Clinical, diagnostic, and surgical characteristics of colorectal endometriosis

Pilyugina E.I., Khilkevich E.G., Mel'nikov M.V., Chuprynin V.D.

1) Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, Moscow, Russia; 2) N.I. Pirogov Russian National Research Medical University, Ministry of Health of Russia, Moscow, Russia

Aim. To investigate clinical, diagnostic, and surgical features of colorectal endometriosis.
Materials and methods. We analyzed medical records of 311 patients who underwent surgery for colorectal endometriosis from January 2018 to December 2020 at the Department of General Surgery of the V.I. Kulakov NMRC for OG&P. Clinical evaluation included general clinical examination, TVUS, MRI, and colonoscopy. The method and scale of surgery were determined by the disease's location, the depth and extent of invasion, and the involvement of surrounding structures.
Results. Patients whose findings from TVUS or MRI were insufficient for diagnosis underwent colonoscopy with targeted biopsy of endometriotic lesions [54/311(17.3%)]. TVUS or MRI findings showed endometriotic lesions infiltrating the bowel wall in 136/311 (43.7%) patients. Most often, complaints correlated with the disease location. Rectal bleeding during menstruation was reported by 55/311 (17.6%) patients; 114/311 (36.6%) women complained of bloating during menstruation. These complaints were not present in patients with the endometriotic infiltrate located in the proximal colon or the small intestine. Loose stools were reported by 76/311 (24.4%) patients. Surgical interventions included shaving of bowel wall affected by endometriotic infiltrate [118/311 (37.9%)], resection of affected bowel and anastomosis [161/311 (51.7%)], resection of affected bowel, and colostomy [29/311 (9.3%)], and appendectomy [3/311 (0.9%)].
Conclusion. Colorectal endometriosis is a gynecological disorder showing infiltrative growth, rapid cell proliferation, neoangiogenesis and can mimic malignancy. Endometriotic lesions can be seen only by laparoscopy, but other methods of preoperative examination should not be neglected. This may help better diagnose the disease and guide pre-surgical planning.

Keywords

colorectal endometriosis
colonoscopy
bowel resection
shaving

Endometriosis is a common gynecological disease defined as the presence and growth of ectopic endometrial tissue outside the uterus [1]. Endometriosis affects up to 10% of all reproductive-aged women worldwide [2]. Colorectal endometriosis is infiltrative endometriosis characterized by pronounced fibrosis, obliterating the bowel lumen, and disrupting bowel evacuation function [3, 4]. The prevalence of colorectal endometriosis among all patients with endometriosis ranges from 5.3% to12% [5]. In 90% of cases, endometrioid infiltrate is located in the rectum or sigmoid colon and is accompanied by symptoms such as constipation, diarrhea, dyschezia, tenesmus, and, rarely, rectal bleeding [6].

Initial diagnostic evaluation of colorectal endometriosis involves gynecological examination and digital rectal examination [7]. Early diagnosis of colorectal endometriosis is practically impossible due to the non-specific clinical picture and low sensitivity of transvaginal ultrasound (TVUS), magnetic resonance imaging (MRI), and colonoscopy in the early stages of the disease [4, 8].

Surgical treatment of deep infiltrative colorectal endometriosis is a highly debated topic in operative gynecology. Being the most effective treatment modality, it allows for achieving complete symptom regression but is a rather traumatic intervention. Most commonly, minimally invasive procedures are used to treat colorectal endometriosis. They include two surgical methods, including radical interventions based on resection of the affected bowel segment and relatively more conservative surgery such as shaving of the bowel wall or full-thickness disc-shaped excision without intestinal resection.

Despite their minimal invasiveness, these methods are traumatic for patients. A lot of work is being done to minimize the scale of surgical intervention without reducing its effectiveness. This is influenced not only by the technical skills of surgeons but also by the perioperative training. Fast-track surgery reduces the risk of complications and length of hospital stay, which has significant economic benefits. This technique has been used in our department since 2016 and has shown promising results [9].

The present study aimed to investigate clinical, diagnostic, and surgical features of colorectal endometriosis.

Materials and methods

The study included 311 patients with colorectal endometriosis who were managed at the Department of General Surgery of the V.I. Kulakov NMRC for OG&P from 2018 to 2020. Of them, 190/311 (61%) patients underwent resection of various parts of the large or small bowel, including 29/311 (9.3%) who required a protective colostomy. Also, 118/311 (37.9%) were operated on by the shaving technique in various parts of the colon. In 14/311 (4.5%) patients, the appendix was involved in the endometrioid infiltrate, and 3/311 (0.9%) patients had isolated appendiceal endometriosis, which required appendectomy.

All patients signed informed consent to participate in the study and were recorded according to the standards of the Ethics Committee of Minzdrav of Russia. The study was reviewed and approved by the Research Ethics Committee of the V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia.

Inclusion criteria were female patients aged 18–49 years, informed consent to participate in the study, and colorectal endometriosis.

Exclusion criteria were infectious diseases, malignant neoplasms, acute pelvic inflammatory diseases, severe non-gynecologic pathology, previous six months hormonal therapy for endometriosis.

The presence, location, and extent of colorectal endometriosis was established by taking patients’ clinical history, detailing complaints, gynecological examination combined with the digital rectal examination, TVUS, MRI or computed tomography (CT), colonoscopy, laparoscopy/laparotomy, and histological examination of surgical specimens.

Pelvic ultrasound examination was performed in the Department of Functional Diagnostics of the V.I. Kulakov NMRC for OG&P (Head – A.I. Gus, Dr. Med. Sci.) on Aloka ProSound Alpha 10 (Japan), Toshiba Xario (Japan), using 3.5 and 5.0 MHz transabdominal and transvaginal probes.

MRI was performed in the Department of Radiology of the V.I. Kulakov NMRC for OG&P (Head – Bychenko V.G., Ph.D.) by standard method on MRI scanners including a 3 Tesla Magnetom Verio (Simens Medical Systems, Germany) and a 1.5 Tesla Signa HDxt (General Electric Medical Systems, USA).

Surgical interventions were performed under endotracheal anesthesia using the standard technique in the Trendelenburg position.

Hysteroscopy was performed in all cases for therapeutic and diagnostic purposes using a rigid hysteroscope with an outer diameter of 5 mm from Karl Storz (Germany), such as 30º Hamou I and 30º Hopkins II. The pathomorphological examination was carried out in the Department of Anatomic Pathology, the V.I. Kulakov NMRC for OG&P (Head – Professor A. Shchegolev).

Results and discussion

The age of the patients ranged from 22 to 49 years (mean age 35.03 years). A comparative analysis of the data of TVUS, MRI/CT, colonoscopy, and laparoscopy/laparotomy was carried out based on the extent of endometriosis, the degree of the small or large bowel involvement in the infiltrate, and adhesion severity.

Complaints and physical examination

The primary and leading complaint of patients with colorectal endometriosis affecting the distal colon was, as a rule, defecation disorders (diarrhea, tenesmus, dyschezia) and rectal bleeding with menses. When the infiltrate was located proximally, the complaints were not specific.

Ultrasound examination

In a previous study, the sensitivity of TVUS to detect intestinal endometriosis was estimated as 74.6%, positive predictive value as 77.8%, and negative predictive value as 56.8%. The average diameter of the endometriotic infiltrate was 3.0 cm, according to laparoscopy – 5.1 cm [10].

Magnetic resonance imaging

In the group of patients with cyclic rectal bleeding and clinical presentation of disorders evacuation function the sensitivity, specificity, positive and negative predictive value were 98.6%, 89.4%, 100.0%, and 89.3%, respectively. The average size of the infiltrate was 3.4 cm, according to laparoscopy – 5.4 cm [10].

Colonoscopy

The sensitivity, specificity, positive and negative predictive value were 80%, 95%, 45.76%, and 16.37%, respectively [10].

In 54/311 (17.3%) patients, the results of TVUS or MRI were insufficient to make a diagnosis, and they underwent colonoscopy with targeted biopsy of the lesions. In 136/311 (43.7%) patients, invasion of the intestinal mucosa was established by TVUS or MRI. Most often, complaints correlated with the location of the pathological process. In 42/311 (13.5%) patients, intestinal infiltration to the mucous membrane was confirmed by colonoscopic findings; in 8/311 (2.5%) women, only an inflammatory reaction was found. In 4/311 (1.3%) patients, it was impossible to pass the tip of the colonoscope beyond the infiltrate. The causes included significant stricture in 2/311 (0.6%) and fixation of the intestine to the pelvic wall and its double barrel-like deformity in 2/3 311 (0.6%). Rectal bleeding during menstruation was reported by 55/311 (17.6%) patients; 114/311 (36.6%) patients complained of bloating during menstruation. These complaints were not present in patients with proximal colon or the small intestine infiltrate location. Loose stools were reported by 76/311 (24.4%) patients.

Laparoscopic findings of colorectal endometriosis do not present any difficulties in visualizing endometriotic infiltrates and assess their size and excise them down to healthy tissue. Colorectal endometriosis was found to affect bowel segments from 2.0 to 8.0 cm. As a rule, they were surrounded by sclerotic tissue of dense cartilaginous consistency. Also, infiltrates could cause double barrel-like deformity, fix it to pelvic walls, or be located in several parts of the large and small bowel.

Laparoscopic findings showed that in 192/311 (61.7%), 28/192 (14.6%), 67/311 (21.5%), and 58/311 (18.6%) patients, endometriotic infiltrates were located in the rectum, upper rectal ampulla, sigmoid colon, and rectosigmoid colon, respectively.

Somewhat less frequently, infiltration occurred in the appendix (17/311 (5.5%)), small intestine [6/311 (1.9%)], cecum [5/311 (1.6%)], and ileocecal junction [2/311 (0.6%)]. Also, the infiltrate was found in the ascending colon [1/311 (0.3%)], and infiltrated the cecum mesentery [1/311 (0.3%)].

Patients, depending on complaints, diagnostic workup results, and intraoperative findings, underwent interventions including "shaving" of the intestinal wall affected by endometrioid infiltration [118/311 (37.9%)], resection of the affected bowel segment with the formation of an anastomosis [161/311 (51.7%)] and resection of the affected bowel segment with colostomy [29/311 (9.3%)], appendectomy [3/311 (0.9%)].

"Shaving" of the affected intestine wall was performed when the intestinal patency was not impaired, and according to the colonoscopic findings, no infiltrate was found beyond the serous layer.

Bowel resection was performed in cases when there were visible signs of stenosis (bowel extension proximal to the infiltrate, stricture, and bowel deformation in the infiltrated area), endometriotic infiltration of the bowel wall beyond the serosa, according to colonoscopic findings.

Operation stages:

1. The afferent bowel segment is mobilized along the bowel wall from the border of healthy tissue behind the infiltrate using harmonic scissors or a bipolar LigaSure coagulator.

2. During mobilization, scar tissue retracting the healthy part of the bowel into the infiltrate is dissected.

3. The bowel is mobilized distally to the infiltrate at a distance that will allow the application of a linear stapler outside the infiltrate.

4. Mobilization is carried out with utmost care for pararectal tissues, as close as possible to the bowel wall. Such mobilization aims to minimize the likelihood of complications such as urinary and defecation disorders in the postoperative period.

5. After transection of the distal end of the colon, the proximal end of the colon is taken with intestinal forceps passed through the left trocar.

6. The trocar is removed from the anterior abdominal wall. The wound is extended to 4–5 cm, through which the bowel is brought out to the anterior abdominal wall using a clamp.

7. The cut-off site is additionally treated, and the site is prepared for anastomosis.

8. The bowel is clamped with a Kocher or Mikulich forceps, and the segment with the infiltration is excised.

9. The edges of the proximal bowel are taken on the Alice clamps. The Mikulich clamp is removed, and the twisted purse-string suture is applied through all bowel layers with the obligatory capture of the mucous membrane 2-3 mm from the edge.

10. The head of the circular stapling device is introduced into the bowel lumen.

11. The purse-string seam is tightened.

12. If necessary, apply a U-shaped seam to ensure a snug fit of the tissues.

13. The diameter of the stapler is selected individually according to the diameter of the adductor.

14. Then, the stapler head is lowered together with the bowel into the abdominal cavity.

15. A purse-string suture is applied to the peritoneum of the operating wound, tied to 1 knot, which is fixed with a soft clamp.

16. The abdominal cavity is additionally sanitized with an antiseptic solution. Additional hemostasis is performed.

17. A circular stapler with a sharp spike is inserted into the lumen of the rectal stump.

18. The site for the anastomosis is selected so that the transverse staple suture is excised as much as possible.

19. During perforation, the bowel wall is gently held with a soft clamp at the site of the shaft contour.

20. Under laparoscopic control, the sharp shaft is removed from the abdominal cavity through a 10 mm trocar.

21. Then, the stapler head is connected to the stapler, the bowel axis is monitored, the anastomosis is carefully examined to exclude tissue and organs from entering the suture.

22. The edges of the sutured bowel ends are brought together. Wait 15–20 seconds, then suture and remove the device from the rectum.

23. A No. 20 Foley catheter is inserted into the rectum, and the balloon is inflated to 20–30 ml.

24. The efferent colon is clamped with a soft intestinal clamp proximal to the anastomosis and filled with methylene blue solution through the Foley catheter to control the tightness of the anastomosis.

25. After the test, an intestinal 9–10 mm silicone probe is inserted into the rectum beyond the anastomosis zone at a distance of 6–7 cm.

26. The bowel is additionally washed with saline.

27. The probe is fixed to the perianal skin.

28. Silicone drains are placed in the abdominal cavity through the right trocar opening.

A video of the operation ispresented on the website https://aig-journal.ru/archive.

The sigmoid colostomy was used as a protective measure. It was removed if anastomosis was less than 8 cm from the anus or more than two hollow organs were opened during surgery (29/311 (9.3%)). Also, colostomy was required in cases of anastomotic failure (4/311 (1.3%)) or the formation of a rectovaginal fistula (3/311 (0.9%)).

Appendectomy was performed when the infiltrate was located in the appendix, which was rigid and injected with vessels.

In 7/311 (2.2%) patients, the postoperative period was complicated by bleeding from the anastomotic area. In 6/311 (1.9%), bleeding was stopped using combined endohemostasis (argon plasma coagulation and clipping). In 1/311 (0.3%) patient, relaparoscopy and hemostatic sutures were performed on the anastomotic area. Two out of 311 (0.6%) had intra-abdominal bleeding and underwent re-laparoscopy. She was found to have diapedesis bleeding; hematoma was evacuated, and hemostasis was performed.

In the early postoperative period, anastomotic leakage and bowel perforation in the anastomotic area were diagnosed in 4/311 (1.3%) patients. Restoration of continuity of the gastrointestinal tract was performed in 3-4 months. In the late postoperative period, 3/311 (0.9%) patients developed rectovaginal fistulas. Subsequently, these patients underwent surgical interventions in several stages, including separation of the fistulous opening and reconstructive surgery. Therefore, 7/311 (2.2%) patients required reoperation and colostomy removal.

The early postoperative period was complicated by peritonitis in 6/311 (1.9%) women. They underwent relaparoscopy, sanitation, and drainage of the small pelvis were performed. Also, 2/311 (0.6%) patients had a pelvic abscess.

Subfebrile hyperthermia was observed in 2/311 (0.6%) women in the postoperative period; it had no underlying pathology and resolved after changing the antibacterial drug (from cefazolin to imipenem).

The diagnosis of endometriosis was confirmed by histological examination of the surgical specimens.

This study used well-known methods of diagnosing this disease, from simple to more complex. It started with a gynecological examination combined with the digital rectal examination, then pelvic TVUS and MRI and colonoscopy followed by diagnostic laparoscopy converted into a therapeutic one. The obtained acoustic characteristics of retrocervical infiltrates are widely known and described in many sources [11–13]. Our previous study showed that TVUS has several limitations in assessing the severity of colorectal endometriosis. Diagnostic accuracy is always different and depends on the size and location of the endometrioid lesions, and in colorectal endometriosis is 87.3% [10]. MRI is a relatively informative diagnostic modality providing findings on the degree of invasion of the endometriotic infiltrate into the colon wall [14–17].

The findings of colonoscopy are consistent with the results of other studies [18–20].

Even though the findings of preoperative workup in most cases correspond to the data obtained intraoperatively, laparoscopy remains the most accurate and informative method for diagnosing endometriosis.

The above surgical interventions are very traumatic for patients and require specialized perioperative training according to the Fast-track surgery regimen. Complications of these operations are pretty dangerous and require long-term treatment. Timely diagnosis, optimal preoperative preparation, surgeon's professional qualification, and balanced perioperative management minimize the risk of complications.

Conclusion

Colorectal endometriosis is a gynecological disorder showing infiltrative growth, rapid cell proliferation, neoangiogenesis and can mimic malignancy. Endometriotic lesions can be seen only by laparoscopy, but other methods of preoperative examination should not be neglected. To select the optimal surgical management strategy and avoid possible complications, pelvic ultrasound, MRI, colonoscopy, and laparoscopy with mandatory histological verification of the surgical specimens should be used as well as preoperative preparation of the patient.

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Received 26.04.2020

Accepted 04.05.2021

About the Authors

Ellina I. Pilyugina, 6th Year Student, Pirogov Russian National Research Medical University, Ministry of Health of Russia. Tel.: +7(965)252-14-84.
E-mail: elya13.11.97@icloud.com. 117997, Russia, Moscow, Ostrovityanova str., 1.
Elena G. Khilkevich, Dr. Med. Sci., Obstetrician-Gynecologist at the Surgery Department, V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia.
Tel.: +7(495)438-77-83. E-mail: e_khilkevich@oparina4.ru. ORCID: 0000-0001-8826-8439. 117997, Russia, Moscow, Ac. Oparina str., 4.
Vladimir D. Chuprynin, Ph.D., Head of the Surgery Department, V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia. Tel.: +7(495)438-35-75.
E-mail: v_chuprynin@oparina4.ru. 117997, Russia, Moscow, Ac. Oparina str., 4.
Mikhail V. Melnikov, Ph.D., Head in Clinical Work, Surgery Department, V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia.
Tel.: +7(495)438-78-33. E-mail: m_melnikov@oparina4.ru. 117997, Russia, Moscow, Ac. Oparina str., 4.

For citation: Pilyugina E.I., Khilkevich E.G., Mel'nikov M.V., Chuprynin V.D. Clinical, diagnostic, and surgical characteristics of colorectal endometriosis.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2021; 5: 135-140 (in Russian)
https://dx.doi.org/10.18565/aig.2021.5.135-140

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