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1
Department of Diagnostic Radiology and Organ Imaging, Chinese University of
Hong Kong, Prince of Wales Hospital, Shatin, New Territories, Hong Kong.
2
Department of Anatomical and Cellular Pathology, Chinese University of Hong
Kong, Prince of Wales Hospital, Shatin, New Territories, Hong Kong.
3
Department of Obstetrics and Gynecology, Chinese University of Hong Kong,
Prince of Wales Hospital, Shatin, New Territories, Hong Kong.
Received November 8, 1999;
accepted after revision February 8, 2000.
Address correspondence to W. T. Yang.
Abstract
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SUBJECTS AND METHODS. Women with biopsy-proven cervical carcinoma prospectively underwent dynamic helical CT and MR imaging before surgery. A metastatic node on CT and MR imaging was defined as a rounded soft-tissue structure greater than 10 mm in maximal axial diameter or a node with central necrosis. Imaging results were compared with pathology, and receiver operating characteristic curves for size and shape were plotted on a hemipelvis basis. Nodal density and signal intensity on CT and MR images, respectively, were reviewed for differences between benign and malignant disease.
RESULTS. A total of 949 lymph nodes were found at pathology in 76 hemipelves in 43 women, of which 69 lymph nodes (7%) in 17 hemipelves (22%) were metastatic. Sensitivity, specificity, positive and negative predictive values, and accuracy of helical CT and MR imaging in the diagnosis of lymph node metastasis on a hemipelvis basis was 64.7%, 96.6%, 84.6%, 90.5%, and 89.5% and 70.6%, 89.8%, 66.7%, 91.4%, and 85.5%, respectively. Receiver operating characteristic curves for helical CT and MR imaging gave cutoff values of 9 and 12 mm in maximal axial diameter, respectively, in the prediction of metastasis. Central necrosis had a positive predictive value of 100% in the diagnosis of metastasis. Signal intensity on MR imaging and density—enhancement pattern on CT in patients with metastatic nodes did not differ from those in patients with negative nodes.
CONCLUSION. Helical CT and MR imaging show similar accuracy in the evaluation of pelvic lymph nodes in patients with cervical carcinoma. Central necrosis is useful in the diagnosis of metastasis in pelvic lymph nodes in cervical cancer.
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Helical CT Protocol
Helical CT examinations were performed on a HiSpeed Advantage scanner
(General Electric Medical Systems, Milwaukee, WI) with the following protocol.
An unenhanced scan was obtained cephalad from the symphysis pubis to the iliac
crest at 7-mm slice thickness, 1.5:1 pitch, and 7-mm reconstruction interval.
A bolus of 120 mL of IV contrast material (iopromide 240 [Ultravist 240];
Schering, Berlin, Germany) was administered using an automatic injector: the
first 100 mL were delivered at a rate of 2.5 mL/sec and the remaining 20 mL at
0.5 mL/sec. Data acquisition was divided into two parts: at 40 sec after the
start of contrast material injection, offering a good arterial phase, and at
180 sec after injection, when veins are optimally enhanced. Scanning was
performed during inspiration using the following parameters: field of view,
320-340 mm; 120 kV; 250-300 mA; matrix, 512 x 512; and a soft-tissue
algorithm reconstruction.
MR Imaging Protocol
MR examinations were performed on a 1.5-T scanner (Gyroscan ACS-NT; Philips
Medical Systems, Best, The Netherlands) using a body coil. All patients
underwent an axial T1-weighted spin-echo sequence (TR/TE, 550/15; field of
view, 350-450 mm; slice thickness, 5 mm with 0.5-mm interslice gap), an axial
turbo spin-echo T2-weighted short-tau inversion recovery sequence (1800/100;
inversion time, 180 msec; field of view, 350-450 mm; slice thickness, 6 mm
with 1.2-mm interslice gap), and a sagittal turbo spin-echo T2-weighted
sequence (2500/150; field of view, 300-450 mm; slice thickness, 4 mm with
0.4-mm interslice gap). Turbo spin-echo dynamic axial scans (500/12 and 4-mm
thickness with no interslice gap) were obtained immediately after hand
injection of 0.1 mmol/kg of gadolinium (Magnevist; Schering) at a rate of 2
mL/sec. A total of six dynamic scans were obtained with an acquisition time of
3 min 45 sec.
Interpretation of Helical CT and MR Images
Both helical CT and MR images were interpreted by two radiologists by
consensus and without knowledge of the findings of the other technique or of
final pathologic diagnosis. For the interpretation of helical CT and MR
images, identification of lymph nodes was conducted on the CT and MR consoles,
with unenhanced arterial and venous phase slices on helical CT arranged
consecutively for the same level. All helical CT and MR images were recorded
on hard copy (3M Medical Imaging Systems, St. Paul, MN) laser images for
reevaluation and cross-reference as necessary. The presence of all pelvic
nodes along the iliac (common, internal, and external) chains was noted
regardless of size. Then, the following criteria for the diagnosis of
metastasis in pelvic nodes were used: maximal axial diameter of more than 10
mm and the presence of central necrosis regardless of nodal size. On both
unenhanced and enhanced CT, central necrosis was defined as a central density
of less than 20 H (Figs.
1A,1B,1C);
on MR imaging, as an intranodal isointense (to water) area on both T1- and
T2-weighted images (Fig. 1D)
that showed no enhancement after contrast material administration (Fig.
2A,2B).
The minimal axial diameter of each lymph node identified on helical CT and MR
imaging was also documented, and the maximal axial diameter-minimal axial
diameter ratio was calculated. In addition, receiver operating characteristic
(ROC) curves on size and shape (maximal axial diameter-minimal axial diameter
ratio) were plotted to verify the accuracy of published cutoff values.
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Dynamic Imaging Evaluation
The inherent nodal tissue contrast as determined by attenuation value and
signal intensity on helical CT and MR imaging, respectively, was assessed on
unenhanced images. Enhancement pattern of the largest node per anatomic
(common, internal, and external iliac) chain was assessed after
contrast-enhanced dynamic CT and MR imaging. The attenuation value of each
node was compared on the unenhanced, arterial phase, and venous phase helical
CT scans. For each node visualized on MR imaging, the signal intensity before
and after the administration of contrast material was noted. Of a total of six
scans, the dynamic scan in which the greatest rate of enhancement occurred was
also noted. In nodes with an area of low density on CT or water isointensity
on MR imaging, respectively, measurements were made from the noncystic portion
of the node.
Pathology
All patients subsequently underwent pelvic lymph node dissection with
anatomic labeling into common, internal, and external iliac groups with
evaluation by a single pathologist. The total number of lymph nodes, number of
metastatic nodes, and maximum size of the largest metastatic lymph node were
documented. The imaging findings were compared with histology, and the
accuracy of each technique in each hemipelvis was determined.
Statistics
For the purpose of calculations of accuracy and ROC analysis of nodal size
and shape, findings were considered true-positive on CT or MR imaging if nodes
in a hemipelvis met the size criterion or showed the presence of central
necrosis (or both) and if at least one positive node was found at dissection
anywhere in that hemipelvis. Findings were considered false-positive on CT or
MR imaging if nodes in a hemipelvis met the size criterion or showed the
presence of central necrosis (or both) and no metastatic node was found at
dissection anywhere in that hemipelvis. Findings were considered
false-negative on CT or MR imaging if nodes in a hemipelvis did not meet the
size criterion or did not show the presence of central necrosis (or both) and
if a metastatic node was found at dissection anywhere in that hemipelvis.
Findings were considered true-negative on CT or MR imaging if nodes in a
hemipelvis did not meet the size criterion or did not show the presence of
central necrosis (or both) and if no metastatic node was found at dissection
anywhere in that hemipelvis.
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Accuracy Using Standard Published Criteria for Size
Helical CT revealed a total of 108 lymph nodes, of which 26 (24%) were
diagnosed as metastatic. MR imaging revealed a total of 380 nodes, of which 40
(11%) were diagnosed as metastatic. Therefore, 76% (82/108) of the nodes
identified on CT had a maximal axial diameter of less than 10 mm, whereas 90%
(340/380) of the nodes seen on MR imaging had a maximal axial diameter of less
than 10 mm. The results of helical CT diagnosis of metastatic lymph nodes on a
hemipelvis basis were as follows: sensitivity, specificity, positive and
negative predictive values, and accuracy were 64.7%, 96.6%, 84.6%, 90.5%, and
89.5% compared with 70.6%, 89.8%, 66.7%, 91.4%, and 85.5%, respectively, for
MR imaging (Table 1). There
were two false-positive and six false-negative findings each using helical CT,
and six false-positive and five false-negative findings using MR imaging
(Tables 2 and
3).
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ROC Verification
Size.—The ROC curves for size on helical CT and MR imaging
are shown in Figures 3 and
4. Optimal maximal axial
diameter and minimal axial diameter for helical CT was 9 and 8 mm,
respectively, with accuracy profiles (sensitivity, specificity, positive and
negative predictive values, and accuracy) of 70.6%, 85.7%, 66.7%, 87.8%, and
81.4% and 64.7%, 81.0%, 57.9%, 85.0%, and 76.3%, respectively
(Table 4). Optimal maximal
axial diameter and minimal axial diameter for MR imaging was 12 and 8 mm,
respectively, with accuracy profiles (sensitivity, specificity, positive and
negative predictive values, and accuracy) of 82.4%, 79.3%, 53.9%, 93.9%, and
80.0% and 76.5%, 81.0%, 54.2%, 92.2%, and 80.0%, respectively
(Table 5).
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Shape.—The optimal maximal axial diameter-minimal axial diameter ratio using both helical CT and MR imaging was 1.3 and gave sensitivity, specificity, positive and negative predictive values, and accuracy of 41.2%, 85.7%, 53.9%, 78.3%, and 72.9% and 47.1%, 86.2%, 50.0%, 84.8%, and 77.3%, respectively (Table 6).
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Central Necrosis
Central necrosis was seen on CT in seven (27%) of 26 and on MR imaging in
seven (17.5%) of 40 abnormal lymph nodes, all of which were pathologically
metastatic. These nodes were seen in a total of nine hemipelves, all of which
had metastasis at pathology. Therefore, the presence of central necrosis had a
positive predictive value of 100% in the diagnosis of metastasis. Pathologic
confirmation of necrosis in metastatic nodes from the anatomic chain
corresponding to imaging was available in five nodes. The mean size (maximal
axial diameter) of nodes with central necrosis on CT was 2.3 cm, with six of
seven nodes measuring more than 2 cm. The mean size (maximal axial diameter)
of nodes with central necrosis on MR imaging was 1.9 cm with four of seven
nodes measuring more than 2 cm. Five nodes with necrosis seen on CT or MR
imaging (or both) had confirmation of nodal necrosis in a metastatic node from
the same anatomic chain at pathology. Two nodes diagnosed as necrotic on CT
(maximal axial diameter of 2.5 and 2.1 cm) were enlarged but not necrotic on
MR imaging. Similarly, two necrotic nodes that were seen on MR imaging
(maximal axial diameter of 2 and 1.5 cm) were enlarged on CT but did not
appear necrotic.
Signal Intensity
The scatterplot of signal intensity measurements obtained from 146 lymph
nodes is shown in Figure 5. The
mean unenhanced signal intensity of nodes from patients with metastasis at
pathology (704 ± 224) was significantly different compared with that of
nodes from patients with benign pathology (833 ± 252) (p =
0.01). However, the enhanced signal intensity of nodes from the metastatic
(1101 ± 260) and benign (1143 ± 278) groups of patients showed
no significant difference (p = 0.4). Likewise, the difference in
unenhanced and enhanced intensity for benign and malignant groups was not
significant (p = 0.09).
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Analysis of the ranking of peak rate or highest gradient of enhancement out of six dynamic MR images showed no significant difference between benign and malignant groups (Wilcoxon's rank sum test, p = 0.5), with the mean ranking for both groups obtained on the third dynamic scan (Fig. 6).
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Dynamic Helical CT
All nodes measured in this study showed enhancement after administration of
contrast material. The mean nodal attenuation value from the benign group was
37.2 H (95% confidence interval [CI], 28.0-46.4) on unenhanced images,
increasing to 59.9 H (95% CI, 43.4-76.4) on the arterial phase images, and to
65.6 H (95% CI, 45.9-85.3) on the venous phase images. For the metastatic
group, the mean nodal attenuation value was 35.5 H (95% CI, 16.4-54.6) on
unenhanced images, increasing to 61.5 H (95% CI, 23.0-99.9) on the arterial
phase images, and to 64.5 H (95% CI, 34.1-94.9) on the venous phase images. No
difference in attenuation value was noted between nodes from patients with
benign and malignant disease on all three (unenhanced, arterial, and venous)
sets of dynamic images (p > 0.05).
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Number of Nodes Identified
MR imaging identified a significantly greater overall number of lymph nodes
(n = 380) compared with helical CT (n = 108). Most MR
imaging-detected nodes (90%) had a maximal axial diameter of 1 cm or less,
compared with 76% of nodes with a maximal axial diameter of 1 cm or less when
using CT. A possible reason for this discrepancy is likely related to the
slice thickness used with CT and MR imaging. Axial MR images used a slice
thickness of 4 mm compared with an effective slice thickness of 10.5 mm on
helical CT (7-mm slice thickness and 1.5:1 pitch). The higher
resolution—related to lower slice thickness on MR imaging—would
enable greater visualization of smaller nodes. The scanning parameters for the
helical CT protocol were considered optimal considering the scanning time,
tube cooling, and radiation dose for dynamic arterial and venous phase
scanning. These parameters will likely improve with newer generation scanners,
which will have a much smaller effective collimation (almost 5 mm) and will
not be limited by concerns for tube cooling and scanning time. Further reasons
that may explain the discrepancy in visibility of the number of lymph nodes
include the ability of MR imaging to differentiate blood vessels from lymph
nodes and the ability of multiplanar MR sequences to offer three-dimensional
evaluation.
Size and Shape
The only generally accepted CT and MR imaging criterion in the diagnosis of
metastatic pelvic lymphadenopathy is size
[15,16,17,18].
Diameter limits ranging from 6 to 15 mm have been used, with 10 mm being the
most commonly used criterion for the upper limit of a normal lymph node
[15,16,17,18].
A minimal axial diameter of more than 1-1.5 cm has been found to be the most
valid criterion for detection of metastatic cervical lymph nodes
[19]. The highest reported
accuracy rate of 93%, to date, for MR diagnosis of metastatic pelvic nodes in
cervical cancer was achieved using a minimal axial diameter of more than 10 mm
[1]. In this study, both
maximal axial diameter and minimal axial diameter were equal in diagnostic
accuracy, with optimal values of 9 and 8 mm, respectively, using helical CT
and 12 and 8 mm, respectively, using MR imaging.
It is accepted that neither MR imaging nor helical CT can depict small metastatic deposits in normal-sized nodes [18]. Additional criteria besides diameter include asymmetry and a rounded or spheric shape. Knowledge of the configuration of lymph nodes would be useful in the evaluation of relatively large (>10 mm) lymph nodes. The maximal axial diameter-minimal axial diameter ratio using both CT and MR imaging showed poor sensitivity in this study. This result may be explained by the fact that axial CT and MR images are not likely to show the maximum cross section of lymph nodes compared with other imaging techniques such as sonography.
Central Necrosis
Central necrosis was seen in 27% and 17% of all abnormal nodes in helical
CT and MR imaging, respectively, and had a positive predictive value of 100%
for metastasis in this study. Most of the necrotic nodes had a maximal axial
diameter of greater than 2 cm, although necrotic nodes were generally smaller
on MR imaging (mean maximal axial diameter, 1.9 cm) than on CT (mean maximal
axial diameter, 2.3 cm). Two necrotic nodes that were seen on CT did not
appear necrotic on MR imaging. It is possible that the presence of
proteinaceous fluid within these nodes resulted in a signal intensity that was
less isointense to water. Also, two necrotic nodes that were seen on MR
imaging did not appear necrotic on CT. These areas of necrosis may have been
less evident on CT because a greater slice thickness was used. To the best of
our knowledge, we are not aware of any reports in the literature describing
the presence of central necrosis in abdominal or pelvic lymph nodes in
cervical cancer when using helical CT or MR imaging. This feature—of
heterogeneous enhancement of nodes with rim enhancement—may prove useful
in differentiating benign from malignant disease because all nodes with
necrosis on helical CT and MR imaging were proven to be metastatic in this
study.
Helical CT
Attenuation of lymph nodes.—Attenuation of lymph nodes on
helical CT is important because lymph nodes are recognized primarily by the
difference between their attenuation and that of surrounding fat. Most lymph
nodes in this study were isodense to muscle on unenhanced images, with no
hyperdense (to muscle) nodes noted.
Contrast enhancement.—Contrast-enhanced helical CT has not, to our knowledge, been assessed in the evaluation of pelvic lymph nodes in cervical cancer. Patients are advanced through the scanner at a continuous rate, thus eliminating interscan delay and respiratory misregistration with helical CT. With bolus contrast administration and rapid volumetric data acquisition during peak vascular enhancement, opacification of major pelvic arteries and veins is excellent [20]. It would seem reasonable to expect increased diagnostic confidence in differentiating vessels from lymph nodes. In the pelvic cavity, there is a long interval between the injection of contrast material and the time of maximum enhancement of veins. Two-phase helical CT was performed in this study to address the difference in time of maximal enhancement between arteries and veins. No significant difference in the attenuation value of the nodes in patients with benign and malignant disease was noted on arterial and venous phase scans. Likewise, the difference in the attenuation value from arterial to venous phase was not different in nodes from patients with benign and from those with malignant disease. It may thus be impossible to differentiate between true- and false-positives by contrast enhancement or density alone. The additional cost of two-phase CT does not seem justified by the lack of additional advantage. "Later" (venous phase) imaging is probably the most important for lymph node detection to differentiate nodes from unopacified veins [21] and therefore is probably preferred if single-phase imaging is used in the pelvis.
MR Imaging
Signal intensity.—The MR characteristics of enlarged nodes
have been described as homogeneous on enhanced T1-weighted images. The
presence of central necrosis, best shown on fat-suppressed and unenhanced
T2-weighted sequences, has previously been described as unhelpful in
differentiating metastatic from nonmetastatic pelvic nodes in cervical cancer
[1]. Our findings in this study
suggest that central necrosis may prove to be of value in the diagnosis of
metastatic pelvic nodes in cervical cancer. Despite a lower unenhanced signal
intensity in malignant nodes when compared with benign nodes, significant
overlap in signal intensity for benign and malignant nodes was observed. Thus,
the ability of MR imaging to characterize lymph nodes on the basis of tissue
characteristics as established by signal intensity appears limited. It seems
likely that increased size (generally >1 cm) and morphologic changes will
remain the primary parameters for identifying abnormal nodes on MR
imaging.
Contrast enhancement.—MR imaging in the neck has shown heterogeneity of signal intensity on T2-weighted and contrast-enhanced T1-weighted images to be a good indicator of metastases in cervical nodes [18, 22, 23]. Heterogeneity of signal intensity has also been noted within a pelvic node in a patient with non-Hodgkin's lymphoma that correlated with central necrosis on CT [24]. Other authors have found it difficult to categorize pelvic lymph nodes on T2-weighted images because of artifacts and poor definition of nodes [1]. Our findings confirm previous findings that there is no significant difference in the degree of contrast enhancement in nodes from patients with metastatic and from those with nonmetastatic disease [1]. The role of dynamic contrast-enhanced MR imaging in the diagnosis of metastatic pelvic lymph nodes appears to be limited. The rate of enhancement, as well as time of peak enhancement as determined by the slice number in the dynamic sequence, showed no difference in nodes from patients with metastatic and from those with nonmetastatic disease.
In conclusion, size as determined by maximal axial diameter and minimal axial diameter was a good discriminant between benign and malignant lymphadenopathy, but shape as determined by the maximal axial diameter-minimal axial diameter ratio was not effective. Central necrosis had a positive predictive value of 100% in the diagnosis of metastasis in pelvic lymph nodes in this study and may be a valuable diagnostic feature when present on both helical CT and MR imaging. In patients with metastatic nodes at pathology, the density-enhancement pattern on CT and the signal intensity on MR imaging did not differ from measurements obtained from patients with benign nodes. The limitation of this observation however is the issue of pathologic proof of benign versus malignant nodes because individual nodes were not specifically sampled on CT and MR imaging. Obtaining histology of individual nodes identified on CT or MR imaging will likely remain technically challenging, although the advent of laparoscopic guidance for pelvic lymph node biopsy may provide a tool by which to sample suspicious nodes identified at cross-sectional imaging.
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