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Intestinal endometriosis amongst other extra-pelvic endometriosis foci presenting as acute/subacute bowel obstruction in women of reproductive age: a retrospective case series study

Abstract

Background

This study aimed to investigate the prevalence and clinicopathological correlates of intestinal endometriosis, amongst other extra-pelvic endometriosis foci, presenting as bowel obstruction in general surgery practice.

Methods

A total of 23 female patients (mean ± SD age: 34.9 ± 6.5 years) who underwent abdominal surgery for acute bowel obstruction and received histopathological diagnosis of endometriosis were included in this retrospective case-series study. Data on patient characteristics, obstetric history, preoperative laboratory and imaging findings, preoperative provisional diagnosis, type of surgical intervention and the pathological diagnosis, and postoperative outcomes were recorded.

Results

Definitive diagnoses on histopathological work-up involved intestinal endometriosis (52.2%), scar endometriosis (26.0%), ovarian endometriosis (13.0%) and inguinal endometriosis (8.7%). Postoperative complication, reoperation and recurrence rates were 8.7%, 8.7%, and 13.0%, respectively. Intestinal endometriosis, when compared to other extra-pelvic endometriosis foci (scar and inguinal), was associated with significantly higher preoperative platelet counts (332.0(284.0-528.0)vs. 239.0(223.0-370.0) 103/µL, p = 0.010), lower albumin levels (4.0(2.7–4.7) vs. 4.5(4.2–4.9) g/dL, p = 0.029), higher rates of preoperative CT utilization (91.7% vs. 0.0%, p < 0.001) and emergent surgery (83.3% vs. 0.0%, p = 0.001) and longer LOS (median 4.5 (1.0–26.0) vs. 1.0(1.0–1.0) days, p = 0.001) along with a non-significant tendency for higher postoperative complication (16.7% vs. 0.0%) and ICU stay (25.0% vs. 0.0%) rates.

Conclusion

Our findings revealed intestinal endometriosis, predominantly in the terminal ileum/appendix, was the most common extra-pelvic cause of acute bowel obstruction. The scar endometriosis, inguinal endometriosis and ovarian endometriosis appeared to be other potential but less prevalent aetiologies in this setting.

Peer Review reports

Background

Endometriosis is a benign gynaecological disease defined as the presence of endometrial tissue outside the uterine cavity, predominantly in the pelvic compartment (ovaries, external surface of the uterus, fallopian tubes, ligaments of the uterus) [1,2,3].

However, endometriosis foci can also be found at the level of intraperitoneal (large intestine, small intestine, and appendix) or extraperitoneal (inguinal region, abdominal scars after gynaecological surgery and caesarean section) extra-pelvic organs [3,4,5].

The bowel is the most affected extra-pelvic location, and intestinal endometriosis comprises 3–37% of all endometriosis cases, which involves rectosigmoid junction (50–90%) in most cases, followed by ileocecal region, appendix and other colon and small bowel segments [2, 6,7,8].

The acute bowel obstruction due to intestinal endometriosis foci is a very rare event with a reported prevalence of 0.1–0.7%, while it often requires urgent medical attention due acute abdominal inflammation and bowel obstruction or perforation [2, 3, 8,9,10,11,12].

Indeed, surgical intervention is considered to be both diagnostic and therapeutic in patients with bowel obstruction secondary to intestinal endometriosis, due to non-specificity of clinical manifestations, biological tests and imaging modalities in diagnosing intestinal endometriosis [13, 14]. Therefore, the final diagnosis is obtained only after surgical resection and histopathological examination [13,14,15,16].

Besides intestinal endometriosis, endometriosis foci in extraperitoneal organs such as inguinal region or abdominal scars after gynaecological surgery and caesarean section may also cause bowel obstruction, in accordance with the extrinsic aetiologies of bowel obstruction (adhesions, hernia) [3,4,5, 17].

The pathophysiology of intestinal endometriosis is complex with a multifaceted interplay of factors, while bowel obstruction in the setting of intestinal endometriosis remains largely unexplored due to its rarity with limited data in the literature, mostly including case reports [2, 3, 5, 8, 9, 12, 13, 15, 16, 18].

This retrospective case series study aimed to investigate the prevalence and clinicopathological correlates of intestinal endometriosis, amongst other extra-pelvic endometriosis foci, presenting as acute bowel obstruction in general surgery practice.

Methods

Study population

A total of 23 female patients (mean±SD age: 34.9±6.5 years) who underwent abdominal surgery for acute or subacute bowel obstruction and received the diagnosis of endometriosis after histopathological examination of resection specimens, local excisions and biopsies were included in this retrospective case-series study. Women of reproductive age (15–49 years) who underwent emergent abdominal surgery for acute bowel obstruction (ileus plus acute abdomen) and those who underwent elective abdominal surgery for subacute bowel obstruction (ileus without acute abdomen - not resolved under observation and medical treatment) were included in the study.

This study was conducted in accordance with the ethical principles stated in the “Declaration of Helsinki” and approved by the Bursa Uludag University Clinical Research Ethics Committee (Date of Approval: 08.07.2024, Protocol No: 2024-10-6). Written informed consent was obtained from each subject.

Assessments

Data on patient characteristics (age, body mass index [BMI], the American Society of Anaesthesiologists [ASA] score), obstetric history (previous pregnancy and delivery method, gravidity, parity, use of assisted reproductive technology [ART], previous endometriosis history), preoperative laboratory and imaging findings, preoperative provisional diagnosis, timing of surgery (elective, emergent), type of surgical intervention and the pathological diagnosis related to type of endometriosis were recorded in each patient. Postoperative outcome parameters included the length of hospital stay (LOS), intensive care unit (ICU) stay, postoperative complications, and follow up data on stoma closure, reoperation, and recurrence rates (based on detection of further endometriosis lesions).

Statistical analysis

Statistical analysis was performed using IBM SPSS Statistics for Windows, version 22.0 (IBM Corp., Armonk, NY). Chi-square (χ2) test was used for the comparison of categorical data, while Mann-Whitney U test was used to compare two independent non-normally distributed variables. Data were expressed as mean ± standard deviation (SD), median (min-max) and percent (%) where appropriate. p < 0.05 was considered statistically significant.

Results

Demographic and obstetric characteristics

Mean ± SD age of female participants was 34.9 ± 6.5 years (range, 26.0 to 47.0 years). Previous pregnancy was evident in 14(60.9%) patients, and the delivery method was caesarean section (C/S) in 30.4% of them. A previous history for endometriosis was noted in 8(34.8%) patients (Table 1).

Table 1 Demographic, obstetric, preoperative and postoperative characteristics (n = 23)

Preoperative work-up and provisional diagnoses

Preoperative imaging included computerized tomography (CT) in 52.2% of patients, while 47.8% of patients were evaluated with preoperative ultrasound (US) (Table 1).

Preoperative imaging revealed no specific findings other than intestinal distension (on US) and transition zones related to ileus (on CT). Overall imaging findings were consistent with the diffuse bowel wall thickening on individual intestinal segments and narrowing of the intestinal lumen, the implantations on bowel wall in rectosigmoid region, cecum, appendix and distal ileum, the transition zone in the obstructed areas and the adhesion particularly between the rectum and vaginal fornix.

The most common preoperative provisional diagnoses were obstructive ileus (21.7%), mass at C/S incision site (21.7%), acute abdomen (17.4%), and inguinal mass-hernia (17.4%) (Table 1).

Surgery and pathological diagnosis

Overall, emergent and elective surgery rates were 52.2% and 47.8%, respectively. The final pathological diagnosis included intestinal endometriosis in 12(52.2%) patients, scar endometriosis in 6(26.0%) patients, ovarian endometriosis in 3(13.0%) patients and inguinal endometriosis in 2(8.7%) patients (Table 1).

Postoperative outcome

Median LOS was 4.0 days (range, 1.0 to 26.0 days), while 13.0% of patients needed ICU stay. Postoperative complications (superficial wound infection) were noted in 2(8.7%) patients. During median 11.7 months (range, 0.3 to 82.7 months) of follow-up, the reoperation (due to prolonged postoperative ileus), stoma closure and recurrence (extra-pelvic endometriosis foci as confirmed by surgical pathology) rates were 8.7%, 21.7% and 13.0%, respectively (Table 1).

Case-wise details

Case-wise details on patient characteristics, preoperative provisional diagnoses, surgical intervention, pathological diagnosis and postoperative outcome are provided in Table 2.

Table 2 Case-wise details

Distribution of study parameters by endometriosis foci

Overall, there was a tendency for increased likelihood of certain clinical, surgical and outcome variables across endometriosis foci, including intestinal endometriosis (utilization of preoperative CT, emergent surgery, ICU stay, prolonged LOS, postoperative complication and recurrence), scar endometriosis (previous C/S delivery, recurrence and reoperation) and ovarian endometriosis (utilization of preoperative CT, lower preoperative albumin levels and platelet counts, emergent surgery, prolonged LOS) (Table 3).

Table 3 Study parameters by endometriosis foci

Study parameters with respect to extra-pelvic endometriosis foci

Intestinal endometriosis, when compared to other extra-pelvic endometriosis foci (scar and inguinal), was associated with significantly higher preoperative platelet counts (median(min-max) 332.0(284.0-528.0) vs. 239.0(223.0-370.0) 103/µL, p = 0.010), lower albumin levels (median(min-max) 4.0(2.7–4.7) vs. 4.5(4.2–4.9) g/dL, p = 0.029), higher rates of preoperative CT utilization (91.7% vs. 0.0%, p < 0.001) and emergent surgery (83.3% vs. 0.0%, p = 0.001) and longer LOS (median(min-max) 4.5 (1.0–26.0) vs. 1.0(1.0–1.0) days, p = 0.001) along with a non-significant tendency for higher rate of postoperative complications (16.7% vs. 0.0%) and ICU stay (25.0% vs. 0.0%) (Table 4).

Table 4 Study parameters with respect to extra-pelvic endometriosis foci

No significant difference was noted between intestinal endometriosis and inguinal/scar endometriosis groups in terms of patient age, BMI, preoperative US utilization, and previous history for endometriosis (41.7% and 25.0%, respectively) (Table 4).

Discussion

Our findings emphasize consideration of extra-pelvic endometriosis, particularly the intestinal endometriosis, as a potential cause of bowel obstruction leading to abdominal surgery in general surgery practice. Surgical pathology remains the primary diagnostic option. Other than higher platelet counts and lower serum albumin levels and higher prevalence of nulliparous women in case of intestinal endometriosis, patient profile or preoperative laboratory investigation was not helpful in differentiating subtypes (intestinal, inguinal or scar) of extra-pelvic endometriosis. Intestinal endometriosis was associated with higher rates of emergent surgery, ICU stay and postoperative complications and a longer LOS, compared to other extra-pelvic endometriosis foci (scar or inguinal).

Acute bowel obstruction secondary to intestinal endometriosis is a diagnostically challenging condition due to nonspecific clinical presentation and lack of specific laboratory or imaging measures [2, 3, 12]. Therefore, definitive diagnosis is based on histopathological confirmation after surgical resection [2, 3, 12, 13, 19, 20].

The intestinal endometriosis (57.7%) was the leading pathological diagnosis in our cohort, followed by scar endometriosis (23.1%), ovarian endometriosis (11.5%) and inguinal endometriosis (7.7%). Previous studies also revealed the bowel as the most affected extra-pelvic site which comprises 3–12% of extra-pelvic endometriosis, mostly in the rectosigmoid junction (50–90%) [6, 9, 14, 21, 22]. However, while the intestinal involvement in endometriosis is common, it rarely causes acute intestinal obstruction and, in this setting, endometriosis has a predilection to obstruct the terminal ileum/appendix which almost always necessitates surgical resection [5, 7, 8, 12, 23,24,25,26]. Notably, terminal ileum/appendix appeared to be predominantly affected region in our patients with intestinal endometriosis, which also explains the presentation characteristics such as bowel obstruction, perforation, acute appendicitis and intussusception, unique to terminal ileum/appendix involvement [13, 22]. Higher platelet counts and lower serum albumin levels in our patients with intestinal endometriosis are typical findings in the setting of bowel obstruction, which reveal systemic inflammation and impaired nutritional status [27].

Indeed, the rectosigmoid involvement is suggested to reflect a tendency for more extensive pelvic and intestinal involvement in patients with known genital endometriosis (ovarian endometriosis in particular), rather than being a frequent site of involvement in case of an incidentally detected isolated intestinal endometriosis [24, 28]. Pathological confirmation of ovarian endometriosis in our three cases seems notable in this regard, supporting the consideration of ovarian endometriosis as a marker for more extensive pelvic and intestinal disease [28]. Notably, higher utilization of preoperative CT, lower preoperative albumin levels, high prevalence of emergent surgery and prolonged LOS were common to both intestinal endometriosis and ovarian endometriosis in our case-series. In fact, given the association of ovarian endometriosis with an increased risk of pelvic and intestinal involvement, involvement of ovaries exclusively by endometriosis without coexistent disease elsewhere is considered a rare event [28]. This emphasizes the likelihood of other pelvic or intestinal disease to be left untreated that if a surgeon identifies and treats only ovarian endometriosis [28].

In a systematic review of 97 case studies involving 107 patients with bowel occlusion due to endometriosis, locations of occlusive endometrial foci were reported to be ileum in 38.3% of the cases, rectosigmoid in 34.5% of the cases, ileocecal junction and the appendix in 14.9% of the cases, and rectum in 10.2% of the cases [3]. Out of 107 patients, 26(24.3%) were previously diagnosed with endometriosis, while the rest (75.7%) were diagnosed with endometriosis in the context of an intestinal occlusion event [3].

Likewise, previous history of endometriosis was evident in one-third of our study population, similarly in intestinal endometriosis and inguinal/scar endometriosis groups. Other studies reported a previous diagnosis of endometriosis in at least half patients with intestinal endometriosis, besides the isolated bowel endometriosis [13, 29,30,31,32,33]. Hence, while most cases with intestinal endometriosis are diagnosed as well as treated with surgery consistent with the nonspecific presentation of the disease, knowledge of pre-existing endometriosis via detailed patient history may help in making clinical decisions for patients [13, 32, 33].

Clinical presentation of extra-pelvic endometriosis is considered highly variable depending on the organ affected, while it is particularly difficult to diagnose pre-operatively in case of intestinal endometriosis due to asymptomatic or non-specific presentation with considerable overlap with other clinical gastrointestinal conditions [13, 19].

The preoperative diagnoses (obstructive ileus, acute abdomen, appendicitis, pelvis/psoas abscess, perforation) in our intestinal endometriosis group, support the consideration of intestinal endometriosis to be commonly misdiagnosed as irritable bowel syndrome, acute appendicitis or diverticulitis, inflammatory bowel disease, intestinal carcinoma, or ovarian pathology [13, 34, 35]. Hence, definitive diagnosis is often delayed due to variable presentation and symptom overlap prompting the gastrointestinal diagnostic workup and is often made incidentally during surgery or following complications such as bowel obstruction, perforation, or ileocecal intussusceptions [15, 21, 31, 32, 36, 37].

Bowel wall infiltration of endometrial-like tissue leads to activation of inflammatory response that promotes the secretion of cytokines and chemokines, creating a microenvironment that contributes to the development of the ectopic endometrial tissue by disrupting normal apoptosis and promoting localized angiogenesis and neuroagiogenesis, particularly in case of deep infiltrating endometriosis [38, 39]. Accordingly, while deep infiltrating endometriosis can cause intestinal stenosis or occlusion in severe cases, the bowel complaints could be caused not only by occluding bulky lesions but also by angulation of the bowel, wall inflammation or neurological issues [40, 41]. The creation of a mass effect in the intestinal lumen or wall, and the pro-fibrotic nature of endometriosis lesions leading to adhesion or stricture formation are considered likely to be responsible for intestinal obstruction, particularly in case of ileocecal involvement, which necessitates complete diagnostic laparoscopy to rule out multicentric foci and almost always warrants surgical resection [3, 15, 16, 42,43,44]. Nonetheless, the drawback of diagnostic phase of laparoscopy (risk of additional intestinal injury) or open approach in identifying occult lesion is notable in this regard, limiting the detection of any bowel lesion [45].

Although histopathologic confirmation with surgery remains the gold standard for diagnosis, transvaginal sonography, magnetic resonance imaging (MRI), double contrast barium enema and CT colonography are the key non-invasive imaging modalities for initial assessment to aid in surgical treatment in intestinal endometriosis. Nonetheless, non-invasive imaging may be inconclusive given the large range of potential sites of deep intestinal endometriosis [13, 46,47,48,49].

Right hemicolectomy, ileocecal resection, anterior resection with double-barrel ostomy were the leading surgical interventions in our cases with intestinal endometriosis, supporting the consideration of segmental resection and primary anastomosis as the favourable technique in these patients, which allows for a radical removal of intestinal endometriosis and minimizes future risk of recurrences, improves pelvic pain, intestinal symptoms and quality of life [13, 42].

Likewise, in a systematic review of 97 studies involving 107 patients with bowel occlusion due to endometriosis the reported surgical interventions included those performed for ileal obstruction (ileocecal resections, right hemicolectomies, ileal resections, ileotransversostomy), ileocecal obstruction (right hemicolectomies and ileocecal resections) and rectal obstruction (anterior rectal resection in three patients, and rectosigmoid resection), sigmoid colon obstruction (Hartman procedures, hemicolectomy with colostomy, sigmoid colectomies with primary anastomosis, and one sigmoid colostomy) [3].

In a meta-analysis of 49 studies examining surgical treatment of bowel endometriosis, overall endometriosis recurrence rate was estimated to be 10%, with a recurrence rate of 5.8% in case of bowel resection with anastomosis [50]. Overall rates for postoperative complication (11.5%), reoperation (7.7%) and recurrence (11.5%) in our patients seem notable in this regard, which appeared to differ across the type of extra-pelvic endometriosis foci, with higher likelihood of postoperative complications and recurrence in case of intestinal endometriosis and higher rate of recurrence and reoperation in case of scar endometriosis.

Hence, our findings emphasize that extra-pelvic endometriosis foci should be suspected in women presenting with bowel obstruction, particularly the intestinal endometriosis in nulliparous women and the scar endometriosis in those with previous C/S delivery [3, 13, 14, 22, 51]. Although reasons for this were not addressed in the current study, increased likelihood of endometriosis in nulliparous women may relate to the risk of increased number of lifelong ovulatory cycles, besides the adverse impact of endometriosis on fertility of the affected women [52,53,54,55].

Ovarian endometriosis was previously described in patients with ileal, ilecocecal or sigmoid colon obstructions, while rectal endometriosis was associated with extensive lesions in the uterus and ovaries [2, 3, 56]. Hence, the likelihood of ovarian endometriosis to be associated with intestinal disease should also be considered, alongside the higher risk of emergent surgery and prolonged LOS in case of both intestinal and ovarian endometriosis. Accordingly, it seems critical to consider endometriosis a gastrointestinal pathology as much as a gynaecological one, and the clinical awareness of gastroenterology physicians and surgeons in this regard seems essential for obtaining optimum patient outcomes through timely diagnosis and appropriate surgical planning, reducing patient morbidity and improving quality of life [16, 31, 57].

The small sample size, which reduces generalizability and possibility of having robust statistical results in endometriosis foci subgroup analyses, and the study’s retrospective nature, which may introduce selection bias, are the major limitations of our study. In addition, the absence of a control group makes it difficult to contextualize the findings or determine causality. Nevertheless, despite these certain limitations, given the rarity of bowel obstruction due to endometriosis, presenting detailed analysis of endometriosis foci in a case-series comprising 23 patients with abdominal surgery for bowel obstruction, our findings make a valuable contribution to the existing literature.

Conclusions

In conclusion, our findings revealed intestinal endometriosis, predominantly in the terminal ileum/appendix, was the most common extra-pelvic cause of acute bowel obstruction. The scar endometriosis, inguinal endometriosis and ovarian endometriosis appeared to be other potential but less prevalent aetiologies in this setting. Accordingly, extra-pelvic endometriosis foci, particularly intestinal endometriosis in nulliparous women and scar endometriosis in those with previous C/S delivery, should be considered as a rare differential in acute bowel obstruction presentations by women of childbearing age in the general surgery practice. Our findings also emphasize the potential association of intestinal and ovarian endometriosis with increased risk of emergent surgery and prolonged LOS, and the higher risk of postoperative recurrence in case of intestinal and scar endometriosis. In this regard, further large-scale studies are necessary to identify clinical risk factors or potential biomarkers for specific endometriosis foci in order to develop diagnostic tools which would possibly reduce the need for surgeries and improve patient quality of life.

Data availability

The data supporting the findings of this study are available within the article, further inquiries can be directed to the corresponding author.

Abbreviations

ART:

Assisted reproductive technology

ASA:

American Society of Anesthesiologists

BMI:

Body mass index

C/S:

Cesarean section

CT:

Computerized tomography

ICU:

Intensive care unit

LOS:

Length of hospital stay

MRI:

Magnetic resonance imaging

SD:

Standard deviation

US:

Ultrasound

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EG: Conceptualization; methodology; data curation; formal analysis; investigation; project administration; writing-original draft preparation. OI: Methodology; Data curation; formal analysis; investigation. NU: Methodology; Data curation; formal analysis; investigation. AS: Data curation; formal analysis; investigation. MS: Data curation; formal analysis; investigation. TY: Methodology; investigation; writing- review & editing; supervision.

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Gurluler, E., Isik, O., Ugras, N. et al. Intestinal endometriosis amongst other extra-pelvic endometriosis foci presenting as acute/subacute bowel obstruction in women of reproductive age: a retrospective case series study. BMC Surg 25, 12 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12893-024-02755-y

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