endometriose

ª Springer Science+Business Media New York 2016
Abdominal
Radiology
Abdom Radiol (2016)
DOI: 10.1007/s00261-016-0956-8
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
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
2
Abstract
While endometriosis typically affects the ovaries, deep
infiltrating endometriosis can affect the gastrointestinal
tract, urinary tract, and deep pelvis, awareness of which
is important for radiologists. Symptoms are nonspecific
and can range from chronic abdominal and deep pelvic
pain to nausea, vomiting, diarrhea, constipation, hematuria, and rectal bleeding. Ultrasound and computed
tomography may show nonspecific soft-tissue density
masses causing bowel obstruction and hydronephrosis.
This constellation of presenting symptoms and imaging
evidence is easily mistaken for other pathologies including infectious gastroenteritis, diverticulitis, appendicitis,
and malignancy, which may lead to unnecessary surgery
or mismanagement. With this, deep pelvic endometriosis
should be considered in the differential diagnosis in a
female patient of reproductive age who presents with
such atypical symptoms, and further work up with
magnetic resonance imaging is imperative for accurate
diagnosis, treatment selection, and preoperative planning.
Key words: Endometriosis—Deep infiltrating
endometriosis—Gastrointestinal tract—Pelvis—Cul-desac—Ultrasound—Magnetic resonance imaging
(MRI)—Computed tomography (CT)
Endometriosis was first reported by Rokitansky in 1860
and affects 1–7% of women, including 6–10% of preCorrespondence to: Ayeh Darvishzadeh; email: [email protected]
menopausal women and 2.5% of postmenopausal women
[1–3] with an average age of diagnosis usually between
25- and 29-year old, increasing with age. Risk factors
include prolonged use of an intrauterine device, uninterrupted menstrual cycles, and a history of a first-degree
relative with endometriosis [4]. The incidence of
endometriosis increases to 17% in women with infertility
and to 50% of women who complain of pelvic pain [5, 6].
Typically, endometriosis implants in the ovaries and
uterosacral ligaments with the classic clinical presentation being a female of reproductive age with cyclical
pelvic pain with menstruation and dyspareunia [7].
Endometriosis, however, can affect other areas including
the pericardium, lungs, and the peritoneum. Roughly
5–15% of endometriosis affects the gastrointestinal tract
[5, 8]. Most commonly, gastrointestinal endometriosis
involves the rectosigmoid colon, followed by the sigmoid
colon, rectum, ileum, appendix, and cecum; this is often
but not always present in conjunction with pelvic
endometriosis.
Deep infiltrating endometriosis (DIE) is defined as
subperitoneal endometrial implants, greater than 5 mm
in depth affecting the gastrointestinal tract, urinary tract,
and pelvic cul-de-sac and is usually associated with
reactive inflammation, fibrosis, adhesions, and smooth
muscle hyperplasia (Fig. 1). Gastrointestinal DIE typically 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 involve the uterosacral ligaments, vagina, and cervix. Patients with endometriosis usually present with chronic,
nonspecific symptoms including nausea, vomiting, diarrhea, constipation, rectal bleeding, dyschezia, deep dys-
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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.
Fig. 1. Schematic of the female reproductive system and
pelvis illustrating typical locations of deep infiltrating
endometriosis. A Uterus and associated structures and colon.
B Sagittal view of the pelvis.
pareunia, and even crippling, chronic pelvic pain [9, 10].
Roughly 27% of intestinal endometriosis results in bowel
obstruction and can necessitate emergency surgery [11,
12].
Since symptoms tend to be nonspecific, the estimated
delay in diagnosis is between 3 and 9 years and is greater
in patients whose primary complaint is pelvic pain as
opposed to those reporting infertility [12, 13]. Furthermore, physical exam is usually insensitive to detect
endometriosis [14] with highly variable findings on exam
depending on size and location of ectopic tissue and
clinical experience of examiners. The most common
clinical findings include palpable nodules at the uterosacral ligament, rectovaginal space, Pouch of Douglas,
rectosigmoid, and posterior wall of the urinary bladder
[15]. However, the diagnostic value of a physical examination is limited by the inability of an examiner to
palpate deep enough into the pelvis, specifically in the
rectosigmoid space. Subsequent delayed diagnosis is
costly, with an estimated cost of $12,419 per woman per
year due to health care costs and loss of productivity [16,
17]. Delay in diagnosis leads to more progressive disease,
which increases the risk of organ damage and greater
need for invasive surgical intervention [15].
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Fig. 3. An asymptomatic 44-year-old woman with a significant family history of colon cancer who on screening colonoscopy was found to have a mass in the sigmoid colon that did
not penetrate through the mucosa. Differential diagnosis at time
of surgery was gastrointestinal stromal tumor, leiomyoma, or
endometriosis. A, B Coronal and axial contrast-enhanced CT
images show a subtle, soft-tissue density thickening in the
sigmoid colon (arrows). Inlet image is zoomed in image of
coronal CT showing circumscribed mass in colon with hyper-
attenuation at mass borders and heterogenous soft-tissue
density body. C Specimen of resected sigmoid colon showing
intramural mass protruding into the sigmoid. D–F Pathology
images of mass shown in C. D Low-power image of histological,
showing colonic mucosa (arrow) with areas of hypertrophic
muscularis propria and endometriosis (asterisk). E High-power
images of benign endometrial gland and endometrial stroma.
F High-power image of endometrial gland and stroma stained
positive with estrogen-receptor immunostaining (brown).
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Fig. 4. 40-year-old female with rectal pain and hematuria. A,
B Transvaginal ultrasound imaging showing a hypoechoic
mass between the urinary bladder and anterior uterus rectum.
C, D Axial and sagittal contrast-enhanced CT images showing
a mildly enhancing mass in between the urinary bladder and
anterior uterus (asterik).
Typically, patients with endometriosis are often
diagnosed with pelvic inflammatory disease, irritable bowel syndrome, Crohn disease, infectious colitis,
diverticulitis, appendicitis, and malignancy [13].
Small, scattered deep endometrial foci can be
especially difficult to detect with computed tomography
(CT) and magnetic resonance imaging (MRI) secondary to limiting in spatial resolution. Recent developments in soft-tissue characterization on MRI,
however, allow for excellent preoperative assessment of
DIE. Laparoscopic surgery with histological confirma-
tion remains the gold standard diagnostic method to
date. However, unanticipated intraoperative biopsies
showing endometriosis often result in a second surgery
after reassessment and proper bowel preparation [18].
Given this, diagnosis of endometriosis involving the
colon and pelvis is important to allow for preoperative
planning, which may include a general surgeon or
urologist.
The objective of this article is to review and discuss
the symptoms and imaging of deep pelvic endometriosis
of the gastrointestinal and urinary tract in order to
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Fig. 5. 41-year-old female presented to the Emergency
Department with severe deep pelvic pain. A–C Axial CT
images with enteral contrast showed a lobulated soft-tissue
density mass causing extrinsic compression and severe
luminal narrowing at the rectosigmoid junction. Imaging find-
ings on CT raised concern for a colorectal neoplasm. D Single-contrast barium enema shows a 7 cm stricture with
serrated appearance and mucosal crenation at the rectosigmoid junction. Subsequent pathology revealed rectosigmoid
endometriosis.
familiarize clinicians with the typical and atypical appearance of suspected DIE on various imaging modalities.
depth. Understanding the imaging of deep infiltrating
endometriosis relies on some factors of its pathophysiology. DIE is associated with reactive inflammation of
the surrounding area, including proliferation of smooth
muscle cells, fibrosis, and adhesions [19]. Endometriotic
implants may also include small, interspersed hemorrhagic foci.
Clinical features and pathophysiology
Deep infiltrating endometriosis consists of subperitoneal
endometrial implants that are greater than 5 mm in
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Fig. 6. 33-year-old female with a 3-year history of severe
pelvic and abdominal pain, constipation, and catamenial rectal bleeding. A Transvaginal ultrasound images of adenomyosis showing cystic anechoic spaces throughout the
myometrium that show low velocity flow with Doppler sonog-
raphy. B, C Axial and coronal contrast-enhanced CT images
show circumscribed broad-based soft-tissue density thickening at the sigmoid colon (arrows). D High-power pathology
section showing endometrial glands and stroma infiltrating the
submucosal and muscularis propria.
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Fig. 7. 34-year-old female presenting with severe right lower
quadrant pain and mild rectal bleeding. A Coronal contrastenhanced CT image of the abdomen and pelvis showing a
hypodense mass at the cecal base and appendix (asterix).
B Delayed urographic phase CT image of the abdomen and
pelvis showing right hydronephrosis and extrinsic ureteral
involvement at the middle right ureter. C Magnetic resonance
urogram and D retrograde right ureteral injection showing mild
hydronephrosis and extrinsic compression and narrowing of the
right ureter at the upper pelvis (blue arrows) E, F Axial contrastenhanced CT images showing dilation of the right ureter
proximal to external compression at the area of endometriosis.
G Final specimen of the appendix showing endometrial
glands and stroma in the lumen of the appendix (asterix).
Final diagnosis was endometriosis of the appendix and right
ureter.
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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 ultrasound 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 lowlying cecum that is positioned medially within the mid-pelvis
with an ill-defined soft-tissue density mass with scattered lowattenuation 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 inflammatory bowel disease or subclinical appendicitis. F Final
pathology confirms endometriosis with histology showing
endometrial glands and stroma in the colonic mucosa (dashed 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 quadrant abdominal pain showing heterogeneous soft-tissue density mass in the cecum (straight arrow). Circumscribed areas
of hypoattenuation suggestive of hemorrhagic foci (round
arrow). Differential diagnosis included acute appendicitis,
cecal malignancy, Crohn’s disease, enterocolitis, and ileocecal tuberculosis. Pathology confirmed cecal endometriosis.
Gastrointestinal tract
In the bowel, DIE implants at the antimesenteric edge of
the serosa and infiltrates through the muscularis propria
into the wall in a progressive manner [20]. Furthermore,
depending on the location of ectopic tissue and depth of
invasion, bowel endometriosis can present in various,
surprising ways. Superficial endometriosis involving only
the serosa can be asymptomatic. Classically, we would
expect patients with DIE to report pelvic pain that peaks
and troughs in a cyclical manner synchronized with the
proliferation and shedding of the ectopic endometrial
tissue with the menstrual cycle [21, 22]. However, patients report chronic deep pelvic pain nausea, vomiting,
diarrhea, constipation, reduced stool caliber, abdominal
bloating, and even ascites [11, 21–27]. Although DIE
rarely infiltrates through to the mucosa, patients may
also present with hematochezia, thought to occur when
swelling of underlying endometrial tissue causes colonic
mucosa to tear [20, 25]. Endometriosis of the appendix
can also occur and may present with profuse rectal
bleeding or mimic acute appendicitis, chronic appendicitis, or a peptic ulcer [28–32].
Patients who present with changes in bowel movements and abdominal pain often undergo colonoscopy
and CT for initial analysis, but the findings can mislead
physicians toward diagnoses of malignancy, inflammatory bowel disease (IBD), ischemic bowel, or chronic
enteritis. On endoscopy, deep endometriosis can present
with slight induration or hyperplastic surface epithelium
of the mucosa (Fig. 2), intramural masses protruding
into the colon causing extrinsic compression and luminal narrowing (Fig. 3), or as masses with central
ulceration and indurated, rolled borders that can mimic
carcinoma [19, 33]. On biopsy, mucosal changes include
distorted colonic glands, blunting of intestinal villi,
pyloric metaplasia, polypoid granulation tissue, and
deep fissures also found in IBD, ischemic bowel, and
chronic enteritis [19].
Urinary tract
Deep infiltrating endometriosis of the urinary tract most
commonly affects the bladder (15%) and the ureters
(4.5%), in women with severe endometriosis [34, 35].
Endometriosis of the bladder can present with hematuria, dysuria, urinary frequency, urinary tract infections, pelvic pain, constipation, diarrhea, and both
urgency or stress urinary incontinence [35–39]. Diagnosis
of bladder endometriosis is confounded by a clinical
presentation that is similar to urinary tract infections,
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overactive bladder syndrome, painful bladder syndrome,
and interstitial cystitis [40]. Bladder endometriosis may
also be associated with ovarian and rectosigmoid lesions,
with one study reporting co-existing disease in 49.2% and
28.9% of cases, respectively [38]. Ureteral endometriosis
typically implants on the external surface of the ureters
and causes external constriction of the ureteral wall,
leading to significant pathology such as progressive renal
function loss. Thus, diagnosing ureteral endometriosis is
critical to prevent kidney damage and significant
hydronephrosis but can be difficult due to either a
complete lack of or nonspecific symptoms. Unfortunately, 47% of patients with ureteral endometriosis require nephrectomy at the time of diagnosis [41].
Common presenting symptoms include dysuria, recurrent urinary tract infections, and hematuria [35]. Correlations between ureteral and rectovaginal endometriosis
and between ureteral and uterosacral ligament
endometriosis have also been reported and should be
considered with women who have evidence of either
other locations [34, 35].
Imaging modalities
Ultrasound
Gastrointestinal tract
Transvaginal ultrasound after bowel preparation
(TVUS-BP) remains the best initial imaging method for
endometriosis, since it can detect foci of deep
endometriosis including which layer of bowel has been
infiltrated, while also being low cost, vastly available,
and not exposing the patient to radiation [37, 42–46]. It
is, however, operator-dependent, time-consuming and
may miss or underestimate the extent of disease.
Improvements in patient preparation allow increased
visualization of the bowel for examination. These include
adequate bowel preparation to minimize fecal contents
and intestinal gas, placing ultrasound gel in the upper
third of the vagina to distend the vaginal dome, and
injecting ultrasound gel in the rectum gain a better view
of the bowel wall [37, 47]. Using TVUS-BP, bowel
endometriosis appears as an irregular hypoechoic mass
with or without hypoechoic or hyperechoic foci penetrating into the hypoechoic muscularis propria layer
wall. It may also show as long, nodular hypoechoic lesions along the intestinal wall [20, 42]. Submucosal lesions appear as hypoechoic gaps in the hyperechoic
submucosa. On color Doppler imaging, the masses show
no blood flow. A number of characteristic appearances
of endometriosis of the rectosigmoid area have been reported, including the ‘‘pyramid sign,’’ the ‘‘comet sign,’’
and the ‘‘Indian headdress sign’’ [48–50]. The lesions are
Fig. 10. 43-year-old female with history of endometriosis c
presenting with 3 months of right lower flank pain and
hematuria. A–C Axial contrast-enhanced images of the pelvis
showing a, irregular contour at the right bladder with a mildly
hyperdense mass extending into the vescicular space. B Delayed imaging showing intravenous-contrast filling the bladder
outlining the irregular mass and C post-contrast image
showing mild hyperattenuation of the mass with attenuation
again similar to myometrium. D Axial T1-weighted MRI image
showing the mass in the lower right bladder wall that appears
isointense to muscle with foci of hyperintensity indicative of
hemorrhagic cysts. E Axial T2-weighted MRI image showing
the mass is hypointense to muscle with hyperintense foci
again indicative of hemorrhagic products. F Final pathology of
the lesion in the bladder wall showing endometrial glands at
the level of the muscularis propria with E, estrogen-receptor
staining positive on immunohistochemistry.
described as pyramidal shaped and are attached to the
anterior rectal wall, pointing anteriorly toward the uterus
[48]. Furthermore, the margins are irregular and one end
appears thinner than the other, similar to a comet, and
thin band-like echoes that spread out from the center of
the mass have been described as like an ‘‘Indian head
dress’’ [49, 50]. Examiners can also look for pelvic
adhesions by assessing the movement of the uterus,
ovaries, and bowel loops with movement of the transducer [37]. TVUS-BP, however, is most useful when
detecting endometriosis of the bladder, rectum, and
rectovaginal septum, with limitations of examining the
proximal gastrointestinal tract [51].
Trans-rectal ultrasound (TRUS) has also shown high
sensitivity and specificity for detecting endometriosis of
the rectovaginal region [52]. Like with TVUS,
endometriosis of the rectosigmoid presents as irregular
hypoechoic masses on the intestinal wall, protruding
through the muscularis layer, and a characteristic ‘‘C’’
shape has been described that identifies the retraction of
the endometriotic nodule due to fibrosis and adhesions
[53]. TRUS is limited in which it cannot be used to assess
DIE of the anterior pelvic cul-de-sac, including the
uterovesical space and bladder, and may require the
patient to be sedated. However, it offers the benefits for
the examiner to perform a fine needle aspiration for
histological confirmation and is better able to determine
the extent of endometriosis infiltration into the intestinal
wall than TVUS [53, 54].
Urinary tract
Ultrasound is the initial imaging method of choice for
urinary tract endometriosis. TVUS the first line method
of diagnosing bladder endometriosis from which the size
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Fig. 11. ‘‘Mushroom cap sign’’ seen with a deep, infiltrating
deposit in the rectum (A sagittal T2, B sagittal T1 FS postgadolinium; C fluoroscopic barium enema with end-to-side
anastomosis; arrows). There is T2 hypointense, enhancing
fibrosis between the torus uterinus and the rectum (A, B; arrowheads), with obliteration of the rectocervical space (D axial
T1 FS postgadolinium; arrow).
of the lesions and infiltration into the detrusor muscle
can be assessed [51]. The endometrial lesions typically
appear as solid ‘‘comma-shaped’’ or spherical hypoe-
choic or isoechoic to the bladder wall masses with
numerous anechoic spaces within, described as ‘‘bubblelike’’ [55–57]. Color Doppler shows few vessels within the
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Fig. 12. 46-year-old female with obliterated anterior and
posterior cul-de-sac secondary to chronic fibrotic
endometriosis. A Sagittal T1FS post-gadolinium and B sagittal T2 imaging shows tethering to the urinary bladder (arrows).
C Sagittal T2 image shows tethering to the rectum (arrow).
D Axial T1 FS and E sagittal T2 images show bilateral ovarian
endometriomas which are T1 hyperintense (D, arrows) with
T2 shading with tethering to the uterine fundus (E, arrows)
creating a ‘‘kissing ovaries’’ appearance (F coronal T2,
arrow).
A. Darvishzadeh et al.: Deep pelvic endometriosis
Fig. 13. A nodular submucosal mass protrudes into the
urinary bladder with punctate foci of T1 hyperintense (A axial
T1 FS, arrow) and predominantly T2 hypointense (B axial T2,
arrow) signal. C Axial T1FS post-gadolinium shows mild
enhancement (arrow). D Cystoscopy with mild mucosal bulge
(arrow).
endometriotic implants [57]. They are typically found at
the posterior bladder wall and cause external compression into the bladder (Fig. 4A, B). TVUS is also used to
assess the ureters, both at rest, while peristalsing in order
to look for endometriosis, ureteral dilation, abnormal
bending, or evidence of obstruction [56, 58]. Ureteral
endometriosis appears as heterogeneous hypoechoic
nodules. Hydronephrosis can be visualized on renal
ultrasound and dilated ureters above the site of
endometriosis may be seen on pelvic or abdominal
ultrasound. These findings can mimic ureteral obstruction by cervical cancer [37].
plasms (Figs. 5, 6). Usually these patients do not undergo workup for DIE, instead undergo explorative
laparotomy or laparoscopy usually with inadequate
preoperative planning, preparation, and patient consent
prior to surgery. Understanding CT imaging of
endometriosis is essential for accurate diagnosis,
prompting appropriate further imaging to evaluate
locations and depth of other ectopic foci. Typically
endometriosis of the colon presents as a soft-tissue density intraluminal mass with mild to moderate contrast
enhancement and may cause eccentric stenosis of the
intestinal lumen. Furthermore, the intestinal wall in close
proximity to the nodule displays mural thickening and
scalloping. Bowel may be angulated or displaced from
the expected locations. Evaluation of cecal and appendiceal endometriosis can be further complicated due to
stenosis by muscular contraction, incomplete distention,
or presence of feces [59]. Due to these confounding factors, two of our cases of endometriosis were mistaken for
appendicitis, cecal malignancy, and inflammatory bowel
disease (Figs. 7, 8, 9). Notably, inflammatory changes of
the nearby bowel and mildly enhancing lymph nodes
may also appear on CT.
Computed tomography and fluoroscopy
Patients with endometriosis with clinical symptoms of
appendicitis, chronic pelvic pain, gastrointestinal symptoms of diarrhea, constipation and possibly reduced
stool caliber, or hematochezia often undergo CT imaging
for diagnosis. On contrast-enhanced CT imaging, DIE
typically appears as a soft-tissue density mass, indistinguishable from other gastrointestinal pathologies
including diverticulitis, and benign or malignant neo-
A. Darvishzadeh et al.: Deep pelvic endometriosis
Fig. 14. ‘‘Kissing ovaries’’ morphology with tethering to the
uterus. A Axial T2 image demonstrates ‘‘kissing ovaries’’
(arrow), the ‘‘dark spot sign’’ (arrowhead), and dark peripheral rind (double arrowhead). B Sagittal T1 FS image
demonstrates
bilateral
hyperintense
endometriomas
(arrows). C T2 hypointense tethering to the uterine serosa
(arrow). D Coronal T2 shows thickening of the uterosacral
ligaments (arrows).
Advancements in the use of CT for endometriosis
have been noted. Roman et al. created a virtual colonoscopy (CTC) that provides an accurate preoperative
roadmap of the length of the colon affected by DIE and
degree of stenosis when compared to magnetic resonance
imaging [60]. CT urography is useful for assessing ureteral involvement (Fig. 7). Iosca et al. report using
multislice CT with colon water distention (MSCT-c) and
intravenous injection of iodinated contrast medium to
identify endometriosis of the intestinal tract and the ureters [61]. On CT, endometriosis of the bladder can
present as an irregular, mildly enhancing mass in the
bladder wall with associated mural thickening (Figs. 4,
10). Furthermore, endometriosis of the ureters causes
fibrosis, leading to hydronephrosis, dilated ureters
proximal to location of implantation and can pull the
lower portion of the ureter medially from the lateral
position (Fig. 7B).
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Double-contrast barium enema (DCBE) is not currently recommended for the diagnosis of endometriosis
due to low specificity. Classically, however, it had been a
helpful method of imaging endometriosis of the gastrointestinal tract, specifically the rectosigmoid colon. On
DCBE, endometriosis appears with characteristic findings including strictures caused by extrinsic mass effect,
shortening, tethering, or flattening of the bowel wall.
Additionally, intramural endometriosis with subsequent
scalloping of antimesenteric border creates the characteristic crenulation pattern seen on DCBE, which may be
the only distinguishing finding (Fig. 5D) [9, 59, 62, 63].
Given that these findings, however, are nonspecific and
are similar to the findings of malignancy, the diagnostic
value of DCBE is limited.
In general, given that most patients are of reproductive age, the use of CT and fluoroscopy is limited by the
patient’s desire to forgo radiation exposure.
Magnetic resonance imaging
MRI is the imaging modality of choice for evaluation of
deep infiltrating endometriosis due to inherent high
sensitivity for detecting blood products and global evaluation of structures compared to the limited reach of
TVUS [59, 64]. Although not implemented at all institutions, MRI sensitivity can be improved by bowel
preparation, administration of an antispasmodic agent to
reduce bowel peristalsis, and administration of vaginal
gel [36]. Use of rectal gel is disputed since it can increase
bowel peristalsis and distort rectal retraction caused by
the endometriosis implants [37, 65]. The timing of MR is
also controversial, however, some authors suggest performing MR 12 days after the first day of the patient’s
last menstrual period when the endometrial blood
products are at their maximum [66]. Evaluation should
include investigation of the gastrointestinal tract and the
deep pelvis, typically based on a tri-compartmental approach, i.e., the anterior, middle, and posterior pelvic
compartments [67, 68].
DIE of the gastrointestinal tract appears as irregular,
eccentric mass/masses infiltrating into the intestinal wall
causing luminal narrowing with associated fibrosis and
smooth muscle hyperplasia appearing at times as irregular, speculated, hypointense lesions on T2-weighted
images. Fat-saturated T1-weighted images show a mass
or thickening, which is isointense to muscle, possibly
with interspersed hyperintense foci that reflect hemorrhagic blood products [37, 65, 66]. Restricted diffusion
with low apparent diffusion coefficient (ADC) values,
although not specific, is also noted [66]. The ‘‘mushroom
cap’’ sign refers to the appearance of rectosigmoidal le-
Fig. 15. 34-year-old female with tri-compartmental involve- c
ment. A axial T1 and B axial T2 images demonstrate an
obliterated posterior cul-de-sac with left ovarian endometrioma (T1 hyperintense, T2 hypointense; arrows). The uterus is
retroflexed and there is a ‘‘kissing ovaries’’ morphology (B).
C sagittal T2 image shows T2 hypointense fibrotic thickening
from the torus uterinus and lower uterine segment to the
rectum (arrows). D sagittal T1 FS shows left ovarian serosal
deposits (hyperintense foci; arrow). E axial T2 shows
involvement of the right distal ureter (hypointense thickening;
arrow). There is T2 thickening of the bilateral uterosacral
ligaments (F coronal T2; arrows) and round ligaments (G axial
T2; arrows). H Laparoscopy showing obliterated posterior culde-sac.
sions on T2-weighted images as a hypointense fibrotic
mass in the muscularis layer that protrudes into the
intestinal lumen with hyperintense submucosal and mucosal layers that cover the mass and create an outline
similar to that of a mushroom cap (Fig. 11) [64]. Other
findings include bowel wall thickening, loss of fat planes
between bowel segments and adjacent organs, and
abnormal angulation of the bowel loops [59, 69]. Increased spatial resolution with the use of a 3.0T MRI
compared to a 1.5T MRI allows for improved detection
of smaller DIE lesions and superficial endometriosis by
showing adhesions and peritoneal irregularities [65].
The anterior compartment includes the bladder, vesico-uterine pouch, vesico-vaginal septum, and distal
ureters. Superficial, serosal implants are typically T2
hypointense and result in ante-flexion and obliteration
of the anterior cul-de-sac (Fig. 12). Lesions that invade
through to the bladder mucosa may demonstrate more
typical T1 hyperintense and T2 hypointense glandular
elements [35, 70] (Figs. 10, 13). Given the rarity of
bladder mucosal invasion, these implants may be missed
at cystoscopy and the patient may be asymptomatic
[67]. MR urography and retrograde ureteral injection
are used to determine extent of ureteral involvement
(Fig. 7).
Middle compartment evaluation includes the uterus,
ovaries, fallopian tubes, and uterine ligaments. The hallmark findings of ovarian endometriomas are T1 hyperintense cysts that demonstrate T2 dark shading and a T2
dark rind due to the accumulation of degraded hemorrhagic blood products. More recently, however, the T2
‘‘dark spot sign’’ has proven to have greater specificity in
discerning endometriomas from other hemorrhagic cysts.
The T2 ‘‘dark spot sign’’ is characterized by discrete, circumscribed areas of increased hypointensity on T2
weighted images within the T2-shaded cyst or against the
cyst wall [71]. Tiny serosal deposits on the ovaries may
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43-year-old female with small bowel obstruction
and circumferential mass at the terminal ileum. A Coronal T2
and c axial T2 show a hypointense, circumferential mass
(arrows). B Coronal T1 FS post-gadolinium shows mass
enhancement (arrow). D B600 showing diffusion restriction
(arrow). E Colonoscopy with tight stricture at the terminal
ileum (arrow).
b Fig. 16.
have punctate areas of T1 hyperintensity with diffusion
restriction. Abutting, retro-positioned ovaries, secondary
to endometriotic adhesions, may create a ‘‘kissing ovaries’’
appearance. Thickening and nodularity of the broad and
round ligaments may also be present (Figs. 14, 15).
The posterior compartment may be significantly involved by deep invasive endometriosis. This compartment includes the rectum, Pouch of Douglas, torus
uterinus, uterosacral ligaments, posterior vaginal fornix,
and rectovaginal septum. Fibrotic changes are commonly seen in this area, manifest as predominantly T2
dark bands [72]. Retrocervical bands extending from the
torus uterinus, uterosacral ligaments, and rectum may
cause partial or complete obliteration of the cul-de-sac
[67]. Obliteration of the cul-de-sac may hide areas of
endometrial involvement on laparoscopic examination
and thus underestimate disease extent at surgery [73].
Serosal deposits involving the rectosigmoid colon may be
superficial, with potential for deeper invasion into the
muscularis propria. Despite the lack of mucosal invasion,
serosal involvement may result in colonic obstruction or
narrowing/stricture (Figs. 11, 15).
Other sites of involvement include the vagina, the
small intestine, the ischio-anal fossa, the sciatic nerve,
abdominal organs such as the liver, and extra-abdominal
locations such as the pleura (Fig. 16) [67]. MR urography and retrograde ureteral injection are used to determine extent of ureteral involvement (Fig. 7C, D).
Laparoscopy
Ultimately, laparoscopy or laparotomy with histological
confirmation of endometriosis remains the gold standard
for diagnosis. Typically, endometriosis is characterized
on laparoscopy as adhesions and serosal fibrosis with
patchy gray-brown discoloration, also called ‘‘powderburn’’ lesions. Macroscopically, the lesions are small
nodules of large cystic glands and endometrial type
stroma that appear on the peritoneal surface as raised,
punctate hemorrhagic areas with hemosiderin deposits,
whitish opacfications, or reddish-blue irregularly shaped
lesions [20, 74].
Summary
Endometriosis is a common disease affecting up to 50%
of women with pelvic pain and can present with a variety
of symptoms making diagnosis difficult. Patients may
suffer due to a delayed diagnosis, incurring health care
costs, and lost income due to decreased productivity with
a significant personal impact. The typical delay in diagnosis ranges from 3 to 9 years and may lead to progressive disease requiring surgical intervention [16, 17].
Thus, an early and precise diagnosis of DIE is ‘‘key.’’
Familiarity with the pathophysiology, clinical presentation, and the imaging features of DIE can aid in the
radiologic diagnosis and guide appropriate and timely
patient management.
Acknowledgements The authors acknowledge the assistance of Eric J.
Gray and Sonia Watson, Ph.D., for editing the manuscript and
Christopher M. Brown for illustration design.
Compliance with ethical standards
Funding No funding was received for this study.
Conflicts of interest The authors declare that they have no conflict of
interest.
Ethical approval All procedures performed in studies involving human
participants were in accordance with the ethical standards of the
institutional and/or national research committee and with the 1964
Helsinki declaration and its later amendments or comparable ethical
standards.
Informed consent Statement of informed consent was not applicable
since the manuscript does not contain any patient data.
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