Abstract
Endoscopic submucosal dissection (ESD) of fibrotic colorectal lesions is difficult and has a high complication rate. There are only a few reports on the utility of orthodontic rubber band (ORB) traction in reducing the difficulty of this procedure. This study aimed to investigate the risk factors for perforation when applying ORB traction during ESD of fibrotic colorectal lesions. We continuously collected the clinical data of 119 patients with fibrotic colorectal lesions who underwent ESD with ORB and clip traction between January 2019 and January 2024. Possible risk factors for perforation were analyzed. The median ORB-ESD operative time was 40 (IQR 28–62) min, and the en bloc and R0 resection rates were 94.1% and 84.0%, respectively. Perforation occurred in 16 of 119 patients (13.4%). The lesion size, lesion at the right half of the colon or across an intestinal plica, the degree of fibrosis, operation time, and the surgeon’s experience were associated with perforation during ORB-ESD (P < 0.05). Multivariate logistic regression analysis showed that lesions in the right colon (OR 9.027; 95% CI 1.807–45.098; P = 0.007) and those across an intestinal plica (OR 7.771; 95% CI 1.298–46.536; P = 0.025) were independent risk factors for perforation during ORB-ESD. ORB-ESD is an effective and feasible approach to treat fibrotic colorectal lesions. Adequate preoperative evaluation is required for lesions in the right colon and across intestinal plicas to mitigate the risk of perforation.
Keywords: Orthodontic rubber band, Endoscopic mucosal dissection, Fibrosis, Perforate
Subject terms: Gastroenterology, Colonoscopy
Introduction
Many factors affect the difficulty of endoscopic submucosal dissection (ESD), including the tumor size and location, lesions spreading across multiple folds, deep submucosal invasion, respiratory movement1, and submucosal lesion fibrosis1–4. Colorectal fibrosis might be associated with multiple factors, including preoperative biopsy, inflammation (e.g., ulcerative colitis), lesions in the caecum, residual or recurrent colorectal lesions after endoscopic treatment, lesions spanning multiple folds, large eminence, mixed nodules, and pseudo-depressed nongranular type in lateral spreading tumors5–8.
In clinical practice, lesion fibrosis is an important reason endoscopists with limited experience cannot independently complete colorectal ESD. Submucosal fibrosis affects the surgical completion rate of junior endoscopists and is sometimes a challenge to senior endoscopists as well. Endoscopists continuously strive to reduce the difficulties posed to ESD by colorectal fibrosis. Our team previously reported that orthodontic rubber band (ORB) traction could improve the efficiency of gastric9 and colorectal10 ESD procedures. However, only a few studies assessed the utility of ORB traction in improving efficiency and reducing the difficulty of ESD when operating fibrotic colorectal lesions. Therefore, this study aimed to explore the application value and risk factors for perforation when using ORB traction during ESD of colorectal lesions complicated by fibrosis.
Data and methods
Patients
We continuously collected data on patients with fibrotic colorectal lesions who underwent ESD with ORB and clip traction at 900TH Hospital of Joint Logistics Support Force hospital between January 2019 and January 2024. The inclusion criteria scheduled to undergo ORB-ESD were: (1) with previous endoscopic mucosal resection (EMR) or endoscopic piecemeal mucosal resection (EPMR) or ESD at any hospital, postoperative residual or recurrent lesion, previous surgical management, or a new colorectal tumor near an anastomosis; (2) EMR treatment was performed for colorectal adenoma, carcinoma, or neuroendocrine tumors, and ESD was added since postoperative pathology indicated that tumor residue or basal incisal margin could not be determined; (3) poor lifting of submucosal injection during ESD, and lesion adhesion, such as white reticular or muscle structure without a blue transparent layer, presented by submucosal injection during ESD. The exclusion criteria were: (1) patients undergoing traditional ESD or ESD with dental floss or magnetic bead traction; (2) patients undergoing hybrid ESD. One hundred and fifty-one patients underwent ESD of fibrotic lesions during the study period. All patients signed a preoperative informed consent form. The study was conducted in accordance with the tenets of the Declaration of Helsinki and was approved by the Ethics Committee of the 900th Hospital of Joint Logistics Support Force hospital (ID 2022-012). After excluding those treated by ESD with dental floss (n = 4) and magnetic bead (n = 3) traction, and traditional (n = 9) and hybrid (n = 16) ESD, the final analysis included 119 patients.
ESD equipment
We used a single-channel therapeutic gastroscope or a therapeutic colonoscope (GIF-Q260J/PCF-Q260JI; Olympus Co., Tokyo, Japan) with a transparent hood ((D-201-11804; Olympus Co., Tokyo, Japan) and water delivery function for ESD. The injection needle was NM-4U injection needle (Olympus Co., Tokyo, Japan), the cutting knife was a 1.5mm DUAL knife e (Olympus Co., Tokyo, Japan) or a golden knife (MK-T-2-195, Micro-tech (Nanjing) Co., Nanjing, China). Other equipment includes electrosurgical generator (VIO200S; Elektromedizin Gmbh, Tubingen, Germany), opening-and-closing clip (Micro-tech (Nanjing) Co., Nanjing, China), 6.5mm inner diameter of ORB and hemostatic forceps (Coagrasper, Olympus Co.).
ORB-ESD procedure
The lesion was marked or not marked, the peripheral mucosa was incised, and the subsequent dissected process was completed after traction with the fox orthodontic rubber band and clips (one clip combined with ORB was placed on one side of the incision mucosa, and the other clip pulled the lesion to the opposite side, exposing the space for dissection and completing the subsequent dissection process) (Fig. 1).
Figure 1.
Procedure of ORB-ESD. (a) Periannular incision; (b) ORB combined clip traction and the submucosa was well exposed; (c) Complete resection of the lesion.
Data recording and definitions
For all included patients, we recorded data pertaining to ORB-ESD-associated perforation, preoperative and operative variables that might affect the incidence of perforation, and ORB traction surgical and postoperative data. Preoperative information included sex, age, lesion shape, location, and size, lesion across an intestinal plica, and previous endoscopic treatment history.
The lesions were classified as polypoid eminence or laterally spreading tumor (LST). Lesion locations included the rectum, the left half of the colon, and the right half of the colon. The left half of the colon included the sigmoid colon and the descending and the left half of transverse colon. The right half of the colon included the right half of the transverse colon, ascending colon, and cecum. The size was divided into lesions ≥ 30 mm and < 30 mm. The history of endoscopic treatments included whether EMR, EPMR, or ESD had been performed and whether the lesion was residual or recurrent. Local recurrent lesions after endoscopic resection were either complete (the lesion appeared in the same site) or residual (the original lesion was only partially resected)11.
Surgical information included degree of fibrosis, submucosal injection lift, visual field exposure, doctor’s experience, duration of operation, en bloc resection, R0 resection and ESD-related adverse events (perforation, bleeding). Perforation was a full penetration through the intestinal wall during ESD, making the omentum visible, or free gas was observed in the abdominal cavity on postoperative abdominal plain radiographs or computed tomography (CT).
The degree of fibrosis was divided into F0, no fibrosis, with a visible blue transparent layer on the submucosa; F1, mild fibrosis, with a submucosal white network observed after submucosal injection; F2, severe fibrosis, showing a white muscle structure and no blue transparent layer under the mucosa12 (Fig. 2). If both F0 and F2 were present, fibrosis was recorded as F2. The surgeon’s experience was divided into expert (≥ 300 colorectal ESD) and non-expert (< 300 procedures) groups.
Figure 2.
(a) F1, mild fibrosis, with a submucosal white network observed after submucosal injection; (b) F2, severe fibrosis, showing a white muscle structure and no blue transparent layer under the mucosa.
ORB-ESD postoperative information included R0 resection (R0 resection was total lesion resection with negative horizontal and vertical margins) (yes/no) and pathology results: M:the lesions were confined to the mucosal layer; SMs: shallow submucosal infiltration (depth < 1000 µm); SMd: deep submucosal infiltration (depth ≥ 1000 µm); NET: neuroendocrine tumour.
Statistical analysis
Statistical analysis was performed using IBM SPSS Statistics for Windows, Version 25.0 (IBM Corp., Armonk, NY, USA). Continuous variables are expressed as means ± SDs or median (interquartile range, IQR), while categorical variables are expressed as counts (percentages). A chi-squared or Fisher exact probability test and multivariate logistic regression analysis were used to evaluate the contribution of each variable to the risk of perforation during ORB-ESD of fibrotic colorectal lesions. Statistical significance was set as P < 0.05.
Results
Clinical baseline patient information
One lesion per patient was treated with ORB-ESD. The 119 patients (age 59.0 ± 12.3 included 67 males (56.3%) and 52 females (43.7%). Table 1 showed the preoperative information of the patients. The median operation time was 40 (IQR 28–62) min. The ORB-ESD procedure was completed by an expert in 88 cases (73.9%) and by a non-expert in 31 cases (26.1%). The en bloc resection rate was 94.1%, and the R0 resection rate was 84.0%. Postoperative pathology detected infiltration of the mucosal layer, SMs, SMd, and NET in 63.0%, 12.6%, 16.0%, and 8.4% of the cases, respectively (Table 1).
Table 1.
Characteristics of patients with fibrotic colorectal lesions treated by ORB-ESD.
| Variable | Total cases (n = 119) |
|---|---|
| Age (years; mean ± SD) | 59.0 ± 12.3 |
| Sex, n (%) | |
| Male | 67 (56.3) |
| Female | 52 (43.7) |
| Lesion size, [mm; median (IQR)] | 15 (10–25) |
| Cause of fibrosis, n (%) | |
| Residual or recurrent tumors associated with EMR/EPMR/ESD | 46 (38.7) |
| Focal fibrosis | 69 (58.0) |
| Neorectal lesions adjacent to an anastomosis | 4 (3.3) |
| Lesion location, n (%) | |
| Rectum | 59 (49.6) |
| Left colon | 33 (27.7) |
| Right colon | 27 (22.7) |
| Lesion morphology, n (%) | |
| Polypoid eminence | 32 (26.9) |
| Granular LST | 28 (23.5) |
| Non-granular LST | 9 (7.6) |
| Lesions combined with scarring | 50 (42.0) |
| Degree of fibrosis, n (%) | |
| F1 | 79 (66.4) |
| F2 | 40 (33.6) |
| Lesion across an intestinal plica, n (%) | 14 (11.8) |
| Operative time [min; median (IQR)] | 40 (28–62) |
| Doctor qualification, n (%) | |
| Expert | 88 (73.9) |
| Non-expert | 31 (26.1) |
| En bloc resection, n (%) | 112 (94.1) |
| R0 resection, n (%) | 100 (84.0) |
| Perforation, n (%) | 16 (13.4) |
| Bleeding, n (%) | 3 (2.5) |
| Pathology results, n (%) | |
| M | 75 (63.0) |
| SMs | 15 (12.6) |
| SMd | 19 (16.0) |
| NET | 10 (8.4) |
ORB, Orthodontic rubber band; ESD, endoscopic mucosal dissection; EMR, endoscopic mucosal resection; EPMR, endoscopic piecemeal mucosal resection; LST, lateral spreading tumor; IQR, interquartile range; M, mucosal lesions; SMs, shallow submucosal infiltration (depth < 1000 µm); SMd, deep submucosal infiltration (depth ≥ 1000 µm); NET, neuroendocrine tumour.
Among the 119 patients, 3 (2.5%) had delayed hemorrhage. The bleeding events were successfully stopped postoperatively using an endoscope. Perforation occurred in 16 patients (13.4%); 15 underwent endoscopic hemostatic clips closure, and one was transferred to surgery. We compared the preoperative, surgical, and postoperative data of patients with perforation (perforated; n = 16) to those without (non-perforated; n = 103) in search of risk factors for perforation during ORB-ESD of fibrotic colorectal lesions.
Comparison of clinical baseline data between the perforated and non-perforated groups
The perforated [age 62.7 ± 9.5 years; six males (37.5%) and ten females (62.5%)] and non-perforated [age 58.46 ± 12.43 years; 61 males (59.2%) and 46 females (40.8%)] groups were similar in sex ratio and age (P = 0.114). Lesions of ≥ 30 mm occurred in 8 (50.0%) patients in the perforated group and 22 (21.4%) in the non-perforated group. The respective values for lesions of < 30 mm were 8 (50.0%) and 81 (78.6%). The rates differed significantly between the groups (P = 0.026). The lesions in the perforated group were in the rectum (4; 25.0%), right colon (4; 25.0%), and left colon (8; 50.0%). The respective rates in the non-perforated group were 55 (53.4%), 19 (18.4%), and 29 (28.2%). The rates differed significantly between the groups (P = 0.019). The proportion of lesions across an intestinal plica in the perforated group was higher than in the non-perforated group (43.8% vs. 7.8%, P = 0.001). Fibrosis in the perforated group was F1 in seven cases (43.7%) and F2 in nine cases (56.3%). The respective rates in the non-perforated group were 72 (69.9%) and 31 (30.1%). The rates differed significantly between the groups (P = 0.049). The groups were similar in the cause of fibrosis (P = 0.516) and the lesion shape (P = 0.397) (Table 2).
Table 2.
Baseline patient characteristics and surgical information compared between the perforated and non-perforated groups.
| Variable | Perforated group (n = 16) |
Non-perforated (n = 103) |
P-value |
|---|---|---|---|
| Age (years; mean ± SD) | 62.7 ± 9.5 | 58.5 ± 12.4 | 0.202T |
| Sex, n (%) | 0.114 C | ||
| Male | 6 (37.5) | 61 (59.2) | |
| Female | 10 (62.5) | 42 (40.8) | |
| Lesion size [mm; median (IQR)] | 20.0 (18.5–30.0) | 15.0 (10.0–25.0) | 0.010 W |
| Lesion size, n (%) | 0.026 F | ||
| < 30 mm | 8 (50.0) | 81 (78.6) | |
| ≥ 30 mm | 8 (50.0) | 22 (21.4) | |
| Cause of fibrosis, n (%) | 0.516 F | ||
| Residual or recurrent tumors associated with EMR/EPMR/ESD | 5 (31.3) | 41 (39.8) | |
| Neorectal lesions adjacent to an anastomosis | 1 (6.3) | 3 (2.9) | |
| Focal fibrosis | 10 (62.5) | 59 (57.3) | |
| Lesion location, n (%) | 0.019 F | ||
| Rectum | 4 (25.0) | 55 (53.4) | |
| Left colon | 4 (25.0) | 29 (28.2) | |
| Right colon | 8 (50.0) | 19 (18.4) | |
| Lesion morphology, n (%) | 0.397 F | ||
| Polypoid eminence | 7 (43.8) | 25 (24.3) | |
| Granular LST | 3 (18.8) | 25 (24.3) | |
| Non-granular LST | 0 (0) | 9 (8.7) | |
| Lesions combined with scarring | 6 (37.5) | 44 (42.7) | |
| Degree of fibrosis, n (%) | 0.049 C | ||
| F1 | 7 (43.7) | 72 (69.9) | |
| F2 | 9 (56.3) | 31 (30.1) | |
| Lesion across an intestinal plica, n (%) | 7 (43.8) | 8 (7.8) | 0.001 F |
| Operative time [min; median (IQR)] | 73.0 (40.3–125.5) | 39.0 (28.0–52.0) | 0.003 W |
| Doctor qualification, n (%) | 0.035 F | ||
| Expert | 8 (50.0) | 79 (76.7) | |
| Non-expert | 8 (50.0) | 24 (23.3) | |
| En bloc resection, n (%) | 12 (75.0) | 100 (97.1) | 0.006 F |
| R0 resection, n (%) | 11 (68.8) | 89 (86.4) | 0.133 F |
| Pathology results, n (%) | 0.146 F | ||
| M | 8 (50.0) | 67 (65.0) | |
| SMs | 4 (25.0) | 11 (10.7) | |
| SMd | 4 (25.0) | 15 (14.6) | |
| NET | 0 (0) | 10 (9.7) |
ORB, Orthodontic rubber band; ESD, endoscopic mucosal dissection; EMR, endoscopic mucosal resection; EPMR, endoscopic piecemeal mucosal resection; LST, lateral spreading tumor; IQR, interquartile range; M, mucosal lesions; SMs, shallow submucosal infiltration (depth < 1000 µm); SMd, deep submucosal infiltration (depth ≥ 1000 µm); NET, neuroendocrine tumour.
TStudent’s t test, WMann-Whitney U test, CChi-squared test, FFisher’s exact test.
Comparison of operative and postoperative variables between the perforated and non-perforated groups
The median operative time of the perforated group was significantly longer than that of the non-perforated group [73.0 (40.3–125.5) vs. 39.0 (28.0–52.0) min, P = 0.003]. In the perforated group, eight cases (50.0%) were performed by experts and 8 (50.0%) by non-experts. The respective numbers in the non-perforated group were 79 (76.7%) and 24 (23.3%). The rates differed significantly between groups (P = 0.035). The en bloc resection rate in the perforated group was lower than in the non-perforated group (75.0% vs. 97.1%, P = 0.006), while the R0 resection rate in the perforated group (68.8%) was similar to that in the non-perforated group (86.4%; P = 0.133). The groups were also similar in the postoperative pathological results (P = 0.146; Table 2).
Multivariate analysis of risk factors for perforation during ORB-ESD of fibrotic colorectal lesions
Table 2 shows that the lesion size, lesion location, whether it crosses an intestinal plica, the degree of fibrosis, the duration of operation, and the experience of the operating physician were associated with perforation during ORB-ESD of fibrotic colorectal lesions (P < 0.05). We incorporated these factors into the multivariate logistic regression model. The results showed that lesions in the right colon (OR 9.027; 95% CI 1.807–45.098; P = 0.007) and those crossing an intestinal plica (OR 7.771; 95% CI 1.298–46.536; P = 0.025) were independent risk factors for perforation during ORB-ESD of fibrotic colorectal lesions (Table 3).
Table 3.
Predictive factors for perforation in colorectal fibrosis treated with ORB-ESD.
| Factors | OR value | 95% CI | P value |
|---|---|---|---|
| Right semicolon | 9.027 | 1.807–45.098 | 0.007 |
| Across the fold | 7.771 | 1.298–46.536 | 0.025 |
ORB, Orthodontic rubber band; ESD, endoscopic mucosal dissection;
Discussion
In this study, ORB-ESD of fibrotic colorectal lesions was safe and effective, with a median operative time of 40 (IQR 28–62) min, en block resection rate of 94.1%, R0 resection rate of 85.5%, bleeding rate of 2.5%, and perforation rate of 13.4%. Multivariate logistic regression analysis suggested that lesions in the right colon and those crossing an intestinal plica were independent risk factors for perforation during ORB-ESD of fibrotic colorectal lesions.
There are many causes of colorectal fibrosis. In this study, fibrosis was caused by endoscopic treatment or surgical resection in 42% of the cases, while the remaining 58.0% were colorectal lesions complicated with fibrosis due to endoscopic biopsy performed for all such lesions before ESD, and some were large uplift or LST type lesions, consistent with previous reports on risk factors for colorectal fibrosis8,13. Colorectal fibrosis is a recognized cause of difficult ESD3,14,15 because fibrosis causes submucosal adhesions, poor lift following submucosal injection, limited surgical field of view, and ineffective electro-knife dissection. It also leads to extended operation time16, increased incomplete resection rate3, and occasional inability to complete the ESD procedure17. Therefore, reducing the difficulty of ESD of fibrotic colorectal lesions is presently a pressing and difficult problem, with reports of hybrid or underwater ESD18, pocket traction3, and internal traction11 aiming to overcome this hurdle.
Tanaka et al.19 reported that ESD of local residual or recurrent colorectal tumors achieved an en bloc resection rate of 96.3%, R0 resection rate of 83.3%, and median operative time of 65 min. The en bloc (94.1%) and R0 (85.5%) resection rates in our study using ORB-ESD with a clip were similar to those of Tanaka et al. However, our median operative time (40 min) was considerably shorter, possibly because the ORB traction can enlarge the submucosal space, even in fibrotic lesions, thus shortening the operative time. Therefore, ORB traction is clinically advantageous for fibrotic colorectal lesions.
It has been reported that the incidence of colorectal perforation during ESD is 1.4–10.4%20–23 and that pathological fibrosis was a risk factor for colorectal perforation13,24. A small-sample study reported perforation rates of 10.8% and 0% when treating colorectal fibrosis by hybrid and underwater ESD, respectively18. Faller et al.11 had a perforation rate of 7.5% when using rubber band traction to assist in resecting colorectal polyp residue or re-issued ESD. The present study used ORB traction during ESD of fibrotic colorectal lesions, resulting in a perforation rate of 13.5% (16/119). This high rate might be because procedures performed by non-experts contributed to half of the perforations. When the non-expert group performed the ESD procedure, the pulling of the ORB may cause the myometrium to lift at part of the adhesion. In the non-expert group, the anatomical space was not clear, leading to the perforation event. Moreover, the median direct lesion size in the perforated group [20.0 (18.5–30.0) mm] was larger than in the non-perforated group [15.0 (10.0–25.0) mm], which may have been a factor in the high perforation rate in this study.
Fibrosis might prolong the operation time because lesion adhesion requires more careful dissection, sometimes with a point dissection. Moreover, the more severe the adhesion, the longer it takes to separate it at the anatomic level, and the higher the ESD-related complication rate25,26. In this study, the rate of cases with severe fibrosis (F2) in the perforated group was higher than in the non-perforated group (56.3% vs. 30.1%), and the operative time was longer (73.0 vs. 39.0 min). Adhesions might also reduce the incomplete, R0, and curative resection rates16,27. In our study, the en bloc (75.0% vs. 97.1%) and R0 (68.8% vs. 86.4%) resection rates in the perforated group were lower than in the non-perforated group.
A lesion across an intestinal plica is a risk factor for perforation during the ESD procedure1,28. Procedures in the right half of the colon are greatly affected by respiratory movement, and endoscope stability is poor in some positions in this region. Consequently, lesions in the right half of the colon were one of the reported factors influencing the difficulty of colorectal ESD operation1,29. Our multivariate logistic regression results showed that lesions in the right half of the colon (OR 9.027, 95% CI 1.807–45.098) and those across an intestinal plica (OR 7.771, 95% CI 1.298–46.536) were independent risk factors for perforation during ORB-ESD of fibrotic colorectal lesions. Preoperative evaluation should be particularly meticulous when such lesions are present, the procedure must be performed cautiously, and allowing more experienced physicians to perform these procedures might be safer.
There were some limitations to this study. First, this was a small sample single-center study. A larger sample multi-center prospective study is needed to confirm our results and promote their clinical application. Second, some scholars reported that the preoperative Vi and Vn pit pattern types were independent risk factors for colorectal fibrosis16. Due to the long period covered by our study, crystal violet staining typing was not performed before ESD in some patients. Therefore, this factor was not included in this study; it could be addressed in future studies.
In summary, colorectal fibrosis poses a high risk of complicating the ESD procedure. This study reconfirmed the effectiveness of ORB traction in colorectal fibrosis treatment. It is particularly important to establish a preoperative treatment plan and reasonable application of an intraoperative traction method (e.g., ORB) in patients with fibrotic colorectal lesions in the right half of the colon or across intestinal plicas.
Author contributions
L.Z., B.X. and F.W.: Data Curation, Writing-original Draft. L.C., B.L., Z.L., X.G. and L.Z.: Data Curation. R.W. and C.J.: software, Validation. D.L. and W.W.: Funding Acquisition, Supervision, Writing-Review & Editing.
Funding
This project was supported by the Fujian Science and Technology Guiding Fund Project [Grant No. 2023Y0070], the Foreign Cooperation Project of the Department of Science and Technology of Fujian Province (2022I0033) and Key Subject Funds of Joint Logistics Support Force [Grant No. LQZD-XH].
Data availability
The data sets used and analyzed in this study are available from the corresponding author upon reasonable request.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
These authors contributed equally: Linfu Zheng, Binbin Xu, and Fuqiang Wang.
Contributor Information
Dazhou Li, Email: LDZ7302999@sina.com.
Wen Wang, Email: wangwenfj@163.com.
References
- 1.Imai, K. et al. Preoperative indicators of failure of en bloc resection or perforation in colorectal endoscopic submucosal dissection: Implications for lesion stratification by technical difficulties during stepwise training. Gastrointest. Endosc.83(5), 954–962 (2016). 10.1016/j.gie.2015.08.024 [DOI] [PubMed] [Google Scholar]
- 2.Félix, C. et al. Outcomes and learning curve in endoscopic submucosal dissection of rectal neoplasms with severe fibrosis: Experience of a Western Center. GE Port. J. Gastroenterol.30(3), 221–229 (2023). 10.1159/000522579 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Tanaka, H. et al. Diagnostic and therapeutic strategies for colorectal tumor with positive muscle-retracting sign. DEN Open4(1), e278 (2024). 10.1002/deo2.278 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Steinbrück, I. et al. Predictive factors for the outcome of unsupervised endoscopic submucosal dissection during the initial learning curve with prevalence-based indication. Dig. Dis. Sci.68(9), 3614–3624 (2023). 10.1007/s10620-023-08026-9 [DOI] [PubMed] [Google Scholar]
- 5.Fukunaga, S. et al. Impact of preoperative biopsy sampling on severe submucosal fibrosis on endoscopic submucosal dissection for colorectal laterally spreading tumors: A propensity score analysis. Gastrointest. Endosc.89(3), 470–478 (2019). 10.1016/j.gie.2018.08.051 [DOI] [PubMed] [Google Scholar]
- 6.Kuroha, M. et al. factors associated with fibrosis during colorectal endoscopic submucosal dissection: Does pretreatment biopsy potentially elicit submucosal fibrosis and affect endoscopic submucosal dissection outcomes. Digestion102(4), 590–598 (2021). 10.1159/000510145 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Tanaka, H. et al. Salvage endoscopic submucosal dissection for local residual/recurrent colorectal tumor after endoscopic resection: Large multicenter 10-year study. Dig. Endosc.33(4), 608–615 (2021). 10.1111/den.13797 [DOI] [PubMed] [Google Scholar]
- 8.Chiba, H. et al. Predictive factors of mild and severe fibrosis in colorectal endoscopic submucosal dissection. Dig. Dis. Sci.65(1), 232–242 (2020). 10.1007/s10620-019-05735-y [DOI] [PubMed] [Google Scholar]
- 9.Li, D. et al. Usefulness of the combined orthodontic rubber band and clip method for gastric endoscopic submucosal dissection. BMC Gastroenterol.22(1), 527 (2022). 10.1186/s12876-022-02606-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Zheng, L. et al. Orthodontic rubber band-assisted endoscopic submucosal dissection: An efficient method for treating superficial colorectal tumors. Gastroenterol. Res. Pract.2022, 2835258 (2022). 10.1155/2022/2835258 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Faller, J. et al. Endoscopic submucosal dissection with double clip and rubber band traction for residual or locally recurrent colonic lesions after previous endoscopic mucosal resection. Endoscopy52(5), 383–388 (2020). 10.1055/a-1104-5210 [DOI] [PubMed] [Google Scholar]
- 12.Matsumoto, A. et al. Outcome of endoscopic submucosal dissection for colorectal tumors accompanied by fibrosis. Scand. J. Gastroenterol.45(11), 1329–1337 (2010). 10.3109/00365521.2010.495416 [DOI] [PubMed] [Google Scholar]
- 13.Kaosombatwattana, U. et al. Preoperative endoscopic predictors of severe submucosal fibrosis in colorectal tumors undergoing endoscopic submucosal dissection. Endosc. Int. Open.7(4), E421–E430 (2019). 10.1055/a-0848-8225 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Lee, S. P. et al. Effect of submucosal fibrosis on endoscopic submucosal dissection of colorectal tumors: Pathologic review of 173 cases. J. Gastroenterol. Hepatol.30(5), 872–878 (2015). 10.1111/jgh.12886 [DOI] [PubMed] [Google Scholar]
- 15.Kamigaichi, Y. et al. Factors for conversion risk of colorectal endoscopic submucosal dissection: A multicenter study. Surg. Endosc.36(8), 5698–5709 (2022). 10.1007/s00464-022-09250-6 [DOI] [PubMed] [Google Scholar]
- 16.Cecinato, P. et al. Left colonic localization, non-granular morphology, and pit pattern independently predict submucosal fibrosis of naïve colorectal neoplasms before endoscopic submucosal dissection. Surg. Endosc.37(4), 3037–3045 (2023). 10.1007/s00464-022-09828-0 [DOI] [PubMed] [Google Scholar]
- 17.Fukuchi, T. et al. Factors influencing interruption of colorectal endoscopic submucosal dissection. Surg. Endosc.35(10), 5497–5507 (2021). 10.1007/s00464-020-08042-0 [DOI] [PubMed] [Google Scholar]
- 18.Cecinato, P. et al. Underwater endoscopic submucosal dissection and hybrid endoscopic submucosal dissection as rescue therapy in difficult colorectal cases. Endosc. Int. Open10(9), E1225–E1232 (2022). 10.1055/a-1882-4306 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Tanaka, H. et al. Short-term and long-term outcomes of submucosal dissection for residual or recurrent colorectal tumors after endoscopic resection: Analysis of a multicenter prospective study. Dig. Endosc.10.1111/den.14752 (2023). 10.1111/den.14752 [DOI] [PubMed] [Google Scholar]
- 20.Yoshida, N. et al. Endoscopic submucosal dissection for colorectal tumors: Technical difficulties and rate of perforation. Endoscopy41(9), 758–761 (2009). 10.1055/s-0029-1215028 [DOI] [PubMed] [Google Scholar]
- 21.Takamaru, H. et al. Predicting and managing complications following colonoscopy: Risk factors and management of advanced interventional endoscopy with a focus on colorectal ESD. Expert. Rev. Med. Devices17(9), 929–936 (2020). 10.1080/17434440.2020.1819788 [DOI] [PubMed] [Google Scholar]
- 22.Gweon, T. G. & Yang, D. H. Management of complications related to colorectal endoscopic submucosal dissection. Clin. Endosc.56(4), 423–432 (2023). 10.5946/ce.2023.104 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Singh, R. R., Nanavati, J., Gopakumar, H. & Kumta, N. A. Colorectal endoscopic submucosal dissection in the West: A systematic review and meta-analysis. Endosc. Int. Open11(11), E1082–E1091 (2023). 10.1055/a-2181-5929 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Lee, E. J. et al. Clinical risk factors for perforation during endoscopic submucosal dissection (ESD) for large-sized, nonpedunculated colorectal tumors. Surg. Endosc.26(6), 1587–1594 (2012). 10.1007/s00464-011-2075-5 [DOI] [PubMed] [Google Scholar]
- 25.Isomoto, H. et al. Clinicopathological factors associated with clinical outcomes of endoscopic submucosal dissection for colorectal epithelial neoplasms. Endoscopy41(8), 679–683 (2009). 10.1055/s-0029-1214979 [DOI] [PubMed] [Google Scholar]
- 26.Takeuchi, Y. et al. Factors associated with technical difficulties and adverse events of colorectal endoscopic submucosal dissection: Retrospective exploratory factor analysis of a multicenter prospective cohort. Int. J. Colorectal Dis.29(10), 1275–1284 (2014). 10.1007/s00384-014-1947-2 [DOI] [PubMed] [Google Scholar]
- 27.Chow, C., Fung, T., Chan, P. T. & Kwok, K. H. Endoscopic submucosal dissection for colorectal polyps: Outcome determining factors. Surg. Endosc.37(2), 1293–1302 (2023). 10.1007/s00464-022-09672-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Imai, K. et al. A risk-prediction model for en bloc resection failure or perforation during endoscopic submucosal dissection of colorectal neoplasms. Dig. Endosc.32(6), 932–939 (2020). 10.1111/den.13619 [DOI] [PubMed] [Google Scholar]
- 29.Tanaka, H. et al. Endoscopic submucosal dissection for tumors involving the ileocecal valve with extension into the terminal ileum: A multicenter study from the Hiroshima GI Endoscopy Research Group. Surg. Endosc.37(2), 958–966 (2023). 10.1007/s00464-022-09542-x [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data sets used and analyzed in this study are available from the corresponding author upon reasonable request.


