A role of anti-Mullerian hormone in external genital endometriosis

To understand a role for anti-Muller hormone (AMH) in the development and course of genital endometriosis, we sought out for and analyzed scientific papers in open electronic sources: PubMed, Scopus, eLibrary. We review a role of AMH in females as well as its importance in functioning of the reproductive system, noting that in developing external genital endometriosis its blood level decreases that may either due to ovarian damage or one of the links in the disease pathogenesis. Potential negative consequences of surgical interventions for ovaries as well as means for their prevention are described. About the Authors A. S. MolotkovRussian Federation Arseniy S. Molotkov – MD, PhD, Associate Professor, Senior Researcher, Department of Gynecology and Endocrinology, Ott Research Institute of Obstetrics, Gynecology and Reproductology; Associate Professor, Department for Obstetrics, Gynecology and Reproductology, Saint Petersburg State Universit Scopus Author ID: 56058571100. Researcher ID: H-9658-2015. Author ID: 670353. SPIN-code: 6359-6472. 3 Mendeleevskaya Liniya, Saint Petersburg 199034; 7 Universitetskaya Emb., Saint Petersburg 199034 M. I. Yarmolinskaya Russian Federation Maria I. Yarmolinskaya – MD, Dr Sci Med, Professor of RAS, Professor, Head of the Department of Gynecology and Endocrinology, Head of the Сenter «Diagnostics and Treatment of Endometriosis», Ott Research Institute of Obstetrics, Gynecology and Reproductology; Professor, Department of Obstetrics and Gynecology, Mechnikov North-Western State Medical University Scopus Author ID: 7801562649. Researcher ID: P-2183-2014. SPIN-code: 3686-3605. 3 Mendeleevskaya Liniya, Saint Petersburg 199034; 41 Kirochnaya Str., Saint Petersburg 191015

1. Victoria M., Labrosse J., Fabien Krief F. et al. Anti Müllerian hormone: more than a biomarker of female reproductive function. J Gynecol Obstet Hum Reprod. 2019;48(1):19–24. https://doi.org/10.1016/j.jogoh.2018.10.015. 2. Josso N., di Clemente N., Gouédard L. Anti-Müllerian hormone and its receptors. Mol Cell Endocrinol. 2001;179(1–2):25–32. https://doi.org/10.1016/s0303-7207(01)00467-1. 3. Kim J.H., MacLaughlin D.T., Donahoe P.K. Müllerian inhibiting substance/anti-Müllerian hormone: a novel treatment for gynecologic tumors. Obstet Gynecol Sci. 2014;57(5):343–57. https://doi.org/10.5468/ogs.2014.57.5.343. 4. Signorile P.G., Petraglia F., Baldi A. Anti-mullerian hormone is expressed by endometriosis tissues and induces cell cycle arrest and apoptosis in endometriosis cells. J Exp Clin Cancer Res. 2014;33(1):46. https://doi.org/10.1186/1756-9966-33-46. 5. Hipp H., Nezhat C., Sidell N. et al. Anti-müllerian hormone in peritoneal fluid and plasma from women with and without endometriosis. Reprod Sci. 2015;22(9):1129–33. https://doi.org/10.1177/1933719115578927. 6. Broer S.L., Broekmans F.J., Laven J.S., Fauser B.C. Anti-Müllerian hormone: ovarian reserve testing and its potential clinical implications. Hum Reprod Update. 2014;20(5):688–701. https://doi.org/10.1093/humupd/dmu020. 7. Weenen C., Laven J.S., Von Bergh A.R. et al. Anti-Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol Hum Reprod. 2004;10(2):77–83. https://doi.org/10.1093/molehr/gah015. 8. Bentzen J.G., Forman J.L., Johannsen T.H. et al. Ovarian antral follicle subclasses and anti-Müllerian hormone during normal reproductive aging. J Clin Endocrinol Metab. 2013;98(4):1602–11. https://doi.org/10.1210/jc.2012-182. 9. Dayal M., Sagar S., Chaurasia A., Singh U. Anti-mullerian hormone: a new marker of ovarian function. J Obstet Gyneacol India. 2014;64(2):130–3. https://doi.org/10.1007/s13224-013-0482-3. 10. Hadlow N., Longhurst K., McClements A. et al. Variation in antimüllerian hormone concentration during the menstrual cycle may change the clinical classification of the ovarian response. Fertil Steril. 2013;99(6):1791–7. https://doi.org/10.1016/j.fertnstert.2013.01.132. 11. Kyweluk M.A., Sievert L.L., Huicochea-Gómez L.H. et al. Variation in levels of AMH among Maya and non-Maya women in Campeche, Mexico. Am J Phys Anthropol. 2018;167(2):282–90. https://doi.org/10.1002/ajpa.23627. 12. Marca A.L., Volpe A. The Anti-Mullerian hormone and ovarian cancer. Hum Reprod Update. 2007;13(3):265–73. https://doi.org/10.1093/humupd/dml060. 13. Bentzen J.G., Forman J.L., Johannsen T.H. et al. Ovarian antral follicle subclasses and anti-müllerian hormone during normal reproductive aging. J Clin Endocrinol Metab. 2013;98(4):1602–11. https://doi.org/10.1210/jc.2012-1829. 14. Bentzen J.G., Forman J.L., Larsen E.C. et al. Maternal menopause as a predictor of anti-Müllerian hormone level and antral follicle count in daughters during reproductive age. Hum Reprod. 2013;28(1):247–55. https://doi.org/10.1093/humrep/des356. 15. Homburg R., Ray A., Bhide, P. et al. The relationship of serum antiMullerian hormone with polycystic ovarian morphology and polycystic ovary syndrome: a prospective cohort study. Hum Reprod. 2013;28(4):1077–83. https://doi.org/10.1093/humrep/det015. 16. Schumacher B.M.L., Jukic A.M.Z., Steiner A.Z. Antimüllerian hormone as a risk factor for miscarriage in naturally conceived pregnancies. Fertil Steril. 2018;109(6):1065–71.e1. https://doi.org/10.1016/j.fertnstert.2018.01.039. 17. Peuranpää P., Hautamäki H., Halttunen-Nieminen M. et al. Low antiMüllerian hormone level is not a risk factor for early pregnancy loss in IVF/ICSI treatment. Hum Reprod. 2020;35(3):504–15. https://doi.org/10.1093/humrep/deaa008. 18. Signorile P.G., Baldi F., Bussani R. et al. Ectopic endometrium in human foetuses is a common event and sustains the theory of müllerianosis in the pathogenesis of endometriosis, a disease that predisposes to cancer. J Exp Clin Cancer Res. 2009;28(1):49. https://doi.org/10.1186/1756-9966-28-49. 19. Signorile P.G., Baldi F., Bussani R. et al. Embryologic origin of endometriosis: analysis of 101 human female fetuses. J Cell Physiol. 2012;227(4):1653–6. https://doi.org/10.1002/jcp.22888. 20. Crispi S., Piccolo, M.T., D'Avino A. et al. Transcriptional profiling of endometriosis tissues identifies genes related to organogenesis defects. J Cell Physiol. 2013;228(9):1927–34. https://doi.org/10.1002/jcp.24358. 21. Shebl O., Ebner T., Sommergruber M. et al. Anti-muellerian hormone serum levels in women with endometriosis: a case–control study. Gynecol Endocrinol. 2009;25(11):713–6. https://doi.org/10.3109/09513590903159 615. 22. Kasapoglu I., Ata B., Uyaniklar O. et al. Endometrioma-related reduction in ovarian reserve (ERROR): a prospective longitudinal study. Fertil Steril. 2018;110(1):122–7. https://doi.org/10.1016/j.fertnstert.2018.03.015. 23. Jayaprakasan K., Becker C., Mittal M. The effect of surgery for endometriomas on fertility: scientific impact paper no. 55. BJOG. 2018;125(6):E19–E28. https://doi.org/10.1111/1471-0528.14834. 24. Kim Y.J., Cha S.W., Kim H.O. Serum anti-Müllerian hormone levels decrease after endometriosis surgery. J Obstet Gynaecol. 2017;37(3):342–6. https://doi.org/10.1080/01443615.2016.1239071. 25. Coccia M.E., Rizzello F., Capezzuoli T. et al. Bilateral endometrioma excision: surgery-related damage to ovarian reserve. Reprod Sci. 2019;26(4):543–50. https://doi.org/10.1177/1933719118777640. 26. Lee D.Y., Kim N.Y., Kim M.J. et al. Effects of laparoscopic surgery on serum anti-Müllerian hormone levels in reproductive-aged women with endometrioma. Gynecol Endocrinol. 2011;27(10):733–6. https://doi.org/10.3109/09513590.2010.538098. 27. Ata B., Turkgeldi E., Seyhan A., Urman B. Effect of hemostatic method on ovarian reserve following laparoscopic endometrioma excision; comparison of suture, hemostatic sealant, and bipolar dessication. A systematic review and meta-analysis. J Minim Invasive Gynecol 2015;22(3):363–72. https://doi.org/10.1016/j.jmig.2014.12.168. 28. Li C.Z., Liu B., Wen Z.Q., Sun Q. The impact of electrocoagulation on ovarian reserve after laparoscopic excision of ovarian cysts: a prospective clinical study of 191 patient. Fertil Steril. 2009;92(4):1428–35. https://doi.org/10.1016/j.fertnstert.2008.08.071. 29. Cranney R., Condous G., Reid S. An update on the diagnosis, surgical management, and fertility outcomes for women with endometrioma. Acta Obstet Gynecol Scand. 2017;96(6):633–43. https://doi.org/10.1111/aogs.13114. 30. Stochino-Loi E., Darwish B., Mircea O. et al. Does preoperative antimüllerian hormone level influence postoperative pregnancy rate in women undergoing surgery for severe endometriosis? Fertil Steril. 2017;107(3):707–13.e3. https://doi.org/10.1016/j.fertnstert.2016.12.013. 31. Dunselman G.A.J., Vermeulen N., Becker C. et al. ESHRE guideline: management of women with endometriosis. Hum Reprod. 2014; 29(3):400–12. https://doi.org/10.1093/humrep/det457. 32. Levine D., Brown D.L., Andreotti R.F. et al. Management of asymptomatic ovarian and other adnexal cysts imaged at US: Society of Radiologists in Ultrasound Consensus Conference Statement. Radiology. 2010;256(3):943–54. https://doi.org/10.1148/radiol.10100213. 33. Endometriosis: diagnosis and management. NICE guideline. Published: 6 September 2017; RCOG. 25 p. Available at: https://www.nice.org.uk/guidance/ng73/resources/endometriosis-diagnosis-and-managementpdf-1837632548293. 34. Saito A., Iwase A., Nakamura T. et al. Involvement of mesosalpinx in endometrioma is a possible risk factor for decrease of ovarian reserve after cystectomy: a retrospective cohort study. Reprod Biol Endocrinol. 2016;14(1):72. https://doi.org/10.1186/s12958-016-0210-9. 35. Roman H., Bubenheim M., Auber M. et al. Antimullerian hormone level and endometrioma ablation using plasma energy. JSLS. 2014;18(3). pii: e2014. https://doi.org/10.4293/JSLS.2014.00002. 36. De Conto E., Matte U., Bilibio J.P. et al. Endometriosis-associated infertility: GDF-9, AMH, and AMHR2 genes polymorphisms. J Assist Reprod Genet. 2017;34(12):1667–72. https://doi.org/10.1007/s10815017-1026-z. 37. Jin H., Won M., Park S.E. et al. FOXL2 is an essential activator of SF-1induced transcriptional regulation of anti-Müllerian hormone in human granulosa cells. PloS One. 2016;11(7):e0159112. https://doi.org/10.1371/journal.pone.0159112. 38. Carrarelli P., Rocha A.L., Belmonte G. et al. Increased expression of antimüllerian hormone and its receptor in endometriosis. Fertil Steril. 2014;101(5):1353–8. https://doi.org/10.1016/j.fertnstert.2014.01.052. 39. Seifer D.B., Merhi Z. Is AMH a regulator of follicular atresia? J Assist Reprod Genet. 2014;31(11):1403–7. https://doi.org/10.1007/s10815-0140328-7. 40. Sefrioui O., Madkour A., Aboulmaouahib S. et al. Women with extreme low AMH values could have in vitro fertilization success. Gynecol Endocrinol. 2019;35(2):170–3. https://doi.org/10.1080/09513590.2018.1505850. Review For citations: Molotkov A.S., Yarmolinskaya M.I. A role of anti-Mullerian hormone in external genital endometriosis. Obstetrics, Gynecology and Reproduction. 2021;15(2):182-188. (In Russ.) https://doi.org/10.17749/2313-7347/ob.gyn.rep.2021.164 JATS XML This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.