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Differentiation between
Malignant and Benign Gastric
Ulcers: CT Virtual Gastroscopy versus
Optical Gastroendoscopy1
ORIGINAL RESEARCH
Chiao-Yun Chen, MD
Purpose: To retrospectively compare computed tomographic virtual
Yu-Ting Kuo, MD, PhD
gastroscopy (VG) and conventional optical gastroendos-
Chien-Hung Lee, PhD
copy for the differentiation of malignant and benign gastric
Tsyh-Jyi Hsieh, MD ulcers.
Chang-Ming Jan, MD
Twei-Shiun Jaw, MD, MMS Materials and The institutional review board approved this study and
Wan-Ting Huang, MD Methods: confirmed that informed consent was not required. Gas-
Fang-Jung Yu, MD tric ulcers in 115 patients (mean age, 64.7 years; range,
31– 86 years; 61 men, 54 women) were evaluated by using
endoscopy and VG. Ulcer shape, base, and margin and
periulcer folds were evaluated by two independent review-
ers. Malignant gastric ulcers were identified by irregular,
angulated, or geographic shape; uneven base; irregular or
asymmetric edges; and disrupted or moth-eaten appear-
ance of periulcer folds near the crater edge and/or clubbed
or fused folds. Benign gastric ulcers were identified by
smooth and regular shapes, even bases, clearly demar-
cated and regular edges, and folds that tapered and con-
verged toward the ulcer. The performance of VG and
endoscopy for the diagnosis of benign and malignant gas-
tric ulcers was evaluated by using histopathologic results
as the reference standard. The McNemar test was used to
compare VG and endoscopic data. A P value less than .05
was considered to indicate a significant difference.
姝 RSNA, 2009
G
astric cancer is one of the most in fact, malignant (8,9). However, be- abdominal CT and 5 years of experience
common causes of death from cause endoscopy is an expensive and in three-dimensional endoluminal ap-
cancer worldwide (1,2). It is the invasive procedure, many patients, proaches and interpretation) identified
second-most common cause of death even those at higher risk levels, might 135 patients with gastric ulcers who had
due to cancer in Asians from China, refuse to undergo such essential endo- undergone endoscopic examination and
Japan, and Korea (3). While it is one of scopic examinations. biopsy, as well as VG, at our institution
the least common cancers in North While investigators (10–14) have between May 2003 and August 2007. All
America, it is the eighth leading cause of found computed tomographic (CT) of the patients in our study were Tai-
cancer death in the United States. In colonography to be a potent imaging wanese. Twenty patients were excluded
2006, there were reported to be more tool for the detection and screening of because they were lost during follow-
than 22 280 new gastric cancer cases, colon cancer, CT has not been widely up, so no final diagnosis was made. The
resulting in about 11 430 deaths in the used for the stomach (15,16). Fortu- remaining 115 patients, with either ma-
United States (4). nately, gastric CT imaging by means of lignant (n ⫽ 76) or benign (n ⫽ 39)
Early diagnosis of this malignancy is three-dimensional virtual gastroscopy gastric ulcers, were included in the
crucial because patient outcome is de- (VG) and air distention of the stomach study. The clinical indications that re-
pendent on detecting it in its initial now makes better detection of subtle sulted from CT examinations in the 76
stages. In Taiwan, for example, overall mucosal changes possible, and it can be patients with malignant ulcers were that
5-year survival rates for this cancer used to provide images that are almost patients were suspected of having ma-
have been reported to be 97.9% for as detailed as those produced by using lignant gastric ulcers at endoscopy (n ⫽
stage IA disease, 92.9% for stage IB dis- endoscopy (15,16). 76). The indications for the 39 patients
ease, 63.2% for stage II disease, 50.1% We therefore conducted this retro- with benign ulcers were as follows: (a)
for stage IIIA disease, 28.7% for stage spective study to compare the perfor- patients were suspected of having ma-
IIIB disease, and 9.3% for stage IV dis- mance of CT VG with that of conven- lignant gastric ulcers at endoscopy (n ⫽
ease (5). tional optical gastroendoscopy in regard 7); (b) intractable gastric ulcers did not
Patients with gastric ulcers have to the differentiation of malignant and heal after 8 weeks of treatment with
been found to be at greater risk for de- benign gastric ulcers. proton-pump inhibitors (n ⫽ 8); (c) ul-
veloping gastric cancer (6,7). Because cer size of more than 3 cm in diameter
malignancy is best treated in its early at endoscopy (n ⫽ 8); (d) gastric ulcers
stages, it is usually recommended that Materials and Methods in the gastric body where it was difficult
all instances of gastric ulcers be fol- to exclude the possibility of malignancy
lowed up with conventional endoscopy Patients at endoscopy (n ⫽ 8); (e) previous bi-
and histopathologic studies until they The protocol for this retrospective opsy results showed cell dysplasia or
have healed to ensure that they are not, study was approved by the institutional atypia (n ⫽ 5); and (f) gastric bleeding
review board of our hospital, Kaohsiung (n ⫽ 3) (Fig 1).
Medical University Hospital, which also The mean age of the 115 patients
Advances in Knowledge determined that informed consent could was 64.7 years (age range, 31– 86
䡲 The sensitivity and specificity for be waived for this undertaking. years). These patients included 61 men
the overall diagnosis at virtual After performing a computerized
gastroscopy (VG) were 92.1% search of the medical records in our
and 91.9%, respectively, and hospital’s radiology files, one author Published online before print
88.2% and 89.5%, respectively, (C.Y.C., with 10 years of experience in 10.1148/radiol.2522081249
for the overall diagnosis at endos- Radiology 2009; 252:410 – 417
copy in the detection of malignant
gastric ulcers. Implication for Patient Care Abbreviation:
VG ⫽ virtual gastroscopy
䡲 Endoscopy was more sensitive for 䡲 While endoscopy and VG are al-
detection of malignancy based on most equally capable of depicting Author contributions:
ulcer base criteria (P ⫽ .034), malignancy by using the criteria Guarantors of integrity of entire study, C.Y.C., C.M.J.,
T.S.J., F.J.Y.; study concepts/study design or data acqui-
and VG was more specific for de- that we studied, decreased dis-
sition or data analysis/interpretation, all authors; manu-
tection of malignancy based on comfort of VG examination may
script drafting or manuscript revision for important intel-
ulcer margin criteria (P ⫽ .034); make it a preferred means of dis- lectual content, all authors; manuscript final version ap-
VG was about as accurate as en- tinguishing benign from malignant proval, all authors; literature research, C.Y.C., C.M.J.,
doscopy in identifying malignant gastric ulcers in the future, partic- T.S.J., W.T.H., F.J.Y.; clinical studies, C.Y.C., Y.T.K.,
ulcer shapes, was more accurate ularly for patients who have con- T.J.H., C.M.J., T.S.J., W.T.H., F.J.Y.; statistical analysis,
in finding the ulcer margin and traindications to or who are un- C.Y.C., C.H.L., F.J.Y.; and manuscript editing, C.Y.C.,
Y.T.K., T.J.H., C.M.J., F.J.Y.
perifold, but was less accurate in able to undergo conventional
depicting ulcer base. endoscopy. Authors stated no financial relationship to disclose.
(mean age, 65.9 years; range, 38 – 84 detector CT scanner (Brilliance 190P; tained from the diaphragmatic domes to 2
years) and 54 women (mean age, 63.4 Philips Medical Systems, Cleveland, Ohio) cm below the lower margin of the air-
years; range, 31– 86 years). The age dis- (26 patients). All patients had fasted for at distended gastric body. The 16-section mul-
tribution was comparable between the least 8 hours and had received 6 g of gas- tidetector CT scanner parameters were set
sexes (P ⫽ .266, t test). The elapsed producing crystals with 10 mL water orally at 1.25-mm collimation, 1.375 pitch, 27.5-
time between CT and endoscopy was to enable distention of the stomach before mm/sec table speed, 1.25-mm reconstruc-
within 7 days (mean, 3 days). Of these the procedures were performed. All of the tion thickness, 0.625-mm reconstruction
patients, 112 underwent endoscopy patients were placed in the supine position interval, 250–300 mAs, and 120 kVp. The
prior to CT VG, and three patients with with their right side elevated at approxi- 64-section multidetector CT parameters
gastric bleeding underwent CT VG prior mately 30°. To ensure adequate gastric dis- were set at 0.625-mm collimation, 1.142
to endoscopy. All of the diagnoses were tention, a scanogram was obtained. An ad- pitch, 0.75-second rotation time, 1.0-mm
confirmed with histopathologic exami- ditional 3 g of gas-producing crystals were reconstruction thickness, 0.5-mm recon-
nation results, and all of the patients given to patients determined to have insuf- struction interval, 250–300 mAs, and 120
with a diagnosis of a benign ulcer were ficient air distention. CT scans were ob- kVp.
followed up for more than 6 months.
Figure 1
Endoscopy
Endoscopy was performed with the pa-
tient in the left lateral position after ad-
ministration of oropharyngeal anesthesia
(Xylocaine; AstraZeneca, Sweden). En-
doscopy, as well as directed biopsy, was
performed by two board-certified experi-
enced gastroenterologists (F.J.Y. and
C.M.J., with 10 and 20 years of experi-
ence, respectively). We analyzed the dif-
ference in age and sex distribution for the
patients examined. Patterns for the two
characteristics were found to be compa-
rable (P ⫽ .495 for sex, 2 test; P ⫽ .257
for age, t test). End-viewing fiberoptic
panendoscopes (GIF-XQ240; Olympus, Figure 1: Flowchart of study enrollment. ENDO ⫽ endoscopy, FP ⫽ false positive, TP ⫽ true positive.
Tokyo, Japan) were used in all patients.
Six specific chosen directed-biopsy speci-
mens from the edge and base of the ulcer
were collected from each patient. Endo-
Figure 2
scopic evaluations were made (F.J.Y. and
C.M.J.). During analysis of the endo-
scopic features, cases of malignant and
benign ulcers were randomly intermixed.
Each gastroenterologist reviewed the en-
doscopic images and made an indepen-
dent evaluation; they then met with each
other, went over every case, and came to
a consensus evaluation.
CT VG Studies
All of the patients underwent multidetec-
tor CT examination following the routine
procedures designed for patients sus-
pected of having abnormal gastric lesions
in our department. CT examinations
were performed by using either a 16- Figure 2: Images of malignant gastric ulcer in 65-year-old man. (a) VG image shows en face view of ulcer
section multidetector CT scanner (Light- and (b) endoscopic image shows minimal oblique view of ulcer at the gastric part of the body with uneven
ulcer base, irregular ulcer shape, irregular ulcer margin, and associated gastric folds with rugae interruption
Speed H16; GE Healthcare, Milwaukee,
(arrows).
Wis) (89 patients) or a 64-section multi-
Reconstructed images from data are knowing that the images had been ob- on radiologic and endoscopic criteria
routinely stored in our picture archiving tained in patients with gastric ulcers but established for the recognition of each
and communication system before three- not knowing the results of endoscopic and (17,18). Our diagnoses were made by
dimensional image processing is per- pathologic examinations. Each of the two examining the available morphologic
formed. The VG images were indepen- gastrointestinal radiologists created and features of ulcer shape, base, and mar-
dently created and interpreted in the reviewed the VG features and made a gins and the relation of the ulcer to the
three-dimensional workstation (AW 4.1; record independently and then met with surrounding folds. Malignant gastric ul-
GE Healthcare) by two authors (T.S.J. each other to go over every case and cers were identified by shapes that were
and Y.T.K., with 10 and 12 years of ab- come to a consensus evaluation. irregular, angulated, or geographic;
dominal CT experience, respectively, as bases that were uneven; edges that
well as 4 years of experience each in the Image Evaluation were irregular or asymmetric; and folds
three-dimensional endoluminal ap- The locations of the gastric ulcers were that appeared to be disrupted or “moth-
proach). During analysis of the VG fea- recorded on both VG and endoscopic eaten” near the crater edge and/or were
tures, the malignant and benign ulcer images. The benign gastric ulcers were clubbed or fused (Fig E1, http:
cases were randomly intermixed. The differentiated from the malignant gas- //radiology.rsnajnls.org/cgi/content/full
two authors analyzed the VG images tric ulcers, and this process was based /2522081249/DC1; Fig 2). Benign gastric
ulcers were identified by shapes that
Figure 3 were smooth and regular, bases that
were even, edges that were clearly de-
marcated and regular, and periulcer folds
that tapered and converged toward the
ulcer (Fig E2, http://radiology.rsnajnls
.org/cgi/content/full/2522081249/DC1;
Fig 3).
A standardized form was completed
independently by the two radiologists
who interpreted the VG images and by
the two gastroenterologists who inter-
preted the endoscopic images. On this
form, the evaluators noted whether the
shapes, bases, margins, or surrounding
folds on each image had primarily be-
nign or malignant features. In addition,
the two gastroenterologists evaluating
the endoscopic images also noted the
Figure 3: Images of benign gastric ulcer in 37-year-old woman. (a) VG image and (b) endoscopic image show presence or absence of any periulcer
en face view of ulcer at the gastric angle with even ulcer base, regular triangular ulcer shape, regular ulcer margin, color change (redness, discoloration, or
and associated regular gastric folds terminating at the ulcer margin (arrows). spotty bleeding) (19). Radiologists and
gastroenterologists initially made inde-
Table 1
Diagnosis of Benign and Malignant Gastric Ulcers according to Criteria at VG and Endoscopy
VG Endoscopy
Periulcer Periulcer
Ulcer Ulcer Ulcer Fold Overall Ulcer Ulcer Ulcer Fold Color Overall
Shape* Base* Margin* Change† Diagnosis* Shape* Base* Margin* Change† Change Diagnosis
Parameter B M B M B M B M B M B M B M B M B M B M B M
pendent records, after which they came mucosa layers with varying degrees of
to a consensus diagnosis at VG and en- inflammation or granulomatous tissue
No fold change was determined at VG examination for 21 patients with benign ulcers and 32 patients with malignant ulcers, and no fold change was determined at endoscopic examination for 22 patients with benign ulcers and 24 patients with malignant ulcers.
88.2 (80.8, 95.5)
89.5 (79.5, 99.5)
Overall Diagnosis
doscopy, respectively. infiltration in the lamina propria.
VG results showed that 98.3%
Overall Diagnosis
88.6
(113 of 115) of patients in this study
…
To perform an overall diagnosis by us- had gastric ulcers. Two patients had
Color Change
doscopic findings for the malignancy of could depict. While endoscopy could
0.847
gastric ulcers, we calculated the ⌽ cor- depict all of the ulcers, it could not be
79.1
relation coefficient for each individual used to differentiate between benign
criterion and the malignancy. These two and malignant ulcers in one patient
* Information regarding VG criteria for two patients with benign ulcers was not evaluated, and information regarding endoscopic criteria for one patient with a benign ulcer was not evaluated.
ative weight for developing a diagnostic distal antrum, and a complete view
score. The receiver operating character- was impossible.
0.913
Endoscopy
85.5
istic curve method was employed to find As can be seen in Tables 1 and 2,
the cutoff value for the optimal diagnostic the interobserver agreement in the
Diagnostic Accuracy, Sensitivity, and Specificity of Criteria of VG and Endoscopy Associated with Malignant Gastric Ulcers
Ulcer Margin*
for sensitivity and specificity). nign gastric ulcers by using VG or en-
0.900
doscopy showed excellent reproduc-
86.0
Statistical Analysis ibility ( ⫽ 0.879 – 0.937 for VG and
By using histopathologic findings as a 0.847– 0.919 for endoscopy). For the
Note.—See Table 1 for numbers used to calculate sensitivity, specificity, and accuracy percentages. Data in parentheses are 95% confidence intervals.
generally accepted standard of evalua- diagnosis of malignant gastric ulcers,
Ulcer Base*
0.870
tion, we compared the sensitivities, VG had a sensitivity and specificity of
86.0
specificities, and accuracies of the diag- 92.1% and 75.7%, respectively, based
noses based on the image characteris- on ulcer shape, 68.4% and 81.1%
Ulcer Shape*
sensitivities and specificities were re- based on ulcer margin, and 95.5% and
0.919
86.8
ported with corresponding 95% confi- 83.3% based on periulcer fold change
dence intervals. Interobserver variability, and had an average accuracy of more
using the following scale: fair agreement shape, 85.5% and 86.8% based on ul-
Periulcer Fold Change†
was indicated by 0.21– 0.40; moderate cer base, 97.4% and 63.2% based on
agreement, 0.41– 0.60; good agreement, ulcer margin, and 90.4% and 70.6%
0.61– 0.80; and excellent agreement, based on periulcer fold change.
0.929
91.9
using the McNemar test. A P value less ual endoscopic findings for the malig-
Ulcer Margin*
VG
than .05 was considered to indicate a sig- nancy of gastric ulcers, the correlation
P values less than .05 indicated a significant difference for values.
0.933
91.2
nificant difference. All statistical opera- coefficients were 0.69, 0.47, 0.80, and
tions were performed by using software 0.80 for ulcer shape, ulcer base, ulcer
68.4 (56.4, 77.9)
81.1 (65.7, 92.2)
(Stata, SE version 9.1 for Windows, margin, and periulcer fold change, re-
Ulcer Base*
2005; Stata, College Station, Tex). spectively, for VG findings and 0.71,
0.879
proved benign gastric ulcers, and 76 (0.80 䡠 fold change) for VG diagnosis
had malignant gastric ulcers (24 at and (0.71 䡠 shape) ⫹ (0.70 䡠 base) ⫹
Specificity (%)
Sensitivity (%)
Accuracy (%)
stage T1, 29 at stage T2, and 23 at (0.68 䡠 margin) ⫹ (0.60 䡠 fold change)
Value‡
Parameter
Table 2
stage T3). Histopathologic study re- for endoscopic diagnosis, with a score
sults revealed that all of the benign of 1 for positive and a score of 0 for
†
ulcers had eroded or defective gastric negative (or no fold change) findings.
The cutoff values for VG findings were change and had an average accuracy of diagnosed as being malignant (Fig 6). In
2.29 and 1.49, respectively, for patients more than 79.1% (Table 2). addition, one malignant gastric ulcer
with and those without the periulcer fold As shown in Table 3, VG and endos- was misdiagnosed as benign at VG but
change and 2.09 and 0.70, respectively, copy had significantly different diagnostic was correctly diagnosed at endoscopy
for endoscopic findings. Patients with results in the evaluation of ulcer base and (Fig E3, http://radiology.rsnajnls.org
overall scores that were larger or equal to ulcer margin (both P ⫽ .034, McNemar /cgi/content/full/2522081249/DC1).
those of the corresponding cutoff values test). Compared with VG, endoscopy was
were determined to have a malignancy. found to more sensitively depict malig-
The sensitivity and specificity for the nancy based on the unevenness of the Discussion
overall diagnosis at VG were 92.1% and ulcer base (Fig 4), while VG had better In this study, we compared the perfor-
91.9%, respectively, and 88.2% and specificity based on the irregularity of the mance of VG and endoscopy in the dif-
89.5% at endoscopy. In addition, endos- ulcer margin (Fig 5). ferentiation between malignant and be-
copy showed 93.4% sensitivity and With both VG and endoscopic crite- nign gastric ulcers and found the diag-
51.3% specificity for periulcer color ria, two benign gastric ulcers were mis- nostic results at VG to be comparable
with those at endoscopy.
VG is a new noninvasive technique
Figure 4 capable of creating high-quality detailed
three-dimensional images of subtle mu-
cosal changes in the stomach. Its image
quality is diagnostically comparable
with that provided at optical endoscopy
(15,21). VG has a wider viewing field
than endoscopy and is better for evalu-
ating high lesser curvature sites and du-
odenal bulbs than conventional optical
endoscopy (19). Because views ob-
tained with a virtual camera can be ad-
justed without substantial limitations,
and because they can be re-formed ret-
rospectively to clear up any blind spots,
VG produces better overall views of the
whole ulcer and better views of the ul-
cer margin than endoscopy (P ⫽ .034).
Because its view comes from several an-
Figure 4: Images of malignant gastric ulcer in 65-year-old woman, with atypical benign morphologic fea-
gles, it offers a more precise measure-
ture of the ulcer base on VG image. (a) VG image shows en face view of ulcer at the low gastric body with even
ment of the abnormality. Even more im-
ulcer base (arrow). (b) Endoscopic image shows oblique view of ulcer and an uneven ulcer base (arrow).
portant, VG is technically less invasive
than endoscopy.
Table 3
Diagnostic Comparison of Individual and Overall Criteria for Imaging Findings at VG and Endoscopy for Patients with Gastric Ulcers
Ulcer Shape at Ulcer Base at Ulcer Margin at Periulcer Fold Change Overall Diagnosis at
Endoscopy Endoscopy Endoscopy at Endoscopy* Endoscopy
Parameter Benign Malignant Benign Malignant Benign Malignant Benign Malignant Benign Malignant
VG†
Benign 29 5 34 19 23 7 11 5 31 8
Malignant 8 70 8 51 1 81 2 40 10 63
2 For McNemar test‡ 0.69 (.405) 4.48 (.034) 4.50 (.034) 1.29 (.257) 0.22 (.637)
Figure 5
Figure 5: Images of benign gastric ulcer in 59-year-old man, with atypical malignant morphologic features of ulcer margin and periulcer fold change on endoscopic
image. VG images show the (a) profile view and (b) en face view of ulcer at gastric antrum with even ulcer base, regular oval ulcer shape, regular ulcer margin, and associ-
ated regular gastric folds terminating at the ulcer margin (arrows). (c) Endoscopic image shows oblique view of ulcer and asymmetric edema of ulcer margin (arrowhead)
and associated gastric folds with bulbous rugae enlargement (arrow). P ⫽ pylorus.
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