MR imaging of endometriosis: Spectrum of disease

+Model

ARTICLE IN PRESS

DIII-947; No. of Pages 17

Diagnostic and Interventional Imaging (2017) xxx, xxx—xxx

REVIEW /Genitourinary imaging

MR imaging of endometriosis: Spectrum of disease C. Bourgioti a,∗, O. Preza a, E. Panourgias a, K. Chatoupis a, A. Antoniou a, M.E. Nikolaidou b, L.A. Moulopoulos a a

Department of Radiology, School of Medicine, National and Kapodistrian University of Athens, Aretaieion hospital, 76, Vassilisis-Sofias Ave., 11528 Athens, Greece b Department of Gynaecology and Obstetrics, Rea maternity hospital, 383, Sygrou Ave., 17564 Athens, Greece

KEYWORDS Index terms: Endometriosis; Pelvic endometriosis; Deep endometriosis; Magnetic resonance imaging (MRI)

Abstract Endometriosis is a common gynecological disorder defined by the presence of endometrial tissue outside the uterus. It is the most common cause of chronic pelvic pain and typically affects the ovaries, uterine ligaments, peritoneum, tubes, rectovaginal septum and bladder. It may, however, be found at various extrapelvic sites, including the perineum, liver, pancreas, lung or even the central nervous system, and in such cases, diagnosis may be quite challenging. Even though definitive diagnosis requires laparoscopy, preoperative identification of endometriosis is important not only to differentiate it from other diseases with similar clinical presentations but also, for accurate presurgical mapping, since complete removal of all endometriotic foci is critical for the effective treatment of the patient’s symptoms. Ultrasound is performed initially, but magnetic resonance imaging (MRI) is increasingly being used, particularly when sonographic findings are unclear, when deep pelvic endometriosis is suspected or when surgery is planned, as it provides better contrast resolution and a larger field of view compared to ultrasound. In this article, we will discuss distinctive MRI appearances of endometriotic foci and we will review common and uncommon locations of endometriosis within the body, in an attempt to familiarize radiologists with its wide spectrum of manifestations. © 2017 Editions franc ¸aises de radiologie. Published by Elsevier Masson SAS. All rights reserved.

∗

Corresponding author. E-mail addresses: [email protected] (C. Bourgioti), [email protected] (O. Preza), [email protected] (E. Panourgias), [email protected] (K. Chatoupis), [email protected] (A. Antoniou), [email protected] (M.E. Nikolaidou), [email protected] (L.A. Moulopoulos). http://dx.doi.org/10.1016/j.diii.2017.05.009 2211-5684/© 2017 Editions franc ¸aises de radiologie. Published by Elsevier Masson SAS. All rights reserved.

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

2

C. Bourgioti et al.

Endometriosis is a common gynecological disorder defined by the presence of endometrial tissue outside the uterus. It is the most common cause of chronic pelvic pain and typically affects the ovaries, uterine ligaments, peritoneum, tubes, rectovaginal septum and bladder. It may, however, be found at various extrapelvic sites, including the perineum, liver, pancreas, lung or even the central nervous system, and in such cases, diagnosis may be quite challenging. Even though definitive diagnosis requires laparoscopy, its preoperative identification of endometriosis is important not only to differentiate it from other diseases with similar clinical presentations, but also for accurate presurgical mapping, since complete removal of all endometriotic foci is critical for the effective treatment of symptoms. Ultrasound is performed initially, but magnetic resonance imaging (MRI) is increasingly being used, particularly when sonographic findings are unclear, when deep pelvic endometriosis is suspected or when surgery is planned, as it provides better contrast resolution and a larger field of view compared to ultrasound. In this article, we will discuss distinctive MRI appearances of endometriotic foci and we will review common and uncommon locations of endometriosis within the body, in an attempt to familiarize radiologists with its wide spectrum of manifestations.

General principles Incidence, location, types and clinical presentation of endometriosis Endometriosis affects up to 10% of women at childbearing age [1,2]. Only 5% of cases involve the postmenopausal population and these are most often in association with exogenous estrogen replacement. Endometriosis can be either intra- (much more frequently ) or extrapelvic in location. Intrapelvic ectopic endometrial glands and stroma are most often in the ovaries but may also involve the uterosacral ligaments and cul-de-sac, serosal surfaces, fallopian tubes, rectosigmoid colon, vagina, cervix, bladder and ureters. Extrapelvic endometriosis is much less frequent, occurring in about 1% of all cases, and may be seen at virtually any anatomic location, including the abdominal wall, surgical scars, diaphragm, liver, kidneys, pancreas or even bones and brain [3]. There are three types of endometriosis. In superficial endometriosis, endometriotic foci (usually very small and identifiable only at laparoscopy) are located at the peritoneal surface or less than 5 mm from it. In deep (or solid infiltrating) endometriosis, endometrial implants are located at least 5 mm away from the peritoneal surface and may invade the retroperitoneal space or the wall of adjacent pelvic organs. Symptomatic patients usually suffer from deep endometriosis. Finally, endometriomas, the third type of endometriosis, present as cystic structures with hemorrhagic content located at the adnexa. Common clinical manifestations, include pelvic pain (cyclical pelvic pain, dysmenorrhea and dyspareunia) and infertility. Deep endometriosis is considered the main cause of chronic pelvic pain in women of reproductive age. Less frequent symptoms, such as: painful constipation,

catamenial diarrhea, rectal bleeding, hematuria or rarely, pneumothorax or epistaxis are closely related to the location of the ectopic, functional endometrium; interestingly, a number of patients may be asymptomatic.

Pathogenesis The etiology of endometriosis is even today under investigation. The most popular theory for its pathogenesis is that of retrograde menstruation, where endometrial cells migrate through the fallopian tubes to the peritoneum during menstruation, and there they grow, under the influence of hormonal and other factors (Sampson’s theory). Coelomic metaplasia (cells of the coelomic epithelium which covers the ovaries and the peritoneum transform to endometrial cells), or growth of ectopic primitive cells outside the mullerian tracts, have also been implicated as possible causes of endometriosis. More recently, other theories such as transformation of circulating stem cells into endometrial tissue are being considered as well [4].

Diagnosis Laparoscopy is the gold standard for the diagnosis of endometriosis [5]. Sometimes, surgical exploration can be complicated, as deep endometriotic plaques may be hidden under extensive adhesions or may not be visible due to a subperitoneal location. One-step surgery (i.e., diagnosis and complete excision of the lesions at the same time) is essential for the successful treatment of endometriosis and, therefore, presurgical mapping of the endometriotic lesions becomes an important issue [5]. Currently, ultrasound is preferred for the initial assessment of both endometriomas and deep pelvic endometriosis. However, transvaginal ultrasound, even with adequate bowel preparation and use of high-frequency probes has important limitations, because of the relatively small field-of-view and operator dependency [6]. MRI is being increasingly used for the evaluation of endometriosis, with reported sensitivity and specificity values ranging from 69—92% and 75—98%, respectively [7—9]. Most authors advocate MRI as an adjunct tool in cases of ultrasound-indeterminate findings, possible ureteral involvement and presurgical mapping [6].

MRI protocol Recently, the European Society of Urogenital Radiology (ESUR) published specific guidelines focusing on patient preparation, optimal MRI sequences and reporting criteria for the evaluation of patients with endometriosis [6]. Fasting (at least 4—6 h prior to the examination) and administration of antiperistaltic agents (intramuscularly or intravenously) is strongly recommended for better image quality. The bladder should be moderately filled; vaginal and/or rectal opacification is optional. The majority of MRI studies are performed at high field magnets (1.5 T or 3 T) with the use of pelvic phased array coils. T2weighted sequences are most suitable for demonstrating pelvic endometriosis; T1-weighted images with and without fat suppression are helpful for depicting ovarian endometriomas. Fat-suppressed, T1-weighted images appear to be

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model

ARTICLE IN PRESS

DIII-947; No. of Pages 17

MR imaging of endometriosis: Spectrum of disease of value for the detection of peritoneal lesions, but data are still under investigation [10,11]. The use of intravenous gadolinium chelate is not mandatory for the evaluation of deep pelvic endometriosis. However, MRI with the adjunct of intravenous administration of gadolinium chelate may provide useful information in cases of atypical adnexal lesions (e.g. cysts with mural nodules). Current data do not support the role of diffusion-weighted imaging (DWI) or susceptibility weighted (SW) images. The MRI protocol applied at our institution is presented in Table 1.

3 Adhesions, in cases of long-standing endometriosis, may be seen, as low signal intensity bands on T2-weighted images of variable thickness, extending between pelvic organs. Sometimes, they may be too thin to be visualized on MRI; indirect signs, such as distorted anatomy (e.g. uterine retraction), dilated tubes, peritoneal inclusion cysts or bowel angulation may suggest the presence of pelvic adhesions [4].

Distribution of endometriosis MRI features of endometriotic foci with histopathologic correlation MRI findings of endometriosis are closely related to the histology of the disease. Since endometriotic foci consist of functional endometrium, they respond to hormonal stimulation during the menstrual cycle as normal endometrium does. Ectopic endometrial glands may appear as foci of variable signal intensity on T2- and T1-weighted images, depending on the age of hemorrhage. Subacute bleeding may result in very high signal intensity on T1-weighted images, which is usually more conspicuous on images with fat suppression, and relatively low signal intensity on T2weighted images. In women with chronic endometriosis, recurrent bleeding of the ectopic endometrium induces the development of reactive fibrosis. These fibrotic endometrial lesions, present with an irregular spiculated contour and relatively low signal intensity on both T1- and T2-weighted images. Careful search for small foci of high signal intensity on T2-weighted and often high signal intensity on T1-weighted images, related to the presence of dilated endometrial glands within the fibrotic tissue, enables the diagnosis since the low signal intensity on T2-weighted images of these lesions is similar to that of the wall of normal pelvic organs. Foci of chronic endometriosis show variable enhancement on MR images obtained after intravenous administration of gadolinium chelate.

Table 1

Frequent sites of endometriosis Endometriomas The adnexa is the most common location of endometriosis. Endometriotic cysts (or endometriomas) are localized forms of ovarian endometriosis; they can be solitary or multiple, unilateral or, in almost 50% of women with endometriosis, bilateral. MRI has high specificity (> 90%) in identifying endometriomas. They are thick wall cysts with blood products related to cyclic bleeding. That is why, endometriomas, typically, present with bright signal intensity on T1-weighted images (T1 shortening is due to the presence of subacute hemorrhage and high protein content) and homogenously low signal intensity on T2-weighted images (T2 shading—caused by accumulation of iron and protein due to repeated bleeding) [12,13]. T2 shading has high sensitivity (93%) but poor specificity (45%) for the diagnosis of endometriomas, and it may occasionally be seen in other hemorrhagic adnexal lesions. In such cases, it may be helpful to look for the T2 dark spot sign which consists of small- usually multiple- foci of very low signal intensity on T2-weighted images within the cyst but not in its wall (Fig. 1). These dark foci on T2-weighted images are highly indicative of long standing hemorrhage (they possibly represent chronic retracted clots) and may, therefore, they may be helpful in discriminating endometriomas from other functional hemorrhagic lesions [14]. Another distinctive MR

Magnetic resonance imaging protocol for endometriosis.

Sequences

Plane

Technical characteristics

T2-weighted

Transverse Sagittal

NSA: 2, ST/G: 4.5/1, matrix: 340 × 350, FOV: 38 NSA: 3, ST/G:3.5/1.2, matrix: 348 × 276, FOV: 25 NSA: 6, ST/G: 4/0.4, matrix: 256/176, FOV: 18

T1-weighted Fat-suppressed T1-weighted ± contrast enhancement DWI (optional)

Transverse oblique (perpendicular to cervical axis or/and along with endometrial cavity axis, when deep endometriosis is suspected) Transverse Transverse

Axial b value = (0,400,1000) s/mm2

NSA: 1, ST/G: 6/2, matrix: 300 × 205, FOV: 36 NSA: 2, ST/G: 4.5/1, matrix: 360 × 252, FOV: 38

NSA:12, ST/G:6/1 matrix: 124X174, FOV: 35

DWI: diffusion weighted imaging, NSA: number of signal acquired; ST (mm): slice thickness; G (mm): Gap; FOV (cm); field of view (right—left).

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

4

C. Bourgioti et al.

Figure 1. 32-year-old woman with known history of endometriosis. T2-weighted MR image in the axial plane shows bilateral endometriomas with multiple small foci of very low signal intensity within the cysts (arrows). These dark foci on T2-weighted MR image are highly indicative of repeated bleeding and possibly represent chronic retracted clots (dark spot sign).

feature of endometrioma is the presence of a low signal intensity peripheral rim on T2-weighted images, caused by hemosiderin-ladden macrophages within the wall of the lesion; fluid-fluid levels, due to recent bleeding, may also be seen on T2-weighted images, with the low signal intensity of the dependent portion caused by the cellular component of bleeding [4]. The differential diagnosis includes hemorrhagic cysts (acute presentation, lack of T2 dark spot sign, resolution in 4—6 weeks), teratomas (the presence of fat is pathognomonic) and ovarian carcinoma (usually solid elements, which enhance on MR images obtained after intravenous administration of gadolinium chelate). Note that a solidappearing wall nodule, a suspicious finding for ovarian malignancy, may also be found in a considerable number of endometriomas (20%). However, in endometriomas, the nodule possibly corresponds to a retracted clot, and, therefore, does not usually show any uptake on MR images obtained after intravenous administration of gadolinium chelate [4]. Multiple bilateral endometriomas (50%) with coexisting adhesions cause retraction of the ovaries which

come to abut each other, the so-called kissing ovaries (Figs. 2 and 3). Rarely, large endometriotic cysts (maximal diameter > 6 cm) may rupture into the peritoneal cavity causing acute abdominal pain and inducing the accumulation of ascites due to peritoneal irritation from blood products (chemical peritonitis) (Fig. 4). Differential diagnosis between rupture of an endometriotic cyst versus any other ovarian haemorrhagic lesion (e.g. a corpus luteum cyst—which is far more common) may be difficult and often laparoscopy is needed to identify the source of bleeding; bilateral hemorrhagic lesions, lobulated ascites (due to presence of adhesions) confined to the pelvis and high serum CA-125 levels, are common findings in women with a ruptured endometriotic cyst [15,16]. Infected endometrioma is also rare, even though it is suggested that women with advanced endometriotic disease are at higher risk for developing an ovarian abscess than those without endometriosis [17]. Possible causes for

Figure 2. 39-year-old woman with long standing endometriosis. T2-weighted MR image in the axial plane demonstrates both ovaries on the right side of the pelvis, abutting each other (kissing ovaries). Also shown is a large endometriotic plaque involving the left round ligament and uterine horn (arrow), RO: right ovary, LO: left ovary.

Figure 3. 34-year-old woman with chronic pelvic pain. A. T2-weighted MR image in the axial plane clearly depicts a thick, low signal intensity band extending from the posterior uterine wall to the bowel, consistent with an adhesion (white arrow). Bilateral endometriomas and retraction of the ovaries (asterisks) to the midline due to co-existing adhesions is also shown (kissing ovaries). B. Laparoscopic image of another woman with advanced pelvic endometriosis shows the presence of adhesions (white arrow) between the posterior uterine wall (U) and the epiploic appendages (A) of the sigmoid (S). Note the endometrioma (E) of the displaced right ovary.

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

MR imaging of endometriosis: Spectrum of disease

5

Figure 4. 24-year-old woman with acute abdominal pain and no history of endometriosis. A. T2-weighted MR image in the axial plane shows a multiloculated cystic mass (solid arrows) in the left adnexa with varying signal intensity in the different compartments. A small hemorrhagic fluid collection is seen in the pelvis (dotted arrow). B. T1-weighted fat-suppressed MR image obtained after intravenous administration of gadolinium chelate in the axial plane shows peripheral enhancement of the lesion (solid arrows) and strong peritoneal enhancement possibly due to inflammation (dotted arrows). C. A large endometrioma (E) with signs of rupture (arrows) and pelvic adhesions (A) was found at laparoscopy. U: uterus.

the dissemination of pathogens (typically polybacterial) to the ovarian endometriomas includes: transvaginal aspiration for in vitro fertilization (IVF), pelvic surgery, ascending genital tract infection, haematogeneous or even contiguous spread from adjacent organ inflammation; rarely, infection may develop spontaneously in a pre-existing endometrioma [18,19]. Imaging findings include the presence of a complex cystic adnexal mass, but, as there are only a few cases described in the literature, there are no typical MRI features for infected endometriomas. Diagnosis is based on clinical evidence and in most cases and surgical drainage is needed to optimize treatment [20]. Most of the endometriotic cysts decrease in size during pregnancy, and this is mainly attributed to high progesterone levels and temporary interruption of the menstrual cycle. However, 12% of ovarian endometriomas may undergo decidualisation (i.e. morphological and functional changes of endometrial stromal cells, which result in formation of desidua, an important structure which supports placentation) during pregnancy. MRI features of decidualized endometriomas includes the presence of solid components, papillary projections and internal septa, quite like borderline tumors or even ovarian cancer. However, it is reported that the mural nodules of the decidualized endometriomas are smaller compared to those of ovarian carcinomas. They follow the signal intensity (SI) of normal endometrial decidua/placenta demonstrating higher signal intensity on T2-weighted images, significantly higher apparent diffusion coefficient (ADC) values and absence of increased signal on diffusion-weighted images with b values of 1500 s/mm2 , compared to the solid components of ovarian carcinomas [21,22]. Most of the decidualized endometriomas are surgically removed because they resemble ovarian malignancies, even though several authors advocate expectance management, as desidualized endometriomas tend to regress rapidly during follow-up studies, unlike ovarian neoplasms [23].

Uterine ligaments The uterosacral ligaments (USL) are major supportive uterine ligaments, which originate horizontally (distal portion)

from the posterolateral aspect of the cervix (torus uterinum) or the upper vaginal dome (cervico-vaginal junction), descend in front of the anterior and lateral part of the rectum (median portion), where they are closely attached to the mesorectal fascia (i.e. the visceral layer of the endopelvic fascia which encircles the rectum and the mesorectal fat) and then course posteriorly, finally inserting into the sacrum [24], piriformis muscles or sacrospinous ligament/coccygeus muscles (proximal portion) [25]. Normally, USLs are visualized as thin, low signal intensity bands of connective tissue on MRI (Fig. 5); thin section (3 mm) oblique transverse T2-weighted MR images (orientated along the course of USLs when visible on sagittal plane or perpendicular to the long axis of the cervix, when USLs are not visible) are recommended for the demonstration of the entire course of the USLs, because of their characteristic anatomical orientation [26]. Uterosacral ligament involvement should always be looked for when endometriosis is suspected, as it is the most common location of deep endometriosis with a reported incidence up to 69.2% [27]. Associated clinical symptoms include pelvic pain and dyspareunia. It may present as asymmetrical (diffuse or focal) ligament thickening (unilateral or bilateral), or even as a nodular mass abutting the ligament. It is more frequent at the horizontal part of the ligament (close to the cervix) and spread to the extraperitoneal retrocervical region and from there to the rectum and vagina may occur. In such cases, retroversion of the uterus or rectal angulation may be observed as well (Figs. 6—8). According to several studies [28,29], radiologists may accurately identify the abnormal uterosacral ligaments, with reported uncertainty values as low as 13.8% [29]. The round ligaments are easily detected as thin low signal structures, coursing from the uterine horns anteriorly to the inguinal canal, and finally attaching to the labia majora. When involved (reported frequency rates range from 0.3% to 14%), they appear thicker (Fig. 9) and show enhancement, particularly well seen on MR images with fat-suppression obtained after intravenous administration of gadolinium chelate [27,30]. This information may be helpful to the surgeons since exploration of the round ligaments during laparoscopic surgery for endometriosis is often

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

6

C. Bourgioti et al.

Figure 5. 28-year-old woman, healthy volunteer. A. Thin (3 mm) section T2-weighted MR image in the axial oblique plane demonstrates the horizontal (distal) portion of the normal, thin USLs extending from the region of cervico-vaginal junction (white arrows). B. Corresponding T2-weighted MR image in the sagittal plane shows the normal horizontal aspect of the left USL (arrow). USLs descend in front of the anterior and lateral part of the rectum (median portion) and finally insert into the sacrum or the adjacent muscles (proximal portion).

overlooked. In case of shortening, thickening or deviation, the round ligaments should be removed [31]. Women with round ligament involvement may present with a painful inguinal mass, if the inguinal segment of the ligament is involved. In such cases, differential diagnosis include more common pathologies of the groin including lymphadenopathy, hernias or soft tissue tumors which in most cases may be readily accessed by imaging.

Pouch of Douglas Endometriosis may frequently involve the rectovaginal pouch (commonly known as pouch of Douglas); usually, MRI may demonstrate ill-defined, solid, hypointense lesions on T2-weighted images, abutting the posterior aspect of the uterine body and cervix. In some cases, MRI may show a considerable amount of glandular tissue and discrete fibrotic reaction, with variable enhancement on MR images obtained after intravenous administration of gadolinium chelate; identification of endometriotic glands as tiny foci

of high signal intensity on T1- and T2-weighted images (representing subacute hemorrhage and/or high viscosity fluid) helps establish the correct diagnosis. Retrocervical lesions may extend to the anterior rectal wall, causing complete or partial obliteration of the pouch of Douglas [32]. Obliteration of the cul-de-sac may hide areas of endometriosis on laparoscopy and, thus, the extend of the disease may be underestimated during surgery [33]; preoperative MRI may be quite useful for identifying endometrial implants localized in the obliterated pouch of Douglas, with reported sensitivity and specificity values up to 89% and 94%, respectively [34].

External adenomyosis Sometimes, deep endometriotic plaques may occur at the uterine surface and from there they may invade the myometrium mimicking adenomyosis (so-called external adenomyosis) or even subserosal leiomyomas [32]. Adenomyosis (i.e. ectopic endometrial glands within the

Figure 6. 30-year-old woman with endometriosis and a history of chronic pelvic pain and dyspareunia. A. T2-weighted MR image in the axial plane shows asymmetrical thickening of the right uterosacral ligament (arrow), a common site for endometriosis. B. T2-weighted MR image in the coronal plane shows uterine angulation (white arrow), due the presence of adhesions. An incidental ovarian cyst is seen on the left (asterisk).

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

MR imaging of endometriosis: Spectrum of disease

7

Figure 7. 43-year-old woman with deep infiltrating endometriosis. A. T2-weighted MR image in the axial plane demonstrates a typical endometriotic plaque at the distal portion of the right uterosacral ligament (USL - long white arrow). Note the endometriotic implants within the paracervical space bilaterally (short white arrows). B. Corresponding T2-weighted MR image in the sagittal plane clearly depicts the entire course of the right USL (white arrow points to the lesion, black to the normal portion of the ligament). C. Laraposcopy confirmed the presence of USL endometriosis (white arrow). Black arrows point to the unaffected part of the right USL.

Figure 8. 39-year-old woman with chronic pelvic pain. A.T2-weighted MR image in the axial plane and corresponding laparoscopy image B. show a retractile endometriotic lesion at the torus uterinum (long arrows). Note the normal round ligament on the left (small arrows). U: uterus, O: ovary.

myometrium) is a common finding in patients with endometriosis, therefore, discrimination between the two entities may be difficult, although necessary due to differences in treatment [35]. Extension of the lesion beyond the uterine contour, continuity with an adjacent endometriotic plaque and visualization of an intact transitional zone favor endometriosis over adenomyosis (Fig. 10). Indistinct margins and

high signal intensity foci on T1-weighted images within the lesion favor endometriosis over leiomyomas [32].

Fallopian tubes Almost 30% of women with endometriosis present with fallopian tube involvement at laparoscopy. Ectopic

Figure 9. 43-year-old woman with known history of endometriosis. A. T2-weighted MR image in the axial plane shows an abnormally thickened left round ligament (black arrow). B. Laparoscopic image shows a thick round ligament on the left (small arrows) and multiple small endometriotic foci on its surface. A dilated left fallopian tube is also demonstrated (FT). U: uterus, O: ovary.

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

8

C. Bourgioti et al. endometriotic implants in its wall [36]. Hydrosalpinges may also occur with pelvic endometriosis, due to chronic adhesions. However, remember that the most frequent cause of hydrosalpinx is pelvic inflammatory disease and not endometriosis [12,20].

Gastrointestinal endometriosis

Figure 10. 29-year-old woman with history of severe deep pelvic endometriosis. T2-weighted MR image in the coronal plane shows a large endometriotic implant invading the myometrium of the uterine fundus (arrow), mimicking adenomyosis. Note that the lesion is separate from the transitional zone (short arrow) ruling out the diagnosis of adenomyosis.

endometrial tissue usually involves the serosal surface of the tube; transmural involvement is a less frequent feature but, even when it occurs, the mucosa is rarely affected. Recurrent hemorrhage within the ectopic glands results in the formation of adhesions, obstruction and finally tubal dilatation. MRI may show a dilated fallopian tube, with high signal content on T1-weighted images, in keeping with subacute bleeding caused by the lesions in its wall (hematosalpinx) (Fig. 11); the T2 shading sign may be absent in endometriotic hematosalpinges [12]. Hyperintense foci on T1-weighted images (dilated endometrial glands) may be seen within the tubal wall. Hematosalpinx is strongly related to the presence of endometriosis. It may be a result of retrograde menstruation in an already obstructed tube due to pelvic adhesions rather than a sequela of

Figure 11. 35-year-old woman with history of deep pelvic endometriosis and hematosalpinges. T1-weighted fat-suppressed MR image in the axial plane of the pelvis shows bilateral sausage-like structures (white arrows), with incomplete internal septa characteristic of dilated tubes. Note the fluid-fluid level within the right fallopian tube (thin white arrow). The high signal intensity of the fluid within the tubes, is in keeping with hemorrhagic content.

The gastrointestinal tract (GI) is the most common site of extragenital endometriosis and it is frequently involved in women with deep invasive endometriosis. The rectosigmoid colon is the most frequently encountered site of GI endometriosis, followed by the sigmoid colon, with a reported incidence up to 65.7% and 19%, respectively. Endometriotic lesions may be multifocal in more than half of all cases with rectal involvement [37]. The ileum, cecum and appendix are other, less frequently involved GI locations, with a reported incidence ranging between 1% and 7% in women with bowel endometriosis; in rare cases, the ileocecal region may be the only site involved [38]. Interestingly, in approximately 30% of cases with rectal and sigmoid involvement, right-sided bowel endometriosis is also present [37]. Furthermore, recent reports addressed a possible association between ileocecal/appendix endometriosis and right ureteral involvement [39]. Therefore, in women with deep invasive endometriosis the bowel proximal to the rectosigmoid junction should also be carefully examined. Endometriotic bowel implants are usually located at the serosal surface, but transmural involvement may occur. Typical MRI findings of deep rectosigmoid endometriosis include a lesion of low signal intensity on T2-weighted images at the bowel wall (induced fibrosis and hypertrophy of the muscularis propria), with a high signal intensity shell projecting into the bowel lumen (protruding mucosa and submucosa); this is the so-called ‘‘mushroom cup’’ sign of endometriosis of the bowel (Fig. 12) [12,20,30,32]. MRI may be useful to demonstrate the involvement of the muscle layer of the bowel wall by endometriotic implants, but it has limitations in assessing true submucosa/mucosa infiltration, which requires more radical surgical treatment [40]. Usually, ileal endometriosis affects the terminal ileum, within an approximately 10 cm distance from the ileocecal valve. However, concurrent lesions may occur at more proximal small bowel loops [37]. Imaging findings include the presence of fibrotic nodular or retractile masses of low signal intensity on T2-weighted images with or without high signal hemorrhagic foci on T1-weighted images with fat suppression, abutting the bowel wall (Fig. 13). Although it is reported that preoperative imaging is usually inadequate to demonstrate ileal involvement and commonly the diagnosis of ileal endometriosis is made during surgical exploration for colorectal endometriosis [38], in the study conducted by Rousset et al., 3.0-T MR enterography exhibited excellent diagnostic performance for the diagnosis and mapping of endometriotic lesions located at the ileocecal region, with 100% positive predictive value [37]. Preoperative work-up for the localization of bowel endometriosis is necessary for optimal therapeutic management. Surgical treatment of deep invasive endometriosis, especially when the rectosigmoid is involved, may be associated with complications such as rectovaginal fistula, pelvic abscess formation or anastomotic leak in cases of segmental

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

MR imaging of endometriosis: Spectrum of disease

9 considered important for the selection of candidates for less radical bowel surgery [40].

Parametrial involvement

Figure 12. 36-year-old woman with history of endometriosis and painful defecation. T2-weighted MR image in the sagittal plane shows endometriotic implant invading both the posterior uterine and the anterior sigmoid wall. The lesion protrudes into the colonic lumen creating the mushroom cap sign with the bright peripheral signal representing the colonic mucosa (white arrow) which surrounds the low signal endometriotic lesion (asterisk).

bowel resection [39]; it is, therefore, suggested that the ‘‘least radical option should be selected’’ [41]. MRI may help surgeons plan more conservative surgical approaches in case of rectal and/or sigmoid involvement like rectal shaving, mucosal skinning or full-thickness anterior rectal wall excision (also known as disc resection); lack of multifocal disease, small size lesions (maximal diameter < 25—30 mm), absence of submocosa/mucosa infiltration, low (less than one third) percentage of intestinal circumference affected by the disease and sufficient distance (> 10 cm) between the rectal endometriotic implant and the annal verge are

Deep pelvic endometriosis may also affects the parametrial space; the prevalence of parametrial involvement is estimated up to 14.5% of cases with deep infiltrating disease [42]. Preoperative MRI may show irregular low signal intensity lesions with or without bright foci on T2-weighted images in the paracervical or paravaginal region (Fig. 7); in case of severe endometriosis, pelvic side wall involvement may be seen on MR images, usually as a mass like fibrotic tissue occupying the parametrial space and extending to the pelvic muscles. Ureteral dilatation is considered an indirect sign of parametrial involvement [42]. Identification of endometrial implants within the parametrial fat is important for surgical planning; in cases with parametrial involvement, parametriectomy may be required for the complete excision of deep endometriosis. This procedure is technically challenging and may be complicated with either ureteral injury or secondary urinary or large bowel dysfunction, due to nerve trauma [43].

Bladder Urinary tract involvement occurs in almost 4% of patients with endometriosis. The posterior bladder wall is most frequent affected (90%). In 50% of patients with bladder endometriosis, there is a history of prior C-section or other gynecologic surgery [12,13]. Women present with dysuria and less often hematuria indicating involvement of the bladder mucosa. MRI demonstrates sensitivity and specificity values equal to 68% and 98%, respectively, for identifying bladder involvement in patients with deep endometriosis [34] and may show endometriotic lesions even in patients with normal cystoscopic findings or with no urinary tract symptoms. Bladder endometriosis appears as a low signal intensity nodule on T2-weighted images with small bright foci at the posterior bladder wall possibly extending to the vesicouterine pouch (Fig. 14) [12,44].

Figure 13. 45-year-old woman with abdominal pain and vomiting. A. T2-weighted MR image in the coronal plane shows a low signal intensity mass-like lesion on the right side of the lesser pelvis (asterisk), inseparable from dilated terminal ileum loops (white arrows in A and B). B. Corresponding T2-weighted MR image in the sagittal plane demonstrates the relation of the mass (asterisk) with the adjacent cecum (C). A large endometriotic lesion invading terminal ileum was found at laparoscopy.

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

10

C. Bourgioti et al. the differential diagnosis of non-calculus ureteric obstruction or/and ureteric intraluminal lesions in young women [46]. Endometriotic plaques with low signal on T2-weighted images with or without bright signal foci, adhesions and ureteral dilatation proximal to the site of obstruction are MRI common findings (Fig. 15). Identification of ureteral endometriosis is important because advanced surgical techniques, like ureter diversion or reimplantation are often required [32].

Less frequent sites of endometriosis Abdominal wall

Figure 14. 40-year-old woman with history of endometriosis and dysuria. T2-weighted MR image in the sagittal plane shows a low signal intensity lesion disrupting the posterior wall of the bladder (arrow). Note the multiple tiny high signal foci within the lesion, representative of the dilated ectopic endometrial glands.

Ureters Ectopic endometrial tissue -often originating from the ovaries or the uterine ligaments- may infiltrate the periureteral fat and ureteral adventitia; involvement of the ureteral wall itself is more rare. Clinical signs of ureteral involvement are frequently absent and that is why, almost half of patients (usually women between 30—35 years of age) with ureteral involvement by endometriosis, already have a non-functioning kidney at diagnosis [32]. Single or bilateral uretero-hydronephrosis may be present even with minimal disease, in patients with extensive deep infiltrating pelvic endometriosis [45]; in rare cases, isolated ureteral endometriosis may be found in the pelvis, resembling a ureteral tumor. That is why endometriosis should be included in

The abdominal wall is the most common location of extraabdominopelvic endometriosis. It is often associated with prior laparoscopic or surgical intervention and, in most cases, there is no history of prior endometriosis. It is estimated that almost 0.03—0.4% of women with a prior C-section and 1.08—2% with prior hysterotomy, will develop endometrial implants at the surgical scar [47]; it is most frequently seen a year after surgery. Common locations include the abdominal subcutaneous tissue and less often the rectus abdominis muscle and its sheath as well as the region of the umbilicus. Clinical symptoms include a constant, atypical localized pain with or without a palpable mass, which can be frequently misdiagnosed [20,47]. MRI is used to define the extent of the disease and to evaluate the imaging characteristics of the lesion (Fig. 16). Fine needle aspiration is often required for the diagnosis. Differential diagnosis includes a desmoid tumor, which may present with very low signal intensity on T2-weighted images due to fibrin deposition without, however, the bright signal on T2-weighted images of the dilated endometrial glands [12], hematoma, sarcoma, lymphoma and primary or metastatic cancer.

Vagina and vaginal vault Vaginal endometriosis is usually associated with perineal scar endometriosis, which is an unusual entity (0.3—1% of women) occurring at the episiotomy scar after prior vaginal delivery. Secondary vaginal vault endometriosis has also been described in women with bilateral oophorectomy

Figure 15. 33-year-old woman with history of left ureteral obstruction due to advanced deep pelvic endometriosis, after ureteral stent placement. A. T2-weighted MR image in the axial oblique plane shows a spiculated, mass like endometriotic lesion abutting left ureter (white arrow). Right ureteral dilatation is also seen (dotted black arrow). B. Corresponding T2-weighted MR image in the sagittal plane demonstrates the distal portion of the left ureter bearing the stent, extending from the mass (white arrow) to the vesicoureteral junction (black arrow).

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

MR imaging of endometriosis: Spectrum of disease

11

Figure 16. 42-year-old woman with history of C-section, referred for a palpable mass in the right anterior abdominal wall. T2-weighted MR image in the axial oblique plane (A) and T1-weighted fat-suppressed (B) MR image in the axial plane of the pelvis depict a round, well demarcated mass invading the right oblique abdominal muscle and the adjacent subcutaneous fat. Note the peripheral low signal intensity ring due to hemosiderin deposition (white arrow in A) and the high signal intensity foci of subacute hemorrhage on the fat-suppressed T1-weighted MR image (white arrow in B).

and hysterectomy due to vaginal-uterine morcellation [32,48,49]. Thickening and loss of the low signal intensity of the posterior vaginal wall on T2-weighted images, are common findings; hemorrhagic nodules and/or ill-defined fibrous masses with or without high signal foci on T2-weighted images may also be seen (Fig. 17) [50].

Abdominal viscera Endometriosis is extremely rare outside the pelvis although it has been reported to affect almost every organ, with the exception of the heart and spleen. Liver endometriosis is a rare entity with less than 30 cases described in the literature, half of which had no previous history of endometriosis [51,52]. It is likely that, some cases of liver endometriosis probably arose from an extracapsular location and then invaded the parenchyma; in such cases, patients may present with right upper quadrant abdominal pain. Liver endometriomas may be imaged as complex masses, with variable amounts of solid and cystic/haemorrhagic components (Fig. 18). Differential diagnosis of liver endometriomas may be challenging and includes primary hepatic tumors (e.g. adenoma), echinococcal cysts, metastases or mucinous neoplasms, which may also demonstrate high signal on T1-weighted images. Intraoperative frozen section biopsy is needed to establish the diagnosis. Pancreatic endometriosis is very rare, with less than 10 cases reported in the medical literature. Clinical presentation or imaging findings are non specific [53]; differential

diagnosis includes other pancreatic tumors, such as mucinous cystic neoplasm or pseudocyst and, therefore, surgical exploration is often required for a definitive diagnosis.

Thoracic endometriosis The thorax is the most frequent extra-abdominal site of endometriosis; however, it is rarely involved. Ectopic endometrial tissue may be found in several thoracic structures including the pleura, lung parenchyma, pericardium or the diaphragm, resulting in a wide spectrum of clinical and radiological manifestations which follow the cyclic endometrial changes, the so-called thoracic endometriosis syndrome [54]. Catamenial pneumothorax is the most common clinical presentation; periodical hemothorax, hemoptysis, chest or scapular pain or even lung nodules are other manifestations. Radiological features are nonspecific; therefore, for most authors, imaging has a limited role in the diagnosis of thoracic endometriosis [55]; it is the association of the symptoms with the menstrual circle which, usually points out the correct diagnosis [56], and thoracoscopy is usually needed to confirm the clinical suspicion. A possible explanation for the thoracic involvement suggests that the ectopic endometrium follows a circle ‘‘route’’ (along with peritoneal fluid) within the abdomen and via the right paracolic gutter may be implanted to the peritoneal surface of the diaphragm; then, endometrial cells through diaphragmatic defects (congenital or

Figure 17. 45-year-old woman with history of vaginal hysterectomy for uterine leiomyomas. A. T2-weighted MR image in the axial plane shows a low signal intensity nodule at the left vaginal wall (arrow). B. Corresponding T1-weighted fat-suppressed MR image in the axial plane shows high signal intensity of the lesion. Histopathological analysis of biopsy specimen revealed endometriosis.

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

12

C. Bourgioti et al.

Figure 18. 38-year-old woman with chronic abdominal pain and no history of endometriosis. T2-weighted image (A) and T1-weighted fatsuppressed MR image obtained after intravenous administration of gadolinium chelate (B) in the coronal plane of the upper abdomen and chest show a sub-diaphragmatic, hemorrhagic lesion extending into the liver parenchyma (arrow). The lesion was biopsied and histological analysis showed endometriosis. T2- weighted MR image in the coronal plane (C) and corresponding T1-weighted MR image in the sagittal plane (D) of the same patient, three months after Gn-RH analogues administration, shows a decrease in the size of the lesion (arrow).

acquired) may be implanted within the thoracic cavity [57,58]. This phenomenon explains the increased frequency of right catamenial pneumothorax [54]. According to another theory (microembolization theory), endometrial cells are implanted in the pulmonary parenchyma via a pulmonary network filter function, forming well circumscribed nodules (solitary or multiple) which are usually located at the peripheral bronchi or, less frequently, within the lung parenchyma. This theory possibly explains the clinical symptom of haemoptysis, as well as the bilateral or left-sided location (30%) of lung nodules [54]. MRI may demonstrate small hyperintense on T1-weighted images endometriotic lesions in the visceral or parietal pleura [54]. Diaphragmatic endometrial implants may be identified as hyperintense foci on all MRI sequences, almost always involving the right hemidiaphragm, and particularly its posteriosuperior surface. Although the small size of the lesions and susceptibility artefacts may limit the diagnostic performance of MRI in cases of thoracic endometriosis, Rousset et al. reported high (> 80%) MRI sensitivity and excellent interobserver agreement in detecting diaphragmatic endometriosis in symptomatic patients [59]. MRI may therefore allow early identification of endometriotic implants in patients with diaphragmatic involvement and may help surgeons to plan the surgical removal of the lesions.

Central nervous system Central nervous system (CNS) endometriosis is extremely rare. Only one case of cerebellar and two of cerebral endometriosis have been reported, one of the latter related to the presence of a ventriculoperitoneal shunt [60]. Patients’ symptoms included headache, seizures or even subarachnoid hemorrhage; in all three cases, MRI showed a cystic brain

lesion with a hemorrhagic level. Final diagnosis was based on histopathological examination. Cases of endometriosis involving the spinal canal, dura, spinal cord and vertebrae have been reported; spinal involvement is associated with periodical low back pain in women of reproductive age [61]. In all cases, only biopsy provides a definitive diagnosis.

Ischiorectal fossa There are only few cases of endometriosis of the ischiorectal fossa in the literature [62], usually originating from an episiotomy incision [50]. In a single report by Ramalingappa et al., ischiorectal fossa endometriosis was described in a woman with uterine outflow obstruction. The authors suggested that due to increased intrauterine pressure, the menstrual blood might have dripped through the pelvic floor into the ischiorectal fossa [62]; however, this hypothesis is questionable. MRI features includes the presence of an ill-defined lesion with hemorrhagic foci or a hemorrhagic nodule within the adipose tissue of the ischiorectal fossa. Differential diagnosis may include a tailgut cyst, which arises from the retrorectal space and may sometimes extend in the ischiorectal fossa [50].

Sciatic nerve The sciatic nerve is a very rare site of endometriosis, with the mechanism of involvement still under debate. The right sided predominance of sciatic nerve endometriosis may be explained by the anatomic location of the sigmoid colon preventing the reflux of cells into the openings of peritoneal outpouchings towards the region of the sciatic notch or actually inhibiting these peritoneal ‘‘pockets’’ from reaching the notch. Coelomic metaplasia and embryonic cell rest theories have also been considered as possible mechanisms

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

MR imaging of endometriosis: Spectrum of disease for endometriosis of the sciatic nerve. [63—65]. Sciatic nerve is the commonest nerve prone to endometriosis (39%), after the nerves of the lumbosacral plexus (57%), which may be affected by direct extension from adjacent endometriotic plaques. Interestingly, perineural spread of endometriosis (i.e. from an adenomyotic uterus to the lumbosacral plexus via pelvic autonomic nerves, and then distally to the sciatic nerve or even proximally to the spinal nerves) has been proposed as an alternative explanation for lumbosacral or sciatic nerve involvement, particularly in the absence of peritoneal disease [66,67]. Progressive cyclic sciatica and a hyperintense mass on T1-weighted images at the region of the lumbosacral plexus or sciatic nerve may suggest the diagnosis; nerve enlargement along with heterogeneous enhancement on MR images obtained after intravenous administration of gadolinium chelate may, also, be demonstrated [67—69]. Current data support the important role of preoperative three-dimensional (3D) MR neurography for evaluating the relationship of the sacral nerve plexus and ectopic endometrial lesions assisting potentially treatment management [70].

13

Figure 19. 12-year-old adolescent presenting with catamenial pain. T2-weighted MR image in the axial plane demonstrates a typical banana-shaped unicornuate uterus (white arrow). A bloodfilled non-communicating uterine horn is seen on the left (asterisk). Patients with obstructive genital tract malformations are at high risk for developing endometriosis.

Nodal involvement Although lymph node infiltration in deep endometriosis is considered to be an atypical finding, some studies suggest that nodal involvement in endometriosis might be just underestimated because most of the surgeons do not routinely perform lymphadenectomy in cases of deep infiltrating endometriosis, as the latter is considered a benign disease. In a study conducted by Noël et al., lymph node involvement was detected in up to 42.3% of 26 patients with rectosigmoid endometriosis [71]. Nodal endometriosis may be the result of extension of deep endometrial implants within the lymphovasular spaces and, from there, via the lymphatic drainage, to the regional lymph nodes [72]. There are no specific MRI features for endometriotic nodes [72].

Endometriosis associated with obstructive genital tract anomalies Normally, menstrual blood flow exits the uterus via the cervical os; retrograde menstruation through the tubal ostia may occur in patients with severe outflow obstruction and may be associated with formation of hematosalpinges and implantation of endometriotic foci at the ovaries or deep in the pelvis [20,73]. Obstruction can occur at different levels of the genital tract, and may be congenital or acquired. Congenital obstructive reproductive tract disorders include the presence of a non-communicating uterine horn with functional endometrium (Fig. 19), cervical agenesis/dysgenesis, vaginal abnormalities (agenesis, transverse septum) or even an imperforate hymen. Although it is reported that the incidence of endometriosis is not higher in patients with Müllerian anomalies, endometriosis is strongly associated with obstructive malformations [74]. Therefore, endometriosis related to a reproductive tract anomaly, may be the cause of chronic pelvic pain in an adolescent patient [20]. Acquired cervical or isthmic stenosis as a postoperative complication (e.g. post-trachelectomy) may be yet another cause of severe outflow obstruction, potentially predisposing to secondary endometriosis [75]. MRI may readily demonstrate

complications of genital tract outflow obstruction, such as hematocolpos, hematometra, and/or hematosalpinx, as well as coexisting endometriosis (Figs. 20 and 21). In addition, MRI provides important information on the morphology of the female reproductive system and it exhibits high accuracy in localizing the site of obstruction along its course, potentially assisting surgical treatment [76].

Endometriosis in men Endometriosis in a male is extremely rare. In most patients, it occurred in association with increased estrogen levels (prostate cancer under hormonal therapy, liver cirrhosis), presumably causing metaplasia of rests of Mullerian cells [77].

Endometriosis-related malignancy Only a small percent of endometriotic lesions (< 2.5%) undergo malignant transformation, most often those located at the ovaries (75%). Endometrioid or clear cell carcinomas are the most common subtypes arising in a preexisting endometrioid cyst; extra-adnexal endometriotic malignancy is of endometrioid sarcomatous histology. Women with endometriosis — related ovarian cancer are younger (at least 10—20 years) and have better prognosis than women who develop ovarian cancer without a history of endometriosis. Typical imaging features of malignant endometriomas, include the presence of a solid components within the endometriotic cyst (they usually appear as contrast-enhanced mural nodules), thick (> 3 mm) internal septa, cyst enlargement on serial follow-up or loss of the T2 shading sign due to tumor secretions (Fig. 22); secondary features such as presence of ascites or peritoneal nodules often indicate malignancy. Tumor markers like CA-125 may be helpful for the discrimination between malignant and non-malignant endometriomas; although CA-125

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

14

C. Bourgioti et al.

Figure 20. 34-year-old woman presenting with prolonged and painful menstruation, two years after abdominal radical trachelectomy for cervical cancer. A. T2-weighted MR image in the sagittal plane clearly demonstrates the hemorrhagic fluid-fluid level within the distended endometrial cavity (small arrows) due to severe stenosis at the uterovaginal anastomosis (long arrow). B. T2-weighted MR image in the axial plane of the same patient shows concomitant right sided hematosalpinx (white arrow). The diagnosis of endometriosis was laparoscopically confirmed.

Figure 21. 24-year-old woman with vaginal agenesis but normal uterus and ovaries. A. T2-weighted MR image in the sagittal plane of the lower abdomen demonstrates a large cystic mass (black arrows) within the left rectus abdominis muscle. B. T1-weighted fat-suppressed MR image in the axial plane of the same patient shows high signal intensity of the mass consistent with subacute hemorrhagic content (white arrow). Pathological examination was diagnostic of endometrioma. Note the hemorrhagic fluid-fluid level within the distended non-communicating endometrial cavity (asterisk in A).

serum levels can also elevated in benign endometriosis, they are usually considerably higher in cases of malignancy [12,13,44]. Interestingly, recent studies report that patients with endometriosis seem to have an increased risk for developing

type I (i.e. endometrioid) endometrial cancer. Additionally, there is some evidence that endometriosis may be related to breast cancer, particularly in patients with initial diagnosis of endometriosis at advanced age (≥ 50 years); however, data remain controversial and require further investigation [78].

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

MR imaging of endometriosis: Spectrum of disease

Figure 22. 39-year-old woman with no history of endometriosis, high Ca-125 and a right adnexal mass on routine ultrasound examination. T2-weighted MR image in the coronal plane shows a cystic and solid mass (black arrows) arising from the right ovary (white arrow). Histolopathological examination of the surgical specimen revealed clear cell carcinoma with sarcomatous elements, arising from a preexisting ovarian endometrioma.

Conclusion In endometriosis, the functional endometrium may be implanted in any tissue within or outside the pelvis and this results to a variety of clinical and imaging manifestations, which, in a considerable number of cases, may constitute a diagnostic challenge. Currently, MRI may be used as a problem-solving tool in cases of indeterminate adnexal findings on sonography, when deep infiltrating endometriosis is suspected, or for presurgical mapping. Knowledge of typical MR imaging features of endometriosis should help radiologists make the appropriate diagnosis. In cases with atypical locations, MRI findings combined with the history of catamenial symptoms may aid the diagnosis.

Disclosure of interest The authors declare that they have no competing interest.

References [1] Von Rokitansky C. Ueber uterusdrüsen — neubildung in uterus — und ovarial-sarcomen. Ztsch K K Gesellsch der Aerzte zu Wien 1860;37:577—81. [2] Giudice LC. Clinical practice. Endometriosis. N Engl J Med 2010;362:2389—98. [3] Markham SM. Extrapelvic endometriosis. In: Modern approaches to endometriosis. Netherlands: Springer; 1991. p. 151—82.

15 [4] Woodward PJ, Sohaey R, Mezzetti Jr TP. Endometriosis: radiologic—pathologic correlation. Radiographics 2001;21:193—216. [5] Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, D’Hooghe T, De Bie B, et al. ESHRE guideline: management of women with endometriosis. Hum Reprod 2014;29:400—12. [6] Bazot M, Bharwani N, Huchon C, Kinkel K, Cunha TM, Guerra A, et al. European society of urogenital radiology (ESUR) guidelines: MR imaging of pelvic endometriosis. Eur Radiol 2016, http://dx.doi.org/10.1007/s00330-016-4673-z. [7] Stratton P, Winkel C, Premkumar A, Chow C, Wilson J, HearnsStokes R, et al. Diagnostic accuracy of laparoscopy, magnetic resonance imaging, and histopathologic examination for the detection of endometriosis. Fertil Steril 2003;79:1078—85. [8] Gougoutas CA, Siegelman ES, Hunt J, Outwater EK. Pelvic endometriosis: various manifestations and MR imaging findings. AJR Am J Roentgenol 2000;175:353—8. [9] Bazot M, Darai E, Hourani R, Thomassin I, Cortez A, Uzan S, et al. Deep pelvic endometriosis: MR imaging for diagnosis and prediction of extension of disease. Radiology 2004;232:379—89. [10] Ha HK, Lim YT, Kim HS, Suh TS, Song HH, Kim SJ. Diagnosis of pelvic endometriosis: fat-suppressed T1-weighted vs conventional MR images. AJR Am J Roentgenol 1994;163:127—31. [11] Tanaka YO, Itai Y, Anno I, Matsumoto K, Ebihara R, Nishida M. MR staging of pelvic endometriosis: role of fat-suppression T1weighted images. Radiat Med 1996;14:111—6. [12] Siegelman ES, Oliver ER. MR imaging of endometriosis: ten imaging pearls. Radiographics 2012;32:1675—91. [13] Grasso RF, Zobel BB, Del Vescovo R, Cazzato RL. Pelvic endometriosis: a MR pictorial review. In: endometriosis-basic concepts and current research trends. InTech Open Access Publisher; 2012. p. 447—58. [14] Corwin MT, Gerscovich EO, Lamba R, Wilson M, McGahan JP. Differentiation of ovarian endometriomas from hemorrhagic cysts at MR imaging: utility of the T2 dark spot sign. Radiology 2014;271:126—32. [15] Lee YR. CT imaging findings of ruptured ovarian endometriotic cysts: emphasis on the differential diagnosis with ruptured ovarian functional cysts. Korean J Radiol 2011;12:59—65. [16] Evangelinakis N, Grammatikakis I, Salamalekis G, Tziortzioti V, Samaras C, Chrelias C, et al. Prevalence of acute hemoperitoneum in patients with endometriotic ovarian cysts: a 7-year retrospective study. Clin Exp Obstet Gynecol 2009;36: 254—5. [17] Chen MJ, Yang JH, Yang YS, Ho HN. Increased occurrence of tubo-ovarian abscesses in women with stage III and IV endometriosis. Fertil Steril 2004;82:498—9. [18] El-Toukhy T, Hanna L. Spontaneous ovarian abscess associated with an endometrioma. J Obstet Gynaecol 2007;27:328—9. [19] Kavoussi SK, Pearlman MD, Burke WM, Lebovic DI. Endometrioma complicated by tubo-ovarian abscess in a woman with bacterial vaginosis. Infect Dis Obstet Gynecol 2006;2006:84140. [20] Bennett GL, Slywotzky CM, Cantera M, Hecht EM. Unusual manifestations and complications of endometriosis–spectrum of imaging findings: pictorial review. AJR Am J Roentgenol 2010;194(Suppl 6):WS34—46. [21] Morisawa N, Kido A, Kataoka M, Minamiguchi S, Konishi I, Togashi K. Magnetic resonance imaging manifestations of decidualized endometriotic cysts: comparative study with ovarian cancers associated with endometriotic cysts. J Comput Assist Tomogr 2014;38:879—84. [22] Takeuchi M, Matsuzaki K, Harada M. Computed diffusionweighted imaging for differentiating decidualized endometrioma from ovarian cancer. Eur J Radiol 2016;85:1016—9. [23] Pateman K, Moro F, Mavrelos D, Foo X, Hoo WL, Jurkovic D. Natural history of ovarian endometrioma in pregnancy. BMC Womens Health 2014;14:128.

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

16 [24] Vu D, Haylen BT, Tse K, Farnsworth A. Surgical anatomy of the uterosacral ligament. Int Urogynecol J 2010;21:1123—8. [25] Umek WH, Morgan DM, Ashton-Miller JA, DeLancey JO. Quantitative analysis of uterosacral ligament origin and insertion points by magnetic resonance imaging. Obstet Gynecol 2004;103:447—51. [26] Bazot M, Gasner A, Ballester M, Daraï E. Value of thinsection oblique axial T2-weighted magnetic resonance images to assess uterosacral ligament endometriosis. Hum Reprod 2011;26:346—53. [27] Gui B, Valentini AL, Ninivaggi V, Marino M, Iacobucci M, Bonomo L. Deep pelvic endometriosis: do not forget round ligaments. Review of anatomy, clinical characteristics, and MR imaging features. Abdom Imaging 2014;39:622—32. [28] Kinkel K, Chapron C, Balleyguier C, Fritel X, Dubuisson JB, Moreau JF. Magnetic resonance imaging characteristics of deep endometriosis. Hum Reprod 1999;14:1080—6. [29] Saba L, Sulcis R, Melis GB, Ibba G, Alcazar JL, Piga M, et al. Diagnostic confidence analysis in the magnetic resonance imaging of ovarian and deep endometriosis: comparison with surgical results. Eur Radiol 2014;24:335—43. [30] Coutinho Jr A, Bittencourt LK, Pires CE, Junqueira F, Lima CM, Coutinho E, et al. MR imaging in deep pelvic endometriosis: a pictorial essay. Radiographics 2011;31:549—67. [31] Crispi CP, de Souza CA, Oliveira MA, Dibi RP, Cardeman L, Sato H, et al. Endometriosis of the round ligament of the uterus. J Minim Invasive Gynecol 2012;19:46—51. [32] Chamié LP, Blasbalg R, Pereira RM, Warmbrand G, Serafini PC. Findings of pelvic endometriosis at transvaginal US, MR imaging, and laparoscopy. Radiographics 2011;31:E77—100. [33] Kataoka ML, Togashi K, Yamaoka T, Koyama T, Ueda H, Kobayashi H, et al. Posterior cul-de-sac obliteration associated with endometriosis: MR imaging evaluation. Radiology 2005;234:815—23. [34] Medeiros LR, Rosa MI, Silva BR, Reis ME, Simon CS, Dondossola ER, et al. Accuracy of magnetic resonance in deeply infiltrating endometriosis: a systematic review and meta-analysis. Arch Gynecol Obstet 2015;291:611—21. [35] Levy G, Dehaene A, Laurent N, Lernout M, Collinet P, Lucot JP, et al. An update on adenomyosis. Diagn Interv Imaging 2013;94:3—25. [36] Outwater EK, Siegelman ES, Chiowanich P, Kilger AM, Dunton CJ, Talerman A. Dilated fallopian tubes: MR imaging characteristics. Radiology 1998;208:463—9. [37] Rousset P, Peyron N, Charlot M, Chateau F, Golfier F, Raudrant D, et al. Bowel endometriosis: preoperative diagnostic accuracy of 3.0-T MR enterography — initial results. Radiology 2014;273:117—24. [38] Ruffo G, Stepniewska A, Crippa S, Serboli G, Zardini C, Steinkasserer M, et al. Laparoscopic ileocecal resection for bowel endometriosis. Surg Endosc 2011;25:1257—62. [39] Gimonet H, Laigle-Quérat V, Ploteau S, Veluppillai C, Leclère B, Frampas E. Is pelvic MRI in women presenting with pelvic endometriosis suggestive of associated ileal, appendicular, or cecal involvement? Abdom Radiol 2016;41: 2404—10. [40] Trippia CH, Zomer MT, Terazaki CR, Martin LR, Ribeiro R, Kondo W. Relevance of imaging examinations in the surgical planning of patients with bowel endometriosis. Clin Med Insights Reprod Health 2016;10:1—8. [41] Wolthuis AM, Tomassetti C. Multidisciplinary laparoscopic treatment for bowel endometriosis. Best Pract Res Clin Gastroenterol 2014;28:53—67. [42] Bazot M, Jarboui L, Ballester M, Touboul C, Thomassin-Naggara I, Daraï E. The value of MRI in assessing parametrial involvement in endometriosis. Hum Reprod 2012;27:2352—8. [43] Ballester M, Santulli P, Bazot M, Coutant C, Rouzier R, Daraï E. Preoperative evaluation of posterior deep-infiltrating endo-

C. Bourgioti et al.

[44]

[45]

[46]

[47]

[48] [49]

[50]

[51]

[52]

[53]

[54]

[55]

[56]

[57]

[58] [59]

[60]

[61] [62] [63]

[64]

[65]

metriosis demonstrates a relationship with urinary dysfunction and parametrial involvement. J Minim Invasive Gynecol 2011;18:36—42. Choudhary S, Fasih N, Papadatos D, Surabhi VR. Unusual imaging appearances of endometriosis. AJR Am J Roentgenol 2009;192:1632—44. Ponticelli C, Graziani G, Montanari E. Ureteral endometriosis: a rare and underdiagnosed cause of kidney dysfunction. Nephron Clin Pract 2010;114:c89—93. Seyam R, Mokhtar A, Al Taweel W, Al Sayyah A, Tulbah A, Al Khudair W. Isolated ureteric endometriosis presenting as a ureteric tumor. Urol Ann 2014;6:94—7. Teh J, Leung J, Dhar S, Athanasou NA. Abdominal wall endometriosis: comparative imaging on power Doppler ultrasound and MRI. Clin Radiol Extra 2004;59:74—7. Choudhury SS, Choudhury MK. Episiotomy scar endometriosis: a case report. J Obstet Gynaecol Barpeta 2014;1:120—1. Llewellyn-Bennett R, Sieunnaire K. Iatrogenic endometriosis of the vaginal vault following a total laparoscopic hysterectomy. West London Med J 2010;2:1—4. Hoeffel C, Crema MD, Azizi L, Lewin M, Monnier-Cholley L, Arrivé L, et al. Magnetic resonance imaging of the ischiorectal fossa: spectrum of disease. J Comput Assist Tomogr 2007;31:251—7. Inal M, Bıc ¸akc ¸i K, Soyupak S, O˘ guz M, Özer C, Demirbas¸ Ö, et al. Hepatic endometrioma: a case report and review of the literature. Eur Radiol 2000;10:431—4. Goldsmith PJ, Ahmad N, Dasgupta D, Campbell J, Guthrie JA, Lodge JP. Case hepatic endometriosis: a continuing diagnostic dilemma. HPB Surg 2009;2009:407206. Plodeck V, Sommer U, Baretton GB, Aust DE, Laniado M, Hoffmann RT, et al. A rare case of pancreatic endometriosis in a postmenopausal woman and review of the literature. Acta Radiol Open 2016;5 [2058460116669385]. Rousset P, Rousset-Jablonski C, Alifano M, Mansuet-Lupo A, Buy JN, Revel MP. Thoracic endometriosis syndrome: CT and MRI features. Clin Radiol 2014;69:323—30. Ceccaroni M, Roviglione G, Giampaolino P, Clarizia R, Bruni F, Ruffo G, et al. Laparoscopic surgical treatment of diaphragmatic endometriosis: a 7-year single-institution retrospective review. Surg Endosc 2013;27:625—32. Machairiotis N, Stylianaki A, Dryllis G, Zarogoulidis P, Kouroutou P, Tsiamis N, et al. Extrapelvic endometriosis: a rare entity or an under diagnosed condition? Diagn Pathol 2013;8:194. Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol 1927;3:93—110. Kirschner PA. Porous diaphragm syndromes. Chest Surg Clin N Am 1998;8:449—72. Rousset P, Gregory J, Rousset-Jablonski C, Hugon-Rodin J, Regnard JF, Chapron C, et al. MR diagnosis of diaphragmatic endometriosis. Eur Radiol 2016;26:3968—77. Sarma D, Iyengar P, Marotta TR, terBrugge KG, Gentili F, Halliday W. Cerebellar endometriosis. AJR Am J Roentgenol 2004;182:1543—6. Dongxu Z, Fei Y, Xing X, Bo-Yin Z, Qingsan Z. Low back pain tied to spinal endometriosis. Eur Spine J 2014;23(Suppl 2):214—7. Ramalingappa A, Reddy Y. A rare presentation of endometriosis. J Obstet Gynaecol India 2012;62(Suppl 1):94—6. Vercellini P, Chapron C, Fedele L, Frontino G, Zaina B, Crosignani PG. Evidence for asymmetric distribution of sciatic nerve endometriosis. Obstet Gynecol 2003;102:383—7. Redwine D. Evidence for asymmetric distribution of sciatic nerve endometriosis. Obstet Gynecol 2003;102:1416 [author reply 1416-7]. Batt RE, Yeh J, Koninckx PR. Asymmetric distribution of sciatic nerve endometriosis. Obstet Gynecol 2004;103:400—1 [author reply 401].

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009

+Model DIII-947; No. of Pages 17

ARTICLE IN PRESS

MR imaging of endometriosis: Spectrum of disease [66] Siquara De Sousa AC, Capek S, Amrami KK, Spinner RJ. Neural involvement in endometriosis: review of anatomic distribution and mechanisms. Clin Anat 2015;28:1029—38. [67] Siquara de Sousa AC, Capek S, Howe BM, Jentoft ME, Amrami KK, Spinner RJ. Magnetic resonance imaging evidence for perineural spread of endometriosis to the lumbosacral plexus: report of 2 cases. Neurosurg Focus 2015;39:E15. [68] Papapietro N, Gulino G, Zobel BB, Di Martino A, Denaro V. Cyclic sciatica related to an extrapelvic endometriosis of the sciatic nerve: new concepts in surgical therapy. J Spinal Disord Tech 2002;15:436—9. [69] Cottier JP, Descamps P, Sonier CB, Rosset P. Sciatic endometriosis: MR evaluation. AJNR Am J Neuroradiol 1995;16:1399—401. [70] Zhang X, Li M, Guan J, Wang H, Li S, Guo Y, et al. Evaluation of the sacral nerve plexus in pelvic endometriosis by three-dimensional MR neurography. J Magn Reson Imaging 2017;45:1225—31. [71] Noël JC, Chapron C, Fayt I, Anaf V. Lymph node involvement and lymphovascular invasion in deep infiltrating rectosigmoid endometriosis. Fertil Steril 2008;89:1069—72. [72] Cacciato Insilla A, Granai M, Gallippi G, Giusti P, Giusti S, Guadagni S, et al. Deep endometriosis with pericolic lymph

17

[73]

[74]

[75]

[76]

[77] [78]

node involvement: a case report and literature review. World J Gastroenterol 2014;20:6675—9. Barbieri RL. Stenosis of the external cervical os: an association with endometriosis in women with chronic pelvic pain. Fertil Steril 1998;70:571—3. Ugur M, Turan C, Mungan T, Kuscu E, Senoz S, Agis HT, et al. Endometriosis in association with müllerian anomalies. Gynecol Obstet Invest 1995;40:261—4. Bourgioti C, Koutoulidis V, Chatoupis K, Rodolakis A, Koureas A, Thomakos N, et al. MRI findings before and after abdominal radical trachelectomy (ART) for cervical cancer: a prospective study and review of the literature. Clin Radiol 2014;69: 678—86. Zhang H, Qu H, Ning G, Cheng B, Jia F, Li X, et al. MRI in the evaluation of obstructive reproductive tract anomalies in paediatric patients. Clin Radiol 2017, http://dx.doi.org/ 10.1016/j.crad.2017.02.002. Martin Jr JD, Hauck AE. Endometriosis in the male. Am Surg 1985;51:426—30. Mogensen JB, Kjær SK, Mellemkjær L, Jensen A. Endometriosis and risks for ovarian, endometrial and breast cancers: a nationwide cohort study. Gynecol Oncol 2016;143:87—92.

Please cite this article in press as: Bourgioti C, et al. MR imaging of endometriosis: Spectrum of disease. Diagnostic and Interventional Imaging (2017), http://dx.doi.org/10.1016/j.diii.2017.05.009