Intestinal endometriotic nodules with a length greater than 2.25 cm and affecting more than 27% of the circumference are more likely to undergo segmental resection, rather than linear nodulectomy

The prevalence of intestinal involvement is estimated at 45–56% of patients with deep infiltrating endometriosis [ 1 , 2 ]. Studies with questionnaires applied to patients with intestinal deep infiltrating endometriosis show that there is an 85–95% improvement in quality of life after surgery [ 3 – 7 ]. Given this improvement, when we opt for surgical treatment of intestinal endometriosis, different surgical techniques are available depending on the characteristics of the intestinal nodule, such as longitudinal length, circumference of the affected intestinal loop, depth and distance from the anal verge [ 8 ]. Among surgical techniques for intestinal endometriosis, one can choose nodulectomy by "shaving" [ 8 – 10 ], "mucosal skinning" [ 10 ], discoid resection [ 11 – 16 ], linear nodulectomy [ 17 – 22 ] or segmental resection [ 17 , 20 , 23 , 24 ]. Although the final decision on which surgical technique is to be used , is always established during the intraoperative period; some studies suggest that the characteristics of the intestinal nodule (longitudinal length, circumference of the intestinal loop affected, layer affected and distance from the anal verge) obtained from a preoperative TVUSBP can help the surgeon decide which intestinal endometriosis resection technique is more likely to be performed [ 25 ]. Regarding the longitudinal length of the intestinal nodule, there is a tendency to perform segmental resection in single nodules larger than 3 cm [ 9 , 13 , 25 ]. Nodulectomy of larger nodules may lead to stenosis of the stapling area; for this reason, some authors suggest that intestinal nodules that infiltrate more than the internal muscular layer or when it affects more than 40% of the circumference of the loop, it should be subjected to segmental resection [ 13 ]. Regarding the distance from the anal verge of the intestinal endometriotic nodule, it is suggested that in excision cases of low intestinal lesions—defined as lesions located less than 5–8 cm from the anal verge—the rate of postoperative complication, with dehiscence or fistula or low anterior rectal resection syndrome, increases from 3–7% to 20% [ 14 , 15 , 17 ]. Evaluating which surgical technique is more likely to be used before surgery, accordingly to TVUSBP, is useful in preoperative planning and advising the patient about morbidity and complications related to each technique [ 8 , 18 ]. The focus of this study is to provide information using preoperative TVUSBP that helps the surgeon in choosing the surgical technique to be used in the treatment of intestinal endometriosis: linear nodulectomy or segmental resection.

Of the 111 records analyzed, 63 met all inclusion and exclusion criteria. Of these 63 patients, 27 underwent linear nodulectomy, and 36 underwent segmental resection. The median age of the patients was 37 years with a range of 27–51 years for the nodular nodulectomy technique and 34 years with a range of 28–46 years for segmental resection; there was no significant difference between the techniques performed ( Table 1 ). Note: The data is expressed as the median (range) (if non normal distribution) or n (percentage). The median surgical time was 90 minutes with a range of 35–180 minutes for the group undergoing linear nodulectomy and 120 minutes with a range of 60–240 minutes for the segmental resection group. The p-value of 0.005 indicated a significant difference ( Table 1 ). The median duration of symptoms before surgery was 36 months with a range of 1–240 months for linear nodulectomy and 48 months with a range of 12–288 months for surgical resection, with no evidence of a significant difference between the groups ( Table 1 ). Of the patients undergoing linear nodulectomy, only 7.4% were asymptomatic, but complained about infertility, and 81.4% had at least one of the symptoms of pelvic/lumbar pain, such as dysmenorrhea, dyspareunia, low back pain or chronic pelvic pain. Approximately 3.7% of patients had hematochezia, and 7.4% had menorrhagia or metrorrhagia, as shown in Fig 6 . The data is expressed in percentages. In patients undergoing segmental resection, 2.8% were asymptomatic. Approximately 80.5% had at least one symptom of pelvic/lumbar pain, such as dysmenorrhea, dyspareunia, low back pain or chronic pelvic pain. Regarding intestinal symptoms, 27.7% had at least one intestinal symptom, such as anal pain, dyschezia, diarrhea, pencil-thin stools, constipation, flatulence or hematochezia. Only 5.5% of the patients had symptoms of dysuria or recurrent urinary tract infection, and 8.3% had complaints of menorrhagia or metrorrhagia, as shown in Fig 6 . We did not find a significant difference between the techniques with respect to symptoms. Regarding the presence of extraintestinal endometriosis, we found greater involvement in patients undergoing intestinal endometriosis excision with the segmental resection technique (36,1%) compared to the linear nodulectomy technique (11.1%), with statistical difference (p = 0.050). Patients submitted to the first technique, showed involvement of the appendix, sigmoid, descending colon, caecum, ileum, left uterine artery and abdominal wall. Among the patients undergoing linear nodulectomy, there was involvement of the left uterine artery, piriformis muscle, left pudendal nerve, left sciatic nerve and right hypogastric nerve. The extent of the disease was assessed using the AFSr criteria while reviewing the surgery videos. Severe endometriosis (stage IV) was present in 69.8% of cases; however, there was no significant difference between the resection techniques performed. We analyzed the presence of endometriosis in other extraintestinal locations (ovaries, round ligament, bladder, vagina, ureter, retrocervical area and uterosacral ligaments) related to the intestinal surgical technique; however, we found no significant difference. The analysis of the receiver operating characteristic (ROC) curve showed a cutoff point of 10.5 cm for the distance from the anal verge. Values below this cutoff point were associated with the segmental resection technique, while values above it were associated with linear nodulectomy. Sensitivity and specificity were calculated for each distance from the anal verge, and for this cutoff value, we found a sensitivity of 76.7% and specificity of 53.6% ( Table 2 ) ( Fig 7 ). A positive predictive value (PPV) of 63.9% and a negative predictive value (NPV) of 68.2% were found. The median for the distance from the anal verge for the nodulectomy group was 11.25cm (Range 8–19) and, for the segmental resection group, it was 10cm (Range 6–17), with p value 0.033. As additional data, there was a significant difference in the relationship of the distance of the endometriosis nodule from the anal verge and with the presence of vaginal endometriotic nodules, with greater distances from the anal verge for intestinal nodules that did not have associated vaginal nodules (median of 12.9 cm) and smaller distances (median of 8.4 cm) when the vagina was involved, with p = 0.001. For the longitudinal length of the intestinal nodule, the ROC curve showed that a value of 2.25 cm was the best equilibrium point between sensitivity (88.9%) and specificity (92%) ( Table 2 ) ( Fig 7 ). A positive predictive value (PPV) of 94.1% and a negative predictive value (NPV) of 85.1% were found. Thus, linear nodulectomy would be used for nodules smaller than 2.25 cm, and segmental resection would be used for nodules larger than 2.25 cm. The median for the longitudinal length of the intestinal nodule for the nodulectomy group was 1.2cm (range 0.3–3.5) and, for the segmental resection group, it was 3.9cm (range 1–17), with p value <0.001. When evaluating the presence of endometriotic nodules in the vagina, there was a significant difference, with smaller intestinal nodule diameters (median of 2.3 cm) in cases in which there was no vaginal involvement and larger diameters (median of 4.9 cm) when there was endometriosis of the vagina, with p = 0.019. Application of ROC curve analysis to the percentage of circumference of the loop affected by the intestinal endometriotic nodule identified a value of 27% as the best equilibrium point between sensitivity (72.1%) and specificity (78.9%) ( Table 2 ) ( Fig 7 ). A positive predictive value (PPV) of 88% was found as well as a negative predictive value (NVP) of 55%. Values higher than this cutoff point of 27%, were associated with the segmental resection technique, while lower values were associated with the linear nodulectomy technique. The median for the percentage of circumference of the loop affected by the intestinal endometriotic nodule for the nodulectomy group was 19% (range 12–40) and, for the segmental resection group, it was 35% (range 12–70), with p value <0.001. Regarding the affected intestinal layer, in the segmental resection technique, 69.4% of cases had mucosal and submucosal involvement, and in the linear resection technique, 93.1% of cases exhibited involvement of the muscular and serosa layers, with p<0.001 showing statistical significance. No intraoperative complications were observed; however, we observed postoperative complications. In the group undergoing linear nodulectomy, one patient (3.7%) developed leakage, which was treated with cavity drainage and antibiotic therapy. Another patient (3.7%) developed stenosis of the anastomosis area, and after failure of dilation attempts, she underwent a new intestinal surgery using the segmental resection technique. In the group undergoing segmental resection, four patients (11.1%) had complications: in one patient (2.7%), a fistula occurred, which resolved without the need for reoperation; in another, urinary retention occurred, which was resolved with instructions to the patient, urinary catheterization and use of bethanechol; transrectal bleeding followed by leakage was observed in another patient, with no progression to fistula; and another patient exhibited difficulty urinating, which was resolved with physical therapy. There was no significant difference between the groups with respect to complications ( Table 1 ).

Transvaginal ultrasonography with bowel preparation for endometriosis mapping was shown to be an effective tool to assist decision-making about the surgical technique to be performed for the treatment of intestinal endometriosis. After obtaining the ROC curve, we determined cutoff values for the longitudinal length of the intestinal nodule (2.25 cm), circumference of the loop (27%) and distance from the anal verge (10.5 cm) separating the segmental resection and linear nodulectomy techniques. Regarding the intestinal layer, we observed that the depth reaching the muscular layer on TVUSBP is more closely associated with the linear nodulectomy technique, while the depth to the submucosal layer is more closely associated with the segmental resection technique.

The study was approved by the ethics committee of the institution (Comitê de Ética em Pesquisa em Seres Humanos da Santa Casa de Misericórdia de São Paulo) under protocol number CAAE 59860916.1.0000.5479, with authorization to review medical records and videos of surgeries. The consent form for this specific study was not obtained because in our institution an informed consent is not necessary for retrospective studies without evaluation, contact, questionnaire or interviews with the patients. In addition once interned at the institution, patients provide written consent to have data of their medical records used in research. All data was fully anonymized before the authors accessed them. One year after the surgical procedure, patients had no clinical follow up at the institution and continue with routine care at primary health care units. In 2019, a cross-sectional observational study was performed and submitted to statistical analysis. This study included 111 medical records of patients diagnosed with endometriosis who underwent videolaparoscopy surgery from April 2010 to November 2014. These patients had clinical symptoms, complaints of infertility or physical examinations that would suggest endometriosis. They were submitted to ultrasonography, performed by a single examiner, suggesting intestinal endometriotic nodules—or images that the examiner can presume intestinal adhesion is present. All patients underwent videolaparoscopy surgery for intestinal endometriosis resection with endometriosis confirmation in anatomopathological examination. The surgeons were aware of the USTVBP result. We included in this study all patients submitted to surgical treatment of bowel endometriosis in our department, by the same surgical team (P.A.A.R., H.S.A.A.R. and F.C.M.R.), during the specified period (2010–2014) regardless of age, parity, previous hormonal or surgical treatment for endometriosis or associated procedures. All patients had a TVUSBP examination performed by a single radiologist (A.L.A.N.) and their surgeries were recorded on DVD. Histological confirmation of intestinal endometriosis was a mandatory inclusion criteria. The exclusion criteria for the study included: loss of medical records, preoperative diagnosis of endometriosis by another image exam, preoperative TVUSBP performed by another radiologist, intestinal resection not performed, intestinal resection done without the use of stapling; surgeries performed by a different surgical team. Of the 111 medical records, 63 patients met all inclusion criteria and were divided into two groups: 36 undergoing segmental resection and 27 undergoing linear nodulectomy ( Fig 1 ). There were 43 patients excluded for not having intestinal endometriosis infiltration at laparoscopy, 4 patients were excluded for not having intestinal endometriosis confirmed in AP examination and 1 patient was excluded because the surgical technique didn´t use staplers, which might have led to different complications. The variables evaluated were age, preoperative symptoms, duration of symptoms, duration of previous treatment, previous surgeries for endometriosis and intra and postoperative complications. Ultrasonography assessed the following parameters: longitudinal length of the intestinal nodule, circumference of the intestinal loop affected, distance from the anal verge and layer affected by the intestinal nodule. In addition, the presence of ovarian endometrioma, round ligament, bladder, vaginal, ureter, retrocervical and uterosacral ligament endometriosis was assessed [ 26 ]. The surgical data was evaluated by reviewing videos stored on DVD and classified according to the American Fertility Society (AFSr) criteria; the surgical time was calculated (from introduction to removal of the optic device from the abdominal cavity), and intraoperative complications were evaluated. Transvaginal ultrasonography with bowel preparation for endometriosis mapping (USTVBP) was performed according to the protocol of our department [ 19 ] and literature [ 23 , 27 , 28 ]. All examinations were performed by the same examiner (A.L.A.N.). The ultrasound devices used were the GE Voluson S6 (GE Healthcare, Zipf, Austria) or IU 22 (Phillips Healthcare, Eindhoven, Netherlands) with 5-9-MHz transducers. Intestinal deep infiltrating endometriosis lesions were defined as hypoechoic nodular thickening with regular or toothed margins (comet shape) or hypoechoic linear thickening with regular or irregular margins and involvement of the muscular or submucosa layers [ 26 , 28 ] (Figs 2 – 4 ). Deep endometriosis nodule in the anterior wall with involvement up to the inner muscle layer (blue arrows). Deep endometriosis nodule in the anterior wall with circumferential involvement of about 30% (blue arrows). Deep endometriosis nodule in the anterior wall with involvement up to the outer muscular layer (blue arrows). The surgeries were performed by senior surgeons with extensive experience in the treatment of deep infiltrating endometriosis (P.A.A.R., H.S.A.A.R. and F.C.M.R.). The surgeons were aware of the USTVBP result. All surgeries were performed laparoscopically using a high-definition (HD) camera and a Xenon Nova 300 W light source, both from Storz. Access to the abdominal cavity was obtained using the closed technique with a Veress needle, incision of the umbilical scar and subsequent umbilical puncture with an 11-mm trocar. Three accessory punctures were performed with 5-mm trocars in the usual triangular arrangement. CO 2 was used to distend the cavity, and the surgeries were recorded on DVD. The surgeries followed the standard procedure of our institution [ 20 ], including the dissection of the retroperitoneal spaces, isolation of the ureters and nerve preservation. During the surgical procedure, harmonic energy and bipolar energy were used for dissection and coagulation as needed. All extra intestinal foci of endometriosis was removed prior to treatment of the intestinal nodule. In the linear nodulectomy technique, the central portion of endometriosis in which there is infiltration of the intestinal wall was isolated using the serous layer shaving technique [ 16 , 20 ]. This allowed the isolation of the point with intestinal infiltration, and reduced the removed area of the healthy intestinal wall. A locking forceps was used for traction of the intestinal nodule, and a linear stapler was introduced through the trocar located in the right iliac fossa; the linear stapler was positioned below the lesion ( Fig 5 ). A 29-mm probe was inserted rectally to assess and confirm that there was no intestinal lumen stenosis, before and/or after stapling [ 20 – 22 ]. 1- In the first step, the linear stapler was positioned 45 degrees from the axis of the intestinal lumen. 2- Next, consecutive staples (usually 2 or 3) were placed below the lesion and parallel to the axis of intestinal lumen. 3- To finish resection, the last stapler was positioned 45 degrees from the axis of the intestinal lumen to completely remove the endometriosis nodule. 4a- final aspect of the surgical specimen (inverted trapezoid shape). 4b- final aspect of the stapling line with a 29mm probe rectally inserted. In the segmental resection technique, transverse linear stapling was performed caudally to the intestinal nodule. Next, the rectosigmoid segment was externalized through an incision in the right iliac fossa for resection under direct view. The proximal margin of the rectosigmoid was then prepared for anastomosis with a circular stapler (CDH33, Ethicon-Brazil). The incision was closed, and a 12-mm trocar was inserted so that the intestinal anastomosis procedure could be finalized by laparoscopy [ 20 , 24 ]. Although the USTVBP can preoperatively define the dimensions of the lesions and suggest one technique or another, the final decision on the surgical technique to be performed (linear nodulectomy or segmental resection) was stablished, intraoperatively, by performing a rectal lumen diameter test, with the insertion of a 29 mm diameter rectal probe. If lumen stenosis was observed, the segmental resection technique was chosen. To determine the sample size, a pilot study was conducted with 10 patients, evaluating the length of the intestinal nodule in preoperative TVUSBP. This data was used to detect a statistically significant difference between the two groups at a significance level of 5% (alpha error) and a test power of 99.9%. The calculated sample size for each group (linear nodulectomy and segmental resection) was 27 cases, with a median length of 1.8 cm and SD of 0.8. The difference in the mean intestinal nodule length between the two techniques was 2.9 cm. Fisher’s exact test was used to evaluate the qualitative variables. To test the normality of quantitative samples, we used the Kolmogorov-Smirnov test or the Shapiro-Wilk test. Variables followed a non normal distribution and are expressed as the median and minimum and maximum variation (range). The Mann-Whitney test was used to evaluate the correlations between numerical variables and categorical variables. The Kruskal-Wallis test was used to compare quantitative variables from three or more groups of data. The chi-square test was used to evaluate the associations between categorical variables, i.e., all qualitative variables, including the ordinal variables. For correlations between numerical variables, Spearman’s correlation coefficient was applied. For inferential analyses, a significance level (α) of 5% was adopted. ROC curves were constructed to determine the cutoff points of the following variables: diameter of the intestinal nodule, circumference of the loop affected and distance from the anal verge.