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08-05-2017
Case of the Month - MAY
Endometriosis infiltrating the sigmoid colon






Yi Dong*, Barbara Braden**, Christoph F Dietrich***

*Department of Ultrasound, Zhongshan Hospital, Fudan University, 200032 Shanghai, China
**Translational Gastroenterology Unit, Oxford University Hospitals, Oxford, UK
***Med. Klinik 2, Caritas-Krankenhaus Bad Mergentheim, Uhlandstr. 7, 97980 Bad Mer-gentheim

Correspondence
Prof. Dr. med. Christoph F. Dietrich
Medizinische Klinik 2
Caritas-Krankenhaus
Uhlandstr. 7
97980 Bad Mergentheim
Tel:+49 7931 58 2201
Email: christoph.dietrich@ckbm.de


Case report
A 24 year old woman complained of recurrent lower abdominal pain for 6 months. She was referred for colonoscopy. There was no palpable mass on digital rectal examination. Blood chemistry, full blood count, coagulation profile, al-fa-fetoprotein and carcinoembryonic antigen were within normal limits.
Colonoscopy revealed a semi-circular polypoid lesion in the sigmoid colon suggesting malig-nancy [Figure 1].

Transabdominal B-mode ultrasound (BMUS) confirmed a 40 mm sized heterogeneous hy-poechoic lesion infiltrating the sigmoid colon [Figure 2].

Contrast enhanced ultrasound (CEUS) showed a rapidly and heterogeneously enhancing lesion during the arterial and venous phases [Figure 3]. Contrast enhanced colour Doppler ultra-sound confirmed the finding.

Endorectal endoscopic ultrasound of the sigmoid colon revealed transmural extension of the mass and confirmed the transcutaneous finding. The lesion was well vascularized [Figure 2].

Subsequently, the patient underwent laparoscopic sigmoid resection. Microscopic examina-tion disclosed endometrial stroma and gland islands located between muscular fibres, subse-rosa and serosa. The pathology result was reported as extragenital endometriosis. The post-operative period was uneventful.

Discussion
Clinically, intestinal endometriosis is rare and may present a major diagnostic challenge. Here we report a case of transmural endometriosis infiltrating the sigmoid colon and present the findings in endoscopy, ultrasound, CEUS and endoscopic ultrasound.

Definition, etiology and pathogenesis
Endometriosis is defined as the presence of endometrial glands and stroma outside the uter-ine cavity. Extragenital endometriosis can affect all organs including the gastrointestinal (GI) and urinary tract. Extragenital endometriosis occurs in about 8 - 12 % of women with endo-metriosis [(1)]. Endometriosis is detected more frequently in the genital organs and pelvic peritoneum, rarely in the gastrointestinal tract, lung, bladder, greater omentum, surgical scars, mesentery, kidneys, the skin and even nasal cavity. The most common site affected within the gastrointestinal tract is the rectosigmoid junction, followed by the ileum and the appendix [(2, 3)]. Endometriosis involving the mucosa of the intestine is very rare and may lead to diagnostic pitfalls and subsequent mismanagement [(4)]. Deep endometriosis is de-fined as endometriosis involving the muscularis layer [(5)]. Deep infiltrating endometriosis is associated with reactive inflammation of the surrounding area, including proliferation of smooth muscle cells, fibrosis, and adhesions. For optimal management of patients with endo-metriosis involving the sigmoid and/or rectum, it is important to understand the clinical con-text and pre-operative imaging characteristics.

The first laparoscopic approach to intestinal endometriosis has been reported in 1980 [(6)]. The assumed pathomechanism for extragenital endometriosis is retrograde spread as pro-posed by Sampson, which refers to propagation of endometrial cells into the peritoneal cavity through the fallopian tubes during menstruation followed by dissemination to other areas [(7)].

Symptoms
Endometrial tissue implanted into the gastrointestinal tract can cause gastrointestinal symp-toms including abdominal pain, rectal bleeding and dyschezia. Symptoms can be similar to irritable bowel syndrome and may even mimic colonic adenocarcinoma [(8)]. Compared with peritoneal and ovarian endometriosis, intestinal endometriosis is more frequently associated with dysmenorrhea, dyspareunia, noncyclic pelvic pain and infertility [(9, 10)], as well as spe-cific bowel symptoms, including cyclic bowel alterations, dyschezia and rectal bleeding [(2)].

A prospective study performed by Roman et al. [(11)] demonstrated that women presenting with rectal endometriosis were more likely to present various digestive complaints such as cyclic defecation pain and cyclic constipation. If left untreated, progressive endometriosis may result in partial or complete bowel obstruction requiring surgical resection [(12)].

The degree of symptoms may not correlate to the size of the lesions and painful symptoms are not indicative of surgical intervention. Some patients with extensive endometriosis affect-ing the rectosigmoid can be almost asymptomatic [(5)], while others with small lesions can present with severe symptoms. This makes it more difficult to determine the need for inter-vention, especially radical surgery. Evaluating only patients with endometriosis in the rec-tosigmoid, 48% and 84% had also ovarian endometriosis and retrocervical lesions, respective-ly [(13)].

Diagnosis
The diagnosis of intestinal endometriosis is often difficult and delayed since the clinical presentation may be confused with other diseases including inflammatory bowel disease (IBD) or neoplasia (adenocarcinoma, lymphoma). Endometriosis may appear as a cystic, solid, or combined solid-cystic lesion and usually involves the serosa or subserosal layer, although it sometimes can involve all layers of the colon. As the infiltration of the intestinal wall by en-dometriosis rarely involves the mucosa, the conventional endoscopic investigations are of lit-tle help in the definition of intestinal involvement [(14)]. When endometriosis involves the intestinal mucosa, it may cause diagnostic difficulties, especially in endoscopic biopsies. The findings may vary depending on the day of the menstrual cycle, the ratio of stromal and glan-dular elements, and the amount of bleeding and inflammatory response in the surrounding tissue.

The majority of patients with intestinal endometriosis are diagnosed at laparoscopy or lapa-rotomy. Diagnosing intestinal endometriosis in the bowel wall involving the serosa, muscularis propria and submucosa is usually straightforward in resected bowel specimen [(15)].

Pre-surgery evaluation
The clinical examination and history of cycle-related symptoms can only raise suspicion for presence of endometriosis. There is still ongoing debate which imaging technique is the most appropriate method for pre-surgical assessment. According to Sampson’s theory of endome-triosis pathomechanism, endometriosis lesions affect the rectosigmoid starting from the sero-sa, invade towards the lumen of the bowel and finally infiltrate the entire wall. The fibrotic component represents around 80% of the lesions in intestinal endometriosis and therefore, surgical management is more difficult [(1, 16)]. The number and size of the lesions, depth of infiltration, percentage of the intestinal wall circumference infiltrated and lymph node in-volvement need to be considered when planning surgery.

In a literature review, Meuleman et al. [(17)] reported that 95% of patients undergoing bowel resection had bowel serosa involvement; 95% had lesions infiltrating the muscularis while 38% had lesions infiltrating the submucosa and 6% had lesions infiltrating the mucosa.

Imaging findings
It is remarkably difficult to diagnose intestinal endometriosis by conventional imaging meth-ods. Endoscopic and imaging findings may mimic other diseases including colitis [(18)], in-flammatory bowel disease [(19)], solitary rectal ulcer syndrome [(20)], colorectal adenoma, and cancer [(21)]. Diagnosing intestinal endometriosis remains a diagnostic challenge [(15)].

Ultrasound, computed tomography (CT), magnetic resonance imaging (MRI) and colonoscopy can be helpful in localising the pathology. Meuleman et al. [(17)] described that in 59% of the studies analyzed, the pre-operative assessment of bowel endometriosis included barium ene-ma (26%), CT (31%) and/or MRI (28%). Advances in imaging technology and adequate training in image analysis have made it possible to identify characteristics of endometriosis nodules pre-operatively [(1)]. The detailed imaging findings allow us to define and plan the optimal surgical procedure. This permits proper patient counselling and consenting. It facilitates ap-propriate selection of a multidisciplinary surgical team aiming at the best patient outcome [(22)].

Ultrasound characteristics for bowel endometriosis, including transabdominal, transrectal, and transvaginal approaches have been described [(23)]. Diagnostic criteria include a hy-poechoic, irregular-shaped area corresponding to a layer of hypertrophic muscularis propria surrounded by a hyperechoic rim including mucosa, submucosa, and serosa [(24)].

When endometriosis involves the recto-sigmoid, transvaginal ultrasound (TVUS) with bowel preparation is able to define not only the size and number of lesions, but also the depth of invasion into the bowel wall and the distance from the anal verge [(13, 25)].

At MRI, a sensitivity of 84% and specificity of 99% has been reported in 60 patients with intes-tinal involvement [(26)].

Treatment
The best treatment approach for patients with asymptomatic bowel endometriosis is still con-troversial. Asymptomatic patients whose lesions were diagnosed incidentally on radiologic imaging do not generally require surgery. However, large lesions that compromise the lumen of the rectosigmoid, cause severe haemorrhage, or progressive disease should be considered for surgery [(27)]. For asymptomatic patients, the indications for surgery are limited to the risk of bowel obstruction and, possibly, to improve fertility after previous IVF failures. For pa-tients who are not trying to conceive, medical treatment should be the first option [(28)].

Although most patients respond to medical treatment, the recurrence rate is very high after cessation of therapy. Therefore, surgery should be considered first choice treatment, especial-ly in young patients and those with severe symptoms. The recurrence rate after total excision is very low. Surgical treatment provides excellent results, with > 85% of women showing com-plete improvement of symptoms and recurrence rates lower than 5% [(29)].

Prognosis
A review evaluating the effect of conservative surgery for rectovaginal and rectosigmoid en-dometriosis on reproductive function demonstrated that the mean pregnancy rate after sur-gery in all patients who wanted to become pregnant, independent of pre-operative fertility status and IVF performance, was 39%, but the spontaneous pregnancy rate was only 24% [(28, 30)].

The completeness of surgical excision seems to determine the rate of recurrence [(31, 32)],. This was shown when clinical and histological characteristics were examined as possible pre-dictive factors for bowel endometriosis recurrence after laparoscopic segmental bowel resec-tion. Three independent predictor factors, positive bowel resection margins, age < 31 years and body mass index ≥ 23 kg/m2, were also significantly associated with recurrence which was observed in 16% of all patients. The complete excision of bowel endometriosis appears most effective for avoiding recurrence of the disease.

Conclusions
Intestinal endometriosis should be considered in female patients of the reproductive age who present with constipation, gastrointestinal bleeding, nausea, vomiting, cramp-like abdominal pain, diarrhoea and pelvic pain. Although definitive diagnosis of rectosigmoid endometriosis is difficult preoperatively, clinical suspicion and appropriate imaging might prevent extensive surgical procedures with higher morbidity. Contrast-enhanced ultrasound is an efficient non-invasive imaging method without any radiation exposure that supports the early diagnosis of intestinal endometriosis and can assess the vascularisation of endometriosis lesion within the different layers of the intestinal wall.

References
1. Abrao MS, Petraglia F, Falcone T, Keckstein J, Osuga Y, Chapron C. Deep endometriosis infiltrating the recto-sigmoid: critical factors to consider before management. Hum Reprod Update 2015;21:329-339.
2. Remorgida V, Ferrero S, Fulcheri E, Ragni N, Martin DC. Bowel endometriosis: presentation, diagnosis, and treatment. Obstet Gynecol Surv 2007;62:461-470.
3. Rana R, Sharma S, Narula H, Madhok B. A case of recto-sigmoid endometriosis mimicking carcinoma. Springerplus 2016;5:643.
4. Jiang W, Roma AA, Lai K, Carver P, Xiao SY, Liu X. Endometriosis involving the mucosa of the intestinal tract: a clinicopathologic study of 15 cases. Mod Pathol 2013;26:1270-1278.
5. Chapron C, Bourret A, Chopin N, Dousset B, Leconte M, Amsellem-Ouazana D, de Ziegler D, et al. Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions. Hum Reprod 2010;25:884-889.
6. Nezhat C, Hajhosseini B, King LP. Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis. JSLS 2011;15:387-392.
7. Acar T, Acar N, Celik SC, Ekinci N, Tarcan E, Capkinoglu E. Endometriosis within the sigmoid colon/extragenital endometriosis. Ulus Cerrahi Derg 2015;31:250-252.
8. Haggag H, Solomayer E, Juhasz-Boss I. The treatment of rectal endometriosis and the role of laparoscopic surgery. Curr Opin Obstet Gynecol 2011;23:278-282.
9. Ruffo G, Scopelliti F, Scioscia M, Ceccaroni M, Mainardi P, Minelli L. Laparoscopic colorectal resection for deep infiltrating endometriosis: analysis of 436 cases. Surg Endosc 2010;24:63-67.
10. Chapron C, Santulli P, de Ziegler D, Noel JC, Anaf V, Streuli I, Foulot H, et al. Ovarian endometrioma: severe pelvic pain is associated with deeply infiltrating endometriosis. Hum Reprod 2012;27:702-711.
11. Roman H, Ness J, Suciu N, Bridoux V, Gourcerol G, Leroi AM, Tuech JJ, et al. Are digestive symptoms in women presenting with pelvic endometriosis specific to lesion localizations? A preliminary prospective study. Hum Reprod 2012;27:3440-3449.
12. Calasanz ER, Nazim M, Kauffman RP. Transmural sigmoid colon endometrioma in a young reproductive age woman. Int J Surg Case Rep 2013;4:253-255.
13. Goncalves MO, Podgaec S, Dias JA, Jr., Gonzalez M, Abrao MS. Transvaginal ultrasonography with bowel preparation is able to predict the number of lesions and rectosigmoid layers affected in cases of deep endometriosis, defining surgical strategy. Hum Reprod 2010;25:665-671.
14. Bergamini V, Ghezzi F, Scarperi S, Raffaelli R, Cromi A, Franchi M. Preoperative assessment of intestinal endometriosis: A comparison of transvaginal sonography with water-contrast in the rectum, transrectal sonography, and barium enema. Abdom Imaging 2010;35:732-736.
15. Nasim H, Sikafi D, Nasr A. Sigmoid endometriosis and a diagnostic dilemma - A case report and literature review. Int J Surg Case Rep 2011;2:181-184.
16. Sampson JA. Metastatic or Embolic Endometriosis, due to the Menstrual Dissemination of Endometrial Tissue into the Venous Circulation. Am J Pathol 1927;3:93-110 143.
17. Meuleman C, Tomassetti C, D'Hoore A, Van Cleynenbreugel B, Penninckx F, Vergote I, D'Hooghe T. Surgical treatment of deeply infiltrating endometriosis with colorectal involvement. Hum Reprod Update 2011;17:311-326.
18. Langlois NE, Park KG, Keenan RA. Mucosal changes in the large bowel with endometriosis: a possible cause of misdiagnosis of colitis? Hum Pathol 1994;25:1030-1034.
19. Gupta J, Shepherd NA. Colorectal mass lesions masquerading as chronic inflammatory bowel disease on mucosal biopsy. Histopathology 2003;42:476-481.
20. Daya D, O'Connell G, DeNardi F. Rectal endometriosis mimicking solitary rectal ulcer syndrome. Mod Pathol 1995;8:599-602.
21. Kelly P, McCluggage WG, Gardiner KR, Loughrey MB. Intestinal endometriosis morphologically mimicking colonic adenocarcinoma. Histopathology 2008;52:510-514.
22. De Ziegler D, Streuli MI, Borghese B, Bajouh O, Abrao M, Chapron C. Infertility and endometriosis: a need for global management that optimizes the indications for surgery and ART. Minerva Ginecol 2011;63:365-373.
23. Kinkel K, Frei KA, Balleyguier C, Chapron C. Diagnosis of endometriosis with imaging: a review. Eur Radiol 2006;16:285-298.
24. Koga K, Osuga Y, Yano T, Momoeda M, Yoshino O, Hirota Y, Kugu K, et al. Characteristic images of deeply infiltrating rectosigmoid endometriosis on transvaginal and transrectal ultrasonography. Hum Reprod 2003;18:1328-1333.
25. Hudelist G, Tuttlies F, Rauter G, Pucher S, Keckstein J. Can transvaginal sonography predict infiltration depth in patients with deep infiltrating endometriosis of the rectum? Hum Reprod 2009;24:1012-1017.
26. Bazot M, Darai E, Hourani R, Thomassin I, Cortez A, Uzan S, Buy JN. Deep pelvic endometriosis: MR imaging for diagnosis and prediction of extension of disease. Radiology 2004;232:379-389.
27. Bachmann R, Bachmann C, Lange J, Kramer B, Brucker SY, Wallwiener D, Konigsrainer A, et al. Surgical outcome of deep infiltrating colorectal endometriosis in a multidisciplinary setting. Arch Gynecol Obstet 2014;290:919-924.
28. Vercellini P, Somigliana E, Vigano P, De Matteis S, Barbara G, Fedele L. Post-operative endometriosis recurrence: a plea for prevention based on pathogenetic, epidemiological and clinical evidence. Reprod Biomed Online 2010;21:259-265.
29. Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J. Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril 2012;98:564-571.
30. Vercellini P, Barbara G, Buggio L, Frattaruolo MP, Somigliana E, Fedele L. Effect of patient selection on estimate of reproductive success after surgery for rectovaginal endometriosis: literature review. Reprod Biomed Online 2012;24:389-395.
31. Sibiude J, Santulli P, Marcellin L, Borghese B, Dousset B, Chapron C. Association of history of surgery for endometriosis with severity of deeply infiltrating endometriosis. Obstet Gynecol 2014;124:709-717.
32. Nirgianakis K, McKinnon B, Imboden S, Knabben L, Gloor B, Mueller MD. Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence. Acta Obstet Gynecol Scand 2014;93:1262-1267.

 

             
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