DOI:10.2214/AJR.04.0651
AJR 2005; 185:1152-1158
© American Roentgen Ray Society
Diagnosis of Gastric Cancer with MDCT Using the Water-Filling Method and Multiplanar Reconstruction: CT–Histologic Correlation
Kensaku Shimizu1,
Katsunori Ito,
Naofumi Matsunaga,
Ayame Shimizu and
Yasuhiko Kawakami
1 All authors: Department of Radiology, Yamaguchi University School of Medicine,
1-1-1 Minamikogushi, Ube, Yamaguchi 755-8505, Japan.
Received April 26, 2004;
revised December 6, 2004;
Address correspondence to K. Shimizu.
Abstract
OBJECTIVE. The purpose of this study was to assess the utility of
MDCT with a thin-sliced multiplanar reconstruction (MPR) technique and
water-filling method for the diagnosis of gastric cancers.
MATERIALS AND METHODS. Sixty-five patients with gastric cancers were
preoperatively examined with MDCT using the water-filling method. The abdomen
was dynamically scanned at 30 and 80 sec after the start of contrast medium
administration. MPR images were reconstructed with a slice width of 1.25 mm
and a slice interval of 1 mm. The detection rate and accuracy of T staging for
gastric cancer were evaluated on MPR images and compared with 5-mm-slice axial
images. In addition, MDCT images were correlated with pathologic findings.
RESULTS. The detection rate of all gastric cancers using the MPR
technique was 65%. The detection rate of advanced gastric cancers was 96.2%
(25 of 26), whereas that of early gastric cancers was 41.2% (14 of 34). There
was a statistically significant difference (p < 0.05) in the
detection rate of early gastric cancers between MPR and 5-mm-slice axial
images. The MDCT appearances of gastric cancers were well correlated with
pathologic findings such as mucinous component or differences in infiltration
of cancer cells. The overall accuracy of CT staging was 85%. MPR images were
superior to axial images for the evaluation of the z-axis extent of
tumor.
CONCLUSION. MDCT with the water-filling method has advantages in
acceptable evaluation of depth invasion of gastric carcinomas and in
visualization of histologic changes in the tumors. MPR images may be a useful
guide for the evaluation of the z-axis extent of tumor.
Introduction
Conventional CT has been considered unsuitable for the detection and
staging of gastric cancer and has been limited to the evaluation of lymph
nodes or distant metastasis. MDCT, which has recently been introduced into
clinical CT practice, allows a high speed of scanning, resulting in increased
z-axis coverage, and routine use of thin slice collimation during a
breath-hold acquisition. As a result, the quality of multiplanar
reconstruction (MPR) images obtained using thin slice collimation has
dramatically improved. High-quality MPR images allow visualization of the fine
anatomic details of the gastric wall in any plane.
Studies have indicated that the water-filling method with gastric CT allows
clear depiction of the gastric wall and gastric tumor without overshooting
artifacts by air in the lumen
[1–5].
The combination of high-quality MPR with the water-filling method has the
potential to improve diagnostic performance for detecting lesions and
determining the depth of invasion of gastric carcinomas. In this study, CT
findings of gastric carcinomas shown by MDCT performed using MPR techniques
and the water-filling method were correlated with pathologic findings to
assess the utility and limitations of MDCT for the diagnosis of gastric
carcinoma.
Materials and Methods
Patients
Sixty-five patients with pathologically proven gastric cancers were
examined with MDCT using the water-filling method between May 2000 and
November 2002. In five patients, gastric cancer was not resected and they were
excluded from this study. Surgical or endoscopic resections were performed in
60 patients at our institute within 1 month after CT examination. The study
group was composed of 44 men and 16 women who ranged in age range from 29 to
87 years (mean, 62.7 years). Pathologically, the tumors were classified as pT1
(invasion to the mucosa or the submucosa) in 34 patients, pT2 (invasion to the
proper muscle) in 12 patients, pT3 (invasion to the serosa) in nine patients,
and pT4 (invasion to adjacent organs or structures) in five patients.
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Fig. 1A —69-year-old man with protruding type of early gastric cancer.
Coronal multiplanar reconstruction shows gastric wall as three-layer structure
on CT. High-attenuating tumor (arrows) is adjacent to third layer. *
= inner layer with high attenuation, ** = middle layer with low attenuation,
*** = outer layer with isoattenuation.
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Fig. 1B —69-year-old man with protruding type of early gastric cancer.
Photomicrograph shows inner layer corresponds to mucosa (*), middle layer to
submucosa (**), and outer layer to proper muscle with serosa (***). Tumor is
adjacent to proper muscle (arrows), as shown on multiplanar
reconstruction (A).
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Scanning Technique
All examinations were performed with an MDCT scanner (Volume Zoom,
Siemens-Asahi Medical). All patients ingested 300–600 mL of tap water to
distend the stomach just before CT. CT scans were obtained with the patient in
the prone position in 57 patients, and they were acquired with the patient in
the supine position in the remaining three patients with the tumor located in
gastric fundus to effectively opacify the lesions by water. After undergoing
unenhanced CT, each patient received 100 mL of nonionic contrast medium IV by
means of a mechanical power injector (Autoenhance A-50, Nemotokyourindo) for
the contrast-enhanced study. Contrast material was injected at a rate of
2.8–3.0 mL/sec with a monophasic rate of injection. Two-phase scanning
was begun 30 and 80 sec after the start of the injection. MDCT was performed
in a breath-hold acquisition during each phase with parameters of 4 x 1
mm collimation and 8 mm/sec table speed. Images were reconstructed at 5-mm
intervals for the screening of the abdomen. In addition, thin-slice
reconstruction was performed with a slice width of 1.25 mm and a slice
interval of 1 mm as source images for MPR of the stomach. Then, MPR images
were routinely obtained in the coronal and sagittal directions with a slice
width of 1.25 mm and a slice interval of 1 mm. MPR images sliced in two
directions (coronal and sagittal views) and thin-slice axial source images
were displayed on a workstation connected to the CT unit.
Image Analysis
Images were interpreted by two independent radiologists experienced in
abdominal CT without prior knowledge of endoscopic, surgical, or histologic
findings. Disagreements in their interpretations were resolved by consensus
after discussion under the attendance of a third radiologist as a tiebreaker.
The review procedure was performed during two separate sessions. First,
5-mm-slice axial images were reviewed for the presence of tumor. During the
second session, the reviewers reviewed thin-slice MPR images sliced in two
directions (coronal and sagittal views) with thin-slice axial images to
evaluate the value of MPR images for the detection of tumor. During the third
session, thin-slice MPR images with thin-slice axial images were reviewed to
determine the depth of invasion of the tumor.
When the presence of gastric tumor was suspected, oblique MPR images
perpendicular to the gastric wall at the suspected region were, in addition,
reconstructed for the evaluation of depth invasion. The presence of tumor and
depth of invasion were evaluated on the basis of changes in the layer
structure of the gastric wall. Typical CT findings of the normal layer
structures of the gastric wall are shown in Figure
1A,
1B. CT revealed a three-layered
structure consisting of an inner layer with high attenuation, a middle layer
with low attenuation, and an outer layer with intermediate attenuation between
an inner and a middle layer. The presence of tumor was suspected if thickening
or irregularity of an inner layer of the gastric wall was evident or wall
thickening with abnormal contrast enhancement was evident.
Staging of depth invasion and corresponding CT findings were as follows: T1
(invasion to the mucosa or the submucosa), when the tumor was not visible on
CT or the tumor was confined to the inner or middle layer of the gastric wall;
T2 (invasion to the proper muscle), when the tumor invasion extended to the
outer layer or outer surface of the gastric wall but the outer surface of the
gastric wall was smooth; T3 (invasion to the serosa), when a nodular or
irregular outer surface of the gastric wall or perigastric infiltration was
evident; and T4 (invasion to adjacent organs and structures), when direct
extension or invasion of the tumor into a contiguous organ or structure was
evident. CT findings of tumors were correlated with histologic findings.
Statistical analysis was performed using a McNemar test.
Results
Detection Rate of Gastric Cancer
Pathologically, 34 patients showed early gastric cancers (pT1) and 26
patients were found to have advanced gastric cancers (pT2–pT4). The
detection rate of all gastric cancers on thin-sliced MPR images was 65% (39 of
the 60 patients), whereas it was 50% (30 of the 60 patients) on 5-mm-slice
axial images (Table 1),
indicating no statistically significant difference (p > 0.05)
between the two. However, there was a statistically significant difference
(p < 0.05) in the detection rate of early gastric cancers between
thin-sliced MPR images (14 of 34 patients, 41.2%) and 5-mm-slice axial images
(7 of 34 patients, 20.5%). The locations of early gastric cancers that were
detected on thin-sliced MPR images but were not visible on 5-mm-slice axial
images were as follows: greater curvature of the gastric angle and antrum
(n = 4), lesser curvature of the gastric angle and antrum (n
= 2), and large curvature of the gastric body (n =1).
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Fig. 2A —Early gastric cancers. 69-year-old man with protruding type
of early gastric cancer. Oblique multiplanar reconstruction perpendicular to
gastric wall shows protruding mass (arrow) of gastric cardia.
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Fig. 2B —Early gastric cancers. 77-year-old man with superficial and
depressed type of early gastric cancer. Coronal multiplanar reconstruction
shows irregularly enhanced lesion (arrows) at lesser curvature of
lower gastric body.
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Fig. 5A —70-year-old man with diffusely infiltrative type of advanced
gastric cancer (pT3). Coronal multiplanar reconstruction shows thickened
gastric wall with abnormal three-layer structure: high-attenuating first layer
(*), low-attenuating second layer (**), and high-attenuating third layer
(arrow).
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Fig. 5B —70-year-old man with diffusely infiltrative type of advanced
gastric cancer (pT3). Photomicrograph shows that high-attenuating first layer
pathologically corresponds to where cancer cells are more closely linked,
mainly at mucosal and submucosal layers (*), and that low-attenuating second
layer (**) corresponds to where tumor cells are diffusely scattered, mainly at
proper muscle layer. In addition, high-attenuating third layer of outer line
of gastric wall corresponds to closely linked proliferation of cancer cells
from subserosal layer to serosa (arrow).
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In 34 early gastric cancers, thin-sliced MPR images depicted 68.8% (11/16)
of submucosal cancers, in which cancer cells invaded to the submucosa, and
they showed 16.7% (3/18) of less invasive mucosal cancers, in which cancer
cells invaded within the mucosa. In contrast, thin-sliced MPR images depicted
96.2% (25 of 26) of advanced gastric cancers. One advanced gastric cancer not
visible on thin-sliced MPR images was a minute ulcerative tumor, a so-called
stage IIc–like advanced cancer.
CT Appearance of Gastric Cancer (CT–Histologic Correlation)
Grossly, gastric cancers were categorized as one of the following types:
protruding, superficial or depressed, ulcerative and localized, ulcerative and
infiltrative, diffusely infiltrative, or nonclassifiable. All protruding early
gastric cancers (n = 6) were clearly depicted as protruding masses on
CT (Fig. 2A). In one patient,
two dilated vessels were clearly displayed at the basement of the tumor on CT
(Fig. 3A,
3B). Superficial or depressed
early gastric cancers (n = 28) were revealed as lesions with
irregular enhancement of the inner layer of the gastric wall
(Fig. 2B), but the detection
rate of this type of gastric cancer was low (28.6%). Protruding advanced
gastric cancers (n = 3) were revealed as a protruding mass in all
patients.
Two lesions were histologically diagnosed as mucinous adenocarcinomas and
had a low-attenuating area in the tumor (Fig.
4A,
4B). The low-attenuating area
histologically corresponded to large mucin pools, mainly in the submucosal and
proper muscle layers (Fig. 4A,
4B). Ulcerative and localized
advanced gastric cancers (n = 4) or ulcerative and infiltrative
advanced gastric cancers (n = 10) were also revealed as a protruding
mass with a central depression in all patients.
Diffusely infiltrative advanced gastric cancers (n = 6) were
revealed as a markedly thickened gastric wall with abnormal two-layer
(n = 3) or three-layer (n = 3) structures (Fig.
5A,
5B). A high-attenuating first
(inner) layer histologically corresponded to where cancer cells were more
closely proliferated, mainly in the mucosal and submucosal layers. A
low-attenuating second layer histologically corresponded to where cancer cells
were diffusely scattered, mainly in the proper muscle layers with an
inflammatory or desmoplastic reaction. A high-attenuating third layer, seen in
50% of this type, was revealed on the serosal surface of the gastric wall and
histologically corresponded to the infiltration of cancer cells from the
subserosal layer to the serosa, resulting in serosal infiltration by the tumor
(Fig. 5A,
5B).
Depth Invasion of Gastric Cancer
The accuracy results for CT staging of gastric cancers in comparison with
that for pathologic staging are summarized in
Table 2. The accuracy of CT
staging using MPR images was 85% (51 of 60). The MPR technique was helpful for
evaluation of the z-axis extent of the tumor in three cases (one
pancreatic invasion and two serosal invasions of the greater curvature of the
gastric angle or antrum) (Fig.
6A,
6B).
On the thin-sliced MPR images, four of the five patients with invasion to
other organs or structures were correctly staged at CT. The accuracies of CT
staging using MPR for pT1, pT2, and pT3 gastric cancers were 94.1%, 66.6%, and
77.8%, respectively. Two of the 34 patients with pT1 tumors and three of the
12 patients with pT2 tumors had tumors that were overstaged as T2 and T3,
respectively (Fig. 7A,
7B), whereas one of the 12
patients with pT2 tumors and two of the nine patients with pT3 tumors had
tumors that were understaged as T1 and T2, respectively.
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Fig. 7B —66-year-old man with protruding type of advanced gastric
cancer (pT2). Photomicrograph shows extraprotrusion of serosa by mucinous lake
(arrow), but serosal infiltration by cancer cells is not
histologically revealed.
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Discussion
Adequate distention of the stomach filled with water as a negative contrast
agent has led to improved visualization of the gastric wall and the gastric
tumor itself without overshooting artifacts derived from intraluminal air
[1–5].
By combining the helical scanning technique with this water-filling method,
the accuracy of the depiction of gastric cancer and its depth of invasion by
CT has remarkably improved
[1–5].
In this study, we combined high-quality thin-sliced MPR using MDCT with the
water-filling method to assess the detection of gastric carcinomas and
determine the depth of invasion of gastric carcinomas, and the diagnostic
ability of these high-resolution MPR images was compared with that of
5-mm-slice axial images.
In our study, the detection rate of advanced gastric cancers with
thin-sliced MPR images was excellent (96.2%), indicating that thin-sliced MPR
using MDCT is a reliable tool for the detection of advanced gastric cancers.
In contrast, there were some difficulties in the detection of early gastric
cancers even when used with thin-sliced MPR, although the detection rate of
early gastric cancers in MPR (41.2%) was significantly higher than that in
5-mm-slice axial images (20.5%). The detection rate for mucosal cancer was
very low (16.7%) in comparison with that for submucosal cancer (68.8%). In
addition, the detection rate for grossly nonprotruding early gastric cancers,
such as stage IIc, was comparatively low (28.6%). These results indicate that
CT is not suited for detection of mucosal cancer or grossly nonprotruding
early gastric cancer—even when used with thin-sliced MPR—because
distinction between well-enhanced mucosal or nonprotruding early gastric
cancer and well-enhanced normal mucosal layers may be difficult on CT.
Takao et al. [5] reported
that the accuracy of detection of early gastric cancers was only 23% using
axial images obtained on a single-detector helical CT scanner with the
water-filling method, which is similar to our result using 5-mm-slice axial
images. In our seven early gastric cancers detected at MPR but not visible on
5-mm-slice axial images, six were located at the large or lesser curvature of
the gastric angle or antrum. Detection of early gastric cancers with
5-mm-slice axial images may be difficult because of partial volume artifacts
where the gastric wall is tangent to the axial scan, such as at the greater or
lesser curvature of the gastric antrum or angle.
In this study, the MDCT findings of the gastric cancers were well
correlated with pathologic findings. In the protruding type of early gastric
cancers, thick vessels were shown at the basement of the tumor both on MDCT
and at pathology (Fig. 3A,
3B). Because thick vessels in
the tumor sometimes become the cause of massive bleeding in endoscopic
polypectomy, this information may be useful on the occasion of polypectomy. In
the diffusely infiltrative type of advanced gastric cancers, abnormal two- or
three-layer structures were depicted in tumors.
Histologically, a high-attenuating abnormal inner layer corresponded to
where cancer cells were closely proliferated, mainly in the mucosal and
submucosal layers, whereas a low-attenuating abnormal second layer
corresponded to where cancer cells were diffusely scattered, mainly in the
proper muscle layer with desmoplastic change and inflammatory reaction. In
addition, the presence of a high-attenuating abnormal third layer on the
serosal surface of the gastric wall suggested the serosal infiltration of the
tumor because this high-attenuating layer histologically corresponded to a
closely linked proliferation of cancer cells from the subserosal layer to the
serosa, indicating direct serosal infiltration by the tumor. These CT findings
associated with the infiltration of cancer cells were helpful in determining
the depth invasion of the tumor.
A characteristic CT appearance was also noted in mucinous gastric
carcinomas. The two mucinous carcinomas in our study also had a large and very
low-attenuating area in the tumor that histologically corresponded to a large
mucin pool (Figs. 4A,
4B and
7A,
7B). The presence of this
large low-attenuating area in the tumor may assist in distinguishing mucinous
from nonmucinous gastric carcinomas. Park et al.
[6] also reported the helical
CT findings of 21 patients with mucinous gastric carcinoma and concluded that
a diffusely thickened, low-attenuating middle or outer layer and preservation
of the thin high-attenuating inner layer could be helpful findings that
suggest mucinous gastric carcinoma. Mucinous carcinoma is rare but is
considered to have a poor prognosis
[7,
8]. Therefore, it is clinically
important to distinguish mucinous from nonmucinous gastric carcinomas on
CT.
It is well known that the depth of invasion of a tumor is one of the
significant prognostic factors for patients with gastric cancer
[9–11].
In addition, minimally invasive surgery or laparoscopic gastrectomy for
gastric cancer has been recently developed to obtain better postoperative
quality of life [12,
13]. To select a proper
indication for these minimally invasive resections, the accuracy of the
preoperative diagnosis to decide the depth of tumor invasion is important
[12,
13]. Our accuracy using
thin-sliced MPR for T staging of gastric cancer was 85%, indicating that CT is
useful in determining the depth of invasion of gastric tumor. In addition, the
MPR technique was helpful for the evaluation of the z-axis extent of
tumor in three cases (one pancreatic invasion and two serosal invasions of the
greater curvature of the gastric angle or antrum). In these three cases, the
depth of tumor invasion could hardly be determined using axial images because
of partial volume artifact where lesions were tangent to the axial scan.
Invasion to other organs is an important prognostic factor and, therefore,
it may be important to visualize the precise relationship between the gastric
tumor and other organs without partial volume phenomenon using high-quality
MPR. On the other hand, accurate distinction between T2 and T3 tumors was
sometimes difficult even using the MPR technique. Dux et al.
[4] reviewed helical hydro-CT
(using axial images) in 112 patients with gastric carcinoma and concluded that
CT was inadequate for accurately diagnosing serosal infiltration of gastric
carcinoma. In our study, three patients with deformities of the outer surface
of the gastric wall were staged as T3 on CT, but serosal infiltration was not
histologically revealed. Deformity of the outer surface of the gastric wall
can occur as a result of factors other than serosal invasion, such as
compression of the serosa by tumor (Fig.
7A,
7B). Conversely, in two
patients with pT3 tumor, serosal infiltration was not diagnosed on CT because
the outer surface of the gastric wall was closely attached to the abdominal
wall or the liver, resulting in understaging as T2 on CT. Thus, MDCT had some
limitations in the evaluation of serosal infiltration.
The limitation of our study is that normal cases, in which gastric cancer
was absent, were included in our study. Therefore, it may be difficult to
weigh the true value of sensitivity and specificity of CT for tumor
detection.
In conclusion, high-quality thin-sliced MPR using MDCT with the
water-filling method has advantages in reliable detection of advanced gastric
cancers, acceptable evaluation of the depth of invasion of gastric carcinomas,
and visualization of histologic changes such as mucinous component or
differences in infiltration of cancer cells, although there are some
difficulties in the depiction of flat mucosal cancer and in accurate
distinction between T2 and T3 tumors in some cases.
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Abstract
Introduction
