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ª Springer Science+Business Media New York 2016 Abdom Radiol (2016)

Abdominal DOI: 10.1007/s00261-016-0956-8

Radiology

Deep pelvic endometriosis: a radiologist’s


guide to key imaging features with clinical
and histopathologic review
Ayeh Darvishzadeh ,1 Wendaline McEachern,2 Thomas K. Lee,3 Priya Bhosale,4
Ali Shirkhoda,1 Christine Menias,5 Chandana Lall1
1
Department of Radiology, University of California Irvine School of Medicine, 1001 Health Sciences Road, Irvine, CA 92617, USA
2
Department of Radiology, Mayo Clinic, Rochester, MN, USA
3
Department of Pathology, University of California Irvine School of Medicine, Irvine, CA, USA
4
Division of Diagnostic Imaging, UT MD Anderson Cancer Center, Houston, TX, USA
5
Department of Radiology, Mayo Clinic, Phoenix, AZ, USA

Abstract menopausal women and 2.5% of postmenopausal women


[1–3] with an average age of diagnosis usually between
While endometriosis typically affects the ovaries, deep 25- and 29-year old, increasing with age. Risk factors
infiltrating endometriosis can affect the gastrointestinal include prolonged use of an intrauterine device, unin-
tract, urinary tract, and deep pelvis, awareness of which terrupted menstrual cycles, and a history of a first-degree
is important for radiologists. Symptoms are nonspecific relative with endometriosis [4]. The incidence of
and can range from chronic abdominal and deep pelvic endometriosis increases to 17% in women with infertility
pain to nausea, vomiting, diarrhea, constipation, hema- and to 50% of women who complain of pelvic pain [5, 6].
turia, and rectal bleeding. Ultrasound and computed Typically, endometriosis implants in the ovaries and
tomography may show nonspecific soft-tissue density uterosacral ligaments with the classic clinical presenta-
masses causing bowel obstruction and hydronephrosis. tion being a female of reproductive age with cyclical
This constellation of presenting symptoms and imaging pelvic pain with menstruation and dyspareunia [7].
evidence is easily mistaken for other pathologies includ- Endometriosis, however, can affect other areas including
ing infectious gastroenteritis, diverticulitis, appendicitis, the pericardium, lungs, and the peritoneum. Roughly
and malignancy, which may lead to unnecessary surgery 5–15% of endometriosis affects the gastrointestinal tract
or mismanagement. With this, deep pelvic endometriosis [5, 8]. Most commonly, gastrointestinal endometriosis
should be considered in the differential diagnosis in a involves the rectosigmoid colon, followed by the sigmoid
female patient of reproductive age who presents with colon, rectum, ileum, appendix, and cecum; this is often
such atypical symptoms, and further work up with but not always present in conjunction with pelvic
magnetic resonance imaging is imperative for accurate endometriosis.
diagnosis, treatment selection, and preoperative plan- Deep infiltrating endometriosis (DIE) is defined as
ning. subperitoneal endometrial implants, greater than 5 mm
in depth affecting the gastrointestinal tract, urinary tract,
Key words: Endometriosis—Deep infiltrating
and pelvic cul-de-sac and is usually associated with
endometriosis—Gastrointestinal tract—Pelvis—Cul-de-
reactive inflammation, fibrosis, adhesions, and smooth
sac—Ultrasound—Magnetic resonance imaging
muscle hyperplasia (Fig. 1). Gastrointestinal DIE typi-
(MRI)—Computed tomography (CT)
cally involves the rectosigmoid, small bowel, colon, and
appendix. DIE of the urinary tract can affect the ureters
and urinary bladder while DIE of the cul-de-sac can in-
Endometriosis was first reported by Rokitansky in 1860 volve the uterosacral ligaments, vagina, and cervix. Pa-
and affects 1–7% of women, including 6–10% of pre- tients with endometriosis usually present with chronic,
nonspecific symptoms including nausea, vomiting, diar-
Correspondence to: Ayeh Darvishzadeh; email: ayehd@uci.edu rhea, constipation, rectal bleeding, dyschezia, deep dys-
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 2. Colonoscopy images of female with endometriosis of


the colon showing A mucosal induration with areas of fibrosis
and punctate hemorrhagic foci and B mass-like protrusion
into the colon.

opposed to those reporting infertility [12, 13]. Further-


more, physical exam is usually insensitive to detect
endometriosis [14] with highly variable findings on exam
depending on size and location of ectopic tissue and
Fig. 1. Schematic of the female reproductive system and clinical experience of examiners. The most common
pelvis illustrating typical locations of deep infiltrating
clinical findings include palpable nodules at the uter-
endometriosis. A Uterus and associated structures and colon.
osacral ligament, rectovaginal space, Pouch of Douglas,
B Sagittal view of the pelvis.
rectosigmoid, and posterior wall of the urinary bladder
[15]. However, the diagnostic value of a physical exam-
ination is limited by the inability of an examiner to
pareunia, and even crippling, chronic pelvic pain [9, 10]. palpate deep enough into the pelvis, specifically in the
Roughly 27% of intestinal endometriosis results in bowel rectosigmoid space. Subsequent delayed diagnosis is
obstruction and can necessitate emergency surgery [11, costly, with an estimated cost of $12,419 per woman per
12]. year due to health care costs and loss of productivity [16,
Since symptoms tend to be nonspecific, the estimated 17]. Delay in diagnosis leads to more progressive disease,
delay in diagnosis is between 3 and 9 years and is greater which increases the risk of organ damage and greater
in patients whose primary complaint is pelvic pain as need for invasive surgical intervention [15].
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 3. An asymptomatic 44-year-old woman with a signifi- attenuation at mass borders and heterogenous soft-tissue
cant family history of colon cancer who on screening colono- density body. C Specimen of resected sigmoid colon showing
scopy was found to have a mass in the sigmoid colon that did intramural mass protruding into the sigmoid. D–F Pathology
not penetrate through the mucosa. Differential diagnosis at time images of mass shown in C. D Low-power image of histological,
of surgery was gastrointestinal stromal tumor, leiomyoma, or showing colonic mucosa (arrow) with areas of hypertrophic
endometriosis. A, B Coronal and axial contrast-enhanced CT muscularis propria and endometriosis (asterisk). E High-power
images show a subtle, soft-tissue density thickening in the images of benign endometrial gland and endometrial stroma.
sigmoid colon (arrows). Inlet image is zoomed in image of F High-power image of endometrial gland and stroma stained
coronal CT showing circumscribed mass in colon with hyper- positive with estrogen-receptor immunostaining (brown).
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 4. 40-year-old female with rectal pain and hematuria. A, C, D Axial and sagittal contrast-enhanced CT images showing
B Transvaginal ultrasound imaging showing a hypoechoic a mildly enhancing mass in between the urinary bladder and
mass between the urinary bladder and anterior uterus rectum. anterior uterus (asterik).

Typically, patients with endometriosis are often tion remains the gold standard diagnostic method to
diagnosed with pelvic inflammatory disease, irrita- date. However, unanticipated intraoperative biopsies
ble bowel syndrome, Crohn disease, infectious colitis, showing endometriosis often result in a second surgery
diverticulitis, appendicitis, and malignancy [13]. after reassessment and proper bowel preparation [18].
Small, scattered deep endometrial foci can be Given this, diagnosis of endometriosis involving the
especially difficult to detect with computed tomography colon and pelvis is important to allow for preoperative
(CT) and magnetic resonance imaging (MRI) sec- planning, which may include a general surgeon or
ondary to limiting in spatial resolution. Recent devel- urologist.
opments in soft-tissue characterization on MRI, The objective of this article is to review and discuss
however, allow for excellent preoperative assessment of the symptoms and imaging of deep pelvic endometriosis
DIE. Laparoscopic surgery with histological confirma- of the gastrointestinal and urinary tract in order to
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 5. 41-year-old female presented to the Emergency ings on CT raised concern for a colorectal neoplasm. D Sin-
Department with severe deep pelvic pain. A–C Axial CT gle-contrast barium enema shows a 7 cm stricture with
images with enteral contrast showed a lobulated soft-tissue serrated appearance and mucosal crenation at the rectosig-
density mass causing extrinsic compression and severe moid junction. Subsequent pathology revealed rectosigmoid
luminal narrowing at the rectosigmoid junction. Imaging find- endometriosis.

familiarize clinicians with the typical and atypical appear- depth. Understanding the imaging of deep infiltrating
ance of suspected DIE on various imaging modalities. endometriosis relies on some factors of its pathophysi-
ology. DIE is associated with reactive inflammation of
the surrounding area, including proliferation of smooth
Clinical features and pathophysiology muscle cells, fibrosis, and adhesions [19]. Endometriotic
Deep infiltrating endometriosis consists of subperitoneal implants may also include small, interspersed hemor-
endometrial implants that are greater than 5 mm in rhagic foci.
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 6. 33-year-old female with a 3-year history of severe raphy. B, C Axial and coronal contrast-enhanced CT images
pelvic and abdominal pain, constipation, and catamenial rec- show circumscribed broad-based soft-tissue density thicken-
tal bleeding. A Transvaginal ultrasound images of adeno- ing at the sigmoid colon (arrows). D High-power pathology
myosis showing cystic anechoic spaces throughout the section showing endometrial glands and stroma infiltrating the
myometrium that show low velocity flow with Doppler sonog- submucosal and muscularis propria.
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 7. 34-year-old female presenting with severe right lower hydronephrosis and extrinsic compression and narrowing of the
quadrant pain and mild rectal bleeding. A Coronal contrast- right ureter at the upper pelvis (blue arrows) E, F Axial contrast-
enhanced CT image of the abdomen and pelvis showing a enhanced CT images showing dilation of the right ureter
hypodense mass at the cecal base and appendix (asterix). proximal to external compression at the area of endometriosis.
B Delayed urographic phase CT image of the abdomen and G Final specimen of the appendix showing endometrial
pelvis showing right hydronephrosis and extrinsic ureteral glands and stroma in the lumen of the appendix (asterix).
involvement at the middle right ureter. C Magnetic resonance Final diagnosis was endometriosis of the appendix and right
urogram and D retrograde right ureteral injection showing mild ureter.
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 9. 46-year-old female with a 1-year history of episodic c


crampy abdominal pain in the mid-epigastric and right upper
quadrant region, presenting to the Emergency Department
with a 1-day history of severe right and epigastric abdominal
pain, nausea, chills and sweats, denies changes in bowel
habits, diarrhea, constipation, or hematochezia. Physical
exam showed tenderness to palpation in epigastric and left
and right lower quadrants of the abdomen. Abdominal ultra-
sound showed no evidence of liver, common bile duct, or
gallbladder abnormality. A–C, Coronal, sagittal, and axial
contrast-enhanced CT images of the abdomen shows a low-
lying cecum that is positioned medially within the mid-pelvis
with an ill-defined soft-tissue density mass with scattered low-
attenuation areas that appear to be emanating from the cecal
base. D, E Coronal and sagittal-delayed CT images with
intraluminal contrast filling the cecum and distal small bowel
showing the cecal mass. Differential diagnosis at time of
imaging included cecal or appendiceal neoplasm, and
inflammatory mass relation to initial presentation of inflam-
matory bowel disease or subclinical appendicitis. F Final
pathology confirms endometriosis with histology showing
endometrial glands and stroma in the colonic mucosa (da-
shed circles) and submucosal (asterix). G Endoscopic image
showing large erythematous mass at the cecum that was soft
and fluctuant with positive pillow sign when compressed.
Fig. 8. Contrast-enhanced coronal abdominal CT image of
38-year-old female with history of episodic right lower quad-
rant abdominal pain showing heterogeneous soft-tissue den-
sity mass in the cecum (straight arrow). Circumscribed areas
of hypoattenuation suggestive of hemorrhagic foci (round Patients who present with changes in bowel move-
arrow). Differential diagnosis included acute appendicitis, ments and abdominal pain often undergo colonoscopy
cecal malignancy, Crohn’s disease, enterocolitis, and ileoce- and CT for initial analysis, but the findings can mislead
cal tuberculosis. Pathology confirmed cecal endometriosis. physicians toward diagnoses of malignancy, inflamma-
tory bowel disease (IBD), ischemic bowel, or chronic
Gastrointestinal tract enteritis. On endoscopy, deep endometriosis can present
with slight induration or hyperplastic surface epithelium
In the bowel, DIE implants at the antimesenteric edge of of the mucosa (Fig. 2), intramural masses protruding
the serosa and infiltrates through the muscularis propria into the colon causing extrinsic compression and lumi-
into the wall in a progressive manner [20]. Furthermore, nal narrowing (Fig. 3), or as masses with central
depending on the location of ectopic tissue and depth of ulceration and indurated, rolled borders that can mimic
invasion, bowel endometriosis can present in various, carcinoma [19, 33]. On biopsy, mucosal changes include
surprising ways. Superficial endometriosis involving only distorted colonic glands, blunting of intestinal villi,
the serosa can be asymptomatic. Classically, we would pyloric metaplasia, polypoid granulation tissue, and
expect patients with DIE to report pelvic pain that peaks deep fissures also found in IBD, ischemic bowel, and
and troughs in a cyclical manner synchronized with the chronic enteritis [19].
proliferation and shedding of the ectopic endometrial
tissue with the menstrual cycle [21, 22]. However, pa-
tients report chronic deep pelvic pain nausea, vomiting, Urinary tract
diarrhea, constipation, reduced stool caliber, abdominal Deep infiltrating endometriosis of the urinary tract most
bloating, and even ascites [11, 21–27]. Although DIE commonly affects the bladder (15%) and the ureters
rarely infiltrates through to the mucosa, patients may (4.5%), in women with severe endometriosis [34, 35].
also present with hematochezia, thought to occur when Endometriosis of the bladder can present with hema-
swelling of underlying endometrial tissue causes colonic turia, dysuria, urinary frequency, urinary tract infec-
mucosa to tear [20, 25]. Endometriosis of the appendix tions, pelvic pain, constipation, diarrhea, and both
can also occur and may present with profuse rectal urgency or stress urinary incontinence [35–39]. Diagnosis
bleeding or mimic acute appendicitis, chronic appen- of bladder endometriosis is confounded by a clinical
dicitis, or a peptic ulcer [28–32]. presentation that is similar to urinary tract infections,
A. Darvishzadeh et al.: Deep pelvic endometriosis
A. Darvishzadeh et al.: Deep pelvic endometriosis

overactive bladder syndrome, painful bladder syndrome, Fig. 10. 43-year-old female with history of endometriosis c
and interstitial cystitis [40]. Bladder endometriosis may presenting with 3 months of right lower flank pain and
also be associated with ovarian and rectosigmoid lesions, hematuria. A–C Axial contrast-enhanced images of the pelvis
with one study reporting co-existing disease in 49.2% and showing a, irregular contour at the right bladder with a mildly
hyperdense mass extending into the vescicular space. B De-
28.9% of cases, respectively [38]. Ureteral endometriosis
layed imaging showing intravenous-contrast filling the bladder
typically implants on the external surface of the ureters
outlining the irregular mass and C post-contrast image
and causes external constriction of the ureteral wall, showing mild hyperattenuation of the mass with attenuation
leading to significant pathology such as progressive renal again similar to myometrium. D Axial T1-weighted MRI image
function loss. Thus, diagnosing ureteral endometriosis is showing the mass in the lower right bladder wall that appears
critical to prevent kidney damage and significant isointense to muscle with foci of hyperintensity indicative of
hydronephrosis but can be difficult due to either a hemorrhagic cysts. E Axial T2-weighted MRI image showing
complete lack of or nonspecific symptoms. Unfortu- the mass is hypointense to muscle with hyperintense foci
nately, 47% of patients with ureteral endometriosis re- again indicative of hemorrhagic products. F Final pathology of
quire nephrectomy at the time of diagnosis [41]. the lesion in the bladder wall showing endometrial glands at
Common presenting symptoms include dysuria, recur- the level of the muscularis propria with E, estrogen-receptor
staining positive on immunohistochemistry.
rent urinary tract infections, and hematuria [35]. Corre-
lations between ureteral and rectovaginal endometriosis
and between ureteral and uterosacral ligament
endometriosis have also been reported and should be
described as pyramidal shaped and are attached to the
considered with women who have evidence of either
anterior rectal wall, pointing anteriorly toward the uterus
other locations [34, 35].
[48]. Furthermore, the margins are irregular and one end
appears thinner than the other, similar to a comet, and
Imaging modalities thin band-like echoes that spread out from the center of
the mass have been described as like an ‘‘Indian head
Ultrasound
dress’’ [49, 50]. Examiners can also look for pelvic
Gastrointestinal tract adhesions by assessing the movement of the uterus,
ovaries, and bowel loops with movement of the trans-
Transvaginal ultrasound after bowel preparation
ducer [37]. TVUS-BP, however, is most useful when
(TVUS-BP) remains the best initial imaging method for
detecting endometriosis of the bladder, rectum, and
endometriosis, since it can detect foci of deep
rectovaginal septum, with limitations of examining the
endometriosis including which layer of bowel has been
proximal gastrointestinal tract [51].
infiltrated, while also being low cost, vastly available,
Trans-rectal ultrasound (TRUS) has also shown high
and not exposing the patient to radiation [37, 42–46]. It
sensitivity and specificity for detecting endometriosis of
is, however, operator-dependent, time-consuming and
the rectovaginal region [52]. Like with TVUS,
may miss or underestimate the extent of disease.
endometriosis of the rectosigmoid presents as irregular
Improvements in patient preparation allow increased
hypoechoic masses on the intestinal wall, protruding
visualization of the bowel for examination. These include
through the muscularis layer, and a characteristic ‘‘C’’
adequate bowel preparation to minimize fecal contents
shape has been described that identifies the retraction of
and intestinal gas, placing ultrasound gel in the upper
the endometriotic nodule due to fibrosis and adhesions
third of the vagina to distend the vaginal dome, and
[53]. TRUS is limited in which it cannot be used to assess
injecting ultrasound gel in the rectum gain a better view
DIE of the anterior pelvic cul-de-sac, including the
of the bowel wall [37, 47]. Using TVUS-BP, bowel
uterovesical space and bladder, and may require the
endometriosis appears as an irregular hypoechoic mass
patient to be sedated. However, it offers the benefits for
with or without hypoechoic or hyperechoic foci pene-
the examiner to perform a fine needle aspiration for
trating into the hypoechoic muscularis propria layer
histological confirmation and is better able to determine
wall. It may also show as long, nodular hypoechoic le-
the extent of endometriosis infiltration into the intestinal
sions along the intestinal wall [20, 42]. Submucosal le-
wall than TVUS [53, 54].
sions appear as hypoechoic gaps in the hyperechoic
submucosa. On color Doppler imaging, the masses show
Urinary tract
no blood flow. A number of characteristic appearances
of endometriosis of the rectosigmoid area have been re- Ultrasound is the initial imaging method of choice for
ported, including the ‘‘pyramid sign,’’ the ‘‘comet sign,’’ urinary tract endometriosis. TVUS the first line method
and the ‘‘Indian headdress sign’’ [48–50]. The lesions are of diagnosing bladder endometriosis from which the size
A. Darvishzadeh et al.: Deep pelvic endometriosis
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 11. ‘‘Mushroom cap sign’’ seen with a deep, infiltrating fibrosis between the torus uterinus and the rectum (A, B; ar-
deposit in the rectum (A sagittal T2, B sagittal T1 FS post- rowheads), with obliteration of the rectocervical space (D axial
gadolinium; C fluoroscopic barium enema with end-to-side T1 FS postgadolinium; arrow).
anastomosis; arrows). There is T2 hypointense, enhancing

of the lesions and infiltration into the detrusor muscle choic or isoechoic to the bladder wall masses with
can be assessed [51]. The endometrial lesions typically numerous anechoic spaces within, described as ‘‘bubble-
appear as solid ‘‘comma-shaped’’ or spherical hypoe- like’’ [55–57]. Color Doppler shows few vessels within the
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 12. 46-year-old female with obliterated anterior and D Axial T1 FS and E sagittal T2 images show bilateral ovarian
posterior cul-de-sac secondary to chronic fibrotic endometriomas which are T1 hyperintense (D, arrows) with
endometriosis. A Sagittal T1FS post-gadolinium and B sagit- T2 shading with tethering to the uterine fundus (E, arrows)
tal T2 imaging shows tethering to the urinary bladder (arrows). creating a ‘‘kissing ovaries’’ appearance (F coronal T2,
C Sagittal T2 image shows tethering to the rectum (arrow). arrow).
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 13. A nodular submucosal mass protrudes into the arrow) signal. C Axial T1FS post-gadolinium shows mild
urinary bladder with punctate foci of T1 hyperintense (A axial enhancement (arrow). D Cystoscopy with mild mucosal bulge
T1 FS, arrow) and predominantly T2 hypointense (B axial T2, (arrow).

endometriotic implants [57]. They are typically found at plasms (Figs. 5, 6). Usually these patients do not un-
the posterior bladder wall and cause external compres- dergo workup for DIE, instead undergo explorative
sion into the bladder (Fig. 4A, B). TVUS is also used to laparotomy or laparoscopy usually with inadequate
assess the ureters, both at rest, while peristalsing in order preoperative planning, preparation, and patient consent
to look for endometriosis, ureteral dilation, abnormal prior to surgery. Understanding CT imaging of
bending, or evidence of obstruction [56, 58]. Ureteral endometriosis is essential for accurate diagnosis,
endometriosis appears as heterogeneous hypoechoic prompting appropriate further imaging to evaluate
nodules. Hydronephrosis can be visualized on renal locations and depth of other ectopic foci. Typically
ultrasound and dilated ureters above the site of endometriosis of the colon presents as a soft-tissue den-
endometriosis may be seen on pelvic or abdominal sity intraluminal mass with mild to moderate contrast
ultrasound. These findings can mimic ureteral obstruc- enhancement and may cause eccentric stenosis of the
tion by cervical cancer [37]. intestinal lumen. Furthermore, the intestinal wall in close
proximity to the nodule displays mural thickening and
scalloping. Bowel may be angulated or displaced from
Computed tomography and fluoroscopy the expected locations. Evaluation of cecal and appen-
Patients with endometriosis with clinical symptoms of diceal endometriosis can be further complicated due to
appendicitis, chronic pelvic pain, gastrointestinal symp- stenosis by muscular contraction, incomplete distention,
toms of diarrhea, constipation and possibly reduced or presence of feces [59]. Due to these confounding fac-
stool caliber, or hematochezia often undergo CT imaging tors, two of our cases of endometriosis were mistaken for
for diagnosis. On contrast-enhanced CT imaging, DIE appendicitis, cecal malignancy, and inflammatory bowel
typically appears as a soft-tissue density mass, indistin- disease (Figs. 7, 8, 9). Notably, inflammatory changes of
guishable from other gastrointestinal pathologies the nearby bowel and mildly enhancing lymph nodes
including diverticulitis, and benign or malignant neo- may also appear on CT.
A. Darvishzadeh et al.: Deep pelvic endometriosis

Fig. 14. ‘‘Kissing ovaries’’ morphology with tethering to the demonstrates bilateral hyperintense endometriomas
uterus. A Axial T2 image demonstrates ‘‘kissing ovaries’’ (arrows). C T2 hypointense tethering to the uterine serosa
(arrow), the ‘‘dark spot sign’’ (arrowhead), and dark periph- (arrow). D Coronal T2 shows thickening of the uterosacral
eral rind (double arrowhead). B Sagittal T1 FS image ligaments (arrows).

Advancements in the use of CT for endometriosis identify endometriosis of the intestinal tract and the ur-
have been noted. Roman et al. created a virtual colo- eters [61]. On CT, endometriosis of the bladder can
noscopy (CTC) that provides an accurate preoperative present as an irregular, mildly enhancing mass in the
roadmap of the length of the colon affected by DIE and bladder wall with associated mural thickening (Figs. 4,
degree of stenosis when compared to magnetic resonance 10). Furthermore, endometriosis of the ureters causes
imaging [60]. CT urography is useful for assessing ur- fibrosis, leading to hydronephrosis, dilated ureters
eteral involvement (Fig. 7). Iosca et al. report using proximal to location of implantation and can pull the
multislice CT with colon water distention (MSCT-c) and lower portion of the ureter medially from the lateral
intravenous injection of iodinated contrast medium to position (Fig. 7B).
A. Darvishzadeh et al.: Deep pelvic endometriosis

Double-contrast barium enema (DCBE) is not cur- Fig. 15. 34-year-old female with tri-compartmental involve- c
rently recommended for the diagnosis of endometriosis ment. A axial T1 and B axial T2 images demonstrate an
due to low specificity. Classically, however, it had been a obliterated posterior cul-de-sac with left ovarian endometri-
helpful method of imaging endometriosis of the gas- oma (T1 hyperintense, T2 hypointense; arrows). The uterus is
retroflexed and there is a ‘‘kissing ovaries’’ morphology (B).
trointestinal tract, specifically the rectosigmoid colon. On
C sagittal T2 image shows T2 hypointense fibrotic thickening
DCBE, endometriosis appears with characteristic find-
from the torus uterinus and lower uterine segment to the
ings including strictures caused by extrinsic mass effect, rectum (arrows). D sagittal T1 FS shows left ovarian serosal
shortening, tethering, or flattening of the bowel wall. deposits (hyperintense foci; arrow). E axial T2 shows
Additionally, intramural endometriosis with subsequent involvement of the right distal ureter (hypointense thickening;
scalloping of antimesenteric border creates the charac- arrow). There is T2 thickening of the bilateral uterosacral
teristic crenulation pattern seen on DCBE, which may be ligaments (F coronal T2; arrows) and round ligaments (G axial
the only distinguishing finding (Fig. 5D) [9, 59, 62, 63]. T2; arrows). H Laparoscopy showing obliterated posterior cul-
Given that these findings, however, are nonspecific and de-sac.
are similar to the findings of malignancy, the diagnostic
value of DCBE is limited.
In general, given that most patients are of reproduc- sions on T2-weighted images as a hypointense fibrotic
tive age, the use of CT and fluoroscopy is limited by the mass in the muscularis layer that protrudes into the
patient’s desire to forgo radiation exposure. intestinal lumen with hyperintense submucosal and mu-
cosal layers that cover the mass and create an outline
similar to that of a mushroom cap (Fig. 11) [64]. Other
Magnetic resonance imaging
findings include bowel wall thickening, loss of fat planes
MRI is the imaging modality of choice for evaluation of between bowel segments and adjacent organs, and
deep infiltrating endometriosis due to inherent high abnormal angulation of the bowel loops [59, 69]. In-
sensitivity for detecting blood products and global eval- creased spatial resolution with the use of a 3.0T MRI
uation of structures compared to the limited reach of compared to a 1.5T MRI allows for improved detection
TVUS [59, 64]. Although not implemented at all insti- of smaller DIE lesions and superficial endometriosis by
tutions, MRI sensitivity can be improved by bowel showing adhesions and peritoneal irregularities [65].
preparation, administration of an antispasmodic agent to The anterior compartment includes the bladder, ve-
reduce bowel peristalsis, and administration of vaginal sico-uterine pouch, vesico-vaginal septum, and distal
gel [36]. Use of rectal gel is disputed since it can increase ureters. Superficial, serosal implants are typically T2
bowel peristalsis and distort rectal retraction caused by hypointense and result in ante-flexion and obliteration
the endometriosis implants [37, 65]. The timing of MR is of the anterior cul-de-sac (Fig. 12). Lesions that invade
also controversial, however, some authors suggest per- through to the bladder mucosa may demonstrate more
forming MR 12 days after the first day of the patient’s typical T1 hyperintense and T2 hypointense glandular
last menstrual period when the endometrial blood elements [35, 70] (Figs. 10, 13). Given the rarity of
products are at their maximum [66]. Evaluation should bladder mucosal invasion, these implants may be missed
include investigation of the gastrointestinal tract and the at cystoscopy and the patient may be asymptomatic
deep pelvis, typically based on a tri-compartmental ap- [67]. MR urography and retrograde ureteral injection
proach, i.e., the anterior, middle, and posterior pelvic are used to determine extent of ureteral involvement
compartments [67, 68]. (Fig. 7).
DIE of the gastrointestinal tract appears as irregular, Middle compartment evaluation includes the uterus,
eccentric mass/masses infiltrating into the intestinal wall ovaries, fallopian tubes, and uterine ligaments. The hall-
causing luminal narrowing with associated fibrosis and mark findings of ovarian endometriomas are T1 hyperin-
smooth muscle hyperplasia appearing at times as irreg- tense cysts that demonstrate T2 dark shading and a T2
ular, speculated, hypointense lesions on T2-weighted dark rind due to the accumulation of degraded hemor-
images. Fat-saturated T1-weighted images show a mass rhagic blood products. More recently, however, the T2
or thickening, which is isointense to muscle, possibly ‘‘dark spot sign’’ has proven to have greater specificity in
with interspersed hyperintense foci that reflect hemor- discerning endometriomas from other hemorrhagic cysts.
rhagic blood products [37, 65, 66]. Restricted diffusion The T2 ‘‘dark spot sign’’ is characterized by discrete, cir-
with low apparent diffusion coefficient (ADC) values, cumscribed areas of increased hypointensity on T2
although not specific, is also noted [66]. The ‘‘mushroom weighted images within the T2-shaded cyst or against the
cap’’ sign refers to the appearance of rectosigmoidal le- cyst wall [71]. Tiny serosal deposits on the ovaries may
A. Darvishzadeh et al.: Deep pelvic endometriosis
A. Darvishzadeh et al.: Deep pelvic endometriosis
A. Darvishzadeh et al.: Deep pelvic endometriosis

b Fig. 16. 43-year-old female with small bowel obstruction of symptoms making diagnosis difficult. Patients may
and circumferential mass at the terminal ileum. A Coronal T2 suffer due to a delayed diagnosis, incurring health care
and c axial T2 show a hypointense, circumferential mass costs, and lost income due to decreased productivity with
(arrows). B Coronal T1 FS post-gadolinium shows mass a significant personal impact. The typical delay in diag-
enhancement (arrow). D B600 showing diffusion restriction nosis ranges from 3 to 9 years and may lead to pro-
(arrow). E Colonoscopy with tight stricture at the terminal
gressive disease requiring surgical intervention [16, 17].
ileum (arrow).
Thus, an early and precise diagnosis of DIE is ‘‘key.’’
Familiarity with the pathophysiology, clinical presenta-
have punctate areas of T1 hyperintensity with diffusion tion, and the imaging features of DIE can aid in the
restriction. Abutting, retro-positioned ovaries, secondary radiologic diagnosis and guide appropriate and timely
to endometriotic adhesions, may create a ‘‘kissing ovaries’’ patient management.
appearance. Thickening and nodularity of the broad and
round ligaments may also be present (Figs. 14, 15). Acknowledgements The authors acknowledge the assistance of Eric J.
Gray and Sonia Watson, Ph.D., for editing the manuscript and
The posterior compartment may be significantly in- Christopher M. Brown for illustration design.
volved by deep invasive endometriosis. This compart-
ment includes the rectum, Pouch of Douglas, torus Compliance with ethical standards
uterinus, uterosacral ligaments, posterior vaginal fornix,
and rectovaginal septum. Fibrotic changes are com- Funding No funding was received for this study.
monly seen in this area, manifest as predominantly T2
Conflicts of interest The authors declare that they have no conflict of
dark bands [72]. Retrocervical bands extending from the interest.
torus uterinus, uterosacral ligaments, and rectum may
cause partial or complete obliteration of the cul-de-sac Ethical approval All procedures performed in studies involving human
participants were in accordance with the ethical standards of the
[67]. Obliteration of the cul-de-sac may hide areas of institutional and/or national research committee and with the 1964
endometrial involvement on laparoscopic examination Helsinki declaration and its later amendments or comparable ethical
and thus underestimate disease extent at surgery [73]. standards.
Serosal deposits involving the rectosigmoid colon may be
Informed consent Statement of informed consent was not applicable
superficial, with potential for deeper invasion into the since the manuscript does not contain any patient data.
muscularis propria. Despite the lack of mucosal invasion,
serosal involvement may result in colonic obstruction or References
narrowing/stricture (Figs. 11, 15). 1. Benagiano G, Brosens I (2006) History of adenomyosis. Best Pract
Other sites of involvement include the vagina, the Res Clin Obstet Gynaecol 20:449–463. doi:10.1016/j.bpob-
small intestine, the ischio-anal fossa, the sciatic nerve, gyn.2006.01.007
2. Kratzer GL, Salvati EP (1955) Collective review of endometriosis
abdominal organs such as the liver, and extra-abdominal of the colon. Am J Surg 90:866–869
locations such as the pleura (Fig. 16) [67]. MR urogra- 3. Missmer SA, Hankinson SE, Spiegelman D, Barbieri RL, Marshall
phy and retrograde ureteral injection are used to deter- LM, Hunter DJ (2004) Incidence of laparoscopically confirmed
endometriosis by demographic, anthropometric, and lifestyle fac-
mine extent of ureteral involvement (Fig. 7C, D). tors. Am J Epidemiol 160:784–796. doi:10.1093/aje/kwh275
4. Sangi-Haghpeykar H, Poindexter AN 3rd (1995) Epidemiology of
endometriosis among parous women. Obstet Gynecol 85:983–992.
Laparoscopy doi:10.1016/0029-7844(95)00074-2
5. Giudice LC, Kao LC (2004) Endometriosis. Lancet 364:1789–
Ultimately, laparoscopy or laparotomy with histological 1799. doi:10.1016/S0140-6736(04)17403-5
confirmation of endometriosis remains the gold standard 6. Cramer DW, Wilson E, Stillman RJ, Berger MJ, Belisle S, Schiff I,
Albrecht B, Gibson M, Stadel BV, Schoenbaum SC (1986) The
for diagnosis. Typically, endometriosis is characterized relation of endometriosis to menstrual characteristics, smoking,
on laparoscopy as adhesions and serosal fibrosis with and exercise. JAMA 255:1904–1908
patchy gray-brown discoloration, also called ‘‘powder- 7. Ballard K, Lane H, Hudelist G, Banerjee S, Wright J (2010) Can
specific pain symptoms help in the diagnosis of endometriosis? A
burn’’ lesions. Macroscopically, the lesions are small cohort study of women with chronic pelvic pain. Fertil Steril 94:20–
nodules of large cystic glands and endometrial type 27. doi:10.1016/j.fertnstert.2009.01.164
stroma that appear on the peritoneal surface as raised, 8. Sakamoto K, Maeda T, Yamamoto T, Takita N, Suda S, Watan-
abe T, Sakamoto S, Kamano T, Takeuchi H, Kinoshita K (2006)
punctate hemorrhagic areas with hemosiderin deposits, Simultaneous laparoscopic treatment for rectosigmoid and ileal
whitish opacfications, or reddish-blue irregularly shaped endometriosis. J Laparoendosc Adv Surg Tech A 16:251–255.
lesions [20, 74]. doi:10.1089/lap.2006.16.251
9. Petta CA, Peloggia A (2015) Imaging techniques for the diagnosis
of deep endometriosis. Austin J Reprod Med Infertil 2:1020
10. Moawad NS, Caplin A (2013) Diagnosis, management, and long-
Summary term outcomes of rectovaginal endometriosis. Int J Womens Health
5:753–763. doi:10.2147/IJWH.S37846
Endometriosis is a common disease affecting up to 50% 11. Slesser AA, Sultan S, Kubba F, Sellu DP (2010) Acute small bowel
of women with pelvic pain and can present with a variety obstruction secondary to intestinal endometriosis, an elusive con-
A. Darvishzadeh et al.: Deep pelvic endometriosis

dition: a case report. World J Emerg Surg 5:27. doi:10.1186/1749- 32. Collins DC (1951) Endometriosis of the vermiform appendix; re-
7922-5-27 view of literature, with addition of nine new instances, one of which
12. Dmowski WP, Lesniewicz R, Rana N, Pepping P, Noursalehi M caused severe melena. AMA Arch Surg 63:617–622
(1997) Changing trends in the diagnosis of endometriosis: a com- 33. Muthyala T, Sikka P, Aggarwal N, Suri V, Gupta R, Nahar U
parative study of women with pelvic endometriosis presenting with (2015) Endometriosis presenting as carcinoma colon in a peri-
chronic pelvic pain or infertility. Fertil Steril 67:238–243. menopausal woman. J Midlife Health 6:122–124. doi:10.4103/0976-
doi:10.1016/S0015-0282(97)81904-8 7800.165592
13. Seaman HE, Ballard KD, Wright JT, de Vries CS (2008) En- 34. Donnez J, Spada F, Squifflet J, Nisolle M (2000) Bladder
dometriosis and its coexistence with irritable bowel syndrome and endometriosis must be considered as bladder adenomyosis. Fertil
pelvic inflammatory disease: findings from a national case-control Steril 74:1175–1181
study—Part 2. BJOG 115:1392–1396. doi:10.1111/j.1471- 35. Gabriel B, Nassif J, Trompoukis P, Barata S, Wattiez A (2011)
0528.2008.01879.x Prevalence and management of urinary tract endometriosis: a clinical
14. Chapron C, Dubuisson JB, Pansini V, Vieira M, Fauconnier A, case series. Urology 78:1269–1274. doi:10.1016/j.urology.2011.07.1403
Barakat H, Dousset B (2002) Routine clinical examination is not 36. Tarumi Y, Mori T, Kusuki I, Ito F, Kitawaki J (2015) Endometrioid
sufficient for diagnosing and locating deeply infiltrating adenocarcinoma arising from deep infiltrating endometriosis involv-
endometriosis. J Am Assoc Gynecol Laparosc 9:115–119 ing the bladder: a case report and review of the literature. Gynecol
15. Hudelist G, Ballard K, English J, Wright J, Banerjee S, Mas- Oncol Rep 13:68–70. doi:10.1016/j.gore.2015.07.003
toroudes H, Thomas A, Singer CF, Keckstein J (2011) Transvagi- 37. Chamie LP, Blasbalg R, Pereira RM, Warmbrand G, Serafini PC
nal sonography versus clinical examination in the preoperative (2011) Findings of pelvic endometriosis at transvaginal US, MR
diagnosis of deep infiltrating endometriosis. Ultrasound Obstet imaging, and laparoscopy. Radiographics 31:E77–100. doi:10.1148/
Gynecol 37:480–487. doi:10.1002/uog.8935 rg.314105193
16. Denny E (2004) Women’s experience of endometriosis. J Adv Nurs 38. Schonman R, Dotan Z, Weintraub AY, Bibi G, Eisenberg VH, Sei-
46:641–648. doi:10.1111/j.1365-2648.2004.03055.x dman DS, Goldenberg M, Soriano D (2013) Deep endometriosis
17. Rogers PA, D’Hooghe TM, Fazleabas A, Giudice LC, Mont- inflicting the bladder: long-term outcomes of surgical management.
gomery GW, Petraglia F, Taylor RN (2013) Defining future Arch Gynecol Obstet 288:1323–1328. doi:10.1007/s00404-013-2917-6
directions for endometriosis research: workshop report from the 39. Leone Roberti Maggiore U, Ferrero S, Salvatore S (2015) Urinary
2011 World Congress of Endometriosis in Montpellier, France. incontinence and bladder endometriosis: conservative management.
Reprod Sci 20:483–499. doi:10.1177/1933719113477495 Int Urogynecol J 26:159–162. doi:10.1007/s00192-014-2487-6
18. Kim JS, Hur H, Min BS, Kim H, Sohn SK, Cho CH, Kim NK 40. Bogart LM, Berry SH, Clemens JQ (2007) Symptoms of interstitial
(2009) Intestinal endometriosis mimicking carcinoma of rectum and cystitis, painful bladder syndrome and similar diseases in women: a
sigmoid colon: a report of five cases. Yonsei Med J 50:732–735. systematic review. J Urol 177:450–456. doi:10.1016/j.juro.2006.
doi:10.3349/ymj.2009.50.5.732 09.032
19. Yantiss RK, Clement PB, Young RH (2001) Endometriosis of the 41. Seracchioli R, Mabrouk M, Manuzzi L, Guerrini M, Villa G,
intestinal tract: a study of 44 cases of a disease that may cause Montanari G, Fabbri E, Venturoli S (2008) Importance of
diverse challenges in clinical and pathologic evaluation. Am J Surg retroperitoneal ureteric evaluation in cases of deep infiltrating
Pathol 25:445–454 endometriosis. J Minim Invasive Gynecol 15:435–439. doi:10.1016/
20. Remorgida V, Ferrero S, Fulcheri E, Ragni N, Martin DC (2007) j.jmig.2008.03.005
Bowel endometriosis: presentation, diagnosis, and treatment. Ob- 42. Goncalves MO, Podgaec S, Dias JA Jr, Gonzalez M, Abrao MS
stet Gynecol Surv 62:461–470. doi:10.1097/01.ogx.0000268688.55 (2010) Transvaginal ultrasonography with bowel preparation is
653.5c able to predict the number of lesions and rectosigmoid layers af-
21. Meyers WC, Kelvin FM, Jones RS (1979) Diagnosis and surgical fected in cases of deep endometriosis, defining surgical strategy.
treatment of colonic endometriosis. Arch Surg 114:169–175 Hum Reprod 25:665–671. doi:10.1093/humrep/dep433
22. Weed JC, Ray JE (1987) Endometriosis of the bowel. Obstet Gy- 43. Bazot M, Darai E, Hourani R, Thomassin I, Cortez A, Uzan S,
necol 69:727–730 Buy JN (2004) Deep pelvic endometriosis: MR imaging for diag-
23. Collier HA, Gonzales LL, Bossert LJ (1962) Cyclic ascites as a nosis and prediction of extension of disease. Radiology 232:379–
manifestation of endometriosis. Report of a case. Obstet Gynecol 389. doi:10.1148/radiol.2322030762
19:681–683 44. Vimercati A, Achilarre MT, Scardapane A, Lorusso F, Ceci O,
24. Macafee CH, Greer HL (1960) Intestinal endometriosis. A report Mangiatordi G, Angelelli G, Van Herendael B, Selvaggi L, Bet-
of 29 cases and a survey of the literature. J Obstet Gynaecol Br tocchi S (2012) Accuracy of transvaginal sonography and contrast-
Emp 67:539–555 enhanced magnetic resonance-colonography for the presurgical
25. Levitt MD, Hodby KJ, van Merwyk AJ, Glancy RJ (1989) Cyclical staging of deep infiltrating endometriosis. Ultrasound Obstet Gy-
rectal bleeding in colorectal endometriosis. Aust N Z J Surg necol 40:592–603. doi:10.1002/uog.11179
59:941–943 45. Hirai M, Shibata K, Sagai H, Sekiya S, Goldberg BB (1995)
26. Anaf V, El Nakadi I, Simon P, Van de Stadt J, Fayt I, Simonart T, Transvaginal pulsed and color Doppler sonography for the evalu-
Noel JC (2004) Preferential infiltration of large bowel ation of adenomyosis. J Ultrasound Med 14:529–532
endometriosis along the nerves of the colon. Hum Reprod 19:996– 46. Sakhel K, Abuhamad A (2012) Sonography of adenomyosis. J
1002. doi:10.1093/humrep/deh150 Ultrasound Med 31:805–808
27. Remorgida V, Ragni N, Ferrero S, Anserini P, Torelli P, Fulcheri E 47. Ferrero S, Biscaldi E, Vellone VG, Venturini PL, Leone Roberti
(2005) The involvement of the interstitial Cajal cells and the enteric Maggiore U (2016) Computed tomographic colonography versus
nervous system in bowel endometriosis. Hum Reprod 20:264–271. rectal-water contrast transvaginal ultrasonography in the diagnosis
doi:10.1093/humrep/deh568 of rectosigmoid endometriosis: a pilot study. Ultrasound Obstet
28. Collins DC (1955) A study of 50,000 specimens of the human Gynecol. doi:10.1002/uog.15905
vermiform appendix. Surg Gynecol Obstet 101:437–445 48. Trippia CH, Zomer MT, Terazaki CR, Martin RL, Ribeiro R,
29. Khoo JJ, Ismail MS, Tiu CC (2004) Endometriosis of the appendix Kondo W (2016) Relevance of imaging examinations in the surgical
presenting as acute appendicitis. Singap Med J 45:435–436 planning of patients with bowel endometriosis. Clin Med Insights
30. Driman DK, Melega DE, Vilos GA, Plewes EA (2000) Mucocele of Reprod Health 10:1–8. doi:10.4137/CMRH.S29472
the appendix secondary to endometriosis. Report of two cases, one 49. Benacerraf BR, Groszmann Y, Hornstein MD, Bromley B (2015)
with localized pseudomyxoma peritonei. Am J Clin Pathol Deep infiltrating endometriosis of the bowel wall: the comet sign. J
113:860–864. doi:10.1309/EUTL-BC88-TLAX-1UJ4 Ultrasound Med 34:537–542. doi:10.7863/ultra.34.3.537
31. Curbelo-Pena Y, Guedes-De la Puente X, Saladich-Cubero M, 50. Guerriero S, Ajossa S, Gerada M, Virgilio B, Angioni S, Melis GB
Molinas-Bruguera J, Molineros J, De Caralt-Mestres E (2015) (2008) Diagnostic value of transvaginal ‘tenderness-guided’ ultra-
Endometriosis causing acute appendicitis complicated with sonography for the prediction of location of deep endometriosis.
hemoperitoneum. J Surg Case Rep. doi:10.1093/jscr/rjv097 Hum Reprod 23:2452–2457. doi:10.1093/humrep/den293
A. Darvishzadeh et al.: Deep pelvic endometriosis

51. Fratelli N, Scioscia M, Bassi E, Musola M, Minelli L, Trivella G 62. Landi S, Barbieri F, Fiaccavento A, Mainardi P, Ruffo G, Selvaggi
(2013) Transvaginal sonography for preoperative assessment of L, Syed R, Minelli L (2004) Preoperative double-contrast barium
deep endometriosis. J Clin Ultrasound 41:69–75. doi:10.1002/ enema in patients with suspected intestinal endometriosis. J Am
jcu.22018 Assoc Gynecol Laparosc 11:223–228
52. Fedele L, Bianchi S, Portuese A, Borruto F, Dorta M (1998) 63. Faccioli N, Manfredi R, Mainardi P, Dalla Chiara E, Spoto E,
Transrectal ultrasonography in the assessment of rectovaginal Minelli L, Mucelli RP (2008) Barium enema evaluation of colonic
endometriosis. Obstet Gynecol 91:444–448 involvement in endometriosis. AJR Am J Roentgenol 190:1050–
53. Rossini LG, Ribeiro PA, Rodrigues FC, Filippi SS, Zago Rde R, 1054. doi:10.2214/ajr.07.3062
Schneider NC, Okawa L, Klug WA (2012) Transrectal ultra- 64. Yoon JH, Choi D, Jang KT, Kim CK, Kim H, Lee SJ, Chun HK,
sound—techniques and outcomes in the management of intestinal Lee WY, Yun SH (2010) Deep rectosigmoid endometriosis:
endometriosis. Endosc Ultrasound 1:23–35. doi:10.7178/eus.01. ‘‘mushroom cap’’ sign on T2-weighted MR imaging. Abdom
005 Imaging 35:726–731. doi:10.1007/s00261-010-9643-3
54. Griffiths A, Koutsouridou R, Vaughan S, Penketh R, Roberts SA, 65. Hottat N, Larrousse C, Anaf V, Noel JC, Matos C, Absil J, Metens
Torkington J (2008) Transrectal ultrasound and the diagnosis of T (2009) Endometriosis: contribution of 3.0-T pelvic MR imaging
rectovaginal endometriosis: a prospective observational study. Acta in preoperative assessment—initial results. Radiology 253:126–134.
Obstet Gynecol Scand 87:445–448. doi:10.1080/000163408019 doi:10.1148/radiol.2531082113
48318 66. Menni K, Facchetti L, Cabassa P (2016) Extragenital
55. Fedele L, Bianchi S, Raffaelli R, Portuese A (1997) Pre-operative endometriosis: assessment with MR imaging. A pictorial review. Br
assessment of bladder endometriosis. Hum Reprod 12:2519–2522 J Radiol 89:20150672. doi:10.1259/bjr.20150672
56. Pateman K, Holland TK, Knez J, Derdelis G, Cutner A, Saridogan 67. Coutinho A Jr, Bittencourt LK, Pires CE, Junqueira F, Lima CM,
E, Jurkovic D (2015) Should a detailed ultrasound examination of Coutinho E, Domingues MA, Domingues RC, Marchiori E (2011)
the complete urinary tract be routinely performed in women with MR imaging in deep pelvic endometriosis: a pictorial essay. Ra-
suspected pelvic endometriosis? Hum Reprod 30:2802–2807. diographics 31:549–567. doi:10.1148/rg.312105144
doi:10.1093/humrep/dev246 68. Loubeyre P, Petignat P, Jacob S, Egger JF, Dubuisson JB, Wenger
57. Savelli L, Manuzzi L, Pollastri P, Mabrouk M, Seracchioli R, JM (2009) Anatomic distribution of posterior deeply infiltrating
Venturoli S (2009) Diagnostic accuracy and potential limitations of endometriosis on MRI after vaginal and rectal gel opacification.
transvaginal sonography for bladder endometriosis. Ultrasound AJR Am J Roentgenol 192:1625–1631. doi:10.2214/AJR.08.1856
Obstet Gynecol 34:595–600. doi:10.1002/uog.7356 69. Kruger K, Behrendt K, Niedobitek-Kreuter G, Koltermann K,
58. Pateman K, Mavrelos D, Hoo WL, Holland T, Naftalin J, Jurkovic Ebert AD (2013) Location-dependent value of pelvic MRI in the
D (2013) Visualization of ureters on standard gynecological preoperative diagnosis of endometriosis. Eur J Obstet Gynecol
transvaginal scan: a feasibility study. Ultrasound Obstet Gynecol Reprod Biol 169:93–98. doi:10.1016/j.ejogrb.2013.02.007
41:696–701. doi:10.1002/uog.12468 70. Balleyguier C, Roupret M, Nguyen T, Kinkel K, Helenon O,
59. Faccioli N, Foti G, Manfredi R, Mainardi P, Spoto E, Ruffo G, Chapron C (2004) Ureteral endometriosis: the role of magnetic
Minelli L, Mucelli RP (2010) Evaluation of colonic involvement in resonance imaging. J Am Assoc Gynecol Laparosc 11:530–536
endometriosis: double-contrast barium enema versus magnetic 71. Corwin MT, Gerscovich EO, Lamba R, Wilson M, McGahan JP
resonance imaging. Abdom Imaging 35:414–421. doi:10.1007/ (2014) Differentiation of ovarian endometriomas from hemor-
s00261-009-9544-5 rhagic cysts at MR imaging: utility of the T2 dark spot sign. Ra-
60. Roman H, Carilho J, Da Costa C, De Vecchi C, Suaud O, Monroc diology 271:126–132. doi:10.1148/radiol.13131394
M, Hochain P, Vassilieff M, Savoye-Collet C, Saint-Ghislain M 72. Siegelman ES, Oliver ER (2012) MR imaging of endometriosis: ten
(2016) Computed tomography-based virtual colonoscopy in the imaging pearls. Radiographics 32:1675–1691. doi:10.1148/rg.326125518
assessment of bowel endometriosis: the surgeon’s point of view. 73. Kataoka ML, Togashi K, Yamaoka T, Koyama T, Ueda H, Ko-
Gynecol Obstet Fertil 44:3–10. doi:10.1016/j.gyobfe.2015.11.008 bayashi H, Rahman M, Higuchi T, Fujii S (2005) Posterior cul-de-
61. Iosca S, Lumia D, Bracchi E, Duka E, De Bon M, Lekaj M, Uc- sac obliteration associated with endometriosis: MR imaging eval-
cella S, Ghezzi F, Fugazzola C (2013) Multislice computed uation. Radiology 234:815–823. doi:10.1148/radiol.2343031366
tomography with colon water distension (MSCT-c) in the study of 74. Mussa FF, Younes Z, Tihan T, Lacy BE (2001) Anasarca and small
intestinal and ureteral endometriosis. Clin Imaging 37:1061–1068. bowel obstruction secondary to endometriosis. J Clin Gastroenterol
doi:10.1016/j.clinimag.2013.07.003 32:167–171

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