Abstract
- Recent advances have been made in minimally invasive treatments for benign tumors, borderline malignant tumors, and early gastric cancer (EGC). Laparoscopic and endoscopic cooperative surgery (LECS) combines laparoscopic and endoscopic approaches performed simultaneously, thereby maximizing the advantages of each modality while overcoming the individual limitations. Consequently, LECS enables precise tumor localization, complete resection with minimal margins, a reduced recovery time, and improved clinical outcomes. The primary indications for LECS include the resection of gastrointestinal stromal tumors and various benign submucosal tumors, and its application has recently been extended to select EGC cases. In South Korea, the Ministry of Health and Welfare has approved LECS as a new medical technology for gastrointestinal tumors in 2024. Several LECS techniques have been developed, including classical LECS, inverted LECS, laparoscopy-assisted endoscopic full-thickness resection, non-exposed endoscopic wall-inversion surgery, a combination of laparoscopic and endoscopic approaches for neoplasia with a non-exposure technique, and closed LECS. Above all, close cooperation between laparoscopic and endoscopic teams is essential for the successful performance of LECS procedures.
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Keywords: Cooperative; Endoscopy; Laparoscopy; Technology
INTRODUCTION
Intraoperative endoscopy is widely used during surgery to identify lesion location and margins, as well as bleeding points, and can be regarded as the starting point for combined laparoscopic and endoscopic procedures. Natural orifice transluminal endoscopic surgery (NOTES) is a minimally invasive approach in which endoscopic instruments reach the peritoneal or thoracic cavity via natural body openings, including oral and anal routes. Due to the technical constraints inherent to conventional NOTES, endoscopic procedures are frequently combined with laparoscopic techniques, an approach known as hybrid NOTES.1 Recently, significant advances have been achieved in minimally invasive treatments for benign tumors, borderline malignant tumors, and early gastric cancer (EGC). Tumors that previously required open surgery can now be resected endoscopically using new techniques, such as endoscopic mucosal resection, endoscopic submucosal dissection (ESD), and endoscopic full-thickness resection (EFTR). At the same time, advances in laparoscopic surgery have enabled many lesions that were once treated by open surgery to be managed using minimally invasive laparoscopic approaches.2 Laparoscopic and endoscopic cooperative surgery (LECS) refers to a surgical technique that integrates laparoscopic and endoscopic methods, which are performed concurrently, integrating intraluminal endoscopic procedures with intraperitoneal laparoscopic surgery. This cooperation enhances the advantages of each technique while overcoming their respective limitations. Consequently, LECS allows precise tumor localization, complete tumor resection with minimal margins, reduced recovery time, and improved clinical outcomes. Owing to its ability to integrate endoscopic mucosal and submucosal dissection with laparoscopic seromuscular resection, LECS demonstrates high efficacy in the management of tumors arising in anatomically complex regions.3 The concept of LECS was first proposed by Hiki et al.4 in 2008 as an innovative combined laparoscopic and endoscopic approach for resecting gastric submucosal tumors. This technique enabled precise tumor localization and tumor resection with maximal preservation of the surrounding normal gastric mucosa, thereby overcoming the limitations of conventional laparoscopic techniques. This approach was subsequently termed classical LECS.5 LECS has also been described by various names, including laparoscopic–endoscopic rendezvous surgery, combined laparoscopic and endoscopic surgery, and hybrid laparoscopic surgery.2
CLASSIFICATION OF LECS
LECS involves cooperative laparoscopic and EFTR and is most commonly performed in the stomach. Based on the sequence of surgical steps, LECS can be broadly classified into two categories: “cut first and suture” and “suture first and cut”.1 The “cut first and suture” technique involves initial tumor resection followed by closure of the gastric wall. This category includes classical LECS, laparoscopy-assisted endoscopic full-thickness resection (LAEFR), and inverted LECS. Although these techniques have a long history, the tumor and gastric mucosa are exposed to the peritoneal cavity and adjacent organs during the procedure, which poses a potential risk of tumor cell dissemination and leakage of gastric contents into the peritoneal cavity. In contrast, the “suture first and cut” technique involves initial laparoscopic suturing performed on the serosal surface of the stomach, resulting in inversion of the gastric wall containing the tumor into the gastric lumen. Once inverted, the lesion was endoscopically resected, and the specimen was subsequently retrieved transorally. These measures effectively reduce the risks of tumor cell dissemination and peritoneal contamination from gastric contents. The lack of direct tumor exposure to the peritoneal cavity has led to the description of this approach as a non-exposure technique. Non-exposed endoscopic wall-inversion surgery (NEWS) was introduced as the first technique based on a “suture first and cut” concept.6
ADVANTAGES OF LECS
LECS offers several advantages by combining the strengths of laparoscopy and endoscopy, particularly in complex cases in which the limitations of each modality alone can be overcome. One of the major advantages of LECS is the accurate identification and localization of lesions. When endoscopy-assisted laparoscopic resection was performed using laparoscopy alone for visual exploration and palpation, tumor identification and localization were possible in 21 of 93 patients (22.6%). However, when endoscopy was combined with laparoscopy to provide an endoscopic endoluminal view, accurate tumor localization was achieved in 92 of the 93 patients (98.9%). This represents a fivefold increase in the tumor detection rate compared with laparoscopy alone and is comparable to the detection rate achieved with open surgery.7 Compared with laparoscopic wedge resection, another important advantage of LECS is the ability to directly visualize the tumor intraluminally during resection. This allows minimal resection of the surrounding normal tissue, thereby reducing postoperative gastric deformities. This benefit is particularly valuable for tumors with intraluminal growth patterns.8
INDICATIONS FOR LECS
The primary indication for LECS is the resection of gastrointestinal stromal tumors (GISTs), which account for approximately 82% of the cases, followed by the resection of various benign submucosal tumors. More recently, LECS has been extended to the treatment of selected EGC cases.2 In GISTs measuring less than 5 cm, laparoscopic resection is considered safe when performed by experienced surgeons, independent of tumor location, provided that oncologically appropriate conditions, including margin-negative resection, preservation of the tumor capsule, and avoidance of spillage, are met.9 Accordingly, gastric GISTs <5 cm are regarded as suitable candidates for LECS, regardless of tumor location. This technique is particularly useful for small, endophytic gastric tumors that are difficult to visualize using laparoscopy alone.5 LECS is now considered applicable to a wider range of lesions, including ulcerated gastric submucosal tumors and EGC confined to the mucosa (T1a) without lymph node metastasis, regardless of location.10 Various non-exposure LECS techniques have been developed to reduce the risk of tumor cell dissemination into the peritoneal cavity in patients with EGC. These techniques are particularly beneficial for lesions that are challenging to manage with ESD, including large intramucosal lesions located at the greater curvature of the gastric body or fornix, as well as lesions with severe ulcer-related scarring.2,10 In South Korea, LECS was approved as a “new medical technology for gastrointestinal tumors” in 2024 by the Ministry of Health and Welfare.3 With this official recognition, LECS is expected to play an increasingly important role as an advanced minimally invasive surgery in the treatment of tumors.
VARIOUS METHODS OF LECS
Classical LECS
Classical LECS is the first LECS technique to be developed and follows the “cut first and suture” approach (Fig. 1).3,7
1) Endoscopic submucosal incision
First, the lesion was identified by endoscopy and laparoscopy. Endoscopy was used to visualize the tumor, and coagulation markings were placed with a 0.5 cm safety margin around the lesion. A circumferential submucosal incision was then made using the ESD technique. Subsequently, an artificial perforation was created in the gastric wall by gently pushing a needle knife through the incision site.
2) Laparoscopic seromuscular incision
A laparoscopic seromuscular incision was made at the perforation site by inserting the tip of an ultrasonically activated device along the circumferential mucosal incision line. As much of the tumor circumference as possible was incised through the full-thickness of the gastric wall. The remaining tumor was elevated in the peritoneal cavity and was completely removed. The vessels surrounding the excision line were controlled by using an ultrasonically activated laparoscopic device.
3) Closure of the incision line
After tumor removal, the gastric wall defect was laparoscopically repaired. Closure is typically achieved using a laparoscopic stapling device; however, laparoscopic hand suturing is favored when the tumor is located near the esophagogastric junction (EGJ) or the pylorus. Following resection, the specimens were collected in specimen bags for retrieval. Finally, endoscopy was performed with gastric insufflation to conduct an air leakage test and confirm the absence of bleeding or postoperative strictures at the resection site.8
Inverted LECS
The inverted LECS was developed by Nunobe et al.10 to prevent intraperitoneal spill and contamination of gastric juice and to minimize tumor contact with surrounding tissues. After the resection margin is defined by endoscopic mucosal incision, several sutures are placed in the gastric wall around the tumor to circumferentially elevate the lesion in a crown-like manner. Each stitch is elevated and fixed to the abdominal wall. After adequate lesion exposure, a full-thickness incision was made using a combination of endoscopic and laparoscopic techniques. Because the lesion was circumferentially lifted, a full-thickness incision was made to direct the tumor into the intragastric cavity, reducing gastric juice contamination and abdominal wall contact. Once the tumor was completely resected, it was released into the gastric cavity and retrieved orally via endoscopy. However, because this technique still requires opening the gastric wall during the procedure, there remains a slight risk of gastric content contamination.
LAEFR
As reported by Abe et al.,11 LAEFR offers the advantage of allowing an appropriately small resection margin because the full-thickness excision of gastric lesions is performed under direct endoscopic visualization. The procedure begins with a submucosal incision around the tumor using endoscopy. Under laparoscopic guidance, intentional perforation of the gastric wall was performed. Subsequently, laparoscopic retraction was performed on the serosal aspect of the gastric wall containing the tumor, and an endoscopic full-thickness incision was made along approximately three-quarters of the previously established circumferential submucosal incision line. Laparoscopic dissection of the remaining seromuscular layer was performed for complete tumor removal, after which the gastric wall defect was repaired using laparoscopic suturing.
NEWS
The NEWS technique was developed to achieve full-thickness resection without tumor exposure to prevent peritoneal seeding of tumors and is primarily intended for the treatment of epithelial neoplasia such as EGC (Fig. 2).6 First, circumferential mucosal markings are created around the lesion under endoscopic guidance. The corresponding serosal markings were made laparoscopically using endoscopic navigation. Subsequently, a circumferential submucosal injection of sodium hyaluronate–indigo carmine solution was administered around the lesion under endoscopic guidance. The seromuscular layer was laparoscopically incised along the serosal markings. The incised seromuscular layers were linearly sutured, resulting in the inversion of the lesion into the gastric lumen. Before completion of the seromuscular suturing, a surgical sponge was inserted between the suture line and the serosal surface of the inverted lesion. This sponge provides countertraction to the mucosa and facilitates subsequent endoscopic procedures. Finally, circumferential mucosal and submucosal incisions were made endoscopically around the inverted lesion to achieve a complete resection. The resected specimen and spacer were retrieved orally, and the mucosal defect was closed using endoscopic clips (Fig. 2). The major advantage of NEWS is that precise tumor resection can be achieved by the direct visualization of both the mucosal and serosal layers using endoscopy and laparoscopy. However, a limitation of NEWS is the size of tumors that can be resected; submucosal tumors must be ≤30 mm in diameter because the resected specimen must be retrieved per orally. In addition, the operative time for NEWS is relatively long.6
Combination of laparoscopic and endoscopic approaches for neoplasia with a non-exposure technique
Combination of laparoscopic and endoscopic approaches for neoplasia with a non-exposure technique (CLEAN-NET), proposed by Inoue et al.,12 enables tumor removal while preserving mucosal continuity of the stomach, which serves as a barrier during the procedure (Fig. 3). This approach represents a non-exposure full-thickness resection technique in which resection is carried out following incision of the seromuscular layer. First, the tumor was identified endoscopically, and coagulation markings were placed with a 10 mm outer margin around the lesion. Subsequently, four full-thickness sutures were placed laparoscopically around the tumor to achieve fixation between the mucosal and seromuscular layers. Under endoscopic guidance, submucosal injection was performed around the sutures to create a circumferential submucosal fluid cushion. Subsequently, laparoscopic dissection of the seromuscular layer was performed along the external aspect of the four full-thickness stay sutures. Next, stay sutures fixed to the tumor were pulled within the peritoneum, drawing the full layer of the gastric wall, including the mucosa. At this stage, the integrity of the mucosal layer serves as a barrier, preventing contamination of the peritoneal cavity by the gastric contents. Finally, a full-thickness specimen containing the lesion was resected and sealed by laparoscopic stapling. The advantage of the CLEAN-NET procedure is that full-thickness resection of the wall can be achieved using a non-exposure technique. However, this technique becomes technically challenging when the lesion is situated on the posterior wall of the upper third of the stomach or cardia. In addition, because the incision line is defined on the serosal surface of the stomach, identifying an adequate resection margin can be difficult, particularly for epithelial neoplasms such as EGC, compared with other modified LECS procedures.8
Closed-LECS
Kikuchi et al.13 introduced closed-LECS as a non-exposure full-thickness resection technique (Fig. 4). In this procedure, the tumor is initially identified endoscopically, followed by placement of mucosal markings around the lesion. A circumferential submucosal incision was endoscopically made along the outer margin of the marked area. Using endoscopic light as a guide, corresponding serosal markings were created along the submucosal incision line. Seromuscular sutures were then placed, with a surgical sponge spacer positioned at the center of a previously marked serosal area. This maneuver results in inversion of the marked lesion and sponge spacer into the gastric lumen. Endoscopic circumferential seromuscular dissection was completed in the final step, followed by peroral extraction of the resected specimen and a sponge spacer. Closed LECS allows the determination of an appropriate resection line under direct endoscopic visualization, which is a major advantage of this technique. One limitation is tumor size; because the specimen must be retrieved per orally, gastric submucosal tumors are generally limited to ≤30 mm in diameter. However, for EGC, lesions >30 mm can also be resected using this technique.8
CONSIDERATIONS FOR LECS PROCEDURES
Recently, ESD has been increasingly performed for submucosal tumors such as GISTs. During ESD for GISTs, special care must be taken to avoid the risks of positive resection margins, tumor spillage, and perforation.5 In addition, traditional LECS methods, such as classical LECS and LAEFR, require intentional gastric perforation during the procedure. Therefore, the risks of leakage of gastric contents into the peritoneal cavity, abdominal infection, and extraluminal tumor seeding via gastric juices must be carefully considered. To overcome these limitations, several modified LECS techniques have been proposed. These include inverted LECS, an improvement over the classical LECS technique, and newly developed non-exposure techniques that enable complete tumor resection without gastric perforation. These non-exposure techniques include NEWS, CLEAN-NET, and closed LECS. These advanced techniques offer the benefit of reducing the risk of gastric juice and peritoneal tumor contamination. These technical innovations have expanded the clinical application of LECS. However, non-exposure techniques are associated with increased procedural complexity, longer operative times, and limitations regarding the recommended tumor size.5 The selection of the LECS technique largely depends on the experience and expertise of the multidisciplinary team. LECS reduces the technical difficulty for both endoscopists and laparoscopic surgeons, and close cooperation allows immediate management of any adverse events that may occur during the procedure.2 Because each LECS technique has distinct advantages and disadvantages, the optimal approach should be selected based on pathology, location, size of the tumor, and the technical complexity of the procedure.
Tumor location
The choice of the LECS technique is closely related to the tumor location. Most LECS approaches are used for lesions located in the greater curvature of the stomach. However, special caution is required for lesions located in the EGJ, lesser curvature, fundus, and pylorus. For lesions located at the EGJ, lesser curvature, and pylorus, LAEFR, NEWS, and closed LECS are suggested, and laparoscopic hand suturing is preferred over stapling to achieve greater precision.5 For lesions located on the posterior wall of the stomach, the CLEAN-NET technique is technically challenging, as it is difficult to identify the resection line and apply traction to the lesion.14 In addition, an inward-growing tumor of the stomach is often difficult to visualize using laparoscopy alone; therefore, endoscopic evaluation before LECS is helpful. Tumors located close to the EGJ or pyloric ring are associated with the risk of postoperative stricture formation. Endoscope-assisted laparoscopic transgastric resection (EATR) is a technique in which the gastric wall is opened laparoscopically, and gastric lesions are resected under direct endoscopic visualization.15 When selecting between endoscope-assisted laparoscopic wedge resection (EAWR) and EATR based on lesion characteristics, EATR is preferred for endophytic submucosal tumors ≤2 cm located on the posterior gastric wall or on the lesser curvature, whereas EAWR is applicable to the majority of other lesions.16 Tsujimoto et al.17 reported that all tumors could be resected using LECS, including prepyloric lesions located within 10 mm of the pyloric ring and lesions located 10–15 mm from the EGJ. Regarding selection of the ideal LECS technique based on tumor features, Tagaya et al.18 suggested that EAWR is more ideal for tumors on the anterior wall and exophytic tumors, whereas EATR is more suitable for tumors less than 4 cm and located on the posterior wall.
Tumor size
Tumor size is a critical factor in the selection of operative techniques for submucosal tumors, including GISTs. According to the National Comprehensive Cancer Network (NCCN), surgical resection is recommended for GISTs measuring 2 cm or larger. In addition, laparoscopic wedge resection is suggested for GISTs ≤5 cm.9 However, when the tumor is large, postoperative deformity of the remnant stomach may occur in some patients, potentially leading to stenosis or gastroparesis. Although laparoscopic wedge resection is a relatively simple and effective treatment option for GISTs, it requires wide resection margins of 1–2 cm from the tumor.19 In contrast, the use of LECS in the treatment of GISTs allows precise delineation of tumor margins, thereby enabling reduction of the resection margin. For wedge resection using a linear stapler, the resulting gastric wall defect is typically more than three times the size of the tumor.20 However, LECS results in a gastric wall defect of less than 1.5 times the tumor size, significantly reducing the risk of gastric deformity or stenosis. Furthermore, because an endoscopic incision is performed under direct visualization of the tumor margin, a more accurate incision line can be established compared with an extraluminal approach.17
Complications of LECS
The overall complication rate of laparoscopic interventions ranges from 0% to 14.0%, including bleeding, infection, anastomotic leakage, luminal stenosis, gastroparesis, and postoperative pneumonia.5 The complication rate for endoscopic procedures varies between 0% and 26.7%, with common issues including bleeding, perforation, and infection.5 LECS has an overall complication rate ranging from 0% to 10%, which is comparable to laparoscopic resection, with common complications including postoperative infection, hemorrhage, pneumonia, and gastroparesis.21 The relatively low complication rate of LECS may be attributed to the ability to perform leakage tests during the procedure, which is not feasible in pure laparoscopic resections, as well as to confirm precise resection and the absence of bleeding along the inner staple line under endoscopic visualization.21
CONCLUSIONS
LECS has been extensively applied in the management of benign gastroduodenal tumors and GISTs, as well as in the treatment of EGC. By integrating the advantages of laparoscopy and endoscopy, LECS overcomes the procedural limitations of laparoscopy alone, particularly in anatomically challenging locations and the management of small or endophytic gastric tumors. Successful LECS procedures require close collaboration between the laparoscopic and endoscopic teams. Such cooperation not only facilitates smooth performance of the procedure but also enables prompt management of adverse events and sharing of the technical burden. LECS has recently been officially recognized in South Korea as a new medical treatment for gastrointestinal tumors, and its indications have expanded to include selected cases of EGC. Accordingly, LECS is expected to play an increasingly important role as an advanced, minimally invasive surgical approach for tumor treatment. Although numerous refined modifications of LECS have been introduced, increased procedural complexity, prolonged operative time, and restrictions regarding recommended tumor size limit its broader adoption. The optimal technique should be selected based on tumor pathology, location, size, and technical complexity of the procedure. Future prospective studies are expected to provide robust evidence regarding the therapeutic efficacy of various LECS techniques for the management of gastroduodenal tumors, including EGC. Recently, third-space robotic and endoscopic cooperative surgery has been introduced as a novel approach combining laparoscopic robotic surgery with endoscopic methods and has demonstrated better outcomes, shorter operative times, reduced postoperative recovery times, and lower complication rates than conventional LECS, generating considerable interest.22
Conflicts of Interest
Jeong Seop Moon is currently serving as a publication committee member in Clinical Endoscopy; however, he was not involved in the peer reviewer selection, evaluation, or decision process of this article.
Funding
None.
Fig. 1.Classical laparoscopic and endoscopic cooperative surgery procedure.
Fig. 2.Non-exposed endoscopic wall-inversion surgery procedure. ESD, endoscopic submucosal dissection.
Fig. 3.Combination of laparoscopic and endoscopic approaches for neoplasia with a non-exposure technique procedure.
Fig. 4.Closed-laparoscopic and endoscopic cooperative surgery procedures. ESD, endoscopic submucosal dissection.
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