Gynecologic tumors: How to communicate imaging results to the surgeon

Abstract

Gynecologic cancers are a leading cause of morbidity and mortality for female patients, with an estimated 88,750 new cancer cases and 29,520 deaths in the United States in 2012. To offer the best treatment options to patients it is important that the radiologist, surgeon, radiation oncologist, and gynecologic oncologist work together with a multidisciplinary approach. Using the available diagnostic imaging modalities, the radiologist must give appropriate information to the surgeon in order to plan the best surgical approach and its timing.

Full text

Cancer Imaging (2013) 13(4), 611625
DOI: 10.1102/1470-7330.2013.0054
REVIEW
Gynecologic tumors: how to communicate imaging
results to the surgeon
Stefania Rizzo
a
, Giuseppina Calareso
a
, Federica De Maria
b
, Vanna Zanagnolo
c
, Roberta Lazzari
d
,
Agnese Cecconi
d
, Massimo Bellomi
a,b
a
Department of Radiology, European Institute of Oncology, via Ripamonti 435, 20141, Milan, Italy;
b
Department of Health
Sciences, University of Milan, via A.di Rudinı` 8, 20142 Milan, Italy;
c
Department of Gynecology, European Institute
of Oncology, via Ripamonti 435, 20141, Milan, Italy;
d
Department of Radiotherapy, European Institute of Oncology,
via Ripamonti 435, 20141, Milan, Italy
Corresponding address: Stefania Rizzo, Department of Radiology, European Institute of Oncology, Via Ripamonti 435,
Milan 20141, Italy.
Email: stefania.rizzo@ieo.it
Date accepted for publication 5 November 2013
Abstract
Gynecologic cancers are a leading cause of morbidity and mortality for female patients, with an estimated 88,750 new
cancer cases and 29,520 deaths in the United States in 2012. To offer the best treatment options to patients it is
important that the radiologist, surgeon, radiation oncologist, and gynecologic oncologist work together with a multi-
disciplinary approach. Using the available diagnostic imaging modalities, the radiologist must give appropriate infor-
mation to the surgeon in order to plan the best surgical approach and its timing.
Keywords: Gynecologic cancers; radiologic results; surgeons.
Introduction
Gynecologic cancers are a leading causes of morbidity
and mortality for female patients, with an estimated
88,750 new cancer cases and 29,520 deaths in the
United States in 2012
[1]
. To offer the best treatment
options to patients, it is important that the radiologist,
surgeon, radiation oncologist, and gynecologic oncologist
work together with a multidisciplinary approach. Using
the available diagnostic imaging modalities, the radiolo-
gist must give appropriate information to the surgeon in
order to plan the best surgical approach and its timing.
Endometrial cancer
Endometrial cancer is the most common gynecologic
malignancy in women in the United States, with 47,130
new cases and 8010 estimated deaths in 2012
[1]
. Patients
are usually of postmenopausal age and may have risk
factors associated with increased estrogen exposure,
such as nulliparity, chronic anovulation, and obesity.
Prognosis of patients with endometrial cancer depends
on a number of factors, including histologic type and
grade, stage, lymphovascular space involvement, and
nodal status.
Management of patients with endometrial
cancer
Endometrial carcinomas are divided into two histologic
subtypes. Type 1 includes endometrioid adenocarcinoma,
the most common histologic subtype (90% of cases of
endometrial cancer), further subdivided into 3 grades
according to degree of differentiation. Type 2 endome-
trial carcinomas include serous papillary and clear-cell
adenocarcinomas. Type 2 and high-grade type 1 are
more aggressive tumors (50% pretest probability of
locally advanced or distant disease at manifestation)
[2]
.
The standard of care for patients with endometrial
cancer is surgical removal, which may include hysterec-
tomy, bilateral oophorectomy, pelvic and lomboaortic
lymphadenectomy, and omental and peritoneal biopsies.
There is still no consensus about the necessity of
performing extensive lymphadenectomy, because lympha-
denectomy is associated with higher morbidity. A combi-
nation of preoperative imaging and intraoperative
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evaluation is therefore helpful in determining whether
this surgical procedure is necessary in each patient
[3]
.
Stratification of patients according to risk factors may
guide the surgeon in avoiding unnecessary lymphadenec-
tomies in low-risk patients. Indeed, low-risk patients may
benefit from hysterectomy with bilateral oophorectomy,
whereas high-risk patients may require pelvic and para-
aortic lymphadenectomy, with the adjunct of omental
and peritoneal biopsies in cases of type II endometrial
cancer.
Preoperative evaluation
Staging, based on the revised International Federation of
Gynecology and Obstetrics (FIGO) classification
[4]
, still
remains surgicopathologic. However, the European
Society of Urogenital Imaging guidelines recommend
magnetic resonance imaging (MRI) for staging, espe-
cially when high-risk endometrial carcinoma is sus-
pected
[5]
, such as in the case of type 2 tumors; in cases
of suspected advanced disease, including cervical stroma
extension, local or distant spread (stages III and IV);
when lymph node enlargement is considered as a road-
map for lymph node sampling; and when there are med-
ical contraindications for extensive surgical staging
[5]
.
MRI is considered the most accurate imaging modality
for preoperative assessment of endometrial carcinoma
because of its excellent soft-tissue contrast resolution,
whereas computed tomography (CT) is neither sensitive
nor specific enough to assess the depth of myometrial or
cervical involvement, owing to the lack of contrast differ-
ence between tumor and myometrium. The MR protocol
for staging endometrial cancer must include T
2
-weighted
sequences in the sagittal, axial oblique plane (perpendic-
ular) and coronal oblique plane (parallel) to the uterine
cavity. If cervical involvement is suspected an additional
axial oblique sequence, perpendicular to the long axis of
the endocervical canal, should be added.
Contrast-enhanced imaging is suggested for higher
accuracy of the diagnosis of deep myometrial invasion.
It is especially recommended for atrophic uteri, if there
are associated adenomyosis or fibroids, or in suspected
advanced tumors (bladder or rectal wall invasion). The
degree of myometrial involvement is associated with
higher risk of nodal metastases. In fact the prevalence
of lymph node metastases increases from 3% with super-
ficial myometrial invasion to 46% with deep myometrial
invasion. Contrast-enhanced MRI of the pelvis shows an
accuracy of about 91% in preoperative identification of
deep myometrial invasion
[6]
.
Diffusion-weighted imaging (DWI) is an adjunctive
tool that gives information about water mobility, tissue
cellularity, and integrity of cellular membranes
[7]
.At
DWI endometrial cancer shows restricted diffusion on
high bvalue (b¼1000 s/mm
2
) images (Fig. 1). The
adjunct of DWI to T
2
-weighted images may aid in the
detection of tumors. Higher-grade tumors demonstrate a
trend to lower apparent diffusion coefficient (ADC)
values compared with lower-grade tumors
[8]
. However,
the role of DWI in assessing the depth of myometrial
invasion is still debated, mainly because of low spatial
resolution
[9]
. Cutoff ADC values able to distinguish
normal tissue from cancerous endometrial tissue are
not yet established
[7]
.
MRI may also provide additional information, such as
uterine size (especially transverse dimension), ascites,
adnexal pathologic conditions, and the presence of peri-
toneal disease, thus helping to determine the surgical
approach. Laparoscopic (robotic) surgery is the preferred
approach for endometrial cancer, but is contraindicated
in patients with peritoneal involvement, large-size uterus,
and/or extrauterine disease
[10]
.
In evaluation of nodal metastases, the role of positron
emission tomography (PET)/CT is under consideration.
Kitajima et al.
[11]
showed overall sensitivity, specificity,
positive predictive value (PPV), negative predictive value
(NPV), and accuracy of PET/CT on a node-based analy-
sis of patients who underwent pelvic, with or without
lomboaortic, nodal dissection of 51.1%, 99.8%, 85.2%,
98.9%, and 98.7%, respectively. However, the sensitivity
in detection of metastatic lesions 4 mm or less in short-
axis diameter was as low as 12.5%
[11]
.
Figure 1 Axial magnetic resonance (MR) T
2
-weighted
image demonstrating endometrial cancer occupying the
whole endometrial canal (A), with hyperintensity at high
bvalue diffusion-weighted imaging (DWI) sequences (B).
612 S. Rizzo et al.

PET/CT may be of particular value in high-risk
patients. Indeed, Crivellaro et al.
[12]
showed moderate
sensitivity (78.6%), and high specificity and accuracy
(98.4% and 94.7%, respectively) of PET/CT in assess-
ment of nodal status of 76 high-risk patients with clinical
stage I endometrial cancer.
Dissemination routes
Nodal metastases from endometrial cancer involve pelvic
and para-aortic nodes. Tumors from the middle and infe-
rior uterus drain to the parametrial and obturator nodes,
whereas those from the proximal body and fundus drain
to the common iliac and para-aortic nodes
[13]
. Lymphatic
drainage from the uterus also occurs to obturator nodes,
and tumor can spread via the round ligament to inguinal
nodes as well. The likelihood of nodal spread increases in
the presence of greater than 50% invasion of the myome-
trium in comparison with those with a lesser amount of
invasion
[3]
.
Imaging reporting
The MRI report should include careful assessment of the
following features: depth of myometrial invasion; cervical
stromal invasion; local and/or regional spread and nodal
status; bladder, bowel mucosa, and/or presence of distant
metastases.
Depth of myometrial invasion (stage IAIB)
The T
2
-weighted and contrast-enhanced sequences, paral-
lel and perpendicular to the plane of the uterus, optimize
visualization of the endometrialmyometrial interface.
The normal endometrium is hyperintense on T
2
images,
whereas tumors are intermediate and heterogeneous in
signal intensity
[3]
. Compared with tumors, the inner myo-
metrium, also called the junctional zone (JZ), is hypoin-
tense on T
2
-weighted images (Fig. 2).
However, the JZ is not well seen in postmenopausal
women (Fig. 3), who represent the vast majority of
patients with endometrial cancer. In these cases con-
trast-enhanced scans, even with subtraction of native
images, are helpful (Fig. 3) because the tumor enhances
less than the normal myometrium, and the invasive
hypointense tumor extends into the myometrium, causing
irregularity and disruption of the enhancing JZ at the
endometrialmyometrial interface (Fig. 4)
[3]
. Maximum
contrast between hyperintense myometrium and hypoin-
tense endometrial tumor occurs 50120 s after adminis-
tration of contrast medium, and this is the most
important phase for accurate assessment of the depth
of myometrial invasion. Differential enhancement
within the endometrial cavity can allow distinction
between tumor, blood products, and debris.
In the revised FIGO staging system, tumors confined
to the endometrium and tumors invading the inner half
of the myometrium are staged as IA tumors, whereas
Figure 3 (A) Axial MR T
2
-weighted image showing diffi-
cult distinction of the inner part of myometrium (also called
the junctional zone) and consequent difficult delineation of
tumor margins (arrow) in a postmenopausal woman with
endometrial cancer. (B) Tumor is better delineated on sub-
tracted postcontrast MR T
1
-weighted image (arrow).
Figure 2 Axial MR T
2
-weighted image showing endome-
trial cancer hypointense to the endometrium and hyperin-
tense to the junctional zone (arrow).
Imaging results for gynecologic tumors 613

tumors invading the outer half of the myometrium are
staged as IB tumors
[4]
.
Cervical stromal invasion (stage II)
The normal cervical stroma is hypointense on
T
2
-weighted images (Fig. 5) and is replaced by
Figure 5 Sagittal (A) and para-axial (B) MR T
2
-weighted
images showing endometrial cancer extending to the
cervix, with preserved hypointense stromal ring, as con-
firmed by regular enhancement at dynamic postcontrast
T
1
-weighted image (C) in an endometrial carcinoma,
International Federation of Gynecology and Obstetrics
(FIGO) stage IIA.
Figure 4 (A) Para-axial MR T
2
-weighted image shows
endometrial cancer extending to the external part of the
myometrium, with disruption of the enhancing junctional
zone (arrows) at the endometrial-myometrial interface,
well delineated also in the dynamic postcontrast MR
T
1
-weighted image (arrows) (B).
614 S. Rizzo et al.

intermediate signal intensity tumor in the case of inva-
sion. Thin-section axial oblique images perpendicular to
the cervical canal improve the assessment of cervical
invasion. Delayed-phase images obtained 34 min after
administration of contrast medium may help the evalua-
tion of cervical stromal invasion (FIGO stage II). The
presence of an intact enhancing cervical mucosa excludes
stromal invasion (Fig. 5). The new FIGO classification
places endocervical glandular tumor extension into stage
I, and cervical stromal invasion into stage II
[4]
.
Local and/or regional spread and nodal
status (stage III)
Tumors that invade the serosa appear as an area of inter-
mediate to high signal intensity that disrupts the contour
of the outer myometrium. The use of DWI improves
depiction of extrauterine metastatic deposits. When
tumor extends into the vagina by direct invasion or meta-
static spread, a segmental loss of low signal intensity in
the vaginal wall on T
2
-weighted images may be seen
at MRI.
Tumors from the middle and inferior uterus drain to
the parametrial, external, and obturator nodes (Fig. 6),
whereas those from the proximal body and fundus drain
to the common iliac and para-aortic nodes. Endometrial
tumors may also spread to the inguinal nodes via the
round ligament. Imaging findings suggestive of nodal
involvement include a short-axis diameter greater than
10 mm, but size criteria have a wide range of sensitivities.
Other features suggesting nodal involvement are presence
of necrosis
[3,14]
, multiplicity, irregular contour, and signal
intensity similar to that of the primary tumor.
DWI may be used to depict drop metastases in the
cervix and vagina, and unexpected extrauterine spread
of disease within the adnexa (Fig. 7) and peritoneum.
It may also help the detection of positive nodes
[15,16]
.
CT performs as well as MRI in identifying extrauterine
spread and identifying nodal metastases.
Bladder, bowel mucosa, and/or distant
metastases (stage IV)
Extension of tumor directly into the normally hyperin-
tense vesical or rectal mucosa is indicative of endometrial
tumor invasion into the bladder or rectum
[2]
. Thickening
of the high-signal-intensity mucosal layer is not indicative
of mucosal invasion, whereas disruption of the hypoin-
tense muscularis layer does not indicate stage IV disease,
because it cannot be visualized at subsequent cystoscopy
or sigmoidoscopy
[2]
.
In summary, the combination of dynamic contrast-
enhanced and T
2
-weighted MRI, recommended by the
European Society for Urologic Research (ESUR) in its
guidelines for endometrial cancer staging, offers a one-
stop examination that gives surgeons a good estimate of
tumor burden that helps them tailor the necessary treat-
ment of patients with endometrial cancer.
Ovarian cancer
Ovarian cancer is the second most common gynecologic
malignancy in women in the United States after uterine
corpus, with an estimated 22,280 new cases and 15,500
deaths in 2012
[1]
.
Management of patients with ovarian
cancer
The optimal treatment for patients with ovarian cancer is
a complete cytoreduction followed by platinum-based
chemotherapy. There is no universal agreement on the
Figure 6 Sagittal MR T
2
-weighted image showing endo-
metrial cancer in the middle part of the uterine corpus,
invading the outer part of myometrium (A), which led
to nodal metastasis to obturator left lymph node (arrow),
as shown in the axial unenhanced MR T
1
-weighted
image (B).
Imaging results for gynecologic tumors 615

definition of optimal cytoreduction. However, recent stu-
dies have shown that no macroscopic residual disease
best correlates with prognosis and long-term sur-
vival
[17,18]
. Extensive disease requires surgery by trained
gynecologic oncology surgeons, at times supported by
general surgeons for complex liver and/or bowel resec-
tions. Since it is more appropriate for patients to undergo
an up-front debulking effort, instead of undergoing sur-
gery as a diagnostic procedure, it is mandatory for the
surgeon to know the exact extent of the disease prior to
take the patient to the operative room.
Neoadjuvant chemotherapy is a treatment option in
patients with medical comorbidities, stage IV disease,
or extensive tumor load. The presence of difficult-to-reach
sites that may preclude optimal debulking (Table 1) sug-
gests that the patient should undergo primary chemother-
apy. However, these criteria may vary, depending on the
aggressiveness of the surgical procedure and the perfor-
mance status of the patient; therefore, they should be
used according to multidisciplinary consensus and be
adapted to the single-institutional protocols
[19]
.
Preoperative evaluation
Ultrasonography (US), CT, and MRI may all be used in
the evaluation of ovarian cancer. Recently, the use of
PET/CT has also been considered of value in patients
with ovarian cancer.
US usually represents the first-level examination to
evaluate adnexal masses in both emergency and none-
mergency settings. Once an ovarian cancer mass has
been demonstrated, the next step is to stage the disease.
CT is currently considered the best imaging technique
for staging ovarian cancer, since it is widely available and
provides all the required information in a short examina-
tion time
[27]
. According to the ESUR guidelines
[28]
,CT
should be extended from the distal thorax to the inguinal
region. Inclusion of the lung bases in the field of view is
recommended because this enables assessment of cardio-
phrenic lymph nodes and pleural effusion
[29]
.
CT provides rapid image acquisition, with an overall
accuracy of 7090% for the detection of implants at all
disease stages
[20,21]
. The most important limitation of CT
is its inability to reliably depict implants with a maximal
diameter of less than 5 mm on the bowel serosa, mesen-
tery, or peritoneum, especially in the absence of
ascites
[20]
. Indeed, the detection rate for small peritoneal
lesions is poor, with reported sensitivities of only 750%
for those with a maximal diameter of less than
10 mm
[21,22]
.
CT and MRI techniques have comparable overall sen-
sitivity for the detection of malignant peritoneal deposits
(92% and 95%, respectively)
[23]
. MRI performed with fat
suppression, delayed contrast-enhanced acquisitions, oral
contrast agents, and functional imaging techniques may
allow diagnostic sensitivity higher than that achieved by
CT. Specifically, the addition of diffusion-weighted
sequences to gadolinium-enhanced MRI may improve
the accuracy of tumor detection, especially for the assess-
ment of mesentery, serosa of the small bowel and colon,
and pelvis (surface of the uterus and bladder)
[24]
, and
may also help to detect very small malignant deposits
[24]
.
However, given the cost, MRI is currently reserved for
selected cases, to characterize complex adnexal masses
and evaluate diffuse peritoneal spread
[20]
.
Recently, PET/CT has been introduced as a diagnostic
tool for patients with ovarian cancer. At staging, the con-
tribution of PET is limited to the improved detection of
lymphadenopathies on the basis of the degree of
[
18
F]fluorodeoxyglucose uptake in metastatic but
normal-sized pelvic and retroperitoneal lymph nodes
[25]
.
In a recent meta-analysis, PET/CT was shown to have
an important role in the evaluation of recurrent ovarian
cancer, with the highest pooled sensitivity (92%) when
compared with PET, CT, and MRI alone
[26]
. PET/CT is
particularly recommended when recurrence is suspected
(e.g., in the case of an increase in the cancer antigen 125
marker) and CT examination does not show disease.
Dissemination routes
The routes of spread of ovarian cancer are intraperitoneal
dissemination, direct invasion of adjacent organs, lym-
phatic spread, and hematogenous spread
[30]
.
Figure 7 Axial MR DWI image in a young patient under-
going staging for endometrial cancer shows hyperintense
left ovary (arrow), indicating presence of disease.
Table 1 Sites of disease that may preclude optimal
debulking in patients with ovarian cancer
Lymph node enlargement above the renal hilum and around the
celiac axis
Abdominal wall invasion
Parenchymal liver metastases
Implants of 42 cm in diaphragm, lesser sac, porta hepatis,
intersegmental fissure, gallbladder fossa, gastrosplenic ligament,
gastrohepatic ligament
Extensive involvement of the small bowel or mesenteric root
Pleural infiltration
Pelvic side-wall invasion
Bladder trigone
616 S. Rizzo et al.

Intraperitoneal dissemination generates seeding of
malignant cells in the Douglas pouch and paravesical
spaces, the paracolic gutters, the Morrison pouch, the
subdiaphragmatic spaces, and the omentum (Fig. 8)
[31]
.
Lymphatic spread may follow either the main lymphatic
ducts along the ovarian veins reaching the para-aortic and
paracaval nodes, the broad ligament reaching the pelvic
lymph nodes, or the round ligament reaching the inguinal
nodes
[32]
. Hematogenous dissemination is uncommon,
the most common sites of disease being the colon
(50%), liver (48%), small intestine (44%), and lung
(34%).
Imaging reporting
The goal of CT scanning at preoperative staging is to
indicate the bulk of disease, with special attention paid
to hard-to-reach sites (Table 1) such as extra-abdominal
lesions, porta hepatis, or mesenteric root lymph nodes, to
make clinicians aware of sites of disease that may pre-
clude optimal debulking
[33,34]
.
One way to constructively communicate imaging
results to the surgeons is by analyzing the abdomen
using a quadrant approach.
In the right upper quadrant, deposits on the liver sur-
face and in the peritoneal spaces, such as the Morrison
space and the gallbladder fossa, may be present (Fig. 9).
Multiplanar reformatting, especially in presence of
ascites, may facilitate the detection of diaphragmatic
nodules
[33,35]
. The presence of disease in the subdiaph-
ragmatic spaces does not preclude complete cytoreduc-
tion, but has to be indicated at preoperative imaging
because it may be missed at a first laparoscopic
approach. The presence of subcapsular implants in the
region extending between the Morrison pouch and the
inferior vena cava (Fig. 10) at the level of the right
hepatic vein must be specifically documented. Indeed,
these sites are at increased risk of intraoperative bleeding
and, according to single-institutional experience, may pre-
clude optimal debulking
[33]
.
In the left upper quadrant, attention should be paid to
deposits within the spleen, the subdiaphragmatic space,
and the lesser sac. Subcapsular splenic deposits produce
a scalloped appearance of the underlying peripheral
parenchyma and might be resected sparing the spleen
(Fig. 11), whereas focal hilar implants are frequently
associated with parenchymal invasion and may require
splenectomy (Fig. 12). The lesser sac is delineated by the
splenorenal ligament and the gastrosplenic ligament.
Involvement of these ligaments (Fig. 13) should be
reported because some surgeons consider these findings
as precluding optimal debulking
[33]
. The evaluation of
the upper quadrants should also include evaluation of
lower thorax, where cardiophrenic lymph nodes and
pleural effusion may be detected. Cardiophrenic lymph
nodes (Fig. 14) are considered enlarged when the short
axis is 45mm
[34]
. According to different institutional
protocols, these lymph nodes may or may not preclude
optimal debulking. Pleural effusion may be reactive to the
presence of malignant deposits on the abdominal dia-
phragmatic surface, although it might also indicate
Figure 8 Intraperitoneal dissemination generates seeding
of malignant cells from the ovaries to the paracolic gutters
(white arrows), in the Morrison pouch (dashed white
arrows), in the subdiaphragmatic spaces (black arrows)
and in the omentum (white arrowheads).
Figure 9 Axial computed tomography (CT) image show-
ing malignant deposits on the liver surface at the level of
the Morrison space (black arrow) and the gallbladder
fossa (white arrow).
Imaging results for gynecologic tumors 617

the presence of malignant cells on the pleural surface
(Fig. 14).
The area of the central abdomen should be carefully
evaluated for presence of lymphadenopathies, omental
deposits, and mesenteric root deposits. Since lymphade-
nectomy is not always performed as routine in patients
with ovarian cancer, indication of suspicious retroperito-
neal lymph nodes may suggest that surgeons perform it.
At present, a noninvasive method to recognize lymph
node metastases with certainty does not exist. However,
if CT shows the presence of lymph nodes with a short
axis 410 mm, suspicion of metastasis should be
raised
[37]
. Of note, retroperitoneal lymphadenopathies
above the renal vessels and around the celiac axis
(Fig. 15) may be difficult sites to resect, so their presence
must be emphasized to the surgeon. Omental deposits are
common in patients with ovarian cancer
[23]
. Imaging
signs of such involvement range from subtle infiltrative
stranding and discrete nodules to confluent masses, also
known as omental cake (Fig. 16). Omental lesions are
not considered a big challenge for surgeons, as they are
routinely removed during debulking surgery. However,
wide adhesions between the omentum and the small
bowel (Fig. 17), as well as lesions of the lesser sac,
may indicate potentially unresectable disease. The CT
appearance of mesenteric disease may vary greatly,
Figure 11 Axial CT image showing subcapsular splenic
deposits (arrows), which produce a scalloped appearance
of the peripheral splenic parenchyma.
Figure 10 Axial CT image showing hypodense lesion on
the posterior surface of the liver (arrow), close to the infe-
rior vena cava.
Figure 12 Axial CT image showing inhomogeneous con-
trast-enhanced lesion (arrow) infiltrating the splenic ves-
sels at the level of the hilum.
Figure 13 Axial CT image shows large and confluent
peritoneal lesions of the gastrosplenic ligament of the
lesser sac (arrows).
618 S. Rizzo et al.

Figure 15 Axial CT image showing pathologic enlarged
(short axis 410 mm) lymph node around the celiac axis
(arrow), which may preclude optimal debulking.
Figure 14 Axial enhanced CT images showing enlarged
right cardiophrenic lymph nodes (A) and small enhancing
nodules on the right pleural surface (arrow) suggesting
stage IV disease (B).
Figure 16 Axial CT images showing different appear-
ances of omental deposits: arrows indicate subtle and
tiny solid nodules infiltrating and stranding the hypodense
omentum (A) and confluent solid masses, also known as
omental cake (B).
Figure 17 Axial CT image showing a wide adhesion
between omental cake and the small bowel (arrows),
which precluded optimal debulking.
Imaging results for gynecologic tumors 619

from clustered small rounded soft-tissue densities
(Fig. 18) to confluent large irregular soft-tissue masses,
distributed around the superior mesenteric vessels
[33]
.
Extensive mesenteric involvement causes rigidity and
retraction, drawing the bowel loops together. A careful
assessment is required
[21,23,38]
because infiltration of the
mesenteric root precludes adequate surgical resection
[39]
.
This finding may also be detected and confirmed by DWI
at MRI examination (Fig. 19).
The pelvis is a frequent site of ovarian masses. A find-
ing suggestive of malignancy is the presence of solid
components (Fig. 20) and contrast-enhanced intranodu-
lar septa (thicker than 3 mm). However, the presence of
small ovaries does not exclude ovarian cancer, since
cancer may arise from the serosal surface of the ovary,
giving directly peritoneal spread with no large ovarian
masses (Fig. 21). Intraperitoneal dissemination generates
seeding of malignant cells in the Douglas pouch and
paravesical spaces. Although rare, any evidence of inva-
sion of the pelvic wall (suspected when the tumor lies
3 mm from the pelvic side wall) should be reported,
because the patient may deserve neoadjuvant chemother-
apy to reduce the bulk of the disease.
Imaging features of bowel involvement in patients with
ovarian cancer may include diffuse serosal infiltration
(Fig. 22A), nodular foci (Fig. 22B), mural thickening
(Fig. 22C), or masses involving the serosa and the adja-
cent mesentery. If the implants are tiny and located on
the serosal surface of the bowel, they may be indistin-
guishable from the bowel wall itself, and only indirect
signs of their presence may be seen, such as pelvic
free fluid. Bowel serosal deposits, frequently seen on
the sigmoid colon and the ileum, may be surgically
resected
[40]
or, depending on the extent of the involved
surface, may be considered an indication for neoadjuvant
chemotherapy
[33]
.
Cervical cancer
Cervical cancer is the third most common gynecologic
malignancy in women in the United States, after uterine
Figure 18 Axial CT image showing clustered small
nodules partially confluent (arrows) along the mesenteric
root. At surgery this infiltration precluded cytoreduction,
and the patient underwent neoadjuvant chemotherapy.
Figure 19 Axial DWI MR image at high bvalue (900)
showing hyperintensity of the mesenteric root (arrow) (A),
confirmed as diffusion-restricted area on apparent diffusion
coefficient (ADC) map (arrow) (B).
Figure 20 Axial CT image showing a large left adnexal
mass (arrow) with solid components, infiltrating the adja-
cent bowel, associated to the presence of pelvic free fluid.
620 S. Rizzo et al.

corpus and ovary, with an estimated 12,170 new cases and
4220 deaths in 2012
[1]
, squamous carcinoma being the
most frequent histologic type (85% and 15% of squamous
cell carcinomas and adenocarcinomas, respectively).
A preponderance of evidence supports a strong causal
link between human papillomavirus (HPV) (most com-
monly HPV types 16 and 18) infection and cervical
neoplasia
[41]
. The introduction of the vaccine against
high-risk HPV types will likely have a major impact on
disease prevention and prevalence
[42]
.
Management of patients with cervical
cancer
Early-stage tumors can be managed with cone biopsy or
simple hysterectomy (stage IA), whereas higher stage
tumors can be treated with either radical surgery/radio-
therapy (IB1IIA, 54 cm) or concomitant chemora-
diotherapy (IIBIVB).
Extension into the parametrium represents a key factor
for management because this is considered a contraindi-
cation to surgery. However, owing to newly introduced
targeted radiotherapy techniques, in some centers large
tumors, even those without parametrial invasion, have
increasingly been treated by chemoradiation therapy
[43]
.
In young patients willing to preserve fertility and with
small invasive tumors, a conservative surgical procedure
(such as trachelectomy) can be performed.
Figure 22 Axial CT images showing different appearances of bowel infiltration by ovarian cancer: inhomogeneous
enhancement of the bowel serosa (A); presence of enhancing nodular masses within the left pelvis (arrows) infiltrating
the distal part of the large bowel (B); presence of abnormal mural thickening of small bowel (arrow) (C).
Figure 21 Axial CT image showing large pelvic nodules
of carcinomatosis (black arrows), with a small solid right
adnexal mass (white arrow).
Imaging results for gynecologic tumors 621

Preoperative evaluation
FIGO staging of cervical cancer is entirely clinical and
does not rely on surgicopathologic findings. This is
mainly due to the need of a staging system that is uni-
versally available. Indeed, cervical cancer is more preva-
lent in developing countries, where more sophisticated
modalities are not available and where patients may not
undergo staging via surgical or diagnostic imaging
techniques.
The FIGO staging procedures include clinical exami-
nation of the cervix (under anesthesia, if necessary), col-
poscopy, lesion biopsy, cystoscopy, and rectoscopy when
indicated
[44]
. Conventional radiographic techniques
included in the FIGO staging are chest X-ray, barium
enema, and intravenous urography.
Since the introduction of the revised FIGO staging
[4]
incorporation of cross-sectional imaging has been encour-
aged, if available, to assess important prognostic factors
such as tumor size, parametrial involvement, adjacent
organ and pelvic side-wall invasion, and evaluation of
lymph node metastases. Specifically, MRI is considered
the best imaging modality to stage early cervical carci-
noma such as FIGO stage 1B1 or greater
[45]
.
According to the ESUR guidelines, the essential pro-
tocol, preferably performed using a 1.5-T magnet, must
include a combination of at least two T
2
-weighted
sequences (sagittal and oblique planes, perpendicular
to the long axis of the cervical canal), and one axial
T
1
-weighted sequence of the pelvis. Many investigators
also acquire at least one sequence from the level of the
renal veins to the pelvic brim so as to obviate an addi-
tional CT examination for evaluation of retroperitoneal
adenopathies and hydronephrosis
[44,46]
.
The use of contrast-enhanced T
1
-weighted sequences is
variable in different centers
[45]
. Evaluation of the earlier
phases of contrast enhancement may help to accurately
delineate small cervical tumors
[47]
. The use of intrave-
nous contrast medium is also recognized as helpful in
the posttreatment setting, to differentiate residual or
recurrent tumor from radiation fibrosis
[6]
.
DWI seems to be a promising technique in the evalu-
ation of cervical cancer
[48,49]
. Cervical cancer shows a
lower ADC in comparison with the normal cervix
(Fig. 23), and the ADC increases after chemoradiother-
apy
[48,50]
. DWI has been considered helpful in the detec-
tion of residual tumor or suspicious lymph nodes after
chemoradiotherapy, and in some cases might be compet-
itive with PET imaging
[9,51]
. However, there is still lack of
standardization of the bvalues used in different centers,
and some applications of DWI still remain confined to
the research setting
[9]
.
PET/CT could be helpful at staging to detect lymph
node and extranodal metastases. However, PET/CT has
limited value in terms of detection of local spread
because of its limited spatial resolution. Data show
better detection of para-aortic involvement with PET
than with MRI or CT
[52]
. In a meta-analysis, sensitivity
Figure 23 Axial MR ADC map showing hypointensity of
cervical cancer (arrow), in comparison with the surround-
ing normal cervix.
Figure 24 Axial (A) and sagittal (B) MR T
2
-weighted
images showing hyperintense FIGO stage IB1 cervical
tumor preserving the hypointense cervical stroma
(arrows).
622 S. Rizzo et al.

of PET reached 73% when the prevalence of lymph
node involvement was more than 15%
[54]
. However, in
patients with negative morphologic imaging, sensitivity of
PET/CT for detection of microscopic lymph node metas-
tases was much lower (almost 34%)
[53]
.
Dissemination routes
Cervical cancer spreads regionally by direct extension to
contiguous structures, such as uterine corpus (stage I),
vagina (stage IIAIIIA), and parametrium (stage IIB). It
can also spread through lymphatic channels to regional
nodes (firstly to iliac and obturator nodes, secondarily to
para-aortic lymph nodes) and, rarely, through hematogen-
ous dissemination to distant organs (stage IVB)
[54]
.
Imaging reporting
The ESUR committee has suggested a checklist to follow
to provide a comprehensive and easy-to-read radiologic
report, helpful in communication with the surgeons when
tailoring treatment options
[45]
. Indeed, to better stage
cervical cancer, MRI may add important information to
the clinical FIGO staging.
Cervical carcinoma appears isointense to the cervical
stroma on T
1
-weighted images, whereas it shows high
signal intensity, surrounded by low signal intensity of
the cervical stroma, on T
2
-weighted images (Fig. 24).
Accurate description of the lesion, including size of the
tumor (the largest size, transversal or longitudinal, indi-
cates T parameter) and distance from the internal os,
must be reported. MRI is particularly helpful in evalua-
tion of patients being considered for fertility-preserving
treatments (i.e., extended cone biopsy or trachelectomy).
In these cases, specific information required comprises
tumor size 52 cm, cervical length 42.5 cm, distance of
the tumor from the internal os 41cm
[45]
.
Vaginal invasion is detected when the normal low
signal intensity of the vaginal wall is replaced by
the high-signal-intensity tumor on T
2
-weighted images
(Fig. 25).
Presence of parametrial invasion, suspected when there
is disruption of the stromal ring (high NPV and moderate
to high PPV), is best demonstrated on oblique axial high
resolution images (Fig. 26). Additional features indicat-
ing parametrial invasion include: spiculated tumor-para-
metrium interface; soft-tissue extension into the
parametria and along the cardinal or uterosacral liga-
ments (Fig. 26); encasement of the periuterine vessels;
and hydro-ureteronephrosis (Fig. 27)
[55]
.
Isthmic invasion, difficult to evaluate by clinical evalu-
ation, should be indicated because this information may
suggest where to locate the brachytherapy coils
[56]
.
Bladder and/or rectal involvement are diagnosed when
there is disruption of the normal hypointense walls on
Figure 25 Sagittal MR T
2
-weighted image showing a
large cervical cancer infiltrating the lower third of the
vagina (arrow) and the upper third of the urethra.
Figure 26 Axial MR T
2
-weighted images showing: disrup-
tion of the stromal ring on the left (arrow) and initial
thickening of the ipsilateral parametrium by a FIGO
stage IIB cervical cancer (A); large cervical cancer invad-
ing parametria associated with thickening of the right
uterosacral ligament (arrow) (B).
Imaging results for gynecologic tumors 623

T
2
-weighted images, with or without a mass protruding
into the lumen. Pelvic side-wall invasion is likely when
the tumor extends within 3 mm of the pelvic side wall
(internal obturator, piriform, or levator ani muscles),
with or without hydronephrosis.
Staging of lymph nodes, based on the size criterion
(10 mm in short axis) still gives a low accuracy to MRI
in the assessment of nodal status (reported ranges of
sensitivity and specificity of 3889% and 7899%,
respectively)
[57,58]
. The presence of intranodal necrosis
may be an adjunctive feature suggesting nodal metastasis.
Conclusion
Imaging is crucial in gynecologic malignancies, for diag-
nosis as well as for arriving at the decision regarding the
best treatment options available. Accordingly, if surgery
is the best treatment option, accurate preoperative ima-
ging assessment allows the surgeon to ensure the most
appropriate surgical procedure for the patient. Greater
involvement in multidisciplinary approaches and team-
work may reduce undertreatments and complications
due to overtreatments, thus eventually increasing patient
survival and quality of life.
Conflict of interest
The authors declare that they have no conflicts of
interest.
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