Ovarian reserve and surgical hemostasis methods for benign ovarian tumors
Ibragimova U.D., Kozachenko I.F., Adamyan L.V.
The surgical strategy for benign ovarian tumors (BOTs) in women of reproductive age should focus on completely removing the pathological formation while minimizing the impact on healthy ovarian tissue to preserve the ovarian reserve. A key aspect of surgical treatment is the implementation of intraoperative hemostasis using various types of energy and hemostatic matrices.
Objective: To assess the state of ovarian reserve in reproductive-aged patients with BOT using different methods of surgical hemostasis.
Materials and methods: The study included 156 patients of reproductive age diagnosed with ovarian teratoma and/or cystadenoma who presented to the V.I. Kulakov NMRC for OG&P between 2022 and 2024. All the patients underwent surgical treatment with laparoscopic access. Two study groups were formed based on the method of surgical hemostasis: fibrin glue was used in group 1 (n=78), while bipolar coagulation was used in group 2 (n=78). Clinical and laboratory examinations were conducted for all patients, including the determination of anti-Müllerian hormone (AMH), estradiol, inhibin B, luteinizing hormone (LH), and follicle-stimulating hormone (FSH) levels in the blood serum on the 3rd-5th day of the menstrual cycle, as well as tumor marker levels (CA-125, CA 19-9, HE 4, CEA). Ultrasound evaluations of the pelvic organs were performed on the 5th–7th day of the menstrual cycle to assess ovarian volume, antral follicle count (AFC), and intraovarian blood flow before and after surgery.
Results: The average age of patients in group 1 was 30.0 (6.7) years, while in group 2 it was 31.0 (7.5) years. Histological examination revealed mature ovarian teratomas in 92/156 (59%) women, serous/mucinous ovarian cystadenomas in 64/156 (41%), and cystadenomas and teratomas in 6/156 (4%). Unilateral formations were observed in 130/156 (83%) patients, while bilateral cysts were present in 26/156 (17%) cases. The sizes of cystic formations ranged from 1.5 to 20.0 cm; the average tumor size in group 1 was 4.0 (3.2) cm, and in group 2 it was 5.0 (4.2) cm. The volume of the ovary with the tumor in group 1 averaged 46.6 (50.4) cm³, with an AFC of 5.0 (5.2) and a resistance index (RI) of 0.9 (0.2). In group 2, the volume of the ovary with the tumor was 45.4 (52.9) cm³, with an AFC of 4.0 (2.6) and an RI of 0.9 (0.1). In group 1, AMH before surgery averaged 2.2 (1.5) ng/ml, while in group 2 it was 2.0 (1.6) ng/ml. After surgery, the volume of the ovary in group 1 averaged 6.9 (1.3) cm³, with an AFC of 6.0 (3.0) and an RI of 0.6 (0.2); in group 2, the ovarian volume was 5.0 (1.3) cm³, with an AFC of 2.0 (2.3) and an RI of 0.9 (1.0). In group 1, AMH after surgical treatment averaged
1.7 (1.9) ng/ml, while in group 2 it was 1.2 (1.0) ng/ml.
Statistically significant differences between the groups were noted in the following parameters: AMH (p=0.017), inhibin B (p=0.008), FSH (p<0.001), ovarian volume (p=0.001), AFC (p<0.001), and RI (p<0.001).
Conclusion: In the surgical treatment of BOT, a critical issue is the maximum preservation of healthy ovarian tissue and reproductive potential of women. Assessing the ovarian reserve before and after surgical treatment allows for the identification of risk factors for its reduction and the selection of the optimal surgical hemostasis method that minimizes trauma to healthy ovarian tissue.
Authors’ contributions: Adamyan L.V., Kozachenko I.F. – conception and design of the study; Kozachenko I.F.,
Ibragimova U.D. – collection and processing of material; Ibragimova U.D., Kozachenko I.F. – statistical analysis, drafting of the manuscript; Adamyan L.V. – editing of the manuscript.
Conflicts of interest: The authors have no conflicts of interest to declare.
Funding: There was no funding for this study.
Ethical Approval: The study was reviewed and approved by the Research Ethics Committee of the V.I. Kulakov NMRC for OG&P (Ref. 10.11.2022).
Patient Consent for Publication: All patients provided informed consent for the publication of their data.
Authors' Data Sharing Statement: The data supporting the findings of this study are available upon request from the corresponding author after approval from the principal investigator.
For citation: Ibragimova U.D., Kozachenko I.F., Adamyan L.V. Ovarian reserve and
surgical hemostasis methods for benign ovarian tumors.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2025; (8): 150-158 (in Russian)
https://dx.doi.org/10.18565/aig.2025.175
Keywords
ovarian cystic lesions
mature ovarian teratomas
ovarian cystadenomas
reproductive age
ovarian reserve
anti-Müllerian hormone
number of antral follicles
surgical treatment
surgical methods of hemostasis
bipolar coagulation
fibrin glue
References
- Su Y.Y., Lin Y.S., Yang L.Y., Pan Y.B., Huang Y.T., Weng C.H. et al. Use of human fibrin glue (Tisseel) versus suture during transvaginal natural orifice ovarian cystectomy of benign and non-endometriotic ovarian tumor: a retrospective comparative study. BMC Surg. 2021; 21(1): 49. https://dx.doi.org/10.1186/s12893-021-01061-1
- Baracat C.M.F., Abdalla-Ribeiro H.S.A., Araujo R.S.D.C., Bernando W.M., Ribeiro P.A. The impact on ovarian reserve of different hemostasis methods in laparoscopic cystectomy: a systematic review and meta-analysis. Rev. Bras. Ginecol. Obstet. 2019; 41(6): 400-8. https://dx.doi.org/10.1055/s-0039-1692697
- Rocha R.M., Barcelos I.D.E.S. Practical recommendations for the management of benign adnexal masses. Rev. Bras. Ginecol. Obstet. 2020; 42(9): 569-76. https://dx.doi.org/10.1055/s-0040-1714049
- Матейкович Е.А., Шевлюкова Т.П., Чернова А.Л. Доброкачественные опухоли и опухолеподобные поражения яичников: структура, методы диагностики, тактика оказания медицинской помощи. Медицинская наука и образование Урала. 2021; 22(1(105)): 100-4. [Mateykovich E.A., Shevlyukova T.P., Chernova A.L. Benign tumors and tumor-like lesions of the ovaries: structure, diagnostic methods, tactics of medical care. Medical Science and Education of Ural. 2021; 22(1(105)): 100-4 (in Russian)]. https://dx.doi.org/10.36361/1814-8999-2021-22-1-100-104
- Соломатина А.А., Михалёва Л.М., Тюменцева М.Ю., Братчикова О.В., Хамзин И.З., Тумасян Е.А., Гашимова А.И., Исмайилова П.Д. Морфофункциональное состояние эндометрия у пациенток до и после органосохраняющих операций по поводу доброкачественных опухолей яичников. Вопросы гинекологии, акушерства и перинатологии. 2022; 21(3): 45-52. [Solomatina A.A., Mikhaleva L.M.,
- Tyumentseva M.Yu., Bratchikova O.V., Khamzin I.Z., Tumasyan E.A., Gashimova A.I., Ismayilova P.D. Morphological and functional features of the endometrium in patients before and after ovary-sparing surgery for benign ovarian tumors. Gynecology, Obstetrics and Perinatology. 2022; 21(3): 45-52 (in Russian)]. https://dx.doi.org/10.20953/1726-1678-2022-3-45-52
- Волченок Д. А., Тихоновская О. А., Петров И. А., Логвинов С. В., Мунгалова А. Д. Состояние овариального резерва у пациенток с функциональными кистами яичников. Journal of Siberian Medical Sciences. 2019; (1): 18-27. [Volchenok D.A., Tikhonovskaya O.A., Petrov I.A., Logvinov S.V., Mungalova A.D. The state of ovarian reserve in patients with functional ovarian cysts. Journal of Siberian Medical Sciences. 2019; (1): 18-27 (in Russian)]. https://dx.doi.org/10.31549/2542-1174-2019-1-18-27
- Matalliotakis M., Matalliotaki C., Zervou M. I., Krithinakis K., Goulielmos G. N., Kalogiannidis I. et al. Retrospective evaluation of pathological results among women with ovarian endometriomas versus teratomas. Mol. Clin. Oncol. 2019; 10(6): 592-6. https://dx.doi.org/10.3892/mco.2019.1844
- Мелкозерова О.А., Клепиков Ю.В., Окулова Е.О. Герминогенные опухоли яичников у детей и подростков: молекулярно-биологические аспекты и проблемы хирургической тактики с позиции сохранения фертильности. Лечение и профилактика. 2021; 11(2): 62-70. [Melkozerova O.A., Klepikov Yu.V., Okulova E.O. Herminogenous ovarian tumors in children and adolescents: molecular-biological aspects and problems of surgical tactics from the position of preserving fertility. Treatment and Prevention. 2021; 11(2): 62-70 (in Russian)].
- Heskett M.B., Sanborn J.Z., Boniface C., Goode B., Chapman J., Garg K. et al. Multiregion exome sequencing of ovarian immature teratomas reveals 2N near-diploid genomes, paucity of somatic mutations, and extensive allelic imbalances shared across mature, immature, and disseminated components. Mod. Pathol. 2020; 33(6): 1193-206. https://dx.doi.org/10.1038/s41379-019-0446-y
- Шевякова Е.В., Байрамкулова Л.М., Шахназарян Н.Г. Анализ лечения зрелых тератом яичника. В кн.: Актуальные проблемы науки и техники: сборник научных статей по материалам II Международной научно-практической конференции, Уфа, 22 мая 2020 г. Уфа: Вестник науки; 2020: 362-7. [Shevyakova E.V., Bayramkulova L.M., Shahnazaryan N.G. Analysis of treatment of mature ovarian teratomas. In: Current problems of science and technology: collection of scientific articles based on the materials of the II International scientific and practical conference, Ufa, May 22, 2020. Ufa: Bulletin of Science; 2020: 362-7 (in Russian)].
- Abramova S., Simfukwe K., Gladkova O., Grachev D., Iseev D. Modern aspects of etiology, mechanisms, pathogenesis and diagnostics of ovarian formations. Bulletin of Science and Practice. 2019; 5(5): 38-45. [Абрамова С.В., Симфукве К., Гладкова О.Н., Грачев Д.С., Исеев Д.Б. Современные аспекты этиологии, механизмов, патогенеза и диагностики образований яичников. Бюллетень науки и практики. 2019; 5(5): 38-45. (in English)]. https://dx.doi.org/10.33619/2414-2948/42/05
- Аradağ C., Demircan S., Turgut A., Çalışkan E. Effects of laparoscopic cystectomy on ovarian reserve in patients with endometrioma and dermoid cyst. Turk. J. Obstet. Gynecol. 2020; 17(1): 15-20. https://dx.doi.org/10.4274/tjod.galenos.2020.37605
- Limaiem F., Lekkala M.R., Mlika M. Ovarian cystadenoma. [Updated 2022 Oct 24]. In: Stat Pearls [Internet]. Treasure Island (FL): Stat Pearls Publishing; 2022 Jan.
- Филиппова Е.С., Козаченко И.Ф., Адамян Л.В., Дементьева В.О. Влияние хирургического лечения эндометриоидных кист яичников на состояние овариального резерва у женщин репродуктивного возраста. Проблемы репродукции. 2018; 24(4): 71-80. [Filippova E.S., Kozachenko I.F., Adamyan L.V., Dementyeva V.O. Influence of surgical treatment of ovarian endometrioid cysts on ovarian reserve in women of reproductive age. Russian Journal of Human Reproduction. 2018; 24(4): 71-80 (in Russian)]. https://dx.doi.org/10.17116/repro20182404171
- Салимова Д.К., Данусевич И.Н., Наделяева Я.Г., Лазарева Л.М., Аталян А.В., Новикова Е.А., Шолохов Л.Ф., Рашидова М.А., Сутурина Л.В. Клинико-лабораторные показатели сниженного овариального резерва у женщин репродуктивного возраста: кросс-секционное исследование. Экология человека. 2022; 29(8): 587-97. [Salimova M.D., Danusevich I.N., Nadelyaeva Y.G., Lazareva L.M., Atalyan A.V., Novikova E.A., Sholokhov L.F., Rashidova M.A., Suturina L.V. Clinical manifestations of decreased ovarian reserve in premenopausal women: a cross-sectional study. Human Ecology. 2022; 29(8): 587-97 (in Russian)]. https://dx.doi.org/10.17816/humeco106718
- Lim H., Park S.J., Paik H., Mun J., Lee E.J., Lee S. et al. Preservation of the ovarian reserve and hemostasis during laparoscopic ovarian cystectomy by a hemostatic agent versus suturing for patients with ovarian endometriosis: study protocol for randomized controlled, non-inferiority trial (PRAHA-2 trial). Trials. 2021; 22(1): 473. https://dx.doi.org/10.1186/s13063-021-05431-1
- Нажмутдинова Д.К., Абдуллаева Л.М., Клычев С.И., Сапаров А.Б., Ашурова У.А. Влияние на овариальный резерв лапароскопической цистэктомии. Журнал теоретической и клинической медицины. 2020; 3: 159-62. [Nazhmutdinova D.K., Abdullaeva L.M., Klychev S.I., Saparov A.B., Ashurova U.A. Effect of ovarian cystectomy on ovarian reserve. Journal of Theoretical and Clinical Medicine. 2020; (3): 159-62 (in Russian)].
- Goczyńska P., Lasocka J., Lachert E. Fibrin glues – the current state of knowledge. Journal of Transfusion Medicine. 2021; 14(4): 214-24. https://dx.doi.org/10.5603/JTM.2021.0012
- Kostrzewa M., Wilczyński J.R., Głowacka E., Żyła M., Szyłło K., Stachowiak G. One-year follow-up of ovarian reserve by three methods in women after laparoscopic cystectomy for endometrioma and benign ovarian cysts. Int. J. Gynaecol. Obstet. 2019; 146(3): 350-6. https://dx.doi.org/10.1002/ijgo.12884
- Адамян Л.В., Мынбаев О.А. Оценка эффективности применения фибринового клея при гинекологических реконструктивно-пластических операциях. В кн.: Кулаков В.И., Адамян Л.В., ред. Эндоскопия в диагностике и лечении патологии матки: Mеждународный конгресс с курсом эндоскопии, Москва, 9-13 июня 1997. М.: Гарант; 1997. Т. 1: 48-56. [Adamyan L.V., Mynbaev O.A. Evaluation of the effectiveness of the use of fibrin glue in gynecological reconstructive and plastic surgeries. In: Kulakov V.I., Adamyan L.V., eds. Endoscopy in the diagnosis and treatment of uterine pathology: International congress with a course of endoscopy, Moscow, June 9-13, 1997. Moscow: Garant; 1997. Vol. 1: 48-56 (in Russian)].
- Chung J.P.W., Law T.S.M., Mak J.S.M., Sahota D.S., Li T.C. Ovarian reserve and recurrence 1 year post-operatively after using haemostatic sealant and bipolar diathermy for haemostasis during laparoscopic ovarian cystectomy. Reprod. Biomed. Online. 2021; 43(2): 310-8. https://dx.doi.org/10.1016/j.rbmo.2021.05.003
- Соломатина А.А., Хамзин И.З., Тюменцева М.Ю., Чабиева Л.Б., Тумасян Е.А., Дулаева А.О. Органосберегающие операции у пациенток с доброкачественными образованиями яичников в аспекте сохранения репродуктивного потенциала. Лечебное дело. 2019; 3: 34-41. [Solomatina A.A., Khamzin I.Z., Tyumentseva M.Yu., Chabieva L.B., Tumasyan E.A., Dulaeva A.O. Organ-preserving surgery in patients with benign ovarian masses in terms of maintaining reproductive potential. Lechebnoe Delo. 2019; 3: 34-41 (in Russian)]. https://dx.doi.org/10.24411/2071-5315-2019-12138
- Пивазян Л.Г., Унанян А.Л., Пойманова О.Ф., Бондаренко Е.Н., Ищенко А.И. Эндометриома: овариальный резерв и тактика ведения. Проблемы репродукции. 2021; 27(5): 77-83. [Pivazyan L.G., Unanyan A.L., Poymanova O.F., Bondarenko E.N., Ishchenko A.I. Endometrioma: ovarian reserve and management. Russian Journal of Human Reproduction. 2021; 27(5): 77-83 (in Russian)]. https://dx.doi.org/10.17116/repro20212705177
- Nowak-Psiorz I., Ciećwież S., Brodowska A., Starczewski A. Treatment of ovarian endometrial cysts in the context of recurrence and fertility. Adv. Clin. Exp. Med. 2019; 28(3): 407-13. https://dx.doi.org/10.17219/acem/90767
- Венцковский Б.М., Жегулович В.Г., Жегулович Ю.В. Овариальный резерв при хирургии яичника. Гемостаз путем временной компрессии как альтернатива воздействия физических энергий и химических средств на яичник. Репродуктивное здоровье. Восточная Европа. 2019; 9(2): 120-6. [Ventskovsky B.M., Zhegulovich V.G., Zhegulovich Yu.V. Ovarian reserve in ovarian surgery. Hemostasis by temporary compression as an alternative to the effects of physical energies and chemicals on the ovary. Reproductive Health. Eastern Europe. 2019; 9(2): 120-6 (in Russian)].
- Кузьмина Н.С., Беженарь В.Ф., Калугина А.С. Опыт интраоперационного использования гемостатических матриц для сохранения овариального резерва у больных с эндометриомами. Проблемы репродукции. 2018; 24(2): 54-62. [Kuzmina N.S., Bezhenar’ V.F., Kalugina A.S. Experience in intraoperative use of hemostatic matrices to preserve the ovarian reserve in patients with endometriomas. Russian Journal of Human Reproduction. 2018; 24(2): 54-62 (in Russian)]. https://dx.doi.org/10.17116/repro201824254-62
Received 27.06.2025
Accepted 29.07.2025
About the Authors
Ummusalimat D. Ibragimova, PhD student, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology,Ministry of Health of Russia, 117997, Russia, Moscow, Ac. Oparin str., 4, amintaeva_umm@mail.ru, https://orcid.org/0009-0008-6984-7193
Irena F. Kozachenko, Dr. Med. Sci., Leading Researcher, obstetrician-gynecologist, Gynecological Department, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, 117997, Russia, Moscow, Ac. Oparin str., 4, irenakozachenko@rambler.ru,
https://orcid.org/0000-0003-1822-9164
Leila V. Adamyan, Academician of the Russian Academy of Sciences, Dr. Med. Sci., Professor, Deputy Director for Research, Head of the Department of Operative Gynecology, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia,
117997, Russia, Moscow, Ac. Oparin str., 4; Chief Specialist in Gynecology of the Ministry of Health of Russia; Head of the Department of Reproductive Medicine and
Surgery of the Faculty of Postgraduate Education, Russian University of Medicine, 127473, Russia, Moscow, Delegatskaya str., 20-1, adamyanleila@gmail.com,
https://orcid.org/0000-0002-3253-4512
Corresponding author: Ummusalimat D. Ibragimova, amintaeva_umm@mail.ru
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