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Review Current perspectives on combining endoscopy and minimally invasive surgery for upper gastrointestinal tumors
Eriko Koizumi1orcid, Osamu Goto2orcid

DOI: https://doi.org/10.5946/ce.2025.472
Published online: May 22, 2026

1Department of Gastroenterology, Nippon Medical School Graduate School of Medicine, Tokyo, Japan

2Department of gastroenterology, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo, Japan

Correspondence: Eriko Koizumi Department of Gastroenterology, Nippon Medical School, Graduate School of Medicine, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8603, Japan E-mail: e-koizumi@nms.ac.jp
• Received: December 28, 2025   • Revised: January 29, 2026   • Accepted: March 3, 2026

© 2026 Korean Society of Gastrointestinal Endoscopy

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Recent advances in endoscopy have expanded the therapeutic spectrum of minimally invasive gastrointestinal surgery. Several modified procedures have been developed to reduce the risk of bacterial contamination and tumor cell dissemination associated with intentional perforation in classical laparoscopic and endoscopic cooperative surgery (LECS), including inverted LECS and non-exposed approaches. Long-term outcomes of these procedures for gastric lesions have recently been reported, supporting their favorable safety and efficacy. Moreover, the incorporation of sentinel lymph node navigation into non-exposed techniques represents a promising strategy for function-preserving gastric cancer surgery, and recent phase III trials have begun to evaluate its clinical value and long-term outcomes. Additionally, endoscopic full-thickness resection has recently been gaining wider acceptance in Japan and is facilitated by staged strategies that integrate endoscopic resection with single-port placement. Combined endoscopic procedures have been applied to the pharynx, esophagus, and duodenum with excellent short-term outcomes; nonetheless, long-term data remain limited. Ongoing innovations and multicenter studies may refine indications, standardize techniques, and validate safety and efficacy. Overall, the integration of endoscopy and surgery is likely to become increasingly critical in achieving both oncological curability and organ preservation in the management of gastrointestinal tumors.
Minimally invasive surgery aims to reduce operative trauma while maintaining oncological and functional safety. In particular, minimally invasive gastrointestinal surgery has evolved from basic laparoscopic procedures to advanced hybrid endoscopic approaches. Compared with conventional open surgery, minimally invasive surgery confers several well-recognized benefits, including a reduced surgical stress response, lower complication rates, earlier return to oral intake, and improved postoperative quality of life.1-3
Gastric endoscopic submucosal dissection (ESD) is a cornerstone of minimally invasive therapy for gastrointestinal epithelial tumors. Established in the early 2000s as a less invasive alternative for early-stage gastric cancer, ESD has continued to evolve through advances in technique, dedicated devices, and novel instruments, and is now widely performed, including in community hospitals. Nevertheless, ESD has several intrinsic limitations. Although advances have reduced adverse events such as bleeding and perforation, three major limitations persist: (1) the procedure can remove only lesions confined to the submucosal layer, (2) specific anatomical locations remain technically challenging for endoscopic access, and (3) indications are inherently limited to tumors without lymph node metastasis.
To address these limitations, the concept of combined endoscopy, also referred to as collaborative surgery, has emerged. This strategy integrates flexible gastrointestinal endoscopy with surgical techniques, enabling the resection of both epithelial and subepithelial tumors (SETs). More than 15 years have passed since the original classical laparoscopic and endoscopic cooperative surgery (LECS) method was introduced in 2008, and numerous modified techniques have since been developed and applied clinically. Long-term outcomes have been reported for some procedures, supporting their clinical utility.
As a result, a wide variety of endoscopic–surgical hybrid techniques with different procedural concepts have been established, including exposed and non-exposed approaches (Table 1). In Western practice, the integration of endoscopy with minimally invasive surgery for upper gastrointestinal tumors is currently driven largely by device-enabled endoscopic full-thickness resection (EFTR). In contrast, in Asia, a broader spectrum of LECS-derived and non-exposure hybrid techniques has been developed and disseminated, reflecting different developmental pathways in minimally invasive upper gastrointestinal surgery (Table 2).
In this narrative review, we summarize current perspectives on combined endoscopic and surgical techniques for upper gastrointestinal tumors, focusing on their application according to anatomical region (Fig. 1).
Classical laparoscopic and endoscopic cooperative surgery
Classical LECS, regarded as the prototype for combined endoscopy and laparoscopy, was introduced by Hiki et al.4 in 2008 and was approved for insurance coverage in Japan in April 2014. The original technique involves local tumor resection performed jointly using laparoscopy and endoscopy, followed by laparoscopic closure of the gastric wall defect. Importantly, a multicenter retrospective study of 126 submucosal tumors demonstrated a 100% R0 resection rate and no recurrence during a median follow-up of 55 months.5 However, classical LECS requires intentional perforation, raising concerns regarding peritoneal contamination and, in ulcerated lesions, potential intraperitoneal tumor dissemination.
Previously, a study of intragastric washing cytology during ESD for gastric cancer by Ohki et al.6 found that cancer cells were detected in 58.0% of the lactated Ringer’s solution samples. Additionally, Goto et al.7 performed stamp cytology by pressing the surface of the specimens against glass slides; in the cancerous group (Papanicolaou class IV or V), CD44v9-positive cells were expressed in 34% of cases, indicating that in early gastric cancer or non-epithelial tumors showing epithelial changes, tumor cells can be detected in the gastric lavage fluid following endoscopic intervention and that perforation may lead to intraperitoneal tumor cell seeding.
Inverted laparoscopic and endoscopic cooperative surgery
To address concerns related to intentional perforation in classical LECS, inverted LECS was developed to reduce leakage of gastric contents. In this procedure, supporting sutures elevate the gastric wall surrounding the lesion toward the peritoneal cavity in a crown-like manner, thereby preventing the spillage of gastric juice.8 Although this remains an “open” technique and cannot fully eliminate the risk of tumor cell dissemination, a single-center series of 215 patients demonstrated favorable outcomes for gastric gastrointestinal stromal tumors (GISTs) with a median size of 30 mm, with 3-year overall and disease-specific survival rates of 98% and 100%, respectively.9
Combination of laparoscopic and endoscopic approaches for neoplasia with a non-exposure technique
A combination of laparoscopic and endoscopic approaches for neoplasia with a non-exposure technique (CLEAN-NET) has been proposed as a completely non-exposed local resection method, with extraluminal-growing type SETs being the best candidates for this technique. Specifically, in this technique, sufficient submucosal injection is performed endoscopically, the seromuscular layer is incised laparoscopically, the lesion is exteriorized, and resection is completed under laparoscopic visualization.10 Onimaru et al.11 previously reported that among 36 gastric SET cases measuring 15–63 mm in diameter, including 33 intraluminal-growing types, the R0 resection rate and postoperative complication rate were 100% and 2.8%, respectively, with no recurrence observed during a median follow-up period of 46 months.

1) Non-exposed endoscopic wall-inversion surgery

Developed contemporaneously with inverted LECS, non-exposed endoscopic wall-inversion surgery (NEWS) enables non-exposed full-thickness resection. The procedure begins with the insertion of one camera port and several trocars into the peritoneal cavity. Mucosal markings are created endoscopically, followed by laparoscopic serosal markings under endoscopic guidance. A submucosal injection is then performed, and the seromuscular layer is circumferentially incised along the serosal markings, followed by laparoscopic suturing of the seromuscular layer with inversion of the lesion into the lumen. Finally, circumferential mucosal and submucosal incisions are made endoscopically around the mucosal markings, and a full-thickness incision is completed. The lesion is retrieved transorally, and the mucosal defect is closed, completing the procedure.12,13 For submucosal tumors, extraluminal lesions can be readily removed by CLEAN-NET or wedge resection, whereas intraluminal or intramural lesions are better approached from the luminal side. In a cohort of 42 gastric submucosal tumors ≤3 cm, long-term follow-up demonstrated 100% overall survival, no recurrence, and preserved gastric function, including nutritional status and gastric emptying.14 For epithelial tumors, NEWS is particularly useful when ESD is technically challenging (e.g., because of severe fibrosis or a fundic location) and is key to sentinel lymph node navigation surgery for gastric cancer.

2) Non-exposed endoscopic full-thickness resection with simple suturing

An alternative procedure to NEWS for achieving non-exposed resection is non-exposed endoscopic full-thickness resection with simple suturing (NESS-EFTR), a technique introduced by Kim et al.15 in 2015 that enables non-exposed removal in a technically straightforward manner. Marking is performed from both the inside and outside of the stomach, and a circumferential incision of the mucosal layer is performed endoscopically, as in ESD. The seromuscular layer is sutured to invert the gastric wall, and EFTR is then completed, followed by endoscopic mucosal suturing with endoloops and clips.15 The technical outcomes of 20 cases of NESS-EFTR performed during sentinel lymph node navigation surgery for gastric cancer have been reported. The complete resection rate was 83.3%, and intraoperative perforation occurred in 27.8% of cases; this was manageable with endoscopic clipping, laparoscopic suturing, or stapling.16
Pure endoscopic full-thickness resection
Pure EFTR allows complete transmural resection using endoscopy alone. For retrieval of solid SETs, the tumor size suitable for EFTR should be <30 mm to maintain resection completeness and safety. Regarding tumor growth pattern, the intraluminal-growing type is a good indication for EFTR. With respect to location, the lesser curvature is considered the best indication because it results in less luminal collapse owing to the presence of connective tissue/omentum behind the gastric wall, and preservation of the vagal nerve may help prevent omentum-related complications and postoperative gastric dysmotility. In this technique, a solution is injected into the submucosa, and the circumferential mucosa around the lesion is incised. Subsequently, the submucosa is dissected around the tumor to expose the muscular attachment, followed by an intentional full-thickness muscle incision. Finally, the defect is closed, and the resected lesion is retrieved transorally. This approach has been most extensively developed in China, where a meta-analysis reported a 96.5% R0 resection rate for gastric submucosal tumors measuring 10–28 mm, with adverse events and surgical conversion in 1% and <1% of cases, respectively, and no recurrence within 12 months.17 In 2024, a prospective multicenter phase II trial in Japan demonstrated successful completion of the endoscopic procedure in 46 patients with intraluminal, nonulcerated gastric GISTs measuring 11–30 mm, achieving pathological R0 and adverse event rates of 77% and 2%, respectively, including one delayed perforation.18
As EFTR has gained wider clinical adoption, the need for an effective and reliable method for defect closure has increased. Various closure methods using endoclips, over-the-scope clips, and endoloop closure techniques, such as the reopenable-clip-over-the-line method, have been performed. Additionally, several closure devices, including endoscopic hand suturing, double-armed bar suturing, and the X-Tack and OverStitch systems, have been proposed.19-24 Each closure technique has both strengths and weaknesses with respect to factors such as maximum defect size, cost, technical difficulty, operating time, complication rate, and detachment rate. The most effective method for defect closure after EFTR has yet to be established.25
Endoscopic resection with one-port pneumoperitoneum
Japan has adopted a cautious approach to EFTR because of issues related to intraoperative management, technical difficulty, and concerns regarding reliable defect closure. Although EFTR was designated as Advanced Medical Technology A in 2020—an official Japanese system for procedures with established safety and promising clinical efficacy, in which the procedure itself is not reimbursed by public insurance, whereas standard perioperative care is covered—its clinical adoption remains limited.26 Accordingly, a stepwise strategy has been proposed, progressing from ESD to endoscopic resection with one-port pneumoperitoneum (EROPP) and ultimately to pure EFTR. In EROPP, a single laparoscopic observation port is introduced through the umbilicus to maintain pneumoperitoneum during endoscopic resection. Notably, this method offers two major advantages: (1) stable intra-abdominal pressure and (2) the ability to promptly convert to conventional laparoscopic surgery when necessary (Fig. 2).27
Sentinel lymph node navigation surgery
A key limitation of ESD is that it is restricted to lesions without lymph node metastasis. Standard gastrectomy with lymph node dissection, although curative, is frequently associated with postoperative functional impairments such as dumping syndrome. Consequently, function-preserving surgeries have gained increasing attention. The sentinel lymph node concept, which refers to the first node to receive lymphatic drainage from a tumor, has been used to guide minimally invasive surgery for gastric cancer. Non-exposed procedures such as NEWS and NESS-EFTR are often performed in conjunction with sentinel node navigation surgery (SNNS).15,28
Currently, multiple phase III trials are underway to assess the long-term efficacy of function-preserving gastrectomy, with a particular focus on SNNS. In Japan, a multicenter, non-randomized phase III study is comparing long-term outcomes and quality of life between SNNS and standard gastrectomy, with results expected in the near future. Moreover, in Korea, the SENORITA trial compared these two approaches in a randomized setting and did not demonstrate non-inferiority in 3-year disease-free survival. Nonetheless, disease-specific and overall survival rates were equivalent, and SNNS achieved superior quality-of-life scores. Furthermore, in China, a multicenter randomized trial is ongoing to evaluate the oncological safety of laparoscopic function-preserving versus standard gastrectomy (Table 3).29 Importantly, favorable results from these studies may promote the broader application of function-preserving gastric surgery, with combined endoscopic approaches becoming increasingly critical.
Palliative laparoscopic and endoscopic cooperative surgery
Over time, the indications for combined endoscopic–surgical approaches have expanded to include early gastric cancer and, more recently, selected cases of advanced disease in which curative resection is not feasible.30-32 Palliative LECS is aimed not at radical oncological clearance but at local control, alleviating symptoms such as bleeding or obstruction while minimizing operative trauma and maintaining quality of life, particularly in older or high-risk patients.
Nonetheless, intentional gastric wall perforation in classical LECS carries a risk of tumor seeding, necessitating the development of non-exposure variants. Technical difficulty near the esophagogastric junction or pylorus restricts applicability, and the oncological benefit is limited to symptom relief rather than curative intent. Nevertheless, as population aging progresses and the need for personalized surgical strategies increases, palliative LECS represents a promising middle ground between aggressive and non-operative management. Further prospective studies are warranted to clarify its indications, long-term outcomes, and impact on survival and quality of life.30-32
Endoscopic laryngopharyngeal surgery (ELPS) combined with ESD is performed for pharyngeal lesions to improve technical outcomes. ELPS is indicated for superficial squamous cell carcinomas of the oropharynx, hypopharynx, and larynx that are limited to the mucosa or superficial submucosa without lymph node metastasis; it is primarily applied to localized lesions (Tis–T1), for which preservation of swallowing and phonatory functions is feasible. In ELPS combined with ESD, under general anesthesia with endotracheal intubation, the larynx is exposed, and tumors are resected using a flexible endoscope in combination with otolaryngologic instruments. This approach is useful at sites that are difficult to treat with ELPS alone, particularly for large lesions, because traction can be applied by grasping the lesion with otolaryngologic instruments. Additionally, narrow-band imaging during endoscopic observation enables more accurate lesion marking. A systematic review of 161 cases identified subcutaneous emphysema, aspiration pneumonia, and bleeding as the most frequent adverse events, with an overall R0 resection rate of 77%.33 Recent long-term studies have demonstrated excellent oncological outcomes, with 1-year overall and disease-specific survival rates of 92%–98% and 95%–100%, respectively.34-41 However, Yamaguchi et al.42 reported metachronous lesions in 26.6% of patients within 3 years after ELPS. Furthermore, the potential development of secondary esophageal carcinoma warrants particular vigilance, and appropriate surveillance is essential.
Thoracoscopic–endoscopic cooperative surgery
For esophageal tumors, thoracoscopic–endoscopic cooperative surgery (TECS) combines submucosal tunneling endoscopic resection with thoracoscopic assistance to treat large esophageal leiomyomas.43,44 Introduced as a relevant procedure in 2016, thoracoscopic–endoscopic submucosal tunneling involves submucosal dissection around the tumor using peroral endoscopic myotomy techniques, followed by endoscopic entry into the thoracic cavity and division of the muscle layer under thoracoscopic guidance.45 Recently, in addition to subepithelial lesions, several technically successful cases of TECS for gastric tube cancer after esophagectomy have been reported.46-48 At present, the accumulation of TECS cases remains insufficient for both epithelial and non-epithelial tumors, and further procedural refinement and evidence accumulation remain future challenges.
Duodenal endoscopic submucosal dissection
For superficial non-ampullary duodenal epithelial tumors (SNADETs), endoscopic treatment with cold snare polypectomy, endoscopic mucosal resection, and ESD is increasingly performed. Similar to gastric epithelial tumors, lesions extending to the superficial submucosal layer without possible lymph node metastasis are the best candidates for endoscopic treatment. According to lesion size, SNADETs measuring <5–10 mm without malignant features, <15–20 mm, and >15–20 mm are resected by cold snare polypectomy, endoscopic mucosal resection, and duodenal ESD, respectively. Duodenal ESD remains technically challenging because the duodenal wall is thin, and exposure to bile and pancreatic juice increases the risk of perforation and bleeding. A systematic review involving 3672 duodenal ESD cases for SNADET reported en bloc resection, R0 resection, intraprocedural perforation, intraprocedural bleeding, delayed perforation, and delayed bleeding rates of 98.1%, 86.3%, 8.5%, 0.01%, 2.0%, and 3.8%, respectively.49 To mitigate postprocedural complications, complete endoscopic closure of the mucosal defect and placement of nasobiliary and nasopancreatic drainage tubes are often performed.
Duodenal laparoscopic and endoscopic cooperative surgery
Duodenal LECS (D-LECS) is a combined endoscopic–laparoscopic approach designed to address the limitations of duodenal ESD. Laparoscopic assistance enhances endoscopic maneuverability and enables reliable defect closure, thereby preventing severe postoperative complications. This technique is often performed for relatively large SNADETs and duodenal subepithelial lesions, such as neuroendocrine tumors; nonetheless, it also represents a stepwise strategy for introducing duodenal ESD. A multicenter retrospective study reported R0 resection, intraoperative complication, and postoperative complication rates of 95.1%, 7.3%, and 4.4%, respectively.50 Regarding the comparison between duodenal ESD and D-LECS, a retrospective comparative study of 113 patients with SNADETs measuring >10 mm evaluated the outcomes of duodenal ESD and LECS. Both procedures achieved 100% en bloc resection, and the curative resection rates were comparable (93.0% vs. 77.0%). There were no significant differences in adverse events (7.0% vs. 23.1%) or 3-year overall survival (97.6% vs. 100%). Therefore, both ESD and D-LECS may be acceptable and effective treatment options for SNADETs, with high survival and low recurrence rates.51
Recent advances in combined endoscopy have expanded the therapeutic scope of minimally invasive gastrointestinal surgery. Non-exposed procedures, including NEWS and NESS-EFTR, enable full-thickness resection while minimizing the risk of peritoneal contamination, thereby providing curative potential for lesions that have been unsuitable for endoscopic treatment alone. In addition, the integration of sentinel lymph node navigation into these non-exposed procedures represents a promising step toward function-preserving and oncologically safe gastric cancer surgery. Minimally invasive approaches have also been applied to the pharynx, esophagus, and duodenum, where conventional ESD is technically demanding. Accumulating evidence indicates high en bloc and R0 resection rates with these procedures. Future efforts should prioritize the standardization of indications, refinement of closure and suturing devices, and the accumulation of multicenter prospective data to validate long-term safety and efficacy. As technology and expertise continue to evolve, combined endoscopy is expected to play an increasingly central role in achieving both radical cure and organ preservation in the management of gastrointestinal tumors.
Fig. 1.
Positions of the instruments in each representative laparoscopic and endoscopic cooperative surgery procedure. The positions of the procedures and the instruments used differed for each procedure. (A) Cooperative laparoscopic and endoscopic surgery. (B) Cooperative thoracoscopic and endoscopic surgery. (C) Endoscopic laryngopharyngeal surgery (ELPS) with endoscopic submucosal dissection (ESD). (D) Duodenal laparoscopic and endoscopic cooperative surgery. e. Actual performance of ELPS with ESD by otolaryngologists and endoscopists.
ce-2025-472f1.jpg
Fig. 2.
A case of endoscopic resection with one-port placement. (A) A 5-mm camera port was inserted through the umbilicus. (B) A 20-mm gastrointestinal stromal tumor in the greater curvature of the upper body that grew into the lumen. (C, D) Mucosal resection and submucosal dissection surrounding the tumor were performed endoscopically. (E, F) The procedure was completed, and the lesion was retrieved transorally. (G, H) In this case, the defect was closed using endoscopic hand suturing.
ce-2025-472f2.jpg
Table 1.
Comparison of representative techniques for upper gastrointestinal tumors
Technique Core concept Exposure to peritoneal cavity Typical indications Full-thickness resection Closure method Key advantages Main limitations
Classical LECS Intentional perforation after endoscopic mucosal incision, followed by laparoscopic full-thickness resection Exposed Gastric SETs (mainly intraluminal growth) Yes Laparoscopic stapling or suturing Simple and reliable; accurate tumor localization Risk of peritoneal contamination and intraperitoneal tumor dissemination
Inverted LECS Tumor inverted toward gastric lumen (“crown method”) during laparoscopic resection Reduced exposure Gastric SETs Yes Laparoscopic suturing or stapling Lower risk of contamination and tumor dissemination than classical LECS Not completely non-exposed; technically demanding
CLEAN-NET Laparoscopic seromuscular dissection with endoscopic guidance without opening gastric mucosa Non-exposed Gastric SETs; selected epithelial lesions Functional full-thickness Laparoscopic suturing or stapling Avoids contamination and tumor dissemination Limited by tumor size and location
NEWS Circumferential seromuscular incision and inversion, followed by endoscopic mucosal incision and intraluminal retrieval Non-exposed Gastric SETs; highly selected early gastric cancers Yes Laparoscopic seromuscular suturing ± endoscopic closure Complete non-exposure; oncologically favorable Technically complex; limited indications
NESS-EFTR Non-exposure EFTR using simple laparoscopic suturing Non-exposed Gastric lesions requiring full-thickness resection Yes Simple laparoscopic suturing Simplified non-exposed concept Limited clinical evidence; technique variability
Pure EFTR Endoscopic full-thickness resection with intentional perforation Exposed Gastric SETs; selected epithelial lesions Yes Endoscopic closure Flexible and adaptable approach Risk of contamination and tumor dissemination; secure closure required
EROPP Endoscopic resection combined with one-port laparoscopic support Variable Upper gastrointestinal lesions requiring safe closure or backup Variable Endoscopic closure ± laparoscopic closure Minimally invasive “safety-net” strategy Not standardized; limited data

LECS, laparoscopic and endoscopic cooperative surgery; SETs, subepithelial tumors; CLEAN-NET, combination of laparoscopic and endoscopic approaches for neoplasia with a non-exposure technique; NEWS, non-exposed endoscopic wall-inversion surgery; NESS-EFTR, non-exposed endoscopic full-thickness resection with simple suturing; EROPP, endoscopic resection with one-port pneumoperitoneum.

Table 2.
Current status of combining endoscopy and minimally invasive surgery for upper gastrointestinal tumors in Asia and Western countries
Aspect Asia Western countries
Clinical adoption More widely adopted in high-volume centers Limited to selected expert centers
Main approaches LECS-derived and non-exposure hybrid techniques Device-enabled endoscopic full-thickness resection
Typical target lesions Gastric subepithelial tumors; selected epithelial tumors Small, size-limited lesions; mainly epithelial or subepithelial tumors
Role of surgery Close collaboration between endoscopists and surgeons Often performed by endoscopists alone using dedicated devices
Conceptual focus Technique development to reduce contamination and tumor dissemination Feasibility and safety using standardized devices
Evidence profile Broader accumulation of technique-oriented clinical reports Mainly device-driven case series and multicenter registries
Current limitations Technical complexity; limited long-term oncological data Lesion size limitations; restricted indications

LECS, laparoscopic and endoscopic cooperative surgery.

Table 3.
The phase III trials on minimally invasive surgery for gastric cancer
Study number Author/status Country Randomization Comparison arms Criteria No. of cases Primary endpoint Secondary endpoint
NCT01804998 Kim et al.29 Korea Randomized LSNNS vs. LSG with D1 dissection cT1N0M0 <3 cm 580 3-Year disease-free survival rate: non-inferiority unproven QOL: SNNS>LSG, nutritional status: SNNS>LSG
UMIN000014401 In progress Japan Non-randomized SNNS vs. routine gastrectomy with D2 dissection cT1N0M0 <4 cm 225 5-Year recurrence-free survival rate QOL, nuturitional status
NCT05160753 In progress China Randomized Laparoscopic function-preserving gastrectomy vs. routine gastrectomy with D2 dissection cT1N0M0 <4 cm 580 3-Year disease-free survival rate QOL, nuturitional status

LSNNS, laparoscopic sentinel lymph node surgery; LSG, laparoscopic standard gastrectomy; QOL, quality of life.

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      Current perspectives on combining endoscopy and minimally invasive surgery for upper gastrointestinal tumors
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      Fig. 1. Positions of the instruments in each representative laparoscopic and endoscopic cooperative surgery procedure. The positions of the procedures and the instruments used differed for each procedure. (A) Cooperative laparoscopic and endoscopic surgery. (B) Cooperative thoracoscopic and endoscopic surgery. (C) Endoscopic laryngopharyngeal surgery (ELPS) with endoscopic submucosal dissection (ESD). (D) Duodenal laparoscopic and endoscopic cooperative surgery. e. Actual performance of ELPS with ESD by otolaryngologists and endoscopists.
      Fig. 2. A case of endoscopic resection with one-port placement. (A) A 5-mm camera port was inserted through the umbilicus. (B) A 20-mm gastrointestinal stromal tumor in the greater curvature of the upper body that grew into the lumen. (C, D) Mucosal resection and submucosal dissection surrounding the tumor were performed endoscopically. (E, F) The procedure was completed, and the lesion was retrieved transorally. (G, H) In this case, the defect was closed using endoscopic hand suturing.
      Current perspectives on combining endoscopy and minimally invasive surgery for upper gastrointestinal tumors
      Technique Core concept Exposure to peritoneal cavity Typical indications Full-thickness resection Closure method Key advantages Main limitations
      Classical LECS Intentional perforation after endoscopic mucosal incision, followed by laparoscopic full-thickness resection Exposed Gastric SETs (mainly intraluminal growth) Yes Laparoscopic stapling or suturing Simple and reliable; accurate tumor localization Risk of peritoneal contamination and intraperitoneal tumor dissemination
      Inverted LECS Tumor inverted toward gastric lumen (“crown method”) during laparoscopic resection Reduced exposure Gastric SETs Yes Laparoscopic suturing or stapling Lower risk of contamination and tumor dissemination than classical LECS Not completely non-exposed; technically demanding
      CLEAN-NET Laparoscopic seromuscular dissection with endoscopic guidance without opening gastric mucosa Non-exposed Gastric SETs; selected epithelial lesions Functional full-thickness Laparoscopic suturing or stapling Avoids contamination and tumor dissemination Limited by tumor size and location
      NEWS Circumferential seromuscular incision and inversion, followed by endoscopic mucosal incision and intraluminal retrieval Non-exposed Gastric SETs; highly selected early gastric cancers Yes Laparoscopic seromuscular suturing ± endoscopic closure Complete non-exposure; oncologically favorable Technically complex; limited indications
      NESS-EFTR Non-exposure EFTR using simple laparoscopic suturing Non-exposed Gastric lesions requiring full-thickness resection Yes Simple laparoscopic suturing Simplified non-exposed concept Limited clinical evidence; technique variability
      Pure EFTR Endoscopic full-thickness resection with intentional perforation Exposed Gastric SETs; selected epithelial lesions Yes Endoscopic closure Flexible and adaptable approach Risk of contamination and tumor dissemination; secure closure required
      EROPP Endoscopic resection combined with one-port laparoscopic support Variable Upper gastrointestinal lesions requiring safe closure or backup Variable Endoscopic closure ± laparoscopic closure Minimally invasive “safety-net” strategy Not standardized; limited data
      Aspect Asia Western countries
      Clinical adoption More widely adopted in high-volume centers Limited to selected expert centers
      Main approaches LECS-derived and non-exposure hybrid techniques Device-enabled endoscopic full-thickness resection
      Typical target lesions Gastric subepithelial tumors; selected epithelial tumors Small, size-limited lesions; mainly epithelial or subepithelial tumors
      Role of surgery Close collaboration between endoscopists and surgeons Often performed by endoscopists alone using dedicated devices
      Conceptual focus Technique development to reduce contamination and tumor dissemination Feasibility and safety using standardized devices
      Evidence profile Broader accumulation of technique-oriented clinical reports Mainly device-driven case series and multicenter registries
      Current limitations Technical complexity; limited long-term oncological data Lesion size limitations; restricted indications
      Study number Author/status Country Randomization Comparison arms Criteria No. of cases Primary endpoint Secondary endpoint
      NCT01804998 Kim et al.29 Korea Randomized LSNNS vs. LSG with D1 dissection cT1N0M0 <3 cm 580 3-Year disease-free survival rate: non-inferiority unproven QOL: SNNS>LSG, nutritional status: SNNS>LSG
      UMIN000014401 In progress Japan Non-randomized SNNS vs. routine gastrectomy with D2 dissection cT1N0M0 <4 cm 225 5-Year recurrence-free survival rate QOL, nuturitional status
      NCT05160753 In progress China Randomized Laparoscopic function-preserving gastrectomy vs. routine gastrectomy with D2 dissection cT1N0M0 <4 cm 580 3-Year disease-free survival rate QOL, nuturitional status
      Table 1. Comparison of representative techniques for upper gastrointestinal tumors

      LECS, laparoscopic and endoscopic cooperative surgery; SETs, subepithelial tumors; CLEAN-NET, combination of laparoscopic and endoscopic approaches for neoplasia with a non-exposure technique; NEWS, non-exposed endoscopic wall-inversion surgery; NESS-EFTR, non-exposed endoscopic full-thickness resection with simple suturing; EROPP, endoscopic resection with one-port pneumoperitoneum.

      Table 2. Current status of combining endoscopy and minimally invasive surgery for upper gastrointestinal tumors in Asia and Western countries

      LECS, laparoscopic and endoscopic cooperative surgery.

      Table 3. The phase III trials on minimally invasive surgery for gastric cancer

      LSNNS, laparoscopic sentinel lymph node surgery; LSG, laparoscopic standard gastrectomy; QOL, quality of life.


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