Possibilities of Using the Method of One-Stage Surgical Activation of the Ovaries in Patients Diagnosed with Infertility Due to Primary Ovarian Failure

Introduction. The relevance of the problem of infertility in the modern world is beyond doubt, which is the basis for the active development and introduction of new surgical methods for the treatment of this disease.

Objective — to show the method of in vitro activation (IVA) of autotransplanted ovarian follicular tissue as a potentially promising infertility therapy for patients with premature ovarian insufficiency with partially preserved ovarian reserve.

Materials and methods. The materials contain 67 analyzed literature sources, of which 10 are Russian-language sources and 57 are English-language sources.

Results and discussions. The analysis of scientific and practical research data will allow evaluating the success of single-stage surgical activation of the ovaries and IVA of the latter using an automaterial, the cortical layer of the ovaries, in women who had previously been diagnosed with infertility on the background of primary ovarian insufficiency (ICD-10 — E28.3/9. Ovarian dysfunction). This literature review examines and analyzes the role of the effect of anti-muller hormone on the effectiveness and effectiveness of assisted reproductive technology treatment, as well as on the formation of premature ovarian insufficiency in women of reproductive age. Against the background of premature ovarian insufficiency, a detailed examination of endometriosis of various localization is relevant (ICD-10 — N80.0–80.9).

Conclusion. Thus, IVA treatment of autotransplanted ovarian follicular tissue is a potentially promising infertility therapy for patients with premature ovarian insufficiency with partially preserved ovarian reserve.

1. Tkachenko LV, Gritsenko IA, Tikhaeva KYu, Sviridova NI, Gavrilova IS, Dolgova VA. Assessment of risk factors and prediction of premature ovarian failure. Obstetrics, Gynecology and Reproduction. 2022;16(1):73–80. (In Russ.). DOI: https://doi.org/10.17749/2313-7347/ob.gyn.rep.2021.273.

2. Salimova MD, Nadelyaeva YaG, Danusevich IN. Modern ideas about clinical and diagnostic criteria for premature ovarian failure (literature review). Acta Biomedica Scientifica. 2020;5(6):42–50. (In Russ.). DOI: https://doi.org/10.29413/ABS.2020-5.6.5.

3. Marchenko LA, Mashaeva RI. Clinical and laboratory criteria for the occult form of premature ovarian failure. Gynecology. 2018;20(6):73–76. (In Russ.). DOI: https://doi.org/10.26442/20795696.2018.6.180069.

4. Yuta K, Kazuhiro K. Fertility preservation in patients with severe ovarian dysfunction. Journal of Visualized Experiments. 2021;(169): e62098. DOI: https://doi.org/10.3791/62098.

5. Tomao F, Spinelli GP, Panici PB, Frati L, Tomao S. Ovarian function, reproduction and strategies for fertility preservation after breast cancer. Critical Reviews in Oncology/Hematology. 2010;76(1):1–12. DOI: https://doi.org/10.1016/j.critrevonc.2009.12.005.

6. Kim S, Lee Y, Lee S, Kim T. Ovarian tissue cryopreservation and transplantation in patients with cancer. Obstetrics & Gynecology Science. 2018;61(4):431–442. DOI: https://doi.org/10.5468/ogs.2018.61.4.431.

7. Donnez J, Dolmans MM. Ovarian tissue freezing: Current status. Current Opinion in Obstetrics and Gynecology. 2015;27(3):222–230. DOI: https://doi.org/10.1097/GCO.0000000000000171.

8. Kawamura K, Kawamura N, Hsueh AJW. Activation of dormant follicles a new treatment for premature ovarian failure? Current Opinion in Obstetrics and Gynecology. 2016;28(3):217–222. DOI: https://doi.org/10.1097/GCO.0000000000000268.

9. Adamyan LV, Dementyeva VO, Asaturova AV, Stepanian AA, Smolnikova VYu, Arakelyan AS, et al. One-step surgery for activation of ovarian function in patients with premature ovarian insufficiency (POI) and “poor” ovarian response. Russian Journal of Human Reproduction. 2020;26(2):58–64. (In Russ.). DOI: https://doi.org/10.17116/repro20202605158.

10. Adamyan LV, Pivazyan LG, Antonova AA. Autoimmunity and premature ovarian insufficiency — up-to-date. Russian Journal of Human Reproduction. 2022;28 (6):116–124. (In Russ.). DOI: https://doi.org/10.17116/repro202228061116.

11. Adamyan LV, Pivazyan LG. Interdisciplinary approach and the current state of the issue of premature ovarian aging (literature review). Russian Journal of Human Reproduction. 2023;29(1):94–103. (In Russ.). DOI: https://doi.org/10.17116/repro20232901194.

12. Dolgushina NV, Adamyan LV, Sheshko EL. Late reproductive age of women: Risks of reproductive function disorders (literature review). Russian Journal of Human Reproduction. 2023;29(4):99–106. (In Russ.). DOI: https://doi.org/10.17116/repro20232904199.

13. Adamyan LV, Dementyeva VO, Asaturova AV, Nazarenko TA. One-step surgical procedure for ovarian function activation (first clinical observation). Russian Journal of Human Reproduction. 2019;25(1):97–99. (In Russ.). DOI: https://doi.org/10.17116/repro20192501197.

14. Tan Z, Hung SW, Zheng X, Wang CC, Chung JP, Zhang T. What we have learned from animal models to understand the etiology and pathology of endometrioma-related infertility. Biomedicines. 2022;10(7):1483. DOI: https://doi.org/10.3390/biomedicines10071483.

15. Luddi A, Marrocco C, Governini L, Semplici B, Pavone V, Luisi S, et al. Expression of matrix metalloproteinases and their inhibitors in endometrium: High levels in endometriotic lesions. International Journal of Molecular Sciences. 2020;21(8):2840. DOI: https://doi.org/10.3390/ijms21082840.

16. Fachin R, Taieb J, Lozano D, Ducot B, Frydman R, Bouyer J. High reproducibility of serum anti-Mullerian hormone measurements suggests a multi-staged follicular secretion and strengthens its role in the assessment of ovarian follicular status. Human Reproduction. 2005;20(4):923–927. DOI: https://doi.org/10.1093/humrep/deh688.

17. Lekamge DN, Barry M, Kolo M, Lane M, Gilchrist RB, Tremellen KP. Anti-Müllerian hormone as a predictor of IVF outcome. Reproductive Biomedicine Online. 2007;14(5):602–610. DOI: https://doi.org/10.1016/s1472-6483(10)61053-x.

18. Kwee J, Schats R, McDonnell J, Themmen A, de Jong F, Lambalk C. Evaluation of anti-Müllerian hormone as a test for the prediction of ovarian reserve. Fertility and Sterility. 2008;90(3):737–743. DOI: https://doi.org/10.1016/j.fertnstert.2007.07.1293.

19. Fraisse T, Ibecheole V, Streuli I, Bischof P, de Ziegler D. Undetectable serum anti-Müllerian hormone levels and occurrence of ongoing pregnancy. Fertility and Sterility. 2008;89(3):723.E9–723.E11. DOI: https://doi.org/10.1016/j.fertnstert.2007.03.084.

20. Nelson SM, Yates RW, Lyall H, Jamieson M, Traynor I, Gaudoin M, et al. Anti-Müllerian hormone-based approach to controlled ovarian stimulation for assisted conception. Journal of Gynecology Obstetrics and Human Reproduction. 2009;24(4):867–875. DOI: https://doi.org/10.1093/humrep/den480.

21. Laml T, Preyer O, Umek W, Hengstschlager M, Hanzal H. Genetic disorders in premature ovarian failure. Human Reproduction Update. 2002;8(5):483–491. DOI: https://doi.org/10.1093/humupd/8.5.483.

22. Hagerman RJ, Leavitt BR, Farzin F, Jacquemont S, Greco CM, Brunberg JA, et al. Fragile-X-associated tremor/ataxia syndrome (FXTAS) in females with the FMR1 premutation. The American Journal of Human Genetics. 2004;74(5):1051–1056. DOI: https://doi.org/10.1086/420700.

23. Hagerman RJ, Hagerman PJ. The fragile X premutation: Into the phenotypic fold. Current Opinion in Genetics and Development. 2002;12(3):278–283. DOI: https://doi.org/10.1016/s0959-437x(02)00299-x.

24. Bodega B, Porta C, Crosignani PG, Ginelli E, Marozzi A. Mutations in the coding region of the FOXL2 gene are not a major cause of idiopathic premature ovarian failure. Molecular Aspects of Human Reproductive Physiology. 2004;10(8):555–557. DOI: https://doi.org/10.1093/molehr/gah078.

25. Ahonen P, Myllärniemi S, Sipilä I, Perheentupa J. Clinical variation of autoimmune polyendocrinopathy-can-didiasis-ectodermal dystrophy (APECED) in a series of 68 patients. The New England Journal of Medicine. 1990;322(26):1829–1836. DOI: https://doi.org/10.1056/NEJM199006283222601.

26. Nagamine K, Peterson P, Scott HS, Kudoh J, Minoshima S, Heino M, et al. Positional cloning of the APECED gene. Nature Genetics. 2019;17:393–398. DOI: https://doi.org/10.1038/ng1297-393.

27. Tan Z, Gong X, Wang CC, Zhang T, Huang J. Diminished ovarian reserve in endometriosis: Insights from in vitro, in vivo, and human studies — a systematic review. International Journal of Molecular Sciences. 2023;24(21):15967. DOI: https://doi.org/10.3390/ijms242115967.

28. Moreno-Sepulveda J, Romeral C, Niño G, Pérez-Benavente A. The effect of laparoscopic endometrioma surgery on anti-Müllerian hormone: A systematic review of the literature and meta-analysis. JBRA Assisted Reproduction. 2022;26(1):88–104. DOI: https://doi.org/10.5935/1518-0557.20210060.

29. Tan Z, Hung SW, Zheng X, Wang CC, Chung JP, Zhang T. What we have learned from animal models to understand the etiology and pathology of endometrioma-related infertility. Biomedicines. 2022;10(7):1483. DOI: https://doi.org/10.3390/biomedicines10071483.

30. Hayashi S, Nakamura T, Motooka Y, Ito F, Jiang L, Akatsuka S, et al. Novel ovarian endometriosis model causes infertility via iron-mediated oxidative stress in mice. Redox Biology. 2020;37:101726. DOI: https://doi.org/10.1016/j.redox.2020.101726.

31. Cacciottola L, Donnez J, Dolmans MM. Can endometriosis-related oxidative stress pave the way for new treatment targets? International Journal of Molecular Sciences. 2021;22(13):7138. DOI: https://doi.org/10.3390/ijms22137138.

32. Bonavina G, Taylor HS. Endometriosis-associated infertility: From pathophysiology to tailored treatment. Frontiers in Endocrinology. 2022;13:1020827. DOI: https://doi.org/10.3389/fendo.2022.1020827.

33. Choi YS, Cho S, Seo SK, Park JH, Kim SH, Lee BS. Alteration in the intrafollicular thiol-redox system in infertile women with endometriosis. Reproduction. 2015;149(2):155–162. DOI: https://doi.org/10.1530/REP-14-0438.

34. Paffoni A, Bolis V, Ferrari S, Benaglia L, Vercellini P, Somigliana E. The gametotoxic effects of the endometrioma content: Insights from a parthenogenetic human model. Reproductive Sciences. 2019;26:573–579. DOI: https://doi.org/10.1177/1933719118777637.

35. Da Broi MG, Malvezzi H, Paz CC, Ferriani RA, Navarro PA. Follicular fluid from infertile women with mild endometriosis may compromise the meiotic spindles of bovine metaphase II oocytes. Human Reproduction. 2014;29(2):315–323. DOI: https://doi.org/10.1093/humrep/det378.

36. Ban Frangež H, Vrtacnik Bokal E, Štimpfel M, Divjak Budihna T, Gulino FA, Garzon S, et al. Reproductive outcomes after laparoscopic surgery in infertile women affected by ovarian endometriomas, with or without in vitro fertilisation: Results from the SAFE (surgery and ART for endometriomas) trial. Journal of Obstetrics and Gynaecology. 2022;42(5):1293–1300. DOI: https://doi.org/10.1080/01443615.2021.1959536.

37. Dongye H, Ji X, Ma X, Song J, Yan L. The impact of endometriosis on embryo quality in in-vitro Fertilization/Intracytoplasmic sperm injection: A systematic review and meta-analysis. Frontiers in Medicine. 2021;8:669342. DOI: https://doi.org/10.3389/fmed.2021.669342.

38. Freis A, Dietrich JE, Binder M, Holschbach V, Strowitzki T, Germeyer A. Relative morphokinetics assessed by time-lapse imaging are altered in embryos from patients with endometriosis. Reproductive Sciences. 2018;25(8):1279–1285. DOI: https://doi.org/10.1177/1933719117741373.

39. Wu CQ, Albert A, Alfaraj S, Taskin O, Alkusayer GM, Havelock J, et al. Live birth rate after surgical and expectant management of endometriomas after In vitro fertilization: A systematic review, meta-analysis, and critical appraisal of current guidelines and previous meta-analyses. Journal of Minimally Invasive Gynecology. 2019;26(2):299–311.E3. DOI: https://doi.org/10.1016/j.jmig.2018.08.029.

40. Nankali A, Kazeminia M, Jamshidi PK, Shohaimi S, Salari N, Mohammadi M, et al. The effect of unilateral and bilateral laparoscopic surgery for endometriosis on anti-mullerian hormone (AMH) level after 3 and 6 months: A systematic review and meta-analysis. Health and Quality of Life Outcomes. 2020;18:314–327. DOI: https://doi.org/10.1186/s12955-020-01561-3.

41. Kutlesic R, Kutlesic M, Milosevic-Stevanovic J, Vukomanovic P, Stefanovic M, Mostic-Stanisic D. Prolactin and hyperprolactinaemia in endometriosis-related infertility: Are there clinically significant connections? Journal of Clinical Medicine. 2024;13(19):5868. DOI: https://doi.org/10.3390/jcm13195868.

42. Lee GJ, Porreca F, Navratilova E. Prolactin and pain of endometriosis. Pharmacology & Therapeutics. 2023;247:108435. DOI: https://doi.org/10.1016/j.pharmthera.2023.108435.

43. Vannuccini S, Clemenz AS, Rossi M, Petraglia F. Hormonal treatments for endometriosis: The endocrine background. Reviews in Endocrine and Metabolic Disorders. 2022;23(3):333–355. DOI: https://doi.org/10.1007/s11154-021-09666-w.

44. Ciriaco P, Muriana P, Carretta A, Ottolina J, Candiani M, Negri G. Catamenial pneumothorax as the first expression of thoracic endometriosis syndrome and pelvic endometriosis. Journal of Clinical Medicine. 2022; 11(5):1200. DOI: https://doi.org/10.3390/jcm11051200.

45. Eisenberg VH, Decter DH, Chodick G, Shalev V, Weil C. Burden of endometriosis: Infertility, comorbidities, and healthcare resource utilization. Journal of Clinical Medicine. 2022;11(4):1133. DOI: https://doi.org/10.3390/jcm11041133.

46. Meixell DA, Mamillapalli R, Taylor HS. Methylation of microribonucleic acid Let-7b regulatory regions in endometriosis. Fertility and Sterility. 2022;3(2):197–203. DOI: https://doi.org/10.1016/j.xfss.2022.03.001.

47. Munrós J, Martínez-Zamora MA, Tàssies D, Reverter JC, Rius M, Gracia M, et al. Total circulating microparticle levels after laparoscopic surgical treatment for endometrioma: A pilot, prospective, randomized study comparing stripping with CO2 laser vaporization. Journal of Minimally Invasive Gynecology. 2019; 26(3):450–455. DOI: https://doi.org/10.1016/j.jmig.2018.05.014.

48. Raffaelli R, Garzon S, Baggio S, Genna M, Pomini P, Laganà AS, et al. Mesenteric vascular and nerve sparing surgery in laparoscopic segmental intestinal resection for deep infiltrating endometriosis. European Journal of Obstetrics & Gynecology and Reproductive Biology. 2018;231:214–219. DOI: https://doi.org/10.1016/j.ejogrb.2018.10.057.

49. Levander G, Normann P. The pathogenesis of endometriosis. Acta Obstetricia et Gynecologica Scandinavica. 1955;34(4):366–398. DOI: https://doi.org/10.3109/00016345509158287.

50. Molotkov AS, Yarmolinskaya MI. The significance of prolactin in the pathogenesis of genital endometriosis and the possibilities of dopamine agonist therapy. Russian Bulletin of Obstetricians and Gynecology. 2015; 15(6):42–47. (In Russ.). DOI: https://doi.org/10.17116/rosakush201515642-47.

51. Bulun SE, Yilmaz BD, Sison C, Miyazaki K, Bernardi L, Liu S, et al. Endometriosis. Endocrine Reviews. 2019;40(4):1048–1079. DOI: https://doi.org/10.1210/er.2018-00242.

52. Hapangama DK, Drury J, Da Silva L, Al-Lamee H, Earp A, Valentijn AJ, et al. Abnormally located SSEA1+/SOX9+ endometrial epithelial cells with a basalis-like phenotype in the eutopic functionalis layer may play a role in the pathogenesis of endometriosis. Human Reproduction. 2019;34(1):56–68. DOI: https://doi.org/10.1093/humrep/dey336.

53. Li D, Li H, Wang Y, Eldomany A, Wu J, Yuan C, et al. Development and characterization of a polarized human endometrial cell epithelia in an air-liquid interface state. Stem Cell Research & Therapy. 2018;9(1):209. DOI: https://doi.org/10.1186/s13287-018-0962-6.

54. Ni Z, Li Y, Song D, Ding J, Mei S, Sun S, et al. Iron-overloaded follicular fluid increases the risk of endometriosis-related infertility by triggering granulosa cell ferroptosis and oocyte dysmaturity. Cell Death & Disease. 2022;13(7):579. DOI: https://doi.org/10.1038/s41419-022-05037-8.

55. Hoek A, Schoemaker J, Drexhage HA. Premature ovarian failure and ovarian autoimmunity. Endocrinology Reviews. 2020;18(1):107–134. DOI: https://doi.org/10.1210/edrv.18.1.0291.

56. Borghese B, Santulli P, Marcellin L, Chapron C. Definition, description, clinicopathological features, pathogenesis and natural history of endometriosis: CNGOF-HAS Endometriosis Guidelines. Gynécologie Obstétrique Fertilité & Sénologie. 2018;46(3):156–167. (In French). DOI: https://doi.org/10.1016/j.gofs.2018.02.017.

57. Kudryavtseva EV, Geets AV, Mangileva YA, Chizhova AV, Patsyuk OV. Modern non-invasive methods for diagnosing endometriosis. Ural Medical Journal. 2023;22(4):140–147. (In Russ). DOI: https://doi.org/10.52420/2071-5943-2023-22–4-140-147.

58. Izumi G, Koga K, Takamura M, Makabe T, Satake E, Takeuchi A, et al. Involvement of immune cells in the pathogenesis of endometriosis. Journal of Obstetrics and Gynaecology Research. 2018;44(2):191–198. DOI: https://doi.org/10.1111/jog.13559.

59. Signorile PG, Cassano M, Viceconte R, Spyrou M, Marcattilj V, Baldi A. Endometriosis: A retrospective analysis on diagnostic data in a cohort of 4,401 patients. In Vivo. 2022;36(1):430–438. DOI: https://doi.org/10.21873/invivo.12721.

60. Muhaidat N, Saleh S, Fram K, Nabhan M, Almahallawi N, Alryalat SA, et al. Prevalence of endometriosis in women undergoing laparoscopic surgery for various gynaecological indications at a Jordanian referral centre: Gaining insight into the epidemiology of an important women’s health problem. BMC Women’s Health. 2021;21(1):381. DOI: https://doi.org/10.1186/s12905-021-01530-y.

61. Becker CM, Bokor A, Heikinheimo O, Horne A, Jansen F, Kiesel L, et al.; ESHRE Endometriosis Guideline Group. ESHRE guideline: Endometriosis. Human Reproduction Open. 2022;2022(2):hoac009. DOI: https://doi.org/10.1093/hropen/hoac009.

62. Bezhenar VF, Kruglov SV, Krylova SV, Izorkina VA, Kravtsov AA. Clinical characteristics of patients and morphological features of infiltrative forms of endometriosis, as well as the results of nerve-saving methods of surgical treatment. Ural Medical Journal. 2019;(5):24–31. (In Russ.). EDN: https://www.elibrary.ru/BLXIBK.

63. Kolanska K, Alijotas-Reig J, Cohen J, Cheloufi M, Selleret L, d’Argent E, et al. Endometriosis with infertility: A comprehensive review on the role of immune deregulation and immunomodulation therapy. The American Journal of Reproductive Immunology. 2021;85(3):e13384. DOI: https://doi.org/10.1111/aji.13384.

64. Tanbo T, Fedorcsak P. Endometriosis-associated infertility: Aspects of pathophysiological mechanisms and treatment options. Acta Obstetricia et Gynecologica Scandinavica. 2017;96(6):659–667. DOI: https://doi.org/10.1111/aogs.13082.

65. Da Broi MG, Ferriani RA, Navarro PA. Ethiopathogenic mechanisms of endometriosis-related infertility. JBRA Assisted Reproduction. 2019;23(3):273–280. DOI: https://doi.org/10.5935/1518-0557.20190029.

66. Da Broi MG, Navarro PA. Oxidative stress and oocyte quality: Ethiopathogenic mechanisms of minimal/mild endometriosis-related infertility. Cell and Tissue Research. 2016;364(1):1–7. DOI: https://doi.org/10.1007/s00441-015-2339-9.

67. Kawamura K, Ishizuka B, Hsueh AJW. Drug-free in-vitro activation of follicles for infertility treatment in poor ovarian response patients with decreased ovarian reserve. Reproductive BioMedicine Online. 2020; 40(2):245–253. DOI: https://doi.org/10.1016/j.rbmo.2019.09.007.