Preliminary differentiation of benign and malignant gastric wall thickening using dual-layer spectral-detector CT

Abstract

Background

Dual-layer spectral-detector computed tomography (DLCT) may have the potential to evaluate gastric wall thickening.

Purpose

To evaluate the efficacy of DLCT quantitative parameters in differentiating between benign and malignant thickening of the gastric wall.

Material and Methods

A total of 58 patients with “gastric wall thickening” who underwent multi-phase abdominal enhanced DLCT scans were included in this study. Of these patients, 33 were malignant and 25 were benign. Parameters such as iodine concentration (IC), effective atomic number (Zeff), and attenuation of the lesions were measured during the arterial phase (AP) and venous phase (VP). Binary logistic regression was employed to calculate the combined prediction probabilities. The accuracy of the DLCT parameters was assessed using receiver operating characteristic (ROC) curves.

Results

The values of IC, nIC, Zeff, normalized Zeff, and attenuation in the AP and VP were significantly higher (all P < 0.05) in the malignant group compared to the benign group. The ROC curves revealed that the IC, Zeff, and attenuation in the VP exhibited high diagnostic performance, with area under the ROC curve (AUC) values of 0.864, 0.862, and 0.840, respectively. The new combination of these three factors and gastric wall thickness had an AUC of 0.884, and the sensitivity and specificity were determined to be 81.8% and 92.0%, respectively.

Conclusion

Spectral CT parameters, particularly the combination of gastric wall thickness, attenuation, IC, and Zeff in VP, have value in distinguishing between benign and malignant gastric wall thickening.

Keywords

Dual-layer spectral-detector computed tomography DLCT spectral computed tomography gastric wall thickening differential diagnosis

Introduction

Gastric cancer ranks as the fifth most prevalent type of cancer and stands as the third leading cause of cancer-related mortality globally (1). There are more than 1 million new cases in the world every year, including about 780,000 deaths (2). Early detection is one of the most crucial aspects affecting therapy and prognosis of the disease as gastric cancer is extremely aggressive and heterogeneous (3). The median survival duration for patients with advanced stomach cancer is fewer than 12 months (4), and gastric cancer tends to be found at the advanced stage. Early detection, diagnosis, and treatment of stomach cancer can increase patients’ clinical therapeutic effect and quality of life.

The diagnostic methods of gastric cancer include gastroscopy, computed tomography (CT), upper gastrointestinal barium meal, and ultrasound, among others (1,5). Gastroscopy is the most important examination for the detection of gastric lesions because of its high detection rate of small lesions and the ability to obtain diseased tissue for biopsy during the examination. Although gastroscopic biopsy is the gold standard for detecting gastric mucosal diseases, it can lead to misdiagnosis due to sampling error. Moreover, the requirement for subsequent endoscopy due to the gastric wall thickening detected on CT results in increased costs and delayed treatment (6). In addition, the invasive procedure of gastroscopy can cause distress, leading to poor compliance with gastroscopy in some patients. The elderly, the frail, and the patients with severe heart and lung diseases may not tolerate endoscopy. At this time, CT examination may be the most valuable diagnostic technique. CT is extensively employed in patients with various abdominal pain disorders (7). CT can be used to observe the lumen, wall, surrounding tissue and lymph node enlargement of the gastrointestinal tract. Gastric cancer mainly shows segmental or diffuse gastric wall thickening on CT, but some benign lesions, such as inflammation, ulcer, polyp, eosinophil infiltration, and Menetrier disease, can also result in significant gastric wall thickening (8). Evaluation of benign and malignant gastric wall thickening can provide a basis for clinical management.

As a new energy imaging mode, dual-layer spectral-detector CT (DLCT) has recently shown its unique properties and advantages. It has two unique detector layers – the upper detector detects and absorbs low-energy X-ray photons, while the lower detector absorbs high-energy X-ray photons (9) – which can obtain high-energy and low-energy data at the same time and generate different image sets: iodine concentration (IC) map; effective atomic number (Zeff) map; virtual monoenergetic images (VMI); virtual non-contrast (VNC) images; and electron density (ED) map. Numerous studies have already demonstrated the value of DLCT: the ED-Zeff ratio in the unenhanced phase was one of the independent predictors for diagnosing invasive adenocarcinoma presenting as pure ground-glass nodules (10). IC and Zeff can enhance the quantitative and qualitative differentiation between upper aerodigestive head and neck squamous cell carcinoma and normal mucosa (11). The area under the receiver operating characteristic (ROC) curve (AUC) of IC in identifying high-grade gliomas was 0.865 (12). In patients with thickened gastric wall shown on CT, it is important to distinguish between benign and malignant conditions. However, the use of DLCT-derived parameters to distinguish between malignant and benign thickening of the gastric wall is still in the exploratory stages. Therefore, the aim of the present study was to investigate the potential of quantitative DLCT parameters in differentiating between benign and malignant gastric wall thickening.

Material and Methods

This retrospective study received approval from our ethics committee and institutional review board (2023-073-02-YJ), and the requirement for written informed consent was waived.

Patients

We searched the CT reports of patients who underwent both unenhanced and contrast-enhanced abdominal CT scan on DLCT for any reason between January 2020 and June 2022 with the keyword “gastric wall thickening” in the PACS in our hospital. We first screened patients with gastric wall thickening as seen in the CT images. The following patients were then excluded: (i) those who underwent surgery before DLCT scan; (ii) those who had no pathology within 1 month after DLCT scan or gastroscopy within 1 month before and after DLCT scan; (iii) those without adequate gastrointestinal preparation; and (iv) those with poor image quality or lesions that could not be measured. Subsequently, based on the electronic medical record system, the age, sex, lesion location (fundus, body, or antrum), gastric wall thickness (on CT images), and histologic diagnosis of each patient were recorded. According to endoscopy or surgical pathology, these individuals were split into benign and malignant groups.

DLCT scan

The examinations were conducted using a DLCT scanner (IQon; Philips Healthcare) for all participants. Craniocaudal scans were performed in all patients in the supine position. Abdominal CT protocols at our institution include non-enhanced, arterial phase, portal phase, and delayed phase. After the non-contrast phase was obtained, iodinated contrast material (Ultravist 370; Schering, Berlin, Germany) was administered into the patients’ antecubital vein at a rate of 3 mL/s at a dose of 1 mL/kg body weight. After administration of the contrast agent, the arterial phase, venous phase, and delayed phase were observed at 25 s, 60 s, and 180 s, respectively. The following scanning parameters were used: collimation = 64 × 0.625 mm; pitch = 1.2; rotation time = 0.5 s; reconstruction matrix = 512 × 512; tube voltage = 120 kVp; tube current = automated modulation in the range of 69–144 mAs.

Image analysis

All DECT data were transferred to the image viewing and postprocessing tool (IntelliSpace Portal version 9.0; Philips Healthcare). A circular or ovoid region of interest (ROI) was selected at the slice where the lesion was most visible in the axial arterial or venous phase images, not smaller than 75 mm², and as large as possible and avoiding necrosis, cystic degeneration, calcification, and large vessels. (For cases with multiple lesions, the largest lesion was just chosen.) Then ROI was copied to other DLCT image sets to obtain the measured values, including CT attenuation values in the non-contrast phase, arterial phase, and venous phase, and IC and Zeff in the arterial phase and venous phase. Normalized IC and Zeff were derived by dividing the IC and Zeff of the lesion to that of abdominal aorta at the same slice (nIC = IC-lesion/IC-abdominal aorta; nZeff = Zeff-lesion/Zeff-abdominal aorta). The measurements were repeated three times and the average values were recorded. Two radiologists (with 5 and 4 years of experience in abdominal radiology, respectively) performed the measurements independently, blinded to clinical details and research design. The average values from two radiologists for each lesion were taken as final records.

Statistical analysis

The statistical analysis was conducted using SPSS version 25.0 (IBM Corp., Armonk, NY, USA). The normal distribution and homogeneity of variance of continuous variables were assessed using the Shapiro–Wilk test and Levene test, respectively. Continuous variables that followed a normal distribution and exhibited homogeneity of variance were represented as mean ± standard deviation (SD), and those that did not follow a normal distribution were expressed using median (interquartile range [IQR]). The t-test or Wilcoxon rank-sum test was used to compare quantitative measures between the two groups. Categorical variables were displayed as frequencies and percentages and analyzed using the chi-square test. The diagnostic efficacy of the quantitative parameters was evaluated using ROC curves. The optimal thresholds were determined based on Youden's index, and the relevant sensitivity and specificity were derived. The combined predictive probabilities were calculated using binary logistic regression. Statistical significance was defined as P < 0.05.

Results

Clinical characteristics

A total of 58 patients with “gastric wall thickening” on enhanced DLCT were included in this study after excluding patients who did not meet the requirements (Fig. 1). Among them, 33 patients were diagnosed with malignant gastric wall thickening and 25 patients were diagnosed with benign gastric wall thickening. Table 1 provides an overview of the basic clinical and CT features of all patients in both the benign and malignant groups. The analysis revealed no significant difference in age (P = 0.931) and lesion location (P = 0.089) between the two groups. However, there were notable differences in sex (P = 0.043) and lesion thickness (P < 0.001).

Fig. 1.

Flowchart of patient selection. DLCT, dual-layer spectral-detector computed tomography.

Table 1.

Patient characteristics.

Characteristics	Benign group (n = 25)	Malignant group (n = 33)	P
Age (years)	59 (54.5–66)	63 (47–68.5)	0.931
Sex			0.043
Male	10 (40)	22 (67)
Female	15 (60)	11 (33)
Lesion site			0.089
Fundus	6 (24)	4 (12)
Body	2 (8)	10 (30)
Antrum	17 (68)	19 (58)
Lesion thickness (mm)	12.4 (11.1–15.5)	19 (15–22.4)	<0.001
Attenuation (HU)
Unenhanced	39.0 ± 6.12	37.8 ± 5.63	0.424
Arterial phase	51.0 (47.3–58.8)	65.7 [(5.7–78.9)	<0.001
Portal venous phase	64.2 (55.6–70.7)	95.1 (71.9–111.3)	<0.001

Values are given as n (%), mean ± SD, or median (range).

P from two-sample t-tests or Wilcoxon rank-sum tests.

Comparison of DLCT parameters between two groups

The comparison of DLCT quantitative characteristics between the benign and malignant groups was shown in Table 2. Except nZap, all DLCT measurements showed non-normal distribution or heterogeneity of variance. Compared with benign gastric wall thickening, the median IC (0.99 vs. 0.51 mg/mL), nIC (0.10 vs. 0.05), Zeff (7.87 vs. 7.59), and mean nZeff (0.71 vs. 0.69) of malignant gastric wall thickening in the arterial phase were higher (all P < 0.05); the median IC (1.95 vs 0.91 mg/mL), nIC (0.40 vs 0.24), Zeff (8.35 vs 7.83), and nZeff (0.88 vs 0.85) in the venous phase were higher (all P < 0.05). Compared with benign gastric wall thickening, malignant gastric wall thickening also showed higher median attenuation values in the arterial phase (65.7 vs. 51.0 HU) and venous phase (95.1 vs. 64.2 HU) (both P < 0.05). There was no significant difference in mean attenuation value (37.8 vs. 39.0 HU) between the two groups in the non-enhanced phase (P = 0.424) (Table 1). Fig. 2 provides box-and-whisker plots comparing benign and malignant gastric wall thickening in terms of DLCT parameters.

Fig. 2.

Box-and-whisker plots comparing benign and malignant gastric wall thickening in terms of DLCT parameters: (a) IC in the AP; (b) IC in the VP; (c) Zeff in the AP; and (d) Zeff in the VP. Boxes show the upper and lower quartiles, and horizontal lines within boxes indicate median values. Whiskers represent 95th and 5th percentiles. AP, arterial phase; DLCT, dual-layer spectral-detector computed tomography; IC, iodine concentration; VP, venous phase; Zeff, effective atomic number. All P < 0.001.

Table 2.

Comparison of parameters detected from dual-layer spectral-detector CT between benign and malignant groups.

Measure	Benign group (n = 25)	Malignant group (n = 33)	P
Arterial phase
IC (mg/mL)	0.51 (0.36–0.80)	0.99 (0.58–1.44)	<0.001
Normalized IC	0.05 (0.03–0.08)	0.10 (0.06–0.14)	0.001
Zeff	7.59 (7.49–7.77)	7.87 (7.63–8.12)	<0.001
Normalized Zeff	0.69 ± 0.04	0.71 ± 0.04	0.038
Venous phase
IC (mg/mL)	0.91 (0.78–1.17)	1.95 (1.31–2.64)	<0.001
Normalized IC	0.24 (0.21–0.29)	0.40 (0.32–0.62)	<0.001
Zeff	7.83 (7.76–7.98)	8.35 (8.06–8.65)	<0.001
Normalized Zeff	0.85 (0.84–0.87)	0.88 (0.86–0.93)	0.001

Values are given as mean ± SD, or median (range). P from two-sample t-tests or Wilcoxon rank-sum tests.

CT, computed tomography; IC, iodine concentration; Zeff, effective atomic number.

Diagnostic value of quantitative parameters

Table 3 and Figs. 3 and 4 show the ROC characteristics of spectral quantitative parameters for malignant gastric wall thickening. CTvp, ICvp, and Zvp had the highest AUCs in attenuation-related variables (CTap, CTvp), IC-related variables (ICap, nICap, ICap, nICap), and effective atomic number related variables (Zap, nZap, ICvp, and nICvp), respectively, which all have high diagnostic value. The optimal threshold was confirmed when the Youden indexes were highest. At the threshold of 71.417 HU, 1.280 mg/mL, and 8.045, the sensitivity and specificity were 78.8%, 78.8%, 78.8% and 80.0%, 88.0%, 88.0%, respectively. After combining thickness, CTvp, ICvp, and Zvp for binary logistic regression to generate combination parameters, combination 1 (thickness, CTvp, ICvp and Zvp) has the highest AUC of 0.884, while the sensitivity was 81.8%, and the specificity was 92.0%. The AUC of combination 2 (CTvp, ICvp, and Zvp) is relatively low, which was 0.844. Fig. 5 showed the DLCT images of a patient with chronic superficial gastritis in whom the parameters did not meet the threshold for predicting malignant gastric wall thickening. Fig. 6 showed the DLCT images of a patient with antral adenocarcinoma in whom the parameters met the threshold for predicting malignant gastric wall thickening.

Fig. 3.

Receiver operating characteristic curves for differentiating benign and malignant based on parameters from dual-layer spectral-detector CT, using continuous variables that were statistically different between the two groups. AP, arterial phase; CT, computed tomography; IC, iodine concentration; n, normalized; VP, portal venous phase; Zeff, effective atomic number.

Fig. 4.

Receiver operating characteristic curves for differentiating benign and malignant based on parameter combination 1 generated from binary logistic regression for gastric wall thickness, attenuation, IC, and Zeff in the venous phase; and combination 2 for attenuation, IC and Zeff in the venous phase. IC, iodine concentration; Zeff, effective atomic number.

Fig. 5.

A 64-year-old woman with chronic superficial gastritis in the antrum on biopsy, who underwent pretreatment dual-layer spectral-detector CT. (a) Axial venous phase contrast-enhanced image, (b) IC map, and (c) Zeff map show gastric wall thickening (green circle). In the venous phase, lesion exhibits attenuation of 55.6 HU, IC of 0.86 mg/mL, and Zeff of 7.84. Values do not meet thresholds for predicting malignant lesion based on thresholds shown in Table 3. CT, computed tomography; IC, iodine concentration; Zeff, effective atomic number.

Fig. 6.

A 55-year-old woman with adenocarcinoma in the antrum on resection, who underwent preoperative dual-layer spectral-detector CT. (a) Axial venous phase contrast-enhanced image, (b) IC map, and (c) Zeff map show gastric wall thickening (green circle). In the portal venous phase, lesion exhibits attenuation of 94.5 HU, IC of 1.96 mg/mL, and Zeff of 8.34. Values meet thresholds for predicting malignant lesion based on thresholds shown in Table 3. CT, computed tomography; IC, iodine concentration; Zeff, effective atomic number.

Table 3.

ROC curve of continuous variables with significant differences between the two groups.

Parameter	AUC	P	Threshold	Youden index	Sensitivity (%)	Specificity (%)
Lesion thickness (mm)	0.818	<0.001	14.250	0.568	84.8	72.0
Attenuation (HU)
Arterial phase	0.773	<0.001	61.250	0.446	60.6	84.0
Venous phase	0.840	<0.001	71.417	0.588	78.8	80.0
Arterial phase
IC (mg/mL)	0.776	<0.001	1.068	0.485	48.5	100
Normalized IC	0.761	0.001	0.088	0.425	54.5	88.0
Zeff	0.775	<0.001	7.922	0.485	48.5	100
Normalized Zeff	0.640	0.07
Venous phase
IC (mg/mL)	0.864	<0.001	1.280	0.668	78.8	88.0
Normalized IC	0.841	<0.001	0.319	0.668	78.8	88.0
Zeff	0.862	<0.001	8.045	0.668	78.8	88.0
Normalized Zeff	0.758	0.001	0.878	0.526	60.6	92.0
Combination 1	0.884	<0.001	0.487	0.738	81.8	92.0
Combination 2	0.844	<0.001	0.471	0.658	81.8	84.0

AUC, area under the ROC curve; IC, iodine concentration value; ROC, receiver operating characteristic; Zeff, effective atomic number.

Discussion

CT is extensively employed in patients with various abdominal pain disorders (7), and radiologists sometimes observe the presence of thickened gastric wall on abdominal CT. Diseases causing gastric wall thickening include benign and malignant gastric tumors, inflammation-related diseases, and liver cirrhosis (13). When the thickness of the gastric wall is ≥1 cm, it will be suspected of malignant tumors. However, these are only morphological criteria and lack the analysis of quantitative parameters.

Dual-energy CT spectral images have very important clinical quantitative value, and a variety of quantitative parameters provided by them can reveal more characteristics of diseases and improve the detection of certain diseases (14,15). Previous studies have reported that quantitative parameters of dual-energy CT can help to distinguish malignant and benign orbital tumors (16), pulmonary metastatic nodules of thyroid cancer and benign nodules (17), intrahepatic cholangiocarcinoma and hepatocellular carcinoma (18), and solitary pulmonary tuberculosis and solitary lung adenocarcinoma (19). Our study suggests the potential application of quantitative indices of DLCT in the differentiation of benign and malignant gastric wall thickening. The study revealed that the DLCT parameters of malignant versus benign gastric wall thickening were significantly different, and the cutoff values of each DLCT parameter used to distinguish malignant from benign gastric wall thickening were determined. The AUCs of attenuation value, IC, and effective atomic number in the venous phase were 0.840, 0.864 and 0.862, respectively. The AUC of the combination of these three parameters was 0.844, which was not significantly improved. The AUC of the combination of these three parameters and gastric wall thickness was 0.884. At the derived threshold, the sensitivity and specificity for differentiating malignant from benign gastric wall thickening were 81.8% and 92.0%, respectively. Therefore, the new variable (Combination 1) improves accuracy by combining information of DLCT parameters and gastric wall thickness. Among them, the improved specificity better avoids unnecessary endoscopy in non-malignant patients (20), as the specificity reflects the ability to identify benign gastric wall thickening.

Previously, Meng et al. (21) evaluated the value of quantitative parameters in dual-energy CT for distinguishing between malignant and benign gastric mucosal lesions, including gastritis (GI) and normal gastric mucosa (NGM), based on the rapid kVp switching system. The IC and nIC of GC were significantly different from those of GI and NGM, except for the nICap of GC compared with GI. The sensitivity of nIC and IC in the portal venous phase for distinguishing GC from benign gastric mucosal lesions was 88.89% and 90.48%, respectively. Feng et al. (20) developed and validated a diagnostic model for preoperative identification of malignant gastric distal wall thickening based on dual-source CT (DSCT). This model included two factors, venous phase spectral curve (VP_SC) and focal enhancement, and showed an AUC of 0.803 in the diagnosis of malignant wall thickening in the distal stomach. Unlike the study by Feng et al., we investigated not only the distal stomach, but the body and fundus of the stomach as well. In addition, previous studies were based on rapid kVp switching or dual-source CT systems, while the application of dual-layer spectral detector CT in the differentiation of benign and malignant gastric wall thickening has not been reported. According to the literature review, this is the first study to use quantitative parameters of DLCT to differentiate malignant and benign gastric wall thickening.

In the IC map, all substances except iodine are suppressed, and iodine-containing pixels are assigned a value of the iodine concentration in each pixel (9). Quantitative IC serves as a reliable measure of blood flow as it aligns with the true iodine deposition in tissues (22), thus reflecting the blood supply of tissues and organs, the angiogenesis of lesions, and hemodynamic changes (23). Unlike normal tissue or benign lesions, the proliferation of tumors relies on the development of new blood vessels. These is evidence suggesting that IC is closely related to vascular endothelial growth factor (VEGF) and micro-vessel density (MVD) in patients with advanced gastric cancer (24). Effective atomic number images are color-coded based on the effective atomic number of the tissue. Zeff refers to the composite atoms of a mixture of various materials or a compound. The effective atomic number is more discriminating than the attenuation of conventional CT images because it can well reflect the material composition of the tissue (25). In our study, the IC value and effective atomic number of malignant gastric wall thickening were higher than those of benign gastric wall thickening in both the arterial and venous phases. Furthermore, we also investigated the normalized IC (nIC) versus normalized Zeff (nZeff) based on the abdominal aorta (26), which can reduce the effect of circulatory differences in different patients. In previous studies, nIC was defined as the tumor's IC divided by the aorta's IC, and nIC was considered a relatively stable indicator and superior to IC in tumor staging and treatment evaluation (27,28). In our study, consistent with the results of IC and Zeff, nIC and nZeff of malignant gastric wall thickening were higher than those of benign gastric wall thickening in both arterial and venous phases.

The findings of this study regarding the role of quantitative parameters of DLCT in differentiating malignant from benign gastric wall thickening are positive. When gastric wall thickening is found on CT, the quantitative parameters of DLCT can be used to preliminarily judge the benign and malignant of gastric wall thickening, so as to decide whether to take further examination, which may reduce the economic burden and time cost of patients. In addition, DLCT quantitative parameters can also assist pathological analysis. For example, DLCT quantitative parameters can predict the most malignant location of the lesion and guide biopsy sampling, thereby reducing sampling error. The patients of non-surgical treatment for whom complete specimens cannot be acquired can also benefit from DLCT (29).

The present study has some limitations. First, the study was retrospective and conducted at a single institution, which would have introduced selection bias. Second, the sample size was somewhat small, and the study was conducted at the level of a group. Future studies with larger patient populations are necessary to improve statistical power. However, the results of this study still show the potential application of spectral CT quantitative parameters in the distinction between benign and malignant gastric wall thickening.

In conclusion, DLCT parameters have high diagnostic value in distinguishing between benign and malignant gastric wall thickening. There were significant differences in DLCT parameters between benign and malignant gastric wall thickening. These findings may contribute to the early detection and treatment of gastric malignancies.

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study has received funding by the Shenzhen Science and Technology Foundation (JCYJ20200109120205924) and “Study on Enhancing the Curriculum for Master of Medicine Programs” of Shenzhen University Medical School.

ORCID iDs

Hongjian Li

Weihua Li

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