Risk factors for a marked decline in anti-Müllerian hormone after minimally invasive ovarian cystectomy

1. Introduction The incidence of ovarian cysts in Korea has risen notably over the past 5 years, with approximately 80% of affected individuals being premenopausal women.[] Benign ovarian cysts, including functional, endometriotic, and dermoid cysts, are prevalent in women of reproductive age. Symptoms associated with large ovarian cysts often include abdominal pain, urinary issues, and gastrointestinal discomfort due to pressure on adjacent structures.[,] Surgical treatment is typically indicated for cysts causing severe pain, exhibiting substantial size, or showing features suggestive of malignancy.[,] Premenopausal patients with benign ovarian cysts are preferably treated with ovarian-preserving surgery.[] Minimally invasive surgery is increasingly preferred due to its smaller incisions, faster recovery, shorter hospital stays, and reduced pain compared to laparotomy.[] Previous studies have shown a decline in ovarian reserve following ovarian cystectomy, attributed to factors such as decreased perfusion, loss of normal ovarian tissue, destruction of antral follicles, edema of normal tissue, and the previous presence of a cyst.[] Evaluating ovarian reserve in reproductive-aged women post-surgery is crucial, with various tests such as serum anti-müllerian hormone (AMH), antral follicle count, ovarian volume, ovarian stromal pulsatility index, ovarian stromal resistance index, luteinizing hormone, follicle-stimulating hormone, follicle-stimulating hormone/luteinizing hormone ratio, and inhibin B levels providing clinically important information.[,] Serum AMH level is commonly used for estimating ovarian function due to its minimal influence from the menstrual cycle or synthetic hormones.[,] This study aimed to identify factors influencing the decline in serum AMH levels after minimally invasive ovarian cystectomy in reproductive-aged women. 2. Materials and methods 2.1. Study design and participants This retrospective cohort study included premenopausal women who underwent ovarian cystectomy for benign cysts from January 1, 2018 to December 31, 2022 at Konkuk University Medical Center. The study was approved by the Institutional Review Board (No. KUMC 2023-10-001). We reviewed medical charts, including clinical characteristics, preoperative and postoperative serum AMH levels, operative records, and histopathological results. Inclusion criteria were women aged ≥ 18 years who provided informed consent to undergo minimally invasive ovarian cystectomy, had benign ovarian cysts with documented cyst dimensions on preoperative imaging, and had both preoperative and postoperative serum AMH levels available within the predefined time frames. Exclusion criteria were patients who underwent additional surgeries, such as myomectomy, or cases where electrocoagulation was the primary method for hemostasis instead of suturing. 2.2. Surgical procedure and data collection Three experienced gynecologists accredited by the Korean Society of Gynecologic Oncology performed the operations. Postoperative serum AMH levels were routinely tested approximately 3 to 4 months after surgery, as significant declines in AMH levels are typically observed within 3 months post-cystectomy.[] For patients included in this study, hemostasis was primarily achieved through continuous non-locking sutures, with minimal use of electrocoagulation. All patients received oxidized regenerated cellulose as a hemostatic agent. Adhesiolysis was classified based on the extent of anatomical abnormality; full adhesiolysis was performed if the posterior cul-de-sac was completely obstructed. No concomitant salpingectomy for hydrosalpinx was performed at the time of ovarian cystectomy in the study population. Operation time was recorded from the start to the end of anesthesia, and postoperative hemoglobin levels were measured the morning after surgery. 2.3. Statistical analysis Data analysis was performed using Statistical Package for the Social Sciences for Windows (version 21.0; SPSS Inc., Chicago). Categorical variables were indicated as numbers and percentages, and continuous variables as mean ± standard deviation. The t-test was used for continuous variables, and the chi-square test for categorical variables. Spearman correlation analysis was conducted to assess the relationship between serum AMH levels and clinical factors. Logistic regression analysis was used to estimate odds ratios (ORs) and 95% confidence intervals (CIs) to characterize the association between the decline in postoperative AMH and clinical factors. A P-value < .05 was considered statistically significant. 3. Results 3.1. Participant characteristics A total of 195 premenopausal women were included in this study (Table 1). The mean age of the patients was 32.4 years. Unilateral ovarian cysts were present in 139 (71.3%) patients, and bilateral ovarian cysts were present in 56 (28.7%) patients. The mean sum of the longest cyst diameter was 8.5 ± 4.3 cm by ultrasonographic measure. Endometriotic cysts were found in 115 (59.0%) patients, while 80 (41.0%) had non-endometriotic cysts. All patients underwent minimally invasive surgery, including robotic or laparoscopic ovarian cystectomy. Eighty (41.0%) patients required adhesiolysis during surgery, while 115 (59.0%) patients did not. Table 1 Clinical characteristics of the patients (N = 195). | Characteristics | Number (%) | |---|---| | Age (yrs) | 32.4 ± 7.5 | | BMI (kg/m2) | 22.3 ± 3.7 | | Gravidity | 0.2 ± 0.6 | | Sum of the longest diameter of the cysts (cm) | 8.5 ± 4.3 | | Location of cyst | | | Unilateral | 139 (71.3%) | | Bilateral | 56 (28.7%) | | Type of surgery | | | Laparoscopy | 68 (34.9) | | Robot | 127 (65.1) | | Histology of ovarian cyst | | | Endometriosis | 115 (59.0%) | | Non-endometriosis | 80 (41.0%) | | Adhesiolysis | | | Yes | 80 (41.0%) | | No | 115 (59.0%) | | Mean duration of surgery (min) | 127.6 ± 56.7 | | Mean decline of postoperative Hb level (g/dL) | 2.2 ± 1.0 | | Serum AMH level (ng/mL) | | | Preoperative | 3.4 ± 2.7 | | Postoperative | 2.4 ± 2.2 | | Rate of decline (%) | 20.8 ± 84.8 | 3.2. AMH levels and surgical factors Preoperative and postoperative mean AMH levels were 3.4 ± 2.7 ng/mL and 2.4 ± 2.2 ng/mL, respectively. The average rate of decline in serum AMH levels after surgery was 20.8%. Several surgical factors were associated with the decline in serum AMH levels (Table 2). Preoperative AMH levels were significantly lower in patients with endometriosis and in those who required adhesiolysis (P = .023 and P = .004, respectively). Postoperative AMH levels were significantly lower in patients with endometriosis (P < .0001), bilateral ovarian cysts (P < .0001), and those who underwent adhesiolysis during surgery (P < .0001). A marked decline of more than 50% in postoperative AMH levels was found in 55 (28.2%) patients. Table 2 Correlation analysis for the relationship between surgical factors and AMH level. | Category | Preoperative | Postoperative | Rate of decline | |||| |---|---|---|---|---|---|---|---| | Mean | P-value | Mean | P-value | Mean | P-value | || | Endometriosis, n | ||||||| | Yes | 115 | 3.0 ± 2.6 | .023 | 1.8 ± 1.8 | <.001 | 31.7 ± 16.4 | .193 | | No | 80 | 3.9 ± 2.8 | 3.2 ± 2.5 | 5.0 ± 118.8 | ||| | Location of cyst, n | ||||||| | Unilateral | 139 | 3.5 ± 2.8 | .193 | 2.7 ± 2.3 | <.001 | 10.6 ± 95.8 | .008 | | Bilateral | 56 | 3.0 ± 2.4 | 1.6 ± 1.5 | 46.0 ± 37.7 | ||| | Surgical approach, n | ||||||| | Laparoscopy | 68 | 3.1 ± 2.3 | .389 | 2.3 ± 2.0 | .661 | 24.3 ± 42.0 | .670 | | Robot | 127 | 3.5 ± 2.9 | 2.4 ± 2.4 | 18.9 ± 100.6 | ||| | Method of hemostasis, n | ||||||| | Coagulation | 87 | 3.3 ± 2.7 | .810 | 2.5 ± 2.3 | .485 | 8.9 ± 117.2 | .080 | | Suture | 108 | 3.4 ± 2.7 | 2.3 ± 2.1 | 30.3 ± 42.2 | ||| | Adhesiolysis, n | ||||||| | Yes | 80 | 2.7 ± 2.3 | .004 | 1.7 ± 1.8 | <.001 | 20.5 ± 125.6 | .972 | | No | 115 | 3.8 ± 2.9 | 2.8 ± 2.3 | 20.9 ± 35.9 | 3.3. Multivariable logistic regression analysis Univariable logistic regression analysis identified advanced age (≥30 years, OR, 2.1; 95% CI: 1.1–4.1; P = .035), endometriosis (OR, 5.3; 95% CI: 2.4–11.6; P < .0001), bilateral ovarian cysts (OR, 3.7; 95% CI: 1.9–7.2; P < .0001), adhesiolysis (OR, 3.0; 95% CI: 1.6–5.6; P = .001), and longer duration of surgery (≥2 hours, OR, 2.7; 95% CI: 1.4–5.1; P = .004) were associated with the marked AMH decline. Multivariable analysis confirmed that endometriosis (OR, 3.2; 95% CI: 1.3–7.9; P = .010) and bilateral ovarian cysts (OR, 2.4; 95% CI: 1.2–5.0; P = .020) were independent predictors of a postoperative decline of ≥50% in serum AMH level (Table 3). Table 3 Logistic regression analysis for AMH decline after surgery. | Category | AMH decline < 50% n = 140 (%) | AMH decline ≥ 50% n = 55 (%) | Univariable analysis | Multivariable analysis | || |---|---|---|---|---|---|---| | OR (95% CI) | P-value | OR (95% CI) | P-value | ||| | Age (yrs) | |||||| | ≥30 | 75 (53.6) | 39 (70.9) | 2.1 (1.1–4.1) | .035 | 1.4 (0.7–3.0) | .335 | | <30 | 65 (46.4) | 16 (29.1) | 1 | 1 | || | Endometriosis | |||||| | Yes | 69 (49.3) | 46 (83.6) | 5.3 (2.4–11.6) | <.0001 | 3.2 (1.3–7.9) | .010 | | No | 71 (50.7) | 9 (16.4) | 1 | 1 | || | Duration of surgery | |||||| | ≥2 h | 61 (43.6) | 37 (67.3) | 2.7 (1.4–5.1) | .004 | 1.7 (0.8–3.5) | .158 | | <2 h | 79 (56.4) | 18 (32.7) | 1 | 1 | || | Location of cyst | |||||| | Bilateral | 29 (20.7) | 27 (49.1) | 3.7 (1.9–7.2) | <.0001 | 2.4 (1.2–5.0) | .020 | | Unilateral | 111 (79.3) | 28 (50.9) | 1 | 1 | || | Surgical approach | |||||| | Robot | 91 (65.0) | 36 (65.5) | 1.0 (0.5–2.0) | 1.000 | || | Laparoscopy | 49 (35.0) | 19 (34.5) | 1 | ||| | Method of hemostasis | |||||| | Suture | 73 (52.1) | 35 (63.6) | 1.6 (0.8–3.1) | .154 | || | Cautery | 67 (47.9) | 20 (36.4) | 1 | ||| | Adhesiolysis | |||||| | Yes | 47 (33.6) | 33 (60.0) | 3.0 (1.6–5.6) | .001 | 1.4 (0.7–3.1) | .352 | | No | 93 (66.4) | 22 (20.0) | 1 | 1 | 3.4. Comparison between endometriosis and non-endometriosis groups Comparative analysis between the endometriosis and non-endometriosis groups revealed that the former group was older (P < .001) and had a higher prevalence of bilateral ovarian cysts (P = .001), adhesiolysis (P < .0001), and longer surgery duration (P = .002). Both preoperative and postoperative serum AMH levels were lower in the endometriosis group compared to the non-endometriosis group (P = .023 and P < .0001, respectively). The rate of decline in serum AMH levels was also significantly higher in the endometriosis group (P = .030) (Table 4). Table 4 Comparison of the clinical characteristics and serum AMH levels between the endometriosis and non-endometriosis groups. | Category | Endometriosis (n = 115) | Non-endometriosis (n = 80) | P-value | |---|---|---|---| | Age (yrs) | 34.1 ± 7.4 | 29.9 ± 6.9 | <.0001 | | BMI (kg/m2) | 22.1 ± 3.4 | 22.7 ± 4.1 | .259 | | Gravidity | 0.2 ± 0.5 | 0.2 ± 0.6 | .814 | | Sum of the largest diameter of the cysts (cm) | 8.3 ± 3.8 | 8.8 ± 4.9 | .458 | | Location of cyst, n (%) | ||| | Unilateral | 72 (62.6) | 67 (83.8) | .001 | | Bilateral | 43 (37.4) | 13 (16.2) | | | Adhesiolysis, n (%) | ||| | Yes | 70 (60.9) | 10 (12.5) | <.0001 | | No | 45 (39.1) | 70 (87.5) | | | Duration of surgery (min) | 137.8 ± 57.9 | 113.0 ± 51.8 | .002 | | Decline of postoperative Hb level (g/dL) | 2.2 ± 1.0 | 2.1 ± 0.9 | .349 | | Serum AMH level (ng/mL) | ||| | Preoperative | 3.0 ± 2.6 | 3.9 ± 2.8 | .023 | | Postoperative | 1.8 ± 1.8 | 3.2 ± 2.5 | <.0001 | | Rate of decline (%) | 31.7 ± 46.4 | 5.0 ± 118.8 | .030 | 4. Discussion A marked decline of more than 50% in AMH levels after minimally invasive ovarian cystectomy was associated with advanced age, endometriosis, prolonged surgical intervention, bilateral ovarian cysts, and adhesiolysis. Multivariable analysis highlighted that endometriosis and bilateral ovarian cysts were independent risk factors for a significant postoperative decline in AMH levels. Endometriosis, in particular, was associated with a greater decrease in AMH levels before and after surgery compared to those without endometriosis. AMH is a marker of ovarian reserve, produced by granulosa cells of preantral and small antral follicles in premenopausal women. Although AMH reflects small antral follicle count, it does not directly reflect the total follicular pool of the ovary.[,,] Serum AMH levels are remarkably stable throughout the menstrual cycle and are minimally affected by hormone use.[,] The secretion of AMH decreases with age, corresponding to a reduction in the number of growing follicles in the ovary. Numerous studies have reported a decline in postoperative serum AMH levels, suggesting mechanisms such as the removal of normal ovarian tissue, thermal damage from electrocoagulation, and decreased ovarian perfusion.[] Previous studies have shown postoperative serum AMH levels decrease by 38 to 73% compared to preoperative levels.[,,] In this study, the overall serum AMH level decreased by 20.8% after minimally invasive ovarian cystectomy, with a more significant decline observed in patients with endometriomas compared to those with non-endometriotic cysts. Endometriotic cysts consist of menstrual debris that induce inflammatory molecules, reactive oxygen species, transforming growth factor-β, and proteinases.[] Endometriosis can cause invagination of the ovarian cortex, reducing follicular density and affecting normal tissue.[,] Peritoneal macrophages secrete proteinases that cause damage to the ovarian tissue in patients with endometriosis.[] Despite this, spontaneous ovulation rates are not significantly affected by the presence of endometrial cysts.[,] However, the impact of surgery on adjacent healthy ovarian tissue may be greater, leading to decreased ovarian reserve. In this study, women with endometriosis had significantly lower preoperative serum AMH levels than those without endometriosis, indicating that endometriosis was already associated with a reduction in ovarian reserve before surgery. Furthermore, the postoperative AMH decline was greater in the endometriosis group, suggesting that endometriotic cystectomy may confer an additional iatrogenic loss of ovarian reserve in these patients. This finding is consistent with previous studies reporting that women with advanced ovarian endometrioma or severe endometriosis show lower preoperative AMH values compared with healthy controls.[] A prospective cohort study reported the effect of laparoscopic cystectomy on AMH in patients with endometriomas.[] The postoperative AMH levels showed long-term decrease in patients with large cysts (>7 cm), bilateral cysts, and stage IV endometriosis. Therefore, it is important to minimize damage to normal ovarian tissue during ovarian cystectomy in patients with endometriosis. Notably, the absolute risk of a marked decline was 40.0% in patients with endometriosis versus 11.2% without. Integrating these figures into preoperative counseling provides clinicians with a more concrete, clinically meaningful risk assessment. Therefore, for reproductive-aged women with endometriosis who wish to conceive, clinicians should discuss the risk of marked postoperative AMH decline prior to surgery, particularly in cases of bilateral, large, or recurrent cysts. For patients with active fertility plans, surgical timing should be carefully weighed against the urgency, and prompt referral for fertility preservation counseling should be considered. Currently, ovarian preservation using minimally invasive surgery is considered the standard surgical treatment for benign ovarian cysts. Ovarian cystectomy is performed using the stripping technique, in which atraumatic grasping forceps hold the cyst wall and the normal ovarian tissue and pull them in opposite directions. After removal of the cyst wall, hemostasis is performed using bipolar forceps. However, excision of the endometrioma is more difficult than excision of other benign cysts. Studies on pathologic specimens have consistently demonstrated distinct ovarian tissue together with ovarian cysts. During laparoscopic surgery, normal ovarian tissue was present in 65% and 32% of endometrioma and non-endometriotic cysts, respectively.[] The rate of ovarian tissue removal during excision of the endometrioma ranges from 54% to 100%.[,] These results suggest that excision of endometriotic cysts is more destructive to normal ovarian tissue than excision of non-endometriotic cysts. Therefore, surgeons should take care to preserve normal ovarian tissue during ovarian cystectomy in patients with endometriosis, including minimizing traction on the ovarian cortex during cyst stripping, limiting the extent of dissection near normal-appearing ovarian tissue, and relying on suturing rather than electrocoagulation for hemostasis, as performed in the present cohort. The independent association between bilateral cysts and marked AMH decline may reflect 2 interrelated mechanisms: a greater cumulative loss of normal ovarian tissue compared to unilateral surgery – where the contralateral ovary may partially compensate – and increased ischemic or inflammatory injury from more extensive surgical manipulation. Although distinguishing between these mechanisms was impossible in this retrospective study, the absolute risk of a marked decline was 48.2% for bilateral cysts versus 20.1% for unilateral cysts. This similar magnitude of absolute risk increase suggests that bilateral cysts and endometriosis contribute comparably to the clinical burden of ovarian reserve loss. Although adjusted for in the multivariable analysis, the unequal distribution between robotic and laparoscopic procedures limits definitive conclusions regarding their equivalence. Instead, our findings raise the possibility that overall operative duration and the associated carbon dioxide pneumoperitoneum may play a more critical role in ovarian tissue damage, although this hypothesis requires confirmation in future studies specifically designed to compare robotic and laparoscopic approaches. In our study, longer operative duration was associated with a greater reduction in postoperative AMH, which may partly reflect the cumulative effect of prolonged pneumoperitoneum and increased surgical manipulation on ovarian vascularization and follicular integrity. Experimental and clinical studies have shown that carbon dioxide pneumoperitoneum at higher pressures can decrease ovarian blood flow, increase oxidative stress, and transiently impair follicular development, supporting the hypothesis that operative time and pneumoperitoneum pressure are important determinants of postoperative ovarian function.[,] The limitations of this study are its retrospective design and relatively small study population. Also, information was lacking on factors that may affect ovarian function, including history of infertility, amenorrhea, and oral contraceptive use. Additionally, postoperative AMH was evaluated only once at 3 to 4 months, preventing assessment of long-term trajectories. Since the decline in ovarian reserve may either be sustained or partially recover over 6 to 12 months, longitudinal studies with repeated measurements for at least one year are warranted.[] However, the strength of our study is that it is the largest-scale study in Korea among patients who underwent ovarian cystectomy as a microinvasive surgery, and suturing was used as the hemostasis method. During ovarian cystectomy, hemostasis is commonly performed using bipolar electrosurgical devices, suturing, and hemostatic sealants. Suturing can offer the advantage of avoiding thermal spread and potential tissue damage. In addition, the same hemostatic method minimizes any misapprehension that could arise when different surgical methods are used. In conclusion, advanced age, endometriosis, bilateral ovarian cysts, prolonged surgical intervention, and adhesiolysis have been associated with decreased postoperative serum AMH after minimally invasive ovarian cystectomy. Among them, endometriosis seems to be a main cause of decreased ovarian reserve during surgery. Therefore, reproductive women with endometriosis should be counseled about the potential risks of decreased ovarian reserve after ovarian cystectomy, and surgeons should be more careful to preserve normal ovarian tissue during minimally invasive ovarian cystectomy in women with endometriosis. Author contributions Conceptualization: Kyeong A. So. Data curation: Eun Bi Jang, Kyeong A. So. Formal analysis: Kyeong A. So. Investigation: Eun Bi Jang, Yoon Sun Kook, A. Jin Lee. Methodology: Eun Bi Jang, Kyeong A. So. Project administration: Eun Bi Jang. Resources: Eun Bi Jang, Yoon Sun Kook. Supervision: Seung-Hyuk Shim, Sun Joo Lee, Tae Jin Kim. Validation: Seung-Hyuk Shim, Sun Joo Lee, Tae Jin Kim. Visualization: A. Jin Lee. Writing – original draft: Eun Bi Jang. Writing – review & editing: Kyeong A. 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