The Outcome of Snare-Assisted Traction Endoscopic Full-Thickness Resection for the Gastric Fundus Submucosal Tumors Originating from the Muscularis Propria

Abstract

Aim:

To explore the feasibility and effectiveness of snare-assisted traction endoscopic full thickness resection (EFTR) on gastric fundus submucosal tumors (SMTs).

Methods:

The clinical and pathological data of patients with gastric SMTs who underwent EFTR treatment at the Endoscopy Center of Kaifeng Central Hospital from January 2018 to June 2023 were collected. Among them, 36 patients underwent snare-assisted traction EFTR (SAT-EFTR) and 46 patients underwent standard EFTR (S-EFTR). The clinical baseline data, operative data, adverse events, and follow-up results of the two groups were collected and compared.

Results:

All patients successfully completed EFTR technique. There were 34 male and 48 female patients, with an average age of (56.62 ± 11.31) years. The average operation time was shorter in the snare-assisted EFTR group than the S-EFTR group (73.39 ± 31.33 minutes versus 92.89 ± 37.57 minutes, P = .014). In addition, the resection speed of the snare-assisted EFTR group was also significantly faster than that of the S-EFTR group (4.04 ± 2.23 versus 2.48 ± 0.93 mm²/min, P < .001). There was no statistically significant difference in the age, gender, lesion size, postoperative fasting duration, and postoperative hospitalization stay between the two groups (P > .05). One patient in the SAT-EFTR group developed delayed postoperative perforation which was close with purse‑string suture technique. All patients were discharged successfully, and there was no recurrence or metastasis during the follow-up period.

Conclusion:

Snare-assisted traction of EFTR could shorten the operation time, reduce the difficulty of the operation, and improve the efficiency of the operation. At the same time, this method is simple and easy to learn, more suitable for beginners, and worthy of clinical promotion and application.

Introduction

The gastric submucosal tumors (SMTs) refer to lesion originating from the layer below the epithelium of the mucosa, which was incidentally discovered during endoscopy examination.¹ The main histological types of SMT include gastrointestinal stromal tumors, leiomyomas, and neuroendocrine tumors.² Due to the potential for malignant transformation in some SMTs, early resection could prevent disease progression.³ Endoscopic full-thickness resection (EFTR) allows for complete removal of the lesion and is particularly suitable for SMTs originating from the muscularis propria (MP) or closely connected to the serosal layer.⁴ The gastric fundus is a common location for SMTs, making it a difficult area for endoscopic treatment due to its unique position. In recent years, traction techniques such as dental floss traction, clip traction, and magnetic control traction have been increasingly used in endoscopic treatment of challenging locations.^5–8 However, there is limited research on the use of a snare-assisted traction EFTR (SAT-EFTR) in the treatment of gastric fundus SMTs originating from the MP. This study aims to evaluate the feasibility, safety, and effectiveness of SAT-EFTR in treating gastric fundus SMTs originating from the MP.

Methods

Study design and patients

From January 2018 to June 2023, a retrospective analysis of data for patients with gastric SMTs treated with EFTR at the Endoscopy Center of Kaifeng Central Hospital were conducted. Inclusion criteria were (1) diagnosed with gastric fundus SMTs by gastroscopy and endoscopic ultrasound (EUS); (2) EUS showed the lesion originated from the MP layer; (3) signed informed consent form. Exclusion criteria were (1) severe cardiovascular or pulmonary diseases making surgery intolerable; (2) severe coagulation disorders; (3) suspicion of tumor malignancy or distant metastasis. All patients signed informed consent forms before endoscopic resection and were informed of the potential benefits and risks of the treatment.

Endoscopic equipment and accessories

The main treatment instruments used in this study included the Olympus GIF-Q260J gastroscope, the Pentax-2670URK ultrasound endoscope, the high-frequency generator (ICC‑200, ERBE; Erbe Elektromedizin GmbH, Germany), the HOOK knife (KD-620LR; Olympus), the IT knife (KD-611L; Olympus), the Dual knife (KD-650L; Olympus), and disposable snare (MTN-PFS-E-24) and clip (ROCC‑D‑26‑195; Microtech Nanjing, China).

Procedures

Snare-assisted traction EFTR

(1) Marking and injection: the lesion was marked starting 5 mm from the edge, and the submucosal injection was started 5 mm from the outer edge of the marked point; (2) incision: circular incision was made around the lesion to expose the tumor; (3) installation of the snare: the snare was fixed at the transparent cap. After reinsertion of the endoscope, the snare was released at the edge of the lesion, and tightened at the edge of the lesion with the assistance of forceps, allowing for “push and pull” of the lesion; (4) full-layer resection: resecting the muscle layer and serosal layer around the lesion and complete removal of the lesion using the snare; (5) clipping: hemostasis was achieved using thermal biopsy forceps to stop bleeding from exposed vessels, and after confirming no bleeding, the “perforation” was closed. For small defects, titanium clips were used for simple closure, and for larger defects, purse string sutures were performed. A gastrointestinal decompression tube was left in place for larger defects.

Standard EFTR

Except the step 3, the remaining steps were consistent with the SAT-EFTR group.

Postoperative management and follow‑up

After the endoscopic procedure, antibiotics, proton pump inhibitors, and nutritional support were routinely applied. If there are no symptoms such as gastrointestinal bleeding, abdominal pain, or distension, a liquid diet could be attempted. Sudden onset of abdominal pain should prompt a computed tomography (CT) scan to determine if there is a concurrent perforation or fistula. If there is vomiting blood or melena, emergency gastroscopy is necessary for endoscopic hemostasis or surgical intervention.

All patients undergo follow-up gastroscopy at 3, 6, and 12 months postoperatively to observe wound healing. For patients with a postoperative pathological diagnosis of stromal tumor, a repeat abdominal CT is recommended at 6 months postoperatively to assess for recurrence or metastasis, followed by annual follow-up visits.

Definitions

The operation time was defined from marking to suturing of the “perforation.” Resection speed (mm2/min) was calculated as the lesion area divided by the resection time. The lesion area was calculated using the formula: 3.14 × (lesion long diameter/2) × (lesion short diameter/2). The resection time was the time from incision of the mucosa to complete resection of the lesion. En bloc resection refers to obtaining a complete single specimen in one piece. Complete resection was defined that both the lateral and bottom margins are negative based on en bloc resection.

Statistical analysis

The data was conducted using SPSS 26.0. Quantitative data was expressed as mean ± standard deviation, and the two groups were compared using the t-test. Qualitative data were presented as frequency (percentage), and the two groups were compared using the chi-square test or the Mann–Whitney U test. A P value of <.05 was considered statistically significant.

Results

Patient characteristics

The patients' clinicopathological data are listed in Table 1. From January 2018 to June 2023, 82 patients with SMTs located in the gastric fundus were enrolled in this study. Among them, 36 patients underwent SAT-EFTR and 46 patients underwent standard EFTR (S-EFTR). There were 34 male and 48 female patients, with an average age of (56.62 ± 11.31) years. The postoperative pathology showed 57 GISTs, 17 leiomyoma, 2 schwannoma, and 6 others. All tumors originated from the MP layer, and some of them revealed extraluminal growth. The median diameter of the lesions was 21.51 mm.

Table 1.

The Comparison of Clinicopathological Data in Both Groups

Variables	Snare assisted EFTR (n = 36)	S-EFTR (n = 46)	P
Age, years	57.72 ± 11.20	55.76 ± 11.57	.442
Gender			.186
Male	12 (33.33%)	22 (47.83%)
Female	24 (66.67%)	24 (52.17%)
Lesion size (mm)	21.51 ± 6.60	19.66 ± 5.73	.178
Origin
Muscularis propria	36 (100.00%)	46 (100.00%)	1.000
Pathology			.095
GISTs	29 (80.55%)	28 (60.87%)
Leiomyoma	6 (16.67%)	11 (23.91%)
Schwannoma	1 (2.78%)	1 (2.17%)
Others	0 (0.00%)	6 (13.04%)

EFTR, endoscopic full thickness resection; GIST; S-EFTR, standard EFTR.

Procedure data

The procedure‑associated data are shown in Table 2. All patients successfully completed EFTR technique without transferring to surgery, and the operative perforation was closed with purse‑string suture technique or simple metallic clips. The en bloc resection rate was 100%. The average operation time was shorter in the snare-assisted EFTR group than the S-EFTR group (73.39 ± 31.33 minutes versus 92.89 ± 37.57 minutes, P = .014). In addition, the resection speed of the snare-assisted EFTR group was also significantly faster than that of the S-EFTR group (4.04 ± 2.23 versus 2.48 ± 0.93 mm²/min, P < .001).

Table 2.

Comparison of Endoscopic Resection Outcomes in Both Groups

Variables	Snare assisted EFTR (n = 36)	S-EFTR (n = 46)	P
Technique success	36 (100.00%)	46 (100.00%)	1.000
En bloc resection	36 (100.00%)	46 (100.00%)	1.000
Complete resection	36 (100.00%)	45 (97.83%)	1.000
Operation time (minutes)	73.39 ± 31.33	92.89 ± 37.57	.014
Resection speed (mm²/min)	4.04 ± 2.23	2.48 ± 0.93	<.001
Suture			.165
Simple metallic clips	27	40
Purse‑string suture	9	6
Adverse events	1 (2.78%)	2 (4.35%)	.707
Delayed bleeding	0 (0.00%)	1 (2.17%)
Delayed operation	1 (2.78%)	1 (2.17%)
Postoperative abdominal discomfort	21 (58.33%)	17 (36.96%)	.054
Postoperative indwelling gastric tube	13 (36.11%)	19 (52.78%)	.632
Fasting duration, day	3.08 ± 0.967	3.24 ± 1.196	.527
Postoperative hospital stay, day	5.94 ± 1.29	6.09 ± 1.26	.616
Follow up, month	33.72 ± 15.06	28.11 ± 18.64	.146

EFTR, endoscopic full thickness resection; S-EFTR, standard EFTR.

Delayed bleeding occurred in 1 patient (S-EFTR group) who was effectively treated with endoscopic hemostasis. One delayed perforation was developed in each group which were closed via the purse‑string suture technique. The average fasting time and postoperative hospital stay were comparable.

Discussion

With the promotion and popularization of gastroscopy and EUS, the detection rate of SMTs in the gastric fundus is increasing.⁶ SMTs in the gastric fundus are mainly GISTs, which have the potential for malignant transformation. In recent years, the therapeutic endoscopic technology has significantly improved. From endoscopic mucosal resection, endoscopic submucosal dissection, endoscopic submucosal excavation to EFTR, it has become an important part of the treatment of gastrointestinal lesions.^5,9,10 EFTR technology originates from endoscopic submucosal dissection. This technique not only ensures complete removal of the lesion but also was not affected by the depth of infiltration, which is suitable for SMTs originating from the MP layer or closely adhering to the serosal layer.

In comparison to surgical procedures, EFTR has several advantages, including minimal trauma, fast recovery, ability for repeated treatment, no visible scarring, and lower treatment costs.¹¹ However, conducting EFTR in the gastric fundus poses specific technical challenges and demands a high level of expertise from the operator. The special anatomical location of the gastric fundus makes it susceptible to the effects of respiration and heart rate, resulting in difficulty in exposing the surgical field. Additionally, its proximity to the diaphragm and spleen, coupled with abundant surrounding blood supply, increases the risk of bleeding during endoscopic treatment. Moreover, performing full-thickness resection at the gastric fundus requires inverting the endoscope, which heightens the technical demands for operating in a reversed position. Furthermore, in EFTR treatment, active perforation leads to the entry of gastric gas into the abdominal cavity, causing a reduction in gastric space despite continuous insufflation and resulting in an unsatisfactory visual field. These factors increase the difficulty and risk of EFTR.

In 2011, Li et al.¹² first reported on the use of dental floss-assisted endoscopic submucosal dissection for the treatment of SMTs in the gastric fundus. They found that assisted traction could provide a clear and effective operational area for endoscopy resection. As a result, traction technology has made significant advancements, leading to the development of new techniques such as elastic clip traction, S-O clip traction, and magnetic control traction.^13–15 The use of these traction techniques could enhance visibility in the operation field, decrease surgical complexity, improve resection efficiency, and decrease the occurrence of adverse events. However, current traction techniques have limitations, including a gradual decrease in tension during the resection process, the need for additional equipment, and high costs.

The snare has become a commonly used accessories in endoscopic treatment due to its safety, ease of use, and cost-effectiveness. When the snare is used for traction, it is inserted into the gastric cavity from outside the gastroscope without occupying the gastroscope's working channel. In this study, patients underwent S-EFTR and SAT-EFTR. The results showed a significant reduction in operation time and an increase in resection speed in the SAT-EFTR group compared to the S-EFTR group. Zhong et al.⁶ reported using SAT-EFTR for the treatment of SMTs in the gastric fundus. They achieved a 100% complete resection rate with no occurrences of delayed bleeding or perforation. Gu et al.¹⁶ found that snare-assisted traction could decrease operation time, enhance surgical success rates, and reduce the incidence of intraoperative bleeding. These findings align with the results of our study. Several studies have shown^10,17,18 that assisted traction techniques could significantly improve the operational efficiency and reduce adverse events in the treatment of SMTs with EFTR in the gastric fundus. Based on our center's experience, the application of snare-assisted traction during EFTR for gastric fundus SMT has several advantages: (1) the snare could fully expose the operational field, facilitating direct visualization of the resection, while avoiding larger blood vessels and pre-coagulating some small blood vessels to reduce bleeding and increase the safety of the operation; (2) during EFTR, the snare is capable of “pushing and pulling,” adjusting the tension based on the resection position, while consistently maintaining traction on the lesion, thus enhancing resection efficiency; (3) snare traction helps prevent the tumor from falling into the abdominal cavity. In conclusion, SAT-EFTR could reduce operation time, improve operational efficiency, and consequently benefit the postoperative recovery of patients.

In this study, a total of 3 patients experienced delayed bleeding or perforation, resulting in an incidence rate of 3.66%, which is consistent with previous study.¹⁹ All three patients showed improvement after proactive endoscopic treatment. It is important to note that there was no significant difference in the incidence of adverse events in the two groups, which is not entirely consistent with the study conducted by Gu et al.¹⁶ This inconsistency may be related to the small sample size in this study. Additionally, there were no cases of recurrence or metastasis among all patients during the follow-up period. This might be attributed to the small number of cases and the relatively short follow-up period. Further prospective, large-sample, multicenter studies are required to validate its efficacy and safety.

In conclusion, during the EFTR treatment for gastric fundus SMT, the utilization of a snare for assisted traction could enhance the operational field, decrease operational complexity, and improve operational efficiency.

Footnotes

Authors' Contributions

J.X.: conceptualization, methodology, software, investigation, formal analysis, writing—original draft; Y.W.: data curation, writing—original draft.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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