Impact of surgical treatment of ovarian endometrioma on fertility

ovarian endometrioma, laparoscopic surgery, fertility, ovarian reserve, recurrence Introducere. Endometriomul ovarian este o manifestare frec­ ven tă a endometriozei și o cauză importantă de infertilitate. În li te ratura de specialitate sunt descrise două metode chirurgicale majore pentru tratamentul acestora: excizia completă lapa­ ro sco pi că și tehnicile conservatoare. Aceste metode diferă sub stan țial în ceea ce privește eficacitatea și riscul de afectare a rezervei ovariene, iar impactul lor asupra fertilității necesită o evaluare critică. Scopul lucrării. Analiza comparativă a im pac tului metodelor chirurgicale majore asupra fertilității fe mei lor cu endometriom ovarian. Materiale și metodă. A fost realizată o revizuire sistematică a literaturii publicate în pe rioa da 2019­2024, utilizând bazele de date PubMed, MEDLINE, Scopus, Cochrane și Google Scholar. Căutarea a fost efectuată folosind termeni specifici: „endometriom ovarian” , „tratament chirurgical” , „rezultate asupra fertilității” și „rezervă ovariană” . Au fost selectate 38 de studii originale, 12 metaanalize și şapte articole de sinteză, iar parametrii analizați au inclus rata re­ curenței, nivelul hormonului antimüllerian și rata sarcinilor spontane. Testele statistice aplicate au fost testul Chi­pătrat și analiza hazardului proporțional Cox. Rezultate. Analiza com pa rativă a tehnicilor chirurgicale evidențiază că excizia com pletă laparoscopică determină o reducere semnificativă a recurenței, față de drenajul sau ablația peretelui chistului (rata recurenței: 12% versus 33%; p<0,01). Totuși, această procedură este asociată cu o scădere mai pronunțată a rezervei ovariene, măsurată prin nivelul AMH, care se reduce, în medie, cu 35% după excizie, față de o diminuare de aproximativ 12% după metodele conservatoare (p<0,05). Rata sarcinilor spontane după excizie este semnificativ mai mare, fiind în jur de 50%, comparativ cu 27% după drenaj sau ablație (p<0,05). Concluzii. Excizia completă laparoscopică a endometriomului ovarian oferă un control superior al bolii și o rată mai mare de sarcini spontane, comparativ cu tehnicile conservatoare. Cu toate acestea, bene­ fi ciul în ceea ce privește fertilitatea trebuie cântărit în raport cu riscul de afectare a rezervei ovariene. Alegerea metodei chi rur­ gi cale trebuie să fie individualizată, luând în considerare vârsta pa cientei, dimensiunea chistului și dorința reproductivă. Cuvinte-cheie: endometriom ovarian, chirurgie laparoscopică, fertilitate, rezervă ovariană, recurență

RezumatIrina Burdeniuc, Hristiana Caproș, Ion Bologan, Corina Darii, Ion Burdeniuc Department of Obstetrics, Gynecology and Human Reproduction, “Nicolae Testemițanu” State University of Medicine and Pharmacy, Chișinău, Republic of Moldova Corresponding author: Irina Burdeniuc E-mail: [email protected]

Endometriosis is a chronic, estrogen-dependent, in - flammatory gynecological disorder defined by the ecto - pic presence of endometrial glands and stroma outside the uterine cavity. The American College of Obstetri - cians and Gynecologists (ACOG) estimates its prevalence at 6-10% among women of reproductive age, with rates reaching 38% in infertile women and up to 87% in those Impactul chirurgiei endometriomului ovarian asupra fertilității Suggested citation for this article: Burdeniuc I, Caproș H, Bologan I, Darii C, Burdeniuc I. Impact of surgical treatment of ovarian endometrioma on fertility. Ginecologia.ro. 2025;49(3):26-34. Submission date: 26.09.2025 Acceptance date: 3.10.2025 27 ginecologia Year XIII • No. 49 (3/2025) with chronic pelvic pain (1). The condition substantially impairs the quality of life, presenting with dysmenor - rhea, dyspareunia, infertility and chronic pelvic pain. Ovarian endometriosis, manifesting as endometrio - mas, is among the most common and clinically significant forms of the disease. Endometriomas are reported in 17- 44% of patients with endometriosis(2). These cysts, typi- cally lined by ectopic endometrial tissue and filled with hemolyzed blood, display the characteristic dark brown appearance known as “chocolate cysts.” They may involve one or both ovaries and are associated with subfertility, obstetric complications and, rarely, malignant transfor- mation, particularly in recurrent or persistent lesions(3). Several pathogenetic mechanisms have been proposed for endometrioma formation, including retrograde im - plantation of endometrial cells on the ovarian surface, coelomic metaplasia and invasion of endometrial tissue into preexisting functional ovarian cysts(4). Nezhat et al. have described two histopathological subtypes: type I (primary) endometriomas – small, fibrotic cysts densely adherent to the ovarian cortex, and type II (secondary) endometriomas, which are larger, thin-walled, and more easily resectable (5). The goals of treatment include symptom relief, pre - vention of disease progression, fertility preservation and recurrence reduction. Surgical intervention, particularly laparoscopic cystectomy using the stripping technique, remains the standard of care for symptomatic or in - fertile patients, demonstrating superior outcomes in terms of pain control, recurrence rates and spontaneous conception compared with drainage or coagulation (6). However, bilateral cystectomy may compromise ovarian reserve, as reflected by postoperative declines in anti- Müllerian hormone (AMH) levels (7). To minimize ovarian damage, alternative or adjunc - tive techniques such as drainage with subsequent cyst wall ablation using CO 2 laser, plasma jet or radiofre - quency have been investigated. While these methods appear less detrimental to ovarian reserve, they carry higher recurrence rates, necessitating careful risk-ben - efit evaluation (8). The optimal management of ovarian endometrio - mas should be individualized, considering patient age, symptom severity, reproductive goals, lesion laterality and prior treatment response. Given its impact on repro- ductive prognosis and quality of life, a multidisciplinary, patient-centered approach is essential in addressing this complex condition.

of the study This study aims to evaluate surgical strategies for the management of ovarian endometriomas, with a focus on their effects on ovarian reserve and fertility outcomes. Specifically, it compares the efficacy and safety of laparo- scopic cystectomy with conservative approaches such as drainage and ablation, in order to determine an optimal therapeutic balance between disease control, recurrence prevention and preservation of reproductive potential. The study underscores the importance of individualized treatment planning, tailored to patient characteristics, clinical context and reproductive goals.

and method A systematic review of the literature published be - tween 2019 and 2024 was undertaken in accordance with established methodological standards. Compre - hensive searches were performed in PubMed, MEDLINE, Scopus, Cochrane Library and Google Scholar using com- binations of the following keywords: “ovarian endome - trioma”, “surgical treatment”, “fertility outcomes”, “ovar- ian reserve”, “AMH levels”, “laparoscopic cystectomy” and “recurrence rate”. Search strategies were adapted for each database, and filters were applied to include studies published in English or Romanian that reported clinically relevant outcomes. In total, 38 original studies met the eligibility cri - teria, comprising 24 prospective and 14 retrospective investigations, supplemented by 12 meta-analyses and seven narrative reviews. Studies were included if they involved patients with histopathologically confirmed ovarian endometriosis who underwent documented surgical treatment (laparoscopic cystectomy, drainage with subsequent laser ablation, or other conservative procedures), and if they reported pre- and postopera - tive anti-Müllerian hormone (AMH) levels, recurrence rates and/or spontaneous pregnancy outcomes. Exclu - sion criteria encompassed single case reports, studies without full-text access and those lacking relevant out - come measures. Primary endpoints included recurrence of endo - metriomas, changes in AMH as a surrogate marker of ovarian reserve and rates of spontaneous conception during postoperative follow-up. Statistical analyses were performed using SPSS and R software. The Chi-square (χ²) test was applied for categorical comparisons, while Cox proportional hazards models were employed to as - sess recurrence risk according to surgical modality. The statistical significance was set at p<0.05.

The analysis of the included studies revealed con - siderable heterogeneity with respect to the surgical techniques employed, the characteristics of the study populations and the outcome measures assessed. Among the 38 original studies selected, the majority compared the efficacy of laparoscopic cystectomy (stripping of the cyst wall) with more conservative approaches, such as drainage followed by ablation of the cyst wall using CO2 laser, argon plasma, or bipolar electrocoagulation. Impact on ovarian reserve Across a total of 31 studies published within the analyzed period, anti-Müllerian hormone (AMH) was employed as the primary biomarker for assessing post - operative ovarian reserve. This methodological choice is justified by the fact that AMH directly reflects granulosa cell function within ovarian follicles, and it is considered a reliable indicator of reproductive potential. 28 Year XIII • No. 49 (3/2025) gynecology The comparative analysis of the findings demonstrat- ed that, in patients undergoing laparoscopic cystectomy, a significant and consistent decline in AMH levels was observed, with the effect being more pronounced in cases of bilateral endometriomas or those exceeding 5 cm in diameter. According to the data summarized in Table 1, the average reduction in AMH during the first three postoperative months ranged between 38% and 58%, indicating a substantial short-term impact on ovarian reserve. By contrast, the application of conservative techniques (such as laser ablation, plasma energy or radiofrequency) Figure 1. Selection and inclusion of studies in the systematic review Table 1 Impact of surgical treatment of ovarian endometriomas on ovarian reserve (AMH) No. Study (author, year) Type of intervention Laterality N (patients) AMH preop. (ng/mL) AMH postop. (ng/mL) AMH decrease (%) 1 Muzii et al., 2020(9) Laparoscopic cystectomy Unilateral 72 3.5 2 -43% 2 Song et al., 2021(10) Cystectomy Bilateral 64 2.8 1.1 -61% 3 Li et al., 2020(12) Cystectomy Unilateral 90 2.9 1.9 -34% 4 Ferrero et al., 2022(13) Cystectomy + ablation Bilateral 77 2.6 1 -61% 5 Uncu et al., 2019(14) Cystectomy Unilateral 48 3.2 2.0 -37% 6 Nisolle et al., 2019(15) Plasma ablation Bilateral 51 2.7 2.3 -15% 38 studies (24 prospective, 14 retrospective) Exclusion criteria included individual case reports, studies lacking full-text availability and those not reporting relevant outcome measures. Eligibility. Studies with histopathologically confirmed ovarian endometriosis, documented surgical intervention, and reporting of pre- and postoperative AMH levels, recurrence rates and/or spontaneous pregnancy rates. Inclusion criteria: studies published between 2019 and 2024, available in English or Romanian. Databases: Scopus, Cochrane Library, and Google Scholar. Search terms: “ovarian endometrioma” , “surgical treatment” , “fertility outcomes” , “ovarian reserve” , “AMH levels” , “laparoscopic cystectomy” and “recurrence rate. ” 29 ginecologia Year XIII • No. 49 (3/2025) was associated with a significantly smaller decline in AMH, estimated at 10-20% within the same follow-up period. However, although these organ-sparing proce - dures better preserve ovarian reserve, they have been correlated with higher recurrence rates of endometrio - mas, thereby raising a clinical dilemma between fertility preservation and the risk of relapse. An important aspect highlighted by a subgroup of 14 studies concerns the role of patient age in ovarian func- tion recovery following surgery. It was observed that women under 30 years of age exhibited a significantly greater capacity to restore AMH levels at 6-12 months postoperatively compared with women over 35 years of age. This difference may be explained by the initially higher ovarian reserve, greater follicular plasticity, and enhanced regenerative capacity of ovarian tissue in younger patients(34). Recurrence rate Evidence derived from 29 clinical studies included in this analysis and summarized in Table 2 demonstrated that the recurrence rate of ovarian endometriomas fol - lowing laparoscopic cystectomy generally ranges from 10% to 20%, with variability primarily attributable to the duration of follow-up, which extended from 12 to 60 months. These findings reinforce the notion that, although cystectomy remains the gold standard in the surgical management of endometriomas, the procedure is not devoid of medium- and long-term recurrence risk. In contrast, drainage and ablation techniques (includ- ing CO 2 laser vaporization, plasma energy and radio - frequency) were associated with substantially higher recurrence rates, reaching 35-40% in certain series. This disparity can be explained by the fact that conserva - tive approaches, while conferring the advantage of im - proved ovarian reserve preservation, frequently leave behind residual viable endometriotic tissue within the cyst wall, thereby serving as a potential source for new lesion formation. Advanced statistical analysis using the Cox propor - tional hazards model further confirmed a significantly elevated relative risk of recurrence with conservative approaches compared to conventional cystectomy. Spe- cifically, a hazard ratio (HR) of 2.3 (95% confidence in - terval; 1.6-3.4; p<0.01) was identified, indicating that organ-sparing methods are associated with more than a twofold higher likelihood of lesion recurrence. The data presented in Figure 2 indicate marked differ- ences in endometrioma recurrence rates according to the surgical technique employed. The lowest recurrence was documented in patients undergoing cystectomy com - bined with in vitro fertilization (IVF), with a mean rate of approximately 9%, followed by simple cystectomy at around 13%. These outcomes suggest that complete excision of the endometrioma capsule, particularly when incorporated into assisted reproduction protocols, offers the most durable disease control. Conversely, the highest recurrence rates were ob - served after incomplete or partial procedures, such as simple drainage (mean recurrence: approximately 40%) and plasma ablation (28-30%). These findings support the concept that conservative techniques, although less detrimental to ovarian parenchyma, are associated with residual viable endometriotic tissue, thereby conferring a substantially increased risk of relapse. Overall, the comparative analysis underscores that minimally invasive or incomplete approaches (drain - age, ablation modalities) are consistently inferior to complete excision in terms of recurrence prevention, limiting their role as definitive therapeutic strategies. Nonetheless, such techniques may retain selective ap - plicability in young patients with diminished ovarian reserve or in those prioritizing preservation of healthy ovarian tissue, provided that the risk-benefit profile is carefully weighed. The comparative analysis of the studies included in this systematic review highlights a significant differ - ence in postoperative recurrence rates according to the Table 2 Recurrence rate of ovarian endometriomas after surgical treatment No. Author, year Intervention Laterality N Follow-up (months) Recurrence rate (%) 1 Muzii et al., 2020(9) Laparoscopic cystectomy Unilateral 72 36 14 2 Song et al., 2021(10) Cystectomy Bilateral 64 48 18 3 Li et al., 2020(12) Cystectomy Unilateral 90 30 12 4 Ferrero et al., 2022(13) Cystectomy + coagulation Bilateral 77 60 22 5 Nisolle et al., 2019(15) Plasma ablation Bilateral 51 18 28 6 Vercellini et al., 2019(18) Cystectomy + hormone therapy Unilateral 55 48 8 7 Wang et al., 2019(19) Radiofrequency ablation Bilateral 66 18 26 30 Year XIII • No. 49 (3/2025) gynecology laterality of endometriomas. As shown in Figure 3, the mean recurrence rate for unilateral lesions was approxi- mately 15.4%, whereas for bilateral endometriomas it reached 24%. This difference may be explained by several clini - cal and technical factors. Bilateral endometriomas are associated with more extensive ovarian involvement, which can complicate surgical management and increase the likelihood of residual disease. Furthermore, inter - ventions involving both ovaries require more cautious preservation of healthy parenchyma, thereby limiting the radicality of excision. In addition, bilateral disease may represent a more aggressive or advanced form of endometriosis, inherently associated with a higher risk of recurrence. These findings underscore the need for careful preop- erative assessment and an individualized surgical strat - egy, particularly in patients with bilateral disease, where the balance between surgical radicality and preservation of ovarian reserve must be judiciously considered. Figure 3. Mean recurrence rate stratified by surgical laterality Figure 2. Average recurrence rate according to the type of surgical intervention for ovarian endometriomas 31 ginecologia Year XIII • No. 49 (3/2025) Fertility outcomes A total of 21 studies, summarized in Table 3, evalu - ated spontaneous pregnancy rates following surgical treatment of endometriomas. The results suggest that patients treated with laparoscopic cystectomy achieved significantly higher spontaneous pregnancy rates, rang- ing from 35% to 50%, compared with those who under- went conservative techniques (ablation, drainage), where rates ranged from 20% to 30%. However, the data also reveal an important clinical nuance: in patients with low preoperative AMH levels or already compromised ovarian reserve, conservative procedures may represent a reasonable option. Although associated with higher recurrence rates, such approaches minimize additional loss of healthy ovarian tissue and may thus preserve, at least partially, short-term repro - ductive potential. In addition, nine studies included patients under - going assisted reproductive technology (IVF/ICSI) and assessed the impact of surgical treatment on controlled ovarian response. Findings indicated that untreated en- dometriomas may be associated with a reduced num - ber of oocytes retrieved, possibly due to mechanisms involving ovarian architectural distortion and chronic local inflammation. Nevertheless, surgical excision – particularly in bilateral cases – may exert an even more pronounced effect through inadvertent removal of primordial follicles and disruption of cortical vascu - larization. This phenomenon leads to a further decline in ovarian reserve, reflected in a diminished ovarian response to stimulation and, consequently, lower rates of mature oocyte retrieval. According to Figure 4, cystectomy alone is associated with a mean spontaneous pregnancy rate ranging from 39% to 46%, demonstrating greater effectiveness com - pared with conservative techniques. Ablation methods (laser, plasma, radiofrequency) show lower efficacy with respect to fertility, with reported rates between 28% and 31%. Combined approaches (cystectomy plus abla - tion) appear to yield the most favorable reproductive outcomes, with rates reaching up to 48.3%. The comparative analysis of the 20 included stud - ies revealed significant differences in postoperative spontaneous pregnancy rates according to the surgical technique employed for the management of ovarian en- dometriomas. The mean pregnancy rate among patients treated with ablation was 29.2%, representing the lowest of the approaches evaluated. By contrast, cystectomy was associated with a mean pregnancy rate of 41.2%, suggesting superior benefit in restoring fertility, albeit No. Study Treatment method Spontaneous pregnancy rate (%) 1 Mehdizadeh et al., 2022(22) Ablation 31.2 2 Yoshino et al., 2021(23) Cystectomy 45.6 3 Barri et al., 2020(24) Ablation 28 4 Pundir et al., 2023(25) Cystectomy + ablation 48.3 5 Muzii et al., 2022(9) Cystectomy 4 0.1 6 Huang et al., 2023(26) Ablation 29.5 7 Vercellini et al., 2020(18) Cystectomy + ablation 46.2 8 Tsolakidis et al., 2021(27) Cystectomy 43.3 9 Ghezzi et al., 2019(28) Ablation 27. 8 10 Ferrero et al., 2023(13) Cystectomy 41.5 11 Canis et al., 2022(29) Cystectomy 38.9 12 Nisolle et al., 2019(15) Cystectomy + ablation 47. 2 13 Audebert et al., 2019(30) Ablation 30.4 14 Song et al., 2021(10) Cystectomy 43.9 15 Ceccaroni et al., 2022(32) Cystectomy 40.7 Table 3 Surgical management of ovarian endometriomas and spontaneous fertility outcomes 32 Year XIII • No. 49 (3/2025) gynecology at the expense of a higher risk of healthy ovarian tissue loss. The highest pregnancy rate, 47.7%, was observed in the group managed with combined techniques (cys - tectomy plus ablation), indicating a potential optimal balance between therapeutic efficacy and preservation of ovarian function. These findings underscore the importance of a per - sonalized approach that accounts not only for disease severity and bilaterality but also for the patient’s re - productive goals. Combined surgical strategies appear to represent a promising alternative for optimizing reproductive outcomes; however, additional prospec - tive, randomized studies are required to confirm their superiority.

The findings presented in the reviewed studies high - light a major clinical dilemma in the management of ovarian endometriomas: the need to achieve effective disease control while simultaneously preserving ovarian function and maintaining fertility. Fertility preservation represents a fundamental ob - jective in all gynecological interventions, particularly among young women of reproductive age who desire a future pregnancy. The impact of surgical procedures on ovarian reserve is well documented, and the loss of ovar- ian function may be irreversible. Consequently, contem- porary therapeutic strategies emphasize the identifica - tion of effective solutions that allow optimal treatment of endometriomas, reduction of recurrence risk and, at the same time, preservation of reproductive potential. Oocyte or embryo cryopreservation constitutes the most reliable and well-documented fertility preserva - tion strategy for patients with ovarian endometriomas, particularly in bilateral cases or in women with low AMH levels. Studies have demonstrated that patients who underwent cryopreservation prior to surgery had reproductive outcomes comparable to women without endometriomas. International societies, such as ESHRE, recommend the integration of this method in women at high risk of diminished ovarian reserve (36). Intraoperative hemostasis plays a critical role in maintaining ovarian integrity. The use of bipolar elec - trocoagulation is associated with greater destruction of ovarian tissue compared with suturing techniques or laser application. Daniilidis et al. demonstrated that the use of hemostatic sutures leads to a significantly smaller postoperative decline in AMH levels, confirming the superiority of this approach in preserving ovarian function(11). Postoperative hormonal therapy, including GnRH analogs, combined oral contraceptives or progestins (e.g., dienogest), contributes to reducing endometrioma recurrence and stabilizing ovarian function. A meta- analysis showed that suppressive hormonal therapy ad- ministered for at least six months significantly reduces the risk of recurrence and allows the postponement of assisted reproductive technology (ART) interventions(37). For patients with persistent infertility or preexist - ing diminished ovarian reserve, an integrated approach – consisting of limited excision of the endometrioma followed by prompt in vitro fertilization (IVF) – may increase the chances of achieving pregnancy. Studies suggest that live birth rates are comparable between patients in whom the endometrioma was excised and those in whom it was left in situ , although the risk of reduced ovarian reserve following surgery remains a critical factor to consider (38). Recent studies indicate that the use of anti-adhesion agents in patients with endometriosis following surgical Figure 4. Mean rate of spontaneous pregnancies by treatment modality 33 ginecologia Year XIII • No. 49 (3/2025) intervention significantly decreases the risk of pelvic adhesion formation, a factor recognized for its nega - tive impact on fertility. By preventing adhesions, these agents help maintain ovarian and tubal mobility, thereby safeguarding the patient’s reproductive capacity and optimizing both spontaneous fertility and the success of assisted reproductive procedures (35).

Ovarian endometriomas represent a frequent and challenging manifestation of endometriosis, with major implications for reproductive health and the quality of life of women of reproductive age. Surgical treatment remains an essential component in the management of symptomatic or infertile patients; however, the choice of surgical technique requires a careful balance between therapeutic efficacy and preservation of ovarian reserve. Findings from this systematic review indicate that laparoscopic cystectomy is associated with lower recur - rence rates and higher spontaneous pregnancy rates compared with conservative approaches, but at the cost of a more pronounced negative impact on ovarian re - serve, as reflected by decreased AMH levels. Alternative

such as ablation or vaporization, while less det- rimental to ovarian function, demonstrate reduced ef - ficacy in preventing recurrence and achieving pregnancy. The analyzed data suggest that combined approaches, which integrate tissue-preserving techniques with the excision of pathological tissue, may provide superior reproductive outcomes and a favorable compromise be- tween radicality and conservation. Furthermore, the laterality of disease (unilateral versus bilateral) signifi - cantly influences both the recurrence risk and ovarian function loss, underscoring the importance of individu- alized preoperative assessment. Fertility preservation must remain a central objec - tive in all gynecological interventions performed in women of reproductive age. Contemporary strategies for safeguarding reproductive potential include several complementary approaches. First, oocyte and embryo cryopreservation represent an effective prophylac - tic measure, particularly for patients with bilateral endometriomas or low anti-Müllerian hormone levels. Second, fertility-sparing surgical techniques, such as partial excision combined with laser vaporization, can limit cortical ovarian damage while maintaining tissue integrity. In addition, the application of protective hemostatic strategies – such as microsurgical suturing – minimizes trauma and tissue destruction compared with electro - coagulation, thereby contributing to ovarian reserve preservation. Postoperative hormonal therapy, including GnRH analogs, combined oral contraceptives or pro - gestins, further reduces recurrence risk and stabilizes ovarian function. For patients with persistent infertility or compro - mised ovarian reserve, combining surgical management with assisted reproductive technologies represents an effective strategy, optimizing reproductive outcomes. Moreover, the use of anti-adhesion barriers prevents the formation of pelvic adhesions, thereby reducing fertility- impairing complications and indirectly contributing to reproductive preservation. By integrating these measures into an individual - ized, multidisciplinary and evidence-based approach, clinicians can ensure both optimal disease control and preservation of fertility in patients with ovarian endo - metriomas. The evidence highlights that a comprehen - sive strategy – combining surgery, preventive measures and assisted reproductive interventions – maximizes reproductive success while minimizing long-term risks. This requires an individualized evaluation of each pa - tient, taking into account the age, the hormonal status, endometrioma size and location, and reproductive inten- tions, to determine the optimal balance between disease control and fertility preservation. 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