Research progress in laparoscopic endoscopic cooperative surgery for early gastric cancer: A narrative review

Abstract

Laparoscopic endoscopic cooperative surgery (LECS) is a cutting-edge minimally invasive technique, applicable not only in benign gastrointestinal and stromal tumors but also in early gastric cancer (EGC). In EGC management, LECS integrates the benefits of laparoscopy and endoscopy. Endoscopy provides precise localization and accurate submucosal dissection, enabling optimal preservation of healthy gastric tissue. Concurrently, laparoscopy facilitates effective suturing, hemostasis, and management of complications such as perforation, as well as lymph node dissection when required, achieving a balance between functional preservation, oncological efficacy, and procedural safety. This article comprehensively reviews recent developments in LECS for EGC, including its history, indications, clinical outcomes, safety profiles, specific surgical protocols, and role in sentinel lymph node navigation surgery. Additionally, it explores future prospects for LECS in EGC treatment.

Key Words: Laparoscopic endoscopic cooperative surgery; Early gastric cancer; Gastric function preservation; Sentinel lymph node; Lymph node dissection

Core Tip: Laparoscopic endoscopic cooperative surgery (LECS) represents a paradigm shift in minimally invasive treatment for early gastric cancer (EGC). By synergistically combining endoscopic precision with laparoscopic safety, it achieves an optimal balance between maximal organ preservation and radical oncologic resection, paving the way for function-preserving surgery. This article comprehensively reviews recent developments in LECS for EGC, including its history, indications, clinical outcomes, safety profiles, specific surgical protocols, and role in sentinel lymph node navigation surgery. Additionally, it explores future prospects for LECS in EGC treatment.

INTRODUCTION

According to the 2024 global cancer statistics published by the International Agency for Research on Cancer of the World Health Organization, gastric cancer remains one of the most prevalent malignancies, with global incidence and mortality rates ranking fifth and fourth, respectively[1]. Early gastric cancer (EGC) is defined as a tumor confined to the gastric mucosa or submucosa, regardless of regional lymph node metastasis[2]. With the widespread adoption of endoscopic screening and growing public awareness of health, the clinical detection rate of EGC has steadily increased[3]. The primary treatment options for EGC currently include endoscopic submucosal dissection (ESD) and radical gastrectomy, each offering distinct advantages and limitations in therapeutic approach and clinical outcomes. While ESD allows for direct removal of the lesion, its main limitation is the absence of lymph node dissection[4]. Research indicates that the lymph node metastasis rate in EGC is approximately 13%[5,6]. The 5-year survival rate for patients with lymph node metastasis is 87.3%, compared to 94.2% for those without metastasis[7,8]. Furthermore, ESD is associated with procedure-related complications such as bleeding and perforation[9]. In cases where postoperative histopathological assessment following ESD reveals high-risk features, additional radical gastrectomy on gastrectomy is indicated. However, post-ESD adhesions may complicate subsequent surgical intervention and potentially compromise oncologic outcomes[10]. In contrast, traditional radical gastrectomy ensures complete tumor resection through systematic lymph node dissection but typically involves extensive gastric resection and complex gastrointestinal reconstruction, significantly altering the stomach’s normal anatomical structure and physiological function[11]. This often results in short-term complications such as delayed gastric emptying and intestinal obstruction[12,13], as well as long-term sequelae like malnutrition, dumping syndrome, and reflux esophagitis[14-16], all of which can severely impact quality of life. Therefore, achieving oncological radicality while maximizing gastric function preservation remains a critical focus in clinical practice.

Function-preserving gastrectomy refers to a set of surgical procedures aimed at preserving the stomach’s normal anatomical structure and physiological function. These techniques include pylorus-preserving gastrectomy, proximal gastrectomy, local gastrectomy, and laparoscopic endoscopic cooperative surgery (LECS), among others[17-20]. LECS, in particular, has garnered significant attention due to its unique ability to enable precise lesion resection while maintaining gastric anatomy and function, thereby improving postoperative quality of life[19]. However, conventional LECS is not without limitations: Intraoperative gastric wall incisions may elevate the risk of intraperitoneal dissemination of tumor cells or gastric contents[21]. Additionally, the feasibility and safety of lymph node dissection via LECS remain suboptimal, prompting the development of various modified approaches to enhance the procedure[22-24]. To further improve surgical safety and therapeutic outcomes, the integration of LECS with sentinel lymph node navigation surgery (SNNS) has emerged as a promising research area. This combined strategy enables minimally invasive resection while assessing regional lymph node metastasis through sentinel lymph node (SLN) localization and pathological evaluation[25,26], facilitating individualized, precision-based treatment. Despite its promise, debates persist over optimal procedural protocols and tracer selection in SLN navigation.

Although several reviews have explored LECS applications in benign gastric tumors and stromal tumors, systematic summaries of its use in EGC remain limited. This article provides a comprehensive review of the current research on LECS for EGC, including the technique’s developmental history, clinical indications, surgical protocols, efficacy and safety outcomes, and its integration with SNNS. Additionally, it offers insights into future directions for LECS in EGC treatment.

SEARCH STRATEGY AND SELECTION CRITERIA

Our literature research was conducted without language restriction using the following databases: PubMed, OVID, and Scopus and Google Scholar. The search included all potential articles published before December 25, 2025 (updated on March 1, 2026). An analytical framework was established for each database by formulating targeted queries to identify pertinent articles. Keywords searched included “laparoscopic endoscopic cooperative surgery”, “early gastric cancer”, “gastric function preservation”, “sentinel lymph node”, “lymph node dissection”, “sentinel lymph node navigation surgery”, “indocyanine green”, “minimally invasive”, and various combinations thereof using Boolean operators such as “AND”, “OR”, and “NOT”. Although no prespecified criteria were established, the studies included in this review had to meet the following requirements: (1) Publication in English or other languages with accompanying English translations; (2) Inclusion of original experimental and clinical studies that explore underlying mechanisms and have been accepted for publication in peer-reviewed journals; (3) A specific focus on LECS and its research on EGC; and (4) Relevant meta-analyses, clinical trials, systematic or narrative reviews, including those employing machine learning research or mathematical models. The following articles were excluded from the analysis if they: (1) Consisted solely from the analysis: Abstracts, correspondence, editorials, expert opinions, or similar articles; or (2) Those that carried retraction notices or watermarks.

THE DEVELOPMENT HISTORY OF LECS

LECS originated in the 1990s, initially used for colonic polyp resections, reflecting the principle of functional preservation in gastrointestinal surgery[27]. In 2008, Japanese researchers Abe et al[28] first reported laparoscopic-assisted endoscopic full-thickness resection combined with lymph node dissection, successfully performing minimally invasive treatment in patients with EGC - marking LECS’s introduction to gastric oncology. That same year, Hiki et al[29] introduced the classic LECS technique, primarily employed for local resection of submucosal tumors, such as gastrointestinal stromal tumors, to achieve complete tumor removal while minimizing unnecessary gastric tissue excision. However, the conventional LECS approach necessitates communication between the gastric and abdominal cavities during surgery, which carries the risk of intraperitoneal contamination by gastric contents and potential tumor seeding or metastasis[30]. To address these concerns, subsequent modifications were developed. Nunobe et al[31] proposed a modified technique known as “inverted LECS”. Additionally, in 2011 and 2012, Japanese researchers Goto et al[32] and Inoue et al[33] independently introduced two “non-exposed” modified techniques - non-exposed endoscopic wall inversion surgery (NEWS) and combined laparoscopic and endoscopic approach for neoplasia with a non-exposure technique (CLEAN-NET). These methods maintain isolation between the gastric and abdominal cavities throughout the procedure, effectively mitigating the risk of contamination and tumor seeding. Technological advancements have continued toward simplification and optimization. In 2017, Professor Kikuchi et al[34] introduced closed LECS, further streamlining surgical steps and enhancing operational feasibility without opening the gastric cavity. In 2019, Kitakata et al[35] proposed an improved version of sealed endoscopic full-thickness resection. Currently, LECS’s application extends beyond the stomach to include early tumor resections in other gastrointestinal regions, such as the duodenum, colon, and rectum[36-38]. However, the feasibility and safety of LECS combined with targeted regional lymph node dissection for localized gastric lesions remain under investigation[39] and require further validation through robust multicenter clinical trials and high-quality comparative studies.

SURGICAL INDICATIONS FOR EGC

The implementation of LECS is determined by a comprehensive assessment of the medical institution’s diagnostic and therapeutic capabilities, the patient’s clinical condition, and the surgeon’s technical expertise[40-42]. Preoperative evaluations, including gastroscopy, endoscopic ultrasound, and contrast-enhanced computed tomography, are essential for assessing tumor size and location, and establishing a pathological diagnosis prior to surgery[43-46]. LECS is primarily indicated for patients with EGC whose tumors fall between the criteria for ESD and those requiring standard radical gastrectomy, aiming to achieve precise tumor resection while minimizing surgical trauma. According to the 6^th edition of the Japanese Gastric Cancer Treatment Guidelines[2], ESD indications include: (1) Differentiated adenocarcinoma, clinically staged as T1a (cT1a), without ulcerative findings; (2) Differentiated adenocarcinoma, cT1a, with ulcerative findings and tumor diameter ≤ 3 cm; (3) Undifferentiated adenocarcinoma, cT1a, without ulcerative findings and diameter ≤ 2 cm; and (4) Undifferentiated adenocarcinoma, clinically staged as T1b (cT1b), with diameter ≤ 3 cm. For patients meeting these ESD criteria but facing technical challenges due to tumor location, size, or ulceration, LECS may offer a safe and effective alternative[31,47,48]. Additionally, the Chinese Clinical Practice Guidelines for Laparoscopic-Endoscopic Cooperative Surgery in Gastrointestinal Tumors consider LECS a suitable option for patients with EGC who do not meet ESD criteria, particularly when exploring less invasive alternatives to standard radical resection[49]. Notably, SLN metastasis is currently a contraindication for LECS[31,50]. Therefore, in patients with EGC who do not meet ESD criteria and are found to have lymph node metastasis, D1 or D1+ lymph node dissection with radical gastrectomy should be performed as per the Japanese guidelines[2].

CLINICAL EFFICACY AND SAFETY OF LECS FOR EGC

LECS has emerged as a minimally invasive strategy for EGC, with accumulating evidence supporting its oncologic efficacy and perioperative safety (Table 1)[21,28,31,33,46,47,51-54]. In terms of oncologic outcomes, studies have reported high R0 resection rates even for large tumors: Cho et al[52] achieved complete resection in 14 patients with tumors up to 90 mm, and Hajer et al[46] reported R0 resection in all 7 patients (mean tumor size 33.5 ± 12.8). Furthermore, available long-term follow-up data indicate no evidence of tumor patients (mean tumor size 33.5 ± 12.8). Furthermore, available long-term follow-up data indicate no evidence of tumor recurrence, underscoring the oncologic adequacy of the procedure. Regarding perioperative safety, LECS demonstrated advantages such as reduced blood loss, a low incidence of postoperative complications, and shorter hospital stays. However, surgical duration, a metric reflecting technical difficulty, varied considerably across studies. For instance, Ludwig et al[53] reported a mean operative time of 44.3 minutes, whereas Abe et al[28] and Okubo et al[21] recorded significantly longer durations (389 minutes and 325.80 ± 17.72 minutes, respectively). This variability may be attributed to factors such as tumor location, the expertise of the multidisciplinary team, and methodological heterogeneity in combined approaches.

Table 1 Summary of studies related to laparoscopic endoscopic cooperative surgery for early gastric cancer.

Ref.	Case count	Tumor size (mm)	Bleeding volume (mL)	Operation time (minute)	Complications	Length of stay (days)	Complete resection rate (100%)	Recrudescence
Okubo et al[21], 2020	25	18.49 ± 2.77	30.8 ± 28.37	325.80 ± 17.72	-	-	-	-
Abe et al[28], 2008	1	30	-	389	0	-	100	0
Nunobe et al[31], 2012	1	60	0	152	0	-	100	0
Inoue et al[33], 2012	16	-	18 (0-92)	-	3	-	-	0
Hajer et al[46], 2018	7	33.5 ± 12.8	-	108	2	6.8	100	0
Aoki et al[47], 2018	7	14.5 ± 3.6	11.3 ± 5.4	181.5 ± 37.9	0	16.3 ± 2.1	100	0
Saito et al[51], 2020	3	9.3 ± 4.0	11.0 ± 6.9	129.3 ± 16.9	0	10 ± 4.4	100	0
Cho et al[52], 2011	14	26 (12-90)	16 (5-30)	143 (110-253)	1	6 (4-10)	100	0
Ludwig et al[53], 2002	18	16 (11-23)	-	44.3 (31-67)	1	7.5 (3-11)	100	0
Hur et al[54], 2014	9	12.0 ± 8.7	-	183.8 ± 71.4	1	5.9 ± 1.3	100	0

In summary, current evidence suggests that LECS is a safe and effective treatment for EGC, achieving favorable oncologic outcomes with a low risk of recurrence and enhanced postoperative recovery. Nevertheless, given that most studies are small case series with incomplete data, large-scale prospective studies are warranted to validate these findings.

SURGICAL PROTOCOLS FOR LECS

Classic LECS

The classic LECS technique was initially proposed by Japanese scholars and later introduced into clinical practice[29,55]. Tumor location, size, and depth were determined via gastroscopy and laparoscopy. Under endoscopic guidance, the tumor margins were marked using electrocoagulation. A 10% glycerol solution was injected into the submucosal layer to facilitate elevation. An initial incision was made using a standard needle knife, followed by insertion of the IT-2 knife tip into the submucosa for circumferential dissection along the pre-marked boundary. Seromuscular layer dissection began from the incision site using either the IT-2 knife or an ultrasonic device. Most of the seromuscular dissection was performed endoscopically with laparoscopic assistance, while any remaining portion was completed laparoscopically. After tumor resection, the specimen was retrieved transabdominally, and the incision was closed using a laparoscopic mechanical stapler (Figure 1).

Figure 1 Classic laparoscopic endoscopic cooperative surgery operation steps. A: Endoscopic injection of 10% glycerol into the submucosa; B: Endoscopic circumferential resection of the mucosa and submucosa, with extensive dissection of the seromuscular layer; C: Complete dissection of the remaining seromuscular layer under laparoscopy; D: Retrieval of the intact tumor tissue through a transabdominal approach, followed by closure of the incision using a laparoscopic mechanical stapler.

Inverted LECS

Inverted LECS reduces the risk of exposure to a certain extent[31,47]. The procedure begins with tumor localization via endoscopy, followed by submucosal injection of 10% glycerol to facilitate dissection and delineate the resection margin. The seromuscular layer is then dissected under laparoscopic guidance using an ultrasonic device. Once the resection extent is confirmed by both endoscopic and laparoscopic assessments, multiple sutures are placed to suspend the gastric wall around the tumor to the abdominal wall, forming a “crown” configuration. During the full-thickness incision under laparoscopy, the tumor is turned into the gastric cavity. After complete resection, the specimen is retrieved transorally, and the defect is closed using a laparoscopic mechanical stapler (Figure 2).

Figure 2 Inverted laparoscopic endoscopic cooperative surgery operation steps. A: Endoscopic submucosal dissection and mucosal resection; B: Sutures suspend the gastric wall, forming a crown-like structure; C: Under laparoscopy, part of the seromuscular layer is dissected, and the tumor is inverted into the gastric cavity; D: Continuation of seromuscular layer dissection, followed by transoral extraction of the intact tumor tissue. The incision is then closed using a laparoscopic mechanical stapler.

NEWS

NEWS was developed as an inversion technique for precise tumor resection[56-58]. Endoscopic mucosal marking is performed to delineate the resection area, with corresponding serosal markings made under laparoscopic guidance to ensure precise localization. Next, 10% glycerol is injected into the submucosal layer to establish an adequate dissection plane. Under laparoscopic visualization, the seromuscular layer is circumferentially incised, and the outer margin of this layer is sutured linearly with 3-0 silk thread to invert the tumor into the gastric cavity. The mucosa and submucosa are then circumferentially resected along the pre-marked boundaries under endoscopic control, and the excised tumor specimen is retrieved transorally. Finally, the mucosal and submucosal resection margins are secured using endoscopic clips (Figure 3).

Figure 3 Non-exposed endoscopic wall inversion surgery operation steps. A: Endoscopic injection of 10% glycerol into the submucosa; B: Circumferential incision of the seromuscular layer under laparoscopy, followed by linear suturing of the outer rim with 3-0 silk sutures; C: Tumor inversion into the gastric cavity; D: Complete removal of the tumor tissue through the oral cavity, with closure of the mucosal and submucosal layer wound edges using endoscopic forceps.

CLEAN-NET

CLEAN-NET is a full-thickness resection method designed for controlled tissue mobilization[33,59]. Following endoscopic marking, multiple 3-0 black silk sutures are placed to secure the full thickness of the gastric wall, establishing a stable connection between the mucosal and seromuscular layers. Under laparoscopic guidance, the seromuscular layer is dissected along the outer side of the sutures, carefully preserving the integrity of the mucosal layer. These sutures serve dual purposes as suspension and traction devices, allowing complete mobilization of the target mucosal segment and promoting bulging of surrounding tissue to form a natural “seal zone”. The resected mucosal tissue and dissected seromuscular layer are then removed en bloc using a mechanical stapler, with surgical margins confirmed to meet oncologic safety criteria. Finally, the specimen is retrieved through the abdominal cavity (Figure 4).

Figure 4 Combined laparoscopic and endoscopic approach for neoplasia with a non-exposure technique operation steps. A: Placement of several 3-0 black silk sutures laparoscopically to fix the full thickness of the gastric wall, followed by dissection of the seromuscular layer along the outside of the sutures; B: The silk thread is pulled to create a natural “sealing area” in the tumor tissue; C: The mucosal tissue and free seromuscular layer are managed using a mechanical stapler; D: Complete removal of the tumor tissue through the abdominal cavity.

Closed LECS

This method allows tumor inversion and resection while keeping the procedure simple[34]. The mucosal boundary around the tumor is marked under endoscopic visualization, followed by submucosal injection of 10% glycerol to facilitate tissue elevation. The mucosa is then circumferentially resected along the pre-marked line under endoscopic guidance. Under endoscopic illumination, the corresponding anatomical margins are delineated within the submucosal layer. Next, under laparoscopic guidance, a sponge gasket is positioned at the center of the incision line by suturing the opposing seromuscular layers with 3-0 silk thread, inverting the tumor tissue and sponge gasket into the gastric cavity. Finally, circumferential resection of the seromuscular layer is completed under endoscopic observation, and the excised specimen, along with the sponge gasket, is retrieved transorally (Figure 5).

Figure 5 Closed laparoscopic endoscopic cooperative surgery operation steps. A: Endoscopic circumferential resection of the mucosa and submucosa; B: Suturing of the seromuscular layers on both sides with 3-0 silk thread, fixing the gasket at the center of the suture line; C: The tumor tissue, along with the gasket, is inverted into the gastric cavity, and the seromuscular layer is circumferentially resected under endoscopic guidance; D: Complete removal of the tumor tissue and gasket through the mouth.

Sealed endoscopic full-thickness resection

This method involves temporarily sealing the gastric serosal surface with a silicone sheet[35,60]. The lesion area is first delineated endoscopically, followed by submucosal injection of glycerol solution to facilitate elevation. A circumferential mucosal incision is made until the muscular layer is fully exposed, and the corresponding serosal region is marked under laparoscopic guidance. The silicone sheet is sutured and fixed to the serosal surface, with thrombin applied to enhance adhesion. Endoscopic dissection is then performed to separate the serosa and muscular layers, followed by the division of connecting sutures. The tumor specimen is retrieved transorally in its entirety. The silicone sheet is then stripped using laparoscopic forceps and removed through the mouth. Throughout the procedure, the stomach is continuously elevated to minimize the risk of gastric fluid leakage. Finally, the gastric wall defect is closed with linear suturing under laparoscopic visualization (Figure 6).

Figure 6 Sealed endoscopic full-thickness resection operation steps. A: Endoscopic circumferential resection of the mucosa and submucosa; B: The silicone sheet is fixed to the serosa at the lesion site with 3-0 silk thread under laparoscopy; C: Endoscopic separation of the seromuscular layer; D: Complete removal of the tumor tissue, aided by silicone sheet spacers, through the mouth. The defect on the gastric wall is sutured linearly via laparoscopy.

Table 2 presents a systematic comparison of established LECS variants. Although all LECS approaches share the fundamental advantage of integrated laparoscopic and endoscopic coordination, they differ meaningfully in procedural emphasis, technical requirements, advantages, and disadvantages. A structured evaluation of these characteristics enables clinicians to select the most appropriate procedure - tailored to both tumor-specific factors and institutional expertise.

Table 2 Advantages and limitations of different laparoscopic endoscopic cooperative surgery.

Surgical strategy	Stripping sequence	Removal method	Suture method	Key benefits	Limitations
Classical LECS	First, the mucosal layer is dissected, followed by dissection of the serosal layer	Abdominal cavity	Mechanical stapler	Precise resection, a relatively straightforward procedure with a short operative duration	Exposure of the gastric cavity may lead to contamination by gastric juice and the implantation and metastasis of tumor cells
Inverted LECS	First, the mucosal layer is dissected, followed by dissection of the serosal layer	Oral cavity	Mechanical stapler	Precise resection; significantly reduced risk of gastric juice contamination, as well as tumor cell implantation and metastasis	There remains exposure of the gastric cavity, and contamination by gastric fluid as well as tumor cell implantation or metastasis cannot be excluded
NEWS	First, the serosal layer is peeled off, followed by the submucosal layer	Oral cavity	Manual suture + endoscopic clips	Precise resection; complete non-exposure technique: Effectively prevents gastric juice contamination, as well as tumor cell implantation and metastasis	The procedure is technically demanding and associated with a prolonged operative duration
CLEAN-NET	The serosal layer, but not the mucosal layer, is dissected	Abdominal cavity	Mechanical stapler	Precise resection; complete non-exposure technique: Effectively prevents gastric juice contamination and tumor cell implantation or metastasis; preservation of mucosal continuity with the tumor encapsulated within the intact mucosa	Determining the appropriate anatomical plane is challenging, which may lead to gastric deformation
Closed LECS	First, the mucosal layer is dissected, followed by dissection of the serosal layer	Oral cavity	Manual suture	Precise resection; complete non-exposure technique: Effective prevention of gastric juice contamination and tumor cell implantation or metastasis; shorter operative duration compared to the two previously described non-exposure methods	Identification of the appropriate anatomical plane is technically challenging
Sealed-EFTR	First, the mucosal layer is dissected, followed by dissection of the serosal layer	Oral cavity	Manual suture	More precise resection margin; temporary serosal sealing: Prevents gastric juice contamination and tumor cell implantation or metastasis	The neoplasm is located at the gastric angulus or along the lesser curvature, which poses a technical challenge for the application of a silicone patch

LECS: Laparoscopic endoscopic cooperative surgery; NEWS: Non-exposed endoscopic wall-inversion surgery; CLEAN-NET: Combination of laparoscopic and endoscopic approaches to neoplasia with non-exposure technique; EFTR: Sealed endoscopic full-thickness resection.

APPLICATION OF SNNS

SLN, which represent the first sites of lymphatic drainage from the primary tumor, offer valuable insights into regional lymph node involvement through biopsy[61,62]. In theory, a negative SLN biopsy indicates the absence of regional lymph node metastasis[63]. However, the complexity of submucosal, subserosal, and intermuscular lymphatic networks within the gastric wall[64,65], along with the presence of larger or more aggressive tumors, increases the incidence of atypical and skip metastases[66,67]. This complexity makes reliance on a single SLN assessment potentially unreliable and clinically risky.

To enhance the accuracy and reliability of lymph node assessment, Miwa et al[68] introduced the concept of the sentinel lymphatic basin (SLB), which divides the gastric lymphatic drainage system into five distinct regions: The left gastric artery area (including lymph nodes No. 1, No. 7, and the cephalic portion of No. 3); the right gastric artery area (comprising No. 5, No. 8a, and the caudal portion of No. 3); the right gastroepiploic artery area (including No. 4d and No. 6); the left gastroepiploic artery area (containing No. 4sa and No. 4sb); and the short gastric artery area (involving No. 11p lymph nodes)[65]. During surgery, resection of the dye-marked SLB significantly increases the detection rate of SLN[69], and this has become a standard approach for SLN biopsy in EGC[70-72]. The standard protocol involves submitting the lymph nodes within the SLB for rapid pathological examination. If the result is positive, a D1/D1+ radical gastrectomy is performed; if negative, unnecessary lymph node dissection is avoided, and the extent of gastrectomy is minimized[73,74]. Research has confirmed the safety and feasibility of SNNS based on SLB[75-77], with the SENORITA trial in South Korea serving as a representative study. The results demonstrated that all patients with negative intraoperative frozen sections did not experience lymph node recurrence during the follow-up period[75]. Commonly used tracers in SNNS include indocyanine green (ICG), blue dye, carbon nanoparticles, and radioactive tracers[78,79]. However, blue dye has poor stability and poses a relatively high risk of allergic reactions[80]; carbon nanoparticles may lead to excessive tissue staining[78]; and radioactive tracers involve logistical complexity, cost, and radiation exposure concerns[81]. Currently, no single tracer meets all clinical requirements, leaving the optimal imaging agent for SLN mapping in EGC unresolved. Among the available options, ICG combined with near-infrared fluorescence imaging shows particular promise due to its non-ionizing nature, low allergenicity, and ability for real-time visualization[82-84]. Studies have reported that SLN detection using this method achieves a sensitivity of up to 100%[85,86], with complete resection rates exceeding 90% in EGC surgery and a low incidence of postoperative complications[87]. Additionally, a long-term randomized clinical trial has demonstrated that ICG-guided laparoscopic surgery is safer than conventional approaches and significantly improves survival outcomes[88]. Consequently, current Chinese clinical guidelines recommend ICG-based near-infrared imaging for lymph node localization in LECS to facilitate precise tumor resection[49]. However, challenges remain, particularly the risk of false-negative results. A Japanese multicenter study reported a false-negative rate as high as 46%, which decreased to 14% only after additional paraffin sectioning and re-evaluation[89]. The main reason for this unreliability was the single-plane frozen section. To address this limitation, ongoing research is focused on integrating intraoperative pathological evaluation with molecular analyses and immunohistochemical staining[90], as well as optimizing tracer injection techniques and sites[91,92]. However, this high false-negative rate represents a substantial oncologic safety concern. A false-negative SLN biopsy may delay definitive radical gastrectomy with systematic lymphadenectomy, thereby permitting persistence of micrometastatic disease and increasing the risk of locoregional recurrence. As a result, current clinical practice guidelines, including those of the Japanese Gastric Cancer Association, do not recommend SLN navigation surgery for routine clinical use[2]. SNNS represents a promising research direction; however, its clinical adoption should be approached with caution until the false-negative rate is adequately addressed and the technique receives formal endorsement in evidence-based clinical practice guidelines.

In summary, SNNS represents a significant advancement toward minimally invasive and individualized management of EGC. By enabling comprehensive assessment of the SLB and integrating advanced tracing modalities such as ICG near-infrared fluorescence imaging, this approach allows for reduced surgical extent and minimized tissue trauma while maintaining oncological radicality.

DISCUSSION

The principal advantage of LECS in the management of EGC resides in the synergistic integration of laparoscopic and endoscopic capabilities. This dual-modality approach facilitates precise, function-preserving resection while concurrently ensuring oncologic safety and minimizing perioperative morbidity.

However, this technological integration entails specific limitations and contraindications. The implementation of LECS critically relies on the integration of endoscopic and laparoscopic techniques, as well as interdisciplinary collaboration, rendering its routine application challenging in the absence of coordinated mechanisms[93,94]. This technique entails a steep learning curve, necessitating that novices first familiarize themselves with procedural workflows through animal experimentation[95]. Subsequently, systematic training and cumulative experience, alongside stringent adherence to standardized protocols under the guidance of experienced surgeons, are imperative for its graded introduction into clinical practice[96,97]. Oncologic safety remains the central subject of ongoing debate surrounding LECS. In patients with documented or suspected lymph node metastasis, the absence of systematic lymphadenectomy in LECS may compromise oncologic outcome. Furthermore, early iterations of the technique employed an intentional gastric wall perforation, raising theoretical concerns regarding peritoneal tumor cell dissemination and subsequent implantation. To date, LECS for EGC remains investigational; its oncologic safety has not been established and requires rigorous validation through prospective, multicenter clinical trials[41]. The economic profile of LECS is characterized by higher initial expenditures, attributable to the combined use of endoscopic and laparoscopic consumables and extended operative duration[98]. However, these incremental costs may be counterbalanced by savings from avoided complications, such as perforations or incomplete resections, which necessitate further management. In terms of procedural reproducibility, the application of LECS varies across institutions, and across different medical institutions. At present, mature experience with LECS remains primarily concentrated in high-volume medical centers, and its feasibility for application in primary healthcare settings still requires further investigation.

A systematic comparison of LECS with ESD and conventional radical gastrectomy (Table 3) provides a clear understanding of the respective advantages and disadvantages of these different surgical approaches, particularly the differences in oncological outcomes, complication rates, exposure risk, and long-term follow-up results. This analysis serves as a reference to inform treatment selection in clinical practice.

Table 3 Comparison of three surgical procedures for early gastric cancer.

Surgical procedures	Oncological outcomes	The incidence of complications	Risk exposure	Long-term follow-up results
LECS	High R0 resection rate, low recurrence rate	Low	The exposed LECS is relatively high, while the non-exposed LECS is relatively low	Long-term survival data beyond five years are still under documentation, yet notable restoration of gastric function and superior quality of life have been consistently observed
ESD	Higher R0 resection rate, higher recurrence rate	The incidence of bleeding and perforation is relatively high	This procedure carries a relatively high risk and poses a potential hazard for intraperitoneal seeding following perforation	The observed favorable five-year survival rate may necessitate subsequent surgical interventions
Traditional radical gastrectomy	High R0 resection rate and extremely low recurrence rate	High	Lower exposure risk	The five-year survival rate is high; however, long-term malnutrition leads to a decline in quality of life

LECS: Laparoscopic endoscopic cooperative surgery; ESD: Endoscopic submucosal dissection.

PERSPECTIVES

LECS is expected to further improve surgical precision and safety through the integration of emerging technologies, such as artificial intelligence-assisted image analysis and robot-assisted surgical systems[99,100]. Future research should focus on strengthening intraoperative protective measures and enhancing the accuracy of intraoperative pathological diagnoses - such as optimizing suturing instruments to improve surgical safety and employing multi-level sectioning techniques and reverse transcription polymerase chain reaction to increase the sensitivity of intraoperative detection. For EGC, if SLN biopsy yields a positive result, local gastric resection combined with targeted regional lymph node dissection via LECS may represent a promising avenue for future clinical investigation. According to the Japanese Gastric Cancer Treatment Guidelines (6^th Edition)[45], the extent of lymph node dissection should be individualized based on tumor location. For tumors in the proximal stomach, D1 or D1+ dissection is recommended: D1 includes lymph nodes No. 1, No. 2, No. 3a, No. 4sa, No. 4sb, and No. 7, while D1+ adds No. 8a, No. 9, and No. 11p. For distal stomach tumors, D1 or D1+ dissection is similarly recommended, with D1 covering lymph nodes No. 1, No. 3, No. 4sb, No. 4d, No. 5, No. 6, and No. 7, and D1+ including No. 8a and No. 9. Moving forward, well-designed multicenter randomized controlled trials are essential to assess the safety and feasibility of LECS combined with targeted lymph node dissection. With close collaboration among multidisciplinary teams, the integration of innovative technologies, and continued accumulation of high-level clinical evidence, this approach holds promise as a novel, minimally invasive therapeutic option for carefully selected patients with EGC, ultimately achieving an optimal balance between functional preservation and oncological efficacy (Figure 7).

Figure 7 Laparoscopic endoscopic cooperative surgery combined with sentinel lymph node navigation surgery treatment for early gastric cancer surgical plan. Red represents the laparoscopic endoscopic cooperative surgery technique; white represents other techniques. ESD: Endoscopic submucosal dissection; LECS: Laparoscopic endoscopic cooperative surgery; D1: First station; D1+: First station plus additional.

CONCLUSION

Although each LECS treatment approach has its limitations, compared to traditional surgery, the resection of EGC is characterized by greater precision, reduced intraoperative bleeding, fewer adverse events, shorter hospital stays, higher rates of complete resection, and lower recurrence rates. By utilizing dual localization through gastroscopy and laparoscopy, this technique facilitates more reliable complete tumor resection and maximizes the preservation of healthy gastric wall tissue. Although challenges remain, these issues are expected to be progressively addressed through multidisciplinary collaboration, technological innovation, and standardized clinical research. In the future, LECS is anticipated to become a standard minimally invasive treatment option for EGC, providing patients with safer and more effective therapeutic outcomes.