European Journal of Radiology 155 (2022) 110488

Contents lists available at ScienceDirect

European Journal of Radiology

journal homepage: www.elsevier.com/locate/ejrad

Effect of visceral adipose tissue on the accuracy of preoperative T-staging of

gastric cancer
Teng Ma a, 1, Xiaojiao Li a, 1, Tong Zhang a, Mingguang Duan a, Qianli Ma b, Lin Cong c,
Zhaoqin Huang a, Ximing Wang a, Yunchao Chen a, *
a
Department of Radiology, Provincial Hospital Affiliated to Shandong First Medical University, Jinan, Shandong 250021, China
b
Department of Radiology, Taian City Central Hospital, Taian, Shandong 271000, China
c
Department of Medical Imaging Interventional Therapy, Provincial Hospital Affiliated to Shandong First Medical University, Jinan, Shandong 250021, China

A R T I C L E I N F O A B S T R A C T

Keywords: Background: Due to the anatomical characteristics of the tumor and the specific variables of the patients, the
Gastric cancer accuracy of preoperative T-staging of gastric cancer needs to be further improved. This study investigated the
Visceral fat content effect of visceral adipose tissue (VAT) on the accuracy of clinical T-staging of gastric cancer.
T staging
Methods: The clinical data of 455 patients who underwent gastrectomy from January 2013 to December 2018
were analyzed retrospectively. Taking the postoperative pathological results as the reference standard, the pa­
tients were divided into accurate staging group and mistaken staging group according to the comparison of
clinical T stage (cT) and pathological T stage (pT). The individual characteristics of the two groups were
compared, including visceral fat content at L2/L3 level calculated on computed tomography, age, sex, tumor size,
tumor location (cardia, stomach body, stomach antrum), and degree of differentiation. Multivariate logistic
regression was used to determine the independent factors affecting the accuracy of cT staging.
Results: Among the 455 patients, 355 patients (78.0 %) had accurate preoperative cT staging and 100 patients
(22.0 %) had inaccurate preoperative cT staging. The average area of VAT in the accurate staging group was
(129.8 ± 72.6) cm2 and that in the mistaken staging group was (74.6 ± 61.6) cm2 (P < 0.001). The optimal cut-
off value of VAT was 97.8 cm2 calculated according to the Yoden index. Multivariate logistic regression analysis
showed that VAT, tumor location and tumor size were independent predictors of cT accuracy.
Conclusions: Patients with lower visceral fat content (<97.8 cm2) based on L2/L3 level had a higher risk of false
staging in preoperative clinical T staging.

1. Introduction surgical approach of locally advanced gastric cancer (T2-T4a) might

Gastric cancer, a worldwide cancer, has caused about 1,000,000 new
cases and 769,000 deaths in 2020 (equivalent to 1 death per 13 deaths
worldwide), ranking fifth and fourth in the global incidence rate and
mortality rate [1]. Although the therapeutic effect has been improved in
the past decade, the survival rate of gastric cancer is still very low [2].
The prognosis of patients with gastric cancer is closely related to the
stage of diagnosis. Clinical studies have found that preoperative neo­
adjuvant chemotherapy is helpful to reduce tumor lesions, avoid path­
ological risk factors and reduce lymph node metastasis [3,4]. This
individualized treatment has become a trend. With the continuous
development of robot assisted surgery and artificial intelligence, the
focus more on laparoscopic resection and be more minimally invasive in
the future [4]. Therefore, more and more accurate initial clinical staging
is needed to select the patients who benefit the most from preoperative
chemotherapy, and determine more targeted surgical procedures, so as
to provide sufficient basis for selecting reasonable treatment mode.
Computer tomography (CT) is the preferred imaging method to deter­
mine the cTNM stage of gastric cancer [5,6]. It is reported that the
overall diagnostic accuracy of multi-slice spiral CT in T-staging is be­
tween 77.1 % and 88.9 % [7]. However, its diagnostic effect on local
partial stage (T3-T4) is not satisfactory, leading to overstaging of gastric
cancer due to its location on the cross-sectional images, the extent of
bare stomach area and the situation of peri-stomach fatty tissue [8]. This

* Corresponding author.
E-mail address: drchenyc@126.com (Y. Chen).
1
The two authors contributed equally.

https://doi.org/10.1016/j.ejrad.2022.110488
Received 25 March 2022; Received in revised form 8 August 2022; Accepted 11 August 2022
Available online 17 August 2022
0720-048X/© 2022 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
T. Ma et al.
suggests that the accuracy of clinical T-staging of gastric cancer would
be different due to the anatomical characteristics of the tumor and the
specific variables of the patient.
The degree of serosal invasion is of great significance for CT staging
[6,9]. The density of adipose tissue adjacent to gastric cancer would
affect the judgment of the degree of serosal invasion [10,11]. However,
for patients with lean constitution and cachexia, due to the low content
of visceral fat, the contrast between tumor, stomach wall and perito­
neum is reduced, which will also trouble the evaluation of tumor infil­
tration. It was shown that lower visceral fat content would increase the
inaccuracy of clinical T-staging of colon cancer [12]. This indicates that
the influence of visceral fat should not be ignored in the local stage of
abdominal and pelvic tumors, especially those from intraperitoneal (for
example, stomach, jejunum, ileum, transverse colon, etc) and inter­
peritoneal organs (for example, ascending colon, descending colon,
liver, etc). CT is the gold standard for evaluating visceral fat [13,14]. It
showed that the correlation between the visceral fat measured on the
axial CT image at the L2/L3 level and the volume of abdominal total
visceral adipose tissue (VAT) was the highest, so this level could be used
as the best anatomical position for abdominal fat measurement [15].
Accordingly, the objective of this study was to determine the corre­
lation between the VAT area on the axial CT image at the L2/L3 level
and the accuracy of clinical T-staging of gastric cancer, adjusting for
other probable impact factors such as age, gender and so on.
2. Materials and methods
2.1. Patients
The data of patients who underwent gastrectomy in our hospital
from January 2013 to December 2018 were analyzed retrospectively.
Inclusion criteria: 1) Patients with gastric cancer confirmed by pathol­
ogy and undergoing surgery; 2) Patients who underwent abdominal CT
examination within 2 weeks before operation. Exclusion criteria: 1)
Previous history of other malignant tumors; 2) Simultaneous occurrence
of multiple site tumors; 3) History of previous abdominal surgery; 4)
Preoperative chemotherapy and radiotherapy; 5) Incomplete clinical
data; 6) No contrast enhanced CT examination was performed or no
operation was performed within 2 weeks; 7) Inadequate distension of
stomach before CT examination. Finally, a total of 455 patients were
included in the study, including 348 males and 107 females, with a
median age of 58 years (IQR 51–66).
2.2. CT examination
Siemens dual source CT (SOMATOM force) was used for the exami­
nations. Patients had to fast for 8 h and drink about 800–1000 mL of
water 15 ~ 30mins before scanning to fill the stomach. Patient was in
supine position. Special positions could be adopted according to the
purpose of examination and the cooperation of the patient. For example,
right lateral decubitus was taken when the tumor was located in the
greater curvature, and prone position when the tumor was located in the
front wall of stomach antrum. The scanning range was from the top of
diaphragm to the upper edge of iliac crest. Plain scanning was performed
first, and then multi-phase enhanced scanning was performed. Scanning
parameters: tube current 300 mA, tube voltage 120 kV, slice thickness 5
mm, interval 5 mm. The reconstructed slice thickness was 1.5 mm and
the reconstructed interval was 1.0 mm. During contrast-enhanced
scanning, 100 mL (74.1 g) of the non-ionic contrast agent Ioversol was
injected with a high-pressure syringe at a flow rate of 3.5 mL/s through
the anterior elbow vein. After the injection of the contrast agent, the
patient was instructed to hold his breath, the arterial phase and venous
phase were performed at 22–30 s, 60–70 s respectively.
2
European Journal of Radiology 155 (2022) 110488
2.3. Imaging evaluation for clinical staging
All CT images were independently analyzed by two senior abdominal
imaging diagnostic physicians (with 12 and 10 years of experience
respectively). The two doctors were unaware of the pathological results
and the purpose of this study. Before the evaluation, both doctors had
sufficient special training for T-stage. When the two disagree, they reach
a consensus after review and consultation. Imaging evaluation was
mainly performed on transaxial images in venous phase, combined with
multiplanar reconstructed images when necessary to determine tumor
site, tumor relationship with surrounding organs (such as liver,
pancreas, diaphragm, colon, etc.) or blood vessels, etc. The tumor was
continuously observed and the level with the greatest extent of lesion
involvement was determined, and the longest diameter of the tumor was
measured (for the whole tumor, not just the enhancing component).
Segmental measurements or a combination of multiplanar reconstructed
images were used for measuring more extensive lesions.
The clinical T stage (cT) standard of gastric cancer refers to the TNM
grading and staging system of gastric cancer formulated by the Amer­
ican Joint Committee on cancer AJCC in the 7th Edition [16]. cT1,
tumor invades lamina propria, muscularis mucosae, or submucosa;cT2,
tumor invades muscularis propria; cT3, tumor penetrates subserosal
connective tissue without invasion of visceral peritoneum or adjacent
structures;cT4, tumor invades serosa (visceral peritoneum) or adjacent
structures; T4a, tumor invades serosa (visceral peritoneum); T4b, tumor
invades adjacent structures such as spleen, transverse colon, liver, dia­
phragm, pancreas, abdominal wall, adrenal gland, kidney, small intes­
tine, and retroperitoneum.
2.4. Pathological staging
Pathological results including pathological T stage (pT) were
collected from case records. The tumor was staged according to the TNM
system of AJCC version 7. All pathological reports of this study were
unanimously determined by at least two pathologists who had received
professional training in gastric cancer pathology.
Taking the postoperative pathological results as the reference stan­
dard, according to the comparison of cT and pT, the patients were
divided into accurate staging group (clinical T stage was consistent with
pathological T stage) and mistaken staging group (clinical T stage was
inconsistent with pathological T stage, including underestimated stages
and overestimated stages).
2.5. VAT measuring
The area of VAT was measured by L2/L3 level [15]. Visceral fat was
segmented and measured by Image J software (https://imagej.nih.gov/
ij). Measurements were performed in a semi-automated fashion with
manual outlining of the VAT border and a density threshold setting
between − 190 and − 30 Hounsfield units. The VAT area was calculated
automatically by Image J software (Fig. 1). This work was done on CT
plain scan images in order to avoid interference of abdominal tissue such
as small blood vessels after enhanced scanning.
2.6. Other characteristics
Patient’s individual characteristics that may have a potential impact
on the accuracy for tumor staging were collected from the case records,
including age, gender, tumor size, tumor location (cardia, stomach
body, stomach antrum), degree of differentiation (Low, medium, high
differentiation and stomach mucinous adenocarcinoma).
2.7. Statistical analyses
Independent sample t-test or nonparametric test was used for
continuous variables, and analysis of variance or Fisher exact test was
T. Ma et al. European Journal of Radiology 155 (2022) 110488

Fig. 1. Measurement of the VAT. Manually draw the outline of VAT on the plain scan image (yellow line), a density threshold setting between − 190 and − 30
Hounsfield units was given to extract the VAT. The VAT area was calculated automatically by Image J software. (A) T1 cancer in 52-year-old man. The VAT was
298.6 cm2; (B) T3 cancer in 54-year-old. The VAT was 34.7 cm2.

used for classified variables. Continuous variables were expressed as
median or mean ± standard deviation, and categorical variables were
expressed as quantity and percentage. For cT staging, the consistency
between observers was analyzed by ICC test. According to the accuracy
of cT staging, the ROC curve of VAT was obtained, and the best cut-off
value was calculated according to Yoden index. According to this, VAT
was divided into high value group and low value group. The potential
influencing factors (variables with p < 0.1 in univariate analysis) were
included in the multivariate logistic regression model to judge the in­
dependent influencing factors affecting the accuracy of cT staging.
Statistical analyses were performed using SPSS 23.0 (IBM Corp.,
Armonk, NY, USA) and R software (R Foundation for Statistical
Computing, Vienna, Austria) with the “rms” package.
3. Results
3.1. Patients’ characteristics and the accuracy of cT diagnosis
In this study, 455 cases were collected and showed in Table 1, 348
males and 107 females, a median age of 58 years (IQR 51–66). There
were 355 patients (78.0 %) with accurate cT diagnosis (accurate staging
group) before operation and 100 patients (22.0 %) with mistaken cT
diagnosis (mistaken staging group) (Fig. 2). Please see Table 2 for the
specific distribution. Analysis of measurement consistency between

Table 1
Patients’ clinical characteristics and accuracy of cT diagnosis.
Variables Accurate Mistaken p Mistaken

Underestimate Overestimate p

Cases (N) 355 100 46 54

Age (Year, IQR) 58（51-66） 57（49-66） 0.095 55（45-64） 60（50-66） 0.140
Sex (N, %) 0.897 0.063
Male 272（76.6） 76（76.0） 31（67.4） 45（83.3）
Female 83（23.4） 24（24.0） 15（32.6） 9（16.7）
Location (N, %) 0.063 0.221
Cardia 66（18.6） 23（23.0） 7（15.3） 16（29.6）
Stomach body 149（42.0） 29（29.0） 14（30.4） 15（27.8）
Stomach antrum 140（39.4） 48（48.0） 25（54.3） 23（42.6）
Size (cm) 5.2 ± 2.8 4.1 ± 2.7 <0.001 4.1 ± 2.5 4.0 ± 2.9 0.936
Differentiation degree (N, %) 0.398# 0.125#
Low 189（53.2） 54（54.0） 28（60.9） 26（48.1）
Median 150（43.3） 38（38.0） 15（32.6） 23（42.6）
High 10（2.8） 6（6.0） 1（2.2） 5（9.3）
Mucinous adenocarcinoma (N, %) 6（1.7） 2（2.0） 2（4.3） 0（0.0）
VAT mean (cm2) 129.8 ± 72.6 74.6 ± 61.6 <0.001 68.7 ± 59.0 79.6 ± 63.9 0.384
VAT group (N, %) <0.001 0.661
Low 125（35.2） 74（74.0） 35（76.1） 39（72.2）
High 230（64.8） 26（26.0） 11（23.9） 15（27.8）

#Fisher exact test.

3
T. Ma et al. European Journal of Radiology 155 (2022) 110488

Table 2
Distribution of cT staging groups.
cT staging (N) pT staging (N) Accurate (N) Underestimate (N) Overestimate (N)

pT1 pT2 pT3 pT4a pT4b Total

cT1 46 12 2 1 0 61 46 15 0
cT2 23 32 5 4 0 64 32 9 23
cT3 3 9 70 19 0 101 70 19 12
cT4a 1 1 11 187 3 203 187 3 13
cT4b 0 0 1 5 20 26 20 0 6
Total 73 54 89 216 23 455 355 46 54

Fig. 2. (A-B) T1 cancer in a 64-year old

man. (A) Axial CT image shows thick­
ening and enhancement of inner
mucosal layer (arrows) at greater cur­
vature of the stomach antrum;(B) Coro­
nal reformatted image shows a tumor as
focal thickening of the stomach wall
with marked enhancement but an
essentially flat surface (arrows). This
lesion was correctly classified as T1can­
cer by both reviewers; (C-D) T2 cancer
in a 66-year old man. (C) Axial CT image
shows well-enhancing mucosal thick­
ening (arrows) and disruption of low-
density-stripe layer (greater than 50%
of the thickness) at greater curvature of
the stomach antrum; (D) Coronal refor­
matted image shows the same findings
(arrows). At histologic analysis, the
outer layers of the muscularis propria
were intact, whereas the inner layers
were infiltrated. The subtle irregularities
of the mucosal surface corresponded to
ulcers at histologic analysis. This lesion
was correctly classified as T2 cancer by both reviewers; (E) 55-year-old man. Axial CT image shows a transmural proximal stomach carcinoma with obliteration of the
fat plane (white arrow) between the stomach wall and the left diaphragm and additional invasion of the latter (black arrow). Due to the bare area of stomach, this
lesion of pT2 was overestimated as cT3; (F) 68-year-old man.Axial CT scan shows a large carcinoma with gross infiltration of the peri-stomach fatty tissue (white
arrow) and invasion of the left diaphragm (black arrow).This lesion of pT3 was overestimated as cT4a.

observers of cT stage ICC was 0.881 (95 % CI, 0.691–0.774). One way
ANOVA showed that age (p = 0.095), location (p = 0.063), tumor size
(p < 0.001) and VAT grouping (p < 0.001) were potentially correlated
with the accuracy of cT staging (Table 1).

3.2. The difference of VAT between accurate staging group and mistaken
staging group

In the accurate staging group, the average area of VAT was (129.8 ±
72.6) cm2, and in the mistaken staging group, the average area of VAT
was (74.6 ± 61.6) cm2. There was significant difference between them
(p < 0.001, Fig. 3 and Fig. 4). According to the accuracy of cT staging,
the ROC curve of VAT was obtained. According to the Yoden index, the
best cut-off value of preoperative VAT was 97.8 cm2, which was divided
into VAT high group and VAT low group. In the mistaken staging group,
74 patients (74 %) were in the VAT low group (<97.8 cm2) and 26
patients were in the VAT high group (≥97.8 cm2) (Table 1). The in­
cidences of accurate and mistaken staging outcomes among VAT groups
and tumor locations were showed in Fig. 5 and Fig. 6. Because we mainly
studied the effect of VAT on cT staging of gastric cancer, we did not use
size as the basis of grouping. According to the Yoden index, the best cut- Fig. 3. Violin-plot for distribution of VAT between accurate (Acc) and mistaken
off value of tumor size was 3.8 cm. (Mis) staging groups.

3.3. Multivariate logistic regression analysis which presented an approximate judgment, was not an accurate
research, so we relaxed the threshold of p-value accordingly. Mean­
The purpose of this study was mainly to assess the effect of VAT on while, the incidence of gastric cancer increases with age, and the cardia
the accuracy of preoperative T-staging of gastric cancer. This study, and antrum were usually poorly dilated, which may have an impact on

4
T. Ma et al. European Journal of Radiology 155 (2022) 110488

Fig. 4. Comparison between the VAT high / low

group. (A)The area of VAT was 303.63 cm2. The
adequate VAT could separate abdominal organs
from adjacent structures, and also provide natural
contrast and better outline of organs and tumor
boundary;(B) The area of VAT was just 39.94
cm2. This lesion of pT3 was overestimated as
cT4b, because the lesion appeared to be indis­
tinguishable from the gallbladder wall and
pancreas. On account of the poor VAT, the
diseased stomach wall was close to the adjacent
organs, and the existence of partial volume effect
led to the blurring of serosal surface, resulting in
false-positive diagnosis.

Fig. 5. The incidences of accurate (Acc) and mistaken, including underestimate (Under) and overestimate (Over), staging in relation to VAT groups. (A) VAT high
group; (B) VAT low group.

Fig. 6. The incidences of accurate (Acc) and mistaken, including underestimate (Under) and overestimate (Over), staging in relation to tumor locations. (A) Cardia;
(B) Stomach body; (C) Stomach antrum.

cT staging. Therefore, we included age and tumor location in the logistic

Table 3
regression analysis. The results showed that location, tumor size and
Multivariate logistic regression analysis.
VAT group were independent predictors of cT accuracy (Table 3). In the
table, the stomach cardia was used as the reference in order to calculate Variables OR 95 %CI p

odds ratio for the body and antrum; and the low group was taken as the Age 1.016 0.993–1.039 0.187
reference according to the grouping order of VAT in Table 2 (low vs Location 0.013
Cardia Reference
high). Based on the derived data, a visual nomogram was built (Fig. 7).
Stomach body 2,920 1.424–5.987
Stomach antrum 1.754 0.905–3.397
4. Discussion Tumor size 1.253 1.123–1.398 <0.001
VAT group <0.001
Through the analysis of 455 patients with gastric cancer, we found Low Reference
High 5.962 3.516–10.110
that the VAT at the L2/L3 level significantly affected the accuracy of
preoperative cT staging, and patients with low VAT (<97.8 cm2) had a

5
T. Ma et al.
Fig. 7. Nomogram for preoperative accuracy of cT. Value assigned to each factor was scored on a scale of O to 100. Mark patient values at each axis, draw a straight
line perpendicular to the point axis, sum the points for all variables can obtain a total score. Then draw a straight line perpendicular to the probability axis.
higher risk of false staging. In addition, we found that the location of the
tumor (cardia, stomach body, stomach antrum) and the size of the tumor
were also related to the accuracy of staging. Therefore, VAT, tumor
location and size are independent predictors of preoperative cT staging
of gastric cancer.
Surgical resection is still the main treatment for early or advanced
gastric cancer. With the pursuit of refinement and minimally invasive
surgery, different patients will benefit from different surgical methods,
such as endoscopic mucosal resection, endoscopic submucosal dissec­
tion, laparoscopic gastrectomy or re-resection after neoadjuvant
chemotherapy [3,4,17]. Accurate preoperative staging of gastric cancer
is of great significance for the formulation of treatment plan, determi­
nation of resectability, curative effect evaluation and postoperative
rehabilitation. Multi slice spiral CT is the most effective diagnostic tool
for preoperative staging of gastric cancer [6], with high tissue contrast
resolution due to the different degree of enhancement of the mucosa,
submucosa and muscle layer, to judge the level of cancer invasion.
However, its diagnostic effect of some lesion stages is not satisfactory,
and the influencing factors may include individual differences in the
layered display of stomach wall by CT [18], the filling status of anterior
stomach cavity, imaging parameters, post-processing technology, tumor
location and specific variables of the patient [8], etc.
In this study, we noticed that the thin patients had less fat content
around the stomach and the stomach wall of the lesion was close to the
surrounding structures. Due to the influence of the resolution on the CT
image, the stomach wall at the lesion site was blurred, resulting in
misjudgment of staging; In patients with severe cachexia, due to the
depletion of adipose tissue in the stomach wall, the display of various
layers of the stomach wall and the evaluation of the outer surface of the
stomach wall would also be affected. The results of this study confirmed
the effect of VAT on T-stage of gastric cancer, which was consistent with
the results of previous studies. Liu [12] showed that low VAT of L2/L3
level (<122 cm2) and tumor proximal position were independent related
factors affecting the accuracy of T-staging of colon cancer; Reduced fat
thickness around the rectum has been reported to be associated with
misprediction of peripheral margin invasion[19]. VAT surrounds
important abdominal organs, mainly in the greater omentum, mesentery
and retroperitoneal space [20], which not only separate abdominal or­
gans from adjacent structures, but also provide natural contrast and
better outline of organs and tumor boundary. For the stomach, colo­
rectal and other hollow organs, the accuracy of CT in the diagnosis of
serous invasion of stomach wall and intestinal wall is not high, mainly
because the imaging manifestations of tumor invasion, carcinomatous
lymphangitis and inflammatory reaction around the tumor are not easy
to distinguish. At present, the main basis for judging serosal involvement
6
European Journal of Radiology 155 (2022) 110488
is the abnormal enhancement of serosal area and the turbidity of peri-
stomach fatty tissue [21,22]. The content of visceral fat in patients is
decreased, which is directly reflected in the reduction of low-density fat
areas around the stomach cavity in CT images. Therefore, it is easy to
cause the small blood vessels around the stomach cavity packed too
closely, aggregation of lymph nodes or adhesion to the adjacent stomach
wall, giving the false impression of extensive vascular invasion. When
there is less peri-stomach fat, the diseased stomach wall is close to the
adjacent organs (such as liver, pancreas, duodenum, etc.), and the ex­
istence of partial volume effect will lead to the blurring of serosal sur­
face, resulting in false-positive diagnosis. At this time, when the
interface between the lesion and the adjacent structure is blurred, it is
difficult to judge whether it is caused by tumor invasion, which puzzles
the accurate staging and even affects the mode of operation [23,24]. In
this study, we selected the axial CT image at the L2/L3 level to measure
the content of VAT. Firstly, the correlation between the content of VAT
at this level and the volume of total abdominal VAT is the highest [15].
Secondly, this level has a close anatomical relationship with the stomach
cavity and adjacent important organs in the anatomical position, so we
carried out the research on it.
In the results of this study, the overall diagnostic accuracy of CT for
preoperative cT staging of gastric cancer is about 78.0 %, which is
consistent with previous research reports [7]. The diagnostic accuracy of
CT for each stage was the lowest in T2 stage, only 50 % (32 / 64), of
which 23 patients with pT1 stage were overestimated, 5 patients with
pT3 stage and 4 patients with T4a stage were underestimated. The
reasons might be: 1) the key difference between T1 and T2 is the
integrity of the low-density area of the submucosa [25]. If the submu­
cosa is obvious, it could be shown as the poorly enhancing zone between
the avidly enhancing cancer and the less avidly enhancing muscularis
propria. At this time, the reliability of diagnosing cT1 is high, but in
many cases, the submucosa structure cannot be shown. Furthermore,
sometimes the low-density area on CT image is caused by edema or fat
deposition. 2) Stomach serosa reaction and inflammatory reaction of
stomach wall in some pT2 patients were mistaken for serosa invasion,
resulting in overestimation of cT3 or even cT4. 12 patients of pT3
staging were overestimated as cT4. The reasons could be that peri-
stomach inflammatory infiltration was mistaken for carcinomatous
infiltration, or that patients with emaciation usually had a correspond­
ing decrease of peri-stomach adipose tissue, which also could make
staging difficult. Therefore, when determining pT3 tumors, it is neces­
sary to consider the physical condition of the individual patient and
carefully observe the stomach serosal surface and peri-stomach fatty
tissue. 24 patients of pT4 staging were underestimated, among which 1
showed intraoperative mesocolon invasion, 3 showed invasion of the
T. Ma et al.
pancreatic capsule but the CT imaging only displayed rough serosal
surface and clear peri-stomach fatty tissue. A plausible explanation is the
notorious inability of imaging to detect small groups of malignant cells
whichever modality is used. There was 1 case of gastric antral cancer
invading the gallbladder, where the gallbladder change was mis­
diagnosed as cholecystitis due to the presence of fossa fluid. During the
operation, the junction between the lesion and the gallbladder was
found unclear, the two merging into a mass. Therefore, it is necessary to
carefully observe whether the organs around the cancer foci are affected
by cancerous or inflammatory infiltration.
In addition, our results showed that the location and size of the
tumor would also affect the accuracy of preoperative cT staging of
gastric cancer. The gross anatomical study found that there were bare
areas without serosal coverage around the cardia, the posterior wall of
the lesser curvature, the attachment of the stomach wall to the hepato-
stomach ligament and the gastrocolic ligament [8]. Even if the cancer
penetrated through the stomach wall and invaded the surrounding fatty
tissue, the stage was cT3 because it did not break through the visceral
peritoneum. However, the span and width of the bare area varied from
person to person. At present, there is no imaging method to clearly
display the thin serosa, so it is impossible to accurately judge the pres­
ence and extent of the bare area, resulting in the over staging of cT4 in
this area. Similarly, tumors in the stomach body are more likely to have
a close relationship with adjacent organs such as pancreas and colon,
which increases the possibility of wrong staging. The size of the tumor is
mainly related to the extent and depth of invasion of the lesion and the
relationship with the surrounding structure, and these factors them­
selves are the difficulties of staging.
Necessarily, this study also constructed a visual nomogram to make
the results of the prediction model for preoperative accuracy of CT more
readable. For example, when a patient with gastric antrum cancer had a
maximum tumor diameter of about 9 cm and the VAT content of about
100 cm2 (High), the Points (indicating the corresponding single-item
point of each variable under different values) corresponding to the
size, location of the tumor and VAT content were 50, 8, and 48
respectively. After adding them up, the Total Points (representing the
total points of the corresponding single-item points after all variables
take values) was 106. Based on the Total Points, a downward vertical
line was drawn to estimate the accuracy of approximately 96.5 % for
preoperative CT staging.
For the diagnosis of preoperative CT staging of gastric cancer,
attention should be paid to the influence of VAT. In addition, there are a
few more experiences to share. First, CT scans can be performed on
patients in special positions if necessary. Second, for patients with
cachexia or weight loss, the water intake can be reduced as appropriate
to avoid excessive dilatation of the stomach cavity. Third, the window
width and window level can be adjusted depending on the structure
under examination. Through the combination of wide and narrow
windows, the internal invasion and infiltration of the primary lesion and
surrounding organs (such as the pancreas) can be observed through the
narrow window and can be quantitatively measured, while the fatty
tissue between the tumor and surrounding organs can be observed
through the wide window. Fourth, patients with apparent external in­
vasion of gastric cancer have a higher probability of invasion of the
pancreas, and tumors in the stomach antrum are prone to invade the
head of the pancreas and have a low resectability rate. Fifth, increased
density and haziness of the fatty tissue between the tumor and the
pancreas is a common imaging feature of pancreatic invasion and
unresectability, even if the tumor and the pancreas are not in direct
contact. It should be paid attention to in clinical evaluation.
Several potential limitations of this study merit comment: 1) Retro­
spective single center design may lead to selection bias, including pa­
tient selection. 2) Only L2/L3 level visceral fat was selected for the
study, rather than all visceral fat in the abdominal cavity. 3) Post­
operative pT staging was needed to verify the accuracy of preoperative
cT staging. Therefore, the study only included patients who chose open
7
European Journal of Radiology 155 (2022) 110488
surgery, while patients who were suitable for endoscopic mucosal
resection (EMR), endoscopic submucosal dissection (ESD) or extensive
metastasis and had not undergone surgical resection were excluded. 4)
Recently, VAT has been subdivided into intraperitoneal VAT (IVAT) and
retroperitoneal VAT (RVAT). Will they have different effects on the
preoperative staging of gastric cancer? We hope to answer this question
through more prospective research in the future.
5. Conclusions
In this study, VAT, tumor location and tumor size based on L2/L3
level are independent related factors affecting the accuracy of preop­
erative cT staging of gastric cancer. Patients with a lower VAT (<97.8
cm2) at L2/L3 level have a higher risk of false staging. Our results pro­
vide a help for accurate staging and preoperative risk stratification in
patients with different VAT and tumor anatomical characteristics.
Funding
The study was funded by the Natural Science Foundation of Shan­
dong (ZR2020MH289), and Academic promotion programme of Shan­
dong First Medical University (2019QL023).
Ethics approval
The clinical registration number of this study is ChiCTR2100045944.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
The datasets generated and/or analysed during the current study are
available from the corresponding author.
References
[1] H. Sung, J. Ferlay, R.L. Siegel, M. Laversanne, I. Soerjomataram, A. Jemal, F. Bray,
Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality
worldwide for 36 cancers in 185 countries, CA Cancer J. Clin. 71 (3) (2021)
209–249.
[2] A.P. Thrift, H.B. El-Serag, Burden of gastric cancer, Clin. Gastroenterol. Hepatol. 18
(3) (2020) 534–542, https://doi.org/10.1016/j.cgh.2019.07.045.
[3] X.Z. Wang, Z.Y. Zeng, X. Ye, J. Sun, Z.M. Zhang, W.M. Kang, Interpretation of the
development of neoadjuvant therapy for gastric cancer based on the vicissitudes of
the NCCN guidelines, World J. Gastrointest Oncol. 12 (1) (2020) 37–53, https://
doi.org/10.4251/wjgo.v12.i1.37.
[4] E.C. Smyth, M. Nilsson, H.I. Grabsch, N.C.T. van Grieken, F. Lordick, Gastric
cancer, Lancet 396 (10251) (2020) 635–648, https://doi.org/10.1016/s0140-6736
(20)31288-5.
[5] Y. Zhang, J. Yu, The role of MRI in the diagnosis and treatment of gastric cancer,
Diagn. Interv. Radiol. 26 (3) (2020) 176–182, https://doi.org/10.5152/
dir.2019.19375.
[6] M.H. Lee, D. Choi, M.J. Park, M.W. Lee, Gastric cancer: imaging and staging with
MDCT based on the 7th AJCC guidelines, Abdom. Imaging 37 (4) (2012) 531–540,
https://doi.org/10.1007/s00261-011-9780-3.
[7] R.M. Kwee, T.C. Kwee, Imaging in local staging of gastric cancer: a systematic
review, J. Clin. Oncol. 25 (15) (2007) 2107–2116, https://doi.org/10.1200/
JCO.2006.09.5224.
[8] S.L. Lee, Y.M. Ku, H.M. Jeon, H.H. Lee, Impact of the cross-sectional location of
multidetector computed tomography scans on prediction of serosal exposure in
patients with advanced gastric cancer, Ann. Surg. Oncol. 24 (4) (2017) 1003–1009,
https://doi.org/10.1245/s10434-016-5670-9.
[9] O. Jeong, S.Y. Ryu, M.R. Jeong, J.W. Sun, Y.K. Park, Accuracy of macroscopic
intraoperative diagnosis of serosal invasion and risk of over- and underestimation
in gastric carcinoma, World J. Surg. 35 (10) (2011) 2252–2258, https://doi.org/
10.1007/s00268-011-1197-1.
[10] J.Y. Kim, W.S. Chung, H.J. Lee, J.H. An, J.S. Son, Usefulness of histologic
differences and perivascular infiltration for preoperative T staging of advanced
gastric cancer using computed tomography, Jpn. J. Radiol. 37 (12) (2019)
817–825, https://doi.org/10.1007/s11604-019-00887-3.
T. Ma et al.
[11] L. Yang, G. Shi, T. Zhou, Y. Li, Y. Li, Q.-Y. Wei, Quantification of the iodine content
of perigastric adipose tissue by dual-energy CT: a novel method for preoperative
diagnosis of T4-stage gastric cancer, PLoS ONE 10 (9) (2015) e0136871, https://
doi.org/10.1371/journal.pone.0136871.
[12] L.H. Liu, G.F. Zhou, J.J. Zhou, S.X. Rao, M.S. Zeng, Impact of visceral adipose tissue
on the accuracy of T-staging by CT in colon cancer, Eur. J. Radiol. 134 (2021),
109400, https://doi.org/10.1016/j.ejrad.2020.109400.
[13] M. Tanaka, H. Okada, Y. Hashimoto, M. Kumagai, H. Nishimura, M. Fukui, Distinct
associations of intraperitoneal and retroperitoneal visceral adipose tissues with
metabolic syndrome and its components, Clin. Nutr. 40 (5) (2021) 3479–3484,
https://doi.org/10.1016/j.clnu.2020.11.030.
[14] A. Shuster, M. Patlas, J.H. Pinthus, M. Mourtzakis, The clinical importance of
visceral adiposity: a critical review of methods for visceral adipose tissue analysis,
Br. J. Radiol. 85 (1009) (2012) 1–10, https://doi.org/10.1259/bjr/38447238.
[15] X. Cheng, Y. Zhang, C. Wang, W. Deng, L. Wang, Y. Duanmu, K. Li, D. Yan, L. Xu,
C. Wu, W. Shen, W. Tian, The optimal anatomic site for a single slice to estimate
the total volume of visceral adipose tissue by using the quantitative computed
tomography (QCT) in Chinese population, Eur. J. Clin. Nutr. 72 (11) (2018)
1567–1575.
[16] K. Washington, 7th edition of the AJCC cancer staging manual: stomach, Ann Surg
Oncol. 17 (12) (2010) 3077–3079, https://doi.org/10.1245/s10434-010-1362-z.
[17] H. Ono, K. Yao, M. Fujishiro, I. Oda, S. Nimura, N. Yahagi, H. Iishi, M. Oka,
Y. Ajioka, M. Ichinose, T. Matsui, Guidelines for endoscopic submucosal dissection
and endoscopic mucosal resection for early gastric cancer, Dig. Endosc. 28 (1)
(2016) 3–15.
[18] C.-Y. Chen, J.-S. Hsu, D.-C. Wu, W.-Y. Kang, J.-S. Hsieh, T.-S. Jaw, M.-T. Wu, G.-
C. Liu, Gastric cancer: preoperative local staging with 3D multi-detector row
European Journal of Radiology 155 (2022) 110488
CT—correlation with surgical and histopathologic results, Radiology 242 (2)
(2007) 472–482.
[19] Y.-W. Kim, S.-W. Cha, J. Pyo, N.-K. Kim, B.-S. Min, M.-J. Kim, H. Kim, Factors
related to preoperative assessment of the circumferential resection margin and the
extent of mesorectal invasion by magnetic resonance imaging in rectal cancer: a
prospective comparison study, World J. Surg. 33 (9) (2009) 1952–1960.
[20] B. Bjørndal, L. Burri, V. Staalesen, J. Skorve, R.K. Berge, Different adipose depots:
their role in the development of metabolic syndrome and mitochondrial response
to hypolipidemic agents, J. Obes. 2011 (2011) 1–15.
[21] A. Kupeli, E. Bulut, A. Cansu, A. Guner, M. Soyturk, G. Danisan, Contribution of
DECT in detecting serosal invasion of gastric cancer, Turk. J. Med. Sci. 49 (3)
(2019) 782–788, https://doi.org/10.3906/sag-1811-168.
[22] R.-J. Sun, L. Tang, Y. Chen, X.-T. Li, Y.u. Sun, Z.-Y. Li, Y.-S. Sun, Feasibility of
differentiating T3 from T4a gastric cancer in different Lauren classification by
determining serosa invasion: diagnostic performance of high enhanced serosa sign,
Chin J. Cancer Res. 30 (2) (2018) 263–271.
[23] H. Zhao, W. Chen, Y. Lin, J. Qin, L. Wang, Analysis of surgery for incurable gastric
cancer, World J. Surg. Oncol. 13 (2015) 339, https://doi.org/10.1186/s12957-
015-0750-z.
[24] D.B. Li, J. You, S.J. Wang, Y.M. Zhou, Pancreaticoduodenectomy for locally
advanced gastric cancer: results from a pooled analysis, Asian J. Surg. 42 (3)
(2019) 477–481, https://doi.org/10.1016/j.asjsur.2018.09.005.
[25] X.-y. Feng, W. Wang, G.-y. Luo, J. Wu, Z.-W. Zhou, W. Li, X.-W. Sun, Y.-F. Li, D.-
Z. Xu, Y.-X. Guan, S. Chen, Y.-Q. Zhan, X.-S. Zhang, G.-L. Xu, R. Zhang, Y.-b. Chen,
K. Takabe, Comparison of endoscopic ultrasonography and multislice spiral
computed tomography for the preoperative staging of gastric cancer - results of a
single institution study of 610 Chinese patients, PLoS ONE 8 (11) (2013) e78846,
https://doi.org/10.1371/journal.pone.0078846.