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Deep Retroperitoneal Pelvic Endometriosis: MR Imaging Appearance with Laparoscopic Correlation1 TEACHING POINTS See last page

Chiara Del Frate, MD ● Rossano Girometti, MD ● Marco Pittino, MD Giovanni Del Frate, MD ● Massimo Bazzocchi, MD ● Chiara Zuiani, MD Deep pelvic endometriosis is defined as subperitoneal infiltration of endometrial implants in the uterosacral ligaments, rectum, rectovaginal septum, vagina, or bladder. It is responsible for severe pelvic pain. Accurate preoperative assessment of disease extension is required for planning complete surgical excision, but such assessment is difficult with physical examination. Various sonographic approaches (transvaginal, transrectal, endoscopic transrectal) have been used for this purpose but do not allow panoramic evaluation. Furthermore, exploratory laparoscopy has limitations in demonstrating deep endometriotic lesions hidden by adhesions or located in the subperitoneal space. Despite some limitations, magnetic resonance (MR) imaging is able to directly demonstrate deep pelvic endometriosis. The MR imaging features depend on the type of lesions: infiltrating small implants, solid deep lesions mainly located in the posterior cul-de-sac and involving the uterosacral ligaments and torus uterinus, or visceral endometriosis involving the bladder and rectal wall. Solid deep lesions have low to intermediate signal intensity with punctate regions of high signal intensity on T1-weighted images, show uniform low signal intensity on T2weighted images, and can demonstrate enhancement on contrastenhanced images. MR imaging is a useful adjunct to physical examination and transvaginal or transrectal sonography in evaluation of patients with deep infiltrating endometriosis. ©

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RadioGraphics 2006; 26:1705–1718 ● Published online 10.1148/rg.266065048 ● Content Codes: 1From

the Department of Radiology, University of Udine, Via Colugna 50, 33100 Udine, Italy (C.D.F., R.G., M.B., C.Z.); and the Department of Gynaecology and Obstetrics, Hospital of San Daniele del Friuli, Udine, Italy (M.P., G.D.F.). Presented as an education exhibit at the 2005 RSNA Annual Meeting. Received March 30, 2006; revision requested May 1; final revision received August 14; accepted August 23. All authors have no financial relationships to disclose. Address correspondence to C.D.F. (e-mail: [email protected]).

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Introduction The definition of deep endometriosis includes rectovaginal lesions as well as infiltrative forms that involve vital structures such as the bowel, ureters, and bladder. According to the definition of this entity by Koninckx et al (1), deeply infiltrating endometriosis is defined as an endometriotic lesion penetrating into the retroperitoneal space or the wall of the pelvic organs to a depth of at least 5 mm. Peritoneal, ovarian, and deep endometriosis may be diverse manifestations of a disease with a single origin (2). Drugs induce temporary quiescence of active deep lesions and may be useful in selected cases. However, in most cases of severely infiltrating disease, surgery is the final solution (2). The preoperative work-up is crucial in order to establish the precise distribution of the deeply infiltrating endometriotic lesions, which is the only means of ensuring complete surgical removal. The success of treatment depends on radical surgical removal. The location and extent of the lesions govern the modalities for the operation, and these are difficult to establish based only on physical examination results. Various sonographic approaches (transvaginal, transrectal, endoscopic transrectal) do not ensure panoramic evaluation of this entity. Furthermore, exploratory laparoscopy presents limitations in detecting deep locations of endometriosis hidden by adhesions or located in the subperitoneal space. Despite some limitations, magnetic resonance (MR) imaging is able to directly depict deep endometriosis. In this article, we provide an overview of the pathologic features, classic locations, clinical features, and classification of deep pelvic endometriosis. Furthermore, we analyze the capability and potential of MR imaging in diagnosis and staging of deep pelvic endometriosis with laparoscopic correlation. Finally, we discuss the treatment of this entity.

Definition Endometriosis is classically defined as the presence of endometrial glands and stroma outside the uterine cavity and musculature. It is unclear whether both glands and stroma are required for the pathologic definition of the disease (3). The ectopic endometrium responds to hormonal

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stimulation with various degrees of cyclic hemorrhage, which result in suggestive symptoms and appearances. The definition of deep endometriosis is based on anatomic assumptions that may prove erroneous. In fact, the term “deep endometriosis” should be reserved for lesions in the retroperitoneal tissue. For practical purposes, several reports include in the so-called deep endometriosis the infiltrative forms that involve vital structures such as the bowel, ureters, and bladder, as well as forms such as many rectovaginal lesions. For the term “deep” to apply, there should be ectopic endometrial tissue penetrating the peritoneum more than 5 mm in depth (2,4).

Pathologic Features Peritoneal implants of endometriosis are classically described as bluish gray “powder burns” at visual inspection. The color is attributed to menstrual blood that becomes encapsulated by fibrotic tissue and then hemolyzed (5). Ectopic endometrium may also appear as nonpigmented clear vesicles, white plaques, and reddish petechiae or flamelike areas. These implants range from several millimeters to 2 cm in diameter and may be superficial or invasive. At microscopic examination, all lesions of both typical and deep endometriosis contain endometrial glands and stroma and may be accompanied by adjacent fibrosis and hemorrhage. On the contrary, the histologic findings of infiltrative lesions of deep pelvic endometriosis are mainly characterized by fibromuscular hyperplasia that surrounds foci of endometriosis, and the foci sometimes contain small cavities. The endometrial glands and stroma infiltrate the adjacent fibromuscular tissue and elicit smooth muscle proliferation and fibrous reaction, resulting in solid nodule formation (1,2). In visceral solid endometriosis, the 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.

Locations The most common locations of endometriosis are the ovaries and the pelvic peritoneum, followed in order of decreasing frequency by deep lesions of the pelvic subperitoneal space, the intestinal system, and the urinary system. Results of pelvic mapping with laparoscopy or laparotomy indicate

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Figure 1. Axial (a) and sagittal (b) T2-weighted fast spin-echo images (repetition time msec/echo time msec ⫽ 5000/118) show the most frequent sites of involvement with peritoneal endometrial implants (多), such as the surface of the ovaries, uterus, bowel, and pouch of Douglas. The red dashed lines indicate the typical locations of deep implants, which occur along uterovesical and rectovaginal septa across peritoneal reflections in the pelvis.

that the cul-de-sac and uterosacral ligaments are the most common pelvic sites of involvement by endometriosis (4,6). Results of another study indicate that the frequency of endometriosis in the posterior cul-de-sac is up to 56% (7) (Fig 1). Deep nodular (solid) endometriosis is typically found in the rectovaginal septum and in other fibromuscular pelvic structures such as the uterine ligaments (69.2%), the vagina (14.5%), and the muscular wall of pelvic organs. In detail, solid endometriosis can involve the alimentary tract (9.9%). Bladder involvement has been described, and similarly the ureter may be involved (6.4%). The rectosigmoid is the most common segment of bowel involved (5,7).

Clinical Features Endometriosis is associated with a wide variety of symptoms, although in many patients it is asymptomatic. Furthermore, the stage of the disease does not necessarily correlate with the seriousness of the symptoms (8). A common symptom is infertility. The prevalence of endometriosis among infertile women undergoing laparoscopy in one study was 14%, but the prevalence of infertility among women with endometriosis cannot be assessed because of the selection bias inherent in laparoscopic diagnosis.

Pelvic pain is a frequent complaint among patients with endometriosis. Such pain generally manifests as secondary dysmenorrhea, worsening primary dysmenorrhea, dyspareunia, or even noncyclic lower abdominal pain and backaches. The pain may be site specific when endometriosis is found in unusual locations outside the pelvis. Although peritoneal endometriosis can be asymptomatic, deep pelvic endometriosis is a cause of pelvic pain, dysmenorrhea, dyspareunia, dyschezia, and urinary symptoms and is associated with infertility. Urinary tract disease may manifest as hydronephrosis caused by ureteral obstruction or as a submucosal lesion within the bladder or ureter. Dyschezia may manifest as rectal involvement by the disease; dyspareunia is often due to endometrial lesions in the cul-de-sac and vagina, while localized tenderness along the uterosacral ligaments and cul-de-sac is often related to endometrial lesions in these sites. Localized tenderness of the cul-de-sac and uterosacral ligaments is frequently found in women with minimal or mild endometriosis. Thickened, nodular uterosacral ligaments or rectovaginal masses may be palpable. Retroverted

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Figure 2. Classification of endometrial implants of the rectovaginal septum. Red spot ⫽ deep implant, yellow line ⫽ visceral peritoneum. Left: Rectovaginal septum lesions, seen in 10% of cases, are located in the rectovaginal septum between the posterior wall of the vagina (V) and the anterior wall of the rectal muscularis. Metaplasia of mu¨llerian remnants has been hypothesized to explain their origin. F ⫽ posterior vaginal fornix, R ⫽ rectum, U ⫽ uterus. Center: The most frequent type of lesion (65% of cases) occurs in the posterior wall of the vaginal fornix. Such implants develop from the posterior fornix toward the rectovaginal septum, without extension to the septum itself or the rectal wall. Right: Hourglass-shaped lesions are found in 25% of cases and are due to posterior extension of a posterior forniceal lesion toward the anterior rectal muscularis.

fixation of the uterus may be noted with obliteration of the posterior cul-de-sac (9).

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It is essential to take the location of the deeply infiltrating endometriotic lesions into account because where pelvic pain is concerned, the success of the surgical operation depends on how radical the surgical removal is (10). With implants in this location, the deep endometriotic lesions are separated according to anatomic distribution, based on their location in the anterior cul-de-sac, posterior cul-de-sac, or pelvic sidewall (2). Anterior cul-de-sac lesions include endometriosis of the bladder detrusor. At surgery, the uterus is anteflexed and the anterior cul-de-sac is obliterated due to extensive adhesions between the peritoneum of the bladder fold and the uterine wall and fundus. The detrusor nodule is almost always palpated medially in the posterior wall or dome of the bladder, adherent to the anterior uterine wall, well above the isthmus, trigone, and vesicovaginal septum (2). Endometriosis of the vesicovaginal septum is anatomically more caudal (2).

Posterior cul-de-sac lesions include retroperitoneal lesions and dependent intraperitoneal locations that may result in infiltrating lesions. The inflammation triggered by bleeding intraperitoneal endometriotic papules in the most dependent portion of the pouch of Douglas may result in adhesions between the adjacent peritoneal surfaces of the anterior rectal wall and posterior vaginal fornix, with subsequent infiltration of the muscular layers of both organs. This means that what is called rectovaginal septum endometriosis may instead be massive disease of the deepest portion of the pouch of Douglas, which has been buried and excluded from the remaining pelvis by adhesions (2). It has been suggested that retroperitoneal deep endometriotic lesions originate from metaplasia of mu¨llerian remnants located in the rectovaginal septum. Furthermore, these retroperitoneal lesions are subclassified into groups by analyzing their locations, as precisely defined with transrectal ultrasonography and MR imaging: rectovaginal septum lesions (type I), posterior wall forniceal lesions (type II), and hourglassshaped lesions (type III) (Fig 2) (11). Rectovaginal septum lesions account for 10% of cases and are usually found to be small. They are situated within the rectovaginal septum be-

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tween the posterior wall of the vaginal mucosa and the anterior wall of the rectal muscularis. The lesion is not linked or attached to the cervix and is situated under the peritoneal fold of the cul-desac of Douglas (11). Posterior wall forniceal lesions account for 65% of cases and develop from the posterior fornix toward the rectovaginal septum. The posterior fornix is retrocervical and corresponds to the vaginal wall and to the posterior wall of the posterior lip of the cervix. These lesions are often small, and there is no extension to the rectovaginal septum or rectal wall (11). Finally, hourglass-shaped lesions, found in 25% of cases, occur when posterior forniceal lesions extend cranially to the anterior rectal wall. These are usually larger lesions, more than 3 cm, with a greater risk of extension to the rectal wall. These lesions always occur under the peritoneal fold of the rectouterine pouch of Douglas. Infiltration of the rectal muscularis is systematically observed in this subtype (11). Pelvic sidewall deep endometriotic lesions include the ureteral locations. The prevalence of ureteral endometriosis ranges from 0.01% to 1% of all women with the disease (12). Endometriosis of the ureter usually arises by extension from pelvic foci and ovarian endometriosis. Endometriosis of the ureter may not necessarily be secondary to endometriotic cysts, but more generally may be due to ectopic implantation of endometrial cells along the lateral gonadal surface and ovarian fossa (11,13).

Diagnosis Diagnosis and evaluation of extension of deep peritoneal endometriosis is difficult with physical examination and explorative laparoscopy and requires palpation and opening of the subperitoneal space in order to confirm and to evaluate the extent of the lesions (14,15). Physical examination and laparoscopic exploration may not allow diagnosis or prediction of the extension of deep pelvic endometriosis, especially in pelvic subperitoneal sites (16). Transvaginal sonography is recommended for diagnosis of endometriomas (17,18) and endometriosis of the bladder (19), but its value for assessment of superficial peritoneal lesions, ovarian foci, and deep pelvic endometriosis is uncertain. Rectal endoscopic sonography with high-frequency probes has been recommended for detection of endometriosis in rectal, rectovaginal, uterosacral, or rectosigmoid locations (20,21), even though high-frequency sonography shows

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poor penetration. The main advantage with rectal endoscopic sonography is that it provides a reliable means of investigation to diagnose any infiltration of the bowel wall (22–24). Preliminary results show that rectal endoscopic sonography appears to perform better than MR imaging for diagnosis of bowel wall infiltration. MR imaging is now commonly used for diagnosis of endometriomas (25,26) and provides a tremendous advantage over other methods of investigation, owing to the possibility of making a complete survey of the anterior and posterior compartments of the pelvis at one time (27). However, its value for diagnosis of endometriosis in the bladder, in superficial peritoneal lesions, and in ovarian foci is controversial (23,25–27); some authors underline the limitations of MR imaging in depicting small endometrial lesions in these sites, even though a recent study demonstrated good sensitivity for detection of small peritoneal implants (28,29). Furthermore, Bazot et al (30) recently demonstrated the high accuracy of pelvic MR imaging in evaluation of deep pelvic endometriosis.

MR Imaging Protocol In our experience, MR imaging studies were performed with a 1.5-T superconducting magnet (Magnetom Avanto; Siemens, Erlangen, Germany) and a surface phased-array coil. Patient preparation required a moderately filled bladder in order to correct the angle of uterine anteversion, leading to better evaluation of the pelvic structures. Furthermore, a half-filled bladder displaces the bowel superiorly, contributing to reduce artifacts from bowel motion, in association with injection of intramuscular hypotonic drugs such as glucagons (1 mg). Excessive bladder distention sometimes represents a source of additional artifacts due to detrusor contractions. On the basis of the characteristics of our system, the standard imaging protocol included a T2-weighted fast spin-echo sequence (5000/118, flip angle ⫽ 150°, matrix ⫽ 230 ⫻ 256, field of view ⫽ 230 ⫻ 230 mm, 20 sections, section thickness ⫽ 4 mm, intersection gap ⫽ 20%, one signal acquired) and a T1-weighted fast spin-echo sequence (865/11, flip angle ⫽ 150°, matrix ⫽ 224 ⫻ 320, field of view ⫽ 230 ⫻ 230 mm, 20 sections, section thickness ⫽ 4 mm, intersection gap ⫽ 20%, one signal acquired), both performed

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Figure 3. Hemorrhagic endometrial implants of the rectovaginal septum in a 26-year-old woman with dyspareunia and dysmenorrhea who presented with a palpable nodule in the posterior vaginal fornix. (a) Axial T1-weighted fast spin-echo fat-suppressed image (852/12) shows multiple round, hyperintense hemorrhagic foci (arrow) in the retrocervical space and pouch of Douglas. (b) Sagittal T1-weighted fast spinecho fat-suppressed image (852/12) shows an endometrial implant in the posterior fornix (arrow), a finding consistent with the palpable nodule. (c) Photograph obtained during laparoscopy (same orientation as in a) shows adhesions (*) and multiple red endometrial implants (arrow) on the surface of the uterus and rectum and in the pouch of Douglas. (d) Photograph obtained after initial lysis of the adhesions (near the tip of the laparoscope) shows that the forniceal implant remains hidden.

in the axial plane. These sequences were performed to ensure complete anatomic evaluation of pelvic organs and detection and preliminary characterization of endometriotic lesions, which appear hyperintense on T1-weighted images and mildly hypointense or hyperintense on T2-weighted images. On the available 1.5-T systems, relaxation times for T2-weighted images vary from 3200 to 5000 msec, with an optimal echo time around 90 msec for a repetition time of 4000 msec to produce optimal contrast of the junctional zone for diagnosing associated adenomyosis.

Because spectrally selective fat saturation allows differentiation between hemorrhagic or fatty content of cystic lesions (endometriomas or dermoid cysts, respectively), increased detection of small implants, and better definition of their conspicuity, a T1-weighted fast spin-echo fat saturation sequence was performed in the axial plane (852/12, flip angle ⫽ 90°, matrix ⫽ 192 ⫻ 256, field of view ⫽ 230 ⫻ 230 mm, 20 sections, section thickness ⫽ 4 mm, intersection gap ⫽ 20%, one signal acquired). A T1-weighted fast spinecho sequence in the sagittal plane (865/11, flip angle ⫽ 150°, matrix ⫽ 256 ⫻ 192, field of view ⫽ 230 ⫻ 230 mm, 20 sections, section thick-

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Figure 4. Endometrial implant of the uterovesical septum in a 36-year-old woman with dysmenorrhea and dysuria. (a) Sagittal T1-weighted fast spin-echo fat-saturated image (852/12) shows a hyperintense hemorrhagic nodule (arrow) in the uterovesical septum. (b) Photograph obtained during laparoscopy (cranial view) shows the region of the uterovesical cul-de-sac after raising of the uterus. The endometriotic nodule (arrow) is attached to the posterior surface of the bladder.

ness ⫽ 4 mm, intersection gap ⫽ 20%, one signal acquired) was added to evaluate the rectovaginal septum. A T1-weighted fast spin-echo fat-suppressed sequence can be performed after injection of contrast material (paramagnetic gadolinium chelates). Use of contrast-enhanced imaging is primarily required to identify solid enhancing nodules within endometriotic cysts when malignant transformation is suspected (31). Contrast medium is also useful to define the extent of active inflammatory processes associated with endometriosis. Enhancement of the peritoneal surface can be demonstrated as localized, subjacent to peritoneal implants, or diffuse, in the case of an inflammatory reaction incited by deep implants in peritoneal reflections over the uterosacral ligaments and within the pouch of Douglas. Parametrial involvement should be suspected in the case of asymmetric signal intensity on contrast-enhanced fat-saturated images. Nevertheless, after intravenous administration of gadopentetate dimeglumine, enhancing inflammatory adhesions or parametrium could be misinterpreted as a focus of endometriosis (32). Some authors avoid contrast-enhanced imaging due to lack of a definite consensus concerning its indications. An accurate preoperative distribution of extension of endometriosis, including deep implants and adhesions, has been demonstrated even without use of gadopentetate dimeglumine (28,29).

MR Imaging Features MR imaging characteristics of deep pelvic endometriosis depend on the type of lesions: infiltrating small implants, solid deep lesions mainly located in the posterior cul-de-sac involving the uterosacral ligaments and torus uterinus, and visceral endometriosis involving the bladder and rectal wall. When the lesion is an implant with deep infiltration, MR imaging may demonstrate only a punctate focus of high signal intensity, which represents a small area of hemorrhage. This correlates with burn implants at laparoscopy (Figs 3, 4). Whenever the implants are white or red, the MR imaging results may be completely negative. Solid deep lesions demonstrate low to intermediate signal intensity with punctate regions of high signal intensity on T1-weighted images, uniform low signal intensity on T2-weighted images, and enhancement, corresponding to the abundant fibrous tissue seen in these lesions at histologic examination (5). The punctate foci of high signal intensity represent regions of hemorrhage surrounded by solid fibrotic tissue (Fig 5). These solid masses of endometriosis may simulate metastatic peritoneal implants from intraperitoneal malignancies such as ovarian carcinoma. These disease processes can be differentiated by the low

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Figure 5. Fibrotic obliteration of the pouch of Douglas in a 27-year-old patient with dyspareunia and pain in the posterior vaginal fornix at clinical examination. (a, b) Axial T1-weighted (865/11) (a) and T2-weighted (5000/118) (b) fast spin-echo images show a low-signal-intensity area of tissue retraction (arrow), which extends from the posterior upper cervix to the pouch of Douglas. (c) Sagittal fat-saturated T1-weighted fast spin-echo image (852/12) shows hyperintense foci (arrow) in the same region as the area of tissue retraction in a and b, a finding consistent with hemorrhagic content. (d) Photograph obtained during laparoscopy (same orientation as in a and b) shows only the superficial part of the endometriotic nodule, which appears as an area of tissue distortion with red hemorrhagic spots (arrow). (e) Photograph from the same examination shows a detail of the deep lesion (near the tip of the laparoscope), which was excised laparoscopically by using a finger placed through the vagina for guidance.

signal intensity on T2-weighted images of solid endometriosis, often in combination with the presence of endometrial cysts (4). Some masses of endometriosis, located in the uterosacral ligament, posterior vaginal fornix, or pouch of Douglas, may be composed of a large proportion of glandular material with little fibrotic reaction, resulting in high signal intensity on T2-weighted images. This solid glandular material will enhance with contrast material administration, thus distinguishing it from necrosis or intratumoral hemorrhage (5). Often, signal intensity is not able to help in depicting deep endometriosis of the uterosacral ligaments, particularly when there is lack of punc-

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Figure 6. Small endometrioma and endometrial implant of the uterosacral ligament in a 28-year-old woman with pelvic pain and infertility. (a) Axial fat-suppressed T1-weighted fast spin-echo image (852/12) shows a small endometrioma in the left ovary. (The endometrioma was histologically proved.) (b, c) Axial fat-suppressed T1-weighted fast spin-echo images (852/12), obtained at contiguous levels, show linear, hyperintense, hemorrhagic endometrial implants (arrow in b) on the surface of the uterus, with a more definite nodular spot in the anterior extremity. (d) Photograph obtained during laparoscopy shows the region of the implants seen in b and c. The hemorrhagic spot in c correlates with a red implant on the left uterosacral ligament (arrow), which is stretched by uterine laterodeviation. Left oophorectomy was performed (*).

tate foci of hemorrhage. In these cases, diagnosis is related to the presence of thickening of the ligaments, bilateral or asymmetric, larger than 9 mm, or nodularity inside the ligament (Fig 6) (4,30). Bladder endometriosis can be demonstrated at MR imaging as morphologic abnormalities, including localized or diffuse bladder wall thickening and signal intensity abnormalities. The majority of patients have spots of high sig-

nal intensity in an abnormal thickening of the bladder wall (Fig 7) (4). MR images of the bladder may be abnormal even in patients with normal cystoscopic results or without urinary symptoms. In fact, as endometriosis seldom

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Figure 7. Deep endometriosis of the bladder wall in a 30-year-old patient with dysuria and infertility. (a) Axial T2weighted fast spin-echo image (5000/118) shows a solid, nodular hypointense mass in the posterior bladder wall. (b) Sagittal T1-weighted fast spin-echo image (865/11) shows multiple hemorrhagic foci in the lesion (arrow) and better demonstrates its craniocaudal extension along the bladder wall. (c) Photograph obtained during laparoscopy shows the vesicouterine cul-de-sac, with the bladder distended before the uterus by a Foley catheter. Linear tight adhesions (arrows) are evident between the bladder and uterus. (d) Photograph from the same examination shows the region depicted in c after lysis of the adhesions (white rectangles). (e) Close-up photograph of the region of the dashed white rectangle in d shows multiple small, black endometrial implants on the surface of the bladder in the zone of the lysed adhesion. (f ) Close-up photograph of the region of the solid white rectangle in d shows the deep endometriotic nodule as tumescence of the bladder surface (arrow) under the lysed adhesion. On the basis of the MR imaging and laparoscopic findings, an open laparotomy was performed to excise the extended bladder lesion, which was confirmed to be a deep endometriotic lesion at pathologic analysis.

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Figure 8. Rectal hemorrhagic endometrial implants and right-sided dermoid cyst in a 26-year-old woman with infertility and severe pelvic pain. The patient also had a left-sided endometriotic cyst (not shown). (a) Axial T1weighted fast spin-echo image (865/11) shows a small hyperintense lesion (arrow) of the rectal wall, which represents an endometrial implant. A high-signal-intensity mass is seen in the right ovary. (b) Axial fat-suppressed T1-weighted fast spin-echo image (852/12) shows the rectal endometrial implant more clearly and also shows other small hyperintense foci in the same region (arrow). The signal intensity of the adnexal mass is markedly decreased, an appearance consistent with a dermoid cyst. (c) Photograph obtained during laparoscopy shows the pouch of Douglas, with the tip of the instrument moving apart the rectum. Multiple red endometrial implants are present, including one on the rectal wall (arrow). (d) Photograph from the same examination shows the dermoid cyst between the tips of the laparoscope, with a red endometrial implant on its surface.

invades the mucosa, lesion identification remains difficult with cystoscopy (4). Deep rectal involvement is more difficult to depict with MR imaging, which has a sensitivity of 33%, particularly with conventional imaging, due to artifacts related to the rectal content. Better results are obtained with addition of phasedarray coils, endovaginal coils, and rectal contrast enema (4). Thickening of the rectal wall in association with specific symptoms, with low signal intensity on T2-weighted images and sometimes

the presence of punctate hyperintense foci of hemorrhage, may be helpful for diagnosis (Fig 8). Solid endometriosis can also develop in cesarean section scars involving the Pfannenstiel incision after cesarean section (5). MR imaging findings are characterized by hemorrhagic signal intensity on T1- and T2-weighted images, especially with fat-saturated sequences, in the context of the myometrium along the surgical scar.

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Figure 9. Deep fibrotic endometriosis of the pouch of Douglas in a 33-year-old woman with dyspareunia and a palpable nodule in the rectovaginal septum. (a) Axial T2-weighted fast spin-echo image (5000/118) shows a nodular region of hypointense tissue (arrow) between the anterior rectal wall and cervix, with some degree of surrounding softtissue distortion. (b) Axial fat-suppressed T1-weighted fast spin-echo image (852/12) shows that the nodule (arrow) is isointense relative to surrounding tissues with no hemorrhagic content, an appearance indicative of its fibrotic nature. (c) Photograph obtained during laparoscopy (same orientation as in a and b) shows the pouch of Douglas during the procedure of nodule excision, which was performed by using a finger placed through the vagina for guidance. The tip of the instrument (near the top of the image) is moving apart the posterior vaginal fornix. The fibrotic endometriotic lesion without hemorrhagic content (arrow) is seen in the rectovaginal septum.

Surgical Management It is essential to take the anatomic distribution of deeply infiltrating endometriotic lesions into consideration for surgical management of patients with this problem. The importance of this point has prompted the gynecologists to propose a “surgical classification” for deeply infiltrating endometriosis, based on the location of the lesions (7). The advantage of this classification is that for each location corresponds a well-established surgical technique that has proved to be efficient (7). When multifocal lesions are present, it is important to associate several surgical procedures. For location of deep pelvic endometriosis in the anterior cul-de-sac, involving the bladder, the treatment of reference is partial cystectomy. This can perfectly well be achieved with laparoscopic surgery (33,34). However, in certain cases the operation should be performed with laparotomy, particularly when there is a need to reimplant the ureter or if an association with bowel involvement is present. In cases of deep pelvic endometriosis located in the posterior cul-de-sac, various techniques have

been proposed (Fig 9). For deeply infiltrating endometriosis of the uterosacral ligaments, surgical removal can take place with laparoscopic surgery (35). If the vagina is involved, the surgical technique is different and classically uses both the laparoscopic and the vaginal approaches. When the bowel wall is infiltrated (Fig 10), although in certain carefully selected cases surgery can be carried out with laparoscopy (36,37), the treatment of reference remains laparotomy (38,39). This is particularly true when resection and anastomosis are needed and because bowel lesions are multifocal in a considerable proportion of cases (7).

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Figure 10. Bowel adhesions due to endometriosis in a 37-year-old patient with dysmenorrhea and infertility. (a) Axial T2-weighted fast spin-echo image (5000/118) shows tight contact between a large hypointense mass of the left ovary and a bowel loop (arrow). (b) Axial contrast-enhanced fat-suppressed T1-weighted fast spin-echo image (852/12) shows that the mass has high signal intensity, a finding indicative of hemorrhagic contents. There is absence of the fat plane between the endometrioma and the bowel loop (arrow), which demonstrates increased angulation. (c) Photograph obtained during laparoscopy shows the tight adhesions between the endometriotic cyst and the bowel loop, which was shown to be the sigmoid colon.

our opinion, MR imaging may be recommended in preoperative assessment of patients with deep pelvic endometriosis.

References

Conclusions MR imaging is a useful modality as an adjunct to physical examination and transvaginal and transrectal sonography in evaluation of patients with deep infiltrating endometriosis. MR imaging demonstrates high sensitivity, specificity, positive and negative predictive values, and accuracy in prediction of the locations and in evaluation of the extension of lesions in patients with this disease, as reported in the several articles published on this topic. All the information offered by MR imaging is useful in planning the best treatment, surgical or medical, for the disease. Therefore, in

1. Koninckx PR, Meuleman C, Demeyere S, Lesaffre E, Cornillie FJ. Suggestive evidence that pelvic endometriosis is a progressive disease, whereas deeply infiltrating endometriosis is associated with pelvic pain. Fertil Steril 1991;55:759 –765. 2. Vercellini P, Frontino G, Pietropaolo G, Gattei U, Daguati R, Crosignani PG. Deep endometriosis: definition and clinical management. J Am Assoc Gynecol Laparosc 2004;11:153–161. 3. Olive DL, Schwartz LB. Endometriosis. N Engl J Med 1993;328:1759 –1769. 4. Kinkel K, Chapron C, Balleyguier C, Fritel X, Dubuisson JB, Moreau JF. Magnetic resonance imaging characteristics of deep endometriosis. Hum Reprod 1999;14(4):1080 –1086. 5. Gougoutas CA, Siegelman ES, Hunt J, et al. Pelvic endometriosis: various manifestations and MR imaging findings. AJR Am J Roentgenol 2000;175: 353–358. 6. Redwine DB. The distribution of endometriosis in the pelvis by age groups and fertility. Fertil Steril 1987;47:173–175.

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7. Chapron C, Fauconnier A, Vieira M, et al. Anatomic distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification. Hum Reprod 2003;18:157–161. 8. Fukaya T, Hoshiai H, Yajima A. Is pelvic endometriosis always associated with chronic pain? A retrospective study of 618 cases diagnosed by laparoscopy. Am J Obstet Gynecol 1993;169:719 – 722. 9. Katayama M, Masui T, Kobayashi S, et al. Evaluation of pelvic adhesions using multiphase and multislice MR imaging with kinematic display. AJR Am J Roentgenol 2001;177:107–110. 10. Garry R. Laparoscopic excision of endometriosis: the treatment of choice. Br J Obstet Gynaecol 1997;104:513–515. 11. Donnez J, Squifflet J. Laparoscopic excision of deep endometriosis. Obstet Gynecol Clin North Am 2004;31:567–580. 12. Donnez J, Spada F, Squifflet J, et al. Bladder endometriosis must be considered as bladder adenomyosis. Fertil Steril 2000;74:1175–1181. 13. Stanley KE, Utz DC, Dockerty MB. Clinically significant endometriosis of the urinary tract. Surg Gynecol Obstet 1965;120:491–502. 14. Chapron C, Dubuisson JB. Laparoscopic treatment of deep endometriosis located on the uterosacral ligaments. Hum Reprod 1996;11:868 – 873. 15. Koninckx PR, Meuleman C, Oosterlynck D, Cornillie FJ. Diagnosis of deep endometriosis by clinical examination during menstruation and plasma Ca-125 concentration. Fertil Steril 1996; 65:280 –287. 16. Koninckx PR, Martin D. Treatment of deeply infiltrating endometriosis. Curr Opin Obstet Gynecol 1994;6:231–241. 17. Mais V, Guerriero S, Ajossa S, et al. The efficiency of transvaginal ultrasonography in the diagnosis of endometrioma. Fertil Steril 1993;60:776 – 780. 18. Guerriero S, Mais V, Ajossa S, et al. The role of endovaginal ultrasound in differentiating endometriomas from other ovarian cysts. Clin Exp Obstet Gynecol 1995;22:20 –22. 19. Fedele L, Bianchi S, Raffaelli R, et al. Preoperative assessment of bladder endometriosis. Hum Reprod 1997;12:2519 –2522. 20. Roseau G, Dumontier I, Palazzo I, et al. Rectosigmoid endometriosis: endoscopic ultrasound features and clinical implications. Endoscopy 2000; 32:525–530. 21. Chapron C, Dubuisson JB. Management of deep endometriosis. Ann N Y Acad Sci 2001;943:276 – 280. 22. Chapron C, Dumontier I, Dousset B, et al. Results and role of rectal endoscopic ultrasonography for patients with deep pelvic endometriosis. Hum Reprod 1998;13:2266 –2270. 23. Fedele L, Bianchi S, Portuese A, Borruto F, Dorta M. Transrectal ultrasonography in the assessment of rectovaginal endometriosis. Obstet Gynecol 1998;91:444 – 448.

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24. Schroder J, Lohnert M, Doniec JM, Dohrmann P. Endoluminal ultrasound diagnosis and operative management of rectal endometriosis. Dis Colon Rectum 1997;40:614 – 617. 25. Zawin M, McCarthy S, Scoutt L, et al. Endometriosis: appearance and detection at MR imaging. Radiology 1989;171:693– 696. 26. Togashi K, Nishimura K, Kimura I, et al. Endometrial cysts: diagnosis with MR imaging. Radiology 1991;180:73–78. 27. Balleyguier C, Chapron C, Dubuisson JB, et al. Comparison of magnetic resonance imaging and transvaginal ultrasonography in diagnosing bladder endometriosis. J Am Assoc Gynecol Laparosc 2002;9:15–23. 28. Zanardi R, Del Frate C, Zuiani C, Del Frate G, Bazzocchi M. Staging of pelvic endometriosis using magnetic resonance imaging compared with the laparoscopic classification of the American Fertility Society: a prospective study. Radiol Med (Torino) 2003;105:326 –338. 29. Zanardi R, Del Frate C, Zuiani C, Del Frate G, Bazzocchi M. Staging of pelvic endometriosis based on MRI findings versus laparoscopic classification according to the American Fertility Society. Abdom Imaging 2003;28(5):733–742. 30. Bazot M, Darai E, Hourani R, et al. Deep pelvic endometriosis: MR imaging for diagnosis and prediction of extension of disease. Radiology 2004; 232:379 –389. 31. Takeuchi M, Matsuzaki K, Uehara H, Nishitani H. Malignant transformation of pelvic endometriosis: MR imaging findings and pathologic correlation. RadioGraphics 2006;26:407– 417. 32. Bis KG, Vrachliotis TG, Agrawal R, Shetty AN, Maximovich A, Hricak H. Pelvic endometriosis: MR imaging spectrum with laparoscopic correlation and diagnostic pitfalls. RadioGraphics 1997; 17:639 – 655. 33. Chapron C, Dubuisson JB. Laparoscopic management of bladder endometriosis. Acta Obstet Gynecol Scand 1999;78:887– 890. 34. Nezhat C, Nezhat F, Nezhat CH, Nasserbakht F, Rosti M, Seidman DS. Urinary tract endometriosis treated by laparoscopy. Fertil Steril 1996;66: 920 –924. 35. Chapron C, Dubuisson JB, Fritel X, et al. Operative management of deep endometriosis infiltrating the uterosacral ligaments. J Am Assoc Gynecol Laparosc 1999;6:31–37. 36. Possover M, Diebolder H, Plaul K, Shneider A. Laparoscopically assisted vaginal resection of rectovaginal endometriosis. Obstet Gynecol 2000;96: 304 –307. 37. Redwine DB, Koning M, Sharpe DR. Laparoscopically assisted transvaginal segmental resection of the rectosigmoid colon for endometriosis. Fertil Steril 1996;65:193–197. 38. Bailey HR, Ott MT, Hartendrop P. Aggressive surgical management for advanced colorectal endometriosis. Dis Colon Rectum 1994;37:747– 753. 39. Coronado C, Franklin RR, Lotze EC, et al. Surgical treatment of symptomatic colorectal endometriosis. Fertil Steril 1990;53:411– 416.

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Del Frate et al

Deep Retroperitoneal Pelvic Endometriosis: MR Imaging Appearance with Laparoscopic Correlation Chiara Del Frate, MD, et al RadioGraphics 2006; 26:1705–1718 ● Published online 10.1148/rg.266065048 ● Content Codes:

Page 1706 On the contrary, the histologic findings of infiltrative lesions of deep pelvic endometriosis are mainly characterized by fibromuscular hyperplasia that surrounds foci of endometriosis, and the foci sometimes contain small cavities. The endometrial glands and stroma infiltrate the adjacent fibromuscular tissue and elicit smooth muscle proliferation and fibrous reaction, resulting in solid nodule formation (1,2). Page 1707 Although peritoneal endometriosis can be asymptomatic, deep pelvic endometriosis is a cause of pelvic pain, dysmenorrhea, dyspareunia, dyschezia, and urinary symptoms and is associated with infertility. Urinary tract disease may manifest as hydronephrosis caused by ureteral obstruction or as a submucosal lesion within the bladder or ureter. Page 1708 With implants in this location, the deep endometriotic lesions are separated according to anatomic distribution, based on their location in the anterior cul-de-sac, posterior cul-de-sac, or pelvic sidewall (2). Page 1711 MR imaging characteristics of deep pelvic endometriosis depend on the type of lesions: infiltrating small implants, solid deep lesions mainly located in the posterior cul-de-sac involving the uterosacral ligaments and torus uterinus, and visceral endometriosis involving the bladder and rectal wall. Page 1711 Solid deep lesions demonstrate low to intermediate signal intensity with punctate regions of high signal intensity on T1-weighted images, uniform low signal intensity on T2-weighted images, and enhancement, corresponding to the abundant fibrous tissue seen in these lesions at histologic examination (5). The punctate foci of high signal intensity represent regions of hemorrhage surrounded by solid fibrotic tissue (Fig 5).