Efficacy of a Traction Device for Endoscopic Submucosal Dissection Using a Scissor-Type Knife: A Randomized Controlled Trial : Official journal of the American College of Gastroenterology | ACG

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ARTICLE: ENDOSCOPY

Efficacy of a Traction Device for Endoscopic Submucosal Dissection Using a Scissor-Type Knife: A Randomized Controlled Trial

Tamaru, Yuzuru MD, PhD1; Kuwai, Toshio MD, PhD FASGE, FJGES1; Miyakawa, Akihiro MD2; Kanazawa, Noriyoshi MD3; Kusunoki, Ryusaku MD, PhD1; Shimura, Haruhisa MD2; Uchiyama, Shiori MD, PhD3; Ishaq, Sauid FRCP, PhD4; Kohno, Hiroshi MD, PhD1

Author Information
The American Journal of Gastroenterology: November 2022 - Volume 117 - Issue 11 - p 1797-1804
doi: 10.14309/ajg.0000000000002019

Abstract

INTRODUCTION

Endoscopic submucosal dissection (ESD) enables en bloc resection regardless of tumor size, permitting high curative resection and low local recurrence rates (1–3). However, colorectal ESD is technically difficult, and certain organ characteristics (e.g., presence of folds and flexures, a narrow lumen, and a thin wall) can make the procedure even more challenging and increase the risk of perforation (2,4).

To overcome these issues, several types of ESD knives have been developed, in particular scissor-type knives provide easy manipulation similar to that provided using the biopsy forceps technique (5,6). There is no need to move the endoscope tip because the electric incision is made after grasping and fixing the area to be resected. Hence, scissor-type knives have been reported to be safer, with a lower perforation rate than needle-type knives, which are commonly used (5,7–11). However, decreased resection speed due to multiple steps, such as knife rotation, grasping, and dissection, is a drawback of scissor-type knives (6,8,11–13).

Traction-assisted methods for colorectal ESD with needle-type knives have been reported to increase the resection speed of colorectal ESD (14–19). However, reports regarding the effectiveness of colorectal ESD using scissor-type knives are few (11). Therefore, we hypothesized that the traction-assisted method could hasten the colorectal ESD procedure with the use of a scissor-type knife for overcoming the drawback of resection speed. For testing this hypothesis, we conducted a randomized controlled trial (RCT) to evaluate the efficacy of a traction device for colorectal ESD using a scissor-type knife.

METHODS

Trial design

This prospective, multicenter, parallel 2-arm, open-label, RCT was conducted at 3 Japanese institutions (Kure Medical Center and Chugoku Cancer Center, Asahi General Hospital, and Yokohama Rosai Hospital). The trial complied with the Declaration of Helsinki, and the trial protocol was approved by the ethics committees of all 3 participating institutions. This trial was registered on May 29, 2020, in the University Hospital Medical Network Clinical Trials Registry as UMIN000040582. All participants provided written informed consent for this trial before enrollment. The article was prepared according to the Consolidated Standards of Reporting Trials 2010 Statement (20).

Inclusion and exclusion criteria of patients

Patients, aged 20–90 years, with laterally spreading, superficial colorectal tumors (SCTs) of 20–50 mm in diameter considered difficult to remove en bloc with endoscopic mucosal resection and an Eastern Cooperative Oncology Group performance status range of 0–2 were screened for inclusion into the study. Patients were excluded if they had (i) an SCT predicted to be deep submucosal invasion cancer using magnifying endoscopic examinations, such as narrow-band imaging (e.g., Japan narrow-band imaging classification type 3) (21); (ii) local recurrence after endoscopic resection; (iii) inflammatory bowel disease or familial adenomatous polyposis; (iv) an inability to discontinue antithrombotic agents and anticoagulants (except for low-dose aspirin); or (v) confirmed or possible pregnancy.

ESD procedure

All procedures were performed by 7 expert endoscopists who were board-certified by the Japan Gastroenterological Endoscopy Society and had an experience of performing colorectal ESD using a scissor-type knife in at least 30 cases, while they had little or no experience in using a traction device.

All procedures were performed using a standard or therapeutic-type colonoscope (PCF-H290ZI, PCF-H290TI, PCF-Q260AZI, GIF-H290T, or GIF-Q260J; Olympus, Tokyo, Japan) with a transparent tip hood (Elastic Touch; Top, Tokyo, Japan, or SB Soft Hood; Sumitomo Bakelite, Tokyo, Japan). The colonoscope insertion and ESD procedure were performed with a CO2 insufflation regulation unit (UCR; Olympus) in all patients. A water-jet fluid solution was typically used with a mechanical water pump (OFP-2; Olympus). A scissor-type knife (Stag-Beetle Knife Jr or Jr 2 [SB Knife Jr (5)/Jr 2 (13); Sumitomo Bakelite, Tokyo, Japan]) was used during the ESD procedures, and which was also used for endoscopic hemostasis in bleeding situations. If repeated coagulation was required, hemostatic forceps (Coagrasper [FD410LR]; Olympus, or RAICHO2; Kaneka Medics, Tokyo, Japan) were used. A high-frequency generator (VIO300D; ERBE, Tubingen, Germany; or ESG 100; Olympus) was setup.

Conventional-ESD

Conventional-ESD (C-ESD) using a scissor-type knife was performed as previously reported (7,10). First, 0.4% sodium hyaluronate (MucoUp; Boston Scientific Japan, Tokyo, Japan) with a small amount of indigo carmine and epinephrine was injected into the submucosal layer using an injection needle. A circumferential incision was initiated from the anal side. The circumferential incision was extended, followed by submucosal dissection in a repeating manner until the entire lesion was resected.

C-ESD was switched to traction-ESD (T-ESD) if it was technically difficult to ensure adequate endoscopic visualization in cases of severe perforation or bleeding or if the duration of the procedure became unacceptably long (total operation duration >120 minutes).

Traction-ESD

For traction-ESD (T-ESD), a traction device was attached to the anal side of the lesion because the ESD procedure using a scissor-type knife is generally performed at a straightforward view. First, a circumferential incision without submucosal dissection was made. After separating the lesion from the surrounding normal mucosa, a partial dissection of the anal side was performed to create the mucosal flap. Subsequently, the traction device was attached to the edge of the peeled mucosal flap, and the other side was properly set. Traction devices and methods (S-O clip [18], clip-with-line traction [22], and multiloop traction device [23]) were selected based on the preference of each institute (Figure 1). The submucosa was dissected under direct visualization assisted by the traction device, and complete resection was achieved (Figure 2, see Supplementary Video 1).

F1
Figure 1.:
Devices used for colorectal endoscopic submucosal dissection in this study. (a) Stag-Beetle Knife Jr. (b) Stag-Beetle Knife Jr 2. (c) S-O clip. (d) Multiloop traction device.
F2
Figure 2.:
Traction-assisted endoscopic submucosal dissection using a scissor-type knife (the SB Knife Jr 2). (a) Circumferential incision is completed. (b) Sufficient traction is provided by the S-O clip, which can maintain good visualization of the submucosal layer. (c) Submucosal dissection proceeds speedily and safely toward the oral side of the lesion with the combination of the SB Knife Jr 2 and S-O clip. (d) En bloc resection is completed.

Outcomes and definitions

The primary outcome was the resection speed. Secondary outcomes included the ESD procedure time; en bloc, complete, and curative resection rates; rate of traction-related damage to the specimen; and incidence of adverse events (intraoperative perforation, delayed perforation, and delayed bleeding).

The resection speed (mm2/min) was defined as the calculated ratio of the resected specimen area (mm2) divided by the procedure time (minutes). The resected specimen area was calculated using the ellipse formula: area (mm2) = longest length (mm)/2 × shortest length (mm)/2 × 3.14. The ESD procedure time was defined as the time from the submucosal injection to the removal of the tumor (including the time to place the traction devices in case of the T-ESD group). En bloc resection was defined as the removal of the entire tumor in a single piece. Complete resection was defined as an en bloc resection with negative horizontal and vertical margins. Curative resection was defined as a histologically complete resection, with no risk of lymph node metastasis by histological examination of the resected specimen as per the Japanese Society for Cancer of the Colon and Rectum guideline criteria (24). Traction-related damage to the specimen was defined as any traction-related tear or split. Perforation was diagnosed if the peritoneal space could be directly observed during the procedure (intraoperative perforation) or if pneumoperitoneum was found on the post-ESD plain chest radiography or computed tomography (delayed perforation). Delayed bleeding was defined if any apparent bleeding or massive melena was observed that required endoscopic hemostasis and/or if the hemoglobin level fell by 2 g/dL or more compared with the last preoperative level.

Histopathologic diagnosis was performed by experienced pathologists at each institute in accordance with the World Health Organization classification system (25), and tumors were classified as adenoma, intramucosal adenocarcinoma, submucosal superficial invasive carcinoma (<1,000 μm), or submucosal deep invasive carcinoma (≥1,000 μm). Lesions were classified into the following 2 macroscopic types of laterally spreading tumors (LSTs): granular LST and nongranular LST (26,27).

Randomization

Randomization was stratified according to institution, location (colon or rectum), and tumor morphology (granular LST or nongranular LST). Subsequently, eligible patients were randomly assigned in a 1:1 ratio to the C-ESD group or T-ESD group through the minimization method (28) using an electronic data capture system (University Hospital Medical Information Network Internet Data and Information system for Clinical and Epidemiological research, Cloud version). The ESD operators and assistants were informed of each patient's study arm assignment a few days before or on the day of the procedure. The allocation table was known only to the operators and assistants. Patients and pathology staff were blinded to the treatment allocated pending the outcome of the histopathologic examination.

Statistical analysis

The sample size was calculated based on the resection speed. In our pilot study, the mean resection speed of the T-ESD group was faster than that of the C-ESD group by 13.8 mm2/min. The common SD of the T-ESD and C-ESD groups were 12.3 and 10.8 mm2/min, respectively. Therefore, we assumed that the mean resection speed of the T-ESD group was shorter than that of the C-ESD group by 9 mm2/min, with a common SD of 15 mm2/min for the 2 groups. We estimated that ≥88 participants would be required to detect a significant difference between the groups with a significance level of 0.05 (2-sided) and a power of 80%. We determined that 100 participants would be required, considering approximately 10% for protocol deviations and dropouts.

Normally distributed continuous variables are reported as mean ± SD and were compared using the Student t test. Continuous variables that were not normally distributed are reported as medians and interquartile ranges, and they were compared using the Mann-Whitney U test. The χ2 test or Fisher exact test was used for analysis of the categorical data. P < 0.05 (2-sided) was considered significant. All statistical analyses were performed using JMP Pro 16 (SAS Institute, Cary, NC).

RESULTS

Baseline characteristics of the enrolled patients and lesions

Between October 2020 and December 2021, 100 patients with SCTs were enrolled in this study (Figure 3). Of these, 2 patients who did not meet the inclusion criteria were excluded. Therefore, 98 patients were randomly assigned to the C-ESD (n = 49) or T-ESD (n = 49) group. Because 1 patient in the T-ESD group underwent ESD for a different lesion, 97 patients (97 lesions) were included in the analysis cohort.

F3
Figure 3.:
Study flowchart of the participants.

The baseline characteristics were well balanced between the 2 groups (Table 1); no significant differences were observed between the groups with respect to age, sex, performance status, tumor location, macroscopic type, or institution. Regarding the histopathologic diagnosis, there were no significant differences between the groups (Table 2). The median resected specimen size was 40 mm in the C-ESD group and 39 mm in the T-ESD group (P = 0.36), and the median tumor size after resection was 31 mm in the C-ESD group and 27 mm in the T-ESD group (P = 0.06).

T1
Table 1.:
Clinicopathological characteristics of patients and lesions (n = 97)
T2
Table 2.:
Clinicopathological characteristics of resected lesions (n = 97)

Resection speed and other ESD-related outcomes

The primary outcome of this study, the mean resection speed, was not significantly different between the C-ESD and T-ESD groups (23.7 ± 12.2 mm2/min vs 25.6 ± 11.4 mm2/min, respectively; P = 0.43) (Table 3). However, the mean procedure time in the T-ESD group was significantly shorter than that in the C-ESD group (47.3 ± 25.6 min vs 62.3 ± 39.7 minutes, respectively; P = 0.03). The proportions of en bloc (100% vs 100%), complete resection (98.0% vs 97.9%; P = 1.00), and curative resection (93.9% vs 91.7%; P = 0.71) were similar between the groups. One case in the C-ESD group required the use of a traction device because the visibility was very poor due to severe fibrosis in the submucosal layer. There were no cases of traction-related damage to the specimen.

T3
Table 3.:
ESD-related outcomes (n = 97)

Regarding adverse events, there was no significant difference between the groups. Perforation during the procedure occurred in only 1 patient in the T-ESD group, which was managed by endoscopic clipping and conservative therapy. Delayed hemorrhage after ESD occurred in only 1 patient in the T-ESD group and was managed by endoscopic hemostasis (Table 3).

Subgroup analyses of resection speed

Regarding the subgroup analysis of the resection speed related to locations, the mean resection speed at the cecum of the T-ESD group was significantly faster than that of the C-ESD group (32.4 ± 9.8 mm2/min vs 16.7 ± 9.3 mm2/min, respectively; P = 0.02). There were no significant differences at the other locations between the groups (Table 4).

T4
Table 4.:
Results of the subgroup analysis of resection speed related to locations between the 2 groups (n = 97)

Regarding the subgroup analysis of the resection speed related to tumor size, for tumors ≥30 mm in diameter, the mean resection speed of the T-ESD group tended to be faster than that of the C-ESD group (34.6 ± 10.5 mm2/min vs 27.8 ± 11.9 mm2/min, respectively; P = 0.054) (Table 5).

T5
Table 5.:
Results of the subgroup analysis of resection speed related to tumor size between the 2 groups (n = 97)

DISCUSSION

In this multicenter RCT, although we did not confirm the superiority of T-ESD over C-ESD for resection speed in the entire cohort, we found that the resection speed of T-ESD was significantly faster than that of C-ESD for lesions in the cecum. In addition, the speed of T-ESD tended to be faster than that of C-ESD for large lesions (≥30 mm). We also comfirmed that the resection rates were sufficiently high and adverse event rates were extremely low in both the groups.

Regarding the resection speed in this study, the use of a traction device could hasten ESD using a scissor-type knife for lesions in the cecum, but there was no difference in the overall location. Traction-assisted techniques have been reported to hasten colorectal ESD using a needle-type knife, regardless of the location, and the following 2 main effects were noted: good visualization of the submucosal layer and appropriate tension of the target tissue, allowing for efficient dissection (11,14–19). Lesions in the cecum were considered as a predicting factor for difficult colorectal ESD because most lesions in the cecum have the muscular layer towering over the cliff at the time of the incision and dissection manipulation (29). In this condition, visibility of the submucosal layer is poor and the risk of perforation is increased, requiring careful dissection operations and a slower dissection speed. The traction device could be more effective for dissections in the cecum than those in other locations for improving the visibility of the submucosal layer and the dissection operation could be performed in a near-horizontal position, allowing for safe and speedy resection of ESD in the cecum.

In addition, there was a tendency for the traction device to hasten colorectal ESD using a scissor-type knife for large lesions (≥30 mm). A tumor size of ≥30 mm is considered a significant predicting factor for difficult colorectal ESD (29). The frequency of fibrosis in the submucosal layer can increase with lesion size because the submucosa is more susceptible to mechanical forces between the submucosal and muscle layer during intestinal peristalsis (30). In addition, gravity can impede the visual field during dissection due to large resection fragment interference (31,32). Under these situations, we believe that the use of a traction device may have increased the resection speed because it improved the view of the submucosal layer, which would have been accompanied by fibrosis and/or large resection fragments. Given these considerations, we recommend using a traction device for colorectal ESD with a scissor-type knife for lesions in the cecum and/or those ≥30 mm. In addition, a traction device may be useful for other lesions if the dissection plane is not clearly visible. We believe that this technique could be an effective solution for overcoming the drawback of scissor-type knives (i.e., slower resection speed). We also found that the procedure time of T-ESD was significantly shorter than that of C-ESD, even in cases of slightly smaller tumor size.

Regarding efficacy and safety, the resection rates were sufficiently high and adverse events rates were extremely low in not only the C-ESD group but also the T-ESD group in this study, similar to those reported in previous studies (11,15,18). The ESD procedure using a scissor-type knife allows incision, dissection, and hemostasis manipulation to be performed by opening and closing the scissor and moving the sheath in and out only and can be performed with the scope tip fixed, eliminating the need to swing it around as required with a needle-type knife. Moreover, after grasping the target tissue, the scissor-type knife can be pulled a little to ensure that the muscle layer is not gripped before energizing; thus, scissor-type knives are uniquely designed to minimize the risk of perforation (7,10). In fact, these characteristics are responsible for the significantly lower perforation and delayed bleeding rates observed in colorectal ESD using a scissor-type knife, compared with those using a needle-type knife (8). Based on our data and these findings, we believe T-ESD could be used without adversely affecting these advantages of scissor-type knives and is expected to provide the same safer ESD as previously reported. Therefore, a scissor-type knife has the potential of being close to an ideal knife for colorectal ESD, especially for lesions in the proximal colon and/or those ≥30 mm.

This study has several limitations. First, endoscopists were not blinded to the group allocation, raising concerns for selection bias. However, we treated the patients in both groups in a qualified manner using the procedures described in the “Methods” section. Second, some details of the treatment strategy, such as knife selection (SB Knife Jr or Jr2), traction device selection, and high-frequency generator selection; ESD methods, including pocket-creation and tunneling method; and prophylactic vessel coagulation and clip closure for a mucosal defect after ESD were left to the discretion of each institution. However, these are standardized at each institution, and randomization was stratified according to the institution. Therefore, this impact is minimal. Third, the tumor size in the T-ESD group tended to be smaller than that in the C-ESD group. Resection speed was calculated on the resection area and therefore depend on the lengths of the resected specimen. Because there was no significant difference in the lengths of the resected specimen between the groups, we considered this not to be a source of bias. Fourth, the sample size, per the subgroup analysis, was small; however, statistically significant difference and trend were observed. To confirm these results, further RCTs with larger sample sizes would be needed. Fifth, long-term outcomes such as the recurrence rate were not evaluated.

In conclusion, colorectal ESD using a scissor-type knife performed either conventionally or with a traction device is technically efficient and safe. The results of our RCT suggested that a traction device for ESD using a scissor-type knife could be effective in increasing the resection speed for lesions in the cecum and/or those ≥30 mm. The addition of a traction device in these difficult cases may help overcome the drawback of slow resection speed reported with the use of a scissor-type knife.

CONFLICTS OF INTEREST

Guarantors of the article: Yuzuru Tamaru, MD, PhD, and Toshio Kuwai, MD, PhD, FASGE, FJGES.

Specific author contributions: Drafting of the article: Y.T.; conception and design: Y.T., T.K.; clinical data collection and interpretation of the data: Y.T., T.K., A.M., N.K., H.S., S.U.; analysis of the data: R.K.; and critical revision of the article for important intellectual content: S.I., H.K. All authors read and approved the final manuscript.

Financial support: None to report.

Potential competing interests: None to report.

Clinical trial registration number: UMIN000040582 (URL: https://www.umin.ac.jp/ctr/index.htm).

Study Highlights

WHAT IS KNOWN

  • ✓ A scissor-type knife provides safer and technically easier colorectal endoscopic submucosal dissection (ESD) than a needle-type knife.
  • ✓ However, slower resection speed was pointed out as its drawback.
  • ✓ Traction-assisted methods for colorectal ESD with a needle-type knife have increased the resection speed.
  • ✓ However, the effectiveness of these methods with a scissor-type knife remains unclear.

WHAT IS NEW HERE

  • ✓ Colorectal ESD using a scissor-type knife with/without traction devices is technically efficient and safe.
  • ✓ Traction devices for ESD using a scissor-type knife in the proximal colon and/or those lesions ≥30 mm may increase the resection speed.
  • ✓ The addition of traction devices in these cases may be a solution for overcoming the drawback of a scissor-type knife.

ACKNOWLEDGEMENTS

The authors extend thanks to Naoko Matsumoto for administrative assistance.

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