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Endometriosis
(E ndom etriomas t o D eep
Infiltrative Endometriosis)
Nicole Hindman, MDa,*, Wendaline VanBuren, MDb
KEYWORDS
Endometriosis Adenomyosis Endometrioma Deep infiltrating endometriosis
KEY POINTS
Endometriosis is a common disease.
In women of reproductive age with pelvic pain, dysmenorrhea, dyspareunia, or infertility, endome-
triosis as a cause should be considered.
Detection of endometriosis on imaging can be subtle; therefore, a targeted approach to imaging
evaluation is recommended.
Targeted ultrasound and MR imaging techniques are effective in the detection of endometriosis.
a
NYU Radiology, NYU School of Medicine, 550 First Avenue, New York, NY 10010, USA; b Mayo Clinic, 200 1st
Street Southwest, Rochester, MN 55905, USA
* Corresponding author.
E-mail address: Nicole.Hindman@nyulangone.org
accurately with imaging. Accurate imaging is These anatomic regions can be subdivided ac-
important for confirming the presence of disease cording to functional and clinical relevance into
and for guiding treatment decisions. anterior, middle, and posterior compartments.18
Treatment of endometriosis is complicated and The anterior compartment includes the insertion
includes conservative approaches combined with site of the ureters, the bladder, the vesicouterine
medical therapies or surgical intervention. The pouch, and the vesicovaginal pouch. The middle
treatment decisions are individualized and compartment contains the uterine body, fallopian
consider the patient’s clinical presentation, dura- tube, and uterine ligaments. The posterior
tion and type of symptoms, the disease extent, compartment contains the uterosacral ligaments,
and location as determined by imaging, the pa- rectovaginal septum, anterior rectal wall, and sig-
tient’s age, reproductive wishes, medication moid colon. A cartoon depiction of the regions
cost/side effects, and surgical cost/patient candi- typically involved by deep endometriosis is shown
dacy for surgery.8–10 The American Society for in Fig. 1. The corresponding normal anatomy for
Reproductive Medicine Practice Committee states the anterior compartment, middle compartment,
that "endometriosis should be viewed as a chronic and posterior compartments is shown for US
disease that requires a lifelong management plan (Fig. 2) and MR imaging (Fig. 3).
with the goal of maximizing the use of medical
treatment and avoiding repeated surgical proced-
Ultrasound
ures.”11 To that end, many patients are stratified
for medical treatment with or without surgical Transvaginal ultrasound (TVUS) is typically the
treatment based on the severity of the symptoms initial imaging evaluation performed in patients
or imaging findings and desire for child-bearing, with pelvic pain and infertility or when there is clin-
with first-line medical therapy typically including ical suspicion for endometriosis. This examination
nonsteroidal anti-inflammatory drugs and hormon- is very accessible compared with MR imaging, and
al (contraceptive) agents, with more severe symp- the sensitivity and specificity for detection of
toms being treated with gonadotropin-releasing ovarian endometriomas and lesions in the rectal
hormones and/or surgery (again, based on clinical wall are high. However, there is controversy in
symptoms, disease severity, and patient factors). the lack of reproducibility in the community of
The resection of endometriomas and endometri- the US technique described by specialized tertiary
otic implants at the time of surgery is important care centers, and the inability of nontertiary care
for symptom control and preservation of fertility.12 centers to reproduce the high sensitivity and spec-
Thorough preoperative planning is essential for ificity rates reported in the literature.
complete endometriosis excision. The best means of detection of deep endometri-
In this article, the authors review the optimal imag- osis on US require a more involved US protocol
ing protocols for US and MR imaging of suspected than that which is traditionally used for screening
endometriosis, review the compartmental approach TVUS. This “specialized endometriosis” US proto-
to dictating these examinations (with a focus on col involves techniques described by the Amer-
mapping of disease before surgical intervention), ican Institute of Ultrasound in Medicine (AIUM)19
discuss the diagnostic criteria (sensitivity and spec- and the International Deep Endometriosis Analysis
ificity of US and MR) for endometriosis detection by (IDEA) groups,20 including use of a targeted phys-
anatomic site, discuss the differential diagnosis, and ical examination before obtaining the images, the
review pearls and pitfalls in diagnosis and what the routine TVUS protocol combined with a dedicated
referring physician needs to know. targeted compartmental transvaginal sonogram
(described in Box 1), with attention primarily to
NORMAL ANATOMY AND IMAGING the posterior compartment (uterosacral ligaments,
TECHNIQUE rectovaginal septum, and rectum), with use of the
“sliding organ” maneuver21 to detect subtle adhe-
Endometriosis most commonly occurs in the sions (see Box 1), with additional more specialized
following locations in the pelvis: the ovaries, techniques also considered (tenderness-guided
uterus, fallopian tubes, uterosacral ligaments, transvaginal sonography; rectal-water transvagi-
broad ligaments, round ligaments, cul-de-sac, nal sonography). For detection of uterovesicular
bladder, ureters, rectovaginal septum, and recto- adhesions/implants, the sliding maneuver is as fol-
sigmoid colon.13–16 The frequency of endometri- lows: the transvaginal probe is placed in the ante-
otic implants in each of these locations, with the rior fornix and the uterus is moved between the
corresponding sensitivity and specificity of detec- probe and 1 hand of the operator that is placed
tion in these regions by specialized endometriosis over the suprapubic region. If the posterior bladder
US and MR, is listed in Table 1.14–17 slides freely over the anterior uterine wall, then the
Endometriosis 277
Table 1
Frequency of endometriosis by pelvic location at surgical laparoscopy, and corresponding sensitivity
and specificity of ultrasound and MR imaging for detection
Frequency Present
in This Location at Specialized
Laparoscopic Endometriosis
Location Evaluation, %13–15 US Detection24,48,49 MR Imaging Detection24,50,51
Retrocervical region/ 60–85 53%–64% sensitivity 86% sensitivity
uterosacral ligaments 93%–97% specificity 84% specificity
Uterus 40 n/a 86% sensitivity
84% specificity
Ovaries 20–40 83% sensitive 90% sensitive
89% specific 98% specific
Bladder 3–20 55% sensitivity 75%–87% sensitive
93.5% specificity 99%–100% specific
Rectosigmoid colon 9.9–37 90% sensitive 85%–91% sensitive
96% specific 72%–89% specific
Rectovaginal septum 11 81% sensitive 81% sensitive
95% specific 86% specific
Vagina 14.5–30 57% sensitive 77%–79% sensitive
99% specific 76%–93% specific
Round ligaments 0.3–14 n/a 20%–40% sensitive
30% specific
Ureters 0.01–1 Limited data: 83% sensitive
92% sensitivity 98.6% specific
100% specificity
Fig. 2. Normal pelvic compartments on transabdominal pelvic sonogram. Transabdominal sonographic images of
a normal pelvis in transverse (A) and long (B). Corresponding images in the same planes in transverse (C) and
long, (D) with color coding of the 3 compartments (blue 5 anterior compartment; orange 5 middle compart-
ment; and red 5 posterior compartment).
to be multilocular (in up to 50%) and bilateral (up to may not be seen, and instead, homogeneous
50%)31 (Fig. 5). However, endometriomas may low-level echoes mimicking that of an endome-
have a variable appearance because of the range trioma may be present. Hemorrhagic cysts are un-
of appearance of the internal blood products within likely to have the peripheral echogenic foci
them, which can cause fluid-fluid levels, echogenic occasionally seen in endometriomas, and they
regions, or a solid appearance.32 In these cases, are less likely to be bilateral or multifocal. Sono-
additional evaluation with MR imaging may be war- graphic follow-up demonstrating resolution at 6
ranted to better evaluate and to exclude to 12 weeks is diagnostic of a hemorrhagic cyst.
malignancy. Another differential diagnosis of an endome-
The primary differential diagnosis of an endome- trioma is an ovarian epithelial neoplasm, which
trioma is a hemorrhagic cyst, which is a common may contain low-level internal homogeneous
cause of pelvic pain (thought to occur from hemor- echoes similar to an endometrioma. This imaging
rhage into a corpus luteum cyst or follicular cyst). appearance was seen in up to 6% of ovarian se-
On US, a hemorrhagic cyst classically has internal rous cystadenomas in the study by Patel and col-
reticular strands with retractile clot; the combina- leagues31 and in up to 20% of mucinous
tion of such features is associated with a likelihood cystadenomas in the study by Van Holsbeke.33
ratio greater than 67.31 However, these features To better evaluate for the presence of malignancy
280 Hindman & VanBuren
Fig. 3. Normal pelvic compartments on the female pelvis MR. Normal axial (A) and sagittal (B) T2-weighted im-
ages of the pelvis are shown. Corresponding images in the same planes of axial (C) sagittal (D) with color coding
of the 3 compartments (blue 5 anterior compartment, orange 5 middle compartment, and red 5 posterior
compartment).
Box 1
Specialized endometriosis ultrasound protocol
1. Before the ultrasound, a targeted physical examination should be performed by the physician (radi-
ologist or gynecologist) reporting fixation of uterus, cervical/vaginal tenderness, visible endometri-
osis implants.
2. Standard ultrasound Transabdominal/Transvaginal pelvic examination (as described by the Practice
Parameter of the AIUM). This includes measuring in 2 tangential planes and documenting the
following: (1) the uterus (including uterine size, shape, and orientation; the endometrium; the my-
ometrium; and the cervix); (2) the adnexa (ovaries and fallopian tubes); and (3) the cul-de-sac
(including attempts to evaluate bowel posterior to the uterus).
a. This is considered “Step 1” of the ultrasound evaluation, looking for signs of adenomyosis or
ovarian endometriomas.
3. Targeted compartmental sonographic evaluation as described by the IDEA group, evaluating the
anterior, middle, and posterior compartments. For this component of the evaluation (steps 2–4 of
the evaluation), the following are required:
a. Step 2 is the evaluation of transvaginal “soft markers” (ie, site-specific tenderness and ovarian
mobility).
b. Step 3 is the evaluation of the pouch of Douglas using the ultrasound “sliding sign.”
c. Step 4 is the assessment for deep infiltrating endometriosis nodules in the anterior and posterior
compartments.
4. Optional: Tenderness guided transvaginal sonography:
A. Evaluation of the cul-de-sac, bowel wall, and rectovaginal septum while gently palpating with the
probe to elicit the areas of tenderness.
B. This technique involves incremental evaluation of the pelvis, beginning with the ovary, moving
posteriorly toward the cul-de-sac slowly, while palpating and evaluating regions of discomfort.
In the medial region, the uterosacral ligaments are assessed, and the posterior cervical lip and rec-
tovaginal septum are evaluated, along with the rectum, and the posterior cervix. The cervix
should be moved slightly with the probe, while observing the movement of the cervix and uterus
with the operator’s hand. Fixated movement will suggest adhesions. The bowel should be
observed for peristalsis (any regions without peristalsis will suggest implants in those regions).
Data from Guerriero S, Condous G, van den Bosch T, et al. Systematic approach to sonographic evaluation of the pelvis
in women with suspected endometriosis, including terms, definitions and measurements: a consensus opinion from
the International Deep Endometriosis Analysis (IDEA) group. Ultrasound Obstet Gynecol 2016;48(3):318-32; and Bena-
cerraf BR, Groszmann Y. Sonography should be the first imaging examination done to evaluate patients with sus-
pected endometriosis. J Ultrasound Med 2012;31(4):651–3.
Box 2
Diagnostic criteria for endometriosis on
ultrasound and MR imaging
US:
Endometrioma:
Cyst with homogeneous internal low-level
echoes
Cyst with peripheral echogenic foci
Multilocular (with above features)
Bilateral (with above features)
Hematosalpinx:
Fig. 4. A 31-year-old woman with pelvic pain and
Extraovarian tubular structure with internal infertility. Transvaginal sonogram in the region of
low-level echoes the right adnexa demonstrates a right ovarian cyst
Extraovarian tubular structure with incom- containing uniform low-level echoes (arrow) with
plete septations (“cog-wheel” appearance) increased posterior through transmission, and no in-
ternal vascularity, consistent with an ovarian
Deep infiltrating endometriosis endometrioma.
Hypoechoic nodular regions internal hyper-
echoic foci or complex cystic areas
pain within the palpable abnormality suggests the
Infiltrating hypoechoic tissue internal hy- diagnosis of an endometrioma. MR may be helpful
perechoic foci or complex cystic areas
for presurgical planning, because both smooth
MR imaging: muscle tumors and abdominal wall endometrio-
Endometrioma: mas are surgically resected; however, the
approach is different (there is a tissue-sparing
Cyst with uniformly high signal on T1- conservative approach for endometriomas, vs
weighted image (T1WI), with corresponding the need for wide negative margins for desmoid
uniformly low signal on T2-weighted image
tumors).
(T2WI; “shading sign” of Togashi)
Cyst with peripheral T2 dark spot
MR
Hematosalpinx: MR Appearance of Endometriomas
Extraovarian tubular structure with internal The MR appearance of endometriomas is classically
high signal on T1WI low signal on T2WI described as uniformly high signal on T1-weighted
Extraovarian tubular structure with incom- images with uniform low signal on T2-weighted im-
plete septations with high signal on TIWI ages, a phenomenon termed “shading” by Togashi
Deep infiltrating endometriosis and colleagues38 in 1991 (Fig. 8). Of 354 pathologi-
cally confirmed lesions, the overall diagnostic sensi-
Ill-defined nodular regions, low signal on
tivity, specificity, and accuracy of the shading sign
T2W1 (usually without high signal on T1WI,
but may occasionally have foci of internal for differentiating endometriomas from other gyne-
high signal on T1WI) cologic lesions were 90%, 98%, and 96%, respec-
tively.38 Since that time, Corwin and colleagues39
Infiltrating retractile regions, low signal on
evaluated a dataset of 74 lesions and found that
T2WI (usually without high signal on T1WI,
but may occasionally have foci of internal the T2 shading sign of Togashi had a sensitivity,
high signal on T1WI) specificity, and positive predictive value of 93%,
45%, and 72%. Corwin and colleagues39 postulated
that the difference in specificity between the 2
studies (in terms of the T2 shading sign) may be a
stimulation of the endometrial glands during the reflection of the different echo time (TE) of the T2-
menstrual cycle. weighted imaging sequences. The Togashi paper
The differential for the sonographic finding of an had an average TE of 60 to 80 milliseconds, but
irregular palpable mass in the abdominal wall is the Corwin paper had an average TE of 95 millisec-
broad and includes smooth muscle tumors of the onds, thus making the study by Corwin and col-
anterior abdominal wall (desmoid tumors and leagues39 more sensitive to a small amount of
fibrous tumors). Typically, the presence of cyclical blood products, but less specific. The Corwin paper
284 Hindman & VanBuren
proposed a new “T2 dark spot sign,” defined as hematosalpinx is seen in isolation, it is suggestive
discrete, markedly hypointense foci within the cyst of endometriosis.41,42 However, in up to 60% of
on T2-weighted images with or without T2 shading, patients with endometriosis with a dilated fallopian
which had a sensitivity of 36%, specificity of 93%, tube seen at the time of surgery, imaging does not
and positive predictive value of 89% for the diag- show internal high signal on T1-weighted im-
nosis of endometrioma as opposed to a hemorrhag- ages.41 In addition, it is atypical to see T2 shading
ic cyst (Fig. 9). within the lumen of the distended fallopian tube
As described above under the Ultrasound sec- even when there is high signal on T1-weighted im-
tion, the primary differential diagnosis of an endo- ages.42 T2 shading is not seen because of the fact
metrioma is a hemorrhagic cyst. Use of the that the endometriotic implants are mostly along
aforementioned T2 shading sign and T2 dark spot the surface of the tube and not within the lumen
sign is associated with a good sensitivity and excel- of the tube, such that the chronic bleeding within
lent specificity for the diagnosis of an endome- the implants leads to adhesions along the tubal
trioma. Other diagnostic considerations include a surface, but not within the lumen.
mature cystic teratoma/dermoid cyst. On MR imag- The differential diagnosis of a hematosalpinx on
ing, a mature cystic teratoma will be high signal on MR imaging is the same as that described above
T1-weighted images without fat saturation (similar under hematosalpinx on US and again includes
to an endometrioma), but unlike an endometrioma, PID or fallopian tube malignancies. Pyosalpinx of
the cystic teratoma will follow the signal of bulk fat PID can be differentiated by the clinical signs of
on every sequence. Thus, on a T1-weighted fre- infection (fever, white count). On MR imaging, hy-
quency selective fat-saturation sequence, the peremia surrounding the fallopian tube with
mature cystic teratoma will be low in signal, whereas stranding in the adjacent fat would suggest a pyo-
an endometrioma will have high signal. salpinx. Fallopian tube carcinoma demonstrates
solid, enhancing internal nodules within the fallo-
pian tube and tends to occur in an older demo-
MR Appearance of Hematosalpinx graphic group.32
Thirty percent of women with endometriosis have
tubal involvement at the time of operative explora-
MR Appearance of Deep Infiltrating
tion.36,40 On MR imaging, hematosalpinx mani-
Endometriosis
fests as a distended tubular structure adjacent to
the ovary demonstrating internal high signal on DIE is defined as a solid endometriotic implant
T1-weighted images (40% of distended tubes in more than 5 mm deep to the peritoneum. Typical
endometriosis have hyperintense contents).41 If a locations include the rectovaginal septum,
Fig. 8. A 30-year-old woman with tricompartmental deep endometriosis. A 30-year-old G0 woman with 2 years’
constant right pelvic pain and deep dyspareunia. Sagittal T2 (A) and axial T1-weighted with fat saturation (B) and
coronal T2 (C). MR imaging shows fibrotic tethering of large right endometrioma (arrowhead in A, B, and D) and
rectosigmoid colon (regular arrow in A, B, and C) deep infiltrative endometriosis to the posterior uterine body
with punctate T1 hyperintense endometriotic implants on the uterine serosa (thin arrow). Intraoperative corre-
lation shows the right ovarian endometrioma (arrowhead in D) and the endometriosis bulging into the rectal
lumen (arrow in E).
286 Hindman & VanBuren
endometriosis. The uterosacral ligaments are the regions will demonstrate progressive enhance-
most commonly involved region of DIE and can ment postcontrast. The presence of internal
be seen as thickened regions of low signal on foci of high signal on T2-weighted images is
T2-weighted images. The rectosigmoid colon is nearly pathognomonic. The differential diagnosis
the most commonly involved intestinal segment of a spiculated enhancing mass in the anterior
(see Fig. 8). This area of the colon needs to be abdominal wall includes smooth muscle tumors
carefully evaluated for length and depth of inva- of the anterior abdominal wall (desmoid tumors
sion by DIE. If the muscularis propria is involved and fibrous tumors). The imaging features (inter-
(seen on imaging as luminal invasion), then pa- nal foci of high signal on T1, low signal on T2, in-
tients may benefit from segmental or partial (sa- ternal cystic foci) combined with the typical
line-lift procedure) resection of the involved symptoms of cyclical pain allow the diagnosis
segment of bowel, and a colorectal surgeon of an abdominal wall endometrioma to be
should be consulted preoperatively with appro- made preoperatively most of the time.
priate consent obtained from the patient.
Bladder involvement typically presents with DIFFERENTIAL DIAGNOSIS
dysuria and less commonly with cyclical hematu- Pearls/Pitfalls/Variants
ria. On MR imaging, bladder involvement by
endometriosis presents with a focus of low signal Pearls
on T2-weighted images, often with internal high T1 bright adnexal lesions may be endometrio-
signal on T2-weighted images, corresponding mas, look for the associated (see Box 2):
to ectopic endometrial glands (Fig. 10). T1- T2 shading sign of ovarian endometrioma
weighted imaging is variable, occasionally T2 dark spot sign of ovarian endometrioma
demonstrating foci of high signal.42 The round Hematosalpinx is specific for endometriosis
ligaments may be involved by endometriosis,
with prevalence of disease involvement of up to Complications/pitfalls
14%13–15 (Fig. 11). The appearance of round lig-
ament involvement on MR imaging is T2 hypoin- Rupture
tense thickening or nodularity with enhancement Infection
postcontrast. Malignant transformation
Abdominal wall endometriosis can occur in pa- Intraluminal (rectal) invasion
tients because of direct implantation of endome- Missing subtle disease
trial glands and stroma during cesarean section Undercalling frozen pelvis
or laparoscopic intervention, with the reported Peritoneal carcinomatosis of another primary
incidence after cesarean section as high as Crohn disease
0.3% and 15%.22 Seventy percent of patients Decidualized endometriosis of pregnancy
with abdominal wall endometriomas have Variants
cyclical pain associated with the patient’s men-
strual cycle; however, the pain may be constant. Abdominal wall endometriosis
On MR imaging, these masses demonstrate var- Perineal endometriosis
iable signal on T1-weighted images (sometimes Ureteral endometriosis
high signal on T1-weighted images is seen, but Diaphragmatic endometriosis
often not), with typically low signal on T2- Appendiceal endometriosis
weighted images, with or without internal foci Invasive endometriosis of the posterior uterine
of high signal on T2-weighted images. These wall
Endometriosis 287
Fig. 10. Bladder wall endometriosis. A 36-year-old woman with cyclical pelvic pain and frequent urinary tract in-
fections. Coronal T2- (A) and axial T1-weighted MR imaging with fat saturation (B) shows bladder invasive endo-
metriosis with T1 and T2 hyperintense glandular foci (arrow in A and B). Image (C) during cystoscopy
demonstrates a submucosal bladder lesion (star) with pathology demonstrating deep endometriosis of the
bladder wall.
Fig. 11. Stage 4 endometriosis on MR imaging. A 38-year-old woman with menorrhagia. Stage 4 endometriosis
with “kissing ovaries” morphology and obliteration of the posterior cul-de-sac by bowel invasive endometriosis.
Coronal (A) and axial (C) T2-weighted MR images show the hypointense fibrotic retraction of both ovaries and
the rectum to the posterior uterus (arrow in C). Thickening of the right round ligament is also seen just anterior
to the right ovary (C, D). Postcontrast T1-weighted images with fat saturation (B) show invasion of the rectum by
the endometriosis (arrow in A and B). Axial T1-weighted imaging with fat saturation (D) shows bilateral T1 hyper-
intense hemorrhagic ovarian endometriomas and ovarian (white arrowhead) and serosal implants (thin arrow).
Intraoperative image (E) shows obliteration of the posterior cul-de-sac by the extensive deep endometriosis.
288 Hindman & VanBuren
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