Diagnostic value of mini-probe endoscopic ultrasound in preoperative tumor nodal (TN) staging of gastric cancer and analysis of factors influencing T-staging accuracy

Introduction

Gastric cancer ranks as the fifth most prevalent malignant neoplasm and the fourth leading cause of cancer-related mortality globally (1). In China, the 5-year relative survival rate for gastric cancer is approximately 27.4% (2). Surgical intervention remains the primary intervention in clinical practice. Accurate preoperative staging, appropriate selection of surgical techniques, individualized chemotherapy regimens, and prognostic assessment are key considerations in surgical management.

Endoscopic ultrasonography (EUS) enables visualization of abnormalities in the structural layers of the gastric wall and has been widely applied in the preoperative staging of gastric cancer, particularly in early-stage disease. While conventional radial or linear EUS is valuable for broader anatomical assessment and staging of advanced tumors, mini-probe EUS offers distinct advantages for evaluating early gastric cancer and precisely delineating the depth of superficial invasion (3). The mini-probe’s frequency (typically 12 or 20 MHz) provides superior resolution of the gastric wall layers, allowing more detailed visualization of mucosal and submucosal structures (4). Additionally, its smaller size and flexibility enable better positioning and contact with lesions, particularly in difficult anatomical locations such as the gastric cardia and angular incisura, where conventional EUS probes may have limited maneuverability. These characteristics make mini-probe EUS particularly suitable for T-staging of early gastric cancers and for guiding decisions regarding endoscopic resection (5,6). The development of mini-probe EUS offers several advantages such as enhanced image resolution, ease of maneuverability, and precise delineation of the digestive tract wall. It facilitates assessment of adjacent organ involvement and provides high accuracy in determining the depth of tumor infiltration. Mini-probe EUS therefore holds considerable clinical value in preoperative evaluation and serves as an effective modality for determining the T stage of gastric tumors.

Despite these benefits, the diagnostic accuracy and clinical applicability of mini-probe EUS in gastric cancer staging, along with the factors influencing its precision, remain incompletely understood. Therefore, the present study aimed to evaluate the clinical value of mini-probe EUS in the preoperative tumor nodal (TN) staging of gastric cancer and to analyze factors associated with T-staging accuracy. We present this article in accordance with the STARD reporting checklist (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-1-993/rc).

Methods

Clinical information

A total of 85 patients diagnosed with gastric cancer (55 males and 30 females; male-to-female ratio: 1.83:1) who were treated at Beijing Huaxin Hospital between January 2018 and June 2025 were included in the study. The patients’ ages ranged from 30 to 83 years [mean ± standard deviation (SD): 65.45±9.86 years; median age: 63 years]. Preoperative staging was performed, and the results were compared with postoperative pathological findings.

Preoperative histopathological diagnoses included 12 cases of high-grade intraepithelial neoplasia, 4 cases of high-grade intraepithelial neoplasia with localized carcinoma, 16 cases of carcinoma, and 53 cases of advanced gastric cancer. All patients underwent preoperative imaging (computed tomography or positron emission tomography-computed tomography) to rule out distant metastasis (M0). Of these, 28 patients underwent endoscopic mucosal resection (EMR) or endoscopic submucosal dissection (ESD), while 57 patients received surgical treatment. Tumor locations were distributed as follows: gastric antrum and angle (48 cases), gastric corpus (21 cases), and gastric fundus and cardia (16 cases). Tumor diameters ranged from 0.6 to 4.0 cm, with an average of 2.43±0.75 cm. Histologically, 69 tumors were differentiated, and 16 were undifferentiated. Ulceration was present in 27 cases and absent in 58 cases.

With respect to tumor infiltration depth, 9 tumors involved the submucosal layer, 21 were intramucosal, 27 involved the muscularis propria, 18 extended to the serosal layer, and 10 breached the serosal layer. All patients underwent standard gastroscopy followed by mini-probe EUS within two weeks prior to surgery to determine the depth of tumor invasion. The EUS findings were compared with pathological results obtained from endoscopic or surgical specimens. All preoperative mini-probe EUS examinations were conducted before any oncologic treatment was administered.

This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Beijing Huaxin Hospital (The First Hospital of Tsinghua University) (No. 2023-29). Written informed consent was obtained from all participants prior to enrollment.

Instruments and examination procedure

All patients fasted for 8 to 10 hours before undergoing the mini-probe EUS. The endoscopic examination was performed using an Olympus GIF-H260 electronic gastroscope paired with an EVIS-260 system platform. The procedure was conducted using an Olympus EU-ME1 ultrasound processor (Olympus, Japan) equipped with a UM-3R ultrasound probe operating at a frequency range of 12 or 20 MHz.

During the examination, 200 to 400 mL of non-aerated water was introduced into the gastric cavity. The mini-probe ultrasound transducer was then inserted through the biopsy channel under direct endoscopic visualization to the target lesion. Evaluated parameters included lesion location, morphology, size, shape, and depth of local infiltration. All procedures were performed by a team of experienced endoscopic ultrasonographers. Postoperative pathological findings served as the reference standard for diagnostic accuracy. Based on the concordance between EUS and pathological staging, patients were categorized into “accurate” and “inaccurate” groups. Clinical characteristics, including tumor diameter, histological differentiation, anatomical site, depth of invasion, gross stage, and presence of regional lymph node metastasis, were analyzed to identify factors influencing EUS diagnostic accuracy.

Evaluation criteria for EUS

Tumor staging via EUS followed the tumor, node, metastasis (TNM) classification system outlined in the eighth edition of the American Joint Committee on Cancer (AJCC) guidelines. The criteria for assessing the depth of tumor invasion were as follows (7):

• uT1 stage (including uT1M and uT1SM): uT1M characterized by thickening of the first and second echogenic layers, with an irregular but structurally intact third layer; uT1SM demonstrated blurring, thickening, thinning, or partial loss of the first through third layers.
• uT2 stage (invasion of the muscularis propria): characterized by loss of the first to third echogenic layers, with the presence of an irregular, hypoechoic mass originating from the fourth layer, protruding towards the gastric lumen.
• uT3 stage (invasion into the subserosa): defined by irregularity and disruption of the fifth echogenic layer, poorly defined echogenic stratification, loss of normal gastric wall architecture, and indistinct boundaries with surrounding tissues.
• uT4 stage (invasion into adjacent organs): indicated by disruption of the hyperechoic zone of the fifth layer, tumor extension into peripheral tissues, and evidence of infiltration of adjacent organs.

Lymph nodes with a diameter less than 3 mm were not visualized on ultrasonography and considered normal. Lymph node metastasis was diagnosed based on the following criteria: (I) lymph node diameter >5 mm and (II) hypoechoic or heterogeneous echotexture comparable to that of the primary tumor. Lymph node staging was classified as N0 (no evidence of metastasis) or N1 (presence of metastatic lymph nodes).

Pathological evaluation

Post-gastroscopy tissue specimens were stained at the margins and base, sectioned at 2 to 3 mm intervals, and embedded for histopathological analysis. Cancer staging was conducted based on the criteria outlined in the 2016 Union for International Cancer Control (UICC) and AJCC cTNM classification system (8).

Statistical analysis

The primary focus of this study was the assessment of local tumor invasion (T stage) and regional lymph node involvement (N stage). As all patients were M0, the analysis pertained to TN staging. The diagnostic accuracy, sensitivity, and specificity of mini-probe EUS for determining gastric cancer staging were calculated by comparing preoperative EUS-based findings with postoperative histopathological results. Statistical analyses were performed using SPSS version 20.0 software (IBM Corp., Armonk, NY, USA). Categorical data were expressed as percentages (%), and intergroup comparisons were performed using the chi-squared (χ²) test. A P value of <0.05 was considered statistically significant.

Results

Comparison of preoperative and postoperative pathological T-staging using mini-probe EUS

A comparison of T-staging results obtained via preoperative mini-probe EUS and postoperative pathological examination is presented in Table 1 and Figures 1-4. The findings indicated a high level of concordance between the two methods (P<0.01), demonstrating the strong diagnostic reliability of mini-probe EUS in evaluating tumor invasion depth in gastric cancer.

Figure 1 Diagnosis of uT1 gastric cancer using mini-probe EUS. (A) Endoscopic appearance of early gastric cancer. (B) Mini-probe EUS image showing characteristics indicative of uT1 gastric cancer. (C) Histopathological examination (HE staining) at magnification ×100, confirming the diagnosis. (D) Higher magnification of the same specimen at ×200, illustrating detailed morphological features consistent with T1 gastric cancer. This figure highlights the concordance between mini-probe EUS findings and the corresponding pathological results. The diagnostic accuracy of mini-probe EUS for T1 gastric cancer is 93.33%, highlighting its reliability in correlating with pathological findings. EUS, endoscopic ultrasonography; HE, hematoxylin and eosin; uT1, invasion of the mucosal layer and submucosa.

Figure 2 Diagnosis of uT2 gastric cancer using mini-probe EUS. (A) Endoscopic appearance of early gastric cancer. (B) Mini-probe EUS image demonstrating features characteristic of uT2 gastric cancer. (C) Histopathological examination (HE staining) at magnification ×100, confirming the diagnosis. (D) Higher magnification of the same specimen at ×200, revealing detailed morphological characteristics consistent with T2 gastric cancer. This figure illustrates the concordance between mini-probe EUS findings and the corresponding pathological results. The diagnostic accuracy of mini-probe EUS for T2 gastric cancer is 89.29%, highlighting its reliability in correlating with pathological findings. EUS, endoscopic ultrasonography; HE, hematoxylin and eosin; uT2, muscularis propria.

Figure 3 Diagnosis of uT3 gastric cancer using mini-probe EUS. (A) Endoscopic appearance of early gastric cancer. (B) Mini-probe EUS image revealing characteristics indicative of uT3 gastric cancer. (C) Histopathological examination (HE staining) at magnification ×100, confirming the diagnosis. (D) Higher magnification of the same specimen at ×200, illustrating detailed morphological features consistent with T3 gastric cancer. This figure emphasizes the concordance between mini-probe EUS findings and the corresponding pathological results. The diagnostic accuracy of mini-probe EUS for T3 gastric cancer is 78.95%, highlighting its reliability in correlating with pathological findings. EUS, endoscopic ultrasonography; HE, hematoxylin and eosin; uT3, serosal layer.

Figure 4 Diagnosis of uT4 gastric cancer using mini-probe EUS. (A) Endoscopic appearance of early gastric cancer. (B) Mini-probe EUS image demonstrating features characteristic of uT4 gastric cancer. (C) Histopathological examination (HE staining) at magnification ×100, confirming the diagnosis. (D) Higher magnification of the same specimen at ×200, revealing detailed morphological characteristics consistent with T4 gastric cancer. This figure illustrates the concordance between mini-probe EUS findings and the corresponding pathological results. The diagnostic accuracy of mini-probe EUS for T4 gastric cancer is 87.50%, highlighting its reliability in correlating with pathological findings. EUS, endoscopic ultrasonography; HE, hematoxylin and eosin; uT4, breaks through the serosal layer and invades adjacent organs.

Evaluation of lymph node metastasis: preoperative mini-probe EUS vs. postoperative pathology

The diagnostic accuracy, sensitivity, and specificity of mini-probe EUS for N-staging are presented in Table 2. The overall accuracy of mini-probe EUS in detecting lymph node metastasis was 76.4% (13/17), with a sensitivity of 76.47% (13/17) and specificity of 85.29% (58/68), indicating satisfactory performance of mini-probe EUS for preoperative assessment of lymph node involvement in gastric cancer.

Clinicopathologic factors influencing T-staging accuracy of mini-probe EUS

Analysis of clinicopathologic factors demonstrated no statistically significant difference in T-staging accuracy between patients with and without lymph node metastasis (P>0.05). However, statistically significant differences were observed when comparing staging accuracy across groups with different lesion locations, lesion diameters, histological differentiation, and the presence or absence of ulceration (P<0.05; Table 3). These findings indicate that lesion characteristics and histopathological features influence the precision of mini-probe EUS-based T-staging.

Discussion

The present study evaluated the clinical utility of mini-probe EUS in the preoperative staging of gastric cancer. The prognosis of gastric cancer is closely linked to tumor stage and the treatment modality; therefore, accurate staging is essential for optimal disease management. Findings from this study indicate that mini-probe EUS offers high diagnostic accuracy in assessing the depth of tumor invasion, making it particularly valuable in early-stage gastric cancer. This capability facilitates the identification of candidates suitable for EMR or ESD, both of which may enhance the likelihood of curative outcomes. The observed high concordance between mini-probe EUS-based preoperative T-staging and postoperative pathological staging further supports its diagnostic value in clinical practice.

According to the cTNM classification system, reported 5-year postoperative survival rates vary markedly by stage, ranging from 91.2% in stage I, 75.1% in stage IIA, 57.7% in stage IIB, 43.2% in stage III, 31.6% in stage IVA, and 7.7% in stage IVB (9). While surgical resection remains the most effective curative approach, endoscopic resection is increasingly favored for early gastric cancer without evidence of lymph node metastasis, particularly for differentiated intramucosal carcinoma (cT1a) without ulceration (10). In contrast, patients with stage IIIB or IV progressive gastric cancer, often require neoadjuvant chemotherapy prior to surgical intervention (11-13). Thus, accurate preoperative staging is critical for guiding individualized treatment strategies, particularly in the context of emerging minimally invasive techniques and neoadjuvant therapies.

Although multiple diagnostic techniques, such as magnifying endoscopy, chromoendoscopy, and narrow-band imaging, are effective in identifying early gastric cancer and delineating tumor margins, they offer limited accuracy in determining the depth of invasion (14-16). In contrast, mini-probe EUS enables detailed visualization of the gastrointestinal wall, facilitates evaluation of adjacent organ involvement, and provides detailed evaluation of tumor infiltration depth. Previous studies have reported high diagnostic accuracy of mini-probe EUS in in preoperative staging of gastric cancer, particularly with respect to T-staging (8,17-19). However, some reports have noted limitations in its accuracy in early-stage gastric cancer, indicating that mini-probe EUS should be used in conjunction with other diagnostic modalities to improve staging reliability (20-22).

In the present study, the overall accuracy of mini-probe EUS for T-staging was approximately 90%, with about 3.5% of cases over-staged and 7% under-staged. The accuracy was higher for early-stage gastric cancer compared to advanced lesions, consistent with findings from previous studies (23). The use of low-frequency probes enhanced tissue penetration, thereby improving diagnostic precision in cases of progressive gastric cancer.

In this study, factors potentially influencing the diagnostic accuracy of mini-probe EUS in the preoperative TN staging of gastric cancer were examined. Both endoscopic appearance and histopathological features of the lesion were found to play critical roles in influencing staging precision. Variables such as tumor location, lesion size, presence of ulceration, and histological differentiation were identified as important factors influencing diagnostic performance. Univariate analysis indicated that tumors with a diameter ≥2 cm, lesions located in the gastric fundus or near the cardia, tumors associated with ulcers, and undifferentiated carcinoma were associated with decreased T-staging accuracy.

The diagnostic precision of mini-probe EUS for tumors in the gastric antrum and body was significantly higher than for those in the fundus or cardia. This difference likely results from challenges maintaining alignment of the ultrasound probe with lesions in the upper stomach. Furthermore, the submucosal layer in the upper third of the stomach is relatively thin and rich in fibrous tissue and vasculature, complicating differentiation of tumor invasion at this level. The posterior wall of the gastric fundus lacks a complete serosal covering, resulting in imaging overlap between the subserosal and serosal layers. On mini-probe EUS, this overlap may appear as a single hypoechoic band, making it challenging to distinguish between T2 and T3 staging and increasing the likelihood of over-staging.

In the present analysis, the diagnostic accuracy of mini-probe EUS was approximately 85% for lesions larger than 2 cm, which was lower than the nearly 98% accuracy observed for lesions ≤2 cm. These findings are consistent with those reported by Li et al. (20) and Pei et al. (21). The reduced accuracy observed in larger lesions may be attributed to the limited acoustic field of high-frequency mini-probes, which are optimized for imaging smaller fields and may fail to capture focal submucosal invasion in larger lesions, resulting in under-staging (24-26). In addition, larger lesions are more likely to induce mesenchymal reactions, such as hyperplasia and fibrosis, during tumor progression. These reactive changes, along with chronic peritumoral inflammation, may mimic tumor infiltration, thereby leading to over-staging.

The presence of ulceration was also identified as a factor reducing the diagnostic accuracy of mini-probe EUS in assessing tumor invasion depth, consistent with previous studies (13,24,26,27). Inflammation and fibrosis associated with ulceration, particularly at the ulcer base, may obscure the true extent of tumor infiltration and impair interpretation, thereby decreasing diagnostic precision (18,26,28,29). To improve the accuracy of assessing infiltration depth, high-frequency probes (providing high local resolution but limited penetration) were used for early gastric cancer, whereas low-frequency probes (12 MHz) were employed for advanced disease to enhance tissue penetration. Alternating frequencies either 12 or 20 MHz, depending on lesion characteristics, improved the reliability of T-staging across the spectrum of disease severity. Mini-probe EUS, therefore, provides a highly effective approach for distinguishing early from advanced gastric cancer and supports appropriate treatment selection, such as EMR or ESD, potentially improving curative outcomes.

Evaluation of lymph node metastasis (N-staging) using mini-probe EUS represents another important aspect of this study. Normal lymph nodes are typically smaller than 3 mm in diameter and exhibit echogenicity similar to surrounding adipose or fibrous tissue, rendering them difficult to detect with sonography. In contrast, metastatic or inflammatory lymph nodes often appear hypoechoic, with echogenicity similar to that of the primary tumor, which can lead to diagnostic ambiguity. Previous reports have indicated that lymph node size, border regularity, and echogenicity serve as useful indicators for identifying metastatic involvement (23,25). Metastatic nodes typically exhibit loss of normal architecture, a round shape, and proximity to the primary lesion. Approximately 50% to 70% of lymph nodes measuring more than 5 mm in diameter detected by mini-probe EUS are metastatic, whereas fewer than 20% of nodes smaller than 4 mm demonstrate malignant features. Importantly, nearly 20% of metastatic nodes measure less than 3 mm in diameter, thereby limiting the sensitivity of mini-probe EUS for their detection (30,31). Additionally, metastatic nodes located at a distance from the primary tumor may not be visualized due to restricted probe penetration, further reducing diagnostic accuracy.

In the current study, mini-probe EUS achieved an N-staging accuracy of approximately 75% with overstaging observed in 10% and understaging in 6%. The use of a low-frequency probe (12 MHz) enhanced visualization of peritumoral lymph node metastasis. However, small or minimally infiltrated lymph nodes often exhibit minimal structural changes, limiting their detectability with low-frequency imaging. Furthermore, due to variations in nodal shape and echogenicity, differentiating metastatic from non-metastatic nodes remains a challenge for mini-probe EUS (30,32,33).

Several limitations of this study should be acknowledged. First, the relatively small sample size and limited number of cases within subgroups precluded the use of multivariate statistical analysis. Second, variability in operator expertise may have influenced the diagnostic accuracy, particularly in the detection of lymph node metastases. Third, the limitation in tissue penetration associated with mini-probe EUS restricted its ability to identify distant lymph nodes. Moreover, the absence of significant structural alterations in micro-infiltrated lymph nodes and the challenge of distinguishing inflammatory responses from metastatic involvement contributed to false-positive and false-negative outcomes (34,35).

To enhance the reliability and generalizability of results, future studies should include larger sample sizes and greater representation of tumors involving the submucosal and subserosal layers. Improved differentiation between superficial and deep submucosal invasion, as well as identification of subserosal penetration, would further enhance the diagnostic accuracy and clinical value of mini-probe EUS in the preoperative staging of gastric cancer.

Conclusions

In summary, mini-probe EUS demonstrated superior diagnostic accuracy in the preoperative T-staging of gastric cancer, with superior performance compared to the N-staging. It showed strong reliability in assessing the depth of tumor infiltration, reinforcing its value in guiding appropriate treatment strategies. Accurate T-staging assists in identifying patients with stage I gastric cancer who may be suitable candidates for EMR or ESD, thereby improving the likelihood of curative resection. However, decreased staging accuracy was observed in lesions located in the gastric fundus or cardia, those measuring ≥2 cm in diameter, and those associated with ulceration. These findings highlight the importance of considering lesion characteristics comprehensively when interpreting EUS results. Given that T-staging relies on precise evaluation of invasion depth, the integration of mini-probe EUS with other complementary imaging or diagnostic techniques may enhance staging accuracy and contribute to the formulation of optimal individualized treatment plans for patients with gastric cancer.

Acknowledgments

We would like to acknowledge the hard and dedicated work of all the staff who implemented the intervention and evaluation components of the study.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-1-993/rc

Data Sharing Statement: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-1-993/dss

Peer Review File: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-1-993/prf

Funding: This study was supported by the Beijing Chaoyang District Science and Technology Commission Fund Project (No. CYSF1823).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-1-993/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Beijing Huaxin Hospital (The First Hospital of Tsinghua University) (No. 2023-29). Written informed consent was obtained from all participants prior to enrollment.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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