Current Endometriosis Classifications (rASRM, #Enzian, AAGL2021) and their Correlation with Operative Time

248 patients underwent laparoscopic surgery for endometriosis at the Department of Gynecology, Obstetrics, and Endocrinology at the Kepler University Hospital (KUK) between 2021 and 2022. After applying the exclusion criteria, 139 patients were included in the study – 64 in 2021 and 75 in 2022. The flowchart of the inclusion process is shown in Fig. 1 . Flowchart of inclusion process. The median age in the dataset is 32 years (IQR = 28–37) with a median BMI of 22.86 kg/m 2 (IQR = 20.31–25.71). Of the patients included, 50.4% had undergone at least one previous abdominal surgery, and eight patients had undergone three or more abdominal surgeries. The most prevalent subtype of endometriosis in the sample was peritoneal endometriosis (85.6%), followed by ovarian endometriosis (49.6%), deep endometriosis (46.8%), and adenomyosis (22.3%). Rectal involvement was observed in 10.1% of patients. According to the AAGL2021 classification, 43.2% of patients were classified as stage 1, 30.9% as stage 2, 5.0% as stage 3 and 20.9% as stage 4, while according to the rASRM classification, 37.5% of study participants were in rASRM stage 1, 12.5% in stage 2, 36.8% in stage 3 and 13.2% in stage 4. The distribution of affected compartments according to the #Enzian classification is provided in the appendix ( Table S1 online). The median “actual” operative time – after subtracting time factors for additional intraoperative measures – was 68.50 minutes (IQR = 46.75–97), with a minimum of 19 minutes and a maximum of 402 minutes. In two cases rectal shaving was required, eight patients had an intestinal resection without stoma and one patient had an intestinal resection with stoma. In one case, the surgical procedure was converted from laparoscopic surgery to laparotomy. As illustrated in Table 2 , a comparison has been made of the operative times of the rASRM and AAGL2021 classifications across different stages. The median operative time increased with stage in both the rASRM classification and the AAGL2021 classification. Using Kendall’s tau correlation, a significant positive correlation (p < 0.001) has been identified between the stages and the duration of surgery in both classifications. Due to the more complex structure and the lack of stages, the evaluation of the #Enzian classification is more complex. Table 3 shows the descriptive statistics for operative time in relation to the compartments of the #Enzian classification. The longest median operative time can be found for surgeries coded C3. Also, A3 and the involvement of compartments FI and FU showed long median operative times. Spearman’s correlation for individual compartments of the #Enzian classification shows significant positive correlations (p < 0.001) between surgery duration and all compartments. A regression analysis was carried out to identify associations between the #Enzian compartments and the operative time as a whole ( Table S2 online). Several parameters are statistically significant, including O2right, C3, C1, FA, and FU, indicating these factors have a significant impact on the operative time in the dataset.

Table S1: Distribution of the compartments of the #Enzian classification. Table S2: Results of the Regression Analysis for the compartments of the #Enzian classification.

Participants in this retrospective data analysis were all patients who underwent laparoscopic endometriosis surgery at the Department of Gynecology, Obstetrics and Gynecological Endocrinology at the Kepler University Hospital in 2021 and 2022. Eligible patients were identified using the digital surgery book of the hospital information system. The following exclusion criteria were formulated: lack of histological evidence of endometriosis, incomplete treatment of endometriosis, as well as additional surgical indications besides endometriosis with an influence on the duration of surgery (e.g., simultaneous hysterectomy, ovarian cysts of a different entity). However, for some frequently performed additional surgical procedures (e.g., hysteroscopy), a time factor was added to enable inclusion in the study (see Table 1 below). These specific correction time factors are based on evaluations of procedure duration in the operating room and have been rounded up to five-minute thresholds. The time factors were subtracted from the total operative time resulting in a corrected operative time that was then used for further calculations. All surgeries were performed by gynecologic surgeons with substantial experience in endometriosis treatment; when necessary, in multidisciplinary collaboration (e.g., colorectal surgeon). The extent of endometriosis was assessed intraoperatively using the rASRM, #Enzian and AAGL2021 classifications. However, the AAGL2021 score was only applied intraoperatively to patients from November 2021 onwards regarding to its publication date. For patients operated before November 2021, the AAGL2021 score was assigned retrospectively based on the surgical report and stored intraoperative images. This partially retrospective staging of the AAGL2021 classification was performed or supervised by the last author (S-H.E.). The study was approved by the Institutional Ethics Committee of the Johannes Kepler University (submission number 1188/2022, date of first approval 08/10/2021). Descriptive statistics, including frequencies, means, medians, interquartile ranges (IQR) and standard deviations, were calculated to summarize the data. Kendall’s tau correlation was used to determine if there was a correlation between the operative time and the rASRM/AAGL2021 classifications. Two tests were used to calculate the correlation between the #Enzian compartments and operative time: Spearman’s correlation and the Mann-Whitney U test (for the F compartments). Generalized linear models for regression analysis were performed to explore whether there were significant associations between the individual compartments of the #Enzian classification and the duration of surgery. The level of significance was set to p < 0.05, and no adjustment for multiple testing was used. Data were analysed using SPSS Statistics 29.0.2.0.

All three classification systems used in our study (#Enzian, AAGL2021 and rASRM) show a considerable impact on operative time, with an increase in duration corresponding to higher stage or specific coding. This underscores the importance of non-invasive classification systems as predictors of surgical complexity and duration. In contrast to the rASRM classification, the AAGL2021 and #Enzian classifications can be used as preoperative diagnostic tools, with the #Enzian offering a more diverse coding. Future research should focus on prospective studies with larger, multi-center datasets to develop algorithms incorporating codings from the #Enzian classification for enhanced preoperative planning. Such advancements could lead to more accurate predictions of surgery duration and better resource allocation.

This study represents a pioneering effort to compare operative times for endometriosis surgery according to codings by the #Enzian, rASRM and AAGL2021 classifications. The findings indicate a significant correlation between extended endometriosis and the length of surgical procedures in all three classifications, whether by stages in the rASRM and AAGL2021 classifications or by compartments in the #Enzian classification. For both four-stage classification systems (rASRM and AAGL2021), the median operative time extended with increasing stages. In the existing literature, there is a lack of explicit studies investigating operative times according to rASRM stage. An indirect correlation was observed in a study by Nicolaus et al. reporting that higher rASRM stages are associated with more complications, leading to longer operative times 9 . However, the rASRM classification does not adequately capture deep endometriosis, which may be a contributing factor why this system alone does not fully reflect the actual surgical effort for more complex cases 10 . Furthermore, the applicability of the rASRM classification in a preoperative non-invasive setting is limited, thereby restricting its use for preoperative planning of operating room resources. Similar to rASRM, there is a shortage of studies reporting surgical duration according to the AAGL2021 stage. A comprehensive search of the PubMed database failed to identify any publications that addressed operating times in relation to the AAGL2021 classification. Even in the original publication on the AAGL2021 classification, no operating times are presented in the surgical validation cohort 7 . However, a study by Abrao et al. on the applicability of ultrasound concluded that patients can be reliably identified preoperatively with the correct AAGL2021 stage 11 . This statement, in conjunction with the presents study’s results, underscores the potential for incorporating AAGL2021 staging into preoperative planning tools. The #Enzian classification, with its detailed coding of endometriosis by affected compartments and size, revealed a more complex relationship with the duration of surgery. Specifically, the compartments C, FI, and FU were associated with the longest median operative times, highlighting the significant impact of deep endometriosis on surgical complexity and duration, particularly in cases of bowel involvement. This finding is in line with the study of Haas et al., in which a multiple regression analysis for predicting operating time based on the Enzian classification showed an extension of the operation time when C3 is involved 12 . Another study by Thomassin-Naggara et al., based on preoperative Enzian codings by MRI, demonstrated that the operating time for Enzian coding C3 was significantly longer than for C2 13 . In both studies an earlier version of the Enzian classification was used, but its basic structure has been retained in the current #Enzian classification. The regression analysis of the #Enzian compartments in our study further identified compartment O (ovarian endometriomas) and FA (adenomyosis) as relevant influencers on surgery duration. A study of Banerjee et al. described that the presence of endometriomas is a good indicator for the presence of rectosigmoid disease and involvement of the posterior cul-de-sac 14 . Other studies have demonstrated a strong association between adenomyosis and deep endometriosis 15 16 . Whether adenomyosis plays an independent role or is merely a surrogate marker of accompanying deep endometriosis cannot be determined by the study’s data. The #Enzian classification can be applied either intraoperatively or by using imaging modalities such as ultrasound or MRI. By precisely mapping endometriosis across anatomical compartments and lesion sizes, the #Enzian demonstrates strong potential as a predictive tool for surgical complexity and duration, particularly through its associations with deep infiltrating compartments like C, FI, and FU, as well as ovarian involvement and adenomyosis. In contrast to rASRM, the AAGL2021 and #Enzian classifications offer preoperative utility, with #Enzian particularly suited for algorithmic tools due to its structured and compartmental format. However, high-quality preoperative mapping and use of detailed classification systems requires in-depth anatomical knowledge and targeted training to ensure consistent and correct use. Systems like #Enzian or AAGL2021 should be regarded as a crucial quality standard to promote continuous improvement in preoperative planning. Recent studies have reported alternative scores for predicting the length of surgery. For instance, the preoperative applicability of the NMS-E (Numerical Multi-Scoring System of Endometriosis) was described in a recent paper 17 . This score demonstrated a robust correlation with the rASRM score and surgical outcomes, and was useful in predicting surgical duration. The Deep Pelvic Endometriosis Index magnetic resonance imaging score (dPEI score) is a newly published preoperative score for women with deep endometriosis based on MRI images. This score is helpful in predicting operating time, length of hospitalisation and postoperative complications 18 . Ebrahimi et al. evaluated a preoperative five-domain ultrasound-based endometriosis staging system (UBESS), which was compared postoperatively with the RANZCOG/AGES system. The results showed that preoperative ultrasound using the UBESS staging system was able to predict the complexity of laparoscopic surgery 19 . The list demonstrates that new endometriosis classifications are springing up, yet a universally accepted classification remains elusive. Fadinger et al. described in their study a first attempt to convert the #Enzian classification into a 4-stage scoring system comparable to the AAGL classification, demonstrating an overlapping of both classification systems. In their opinion, there should be a universal classification in the future that incorporates the strengths of existing classifications 20 . The strength of the study lies in its direct comparison of three distinct endometriosis classifications within a single data set of a diverse endometriosis population. Consistent surgical procedures by physicians at an endometriosis center certified by EuroEndoCert ensure high standards of care and expertise 21 . However, limitations of the study must be acknowledged including its retrospective study design and single-center data collection. Experience in endometriosis surgery and individual surgical technique plays an important role in the duration of surgery, making it challenging to extrapolate the time data to other centers. Additionally, a larger study population would facilitate a more nuanced analysis of the complex #Enzian coding system, maybe enabling a preoperative planning tool. While certain compartments in the #Enzian classification (e.g., C3, FI, FU) showed statistically significant associations with prolonged operative time in the regression analysis, these findings must be interpreted with caution due to the small sample sizes in those subgroups, increasing the risk of overfitting or type I error. However, it is important to emphasize that the statistically significant findings in our study align well with clinical experience and plausibility. The time factors employed for minor additional intraoperative interventions may introduce inaccuracies in the actual operative time, though this is presumed to have no substantial impact on the study’s findings.

Endometriosis is a chronic gynecological disease that affects approximately 10% of women of reproductive age. It is defined as the presence of endometrial tissue outside the uterus, which may manifest as peritoneal lesions, ovarian cysts (known as endometriomas), or deep endometriosis 1 2 3 . Commonly used classification systems for endometriosis are the rASRM, the #Enzian, and the AAGL2021 classification. The rASRM score is the most widely used classification system, but hardly describes deep endometriosis 4 5 . The #Enzian classification describes superficial and deep endometriosis, as well as ovarian endometriosis, adhesions and adenomyosis 6 . The AAGL2021 classification is a 4-stage system analogous to the rASRM classification but has been developed to better reflect surgical complexity of endometriosis surgery by using a more detailed mapping 7 . The treatment options for endometriosis vary depending on the symptomatology and results of non-invasive diagnostics, with surgery being one of the primary treatment pillars, along with hormonal treatment. Preoperative planning plays a critical role in optimizing health resource management, particularly in the context of endometriosis surgery, where operative times can vary significantly based on disease extent and complexity. Optimal estimation of the planned surgery duration can achieve improved operating room efficiency, more accurate scheduling, reduced patient waiting times and better resource allocation 8 . To the best of our knowledge, no publication has evaluated the duration of endometriosis surgery in relation to the stage of all three classification systems mentioned above within the same patient cohort. The aim of this study was to evaluate the correlation between the rASRM, #Enzian, and AAGL2021 classifications and the duration of surgery. The main intention was to ascertain which of these classifications most accurately reflects the duration of surgery and should be employed to plan operating room resources.