Correlation of Endoscopic Findings with Suspected Intestinal Endometriosis in the Distal Sigmoid and Rectum as Observed on Transrectal Ultrasonography

The differential diagnoses of abdominal or chronic pelvic pain include diseases such as irritable bowel syndrome, inflammatory bowel disease, abdominal tumors, and intes- tinal endometriosis. 1–3 Currently, there is no endoscopic definition regarding intestinal involvement in endometriosis (EDT), which may lead to failure or delay in diagnosis. Endometriosis is a benign gynecological disease, de fined by the presence of tissue similar to that of the endometrium, glands, and/or stroma that is located outside the uterine cavity and responsive to hormonal stimuli. 4–7 When EDT infiltrates the wall of the rectum or colon, colonoscopy may exhibit deviations from normal findings. However, few stud- ies to date have described these changes or an actual

► endometriosis ► sigmoidoscopy ► colonoscopy ► sigmoid colon ► rectal diseases

Introduction Colonoscopy enables detailed endoscopic evaluation of the interior of the colon. Changes observed via colonoscopy may be subtle or pronounced and can sometimes mimic those of other diseases, s uch as deep intestinal endometriosis. The diagnosis of endometriosis in the distal sigmoid and rectum by colonoscopy has been described in previous case reports.

We aimed to correlate the endoscopic changes found in the distal sigmoid and rectum with the presence of endometrial deposits con firmed by transrectal ultrasound (TRUS).

We included 50 female patients referred to the endoscopy department at our institution for colonoscopy, rectosig moidoscopy, or TRUS, who exhibited one or more symptoms associated with endometriosis.

The colonoscopic findings were normal in 36 patients but showed alterations in 14 patients. Among the latter, TRUS revealed involvement of the sigmoid and/or rectal wall in 11 patients.

The endoscopic changes in the distal sigmoid or rectum described in this study were strongly associated with endometrial deposits con firmed using TRUS. received November 18, 2022 accepted after revision January 23, 2023 DOI https://doi.org/ 10.1055/s-0043-1764194. ISSN 2237-9363. © 2023. Sociedade Brasileira de Coloproctologia. All rights reserved. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDeri vative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/ licenses/by-nc-nd/4.0/) Thieme Revinter Publicações Ltda., Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil Original Article THIEME 36 Article published online: 2023-03-22 association with endometrial deposits located near or in fil- trating the wall of the colon and rectum. 3,4 The appearance and maintenance of endometrial deposits are dependent on hormonal stimulation. Therefore, the incidence of the disease is higher in reproductive-age wom- en and does not commonly occur before menarche, or in postmenopausal women who are not exposed to estrogen replacement therapy. It is estimated that the incidence of EDT among reproductive-age women is between 5 and 15%. 5,8,9 The most common sites of deep intestinal EDT implantation are the ovaries, fundus of the Douglas ’ pouch, round ligament, uterosacral ligament, uterus, uterine tubes, sigmoid colon, and appendix 4,6,10–12)). In cases of EDT that affects the intestinal segments, the sites with the highest incidence rates are the rectum and the distal sigmoid, accounting for up to 95% of intestinal implants. 3,13–15 Transrectal ultrasound (TRUS) examination is one of the most specific methods used for the diagnosis and evaluation of intestinal involvement of endometrial deposits. The use of rigid transducers similar to those used in transvaginal ultra- sound or endoscopes with ultrasound transducers on their end enable examination of the entire rectum and sigmoid when studying the disease using the echo-logic classi fica- tion, which allows the detailing of the degree of invasion of the rectal or colonic wall (T1 when there is no invasion, T2 for involvement of the serosa, T3 when the muscularis propria is involved, T4 for involvement of the submucosa, and T5 when the mucosa is involved). 16 Histological con firmation is pos- sible via laparoscopy or echo-guided puncture (solely for endometrial deposits); therefore, the diagnosis can be made based on clinical and radiological examinations alone. These imaging studies are important for diagnosis, classi fication, and surgical planning, when necessary, and include the following: abdominal ultrasonography, transvaginal ultraso- nography (TRUS), three-dimensional transvaginal ultraso- nography, magnetic resonance imaging (MRI), double contrast barium enema, water enema computed tomogra- phy, colonoscopy, and virtual colonoscopy, although these all have specific indications and limitations. 6,16–28 Laparoscopy displays low detection accuracy in the case of endometrial deposits in the rectum or distal sigmoid. Transvaginal ultra- sonography, transrectal endoscopy, and MRI are the most appropriate options, with similar results. 13 It is important to emphasize that TRUS is a minimally invasive and highly accurate modality; it is considered one of the best preoperative examinations to determine the degree of invasion of lesions in the intestinal wall, especially in the rectum and distal sigmoid, thereby providing important information for surgical planning. 18,22,29,30 Therefore, this study aimed to correlate the endoscopic changes found in the distal sigmoid and rectum with the presence of endometrial deposits con firmed via TRUS.

This was a prospective cross-sectional study approved by the Research Ethics Committee CAAE: 32790414.3.0000.5461. The study population included female patients between 18 and 55 years of age who were referred to the endoscopy department of our institution for colonoscopy, rectosigmoi- doscopy, or TRUS, who presented with one or more of the following symptoms associated with EDT: abdominal pain, pain during defecation, rectal bleeding, dyspareunia, and infertility. All participants provided written informed consent. This is a pioneering study comparing endoscopic and sonographic findings in patients with EDT that affects the rectosigmoid. No consistent data for sample size calculation were found in the literature and, therefore, a pilot study with 50 individuals was conducted to determine the required number of patients. The exclusion criteria were as follows: patients with active, or a history of, cancer; inadequate preparation of the rectum and/or distal sigmoid (Boston scale equal to 0 or 1 in the rectum or distal sigmoid); refusal to participate; relative or absolute contraindications to colonoscopy or TRUS; and relative or absolute contraindications to sedation or anesthesia. Participants agreed to undergo laparoscopy or laparotomy with surgical intervention in the rectum and/or distal sigmoid and/or gynecological interventions (except for cesarean section and/or resection of ovarian cysts). The following variables were evaluated in this study: Clinical variables: 1) Pain upon direct pressure on the vaginal fornix during sexual intercourse (deep dyspareunia) and/or vaginal examination; 2) chronic pelvic pain (constant infraumbilical pain for more than 30 days and/or pain associated with menstruation for more than 3 cycles); and 3) intestinal bleeding with red blood and without hemody- namic repercussion in the previous 7 years. Endoscopic variables: 1). Fold thickening (with preserved circular anatomy of the organ and one or more haustrations with visually altered thickness) ( ►Fig. 1 ); 2) bulging without nodules (with visually altered circular anatomy of the organ and semicircular bulging without notches or other bulges above it ( ►Figs. 2A B ); 3) bulging with lobulation (visually altered circular anatomy of the organ, noting bulging shaped like an irregular semicircle, with notches or other bulges) (►F i g .3 A ,B ,C ); 4). alteration of the mucosa (enanthema, Fig. 1 Fold thickening. J Coloproctol Vol. 43 No. 1/2023 © 2023. Sociedade Brasileira de Coloproctologia. All rights reserved. Association between Altered Endoscopic Findings and Endometriosis Pfuetzenreiter et al. 37 edema, unusual coloration, and/or increased vasculariza- tion) ( ►Fig. 4 ); and 5) obstruction of the rectum and/or distal sigmoid (probe unable to pass through the rectum or distal sigmoid) ( ►Fig. 5 ). The patients referred to the department for TRUS or rectosigmoidoscopy underwent distal sigmoid colon and rectum preparation with two applications of 130 mL of a solution containing sodium phosphate monobasic (160 mg/mL) þ sodium phosphate dibasic (60 mg/mL) via the rec - tum; the first application was performed the night preceding the exam, and the second application was performed 1 hour before the exam. For patients referred for colonoscopy, the preparation of the entire colon and rectum included a low- residue liquid diet and two bisacodyl tablets (5 mg) the day before the examination. On the day of the procedure, the preparation was completed with the ingestion of a mannitol solution (500 mL of 20% mannitol with 500 mL of water, orange juice, isotonic, or similar beverage) and, if necessary, rectal lavage with 500 to 1,000 mL of 0.9% saline solution, repeating the procedure until two clear liquid rectal dis- charges occurred. The patients who ful filled the inclusion criteria were provided with a questionnaire and invited to Fig. 2 (A) Bulging without nodules. ( B) Bulging without nodules. Fig. 3 (A) Bulging with nodules. ( B) Bulging with nodules. ( C) Bulging with nodules. Fig. 4 Changes in the mucosa. Fig. 5 Obstruction. J Coloproctol Vol. 43 No. 1/2023 © 2023. Sociedade Brasileira de Coloproctologia. All rights reserved. Association between Altered Endoscopic Findings and Endometriosis Pfuetzenreiter et al.38 participate in the study. Those who agreed to participate signed the consent form and had their concerns, if any, addressed. The endoscopic examinations of the distal sigmoid and rectum were all performed by the same endoscopist, who had performed over 2,000 colonoscopies. After the endo- scopic examination, ultrasound examination was conducted by the hospital ’s physician, who had performed over 3,000 TRUS procedures and who was blinded to the endoscopic findings of the already-sedated patients. The procedures were performed using Olympus, Fujinon and/or Hitachi-Aloka devices (Olympus Corporation, Tokyo, Japan; Fuji film, Tokyo, Japan; Hitachi Aloka Medical Ltd, Tokyo, Japan). After data collection, the clinical and endoscopic variables were stratified, and sensitivity and speci ficity were calculat- ed. The positive predictive value (PPV), negative predictive value (NPV), and accuracy were also calculated with a confidence interval (CI) of 95%.

The present study targeted 53 patients enrolled between August 4, 2014, and September 4, 2015. Of the 53 patients, 3 were excluded: 2 did not consent to participate and 1 had incomplete colon preparation. Therefore, 50 patients (age: 21–51 [mean: 35.8 /C6 7.2] years) were included in the analysis. The most frequently reported symptoms were chronic pelvic pain ( n ¼ 29; 58.0%) and abdominal pain ( n ¼ 27; 54.0%). Thirty-six patients (72.0%) exhibited normal colonoscopic findings; the other 14 (28%) were strati fied based on our endoscopic variables as follows: 5 patients (10%) with fold thickening, 5 (10%) with bulging without nodules, 3 (6%) with bulging with nodules, and 1 (2%) with changes in the mucosa. According to the TRUS findings, 33 (66.0%) patients had suspected endometriosis, but only 14 (28%) had endometri- otic lesions in contact with the rectum or sigmoid, in the following proportion: rectum (6 patients, 12%) and sigmoid (8 patients, 16%) ( ►Table 1 ). ►Table 2 shows the demographic and clinical character- istics of the 14 patients with intestinal endometriosis: age, symptoms, endoscopic findings, history of pelvic surgery, presence of free fluid in the cavity, location of the foci of intestinal endometriosis, and the degree of in filtration in the wall of the sigmoid colon or rectum. In 9 of the 14 patients, it was possible to evaluate the circumferential involvement of the colon or rectum, distrib- uted as follows: 1/8 of the circumference (1 patient), 1/4 (2 patients), 1/3 (4 patients), and 1/2 (2 patients). The correlation of the endoscopic findings with the pres- ence of endometriosis, regardless of location, provided the following results ( ►Table 3 ): prevalence of 66.0% (95%CI: 51.0–78.8%), sensitivity of 36.4% (95%CI: 20.4 –54.9%), speci- ficity of 88.2% (95%CI: 63.6 –98.5%), PPV of 85.7% (95%CI: 57.2–98.2%), NPV of 41.7% (95%CI: 25.5 –59.2%), accuracy of 54.0% (95%CI: 39.3 –68.2%), positive likelihood ratio of 3.1 (95%CI: 0.8 –12.3), negative likelihood ratio of 0.7 (95%CI: 0.5–1.0), and area under the receiver operating characteristic (ROC) curve of 0.623 (95%CI: 0.508 –0.738). The results shown in ►Table 4 were obtained by crossing the endoscopy data with the presence of endometriosis in the rectum or distal sigmoid and were as follows: prevalence of 28.0% (95%CI: 16.2 –42.5%), sensitivity of 78.6% (95%CI: 49.2–95.3%), speci ficity of 91.7% (95%CI: 77.5 –98.3%), PPV of 78.6% (95%CI: 49.2 –95.3%), NPV of 91.7% (95%CI: 77.5 – 98.3%), accuracy of 88.0% (95%CI: 75.7 –95.5%), positive like- lihood ratio of 9.43 (95%CI: 3.0 –28.8), negative likelihood ratio of 0.2 (95%CI: 0.1 –0.6), and area under the ROC curve of 0.851 (95%CI: 0.733 –0.942). The presence of an endometriosis lesion and the degree of infiltration in the sigmoid or rectum in patients who dis- played alterations during the endoscopic evaluation are described in ►Table 5 . It is important to note that the endoscopic changes and the ultrasound findings were locat- ed at the same distance from the anal verge. In addition, the endoscopic images ( ►Figs. 1 , 2, 3 and 4) that yielded 91.7% (95%CI: 77.5 –98.2%) speci ficity for intestinal endometriosis in the rectum or sigmoid. The endoscopic and ultrasonographic alterations were marked using the distance between the anal verge and the endometrial deposit, con firming that the endoscopic alter- ations found were the same as those present in the ultrasound.

Efforts regarding early diagnosis of EDT are valuable because of its importance in reproductive-aged women, the dif ficulty of its diagnosis, the cost associated with the diagnosis and/or treatment, and particularly the decline in the quality of life of affected patients. Therefore, this study demonstrates the importance of thorough evaluation of the distal sigmoid and rectum in women of childbearing age who present with symptoms associated with deep EDT and are referred Table 1 Location and in filtration of endometriosis foci diagnosed by transrectal ultrasound: Correlation between the endoscopic findings n% Main focus of endometriosis Rectum 6 18.2 Sigmoid 8 24.2 Other location 19 57.5 Infiltration Serosa 1 3.0 Muscularis propria 6 18.2 Submucosa 7 21.2 Without in filtration 19 57.6 J Coloproctol Vol. 43 No. 1/2023 © 2023. Sociedade Brasileira de Coloproctologia. All rights reserved. Association between Altered Endoscopic Findings and Endometriosis Pfuetzenreiter et al. 39 for colonoscopy, with emphasis on speci fic endoscopic alter- ations that may be associated with endometrial deposits, to enable an early diagnosis. The characteristics of the population in this study were similar to those described in previous literature. The patients were aged 21 to 51 (mean 35.8 /C6 7.2) years, which is in line with the age associated with a higher incidence of EDT. 5–7 The most common symptoms observed in the study were similar to those of other studies, 4,7,8 with chronic pelvic (58%) and abdominal (54%) pains being the most frequent. Table 2 Demographic and clinical characteristics of the 14 patients with intestinal endometriosis included in the study: Correlation between the endoscopic findings and intestinal endometriosis in the distal sigmoid and rectum, as con firmed via transrectal ultrasound in São Paulo in 2014 to 2015 ( n ¼ 50) Nr. of patient Age Symptoms Pelvic surgery Colonoscopy Free fluid Location of endometriosis Infiltration 54 7 A b d o m i n a l þ pelvic pain Bulging with nodules No Sigmoid Submucosa 11 46 Abdominal þ pelvic pain Fold thickening Yes Sigmoid Muscularis propria 13 34 Infertility and abdominal þ pelvic þ fundus of the pouch pain Bulging Yes Sigmoid Muscularis propria 14 36 Infertility and pelvic pain Bulging with nodules No Sigmoid Submucosa 18 26 Pelvic pain Normal No Rectum Serosa 19 29 Pelvic þ fundus of the pouch pain Cesarean section Bulging No Rectum Muscularis propria 26 34 Abdominal pain Bulging with nodules Yes Sigmoid Mucosa 28 44 fertility and abdominal þ fundus of the pouch pain Bulging with nodules Yes Rectum Muscularis propria 30 40 Pelvic þ abdominal pain Changes in the mucosa No Rectum Submucosa 34 38 Pelvic þ abdominal þ fundus of the pouch pain and intestinal bleeding Cesarean section Bulging Yes Sigmoide Submucosa 35 37 Pelvic pain Bulging Yes Sigmoid Muscularis propria 42 33 Infertility and abdominal pain Normal No Sigmoid Submucosa 47 32 Abdominal pain Thickening No Rectum Submucosa 50 40 Pelvic þ abdominal pain Cesarean section Normal No rectum Muscularis propria Table 3 Results of endoscopy and transrectal ultrasound: Correlation between the endoscopic findings and intestinal endometriosis in the distal sigmoid and rectum, as con firmed via transrectal ultrasound in São Paulo in 2014 to 2015 ( n ¼ 50) Endoscopy Transrectal ultrasound – endometriosis Total No Yes n( % ) n( % ) n( % ) Normal 15 (30) 21 (42) 36 (72) Altered 2 (4) 12 (24) 14 (28) Total 17 (34) 33 (66) 50 (100) Table 4 Results of endoscopy and transrectal ultrasound of the patients with intestinal endometriosis: Correlation between the endoscopic findings and intestinal endometriosis in the distal sigmoid and rectum, as con firmed via transrectal ultrasound in São Paulo in 2014 to 2015 ( n ¼ 50) Endoscopy Transrectal ultrasound – intestinal endome- triosis Total No Yes n( % ) n( % ) n( % ) Normal 33 (66) 3 (6) 36 (72) Altered 3 (6) 11 (22) 14 (28) Total 36 (72) 14 (28) 50 (100) J Coloproctol Vol. 43 No. 1/2023 © 2023. Sociedade Brasileira de Coloproctologia. All rights reserved. Association between Altered Endoscopic Findings and Endometriosis Pfuetzenreiter et al.40 The endoscopy results revealed that 36 (72.0%) patients had normal findings, and the other 14 (28%) were strati fied according to the endoscopic variables. It was, therefore, observed that mucosal involvement in endometriosis was a rare event, as described in the literature. The results of TRUS showed a prevalence of endometriosis of 66% (33 patients) in the study population, likely due to the fact that the sample comprised those with a previous diag- nosis of or symptoms strongly suggestive of EDT. The patients were strati fied into two groups. One group comprised patients with EDT but with the focus distant from the rectum or sigmoid: the other group comprised patients with EDT adhered to or in contact with the rectum or distal sigmoid. We diagnosed 14 patients with EDT adhered to or in contact with the rectum or sigmoid, resulting in an incidence rate of intestinal EDT of 28% ( ►Table 4 ), a fact, again, explained by the characteristics of the study population. ►Table 5 describes the characteristics of the patients with endometriotic lesions in the rectum or sigmoid and shows that all presented with chronic abdominal and/or pelvic pain as symptoms, suggesting that intestinal foci are, in fact, associated with a higher incidence of pain in these patients. The observed endoscopic changes were fold thickening, bulging, bulging with nodules, and mucosal changes. No patient presented with obstruction of the sigmoid or rectum. Infiltration of the serosa, muscularis propria, submucosa, and mucosa was observed, but it was not possible to estab- lish a relationship between the degree of in filtration and endoscopic findings due to the low sample size representing each variable. The analysis of the data regarding the presence of EDT and its location showed a low sensitivity of endoscopy for the diagnosis of EDT in the pelvic cavity (only 36.4%), which suggests that endoscopic examination is not indicated for the diagnosis of pelvic EDT. However, the data on speci ficity (88.2%) and PPV (85.7%) demonstrate that endoscopy does present some association with EDT in this location. The analysis of the relation between the presence of intestinal EDT and the changes evaluated in this study (endoscopic variables) yielded better results: a sensitivity of 78.6%, speci ficity of 91.7%, PPV of 78.6%, and NPV of 91.7%. These confirm that in the present study, the changes detected in the endoscopic assessment were strongly associated with intestinal EDT in the rectum and distal sigmoid. Among patients with endoscopic alterations, three exhib- ited false positive results for deep EDT and all three displayed fold thickening on endoscopy. When this variable was ana- lyzed individually, five cases were detected, two with endo- metriosis in the rectum or sigmoid and three false positives. This suggests that if the variable fold thickening is excluded from the analysis, a table with more speci fic endoscopic variables is obtained, albeit with a lower sensitivity for EDT in those segments. The small sample size associated with each variable means that the CIs associated with the sensi- tivity, specificity, and accuracy values speci fic to each endo- scopic variable were too wide-ranging. The study possessed some limitations, the most impor- tant being the small number of existing studies on the subject, which prevented us from performing a statistical calculation to determine the minimum number of patients, thereby prompting us to conduct an initial study with 50 patients. The fact that data collection was performed at an endoscopy department that specializes in colonoscopy and TRUS, with a signi ficant number of patients referred to the department already having a diagnosis of deep EDT, was critical for the results obtained. It is important to note that all of the tests were performed by the same two endoscopists with experience in cases of deep EDT, a fact that possibly affected the final result.

Endoscopic changes detected in the distal sigmoid colon and rectum were correlated with the presence of EDT in these segments, as con firmed using TRUS. Considering the results and limitations of the study, it can be suggested that colonoscopies performed in patients, with pelvic and/or chronic abdominal pain should include Table 5 Patients with endoscopic changes and correlation with transrectal ultrasound : Correlation between endoscopic findings and intestinal endometriosis in the distal sigmoid and rectum, as con firmed via transrectal ultrasound in São Paulo in 2014 to 2015 ( n ¼ 50) Nr. of patient Age Endoscopic change

TRUS/ infiltration 5 47 Bulging with nodules Submucosa 11 46 Fold thickening Muscularis propria 13 34 Bulging without nodules Muscularis propria 14 36 Bulging with nodules Submuocsa 19 29 Bulging without nodules Muscularis propria 25 39 Fold thickening Without in filtration/ without endometriosis 26 34 Bulging with nodules Mucosa 28 44 Bulging without nodules Muscularis propria 30 40 Changes in the mucosa Submucosa 33 51 Fold thickening Without in filtration/ with endometriosis 34 38 Bulging without nodules Submucosa 35 37 Bulging without nodules Muscularis propria 43 29 Fold thickening Without in filtration/ without endometriosis 47 32 Fold thickening Submucosa J Coloproctol Vol. 43 No. 1/2023 © 2023. Sociedade Brasileira de Coloproctologia. All rights reserved. Association between Altered Endoscopic Findings and Endometriosis Pfuetzenreiter et al. 41 a thorough examination of the rectum and distal sigmoid, focusing on the alterations described in the present study. If some of these changes are detected, an examination for the confirmation of intestinal EDT should be requested. Future studies focusing on these endoscopic changes in different populations and involving larger sample sizes are required to con firm these results. However, the information reported herein is relevant and should be disseminated among colonoscopists both in training and in practice. Conflict of Interests The authors have no con flict of interests to declare.

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