A novel endoscopic hand-suturing technique for defect closure after colorectal endoscopic submucosal dissection: a pilot study

• Abstract
• Introduction
• Methods
• Patients
• Endoscopic hand-suturing
• Post-ESD management
• Assessments
• Results
• Discussion
• References

Abstract

Background This study aimed to demonstrate the feasibility of endoscopic hand-suturing (EHS) and attainability of sustained closure after colorectal endoscopic submucosal dissection (ESD).

Methods EHS was defined as uninterrupted endoscopic suturing of the mucosal defect after colorectal ESD using an absorbable barbed suture and a through-the-scope needle holder. Following individual EHS training using an ex vivo porcine colonic model, two experienced endoscopists performed EHS. Repeat colonoscopy was performed on the third or fourth day after ESD to examine the EHS site. The primary end point was the complete EHS closure rate, and secondary end points were sustained closure and post-ESD bleeding rates.

Results 11 lesions were included. Median size of the mucosal defect was 38 mm (range 25 – 55 mm) and the lesion characteristics were as follows: lower rectum/upper rectum/ascending colon/cecum = 3/3/2/3, and 0-IIa/0-Is + IIa/others = 5/4/2. EHS was not attempted in two patients owing to difficulty in colonoscope reinsertion after ESD and intraoperative perforation, respectively. EHS was performed for nine lesions, and the complete EHS closure rate was 73 %. Median procedure time for suturing was 56 minutes (range 30 – 120 minutes) and median number of stitches was 8 (range 6 – 12). Sustained closure and post-ESD bleeding rates were 64 % and 9 %, respectively.

Conclusions EHS achieved complete and sustained closure in the colorectum. However, EHS is not currently clinically applicable given the long procedure time. Further modifications of the technique and devices are desirable.

Introduction

Endoscopic resection is routinely performed to remove colorectal neoplasms with negligible risk of lymph node metastasis. Specifically, endoscopic submucosal dissection (ESD) was developed to allow en bloc resection of colorectal neoplasm regardless of size and location [1] [2] [3]. Because of the ability to remove lesions in one piece, ESD has been shown to be associated with a low recurrence rate, while facilitating precise histological assessment of the resected specimen [4] [5] [6]. Guidelines for the treatment of colorectal lesions recommend ESD as the treatment of choice for intramucosal carcinoma or carcinoma with slight submucosal invasion (≤ 1000 μm) [7] [8]. Although ESD of colorectal neoplasm is technically demanding, ongoing development of devices and techniques enables safe and efficient colorectal ESD, even for sizable lesions. Several studies have demonstrated favorable short and long term outcomes of ESD for colorectal neoplasm [9] [10].

Although colorectal ESD has been widely accepted as a minimally invasive treatment option for early colorectal neoplasm, post-ESD bleeding is one of the major adverse events, occurring in 1.5 % – 2.2 % of cases, and may require prolonged hospitalization as well as emergency endoscopy for hemostasis [6] [9] [11] [12] [13] [14]. Although several endoscopic prophylactic closure techniques have been proposed for the prevention of post-ESD bleeding of the colorectum, there is currently no standardized approach, particularly for an extensive mucosal defect [15] [16] [17] [18].

Recently, Goto et al. developed endoscopic hand-suturing (EHS) to close large mucosal defects after ESD. A former pilot study demonstrated technical feasibility and sustained closure of mucosal defects after gastric ESD [19]. However, there are no data regarding the clinical use of EHS for defect closure after colorectal ESD. The aim of this study was to assess the technical feasibility of EHS and attainability of sustained closure after colorectal ESD

Methods

Patients

This was a pilot study conducted at a single referral institution. Patients with colorectal lesions eligible for ESD and referred to the National Cancer Center Hospital were prospectively enrolled in the study. Inclusion criteria were: a) endoscopically diagnosed colorectal neoplasm confined to the mucosa or superficial submucosal invasive neoplasm, 20 – 50 mm in size; b) age ≥ 20 years; c) Eastern Cooperative Oncology Group performance status 0 – 1. All lesions were clinically diagnosed as colorectal adenoma or adenocarcinoma, with the depth of invasion confined to the mucosa or submucosa < 1000 μm, based on endoscopic features of Type 2A or Type 2B according to the Japan NBI Expert Team classification and a noninvasive pattern in pit pattern diagnosis [20] [21]. Patients with coagulopathy (platelet count < 5 × 10⁴, prothrombin time international normalized ratio > 2, or medical conditions requiring the continuous use of antithrombotic agents), or prior abdominal surgery or radiation were excluded. The study was conducted in accordance with the ethical principles included in the Declaration of Helsinki. We obtained approval from the institutional review board, and written informed consent was obtained from all patients. The study was registered with University hospital Medical Information Network (UMIN000031512).

Endoscopic hand-suturing

ESD was performed as described previously [22]. After en bloc resection, EHS was performed. EHS was defined as continuous endoscopic suturing using a needle and suture with a prototype through-the-scope needle holder. Before EHS, submucosal injection was performed along the edges of the mucosal defect in order to prevent needle puncture deeper than the submucosa and to ensure procedural safety. For EHS, a therapeutic colonoscope (PCF-Q260JI or PCF-H290T; Olympus Medical Systems Corp., Tokyo, Japan) and a V-loc 180 absorbable barbed suture (VLOCL0604; Covidien, Mansfield, Massachusetts, USA) were used. The tail of the suture was knotted by hand. For safety reasons, the suture was delivered to the rectum or the colon with the needle captured within an oblique distal attachment to conceal the needle tip. Alternatively, the needle was introduced through an overtube using a prototype through-the-scope needle holder (Olympus Medical Systems Corp., Tokyo, Japan), which grasped the suture at approximately 5 mm from the needle to avoid the rigid curved needle from causing injury to the mucosa ([Fig. 1]). In the colon and rectum, the suture thread was released and the needle was grasped. The mucosal rim of the defect was sequentially sutured from side to side in a zigzag fashion, at 5 – 10-mm intervals under endoscopic view, thereby apposing the two edges of the defect ([Fig. 2], [Fig. 3], [Video 1]). After suturing, the remaining suture and needle were cut with scissor forceps and withdrawn within the distal attachment or through the overtube.

Video 1 Endoscopic hand-suturing technique for defect closure after colorectal endoscopic submucosal dissection.

Two experienced endoscopists (S.A. and Y.S.) performed EHS. As neither endoscopist had prior experience of EHS, they received EHS training in 10 mucosal defects in an ex vivo porcine model before the study. Given the technical difficulty of EHS closure in the proximal colon and the learning curve, the first five EHS procedures were performed for lesions in the rectum or sigmoid colon. Subsequent suturing was performed for six lesions in any location. EHS was attempted only for lesions for which en bloc resection had been achieved; it was not performed after piecemeal resection, intraoperative perforation, or if difficult scope reinsertion was experienced after removal of the specimen.

Post-ESD management

Patients were allowed to drink water on the day after the procedure and to consume a liquid diet beginning on postoperative day 2, according to the clinical pathway for colorectal ESD at our hospital [23]. Follow-up endoscopy was performed on day 3 – 4 after ESD to examine the EHS site. Those patients with lesions in locations other than the cecum were discharged home on day 4 and those with cecal lesions were discharged on day 5. All patients were followed up in the outpatient clinic after discharge.

Assessments

The primary end point was the rate of complete EHS closure, defined as completely apposed mucosal defect edges immediately after EHS. Secondary end points were EHS closure time, sustained EHS closure rate, and post-ESD bleeding rate. The EHS closure time was defined as the procedure time from reinsertion of the colonoscope to when the remaining suture and needle was cut. Sustained EHS closure was defined as completely apposed mucosal defect edges during follow-up endoscopy. Post-ESD bleeding was defined as clinical evidence of bleeding, manifesting as melena or hematochezia after the procedure for which endoscopic hemostasis was required [8] [24]. The primary and secondary end points were analyzed in an intention-to-treat fashion.

Results

A total of 11 colorectal neoplasms in 11 patients were enrolled in the study between June and November 2018. There were eight eligible patients with lesions in the rectum or sigmoid colon in the initial stage. Of these, five patients were enrolled into the study. The other three were registered to other clinical trials or could not be part of the study due to unavailability of the two endoscopists. In addition, there were 13 eligible patients with colorectal lesions in the second stage. Of these, six patients were enrolled, and the other seven were not included for the same reasons mentioned above.

En bloc resection was achieved in all cases. Median lesion size and specimen size based on histologic assessment were 35 mm and 38 mm, respectively. Macroscopic appearance was mainly Type 0-IIa and Type 0-Is + IIa (granular type laterally spreading tumor) in the Paris classification ([Tab. 1]). Of these, intraoperative perforation occurred in one patient whose lesion was located in the cecum. In addition, the colonoscope was not able to reach the mucosal defect after en bloc resection in one lesion located in the ascending colon owing to a long, tortuous sigmoid and transverse colon with severe adhesion, despite the use of balloon-assisted colonoscopy through an overtube. EHS was not attempted in these two cases. Thus, EHS was performed in nine patients in total.

Complete EHS closure was accomplished in eight patients, giving a complete closure rate of 73 % (8/11). The median procedure time for EHS was 56 minutes, and the median number of stitches was 8. On follow-up endoscopy, sustained EHS closure was confirmed in seven patients, giving a sustained closure rate was 64 % (7/11). In one patient with unsustained EHS closure, complete EHS closure was achieved for the 30-mm mucosal defect, albeit requiring 90 minutes owing to poor needle manipulation in retroflexion and its proximity to the anal canal. Despite a successful complete closure, follow-up endoscopy revealed that the suture had fallen out. Post-ESD bleeding occurred in one patient for whom complete EHS closure was unsuccessful. Thus, the post-ESD bleeding rate was 9 % (1/11) ([Tab. 2]). Another patient developed fever but was conservatively treated with antibiotics. No adverse events occurred with EHS; intraoperative perforation occurred in the one patient in whom EHS was not attempted. The complete closure rate, the sustained closure rate, and the post-ESD bleeding rate in patients undergoing EHS (per-protocol analysis) were 89 %, 78 %, and 11 %, respectively.

Discussion

This study demonstrated that EHS achieved large mucosal defect closure after colorectal ESD in humans. In addition, EHS closures were maintained in 64 % of cases on follow-up endoscopy. In the literature, post-ESD bleeding is reported in 1.5 % – 2.2 % of cases [6] [9] [11] [12] [13] [14]. Some retrospective studies have investigated factors associated with bleeding after colorectal ESD. Although results among studies were inconsistent, location of lesion in the rectum was an independent risk factor for delayed bleeding after colorectal ESD in all studies [25] [26] [27] [28]. Among these studies, Seo et al. showed that the risk factors for delayed bleeding were tumor location in the rectosigmoid colon (odds ratio [OR] 6.49, 95 % confidence interval [CI] 1.96 – 21.42; P = 0.002), large tumor ≥ 30 mm (OR 2.10, 95 %CI 1.01 – 4.40; P = 0.048), and use of antiplatelet agents except for aspirin alone (OR 4.04, 95 %CI 1.44 – 11.30; P = 0.008) in the multivariate analysis. The authors also developed a risk scoring model for predicting delayed bleeding. Two points were assigned to tumor location in the rectosigmoid colon, and one point each to large tumor ≥ 30 mm and use of antiplatelet agents except for aspirin alone. Patients with a total of 3 points were categorized into the high risk group [27]. Moreover, a meta-analysis reported that delayed perforation developed in 0.22 %, and was more common in Western countries than in Asia (1.2 % vs. 0.18 %) [29]. Although rare, delayed perforation is potentially serious and required emergency surgery in some cases. Furthermore, post-ESD electrocoagulation syndrome is also known as one of the common adverse events after colorectal ESD, especially in the cecum and ascending colon, and if tumor size is > 30 mm [30] [31] [32]. Some studies revealed that prophylactic defect closure was beneficial to avoid post-ESD electrocoagulation syndrome [33] [34], even though this was technically demanding for sizable mucosal defects. Thus, rapid healing of iatrogenic colorectal ulceration after ESD can be expected with securely performed EHS, leading to potential reduction in post-ESD bleeding, delayed perforation, and post-ESD electrocoagulation syndrome, particularly in high risk patients.

To date, several studies have indicated the technical feasibility of endoscopic defect closure after colorectal ESD using endoclip or other endoscopic devices [15] [16] [17]. Although simple clip closure and over-the-scope clips are promising tools to achieve secure closure, the size of the clips limits the magnitude of defects eligible for this closure method. In addition, in an ex vivo study, suturing was considered to be the more reliable technique to securely close mucosal defects compared with clipping and looping with an endoloop [35].

To the best of our knowledge, this is the first study of endoscopic suturing attempted in the proximal colon. Kantsevoy et al. reported endoscopic suturing using a commercially available suturing device [36]. However, this method required a double-channel gastroscope and it was not applicable to the proximal colon owing to the limited scope length. Our EHS method can be performed using a single-channel pediatric colonoscope with the use of an overtube, illustrating the other advantage of this method. EHS may be the more desirable endoscopic mucosal closure method, given its similarity to surgical closure and flexibility with regard to lesion location.

Nevertheless, our study revealed that EHS closure was technically demanding and time consuming. There were reasons for the long procedure time, indicating technical difficulty in EHS. First, colon EHS was performed in a narrower working space due to colonic folds compared with stomach EHS. It was immensely challenging to grasp the needle with the prototype through-the-scope needle holder with its small grasping jaws, and to maintain the tip of needle perpendicular to the mucosa throughout. Notably, the needle manipulation was much poorer in the retroflexed position in the colon when compared with the stomach procedure. We experienced one unsustained EHS closure near the anal verge. The unsustained closure occurred possibly because of insufficient tightening of the suture due to difficult needle manipulation in retroflexion, and poor approximation of the defect edges near the anal verge given the surrounding connective tissue outside the rectal lumen. Second, we used a single-channel colonoscope during EHS of the colorectum even in the distal colon, whereas a double-channel gastroscope was used in the stomach in the Goto study [19]. Needle grasping and releasing were easier when both accessory channels were utilized. Third, while uninterrupted suturing was performed laterally in the stomach in the Goto study, we were required to suture proximally to distally to avoid post-EHS colorectal stricture. Furthermore, scope access to the proximal colon may be limited after ESD even with the use of an overtube, as experienced in our study. These factors could explain the technical difficulty of EHS in the colorectum. Further refinement of the needle holder, particularly of the grasping jaws, and technical improvement such as the use of a double-channel gastroscope in the rectum and sigmoid colon are warranted before EHS can be adopted into routine clinical use.

There were several limitations to the study. First, the study was a single-center pilot study with a small sample size. Second, EHS was performed by two expert endoscopists and we cannot comment on the reproducibility of EHS defect closure by less experienced endoscopists. Third, the follow-up period to assess sustained EHS closure was relatively short. Finally, it remains unknown whether EHS is technically and clinically feasible for an extensive mucosal defect because the largest tumor size included in the study was 50 mm. Given these limitations, it is not possible to conclude that this technique offers secure and refined endoscopic closure. Further multicenter clinical studies with larger numbers of patients are required to investigate the efficacy and generalizability of this technique. A satisfactory method for successful suturing after colorectal ESD remains to be established.

In conclusion, EHS could achieve complete and sustained defect closure in the colorectum. However, the technique is not currently feasible in routine clinical practice given the long procedure time. Further modifications in the devices and technique are necessary to shorten the procedure time and overcome the technical challenges.

Competing interests

The study was supported by Olympus Corp.

Acknowledgment

This study was supported by Olympus Corp. research grant. We would like to thank Dr. Shih Yea Sylvia Wu (Endoscopy Division, National Cancer Center Hospital) for her kind support of this article.

• References

• 1 Yahagi N, Fujishiro M, Omata M. Endoscopic submucosal dissection of colorectal lesion. Dig Endosc 2004; 16: S178-S181
  CrossrefPubMedSearch in Google Scholar
• 2 Yamamoto H, Kawata H, Sunada K. et al. Successful en-bloc resection of large superficial tumors in the stomach and colon using sodium hyaluronate and small-caliber-tip transparent hood. Endoscopy 2003; 35: 690-694
  Thieme ConnectPubMedSearch in Google Scholar
• 3 Saito Y, Emura F, Matsuda T. et al. A new sinker-assisted endoscopic submucosal dissection for colorectal cancer. Gastrointest Endosc 2005; 62: 297-301
  CrossrefPubMedSearch in Google Scholar
• 4 Oka S, Tanaka S, Saito Y. et al. Local recurrence after endoscopic resection for large colorectal neoplasia: a multicenter prospective study in Japan. Am J Gastroenterol 2015; 110: 697-707
  CrossrefPubMedSearch in Google Scholar
• 5 Kobayashi N, Saito Y, Uraoka T. et al. Treatment strategy for laterally spreading tumors in Japan: before and after the introduction of endoscopic submucosal dissection. J Gastroenterol Hepatol 2009; 24: 1387-1392
  CrossrefPubMedSearch in Google Scholar
• 6 Nakajima T, Saito Y, Tanaka S. et al. Current status of endoscopic resection strategy for large, early colorectal neoplasia in Japan. Surg Endosc 2013; 27: 3262-3270
  CrossrefPubMedSearch in Google Scholar
• 7 Hashiguchi Y, Muro K, Saito Y. et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol 2020; 25: 1-42
  CrossrefPubMedSearch in Google Scholar
• 8 Tanaka S, Kashida H, Saito Y. et al. JGES guidelines for colorectal endoscopic submucosal dissection/endoscopic mucosal resection. Dig Endosc 2015; 27: 417-434
  CrossrefPubMedSearch in Google Scholar
• 9 Saito Y, Uraoka T, Yamaguchi Y. et al. A prospective, multicenter study of 1111 colorectal endoscopic submucosal dissections (with video). Gastrointest Endosc 2010; 72: 1217-1225
  CrossrefPubMedSearch in Google Scholar
• 10 Yamada M, Saito Y, Takamaru H. et al. Long-term clinical outcomes of endoscopic submucosal dissection for colorectal neoplasms in 423 cases: a retrospective study. Endoscopy 2017; 49: 233-242
  Thieme ConnectPubMedSearch in Google Scholar
• 11 Tanaka S, Tamegai Y, Tsuda S. et al. Multicenter questionnaire survey on the current situation of colorectal endoscopic submucosal dissection in Japan. Dig Endosc 2010; 22 (Suppl. 01) S2-8
  CrossrefPubMedSearch in Google Scholar
• 12 Oka S, Tanaka S, Kanao H. et al. Current status in the occurrence of postoperative bleeding, perforation and residual/local recurrence during colonoscopic treatment in Japan. Dig Endosc 2010; 22: 376-380
  CrossrefPubMedSearch in Google Scholar
• 13 Saito Y, Kawano H, Takeuchi Y. et al. Current status of colorectal endoscopic submucosal dissection in Japan and other Asian countries: progressing towards technical standardization. Dig Endosc 2012; 24 (Suppl. 01) 67-72
  CrossrefPubMedSearch in Google Scholar
• 14 Takeuchi Y, Iishi H, Tanaka S. 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 2014; 29: 1275-1284
  CrossrefPubMedSearch in Google Scholar
• 15 Fujihara S, Mori H, Kobara H. et al. The efficacy and safety of prophylactic closure for a large mucosal defect after colorectal endoscopic submucosal dissection. Oncol Rep 2013; 30: 85-90
  CrossrefPubMedSearch in Google Scholar
• 16 Otake Y, Saito Y, Sakamoto T. et al. New closure technique for large mucosal defects after endoscopic submucosal dissection of colorectal tumors (with video). Gastrointest Endosc 2012; 75: 663-667
  CrossrefPubMedSearch in Google Scholar
• 17 Wang J, Zhao L, Wang X. et al. A novel endoloop system for closure of colonic mucosal defects through a single-channel colonoscope. Endoscopy 2017; 49: 803-807
  Thieme ConnectPubMedSearch in Google Scholar
• 18 Nishizawa T, Akimoto T, Uraoka T. et al. Endoscopic string clip suturing method: a prospective pilot study (with video). Gastrointest Endosc 2018; 87: 1074-1078
  CrossrefPubMedSearch in Google Scholar
• 19 Goto O, Sasaki M, Akimoto T. et al. Endoscopic hand-suturing for defect closure after gastric endoscopic submucosal dissection: a pilot study in animals and in humans. Endoscopy 2017; 49: 792-797
  Thieme ConnectPubMedSearch in Google Scholar
• 20 Sano Y, Tanaka S, Kudo SE. et al. Narrow-band imaging (NBI) magnifying endoscopic classification of colorectal tumors proposed by the Japan NBI Expert Team. Dig Endosc 2016; 28: 526-533
  CrossrefPubMedSearch in Google Scholar
• 21 Matsuda T, Fujii T, Saito Y. et al. Efficacy of the invasive/non-invasive pattern by magnifying chromoendoscopy to estimate the depth of invasion of early colorectal neoplasms. Am J Gastroenterol 2008; 103: 2700-2706
  CrossrefPubMedSearch in Google Scholar
• 22 Saito Y, Otake Y, Sakamoto T. et al. Indications for and technical aspects of colorectal endoscopic submucosal dissection. Gut Liver 2013; 7: 263-269
  CrossrefPubMedSearch in Google Scholar
• 23 Aoki T, Nakajima T, Saito Y. et al. Assessment of the validity of the clinical pathway for colon endoscopic submucosal dissection. World J Gastroenterol 2012; 18: 3721-3726
  CrossrefPubMedSearch in Google Scholar
• 24 Tajiri H, Kitano S. Complications associated with endoscopic mucosal resection: definition of bleeding that can be viewed as accidental. Dig Endosc 2004; 16: S134-S136
  CrossrefPubMedSearch in Google Scholar
• 25 Ogasawara N, Yoshimine T, Noda H. et al. Clinical risk factors for delayed bleeding after endoscopic submucosal dissection for colorectal tumors in Japanese patients. Eur J Gastroenterol Hepatol 2016; 28: 1407-1414
  CrossrefPubMedSearch in Google Scholar
• 26 Okamoto K, Watanabe T, Komeda Y. et al. Risk factors for postoperative bleeding in endoscopic submucosal dissection of colorectal tumors. Oncology 2017; 93 (Suppl. 01) 35-42
  CrossrefPubMedSearch in Google Scholar
• 27 Seo M, Song EM, Cho JW. et al. A risk-scoring model for the prediction of delayed bleeding after colorectal endoscopic submucosal dissection. Gastrointest Endosc 2019; 89: 990-998
  CrossrefPubMedSearch in Google Scholar
• 28 Terasaki M, Tanaka S, Shigita K. et al. Risk factors for delayed bleeding after endoscopic submucosal dissection for colorectal neoplasms. Int J Colorectal Dis 2014; 29: 877-882
  CrossrefPubMedSearch in Google Scholar
• 29 Akintoye E, Kumar N, Aihara H. et al. Colorectal endoscopic submucosal dissection: a systematic review and meta-analysis. Endosc Int Open 2016; 4: E1030-E1044
  Thieme ConnectPubMedSearch in Google Scholar
• 30 Ito S, Hotta K, Imai K. et al. Risk factors of post-endoscopic submucosal dissection electrocoagulation syndrome for colorectal neoplasm. J Gastroenterol Hepatol 2018; 33: 2001-2006
  CrossrefPubMedSearch in Google Scholar
• 31 Yamashina T, Takeuchi Y, Uedo N. et al. Features of electrocoagulation syndrome after endoscopic submucosal dissection for colorectal neoplasm. J Gastroenterol Hepatol 2016; 31: 615-620
  CrossrefPubMedSearch in Google Scholar
• 32 Jung D, Youn YH, Jahng J. et al. Risk of electrocoagulation syndrome after endoscopic submucosal dissection in the colon and rectum. Endoscopy 2013; 45: 714-717
  Thieme ConnectPubMedSearch in Google Scholar
• 33 Lee SP, Sung IK, Kim JH. et al. Effect of prophylactic endoscopic closure for an artificial ulceration after colorectal endoscopic submucosal dissection: a randomized controlled trial. Scand J Gastroenterol 2019; 54: 1291-1299
  CrossrefPubMedSearch in Google Scholar
• 34 Yamasaki Y, Takeuchi Y, Iwatsubo T. et al. Line-assisted complete closure for a large mucosal defect after colorectal endoscopic submucosal dissection decreased post-electrocoagulation syndrome. Dig Endosc 2018; 30: 633-641
  CrossrefPubMedSearch in Google Scholar
• 35 Goto O, Sasaki M, Ishii H. et al. A new endoscopic closure method for gastric mucosal defects: feasibility of endoscopic hand suturing in an ex vivo porcine model (with video). Endosc Int Open 2014; 2: E111-116
  Thieme ConnectPubMedSearch in Google Scholar
• 36 Kantsevoy SV, Bitner M, Mitrakov AA. et al. Endoscopic suturing closure of large mucosal defects after endoscopic submucosal dissection is technically feasible, fast, and eliminates the need for hospitalization (with videos). Gastrointest Endosc 2014; 79: 503-507
  CrossrefPubMedSearch in Google Scholar

Corresponding author

Publication History

Received: 07 November 2019

Accepted: 04 February 2020

Article published online:
23 March 2020

© Georg Thieme Verlag KG
Stuttgart · New York

• References

• 1 Yahagi N, Fujishiro M, Omata M. Endoscopic submucosal dissection of colorectal lesion. Dig Endosc 2004; 16: S178-S181
  CrossrefPubMedSearch in Google Scholar
• 2 Yamamoto H, Kawata H, Sunada K. et al. Successful en-bloc resection of large superficial tumors in the stomach and colon using sodium hyaluronate and small-caliber-tip transparent hood. Endoscopy 2003; 35: 690-694
  Thieme ConnectPubMedSearch in Google Scholar
• 3 Saito Y, Emura F, Matsuda T. et al. A new sinker-assisted endoscopic submucosal dissection for colorectal cancer. Gastrointest Endosc 2005; 62: 297-301
  CrossrefPubMedSearch in Google Scholar
• 4 Oka S, Tanaka S, Saito Y. et al. Local recurrence after endoscopic resection for large colorectal neoplasia: a multicenter prospective study in Japan. Am J Gastroenterol 2015; 110: 697-707
  CrossrefPubMedSearch in Google Scholar
• 5 Kobayashi N, Saito Y, Uraoka T. et al. Treatment strategy for laterally spreading tumors in Japan: before and after the introduction of endoscopic submucosal dissection. J Gastroenterol Hepatol 2009; 24: 1387-1392
  CrossrefPubMedSearch in Google Scholar
• 6 Nakajima T, Saito Y, Tanaka S. et al. Current status of endoscopic resection strategy for large, early colorectal neoplasia in Japan. Surg Endosc 2013; 27: 3262-3270
  CrossrefPubMedSearch in Google Scholar
• 7 Hashiguchi Y, Muro K, Saito Y. et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol 2020; 25: 1-42
  CrossrefPubMedSearch in Google Scholar
• 8 Tanaka S, Kashida H, Saito Y. et al. JGES guidelines for colorectal endoscopic submucosal dissection/endoscopic mucosal resection. Dig Endosc 2015; 27: 417-434
  CrossrefPubMedSearch in Google Scholar
• 9 Saito Y, Uraoka T, Yamaguchi Y. et al. A prospective, multicenter study of 1111 colorectal endoscopic submucosal dissections (with video). Gastrointest Endosc 2010; 72: 1217-1225
  CrossrefPubMedSearch in Google Scholar
• 10 Yamada M, Saito Y, Takamaru H. et al. Long-term clinical outcomes of endoscopic submucosal dissection for colorectal neoplasms in 423 cases: a retrospective study. Endoscopy 2017; 49: 233-242
  Thieme ConnectPubMedSearch in Google Scholar
• 11 Tanaka S, Tamegai Y, Tsuda S. et al. Multicenter questionnaire survey on the current situation of colorectal endoscopic submucosal dissection in Japan. Dig Endosc 2010; 22 (Suppl. 01) S2-8
  CrossrefPubMedSearch in Google Scholar
• 12 Oka S, Tanaka S, Kanao H. et al. Current status in the occurrence of postoperative bleeding, perforation and residual/local recurrence during colonoscopic treatment in Japan. Dig Endosc 2010; 22: 376-380
  CrossrefPubMedSearch in Google Scholar
• 13 Saito Y, Kawano H, Takeuchi Y. et al. Current status of colorectal endoscopic submucosal dissection in Japan and other Asian countries: progressing towards technical standardization. Dig Endosc 2012; 24 (Suppl. 01) 67-72
  CrossrefPubMedSearch in Google Scholar
• 14 Takeuchi Y, Iishi H, Tanaka S. 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 2014; 29: 1275-1284
  CrossrefPubMedSearch in Google Scholar
• 15 Fujihara S, Mori H, Kobara H. et al. The efficacy and safety of prophylactic closure for a large mucosal defect after colorectal endoscopic submucosal dissection. Oncol Rep 2013; 30: 85-90
  CrossrefPubMedSearch in Google Scholar
• 16 Otake Y, Saito Y, Sakamoto T. et al. New closure technique for large mucosal defects after endoscopic submucosal dissection of colorectal tumors (with video). Gastrointest Endosc 2012; 75: 663-667
  CrossrefPubMedSearch in Google Scholar
• 17 Wang J, Zhao L, Wang X. et al. A novel endoloop system for closure of colonic mucosal defects through a single-channel colonoscope. Endoscopy 2017; 49: 803-807
  Thieme ConnectPubMedSearch in Google Scholar
• 18 Nishizawa T, Akimoto T, Uraoka T. et al. Endoscopic string clip suturing method: a prospective pilot study (with video). Gastrointest Endosc 2018; 87: 1074-1078
  CrossrefPubMedSearch in Google Scholar
• 19 Goto O, Sasaki M, Akimoto T. et al. Endoscopic hand-suturing for defect closure after gastric endoscopic submucosal dissection: a pilot study in animals and in humans. Endoscopy 2017; 49: 792-797
  Thieme ConnectPubMedSearch in Google Scholar
• 20 Sano Y, Tanaka S, Kudo SE. et al. Narrow-band imaging (NBI) magnifying endoscopic classification of colorectal tumors proposed by the Japan NBI Expert Team. Dig Endosc 2016; 28: 526-533
  CrossrefPubMedSearch in Google Scholar
• 21 Matsuda T, Fujii T, Saito Y. et al. Efficacy of the invasive/non-invasive pattern by magnifying chromoendoscopy to estimate the depth of invasion of early colorectal neoplasms. Am J Gastroenterol 2008; 103: 2700-2706
  CrossrefPubMedSearch in Google Scholar
• 22 Saito Y, Otake Y, Sakamoto T. et al. Indications for and technical aspects of colorectal endoscopic submucosal dissection. Gut Liver 2013; 7: 263-269
  CrossrefPubMedSearch in Google Scholar
• 23 Aoki T, Nakajima T, Saito Y. et al. Assessment of the validity of the clinical pathway for colon endoscopic submucosal dissection. World J Gastroenterol 2012; 18: 3721-3726
  CrossrefPubMedSearch in Google Scholar
• 24 Tajiri H, Kitano S. Complications associated with endoscopic mucosal resection: definition of bleeding that can be viewed as accidental. Dig Endosc 2004; 16: S134-S136
  CrossrefPubMedSearch in Google Scholar
• 25 Ogasawara N, Yoshimine T, Noda H. et al. Clinical risk factors for delayed bleeding after endoscopic submucosal dissection for colorectal tumors in Japanese patients. Eur J Gastroenterol Hepatol 2016; 28: 1407-1414
  CrossrefPubMedSearch in Google Scholar
• 26 Okamoto K, Watanabe T, Komeda Y. et al. Risk factors for postoperative bleeding in endoscopic submucosal dissection of colorectal tumors. Oncology 2017; 93 (Suppl. 01) 35-42
  CrossrefPubMedSearch in Google Scholar
• 27 Seo M, Song EM, Cho JW. et al. A risk-scoring model for the prediction of delayed bleeding after colorectal endoscopic submucosal dissection. Gastrointest Endosc 2019; 89: 990-998
  CrossrefPubMedSearch in Google Scholar
• 28 Terasaki M, Tanaka S, Shigita K. et al. Risk factors for delayed bleeding after endoscopic submucosal dissection for colorectal neoplasms. Int J Colorectal Dis 2014; 29: 877-882
  CrossrefPubMedSearch in Google Scholar
• 29 Akintoye E, Kumar N, Aihara H. et al. Colorectal endoscopic submucosal dissection: a systematic review and meta-analysis. Endosc Int Open 2016; 4: E1030-E1044
  Thieme ConnectPubMedSearch in Google Scholar
• 30 Ito S, Hotta K, Imai K. et al. Risk factors of post-endoscopic submucosal dissection electrocoagulation syndrome for colorectal neoplasm. J Gastroenterol Hepatol 2018; 33: 2001-2006
  CrossrefPubMedSearch in Google Scholar
• 31 Yamashina T, Takeuchi Y, Uedo N. et al. Features of electrocoagulation syndrome after endoscopic submucosal dissection for colorectal neoplasm. J Gastroenterol Hepatol 2016; 31: 615-620
  CrossrefPubMedSearch in Google Scholar
• 32 Jung D, Youn YH, Jahng J. et al. Risk of electrocoagulation syndrome after endoscopic submucosal dissection in the colon and rectum. Endoscopy 2013; 45: 714-717
  Thieme ConnectPubMedSearch in Google Scholar
• 33 Lee SP, Sung IK, Kim JH. et al. Effect of prophylactic endoscopic closure for an artificial ulceration after colorectal endoscopic submucosal dissection: a randomized controlled trial. Scand J Gastroenterol 2019; 54: 1291-1299
  CrossrefPubMedSearch in Google Scholar
• 34 Yamasaki Y, Takeuchi Y, Iwatsubo T. et al. Line-assisted complete closure for a large mucosal defect after colorectal endoscopic submucosal dissection decreased post-electrocoagulation syndrome. Dig Endosc 2018; 30: 633-641
  CrossrefPubMedSearch in Google Scholar
• 35 Goto O, Sasaki M, Ishii H. et al. A new endoscopic closure method for gastric mucosal defects: feasibility of endoscopic hand suturing in an ex vivo porcine model (with video). Endosc Int Open 2014; 2: E111-116
  Thieme ConnectPubMedSearch in Google Scholar
• 36 Kantsevoy SV, Bitner M, Mitrakov AA. et al. Endoscopic suturing closure of large mucosal defects after endoscopic submucosal dissection is technically feasible, fast, and eliminates the need for hospitalization (with videos). Gastrointest Endosc 2014; 79: 503-507
  CrossrefPubMedSearch in Google Scholar