Logistic regression analysis of imaging characteristics of transvaginal ultrasonography for predicting severe endometriosis by r-ASRM classification via laparoscopy

Endometriosis (EMT) refers to the presence of active EMT tissues (glands and stroma) outside of the uterus (1), causing unbearable chronic pain and infertility. Approximately 30% ~ 50% of women with endometriosis struggle with infertility, and 25% ~ 50% of women with infertility also have endometriosis (2). Laparoscopic surgery is the most common intervention for EMT (3). Since 1996, the revised American Society for Reproductive Medicine (r-ASRM) classification system has been widely used worldwide for the staging of EMT lesions via laparoscopic visualization, categorizing EMT in the pelvic area into four stages: minimal (stage I), mild (stage II), moderate (Stage III), and severe (stage IV) EMT (4). However, r -ASRM classification is done after laparoscopic surgery, which also indicates that the necessity of laparoscopic surgery should be effectively evaluated. Since the r -ASRM classification system does not include many affected organs and anatomical structures in the pelvic cavity, it has not been directly applied in preoperative examination (5). The early diagnosis of EMT before treatment and accurate assessment after treatment is essential for the effective clinical management (6,7). The diagnosis of EMT is challenged due to the heterogeneity of the disease, uncertainty in pathogenesis, asymptom, and complication with adenomyosis (8). Currently, the diagnosis of EMT Q. Su1, H. Luo2, J. Guo1, H. Ning2, Zh. Xu2, Ch. Zhen3, J. Chen2, F. Wang3, Q. Li4, P. Wang1* 1Department of Ultrasonography, The Third Affiliated Hospital, Southern Medical University, Guangzhou, 510630, Guangdong, China 2Department of Ultrasound, Foshan Women and Children Hospital Affiliated to Guangdong Medical University, 528000, Guangdong, China 3Department of Ultrasound, The First People's Hospital of Foshan, Foshan,528000, Guangdong, China 4Department of Gynecology, Foshan Women and Children Hospital Affiliated to Guangdong Medical University, Foshan, 528000, Guangdong, China

Background: To explore the relation between results of transvaginal ultrasonography and the revised American Society for Reproductive Medicine (r -ASRM) staging based on laparoscopy in patients with endometriosis (EMT) and to establish a prediction model for risk of severe endometriosis based on the imaging characteristics of transvaginal ultrasonography. Materials and Methods: A retrospective study was performed between April 2022 and May 2023 on women with EMT. The laparoscopic surgery results were used as the golden standard. Patients were divided into the minimal-to-moderate endometriosis (stage I -III) and severe endometriosis (stage IV) groups based on r -ASRM classification. The transvaginal ultrasonography imaging characteristics were extracted to establish a logistic regression model. Results: Among 200 patients with endometriosis, there were 78 cases of minimal -to-moderate endometriosis (stage I -III) and 122 cases of severe endometriosis (stage IV). Multivariate analysis showed that the maximum diameter of endometriomas in the right ovary, occurrence of unilateral or bilateral ovarian endometriomas, and degree of obliteration of the rectouterine pouch were independent predictors for the r -ASRM stage of endometriosis. The logistic regression model established using the above three variables had a sensitivity of 82.0%, a specificity of 93.6%, an accuracy of 86.5%, and an area under the curve of 0.933 (standard error 0.016, P < 0.005, 95% confidence interval: 0.901, 0.965). Conclusion: Based on laparoscopic visualization, the radiomic features of preoperative transvaginal ultrasonography in patients with endometriosis were correlated with the endometriotic stage. The established model using these characteristics accurately predicted the r -ASRM stage of endometriosis after laparoscopic surgery. ► Original article

Endometriosis, laparoscope, regression analysis, ultrasonography. *Corresponding author: Ping Wang, Ph.D., E-mail: [email protected] Received: January 2023 Final revised: January 2024 Accepted: February 2024 Int. J. Radiat. Res., October 2024; 22(4): 991-998 DOI: 10.61186/ijrr.22.4.998 includes ultrasonography, magnetic resonance imaging (MRI), measurement of the serum cancer antigen 125 level, and laparoscopic surgery. Histological confirmation of ectopic endometrial tissue via laparoscopy remains the gold standard for the diagnosis of EMT, while the applicability is limited by the invasive procedure (6). Transvaginal ultrasonography has the advantages as follows: (i) the accurate prediction of EMT severity by displaying the fine structure of organs and tissues in the pelvic cavity; (ii) the effective evaluation of the distribution and infiltration of deep infiltrating EMT (DIE) lesions in various parts of the pelvic cavity. Transvaginal ultrasonography has become the first -line approach for screening EMT (9,10). Compared with MRI, transvaginal ultrasonography shows relatively higher specificity in the detection of deep infiltrating endometriosis (11). Moreover, the transvaginal ultrasonography and MRI show no systemic difference in the EMT detection compared with the intraoperative measurement, and transvaginal ultrasonography is more recommended for the diagnostic examination due to its high availability, low cost and similar accuracy relative to MRI (12,13). In the present study, we analyzed the correlation between the transvaginal ultrasonography imaging characteristics in EMT and r-ASRM classification after laparoscopic surgery to assess the surgical difficulty preoperatively, which might provide the theoretical basis and novel clues for the effective and accurate diagnosis and management of EMT.

Research participants We retrospectively analyzed the clinical data of 200 patients (aged 19-51 years) with DIE screened by transvaginal ultrasonography in Foshan Maternal and Child Health Hospital (Guangdong Province, China) from August 2021 to December 2022. All patients underwent laparoscopic surgery for treatment, and EMT was pathologically confirmed. The clinical data collected in this study included clinical symptoms and signs, surgical records, surgical staging, and pathological data. The laparoscopic surgery-based r-ASRM classification included four EMT stages: minimal (stage I), mild (stage II), moderate (stage III), and severe (stage IV). Laparoscopic surgery results were used as the gold standard. Patients were divided into two groups based on their r-ASRM stage: the minimal-to- moderate group (stage I-III) and the severe group (stage IV). Research apparatus and methods A Samsung WS80 A Ultrasound Machine was used, with an intracavity probe frequency ranging from 5 to 9 Mega Hertz ( MHz) and 9 to 12 MHz. An 992 abdominal probe was used with a frequency ranging from 5 to 9 MHz. Ultrasonography The patient took the lithotomy position , after which their vagina, uterus, anterior pelvic cavity, posterior pelvic cavity, and specific tender points were successively scanned through the vagina. The collected cases were independently reviewed by two blinded radiologists (each with more than 5 years of ultrasonography experience ). They analyzed the images following the consensus issued by the International Deep EMT Analysis Group (referred to as consensus) (14) and discrepancies were resolved by

between the two radiologists. The location, number, size and imaging manifestation of EMT lesions were recorded in a standardized report. Laparoscopic surgery Experienced surgeons operated on all patients. The pelvic and abdominal cavity and the EMT lesions were assessed. After removing the connective tissues to expose the affected areas completely, the lesions, including the adjacent tissue up to 0.5 centimeters from the outer edge, were excised. The appearance of the abdominal adhesions, the uterus, the uterosacral ligament, fallopian tubes, the rectum and the presence of EMT lesions were recorded. A postoperative r- ASRM scoring table was completed to classify the EMT as minimal (stage I), mild (stage II), moderate (stage III), or severe (stage IV). Statistical analysis The SPSS23.0 software package (IBM, Armonk, NY, USA) was used for the statistical analysis of the data. Normally distributed data were compared using the t- test and presented as the mean ± standard deviation. Non-normally distributed data were compared using the rank sum test and are presented as median (M) and interquartile range (P25, P75). Count data were compared using the chi-square test and were presented as frequency (n) and percentage (%). Multivariate analysis was carried out by binary logistic regression. P < 0.05 was considered significant.

Results of r-ASRM classification of endometriotic lesions Among 200 patients with EMT, according to the r-ASRM classification, there were 78 cases of minimal -to-moderate EMT (stage I – III) and 122 cases of severe EMT (stage IV). Table 1 shows the clinical characteristics and affected sites of all patients in this study. The ultrasound imaging features of different lesions are shown in figures 1 -4. As shown in figure 1, the ovaries of this patient were partly joined Int. J. Radiat. Res., Vol. 22 No. 4, October 2024 together, termed as “kissing ovaries” sign, and bilateral ovarian endometriotic cysts were also observed. Figure 2 showed that this DIE patient presented nodules infiltrating the right uterosacral ligament. Figure 3 exhibited that the lesion of this DIE patient was located at the intestines with blur and spiculate boundary as the “Indian headdress”. Figure 4 showed the rectouterine pouch obliteration. The lesion adheres to surrounding tissues, and the rectum slid against the uterine wall, termed as uterine sliding sign. Bilateral uterosacral ligament and intestinal DIE under the hysteroscopic are shown in figures 5 and 6. As shown in figure 5, the observation under a hysteroscope identified the infiltrating nodules at bilateral uterosacral ligament of the DIE patient. Figure 6 indicated that the patient presented endometriotic cyst in the right ovarian and the intestinal lesion under a hysteroscope. Su et al. / A model using transvaginal ultrasonography to predict EMT 993 I-III (n=78) IV (n=122) t/c2 P Age (years) 33.62±5.87 34.33±7.61 0.742 0.459 Age of menarche 12.87±1.21 13.01±1.08 0.832 0.407 marital status 0.619 0.431 Married (n) 59 98 Unmarried (n) 19 24 Pregnancy history 1.518 0.218 Yes 24 48 No 54 74 BMI (kg/m2) 23.8±4.2 24.1±3.9 0.507 0.613 Infertility 22 41 0.643 0.423 Uterine adenomyosis No 61 69 9.801 0.002 Yes 17 53 Uterine size No 68 89 5.707 0.017 Yes 10 33 Ovarian lesions No 9 3 57.199 0.000 Unilateral involvement 65 49 Bilateral involvement 4 70 Ovarian dislocation movement Exist 25 11 38.359 0.000 One-sided disappearance 34 28 Bilateral disappearance 19 83 Rectal notch with or without occlusion No 42 5 82.715 0.000 One-sided occlusion 32 51 Bilateral occlusion 4 66 Douglas' lieaments DIE No 41 33 26.803 0.000 Hemi 30 38 Bilateral 7 51 Rectal / sigmoid colon DIE No 67 77 12.250 0.000 Yes 11 45 DIE of the serosal layer of the posterior uterine wall No 71 86 11.887 0.001 Yes 7 36 Anterior vaginal fornix with tenderness No 77 120 0.041 0.839 Yes 1 2 The posterior vaginal fornix was tender No 61 100 0.429 0.512 Yes 17 22 The left appendage area was tender No 53 80 0.120 0.729 Yes 25 42 The right accessory area was tender No 60 82 2.179 0.140 Yes 18 40 The left sacral ligament was tender No 65 92 1.770 0.183 Yes 13 30 The right sacral ligament was tender No 74 97 9.059 0.003 Yes 4 25 Table 1. Baseline characteristics of patients. BMI: body mass index; DIE: deep infiltrating endometriosis. Univariate analysis of the diagnostic efficacy of imaging characteristics Based on univariate analysis, we analyzed a total of 49 variables, including age, the presence of adenomyosis, uterine size, ovarian EMT, the disappearance of bilateral ovarian malposition and motion, the degree of obliteration of the rectouterine pouch, DIE size and DIE distribution in the fallopian tube, kidney, renal ureters, urethra, bladder, bladder uterine peritoneal reflection , rectouterine pouch, rectovaginal septum, rectum/ sigmoid colon, serosa of the posterior uterine wall and posterior fornix of the vagina. The results of the univariate analysis showed that the r-ASRM stage of EMT lesions was correlated with the presence of adenomyosis, uterine enlargement, the occurrence of unilateral or bilateral ovarian endometrioma, the disappearance of unilateral or bilateral ovarian malposition and motion, the degree of the rectouterine pouch obliteration , the degree of uterosacral ligament involvement, involvement of the rectum/ sigmoid colon, involvement of the serosa of the posterior uterine wall, the presence of tenderness in the right uterosacral ligament, the maximum diameters of chocolate cysts in the left and right ovaries, maximum diameters of DIE lesions located in the left and right uterosacral ligaments, the maximum diameter and infiltration depth of intestinal DIE lesions, and the maximum diameter and infiltration depth of EMT lesions in the serosa of the posterior uterine wall (all P < 0.05, see table 2 for details). 994 Int. J. Radiat. Res., Vol. 22 No. 4, October 2024 Figure 1. A representative transvaginal ultrasonography image showed the kissing ovaries sign with bilateral ovarian endometriotic cysts. Figure 2. Representative transvaginal ultrasonography images showed right uterosacral ligament deep infiltrating endometriosis (DIE). Figure 3. A representative transvaginal ultrasonography image showed the Indian headdress sign of intestinal DIE. Figure 4. Representative transvaginal ultrasonography images of a DIE patient with the obliteration of the rectouterine pouch. The lesion adheres to surrounding tissues, and the presented uterine sliding sign indicated the obliteration of the rectouterine pouch. Figure 6. Right ovarian endometriotic cyst (“white arrow” as shown) and intestinal DIE (“black arrow” as shown) under the hysteroscope. Figure 5. Bilateral uterosacral ligament in a DIE patient under the hysteroscope. Multivariate analysis of the diagnostic value of imaging characteristics Multivariate binary logistic regression analysis was conducted with r- ASRM Stage IV as the dependent variable. Our results showed that the size of the right ovarian endometrioma , the occurrence of unilateral or bilateral ovarian endometrioma, and the degree of obliteration of the rectouterine pouch were independent predictors for r -ASRM stage in EMT patients (P < 0.05, table 3). The following logistic regression equation was established: −7.901 + (0.031 × maximum diameter [long diameter, unit: mm] of right ovarian endometrioma) + (2.437 × unilateral or bilateral ovarian endometrioma occurrence) + (2.888 × degree of rectouterine pouch obliteration). Table 4 showed the assigned values for regression analysis, with an intercept of − 0.337. The receiver operating characteristic (ROC) curve was prepared using the predicted values. The predic- tive ability of this model was evaluated using the area under the ROC curve ( figure 7 ) . The logistic regression model established based on the imaging characteristics of ultrasonography showed a sensi- tivity of 82.0%, a specificity of 93.6%, an accuracy of 86.5%, and an area under the curve of 0.933 (standard error 0.016, P < 0 .05, 95% confidence in- terval: 0.901, 0.965). Table 3. Binary logistic regression results. Su et al. / A model using transvaginal ultrasonography to predict EMT 995 I-III (n=78) IV (n=122) T/Z P Age 33.62±5.87 34.33±7.61 -0.744 0.458 Long diameter of left ovary 0.00 (0.00, 57.25) 36.00 (0.00, 70.00) -2.538 0.011 Long diameter of right ovary 0.00 (0.00, 56.25) 48.50 (21.75, 72.25) -4.698 0.000 DIE diameter of left uterosacral ligament 0.00 (0.00, 10.00) 7.50 (0.00, 13.00) -2.434 0.015 DIE diameter of right uterosacral ligament 0.00 (0.00, 0.00) 9.00 (0.00, 15.00) -5.461 0.000 Intestinal DIE length 0.00 (0.00, 0.00) 0.00 (0.00, 16.00) -3.514 0.000 Gut DIE depth 0.00 (0.00, 0.00) 0.00 (0.00, 6.00) -3.536 0.000 The DIE length of the uterine serosal layer 0.00 (0.00, 0.00) 0.00 (0.00, 10.00) -3.436 0.001 The DIE depth of the uterine serosal layer 0.00 (0.00, 0.00) 0.00 (0.00, 4.00) -3.412 0.001 Table 2. Univariate analysis of the diagnostic efficacy of imaging characteristics. DIE: deep infiltrating endometriosis. B standard error Wald conspicuousness OR The 95% confidence intervals of the OR lower limit superior limit Left of left size (long diameter in mm) 0.022 0.012 3.742 0.053 1.023 1.000 1.046 Right sac size (long diameter in mm) 0.031 0.013 5.978 0.014 1.032 1.006 1.058 Left uterosacral ligament DIE diameter (in mm) 0.028 0.059 0.219 0.640 1.028 0.916 1.154 Right uterosacral ligament DIE diameter (in mm) 0.065 0.065 0.987 0.320 1.067 0.939 1.212 DIE length (in mm) 0.052 0.067 0.615 0.433 1.054 0.925 1.201 DIE depth (in mm) 0.004 0.139 0.001 0.979 1.004 0.764 1.318 DIE of uterine serous layer (in mm) 0.169 0.126 1.801 0.180 1.184 0.925 1.515 DIE depth of uterine serosa layer (in mm) -0.296 0.286 1.071 0.301 0.744 0.425 1.303 Uterine adenomyosis -.593 0.655 0.820 0.365 0.553 0.153 1.994 uterine size 1.055 0.825 1.635 0.201 2.871 0.570 14.456 Ovarian lesions 2.437 0.770 10.025 0.002 11.440 2.531 51.714 Ovarian dislocation movement -.385 0.466 0.682 0.409 0.680 0.273 1.697 Rectal notch with or without occlusion 2.888 0.585 24.407 0.000 17.951 5.709 56.446 Douglas' lieaments DIE 0.420 0.739 0.322 0.570 1.521 0.357 6.476 A DIE of the rectosigmoid colon -0.976 1.410 0.480 0.489 0.377 0.024 5.968 DIE of the serosal layer of the posterior uterine wall 0.201 1.915 0.011 0.916 1.222 0.029 52.103 The right sacral ligament was tender 0.347 0.927 0.140 0.708 1.415 0.230 8.709 OR: odds ratio; DIE: deep infiltrating endometriosis. Test the outcome variable AUC standard errora The asymptotic significanceb Asymptotic 95% confidence interval lower limit superior limit Right sac size (long diameter in mm) 0.694 0.039 0.000 0.618 0.770 Ovarian lesions 0.774 0.033 0.000 0.710 0.838 Rectal notch with or without occlusion 0.849 0.028 0.000 0.795 0.903 prediction model 0.933 0.016 0.000 0.901 0.965 Table 4. The area below the curve. AUC: area under the curve.

EMT-induced chronic pelvic pain and infertility seriously affect the quality of life of childbearing women globally. The most important role of r-ASRM classification is to predict the postoperative capabilities of natural pregnancy in patients with EMT and provide treatment options ( 1 5 ) . Laparoscopic resection of EMT lesions is the most common treatment method for EMT. However, the procedure is challenging, highly dependent on the clinical experience and surgical skills of surgeons and may trigger postoperative complications/ trauma. Thus, physicians are suggested to consider the preoperative imaging results to provide individualized treatment plans. With the development of high -frequency endo-cavity probes, more imaging details are obtained with pelvic ultrasound information for the diagnosis of EMT. Previous studies have indicated that the adenomyosis is associated with endometriosis, especially the deep infiltrating lesions, and the severity of EMT was evaluated based on ASRM on preoperative transvaginal ultrasonography, and the

of transvaginal ultrasonography are closely correlated with those of the laparoscopic examination (16,17). Moreover, adenomyosis, right endometrioma, right endometrioma ≥ 5 cm are regarded as independent risk factors for EMT (18). A previous work also revealed that the transvaginal ultrasound sliding sign shows high sensitivity in the prediction of pouch of Douglas obliteration (19). In the present study, we retrospectively analyzed the clinical data and ultrasonography imaging characteristics of EMT patients with confirmed r-ASRM stages after laparoscopic surgery. Our results showed that patients with adenomyosis and uterine enlargement showed severe EMT and a high risk of involvement of bilateral ovaries, bilateral uterosacral ligaments, the rectum/ sigmoid colon, and the serosa of the posterior uterine wall (all P < 0.05), resulting in the disappearance of bilateral ovarian malposition and motion, complete obliteration of the rectouterine pouch, and tenderness in the right uterosacral ligament. T hree independent predictors were screened out after univariate analysis, including the maximum diameter of the right ovarian endometrioma, the degree of obliteration of the rectouterine pouch, and unilateral or bilateral ovarian involvement (table 2) and the results are in line with the previous findings. The classical theory of EMT pathogenesis is retrograde menstruation, in which endometrial , epithelial and stromal cells in the blood flow back into the pelvic cavity instead of the vagina, stimulating the proliferation of connective tissue or smooth muscle tissue to form lesions ( 2 0 , 2 1 ). Also, anatomical and hormonal factors are considered to affect left lateral predisposition to EMT. For example, the presence of a sigmoid colon reduces the blood flow to the left side of the pelvic cavity, which may delay the clearance of endometrial cells through tubal reflux during menstruation, supporting the retrograde menstruation theory (22-24). In th e present study, the maximum diameter of the endometrioma in the right but not the left ovary had predictive power (table 3), which was consistent with the findings reported by Ulukus et al . that the incidence of ovarian endometrioma on the right side was higher than that on the left side in patients with severe EMT (25). In the r-ASRM classification, the degree of adhesions on the ovaries greatly contributes to the r-ASRM score. However, ovarian malposition and motion had no independent predictive value in our study. This may be related to the influence of subjective factors, such as the imaging methods and the operator’s judgment. A multicenter study reveals that the transvaginal ultrasound is of high accuracy in the prediction of ASRM staging for EMT (26). A recent study by Yang et al. have established a preoperative prediction model for the evaluation of risk factors related to severe EMT, with good diagnostic performance (AUC = 0.846) (27). In the present study, we combined multiple imaging characteristics of ultrasonography and clinical-related factors to establish a model for predicting severe EMT (r-ASRM classification stage IV) via laparoscopic visualization through multivariate logistic regression analysis. The established model had a sensitivity of 82.0%, a specificity of 93.6%, an accuracy of 86.5%, and an area under the curve of 0 .933 ( standard error 0.016, P < 0.05, 95% confidence interval: 0.901, 0.965) in predicting severe EMT (table 4, figure 7) . The predictive variables were all easy-to-obtain features that did not require invasive examinations. 996 Int. J. Radiat. Res., Vol. 22 No. 4, October 2024 Figure 7. Receiver operating characteristic (ROC) curve evaluates the predictive ability of the logistic regression model established in this study for severe endometriosis. The curve shows an area under the curve of 0.933, a standard error of 0.016, P < 0.05 and a 95% confidence interval of (0.901, 0.965). Our established model was simple, practical and easy to opera te, with good performance relative to the previous models and could be applied in a real-time, fast, and repetitive manner in clinical practice. In the era of precision medicine, a single indicator can no longer fulfill individualized treatment needs. It is necessary to comprehensively analyze the available information and screen out the risk factors to improve diagnostic accuracy. The prediction model established in this study is an easy-to-use tool with clinical value. The risk of severe EMT in each patient was determined using a simple equation, facilitating individualized treatment and assisting physicians in accurately determining each patient's disease severity and surgical difficulties. Nevertheless, this study has some limitations. Elastography and contrast -enhanced ultrasonography have rapidly developed in recent years. Diagnostic ultrasound is no longer limited to simple grayscale and color Doppler imaging. Moreover, MRI has a certain value in the diagnosis and preoperative staging of EMT (28) . These factors were not included in this study. Follow-up research with larger samples should be conducted to further establish a prediction model in combination with multimodal imaging indicators to verify th e accuracy and practicability of our model.

Transvaginal ultrasonography is valuable for EMT staging. The regression model established in this study using ultrasonic imaging characteristics effectively predicted the r- ASRM stage of EMT lesions, providing a basis for the diagnosis and treatment of EMT, assisting surgeons in predicting the degree of surgical risk before surgery accurately and improving individualized surgical treatment. ACKNOWLEDGMENT Not applicable. Funding: This article is one of the achievements of the medical research project "Application of Endo- scopic Ultrasound Elastic Imaging Technology Com- bined with Color Doppler in the Diagnosis of Deep Localized Endometriosis of the Pelvic Cavity" by the Foshan Municipal Health Bureau (project approval number 20210394). Conflict of interests: All authors declared no conflicts of interest. Data availability statements: The data that support the findings of this study are available on request from the corresponding a uthor upon reasonable request. Ethical consideration: Not applicable. Author contribution: Q.S.: Conceptualization, data analysis, original draft; H.L., J.G.: H.N.: data collection, data analysis, reviewing and editing; Z.X., C.Z., J.C.: data collection, data analysis, reviewing; P.W.: Conceptualization, Supervision, reviewing and editing. All authors have read and approved the final version of the manuscript.

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