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A Radiologist's Opint of View Darvishzadeh2016
A Radiologist's Opint of View Darvishzadeh2016
Radiology
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
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
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