Abstract
Background:
Endoscopic submucosal dissection (ESD) is a minimally invasive surgical procedure used for en bloc removal of colorectal tumors. Although colorectal ESD is ideally conducted under conscious sedation, it is often performed under general anesthesia because of its complexity and lengthy duration. Currently, there is limited research on colorectal ESD performed under conscious sedation. The purpose of this study was to evaluate the effectiveness, safety, and economic cost of colorectal ESD under conscious sedation compared to general anesthesia.
Materials and Methods:
Retrospective analysis of 301 patients who underwent ESD treatment for colorectal tumors at the Endoscopy Center of Peking University Cancer Hospital from January 2018 to November 2020. Patients were divided into the sedation group (group S, n=88) and the general anesthesia group (group A, n=213) based on the anesthetic method. To balance the confounding factors between the 2 groups, 75 matched pairs were obtained after using propensity score matching (PSM). Intraoperative and postoperative parameters were then compared between the matched groups.
Results:
After PSM, there was no statistically significant difference between group S and group A in terms of the surgical time, en bloc resection rate, and complete resection rate. There was also no statistically significant difference in the occurrence rates of bleeding, perforation, and post-ESD electrocoagulation syndrome (PEECS) between the 2 groups. However, the length of hospital stay was significantly shorter in group S (1.23±0.89d) than in group A (5.92±3.05d) (P<0.05). The hospitalization costs were also significantly lower in group S (16482.34±13154.32 yuan) compared with group A (34743.74±13779.40 yuan) (P<0.05).
Conclusions:
Compared to general anesthesia, performing ESD for colorectal tumors under conscious sedation has equivalent effectiveness and safety while shortening the hospital stay and reducing the economic costs.
Key Words: Colorectal tumors, endoscopic submucosal dissection, conscious sedation, general anesthesia, propensity score matching
Endoscopic submucosal dissection (ESD) is a method of completely removing colorectal tumors. It is less invasive than surgical resection. Compared to traditional endoscopic mucosal resection (EMR), ESD has a higher rate of en bloc resection (84% for ESD vs. 33% for EMR)1 and a lower local recurrence rate (1.4% for ESD vs. 6.8% for EMR).2 With the widespread use of ESD, the choice of sedation/anesthesia method during ESD has been given great attention.
Endotracheal intubation under general anesthesia ensures continuous airway protection, facilitating the prompt detection and management of intraoperative emergencies. It also induces complete sedation in patients, preventing sudden movements or discomfort reactions that could interfere with surgery and thereby reducing surgery-related complications. Consequently, in China, most hospitals perform ESD under general anesthesia. However, colorectal ESD is significantly affected by respiratory movements, and patients often need to hold their breath or change positions during the procedure to cooperate with the surgeon.3 Therefore, expert consensus suggests that colorectal ESD can be performed under moderate sedation. For patients undergoing longer procedures with larger wounds, general anesthesia with endotracheal intubation can be used to prevent and treat surgical complications.4 The Japanese Society of Gastrointestinal Endoscopy Sedation Guidelines recommend the use of benzodiazepines combined with analgesics for sedation during colorectal ESD.5 Nevertheless, conscious sedation is not extensively used because of limited experience and concerns regarding the potential side effects and complications associated with sedatives.
The purpose of this study was to evaluate the efficacy, safety, and economic cost of colorectal tumor ESD under conscious sedation compared to general anesthesia.
MATERIALS AND METHODS
Patients
A retrospective study was conducted on 301 patients with colorectal tumors who underwent ESD treatment at the Endoscopy Center of Peking University Cancer Hospital from January 2018 to November 2020. Patients were excluded if they had colorectal tumors infiltrating the muscular layer or associated lymph node metastasis. Patients with tumor sizes ≤3 cm, tolerable discomfort during colonoscopy, living near the hospital, or at high risk for general anesthesia were recommended conscious sedation. Patients estimated to have tumor sizes >3 cm or lesions located in challenging areas such as the sigmoid colon, splenic flexure, transverse colon, hepatic flexure, or cecum were recommended general anesthesia. They were assigned to the conscious sedation group (group S) or the general anesthesia group (group A) based on the anesthesiologist’s recommendation and the patient’s intention after thorough consultation. The present study was approved by the Ethics Committee of Peking University Cancer Hospital (2017KT103) in accordance with the Declaration of Helsinki. Written informed consent was obtained from all patients or their families. All surgeries were performed by the same experienced ESD expert. Induction of general anesthesia and administration of conscious sedation were performed by anesthesiologists in all patients.
Anesthesia Methods
Sedation group: After confirming that there were no contraindications (such as glaucoma, prostate hypertrophy, and arrhythmia), patients were given 10mg diazepam and 50mg pethidine intramuscularly 15 minutes before surgery for sedation and analgesia. An intramuscular injection of 10mg scopolamine butylbromide was given for antispasmodic effects, and additional doses were administered during the surgery as per the surgeon’s request.
General anesthesia group: Upon entering the surgical suite, patients were subjected to intravenous access and electrocardiographic monitoring. Rapid induction of anesthesia was achieved using midazolam, propofol, vecuronium, and fentanyl, followed by endotracheal intubation. Anesthesia was maintained with sevoflurane, fentanyl, and vecuronium until the end of the surgery, and specific anesthetic drug choices were made by the anesthesiologist based on the patient’s condition.
Colorectal ESD Procedure
A single-channel colonoscope (PCF-260J; Olympus Co., Tokyo, Japan) was used in all ESD procedures. A premixed sterilized solution of glycerol (10% glycerol and 5% fructose; Cisen Pharmaceutical, Co., Ltd., Shandong, China) with indigo carmine was injected into the submucosal layer. A single-use electrosurgical knife with water injection function (Micro-Tech Co., Nanjing, China) was used for lesion marking, incision, and dissection, alongside an electrosurgical unit (VIO 200S; ERBE Elektromedizin GmbH, Tübingen, Germany). The ENDO CUT Q mode (parameter setting effect 3, cutting duration 2, and cutting interval 4) was applied for both mucosal incision and submucosal dissection. Hemostasis was achieved with the FORCED COAG E2 mode, with the power set to 40 W. Using hemoclips (Micro-Tech Co.) to close the wound.
Main Study Indicators
According to the postoperative pathologic results, the pathologic diagnosis was classified as low-grade intraepithelial neoplasia, high-grade intraepithelial neoplasia, intramucosal carcinoma, submucosal carcinoma, muscularis propria carcinoma, neuroendocrine tumors, and others. According to the Paris classification,6 the macroscopic morphology of tumorous lesions can be divided into polypoid (0–I) and nonpolypoid (0–II, 0–III). In this study, the macroscopic morphology of the lesions was divided into polypoid and nonpolypoid lesions and submucosal tumors (SMTs). The main indicators for evaluating the efficacy of ESD resection after surgery included en bloc resection and complete resection. En bloc resection refers to the complete removal of the lesion as a single specimen under endoscopy. Complete resection is defined as en bloc resection with tumor-free lateral and vertical margins.7 Bleeding included intraoperative bleeding and delayed bleeding. Intraoperative bleeding was defined as a decrease in hemoglobin over 2 mg/dL or the need for transfusion during the procedure. Delayed bleeding refers to the appearance of obvious bloody stools after treatment or the need for hemostatic measures after treatment. Perforation was divided into intraoperative perforation and delayed perforation according to the time of occurrence. Intraoperative perforation was diagnosed when tissue or mesenteric fat was directly observed during the ESD surgery. Delayed perforation refers to the sudden appearance of peritoneal irritation symptoms or chest pain after ESD without immediate symptoms or free gas present on abdominal radiographs or chest and abdominal CT scans.8 The diagnostic criteria for post-ESD electrocoagulation syndrome (PEECS) are localized abdominal pain accompanied by fever or an inflammatory response after ESD and no delayed perforation. The surgery time refers to the time between the insertion and withdrawal of the endoscope from the anus.
Statistical Analysis
SPSS 22.0 software was used for statistical analysis. Categorical data were expressed as a number (percentage), and a chi-squared test was used to identify differences between the 2 groups. Numerical data for normal distribution were expressed as the mean±SD, and the Student t test was used to determine differences between the 2 groups. Numerical data for a skewed distribution were expressed as a median interquartile range, and the Mann-Whitney U test was applied. Differences were considered statistically significant at P<0.05.
Propensity score matching (PSM) was used to balance selection bias and confounding factors between the 2 groups. The grouping variable was the dependent variable. Five factors that might affect the results of ESD, including BMI, tumor location, morphology, size, and pathologic classification, as well as multiple lesions resected by endoscopy, were considered covariates. The propensity score was calculated using logistic regression, and a 1:1 nearest neighbor matching method was used with a caliper value of 0.01 to ensure the quality of the matching results. The inter-group covariate balance was tested for the matched samples. Statistical analysis was performed using the newly matched samples.
RESULTS
Comparison of Clinicopathologic Characteristics between the 2 Groups Before PSM
A total of 301 patients with colorectal cancer were included in the study before PSM. Patients were divided into group S (n=88) and group A (n=213) based on the anesthesia method. There were no significant differences in age, sex, smoking history, alcohol history, hypertension, diabetes, cardiovascular disease, or tumor location between the 2 groups. However, the 2 groups had significant differences in BMI, tumor size, morphology, and pathologic diagnosis (all P<0.05), as shown in Table 1.
TABLE 1.
Comparison of Clinicopathologic Characteristics between the 2 Groups Before PSM
Observed Indicators | Group S N=88 | Group A N=213 | χ2/t | P |
---|---|---|---|---|
Sex, male n (%) | 49 (55.7) | 126 (59.2) | 0.309 | 0.579 |
Age (y) | 60.28±10.94 | 61.03±11.54 | −0.517 | 0.606 |
BMI(kg/m2) | 23.61±2.70 | 24.45±3.31 | −2.097 | 0.037* |
History of smoking, n (%) | 24 (27.3) | 63 (29.6) | 0.161 | 0.688 |
History of drinking, n (%) | 8 (9.1) | 30 (14.1) | 1.408 | 0.235 |
Hypertension, n (%) | 30 (34.1) | 62 (29.1) | 0.729 | 0.393 |
Diabetes, n (%) | 13 (14.8) | 25 (11.7) | 0.520 | 0.471 |
cardiovascular disease, n (%) | 10 (11.4) | 22 (10.3) | 0.070 | 0.791 |
Pathologic tumor size (cm) | 1.86±1.19 | 3.09±2.13 | −6.379 | 0.000* |
Location, n (%) | 4.571 | 0.102 | ||
Rectum | 45 (51.1) | 83 (39.0) | ||
Left hemi-colon | 19 (21.6) | 47 (22.1) | ||
Right hemi-colon | 24 (27.3) | 83 (39.0) | ||
Morphology, n (%) | 12.742 | 0.002* | ||
0-I | 18 (20.5) | 79 (37.1) | ||
0-II/0-III | 53 (60.2) | 117 (54.9) | ||
SMTs | 17 (19.3) | 17 (8.0) | ||
Pathologic diagnosis, n (%) | 15.980 | 0.010* | ||
Low-grade intraepithelial neoplasia | 39 (44.3) | 87 (40.8) | ||
High-grade intraepithelial neoplasia | 19 (21.6) | 53 (24.9) | ||
Intramucosal carcinoma | 1 (1.1) | 25 (11.7) | ||
Submucosal carcinoma | 8 (9.1) | 21 (9.9) | ||
Muscularis propria carcinoma | 1 (1.1) | 2 (0.9) | ||
NETs | 14 (15.9) | 15 (7.0) | ||
Others | 6 (6.8) | 10 (4.7) | ||
Endoscopic resection of multiple lesions, n (%) | 34 (38.6) | 88 (41.3) | 0.185 | 0.667 |
0–I indicates the morphology of the tumor is polypoid; 0–II/0–III, the morphology of the tumor is nonpolypoid; BMI, body mass index; ESD, endoscopic submucosal dissection; group A, patients undergoing colorectal ESD under general anesthesia; group S, patients undergoing colorectal ESD under conscious sedation; NET, neuroendocrine tumor; PSM, propensity score matching; SMT, submucosal tumor.
Comparison of Clinicopathologic Characteristics between the 2 Groups After PSM
A total of 75 matched pairs were obtained after PSM. There were no statistically significant differences between the 2 groups in terms of sex, age, BMI, smoking history, alcohol history, hypertension, diabetes, cardiovascular disease, tumor size, location, morphology, pathologic diagnosis, or the endoscopic resection of multiple lesions, as shown in Table 2.
TABLE 2.
Comparison of the Basic Characteristics and Tumor Features between the 2 Groups After PSM
Observed Indicators | Group S N=75 | Group A N=75 | χ2/t | P |
---|---|---|---|---|
Sex, male n (%) | 42 (56.0) | 43 (57.3) | 0.027 | 0.869 |
Age (y) | 61.83±10.45 | 62.31±13.11 | −0.248 | 0.804 |
BMI(kg/m2) | 23.79±2.73 | 23.57±3.10 | 0.453 | 0.651 |
History of smoking, n (%) | 21 (28.0) | 23 (30.7) | 0.129 | 0.720 |
History of drinking, n (%) | 7 (9.3) | 16 (21.3) | 4.160 | 0.041 |
Hypertension, n (%) | 30 (40.0) | 19 (25.3) | 3.667 | 0.055 |
Diabetes, n (%) | 12 (16.0) | 6 (8.0) | 2.273 | 0.132 |
cardiovascular disease, n (%) | 9 (12.0) | 7 (9.30) | 0.280 | 0.597 |
Pathologic tumor size (cm) | 2.01±1.21 | 2.05±0.96 | −0.216 | 0.829 |
Location, n (%) | 0.036 | 0.982 | ||
Rectum | 36 (48.0) | 35 (46.7) | ||
Left hemi-colon | 17 (22.7) | 17 (22.7) | ||
Right hemi-colon | 22 (29.3) | 23 (30.7) | ||
Morphology, n (%) | 0.284 | 0.867 | ||
0-I | 18 (24.0) | 16 (21.3) | ||
0-II/0-III | 46 (61.3) | 46 (61.3) | ||
SMTs | 11 (14.7) | 13 (17.3) | ||
Pathologic diagnosis, n (%) | 4.712 | 0.593 | ||
Low-grade intraepithelial neoplasia | 33 (44.0) | 35 (46.7) | ||
High-grade intraepithelial neoplasia | 18 (24.0) | 14 (18.7) | ||
Intramucosal carcinoma | 1 (1.3) | 4 (5.30) | ||
Submucosal carcinoma | 8 (10.7) | 5 (6.7) | ||
Muscularis propria carcinoma | 1 (1.3) | 0 (0) | ||
NETs | 9 (12.0) | 13 (17.3) | ||
Others | 5 (6.7) | 4 (5.3) | ||
Endoscopic resection of multiple lesions, n (%) | 29 (38.76) | 32 (42.7) | 0.249 | 0.618 |
0–I indicates the morphology of the tumor is polypoid; 0–II/0–III, the morphology of the tumor is nonpolypoid; BMI, body mass index; ESD, endoscopic submucosal dissection; group A, patients undergoing colorectal ESD under general anesthesia; group S, patients undergoing colorectal ESD under conscious sedation; NET, neuroendocrine tumor; PSM, propensity score matching; SMT, submucosal tumor.
Comparison of ESD Treatment Outcomes Between the 2 Groups After PSM
After PSM, there were no statistically significant differences between the 2 groups in terms of surgery time, en bloc resection rate, or complete resection rate. In addition, there were no statistically significant differences in the occurrence rates of bleeding, perforation, or PEECS between the 2 groups. The length of hospital stay in group S was 1.23±0.89 days, significantly shorter than the 5.92±3.05 days in group A (P<0.05). The hospitalization costs in group S were 16482.34±13154.32 yuan, significantly lower than 34743.74±13779.40 yuan in group A (both P<0.05) (Table 3).
TABLE 3.
Comparison of ESD Treatment Outcomes Between the 2 Groups After PSM
Group S N=75 | Group A N=75 | χ2/t | P | |
---|---|---|---|---|
Surgery time (min) | 51.17±30.62 | 58.20±42.35 | −1.164 | 0.246 |
En bloc resection, n (%) | 73 (97.3) | 73 (97.3) | 1 | |
Complete resection, n (%) | 68 (90.7) | 70 (94.6) | 1.422 | 0.491 |
Bleeding, n (%) | 0 (0) | 0 (0) | ||
Perforate, n (%) | 2 (2.7) | 7 (9.3) | 1.891 | 0.169 |
PEECS | 0 (0) | 3 (4.0) | 1.361 | 0.243 |
Length of stay (d) | 1.23±0.89 | 5.92±3.05 | −12.779 | 0.000 |
Hospitalization cost (yuan) | 16482.34±13154.32 | 34743.74±13779.40 | 8.302 | 0.000 |
ESD indicates endoscopic submucosal dissection; group A, patients undergoing colorectal ESD under general anesthesia; group S, patients undergoing colorectal ESD under conscious sedation; PEECS, post-ESD electrocoagulation syndrome.
DISCUSSION
With the continuous development of minimally invasive diagnosis and treatment technology in digestive endoscopy, ESD has become one of the main treatment methods for colorectal tumors. Conscious sedation is the best anesthesia method for colorectal ESD, which can improve patient satisfaction, eliminate pain, and enable patients to react during the treatment process, thereby promoting the smooth progress of the surgery. In Japan, ESD is usually performed under conscious sedation in the endoscopy room, but there is a lack of clinical experience and standardized criteria for performing colorectal ESD under conscious sedation in China. This study confirms the feasibility of performing colorectal ESD under conscious sedation by comparing it with colorectal ESD under general anesthesia. Because this study was retrospective, it was not possible to control for covariates between the 2 groups before surgery. In addition, the sample size of group S was small, while that of group A was large. Therefore, we used propensity score matching to effectively improve the balance of covariates between the groups, eliminate group selection bias, and make the research results more realistic. Based on our study, colorectal ESD under conscious sedation was effective, safe, and cost-effective. This was mainly demonstrated through the following aspects.
Conscious Sedation is Effective for Colorectal ESD
ESD is superior to EMR because it can completely remove lesions. En bloc resection can accurately determine whether the specimen margin is negative and reduce the risk of postoperative recurrence.9 A meta-analysis showed that the en bloc resection rate for ESD in the treatment of colorectal tumors is 91%, and the complete resection rate is 82.9%.10 In this study, both the en bloc resection rate and the complete resection rate in group S and group A were higher than those reported previously, and there was no statistically significant difference between the 2 groups. The duration of ESD surgery is associated with tumor size, with larger tumors requiring longer operating times.11 Studies have shown that when tumor size exceeds 40mm, it increases the duration of the surgery.11,12 In this study, the tumor size in group S was 2.01±1.21cm, with a surgery time of 51.17±30.62 minutes, while in group A, the tumor size was 2.05±0.96 cm, with a surgery time of 58.20±42.35 minutes. There was no statistically significant difference between the 2 groups. However, in this study, the surgery time was defined as the time between the insertion and removal of the endoscope and did not include the time for anesthesia preparation and postoperative recovery. Therefore, the total surgery time for general anesthesia, including anesthesia preparation and postoperative recovery, might be longer.
Under Conscious Sedation, Colorectal ESD has no Effect on the Occurrence of Surgical Complications
The main complications of ESD are bleeding and perforation. Perforation is the most common and serious complication in colorectal ESD. A meta-analysis of nearly 3000 cases showed that the incidence of bleeding and perforation in colorectal ESD was 2% and 4%, respectively.13 Perforations during ESD are mostly minor and can typically be closed endoscopically using clips. In our study, neither group S nor group A had delayed intraoperative or postoperative bleeding. In group S, there were 2 cases (2.7%) of intraoperative perforation, with 1 case managed by endoscopic clipping and 1 case where cancer infiltration was detected during the procedure, subsequently requiring surgical treatment. In group A, there were 7 cases (9.3%) of perforation, including 6 cases of intraoperative perforation. Of these 6 cases, 5 were clipped under endoscopy. However, in 1 case located in the cecum where endoscopic repair was not feasible, laparoscopic repair was performed. The remaining case had delayed perforation 2 days postoperatively and was successfully managed with conservative treatment.
Post-ESD electrocoagulation syndrome (PEECS) is another complication after ESD. Due to the lack of clear diagnostic criteria for PEECS, its incidence rate varies widely, ranging from 4.8% to 40.2%.14 The main pathogenesis of PEECS is related to transmural thermal injury and local bacterial infection. In our study, no PEECS occurred in group S. This may be because PEECS symptoms typically appear within 12 to 48 hours after surgery, while most group S patients in our study were discharged on the same day of surgery from the day ward, potentially missing some patients who developed PEECS symptoms after discharge. In contrast, 3 patients in group A met the diagnostic criteria for PEECS, and all recovered after conservative treatment. The low incidence of PEECS in our center may be attributed to our practice of not performing electrocoagulation treatment on wounds smaller than 5cm and without bleeding points after ESD, but rather using metal clips for closure, thereby reducing unnecessary electrocoagulation injury and preventing wound infection. However, the specific correlation deserves further investigation.
Colorectal ESD Performed Under Conscious Sedation Can Save Economic Costs
With the improvement of the ESD technique and the achievement of stable postoperative courses, treatments with short hospital stays have become feasible. In Japan, due to medical insurance policies, the length of hospital stay after ESD can be as long as 5 to 7 days.15 However, a study conducted in Japan suggested that patients can be discharged within 3 days after ESD if no abnormalities are detected during or on the first day after the procedure.16 In Europe, the post-ESD hospitalization period ranges from 2 to 4 days.17 Some studies suggest that simple colorectal ESD can be safely performed in outpatient or day surgery settings.18,19 In our study, patients in Group S underwent preoperative examinations and preparations before admission and were discharged on the same day of surgery after postoperative observation without any discomfort. Therefore, the length of stay in group S is significantly reduced, optimizing the utilization of medical resources. In contrast, patients in group A had a longer average length of stay of 5.92 days. The main reasons for this were as follows: (1) patients will be admitted to the hospital 1 day before the surgery or even longer for preoperative preparation, (2) patients under general anesthesia require close observation for anesthesia or surgery-related complications within 24 hours postoperatively, (3) although there was no statistically significant difference in the incidence of complications between the 2 groups, the A group had more patients with perforation and PEECS compared to the S group, resulting in longer hospital stays for these patients, and (4) some patients request to extend their hospital stay.
According to reports, the benchmark cost estimate for ESD treatment in China, including 4 days of postoperative hospitalization, is ~$5400.20 In our study, the average hospitalization cost for group S was 16482.34±13154.32 yuan, significantly lower than the reported value, while for group A it was 34743.74 yuan, close to the reported value. The reduced hospitalization cost in group S was mainly because of the absence of costs associated with general anesthesia and the decrease in treatment and nursing costs resulting from the reduction in hospitalization days. Therefore, performing colorectal ESD under conscious sedation in a day ward can save medical costs, optimize the use of medical resources, and reduce the economic burden on patients.
There were several limitations to this study. First, it is a single-center retrospective study with a relatively small sample size. Second, endoscopists tend to prefer general anesthesia for patients with anticipated difficult surgeries when choosing the anesthesia method. Although the PSM method can help balance the differences in characteristics between the 2 groups of patients, it may still influence the study results. Third, because patients in the S group were admitted to the day ward and most of them were discharged on the same day of surgery, delayed postoperative complications may not have been promptly identified and recorded, potentially impacting the accuracy of the results.
CONCLUSIONS
Compared to general anesthesia, performing ESD for colorectal tumors under conscious sedation has equivalent effectiveness and safety while shortening the hospital stay and reducing the economic costs.
Footnotes
Y.L. and J.W. contributed equally to this work; Y.L. and J.W. performed in analysis and interpretation of the data, and drafting of the manuscript; Q.W. conceived and designed the study; Y.H. helped to perform the analyses and critically revised the article for important intellectual content. All authors approved the final draft submitted.
The study was supported by Beijing Hospitals Authority Clinical Medicine Development of Special Funding Support, No. XMLX202143; Capital’s Funds for Health Improvement and Research, No. 2020-2-2155; Hygiene and Health Development Scientific Research Fostering Plan of Haidian District Beijing, HP2024-19-503002; Shaanxi Provincial Key R&D Program, No. 2024SF-YBXM-133.
Data supporting this research article are available from the corresponding author or first author upon reasonable request.
The authors declare no conflicts of interest.
Contributor Information
Yanrong Li, Email: liyanrong7645@163.com.
Jing Wang, Email: wangjing_pku@bjmu.edu.cn.
Ye Hong, Email: sxchhy@163.com.
Qi Wu, Email: wuqi1973@bjmu.edu.cn.
REFERENCES
- 1. Saito Y, Fukuzawa M, Matsuda T, et al. Clinical outcome of endoscopic submucosal dissection versus endoscopic mucosal resection of large colorectal tumors as determined by curative resection. Surg Endosc. 2010;24:343–352. [DOI] [PubMed] [Google Scholar]
- 2. Oka S, Tanaka S, Saito Y, et al. Local recurrence after endoscopic resection for large colorectal neoplasia: a multicenter prospective study in Japan. Official J Am College Gastroenteroly| ACG. 2015;110:697–707. [DOI] [PubMed] [Google Scholar]
- 3. Kinugasa H, Higashi R, Miyahara K, et al. Dexmedetomidine for conscious sedation with colorectal endoscopic submucosal dissection: a prospective double-blind randomized controlled study. Clin Transl Gastroenterol. 2018;9:167. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. Chinese Society of Digestive Endoscopy, Chinese Medical Association. Common consensus on anesthesia management for common digestive endoscopic surgeries. Chinese Journal of Clinical Anesthesia. 2019;35:177–185 [Google Scholar]
- 5. Obara K, Haruma K, Irisawa A, et al. Guidelines for sedation in gastroenterological endoscopy. Dig Endosc. 2015;27:435–449. [DOI] [PubMed] [Google Scholar]
- 6. Participants in the Paris Workshop. The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 2003;58(6 Suppl):S3–S43. [DOI] [PubMed] [Google Scholar]
- 7. Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) guideline. Endoscopy. 2015;47:829–854. [DOI] [PubMed] [Google Scholar]
- 8. Tanaka S, Kashida H, Saito Y, et al. Japan Gastroenterological Endoscopy Society Guidelines for colorectal endoscopic submucosal dissection/endoscopic mucosal resection. Dig Endosc. 2020;32:219–239. [DOI] [PubMed] [Google Scholar]
- 9. Fuccio L, Ponchon T. Colorectal endoscopic submucosal dissection (ESD). Best Prac Res Clin Gastroenterol. 2017;31:473–480. [DOI] [PubMed] [Google Scholar]
- 10. Fuccio L, Hassan C, Ponchon T, et al. Clinical outcomes after endoscopic submucosal dissection for colorectal neoplasia: a systematic review and meta-analysis. Gastroint Endosc. 2017;86:74–86.e17. [DOI] [PubMed] [Google Scholar]
- 11. Sato K, Ito S, Kitagawa T, et al. Factors affecting the technical difficulty and clinical outcome of endoscopic submucosal dissection for colorectal tumors. Surg Endosc. 2014;28:2959–2965. [DOI] [PubMed] [Google Scholar]
- 12. Agapov M, Dvoinikova E. Factors predicting clinical outcomes of endoscopic submucosal dissection in the rectum and sigmoid colon during the learning curve. Endosc Int Open. 2014;2:E235–E240. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Repici A, Hassan C, Pessoa DDP, et al. Efficacy and safety of endoscopic submucosal dissection for colorectal neoplasia: a systematic review. Endoscopy. 2012;44:137–150. [DOI] [PubMed] [Google Scholar]
- 14. Qiu J, Ouyang Q, Zhang Y, et al. Post-endoscopic submucosal dissection electrocoagulation syndrome: a clinical overview. Expert Rev Gastroenterol Hepatol. 2022;16:1079–1087. [DOI] [PubMed] [Google Scholar]
- 15. Murata A, Okamoto K, Muramatsu K, et al. Time trend of medical economic outcomes of endoscopic submucosal dissection for gastric cancer in Japan: a national database analysis. Gastric Cancer. 2014;17:294–301. [DOI] [PubMed] [Google Scholar]
- 16. Tomiki Y, Kawai M, Takehara K, et al. Clinical pathway to discharge 3 days after colorectal endoscopic submucosal dissection. Dig Endosc. 2015;27:679–686. [DOI] [PubMed] [Google Scholar]
- 17. Probst A, Ebigbo A, Märkl B, et al. Endoscopic submucosal dissection for early rectal neoplasia: experience from a European center. Endoscopy. 2017;49:222–232. [DOI] [PubMed] [Google Scholar]
- 18. Ohya T, Marsk R, Pekkari K. Colorectal ESD in day surgery. Surg Endosc. 2017;31:3690–3695. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Roberta M, Alessia GP, Milena DL, et al. Cost analysis and outcome of endoscopic submucosal dissection for colorectal lesions in an outpatient setting. Digestive and Liver Disease: Official Journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver. 2019;51:391–396. [DOI] [PubMed] [Google Scholar]
- 20. Cui N, Zhao Y, Yu H. Cost analysis of endoscopic submucosal dissection for the treatment of colorectal lesions in China. Biomed Res Int. 2019;2019:6983896. [DOI] [PMC free article] [PubMed] [Google Scholar]