Second surgery for recurrent unilateral endometriomas and impact on ovarian reserve: a case-control study. Fertil Steril. 2015;103(5):1236–1243. Wilkosz P, Greggains GD, Tanbo TG, Fedorcsak P. Female reproductive decline is determined by remaining ovarian reserve and age. PLoS One. 2014;9(10):343–349. Bukovsky A, Caudle MR, Svetlikova M, Upadhyaya NB. Origin of germ cells and formation of new primary follicles in adult human ovaries. Reprod Biol Endocrinol. 2004;2:20. Bukovsky A, Svetlikova M, Caudle MR. Oogenesis in cultures derived from adult human ovaries. Reprod Biol Endocrinol. 2005;3:17. Johnson J, Bagley J, Skaznik-Wikiel M, et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell. 2005;122(2):303–315. Coccia ME, Rizzello F. Ovarian reserve. Ann N Y Acad Sci. 2008;1127:27–30. Author information Authors and Affiliations Corresponding author Additional information Authors’ Note Approval for the study was obtained by the local institution review board (OS 16.263, 18/7/2016). Maria Elisabetta Coccia played a role in major contribution to conception and design, and interpretation of data, drafting the article, and final approval of the version to be published. Francesca Rizzello made a substantial contribution to the acquisition, analysis of data, drafting and revising the article critically, and final approval of the version to be published. Tommaso Capezzuoli, Paolo Evangelisti, Cinzia Cozzi, and Felice Petraglia revised the article critically and contributed to final approval of the version to be published. All authors have approved the submitted version of the manuscript. Rights and permissions About this article Cite this article Coccia, M.E., Rizzello, F., Capezzuoli, T. et al. Bilateral Endometrioma Excision: Surgery-Related Damage to Ovarian Reserve. Reprod. Sci. 26, 543–550 (2019). https://doi.org/10.1177/1933719118777640 Published: Version of record: Issue date: DOI: https://doi.org/10.1177/1933719118777640