MR Imaging in Deep Pelvic Endometriosis: A Pictorial Essay 1

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Women’s Imaging

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MR Imaging in Deep Pelvic Endometriosis: A Pictorial Essay1 Online-Only CME See www.rsna .org/education /rg_cme.html

LEARNING OBJECTIVES After reading this article and taking the test, the reader will be able to: ■■Identify

the normal anatomy of the female pelvis.

■■List

the various anatomic sites of deep infiltrating endometriosis involvement.

■■Describe

the most common MR imaging findings of deep pelvic endometriosis.

Antônio Coutinho, Jr, MD • Leonardo Kayat Bittencourt, MD • Cíntia E. Pires, MD • Flávia Junqueira, MD • Cláudio Márcio Amaral de Oliveira Lima, MD • Elisa Coutinho, MD • Marisa A. Domingues, MD • Romeu C. Domingues, MD • Edson Marchiori, MD, PhD Deep pelvic endometriosis is an important gynecologic disorder that is responsible for severe pelvic pain and is defined as subperitoneal invasion that exceeds 5 mm in depth. Deep pelvic endometriosis can affect the retrocervical region, uterosacral ligaments, rectum, rectovaginal septum, vagina, urinary tract, and other extraperitoneal pelvic sites. It is commonly associated with dysmenorrhea, dyspareunia, pelvic pain, urinary tract symptoms, and infertility. Because surgery remains the best therapeutic option for affected patients, the accurate preoperative assessment of the extension of endometriotic disease is extremely important. Pelvic magnetic resonance (MR) imaging is a noninvasive method with high spatial resolution that allows multiplanar evaluation of deep pelvic endometriosis and good tissue characterization, but without the use of ionizing radiation or iodinated contrast agents. MR imaging yields important findings that help grade the disease and identify subperitoneal lesion extension and other associated disease entities, thereby facilitating accurate diagnosis and adequate treatment. Radiologists should be familiar with the MR imaging findings of deep infiltrating endometriosis in various anatomic locations so that they can provide information that allows adequate presurgical counseling. ©

RSNA, 2011 • radiographics.rsna.org

RadioGraphics 2011; 31:549–567 • Published online 10.1148/rg.312105144 • Content Codes: 1 From the Clínica de Diagnóstico Por Imagem (CDPI), Av das Américas 4666, Sala 325, Barra da Tijuca, Rio de Janeiro, RJ 22649900, Brazil (A.C., L.K.B., C.E.P., F.J., E.C., M.A.D., R.C.D.); Multi-Imagem, Rio de Janeiro, Brazil (A.C., L.K.B., E.C., M.A.D., R.C.D.); Fátima Digittal, Nova Iguaçu, Brazil (A.C., C.M.A.d.O.L., E.C.); Department of Radiology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil (L.K.B., F.J., E.M.); and Carlos Bittencourt Diagnóstico, Rio de Janeiro, Brazil (L.K.B.). Recipient of a Cum Laude award for an education exhibit at the 2009 RSNA Annual Meeting. Received May 28, 2010; revision requested July 7; final revision received November 8; accepted November 16. For this CME activity, the authors, editors, and reviewers have no relevant relationships to disclose. Address correspondence to L.K.B. (e-mail: [email protected]).

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Introduction

Endometriosis is defined as the presence of functional endometrial glands and stroma outside the uterine cavity. It is a common and important gynecologic disorder that primarily affects women of reproductive age, who may be either symptomatic or asymptomatic, and has an estimated prevalence of 5%–20% (1–3). The ectopic endometrium responds to hormonal stimulation with various degrees of cyclic hemorrhage, resulting in symptoms and imaging features that suggest the diagnosis of endometriosis (4). Radiologists often use the terms endometriosis and endometriomas interchangeably. However, it is important to remember that endometriomas constitute only a part of the disease process known as endometriosis, which also includes endometriotic implants (peritoneal and extraperitoneal) and adhesions (2). Deep pelvic endometriosis, also known as deep infiltrating endometriosis involvement, is defined as subperitoneal invasion by endometriotic lesions that exceeds 5 mm in depth. It can affect fibromuscular pelvic structures, such as the rectovaginal septum and uterosacral ligaments (69.2% of cases), as well as the vagina (14.5%), alimentary tract (9.9%), urinary tract (6.4%), and other extraperitoneal pelvic sites (5). Although peritoneal endometriosis is often asymptomatic, deep pelvic endometriosis is frequently associated with dysmenorrhea, dyspareunia, pelvic pain, urinary tract symptoms, and infertility. Unusual findings such as pneumothorax and epistaxis may be seen when endometriotic implants occur in atypical locations outside the pelvis. In this article, we discuss deep pelvic endometriosis in terms of its etiology and pathogenesis, as well as its diagnosis and evaluation. In addition, we describe MR imaging protocol in affected patients, the normal anatomy and MR imaging appearances of the female pelvis, and the most common manifestations of deep pelvic endometriosis at MR imaging.

Etiology and Pathogenesis

The etiology and pathogenesis of endometriosis are still unclear and are probably multifactorial. Three theories of histopathogenesis have been proposed: the metastatic theory, the metaplastic theory, and the induction theory. In addition, researchers are presently investigating the role

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of growth factors, immunity, and other mechanisms that may contribute to the development of this disorder (2). The metastatic theory is the most widely accepted theory at present. According to this theory, endometriosis results from the metastatic implantation of endometrial tissue from retrograde menstruation—that is, viable endometrial tissue refluxes through the fallopian tube during menstruation and is then deposited on the peritoneal surface or pelvic organs (6). One major piece of evidence to support this theory is the anatomic pattern of the disease distribution within the dependent areas of the pelvis. Endometriosis is also seen with greater frequency in women with excessive retrograde flow due to obstructive anomalies of müllerian duct development (2). However, because up to 90% of women have physiologically bloody peritoneal fluid during the perimenstrual period, it is probable that other factors, such as impairment of the immune response during the removal of peritoneal menstrual debris, also play a role in the pathogenesis of endometriosis (2). Other possible means of metastatic spread include the transport of endometrial cells to distant sites from the pelvis via the bloodstream or lymphatic channels, and iatrogenic spread during needle biopsy or surgery. In particular, extraperitoneal pelvic sites of endometriotic involvement such as the perineal area in the absence of previous surgical manipulation are believed to be associated with benign lymphatic metastasis of endometriosis, since there is abundant lymphatic communication between the uterus, cervix, vagina, and perineum (7). Moreover, there have been several reports of extrapelvic endometriosis, even in organs far from the endometrial cavity (eg, lungs, brain), which strengthens the potential for the lymphatic or vascular spread of endometrial cells (8). The metaplastic theory of pathogenesis is related to the metaplastic differentiation of serosal surfaces (coelomic epithelium) or the remnants of müllerian tissue. This theory suggests the possibility of peritoneal cells differentiating into functioning endometrial cells, since both endometrial and peritoneal cells derive from coelomic wall epithelium. The strongest evidence for this theory is the demonstration of endometriosis in women who lack functional eutopic endometrium (including those with Turner syndrome, gonadal dysgenesis, or uterine agenesis) as well as in men (2).

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The induction theory combines the first two proposed mechanisms and suggests that shed endometrium releases substances that induce undifferentiated mesenchyme to form endometriotic tissue (2).

Diagnosis and Evaluation

The diagnosis and evaluation of the extension of deep pelvic endometriosis is difficult with physical examination and laparoscopic exploration alone, not only because it requires the palpation and opening of the subperitoneal space to confirm the presence of the lesions, but also because these methods may not allow the diagnosis or prediction of disease extension, especially in pelvic subperitoneal sites and in regions that are obscured by pelvic adhesions (9). Transvaginal ultrasonography (US) is usually the first imaging technique used to diagnose endometriosis and remains the most accessible technique. It is the method of choice for differentiating endometriomas from other ovarian cysts. In recent years, certain studies have emphasized the use of transvaginal US in identifying deep endometriosis, especially in detecting lesions of the rectal wall and retrocervical space, and promising results have been described in terms of the evaluation capacity and tolerability of this technique (10). However, the accuracy of transvaginal US in the detection of some deep endometriotic lesions may vary depending on the location of the lesions and the experience of the operator. Rectal endoscopic US with high-frequency probes has been recommended for the detection of endometriosis in the rectum, rectovagina, uterosacrum, and rectosigmoid region (11), even though high-frequency US has poor penetration. The main advantage of this method is that it provides a reliable means of diagnosing bowel wall infiltration, being superior to MR imaging in this respect (9,12,13). Because the standard treatment for deep endometrial extensions is complete surgical excision of the endometriotic lesions, presurgical diagnosis and accurate knowledge of the precise location of the lesions are essential prerequisites for successful outcomes. Therefore, the preoperative workup is extremely important and is generally limited when evaluated only by clinical manifestations and US findings. MR imaging is a noninvasive imaging method with high spatial resolution that allows multiplanar evaluation and good tissue characterization, but without the use of ionizing radiation or iodinated

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contrast agents. In addition, it is highly accurate in the diagnosis of infiltrating extraperitoneal endometriosis and allows the identification of lesions that are hidden by adhesions and the evaluation of subperitoneal lesion extension (3,9). MR imaging also possesses a huge advantage over other imaging modalities in that it allows a complete survey of the anterior and posterior compartments of the pelvis to be made with a single study (14).

MR Imaging Protocol

At our institution, examinations are performed regardless of the stage of the patient’s menstrual cycle, since there is still no strong evidence that MR imaging performed during the menstrual period has greater diagnostic accuracy (15). However, the dates of the patient’s last menstrual period are always recorded for purposes of interpretation. Patients are requested to fast for 6 hours before the examination; no special bowel preparation is required. MR imaging is performed with moderate repletion of the patient’s bladder, since an empty or overfilled bladder may obliterate the adjacent recesses and compromise the identification of smaller lesions. An intravenously administered antispasmodic agent, scopolamine-N-butyl bromide (Buscopan; Boehringer Ingelheim, Itapecerica, Brazil), is administered immediately before the examination to reduce motion artifacts caused by peristalsis and to attenuate uterine contractions. Although it is not essential for the evaluation of endometriosis, intravaginal aqueous gel (50 mL) is frequently administered to distend the vaginal cavity and allow better assessment of the retrocervical area and vaginal fornices. However, endorectal gel or saline solution is administered only in the presence of symptoms that may be related to rectal involvement, such as constipation, hematochezia, or painful defecation. Images in this study were acquired on a 3-T imager (Tim TRIO; Siemens, Erlangen, Germany). Our standard imaging protocol is detailed in the Table and includes an axial dark fluid inversion-recovery T1-weighted sequence; axial and sagittal fat-suppressed fast spin-echo T1weighted sequences; and axial, oblique coronal, and sagittal T2-weighted sequences. Intravenous administration of a gadolinium chelate (Dotarem; Guerbet, Villepinte, France) is frequently performed, and the dynamic acquisition of axial and sagittal volumetric fat-saturated T1-weighted

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MR Imaging Protocol for Deep Pelvic Endometriosis Imaging Sequence

Parameter

Dark Fluid Inversion-Recovery T1-weighted

Imaging planes

Axial

Repetition time (msec) Echo time (msec) Inversion time (msec) Field of view (mm) Section thickness (mm) Intersection gap (%) Matrix No. of signals acquired

1900 20 768 250 × 230 4 30 256 × 256 1

T2-weighted Axial, oblique coronal, sagittal 3610 108 ... 240 × 240 3.5 10 384 × 326 2

images then takes place in the precontrast phase. Beginning 10 seconds after the injection of the gadolinium chelate, axial and sagittal contrast material–enhanced images are acquired, and these images yield the most information. In cases of suspected ureteral involvement, MR urographic techniques are used to obtain (for example) coronal heavily T2-weighted images or threedimensional reconstructed images from coronal volumetric excretory phase T1-weighted data. Fat-suppressed T1-weighted sequences are the most sensitive for the detection of bloody foci, whereas high-resolution T2-weighted sequences are used for the evaluation of fibrotic lesions, notably those that involve the pelvic ligaments, retrocervical space, or prevesical recess. In addition, for the diagnosis of endometriomas, a combination of T1-weighted and T2-weighted sequences is useful, owing to the “shading” effect that characterizes these lesions.

Normal Anatomy and MR Imaging Appearances of the Female Pelvis

The anatomy of the female pelvis and perineum is best understood when these regions are subdivided according to functional and clinical requirements into anterior, middle, and posterior compartments (16).

Anterior Compartment The contents of the anterior compartment of the pelvis include the urinary bladder and urethra.

Fat-suppressed Fast Spin-Echo T1-weighted

Dynamic Gadoliniumenhanced Volumetric Fatsaturated T1-weighted

Axial, sagittal

Axial, sagittal

706 14 ... 250 × 250 4 45 230 × 256 1

2.46 0.94 ... 380 × 380 1.5 20 256 × 256 1

These structures are located in the lesser pelvis, anterior to the uterus-vagina and posterior to the pubic symphysis. Fat planes known as the vesicovaginal septum and prevesical space separate these structures (Fig 1) (16). The bladder dome is covered by peritoneum, which creates an anterior fold with the pelvic wall known as the prevesical recess, and a posterior fold over the uterus known as the vesicouterine pouch or anterior cul-de-sac. The latter location is a common site of deep infiltrating endometriosis involvement (16). The ureters course posteromedially over the external iliac vessels toward their respective meatuses on the bladder. Each ureter passes through the paracervical space, lateral to the uterosacral ligaments and immediately inferior to the cardinal ligaments. Oblique coronal T2-weighted MR images (obtained parallel to the short axis of the uterus) are used to evaluate these relationships, and parasagittal T2-weighted images are used to assess the ureteral meatuses.

Middle Compartment The middle compartment contains the female genital organs, including the ovaries, uterine tubes, uterus, and vagina. The broad ligaments are peritoneal folds between the uterus and the lateral walls of the pelvis and are also a part of the rectouterine and vesicouterine folds. The ovaries lie in the ovarian fossa and are suspended from a double fold of peritoneum known as the mesovarium. Behind the ovarian fossa are extraperitoneal structures, including the ureters and the internal iliac vessels in particular (16).

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Figure 1.  Normal anatomy of the anterior compartment. (a) Sagittal T2-weighted MR image shows the bladder (*), prevesical space (outlined in white), vesicouterine pouch (outlined in red), and vesicovaginal septum (outlined in yellow). (b) Model of the female pelvis (sagittal view) shows the prevesical recess (black *), vesicouterine pouch (white *), fat-occupied prevesical space (black arrow), and vesicovaginal septum (white arrow).

Figure 2.  Normal anatomy of the posterior compartment. Parasagittal (a) and midsagittal (b) T2-weighted MR images show the perineal body (white arrow in a), rectovaginal septum (* in a, outlined in red in b), and rectovaginal pouch (black arrow in a, outlined in white in b).

Posterior Compartment The posterior compartment is dominated by the rectum and its surrounding connective tissue. The morphologic demarcation of this compartment is formed by the rectal fascia, which is visible at MR imaging as a thin hypointense structure that borders the perirectal compartment (16). The rectovaginal septum is a thin membranous partition that is usually filled with fat. It is located between the posterior vaginal wall and the anterior rectal wall and extends from the

deepest part of the pouch of Douglas to the top of the perineal body (Fig 2) (16). In the absence of interstitial fat, the vaginal and rectal walls are indistinguishable on MR images (4). When the vagina and rectum are distended with gel, they are usually clearly delineated as well-defined, regular, thin hypointense structures with a thickness of 3 mm or less (17). The rectouterine folds contain considerable fibrous tissue and nonstriated muscular fibers

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that are attached to the front of the sacrum and constitute the uterosacral ligaments. The latter structures are visible at MR imaging as thin, semicircular hypointense cords that originate from the lateral margin of the uterine cervix and the vaginal vault and course dorsocranially toward the sacrum (Fig 3) (15). The torus uterinus is a small transverse thickening that binds the original insertion of the uterosacral ligaments behind the posterior cervix; however, it is not clearly defined on MR images in the absence of pathologic thickening (17). The retrocervical area is a virtual extraperitoneal space behind the cervix, situated in the same plane as the rectovaginal pouch and above the rectovaginal septum (Fig 3). The vaginal fornices are the deepest portions of the vagina and extend into the recesses created by the extension of the cervix into the vaginal space. The posterior vaginal fornix is the larger recess and is located posterior to the uterine cervix; it appears as a curved regular cavity, with the vaginal cuff attached to the posteroinferior part of the cervix (5). The rectovaginal pouch, or pouch of Douglas, is a deep peritoneal pouch situated between the bilateral rectouterine folds. It is the most inferior part of the peritoneal cavity, covering part of the vagina and rectum, and its base is the upper limit of the rectovaginal septum. The rectovaginal pouch extends to the middle third of the vagina in 93% of women (16). It is usually not clearly depicted unless peritoneal fluid is present.

Abnormal MR Imaging Findings

For a better understanding of the signal intensity characteristics of deep endometriosis at MR imaging, a review of the histologic findings of this disease entity is necessary. At microscopic examination, deep endometriosis is mainly characterized by fibromuscular hyperplasia that surrounds sparse ectopic endometrial glands. The ectopic endometrial foci, as well as eutopic endometrium, respond to hormonal stimulation with various degrees of cyclic hemorrhage. The episodes of bleeding within these foci result in a variable inflammatory response and fibrous reaction. In some cases, endometriosis may lack glands, and the term stromal endometriosis is then used. The endometrial glands and stroma infiltrate the adjacent fibromuscular tissue and elicit smooth muscle proliferation and fibrous reaction,

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resulting in the formation of solid nodules (1,4). In visceral solid endometriosis, these implants adhere to the serosal surface of the bowel and may invade the muscular layers, eliciting marked smooth muscle proliferation. Stricture formation and obstruction may result (5). Relatively acellular regions of fibrous tissue, as well as compact smooth muscle, have intermediate signal intensity on T1-weighted MR images and low signal intensity on T2-weighted images (17). Consequently, on T2-weighted images, solid endometriotic masses or nodules will appear as hypointense masses with irregular, indistinct, or stellate margins due to the presence of abundant fibrous tissue and smooth muscle proliferation. Deep endometriotic lesions may also be depicted as irregular and predominantly hypointense soft-tissue thickening with T2-weighted sequences. Therefore, the involvement of anatomic structures such as the uterosacral ligaments or the vaginal or rectal wall should be suspected when these structures have a hypointense thickened or nodular appearance on T2-weighted images (18). In addition, intermingled hyperintense foci may be observed with T2-weighted sequences, findings that correspond to dilated ectopic endometrial glands. On T1-weighted or fat-suppressed T1-weighted MR images, these foci may have either high or low signal intensity, depending on the presence or absence of bloody content, respectively. Some endometriomas may show restricted diffusion on diffusion-weighted images, probably due to intracystic blood clots (19). Lesion enhancement may or may not occur after the intravenous administration of contrast material, depending on the proportions of inflammatory reaction, glandular tissue, and fibrosis that are present.

Anterior Compartment Deep endometriotic lesions of the anterior compartment include endometrial implants within the vesicouterine pouch, vesicovaginal septum, bladder (detrusor muscle), and ureter. Endometriotic lesions of the urinary tract are associated with lesions in other pelvic locations in up to 50%–75% of cases (14,20,21), and it has been shown that patients with ureteral and bladder endometriosis have more advanced stages of the disease (stages III and IV according to the 1996 American Society of Reproductive Medicine criteria) than do those without urinary tract involvement (22).

RG  •  Volume 31  Number 2 Figure 3.  Normal anatomy of the female pelvis. (a, b) Axial (a) and sagittal (b) T2-weighted MR images show the uterosacral ligaments (arrows in a), rectovaginal pouch (* in b), and retrocervical area (outlined in b). (c, d) Laparoscopic images show the uterosacral ligaments (arrows in c), rectovaginal pouch (* in c), and retrocervical area (outlined in d). (e) Drawing of the female pelvis (oblique coronal view, superoinferior orientation) shows the ureters (arrows), uterosacral ligaments (arrowheads), cardinal ligaments and parametrium (black *), and round ligaments (white *). Note that the ureters course lateral to the uterosacral ligaments and immediately caudal to the cardinal and broad ligaments.

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Figure 4.  Endometriosis of the vesicouterine pouch in a 27-year-old woman with chronic pelvic pain. Sagittal T2-weighted (a), sagittal fat-suppressed T1-weighted (b), and oblique coronal T2-weighted (c) MR images depict irregular thickening of the upper external aspect of the bladder wall (arrowheads in a, arrows in c) that partially obliterates the vesicouterine recesses. Tiny bloody foci (arrow in b) are also seen, adding specificity to the finding.

On T2-weighted images, endometriosis of the vesicouterine pouch manifests as hypointense nodular formations (Fig 4) that typically adhere to the anterior uterine surface, forming an obtuse angle with the vesical wall. These lesions are usually associated with anteflexion of the uterus and obliteration of the anterior culde-sac due to extensive adhesions between the peritoneum of the bladder fold and the uterus. Endometriotic involvement of the vesicovaginal septum is also related to urinary complaints and can manifest as a cystic lesion that resembles an endometrioma (Fig 5). When there is bladder involvement, endometriotic implants are often confined to the serosal surface (extrinsic involvement); however, they can also infiltrate the muscular layer and manifest as mural masses that project into the lumen (intrinsic involvement) (Fig 6) (2). Extrinsic disease is more common, although it is often asymptomatic and is probably explained by the retrograde menstruation (metastatic) theory. Typically, there is also involvement of the vesicovaginal recess, the anterior corporal uterine serosa, or even the insertions of the uterine round ligaments.

Deep lesions may be symptomatic in up to 75% of cases, mostly with irritative voiding symptoms, suprapubic pressure (23), or cyclic hematuria (24). These lesions are more likely to be related to iatrogenic endometrial implantation, and there is a history of pelvic surgery in 43%–50% of cases. Therefore, bladder endometriosis should be considered in any patient being evaluated for endometriosis who presents with urinary tract symptoms after having undergone hysterectomy or some other gynecologic surgical procedure. Because vesical endometriosis seldom invades the mucosa, MR imaging may show abnormalities, even in patients with normal cystoscopic results or with no urinary tract symptoms (5). Bladder endometriosis can be seen at MR imaging as morphologic abnormalities (including localized or diffuse hypointense thickening of the vesical wall on T2-weighted images) that replace the normal signal of detrusor

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Figure 5.  Endometriotic involvement of the vesicovaginal septum in a 37-year-old woman who had undergone hysterectomy and presented with chronic dysuria. US showed a focal mass bulging into the posterior vesical wall. (a) Sagittal T2-weighted MR image shows a hypointense nodule (arrows) in the vesicovaginal septum. (b) On an axial fat-suppressed T1-weighted MR image, the lesion (arrowhead) has high signal intensity, which did not decrease on subsequent images. This finding indicates proteinaceous or bloody content and causes the lesion to resemble an endometrioma.

muscle. Eventually, intermingled hyperintense foci may be observed on T2-weighted images, findings that correspond to the dilated endometrial glands, with or without bloody content (25). At contrastenhanced imaging, the lesion is more enhanced than the normal bladder detrusor (15). As with bladder involvement, extrinsic endometriosis is the most common form of ureteral involvement. Endometriosis virtually never involves the ureter above the level of the pelvic brim (26). Signs and symptoms of the disease

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Figure 6.  Intrinsic bladder endometriosis in a 22-year-old woman who had undergone a cesarean section and presented with cyclic voiding symptoms but no hematuria. (a) Axial T2-weighted MR image shows hypointense irregular focal wall thickening (arrow) on the left posterolateral aspect of the bladder. Note the relative sparing of the perivesical fat (*) and the absence of enlarged lymph nodes. (b) Axial fat-suppressed T1-weighted MR image reveals that the area of wall thickening contains small intermingled hyperintense foci (arrow), a finding that indicates bloody content and that was crucial for differentiating between endometriosis and cancer. The patient underwent cystoscopy to exclude bladder cancer, and the tentative diagnosis of intrinsic bladder endometriosis was confirmed.

may be related to pelvic endometriosis itself (menstrual symptoms, dysmenorrhea, dyspareunia, gross hematuria, and pelvic masses) or secondary to urinary tract involvement (flank pain, obstruction, and decline of renal function) (27). In extrinsic involvement, endometrial tissue invades the ureteral adventitia and surrounding connective tissues (13). It originates from adjacent disease of the ovary, broad ligaments, or uterosacral ligaments (27) and follows these anatomic landmarks. In addition, scar tissue

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Figure 7.  Ureteral endometriosis in a 31-year-old woman with chronic pelvic pain and left hydronephrosis. (a) Axial T2-weighted MR image shows hypointense irregular and spiculated thickening and stranding of the perivesical fat on the left side (arrows). The ureter (arrowhead) traverses the involved area, a finding that is suggestive of infiltrating endometriosis. (b) Parasagittal T2-weighted MR image reveals moderate dilatation of the left ureter (arrowheads) to the level of the insertion of the ipsilateral uterosacral ligament (arrow), which is irregular and thickened, indicating associated deep endometriosis. (c) Fat-suppressed T1-weighted MR image shows a cystic lesion (arrow) whose high signal intensity indicates proteinaceous or bloody content. The lesion resembles an endometrioma located medial to hypointense thickening of the perivesical fat. (d) Three-dimensional contrast-enhanced fat-suppressed excretory phase T1-weighted MR urogram shows the repercussions of the findings in a–c to the urinary system. The left ureter is severely narrowed in its lower third (arrowhead), with associated upstream dilatation up to the renal pelvis (*).The lesion (arrow) is seen adjacent to the narrowed ureter and represents an endometrioma.

or fibrosis without true endometriotic invasion of the ureter may also be classified as extrinsic disease. Impairment of renal function may be observed in up to 30% of such cases (28). The ectopic endometrial tissue can also directly infiltrate the muscularis propria, lamina propria, or ureteral lumen (29) from deep infiltrating periureteral lesions or, hypothetically, from lymphatic or venous metastases (intrinsic form) (30–33), causing obstructive symptoms or resulting in cyclic hematuria when the ureteral mucosa is affected (28).

At MR imaging, ureteral endometriosis usually appears as irregular hypointense nodules on T2weighted images (Fig 7). Extrinsic disease may be suspected when the interface of fat between the nodule and ureter is no longer visible. However, MR imaging appears to lead to overestimation of

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Figure 8.  Bladder endometriosis with ureteral involvement in a 33-year-old woman who presented with cyclic dysuria and pelvic pain, but no signs of hematuria or weight loss. (a) Axial T2-weighted MR image reveals hypointense irregular focal thickening located in the left posterolateral aspect of the bladder wall (arrows) and extending into the perivesical fat (arrowheads). (b) Sagittal T2weighted MR image shows the perivesical and bladder wall thickening (arrow), as well as upstream ureteral dilatation (arrowheads). (c) Oblique coronal T2-weighted MR image shows an infiltrating lesion (*) encasing the lower third of the ureter (arrows). (d) Three-dimensional contrast-enhanced coronal reformatted fat-suppressed T1-weighted MR image shows a dilated left ureter (solid arrows) and a deep infiltrating endometriotic lesion involving the wall of the bladder (B) and the lower third of the ureter (arrowheads). There is also a hyperintense component in the bladder submucosa (open arrow), a finding that indicates bloody content. C = cervix, U = uterus.

this finding (34). Retractile adhesions, which are visible as periureteral hypointense lines arranged in confluent angles, may be present. Ureteral dilatation cranial to the obstruction site is also a common finding that should always be a cause for concern. This finding ought to be reported promptly to the referring physician, since serious impairment of renal function may develop if the finding goes unreported (34).

It is important to identify ureteral wall involvement whenever it occurs (Fig 8), since resection of the affected segment is required in such cases and usually necessitates the presence of a urologist due to the thinness of the ureteral wall and the technically challenging nature of the manipulation. In addition, the treatment of ureteral endometriosis may often require ureteral diversion or reimplantation techniques, which are more advanced than those required in standard gynecologic practice. Conversely, when only the bladder is involved, surgical treatment usually requires resection and primary repair of the affected segment, which is a more feasible task and does not usually necessitate the presence of a urologist.

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Figure 9.  Bladder endometriosis with urethral involvement in a 31-year-old woman. (a, b) Sagittal T2-weighted (a) and fat-suppressed T1-weighted (b) MR images obtained during the patient’s menstrual period show massive irregular thickening of the anteroinferior bladder wall (arrow in a) that extends to the vesical trigone and the upper urethra and is associated with tiny interspersed bloody foci (arrowhead in b), findings that are consistent with a diagnosis of bladder endometriosis. Note the smooth outer contour of the bladder wall, as well as the normal-appearing prevesical fat (arrowheads in a). Such massive focal wall thickening with no signs of extravesical extension or perivesical fat stranding makes a diagnosis of bladder cancer less likely. (c) Axial T2-weighted MR image shows irregular hypointense thickening on the anterior contour of the urethra (*), a finding that indicates endometriotic involvement by direct extension from the bladder lesion.

Isolated urethral endometriosis is not well described in the literature. Urethral involvement is more frequently observed as contiguous extension from the bladder; thus, the imaging findings are the same as those described for bladder endometriosis (Fig 9). Nevertheless, there has been at least one case report in which endometriosis appeared as a urethral diverticulum (35).

Middle Compartment Endometriosis of the middle compartment includes involvement of the uterus, ovaries, fallopian tubes, and uterine ligaments. When the uterus is involved, implants may be seen on the serosal surface, along with diffuse peritoneal enhancement on contrast-enhanced fat-saturated MR images. Although adenomyosis is histologically characterized by the presence of ectopic endometrial tissue within the myometrium (25), it is considered to be an entirely different medical condition due to its distinctive characteristics and clinical implications and therefore is not discussed in this article. Endometrial involvement of the ovaries, which are the most common site for such involvement, may manifest as either (a) small and shallow endometrial implants, which lead to

adjacent paraovarian scarring and adhesions; or (b) ovarian enlargement, which is attributable to repeated episodes of hemorrhage, resulting in endometriotic cysts (endometriomas) (25,36). However, these manifestations are considered to be lesions associated with endometriosis and are not included in the spectrum of deep pelvic endometriotic diseases. Uterine ligaments, such as the broad ligaments and round ligaments of the uterus, may also be affected by endometriosis. Such cases usually manifest as thickening and nodularity of these struc-

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Figure 10.  Endometriotic involvement of the uterine ligaments in a 31-year-old woman with chronic pelvic pain and a known history of endometriosis. Axial gadolinium-enhanced fat-suppressed late-phase T1-weighted MR image shows homogeneous late enhancement of thickened round uterine ligaments (arrows) due to involvement of their uterine insertions by an endometriotic lesion. Figure 11.  Endometriotic involvement of the posterior pelvic compartment in a 29-year-old woman with hypermenorrhea, dyspareunia, and dysmenorrhea. Earlier MR imaging showed retrocervical endometriosis with fibrotic obliteration of the rectovaginal pouch. Sagittal (a) and axial (b) T2-weighted MR images show an irregular hypointense mass (arrowhead) that extends from the posterior cervix inferiorly to the vaginal fornix. Note the presence of a subserous leiomyoma in the anterior uterine wall (black arrow in a), focal adenomyosis in the corporal anterior uterine wall (white arrow), and a right follicular ovarian cyst (* in b).

tures, findings that may be palpable at physical examination. Contrast enhancement may occur due to inflammatory reaction (Fig 10) (25,36). Involvement of the fallopian tubes usually occurs in the subserosal layer (25) and is strongly associated with infertility. Evidence of parametrial involvement can be difficult to discern at MR imaging due to the surrounding vascular structures. However, any asymmetry in signal intensity should raise suspicion for the disease (25,36).

Posterior Compartment Deep retroperitoneal endometriotic lesions of the posterior compartment include involvement of

the rectovaginal pouch, retrocervical area–torus uterinus, uterosacral ligaments, posterior vaginal fornix, rectovaginal septum, and rectum. Deep solid lesions involving the rectovaginal pouch (pouch of Douglas) usually appear as ill-defined hypointense tissue thickening on T2-weighted images. However, some foci of endometriosis at this site may also manifest with an abundant glandular component and discrete fibrotic reaction. In such cases, the endometriotic foci have high signal intensity on T1-weighted images (reflecting blood content) and variable signal intensity on T2-weighted images, and the solid glandular component shows variable enhancement after the intravenous administration of contrast material. Obliteration of the pouch of Douglas occurs when retrocervical lesions extend to the anterior rectal wall (Fig 11) (16,37).

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Figure 12.  Endometriotic involvement of the retrocervical area in a 33-year-old woman with dyspareunia. At earlier MR imaging examinations, an endometrial implant was seen in this area. (a) Sagittal T2-weighted MR image shows an irregular, solid, nodular hypointense mass (arrow) slightly inferior to the uterine torus, with intermingled hyperintense foci (arrowhead). (b) On an axial fat-suppressed T1-weighted MR image, the intermingled foci (arrow) remain hyperintense, a finding that indicates bloody content.

Most retroperitoneal endometriotic lesions are found in the retrocervical area (Fig 12), above the attachment of the vaginal cuff to the posterior cervix. Retrocervical involvement is most commonly associated with uterosacral ligament involvement and may extend inferiorly to the vaginal cuff or posteriorly to the rectal wall (16). When the lesion is located at the torus uterinus, uterine retroversion or angular rectal attraction are often associated findings, reflecting the fibrotic component (15). These retroperitoneal lesions may involve the rectovaginal septum alone, without any link or attachment to the cervix, between the posterior wall of the vaginal mucosa and the anterior rectal wall under the peritoneal fold of the pouch of Douglas. Such lesions are usually small and account for 10% of retroperitoneal endometriotic lesions (5). MR imaging findings of involvement of the uterosacral ligaments are usually discrete (Fig 13). Morphologic abnormalities, such as bilateral or asymmetric hypointense thickening and nodules within these ligaments, should be viewed as helpful diagnostic information (5,37). The proximal medial portion of the uterosacral ligaments is most commonly affected by endometriosis. Because of the proximity of the anterior and lateral walls of the rectum and lateral vaginal fornices to the uterosacral ligaments, endometriosis at this site may extend directly to the rectum or vaginal fornices. The rectosigmoid is the segment of bowel that is most commonly involved by endometriosis. The implants are usually serosal but can eventually erode through the subserosal layers and cause

marked thickening and fibrosis of the muscularis propria. An intact overlying mucosa is almost always present, since the implanted tissue only rarely invades through to the mucosa (2,38). Adhesions, bowel strictures, and gastrointestinal obstruction may result from the inflammatory response to cyclic hemorrhage. Deep rectal involvement is more difficult to depict with MR imaging, which has a sensitivity of only 33% (5); this is particularly true for conventional imaging, since black plaque can be mistaken for the black gas contents of the rectum. The presence of hypointense parietal thickening on T2-weighted MR images, with or without intermingled hemorrhagic foci (which are associated with specific symptoms), may be helpful in making the diagnosis.

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Figure 13.  Endometriotic involvement of the uterosacral ligaments in a 31-year-old woman who presented with pelvic pain, dyspareunia, and painful defecation. Earlier MR imaging showed involvement of these structures. (a, b) Coronal (a) and axial (b) T2-weighted images show hypointense irregular spiculated nodular thickening of the right uterosacral ligament (white arrow in a), with minimal intermingled hyperintense foci. These findings create an arciform abnormality (arrowheads in b) that extends to the anterior rectal wall, where there is focal parietal thickening (black arrow). (c) Axial fat-suppressed T1-weighted MR image shows hyperintense foci (solid arrows), a finding that indicates bloody content. Open arrow indicates focal parietal thickening. (d) Laparoscopic image obtained in a different patient shows involvement of the uterosacral ligaments (arrows).

Other Sites Deep endometriosis can also demonstrate isolated involvement of the vagina (Fig 14), intestinal loops (Fig 15), or other extraperitoneal sites, such as the ischioanal (ischiorectal) fossa (Fig 16) and sciatic nerve (Fig 17). Cyclic sciatica due to implantation of endometrial tissue in the sciatic nerve in the region of the sciatic notch is a very

unusual type of sciatica. It manifests as cyclic episodes of pain in the distribution of the sciatic nerve that coincide with menstruation. If cyclic sciatica is not treated, a sensorimotor mononeuropathy of the sciatic nerve develops (39).

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Figure 14.  Isolated endometriotic involvement of the vagina in a 38-year-old woman who had undergone hysterectomy and presented with dyspareunia and chronic pelvic pain. Earlier MR imaging showed vaginal involvement. (a) Axial T2-weighted MR image shows a hypointense nodule (arrows) in the posterior upper third of the vagina. (b) Axial T1-weighted MR image shows minimal intermingled hyperintense foci (arrowheads), a finding that indicates bloody content.

Figure 16.  Endometriotic involvement of the ischioanal fossa in a 32-year-old woman who presented with right hip pain. The patient had no history of perineal surgery. (a) Axial T2-weighted MR image shows solid, predominantly glandular endometriosis (arrows) in the ischioanal fossa located close to the right ischiatic tuberosity and involving the internal obturator muscle and anal sphincter. (b, c) Axial T1-weighted (b) and fat-saturated T1-weighted (c) MR images show intermingled hyperintense foci (arrow), a finding that indicates bloody content. Arrowhead in b indicates cortical sclerosis. (d) Coronal T1-weighted MR image shows significant bone reaction (cortical sclerosis) in the medial aspect of the right ischiatic tuberosity (arrowhead).

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Figure 15.  Sigmoid endometriosis in a 30year-old woman who experienced painful defecation and hematochezia during her menstrual period. (a, b) Sagittal (a) and coronal (b) T2weighted MR images obtained after the administration of a saline rectal enema and intravaginal aqueous gel show hypointense nodular thickening of the sigmoid wall (arrows) adhering to the posterior uterine serosa (arrowhead in a). (c) Sagittal gadolinium-enhanced fatsuppressed late-phase T1-weighted MR image shows enhancement of the lesion (arrow). The findings in a–c are consistent with a diagnosis of sigmoid endometriosis.

Figure 17.  Cyclic sciatica in a 27-year-old woman. Earlier MR imaging showed sciatic nerve involvement. (a) Axial MR image shows hypointense irregular spiculated soft-tissue thickening (arrows) in the left sciatic notch. (b) Axial fat-suppressed T1-weighted MR image shows minimal intermingled hyperintense foci (arrows), a finding that indicates bloody content. (c) Axial gadolinium-enhanced fatsuppressed late-phase T1-weighted MR image shows enhancement of the lesion (arrows).

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Figure 18.  Deep endometriosis at various sites in a 35-year-old woman who presented with chronic pelvic pain, infertility, and dysuria. Earlier MR imaging showed endometriotic involvement of the urinary bladder, rectovaginal septum, and retrocervical area. (a, b) Sagittal (a) and axial (b) T2-weighted MR images demonstrate hypointense focal thickening of the right posterolateral wall of the bladder (black arrow) with punctate intermingled bleeding, along with an extraperitoneal, irregular hypointense nodule (white arrows) that mainly involves the retrocervical area and the upper portion of the rectovaginal septum. (c) Axial fat-saturated T1-weighted MR image shows the nodule. Arrowhead = punctate bleeding.

Many times, foci of deep endometriosis are simultaneously observed at different sites (Fig 18), including the retrocervical region, uterosacral ligaments, and rectovaginal and vesicovaginal septa, in addition to other hollow viscera (33,40).

Conclusions

Deep pelvic endometriosis is an important gynecologic disorder that is responsible for severe pelvic pain, for which surgery remains the best therapeutic option. Because successful treatment requires lesion removal with radical surgery, the accurate preoperative assessment of the extension of endometriotic disease is extremely important. Physical examination alone does not provide adequate preoperative information. Furthermore, exploratory laparoscopy is limited in demonstrating deep endometriotic lesions that may be hidden by adhesions or located in the subperitoneal space. Pelvic MR imaging is a noninvasive method with high spatial resolution that allows multiplanar

evaluation and good tissue characterization, but without the use of ionizing radiation or iodinated contrast agents. It has a high diagnostic accuracy for endometriosis and allows the identification of lesions that are hidden by adhesions and the evaluation of endometriotic extension of subperitoneal lesions. MR imaging yields important findings that help grade deep endometriosis and identify subperitoneal lesion extension and other associated disease entities, and provides key information for the diagnosis and adequate treatment of deep pelvic endometriosis. Radiologists should be familiar with the MR imaging findings of deep infiltrating endometriosis in various locations so that they can provide information that allows adequate preoperative counseling.

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This article meets the criteria for 1.0 AMA PRA Category 1 Credit TM. See www.rsna.org/education/rg_cme.html.

Teaching Points

March-April Issue 2011

Imaging of the Postoperative Cranium Audrey G. Sinclair, MBBCh, MRCP, FRCR • Daniel J. Scoffings, MBBS, MRCP, FRCR RadioGraphics 2010; 30:461–482 • Published online 10.1148/rg.302095115 • Content Codes:

Page 550 Deep pelvic endometriosis, also known as deep infiltrating endometriosis involvement, is defined as subperitoneal invasion by endometriotic lesions that exceeds 5 mm in depth. Page 553 The rectovaginal septum is a thin membranous partition that is usually filled with fat. It is located between the posterior vaginal wall and the anterior rectal wall. Page 554 Therefore, the involvement of anatomic structures such as the uterosacral ligaments or the vaginal or rectal wall should be suspected when these structures have a hypointense thickened or nodular appearance on T2-weighted images. Page 556 Therefore, bladder endometriosis should be considered in any patient being evaluated for endometriosis who presents with urinary tract symptoms after having undergone hysterectomy or some other gynecologic surgical procedure. Because vesical endometriosis seldom invades the mucosa, MR imaging may show abnormalities, even in patients with normal cystoscopic results or with no urinary tract symptoms. Page 559 (Figure on page 559) It is important to identify ureteral wall involvement whenever it occurs (Fig 8), since resection of the affected segment is required in such cases and usually necessitates the presence of a urologist due to the thinness of the ureteral wall and the technically challenging nature of the manipulation. In addition, the treatment of ureteral endometriosis may often require ureteral diversion or reimplantation techniques, which are more advanced than those required in standard gynecologic practice. Conversely, when only the bladder is involved, surgical treatment usually requires resection and primary repair of the affected segment, which is a more feasible task and does not usually necessitate the presence of a urologist.

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