Short-term outcome of endoscopic submucosal dissection using a clutch cutter for subepithelial lesions within the esophagogastric submucosa: a Japanese prospective observational study

Article information

Clin Endosc. 2024;.ce.2024.094
Publication date (electronic) : 2024 October 10
doi : https://doi.org/10.5946/ce.2024.094
1Endoscopy Center, Aso Iizuka Hospital, Iizuka, Japan
2Department of Gastroenterology, Aso Iizuka Hospital, Iizuka, Japan
3Department of Pathology, Aso Iizuka Hospital, Iizuka, Japan
4Clinical Research Support Office, Aso Iizuka Hospital, Iizuka, Japan
Correspondence: Kazuya Akahoshi Endoscopy Center, Aso Iizuka Hospital, 3-83 Yoshio, Iizuka 820-8505, Japan E-mail: kakahoshi2@aol.com
Received 2024 April 21; Revised 2024 June 4; Accepted 2024 June 10.

Abstract

Background/Aims

The efficacy and safety of endoscopic submucosal dissection using a clutch cutter (ESD-CC) for subepithelial lesions within the esophagogastric submucosa (SELEGSM) has not been investigated. This study aimed to assess the efficacy and safety of ESD-CC for the treatment of SELEGSM.

Methods

This prospective study included 15 consecutive patients with 18 SELEGSMs diagnosed by endoscopic ultrasonography. The primary outcomes were short-term outcomes including en bloc resection rate, R0 resection rate, procedure time, and complication rate. The secondary outcome was final histological diagnosis.

Results

Among the participants, 18 lesions were identified: 12 in the stomach (nine patients) and six in the esophagus (six patients). The en bloc resection rate was 94.4% (17/18). The R0 resection rate was 88.9% (16/18). The median operating time was 39 min, and no instances of perforation or bleeding were observed. The final diagnoses of SELEGSM included six neuroendocrine tumors (33.3%), six granular cell tumors (33.3%), two ectopic pancreases (11.1%), one inflammatory fibroid polyp (5.6%), one leiomyoma (5.6%), one lipoma (5.6%), and one leiomyosarcoma (5.6%).

Conclusions

ESD-CC appears to be a technically efficient and safe approach for SELEGSM resection, suggesting its potential as a valuable treatment option.

Graphical abstract

INTRODUCTION

The clutch cutter (CC) was designed to mitigate the risk of adverse effects associated with endoscopic submucosal dissection (ESD) when using standard knives. This device uses electrosurgical currents to grasp, pull, coagulate, and incise the target tissue.1,2 In previous studies focusing on early stage epithelial neoplasms, ESD performed with CC (ESD-CC) demonstrated a high histologic complete resection (R0 resection) rate and a low incidence rate of adverse events.3-7 However, the outcomes of treating subepithelial lesions within the esophagogastric submucosa (SELEGSM) using ESD-CC have not yet been investigated. This study aimed to evaluate the efficacy and safety of ESD-CC for the treatment of SELEGSM.

METHODS

Patients and lesions

This prospective study enrolled 15 patients with 18 SELEGSMs who underwent ESD-CC at Aso Iizuka Hospital between June 2007 and April 2020. The inclusion criterion for ESD-CC was the presence of SELEGSM which were not continuous with the muscularis propria, as diagnosed by preoperative endoscopic ultrasound (EUS).

CC short type

The short-type Clutch Cutter (model DP2618DT-35; Fujifilm) (Fig. 1) features serrated jaws that enable the endoscopist to securely grasp the targeted tissue. These jaws measure 0.4 mm in width and 3.5 mm in length, can rotate 360°, and has insulated external surfaces to minimize electrical tissue damage.2,7 The insert was 2.7 mm in diameter. CC facilitates the management of the entire ESD process. The high-frequency generator used is the VIO 300D (Erbe). For marking, the forced coagulation mode was set to 30 W with an effect level of 3. Mucosal incision and submucosal dissection were performed using the Endocut-Q mode (effect 2, duration 3, interval 1), whereas the soft coagulation mode (effect 5, 100 W) was used for preventive coagulation and hemostasis.

Fig. 1.

Distal tip of the short-type Clutch Cutter (DP2618DT-35; Fujifilm).

ESD-CC procedures

ESD-CC was performed using a single working channel procedural endoscope with a water jet system (EG-450RD5, EG-530RD5: Fujifilm; Q260J: Olympus). To ensure the adequacy of the endoscopic view and to apply tension to the submucosal tissue in the field of view during ESD-CC, a clear hood was fitted to the endoscope tip. The techniques used for ESD-CC have been detailed elsewhere.2,7 The ESD-CC method involves injection of a solution containing 10% glycerin, 0.9% NaCl, and 5% fructose (Glyceol; Chugai Pharmaceutical Co.) or hyaluronic acid (MucoUp; Boston) combined with a small volume of epinephrine and indigo carmine dye into the submucosal layer. Mucosal incision and submucosal dissection were performed to excise the lesion completely using the CC. Bleeding veins or arteries were secured, maneuvered, and coagulated with the CC using an electrosurgical current to halt the bleeding. All incisions and coagulation procedures were performed after the target area was secured and moved away from the proper muscle layer. The lesion was completely resected.

Histopathological evaluation

The excised specimens were sectioned at 2-mm intervals perpendicular to the surface. Tumor diameter, depth of infiltration, histological type, vascular and lymphatic involvement, and presence of tumors at the vertical and horizontal margins were assessed.

Evaluation of ESD-CC efficacy and adverse effects

The operating time was measured from initial injection into the submucosa to completion of submucosal dissection. If the lesion was removed in a single piece and the resection margin was visibly tumor-negative, the resection was considered en bloc. Resection was deemed tumor-negative (R0) if the vertical and lateral sections showed no microscopic evidence of tumor cells, irrespective of the histological characteristics.

Perforation during ESD-CC was identified endoscopically, whereas perforation after ESD-CC was judged based on abdominal pain and/or the detection of free air through plain radiography and/or computed tomography following ESD-CC. Bleeding after ESD-CC was defined as the clinical evidence of bleeding that necessitated endoscopic hemostasis.7

Statistical analysis

Fisher’s exact test and Wilcoxon rank sum test were used for statistical analyses, as appropriate, with STATA ver. 18.0 (STATA Corp. LLC). Statistical significance was set at p<0.05. significant.

Ethical statement

This study was approved by the Ethics Committee of the Aso Iizuka Hospital (registration number: 12120). All patients provided written informed consent, in accordance with the Declaration of Helsinki.

RESULTS

The clinicopathological characteristics are detailed in Table 1. Table 2 summarizes the technical outcomes. The technique of grasping and pulling or lifting the target tissue before excision facilitated precise cutting of the target area and enabled application of adequate pre-cut coagulation (Supplementary Video 1). The en bloc resection rate was 94.4% (esophagus, 100%; stomach, 91.7%) and the R0 resection rate was 88.9% (esophagus, 100%; stomach, 83.3%). Figure 2 shows a representative example of ESD-CC applied to an esophageal granular cell tumor. In cases where R0 resection was unattainable, ESD-CC was discontinued in one instance (case no. 12) (Fig. 3) because of tumor invasion into the muscularis propria, which was identified during ESD (the postsurgical resection diagnosis was a granular cell tumor infiltrating the muscularis propria). In another case (case no. 14), the vertical margin could not be evaluated because of thermal degeneration. The median operation duration was 39 min (esophagus, 27.5; stomach, 45). No complications were observed. The final diagnoses for esophageal lesions were granular cell tumors in five cases (83.3%) and leiomyoma in one case (16.7%). Gastric lesions were diagnosed as neuroendocrine tumors in six cases (50.0%), ectopic pancreas in two cases (16.7%), granular cell tumor in one case (8.3%), inflammatory fibroid polyp in one case (8.3%), lipoma in one case (8.3%), and leiomyosarcoma in one case (8.3%).

Characteristics of 15 patients with 18 lesions who underwent ESD-CC for SELEGSM

Technical results of the ESD using the clutch cutter (n=18)

Fig. 2.

A representative case of endoscopic submucosal dissection using the clutch cutter (ESD-CC) for an esophageal granular cell tumor. (A) Endoscopic image showing a flat granular cell tumor located in the lower esophagus. (B) Endoscopic ultrasonography revealing a hypoechoic mass (T) located in the deep mucosal and submucosal layer. (C) Endoscopic image showing submucosal dissection deeper than the lower edge of the tumor (T), maintaining a negative vertical margin. (D) Macroscopic image of the en bloc resected specimen obtained by ESD-CC.

Fig. 3.

Endoscopic view of submucosal dissection using the clutch cutter for a gastric granular cell tumor (T) showing invasion of the muscularis propria.

DISCUSSION

SELEGSM encompasses a broad spectrum of diseases ranging from benign to malignant conditions.8,9 Despite this diversity, a significant proportion of these tumors penetrate deeply into the submucosa,10 necessitating the use of specialized techniques to achieve curative resection with clear vertical margins.11-15 Conventional endoscopic polypectomy and endoscopic mucosal resection (EMR) for SELEGSM have a high rate of positive vertical margins (0%–16.7%); therefore, several modified EMRs (band ligation-assisted, cap-assisted, and underwater) have been developed, which have lowered the rates of positive vertical margins (0%–3.7%) in retrospective case series.14-16 These methods are effective, simple, safe, and low-cost, but are limited to small lesions and theoretically do not allow direct endoscopic visual control of the resection depth. Kim et al.16 reported that ESD (2.6%) had a significantly lower rate of positive vertical margins than did EMR (16.7%) in the endoscopic resection of gastric neuroendocrine tumors. In this context, ESD is preferred over conventional EMR as it involves precise submucosal dissection immediately above the proper muscle layer under endoscopic visualization, coupled with accurate histologic evaluation of the resected specimen.17-20 However, technical literature on the use of a conventional knife for ESD in SELEGSM is limited.12,13,18,19,21 Furthermore, data on ESD-CC are lacking. To our knowledge, this is the first prospective study to investigate the technical efficacy of ESD-CC in SELEGSM.

ESD presents technical challenges and carries a considerable risk of complications such as bleeding and perforation.22 Each stage of the procedure requires specialized instruments including special knives or hemostatic forceps.2,23 ESD-CC offers four safety advantages: (1) accurate targeting through tissue fixation, (2) reliable hemostasis via tissue compression, (3) reduced electrical tissue injury to the muscularis propria by elevating the grasped tissue, and (4) minimal external electrical damage through external insulation.2,7 This study demonstrated that intraoperative bleeding could be efficiently managed using CC alone without the need for hemostats, allowing all ESD phases to be executed exclusively with CC (1-device ESD method). Previous studies have established ESD-CC as a safe (perforation rate: 0%–3.6%, delayed bleeding rate: 0%–4.2%) and effective (en bloc resection rate: 88.9%–100%) technique for the removal of early gastrointestinal epithelial tumors using a single device.2-7 This method is straightforward and easy to learn, involving merely the repetitive actions of grasping and elevating the target tissue, followed by coagulation or incision with an electrosurgical current. Notably, the self-completion rates of ESD by novice endoscopists were significantly higher with CC than with conventional knives (61.7% vs. 24.5%; p<0.001).5

Table 3 shows a comparison of the SELEGSM ESD outcomes between conventional knives12,13,18,19 and CC (this study). The en bloc and R0 resection rates for ESD using conventional knives were 88.2% to 100% and 73.3% to 100%, respectively. In contrast, the en bloc and R0 resection rates for ESD with CC were 94.4% and 88.9%, respectively. The en bloc and R0 resection rates were comparable between the ESD-conventional knives knives and ESD-CC methods. Perforation, a significant adverse event of ESD for SELEGSM, has a reported frequency of 0% to 11.7%.12,13,18,19 In this study, the perforation rate of ESD-CC was 0%. Delayed bleeding, another major adverse effect of ESD, has a reported frequency of 0% to 13.3%. Meanwhile, the frequency of delayed bleeding in patients who underwent ESD-CC was 0%, and the frequencies of perforation and delayed bleeding were comparable between the ESD-conventional and ESD-CC methods. The precise and effective hemostatic capabilities of the CC, akin to hemostatic forceps,2 are crucial for preventing perforation and delayed bleeding post-ESD. This and previous studies2-7 highlight the ability of CC to perform effective pre-cut coagulation, while ensuring immediate cessation of unintentional bleeding without the need to switch hemostatic forceps. This method, therefore, significantly reduces the risk of ESD-related adverse events. However, to date, studies on the technical outcomes of ESD for SELEGSM have reported only a small number of cases from advanced ESD centers.12,13,18,19 Further case studies are required to validate these findings.

Reported technical results of ESD for SELEGSM including those of the current study

The present study had a specific limitation: it involved a small sample size of 15 patients from a single center. To thoroughly assess the effectiveness of our method, further large controlled randomized trials comparing CC with an insulation-tipped knife, needle-type knife, or other devices should be conducted.

In conclusion, our preliminary outcomes suggest that ESD-CC is a viable choice for endoscopic treatment of SELEGSMs. This method requires only a single resection device (CC) and is effective, safe, and technically straightforward.

Supplementary Material

Supplementary Video 1.

ESD using the Clutch Cutter on leiomyoma of the cervical esophagus.

ce-2024-094-Supplementary-Video-1.mp4

Supplementary materials related to this article can be found online at https://doi.org/ce.2024.094.

Notes

Conflicts of Interest

Kazuya Akahoshi and Fujifilm have applied for a patent for the Clutch Cutter described in this article. Japan, China, and the EU have already granted patents. The co-authors have no potential conflicts of interest.

Funding

This research was conducted with the assistance of a research grant (AIH-CRG2021-1) from the Aso Iizuka Hospital.

Acknowledgments

We thank Phoebe Chi, MD, from Edanz (https://jp.edanz.com/ac) for editing the draft of this manuscript.

Author Contributions

Conceptualization: KazuyaA; Data curation: KazuyaA; Formal analysis: KazuyaA, HK; Funding acquisition: KazuyaA; Investigation: KazuyaA, KI, KazuakiA, SO, ST, YO, MO; Methodology: KazuyaA, KI, KazuakiA, SO, ST, YO, MO; Project administration: KazuyaA; Resources: KazuyaA; Software: KazuyaA; Supervision: KazuyaA; Validation: KazuyaA; Visualization: KazuyaA; Writing–original draft: KazuyaA; Writing–review & editing: all authors.

References

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Article information Continued

Fig. 1.

Distal tip of the short-type Clutch Cutter (DP2618DT-35; Fujifilm).

Fig. 2.

A representative case of endoscopic submucosal dissection using the clutch cutter (ESD-CC) for an esophageal granular cell tumor. (A) Endoscopic image showing a flat granular cell tumor located in the lower esophagus. (B) Endoscopic ultrasonography revealing a hypoechoic mass (T) located in the deep mucosal and submucosal layer. (C) Endoscopic image showing submucosal dissection deeper than the lower edge of the tumor (T), maintaining a negative vertical margin. (D) Macroscopic image of the en bloc resected specimen obtained by ESD-CC.

Fig. 3.

Endoscopic view of submucosal dissection using the clutch cutter for a gastric granular cell tumor (T) showing invasion of the muscularis propria.

Table 1.

Characteristics of 15 patients with 18 lesions who underwent ESD-CC for SELEGSM

Patient Age (yr)/sex Organ/location EUS findings of SELEGSM
Pre-ESD-CC histological diagnosis (biopsy) Post-ESD-CC histological diagnosis R0 resection/additional treatment
Diameter (mm) Continuity with muscularis propria Echo level
1 62/M Esophagus/middle thoracic 15 No Hypoechoic Granular cell tumor Granular cell tumor Yes/none
2 45/F Esophagus/cervical 6 No Hypoechoic Granular cell tumor Granular cell tumor Yes/none
3 53/F Esophagus/middle thoracic 5 No Hypoechoic Granular cell tumor Granular cell tumor Yes/none
4 51/F Esophagus/middle thoracic 6 No Hypoechoic Granular cell tumor Granular cell tumor Yes/none
5 40/M Esophagus/lower thoracic 6 No Hypoechoic Granular cell tumor Granular cell tumor Yes/none
6 42/F Esophagus/cervical 8 No Anechoic Leiomyoma Leiomyoma Yes/none
7 50/F Stomach/antrum 8 No Hypoechoic Not conclusive Ectopic pancreas Yes/none
8 59/F Stomach/cardia 31 No Hyperechoic Well differentiated adenocarcinoma/not conclusive for SEL 10 mm intra- mucosal adenocarcinoma on 30 mm lipoma Yes (lipoma including intra-mucosal cancer)/none
9 72/F Stomach/body 3 No Hypoechoic Neuroendocrine tumor Neuroendocrine tumor Yes/none
10 71/M Stomach/antrum 5 No Hypoechoic Not conclusive Ectopic pancreas Yes/none
11 77/F Stomach/body 9 No Hypoechoic Neuroendocrine tumor Neuroendocrine tumor Yes/none
11 77/F Stomach/body 3 No Hypoechoic Neuroendocrine tumor Neuroendocrine tumor Yes/none
12 38/F Stomach/body 9 No Hypoechoic Not conclusive Granular cell tumor Discontinuance/surgery
13 78/F Stomach/antrum 7 No Hypoechoic Not conclusive Inflammatory fibroid polyp Yes/none
14 74/F Stomach/cardia 12 No Hypoechoic Not conclusive Leiomyosarcoma No/none
15 46/F Stomach/body 4 No Hypoechoic Neuroendocrine tumor Neuroendocrine tumor Yes/none
15 46/F Stomach/body 5 No Hypoechoic Neuroendocrine tumor Neuroendocrine tumor Yes/none
15 46/F Stomach/cardia 4 Yes Hypoechoic Not conclusive Neuroendocrine tumor Yes/none

ESD-CC, endoscopic submucosal dissection using a clutch cutter; SELEGSM, subepithelial lesions within the esophagogastric submucosa; M, male; F, female; SEL, subepithelial lesion.

Table 2.

Technical results of the ESD using the clutch cutter (n=18)

Overall (n=18) Esophagus (n=6) Stomach (n=12) p-value (esophagus vs. stomach)
Median diameter of the lesion (mm) 8 [4–14] (3–31) 10 [8–14] (4–15) 8 [8–12.5] (3–31) 0.480
Median diameter of resected specimen (mm) 25 [18–25] (10–60) 25 [18–25] (15–25) 25 [17–40] (10–60) 0.715
En bloc resection rate 17 (94.4) 6 (100.0) 11 (91.7) 1.00
R0 resection rate 16 (88.9) 6 (100.0) 10 (83.3) 0.529
Median operating time (min) 39 [20–63] (15–89) 27.5 [18–59] (15–63) 45 [25–82] (18–89) 0.171
Complication rate 0 (0) 0 (0) 0 (0) -
Perforation rate 0 (0) 0 (0) 0 (0) -
 Intra-ESD perforation rate 0 (0) 0 (0) 0 (0) -
 Post-ESD perforation rate 0 (0) 0 (0) 0 (0) -
Bleeding rate 0 (0) 0 (0) 0 (0) -
 Intra-ESD uncontrollable bleeding rate 0 (0) 0 (0) 0 (0) -
 Post-ESD bleeding rate 0 (0) 0 (0) 0 (0) -

Values are presented as median [interquartile range] (range) or number (%).

ESD, endoscopic submucosal dissection; -, incalculable.

Table 3.

Reported technical results of ESD for SELEGSM including those of the current study

Study Year Organ No. of lesions Device Procedure time (min) En bloc resection rate (%) R0 resection rate (%) Delayed bleeding rate (%) Perforation rate (%)
Hoteya et al.12 2009 Stomach 9 Hook knife, Flex knife 116.1 100 100 0 0
Białek et al.18 2012 Stomach 15 Needle knife, IT-knife ND 100 100 ND ND
Catalano et al.19 2013 Stomach 17 Hook knife, IT-knife 107.6 88.2 88.2 0 11.7
Kobara et al.13 2020 Esophagus, stomach 15 Needle knife ND 100 73.3 13.3 6.7
Our study 2024 Esophagus, stomach 18 Clutch Cutter 45.4 94.4 88.9 0 0

ESD, endoscopic submucosal dissection; SELEGSM, subepithelial lesions within the esophagogastric submucosa; ND, not described.