The problem of recurrence of ovarian endometriomas
https://doi.org/10.21886/2219-8075-2025-16-1-5-13
Abstract
Objective: this article is a scientific review of the literature devoted to the important problem of ovarian endometrioma recurrence in the postoperative period. The data were analyzed based on foreign and domestic sources e-Library, Springer Nature, Wiley Journals, PubMed for 2016–2023 using the following keywords: «endometrioma», «risk factors», «recurrence», «prediction», «biomarkers». In the process of literature review, a significant relationship between infertility and ovarian endometriosis has been established, but all mechanisms in the occurrence of infertility in ovarian endometriomas remain incompletely understood. Noninvasive markers involved in the pathogenesis of the disease - apoptosis, angiogenesis, adhesion, as well as the possibilities of the diagnostic model of noninvasive diagnosis of endometriomas in the postoperative period are described in detail. The data on the effectiveness of drug therapy, as a way of preventing postoperative recurrence of the disease are highlighted and summarized.
About the Authors
V. B. Tskhay
Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University; Federal Siberian Research Clinical Centre, Federal Medical-Biological Agency
Russian Federation
Competing Interests:
Russian Federation
Vitaly B. Tskhay, Dr. Sci. (Med.), Professor, Head of the Department of Perinatology, Obstetrics and Gynecology; Scientific consultant
Krasnoyarsk
Competing Interests:
Authors declare no conflict of interest
E. K. Grebennikova
Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University
Russian Federation
Competing Interests:
Russian Federation
Elvira K. Grebennikova, Cand. Sci. (Med.), Associate Professor of the Department of Perinatology, Obstetrics and Gynecology
Krasnoyarsk
Competing Interests:
Authors declare no conflict of interest
Ju. N. Skuratova
Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University
Russian Federation
Competing Interests:
Russian Federation
Yulia N. Skuratova, Assistant at the Department of Perinatology, Obstetrics and Gynecology
Krasnoyarsk
Competing Interests:
Authors declare no conflict of interest
References
1. Bergman-Larsson J, Gustafsson S, Méar L, Huvila J, Tolf A, et al. Combined expression of HOXA11 and CD10 identifies endometriosis versus normal tissue and tumors. Ann Diagn Pathol. 2022;56:151870. https://doi.org/10.1016/j.anndiagpath.2021.151870
2. Adamyan LV, Alyasova AV, Pivazyan LG, Stepanian AA. Immunological aspects of endometriosis: pathophysiological mechanisms, diagnosis, autoimmunity, targeted therapy and modulation. Russian Journal of Human Reproduction. 2024;30(2):15-31. (In Russ.) https://doi.org/10.17116/repro20243002115
3. Podzolkova N.M., Fadeev I.E., Mass E.E., Poletova T.N., Sumyatina L.V., Denisova T.V. Non-invasive diagnosis and non-surgical treatment of endometriosis: A review. Gynecology. 2022;24(3):167-173. (In Russ.) https://doi.org/10.26442/20795696.2022.3.201508
4. Balan V.E., Orlova S.A., Titchenko Iu.P., Fedorov A.A. Noninvasive markers of endometriosis and their dynamics during hormone therapy. Russian Journal of Human Reproduction. 2018;24(5):77-81. (In Russ.) https://doi.org/10.17116/repro20182405177
5. Sun M, Xu P, Zou G, Wang J, Zhu L, Zhang X. Extrinsic Adenomyosis Is Associated With Postoperative Recurrence of Ovarian Endometrioma. Front Med (Lausanne). 2022;8:815628. https://doi.org/10.3389/fmed.2021.815628
6. Choi SH, Kim S, Lee SW, Won S, Shim SH, et al. Recurrence, Reoperation, Pregnancy Rates, and Risk Factors for Recurrence after Ovarian Endometrioma Surgery: Long-Term Follow-Up of 756 Women. Yonsei Med J. 2023;64(3):204-212. https://doi.org/10.3349/ymj.2022.0278
7. Solopova A.G., Achkasov E.E., Moskvichyova V.S., Grigorevskaya E., Ampilogova D.M. External genital endometriosis: treatment and rehabilitation. Obstetrics, Gynecology and Reproduction. 2021;15(1):70-79. (In Russ.) https://doi.org/10.17749/2313-7347/ob.gyn.rep.2020.148
8. Davydov A.I., Mikhaleva L.M., Tairova M.B., Patsap O.I. Ovarian endometriosis: a form of genital endometriosis or a separate nosological entity? Issues of gynecology, obstetrics and perinatology. 2019;18(5):5–12. (In Russ.) https://doi.org/10.20953/1726-1678-2019-5-5-12.
9. Gałczyński K, Jóźwik M, Lewkowicz D, Semczuk-Sikora A, Semczuk A. Ovarian endometrioma – a possible finding in adolescent girls and young women: a mini-review. J Ovarian Res. 2019;12(1):104. https://doi.org/10.1186/s13048-019-0582-5
10. Yarmolinskaya M.I., Rusina E.I., Khachaturyan A.R., Florova M.S. Clinical picture and diagnosis of genital endometriosis. Journal of obstetrics and women’s diseases. 2016;65(5):4-21. https://doi.org/10.17816/JOWD6554-21
11. Sasaran V, Alexa Bad CM, Muresan D, Puscasiu L. Ultrasound pattern and diagnostic accuracy of primary ovarian endometrioma and its recurrence: a pictorial essay. Med Ultrason. 2020;22(2):230-235. https://doi.org/10.11152/mu-2331
12. Huang G, Fan X, Zhu P. Analysis of recurrence factors associated with conservative surgery for ovarian-type endometriosis. Ann Transl Med. 2022;10(5):255. https://doi.org/10.21037/atm-22-189
13. Becker CM, Bokor A, Heikinheimo O, Horne A, Jansen F, et al. ESHRE guideline: endometriosis. Hum Reprod Open. 2022;2022(2):hoac009. https://doi.org/10.1093/hropen/hoac009
14. Leyland N, Casper R, Laberge P, Singh SS; SOGC. Endometriosis: diagnosis and management. J Obstet Gynaecol Can. 2010;32(7 Suppl 2):S1-32. PMID: 21545757
15. Carmona F, Martínez-Zamora MA, Rabanal A, MartínezRomán S, Balasch J. Ovarian cystectomy versus laser vaporization in the treatment of ovarian endometriomas: a randomized clinical trial with a five-year follow-up. Fertil Steril. 2011;96(1):251-254. https://doi.org/10.1016/j.fertnstert.2011.04.068
16. Muzii L, Achilli C, Lecce F, Bianchi A, Franceschetti S, et al. Second surgery for recurrent endometriomas is more harmful to healthy ovarian tissue and ovarian reserve than first surgery. Fertil Steril. 2015;103(3):738-743. https://doi.org/10.1016/j.fertnstert.2014.12.101
17. Yang X, Bao M, Hang T, Sun W, Liu Y, et al. Status and related factors of postoperative recurrence of ovarian endometriosis: a cross-sectional study of 874 cases. Arch Gynecol Obstet. 2023;307(5):1495-1501. https://doi.org/10.1007/s00404-023-06932-x
18. Tikhomirov A.L. Endometriosis: quality of life, prognosis and prevention. Obstetrics and gynecology:news, opinions, training. 2020;8(3):132-136 (In Russ.) https://doi.org/10.24411/2303-9698-2020-13022
19. Orazov M.R., Radzinskiy V.E., Khamoshina M.B., Kavteladze E.V., Pukhalskaya I.F., et al. Treatment efficacy of infertility due to recurrent external genital endometriosis. Gynecology. 2019;21(1):38-43. (In Russ.) https://doi.org/10.26442/20795696.2019.1.190230
20. Li XY, Chao XP, Leng JH, Zhang W, Zhang JJ, et al. Risk factors for postoperative recurrence of ovarian endometriosis: longterm follow-up of 358 women. J Ovarian Res. 2019;12(1):79. https://doi.org/10.1186/s13048-019-0552-y
21. Muzii L, Galati G, Mattei G, Chinè A, Perniola G, et al. Expectant, Medical, and Surgical Management of Ovarian Endometriomas. J Clin Med. 2023;12(5):1858. https://doi.org/10.3390/jcm12051858
22. Shaltout MF, Elsheikhah A, Maged AM, Elsherbini MM, Zaki SS, et al. A randomized controlled trial of a new technique for laparoscopic management of ovarian endometriosis preventing recurrence and keeping ovarian reserve. J Ovarian Res. 2019;12(1):66. https://doi.org/10.1186/s13048-019-0542-0
23. Tan Z, Gong X, Li Y, Hung SW, Huang J, et al. Impacts of endometrioma on ovarian aging from basic science to clinical management. Front Endocrinol (Lausanne). 2023;13:1073261. https://doi.org/10.3389/fendo.2022.1073261
24. Bakhtiyarov K.R., Semeryuk T.A., Churganova A.A. Preservation of the ovarian reserve in patients with endometriosis. Zdorov’e i obrazovanie v XXI veke. 2018;20(5):9-14 (In Russ.). eLIBRARY ID: 34964673 EDN: XOCTCX
25. Bonavina G, Taylor HS. Endometriosis-associated infertility: From pathophysiology to tailored treatment. Front Endocrinol (Lausanne). 2022;13:1020827. https://doi.org/10.3389/fendo.2022.1020827
26. Kasapoglu I, Ata B, Uyaniklar O, Seyhan A, Orhan A, et al. Endometrioma-related reduction in ovarian reserve (ERROR): a prospective longitudinal study. Fertil Steril. 2018;110(1):122-127. https://doi.org/10.1016/j.fertnstert.2018.03.015
27. Filip L, Duică F, Prădatu A, Crețoiu D, Suciu N, et al. Endometriosis Associated Infertility: A Critical Review and Analysis on Etiopathogenesis and Therapeutic Approaches. Medicina (Kaunas). 2020;56(9):460. https://doi.org/10.3390/medicina56090460
28. Orazov M.R., Khamoshina M.B., Abitova M.Z., Mikhaleva L.M., Volkova S.V., et al. Ovarian endometriosis associated infertility: a modern view to the problem. Gynecology. 2020;22(5):44-49. (In Russ.) https://doi.org/10.26442/20795696.2020.5.200405
29. Sengoku K, Miyamoto T, Horikawa M, Katayama H, Nishiwaki K, et al. Clinicopathologic risk factors for recurrence of ovarian endometrioma following laparoscopic cystectomy. Acta Obstet Gynecol Scand. 2013;92(3):278-284. https://doi.org/10.1111/aogs.12051
30. Yang F, Liu B, Xu L, Liu H. Age at surgery and recurrence of ovarian endometrioma after conservative surgery: a meta-analysis including 3125 patients. Arch Gynecol Obstet. 2020;302(1):23-30. https://doi.org/10.1007/s00404-020-05586-3
31. Kachalina T.S., Bogatova M.E., Kuznetsov S.S., Lazukin V.F. Risk factors for recurrence of ovarian endometriomas after surgical treatment: retrospective cohort study. Sechenov Medical Journal. 2020;11(4):60–71. (In Russ.) https://doi.org/10.47093/2218-7332.2020.11.4.60-71
32. Borisova AV, Kozachenko AV, Frankevich VE, Chagovets VV, Kononokhin AS, et al. Risk factors for recurrence of external genital endometriosis after surgical treatment: prospective cohortant study. Meditsinskiy sovet = Medical Council. 2018;(7):32-38. (In Russ.) https://doi.org/10.21518/2079-701X-2018-7-32-38
33. Ding S, Lin Q, Zhu T, Li T, Zhu L, et al. Is there a correlation between inflammatory markers and coagulation parameters in women with advanced ovarian endometriosis? BMC Womens Health. 2019;19(1):169. https://doi.org/10.1186/s12905-019-0860-9
34. Ling X, Wang T. Diagnostic and prognostic value of coagulation-related factors in endometriosis. Am J Transl Res. 2022;14(11):7924-7931. PMID: 36505289; PMCID: PMC9730110.
35. Begovich E., Solopova A.G., Idrisova L.EH., Khlopkova S. Quality of life and rehabilitation technologies in patients with external genital endometriosis. Vrach. 2021;32(8):11-17. (In Russ.). https://doi.org/10.29296/25877305-2021-08-02
36. Luo J, Song Z, Zhang T, Chu K, Li J, et al. Upregulation of h-TERT and Ki-67 in ectopic endometrium is associated with recurrence of endometriosis. J Zhejiang Univ Sci B. 2022;23(2):158-163. https://doi.org/10.1631/jzus.B2100502
37. Adamyan LV, Aznaurova YaB. Biomarkers of endometriosis — current trends. Problemy reprodukcii. 2018;24(1):57-62. (In Russ.). https://doi.org/10.17116/repro201824157-62
38. Mezhlumova NA, Bobrov MYu, Adamyan LV. Biomarkers of endometriosis: problems and possibilities of early detection of disease recurrence (a review). Russian Journal of Human Reproduction. 2018;24(6):139-148. (In Russ.) https://doi.org/10.17116/repro201824061139
39. Chmaj-Wierzchowska K, Kampioni M, Wilczak M, Sajdak S, Opala T. Novel markers in the diagnostics of endometriomas: Urocortin, ghrelin, and leptin or leukocytes, fibrinogen, and CA-125? Taiwan J Obstet Gynecol. 2015;54(2):126-130. https://doi.org/10.1016/j.tjog.2014.08.004
40. Kimber-Trojnar Ż, Pilszyk A, Niebrzydowska M, Pilszyk Z, Ruszała M, Leszczyńska-Gorzelak B. The Potential of NonInvasive Biomarkers for Early Diagnosis of Asymptomatic Patients with Endometriosis. J Clin Med. 2021;10(13):2762. https://doi.org/10.3390/jcm10132762
41. Abitova M.Z., Orazov M.R., Khamoshina M.B., Volkova S.V., Aryutin D.G., Demina О.А. Ovarian endometriosis-relapse prediction: a modern paradigm. Akusherstvo i ginekologiya: novosti, mneniya, obuchenie [Obstetrics and Gynecology: News, Opinions, Training]. 2020;8(3):115-120. (in Russ.) https://doi.org/10.24411/2303-9698-2020-13019
42. Brătilă E, Brătilă CP, Comandaşu DE, Bauşic V, Vlădescu CT, et al. The assessment of immunohistochemical profile of endometriosis implants, a practical method to appreciate the aggressiveness and recurrence risk of endometriosis. Rom J Morphol Embryol. 2015;56(4):1301-1307. PMID: 26743275.
43. Zhang J, Wang H, Meng Q, Chen J, Wang J, Huang S. Expression of MTA1 in endometriosis and its relationship to the recurrence. Medicine (Baltimore). 2018;97(35):e12115. https://doi.org/10.1097/MD.0000000000012115
44. Guo SW. Recurrence of endometriosis and its control. Hum Reprod Update. 2009;15(4):441-461. https://doi.org/10.1093/humupd/dmp007
45. Sansone AM, Hisrich BV, Young RB, Abel WF, Bowens Z, et al. Evaluation of BCL6 and SIRT1 as Non-Invasive Diagnostic Markers of Endometriosis. Curr Issues Mol Biol. 2021;43(3):1350-1360. https://doi.org/10.3390/cimb43030096
46. Pshenichnyuk E.Yu., Asaturova A.V., Adamyan L.V., Zaitsev N.V. Immunohistochemical features of eutopic and ectopic endometrium in patients with recurrent ovarian endometrioid cysts. Obstetrics and Gynegology. 2018;(3):84-95 (In Russ.). https://doi.org/10.18565/aig.2018.3.84-95
47. Selcuk S, Cam C, Koc N, Kucukbas M, Ozkaya E, et al. Evaluation of risk factors for the recurrence of ovarian endometriomas. Eur J Obstet Gynecol Reprod Biol. 2016;203:56-60. https://doi.org/10.1016/j.ejogrb.2016.05.008
48. Xu X, Chen Y, Yu Q, Wang J, Xu P, et al. The presence of living endometrial cells in ovarian endometriotic cyst fluid may contribute to the recurrence of endometriosis after surgical excision of endometriomas. J Ovarian Res. 2022;15(1):89. https://doi.org/10.1186/s13048-022-01018-9
49. Artymuk N.V., Zotova O.A., Vaulina E.N. Endometriomas: the effectiveness of combination treatment. Gynecology. 2021;23(6):536-541. https://doi.org/10.26442/20795696.2021.6.201173
50. Wacharachawana S, Phaliwong P, Prommas S, Smanchat B, Bhamarapravatana K, Suwannarurk K. Recurrence Rate and Risk Factors for the Recurrence of Ovarian Endometriosis after Laparoscopic Ovarian Cystectomy. Biomed Res Int. 2021;2021:6679641. https://doi.org/10.1155/2021/6679641
51. Makarenko T.A., Galkina D.E., Borisova E.A. Conservative treatment strategies for endometrioid ovarian cysts: A review. Gynecology. 2023;25(1):4-10. https://doi.org/10.26442/20795696.2023.1.201803
52. Wattanayingcharoenchai R, Rattanasiri S, Charakorn C, Attia J, Thakkinstian A. Postoperative hormonal treatment for prevention of endometrioma recurrence after ovarian cystectomy: a systematic review and network meta-analysis. BJOG. 2021;128(1):25-35. https://doi.org/10.1111/1471-0528.16366
53. Endometriosis. Clinical guidelines. Moscow: Ministry of Health of the Russian Federation. 2020. (In Russ.).
54. Bezhenar’ VF, Iarmolinskaia MI, Baĭliuk EN, Tsypurdeeva A.A., Tsitskarava D.Z., et al. The comparison of the efficacy of different regimens of postoperative hormonal therapy in infertile women with endometriosis. Russian Journal of Human Reproduction. 2015;21(4):89-98. (In Russ.) https://doi.org/10.17116/repro201521489-98
55. Chernukha G.E., Dumanovskaya M.R., Ilina L.M. Ovarian endometriosis and fertility preservation problem. Gynecology. 2021;23(2):110-116. https://doi.org/10.26442/20795696.2021.2.200822
56. Namazova M.R., Orlova E.S., Artemova O.I. Pathogenetic aspects of development of adenomyosis and endometriosis (a review). Siberian Medical Review. 2023;(4):5-14. (In Russ.). eLIBRARY ID: 54671137 EDN: ULHGGK
57. Gu Z, Li X, Shi J, Wu Y, Zhang J, et al. The Development of Predictive Nomogram of Recurrence for Patients With Endometrioma After Cystectomy Who Were Younger Than 45 Years Old and Received Postoperative Therapy. Front Med (Lausanne). 2022;9:872481. https://doi.org/10.3389/fmed.2022.872481
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For citations:
Tskhay V.B., Grebennikova E.K., Skuratova J.N. The problem of recurrence of ovarian endometriomas. Medical Herald of the South of Russia. 2025;16(1):5-13. (In Russ.) https://doi.org/10.21886/2219-8075-2025-16-1-5-13
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