Deep endometriosis (DE) is one of three phenotypes of endometriosis in addition to peritoneal endometriosis and ovarian endometriosis.
Abstract: Ultrasonography is the first line tool to diagnose bowel endometriosis and is useful to assess extent of endometriosis before surgical treatment. Bowel endometriosis lesions appear as hypoechoic lesions or thickenings of the bowel wall. Or they may be solid lesions varying in size with regular or irregular contours. Extent of endometriosis to consider before bowel surgery is firstly lesion size that can be decisive in choice of surgical technique. Secondly the distance from the inferior border of the bowel lesion to the anal verge which represents an estimate of the anastomosis height. Detailed anatomy mapping with ultrasound to evaluate extent of bowel endometriosis involvement should be performed.
Keywords: Bowel endometriosis, deep endometriosis, ultrasonography, IDEA terminology
Authors: Mee Kristine Aas-Eng1
- Department of Obstetrics and Gynecology, Oslo University Hospital, Oslo, Norway
Reviewed by: Mathew Leonardi and Karen Fung-Kee-Fung
Endometriosis is defined as endometrium-like glands and stroma outside the uterus (1). It clinically presents with cyclical or chronic pelvic pain and/or infertility. Deep endometriosis (DE) is one of three phenotypes of endometriosis in addition to peritoneal endometriosis and ovarian endometriosis (2). A recent AAGL, ESHRE and WES consensus defines DE as “endometrium-like tissue lesions in the abdomen, extending on or under the peritoneal surface. They are usually nodular, able to invade adjacent structures, and associated with fibrosis and disruption of normal anatomy” (1). This is different to peritoneal endometriosis on the bowel that is superficial peritoneal lesions not DE (1). Bowel endometriosis is most commonly located on the rectum (3).
N80.4: endometriosis of rectovaginal septum and vagina
N80.5: endometriosis of intestine
The prevalence of bowel endometriosis is 5-12% among women and individuals assigned female at birth that have been treated surgically for endometriosis (4), with up to 71% located on the rectosigmoid (3). Other gastrointestinal locations are the ileum, cecum and appendix (3). A French nationwide study found that 10-20% bowel surgery was performed in women treated surgically for endometriosis (5). In a retrospective study based on transvaginal ultrasound (TVS) examination of 373 women symptomatic of endometriosis found an 8% prevalence of bowel endometriosis (6).
The origin of bowel endometriosis remains unclear although it is likely multifactorial. In the past the most common theory was retrograde menstruation and metaplasia. With Sampson’s theory implantation of serosal endometrial cells into the muscularis layer is aided by repeated tissue injury and repair causing smooth muscle hyperplasia and fibrosis (7-9). Histologically bowel endometriosis involves most commonly the bowel muscularis layer, rarely affecting the mucosa (10). Thus, rectal bleeding is rare among individuals with bowel endometriosis. Thickening of the bowel wall and adhesions may cause a narrowing of the bowel lumen may in the worst cases lead to obstructive symptoms (11).The retrograde theory is further supported based on observations of the distribution of bowel endometriosis being most commonly located in the left posterior compartment (3) as the rectosigmoid and left adenexa that act as a barrier of retrograde menstruation leading to accumulation of blood in the peritoneal fluid (12). However, retrograde mentrutration is a normal physiological phenomenon as 90% of women have blood in their peritoneal fluid (13). Metaplasia has been proposed as alternative theory that endometriosis derives from peritoneal cells (14) or Müllerian remnants (15). Deep endometriosis has been proposed to be adenomyosis externa being histologically different to the other phenotypes based on histological studies of endometriosis of the rectovaginal septum found the presence of smooth muscle, as well as endometrial glands, similar to adenomyotic lesions (15). Although others have argued that deep enometriosis develops intraperitoneally and not from the rectovaginal septum (16). However, the adenomyosis externa theory has been challenged as smooth muscle components is found in other locations of endometriosis (17). The complexity of the origin of endometriosis is emphasised by evidence of lymphatic spread of endometrial cells among individuals with deep posterior compartment disease that may explain extra-pelvic presence of endometriosis (18).
The recent genetic-epigenetic (GE) theory suggests that GE predispostion and incidents need to occur to iniate progression of the three phenotypes of endometriosis (19). The aggressive nature of bowel endometriosis may be explained by cancer associated mutations found in epithelial cells (20). GE theory can explain why not all individuals with retrograde menstruation and implantation get endometriosis. Previously predisposing factors may instead be the result of GE changes causing insults, like differences in the endometrium among individuals with endometriosis, or biochemical or immunological factors influencing the development of peritoneal, ovarian and DE (19).
Clinical history and examination are fundamental in diagnosising bowel endometriosis. Individuals may report deep dysparunia, cyclical or chronic pelvic pain, dyschezia and altered bowel habits. Altough some individuals may be asymptomatic. Non-cyclical chronic pelvic pain is more common agong individuals with bowel endometriosis (21). Gastrointetinal complaints may occur among individuals withouth DE (22). This makes diagnosis challenging as individuals with bowel endometriosis have similar symptoms like bloating and alereted bowel habits to that of inflammatory bowel disease (23). Severity of dyschezia is correlated with rectosigmoid lesion size as defined by the revised Enzian classificaiton (24). Recently there has been a shift in diagnosis moving away from diagnostic laparoscopy to imaging with TVS and/or magnetic resonance imaging as the gold-standard for diagnosing DE (25, 26). Diagnosis of bowel endometriosis and describing DE extent is important in counselling and optimizing management of bowel endometriosis (27).
The International Deep Endometriosis Analysis (IDEA) group consensus states how to describe and measure ultrasonographic features of DE (28). It divides the pelvis into the anterior and posterior compartment. Bowel endometriosis is located in the posterior compartment. Bowel endometriosis is characterized by hypoechoic thickening of muscularis propria, or as hypoechoic solid nodules with or without hyperechoic foci (28). To assist in identifing bowel endometriosis, the “sliding sign” can be applied by assessing if the rectum slides or is adherent to the retrocervical region and/or uterus (28, 29). A negative sliding sign means that the bowel is adherent and indicates Pouch of Douglas obliteration increasing the risk of bowel endometriosis (29-31). The presence of endometriomas can guide the clinician to look for bowel endometriosis as endometriomas indicates increased disease severity (32).
Bowel endometriosis can be isolated, multfocal, i.e. multipe lesions affecting the same segment of the bowel, and/or multicentric, i.e. multipe lesions affecting several bowel segments (28). A morphological description of type of lesion is recommended i.e. like the comet, moose antler sign and the distance from the inferior part of the lesion to the anal verge (28). Additionally, lesion length, thickness and tranverse measurements is advised (28). There are several classifications systems for endometriosis (33). The #Enzian classification is currently the only classification describing peritoneal, ovarian and DE(27) that correlates with pre-operative findings (34).
The aim of treatment is to alleviate symptoms and improve feritlity and should be tailored to inividual needs. Treatment of bowel endometriosis can be divided into medical and surgical treament. Endometriosis associated pain is complex to treat but first line management is usually medical treatment with analgesics and hormonal treatment, unless the individual has fertility wish (25, 35). If medical treatment fails and/or if the individual have symptoms of sub-occlusion surgical treatment may be necessary (36, 37). When considering surgical managment of bowel endometriosis the distance between the inferior border of the lesion and the anal verge can be measured using transvaginal ultrasonography (21). This is an important marker for estimating anastomosis height and assessing the risk of complications like anastomotic leakage and rectovaginal fistula (38, 39). Type of bowel procedure performed can be guided according to lesion size measured with ultrasongraphy (40, 41). Bowel procedures can generally be divided into three types. Firstly, shaving, which is cutting away the bowel lesion and fibrosis withtout entering the bowel lumen. Whilst discoid excision and segmental resections opens the bowel lumen and removing the lesion and is associated with a higher risk of complications (39, 42).
Bowel endometriosis rarely occurs alone and is associated with increased disease severity and pain (24). It is a benign disease that may have a significant impact on the quality of life and fertlity which poses a socioeconomic burden on the individual but also on their families and society (43). Individuals with all types of endometriosis have an increased risk of ovarian cancer, in particular endometroid and clear cell carcinomas (44). The risk of ovarian cancer is highest among women with ovarian endometriomas (44). However, no incrased risk of gynecological cancers was found for peritoneal or DE (44). DE is not associated with an increased risk of other types of cancers (45).
Disease development for bowel endometriosis is not yet established and can progress despite hormonal treatment (46, 47). However, some argue that lesion growth is self-limited and does not grow rapidly (48).The risk of recurrence of bowel endometriosis is higher among women treated with shaving compared to the other two techinques most likely due to residual disease (49). Pouch of Douglas obliteration diagnosed on TVS after bowel surgery may raise suspicion of residual disease or recurrence of bowel endometriosis (50, 51).
Bowel endometriosis may share similar symptoms to rectal cancer, inflammatory bowel disease, diverticulitis and irritable bowel syndrome, like abdominal pain, bloating, altered bowel habits and rarely rectal bleedning (23, 52). However, bowel endometriosis usually presents in women of reproductive age with worsening of pain and gastrointestinal symptoms during menstrual cycle or ovulation or that may have become chronic. Unlike rectal cancer bowel endometriosis usually is located on the anterior rectal wall and rarely penetrates the mucosa (53), whilst rectal cancer can be located on any part of the circumference of the bowel wall (54).
1. International working group of AAGL E, ESHRE, WES, Vermeulen N, Abrao MS, Einarsson JI, Horne AW, et al. Endometriosis classification, staging and reporting systems: a review on the road to a universally accepted endometriosis classification†,‡. Human Reproduction Open. 2021;2021(4).
2. Nisolle M, Donnez J. Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities. Fertility and Sterility. 1997;68(4):585-96.
3. Chapron C, Chopin N, Borghese B, Foulot H, Dousset B, Vacher-Lavenu MC, et al. Deeply infiltrating endometriosis: pathogenetic implications of the anatomical distribution. Hum Reprod. 2006;21(7):1839-45.
4. Gray LA. Endometriosis of the bowel: role of bowel resection, superficial excision and oophorectomy in treatment. Ann Surg. 1973;177(5):580-7.
5. von Theobald P, Cottenet J, Iacobelli S, Quantin C. Epidemiology of Endometriosis in France: A Large, Nation-Wide Study Based on Hospital Discharge Data. BioMed Research International. 2016;2016:3260952.
6. Orlov S, Jokubkiene L. Prevalence of endometriosis and adenomyosis at transvaginal ultrasound examination in symptomatic women. Acta Obstetricia et Gynecologica Scandinavica. 2022;101(5):524-31.
7. Sampson JA. Heterotopic or misplaced endometrial tissue. American Journal of Obstetrics and Gynecology. 1925;10(5):649-64.
8. Zhang Q, Duan J, Olson M, Fazleabas A, Guo SW. Cellular Changes Consistent With Epithelial-Mesenchymal Transition and Fibroblast-to-Myofibroblast Transdifferentiation in the Progression of Experimental Endometriosis in Baboons. Reprod Sci. 2016;23(10):1409-21.
9. Meuleman C, Tomassetti C, D'Hoore A, Van Cleynenbreugel B, Penninckx F, Vergote I, et al. Surgical treatment of deeply infiltrating endometriosis with colorectal involvement. Hum Reprod Update. 2011;17(3):311-26.
10. Kavallaris A, Köhler C, Kühne-Heid R, Schneider A. Histopathological extent of rectal invasion by rectovaginal endometriosis. Hum Reprod. 2003;18(6):1323-7.
11. Katsikogiannis N, Tsaroucha A, Dimakis K, Sivridis E, Simopoulos C. Rectal endometriosis causing colonic obstruction and concurrent endometriosis of the appendix: a case report. J Med Case Rep. 2011;5:320.
12. Vercellini P, Chapron C, Fedele L, Gattei U, Daguati R, Crosignani PG. Evidence for asymmetric distribution of lower intestinal tract endometriosis. Bjog. 2004;111(11):1213-7.
13. Halme J, Hammond MG, Hulka JF, Raj SG, Talbert LM. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol. 1984;64(2):151-4.
14. Gruenwald P. Origin of endometriosis from the mesenchyme of the celomic walls. American Journal of Obstetrics and Gynecology. 1942;44(3):470-4.
15. Donnez J, Nisolle M, Casanas-Roux F, Bassil S, Anaf V. Rectovaginal septum, endometriosis or adenomyosis: laparoscopic management in a series of 231 patients. Hum Reprod. 1995;10(3):630-5.
16. Vercellini P, Aimi G, Panazza S, Vicentini S, Pisacreta A, Crosignani PG. Deep endometriosis conundrum: evidence in favor of a peritoneal origin. Fertil Steril. 2000;73(5):1043-6.
17. Anaf V, Simon P, Fayt I, Noel J-C. Smooth muscles are frequent components of endometriotic lesions. Human Reproduction. 2000;15(4):767-71.
18. Keichel S, Barcena de Arellano ML, Reichelt U, Riedlinger WF, Schneider A, Köhler C, et al. Lymphangiogenesis in deep infiltrating endometriosis. Hum Reprod. 2011;26(10):2713-20.
19. Gordts S, Koninckx P, Brosens I. Pathogenesis of deep endometriosis. Fertil Steril. 2017;108(6):872-85.e1.
20. Anglesio MS, Papadopoulos N, Ayhan A, Nazeran TM, Noë M, Horlings HM, et al. Cancer-Associated Mutations in Endometriosis without Cancer. N Engl J Med. 2017;376(19):1835-48.
21. Aas-Eng MK, Dauser B, Lieng M, Diep LM, Leonardi M, Condous G, et al. Transvaginal sonography accurately measures lesion-to-anal-verge distance in women with deep endometriosis of the rectosigmoid. Ultrasound Obstet Gynecol. 2020;56(5):766-72.
22. Roman H, Ness J, Suciu N, Bridoux V, Gourcerol G, Leroi AM, et al. Are digestive symptoms in women presenting with pelvic endometriosis specific to lesion localizations? A preliminary prospective study. Hum Reprod. 2012;27(12):3440-9.
23. Chiaffarino F, Cipriani S, Ricci E, Roncella E, Mauri PA, Parazzini F, et al. Endometriosis and inflammatory bowel disease: A systematic review of the literature. Eur J Obstet Gynecol Reprod Biol. 2020;252:246-51.
24. Montanari E, Dauser B, Keckstein J, Kirchner E, Nemeth Z, Hudelist G. Association between disease extent and pain symptoms in patients with deep infiltrating endometriosis. Reprod Biomed Online. 2019;39(5):845-51.
25. ESHRE. Guideline Endometriosis 2022. [Available from: https://www.eshre.eu/Guidelines-and-Legal/Guidelines/Endometriosis-guideline (Acessed 1st May 2022).
26. Goncalves MO, Siufi Neto J, Andres MP, Siufi D, de Mattos LA, Abrao MS. Systematic evaluation of endometriosis by transvaginal ultrasound can accurately replace diagnostic laparoscopy, mainly for deep and ovarian endometriosis. Human Reproduction. 2021;36(6):1492-500.
27. Keckstein J, Saridogan E, Ulrich UA, Sillem M, Oppelt P, Schweppe KW, et al. The #Enzian classification: A comprehensive non-invasive and surgical description system for endometriosis. Acta Obstet Gynecol Scand. 2021;100(7):1165-75.
28. Guerriero S, Condous G, van den Bosch T, Valentin L, Leone FP, Van Schoubroeck D, et al. Systematic approach to sonographic evaluation of the pelvis in women with suspected endometriosis, including terms, definitions and measurements: a consensus opinion from the International Deep Endometriosis Analysis (IDEA) group. Ultrasound Obstet Gynecol. 2016;48(3):318-32.
29. Hudelist G, Fritzer N, Staettner S, Tammaa A, Tinelli A, Sparic R, et al. Uterine sliding sign: a simple sonographic predictor for presence of deep infiltrating endometriosis of the rectum. Ultrasound in Obstetrics & Gynecology. 2013;41(6):692-5.
30. Khong SY, Bignardi T, Luscombe G, Lam A. Is pouch of Douglas obliteration a marker of bowel endometriosis? J Minim Invasive Gynecol. 2011;18(3):333-7.
31. Reid S, Lu C, Casikar I, Reid G, Abbott J, Cario G, et al. Prediction of pouch of Douglas obliteration in women with suspected endometriosis using a new real-time dynamic transvaginal ultrasound technique: the sliding sign. Ultrasound Obstet Gynecol. 2013;41(6):685-91.
32. Banerjee SK, Ballard KD, Wright JT. Endometriomas as a marker of disease severity. J Minim Invasive Gynecol. 2008;15(5):538-40.
33. Aas-Eng MK, Keckstein J, Condous G, Abrão MS, Hudelist G. Deep endometriosis: Can surgical complexity and associated risk factors be evaluated with transvaginal sonography and classification systems? European Journal of Obstetrics & Gynecology and Reproductive Biology. 2022;276:204-6.
34. Hudelist G, Montanari E, Salama M, Dauser B, Nemeth Z, Keckstein J. Comparison between Sonography-based and Surgical Extent of Deep Endometriosis Using the Enzian Classification - A Prospective Diagnostic Accuracy Study. J Minim Invasive Gynecol. 2021;28(9):1643-9.e1.
35. Maddern J, Grundy L, Castro J, Brierley SM. Pain in Endometriosis. Front Cell Neurosci. 2020;14:590823.
36. Ferrero S, Camerini G, Ragni N, Venturini PL, Biscaldi E, Remorgida V. Norethisterone acetate in the treatment of colorectal endometriosis: a pilot study. Hum Reprod. 2010;25(1):94-100.
37. Working group of ESGE E, WES, Keckstein J, Becker CM, Canis M, Feki A, et al. Recommendations for the surgical treatment of endometriosis. Part 2: deep endometriosis †‡¶. Human Reproduction Open. 2020;2020(1).
38. Abrão MS, Petraglia F, Falcone T, Keckstein J, Osuga Y, Chapron C. Deep endometriosis infiltrating the recto-sigmoid: critical factors to consider before management. Human Reproduction Update. 2015;21(3):329-39.
39. Bendifallah S, Puchar A, Vesale E, Moawad G, Daraï E, Roman H. Surgical Outcomes after Colorectal Surgery for Endometriosis: A Systematic Review and Meta-analysis. J Minim Invasive Gynecol. 2021;28(3):453-66.
40. Aas-Eng MK, Lieng M, Dauser B, Diep LM, Leonardi M, Condous G, et al. Transvaginal sonography determines accurately extent of infiltration of rectosigmoid deep endometriosis. Ultrasound Obstet Gynecol. 2021;58(6):933-9.
41. Malzoni M, Casarella L, Coppola M, Falcone F, Iuzzolino D, Rasile M, et al. Preoperative Ultrasound Indications Determine Excision Technique for Bowel Surgery for Deep Infiltrating Endometriosis: A Single, High-Volume Center. J Minim Invasive Gynecol. 2020;27(5):1141-7.
42. Hudelist G, Tammaa A, Aas-Eng MK, Kirchner L, Fritzer N, Nemeth Z, et al. Outcome of sonography-based minimally invasive surgery for deep infiltrating endometriosis of the ureter and urinary bladder - a retrospective cohort study. Acta Obstet Gynecol Scand. 2018;97(3):277-84.
43. Nnoaham KE, Hummelshoj L, Webster P, d'Hooghe T, de Cicco Nardone F, de Cicco Nardone C, et al. Impact of endometriosis on quality of life and work productivity: a multicenter study across ten countries. Fertil Steril. 2011;96(2):366-73 e8.
44. Saavalainen L, Lassus H, But A, Tiitinen A, Härkki P, Gissler M, et al. Risk of Gynecologic Cancer According to the Type of Endometriosis. Obstet Gynecol. 2018;131(6):1095-102.
45. Saavalainen L, Lassus H, But A, Tiitinen A, Härkki P, Gissler M, et al. A Nationwide Cohort Study on the risk of non-gynecological cancers in women with surgically verified endometriosis. International Journal of Cancer. 2018;143(11):2725-31.
46. Millochau JC, Abo C, Darwish B, Huet E, Dietrich G, Roman H. Continuous Amenorrhea May Be Insufficient to Stop the Progression of Colorectal Endometriosis. J Minim Invasive Gynecol. 2016;23(5):839-42.
47. Egekvist AG, Marinovskij E, Forman A, Kesmodel US, Graumann O, Seyer-Hansen M. Conservative treatment of rectosigmoid endometriosis: A prospective study. Acta Obstet Gynecol Scand. 2019;98(9):1139-47.
48. Koninckx PR, Ussia A, Wattiez A, Adamyan L, Martin DC, Gordts S. The severity and frequency distribution of endometriosis subtypes at different ages: a model to understand the natural history of endometriosis based on single centre/single surgeon data. Facts Views Vis Obgyn. 2021;13(3):209-19.
49. Bendifallah S, Vesale E, Daraï E, Thomassin-Naggara I, Bazot M, Tuech JJ, et al. Recurrence after Surgery for Colorectal Endometriosis: A Systematic Review and Meta-analysis. J Minim Invasive Gynecol. 2020;27(2):441-51.e2.
50. Martire FG, Zupi E, Lazzeri L, Morosetti G, Conway F, Centini G, et al. Transvaginal Ultrasound Findings After Laparoscopic Rectosigmoid Segmental Resection for Deep Infiltrating Endometriosis. Journal of Ultrasound in Medicine. 2021;40(6):1219-28.
51. Alhayo S, Leonardi M, Lu C, Gosal P, Reid S, Barto W, et al. Ultrasound evaluation of pouch of Douglas obliteration and rectal deep endometriosis in women who have had previous combined colorectal and gynaecological laparoscopic surgery for rectal endometriosis: A pilot study. Australian and New Zealand Journal of Obstetrics and Gynaecology. 2020;60(2):258-63.
52. Chiaffarino F, Cipriani S, Ricci E, Mauri PA, Esposito G, Barretta M, et al. Endometriosis and irritable bowel syndrome: a systematic review and meta-analysis. Arch Gynecol Obstet. 2021;303(1):17-25.
53. 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(5):1012-7.
54. Horvat N, Rocha CCT, Oliveira BC, Petkovska I, Gollub MJ. MRI of Rectal Cancer: Tumor Staging, Imaging Techniques, and Management. RadioGraphics. 2019;39(2):367-87.
This article should be cited as: Aas-Eng, MK: Bowel endometriosis, Visual Encyclopedia of Ultrasound in Obstetrics and Gynecology, www.isuog.org, September 2022.
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