Lesion size and location in deep infiltrating bowel endometriosis: Correlation with gastrointestinal dysfunction and pain

Daria Pashkunova: Project development, data collection, and manuscript writing. Ezgi Darici: Manuscript writing. Birgit Senft: Statistical analysis. Attila Bokor: Project development, data collection, and manuscript writing. Theresa Hudelist: Data collection. Ayman Tammaa: Data collection. Gernot Hudelist: Project development, data collection, and manuscript writing. All authors commented on the manuscript. All authors read and approved the final manuscript.

The Institutional Review Board at Hospital St. John of God approved the study on January 20, 2017 (reference number 2017/1‐BB).

A total of 162 consecutive patients underwent surgery for deep colorectal endometriosis between April 2017 and May 2022. Eleven patients were not included since they did not opt to take part in the study leaving 151 patients for the final analysis. The baseline characteristics of the patients included in this study are described in Table  1 . Preoperative LARS scores are depicted in Table  2 . When investigating a possible correlation between lesion size and GI dysfunction described by LARS‐like symptoms, no statistical correlation was observed ( r  = 0.04, p  = 0.314, Figure  1 ). Since only six women presented with colorectal DE lesions below 1 cm in diameter (#Enzian C1), #Enzian C1 and #Enzian C2 were combined. However, no significant correlation to LARS scores was detected ( p  = 0.611). Furthermore, LAVD and GI dysfunction reflected by LARS scores did not reveal a significant correlation ( r  = 0.108, p  = 0.185, Figure  2 ). Preoperative LARS scores in patients with symptomatic colorectal deep endometriosis (DE). Abbreviations: LARS, low anterior resection syndrome; SD, standard deviation. Correlation between low anterior resection syndrome (LARS) and #Enzian compartment C (rectum). Correlation between anatomical localization of bowel deep endometriosis (DE) and low anterior resection syndrome (LARS) scores. Likewise, no statistically significant difference was observed between NRS scores of dyschezia, dyspareunia, and dysmenorrhea and lesion size ( p  = 0.440, p  = 0.136, and p  = 0.221, respectively; Figure  3 ). Additionally, no statistically significant correlation was found between LAVD and dyschezia ( r  = 0.013, p  = 0.892), dyspareunia ( r  = 0.087, p  = 0.395), or dysmenorrhea ( r  = −0.031, p  = 0.705). Correlation of dyschezia (Numeric Rating Scale [NRS] scores) and #Enzian C compartment. Concomitant DE involvement of the vagina and/or rectovaginal space (RVS), documented as #Enzian compartment A was observed in 80/151 (53%) patients, while DE of the sacrouterine and/or cardinal ligaments/parametrium reflected by #Enzian compartment B was observed in 140 (92.7%) patients. Both compartments were affected in 79 patients (52.3%). Involvement of #Enzian compartment A and/or #Enzian compartment B was neither found to have an impact on the severity of preoperative dysmenorrhea ( p  = 0.128) or dyschezia ( p  = 0.493) nor on LARS scores ( p  = 0.078) but showed a trend toward affecting GI function ( p  = 0.078). However, a positive correlation was observed for DE affecting the vagina/RVS (#Enzian compartment A) and/or sacrouterine ligaments (#Enzian compartment B) and the severity of preoperative dyspareunia ( p  = 0.035; Figure  4 ). The presence or absence of preoperative hormonal treatment within 3 months prior to surgery neither showed an influence on LARS scores ( p  = 0.402) nor dysmenorrhea ( p  = 0.263) or dyschezia ( p  = 0.487). Correlation of low anterior resection syndrome (LARS) scores and dyschezia with #Enzian compartment A and/or B.

In the present study, we investigated a possible association between the size and anatomical location (LAVD) of colorectal DE and GI dysfunction and pain symptoms. We neither observed a correlation between size of colorectal DE and GI dysfunction or pain symptoms nor a correlation between LAVD and these parameters. However, a positive correlation was observed between the presence of vaginal DE (#Enzian compartment A) and/or DE of the sacrouterine ligaments (#Enzian compartment B) and the severity of preoperative dyspareunia ( p  = 0.035). Furthermore, we observed a trend for an association between additional DE involvement in these anatomical compartments and GI dysfunction. So far, there are only limited data on the association between the anatomical extent of DE and pain symptoms such as dysmenorrhea, dyspareunia, dysuria, or dyschezia. In a previous study by Montanari et al, 6 the authors found a correlation between the severity of dyspareunia and dyschezia and lesion size in the respective #Enzian compartments B and C. However, in the study by Montanari et al., the Spearman's correlation coefficient of 0.127 for compartment B and 0.334 for compartment C only indicated a weak correlation for these variables. This finding suggests that while the presence of DE in the posterior compartment does cause dyspareunia, the size of the lesion may only have a limited impact on the severity of symptoms. 6 This is supported by the observation of the present work where a significant correlation was observed between dyspareunia and posterior and/or lateral compartment DE (#Enzian A and/or B sites). Another study by Abrao et al. analyzed the progression of DE over time in 164 consecutive endometriosis patients retrospectively and reported a direct correlation between the severity of dyschezia and the length of the bowel lesion ( p  = 0.047). Moreover, dyspareunia was more severe in patients with higher estimated bowel circumference involvement ( p  = 0.037). 7 Our findings do not support this observation which may on one hand be explained by the fact that we did not use sonography as a measuring tool but obtained measurements from surgical specimens which may be more accurate as a gold standard test. It has been proposed that digestive complaints reported by women with DE infiltrating the rectosigmoid could be explained by several mechanisms: cyclic micro‐hemorrhages, inflammation of the bowel wall fixation of the rectum, and the increased prevalence of dolichocolon and rectal stenosis. 3 This is supported by the presence of LARS‐like symptoms in women with untreated colorectal DE. Reh et al. reported that 18.6% of the patients with bowel DE presented with a major LARS and 27.8% with a minor LARS presurgically compared to 2.1% and 9.4% of control patients. 4 Possible explanations of our findings demonstrating a lack of a positive correlation between extent and location (LAVD) of colorectal DE and GI dysfunction are multiple: Firstly, GI function may be influenced by the irritation of autonomic nerves innervating the bowel. This irritation may be attributed to the inflammatory changes present in various pelvic organs and locations affected by DE not necessarily limited to the rectum. Secondly, pelvic adhesions caused by DE may additionally affect bowel mobility and thereby function. 19 This condition may cause irregular angulations of the digestive tract, which again can impair stool progression and result in GI symptoms. In contrast, a larger non‐fixated lesion without any abnormal distortion may manifest with milder symptoms. This is supported by our observation of a trend towards increased rates of bowel dysfunction in women with additional DE in #Enzian A and/or B compartments which is commonly associated with reduced mobility and fixation of the bowel to these structures. Furthermore, GI symptoms observed in patients with endometriosis have been documented to occur with a similar frequency as gynecological pain symptoms, regardless of the presence or absence of colorectal DE. 20 Maroun et al. found that while 90% of women diagnosed with endometriosis reported gastrointestinal (GI) symptoms, intestinal involvement was only verified in 7.5% of the patients, suggesting that GI symptoms are predominantly unrelated to bowel involvement. 20 Moreover, in the present study, we did not investigate the coexistence of adenomyotic lesions. In the presence of adenomyosis symptoms such as dysmenorrhea, dyspareunia, non‐cyclic pelvic pain, and bladder and GI pain have been observed more frequently. 21 Finally, dolichocolon, which is regarded as a causative factor of chronic abdominal pain, constipation, and bloating, has been observed with high prevalence in women with colorectal DE. 22 As a consequence, the presence of dolichocolon may also contribute to GI dysfunction independent of DE lesion size and location. The strengths of the present study are the prospective nature and the high quality of endometriosis ultrasound scans and surgeries performed as demonstrated in previous studies. Furthermore, the use of the #Enzian classification allows for a more accurate description of the disease extent which is in contrast to previous works investigating the influence of DE size and anatomical localization and patient's symptoms. 8 , 23 , 24 The relevant limitations of this study are as follows: firstly, the general complexity of bowel dysfunction and the multitude of contributing factors (i.e., adenomyosis, the possible influence of the degree of anatomical stenosis which was not evaluated in the present work) which have not been fully elucidated to date but may additionally contribute to respective symptoms. Secondly, we did not fully reach the number of patients suggested by the a priori power analysis (151 instead of 153) and do question why a relevant number of women did not opt to be included in this study. In summary, the results of the present study suggest that GI dysfunction and pain symptoms do occur irrespective of anatomical extent and location (LAVD) of colorectal DE in women with bowel endometriosis. However, DE additionally affecting the vagina/rectovaginal space and/or the sacrouterine ligaments/parametrium (#Enzian compartments A and/or B) may contribute to worsening of bowel dysfunction and are associated with increased rates of dyspareunia.

The present work does not demonstrate a correlation between colorectal DE lesion size and anatomical location (LAVD) and GI dysfunction or intensity of dyschezia and dysmenorrhea. Involvement of additional vagina/rectovaginal space (#Enzian compartment A) and/or sacrouterine ligaments/parametrium (#Enzian compartment B) has a significant impact on the degree of dyspareunia in women with colorectal DE. These findings should be considered in clinical decision‐making processes, especially in patients for whom colorectal surgery is considered for treatment of bowel endometriosis.

Deep colorectal endometriosis (DE) affects 5%–12% of women diagnosed with DE. 1 Women suffering from DE frequently report gastrointestinal (GI) dysfunction. 2 Within this, over 60% of these patients report dyschezia and about 50% cyclic constipation. 3 In addition, several studies have shown that colorectal DE also causes features that are similar to postsurgical low anterior resection syndrome (LARS), so‐called LARS‐like symptoms. Although the relation between preoperative GI symptoms and LARS scores is scarce due to a lack of normative data, it has been previously reported that LARS‐like symptoms are present in 27.8% (minor LARS) and 18.5% (major LARS) of patients with untreated colorectal DE. 4 In symptomatic patients, a possible association between the localization of the endometriotic lesions and the type and intensity of symptoms has been discussed. 5 , 6 Rocha et al. examined the influence of the number of anatomical compartments affected by DE on the severity of pain symptoms. Dysmenorrhea and dyschezia were found to be correlated with DE of the posterior compartment. 5 A retrospective study by Abrao et al. evaluated the progression of bowel endometriosis and related pain symptoms over time. Patients with severe dyspareunia exhibited a greater circumference of colorectal DE nodules ( p  = 0.037) and those with increasing dyschezia were observed to be positively correlated with increased length of colorectal nodules ( p  = 0.047). 7 The #Enzian classification classifies colorectal DE in three severity grades referring to the lesion's largest diameter. 8 There appears to be a significant correlation between the involvement of specific #Enzian compartments affected by DE and intensity of pain symptoms. 6 , 9 However, to which extent the size of bowel DE lesions does affect the degree of GI dysfunction and dyschezia has not yet been established. Only a few studies evaluated the association of pain symptoms with the endometriotic lesion size affected by DE. 5 , 6 In the present work, we aimed to investigate how far colorectal DE lesion size and their anatomical location (LAVD) affect GI dysfunction reflected by LARS‐like symptoms and the intensity of preoperative pain symptoms.

The authors have no conflicts of interest to declare.

In this prospective cohort study, women scheduled for surgery for symptomatic colorectal DE (documented as #Enzian compartment C) by either nerve‐vessel sparing full‐thickness segmental resection (NVSSR) or full‐thickness discoid resection (FTDR) at the Hospital St. John of God Vienna and the Rudolfinerhaus Private Clinic Vienna from April 2017 to May 2022 were investigated. The primary outcome of the present study was the correlation between colorectal DE lesion size and location (LAVD) and GI function impairment, as measured by the LARS score. The secondary outcomes were possible associations between colorectal DE lesion size and location (LAVD) and pain intensity, assessed by the NRS score. Moreover, the influence of concomitant involvement of other anatomical sites (vagina and/or rectovaginal space (RVS), documented as #Enzian compartment A, and/or cardinal ligaments/parametrium reflected by #Enzian compartment B) on severity of symptoms was investigated. Patients were included with the diagnosis of DE as demonstrated by transvaginal sonography (TVS), performed by G.H., expert‐level sonographer (EFSUMB level III). Exclusion criteria were history of psychiatric disorders, previous surgery for DE, acute or subacute mechanical obstruction by DE causing ileus, malignancy, or chronic inflammatory bowel disorders as well as inability to undergo TVS. Lesion length, uni‐ or multifocality, and lesion height as measured by LAVD as well as the presence of other DE sites were determined within 2 months prior to surgery based on the International Deep Endometriosis Analysis group (IDEA) consensus and the #Enzian classification. 8 , 10 , 11 , 12 Other sonographic findings of DE lesions were similarly described, including compartment A, which encompasses the vagina, retrocervical area, and rectovaginal space, and compartment B, including sacrouterine and cardinal ligaments as well as the pelvic side wall. All surgical procedures were performed by one main gynecological surgeon (G.H.) in a multidisciplinary team setting consisting of two colorectal surgeons (B.D and T.B) and one urological surgeon in two hospitals. The primary indication for surgery was quality of life–reducing pain not responding to conservative treatments and/or infertility. In all institutions, the goal of surgical treatment was to remove all macroscopically evident endometriotic foci while preserving and/or enhancing fertility. In patients with bowel DE >3 cm in diameter as well as in patients with multiple, that is, more than one bowel lesion, NVSSR was performed. 13 , 14 FTDR was performed for lesions <3 cm in diameter. Initially, all procedures were performed laparoscopically. Surgical steps of NVSSR and FTDR have been described previously. 15 The height (LAVD) of colorectal DE was assessed intraoperatively, while its length was assessed following resection by using sterile measuring tape on the specimen and consequently subclassified in three severity stages reflected by #Enzian classification: #Enzian C1 includes lesions below 1 cm in longitudinal diameter; #Enzian C2 lesions from 1 to 3 cm; and #Enzian C3 lesions refer to lesions extending 3 cm in length. 8 Sigmoidal lesions (FI) were included in the grading system. Histological proof of DE was obtained on a routine basis. 13 LAVD was equally assessed intraoperatively. DE of vagina, rectovaginal space, sacrouterine ligaments, and pelvic side wall was likewise described using #Enzian classification. Clinical characteristics including age, body mass index (BMI), gravidity, parity, and previous surgical treatments were recorded. Preoperative hormonal treatment within 3 months prior to surgery was assessed in each patient, as it could have a potential influence on the severity of preoperative symptoms. Potential pre‐existing GI dysfunction in patients was assessed using the LARS questionnaire, which was completed up to 1 week prior to surgery. Patients were requested to select responses that best described their daily lives over the past 4 weeks. The LARS questionnaire was primarily designed to assess the bowel function of patients with rectal cancer after undergoing low anterior resection (LAR) but has also been used to assess bowel function after radical resection of bowel endometriosis. 16 This questionnaire consists of five questions, covering a range of probable bowel problems, such as incontinence, urgency, frequent bowel movement, and altered stool consistency. Answers are summed up resulting in three main subgroups: no LARS (0–20 points), minor LARS (20–29 points), and major LARS (30–42 points; Appendix  S1 ). 12 Pain symptoms, in particular dysmenorrhea, dyspareunia, and dyschezia, were assessed using Numeric Rating Scale (NRS), in which the patient selects a whole number (0–10) to describe the pain intensity. Pain assessment was conducted simultaneously with LARS scores, reflecting likewise last 4 weeks. 17 (Table  1 ). STROBE criteria were followed for reporting. 18 The study was approved by the local IRB (Institutional Review Board at Hospital St. John of God; reference number 2017/1‐BB/date:20.01.2017). Baseline characteristics of patients undergoing surgery for colorectal deep endometriosis (DE). Note : Data are presented as mean ± SD. Abbreviations: BMI, body mass index; NRS, Numeric Rating Scale. Assuming a rather small correlation with a power of 0.8 and a probability of error of 5%, the power analysis using G*Power resulted in a sample size of 153 patients. All parameters were not distributed normally except age. Descriptive statistics for metric variables are given with mean values and standard deviations, and categorical data are presented with frequencies and percentages. The normal distribution was checked using the Kolmogorov–Smirnov test and Shapiro–Wilk test as well as visually using a histogram. The variables LARS preoperative and all NRS scales showed significant deviations from the normal distribution in both tests; all p ‐values were in the range <0.001. Mann–Whitney U test was used for the comparison of non‐normally distributed parameters. Correlations between ordinal or metric non‐normally distributed data were tested using Spearman correlation. To investigate the impact of concomitant involved compartments (vagina and/or rectovaginal space (RVS), documented as #Enzian compartment A, and/or cardinal ligaments/parametrium reflected by #Enzian compartment B), one‐sided p‐value was performed for statistical testing, given the implausibility that the inclusion of DE lesions other than colorectal could have a positive impact on preoperative symptoms. All statistical analyses were performed using SPSS 28 (SPSS Inc., Chicago, Illinois, USA) software program. A value of p  ≤ 0.05 was considered to be statistically significant.

Appendix S1.