Journal of Medical Imaging and Radiation Oncology

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Journal of Medical Imaging and Radiation Oncology 61 (2017) 767 773 MEDICAL IMAGING PICTORIAL ESSAY MRI findings in deep infiltrating endometriosis: A pictorial essay Anitha L Thalluri, 1 Steven Knox

University of Adelaide, Adelaide, South Australia, Australia AL Thalluri MBBS; S Knox MBBS FRANZCR; T Nguyen MBBS FRANZCR.

1 Journal of Medical Imaging and Radiation Oncology 61 (2017) MEDICAL IMAGING PICTORIAL ESSAY MRI findings in deep infiltrating endometriosis: A pictorial essay Anitha L Thalluri, 1 Steven Knox 1,2,3 and Thi Nguyen 2,3 1 Department of Radiology, Royal Adelaide Hospital, Adelaide, South Australia, Australia 2 Benson Radiology, Adelaide, South Australia, Australia 3 Department of Medicine, University of Adelaide, Adelaide, South Australia, Australia AL Thalluri MBBS; S Knox MBBS FRANZCR; T Nguyen MBBS FRANZCR. Correspondence Dr Anitha L Thalluri, Department of Radiology, Level 3, Royal Adelaide Hospital, North Terrace, Adelaide, SA 5000, Australia. anitha.thalluri@gmail.com Conflict of interest: None. Submitted 28 January 2017; accepted 4 September doi: / Introduction Endometriosis is a chronic gynaecological disorder characterized by the presence of endometrial mucosa outside of the uterine cavity. 1 It affects approximately 10% of women during reproductive age and is found in 20 50% of women with infertility and approximately 90% of women with chronic pelvic pain. 1 Imaging is useful in confirming the diagnosis and staging the extent of pelvic disease, which can be underestimated on clinical grounds alone. MRI is considered more accurate than ultrasound in viewing complex and severe cases of endometriosis. 1 Deep infiltrating endometriosis is a characterized by endometriotic tissue invasion to a depth of more than 5 mm. 2 This may result in obliteration of anatomic compartments secondary to fibrosis and adhesions. MRI can have a key role in pre-surgical mapping of suspected complex endometriosis, and in advanced cases, can assist in planning gynaecologic surgical approach and the potential need for multispecialty involvement. The imaging findings of endometriosis relate to either direct visualization of the ectopic endometriotic deposits or the fibrosis and regional anatomical distortion which occurs due to repeated cycles of haemorrhage and inflammation. Summary Endometriosis is an important gynaecological disorder which can impact significantly on an individual s quality of life and has major implications on fertility. Deep infiltrating endometriosis is a severe form of endometriosis which can cause obliteration of anatomic compartments. Laparoscopy remains the gold standard for diagnosis of endometriosis, although is an invasive procedure that has the potential to be hindered by obliterative disease. Ultrasound is often employed as the first-line imaging modality when endometriosis is suspected, however, MRI is more accurate in assessment of complex disease. Pre-operative MRI is highly specific in the diagnosis of endometriosis and characterization of disease extent, and plays a key role in guiding surgical management. MRI findings in deep infiltrating endometriosis are described. Key words: endometriosis; female; fertility; gynaecology; magnetic resonance imaging. MRI scan technique At our institution, endometriosis characterization on MRI is achieved through the acquisition of multi-planar T2- weighted images (T2WI) and T1-weighted images (T1WI). Post-gadolinium and diffusion-weighted sequences are not acquired unless unexpected pathology (including suspicion for pelvic malignancy or sepsis) is identified. The patient is fasted for four hours and if possible, a moderately filled bladder is recommended. Transvaginal gel is not typically employed. At the time of imaging, a spasmolytic agent (hyoscine butylbromide 40 mg IV in 2 ml) is administered (unless contraindicated), to reduce image degradation from regional peristalsis. Our scan protocol is listed in Table 1. Scan time is usually achieved within 30 minutes. The following are MRI findings in deep infiltrating endometriosis (Table 2). MRI features of pelvic endometriosis Posterior cul-de-sac obliteration The posterior cul-de-sac (recto-uterine pouch) represents the lowest portion of the abdomino-pelvic cavity in Journal of Medical Imaging and Radiation Oncology 767

2 AL Thalluri et al. Table 1. Pre-menopausal pelvic MRI suggested protocol (in order of acquisition) Conventional Cartesian sagittal T2WI TSE T2WI 3-D volumetric (SPACE) sequence T1WI axial TSE T1WI VIBE Dixon Repeat T2WI sagittal sequence Time of repetition (ms) Parameters as per Time of echo (ms) Slice thickness (mm) Gap (mm) 1 n/a 1.8 n/a Pixel size (mm) Averages Slices per slab Phase direction H-F H-F R-L A-P Echo spacing (ms) n/a Field of view Scan time 4:02 4: Conventional Cartesian sagittal T2WI TSE the supine position. 3,4 Disease here is responsible for the majority of symptomatic cases of endometriosis 3 and may significantly hinder laparoscopic assessment and treatment due to poor access and visualization as result of compartment obliteration. 5 On MRI, posterior cul-de-sac disease is characterized by endometrial plaques which display T1 hyperintensity and variable T2 signal, dependent on the composition of haemorrhage, glandular content and fibrosis. Active haemorrhagic endometrial implants typically appear hyperintense on T1WI and T2WI, relative to adjacent muscle due to a high glandular/blood content. Regions of chronic dense fibrosis appear hypointense on all sequences due to a higher composition of fibrosis and smooth muscle hypertrophy. In advanced cases, regional fibrosis may result in dense adhesions between the uterosacral ligaments, uterine serosa, ovaries, rectum and vagina, with obliteration of the recto-uterine pouch (Fig. 1). 5 Adhesions may appear as subtle low signal strands between organs and bowel loops. MRI accuracy has been reported as 71.9% in demonstrating features of posterior cul-de-sac obliteration and 61.4% for highlighting adhesions in the posterior cul-de-sac. 5 Upper rectal distortion Intestinal endometriosis occurs in 12 37% of endometriosis patients 1 with the rectosigmoid colon the most commonly affected region. 2 Clinical features vary from mild to severe and include cyclical abdominal pain, constipation/diarrhoea, dyschezia and haematochezia. 6 Implants are usually serosal and have the potential to erode through the sub-serosal layers (although will rarely involve the mucosa), with resultant thickening and fibrosis of the muscularis propria. 2 Cyclical haemorrhage and intermittent leakage of endometriotic contents result in a chronic inflammatory reaction leading to the formation of adhesions and bowel strictures. A pre-operative diagnosis of bowel involvement may highlight the need for colorectal input should bowel resection be required. 2 On MRI, bowel adhesions are visualized similar to posterior cul-de-sac adhesions; there may be clustering or tethering of bowel loops with direct bands, poor interface visualization and loss of pericolic or peri-mesenteric fat planes (Fig. 2a). 5 The mushroom cap sign is considered a characteristic feature of severe invasive endometriosis of the rectosigmoid on T2WI. 7 This consists of a low signal intensity base of the mushroom, due to hypertrophy and fibrosis of the muscularis propria, and a high intensity cap, representing the mucosa and submucosa which have been displaced into the bowel lumen (Fig. 2b). 7 Ovarian endometriomas Endometriomas represent thick-walled cysts, containing degenerated blood products. They can involve a variety of pelvic locations with the majority occurring within the ovaries. MRI is the best imaging modality for identifying endometriomas, with a specificity of 98%. 8 Endometriomas appear hyperintense to water on T1WI pre- and post-fat saturation (Fig. 3a), and are T2 hypointense when compared to normal adjacent ovarian follicles. 5,7 The T2 hypointensity ( shading sign ) is related to the high concentration of protein and iron from cyclical haemorrhage, and in combination with T1 hyperintensity, is highly suggestive of endometriomas (Fig. 3b). 1,9 The shading sign can vary from faint, layered signal loss to complete signal loss, depending on the concentration of blood degradation products. 10 The shading sign helps to differentiate between endometriomas and other blood containing lesions, such as haemorrhagic adnexal cysts, with a diagnostic accuracy of 91 96%. 10 Haemorrhagic adnexal cysts are hyperintense on T1WI like endometriomas, but are brighter on T2WI in comparison to endometriomas. The fluid in physiologic haemorrhagic cysts is less viscous with a lower protein/iron content, and shading is less likely to be present. Haemorrhagic cysts are also usually unilocular, thin walled and resolve with time whilst endometriomas are more commonly large, multilocular, thick-walled and chronic

3 MRI in deep infiltrating endometriosis Table 2. Summary of MRI findings in deep infiltrating endometriosis Finding MRI findings Comments Posterior cul-de-sac obliteration Endometrial plaques: T1 T2 variability Dense adhesions between uterosacral ligaments, uterine serosa, ovaries, rectum and vagina: Responsible for majority of symptomatic endometriosis A feature of severe disease May limit surgical visualization T1 & T2 Haematosalpinx T1 within dilated fallopian tube Highly specific feature of endometriosis Strong association with infertility Ovarian endometrioma Uterine serosal plaque Elevated vaginal fornices Fixed anteversion or retroflexion Upper rectal distortion Thickened uterosacral ligament Large, often multilocular, thick-walled, cystic lesion T2 ( shading sign ) and T1 is pathognomonic for endometriomas medialized ovaries T1 due to haemorrhagic/proteinaceous content. T2 suggests cystic areas with active glandular deposits T1 T2 suggests predominantly fibrous component Enhancement post-gadolinium administration Upper level of fornix superior to angle of the uterine isthmus Acute angulation of fornix Fornix pulled in superior direction with stretching of vaginal wall Thickening of superior 1/3 of posterior vaginal wall nodularity Nodules: T2 T1 (if active haemorrhagic deposits) Anteversion: T1 T2 nodules/bands on anterior uterine wall Anterior cul-de-sac obliteration (if severe). Retroversion: Torus uterinus thickening Distorted/shortened of posterior lower uterine surface Irregular configuration/shortening of posterior uterine surface (tethering) Anterior/posterior cul-de-sac obliteration (if severe) Effacement, distortion of fat planes and loss of interface between organs Obliteration of fat planes Poor interface visualization Stranding between rectum and adjacent organs Mushroom cap sign T2 at base & T2 at cap Bilateral asymmetrical thickening & T2 T1 within ligament (glandular material) Most common site for endometriosis and endometriomas High association with severity of disease Differential diagnoses: haemorrhagic adnexal cyst, ovarian dermoid cyst, peritoneal inclusion cyst Differential diagnoses: uterine leiomyoma Due to regional tethering secondary to adhesions Due to regional tethering secondary to adhesions Due to regional tethering secondary to adhesions Rectosigmoid is most commonly affected part of intestine Mushroom cap sign is specific to severe, invasive rectal involvement May indicate need for colorectal surgical input Common symptoms: abdominal pain, constipation/diarrhoea, dyschezia and haematochezia A feature of severe disease Anteflexion or retroflexion of uterus There is wide population variation in the degree of normal version and flexion of the uterus. Distinguishing normal physiologic version/flexion from pathologic tethering is an important consideration when underlying endometriosis is suspected. Anteflexion of the uterus may occur when there is endometriosis and adhesion formation in the anterior compartment between the bladder peritoneal reflection and the anterior uterine serosa. On T2WI, endometriosis of the vesicouterine pouch may appear as hypointense nodules or bands, situated on the anterior uterine wall. In severe cases, these may result in obliteration of the anterior cul-de-sac. 2 Retroflexion of the uterus occurs when there is endometriotic involvement of the posterior compartment, in particular the uterosacral ligaments. 7 The torus uterinus is a small transverse thickening that binds the original insertion of the uterosacral ligaments to the posterior cervix. On MRI, the torus uterinus is usually unable 769

AL Thalluri et al. Fig. 1. Sagittal T2WI of posterior cul-de-sac obliteration with retroflexion of the uterus in two patients.

Sagittal T2WI of the posterior cul-de-sac demonstrating rectal distortion with visible adhesions between the rectal and uterine serosa and tethering of bowel loops (white arrows) and severe posterior

4 AL Thalluri et al. Fig. 1. Sagittal T2WI of posterior cul-de-sac obliteration with retroflexion of the uterus in two patients. Patient 1 with adhesions and fibrosis, which is evident as low T2 signal bands between the uterine serosa and rectum (white arrows). Retroflexion of the uterus is also identified (orange arrow). Patient 2 with denser fibrotic plaque formation in the posterior cul-de-sac, involving uterine serosa and adjacent rectal serosa (arrow heads). Fig. 2. Sagittal T2WI of the posterior cul-de-sac demonstrating rectal distortion with visible adhesions between the rectal and uterine serosa and tethering of bowel loops (white arrows) and severe posterior cul-de-sac endometriosis and invasive rectal disease with a distinct mushroom cap sign. Note the low T2 signal fibrotic base (yellow arrow) and the high T2 signal mucosal/submucosal intraluminal cap (white arrow heads). Fig. 3. Ovarian endometriomas in two patients. Axial fat suppressed T1WI demonstrating two large adnexal endometriomas (orange arrows). Coronal T2WI with the T2 shading sign visible (white arrow). Both features support haemoconcentration and are consistent with ovarian endometriomas. to be viewed unless there is pathological thickening present, such as in endometriotic involvement. 11 This causes fibrosis of the ligaments, tethering the uterus posteriorly and resulting in uterine retroflexion (Fig. 4). When retroflexion of the uterus has occurred, there is often irregular configuration or shortening of the posterior surface of the uterus, which is indicative of tethering

MRI in deep infiltrating endometriosis Fig. 5. Coronal 3D- T2WI showing a thickened uterosacral ligament (white arrow). Fig. 4.

Thickened uterosacral ligament The uterosacral ligament attaches the cervix to the sacrum and holds the uterus in position.

ligament endometriosis greater than 90% on MRI. 7 The proximal, medial uterosacral ligament portion is the most commonly affected part by endometriosis.

5 MRI in deep infiltrating endometriosis Fig. 5. Coronal 3D- T2WI showing a thickened uterosacral ligament (white arrow). Fig. 4. Sagittal TSE T2WI demonstrating torus uterinus fibrosis and thickening (orange arrow) and with resultant shortening causing pathologic uterine retroflexion. Thickened uterosacral ligament The uterosacral ligament attaches the cervix to the sacrum and holds the uterus in position. The uterosacral ligament, in addition to the posterior cul-de-sac, is the most common pelvic sites of involvement in deep pelvic endometriosis, with specificity for the diagnosis of uterosacral ligament endometriosis greater than 90% on MRI. 7 The proximal, medial uterosacral ligament portion is the most commonly affected part by endometriosis. T2WI may show bilateral, asymmetrical hypointense thickening (Fig. 5) and glandular material is also often evident within the ligament. 9 Given the proximity of adjacent organs, uterosacral endometriosis may extend directly to the rectal wall and vaginal fornices. 7 Haematosalpinx Endometriotic involvement of the fallopian tubes usually occurs within the sub-serosal layer and is strongly associated with infertility due to resultant peritubal adhesions and subsequent tubal obstruction. 7 On MRI, the presence of T1 hyperintense blood products within a dilated tube (haematosalpinx) is highly specific for endometriosis, and may be the only feature of disease on MRI (Fig. 6). 7 Elevated vaginal fornices Vaginal forniceal elevation may occur in endometriosis as a result of regional adhesions (Fig. 7). There are several MRI features of forniceal elevation including the upper level of the fornix being superior to the angle of the uterine isthmus, acute angulation of the fornix, or the fornix being visibly pulled in a superior direction with subsequent stretching of the vaginal wall. 7 Thickening of the superior one-third of posterior vaginal wall with or without nodularity may also be visualized. 7 Nodules are Fig. 6. Axial T1WI without and with fat suppression demonstrating haematosalpinx with T1 signal hyperintensity within a dilated fallopian tube. 771

AL Thalluri et al. Fig. 7. Sagittal T2WI showing elevated vaginal fornices (white arrow) and normal posterior vaginal fornices for comparison (orange arrow). Fig. 8.

arrows). identified as low signal intensity foci on T2WI. 1 T1WI (particularly fat saturated images) may show high signal intensity indicative of active/subacute haemorrhagic deposits.

6 AL Thalluri et al. Fig. 7. Sagittal T2WI showing elevated vaginal fornices (white arrow) and normal posterior vaginal fornices for comparison (orange arrow). Fig. 8. Sagittal T2WI demonstrating posterior uterine plaques (orange arrows) with bowel serosal involvement and axial T1WI of different patient, showing T1 hyperintense posterior uterine plaques (orange arrows). identified as low signal intensity foci on T2WI. 1 T1WI (particularly fat saturated images) may show high signal intensity indicative of active/subacute haemorrhagic deposits. 1 Uterine serosal plaques MRI accuracy for the detection of uterine serosal implants when correlated with laparoscopy/laparotomy has been reported at approximately 81%. 5 Similar to plaques in other locations, they display low to intermediate T2 signal intensity, commonly associated with small cystic areas with active glandular deposits (Fig. 8a). On T1WI, a plaque has low-intermediate signal, often with punctate hyperintense haemorrhagic/proteinaceous foci (Fig. 8b). 9 In conclusion, endometriosis is an important gynaecological disorder which can impact significantly an individual s quality of life and has major implications on fertility. Pre-operative MRI has high specificity for the diagnosis and characterization of disease extent, and may guide surgical management, which remains the mainstay of curative treatment. References 1. Chamie LP, Blasbalg R, Pereira RMA, Warmbrand G, Serafini PC. Findings of pelvic endometriosis at transvaginal US, MR imaging, and laparoscopy. Radiographics 2011; 31: E Coutinho A, Bittencourt LK, Pires CE et al. MR imaging in deep pelvic endometriosis: a pictorial essay. Radiographics 2011; 31: Manganaro L, Vittori G, Vinci V et al. Beyond laparoscopy: 3-T magnetic resonance imaging in the evaluation of posterior cul-de-sac obliteration. Magn Reson Imaging 2012; 30: Drake R, Vogl W, Mitchell A. Gray s Anatomy for Students, 3rd edn. Churchill Livingstone, Philadelphia, p. 772

7 MRI in deep infiltrating endometriosis 5. Kataoka ML, Togashi K, Yamaoka T et al. Posterior cul-de-sac obliteration associated with endometriosis: MR imaging evaluation. Radiology 2005; 234: Erkan N, Caliskan C, Yildirim Y, Vardar E, Korkut M. Rectosigmoid endometriosis. Turk J Gastroenterol 2008; 19: Siegelman ES, Oliver ER. MR imaging of endometriosis: ten imaging pearls. Radiographics 2012; 32: Togashi K, Nishimura K, Kimura I et al. Endometrial cysts: diagnosis with MR imaging. Radiology 1991; 180: Rendle J. Endometriosis: a radiological review. Malta Med J 2011; 23: Glastonbury CM. The shading sign. Radiology 2002 Jul; 224: Siegelman ES, Outwater EK. State of the art tissue characterization in the female pelvis by means of MR imaging. Radiology 1999; 212:

Accuracy of transvaginal ultrasound and magnetic resonance imaging in diagnosis and extension of pelvic endometriosis

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