Traction-assisted endoscopic subserosal dissection for gastric subepithelial tumors: A case series study (with video)

Abstract

BACKGROUND

Endoscopic subserosal dissection (ESSD) is a novel technique for treating gastric subepithelial tumors (SETs) originating from the muscularis propria (MP) layer. This technique preserves serosal integrity and prevents perforation, but it requires advanced technical skills due to limited operational perspective and complex maneuvering. Endoscopic traction technique has been shown to improve visualization during endoscopic procedures, reduce procedural difficulty, and thereby lower the risk of complications. We integrated these two approaches and refined them into a novel therapeutic method.

AIM

To introduce traction-assisted ESSD, and evaluate its safety and feasibility in the treatment of gastric SETs.

METHODS

This single-center, retrospective case series included 22 patients diagnosed with gastric SETs of MP origin. All procedures were performed by a single experienced endoscopist using traction-assisted ESSD.

RESULTS

Traction-assisted ESSD was performed in 22 patients with a 100% complete resection rate. The average lesion size was 1.7 ± 1.2 cm (range: 0.6-6.5 cm), and the average operative duration was 32.3 ± 15.4 minutes (range: 12-71 minutes). The lesions were diagnosed as gastrointestinal stromal tumors (8 cases), leiomyomas (10 cases), and spindle cell tumors (4 cases). All gastric wall defects were successfully closed endoscopically, with no adverse events such as bleeding, perforation, or peritonitis.

CONCLUSION

Traction-assisted ESSD is a feasible and safe technique for treating gastric SETs originating from the MP layer.

Key Words: Stomach neoplasms; Subepithelial tumor; Endoscopic mucosal resection; Traction; Subserosal dissection

Core Tip: The primary innovation of this study is the first-time integration of the endoscopic traction technique with endoscopic subserosal dissection, establishing a novel endoscopic strategy for managing gastric subepithelial tumors originating from the muscularis propria layer. This approach integrates the key advantages of both endoscopic subserosal dissection and traction techniques, enabling complete resection of the lesion while preserving serosal integrity - thereby substantially reducing the risk of serious complications. Moreover, it reduces procedural difficulty and enhances reproducibility.

INTRODUCTION

Gastric subepithelial tumors (SETs) are often asymptomatic and most frequently found incidentally during endoscopic procedures. However, as endoscopic screening becomes more widespread and endoscopic techniques continue to advance, the detection and diagnostic accuracy related to gastric SETs have progressively improved. Gastric SETs may originate from the muscularis mucosa, the submucosa and the muscularis propria (MP) layer. Many of the gastric SETs originating from the MP layer are pathologically classified as gastrointestinal stromal tumors (GISTs), while a smaller proportion includes leiomyomas, schwannomas, and other rare tumors[1]. GISTs exhibit malignant potential, and treatment options include surgical resection, pharmacotherapy, and endoscopic intervention[2]. Accumulating evidence suggests that endoscopic intervention for gastric SETs that originate from the MP layer demonstrates comparable clinical efficacy to surgical resection, while offering advantages such as reduced invasiveness and faster postoperative recovery[3,4].

With regard to endoscopic treatment methods, endoscopic submucosal dissection (ESD), endoscopic full-thickness resection (EFTR), submucosal tunneling endoscopic resection, and laparoscopic-endoscopic surgery have been widely adopted in recent years[1-3]. Based on this, some scholars have observed that the layer between the serosa and the MP also consists of loose connective tissue similar to the submucosa. Consequently, they developed and introduced endoscopic subserosal dissection (ESSD), a technique that preserves the integrity of the serosa and minimizes the risk of perforation[5]. However, this procedure is challenging due to limited operational perspective, complex maneuvers, and the need for advanced endoscopic skills. Endoscopic traction technique has been shown to improve visualization during endoscopic procedures, reduce procedural difficulty, and thereby lowering the risk of complications[6]. Therefore, we aimed to incorporate traction into ESSD for the treatment of gastric SETs originating from the MP layer and evaluate the feasibility and safety of this approach.

MATERIALS AND METHODS

Patients

We retrospectively reviewed the medical records of patients with gastric SETs originating from the MP layer who underwent traction-assisted ESSD in the Department of Gastroenterology, Qilu Hospital of Shandong University (Qingdao) from July 2022 to December 2024. All patients were diagnosed with gastric SET by computed tomography (CT), gastrointestinal endoscopy, and endoscopic ultrasonography before operation.

Clinical data, endoscopic findings, pathological results, and other relevant information were collected and analyzed. The study was conducted in accordance with the principles outlined in the Declaration of Helsinki. Written informed consent was obtained from all participants. The study protocol was reviewed and approved by the Ethics Committee of Qilu Hospital (Qingdao), Shandong University, approval No. KYLL-2020080.

Traction-assisted ESSD procedure and postoperative management

The following equipment was used: Gastroscope (Pentax-i5000 main unit, EG-29-i10 endoscope), injection needle (Olympus, NM-400U-0523), electrothermal hemostatic forceps (Olympus, FD-410 LR), metal clip (Nanjing Minimally Invasive Company, ROCC-D-26-195-C), Dual Knife (Olympus, KD-650 L), and a high-frequency electrosurgical unit (ERBE-VIO 300D). All endoscopic surgeries were performed by the same experienced physician under general anesthesia with tracheal intubation. The detailed procedure steps of the modified method were as follows (Figure 1, Video): (1) Marking, injection, and incision: The lesion was marked at the edge with the Dual Knife in the electrocoagulation mode. The mixed solution containing adrenaline, methylene blue, sodium hyaluronate, and normal saline was injected under the mucosa at the marked edge. The Dual Knife was used to incise the mucosal layer around the lesion along the mark, dissect the submucosal layer, and expose the MP; (2) The clip tied with dental floss was attached to the mucosa at the lesion site. The traction technique (clip-with-line method or pulley method) was used to pull the lesion into the gastric cavity; (3) The MP was incised; (4) The subserosal injection was administered to further separate the serosa from the MP; (5) The gap between the serosa and the MP was fully exposed with the help of the traction technique. The lesion was completely resected keeping the tumor capsule intact, and maintaining the integrity of the serosa; (6) Wound management: If necessary, electrothermal hemostatic forceps were used to stop bleeding from the wound after dissection. Endoscopic suture techniques (such as clips, nylon string purse suture, etc.) were used to close the gastric wall wound; and (7) The lesion was collected and processed. A nasogastric tube was inserted under direct endoscopic vision and connected to the gastrointestinal decompressor.

Figure 1 Detailed traction-assisted endoscopic subserosal dissection procedure steps. A: Mark the edge of the lesion with the Dual knife; B: Incise the mucosal layer around the lesion along the mark; C: Dissect the submucosal layer, and expose the lesion and the muscularis propria; D: Incise the muscularis propria; E: Administer the ubserosal injection to separate the serosa from the muscularis propria; F: Use the traction technique to pull the lesion into the gastric cavity, and expose the space between the serosa and the muscularis propria; G: Resect the lesion completely, and maintain the integrity of the serosa; H: Close the gastric wall wound; I: Retrieve the lesion specimen.

Detailed explanation of the endoscopic traction technique: The metal clip was inserted into the biopsy channel ex-vivo. One end of the dental floss was secured to the metal clip. The floss was allowed to extend naturally, with the remaining portion kept close to the outer wall of the endoscope rather than inside the biopsy channel. The endoscope was maneuvered to attach the metal clip onto the mucosal surface of the lesion. Following this step, one end of the floss was anchored to the mucosal surface of the lesion via the metal clip, while the other end remained external to the patient’s body. The assistant then manipulated the floss with continuous gentle pulling to deliver adequate traction and achieve sufficient exposure of the surgical field. Given interindividual variability in lesion location and endoscopic approach angle, traction provided by the single floss was occasionally suboptimal. In such cases, a second metal clip was used to fix the floss at an alternative site on the gastric mucosa, creating a pulley-like anchoring structure. Adjustment of the anchoring position allowed flexible modulation of the traction direction to meet procedural needs.

The patients were not permitted to eat for two days after surgery, and received total parenteral nutrition during this time. Standard postoperative care included routine antibiotics and treatment with proton pump inhibitors. If there were no complications such as abdominal pain, bleeding, or fever by the third postoperative day, a clear liquid diet was started and gradually advanced to soft solids. Continuous monitoring for complications was essential throughout the perioperative period.

Statistical analysis

SPSS 27.0 (IBM, Armonk, NY, United States) was used to statistically analyze patient data. The data were expressed as mean ± SD with minimum and maximum, or expressed as rates.

RESULTS

This study enrolled 22 patients with gastric SETs originating from the MP layer who underwent traction-assisted ESSD. Of the 22 patients, four were male and 18 were female, ranging in age from 38 years to 71 years. The diameter of the lesions ranged from 0.6 cm to 6.5 cm, with an average of 1.7 ± 1.2 cm. The operative duration ranged from 12 minutes to 71 minutes, with an average of 32.3 ± 15.4 minutes. Of the 22 lesions, 11 were located in the gastric fundus, nine in the gastric corpus, and two in the junction between the fundus and corpus. Nineteen patients were treated using the clip-with-line method, and three were treated using the pulley method. All patients had minor intraoperative bleeding, which was effectively managed with endoscopic hemostasis and did not interfere with the procedure. No delayed postoperative bleeding occurred. The wounds were successfully closed using endoscopic suturing methods, such as clips and nylon string purse sutures. There were no cases of intraoperative or delayed postoperative gastrointestinal perforation or peritonitis. No patient required surgical intervention. Postoperative pathological analysis revealed that eight cases were identified as GISTs, including four low-risk cases and four extremely low-risk cases. Ten were leiomyomas, and four were spindle cell tumors (unclassified). These four cases were unclassified due to the lack of immunohistochemical staining results including smooth muscle actin, caldesmon, CD117, Dog-1, CD34, S-100, Ki-67. Pathological findings in all cases confirmed complete tumor resection with intact tumor capsules, achieving a 100% complete resection rate (Table 1). Follow-up evaluation was performed one year postoperatively, and gastroscopic examination revealed no evidence of lesion recurrence.

Table 1 Characteristics of the patients and endoscopic procedures of traction-assisted endoscopic subserosal dissection, mean ± SD.

Variable	Statistics
Age (years)	54.3 ± 8.7 (38-71)
Sex
Male	4
Female	18
Location
Fundus	11
Corpus	9
Junction between the fundus and corpus	2
Tumor size (cm)	1.7 ± 1.2 (0.6-6.5)
Operative duration (minute)	32.3 ± 15.4 (12-71)
Traction techniques
Clip-with-line method	19
Pulley method	3
Histopathological diagnosis
Gastrointestinal stromal tumor	8
Leiomyoma	10
Spindle cell tumor	4
Complete resection rate (%)	100
Adverse events	0

DISCUSSION

Most patients with gastric SETs have no symptoms and the lesions are detected during endoscopic examination. The pathological type of such lesions is likely GISTs[1]. However, it is difficult to obtain a conclusive pathological diagnosis before surgery. Therefore, clinicians often refer to the diagnosis and treatment guidelines of GIST to treat such lesions. The treatment methods for GISTs include surgical operations (open surgery, laparoscopic surgery), drug therapy and endoscopic treatments[2]. Surgical treatment has a definite curative effect; however, the trauma involved is significant. For smaller diameter lesions, more and more doctors pursue minimally invasive treatment methods. With the development of endoscopic technology, a variety of endoscopic treatment methods have been used to treat GISTs. Endoscopic treatment methods such as ESD, EFTR, submucosal tunneling endoscopic resection and laparoscopic-endoscopic cooperative surgery are now relatively mature techniques, which have been confirmed by many studies[1,3,4,7-9]. However, the above endoscopic treatment methods all face the problems of active or passive gastrointestinal perforation during the operation and difficulty in suturing after perforation. Some patients may develop peritonitis; in severe cases, surgical repair of the perforation is necessary. Consequently, fasting duration is prolonged, broader-spectrum or higher-potency antibiotics are needed, hospitalization is extended, and total healthcare expenditures increase. Furthermore, postoperative pain, fever, and prolonged fasting collectively contribute to adverse effects on patients’ emotional well-being and psychological health. Therefore, doctors such as Lei Wang invented ESSD[5]. This endoscopic method is used to treat lesions originating from deep layers such as the MP, and does not rely on laparoscopic assistance. The most crucial factor in ESSD is to keep the serosa intact during the operation. Preserving the intact serosa effectively separates the gastric cavity from the abdominal cavity, thereby reducing the risks of gastric juice leakage, tumor metastasis, and elevated intra-abdominal pressure that may result from gastric wall perforation. In addition, the closed space with an intact serosa is more conducive to controlling gastric cavity pressure, thus enabling suturing of the wound. The key to the ESSD technique lies in expanding the subserosal layer to separate the serosa from the MP. The subserosal layer is very thin and is composed of loose connective tissue similar to the submucosa. During the expansion process, it is necessary to obtain a clear operational field of view as much as possible to reduce the occurrence of serosa perforation.

However, limited by factors such as instruments, it is difficult to obtain a clear endoscopic operational field of view for complex operations in certain positions. As a result, the operation time is relatively long, and complications such as perforation are likely to occur[10]. To solve this problem, doctors have invented various endoscopic traction techniques, which can be generally divided into in-vivo traction techniques and ex-vivo traction techniques[6,11-13]. The clip-with-line method is a type of ex-vivo traction technique. First, a metal clip with a pre-tied dental floss is fixed at a specific position of the lesion, and then the dental floss is pulled outside the patient's body to generate an appropriate traction force on the lesion, thus better exposing the operational field of view. The pulley method is based on the clip-with-line method. By adding a fixed metal clip at an appropriate position inside the body, a suitable traction direction can be provided. The above two endoscopic traction techniques are simple to operate, with economic and easily accessible materials. They can be applied in endoscopic treatment of the esophagus, stomach, colorectum, and are currently widely used endoscopic traction techniques[12].

The primary innovation of this study is the first-time integration of the endoscopic traction technique with ESSD, establishing a novel endoscopic strategy for the management of gastric SETs originating from the MP layer. This treatment method can be used to treat lesions with a diameter of 0.5-5.0 cm, but it is not suitable for the following situations: (1) Extracavitary growth of gastric SETs; (2) Poorly defined tumor boundaries; and (3) Radiological evidence of regional lymph node or distant metastasis on CT. In this study, there was one case where the lesion was pre-operatively evaluated to have a diameter of less than 5.0 cm, but the postoperative pathological examination confirmed that the lesion size was about 6.5 cm, and it was also successfully and completely resected. If intraoperative examination revealed that the lesion was tightly adherent to the serosa or extracavitary growth - resulting in inadequate exposure of the subserosal layer - the procedure was converted to EFTR. Cases that were unsuitable for ESSD and required conversion to EFTR were excluded from this study.

The traction technique not only provides a clearer operative field of view, reduces the difficulty of endoscopic operation, and shortens the operation time, but also helps maintain the integrity of the serosa, making suturing of the postoperative wound simpler and more efficient. Although additional teps such as subserosal injection and using the clip-with-line to pull the lesion were added compared with traditional endoscopic procedures such as ESD and EFTR, the operation time was not significantly prolonged compared with previous studies on ESD for resection of gastric SETs[1,3]. This study included 22 patients, with an average operative duration of 32 minutes and a maximum of 71 minutes. Traction-assisted ESSD integrates the key advantages of ESSD and traction techniques. It ensures complete resection of the lesion while preserving the integrity of the serosa, thereby substantially reducing the risk of serious complications. In previous case series studies of ESSD, the incidence of intraoperative perforation ranged from 16.7% to 18.2%[5,14]. However, in this study, neither intraoperative or postoperative serosal perforation nor other complications such as intraoperative massive hemorrhage and postoperative delayed bleeding occurred, and none required surgical intervention for remedial management. Furthermore, the application of traction-assisted ESSD was not limited by the location of the lesion. In our study, the lesions were distributed at multiple sites in the fundus and body of the stomach. Complete tumor resection was confirmed in all cases by pathological examination, with intact tumor capsules and a 100% lesion resection rate. Complete resection effectively prevented tumor dissemination that could result from capsule rupture.

The postoperative follow-up strategy should be based on the pathological findings. Given the malignant potential of GISTs, endoscopic surveillance is recommended at 3 months, 6 months, and 12 months after treatment to assess wound healing and tumor recurrence. For low-risk patients, a CT scan should be performed every 6-12 months within 5 years after surgery. For medium- and high-risk patients, additional treatment - such as molecularly targeted drug therapy or repeat surgery - is recommended following endoscopic resection. In this study, pathological findings in the patients revealed low-risk or very low-risk GISTs and leiomyomas. All patients underwent gastroscopy and CT reexamination one year after endoscopic resection, and none showed evidence of tumor recurrence. Some patients have been followed up for approximately three years, and to date, no tumor recurrence has been observed.

To date, the available literature on ESSD consists exclusively of case reports and case series. The overall number of cases is relatively small, and there is a lack of comparative studies between ESSD and established treatment methods - such as surgery and EFTR. Our study has several similar limitations: It is a retrospective, single-center study with a relatively small sample size and no control group; additionally, potential operator-dependent bias may exist. This endoscopic strategy still requires studies with a larger sample size, a higher level of evidence, and a longer follow-up time for confirmation.

CONCLUSION

Traction-assisted ESSD is a feasible and safe technique for treating gastric SETs originating from the MP layer. Further large prospective controlled studies are required.

ACKNOWLEDGEMENTS

I would like to express my sincere gratitude to all those who have contributed to this research. Meanwhile, I am thankful to all colleagues and friends for their assistance and cooperation throughout the research, as well as their insightful perspectives and selfless support.