Table of Contents  

Chibuzo and Venyo: Endometriosis of the colon – a review of the literature

Introduction

Endometriosis was first described by von Rokitansky Kitansky in 1860 as the presence of functioning endometrial tissue at sites outside the uterus,13 but the term was first used by John Sampson in 1921.4 Katsikogiannis et al.3 found fewer than 20 reported cases of large bowel obstruction caused by endometriosis over a period of 10 years in their review. Large bowel endometriosis was first described by Marshak and Friedman5 and, independently, by Grimes,6 in 1950. In view of the rarity of endometriosis of the colon (EC), most clinicians may be unfamiliar with its diagnostic features. This review of the literature on endometriosis is divided into (a) a general overview, (b) a review of some reported cases and (c) narrations of some reported cases of endometriosis of the colon.

Literature review

General overview

Epidemiology

Up to one-third of patients with endometriosis have involvement of the large or small bowel.7,8 It is reported to be rare in pre- and post-menopausal women,9 but 5–15% of menstruating females having some degree of endometriosis.811

Endometriosis can be broadly classified into pelvic and extrapelvic endometriosis (otherwise known as extragenital endometriosis).9,12 Pelvic endometriosis (PE) involves the internal female genitalia and surrounding pelvic peritoneum, while extrapelvic involvement could affect a wide range of other sites, from the intestines to even the heart.9,10 Of the extrapelvic type, intestinal involvement is the most common, occurring in 3.8–37% of cases,8,10,13,14 with colonic involvement in 12–25% of all cases of endometriosis.15 Interestingly, despite the rarity of EC, involvement of the rectum and sigmoid accounts for up to 95% of extrapelvic endometriosis.9 A case report of transverse colonic involvement is documented by Anaf et al.16 Other parts of the bowel that could be affected by extrapelvic endometriosis include the caecum (3.5%),17 distal ileum (2–16%) and the appendix (3–18%).18,19

Most patients who develop colonic endometriosis have a prior diagnosis of or associated pelvic endometriosis;12 however, some present ab initio with intestinal endometriosis.12 Kaufman et al.,20 in their review, found that 44% had no prior diagnosis of endometriosis.

The median age at diagnosis is in the fourth decade, between 34 and 40 years.21 At the time of this review, no case of colonic endometriosis in a male had been reported. However, there are reports of paratesticular, abdominal wall, appendiceal, bladder and prostate involvement in males.22

Sites

The most common sites of colonic endometriosis are the rectosigmoid colon (in up to 73% of cases) and the rectovaginal septum (13% of cases).23 Other common sites, in descending order, include the sigmoid colon, rectum and caecum.14,23 Endometriosis can involve any portion of the colonic wall, from the mucosa to the serosa.13 (See Figure 1 for the anatomy of the pelvis and possible sites of involvement.)

FIGURE 1

Pelvic structures where endometriosis may develop. Reproduced from Fischer et al. Diagnosis and management of endometriosis: pathophysiology to practice. APGO Educational Series on Women’s Health Issues. Crofton, MD, USA: APGO. Available from: https://www.apgo.org/elearn/endo/endomonon2.pdf.24 Permission kindly provided by Jespersen and Associates LLC, and the Association of Professors of Obstetrics and Gynaecology, Copyright © 2012. All rights reserved. Articles published by this open-access journal are distributed under the Creative Commons Attribution Non-Commercial Licence which permits use, distribution, and reproduction in any medium provided the original work is properly cited, the use is non-commercial and is otherwise in compliance with the licence.

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Focal involvement is more common, but 15–35% have multifocal colonic involvement, which could be micro- or macroscopic.12 Subserosal endometriotic invasion that extends more than 5 mm beyond the peritoneum, was previously referred to as deep infiltrating or deep pelvic endometriosis, but is now termed fibrotic endometriosis.24,25

Pathogenesis

Retrograde implantation theory

The most widely accepted theory is that proposed by Sampson in 1921.4 During menses, endometrial tissue is extruded via the fallopian tubes, resulting in seeding of extrapelvic structures. In support of this theory, it is known that menstrual regurgitation occurs in 76–99% of women.4,15 These effluents have been demonstrated to contain viable endometrial cells that replicate when transplanted to other body parts. Countering this theory is the small number of women with endometriosis, as the number might be expected to be higher. This suggests that genetic predisposition, deficient cell-mediated immunity or excessive production of auto-antibodies to endometrial cells may determine whether or not a patient develops endometriosis.4

In bowel endometriosis, the deposited endometrial tissue is usually asymptomatic and may be seen grossly as serosal implants. The lesions from the serosa spread inwards. They trigger the release of inflammatory mediators such as tumour necrosis factor and prostaglandins, which induce tissue reactions, scarring and increased smooth muscle contractions, resulting in cramps and diarrhoea.26 In the muscularis propria, these nodules initiate contiguous muscular hyperplasia and fibrosis, which can progress to luminal stenosis.12 Under hormonal influence, proliferation of the endometriotic tissue leads to inflammation and progressive scarring,13 resulting in mild symptoms, such as increased flatulence, change in bowel habits, decrease in stool calibre, etc. An increase in the number of steroid receptors and Ki-67 indices confirms that proliferation is hormone induced.26 With time, there is healing by fibrosis, leading to stenosis and an increased risk of obstruction.10 Severe pain and rectal spasms are due to invasion of the myenteric and submucosal plexuses.4 Motility disorders are the result of inhibition of the sympathetic plexuses and disruption of the interstitial cells of Cajal.26

Coelomic metaplasia theory

This theory was propounded by Heinrich von Waldeyer in 187024 and was supported by Robert Meyer in 1919.15 Coelomic epithelium has the same embryological origin as the pelvic peritoneum, the ovaries and Müllerian duct derivatives. Thus, with time, metaplasia may occur, resulting in endometriosis.Women in their reproductive years are the most affected, which has been stated as between 25 and 29 years in one study,12 and between 34 and 40 years in another study.21 This is not supported by the fact that the majority of cases of bowel endometriosis occur during the third and fourth decades of life, and not in older patients, who are more prone to have metaplasia.4 Although it is the only theory able to cater for endometriosis occurring in post-menopausal women or males, at the time of this review, no case of bowel endometriosis in a male has been reported.

Induction theory

Induction theory is an extension of the coelomic metaplasia theory.24 According to this theory, endogenous or immunological substances released by the endometrium and transported in the blood induce endometrial differentiation from undifferentiated cells.24

Lymphovascular spread

Halban postulated that lymphovascular spread is via the blood and lymphatic vessels.15

Iatrogenic dissemination

Spread following surgical procedures, or iatrogenic dissemination, in a patient with pelvic endometriosis has been documented.4

Genetics

A monozygotic twin whose twin pair has endometriosis of the colon has a 15-fold risk of also developing the same condition, while first-degree relatives have a 7-fold increased risk.22 It may be linked to human leukocyte antigen.4,22 Possible relationships to KRAS (V-Ki-ras2 Kirsten rat sarcoma viral oncogene homologue)/MAPK (mitogen-activated protein kinase) and PTEN (phosphatidylinositol-3,4,5-trisphosphate 3-phosphatase)/PI3K (phosphatidylinositol-4,5-bisphosphate 3-kinase) are being investigated.24

Autoimmune disorders

Autoimmune disorders, such as asthma, inflammatory bowel disorders and hypothyroidism, are more common in women with endometriosis.27 There is a strong association between coexisting inflammatory bowel disease and the development of endometriosis.26

Clinical features

Colonic endometriosis is typically diagnosed incidentally,7 but there are reports of endometriosis of the colon presenting with dyschezia,7,9 diarrhoea, constipation (25–40%),7,9,28 abdominal pain (76.5%),7,8,28 tenesmus,10 passage of mucus per rectum,29 cyclical or non-cyclical bleeding per rectum10,16 or, rarely, intestinal obstruction (12%).10,28 These non-specific symptoms, and the multitude of asymptomatic cases, can delay diagnosis by 8–11 years.15,28

According to Jubanyik and Comite,18 the symptoms of intestinal endometriosis, which include crampy abdominal pain, abdominal distension, diarrhoea, constipation, tenesmus and haematochezia, are cyclical in approximately 40% of patients, and they can vary depending on site. Nevertheless, clinicians should note that the cyclical symptoms are not exclusive to endometriosis. The classic triad of dysmenorrhoea, dyspareunia and infertility as a sequel of concomitant pelvic disease may also exist.13

Townell30 emphasized the importance of a thorough physical examination. The vaginal examination may reveal tender cervical nodules and a fixed bulky uterus that reduces in tenderness, size and fixity at various times in the cycle.30 This could form the basis of pain mapping as currently practised.24

Endometriosis of the colon is rarely associated with neoplasms or pre-malignant conditions.31

Macroscopic features

Microscopic features of endometriosis of the colon are presented in Figures 2(d and e) and 3.

FIGURE 2

CT (computerized tomography) colonoscopy images, microscopic and endoscopic views, of endometriosis of the colon in a patient. (A) Axial image from virtual colonoscopy demonstrating a sigmoid mass (arrows). (B) Coronal multiplanar reconstruction demonstrating the mass (short arrows) and its relationship to the bladder (long arrow). (C) Axial virtual colonoscopic image demonstrating a segmental area of thickening (arrows) in the descending colon. (D) Endometriosis (long arrow) on the left extending to involve the epithelium of the colon (short arrows on the right) (E) Endometriosis (arrows) involving the muscularis propria of the bowel. Note the characteristic stroma associated with the glandular epithelium. (F) Endoscopic view showing a lobular mass in the lumen of the sigmoid colon. Reproduced with permission from Samet et al. Colonic endometriosis mimicking colon cancer on a virtual colonoscopy study: a potential in diagnosis. Case Rep Med 2009; 2009, 379578.9 Copyright © Jonathan D. Samet et al. This is an open access article distributed under the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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FIGURE 3

Endometrioid adenocarcinoma macroscopically and microscopically displayed showing immunoreactivity for ER and CK7. (a) Gross appearance of the cut surface of the rectum with an endometriotic lesion. (b) Immunological staining of the endometriotic specimen in (a) with a strong positive reaction to ER. (c) Immunological staining of the endometriotic specimen in (a) with a strong positive reaction to CK7. Reproduced from Lee H, Kim K. Intestinal endometriosis: clinicopathologic analysis of 15 cases including a case of endometrioid adenocarcinoma. Korean J Pathol 2009; 43:120–5,39 with permission from the Korean Journal of Pathology under the Creative Commons Attribution Non-Commercial Licence. Under this type of licence, readers are free to use, reproduce, or disseminate or display the open access content of this journal for non-commercial purposes.

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Macroscopic examination of EC specimens may reveal serosal and subserosal nodules less than 5 cm in diameter with smooth muscle hypertrophy.7 The hypertrophic smooth muscle could promote intestinal obstruction. The grey cut surface may have minute areas of haemorrhage which, if subserosal, can cause adhesions (Figures 3a and 4).

FIGURE 4

Caecal endometriotic lesion. Reproduced with permission from Otaghvar et al. Caecal endometriosis presenting as acute appendicitis. Case Rep Surg 2014; 2014:519631.17 Permission provided under Creative Commons Attribution Licence enabling the unrestricted use distribution of articles in any medium provided the original work is properly cited.

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Microscopic examination of EC tends to reveal endometrial glands, endometrial stroma and haemosiderin in deeper layers of the colon, usually surrounded by smooth muscle.7,32 This is referred to as the ‘diagnostic triad’ of endometriosis.14 There may be colonic epithelial inflammation and ulcers, mimicking inflammatory bowel disease or solitary rectal ulcer syndrome.7,14 The mucosa is usually normal but the bowel wall may be fibrotic. Cilia help to differentiate the endometrial glands from colonic glands.7 Polypoid lesions may be seen (termed ‘polypoid endometriosis’) more in post-menopausal women and where there is mucosal involvement.14 There are sparse reports of mucosal involvement.9,14 Subserosal and muscularis propria involvement is most common.8,33,34 In a review of 96 patients with symptomatic bowel endometriosis, Kaufman et al.20 reported that 19% had mucosal involvement, while 39%, 34% and 6% had involvement of the submucosa, muscularis propria and pericolic fat, respectively.

Quite often endometriosis infiltrates along nerves of the bowel wall.7,16 Abrao et al.35 examined 35 cases of bowel endometriosis and found positive lymph nodal involvement in 26.3%. They reported that lymph node enlargement occurred in all specimens with endometriotic lesions ≥ 1.75 cm thick, and that positive nodal involvement occurred in all cases with over 80% circumferential bowel involvement.

An important distinction is that serosal involvement alone without subserosal penetration is ‘peritoneal’ and not bowel endometriosis.26

Immunohistochemical staining characteristics

Positive staining

Endometriosis of the colon has been documented to stain positively with:

  • oestrogen receptor (ER)14 (see Figure 3b for an example)

  • progesterone receptor (PR)14

  • CD-1014,36 endometriotic stromal cells

  • cytokeratin (CK) 7 (see Figure 3c for an example), ER, CK20 and CDX2 are helpful14

  • vimentin11,36 for the stroma.

It is noteworthy that CK20 stains negatively for endometrial glands. Other positive immunostaining markers include Wilms tumour 1 protein, S-100 (for involvement of neural plexuses),37 smooth muscle actin and CD-117.14 B catenin expression may be used as an immunocytomarker.36

Negative staining

Endometriosis of the colon, on immunohistochemical staining, stains negatively with:

  • CDX24

  • carcinoembryonic antigen (CEA).4

However, Jiang et al.14 found CDX2 useful. Imprint touch cytology has been also used in the diagnosis of endometriosis,36 with EC appearing as non-overlapping cohesive epithelial sheets. Frozen section biopsy was not found to be helpful.36

Investigations

Preoperative diagnosis is difficult.9,10,14 Since only mass lesions are readily identifiable, early diagnosis of extraluminal lesions becomes challenging.12

Radiological investigations

Transvaginal ultrasonography is 91% sensitive but cannot provide information on the distance of the mass from the anal verge, masses beyond the rectum or the thickness of bowel wall involved.12 Transrectal ultrasonography (TRUS) is able to provide this information but is still unable to visualize masses proximal to the rectum.12 Benbara et al.38 reported a sensitivity of 100% for TRUS. Both methods will characterize endometriotic lesion(s) as mainly hypoechoic mass/masses of mixed echogenicity.12 These modalities are better for rectovaginal endometriosis.25

A double-contrast barium enema will show mucosal crenulations, imprints from an ‘extrinsic mass’ or large lesions;12 however, it cannot determine the depth of involvement.29

Magnetic resonance imaging (MRI) is less sensitive12 (55% according to Benbara et al.38) unless enhanced by contrast, as the density of endometrial tissue is similar to that of the adnexa.12,29

The most sensitive radiological imaging modality (up to 98.7% sensitivity and 91% specificity) is multislice or multidetector computerized tomographic enteroclysis (MSCTe or MDCTe)12 (Figure 5).

FIGURE 5

MDCTe, coronal reconstruction, showing an endometriotic nodule infiltrating the muscularis propria of the sigmoid colon (shown by arrowheads), the mucosa is not infiltrated. Reproduced from Ferrero et al. Bowel endometriosis: recent insights and unsolved problems. World J Gastrointest Surg 2011; 3:31–8,29 with permission from the World Journal of Gastrointestinal Surgery and Baishideng Publishing Group, Inc. Copyright © 1995–2014 Baishideng Publishing Group Inc. All rights reserved. Articles published by this open-access journal are distributed under the Creative Commons Attribution-Non-Commercial Licence which permits use, distribution, and reproduction in any medium provided the original work is properly cited, the use is non-commercial and is otherwise in compliance with the licence.

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It has been reported that CT scans or barium enemas usually reveal an extrinsic compression, stenosis or filling defect and are only 70% sensitive or specific10 (see Figure 2a, b and c for examples of CT colonoscopy showing EC) and that MRI would appear to be the most sensitive imaging technique for intestinal endometriosis (up to 80–90%).13,40 Nevertheless, the gold standard for the diagnosis of intestinal endometriosis is laparoscopy or laparotomy.10,12

Endoscopic

Colonoscopy fails to identify those without mucosal involvement, who constitute the majority of EC cases.10,12 Although Samet et al.9 found virtual colonoscopy useful, according to Conzo et al.13 it does not increase the sensitivity of diagnosis. Laparoscopy has been stated to be the gold standard.10,12,14 It confirms diagnosis without laparotomy,10 as a biopsy can still be taken and extrinsic lesions adequately visualized13 (see Figure 2f for an endometriotic lesion viewed using laparoscopy). However, it has shortcomings for the diagnosis of rectovaginal endometriosis, whereby the depth of tissue involvement cannot be determined laproscopically. Adhesions necessitate conversion from laproscopic to open surgery.25

Biomarkers

Carbohydrate antigen (CA)-125 is the only tumour marker found to be elevated in endometriosis.15,28,36

Treatment

Various factors determine the treatment modality chosen. These include the patient’s age, sex, desire to conceive and presence of obstructive symptoms.10 No consensus exists, but the goal of treatment is to eliminate symptoms, debulk endometrial tissue and stop disease progression.41 A combination of medical and surgical therapies may be required, given the high rate of recurrence.24

Endometriosis of the colon may be treated by the following means.

Medical therapy

This therapy aims to control pain and create a ‘hypo-oestrogenic’ environment to retard the growth of endometriotic nodules.24

Pain medication

First-line treatment for deep pelvic pain consists in non-steroidal anti-inflammatory drugs with combined oral contraceptive pills.4,15,42 Gonadotropin-releasing hormone (GnRH) agonists, such as leuprolide acetate (Lupron Depot®, AbbVie, North Chicago, IL, USA), goserelin (Zoladex®, AstraZeneca, London, UK) and triptorelin (Decapeptyl®, Ipsen, Paris, France; Gonapeptyl Depot®, Ferring, Saint-Prex, Switzerland), were previously used as second-line drugs.15 At the time of this review, they were recommended as first-line therapy for pain.24 However, they should not be used for more than 6 months to 1 year as they have been shown to promote hypo-oestrogenism and, consequently, osteopenia.24

Progestogens are useful for pain control and have been documented to have fewer side-effects than contraceptive pills.24,26 However, GnRH agonist have a better side-effect profile.26

Hormonal therapy

Megestrol,11,14 either as oral formulation (Megace®, Swedish Orphan, Stockholm, Sweden) or as an intrauterine device,24 medroxyprogesterone acetate (Provera®, Pfizer, New York, NY, USA) or norethisterone acetate (NEA) may be used to relieve the pelvic pain and other pelvic symptoms of associated PE.4,24 Ferrero et al.43 found a reduction in diarrhoea, mucus passage and cramping, but not in constipation or bloating, in patients with EC treated with NEA. It is important for the physician and patient to bear in mind the risk of progression of EC despite the use of combined oral contraceptive pills.37

Danazol, a synthetic androgen, reduces the number of steroid receptors and therefore creates a beneficial hypo-oestrogenic environment;13,24 however, masculinization is a side-effect.24

Aromatase inhibitors, such as anastrozole and letrozole, are useful in deep endometriosis.15,44 Endometriotic nodules produce aromatase to further preserve and ensure oestrogen for their survival.24 Goserelin affects ovarian oestrogen but not that of peripheral tissues so it may be combined with an aromatase inhibitor,29 which would be able to inhibit aromatase from peripheral sources. In premenopausal women, Ferrero et al.45 showed that inhibition of aromatase was more effective when the aromatase inhibitor was combined with triptorelin rather than NEA.45 Soysal et al.46 were also able to demonstrate the benefit of combining an aromatase inhibitor (anastrozole) with a GnRH agonist (goserelin) in the adjuvant setting with improved outcomes and fewer recurrences. Triptorelin plus tibolone (Livial®, MSD, Kenilworth, NJ, USA) is another useful combination.15 Iron chelators have been documented to be useful in early disease.15

Luteinizing hormone-releasing hormone analogues, such as Danatrol® (danazole, Sanofi-Aventis, Paris, France), can be used to decrease vascularity of the lesions before surgery.41 Neoadjuvant use of GnRH agonists for the same purpose, and to decrease the size of the lesions, is also advocated.24

Medical marijuana (Cannabis indica) has been suggested for use in colorectal endometriosis as the high concentrations of cannabidiol possibly reduce the chronic inflammation of endometriosis and reduce pain and symptoms.47

Experimentation with resveratrol, epigallocatechin-3-gallate, angiogenesis inhibitors, immunomodulators, among others, to reduce the size of endometriotic nodules and symptoms is being undertaken.24

Surgical therapy

Surgical intervention may be required if endometriosis produces obstructive symptoms4,12 or recurrent bleeding,13 is non-responsive to pharmacotherapy, or to reduce the risk of malignant transformation.13 Options include conservative (superficial or full thickness) resections, segmental resections and extended debulking.13 Conservative resections can be carried out when the nodules are less than 3 cm in diameter or there is only superficial involvement without stricture formation.13 These may include shaving or disc excision.12,29 Moustafa and Elnasharty48 reviewed various surgical approaches to rectal endometriosis and concluded that there was no significant difference in the outcome or fertility between those who had conservative approaches and those who had formal resections, but the former group experienced fewer complications, such as fistulae and leaks, and required a shorter hospital stay. Thus, these authors recommended conservative approaches when possible.

Segment resection is carried out when > 50% of the bowel circumference is involved or when there are multiple nodules or a nodule > 3 cm in diameter.25 Chowdhury and Yue26 recommended hormonal therapy in those with stenosis resulting in bowel circumference < 60% of normal.

Endoluminal stenting may also relieve obstruction.15 Adjuvant surgeries, such as unilateral parametrectomy, have also been proposed to improve symptoms and reduce pain.49

Differential diagnosis

The differential diagnoses of EC include adenocarcinoma of colon.4 Ninety-eight per cent of colonic carcinomas are adenocarcinomas.50 Colonic carcinomas are rarely associated with endometriosis and unopposed oestrogen therapy.9 Colonic endometriosis is often a diagnostic challenge and should be considered in young women with lower gastrointestinal tract symptoms.21 These cases usually involve the serosa, have endometrioid histology and squamous differentiation, but spare the mucosa and need to be differentiated from colonic carcinoma since their staging and treatment may be different.50

Other disorders to consider in the differential diagnosis include colitis,14 actinic colitis,13 diverticulitis,13 appendicitis,17 idiopathic inflammatory bowel disease, which could be either constipation or diarrhoea predominant,13,34 solitary rectal ulcer syndrome, mucosal prolapse (due to inflammation and fibromuscular dysplasia) and adenoma with low-grade dysplasia.13

Prognosis

The risk of recurrence after adequate treatment is high (up to 30%).10 The benefit of GnRH analogues in preventing this is debatable. Conservative surgical resection increases the risk.13 Laparoscopic intervention, initiated by Nehzat in 1989,12 and nodulectomy are reported to be associated with better fertility post-operatively.12,29

Post-menopausal status and prior use of hormone replacement therapy increase the risk of associated malignancy or malignant transformation,10 which occurs in 3–10.8% of patients.13,51

Review of reported cases

Forty-one case reports of EC, retrieved from various databases, were reviewed. Reviews and articles not fully accessible were excluded. Data analysis was carried out with Statistical Package for the Social Sciences, version 17 (SPSS Inc., Chicago, IL, USA). Fisher’s exact test was used to determine associations; P-values < 0.05 were considered significant.

There was a Caucasian predominance (49%) in the reported cases found, and only 2% of patients were Negroids. In 5% of the reviewed cases race was not specified. Contributions were from Europe (42%), Asia (27%), North America (20%), South America (7%) and Africa (5%).

The mean age of women with EC was 39.83 ± 10.93 years (median 40 years), ranging between 23 and 85 years. Only three women (7%) were post-menopausal; in seven (17%) cases no information on menopausal status was provided. Three women (7%) were gravid, two of whom presented with perforation. A significant association was found between gravidity and perforation (Fisher’s exact test, P = 0.003), but not between gravidity and multifocality or presentation in obstruction. Fourteen (34%) had previously undergone pelvic surgery while 12 (29%) were already known to have PE. No significant association was found between oral contraceptives or hormone replacement therapy use and the risk of perforation or obstruction.

The sigmoid colon was the most common site of EC (18 women, 44%), followed by the rectosigmoid colon (15 women, 37%), rectum (nine women, 22%)] caecum (four women, 10%) and the descending colon (one woman, 2%). No EC was found in the ascending or transverse colons. The rectum and sigmoid therefore accounted for 86% of EC among the reviewed cases. Eight cases (17%) had bifocal involvement, with one (2%) having trifocal involvement. The sites most affected by multifocality were the caecum and the rectum. Appendiceal endometriosis was found in one case in association with rectal endometriosis.

Abdominal pain (63%) and obstruction (49%) were the most common modes of presentation. Two of the four with caecal involvement had intussusception. Other presentations included haematochezia (27%), dyschezia (24%), pelvic pain (24%), bloating (24%), loose stools (17%), nausea or vomiting (12%) and perforation (10%).

Of the 25 patients with concomitant pelvic lesions, 11 had sigmoid EC, but there was no significant association between any tumour site and presence of concomitant pelvic lesions.

The most common suspected clinical diagnosis was cancer (39%). Eleven (27%) were suspected to have EC. Other pre-investigation diagnoses included diverticular abscess, gastrointestinal stromal tumours, inflammatory bowel disease (2% each), acute diffuse peritonitis in pregnancy (5%) and tuberculous colitis (5%). Tuberculous colitis was suspected in tropical countries such as Nigeria and India.

Although laparoscopy is documented to be the gold standard, it was not performed in 29 (70%) of the cases reviewed (Figure 6). Endoscopy was the most common investigation undertaken [26 cases (63%)] (Table 1), with normal findings in four cases (15%), hyperaemia in one case (4%) and polyp in one case (4%), amounting to a sensitivity of 77%. Fifty-four per cent of the histology results from colonoscopic biopsies taken did not aid diagnosis; 10 (38%) were negative biopsies, two (8%) were inconclusive and two (8%) were reported as inflammatory processes. No significant association was found between mucosal involvement and a negative biopsy (P = 0.095).

FIGURE 6

Surgical options among patients with EC.

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TABLE 1

Test or procedure which confirmed EC diagnosis

Test/procedure Frequency of EC confirmation by test Per cent Cumulative per cent
No information 1 2.4 2.4
Histology after laparotomy 20 48.8 51.2
Laparotomy 9 22.0 73.2
Laparoscopy 7 17.1 90.3
EUS 1 2.4 92.7
Colonoscopy biopsy 3 7.3 100.0
Total 41 100.0

EUS, endoscopic ultrasound.

The muscularis propria was the most common site of EC, whereas the mucosa was the least common (Figure 7). A significant association was found between a rectosigmoid EC site and mucosal involvement (Fisher’s exact test, P = 0.018). Five of the women with mucosal involvement had haematochezia, but no significant association was found (P = 0.105). Two of the five patients with nodal involvement had deep infiltrating endometriosis (DIE). No significant association was found between those who had muscularis propria involvement and those presenting with obstruction.

FIGURE 7

Percentage involvement of histological layers by EC.

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Only one patient was documented to have a recurrence, while two, aged 61 and 85 years, had associated cancer. The risk of cancer coexisting with EC increased with a post-menopausal status (P = 0.004). Although both patients with cancer had sigmoid colonic EC, there was no significant association (P = 0.077).

Inadequate reporting of hormonal therapy [six patients (15%) used GnRH and two patients (5%) used danazol] was found and no conclusions could be drawn from the information gathered. Interestingly, the patient in the case report by Dimoulios et al.21 presented with obstruction, but did not require surgery (Figure 6), and had complete resolution of EC with GnRH monotherapy.

Miscellaneous narrations and discussions from some reported cases

Variegated presentations and histological patterns

Jiang et al.14 reviewed 15 cases (seven biopsies and eight resections) from 14 patients. They reported a mean age of 48 years (range 31–66 years). The endometriotic lesion most commonly occurred in the rectum (73%). The remainder were in the sigmoid colon (20%) and ileum (7%). The most common indication for biopsy was a polypoid lesion viewed at endoscopy (eight cases). Fourteen cases had both endometrial glands and stroma, whereas one involved only the stroma. Epithelial, mainly tubal, metaplasia was seen in all cases. Some cases mimicked chronic active colitis or enteritis histologically. They discovered immunohistochemical stains (CK7, CK20, CDX2 and ER) for atypical cases and recommended dual immunostaining in inconclusive cases. One patient had cancer and was treated with megestrol.

Lee and Kim39 reviewed 18 samples from 15 patients with a median age of 41 years. Two were asymptomatic. Bowel endometriosis was diagnosed incidentally at surgery for other indications (infertility and villotubular adenoma). There was a misdiagnosis in all of the patients from clinical and radiological findings. Five patients (33.3%) were diagnosed with colon cancer, another five patients were diagnosed with ovarian cysts, three patients (20%) with submucosal tumours of the colon, one patient (6.7%) with invasive ovarian cancer and one patient with appendicitis. The mode of eventual diagnosis varied. Four had been diagnosed from endoscopic biopsies, one of whom had repeated negative biopsies necessitating surgical intervention, and 10 of whom had diagnostic surgeries ab initio. There was rectal involvement in 53.3% and sigmoid involvement in 6.7% of patients. Eight patients (53.3%) had associated PE and one patient (6.7%) had adenomyosis. Seventeen samples were stained immunochemically using CK7 and CK20, CD-10, ER and PR. CK20 was uniformly negative in the 17 samples. A single case was negative for ER and PR but strongly positive for CD-10 (stromal indicator). Two patients had endometrioid adenocarcinoma, seen as mucinous epithelium, with strong immunopositivity for ER and CK7.

According to Slaughter and Gala,42 laparoscopic visualization and histological confirmation remains the gold standard for diagnosing endometriosis. This is corroborated by other studies.4,10,12 Macroscopically, endometriotic lesions have a variety of appearances which include powder burns and red, blue–black, yellow, white, clear vesicular and peritoneal windows. When extensive, endometriosis can lead to the formation of adhesions and cysts.42

Dimoulios et al.21 reported sigmoid endometriosis in a 35-year-old woman whose initial diagnostic workup was suggestive of carcinoma of colon. Her presenting symptoms included rectal bleeding (which was initially cyclical), episodes of severe lower abdominal pain and abdominal distension, constipation and passage of small-calibre stools. Colonoscopy on day 20 of her menstrual cycle, revealed an extensive erythematous polypoid stenosing mucosal lesion at the rectosigmoid junction. They authors reported that histological evidence obtained from this second colonoscopy, together with ultrasound of pelvis, led to the final diagnosis of intestinal endometriosis. Her serum CA-125 (measured on day 5 of her menstrual cycle) was 210  IU (international unit)/ml (normal range < 35 IU/ml), but CEA and CA-19-9 were normal [1.7 ng/ml =(normal range < 5 ng/ml) and 6.1 IU/ml (normal < 37 IU/ml), respectively]. She underwent laparoscopic diagnosis and removal of visible lesions. She received adjuvant leuprolide acetate, 3.75 mg/month via intramuscular injection. After 5 months of drug treatment repeat colonoscopy revealed regression of the stenosing lesion and a normal CA-125 of 28 IU/ml. She remained asymptomatic.

Abrao et al.52 reported the case of a 31-year-old woman with pelvic pain who underwent laparoscopic resection of sigmoid colon for endometriosis. Histological examination of the resected bowel revealed an endometriotic lesion affecting the entire width of the sigmoid colon. Within this was found epithelial granulomas with birefringent and partially calcified eggs characteristic of Schistosoma mansoni. It was concluded that endometriosis and schistosomiasis may be present simultaneously in patients with bowel symptoms and pelvic pain.

Andersen et al.53 reported a case of acute obstruction of the sigmoid colon which was caused by endometriosis in a 35-year-old woman. Although endometriosis occasionally causes relative stenosis of the bowel, total obstruction is rarely seen. It is important to be on the alert for aetiologies of neoplastic nature, but the less common non-neoplastic causes should not be forgotten.

Malignant associations

Reports and reviews of coexisting malignancy or malignant transformations are rare. Yantiss et al.31 reported 17 cases of gastrointestinal endometriosis that were complicated by neoplasms (14 cases) or precancerous changes (three cases). The presentations included chronic abdominal pain, hypermenorrhoea, intestinal obstruction, haematochezia, acute abdomen and alteration of bowel habit. Eight of 11 patients who had hysterectomies had received unopposed oestrogen therapy. The colonic lesions were mostly in the rectum and sigmoid colon. The histological types of the malignant lesions were endometrioid adenocarcinomas, Müllerian adenosarcomas, endometrioid stromal sarcoma (ESS), endometrioid adenofibroma of borderline malignancy with carcinoma in situ, atypical hyperplasias and endometrioid adenocarcinoma in situ. Serosa and muscularis propria involvement was universal, with only two involving the mucosa.

Yantiss et al.31 advised pathologists to be aware of the possibility of a genital tract tumour when evaluating intestinal neoplasms in females, especially if they have a history of endometriosis and have received unopposed oestrogen therapy.

Lankerani et al.54 reported a 42-year-old woman with endometriosis of the oviducts. She underwent hysterectomy and oophorectomy. Endometriosis, with chocolate cyst of one ovary, was found. There was an associated malignant tumour in the bowel serosa. Histological examination revealed direct transition from benign epithelium in the ectopic endometrial glands to dysplastic tissue. The tumour included elements of yolk sac (endodermal sinus tumour), choriocarcinoma and teratoma in different areas of the tissue examined.

Cho et al.55 reported that the majority of malignant tumours that arise in ovarian and extraovarian endometriosis are carcinomas. ESS and mixed Müllerian tumours arising in intestinal endometriosis are rare, but have been described. Most are endometrioid carcinomas, but sarcomatous differentiation is possible.39 They are collectively called endometriosis-associated intestinal tumours (EAIT), as proposed by Sampson in 1925.26 Cho et al.55 reported a case of ESS of the sigmoid colon which arose in endometriosis in a 48-year-old woman. They also reviewed six other cases of endometrial stromal sarcoma originating in intestinal endometriosis tissue in the English literature in women aged between 36 years and 64 years. The presenting symptoms were pain, bloody diarrhoea and tenesmus. Some of the patients had a previous history of endometriosis. The rectosigmoid colon was the most common tumour site. The histological features were the same as their uterine counterpart. No mortality was reported. They further suggested that this rare tumour should not be confused with gastrointestinal stromal tumour clinically or histologically.

McCluggage et al.56 reported a 65-year-old woman who presented with lower abdominal cramps and passage of blood and mucus from the rectum. Barium enema revealed a possible malignant stricture of the rectosigmoid and she underwent an anterior resection. Small haemorrhagic peritoneal nodules were seen, suggestive of endometriosis, but she had multiple metastatic lesions in the liver, giving the impression of a malignancy. A polypoid ulcerated tumour involved the mucosa and infiltrated through the entire colonic wall grossly and microscopically, and extended into the peripheral fatty tissue. Histology of a liver biopsy showed metastatic clear cell carcinoma. Immunohistochemical staining showed diffuse strong positive membrane staining of tumour cells with CA-125 and CK7, but not for CK20, which stained adjacent normal colonic mucosa. Staining for type IV collagen and laminin showed positivity of the hyalinized cores within the papillary areas and the cells lining the cystic structures stained strongly with Ber-EP4. It was considered likely that the colonic clear cell carcinoma originated in endometriotic tissue, based on the presence of a cystic structure at the deep aspect of the tumour, which was lined by cells with eosinophilic cytoplasm. Although endometrial-type stroma was not identified, the morphological findings were similar to those that can be seen in long-standing endometriosis. Furthermore, at laparotomy, there was a clinical impression of endometriosis surrounding the tumour with multiple small haemorrhagic pelvic and abdominal nodules.

According to Hoang et al.,57 malignant transformation is not a frequent complication of endometriosis. The influence of oestrogen exposure on the incidence of EAIT is well recognized. The ovary is the primary site in 79% of cases and extragonadal sites are identified in 21% of cases. Primary involvement of these types of tumours with the colon and/or rectum is a rare clinical entity. Endometrioid carcinoma is a common histological type that remains a diagnostic challenge and the main differential diagnosis includes colorectal carcinoma. They reported a case of malignant transformation which arose in colonic endometriosis. The patient had undergone a total hysterectomy and bilateral salpingo-oophorectomy (BSO) 10 years prior to her presentation with haematochezia. She was treated by surgical resection. The authors stated that immunohistochemical staining in addition to the usual histopathology is critical for the accurate diagnosis of the endometriosis-associated intestinal tumour.

Multifocality

Multifocal bowel involvement is not common. Katsikogiannis et al.3 reported coexisting sigmoid and appendiceal endometriosis presenting with intestinal obstruction in a 36-year-old woman following a prolonged period of contraception use. Intraoperatively, adhesions between the sigmoid, uterus, left ureter and appendix were found. The appendiceal findings were incidental. She had an appendectomy, rectosigmoidectomy, Hartmann’s procedure and temporary transverse colostomy, which was taken down 6 months later. She received triptorelin (3.75 mg) monthly. She was asymptomatic at follow-up 1 year later.

Caselli et al.58 reported multifocal involvement of the proximal and midsigmoid colon, as well as the rectosigmoid junction, in a woman with no prior diagnosis of endometriosis or pelvic surgery (Table 2).

TABLE 2

Compilation of the reviewed cases with salient information retrieved

No. Reference Location Race Age (years) Tumour site Gynaecological history Mucosal involvement Method of diagnosis
1 Bartkowiak et al.23 Poland Cn 53 S P0; 1-year Estraderma and Depo-Provera® No Colonoscopy
2 Katsikogiannis et al.3 Greece Cn 36 R; App P2; OCPs No Laparotomy
3 Caselli et al.58 Chile Cn 41 Prox and midS; RS No (SM, MP + Se) CECT
4 Ohsaki et al.36 Japan M 45 S ITC
5 Dimoulios et al.21 Greece Cn 35 RS P2 Yes Repeat colonoscopy on day 20 of cycle – diagnostic biopsy
6 Ghevariya et al.11 USA Cn 28 RS No; SM Surgical resection
7 Seminiero et al.8 USA Cn 27 RS P1 MP + Se EUS
8 Kupersmith et al.62 USA Cn 42 RS P0 Emergency laparotomy
9 Samet et al.9 USA Cn 51 S P0 Yes; full thickness; one positive lymph node Contrast virtual colonoscopy + biopsy
10 Lin et al.10 China M 33 R P0; 6 months; hormonal therapy No; SM + MP + SF + Se Laparotomy
11 Conzo et al.13 Italy Cn 42 RS Yes; full thickness Laparotomy
12 Nasim et al.15 Ireland Cn 32 S P0 No; melanosis coli Laparotomy
13 Sassi et al.41 Tunisia M 35 RS P3 Yes; full thickness; one positive LN Laparotomy
14 Insilla et al.64 Italy Cn 37 S P0 No; SM + MP + SF + Se Laparoscopy; positive immunostaining (CD10, ER, PR)
15 Costa et al.63 Italy Cn 32 S; RS G1; GAD, 25 weeks Laparotomy
16 Jayant et al.65 India M 23 S No; SM + MP Laparotomy
17 Tade66 Nigeria N 29 RS Laparotomy
18 Otaghvar et al.17 Iran M 43 C Irregular menses; dysmenorrhoea No; Se + MP Laparotomy
19 Agito et al.67 USA Cn 85 S BSO + hysterectomy; hormone replacement for 40 years; post-menopausal No Laparotomy
20 Alhumidi and Hamodat68 Saudi Arabia M 41 S (two foci) No Laparotomy
21 Pisanu et al.69 Italy Cn 37 R Laparotomy
22 Midorikawa et al.70 Japan M 42 R Pre-menopausal No (SM + MP + Se) Laparotomy
23 Wang et al.71 USA 61 S No; MP + SM; mesenteric nodal involvement; Müllerian adenocarcinoma Laparotomy
24 Varras et al.61 Greece Cn 43 S No Laparotomy
25 Amendolara et al.72 Italy Cn 45 S No; MP + SM Laparoscopy
26 Hernández Magro et al.73 Mexico 32 RS P1+1 Yes; transmural Imaging studies, histology
27 Bascombe et al.74 Trinidad and Tobago 37 S P1 No; MP Histology
28 Ropacka-Lesiak et al.75 Poland Cn 27 RS; R (distal 1/3) P0; dysmenorrhoea MP, DIE Imaging (not specified) led to suspicion
29 Rambuszek and Miłek76 Poland Cn 32 RS Histology
30 Lee et al.77 South Korea M 48 S No; MP Laparoscopy
31 Park et al.78 South Korea M 42 RS P0; 10-month fertility pills (Drosperinone – ethinyl oestradiol)b Yes; M + SM + Se Histology
32 Murji and Sobel79 Canada 42 RS 20 years of smoking No; DIE Histology
33 Uchiyama et al.80 Japan M 57 R No; MP + Se Histology
34 Lanitis et al.81 Greece Cn 40 RS P1 No; SM + MP + Se + LN; right ovarian endometriosis and corpus luteal cyst Histology
35 Indraccolo et al.82 Italy Cn 36 C, R, ICV P0; low-dose oestrogen pills for 5 years; stopped 1 year before presentation No Laparoscopy
36 Pickron and Cooper83 USA 40 C G2P2 No information Laparoscopy
37 Garg et al.84 UK 44 S No; MP Laparotomy
38 Gupta et al.85 Nepal M 30 R P0 No; SM + MP + Se + Sr; ovarian and FT involvement Laparotomy
39 Yoshida et al.86 Japan M 43 S P0 No Laparoscopy
40 McCullough et al.87 UK 37 C, S 5 years OCP Yes Histology
41 Ford et al.88 UK Cn 28 R No; MP Laparoscopy

{ label (or @symbol) needed for fn } App, appendix; C, caecum; CECT, contrast-enhanced CT; Cn, Caucasian; D, descending colon; FT, fallopian tube; GAD, gestational age by date; G2P2, pregnant with third child (two prior pregnancies carried to term); ICT, imprint cytology; M, mongoloid; MP, muscularis propria; N, Negroid; OCP, oral contraceptive pill; P0, nulliparous; P1, para 1; P1 + 1, one child and one miscarriage; P2, para 2; P3, para 3; R, rectum; RS, rectosigmoid; S, sigmoid; Se, subserosa; SF, serosal fat; SM, submucosa; Sr, serosa.

a Oestradial (Estraderm®, Novartis, Basel, Switzerland).

b Acondro®, Mylan, Amsterdam, the Netherlands/Dretine®, Teva, Petah Tikva, Isreal/Lucette®, Consilient, London, UK/Yacella®, Morningside, Enderby, UK.

Hormonal influences on endometriosis of the colon

Given the case report by Katsikogiannis et al.,3 one cannot help but wonder if chronic use of contraceptives promotes endometriosis. Ferrero et al.37 reported progression of bowel endometriosis in a woman on contraceptives, but did not implicate the contraceptives. According to these authors, contraceptives, although useful for pain control, do not prevent progression of bowel endometriosis.37

Kawate et al.59 reported malignant transformation in a patient who had been on hormone replacement following a hysterectomy for fibroids. She developed adenocarcinoma from a sigmoid colonic endometriosis. Anaf et al.60 conducted a study on four women with laparoscopic and histological evidence of bowel endometriosis, three of whom were asymptomatic for the bowel lesions. All of these patients underwent ovarian stimulation with GnRH, human menopausal gonadotrophins and induction with human chorionic gonadotrophin to control pelvic endometriotic symptoms, and all progressed to symptomatic and partially occlusive colonic disease, which required resection.60

Perforation: pregnancy or obstruction related?

Varras et al.,61 as well as Samet et al.,9 reported that intestinal endometriosis may manifest with rectal bleeding, intestinal obstruction and rarely with perforation of bowel or malignant transformation. Kupersmith et al.62 reported a case of bowel perforation in a 42-year-old nulliparous woman with a previous diagnosis of pelvic endometriosis. She presented with a 4-day history of bloating and abdominal distension. Erect and decubitus chest radiographs showed pneumoperitoneum. An emergency laparotomy revealed a caecal perforation due to a complete obstruction from a rectosigmoid endometriotic lesion. Costa et al.63 reported stercoral double perforation in the left side of the sigmoid and rectosigmoid in a 32-year-old woman 25 weeks into pregnancy, who presented with a 4-hour history of pelvic pain. She had no prior diagnosis of endometriosis or pelvic surgery. Endometriosis was diagnosed laparoscopically. She had a stapled closure of the rectum and sigmoid colostomy, which was taken down 3 months later. The authors proposed that increased intra-abdominal pressure and decidualization of endometriotic nodules in pregnancy were responsible. This is another case of multifocal involvement in the face of increased hormone exposure. Chowdhury and Yue26 found that 42.8% of bowel perforations from EC were in pregnancy, because progestogens, which should cause a regression of the nodules, promoted decidualization and atrophy, and rallowed for stercoral perforations.

Reports of intestinal obstruction without perforation are more common. Lin et al.10 reported a case of a 33-year-old nulliparous woman with a prior history of endometriosis who underwent hysterectomy and right salpingo-oophorectomy. She presented with passage of loose stools during menses, alternating with constipation at other times. She developed obstructive symptoms. Abdominopelvic CT showed regional ascites and a rectosigmoid lesion. Lower gastrointestinal endoscopy showed a stricture 10 cm above the anal verge and an irregular mucosal swelling. Pelvic MRI showed regional wall thickening of the sigmoid colon spanning 6 cm. CA-125 was elevated but CEA levels were normal (52.2 IU/ml and 0.8 ng/ml, respectively). Colonoscopic biopsy was negative. A transverse colostomy relieved the obstruction and later laparotomy revealed the upper rectum encased by adhesions, an endometrioma of the right ovary and multiple inferior mesenteric lymph nodes. She had colonic resection and colorectal anastomosis with excision of the endometrioma. Histology was reported as endometrial glands and stroma involving the submucosa, muscle, subserosal fat and adipose tissue. The patient’s colostomy was taken down 3 months later.

Investigating EC

The investigation of choice is still debatable, but most authors recommend laparoscopy as the gold standard.10,12,26,29 Samet et al.9 reported a case of sigmoid endometriosis in a 51-year-old woman who presented with change in bowel habits, haematochezia and abdominal pain. She had a history of pelvic endometriosis and infertility. A complete colonoscopic evaluation was not possible because of stenosis of the sigmoid colon, necessitating the use of virtual colonoscopy. This revealed an apple core deformity in the sigmoid, with left colonic wall nodularity and segment thickening. The patient developed intestinal obstruction within a week of presentation and underwent surgery. Intraoperative findings were a 3 cm mass involving the bladder and sigmoid colon. Pathological examination of the specimen showed endometriosis with full-thickness bowel wall hyperplasia and lymph node involvement. There was no evidence of malignancy. This is one of the few reports of mucosal involvement by endometriosis.

According to Dimoulios et al.,21 the clinical, radiological and endoscopic picture of endometriosis of the colon may be confused with neoplasms, ischaemic colitis, inflammatory bowel disease, post-radiation colitis, diverticular disease or infection. Even though endoscopic diagnosis of colonic endometriosis had been reported by Bozdech,89 quite often the endoscopic appearance, even if there is mucosal involvement, is not diagnostic.10,13 In the case reported by Lin et al.,10 the initial biopsy taken during a lower gastrointestinal series failed to reveal endometriosis.10 The timing of the colonoscopy and biopsy in relation to the menstrual cycle determines diagnostic potential. In the case report by Dimoulios et al.,21 the diagnosis was made only when the biopsy was taken on the 20th day of the cycle.

As reported by Scully et al.,90 biopsies obtained by means of endoscopy usually yield insufficient tissue for definite pathological diagnosis. Furthermore, some authors91,92 reported that endometriotic deposits can induce secondary mucosal changes, which mimic findings of other diseases, such as inflammatory bowel disease, ischaemic colitis or even a neoplasm, increasing the non-specificity of endoscopy.

Caecal endometriosis may be misdiagnosed as appendicitis.17 Otaghvar et al.17 reported the case of a 43-year-old woman who presented with a 1-day history of right lower quadrant abdominal pain diagnosed as appendicitis. Intraoperatively, however, a 3-cm brown mass was found on the caecum with mesoappendiceal lymphadenopathy. She then underwent right hemicolectomy for the suspected caecal tumour, which histological examination revealed to be EC.

Treatment options

As regards treatment, a relative algorithm exists. According to Urbach et al.,93 the treatment options for endometriosis of the colon include surgery or hormonal manipulations, depending upon the age of the patient, the patient’s desire to maintain fertility and also the severity and complications of the disease. With regard to surgical treatment, it has been reported that laparoscopic surgical treatment of colorectal endometriosis inclusive of advanced stages of the disease is feasible and effective in almost all patients, and results in fewer side-effects and better fertility rates than traditional techniques.12,94 Benbara et al.38 reported that only 8 of 20 patients who underwent open resection of rectal endometriotic lesions subsequently conceived naturally. They stated that the medications used in the management of endometriosis, such as danazol, high-dose progestins and GnRH agonists, have equivalent efficacy.21,38,95 It has also been stated that the choice of which medication to use in the treatment of endometriosis of the colon is guided by the side-effects and costs; danazol and GnRH agonists are of equivalent cost but GnRH agonists are usually better tolerated.13 Whatever the basis for drug recommendation, the patient’s informed choice may need to be followed.21

Endometriosis of the colon and race

Africans, Hispanics and Asians have a much lower incidence of endometriosis than Caucasians.42 Forty-nine per cent of the EC cases reviewed occurred in Caucasians. Reports in blacks or from Africa are uncommon.66,96 It is uncertain if the disease is rare or the database is inadequate. Weed97 reported no significant racial disparity in the prevalence of endometriosis. In our literature search we found only a single report of bowel endometriosis in a 29-year-old Negroid Nigerian woman.

Misdiagnosis of endometriosis as fibroids in black women has also been implicated in the apparent racial disparity.98 A common misdiagnosis is fibroids.98 Another example of misdiagnosis in the literature involved a 23-year-old Indian woman who presented with a 6-month history of recurrent cramping abdominal pain and a 1-week history of abdominal distension and vomiting. The patient was thought to have abdominal tuberculosis complicated by bowel perforation and an emergency ileostomy was carried out. Later investigations found a stricturing sigmoid colonic lesion, which was resected, and there was histological evidence of endometriosis.65

Many other cases of endometriosis of the colon have been reported with a variety of presentations, some of which have been purely endometriosis and others have been associated with other lesions (see Table 2).

Conclusion

Reports in Negroids are rare. The sigmoid and rectosigmoid are the most common sites for EC. The muscularis propria is the most common site of EC, whereas mucosal involvement is the least common. Mucosal involvement is more likely with rectosigmoid EC. The most common presentations are abdominal pain and intestinal obstruction. Intestinal perforations are uncommon, but the risk increases with pregnancy. Multifocal involvement is rare. The risk of associated cancer is low but increases with post-menopausal status. No report of EC was found in males.

Acknowledgements

We wish to acknowledge:

The World Journal of Gastrointestinal Surgery and the Baishideng Publishing Group, Inc., which granted copyright permission for reproduction of contents from their journal under the Creative Commons Attribution Licence for non-commercial use.

The Korean Journal of Pathology, which granted copyright permission for reproduction of content, including figures from their journal under the Creative Commons Attribution Non-Commercial Licence for non-commercial use.

The editorial board of Case Reports in Surgery, which granted copy right permission under the Creative Commons Attribution Licence enabling the unrestricted use and distribution of articles in any medium provided the original work is properly cited.

Jespersen and Associates LLC and the Association of Professors of Obstetrics and Gynaecology, which granted copyright permission for reproduction of their figure under the Creative Commons Attribution-Non-Commercial Licence which permits use, distribution and reproduction in any medium provided the original work is properly cited, the use is non-commercial and is otherwise in compliance with the licence.

Dr Nat Pernick, President of PathologyOutlines.com, for directing the authors to the original source of some of the figures in Figure 2.

Case Reports in Medicine (a Hindawi Publishing Corporation open access journal), which granted copyright permission for figures from their journal to be reproduced under the Creative Commons Attribution Licence for non-commercial use provided the original work is properly cited.

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