Clinical application of oral contrast-enhanced ultrasound in evaluating the preoperative T staging of gastric cancer

Abstract

BACKGROUND

Oral contrast-enhanced ultrasound (OCEUS) is widely used in the noninvasive diagnosis and screening of gastric cancer (GC) in China.

AIM

To investigate the clinical application of OCEUS in evaluating the preoperative T staging of gastric cancer.

METHODS

OCEUS was performed before the operation, and standard ultrasound images were retained. The depth of infiltration of GC (T-stage) was evaluated according to the American Joint Committee on Cancer 8^th edition of the tumor-node-metastasis staging criteria. Finally, with postoperative pathological staging as the gold standard reference, the sensitivity, specificity, negative predictive value, positive predictive value, and diagnostic value of OCEUS T staging were evaluated.

RESULTS

OCEUS achieved diagnostic accuracy rates of 76.6% (T1a), 69.6% (T1b), 62.7% (T2), 60.8% (T3), 88.0% (T4a), and 88.7% (T4b), with an average of 75.5%. Ultrasonic T staging sensitivity exceeded 62%, aside from T1b at 40.3%, while specificity was over 91%, except for T3 with 83.5%. The Youden index was above 60%, with T1b and T2 being exceptions. OCEUS T staging corresponded closely with pathology in T4b (kappa > 0.75) and moderately in T1a, T1b, T2, T3, and T4a (kappa 0.40-0.75), registering a concordance rate exceeding 84%.

CONCLUSION

OCEUS was effective, reliable, and accurate in diagnosing the preoperative T staging of GC. As a noninvasive diagnostic technique, OCEUS merits clinical popularization.

Key Words: Gastric cancer; Oral contrast-enhanced ultrasound; Tumor-node-metastasis staging; Noninvasive diagnosis and screening; Clinical value

Core Tip: This study evaluated the efficacy of oral contrast-enhanced ultrasound (OCEUS) for preoperative T staging of gastric cancer, adhering to the American Joint Committee on Cancer 8^th edition criteria. The results demonstrated the high diagnostic accuracy, reliability, and noninvasive advantages of OCEUS, supporting its use as a valuable tool for clinical staging and potentially improving treatment strategies for patients with gastric cancer.

INTRODUCTION

Gastric cancer (GC) is one of the most common malignant tumors of the digestive tract. Recently published global cancer research data show that the incidence of GC ranked fifth in the world in 2020[1], and it is reported to be even higher in China, ranking fourth in incidence of malignant tumors and third in mortality rate, seriously threatening people's lives and health[2]. There are regional differences in the survival and prognosis of patients with GC at home and abroad. The reason for this discrepancy may be due to differences in the staging criteria for GC[3,4], which are considered highly ambiguous. The current international standard for GC staging is based on the Union for International Cancer Control and American Joint Committee on Cancer (AJCC) tumor-node-metastasis (TNM) staging system (8^th edition)[5]. According to postoperative pathological observations of the depth of tumor infiltration into the gastric wall, tumors are classified into T1-T4 stages, and imaging T staging is based on pathological criteria[6].

Different imaging techniques, such as endoscopic ultrasonography (EUS), computed tomography (CT), magnetic resonance imaging (MRI), and positron emission tomography/CT, have good diagnostic efficacy in judging the size and range of cancer, depth of invasion and lymph node metastasis[6,7], and they can accurately perform TNM staging of GC.

Oral contrast-enhanced ultrasound (OCEUS), a noninvasive, free from radiation hazards, and convenient screening method for GC, could be a beneficial supplement to T staging of GC[8]. OCEUS has been widely used in China for a long time, but outside of China, filling of the stomach cavity is still performed with drinking water when performing gastric ultrasound[9,10].

We explored the clinical value of OCEUS in preoperative T staging of GC to improve the acceptance and recognition of OCEUS worldwide.

MATERIALS AND METHODS

Data retrieval

A retrospective analysis of the medical records of GC patients was performed. All clinical data were completely anonymous, and the requirement for informed consent was waived by our ethics committee. In this study, the following inclusion criteria were used to determine GC cases: (1) GC confirmed by pathological results after surgical resection of the gastric mass; (2) Performance of preoperative OCEUS examination, with clear ultrasound images; (3) Postoperative pathological results clearly describing the depth of the mass infiltration; and (4) Accurate basic clinical information. The exclusion criteria were as follows: (1) Patients with GC confirmed by gastroscopic biopsy without surgery; (2) Patients with suspected GC by gastroscopic biopsy but confirmed nonGC by postoperative pathology; (3) Patients with poor image quality on OCEUS examination, which impacts the staging judgement; and (4) Patients with preoperative gastric tumors receiving radiotherapy, chemotherapy, endoscopic partial resection or other treatment.

Methods of OCEUS examination

Instruments: Color Doppler ultrasound diagnostic instruments such as Mindray DC-80, Philips EPIQ5, Samsung RS80A, Supersonic Aixplorer, Canon Aplio i800, convex array probes (frequency 3.5-5 MHz), and line array probes (frequency 7.5-15 MHz) were used.

Oral contrast agent for assistive display: The gastrointestinal oral contrast-assisted display agent was produced by China Yanbian Junyi Medical Technology Company Limited. The main ingredients are lotus root, coix seed, orange peel, rice, corn, and soybean.

Methods

A total of 25 g of gastrointestinal oral contrast assistant display agent was brewed with 500 mL boiling water and mixed thoroughly to achieve a paste. The subject fasted for 8-12 hours, followed by oral intake of the display agent. The clinician initiated ultrasound to perform continuous dynamic examinations of multiple sections. The order of scanning was as follows: Cardia; the gastric fundus; the anterior and posterior walls of the gastric body; the size curve of the gastric body; the gastric angle; the gastric antrum; the duodenal bulb; the descending part; the horizontal part; the perigastric and distant lymph nodes; the liver; the pancreas; the abdominal cavity; and the pelvic cavity. The examination positions were the left lateral position, supine position, and right lateral position. Multisection scanning was used to observe the structure of the gastric wall and the shape and peristalsis of the stomach. After the location of the lesion was determined, the thickness and the maximum upper and lower diameters of the lesion were measured, the standard images were retained, and the hierarchical structure of the gastric wall was examined by local magnification. All operations were performed by physicians with expertise in gastrointestinal ultrasound diagnostic procedures.

Research methods

The OCEUS results and pathological results of GC patients were obtained from the Picture Archiving and Communication System. First, two intermediate gastrointestinal ultrasound physicians collected basic clinical data and postoperative pathological descriptions of the tumor infiltration depth data according to the pathological description of gastric mass infiltration depth to determine the pathological T staging (pT). In cases of disagreement, consensus was achieved through discussion. Second, the other two senior gastrointestinal ultrasound doctors used the double-blind method to analyze the infiltration depth of the gastric mass according to the OCEUS images and determined the clinical T staging, namely, ultrasound T staging (T). In cases of disagreement, consensus was achieved through discussion. Finally, the consistency of T and pT was compared, and the diagnostic efficacy of T was evaluated.

Evaluation criteria

PT criteria for GC: PT was performed according to the diagnostic criteria of the AJCC TNM staging system (8^th edition), as shown in Table 1. Ultrasonic T staging criteria for GC: According to the relevant literature[11,12], the ultrasound image of a normal gastric wall shows five layers represented by the parallel arrangement of three hyperechoic bands and two hypoechoic bands, indicating the following structures from inside to outside: The interface echo of the mucosal layer and gastric cavity (superficial mucosal layer), the interface echo of the mucosal lamina propria and muscular layer (deep mucosal layer), the interface echo of the muscularis mucosa and submucosa, the echo of the muscularis propria, and the echo of the serosal layer and external serosal tissue. T was performed according to the degree of infiltration of the gastric lesion revealed by OCEUS, as shown in Table 1.

Table 1 Pathological and ultrasonic T staging criteria.

T stages	Pathological definition	Ref. ultrasonic imaging
T1a	The tumor invades the lamina propria or the mucosal muscularis layer	Layer 1 (superficial mucosal layer) continuity interrupted, Layer 2 (deep mucosal layer) low-echo thickening, Layer 3 (submucosa) remains continuous
T1b	The tumor invades the submucosa	Layer 3 (submucosa) high-echo continuity interrupted, muscularis propria layer and serosa layer is intact
T2	The tumor invades the muscularis propria	Layer 4 (muscularis propria) low-echo invasion, with the outer layer retaining a smooth echo boundary
T3	The tumor penetrates the subserosal connective tissue but does not invade the visceral peritoneum	Each layer structure completely disappears, but the outermost layer retains a smooth high-echo band (serosal layer)
T4a	The tumor invades the serosal membrane (visceral peritoneum) but not the adjacent structures/organs	Each layer structure completely disappears, and the high-echo band (serosal layer) disappears, or there is a clearly visible serosal layer high-echo line breakthrough with a burr sign or crab foot sign
T4b	Tumors invade the adjacent structures/organs	The whole layer is involved, and the echo boundary between the adjacent organ structure (aorta, pancreas, liver, etc.) disappears, and it adheres with the adjacent organs without relative movement

Statistical analysis

All the study data were statistically analyzed and plotted using SPSS 26.0 and MedCalc software. The count data are expressed as the number of cases (n) or percentage (%), and comparisons between groups were performed using the χ² test or Fisher’s exact probability method. The postoperative pathological results were used as the "gold standard"; the accuracy rate was expressed as a percentage when the sensitivity, specificity, positive predictive value, and negative predictive value of OCEUS examination for preoperative T staging of GC were determined. The following formula was applied: Sensitivity = {true positive (TP)/[TP + false negative (FN)]} × 100%, where TP refers to cases where the test correctly identifies the presence of the disease, and FN refers to cases where the test incorrectly identifies the absence of the disease when it is actually present; specificity = [true negative (TN)/{[false positive (FP) + TN]} × 100%, where TN refers to cases where the test correctly identifies the absence of the disease, and FP refers to cases where the test incorrectly identifies the presence of the disease when it is actually absent; positive predicted value (PPV) = [TP/(TP + FP)] × 100%; negative predicted value = [TN/(TN + FN)] × 100%; and diagnostic accuracy (DA) = [(TP + TN)/(TP + TN + FP + FN)] × 100%. The consistency was tested using the kappa method: 0.01-0.40 was considered poor consistency, 0.40-0.75 was considered moderate consistency, and 0.75-1.00 was considered good consistency. P < 0.05 (bilateral test) indicated that the difference was statistically significant.

RESULTS

Clinical characteristics of the patients

A total of 1756 patients with suspected gastric tumors received surgical treatment at Sichuan Provincial People's Hospital from July 2018 to July 2022, of which 1387 patients were pathologically diagnosed with malignant gastric tumors and 369 with benign tumors. All patients were confirmed pathologically after surgical resection. Therefore, based on the exclusion criteria, there were: (1) 0 cases of GC confirmed by gastroscopic biopsy but not by surgery; (2) 89 cases of GC suspected by gastroscopic biopsy but not confirmed by postoperative pathology; (3) 256 cases with poor image quality of the OCEUS affecting the staging; and (4) 222 cases of GC receiving radiotherapy, chemotherapy, endoscopic partial resection, or other treatments before surgery. A total of 1387 cases of GC were confirmed via gastroscopy and surgery, and lesions were identified via ultrasound. A total of 318 cases of GC were not accurately diagnosed by ultrasound, including 186 cases (186/256) with poor image quality and 132 cases (132/909) with good image quality.

After all inappropriate cases were excluded, a total of 909 patients who met the above conditions were included in the study, including 636 males and 273 females aged 22 to 90 years (62.40 ± 11.14). Depending on the site and extent of the lesions, the cases were categorized mainly as gastric antrum cancer (226 cases, 24.8%) or multiple GC (347 cases, 38.1%). OCEUS revealed that the thickness diameter (depth of infiltration) of the gastric mass was 14.24 ± 6.45 mm, and the maximum upper and lower diameters were 50.49 ± 22.45 mm. All patients underwent OCEUS examination within one week before surgery. The clinical parameters of the patients with GC included in this study are shown in Table 2.

Table 2 Clinical parameters of gastric cancer patients, n (%).

Clinical parameters	Number of cases
Sex: Male/female	636 (69.9)/273 (30.1)
Age (year)	62.40 ± 11.14
Ultrasound shows the thickness diameter of gastric mass (mm, mean ± SD)	14.24 ± 6.45
Ultrasound shows the maximum upper and lower diameter of gastric mass (mm, mean ± SD)	50.49 ± 22.45
Anatomical location of gastric masses
Cardia & esophagogastric junction	46 (5.0)
Stomach fundus	42 (4.6)
Stomach body	93 (10.2)
Gastric antral	226 (24.8)
Pyloric canal	18 (1.9)
Greater curvature of stomach	51 (5.6)
Lesser curvature of stomach	86 (9.4)
Partial overlapping lesions of stomach	347 (38.1)

Results of OCEUS-based diagnosis in preoperative T-staging of GC

All patients were categorized with postoperative pT as the "golden standard". The pT-staging of GC included 32 cases of T1a, 57 cases of T1b, 94 cases of T2, 204 cases of T3, 416 cases of T4a, and 106 cases of T4b. Pathological T-staging confirmed that 79.8% (726/909) of the patients included in this study had T3, T4a, or T4b disease. According to the ultrasonic T-staging criteria, the T-staging results with OCEUS were as follows: 30 cases of T1a, 33 cases of T1b, 94 cases of T2, 296 cases of T3, 367 cases of T4a and 89 cases of T4b. The DA of OCEUS was 76.6% for T1a, 69.6% for T1b, 62.7% for T2, 60.8% for T3, 88.0% for T4a, 88.7% for T4b, and 75.5% overall. These findings indicated that most patients with advanced GC were included in this study and that OCEUS demonstrated high DA for the preoperative T staging of GC. The specific results are shown in Table 3, and a typical case chart of the OCEUS is shown in Figures 1 and 2.

Figure 1 Oral contrast-enhanced ultrasound pattern chart of layers of the gastric wall. A: Gastric cancer T staging pattern chart; B: Oral contrast-enhanced ultrasound pattern chart; C: Gastric oral contrast-enhanced ultrasound (OCEUS) high-frequency ultrasound pattern chart; D: Gastric OCEUS low-frequency ultrasound pattern chart. OCEUS reveals three high and two low five-layer structures of the gastric wall. L1: Mucosal epithelium and gastric cavity interface echo layer (high echo); L2: Deep mucosa (low echo); L3: Submucosa (high echo); L4: Muscularis propria (low echo); L5: Serosa (high echo); STO: Stomach cavity (equal echo).

Figure 2 Case demonstration of each oral contrast-enhanced ultrasound T-stage. A: Ultrasound T1a-stage; B: Ultrasound T1b-stage; C: Ultrasound T2-stage; D: Ultrasound T3-stage; E: Ultrasound T4a-stage; F: Ultrasound T4b-stage. L2: Deep mucosa; L3: Submucosa; L4: Muscularis propria; L5: Serosa; STO: Stomach cavity.

Table 3 Comparison of oral contrast-enhanced ultrasound T-stages and pathological T-stages.

OCEUS T-stage	No. of cases	Pathological T-stage						Correct diagnosis rate (%)
		T1a	T1b	T2	T3	T4a	T4b
T1a	30	23	7	0	0	0	0	76.66
T1b	33	4	23	6	0	0	0	69.69
T2	94	5	19	59	8	3	0	62.76
T3	296	0	7	22	180	82	5	60.81
T4a	367	0	1	7	14	323	22	88.01
T4b	89	0	0	0	2	8	79	88.76
Summation	909	32	57	94	204	416	106	75.57

OCEUS: Oral contrast-enhanced ultrasound.

Diagnostic efficacy analysis of the OCEUS T-staging results

The sensitivity of all ultrasound T-staging was greater than 62%, with the exception of the T1b stage (the sensitivity evaluation was 40.3%). The specificity of all ultrasound T-staging was greater than 91%, with the exception of the T3 stage (the specificity evaluation was 83.5%). The Youden index exceeded 50%, except for T1b, indicating that the OCEUS method was reasonably effective in identifying real patients.

The consistency rate of ultrasound T-staging was greater than 80%, although the consistency between ultrasound cT-staging and pathological pT-staging of T4b tumors was good (kappa value > 0.75). Other ultrasound T-staging and pathological pT-staging methods were moderately consistent (kappa value between 0.4 and 0.75), and the total kappa value was 0.66, indicating that OCEUS demonstrated good reliability in the preoperative T-staging of GC.

The PPV of ultrasound T-staging was also good, with the highest T4b of 88.7%, and the negative predictive value was generally high, with the lowest T4a of 82.8%, indicating that OCEUS had good benefits in the preoperative T-staging of GC, especially for T4 GC. The specific results are shown in Table 4.

Table 4 The diagnostic value of oral contrast-enhanced ultrasound T-staging compared with pathological T-staging of gastric cancer (%).

OCEUS T-stage	Validity			Reliability		Revenue
	Sensitivity	Specificity	Youden index	Coincidence rate	Kappa value	Positive predictive value	Negative predictive value
T1a	71.87	99.2	71.07	98.23	0.73	76.66	98.97
T1b	40.35	98.82	39.17	95.15	0.49	69.69	96.11
T2	62.76	95.71	58.47	92.29	0.58	62.76	95.71
T3	88.23	83.54	71.77	84.59	0.62	60.81	96.08
T4a	77.64	91.07	68.71	84.92	0.69	88.01	82.84
T4b	74.52	98.75	73.27	95.92	0.79	88.76	96.71

OCEUS: Oral contrast-enhanced ultrasound.

DISCUSSION

Accurate preoperative clinical staging of GC is of paramount importance in guiding treatment decisions and predicting patient outcomes. Commonly utilized imaging modalities for clinical staging include CT, MRI, and EUS. Notably, MRI has demonstrated the highest accuracy, approximately 82.9%, in T-staging, outperforming CT at 71.5% and EUS at approximately 75%[6,13]. A multicenter retrospective study conducted in the United States revealed that the clinical T-staging accuracy was only 46.2%, emphasizing the need to combine multiple imaging methods to achieve accurate preoperative staging[14].

OCEUS has become increasingly feasible in clinical practice owing to advancements in gastric window ultrasound contrast agents and improved ultrasound imaging equipment. Its clinical significance has been recognized, positioning OCEUS as a noninvasive, safe, and efficient imaging technique. The Guidelines for the Diagnosis and Treatment of GC 2022 Edition issued by the National Health Commission of the People's Republic of China clearly emphasize OCEUS as a valuable supplement to gastroscopy and other imaging examinations, expanding its application scope. OCEUS particularly benefits pediatric and elderly patients who are intolerant to gastroscopy, those with large esophageal obstructions, radiation-sensitive individuals, and patients with mobility challenges. Importantly, gastrointestinal oral ultrasound contrast agents, which are primarily composed of edible materials, have been shown to be safe and are approved for use in China. In this study, we observed that uniform filling of the gastric cavity with an echo contrast agent created a distinct echo area within the gastric cavity, facilitating a clear view of the five-layer structure of the gastric wall[11,15]. This view enabled precise assessment of tumor infiltration depth, surrounding organ invasion, and lymph node metastasis. OCEUS overcomes the common limitations of other imaging techniques, including reduced echogenicity and thickening of the gastric wall, indistinct display of the five-layer structure of the gastric wall, mucosal interruptions, ulcers, and mass formations.

OCEUS has proven valuable in determining the size, location, and depth of mass infiltration, thereby assisting in surgical planning and therapeutic decision-making. This study focused primarily on T-staging, given its pivotal role in treatment modality selection. The criteria for ultrasound T-staging rely on the depth of tumor infiltration into the gastric wall and the presence of serosal invasion or involvement of surrounding organs. Ultrasound demonstrated satisfactory accuracy, exceeding 60%, with an impressive 88.7% accuracy for T4b staging, culminating in an overall accuracy of 75.5%. The moderate consistency, as indicated by a kappa value of 0.66 compared with pathological T-staging, highlights its reliability. Notably, ultrasound T-staging exhibited adequate sensitivity and specificity for evaluating T1a, T3, T4a, and T4b tumors, surpassing 71%, with Youden index values exceeding 0.68. PPVs also yielded satisfactory results, consistently exceeding 60%, albeit slightly lower than those reported in a prior 40-case single-center study in China[16]. These findings reinforce ultrasound T-staging as a valuable tool for the preoperative T-staging of GC.

In the context of ultrasonic T1a/T1b staging, the accuracy was not excellent. This limitation may be attributed to various factors, including the frequency and image quality of extracorporeal ultrasound, the size of the T1 lesions, and the inherent difficulty of imaging lesions located centrally or visualizing intraluminal lesions from an external perspective. Achieving high accuracy in the visualization of early GC infiltration depth remains a challenge. In contrast, the accuracy of T4a and T4b staging was excellent. This impressive accuracy is particularly important, as serosal invasion diagnosis remains challenging, especially with EUS, thus accentuating the contribution of OCEUS in advanced GC T-staging[17,18].

While ultrasound T2/T3 staging exhibited acceptable consistency with the pathological T-stage (kappa > 0.58), it demonstrated lower accuracy levels of 62.7% and 60.8%, along with corresponding PPVs. The challenges in this context stem from the hyperechoic nature of both subserosal connective tissue and the serosa in ultrasonic images. Distinguishing between these layers and accurately assessing infiltration depth when tumors reach the deep muscularis propria of the gastric wall present difficulties. Pathologists also face subjectivity in determining tumor proximity or penetration of the serosal layer[19], contributing to the potential between ultrasound and pathological T-staging. Additionally, GC-related inflammatory reactions in the serosal surface and perigastric area can obscure the visual clarity of the serosal layer, potentially leading to overstaging of T3 tumors[20]. Ultrasonic T4a/T4b staging for pathologically advanced GC, in contrast, yields clear and typical signs under OCEUS and pathological examination. With a substantial number of cases (522/909), this study achieved the highest DA and PPV, exceeding 88.0%. These findings underscore the suitability of ultrasonic T-staging for clinically evaluating advanced GC.

Compared with other traditional diagnostic methods for T-staging, OCEUS studies are limited in number, but the larger sample size examined in this study bolsters confidence in the results[8]. Clinically, EUS and CT remain the primary choices for the preoperative T-staging of GC, followed by MRI. Gastric contrast-enhanced ultrasound is less frequently utilized.EUS, with its combined ultrasound and endoscopy functions, has an accuracy of 75.0% for the T-staging of GC[13]. However, the invasiveness of EUS limits its utility in patients with endoscopic contraindications and those who are averse to invasive procedures. CT, especially multidetector CT, has significantly improved the accuracy of GC T-staging, achieving rates exceeding 90.0%[21,22]. Its superiority lies in detecting T4 tumors and distant metastases[23]. In recent years, MRI has also demonstrated value in the preoperative T-staging of GC, with sensitivity and specificity rates of 76% and 89%, respectively[24]. These modalities have enriched clinical evaluation and treatment approaches for GC. Moreover, in China, gastric double contrast-enhanced ultrasonography has been explored and has shown DA rates reaching 82.3% for T staging[12]. Recent meta-analyses have indicated that OCEUS excels in T1-T2 staging but has slightly reduced accuracy for T3-T4 stages, with an overall sensitivity and specificity of 94% and 91%, respectively[8,25]. In addition, five studies involving 536 patients were included in the OCEUS analysis[26], which yielded a combined sensitivity of 0.733, a combined specificity of 0.982 and an area under the curve of 0.93. These findings suggest that OCEUS can serve as a feasible supplementary tool for the clinical T-staging of GC.

In summary, multiple imaging techniques complement each other in assessing the depth of tumor invasion (T-staging) in GC, and OCEUS presents distinct clinical value in this regard. The European Federation of Societies for Ultrasound in Medicine and Biology and the Japan Society for Ultrasound in Medicine have both highlighted the utility of OCEUS in diagnosing and monitoring a spectrum of gastrointestinal diseases[27,28]. Their guidelines and consensus emphasize the practicality of OCEUS for conditions such as GC, gastric ulcers, gastrointestinal stromal tumors, and inflammatory bowel diseases. Additionally, physicians who lack experience in gastrointestinal ultrasound may benefit from standardized scanning, which could help reduce the incidence of missed diagnoses and improve the detection of lesions, thereby allowing more accurate assessments of the preoperative T staging of GC and greatly enhancing the clinical application value of OCEUS.

However, it is essential to acknowledge the limitations of OCEUS. First, the impact of physician expertise on diagnostic outcomes is a potential source of variability. OCEUS is strongly dependent on the operator, necessitating that the physician responsible for performing gastric filling ultrasound possesses a minimum of five years of experience in abdominal ultrasound. Furthermore, the physician is required to undergo a rigorous six-month standardized training program in OCEUS to ensure diagnostic consistency. Without meeting these criteria, inexperienced physicians may encounter difficulties in accurately assessing the preoperative T staging of GC. Second, our study focused primarily on patients with advanced GC cases, limiting the ability of OCEUS to assess early-stage tumors. Additionally, the exclusion of the preoperative N-staging evaluation is another limitation worth noting. Finally, the patient's own condition may also affect the judgment of the sonographer, such as abdominal flatulence, obesity, and the degree of cooperation of patients during the examination.

CONCLUSION

In summary, OCEUS has advantages in evaluating the preoperative T-staging of GC, with high DA. Additionally, the noninvasive nature, real-time dynamicity, repeatability, and ease of application of OCEUS improve its clinical application to clearly display lesions in the gastric cavity, gastric wall and perigastric area and observe the depth of GC infiltration into the gastric wall. This technique has high clinical practical value and merits clinical popularization.

ACKNOWLEDGEMENTS

We express our sincere gratitude to the experts from the Gastrointestinal Subspecialty Group of the Department of Ultrasound Medicine at Sichuan Provincial People's Hospital, as well as the valuable contributions from our pathology colleagues. Furthermore, we are thankful for the profound feedback from our colleagues and the editorial team, which played a significant role in enhancing this study.