Gastric submucosal tumors (SMTs) are common neoplasms observed during upper gastrointestinal endoscopy, with an incidence rate of approximately 0.36% (1). While most SMTs are benign, up to 13% have malignant potential, particularly those originating from the muscularis propria layer (2). Small gastric SMTs (less than 2 cm in diameter), including “mini-SMTs” (1–2 cm) and “micro-SMTs” (<1 cm), are often detected through gastroscopy screening and primarily occur in the upper part of the stomach, especially near the gastroesophageal junction. Gastrointestinal stromal tumors (GIST) account for almost half of small gastric SMTs, followed by leiomyomas (3). These small gastric SMTs are generally regarded as having a low or very low risk of malignancy, and conservative follow-up or endoscopic resection (ER) is a common treatment approach (4). Indeed, ER has become a widely accepted option to avoid the psychological stress and economic burden of long-term follow-up along with the risk of delaying the optimal timing for treatment (5).

The premise of ER for SMTs is the absence of metastasis, and the goal is complete resection without major morbidity. For SMTs originating from the muscularis propria layer and potentially closely adhering to the serosal layer, endoscopic full-thickness resection (EFTR) is preferred under endoscopy (1). However, EFTR intentionally perforates and removes the entire tumor within the gastric wall, which may damage the rich vascular network outside the serosa layer. This can significantly increase the risk of massive hemorrhage over other ER techniques (6). In addition, sufficient exposure to the surgical field is required during operation given the high risk that the tumor will fall into the peritoneal cavity. Effective closure of defects during subsequent tumor resection is crucial to avoid peritonitis, pneumoperitoneum, and delayed perforation (7). While EFTR achieves a high en bloc resection rate for gastric SMTs, the technical difficulty and risk of complications associated with this technique restrict its widespread use. In recent years, some incision closure devices have been developed to simplify the closure such as Over-Stitch system and the over-the-scope clip (OTSC) (8, 9). Non-exposed EFTR techniques have also been designed to prevent massive hemorrhage and perforation by removing the isolated tumor above preclosed serosa using special ligation apparatuses such as the full-thickness resection device (FTRD) and the GERDX device (10). However, these devices are expensive and inaccessible, limiting their application in small- to-medium sized endoscopy centers.

In this study, we modified the conventional EFTR procedure using accessible and economical endoscopic instruments, simplifying and optimizing the procedures, making the operation more efficient and reducing the risk of complications. The aim of this study was to evaluate the safety and feasibility of modified EFTR for micro-SMTs.

This study described the use of a modified EFTR for micro-SMTs. This technique has the advantages of accurate localization of gastric micro-SMTs, a small incision, low incidence of bleeding and perforation, and easy tumor dissection and incision suturing. This retrospective study preliminarily demonstrated the clinical safety and efficacy of this modified EFTR. All tumors underwent R0 resection, no serious adverse events occurred after operation, and no tumor residual and recurrences occurred during follow-up.

Gastric SMT is usually asymptomatic, found incidentally during endoscopic screening, and difficult to accurately diagnose even after biopsy or EUS-FNA (11). Endoscopic treatment is an effective, safe, economical, and minimally invasive method for accurate histopathological evaluation and cure of SMTs (12). Thus, the value of endoscopic treatment of micro-SMTs during the early stages of disease should not be underestimated. EFTR evolved from ESD and is a preferred method for treating SMTs that originate from the deep muscularis propria layer. The feature of EFTR is to ensure en bloc resection of the tumor and perform iatrogenic perforation (13). Even for experienced operators, this is an extremely challenging job. These operations often cause iatrogenic perforation, greatly increasing the risk of intraoperative bleeding that causes the gastric cavity to collapse, limiting the operative field, and leading to operational difficulties. In addition, tumors growing extraluminal are at risk of falling into the peritoneal cavity during resection. However, the annular perforation and edema in the incision edge make it more difficult to close the incision. Long-time intraperitoneal exposure to gastric contents and air further increases the risk of local peritonitis and pneumoperitoneum. With the progress of endoscopic technology, the effectiveness of nonexposed EFTR in reducing the risk of bleeding and perforation has been confirmed in a number of studies, however, the paucity and maneuverability of the special equipment required, and the size and anatomic location of resectable lesions may limit their widespread applicability (10).

This study took advantage of the non-exposed EFTR presealing serosal layers and achieves this effect using affordable and easily accessible devices such as transparent caps and loops (10, 14). The transparent cap we used had a diameter of 13.9 mm and a front mounting exposed length of 5 mm. In theory, tumors within 11.2-mm in diameter can be completely attracted into the cap channel using an effective suction volume. Thus, it is feasible to use transparent cap suction combined with nylon rope ligation to completely capture <11.2 mm tumors by positioning and exposing the intraluminal surface. Closure of serosa and pre-devascularization can be easily achieved using caps and loops. Clips were then used to reduce tension around the ligated root to further reduce the risk of delayed perforation. The flexibility of these devices could make them suitable for all regions of the stomach.

Adequate tumor exposure before resection is essential for en-bloc resection, allowing more accurate and complete tumor capture in a limited space. In this study, the submucosal injection and incision steps of conventional EFTR were retained and optimized. Indeed, the R0 resection rate of modified EFTR was higher than that of non-exposed EFTR reported in prior studies (100% vs. 81.2%–87.0%) (10). Another highlight of the modified EFTR described in the current study is accurate marker localization and small incision. After conventional EFTR marker injection, micro-SMTs are prone to shift under the water pad due to their small size, requiring a complete mucosal incision outside the marker or additional incision to find the displaced tumor. Using the modified EFTR, the tumor position was vertically locked below the marker point at the center of the water pad using accurate marker positioning and injection. The tumor was also accurately exposed by a small incision through the medial incision of the peripheral marker point. In addition, the use of an insulation-tip knife to cut at the top of the tumor not only reduce the risk of perforation during mucosal incision by inexperienced operators but also reduce the risk of damage to the tumor capsule during incision. This study optimized EFTR and achieved a high technical success rate using simplified operational steps. This can be attributed to the strict compliance of indications and the highly scientific operative design.

The modified EFTR in this study greatly reduces the difficulty of operation, while preserving the effectiveness and safety of the endoscopic procedures to the greatest extent. The biggest technical difficulties of conventional EFTR are tumor dissection and incision closure. A retrospective study from different tertiary hospitals in China evaluated 35 gastric GISTs (<2 cm) who received conventional EFTR with a mean procedure time of 91 ± 63 minutes (10). Another large retrospective study in a tertiary referral center in China assessed 536 patients with upper intestinal SMTs arising from the muscularis propria. Those managed with conventional EFTR or STER had a complication rate of 12.9%, including 12.1% with perioperative perforation and 1.8% with perioperative bleeding (6). Meanwhile, the current study demonstrated a shorter procedure time (51.38 min, IQR 34.25 min) and fewer complications(0%). Since the modified operation uses a transparent cap to assist in capturing the tumor and close the serosa layer rather than conventional endoscopic dissection technology to separate the tumor, the modified endoscopic procedure is simpler and carries a lower risk of bleeding and perforation. Remarkably, modified EFTR is likely to have a shorter learning curve than conventional EFTR, which requires more ESD and submucosal endoscopic skills and experience.

This study has several limitations. First, this was a retrospective study conducted in a single endoscopic center with a small sample size. Second, the study lacked a control group. Third, the efficacy of the modified method may be limited by the diameter of the transparent cap and the suction force of the endoscope. This study is theoretically only applicable to micro-SMTs. Future research should directly compare the technical success rate and adverse events of the conventional and modified technique using multicenter, large-sample, and long-term clinical observational studies. If a large-diameter transparent cap and a precise suction device are developed in the future, it is expected to expand the indications for this modified EFTR of gastric SMTs with a diameter of more than 1 cm.

In conclusion, the modified EFTR technique described here significantly reduces the challenges of endoscopic en bloc resection of gastric micro-SMTs without a need for additional auxiliary high-value instruments and carries a lower risk of bleeding, perforation, and infection. This method should be more widely adopted and applied in clinical settings.

The original contributions presented in the study are included in the article/ Supplementary Material . Further inquiries can be directed to the corresponding author.

The studies involving humans were approved by the ethics committee of Shenzhen Guangming District People’s Hospital. The studies were conducted in accordance with the local legislation and institutional requirements. In this study, data obtained from previous clinical diagnosis and treatment and the risk to the subjects was not greater than the minimal risk. Waiver of informed consent would not adversely affect the rights and health of the subjects. If informed consent is required, patients may have abdominal pain and other somatic symptoms during the observation of postoperative complications after knowing the change of operative methods, which will affect the credibility of postoperative observation and the study will not be conducted rigorously. The privacy and personally identifiable information of the subjects were protected. Follow-up in this study was based on the frequency and content recommended by the current clinical guidelines, and there was no need to obtain additional subject information.

YZ: Conceptualization, Funding acquisition, Project administration, Validation, Writing – original draft. YH: Data curation, Formal analysis, Methodology, Software, Writing – review & editing. WC: Conceptualization, Data curation, Formal analysis, Supervision, Visualization, Writing – original draft, Writing – review & editing. JW: Data curation, Investigation, Methodology, Validation, Writing – review & editing. XL: Investigation, Methodology, Validation, Writing – review & editing. HP: Investigation, Validation, Writing – review & editing. JZ: Investigation, Validation, Writing – review & editing. QF: Investigation, Validation, Writing – review & editing.