You are on page 1of 15

I m a g i n g Sp e c t r u m of

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.

INTRODUCTION regions (cul-de-sac, rectovaginal space, uterine


body, and uterosacral ligaments). Laboratory tests
Endometriosis is a common, benign disorder are limited in the diagnosis of endometriosis (CA-
defined as the presence of endometrial tissue at 125 has a detection rate of only 54% in patients
extrauterine sites, typically involving the pelvis. The with severe endometriosis5 and is neither sensitive
cause and pathogenesis of endometriosis are nor specific for the diagnosis). The gold standard
incompletely understood and appear to be due to for diagnosis of endometriosis has traditionally
multifactorial causes, including the presence of been surgical visualization and biopsy; however,
ectopic endometrial tissue, altered immunity, dis- in recent years, diagnostic laparoscopy (surgery
rupted cell proliferation and apoptosis, and disor- performed in order to diagnose endometriosis,
dered endocrine signaling and genetics.1 The not to treat endometriosis) is becoming less com-
prevalence estimates of endometriosis vary, with mon at university hospitals.6 Replacement of diag-
1% of all women who undergo major gynecologic nostic laparoscopy by noninvasive imaging is due
surgery having evidence of endometriosis, and 9% to the improvement in diagnostic capability of pre-
to 50% of all women undergoing laparoscopy for operative imaging (typically ultrasound [US] and
infertility having evidence of endometriosis.2,3 It is MR imaging) for the detection of endometriosis.6
estimated that there is a 10% prevalence of endo- Endometriosis typically manifests in 3 ways:
metriosis in women of reproductive age.4 The ovarian endometriomas, superficial peritoneal im-
classic symptoms of endometriosis are dysmenor- plants, and deep infiltrating endometriosis (DIE).
rhea, pelvic pain, dyspareunia, and/or infertility. DIE is defined as a solid endometriotic implant
Typically, once endometriosis is clinically sus- more than 5 mm deep to the peritoneum.7 Both
pected, patients are evaluated on physical exami- ovarian endometriomas and DIE can be detected
radiologic.theclinics.com

nation for tenderness in commonly involved pelvic

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

Radiol Clin N Am 58 (2020) 275–289


https://doi.org/10.1016/j.rcl.2019.11.001
0033-8389/20/Ó 2019 Elsevier Inc. All rights reserved.
276 Hindman & VanBuren

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

Abbreviation: n/a, not applicable.

sliding sign is positive and the uterovesical region MR Imaging


is classified as nonobliterated. If the bladder does
MR imaging of the pelvis is frequently performed
not slide freely over the anterior uterine wall, then
for the detection of endometriosis, either as the
the sliding sign is negative and the uterovesical re-
second-line imaging examination (after US) for
gion is classified as obliterated.
the detection/confirmation of endometriosis or as
In specialized tertiary care centers where atten-
the initial examination in a patient for whom there
tion to this meticulous technique is followed, US
is a high clinical suspicion for endometriosis. MR
has the potential for high sensitivity and specificity
imaging can be performed with either a 1.5-T or
(as high as 95% sensitivity and 96%
3-T magnet, using a high-resolution phased-array
specificity)14,15,17,22,23 in detection of posterior
surface coil for improved resolution. There is no
compartment and bowel endometriosis (see Ta-
consensus regarding whether to perform the ex-
ble 1). Other techniques that have been suggested
amination around the timing of the patient’s men-
for improved sensitivity include using a transrectal
strual cycle.24 Fasting before the examination for
approach and/or a bowel preparation for better
4 hours is typically recommended in order to
visualization of the bowel wall as well as instillation
empty the upper gastrointestinal tract so that the
of extra gel in the vagina.21 Limitations of sono-
patient will not have material to vomit with supine
graphic technique, despite meticulous efforts,
positioning, with antiperistaltic administration, or
include anterior compartment detection of endo-
after intravenous (IV) contrast administration. The
metriosis (bladder and vesicouterine pouch detec-
bladder should be moderately full to improve
tion) and detection within the middle compartment
detection of implants in the anterior compartment.
(torus uterinus and round ligaments). However,
Some practices recommend a bowel enema to
because posterior compartment endometriosis is
clear out the colon; however, others have reported
the most frequently involved compartmental re-
equal sensitivity and specificity without an
gion by deep endometriosis, this modality, when
enema.24,25
performed with specialized endometriosis sono-
Patients are positioned supine on the scanner,
graphic technique, represents an effective
with abdominal strapping after phased coil array
screening examination in this population.
278 Hindman & VanBuren

shot TSE images is considered standard in addi-


tion to true T2 TSE-weighted images, particularly
because these allow for a larger field of view to
assess for ureteral endometriosis and hydroneph-
rosis in the kidneys. T1-weighted images without
and with fat suppression are standard, because
the fat suppression is useful for the detection of
subtle foci of hemorrhage, which may be obscured
on non–fat-saturated images. Dixon technique or
conventional in- and out-of-phase T1-weighted
images are useful for the differentiation of fat-
containing lesions, such as dermoid cysts from
endometriomas, both of which have high signal
on non–fat-saturated T1-weighted images. The
addition of diffusion-weighted images,
susceptibility-weighted images, and postcontrast
images is considered optional in the imaging for
endometriosis.25–28

Fig. 1. The regions of the normal female pelvis. IMAGING PROTOCOLS


Ovarian endometriomas are found in the ovaries. Imaging Findings/Pathology
Deep endometriosis can involve any region of the
pelvis. For functional and clinical relevance, the pelvis
The main different types of endometriotic lesions
can be artificially divided into the posterior, middle, are ovarian endometriomas, superficial peritoneal
and anterior compartments. The posterior compart- implants, and DIE (see Box 1 and Table 2).
ment includes the posterior cul-de-sac (Post CDS), Ovarian endometriomas occur when ectopic
which comprises the uterosacral ligaments (USL), rec- endometrial tissue in the ovary hemorrhages,
tovaginal septum (not shown), anterior rectal wall forms a hematoma, and is enveloped by ovarian
(not shown), and sigmoid colon (Sigmoid). In the mid- parenchyma.29 On gross pathology, endometrio-
dle compartment, deep endometriosis can involve the mas have thick fibrotic walls, associated with
uterine body (Uterus), fallopian tubes (FT), and uter- dense fibrotic adhesions with internal contents
ine ligaments; here the broad ligament is shown
containing thick chronic blood products (thus the
(BL). In the anterior compartment, deep endometri-
osis can involve the bladder (Bladder), vesicouterine
common pathologic term “chocolate cyst”).30 Su-
pouch/vesicovaginal pouch (depicted as the anterior perficial peritoneal implants of endometriosis are
cul-de-sac [Ant CDS]). SB, small bowel. (Used with “powder burn” regions (<5 mm deep) seen on lap-
permission of Mayo Foundation for Medical Educa- aroscopy that are below the resolution of US or
tion and Research, all rights reserved.) MR imaging. DIE is defined as a solid endometri-
otic implant more than 5 mm deep to the
peritoneum.7
placement. Antiperistaltic agents are generally rec-
ommended; however, the type of agent (oral agents,
DIAGNOSTIC CRITERIA
nonoral agents), dose, and route (intramuscular,
Ultrasound
subcutaneous, or IV) is debated; at New York Uni-
versity, the authors give 1 mg IV glucagon immedi- Sonographic appearance of endometriomas
ately before the acquisition of the 3-plane Ovarian endometriomas occur when ectopic endo-
T2-weighted images (because these are the most metrial tissue in the ovary hemorrhages, forms a he-
sensitive sequences for the detection of subtle matoma, and is enveloped by ovarian parenchyma
endometriosis, after which the glucagon often wears (Box 2). An ovarian endometrioma has different im-
off). The administration of vaginal (gel) and rectal aging appearances on US, with the classic appear-
contrast (gel or water) is optional; the authors have ance being a cyst containing homogeneous
the patient self-administer vaginal gel via a syringe uniform low-level echoes with increased posterior
on the table before placing the phased array coil. through transmission (Fig. 4). This finding has
For MR imaging sequences (Table 2), 3-plane 2- been described in as many as 95% of endometrio-
dimensional T2 turbo spin echo (TSE) -weighted mas and only 19% of nonendometriomas.31
images are standard for acquisition; 3-dimensional Another feature is the presence of peripheral echo-
T2-weighted images are considered optional genic foci (thought to reflect cholesterol deposits)
(because of their decreased contrast resolution). seen in up to 36% of endometriomas versus only
Half-Fourier acquisition in coronal plane single- 6% of nonendometriomas.31 Endometriomas tend
Endometriosis 279

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).

(cystadenocarcinomas) in these cases, careful The differential diagnosis of a hematosalpinx in-


interrogation of the cyst should be performed to cludes pelvic inflammatory disease (PID) or fallo-
assess for internal solid components, such as pian tube malignancies. Pyosalpinx of PID can
papillary projections, mural nodules, and thick- be differentiated clinically by the presence of
ened septations. Ultimately, MR imaging can be extreme tenderness on examination as well as
performed in equivocal cases. the clinical signs of infection (fever, white count).
On imaging, hyperemia surrounding the fallopian
Sonographic appearance of hematosalpinx tube with fatty proliferation/edema in the adjacent
Endometriosis involves the fallopian tubes up to fat suggests a pyosalpinx. Fallopian tube carci-
6% of the time in endometriosis, and noma presents sonographically with solid,
external adhesions from pelvic endometriosis vascular internal nodules within the fallopian tube
may also obstruct the fallopian tubes (up to and tends to occur in an older demographic
26% of the time).34 On US, hematosalpinx group.32
appears as an extraovarian tubular structure
with low-level internal echoes. A “cog-wheel” Sonographic appearance of deep infiltrating
appearance of the longitudinal folds can be endometriosis
seen when the tube is imaged in cross-section.35 Deep endometriosis on sonography is subtle and
The presence of a hematosalpinx may be the presents as hypoechoic nodular or infiltrating re-
only sign on imaging of endometriosis in the gions in classic locations in the pelvis (in the pos-
pelvis.36 terior compartment, uterosacral ligaments,
Endometriosis 281

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.

rectovaginal septum, rectosigmoid, or bladder) suspected, and additional evaluation with MR is


(Fig. 6). Occasionally, the infiltrative regions of recommended.
DIE may have internal hyperechoic foci or complex
internal cysts.21,37 Abdominal wall endometriosis
The differential diagnosis for DIE includes ma- Abdominal wall endometriosis typically occurs at
lignancy, particularly within the posterior the site of prior surgery or trauma in the abdominal
compartment, which is a common site for perito- wall. It can occur independently of the presence of
neal implants to distribute. To help differentiate endometriosis elsewhere in the body and is
endometriosis from malignant peritoneal disease, thought to occur secondary to direct implantation
the history is useful (malignancy is unlikely in a of endometrial cells into the abdominal wall during
young premenopausal patient without signs and surgery.37 This phenomenon has an incidence of
symptoms of bloating or weight loss), and the between 0.3% and 15% after cesarean section.22
presence of additional sites of endometriosis in On sonography, these typically palpable nodules
the pelvis (ovarian endometriomas) supports the have hypoechoic echotexture, irregular borders,
diagnosis of endometriosis.32 However, if the and increased vascularity, with or without internal
lesion is large, hypervascular, and there are no cysts (Fig. 7). Typically, patients present with
other sites of disease, malignancy should be cyclical pain in the nodule, corresponding to the
282
Hindman & VanBuren
Table 2
Endometriosis MR protocol at 3 T

Field of Repetition Echo B Value Contrast


Sequence Plane Slice Thickness, mm View, cm Matrix Time (ms) Time (ms) No. Averages (s/mm2) Delay
Patient self-administers 3  12-cc syringes; vaginal contrast (US gel)
Tru FISP T1/T2 3 plane 7-8 40 192  144 700 1.13 1
Scout Cor/Sag/Ax
Inject IV glucagon, do T2 sequences immediately after injection
T2 TSE T2 Sag 4 30–35 512  256 4870 102 2
(adjust
to body
habitus)
HASTE T2 Cor 5 320  256 Infinite 93 1
T2 TSE T2 Ax 4 448  291 5110 99 2
Diffusion T2 Ax 6 160  120 6600 70 2 b0, b50,
b100, b400,
b800
In/out T1 Ax 5 256  232 168 1.1/2.2 (3T) 1
Pre-VIBE T1 Sag 2.5 256  205 3 1.22 1
Pre-VIBE T1 Ax 3 256  179 2.6 1.05 1
Post-VIBE T1 Sag/Ax 2.5 256  205 3 1.22 1 30, 60, 180 s

The example given is for Siemens 3T Magnetom VIDA (Erlangen, Germany).


Abbreviations: Ax, axial; Cor, coronal; Sag, sagittal.
Endometriosis 283

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

Fig. 5. A 41-year-old woman with pel-


vic pain with US showing “kissing
ovaries.” Transvaginal sonogram in
an oblique plane through the pelvis
(A) demonstrates posterior displace-
ment of both ovaries behind the
uterus. The right ovary (labeled in B)
contains an endometrioma (blue),
which contacts the left ovary, which
also has an endometrioma (orange).
This configuration is termed “kissing
ovaries” and is consistent with
endometriosis.

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. 6. A 31-year-old woman with


rectovaginal endometriotic implant.
Transvaginal sonogram in the sagittal
plane centered on the cervix is shown
in (A), with the rectovaginal implant
(of the same image) demonstrated,
shaded in red in (B).
Endometriosis 285

uterosacral ligaments, rectosigmoid colon, uterine


body, round ligaments, bladder, and vagina. DIE
has a varied imaging appearance on MR imaging,
typically demonstrating low signal on T1-weighted
images with corresponding low signal on T2-
weighted images, with a spiculated, fibrotic
appearance. Preoperative imaging has tradition-
ally been performed with TVUS, which has an
excellent sensitivity and specificity for detection
of ovarian endometriomas, but a limited sensitivity
for detection of DIE,43 and has a high operator
variability. Older studies with MR imaging demon-
strated limited accuracy in detection of endometri-
osis; however, with advanced MR imaging
Fig. 7. A 40-year-old woman with a cesarean section techniques and increased awareness by radiolo-
scar endometrioma. A 40-year-old woman with gists of this entity, along with the superior repro-
cyclical pain of the anterior abdominal wall and a his- ducibility of MR imaging scans (as opposed to
tory of prior cesarean section. Axial transabdominal transvaginal sonography), newer studies have
sonogram demonstrates a hypoechoic to slightly isoe- demonstrated a high interobserver agreement for
choic mass of the anterior abdominal wall with low- MR imaging in detection of deep
level internal vascularity. This mass was excised and endometriosis.26,44–46
was consistent with endometriosis. Table 1 describes the frequency of involve-
ment of each region in the pelvis by

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

Fig. 9. T2 dark spot sign. A 35-year-


old woman with axial T1- (A)
weighted and axial T2- (B) weighted
images through the pelvis showing a
uniformly high signal (on T1-
weighted images, A) right ovarian
cyst, which demonstrates both uni-
form loss of signal on T2-weighted
images, consistent with shading as
well as a more focal T2 dark spot (ar-
row in B), consistent with an ovarian
endometrioma.

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.

WHAT THE REFERRING PHYSICIAN NEEDS TO  Endometriosis does not have


KNOW pathognomonic-associated symptoms or bio-
markers. Most patients who are sent for imag-
 Endometriosis is a common gynecologic con- ing present with chronic pelvic pain or
dition (estimated 10% prevalence in women infertility.47
of reproductive age).4

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

 Endometriosis is classified intraoperatively in 9. Schenken RS. Familial endometriosis. J Soc Gyne-


the 3 following ways: (1) a superficial perito- col Investig 2003;10(3):123.
neal lesion (occult on imaging), (2) an ovarian 10. Schenken RS. Delayed diagnosis of endometriosis.
endometrioma, or (3) deep endometriosis (en- Fertil Steril 2006;86(5):1305–6 [discussion: 1317].
dometriotic lesions extending >5 mm below 11. Practice Committee of the American Society for
the peritoneum). Knowledge of the extent of Reproductive Medicine. Treatment of pelvic pain
involvement of endometriosis in the pelvis is associated with endometriosis: a committee opinion.
useful in determining appropriate therapy.18 Fertil Steril 2014;101(4):927–35.
 Unless trained, many general radiologists do 12. de Ziegler D, Borghese B, Chapron C. Endometri-
not notice regions of deep endometriosis on osis and infertility: pathophysiology and manage-
pelvic MR imaging. If radiologists can detect ment. Lancet 2010;376(9742):730–8.
this disease, it helps clinicians to appropri- 13. Chamie LP, Blasbalg R, Pereira RM, et al. Findings
ately consider care options/fertility options of pelvic endometriosis at transvaginal US, MR im-
for the patient. aging, and laparoscopy. Radiographics 2011;
 Describing endometriosis in terms of its 31(4):E77–100.
compartment of involvement (anterior, mid- 14. Chapron C, Fauconnier A, Vieira M, et al. Anatomical
dle, and posterior) helps the operative sur- distribution of deeply infiltrating endometriosis: sur-
geon know the degree of dissection required gical implications and proposition for a classifica-
and the operative approach. tion. Hum Reprod 2003;18(1):157–61.
 US and MR imaging may underestimate dis- 15. Gui B, Valentini AL, Ninivaggi V, et al. Deep pelvic
ease extent of endometriosis. If there is 3- endometriosis: don’t forget round ligaments. Review
compartmental involvement on imaging, it of anatomy, clinical characteristics, and MR imaging
will likely correspond to a “frozen pelvis” for features. Abdom Imaging 2014;39(3):622–32.
the operative surgeon (ie, multiple adhesions 16. Foti PV, Farina R, Palmucci S, et al. Endometriosis:
between organs and/or bowel). clinical features, MR imaging findings and patho-
logic correlation. Insights Imaging 2018;9(2):
149–72.
DISCLOSURE 17. Chamie LP, Pereira RM, Zanatta A, et al. Transvagi-
nal US after bowel preparation for deeply infiltrating
No financial disclosures.
endometriosis: protocol, imaging appearances, and
laparoscopic correlation. Radiographics 2010;30(5):
1235–49.
REFERENCES
18. Coutinho A Jr, Bittencourt LK, Pires CE, et al. MR im-
1. Giudice LC. Clinical practice. Endometriosis. N Engl aging in deep pelvic endometriosis: a pictorial
J Med 2010;362(25):2389–98. essay. Radiographics 2011;31(2):549–67.
2. Chatman DL, Ward AB. Endometriosis in adoles- 19. American Institute of Ultrasound in Medicine (AIUM),
cents. J Reprod Med 1982;27(3):156–60. American College of Radiology (ACR), American
3. Sangi-Haghpeykar H, Poindexter AN 3rd. Epidemi- College of Obstetricians and Gynecologists
ology of endometriosis among parous women. Ob- (ACOG), Society for Pediatric Radiology (SPR), So-
stet Gynecol 1995;85(6):983–92. ciety of Radiologists in Ultrasound (SRU). AIUM
4. Bazot M, Bharwani N, Huchon C, et al. European So- practice guideline for the performance of ultrasound
ciety of Urogenital Radiology (ESUR) guidelines: MR of the female pelvis. J Ultrasound Med 2014;33(6):
imaging of pelvic endometriosis. Eur Radiol 2017; 1122–30.
27(7):2765–75. 20. Guerriero S, Condous G, van den Bosch T, et al.
5. Cheng YM, Wang ST, Chou CY. Serum CA-125 in Systematic approach to sonographic evaluation of
preoperative patients at high risk for endometriosis. the pelvis in women with suspected endometriosis,
Obstet Gynecol 2002;99(3):375–80. including terms, definitions and measurements: a
6. Menakaya UA, Rombauts L, Johnson NP. Diagnostic consensus opinion from the International Deep
laparoscopy in pre-surgical planning for higher Endometriosis Analysis (IDEA) group. Ultrasound
stage endometriosis: is it still relevant? Aust N Z J Obstet Gynecol 2016;48(3):318–32.
Obstet Gynaecol 2016;56(5):518–22. 21. Benacerraf BR, Groszmann Y. Sonography should
7. De Cicco C, Corona R, Schonman R, et al. Bowel be the first imaging examination done to evaluate
resection for deep endometriosis: a systematic re- patients with suspected endometriosis.
view. BJOG 2011;118(3):285–91. J Ultrasound Med 2012;31(4):651–3.
8. Schenken RS. Endometriosis classification for infer- 22. Bazot M, Lafont C, Rouzier R, et al. Diagnostic accu-
tility. Acta Obstet Gynecol Scand Suppl 1994;159: racy of physical examination, transvaginal sonogra-
41–4. phy, rectal endoscopic sonography, and magnetic
Endometriosis 289

resonance imaging to diagnose deep infiltrating 37. Chamie LP, Ribeiro D, Tiferes DA, et al. Atypical
endometriosis. Fertil Steril 2009;92(6):1825–33. sites of deeply infiltrative endometriosis: clinical
23. Chamie LP, Blasbalg R, Goncalves MO, et al. Accu- characteristics and imaging findings. Radiographics
racy of magnetic resonance imaging for diagnosis 2018;38(1):309–28.
and preoperative assessment of deeply infiltrating 38. Togashi K, Nishimura K, Kimura I, et al. Endometrial
endometriosis. Int J Gynaecol Obstet 2009;106(3): cysts: diagnosis with MR imaging. Radiology 1991;
198–201. 180(1):73–8.
24. Bazot M, Darai E. Diagnosis of deep endometriosis: 39. Corwin MT, Gerscovich EO, Lamba R, et al. Differen-
clinical examination, ultrasonography, magnetic tiation of ovarian endometriomas from hemorrhagic
resonance imaging, and other techniques. Fertil cysts at MR imaging: utility of the T2 dark spot
Steril 2017;108(6):886–94. sign. Radiology 2014;271(1):126–32.
25. Manganaro L, Vittori G, Vinci V, et al. Beyond lapa- 40. Kim MY, Rha SE, Oh SN, et al. MR imaging findings
roscopy: 3-T magnetic resonance imaging in the of hydrosalpinx: a comprehensive review. Radio-
evaluation of posterior cul-de-sac obliteration. graphics 2009;29(2):495–507.
Magn Reson Imaging 2012;30(10):1432–8. 41. Outwater EK, Siegelman ES, Chiowanich P, et al.
26. Bazot M, Darai E, Hourani R, et al. Deep pelvic Dilated fallopian tubes: MR imaging characteristics.
endometriosis: MR imaging for diagnosis and pre- Radiology 1998;208(2):463–9.
diction of extension of disease. Radiology 2004; 42. Siegelman ES, Oliver ER. MR imaging of endometri-
232(2):379–89. osis: ten imaging pearls. Radiographics 2012;32(6):
27. Bazot M, Gasner A, Ballester M, et al. Value of thin- 1675–91.
section oblique axial T2-weighted magnetic reso- 43. Savelli L, Manuzzi L, Pollastri P, et al. Diagnostic ac-
nance images to assess uterosacral ligament endo- curacy and potential limitations of transvaginal so-
metriosis. Hum Reprod 2011;26(2):346–53. nography for bladder endometriosis. Ultrasound
28. Bazot M, Gasner A, Lafont C, et al. Deep pelvic Obstet Gynecol 2009;34(5):595–600.
endometriosis: limited additional diagnostic value 44. Varol N, Maher P, Healey M, et al. Rectal surgery for
of postcontrast in comparison with conventional endometriosis–should we be aggressive? J Am As-
MR images. Eur J Radiol 2011;80(3):e331–9. soc Gynecol Laparosc 2003;10(2):182–9.
29. Brosens IA, Puttemans PJ, Deprest J. The endo- 45. Bazot M, Thomassin I, Hourani R, et al. Diagnostic
scopic localization of endometrial implants in the accuracy of transvaginal sonography for deep pel-
ovarian chocolate cyst. Fertil Steril 1994;61(6): vic endometriosis. Ultrasound Obstet Gynecol
1034–8. 2004;24(2):180–5.
30. Woodward PJ, Sohaey R, Mezzetti TP Jr. Endometri- 46. Abbott JA, Hawe J, Clayton RD, et al. The effects
osis: radiologic-pathologic correlation. Radio- and effectiveness of laparoscopic excision of endo-
graphics 2001;21(1):193–216 [questionnaire: 288– metriosis: a prospective study with 2-5 year follow-
94]. up. Hum Reprod 2003;18(9):1922–7.
31. Patel MD, Feldstein VA, Chen DC, et al. Endometrio- 47. Agarwal SK, Chapron C, Giudice LC, et al. Clinical
mas: diagnostic performance of US. Radiology diagnosis of endometriosis: a call to action. Am J
1999;210(3):739–45. Obstet Gynecol 2019;220(4):354.e1-12.
32. Jones LP, Morgan MA, Chauhan A. The sonographic 48. Guerriero S, Ajossa S, Minguez JA, et al. Accuracy
spectrum of pelvic endometriosis: pearls, pitfalls, of transvaginal ultrasound for diagnosis of deep
and mimics. Ultrasound Q 2019;35(4):355–75. endometriosis in uterosacral ligaments, rectovaginal
33. Van Holsbeke C, Zhang J, Van Belle V, et al. septum, vagina and bladder: systematic review and
Acoustic streaming cannot discriminate reliably meta-analysis. Ultrasound Obstet Gynecol 2015;
between endometriomas and other types of 46(5):534–45.
adnexal lesion: a multicenter study of 633 adnexal 49. Nisenblat V, Bossuyt PM, Farquhar C, et al. Imaging
masses. Ultrasound Obstet Gynecol 2010;35(3): modalities for the non-invasive diagnosis of endo-
349–53. metriosis. Cochrane Database Syst Rev 2016;(2):
34. Jenkins S, Olive DL, Haney AF. Endometriosis: path- CD009591.
ogenetic implications of the anatomic distribution. 50. Scardapane A, Lorusso F, Bettocchi S, et al. Deep
Obstet Gynecol 1986;67(3):335–8. pelvic endometriosis: accuracy of pelvic MRI
35. Rezvani M, Shaaban AM. Fallopian tube disease in completed by MR colonography. Radiol Med 2013;
the nonpregnant patient. Radiographics 2011; 118(2):323–38.
31(2):527–48. 51. Valentini AL, Gui B, Micco M, et al. How to improve
36. Gougoutas CA, Siegelman ES, Hunt J, et al. Pelvic MRI accuracy in detecting deep infiltrating colo-
endometriosis: various manifestations and MR imag- rectal endometriosis: MRI findings vs. laparoscopy
ing findings. AJR Am J Roentgenol 2000;175(2): and histopathology. Radiol Med 2014;119(5):
353–8. 291–7.

You might also like