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GENITOURINARY IMAGING 1047

T2-Hypointense Adnexal
Lesions: An Imaging
Algorithm1
Alla Khashper, MD • Helen C. Addley, MRCP, FRCR • Nesreen Abourokbah,
CME FEATURE
MD • Stephanie Nougaret, MD • Evis Sala, MD, PhD, FRCR • Caroline
See www.rsna
.org/education Reinhold, MD, MSc
/rg_cme.html
T2-weighted sequences are an integral part of magnetic resonance
LEARNING (MR) imaging performed for the characterization of adnexal lesions.
OBJECTIVES A relatively small number of these lesions demonstrate low signal
FOR TEST 3 intensity on T2-weighted MR images. In the majority of cases, a spe-
After completing this cific diagnosis can be made by interpreting the signal intensity of the
journal-based CME
activity, participants lesion with respect to certain pathologic correlates, including blood
will be able to: products, smooth muscle, fibrous tissue, and calcification, as well as
■■List the poten-
tial causes of T2-
high lesion cellularity. For example, lesions that are at least as dark
hypointense adnexal as skeletal muscle are almost always benign, whereas those whose T2
lesions.
signal intensity is higher than that of skeletal muscle constitute a more
■■Discuss the differ-
ential diagnosis and heterogeneous group composed of benign, borderline, and malignant
characteristic MR disease entities. The authors propose a diagnostic algorithm that takes
imaging findings
for T2-hypointense these features into account, as well as the appearances of the lesion
adnexal lesions. with additional pulse sequences, to aid in the correct interpretation of
■■Describe an imag-
ing algorithm for
T2-hypointense adnexal lesions. Knowledge of the anatomy, the T1-
these lesions that is weighted imaging features, and the enhancement characteristics of ad-
based on a multi-
sequential MR im-
nexal lesions allows accurate characterization of these lesions, resulting
aging and multimo- in appropriate patient management.
dality approach.
©
RSNA, 2012 • radiographics.rsna.org

RadioGraphics 2012; 32:1047–1064 • Published online 10.1148/rg.324115180 • Content Codes:


1
From the Department of Radiology, McGill University Health Center, 1650 Cedar Ave, Suite C5 118, Montreal, QC, Canada H3G 1A4 (A.K., N.A.,
C.R.); Department of Radiology, Addenbrooke’s Hospital, Cambridge, England (H.C.A., E.S.); and Department of Radiology, St Eloi Hospital, CHU
Montpellier, Montpellier, France (S.N.). Recipient of a Certificate of Merit award for an education exhibit at the 2010 RSNA Annual Meeting. Received
November 22, 2011; revision requested December 14 and received March 1, 2012; accepted March 2. For this journal-based CME activity, the authors,
editor, and reviewers have no relevant relationships to disclose. Address correspondence to A.K. (e-mail: khashper@yahoo.com).
©
RSNA, 2012
1048  July-August 2012 radiographics.rsna.org

Introduction though multiplanar MR imaging is superior to


Magnetic resonance (MR) imaging is optimal other imaging techniques in demonstrating the
for the evaluation of adnexal masses due to its pelvic anatomy, identification of specific anatomic
multiplanar capability and inherent soft-tissue structures and of the origin of the lesion can re-
contrast. The MR imaging features of inde- main a diagnostic challenge in some cases.
terminate adnexal masses can provide unique
morphologic information regarding the lesion, Location of T2-
including its location, size, and cystic-solid Hypointense Adnexal Lesions
composition (1). T2-weighted sequences are an When a parauterine adnexal mass is visualized,
integral part of MR imaging performed for the verification of the origin of the mass is essential
characterization of adnexal masses. The major- for appropriate patient management. If the go-
ity of adnexal lesions contain cystic compo- nadal vessels lead to the lesion and no ipsilateral
nents, which demonstrate high signal intensity ovary is visualized, an ovarian lesion is considered
on T2-weighted images. The finding of a T2- to be a possibility. On the other hand, visualiza-
hypointense adnexal lesion is less common and tion of both ovaries as separate and distinct from
should be interpreted with respect to specific the lesion confirms that the lesion is extraovarian
pathologic correlates, including blood products, in origin. Visualization of hyperintense ovarian
smooth muscle, fibrous tissue, and calcification, follicles or of a functional cyst at T2-weighted
as well as high lesion cellularity. In this article, imaging helps identify the ovaries. The presence
we discuss the differential diagnosis for T2-hy- of a pedicle between the uterus and the lesion
pointense adnexal lesions and describe imaging indicates that the lesion arises from the uterus.
features that allow a more specific diagnosis. In Dynamic ultrasonography (US) may be helpful
addition, we propose a diagnostic algorithm that for demonstrating movement of the mass with
takes these features into account, as well as the the uterus; however, the pedicle of a subserosal
appearances of the lesion with additional pulse pedunculated leiomyoma can be very narrow and
sequences, to aid in the correct interpretation of is more easily identified at MR imaging (3). The
T2-hypointense adnexal lesions. “bridging vessel” sign represents tortuous vas-
cular structures passing between the uterus and
Normal Anatomy the lesion and may be seen at US; however, this
of the Adnexa Uteri sign is most clearly depicted at gadolinium-based
To accurately characterize indeterminate adnexal contrast material–enhanced T1-weighted imaging
lesions, it is important to first be familiar with or T2-weighted imaging, which nicely demon-
their normal appearance and to assess the relation- strate vascular flow voids (3). The bridging vessel
ship of the lesion to the pelvic organs. The adnexa sign confirms that the lesion originates from the
include the fallopian tubes and the ovaries as well uterus and excludes an ovarian origin (Fig 1),
as structures that originate from the uterus and although intravenous administration of contrast
its supporting ligaments. Identifying the anatomic material can be helpful in confirming an ovarian
origin of an adnexal lesion aids in characterizing vascular supply to the mass (4).
the lesion and narrowing the differential diagnosis. In the setting of an adnexal mass that is neither
The imaging appearance of the ovaries will vary ovarian nor uterine in origin, the possibility of
depending on the patient’s physiologic state (stage tubal disease must be considered. Tubal masses
of menstrual cycle, age, pregnancy status) or previ- are separate from the uterus as well as the ovary,
ous treatment and procedures. The fallopian tube although they may be attached to the ovary by
is a serpentine structure filled with interdigitating adhesions. The most common T2-hypointense
plicae, and typically no lumen is visualized (2). tubal lesion is hematosalpinx (discussed later), fol-
The identification of a tubal structure separate lowed by tubal leiomyoma, fibroma, and abscess.
from the ovary aids in making the diagnosis. Al- Although extrauterine leiomyomas are uncom-
mon, they can arise from a fallopian tube or round
ligament. Endovaginal US may provide assurance
RG  •  Volume 32  Number 4 Khashper et al  1049

Figure 1.  Exophytic subserosal leiomyoma in a 47-year-old woman. (a) Endovaginal Doppler US
image shows the bridging vessel sign (arrow) between the uterus (Ut) and a mass. (b) Short-axis
T2-weighted MR image shows a heterogeneous, predominantly hypointense mass, with vascular
flow voids (arrows) between the uterus and the mass. (c) Coronal T2-weighted MR image shows
splitting of the myometrium toward the mass (arrows), as well as a separate and distinct normal left
ovary (arrowheads).

of separation of the uterus and ovaries from the are, therefore, T2 hyperintense. However, there
mass. MR imaging is extremely useful due to its are a few distinctive histologic and morphologic
superb multiplanar capability and its capacity to entities that result in shortening of T2 relaxation
demonstrate the typical signal characteristics of time and hence manifest with low signal intensity
leiomyoma (see “Smooth Muscle”) (5). at T2-weighted imaging, including blood products,
muscle, fibrous tissue, calcification, air or flow-
Signal Characteristics of related artifact, and paramagnetic substances such
T2-Hypointense Adnexal Lesions as melanin (7). For the purposes of this article, T2-
Tissue characterization at MR imaging is based hypointense adnexal masses are grouped according
primarily on differences in longitudinal (T1) and to their predominant component (Table 1).
transverse (T2) relaxation times (6). The majority
of adnexal lesions contain cystic components and
1050  July-August 2012 radiographics.rsna.org

We divide T2-hypointense adnexal lesions into


Table 1
two subgroups. The first subgroup includes masses Classification of T2-Hypointense Adnexal Masses
that are as dark as or darker than skeletal muscle according to Predominant Component
on T2-weighted MR images, whereas the second
Blood products
subgroup contains lesions whose T2 signal inten-
 Endometrioma
sity is higher than that of skeletal muscle (Table 2).
  Hemorrhagic cyst
T2-hypointense adnexal lesions that are at least as  Hematosalpinx
dark as skeletal muscle help narrow the differential   Cystic adenomyosis
diagnosis and improve specificity. Nearly all of Smooth muscle
these lesions are benign nonaggressive entities. Ad-   Uterine leiomyoma
nexal lesions that are hypointense on T2-weighted Fibrous tissue
MR images, but whose signal intensity is higher  Fibroma
than that of skeletal muscle, are a more heteroge-  Fibrothecoma
neous group composed of benign, borderline, and  Cystadenofibroma
malignant disease entities. In the appropriate clini- Mixed cellularity
cal context, these entities should be included in   Brenner tumor
the differential diagnosis for lesions that are not as   Struma ovarii
hypointense as skeletal muscle.   Krukenberg tumor

Pathologic Correlates
Table 2
Blood Products Classification of T2-Hypointense Lesions
The signal characteristics of a hemorrhagic le- according to Degree of Signal Loss
sion at MR imaging depend on the age of the T2 isointense relative to muscle
hemorrhage and whether the blood products are  Endometrioma
intracellular or extracellular in location (Table 3),   Cystic adenomyosis
even though time-related changes in hemorrhage  Hematosalpinx
are not as predictable for extracranial bleeding as  Leiomyoma
for intracranial bleeding. Intracellular deoxyhe-  Fibroma
moglobin (acute hemorrhage) and intracellular  Fibrothecoma
methemoglobin (early subacute hemorrhage)  Cystadenofibroma
  Struma ovarii
result in T2 shortening and are, therefore, T2
T2 hypointense relative to muscle
hypointense. Intracellular deposits of ferritin or
  Hemorrhagic cyst
hemosiderin in the wall of a mature hematoma   Malignant transformation of endometrioma
also lead to decreased T2 signal intensity due to   Mucinous cystic neoplasm
magnetic susceptibility effects. In contrast, extra-   Krukenberg tumor
cellular methemoglobin (late subacute hemor-
rhage) is T2 hyperintense, whereas intracellular
methemoglobin results in high T1 values due to
paramagnetic effects (7). images (Fig 2) and, in the case of a solitary lesion,
a T1-hyperintense and T2-hypointense cyst (Fig
Endometrioma.—At US, an endometrioma typi- 3) (12). Homogeneous T2 shading is a character-
cally appears as a homogeneous hypoechoic mass istic feature of endometrioma. The term shading
with low-level echoes. MR imaging has been refers to signal loss on T2-weighted MR images in
shown to be more specific than US or computed an ovarian cyst that appears hyperintense on T1-
tomography (CT) for the diagnosis of endometri- weighted images (13). Hemorrhage-containing
oma (9). Iron overload (10), a high concentration lesions that (like skeletal muscle) are markedly
of protein, and increased viscosity over time are hypointense on T2-weighted images are highly
well-recognized characteristics of endometriomas specific for endometriomas. However, not all en-
due to repeated bleeding and degradation of old dometriomas show this degree of T2 shortening,
blood products, resulting in low T2 signal inten- depending on their age, the amount of hemosid-
sity (11). Diagnostic MR imaging criteria with a erin, and the protein concentration. Dependent
high specificity for endometriosis include multiple layering and a hypointense fluid level representing
hyperintense cysts on fat-suppressed T1-weighted different-aged blood products can be seen within
an endometrioma. A hypointense peripheral ring
caused by hemosiderin staining may be seen in
RG  •  Volume 32  Number 4 Khashper et al  1051

Figure 2.  Endometriomas in a 26-year-old woman. Axial


fat-saturated T1-weighted MR image reveals multiple bilat-
eral hyperintense ovarian cysts, findings that are compatible
with endometriomas. Bilateral ovarian cysts were also seen
at abdominal US.

Figure 3.  Solitary endometrioma in a 48-year-old woman. (a) Axial fat-saturated T1-weighted MR image shows
a hyperintense lesion (arrow) in the left ovary. (b) Axial T2-weighted MR image demonstrates homogeneous loss of
signal within the lesion (arrow), a finding that represents the “shading” sign.

Table 3
Signal Intensity Characteristics of Hemorrhagic Lesions at MR Imaging

T1 T2 Signal
Principal Component Time Range Age of Hemorrhage Signal Intensity Intensity
Intracellular oxyhemoglobin Hyperacute Minutes–24 h Low-intermediate High
Intracellular deoxyhemoglobin Acute 1–3 d Low Low
Intracellular methemoglobin Early subacute 3–7 d High Low
Extracellular methemoglobin Late subacute 1 wk–months High High
Hemosiderin and ferritin Chronic Months–years Very low Very low
Source: Reference 8.

chronic lesions (14). Margins that are slightly histologic subtypes include endometrioid and
angled or distorted and not completely round due clear cell carcinoma (16). Suspicious features
to adjacent scarring and fibrosis are also charac- include a large or growing endometrioma and
teristic of endometriomas. lack of the characteristic shading on T2-weighted
Malignant transformation is a rare complica- images. Loss of T2 shading following malignant
tion of endometriosis and is estimated to occur
in about 1% of patients (15). The most common
1052  July-August 2012 radiographics.rsna.org

Figure 4.  Malignant transformation of an endometrioma in a 37-year-old woman. (a) Axial fat-saturated T1-weighted
MR image shows a unilocular, homogeneously hyperintense left ovarian lesion containing hypointense nodules (arrows).
(b) On an axial T2-weighted MR image, the mass is intermediately hypointense and contains hyperintense nodules
(arrows) but nevertheless has higher signal intensity than does skeletal muscle (*). (c) Axial contrast-enhanced T1-
weighted MR image demonstrates enhancing solid mural nodules. (d) Subtraction T1-weighted MR image more
clearly depicts the nodules (arrows). Endometrioid carcinoma was proved at pathologic analysis.

transformation of an endometrioma is thought to >1 cm) (20), are related to ovulation and are
be related to dilution of the hemorrhagic content typically not seen after menopause (21). Dis-
by tumor secretion (Fig 4) (17). tinguishing between a hemorrhagic cyst and an
In these cases, careful assessment for the endometrioma remains a diagnostic problem in
presence of an enhancing mural nodule must some cases (22). Both entities may have similar
be made. Solid mural nodules seem to be the US features and appear hyperintense on fat-sup-
most valuable imaging finding in suggesting pressed T1-weighted MR images. Frequently,
malignant transformation of an endometrioma endometriomas will have a very bright “light
(18). Positive enhancement of the nodule is bulb” appearance, which can help differenti-
best appreciated on dynamic contrast-enhanced ate them from hemorrhagic cysts. Hemorrhagic
subtraction T1-weighted MR images (19), on cysts may also be hypointense on T2-weighted
which the nodule is clearly highlighted on a MR images, although they are more commonly
background of unchanged signal intensity in the hyperintense. Hemorrhagic cysts show hetero-
rest of the lesion. geneous and relatively mild signal loss with no
shading on T2-weighted images, whereas en-
Hemorrhagic Ovarian Cyst.—Functional hem- dometriomas show marked T2 signal loss. This
orrhagic ovarian cysts, including follicular cysts is due to the absence of repeated bleeding and,
(usually <1 cm) and corpus luteal cysts (often therefore, a lower concentration of blood prod-
ucts and viscosity in hemorrhagic cysts than in
endometriomas (Fig 5).
RG  •  Volume 32  Number 4 Khashper et al  1053

Figure 5.  Hemorrhagic right ovarian cyst in a 39-year-old woman. (a) Short-axis fat-saturated T1-
weighted MR image shows a predominantly hyperintense right ovarian lesion (arrow). (b) On an axial T2-
weighted MR image, the lesion (white arrow) demonstrates mild signal loss relative to skeletal muscle (*)
and typical endometrioma (cf Fig 3). Note the functional simple cyst (black arrow) in the left ovary.

Figure 6.  Endometriosis in a 33-year-old woman with hematosalpinx. (a) Axial fat-saturated T1-weighted
MR image demonstrates bilateral hyperintense serpentine structures (arrows) and the waist sign (arrow-
heads), findings that are compatible with hematosalpinx. (b) Axial T2-weighted MR image reveals hypoin-
tense blood contents (arrows) in the fallopian tubes. The presence of hypointense irregular plaque in the
cul-de-sac (arrowhead) associated with bowel tethering confirms the diagnosis of pelvic endometriosis.

Functional hemorrhagic ovarian cysts are more findings of a hematosalpinx are T2 hypointen-
commonly unilateral than bilateral and show a sity, a tubular shape with small round projec-
thin, well-defined smooth wall. Hemorrhagic cysts tions, and diametrically opposed indentations
frequently contain heterogeneous contents due to in the walls resulting in the “waist” sign, which
clot formation and retraction. At follow-up imag- reflects a tubular cystic structure with a folded
ing performed after a few physiologic cycles, a configuration (23). Hematosalpinx may be the
hemorrhagic cyst will demonstrate complete or only imaging finding of pelvic endometriosis
partial resolution, whereas an endometrioma usu- (24). However, it may in fact be associated with
ally has a stable and persistent appearance. endometriosis; therefore, detection of a hema-
tosalpinx should prompt careful evaluation for
Hematosalpinx.—A hematosalpinx can be rec- endometrial deposits and endometriomas, and
ognized at both US and MR imaging as a tubu- vice versa (Fig 6).
lar or corkscrew-shaped structure centered in
the fallopian tube. The most helpful and specific
1054  July-August 2012 radiographics.rsna.org

Figure 7.  Cystic adenomyosis in a 26-year-old woman.


(a) Endovaginal US image shows an apparent cyst
with low-level echoes (arrow) to the left of the uterus
(Ut), a finding that suggests a left-sided endome-
trioma. (b) Axial fat-saturated T1-weighted MR image
shows a hyperintense hemorrhagic lesion (arrow) in the
left cornu surrounded by myometrium. The left ovary
(arrowheads) appears separate and distinct. (c) Axial
T2-weighted MR image helps confirm a uterine lesion
(arrow) with very low signal intensity comparable to
that of skeletal muscle (*). These findings are consistent
with cystic adenomyosis. Arrowheads = left ovary.

Cystic Adenomyosis.—Subserosal cystic adeno- ages, which results from the T2 shortening effects
myosis of the uterus may also mimic a T2-hy- of intramuscular actin, myosin, and collagen, as
pointense adnexal lesion (25). It is characterized well as decreased extracellular fluid relative to sur-
by a cystic myometrial lesion with extensive glan- rounding tissues (28). Normal pelvic structures
dular changes and hemorrhage. The hemorrhage that demonstrate very low signal intensity on T2-
can be seen at different stages of organization, weighted MR images include the junctional zone
from subacute blood to hemosiderin deposits in of the uterus; the vaginal, urethral, and rectal mus-
the wall of the adenomyotic cyst, and thus can cularis; and the bladder detrusor muscle (7). Uter-
appear similar to an endometriotic cyst (26). ine leiomyoma represents the classic example of a
The uterine origin of cystic adenomyosis can be pelvic neoplasm that is composed predominantly
confirmed on the basis of (a) the presence of of smooth muscle and therefore typically demon-
myometrial splaying around the lesion, (b) visu- strates low signal intensity on T2-weighted MR
alization of the bridging vessel sign, and (c) iden- images and low to intermediate signal intensity on
tification of the ovaries as separate and distinct T1-weighted images (Fig 8). This characteristic
entities (Fig 7) (27). signal intensity aids in making the diagnosis and is
seen in up to 60% of uterine leiomyomas, showing
Smooth Muscle a hyaline subtype of degeneration. The T2 signal of
Compared with other soft tissues in the body, both leiomyomas may vary in less common subtypes of
smooth muscle and skeletal muscle demonstrate degeneration (cystic, myxoid, and red) due to the
lower signal intensity on T2-weighted MR im- presence of specific components (edema, hemor-
rhage, necrosis, and calcification) or in unusual
subtypes (lipoleiomyoma and myxoid leiomyoma)
RG  •  Volume 32  Number 4 Khashper et al  1055

Figure 8.  Multiple uterine leiomyomas in a 66-year-old woman. (a) Coronal T2-weighted MR image
depicts predominantly hypointense intramuscular (white arrow) and exophytic (black arrow) subserosal
leiomyomas. The exophytic leiomyoma should be differentiated from an adnexal mass. (b) On an axial fat-
saturated T1-weighted image, the leiomyomas (arrows) are isointense relative to uterine myometrium (*).

(29), resulting in a heterogeneous “cobblestone” The solid fibrous component of fibroma, fibro­
appearance. Exophytic uterine leiomyomas may thecoma, and cystadenofibroma characteristically
mimic adnexal masses in some cases. In these demonstrates very low T2 signal intensity, allow-
instances, determining the origin of the mass will ing the differentiation of these benign tumors
allow a correct diagnosis to be made. from malignant solid ovarian lesions.
Extrauterine leiomyomas are rare and often Although MR imaging criteria for malignant
pose a significant diagnostic challenge. These ovarian tumors include visualization of a solid
masses may originate from the adnexa, including mass or a large solid component in association
the ovaries, fallopian tubes, and round ligament. with a cystic mass, awareness of the typical MR
Parasitic leiomyoma arises from the broad liga- imaging characteristics of fiber-containing tu-
ment of the uterus and, unlike other leiomyomas, mors allows the diagnosis of benign ovarian dis-
can grow after hysterectomy. Primary ovarian ease to be made.
leiomyoma is a very rare pathologic entity, with
less than 80 cases having been reported in the Fibroma and Fibrothecoma.—Fibroma and
literature. .Ovarian leiomyoma coexists with uter- fibrothecoma represent a spectrum of benign
ine leiomyoma in 80% of cases, with typical MR stromal ovarian tumors composed of fibrous
imaging characteristics similar to those of smooth tissue and theca cells. Fibromas can be as-
muscle (5). Because leiomyomas are the most sociated with ascites and pleural effusions in
common gynecologic tumors and are usually be- classic Meigs syndrome (30), or with elevated
nign, they should be included in the differential carcinogenic antigen levels (31). These solid
diagnosis given the characteristic T2 hypointen- tumors have a variable appearance at US and
sity of smooth muscle tumors. not uncommonly remain indeterminate. With
T1-weighted sequences, fibrothecomas demon-
Fibrous Tissue strate nonspecific hypo- to isointensity with mild
Fibrous tissue represents low-cellularity or acellu- enhancement following the intravenous adminis-
lar material in combination with spindle, oval, or tration of a gadolinium chelate.
round cells that result in collagen formation. Fi- Therefore, identification of the characteristic
brosis typically demonstrates intermediate signal predominantly low signal intensity of fibromas
intensity on T1-weighted MR images and very at T2-weighted imaging allows their differentia-
low signal intensity on T2-weighted images (7). tion from other solid ovarian masses (32) (Fig 9).
1056  July-August 2012 radiographics.rsna.org

Figure 9.  Ovarian fibroma in a 71-year-old woman. (a) Sagittal T2-weighted MR image demonstrates a very low-
signal-intensity ovarian mass (arrow), a finding that is typical of fibroma. The presence of a few simple cysts (arrow-
head) helps verify the ovarian origin of the lesion. (b) On a sagittal contrast-enhanced T1-weighted MR image, the
fibroma (arrow) shows mild enhancement.

Figure 10.  Left ovarian fibrothecoma in a 65-year-old


woman. (a) Axial T2-weighted MR image shows a het-
erogeneously hypointense ovarian mass, with the most
hypointense components (arrowheads) representing
fibrous tissue. Ut = uterus. (b) Short-axis T2-weighted
MR image shows an endometrial polyp (arrow) and a
uterus (Ut) that is hyperstimulated for the patient’s age.
(c) Postcontrast T1-weighted MR image demonstrates
multifocal endometrial enhancement (arrow) as well as
mild enhancement of the fibrothecoma (arrowheads).
Ut = uterus.

Fibrothecomas are responsible for the endocrine


activity that results in endometrial hyperplasia
and polyps in some cases (33). Visualization of
a thickened endometrium or endometrial polyp
associated with a hypointense ovarian mass at
T2-weighted imaging favors the diagnosis of a
fibrothecoma (Fig 10). In larger lesions, vari- fibrous components can be seen in associa-
ous combinations of T2-hypointense theca and tion with T2-bright edema and cysts, resulting
in mixed low to high signal intensity on T2-
weighted MR images (32).
RG  •  Volume 32  Number 4 Khashper et al  1057

Figures 11, 12.  (11) Ovarian cystadeno-


fibroma in a 74-year-old woman. (a) Endo-
vaginal Doppler US image depicts an indeter-
minate cystic ovarian mass with a thick wall.
(b) On an axial T2-weighted MR image, the
fibroid solid component in the cystic wall has
the typical very low-signal-intensity appear-
ance (arrows). (c) Axial contrast-enhanced
subtraction T1-weighted MR image shows
mild enhancement of the fibroid solid compo-
nent (arrows). (12) Ovarian cystadenofibroma
in a 65-year-old woman. Coronal T2-weighted
MR image shows a left ovarian mass (arrow)
that is partially multicystic and partially solid.
The solid component has considerable hypoin-
tense signal, similar to skeletal muscle (*).

ing. The imaging appearance of cystadenofibro-


mas varies depending on whether the cystic or
fibrous component predominates (Figs 11, 12).
In patients with primarily cystic cystadenofi-
bromas, the solid fibrous component may result
Cystadenofibroma.—Cystadenofibroma is an- in irregular wall thickening (possibly >3 mm)
other example of a usually benign ovarian tumor with mild enhancement on postcontrast im-
that contains fibrous stroma in combination ages. Therefore, recognition of the typical very
with an epithelial cystic component. These tu- low-signal-intensity appearance of the solid fi-
mors are classified according to epithelial cell brous component at T2-weighted imaging plays
type into serous, endometrioid, mucinous, clear a crucial role in assessing for possible ovarian
cell, and mixed subtypes, whereas the relation- malignancy (35). Although most ovarian cystad-
ship between epithelial proliferation and the enofibromas are benign, they do have malignant
stromal component of the tumor is used to clas- potential and therefore are removed surgically.
sify tumors as benign, borderline, or malignant However, making the correct diagnosis of cyst-
(34). At MR imaging, a cystadenofibroma typi- adenofibroma may help avoid unnecessary ex-
cally appears as a multiloculated cystic mass, tensive surgery.
with a solid fibrous component that demon-
strates low signal intensity at T2-weighted imag-
1058  July-August 2012 radiographics.rsna.org

Figure 13.  Brenner tumor in a 77-year-old woman.


(a) Axial T2-weighted MR image shows a complex left
ovarian mass with a significantly hypointense solid
component dorsally (arrowheads) and a multicystic
component with hypointense septa ventrally (arrows).
(b) Corresponding axial contrast-enhanced T1-weighted
MR image shows mild enhancement of the dorsal solid
component (arrowheads) as well as septal enhancement
within the multicystic component (arrows). (c) Contrast-
enhanced CT scan reveals coarse calcifications dorsally
(arrow), in addition to a few cysts. Pathologic analysis
demonstrated Brenner tumor in the dorsal aspect of the
lesion as well as an associated cystadenofibroma ventrally.

Mixed-Cellularity Tumors

Brenner Tumor.—Brenner tumor is an uncom-


mon epithelial-stromal tumor that represents hypovascular. The presence of calcification and
about 2% of ovarian neoplasms and typically coexisting epithelial neoplasms favors a diagno-
contains a fibrous stromal component in associa- sis of Brenner tumor over fibrothecoma. In rare
tion with calcifications and transitional cells that cases, benign Brenner tumor shows “borderline”
are histologically similar to urothelial epithelium characteristics or even malignant transformation
(36). The fibrous components, as well as calcifi- to transitional cell carcinoma (38). According to
cations (when present), are markedly hypointense a few MR imaging studies, borderline Brenner
on T2-weighted MR images. Brenner tumors tumors typically manifest as cystic masses with
are usually discovered incidentally at pathologic papillary and solid elements (38), whereas ma-
analysis, and up to 20% of these tumors are as- lignant Brenner tumors typically manifest as
sociated with mucinous cystadenomas or other multilocular cystic masses with large solid com-
epithelial neoplasms (37). In these cases, the le- ponents. In such borderline or even malignant
sion has a complex cystic and solid appearance, tumors, a solid component composed of poorly
with the Brenner tumor (representing the solid differentiated cells demonstrates iso- to hyperin-
part) characteristically demonstrating very low tensity at T2-weighted MR imaging, as opposed
signal intensity at T2-weighted imaging (Fig 13). to the marked T2 hypointensity of the fibrous
Although the T2-weighted imaging findings of stromal component seen in the more typical be-
Brenner tumors overlap with those of fibrotheco- nign Brenner tumors (39).
mas, Brenner tumors typically demonstrate at
least moderate enhancement after contrast mate- Struma Ovarii.—Struma ovarii is a rare type of
rial administration, whereas fibrothecomas are ovarian lesion that accounts for 0.30%–0.65%
of ovarian tumors and 2% of ovarian teratomas
(40). Struma ovarii is a highly specialized form
RG  •  Volume 32  Number 4 Khashper et al  1059

Figure 14.  Struma ovarii in a 59-year-old woman. (a) Sagittal T2-weighted MR image shows a multiloculated,
heterogeneous left ovarian lesion with very low signal intensity (arrow). (b, c) Corresponding axial in-phase (b)
and opposed-phase (c) T1-weighted MR images reveal a hypointense mass with chemical shift artifact in its ventral
aspect (arrowhead), a finding that is compatible with a small amount of fat. (d) Axial postcontrast T1-weighted MR
image shows significant enhancement of the ovarian lesion (arrow) with sparing of its inferior aspect.

of ovarian teratoma and is composed entirely or microscopic fat, as indicated by signal drop-off
predominantly of thyroid tissue with large fol- and surrounding chemical shift artifact on op-
licles containing colloid material (41). About posed-phase T1-weighted MR images. Struma
5% of patients with struma ovarii develop clini- ovarii typically demonstrates strong enhance-
cal evidence of hyperthyroidism (42). At US, ment of the solid components on postcontrast
struma ovarii has a nonspecific solid and cystic T1-weighted images (Fig 14). At times, it can be
appearance. High-attenuation cystic compo- difficult to distinguish these lesions from border-
nents and calcifications may be recognized at line mucinous epithelial ovarian lesions. In mu-
CT. MR imaging demonstrates a loculated cinous lesions, the T1 and T2 relaxation times
cystic mass with variable signal characteristics. are shortened owing to the high protein content
Cystic spaces may show marked hypointensity and viscosity of the mucinous tumor, with high
at T2-weighted imaging and intermediate sig- signal intensity on T1-weighted images and low
nal intensity at T1-weighted imaging due to the signal intensity on T2-weighted images (44). In
thick, gelatinous colloid of the struma, whereas addition, mucinous ovarian neoplasms (Fig 15)
other locules are T1 hyperintense owing to
hemorrhage (43). Some locules may contain
1060  July-August 2012 radiographics.rsna.org

Figure 15.  Borderline mucinous ovarian neoplasm in a 52-year-old woman. (a) Axial T2-weighted MR image de-
picts a multicystic septated lesion (arrowheads) with mixed hypo- and hyperintensity, although the hypointense
aspect of the mass demonstrates relatively mild signal loss compared to skeletal muscle (*). (b) Axial fat-saturated
T1-weighted MR image shows the lesion (arrowheads) with heterogeneous mixed hyper- and hypointensity, a com-
mon characteristic of mucinous tumor.

Figure 16.  Metastatic right ovarian Krukenberg tumor in a 48-year-old woman with gastric cancer. (a) Axial T2-
weighted MR image shows a hypointense right ovarian lesion (arrows) that nonetheless appears less dark than adjacent
muscle (*) or the uterus (Ut). (b) On a corresponding axial contrast-enhanced T1-weighted MR image, the ovarian
mass (arrows) demonstrates marked enhancement.

are typically less hypointense than struma ovarii Krukenberg Tumor.—Krukenberg tumors are
on T2-weighted MR images. Struma ovarii are metastatic ovarian adenocarcinomas that most
benign in 95% of cases and usually occur in commonly originate from the stomach (70% of
premenopausal women; therefore, preoperative cases), followed by the breast, colon, and appen-
diagnosis is essential to avoid unnecessary radi- dix. Krukenberg tumors account for 1%–2% of
cal surgery (45). all ovarian tumors worldwide and are bilateral in
60%–80% of patients (46). The ovaries are usually
not recognized. Krukenberg tumors commonly
appear as solid masses with well-demarcated or
RG  •  Volume 32  Number 4 Khashper et al  1061

Figure 17.  Diagram illustrates a diagnostic algorithm for T2-hypointense adnexal masses. ↑T1 SI = high signal in-
tensity on T1-weighted images, ↓T1 SI = hypo- or isointensity on T1-weighted images, + enhancement = enhanced
solid component, − enhancement = no enhancement detected.

(owing to cystic necrosis or hemorrhage) ill-de- mass is visualized, an algorithmic approach to


fined intratumoral cysts. They often demonstrate image analysis can help significantly narrow the
variable hypointensity on T2-weighted images due differential diagnosis (Fig 17).
to the presence of metastatic mucin-filled signet- First, the radiologist should exclude a uterine
ring cells in the ovarian stroma and abundant origin for the lesion by assessing for the bridging
collagen formation (Fig 16) (47). Moderate to vessel sign, splaying of the myometrium, and sep-
marked enhancement of the solid component and arate identification of the ovaries on T2-weighted
pericystic rim is noted, a finding that is unusual and postcontrast T1-weighted MR images. Exo-
in other solid ovarian lesions (48). Krukenberg phytic pedunculated leiomyoma and cystic ad-
tumor is a rare but significant malignancy that enomyosis are the most common T2-hypointense
should be included in the differential diagnosis for uterine lesions that can mimic an ovarian mass.
T2-hypointense adnexal masses in the appropriate When a uterine source for an adnexal lesion
clinical context. For differential purposes, the pos- is ruled out, attention should be paid to the de-
sibility of Krukenberg tumors may be considered gree of signal loss on T2-weighted MR images.
in cases of heterogeneous solid and cystic bilateral Endometrioma, leiomyoma, fibrous lesions, he-
ovarian masses that show at least moderate en- matosalpinx, and struma ovarii can all show very
hancement, as well as T2 hypointensity of the solid low signal intensity on T2-weighted images that
component that is relatively mild compared with is comparable to that of skeletal muscle (7). Ap-
the signal intensity of skeletal muscle. plying this criterion results in very high specificity
for a benign lesion, allowing appropriate conser-
Diagnostic Workup of vative or (if surgical removal is indicated) lapa-
T2-Hypointense Adnexal Lesions roscopic management. When an adnexal lesion
Both benign and malignant adnexal masses show is hypointense on T2-weighted images but has a
variable signal intensity on T2-weighted MR im-
ages. However, when a T2-hypointense adnexal
1062  July-August 2012 radiographics.rsna.org

Table 4
Diagnostic Workup of T2-Hypointense Adnexal Masses

Helpful
Type of Mass Key Features Imaging Examinations
Uterine origin
  Uterine leiomyoma, Visualization of ovaries as separate and distinct T2W, C+ T1W
cystic adenomyosis entities, splitting of myometrium, bridging vessel
sign (vascular flow voids)
Hemorrhagic
 Endometrioma Hyperintensity remaining after fat saturation, FS T1W
“multiplicity” sign
Adhesions T2W, C+ T1W
  Malignant transformation Loss of shading T2W
of endometrioma Solid nodule C+ subtraction T1W
 Hematosalpinx Hyperintense serpentine structure FS T1W
Fibrotic
 Fibrothecoma Endometrial thickening or polyps T2W, C+ T1W
 Cystadenofibroma Hypointense thick walls of the cyst US, T2W
Mixed cellularity
  Brenner tumor Coarse calcifications CT
Associated neoplasm US, CT, MR imaging
  Struma ovarii Calcifications CT
Strong enhancement C+ T1W
Note.—C+ = contrast-enhanced, FS = fat-saturated, T1W = T1-weighted MR imaging, T2W = T2-weighted
MR imaging.

signal intensity that is clearly higher than that of endometrioma, cystic adenomyosis, and hemato-
skeletal muscle, the specificity for benign disease salpinx. Mucinous epithelial neoplasms may also
decreases and there is greater overlap with findings be T2 hypointense and T1 hyperintense, although
for malignant lesions. Lesions within this group to a lesser extent.
include both benign and malignant entities (eg, Loss of shading on T2-weighted MR images
hemorrhagic cyst, malignant transformation of an compared with prior images, and visualization of
endometriotic cyst, mucinous epithelial neoplasm, an enhancing mural nodule within an endometri-
and Krukenberg tumor) (Table 2). Therefore, the otic cyst on postcontrast T1-weighted images, are
degree of signal loss relative to skeletal muscle at highly suggestive of malignant transformation of
T2-weighted imaging provides an additional crite- the endometrioma.
rion for characterizing adnexal lesions. Visualization of a thickened endometrium or
The classic imaging features of the lesion at an endometrial polyp associated with a signifi-
MR imaging performed with additional sequences cantly T2-hypointense ovarian mass would favor
as outlined earlier help further characterize T2- the diagnosis of a fibrothecoma. A Brenner tumor
hypointense adnexal masses (Table 4). Hemor- can be diagnosed in the setting of a markedly T2-
rhagic adnexal lesions, particularly those with hypointense ovarian mass that shows moderate
recurrent bleeding, are typically hyperintense on vascularity, is associated with an epithelial neo-
fat-saturated T1-weighted MR images and include plasm, and contains coarse calcifications (better
appreciated at CT). A multiloculated cyst with
thick, markedly T2-hypointense walls is sugges-
RG  •  Volume 32  Number 4 Khashper et al  1063

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TM
This journal-based CME activity has been approved for AMA PRA Category 1 Credit . See www.rsna.org/education/rg_cme.html.
Teaching Points July-August Issue 2012

T2-Hypointense Adnexal Lesions: An Imaging Algorithm


Alla Khashper, MD • Helen C. Addley, MRCP, FRCR • Nesreen Abourokbah, MD • Stephanie Nougaret, MD •
Evis Sala, MD, PhD, FRCR • Caroline Reinhold, MD, MSc
RadioGraphics 2012; 32:1047–1064 • Published online 10.1148/rg.324115180 • Content Codes:

Page 1048
The “bridging vessel” sign represents tortuous vascular structures passing between the uterus and the
lesion and may be seen at US; however, this sign is most clearly depicted at gadolinium-based contrast
material–enhanced T1-weighted imaging or T2-weighted imaging, which nicely demonstrate vascular
flow voids (3).

Page 1050
T2-hypointense adnexal lesions that are at least as dark as skeletal muscle help narrow the differential diag-
nosis and improve specificity.

Page 1050
The term shading refers to signal loss on T2-weighted MR images in an ovarian cyst that appears hyperin-
tense on T1-weighted images (13).

Page 1052
Hemorrhagic cysts show heterogeneous and relatively mild signal loss with no shading on T2-weighted
images, whereas endometriomas show marked T2 signal loss.

Page 1055
The solid fibrous component of fibroma, fibro­thecoma, and cystadenofibroma characteristically demon-
strates very low T2 signal intensity, allowing the differentiation of these benign tumors from malignant
solid ovarian lesions.

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