Abstract
Background
Ovarian endometrioma (OMA) is the most prevalent form of endometriosis. Conservative surgical management of the condition is associated with a relatively high recurrence rate, the degree of which is potentially linked to disease severity. Recently, the American Association of Gynecologic Laparoscopists (AAGL) staging system was developed to reflect the severity of endometriosis and the surgical complexity. However, its predictive value for recurrence following conservative surgery in OMA patients remains unestablished.
Methods
To evaluate the predictive value of the AAGL staging system for recurrence following conservative surgery in OMA patients. A retrospective cohort study was conducted at Fuzhou University Affiliated Provincial Hospital and included patients who were diagnosed with OMA and underwent conservative surgery (ovarian cystectomy) between January 1, 2018, and December 31, 2022. All patients were assessed with the AAGL staging system and the revised American Society for Reproductive Medicine (r-ASRM) staging system according to the intraoperative findings. The primary outcome was the postoperative recurrence rate. Secondary outcomes included the consistency between the AAGL and r-ASRM systems in assessing patient condition and the correlation between the AAGL stage and surgical complexity as defined by the endometriosis surgery complexity score. Maximally selected rank statistics were used to determine the optimal AAGL score threshold and assess the correlation between the AAGL score and recurrence risk. Landmark analysis was used to assess the predictive value of the AAGL staging system for recurrence following conservative surgical treatment for OMA. Kappa statistics were used to analyse the consistency between the AAGL and r-ASRM staging systems. Kendall’s coefficient of concordance was used to assess the relationships between the staging systems and the surgical complexity.
Results
A total of 299 patients with OMA were included in the study. A total of 49 patients (16.4%) experienced postoperative recurrence, whereas 250 patients (83.6%) did not. The median postoperative follow-up duration was 39.6 months. The cumulative recurrence rates at 12, 24, 36, 48, and 60 months post-surgery were 2.4%, 7.0%, 13.1%, 23.3%, and 29.6%, respectively. Patients with an AAGL score > 16 had a significantly greater risk of recurrence following conservative surgery than those with an AAGL score ≤ 16 (P = 0.022). At 36 months post-conservative surgery and beyond, patients with an AAGL score > 16 presented a significantly higher recurrence rate than did those with a score ≤ 16 (P = 0.043). A comparison of the AAGL and r-ASRM systems in all patients revealed poor agreement between the two in terms of disease stage (weighted κ = 0.243). Furthermore, the AAGL staging system demonstrated stronger concordance with the surgical complexity scale than the r-ASRM system did (Kendall W coefficient = 0.613, P = 0.005; Kendall W coefficient = 0.552, P = 0.106, respectively).
Conclusions
The cumulative recurrence rate following conservative surgery for OMA patients progressively increased over time. The AAGL staging system was useful for predicting recurrence in OMA patients following conservative surgery, particularly starting at 36 months post-surgery. The AAGL staging system offers an improved assessment of surgical complexity in OMA patients.
Keywords: Ovarian endometrioma, AAGL staging system, Ovarian cystectomy, Recurrence, Risk factors
Introduction
Endometriosis is a chronic, oestrogen-dependent condition characterized by the presence and growth of endometrial tissue (glands and stroma) outside the uterine cavity [1]. The clinical manifestations primarily include chronic pelvic pain, dysmenorrhea, and dyspareunia, and this condition is strongly associated with increased infertility risk, significantly impacting patients’ quality of life and overall well-being [2]. Globally, endometriosis affects approximately 5–10% of women of reproductive age [3], with an estimated total of 176 million affected individuals [4].
Ovarian endometrioma (OMA) represents the most common subtype of endometriosis, accounting for approximately 17–44% of endometriosis cases [4, 5]. Current primary treatments for OMA involve pharmacological and surgical interventions [6]. Conservative surgery, typically referring to laparoscopic ovarian cystectomy, is indicated when an endometrioma of at least 3 cm in diameter is detected via ultrasonography in patients presenting with pain, infertility, or both [7–9]. However, conservative OMA surgery is associated with high recurrence rates, averaging 20% and 50% at 2 and 5 years, respectively. Recurrence rates are even higher in younger patients, those with more severe disease [10, 11], and those with incomplete lesion excision, frequently necessitating secondary surgery. Repeated OMA excisions can lead to diminished ovarian reserve, potentially even premature ovarian failure [12, 13]. Furthermore, the likelihood of postoperative pelvic adhesions is significantly increased [14].
Therefore, an accurate and efficient staging system is crucial for assessing the severity of disease and guiding conservative surgical treatment strategies for OMA patients following conservative surgery. The existing staging systems for endometriosis are the revised American Society for Reproductive Medicine (r-ASRM) classification [15] and the American Association of Gynecologic Laparoscopists (AAGL) staging system [16]. The r-ASRM system is widely utilized in clinical practice because of its simplicity and ease of application. However, it does not incorporate scoring information related to deep infiltrating endometriosis (DIE) and has a limited ability to predict fertility outcomes [3, 17, 18]. In 2021, the AAGL proposed an endometriosis staging system, which is consistent with the r-ASRM staging system in comprehensively describing the severity of the disease, while also better reflecting the complexity of surgery and demonstrating stronger reliability [16, 19].
However, no previous studies have used AAGL staging to predict postoperative recurrence in endometriosis patients. Therefore, the aim of this study was to explore the predictive value of the AAGL staging system for postoperative recurrence after conservative surgery in OMA patients while analysing the correlation between this staging system and the complexity of surgery to provide a reference basis for the clinical treatment of OMA patients.
Materials and methods
Study design and participants
This retrospective cohort study included patients hospitalized in the Department of Gynecology at Fuzhou University Affiliated Provincial Hospital who underwent conservative surgery (ovarian cystectomy) between January 1, 2018, and December 31, 2022. All patients provided verbal informed consent, and the study was approved by the Ethics Committee of Fuzhou University Affiliated Provincial Hospital (K2024-12–060).
We included patients aged 18–45 years who underwent laparoscopic OMA cystectomy during hospitalization and who had postoperative histopathological confirmation of OMA. The exclusion criteria were as follows: (1) concomitant gynaecological, colorectal, and/or urinary tract malignancies or infections; (2) secondary surgery for OMA; (3) incomplete medical or surgical records; (4) loss to follow-up; and (5) contraindications to gonadotropin-releasing hormone agonists (GnRH-a), progestins, or oral contraceptives.
All patients underwent laparoscopic ovarian cystectomy. All surgical procedures were performed by experienced physicians holding the position of associate chief physician or higher, and the postoperative medication treatment plan was based on the surgeon’s advice and the patient’s preferences. Clinical data included the patient’s age at surgery, body mass index (BMI), symptoms, history of dysmenorrhea, pregnancy history, history of pelvic surgery, presence of concurrent adenomyosis or uterine fibroids, and preoperative serum carbohydrate antigen 125 (CA125) levels. Surgical duration, intraoperative blood loss, maximum ovarian cyst diameter, unilateral or bilateral cysts, and the presence of DIE, defined as lesions that infiltrate more than 5 mm beneath the peritoneal surface or invade the muscularis propria of hollow viscera [3], were collected from individual surgical records. AAGL scoring and staging and r-ASRM scoring and staging were performed on the basis of the intraoperative findings. Patient postoperative symptom improvement, postoperative medication usage, pregnancy outcomes, and disease recurrence (including time to recurrence) were assessed via a standardized questionnaire.
Assessment of endometriosis recurrence
We defined endometriosis recurrence as the presence of a round, thick-walled cyst on transvaginal ultrasound, with a minimum diameter of 20 mm, containing homogeneous hypoechoic fluid with scattered internal echoes and no papillary projections. This also applied to patients with multiple ovarian endometriomas even if each had a diameter less than 20 mm as long as the combined diameter was greater than 20 mm [20–24].
Outcome measures
The primary outcome was the postoperative recurrence rate. The secondary outcomes included the consistency between the AAGL and r-ASRM staging systems in assessing the patients’ conditions, the correlations between the AAGL stage and surgical complexity as defined by the endometriosis surgery complexity score, and the pregnancy outcomes of the patients following conservative surgery for OMA. Clinical pregnancy was defined as a pregnancy in which the presence of a gestational sac was documented on first-trimester ultrasound or what resulted in a birth [25, 26]. The pregnancy rate was calculated only in with respect to patients who desired pregnancy following conservative surgery.
Statistical analyses
Normally distributed data are presented as the mean and standard deviation (SD), whereas data that did not conform to a normal distribution are presented as the median and interquartile range. Categorical variables are expressed as frequencies and percentages (%). Restricted cubic splines (RCS) analysis was conducted to evaluate the nonlinearity of the relationship between the AAGL score and the postoperative recurrence risk in patients with OMA. Kaplan-Meier analysis was performed to construct recurrence curves. Maximally selected rank statistics were used to determine the optimal cutoff value of the AAGL score for recurrence and to analyse the association between the AAGL score and recurrence risk.
Univariable Cox regression models were initially employed to identify potential risk factors for postoperative recurrence in patients with OMA. Variables that yielded a P value < 0.2 in the univariable analysis were then evaluated using the Akaike Information Criterion (AIC) to optimize model variable selection. Variables that contributed to a lower AIC value, indicating better model fit while penalizing overfitting, were subsequently included in the multivariable Cox regression models for further adjustment and to identify independent risk factors, and hazard ratios (HRs) with 95% confidence intervals (CIs) were calculated for each variable. Landmark analysis was used to evaluate the predictive value of the AAGL staging system for recurrence rates after conservative surgery for OMA. The kappa statistic was used to assess the agreement between the AAGL and revised r-ASRM staging systems. Kendall’s coefficient of concordance was calculated to examine the correlations between the two staging systems and surgical complexity. All the statistical analyses were performed using SPSS, version 24.0 (IBM, Armonk, NY, USA) and R, version 4.3.0. A P value of < 0.05 was considered to indicate statistical significance.
Results
A total of 299 women with OMA who underwent conservative surgery were eligible for inclusion. In total, 49 (16.4%) had a recurrence of ovarian cysts and 250 (83.6%) women did not recur (Fig. 1). The time to postoperative recurrence ranged from 3 to 65 months, with a median time of 27 (18.0–41.0) months.
Fig. 1.
Flow diagram showing patient inclusion in the study. OMA, ovarian endometrioma; GnRH-a, gonadotropin-releasing hormone agonist
The baseline characteristics of the study cohort are shown in Table 1. Among the 299 patients with OMA, 54.5% (n = 163) had dysmenorrhea before surgery. The average surgical duration was approximately 91 ± 41 min, and the volume of intraoperative blood loss was approximately 64 ± 77 mL. AAGL staging and r-ASRM staging were performed separately according to the intraoperative conditions. There were 31 patients (10.4%), 86 patients (28.8%), 79 patients (26.4%), and 103 patients (34.4%) with AAGL stages Ⅰ, Ⅱ, Ⅲ, and Ⅳ, respectively. There were 133 patients (44.5%) and 166 patients (55.5%) with r-ARSM stages III and IV, respectively, and no patients had r-ARSM stages Ⅰ and Ⅱ. In addition, 30.0% of patients (n = 89) had combined DIE; 55.9% (n = 167) of patients received medication for no more than 6 months after surgery (mainly GnRH-a or combination therapy, with 49.5% (n = 148) and 38.5% (n = 115) of patients, respectively).
Table 1.
Patients’ baseline characteristics
| Characteristic | |
|---|---|
| Age at surgery, years | |
| < 35 | 194 (64.9%) |
| ≥ 35 | 105 (35.1%) |
| BMI, kg/m2 | |
| < 25.0 | 270 (90.3%) |
| ≥ 25.0 | 29 (9.7%) |
| Dysmenorrhea | |
| No | 136 (45.5%) |
| Yes | 163 (54.5%) |
| Gravidity | |
| 0 | 142 (47.5%) |
| ≥ 1 | 157 (52.5%) |
| Parity | |
| 0 | 151 (50.5%) |
| ≥ 1 | 148 (49.5%) |
| History of pelvic surgery | |
| No | 244 (81.6%) |
| Yes | 55 (18.4%) |
| Combined with uterine fibroids or adenomyosis | |
| No | 203 (67.9%) |
| Yes | 96 (32.1%) |
| Serum CA125, U/mL | |
| Median (interquartile range) | 64 (40–104) |
| Unknown | 43 (14.4%) |
| Duration of the surgery, min | 80 (60–110) |
| Intraoperative bleeding volume, mL | 50 (30–60) |
| r-ASRM staging | |
| Ⅲ | 133 (44.5%) |
| Ⅳ | 166 (55.5%) |
| AAGL staging | |
| Ⅰ | 31 (10.4%) |
| Ⅱ | 86 (28.8%) |
| Ⅲ | 79 (26.4%) |
| Ⅳ | 103 (34.4%) |
| Concomitant DIE | |
| No | 210 (70.2%) |
| Yes | 89 (29.8%) |
| Side classification of the cyst | |
| Unilateral | 198 (66.2%) |
| Bilateral | 101 (33.8%) |
| Maximum diameter of the cyst, cm | |
| < 5 | 36 (12.0%) |
| 5–10 | 220 (73.5%) |
| > 10 | 43 (14.4%) |
| Medication therapy after the surgery | |
| No | 12 (4.0%) |
| GnRH-a | 148 (49.5%) |
| Progestin | 21 (7.0%) |
| Oral contraceptive pills | 3 (1.0%) |
| Combination therapy | 115 (38.5%) |
| Combination therapy | |
| No | 184 (61.5%) |
| Yes | 115 (38.5%) |
| Postoperative medication duration, months | |
| 0 | 12 (4.0%) |
| ≤ 6 | 167 (55.9%) |
| > 6 | 120 (40.1%) |
| Pregnancy after the surgery | |
| No | 217 (72.6%) |
| Yes | 82 (27.4%) |
Cumulative recurrence rate of OMA patients after Conservative surgery
All participants were followed up for 6–78 months. The median time of follow-up time was 40 months. During this period, 49 patients (16.4%) recurred, whereas 250 patients (83.6%) did not. Kaplan-Meier analysis revealed cumulative recurrence rates of 2.4%, 7.0%, 13.1%, 23.3%, and 29.6% at 12, 24, 36, 48, and 60 months after conservative surgery, respectively. Overall, the cumulative recurrence rate gradually increased over time (Fig. 2).
Fig. 2.
Cumulative recurrence rates of OMA patients following conservative surgery
Exploration of the predictive value of the AAGL score for endometriosis recurrence after conservative surgery in OMA patients
As illustrated in Fig. 3A, the HR tended to a increase with greater AAGL scores; however, the association did not reach statistical significance, as indicated by the P values for both the overall fit (P for overall = 0.775) and the nonlinear component (P for nonlinearity = 0.766). Notably, the nonsignificant P value for nonlinearity (0.766) suggests that the relationship between the AAGL scores and the recurrence risk did not deviate significantly from a linear associtation.
Fig. 3.
Value of the AAGL score in predicting recurrence in OMA patients follwing conservative surgery. A Exploration of the potential relationship between the AAGL score and the risk of recurrence. B Probability of nonrecurrence following conservative surgery in OMA patients with an AAGL score ≤ 16 and > 16
The optimal threshold for the AAGL score was calculated via the maximally selected rank statistics algorithm. We found that, compared with OMA patients with an AAGL score ≤ 16, patients with an AAGL score > 16 had a significantly greater risk of recurrence following conservative surgery (P = 0.022), as shown in Figs. 3B.
Univariable and multivariable analyses of risk factors associated with recurrence in OMA patients following conservative surgery
After univariable Cox regression analysis, we found that the serum CA125 levels, intraoperative bleeding volume, and the AAGL score > 16 were closely associated with the risk of recurrence after conservative surgery in OMA patients (all P values < 0.05) (Table 2).
Table 2.
Univariate and multivariate Cox regression analyses for recurrence after Conservative surgery in OMA patients
| Factors | Unadjusted | Adjusted | ||
|---|---|---|---|---|
| HR(95% CI) | P value | HR(95% CI) | P value | |
| Age at surgery, years | ||||
| < 35 | 1.00 | - | - | |
| ≥ 35 | 1.38(0.78–2.44) | 0.262 | - | - |
| BMI, kg/m2 | ||||
| < 25.0 | 1.00 | - | - | |
| ≥ 25.0 | 0.59(0.18–1.88) | 0.368 | - | - |
| Dysmenorrhea | ||||
| No | 1.00 | - | ||
| Yes | 1.60(0.90–2.68) | 0.109 | - | - |
| Gravidity | ||||
| 0 | 1.00 | - | - | |
| ≥ 1 | 1.03(0.59–1.80) | 0.922 | - | - |
| Parity | ||||
| 0 | 1.00 | - | - | |
| ≥ 1 | 1.16(0.67–2.03) | 0.594 | - | |
| History of pelvic surgery | ||||
| No | 1.00 | - | - | |
| Yes | 1.34(0.70–2.57) | 0.373 | - | - |
| Combined with uterine fibroids or adenomyosis | ||||
| No | 1.00 | - | - | |
| Yes | 1.13(0.61–2.07) | 0.700 | - | - |
| Preoperative serum CA125 | 1.03(1.01–1.05) | 0.011 | 1.02(1.00–1.05.00.05) | 0.045 |
| Duration of the surgery | 1.01(1.00–1.01.00.01) | 0.103 | - | - |
| Intraoperative bleeding volume | 1.02(1.01–1.04) | 0.006 | 1.02 (1.00–1.04.00.04) | 0.017 |
| r-ASRM staging | ||||
| Ⅲ | 1.00 | - | - | |
| Ⅳ | 1.78(0.97–3.25) | 0.063 | - | - |
| AAGL staging | ||||
| Ⅰ | 1.00 | - | - | |
| Ⅱ | 2.01(0.44–9.19) | 0.367 | - | - |
| Ⅲ | 2.76(0.62–12.28) | 0.477 | - | - |
| Ⅳ | 3.80(0.90–16.05.90.05) | 0.069 | - | - |
| AAGL scores | ||||
| ≤ 16 | 1.00 | - | - | |
| > 16 | 2.00(1.09–3.68) | 0.025 | 1.96 (1.06–3.61) | 0.032 |
| Concomitant DIE | ||||
| No | 1.00 | - | - | |
| Yes | 1.02(0.54–1.92) | 0.956 | - | - |
| Side classification of the cyst | ||||
| Unilateral | 1.00 | - | - | |
| Bilateral | 1.70(0.98–2.97) | 0.060 | - | - |
| Maximum diameter of the cyst, cm | ||||
| < 5 | 1.00 | - | - | |
| 5–10 | 1.13(0.40–3.17) | 0.819 | - | - |
| > 10 | 0.95(0.40–2.25) | 0.898 | - | - |
| Medication therapy after the surgery | ||||
| No | 1.00 | - | - | |
| GnRH-a | 0.64(0.20–2.06) | 0.452 | - | - |
| Progestin | 0.32(0.03–3.06) | 0.320 | - | - |
| Oral contraceptive pills | 0.83(0.14–4.95) | 0.835 | - | - |
| Combination therapy | 0.00(0.00-Inf) | 0.997 | - | - |
| Postoperative medication duration, months | ||||
| 0 | 1.00 | - | - | |
| ≤ 6 | 0.69(0.21–2.25) | 0.536 | - | - |
| > 6 | 0.53(0.15–1.82) | 0.312 | - | - |
| Pregnancy after the surgery | ||||
| No | 1.00 | - | - | |
| Yes | 0.80(0.43–1.49) | 0.476 | - | - |
BMI body mass index, CA125 carbohydrate antigen 125, r-ASRM revised-American Society for Reproductive Medicine, AAGL American Association of Gynecological Laparoscopists, DIE deep invasive endometriosis, GnRH-a gonadotropin-releasing hormone agonist
Candidate variables, that is, those with a P < 0.2 in the univariable analysis, were considered for inclusion in the multivariable model. The final selection of variables for the multivariable Cox analysis was determined on the basis of the AIC to ensure model parsimony. The results revealed that preoperative serum CA125 levels, intraoperative bleeding volume, and an AAGL score > 16 were independent risk factors for postoperative recurrence in OMA patients who underwent conservative surgery (HR 1.02, 95% CI 1.00–1.05.00.05, P = 0.045; HR 1.02, 95% CI 1.00–1.04.00.04, P = 0.017; HR 1.95, 95% CI 1.06–3.61, P = 0.032 respectively) (Table 2).
Further analysis of the predictive value of the AAGL score for postoperative recurrence in OMA patients following conservative surgery
We further explored the correlation between AAGL stage and follow-up time through Kaplan-Meier analysis (as shown in Fig. 3B) and found that patients with AAGL scores > 16 had a higher recurrence rate than those with AAGL scores ≤ 16 at the same time point. Furthermore, the landmark analysis revealed that among patients who remained recurrence-free beyond 36 months postoperatively, those with an AAGL score > 16 had a significantly higher recurrence rate than those with an AAGL score ≤ 16 (P = 0.043) (Fig. 4).
Fig. 4.
Comparison of recurrence rates between patients with an AAGL score > 16 and ≤ 16 among the remaining nonrecurrence patients before and after 36 months post-conservative surgery
Comparison of the consistency between AAGL and r-ASRM staging systems
All patients were staged according to the AAGL and r-ASRM staging systems. We found poor consistency between the two staging systems in disease staging (weighted κ = 0.243) (Table 3). Only 37.8% (n = 113) of patients were in the same stage according to the AAGL or r-ASRM staging systems. Among the 117 (39.1%) patients with AAGL stages I and II who underwent r-ASRM staging, 105 progressed to stage III, and 12 progressed to stage Ⅳ.
Table 3.
Comparison of consistency between AAGL and r-ASRM staging
| Staging, n (%) | r-ASRM | Total, n (%) | κ | |||
|---|---|---|---|---|---|---|
| AAGL | I | Ⅱ | Ⅲ | Ⅳ | 0.243 | |
| I | - | - | 31 (10.4) | 0 | 31 (10.4) | |
| Ⅱ | - | - | 74 (24.8) | 12 (4.0) | 86 (28.8) | |
| Ⅲ | - | - | 19 (6.4) | 60 (20.1) | 79 (26.5) | |
| Ⅳ | - | - | 9 (3.0) | 94 (31.4) | 103 (34.4) | |
| Total, n (%) | - | - | 133 (44.5) | 166 (55.5) | 299 (100) | |
Comparison of the correlations between the AAGL and r-ASRM stages and surgical complexity
Approximately 36.1% (n = 108) of patients had AAGL staging consistent with the surgical complexity scale, whereas only 7.7% (n = 23) of patients had r-ASRM staging consistent with the surgical complexity scale (Table 4). Compared with the consistency between the r-ASRM stage and surgical complexity scale (Kendall W coefficient = 0.552, P = 0.106), the consistency between the AAGL stage and surgical complexity scale was greater (Kendall W coefficient = 0.613, P = 0.005).
Table 4.
Comparison of the correlation between the AAGL and r-ASRM stages and surgical complexity in endometriosis patients
| Surgical complexity | ||||||||
|---|---|---|---|---|---|---|---|---|
| Staging, n (%) | A | B | C | D | ||||
| AAGL | r-ASRM | AAGL | r-ASRM | AAGL | r-ASRM | AAGL | r-ASRM | |
| Ⅰ | - | - | 30 (10.0) | 0 | 1 (0.3) | 0 | 0 | 0 |
| Ⅱ | - | - | 68 (22.7) | 0 | 18 (6.0) | 0 | 0 | 0 |
| Ⅲ | - | - | 40 (13.4) | 111 (37.1) | 39 (13.0) | 22 (7.4) | 0 | 0 |
| Ⅳ | - | - | 30 (10.0) | 57 (19.1) | 72 (24.8) | 108 (36.1) | 1 (0.3) | 1 (0.3) |
| Total | 168 | 168 | 130 | 130 | 1 | 1 | ||
Comparison of consistency between AAGL stages and surgical complexity: Kendall W coefficient = 0.613, P = 0.005
Comparison of consistency between r-ASRM stages and surgical complexity: Kendall W coefficient = 0.552, P = 0.106
Pregnancy outcomes in OMA patients after Conservative surgery
During the follow-up, of the enrolled patients, 94 patients (31.4%) expressed a desire for fertility. Following ovarian cystectomy, 82 patients (87.2%) achieved clinical pregnancy, 66 patients (22.0%) conceived naturally and 16 patients (5.3%) conceived after undergoing assisted reproductive technologies. The median time to the first pregnancy was 14.0 months (3.0–62.0 months). Among the patients with fertility requirements, 19 patients reported recurrence, 14 patients (73.7%) achieved clinical pregnancy postoperatively. Among the 75 patients without recurrence who desired fertility, 68 patients (90.7%) successfully conceived. The clinical pregnancy rates differed significantly between patients with and without recurrence (P = 0.043).
Discussion
Our findings demonstrate that patients who undergo conservative surgery for OMA exhibit an increasing risk of recurrence over time, which aligns with current research [27]. The key risk factors identified include the complexity of the surgical procedure, the involvement of both ovaries, and the presence of dysmenorrhea [21, 27–30]. Furthermore, our study revealed that the serum CA125 level, intraoperative bleeding volume, and an AAGL score > 16 were independently associated with an increased risk of recurrence postsurgery.
An accurate staging system is essential for evaluating the condition of endometriosis patients and guiding their treatment [31], as it plays a significant role in lowering the postoperative recurrence rate. According to the World Endometriosis Society, the r-ASRM staging system is currently the most widely used system in clinical settings, but its usefulness for predicting prognosis is limited [18, 32, 33]. In contrast, the AAGL staging system used in this study has shown some preliminary correlations with infertility, pain levels, and surgical complexity; however, it has not yet been thoroughly validated [32]. In our research, for the first time, we demonstrated that patients with OMA and an AAGL score exceeding 16 experienced a notably higher recurrence rate after conservative surgery, especially at 36 months post-surgery. This increased recurrence risk may be attributed to the greater likelihood of deeply infiltrating lesions or extensive pelvic adhesions in high-score patients, which increases the likelihood of residual lesions after surgery [34]. Additionally, ectopic endometrial tissue may reimplant and grow within the ovaries, contributing to recurrence risk [35]. In our cohort, patients experienced a longer time to recurrence than reported in studies without postoperative hormonal treatment [9, 36, 37]. Postoperative hormonal therapy may prevent recurrence by reducing ovulation, inhibiting endometrial cell activity, and lowering the chance of these cells reimplanting in the abdominopelvic cavity [20, 22].
A retrospective study conducted by Jason Mak and colleagues revealed that the AAGL staging system exhibited 26% lower consistency with surgical complexity compared with the r-ASRM staging system [38, 39]. In contrast, the findings of Mauricio S. Abrao and his team aligned with our own results, both demonstrating that the AAGL staging system was more consistent with surgical complexity than the r-ASRM staging system was. The discrepancies in these findings may stem from differences in the expertise of gynaecologists in evaluating endometriosis cases, as well as variations in their interpretation of intraoperative findings and the application of staging systems.
Our study results provide valuable insights for managing patients with OMA following conservative surgery, particularly in areas such as follow-up care, pregnancy management, and postoperative adjuvant therapy. Notably, we observed that patients with an AAGL score above 16 faced a significantly greater risk of recurrence 36 months or more after surgery. By leveraging this scoring system, clinicians can identify OMA patients at high risk of postoperative recurrence and implement targeted interventions, such as combination drug therapies [14, 16, 22, 34, 35, 38–41], to improve their outcomes. Additionally, the alignment of the AAGL staging system with surgical complexity enables clinicians to tailor the most effective surgical approach for each OMA patient. Patients who undergo conservative surgery for OMA have a high recurrence rate, which changes over time and presents with diverse clinical symptoms. Given the importance of long-term follow-up for patient outcomes, future studies should investigate the most effective long-term follow-up schedule for these patients.
To our knowledge, few studies have examined the AAGL staging system for endometriosis and its association with recurrence in OMA patients following conservative surgery. Our research not only highlights the predictive utility of the AAGL staging system for postoperative recurrence of OMA, but also, through a comparative analysis with the r-ASRM staging system, demonstrates its alignment with surgical complexity. These findings offer valuable insights for the preoperative evaluation of patients with OMA and support decision making about their postoperative care.
We recognize the limitations inherent in our study, which is a single-centre retrospective analysis. The study’s geographic constraints and potential recall bias may impact the general applicability and precision of the findings. In this study, the indications for conservative surgery in patients with OMA were primarily based on the Chinese guidelines for endometriosis. These indications included failure of medical treatment, co-occurrence with infertility, and ovarian cysts with a diameter ≥ 4 cm. In clinical practice, surgical intervention was also selected for patients with suspected malignant transformation of ovarian cysts. Notably, the criterion of ovarian cyst size ≥ 4 cm is not included in the ESHRE guidelines [7]. Variations in the selection of surgical indications may affect the generalizability of this study. In our cohort, the number of patients using each type of medication was relatively small, and only 12 patients (4.0%) did not receive postoperative pharmacological treatment. Therefore, further analysis was not feasible, making it difficult to evaluate the impact of postoperativemedical therapy or different treatment plans on postoperative recurrence rates.
Conclusion
In this retrospective analysis, we observed that the cumulative recurrence rate of OMA following conservative surgery exhibited a progressive annual increase. The AAGL staging system demonstrated notable utility in predicting recurrence in these patients, with an especially pronounced predictive accuracy at 36 months postsurgery and beyond. Furthermore, compared with the r-ASRM staging system, the AAGL staging system provided a more effective evaluation of surgical complexity in patients with OMA.
Acknowledgements
We would like to express our sincere gratitude to all the participants of this cohort study. We appreciate the valuable comments and support provided by Prof. Lin and Prof. Shen, which helped improve the study.
Clinical trial number
Not applicable.
Authors’ contributions
Huimin Qiu: Writing – review and editing, Investigation, Conceptualization, Formal analysis; Wanqi Lin: Writing – original draft, Conceptualization, Formal analysis; Shaowei Lin: Data curation, Formal analysis, Methodology; Minghong Shen: Project administration, Supervision, Writing – review and editing; Liang Lin: Project administration, Supervision, Writing – review and editing.
Funding
This study was supported by Fujian Provincial Natural Science Foundation Project (grant number No. 2022J011022); Joint Funds for the innovation of science and Technology, Fujian province (grant number No. 2024Y9079); and Fuzhou University Affiliated Provincial Hospital Huo Shi Fund Project (grant number No. 2020HSJJ19).
Data availability
The data underlying this article will be shared by the corresponding author upon reasonable request. Please note that the cross-border sharing of original clinical data is subject to compliance with Chinese law.
Declarations
Ethics approval and consent to participate
All patients provided verbal informed consent, and the study was approved by the Ethics Committee of Fuzhou University Affiliated Provincial Hospital (K2024-12-060), in accordance with the Declaration of Helsinki.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s Note
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Huimin Qiu, Wanqi Lin and Shaowei Lin contributed equally to this work.
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Minghong Shen, Email: fjslyyshenmh@163.com.
Liang Lin, Email: kitty342@163.com.
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