Laparoscopic ultrasound versus intraoperative gastroscopy for tumor localization in laparoscopic gastrectomy: a comparative cohort study

Abstract

Background

Precise tumor localization remains a technical challenge in laparoscopic gastrectomy. This study aimed to evaluate the efficacy and safety of laparoscopic ultrasound (LUS) as an alternative to conventional intraoperative gastroscopy (IOG) for tumor localization during laparoscopic radical gastrectomy.

Methods

We conducted a retrospective analysis of 58 patients who underwent laparoscopic radical gastrectomy between February 2023 and December 2024. Patients were categorized into LUS-guided (n = 22) and conventional IOG-guided (n = 36) localization groups. Intraoperative parameters (localization success, procedural times, blood loss), postoperative recovery metrics, complications, pathological outcomes, and short-term oncological results were compared between the two groups. Continuous variables were expressed as mean ± standard deviation or median with interquartile range and compared using Student’s t-test or Mann-Whitney U test. Categorical variables were presented as frequencies (%) and compared using χ² test or Fisher’s exact test. Statistical significance was set at p < 0.05.

Results

LUS demonstrated comparable localization success rates (95.5% vs. 100%, p = 0.379) with significantly shorter mean localization time (3.83 ± 0.26 vs. 4.06 ± 0.16 min, p = 0.001) and reduced total operative time (218.68 ± 28.48 vs. 240.69 ± 26.71 min, p = 0.004). Both groups showed equivalent safety profiles with no significant differences in complication rates (27.2% vs. 30.6%, p = 1.000). Pathological outcomes were excellent in both groups, with 100% R0 resection rates and comparable lymph node yields (32.5 vs. 38.0, p = 0.320). Short-term recurrence rates were equivalent (4.5% vs. 5.6%, p = 1.000) after a mean follow-up of 12 months.

Conclusion

LUS-guided tumor localization represents an efficient and effective alternative to IOG, significantly reducing operative time while maintaining equivalent safety and oncological outcomes. This surgeon-controlled technique integrates seamlessly into the laparoscopic workflow and offers a practical solution for intraoperative tumor localization in minimally invasive gastric surgery.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12893-025-03426-2.

Introduction

Gastric cancer remains a significant global health burden, ranking as the fifth most common malignancy and the third leading cause of cancer-related mortality worldwide. Recent estimates indicate approximately 970,000 new cases and 660,000 deaths annually as of 2022 [1]. Nations with advanced healthcare infrastructure have observed a rising incidence of early gastric cancer (EGC) at diagnosis, a trend largely attributed to the implementation of standardized endoscopic screening programs [2]. EGC is clinically defined as a tumor confined to the mucosa or submucosa, irrespective of lymph node status [3].

While laparoscopic gastrectomy has become the standard treatment for resectable EGC—offering superior postoperative recovery outcomes compared to open surgery [4–7], it presents a unique intraoperative challenge. As EGC is undetectable on the gastric serosal surface, preoperative endoscopic clipping is often employed for tumor localization. Whereas open surgery allows for direct clip palpation, the lack of tactile feedback in laparoscopy makes this localization impossible [8]. Consequently, the precise identification of tumor margins to determine appropriate resection boundaries, the extent of gastrectomy, and lymphadenectomy parameters becomes considerably challenging, potentially compromising both oncological precision and functional outcomes.

Current strategies for intraoperative tumor localization exhibit significant limitations. Preoperative endoscopic marking techniques, such as titanium clip placement or dye injection (e.g., India ink, indocyanine green), are hampered by risks of marker dislodgement prior to surgery, dye diffusion, tissue contamination, foreign body reactions, and potential peritonitis [8–10]. Intraoperative gastroscopy (IOG), often considered the gold standard [11], necessitates complex coordination between surgical and endoscopic teams, distends the gastric lumen thereby compromising the operative field and increasing surgical difficulty, prolongs operation time, complicates endoscopic manipulation due to different positioning requirements, and increases the risk of intraoperative infection [12–14]. Advanced techniques like fluorescence imaging remain constrained by cost and limited clinical availability [8]. Consequently, there exists a clear and unmet clinical need for a reliable, real-time, and seamlessly integrated intraoperative localization modality compatible with the laparoscopic surgical workflow.

Laparoscopic ultrasound (LUS) presents a promising solution to address tactile limitation of laparoscopy. By applying high-frequency transducers (typically 5–10 MHz) directly to the gastric serosa, LUS provides real-time, high-resolution cross-sectional imaging of tumor morphology and gastric wall layers, unimpeded by pneumoperitoneum [15]. Its clinical utility is well-established in hepatobiliary and pancreatic surgery for lesion detection and margin assessment [16, 17]. The demonstrated efficacy of preoperative endoscopic ultrasound (EUS)—with meta-analyses confirming a pooled sensitivity of 81% (range 64–94%) and specificity of 89% (range 67–100%) for T-staging in early gastric cancer [18]—provides a strong mechanistic foundation for LUS. This evidence robustly suggests its potential reliability in visualizing subsurface tumors. Theoretically, LUS offers a surgeon-controlled imaging tool that integrates seamlessly into the laparoscopic workflow, eliminating the need for additional instrumentation or procedural disruption.

Despite this compelling rationale and proven efficacy in other surgical specialties, robust evidence supporting LUS application in LG remains limited [8]. Therefore, this retrospective cohort study aimed to evaluate the clinical value of LUS for tumor localization by comparing its performance against conventional IOG in a consecutive cohort undergoing LG, assessing localization success rates, operative efficiency, and safety outcomes.

Patients and methods

Patients

This retrospective cohort study was conducted in compliance with the principles of the Declaration of Helsinki [19] and received approval from the Institutional Review Board of Wenzhou People’s Hospital. The reporting of this study adheres to the STROBE guidelines [20]. Consecutive patients aged 18–85 years who underwent LG for gastric cancer between February 2023 and December 2024 were considered for enrollment. Patients were categorized into two groups based on the intraoperative localization technique they received: either LUS localization or the IOG localization. Inclusion criteria required a preoperative pathological confirmation of gastric adenocarcinoma, including tumors of the gastroesophageal junction (Siewert type II and III), clinical T-stage T1-T3 without serosal involvement (as assessed by endoscopic and CT imaging), and no evidence of distant metastasis. Exclusion criteria encompassed: Siewert type I GEJ cancers; intraoperative discovery of T4 disease; a history of major abdominal surgery or severe adhesions; concurrent or recent active malignancy; pregnancy or lactation; a body mass index (BMI) ≥ 35 kg/m²; conversion to open surgery; or insufficient data.

Data were systematically extracted from Electronic Medical Records (EMR) using a standardized collection form. Preoperative data included general patient information (sex, age, BMI, tumor location, preoperative clinical symptoms) and preoperative blood tests (WBC, Hb, CRP). Intraoperative data encompassed localization success rates and time required for successful localization for both groups, with IOG localization time defined as the time from gastroscope entering incisors to successful tumor identification and LUS localization time measured from LUS probe entering trocar port to successful tumor identification; additionally, surgery date, surgical approach, operation duration, and intraoperative blood loss were recorded. Postoperative parameters included POD1 blood tests (WBC, Hb, CRP), time to first flatus, time to first liquid intake, complications (anastomotic leakage, bleeding, gastroparesis, chylous leakage, surgical site infection, pulmonary infection), postoperative hospital stay, total hospital stay, and total hospitalization costs. Pathological data included tumor location, histological type, maximum tumor diameter, tumor differentiation, resection margin status, depth of tumor invasion, pathological stage, total lymph nodes retrieved, number of positive lymph nodes, and detailed pathological staging. Postoperative follow-up data regarding recurrence and survival status were collected.

Preoperative assessment and surgical planning

All patients underwent a standardized preoperative workup. Informed consent for the surgical procedure, including potential risks and alternatives, was obtained from all patients or their legal guardians after a detailed discussion. Diagnosis of gastric cancer was confirmed histologically via endoscopic biopsy at our institution. Preoperative assessment included laboratory studies (complete blood count, chemistry panels, coagulation profile, gastrointestinal tumor markers), cardiopulmonary evaluation (electrocardiogram, echocardiography, pulmonary function tests), and imaging comprising chest CT and contrast-enhanced abdominal CT. Clinical T-staging was determined by integrating findings from the contrast-enhanced abdominal CT and the initial diagnostic endoscopy; endoscopic ultrasound (EUS) was not employed in our routine staging protocol.

Comorbidities such as hypertension and diabetes were optimized preoperatively to ensure all patients met American Society of Anesthesiologists (ASA) physical status [21] class I or II criteria prior to surgery. The choice of procedure (distal, total, or proximal gastrectomy) and the planned extent of lymphadenectomy were determined by the tumor’s location and clinical stage, in accordance with established guidelines [22, 23].

A critical surgical principle was the achievement of an R0 resection. The required gross resection margin was determined intraoperatively based on the suspected T-stage and macroscopic tumor type (Borrmann classification): >2 cm for T1 tumors; ≥3 cm for T2 + Borrmann I-II tumors; and ≥ 5 cm for T2 + Borrmann III-IV tumors. For tumors involving the cardia or pylorus, where a 5 cm margin was not feasible, intraoperative frozen section analysis of the resection margin was mandated to confirm a negative margin [22, 24].

Surgical procedure

All procedures were performed by a consistent surgical team following established protocols. Under general anesthesia, patients were positioned in a supine split-leg position. After standard antiseptic preparation and draping, pneumoperitoneum was established and maintained at 12–15 mmHg. A five-port technique was employed using both 5-mm and 12-mm trocars strategically placed for optimal access. After pneumoperitoneum, the abdomen was accessed for any metastasis.

Intraoperative tumor localization protocol

Precise tumor localization was performed using one of two techniques:

1. For the LUS Group:

   The ultrasound probe was introduced through a 12-mm trocar to perform a systematic examination of the gastric wall (Fig. 1). The normal gastric architecture was identified by its characteristic five-layer sonographic signature of alternating hyperechoic and hypoechoic bands (Fig. 2).

   Tumor identification relied on disruption of this normal stratification pattern. T1 stage tumors demonstrated preservation of the muscularis propria with involvement limited to the first three layers, showing characteristic mucosal disruption and submucosal invasion patterns (Fig. 3a). T2 stage lesions exhibited interruption and thickening of the muscularis propria while maintaining serosal (Fig. 3b). Advanced T3-T4 tumors displayed full-thickness wall invasion with serosal disruption and perigastric fat involvement (Fig. 3c). Upon LUS confirmation, the tumor was marked with vascular clips under direct laparoscopic visualization (Fig. 3d). The accuracy of localization was subsequently verified through specimen examination (Fig. 3e).

2. For the IOG Group:

   The IOG group received conventional dual-scope localization performed by an experienced endoscopist in coordination with the surgical team. This technique employed transillumination through the gastric wall with simultaneous endoscopic light source approximation and laparoscopic light diminishment to achieve preliminary localization (Fig. 4a). Endoscopic titanium clips were then deployed around the tumor periphery, allowing laparoscopic palpation and visual confirmation under combined endoscopic guidance (Fig. 4b). The precise correlation between the endoscopic clip placement and the tumor margins was confirmed on the gross specimen (Fig. 4c).

3. Salvage protocol.

   A standardized salvage protocol ensured universal technical success. Cases with unsuccessful or equivocal LUS localization immediately transitioned to IOG as the definitive method. Any discrepancy between localization techniques was resolved in favor of the IOG findings, with LUS results deemed unsuccessful in such instances. This systematic approach guaranteed successful tumor identification in all cases, enabling appropriate surgical resection planning based on established margin guidelines according to tumor stage and location.

Fig. 1.

Laparoscopic ultrasound setup and procedural workflow for tumor localization: a The ultrasound main unit used for imaging. b The laparoscopic linear array probe. c The surgeon manipulating the probe to achieve close contact with the gastric wall for real-time examination

Fig. 2.

Laparoscopic ultrasound image of the normal gastric wall: The normal gastric wall exhibits a characteristic five-layer sonographic architecture, comprising alternating hyperechoic and hypoechoic bands. From lumen outward: Layer 1 (hyperechoic), the superficial mucosa; Layer 2 (hypoechoic), the deep mucosa (including the muscularis mucosae); Layer 3 (hyperechoic), the submucosa; Layer 4 (hypoechoic), the muscularis propria; Layer 5 (hyperechoic), the serosa

Fig. 3.

Laparoscopic ultrasound T-staging of gastric cancer: imaging correlation with histopathological invasion: a T1 tumor: Disruption of layers 1–3 (mucosa, deep mucosa, and submucosa) with an intact muscularis propria (layer 4). b T2 tumor: Invasion into the muscularis propria (layer 4), which appears interrupted and thickened, with an intact serosa (layer 5). c T3 tumor: Full-thickness invasion with disruption of the serosa (layer 5). d Intraoperative vascular clip marking of the tumor margin following successful laparoscopic ultrasound localization. e Surgical specimen confirming the precision of ultrasonographic margin marking

Fig. 4.

Intraoperative gastroscopic tumor localization: a Laparoscopic view showing transillumination from the gastroscope (white arrow) identifying the tumor site. b Endoscopic placement of titanium clips to demarcate the tumor margins. c Gross surgical specimen confirming the accuracy of the localization

Resection and reconstruction

Following precise tumor localization, radical gastrectomy was performed according to the demarcated margins, with the surgical approach—total, distal, or proximal gastrectomy—determined by tumor characteristics and location. All procedures incorporated D2 lymphadenectomy following established oncological principles, with the extent of nodal dissection tailored to the specific resection. Specifically, total gastrectomy included comprehensive clearance of lymphatic stations 1, 2, 3, 4sa, 4sb, 4d, 5, 6, 7, 8a, 9, 10, 11p, and 11d, followed by Roux-en-Y esophagojejunostomy reconstruction. Distal gastrectomy encompassed dissection of stations 1, 3, 4sb, 4d, 5, 6, 7, 8a, 9, 11p, and 12a, with reconstruction via Roux-en-Y gastrojejunostomy. Proximal gastrectomy involved clearance of stations 1, 2, 3, 4sa, 4sb, 7, 8a, 9, and 11p, followed by double-tract reconstruction, jejunal interposition, or anti-reflux esophagogastrostomy utilizing the double-flap technique. All reconstructive procedures were completed through a 6 cm midline supra-umbilical incision, which simultaneously served for specimen retrieval in this hybrid laparoscopic-assisted approach. Following anastomotic construction, meticulous verification of hemostasis and anastomotic integrity was performed, closed-suction drainage systems were positioned strategically, and abdominal closure was accomplished in anatomical layers.

Postoperative management

Patients were managed according to enhanced recovery protocols. Routine care included NPO status with intravenous support, prophylactic antibiotics, multimodal analgesia, and nutritional support. Daily clinical monitoring assessed vital signs, drainage output, and abdominal findings.

Systematic laboratory surveillance included complete blood count, biochemistry panels, and coagulation profiles on postoperative days 1, 3, and 5. All patients underwent routine chest and abdominal CT on postoperative day 5. Recovery milestones including return of bowel function and resumption of oral intake were documented.

Complications were classified using the Clavien-Dindo system [25], with specific attention to: anastomotic leakage, bleeding requiring intervention, chylous leakage (drain output >200 mL/day with triglycerides >110 mg/dL), gastroparesis, surgical site infection, and pulmonary infection.

Follow-Up

Postoperative follow-up was conducted for 6–28 months through outpatient records, inpatient records, and telephone interviews, with follow-up time calculated from surgery date to tumor recurrence or last follow-up (cutoff date: approximately June 2025); follow-up protocol included quarterly tumor markers in year 1 with semiannual CT scans and annual endoscopy, transitioning to semiannual tumor markers and CT scans with annual endoscopy after the first year, with additional gastroscopy performed promptly for any abnormal tumor markers or imaging findings.

Definitions

The LUS localization time was defined as the time interval commencing from the insertion of the laparoscopic ultrasound probe through the designated 12-mm trocar—situated along the right midclavicular line approximately 2 cm superior to the umbilicus—until conclusive sonographic identification of the tumor was achieved. The IOG localization time was measured from passage of the gastroscope beyond the incisors to conclusive endoscopic visualization of the tumor. Total operative time encompassed the period from initial skin incision to final skin closure, including both primary localization and any necessary salvage procedures.

Statistical analysis

All statistical analyses were performed using SPSS software (version 27.0, IBM Corp.). Continuous variables are expressed as mean ± standard deviation or median with interquartile range, as appropriate, and were compared using Student’s t-test or the Mann-Whitney U test. Categorical variables are presented as frequencies (percentages) and were compared using the χ² test or Fisher’s exact test. A two-sided p-value < 0.05 was considered statistically significant. Due to the limited sample size (n = 58), which precluded a robust multivariate model, only univariate analyses were conducted to avoid overfitting; therefore, all results are reported as descriptive outcomes from these univariate comparisons.

Results

Patient selection and baseline characteristics

A retrospective analysis of 58 patients undergoing laparoscopic radical gastrectomy identified 22 patients who constituted the LUS group and 36 patients who constituted the IOG group. The preoperative demographic and clinical characteristics of both groups are presented in Table 1. There were no statistically significant differences in sex distribution (63.6% vs. 63.9% male, p = 0.985), age (63.91 ± 10.73 vs. 67.14 ± 10.94 years, p = 0.277), body mass index (22.07 ± 2.98 vs. 22.06 ± 3.18 kg/m², p = 0.236), tumor location (p = 0.754), or clinical symptoms (p = 0.267).

Table 1.

Comparison of general clinical data

Variables	LUS Group (n = 22)	IOG Group (n = 36)	Statistical Value	P-value
Sex (n)			0.000	0.985
Male	14 (63.6%)	23 (63.9%)
Female	8 (36.4%)	13 (36.1%)
Age (years)	63.91 ± 10.73	67.14 ± 10.94	1.099	0.277
BMI (kg/m²)	22.07 ± 2.98	22.06 ± 3.18	-1.197	0.236
Tumor Location			1.198	0.754
Cardia	3 (13.6%)	2 (5.6%)
Gastric body	4 (18.2%)	6 (16.7%)
Gastric antrum	11 (50.0%)	21 (58.3%)
Gastric angle	4 (18.2%)	7 (19.4%)
Symptoms			2.640	0.267
Asymptomatic	14 (63.6%)	15 (41.7%)
Upper GI symptoms	6 (27.3%)	16 (44.4%)
GI bleeding	2 (9.1%)	5 (13.9%)

Abbreviations: LUS Laparoscopic Ultrasound, IOG Intraoperative Gastroscopy, BMI Body MassIndex, GI Gastrointestinal

Surgical procedures and decision-making

The choice between laparoscopic total gastrectomy (LTG), distal gastrectomy (LDG), or proximal gastrectomy (LPG) was guided by the tumor location and the resection margins defined by the respective intraoperative localization technique (LUS or IOG). The distribution of surgical procedures is detailed in Table 2. In the LUS group, LTG was performed in 9 patients (40.9%), LDG in 12 (54.5%), and LPG in 1 (4.5%). In the IOG group, LTG was performed in 12 patients (33.3%), LDG in 23 (63.9%), and LPG in 1 (2.8%). There was no significant difference in the distribution of procedures between the two groups (p = 0.764). In both cohorts, the decision to perform LTG versus LDG/LPG was based on the localized tumor’s proximity to the cardia or pylorus, ensuring adherence to oncological margin principles. The accuracy of the assigned localization method (LUS or IOG) provided the necessary spatial information to determine the appropriate extent of resection.

Table 2.

Comparison of intraoperative data

Variable	LUS Group (n = 22)	IOG Group (n = 36)	Statistical Value	P-value
Localization Success, %	95.5	100	–	0.379
Overall Localization Time, min	3.83 ± 0.26	4.06 ± 0.16	4.332	0.001
Localization Time by Site, min
Cardia	4.09 ± 0.19	3.83 ± 0.15	-1.590	0.210
Gastric body	3.69 ± 0.19	4.08 ± 0.16	3.513	0.008
Gastric antrum	3.82 ± 0.27	4.09 ± 0.15	3.636	0.001
Gastric angle	3.78 ± 0.26	4.03 ± 0.15	2.094	0.066
Surgical Procedure, n (%)			0.538	0.764
Total gastrectomy (LTG)	9 (40.9%)	12 (33.3%)
Distal gastrectomy (LDG)	12 (54.5%)	23 (63.9%)
Proximal gastrectomy (LPG)	1 (4.5%)	1 (2.8%)
Total Operative Time, min	218.68 ± 28.48	240.69 ± 26.71	2.97	0.004
Estimated Blood Loss, ml	50 (20, 300)	50 (10, 300)	-0.740	0.459

Abbreviations: LUS Laparoscopic Ultrasound, IOG Intraoperative Gastroscopy, LTG Laparoscopic Total Gastrectomy, LDG Laparoscopic Distal Gastrectomy, LPG LaparoscopicProximal Gastrectomy

Intraoperative outcomes

Tumor localization was successful in 21 of 22 patients (95.5%) in the LUS group, with one failure involving a T1a (0.5 cm) tumor at the gastric angle; concurrent IOG confirmed the location in this case. The success rate in the IOG group was 100% (p = 0.379). The mean overall localization time was significantly shorter in the LUS group (3.83 ± 0.26 min) compared to the IOG group (4.06 ± 0.16 min; p = 0.001). This reduction was significant for tumors located in the gastric body (3.69 ± 0.19 vs. 4.08 ± 0.16 min, p = 0.008) and antrum (3.82 ± 0.27 vs. 4.09 ± 0.15 min, p = 0.001).

Surgical procedure selection—laparoscopic total gastrectomy (LTG), distal gastrectomy (LDG), or proximal gastrectomy (LPG)—was guided by tumor location and resection margins defined through the respective localization technique. In the LUS group, LTG was performed in 9 patients (40.9%), LDG in 12 (54.5%), and LPG in 1 (4.5%). Correspondingly, in the IOG group, LTG was performed in 12 patients (33.3%), LDG in 23 (63.9%), and LPG in 1 (2.8%). The distribution of procedures did not differ significantly between groups (p = 0.764). In both cohorts, the decision to perform LTG versus LDG/LPG was based on the tumor’s proximity to the cardia or pylorus to ensure adequate oncological margin.

Consequently, the total operative time was significantly shorter in the LUS group (218.68 ± 28.48 min vs. 240.69 ± 26.71 min, p = 0.004). Estimated blood loss was comparable between groups (50 ml for both, p = 0.459) (Table 2; Fig. 5).

Fig. 5.

Comparative procedural metrics between laparoscopic ultrasound and conventional gastroscopic localization techniques: a Overall tumor localization time. b Localization time stratified by tumor location. c Total operative time

Postoperative outcomes

Recovery parameters are detailed in Table 3. The time to first flatus (2 days, p = 0.979), time to liquid diet (5.73 ± 1.24 vs. 5.72 ± 1.47 days, p = 0.989), postoperative hospital stays (13 vs. 13.5 days, p = 0.235), and total hospitalization costs (¥61,253.50 ± ¥13,715.36 vs. ¥65,854.29 ± ¥11,885.78, p = 0.183) did not differ significantly between the LUS and IOG groups. The overall postoperative morbidity was comparable (Table 4). The rate of non-infectious complications was 13.6% in the LUS group and 13.9% in the IOG group (p = 1.000), with specific complications including anastomotic leak (4.5% vs. 2.8%, p = 1.000) and chylous leak (9.1% vs. 2.8%, p = 0.551). The rate of infectious complications was also similar between groups (13.6% vs. 16.7%, p = 1.000).

Table 3.

Comparison of postoperative data

Variables	LUS Group (n = 22)	IOG Group (n = 36)	Statistical Value	P-value
Time to First Flatus (days)	2 (1, 3)	2 (1, 3)	-0.026	0.979
Time to Liquid Diet (days)	5.73 ± 1.24	5.72 ± 1.47	-0.103	0.989
Postoperative Hospital Stay (days)	13 (9, 20)	13.5 (9, 39)	-1.187	0.235
Hospitalization Costs (¥)	61,253.50 ± 13,715.36	65,854.29 ± 11,885.78	1.349	0.183

Abbreviations: LUS Laparoscopic Ultrasound, IOG Intraoperative Gastroscopy

Table 4.

Postoperative complications

Variables	LUS Group (n = 22)	IOG Group (n = 36)	P-value
Non-Infectious Complications (n)	3 (13.6%)	5 (13.9%)	1.000
Anastomotic bleeding	0 (0%)	1 (2.8%)	1.000
Anastomotic leak	1 (4.5%)	1 (2.8%)	1.000
Gastroparesis	0 (0%)	2 (5.6%)	0.521
Chylous leak	2 (9.1%)	1 (2.8%)	0.551
Infectious Complications (n)	3 (13.6%)	6 (16.7%)	1.000
Surgical site infection	1 (4.5%)	2 (5.6%)	1.000
Pulmonary infection	2 (9.1%)	5 (13.9%)	0.698

Abbreviations: LUS Laparoscopic Ultrasound, IOG Intraoperative Gastroscopy

After a mean follow-up of 12 months, recurrence rates (4.5% vs. 5.6%, p = 1.000) and disease-free survival (DFS) were equivalent between the LUS and IOG groups (Supplementary Table 1, Fig. 6).

Fig. 6.

Kaplan-Meier curves comparing disease-free survival (DFS) between laparoscopic ultrasound and conventional gastroscopy localization groups

Pathological outcomes

Pathological assessment demonstrated equivalent radicality of resection between groups (Table 5). All patients achieved R0 resection. The lymph node yield was comparable between the LUS and IOG groups (32.5 vs. 38.0 nodes, p = 0.320). There were no significant intergroup differences in the number of positive lymph nodes (1.0 vs. 3.0, p = 0.225), tumor diameter (3.15 ± 1.50 cm vs. 3.53 ± 1.03 cm, p = 0.296), histologic type (p = 0.537), T stage (p = 0.118), or overall pathologic stage (p = 0.181).

Table 5.

Pathological data comparison

Variables	LUS Group (n = 22)	IOG Group (n = 36)	Statistical Value	P-value
Histological Type (n)			1.242	0.537
Adenocarcinoma	13 (59.1%)	21 (58.3%)
Signet ring cell carcinoma	7 (31.8%)	14 (38.9%)
Adenocarcinoma + neuroendocrine cancer	2 (9.1%)	1 (2.8%)
Pathological Stage			3.424	0.181
I	9 (40.9%)	8 (22.2%)
II	6 (27.3%)	8 (22.2%)
III	7 (31.8%)	20 (55.6%)
Pathological T Stage			5.870	0.118
T1a	4 (18.2%)	3 (8.3%)
T1b	6 (27.3%)	3 (8.3%)
T2	2 (9.1%)	6 (16.7%)
T3	10 (45.5%)	24 (66.7%)
Histological Grade			2.620	0.270
Well-differentiated	0 (0%)	2 (5.6%)
Moderately-differentiated	6 (27.3%)	5 (13.9%)
Poorly-differentiated	16 (72.7%)	29 (80.6%)
Max Tumor Diameter (cm)	3.15 ± 1.50	3.53 ± 1.03	1.061	0.296
Lymph Nodes Retrieved (n)	32.5 (17, 58)	38.0 (15, 49)	-0.994	0.320
Positive Lymph Nodes (n)	1.0 (0, 7)	3.0 (0, 7)	-1.138	0.225
Lymph Node Positivity (%)	2.64% (0,26.32%)	9.08% (0,27.78%)	-0.920	0.358
Negative Margin Rate	100% (22/22)	100% (36/36)	-	-

Abbreviations: LUS Laparoscopic Ultrasound, IOG Intraoperative Gastroscopy

Discussion

Precise intraoperative tumor localization remains a critical challenge in minimally invasive gastric surgery, particularly for early-stage and non-palpable lesions where the loss of tactile feedback can significantly compromise resection accuracy. The fundamental limitation of laparoscopy lies in its inability to visualize subsurface tumors, creating a dependency on external localization methods that disrupt surgical workflow and introduce additional complexity [8]. This challenge is especially pertinent in the context of EGC, where the rising incidence of small, non-ulcerated lesions demands increasingly precise localization techniques to guide function-preserving resections. Various techniques have been developed to address this need, as discussed previously; however, each presents distinct limitations in clinical practice [8–10, 12].

LUS addresses these limitations by providing real-time, high-resolution cross-sectional imaging of gastric wall architecture. This technology utilizes the established sonographic principle of five-layer gastric wall visualization, enabling identification of tumor-induced architectural disruptions while maintaining procedural autonomy [15, 26]. Our experience demonstrates that LUS not only matches but potentially surpasses conventional techniques in key operational metrics while maintaining equivalent oncological outcomes.

Our results show that surgeon-performed LUS achieved high localization accuracy (21/22 patients, 95.5%) comparable to conventional IOG (100%; p = 0.379). The single failure involved a 0.5 cm T1a tumor at the gastric angle, subsequently verified by concurrent IOG. This suggests that very small T1a-stage tumors (< 1 cm) in challenging anatomical locations may present detection difficulties. For such cases, we recommend preoperative endoscopic titanium clip placement, which provides hyperechoic landmarks with posterior acoustic shadowing [27]. To optimize imaging quality, we implemented technical measures to minimize gas interference, including standardized preoxygenation maneuvers, gastric decompression, intraperitoneal water immersion, and maintaining optimal probe contact. Particularly for the most technically demanding locations, such as the gastroesophageal junction or high posterior wall, these general principles were augmented with specific maneuvers: complete mobilization of the distal esophagus to create a surgical window, reverse Trendelenburg positioning for exposure, and dedicated caudal-dorsal gastric traction with longitudinal probe alignment. This tailored, systematic approach effectively overcame the restricted spatial anatomy and enabled consistent tumor identification.

Beyond accuracy, LUS demonstrated superior operational efficiency with significantly shorter localization times compared to IOG (3.83 ± 0.26 vs. 4.06 ± 0.16 min). This advantage was particularly notable for gastric body and antrum tumors. The learning curve for LUS proved manageable, with localization times showing a decreasing trend as experience accumulated. Our team’s prior experience with LUS in hepatobiliary surgery facilitated this process. For broader adoption, we recommend a structured training pathway including formal ultrasound training, initial practice with IOG correlation, beginning with larger T2/T3 tumors, and IOG verification for initial independent cases.

The demonstrated accuracy and efficiency of LUS translate directly to its core clinical role: providing the definitive spatial information required for surgical decision-making. In this study, the comparable distribution of total, distal, and proximal gastrectomies between the LUS and IOG groups confirms that both techniques equally supported the critical choice of resection extent. By reliably defining tumor margins in relation to the cardia and pylorus, LUS enabled the same oncological principle applied with IOG: to perform the most limited resection that ensures an R0 margin. This establishes LUS not merely as a localizing tool, but as a reliable guide for determining the optimal surgical strategy.

The safety profile of LUS was exemplary, with no LUS-related intraoperative complications (bleeding or visceral injury) observed in our series. Combined with its efficiency advantages, LUS contributed to significantly reduced total operative time (218.68 ± 28.48 vs. 240.69 ± 26.71 min), resulting from eliminated endoscopist coordination requirements and avoidance of gastric insufflation.

Notably, preoperative staging in this cohort was performed without routine Endoscopic Ultrasound (EUS), reflecting a common clinical scenario in many centers. Our results demonstrate that LUS remains effective in this context, providing valuable intraoperative staging information that complements findings from contrast-enhanced CT and endoscopy.

Economically, while total hospitalization costs did not differ significantly (¥61,253.50 ± 13,715.36 vs. ¥65,854.29 ± 11,885.78; p = 0.183), the trend favoring LUS is notable given the absence of additional charges compared to substantial endoscopy-related fees for IOG.

We acknowledge several limitations in our study, including its retrospective, single-center design and the non-randomized allocation of the localization technique based on surgeon preference and technological availability, which introduces a potential for selection bias. Additional limitations are the relatively small sample size and the short history of LUS application, which restricts the availability of long-term follow-up data. To address these limitations, we recommend future multicenter prospective studies with larger cohorts, standardized training protocols, and initial LUS validation with concurrent IOG during the learning phase, particularly for T2/T3 tumors.

In conclusion, LUS enables precise and rapid intraoperative localization of gastric tumors, guiding optimal surgical strategies with high safety and reliability. The technique demonstrates significant clinical value through reduced operative times, comparable oncological outcomes, and potential economic benefits. As experience grows, LUS holds substantial promise for widespread adoption in laparoscopic gastric cancer surgery.

Authors’ contributions

D.K.Y. and P.W. contributed equally to the study design, data collection, and initial manuscript drafting. L.M., D.B., Y.H., Z.Y., H.H., and S.L. participated in data collection and analysis. Y.H. provided critical revisions and acted as the corresponding author. All authors reviewed and approved the final manuscript.

Funding

None.

Data availability

All the data for this study will be made available upon reasonable request to the corresponding author.

Declarations

Ethics approval and consent to participate

This retrospective cohort study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board (IRB) of Wenzhou People’s Hospital (Approval Code: KY-20512-05). The IRB waived the requirement for informed consent for the use of anonymized patient data in this retrospective analysis. However, informed consent for the surgical procedure was obtained from all patients or their legal guardians as part of routine clinical care.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.