ENDO_STAGE Magnetic Resonance Imaging: Classification to Screen Endometriosis

Marc Bazot, Emile Daraï, Émile Daraï, Giuseppe Benagiano, Giuseppe P Benagiano, Caroline Reinhold, Amélia Favier, Horace Roman, Jacques Donnez, Sofiane Bendifallah
Journal of clinical medicine · 2022 · vol. 11(9) , pp. 2443 · doi:10.3390/jcm11092443 · PMID:35566569 · PMC9101650 · W4224950722
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⚙ AI-generated summary by claude@2026-06, 2026-06-08 ⓘ

A new Endo-Stage MRI classification for endometriosis was developed and validated, showing improved prediction of surgical complications compared to the rASRM classification.

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⚙ AI-generated deep summary by claude@2026-06, 2026-06-12 · read from full text ⓘ

The study developed and evaluated a new MRI-based staging and triage system for suspected pelvic endometriosis, using women who underwent surgery at a Paris hospital and had preoperative pelvic MRI interpreted prospectively (n=751; MRI outside the institution was excluded). Endo-Stage MRI defined six stages (0–V) based on anatomical location and lesion extent and grouped stages into low, intermediate, and high surgical-risk categories; it was compared with rASRM staging and assessed for predicting intra- and postoperative complications (Clavien–Dindo grade I–IV), severe complications, and voiding dysfunction requiring self-catheterization for more than one month. Higher Endo-Stage MRI stages and triage risk categories correlated with higher complication rates, and multivariate analyses found the triage system independently associated with worse surgical outcomes; it also showed higher discrimination than rASRM for predicting overall complications (AUC 0.78 vs 0.61). A key limitation stated is that radiologists’ intra- and inter-observer agreement was not evaluated because the authors did not retrospectively review MRI studies. This paper is centrally about endometriosis — it proposes and validates an Endo-Stage MRI classification system to preoperatively stage disease and predict surgical complications in pelvic endometriosis.

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Abstract

Introduction: Transvaginal sonography is the first-line imaging technique to diagnose endometriosis, but magnetic resonance imaging is more accurate in staging the extent of lesions, especially for deep pelvic endometriosis. The revised American Society for Reproductive Medicine and Enzian classifications are commonly used to stage the extent of endometriosis. However, a review underlined their weaknesses in terms of complexity, lack of clinical reproducibility and low correlation with surgical complications and fertility outcomes. Thus, to this day, in clinical practice, there is a lack of consensual, standardized or common nomenclature to stage the extent of endometriosis, posing a worldwide challenge. Objectives: The aims of our study were to: (i) develop a new classification (entitled Endo-Stage MRI) based on patterns of endometriosis as observed with magnetic resonance imaging; (ii) compare results with those of the rASRM classification; (iii) estimate the Endo-Stage MRI accuracy to predict the rate of surgical complications; and (iv) propose an Endo-Stage MRI system of triage (low, intermediate, high) that correlates with the risk of surgical complications. The goal is to improve the effectiveness of care pathways and allow for the planning of a multidisciplinary approach when necessary. Patients and methods: A single-center observational study using available clinical and imaging data. According to anatomical locations and the extent of endometriotic lesions, a standardized classification comprising six stages of severity (0–5) was designed. Results: A total of 751 patients with pelvic endometriosis underwent surgery from January 2013 to December 2018 in a tertiary care university hospital. Their Endo-Stage MRI classification was correlated with: (i) the rate of overall complications (grade I–IV Clavien-Dindo classification, (ii) the rate of major complications (grades III–IV) and (iii) the rate of voiding dysfunction requiring self-catheterization lasting more than one month. According to the Endo-Stage MRI classification, stages 0, 1, 2, 3, 4 and 5 were observed in 26 (3%), 156 (21%), 40 (5%), 22 (3%), 290 (39%) and 217 (29%) patients, respectively. Using the proposed Endo-Stage MRI system as triage, low (stages 0–2), intermediate (stages 3–4) and high-risk (stage 5), complications were observed in 29 (13%), 109 (34.9%) and 103 (47.4%) patients, respectively. In multivariate analysis, the Endo-Stage MRI system of triage was strongly predictive of surgical complications and achieved higher accuracy than the revised American Society for Reproductive Medicine classification (AUC: 0.78 (95% CI, 0.76–0.80) vs. 0.61 (95% CI, 0.58–0.64)). Conclusion: Our study proposes a new imaging classification of endometriosis coined Endo-Stage MRI classification. The results suggest that when applied to a clinical situation, it may improve care pathways by providing crucial information for identifying intermediate and/or high-risk stages of endometriosis with increased rates of surgical complications. To make this classification applicable, a multicentric validation study is necessary to assess the relevancy and clinical value of the current anatomical MRI classification.
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Section 2

The database of the Pathology Department of the Tenon University Hospital, Sorbonne University, Paris, was screened from January 2013 to December 2018 to identify women who had undergone surgery for suspected pelvic endometriosis ( n = 1293). The database of the Radiology Department was then searched to identify among these patients those who had MRI evaluation before surgery. Patients with preoperative MRI performed outside this institution ( n = 542) were excluded from the present investigation. The study was approved by the Ethics Committee of the National College of French Obstetricians and Gynecologists (CNGOF) (reference number: CEROG 2012-GYN-10-03). MRI sequences were acquired at 1.5 T (GE HDXT, Milwaukee, WI, USA) or 3 T (GE Architect, Milwaukee, WI, USA) using a phased pelvic array. The acquisition protocol, including sequences and parameters, followed guidelines recently published by the European Society of Urogenital Radiology (ESUR) ( Table 1 ) [ 11 ]. Bowel preparation by enema and antiperistaltic drug administration (Glucagen ® , Novo Nordsik) were routinely offered to the patients. Vaginal and rectal opacification and gadolinium injection were not included in our routine MRI protocol. All MRI examinations were performed and interpreted prospectively by radiologists, and all the data present in the formal reports were entered in an Excel spreadsheet. No attempt was made to review the MRI studies retrospectively to evaluate intra and inter-observer agreement among radiologists. Pelvic endometriosis was diagnosed in accordance with previously described criteria [ 12 , 13 , 14 ]. Surgery was performed by different experienced gynecological surgeons according to surgical procedures previously published [ 15 , 16 , 17 , 18 , 19 , 20 ]. Deep pelvic endometriosis, also called deep infiltrating endometriosis, is defined as infiltration of the implant of endometriosis under the surface of the peritoneum, as previously described [ 13 ]. All surgical, pathological and outcomes findings documented in the official medical files were entered in an Excel spreadsheet.

Section 3

Based on the International Federation of Gynecology and Obstetrics (FIGO) classification for staging gynecological cancers and on the British Royal College of Obstetricians and Gynecologists (RCOG) scoring of surgical complexity [ 21 , 22 ], a new standardized classification (coined Endo-Stage MRI), was designed under the supervision of a gynecological subspecialty radiologist (MB) with more than 25 years of experience in MRI of endometriosis and a skilled surgeon (SB) with 5 years of surgical experience in endometriosis. Briefly, as shown in Table 2 , six Endo-stages of MRI (0 to V) were created according to the anatomical location, the extent of endometriotic lesions and European Society of Human Reproduction and Embryology (ESHRE) guidelines [ 9 ]. The aim was to follow the evolution of pelvic endometriosis, as suggested by Nisolle and Donnez [ 23 ]. Stage 0 : refers to the presence of only superficial peritoneal endometriosis irrespective of the locations involved (ovarian fossa, vesico-uterine fold, pouch of Douglas) and/or uni or bilateral ovarian endometrial cyst (size ≥1 cm) ( Figure 1 ). Stage I : defines the presence of retro-cervical DPE, including isolated involvement of the torus (1A), or the torus and uni or bilateral uterosacral ligament endometriosis (1B) ( Figure 2 ). Stage II : relates to DPE involving the vagina (2A), or the rectovaginal septum (2B) ( Figure 3 ). Stage III : refers to parametrial (Stage 3A), sacro-recto-genital septum (3B) or lateral pelvic wall (Stage 3C) disease ( Figure 4 ). Stage IV : indicates the involvement of the bladder (5A) or the rectum (5B) ( Figure 5 ). Stage V : defines the presence of more than three pelvic DPE locations ≥stage 2 (5A) or more than three pelvic DPE locations ≥ stage 2, associated with the involvement of distant intra-abdominal organs (ileum/cecum/ appendix or diaphragm) (5B) ( Figure 6 ). Finally, as indicated in the last column of Table 2 , an MRI system of triage to predict complications is proposed. This aims at predicting the outcomes of surgery with accuracy in terms of intra or post-operative complications. It is subdivided into three risk categories: low , intermediate and high .

Section 4

The accuracy of the Endo-MRI classification was estimated according to its correlation with: (i) the rate of overall complications (grade I–IV Clavien–Dindo classification (CDC)) [ 24 ], (ii) the rate of severe complications (grades II–IV CDC) and (iii) the rate of voiding dysfunction requiring self-catheterization lasting more than one month. The performance of the Endo-Stage MRI classification was quantified with respect to discrimination criteria [ 25 , 26 ]. Discrimination (i.e., whether the relative ranking of individual predictions is in the correct order) was quantified using the area under the curve (AUC) of the receiver operating characteristics (ROC) with a confidence interval (CI). The AUC is a summary measure of the ROC that reflects the ability of a test to discriminate the outcomes across all possible levels of positivity. AUC ranges from 0 to 1, and a model is considered to have a poor, fair or good performance if the AUC lies between 0.5 and 0.6, 0.6 and 0.7 or is greater than 0.8, respectively [ 27 ]. Stages of the new Endo-Stage MRI were compared to those of the rASRM classifications according to discrimination criteria quantified by the receiver operating characteristic curve (ROC-AUC) to estimate their accuracy [ 27 , 28 ]. Descriptive analysis was based on Student’s t -test and the Mann–Whitney test for parametric and nonparametric continuous variables, respectively, and the Chi-square test or Fisher’s exact test, as appropriate, for categorical variables. Values of p < 0.05 were considered to denote differences. The data were managed with an Excel database (Microsoft, Redmond, WA, USA) and analyzed using R 2.15 software, available online.

Intro

Endometriosis is defined as the presence of endometrium-like tissue outside the uterus [ 1 ]. A recent systematic review, including 11 studies, analyzed the prevalence of endometriosis in the general population, which ranged from 0.8% to 28.6%, with an overall estimation of 4.4% [ 2 ]. In addition, the pooled estimated prevalence of endometriosis was 33.5% in women who underwent surgery for benign gynecological conditions, 23.8% in infertile women, and 49.7 % in women with chronic pelvic pain [ 2 ]. Transvaginal sonography is the first-line imaging technique to diagnose endometriosis, but magnetic resonance imaging (MRI) is more accurate in staging the extent of lesions, especially for deep pelvic endometriosis (DPE) [ 3 , 4 , 5 ]. The revised American Society for Reproductive Medicine (rASRM) and Enzian classifications are commonly used to stage the extent of endometriosis [ 6 , 7 ]. However, a review underlined their weaknesses in terms of complexity, lack of clinical reproducibility and low correlation with surgical complications and fertility outcomes [ 8 ]. Thus, to this day, in clinical practice, there is a lack of consensual, standardized or common nomenclature to stage the extent of endometriosis, posing a worldwide challenge. Recently, the World Endometriosis Society (WES) highlighted the need for a reproducible preoperative imaging system of triage to better characterize the extent of endometriosis and improve clinical management [ 9 ]. A new classification entitled “Deep pelvic endometriosis classification index” (dPEI) was recently published underlining the value of MRI to stage endometriosis, but with some limitations on the strict definition of the various compartments and a lack of external validation [ 10 ]. In line with these recent developments, we carried out an investigation aimed at: (i) developing a new classification system (entitled Endo-Stage MRI) based on patterns of endometriosis on MRI, (ii) comparing its value to the rASRM classification, (iii) estimating the Endo-Stage MRI accuracy in predicting surgical outcomes in terms of complications and (iv) proposing an Endo-Stage MRI system of triage (low, intermediate, high) that correlates with the risk of surgical complications. The overall intent is to improve the effectiveness of care pathways and allow for the planning of a multidisciplinary approach when necessary.

Results

From the surgical, histopathologic and radiological databases of the Tenon University Hospital, we identified 751 patients who underwent preoperative MRI from January 2013 to December 2018. The surgical and patients characteristics are summarized in Table 3 . The median age and body-mass index (BMI) were 33 years (range: 19–60 years) and 22.5 kg/m 2 (range: 12–42), respectively. Surgery was performed by laparoscopy, laparotomy and after conversion in 87% (651), 10% (76) and 3% (24) of cases, respectively. According to Endo-Stage MRI classification, Stages 0, I, II, III, IV and V were observed in 26 (3%), 156 (21%), 40 (5%), 22 (3%), 290 (39%) and 217 (29%) patients, respectively. Based on the Endo-Stage MRI system of triage in low (stages 0-I-II), intermediate (stages III–IV) and high-risk (stage V) cases, overall complications rates were observed in 29 (13.0%), 109 (34.9%) and 103 (47.4%) patients, respectively. Using the Clavien–Dindo classification, the more serious complications (grades III–IV CDC and self-catheterization >1 month) were present in 32%, 11% and 16% of the patients, respectively. Utilizing the Endo-Stage MRI classification, the complications rates were positively and significantly correlated with the different stages: The more severe the disease was, the more important were the complications. Details concerning grades III–IV CDC and self-catheterization are provided in Table 4 . Based on the Endo-Stage MRI system of triage, differences were observed in the overall complication rate ( p < 0.001), grades III–IV CDC ( p 1 month ( p 1 month. Using a multivariate analysis, independent of age, BMI, history of surgery and surgical approaches, the Endo-Stage MRI system of triage was statistically associated with poor surgical outcomes, i.e., overall complications (<0.001), grades III–IV CDC (1 month (1 month are reported in Figure 7 . This indicates that Endo-Stage MRI classification provides higher accuracy than ASRM (AUC: 0.78 (95% CI, 0.76–0.80) vs. 0.61 (95% CI, 0.58–0.64)).

Conclusions

The proposed Endo-MRI classification system has been designed to allow for uniform reporting of different phenotypes of endometriosis. We believe this imaging classification will facilitate uniform reporting between physicians and improve the effectiveness of patient care pathways. In the future, we plan to conduct a multicentric validation study to achieve clinically relevant improvements and consensus on this reporting system.

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