Subscribe to RSS
DOI: 10.1055/a-1884-7849
Anchoring endoscopic mucosal resection versus conventional endoscopic mucosal resection for large nonpedunculated colorectal polyps: a randomized controlled trial
Abstract
Background Colorectal polyps > 10 mm in size are often incompletely resected. Anchoring-endoscopic mucosal resection (A-EMR) is the technique of making a small incision at the oral side of the polyp using a snare tip after submucosal injection to avoid slippage during ensnaring. This study was performed to evaluate whether A-EMR could increase the complete resection rate for large colorectal polyps compared with conventional endoscopic mucosal resection (C-EMR).
Methods Polyps with sizes of 10–25 mm were randomly allocated to either the A-EMR or the C-EMR groups.
Results 105 and 106 polyps were resected using A-EMR and C-EMR, respectively. In the intention-to-treat population, the complete resection rate was 89.5 % in the A-EMR group and 74.5 % in the C-EMR group (relative risk [RR] 1.20, 95 %CI 1.04 to 1.38; P = 0.01). The en bloc resection rates for the A-EMR and C-EMR groups were 92.4 % vs. 76.4 % (RR 1.21, 95 %CI 1.06 to 1.37; P = 0.005) and R0 resection rates were 77.1 % vs. 64.2 % (RR 1.18, 95 %CI 0.98 to 1.42; P = 0.07), respectively. The median (interquartile range [IQR]) total procedure time was 3.2 (2.6–4.1) minutes in the A-EMR group and 3.0 (2.2–4.6) minutes in the C-EMR group (median difference 0.2 minutes, 95 %CI −0.22 to 0.73; P = 0.25). There was one episode of delayed bleeding and one perforation in the C-EMR group.
Conclusions A-EMR was superior to C-EMR for the complete resection of large colorectal polyps. A-EMR can be considered one of the standard methods for the removal of colorectal polyps of 10 mm or more in size.
#
Introduction
Colonoscopy reduces the incidence and mortality of colorectal cancer (CRC) by detecting and removing premalignant polyps. However, post-colonoscopy CRCs account for 9 % of all CRCs, and 20 %–30 % of post-colonoscopy CRCs are likely related to incomplete resection [1] [2].
Conventional endoscopic mucosal resection (C-EMR) is the preferred method for the resection of large nonpedunculated polyps because the submucosal injection is expected to reduce the risk of deep mural injuries from electrocautery and increase the complete resection rate by securing a clear margin of normal tissue [3] [4] [5]. However, the incomplete resection and local recurrence rates of EMR for polyps > 10 mm in size have been reported to be as high as 20 % and 15 %, respectively [6] [7] [8].
Anchoring-EMR (A-EMR) or “tip-in EMR” is a method for the complete resection of large-sized colorectal polyps [9] [10] [11] [12] [13] [14] [15] [16]. The only difference between A-EMR and C-EMR is the process of making a small mucosal incision at the oral side of the lesion, which is helpful for deploying the snare in a wider area laterally and avoiding slippage during ensnaring by anchoring the snare tip into the submucosal layer. To date, however, only a small-sized randomized study has been conducted to compare A-EMR and C-EMR for large nonpedunculated colorectal polyps [16]. Therefore, this study was performed to evaluate the efficacy and safety of A-EMR compared with C-EMR for the endoscopic removal of nonpedunculated polyps of 10–25 mm in size.
#
Methods
Study design
This was a prospective, randomized, controlled, parallel, superiority, single-center trial. The study was conducted at Seoul St. Mary’s Hospital, The Catholic University of Korea, Seoul, South Korea. Nonpedunculated polyps with sizes of 10–25 mm detected during colonoscopy were randomly allocated to the A-EMR or C-EMR groups.
All procedures were conducted in accordance with the Declaration of Helsinki and the study protocol was approved by the Institutional Review Board (KC20EISE0171). All patients provided their written informed consent before participating in the study. The study was reported according to the CONSORT guidelines.
#
Study participants
The participants were prospectively enrolled between April 2020 and January 2021. We included patients aged 19–85 years undergoing endoscopic resection for one or more nonpedunculated polyps that were 10–25 mm in diameter. The exclusion criteria were: (i) having a known or suspected malignant polyp, a previously incompletely resected polyp, a subepithelial lesion, or a pedunculated polyp; (ii) inflammatory bowel disease; (iii) the uninterrupted use of antithrombotic drugs; and (iv) presence of a coagulopathy.
The baseline characteristics of the eligible participants including their demographic data and the indications for colonoscopy (polypectomy, positive fecal occult blood test, colorectal cancer screening or surveillance, and abdominal symptoms) were collected.
#
Interventions
All patients were prepared with 1 L of polyethylene glycol plus ascorbic acid solution (Taejoon Pharm, Seoul, South Korea) or 4 L of polyethylene glycol solution (Taejoon Pharm). The procedures were performed by two experienced endoscopists with over 10 000 colonoscopy cases (L.B.I and C.Y.S.) and one less experienced endoscopist with fewer than 1000 colonoscopy cases (O.C.K.). All endoscopists had a self-learning of at least 20 A-EMRs with reference to Japanese and European video sources before the trial was started [10] [16].
All the procedures were carried out with a high definition RGB sequential video-endoscopy system (CV-290; Olympus Co., Tokyo, Japan). A high definition colonoscope with magnification function (CF-HQ290I or PCF-260AZI; Olympus) was used for all procedures. Once a polyp was identified, eligibility was assessed by the endoscopic findings, and eligibility for the study was confirmed. Because the resection technique (A-EMR or C-EMR) was allocated for the patient, multiple eligible polyps in each patient were resected using the same resection technique.
Normal saline with or without a few drops of an indigo carmine solution was used for submucosal injection. A 25- or 15-mm oval snare (Olympus or Taewoong Medical, Gimpo, Korea) with Endocut Q/I or the forced coagulation current of the electrosurgical unit (VIO300D; Erbe Elektromedizin GmbH, Tübingen, Germany) was used for resection. The polyp size was measured by comparison with the size of the deployed snare. En bloc resection at the initial snaring was attempted in all cases.
The A-EMR procedure included the following: (i) submucosal injection; (ii) a small mucosal incision being made at the oral side of the polyp with a snare tip using cut current; (iii) the polyp including the surrounding normal mucosa being snared, while keeping the snare tip in the submucosal layer; and (iv) resection using electrocautery ([Fig. 1]; [Video 1]). A mucosal incision at the oral side was omitted in the C-EMR procedure. After resection, the mucosal defect was washed with a waterjet and the resection margin was meticulously observed with white-light, narrow-band imaging (NBI), and magnifying NBI endoscopy to identify any residual polyp tissue. Magnifying chromoendoscopy with indigo carmine was additionally performed for residual histologic examination when the appearance with magnifying NBI endoscopy was uncertain.
Video 1 A video demonstrating the anchoring endoscopic mucosal resection (A-EMR) procedure.
Quality:
When the optical decision was not clear because of cautery artifacts, distorted pit/microvascular patterns, tearing of the resection margin, and continuous oozing, among other reasons, a forceps biopsy was performed where residual polyp tissue was most likely to be present. When residual tissue was apparent endoscopically, additional snaring was performed. Endoscopic closure was performed where there was blood spurting, continuous oozing for more than 30 seconds, a visible vessel, or deep mural injury. Protruded and superficial polyps were categorized as Paris classification type I and type II, respectively [17]. The location of colorectal polyps was classified as the right colon (from the cecum to the splenic flexure), the left colon (from the splenic flexure to the sigmoid colon), and the rectum. Ineligible polyps were treated according to the usual clinical practice of our department.
#
Histological examination
Each resected specimen was initially examined by the pathologists in charge according to the routine procedure of our institution and reviewed again by the experienced gastrointestinal pathologist (L.S.H.), who was blinded to the clinical information. Any specimens with a histologic discrepancy were reviewed and discussed by the pathologist in charge and the gastrointestinal pathologist. Histological classification was conducted based on the World Health Organization classifications.
#
Outcome parameters
The primary outcome of this study was the difference in complete resection rates between the A-EMR and C-EMR groups. En bloc resection was classified as the resection of the polyp in one piece. Complete resection was defined as en bloc resection and the absence of residual polyp with endoscopic confidence, or en bloc resection and negative forceps biopsy for a suspicious resection margin.
Secondary outcomes included the en bloc resection rate, R0 resection rate, total procedure time, procedure time until the completion of the first snaring, and the incidence of adverse events. R0 resection was defined as a histologic examination showing the absence of polyp tissue at the margin of the resected specimen, while R1 resection was the presence of neoplastic tissue at the margin. Rx resection was recorded when the involvement of the resection margin could not be determined because of electrocautery effects or a tangential tissue section.
The total procedure time was measured as the time from the submucosal injection to complete removal of the polyp, and the procedure time until the completion of the first snaring was the time from the submucosal injection to the completion of the first snare resection.
Perforation was defined as a full-layered defect of the colonic wall that needed immediate endoscopic or surgical intervention. Immediate bleeding was not regarded as an adverse event when it was managed immediately by endoscopic hemostatic procedures. Delayed bleeding was defined as overt bleeding within 7 days after the colonoscopic procedure that required a separate endoscopic hemostatic procedure. All patients were supposed to visit our outpatient clinic within 2 weeks to be checked for any adverse events after polypectomy and to receive their histologic diagnosis and post-polypectomy colonoscopy surveillance plan. They were also asked whether they had experienced abdominal pain, tarry stool, hematochezia, and/or dizziness, and they underwent a brief physical examination.
#
Sample size calculation
We hypothesized that the complete resection rate for nonpedunculated polyps of 10–25 mm would be between the en bloc resection rate and the R0 resection rate. Previous studies have reported that the en bloc and R0 resection rates of C-EMR for colorectal polyps of 10–20 mm were 75.0 %–85.7 % and 50.0 %–67.3 %, respectively [18] [19]. Pioche et al. [10] reported that the en bloc resection rate and R0 resection rate of A-EMR for colorectal polyps of 8–20 mm were 92.0 % and 82.8 %, respectively. Therefore, combining our preliminary experience with C-EMR and A-EMR for colorectal polyps of 10–25 mm, we estimated that the complete resection rate of C-EMR and A-EMR for such colorectal polyps would be approximately 72 % and 88 %, respectively. Thus, the required sample size was 105 polyps for each group with a two-sided α-value of 0.05, a power of 80 %, and a 10 % dropout rate.
#
Randomization and monitoring
A stratified permuted block randomization method was employed. A research assistant who was not involved in clinical practice generated the random allocation sequence, and the contents were concealed until the intervention group was assigned at the time of polyp resection. The patients were blinded to the allocated treatment method before and during the endoscopic procedures.
#
Statistics
The primary outcome was analyzed by intention-to-treat (ITT) analysis. Categorical outcomes were represented by the relative risk (RR) with 95 %CI. Continuous outcomes were represented by the median difference with 95 %CI. As each patient could have more than one polyp, the generalized estimating equations (GEE) were used to control for within-patient correlations. We also performed pre-planned subgroup analyses based on the size, morphology, and the location of lesions using GEE. P < 0.05 was considered to indicate significance. All statistical analyses were carried out using R Statistical Software (version 4.2.0; R Core Team, 2021).
#
#
Results
Patients and polyp characteristics
A total of 532 patients were enrolled in the study between April 2020 and January 2021 ([Fig. 2]). Among them, 368 patients were excluded because they did not have any eligible polyps during colonoscopy (no polyp; n = 109), had only a pedunculated polyp (n = 7), only polyps < 10 mm (n = 245), only polyps > 25 mm (n = 4), or only endoscopically malignant polyps (n = 3). Finally, 84 patients with 105 eligible polyps and 80 patients with 106 eligible polyps were randomly allocated into the A-EMR and C-EMR groups, respectively. An eligible polyp in each of two patients who were initially allocated into the A-EMR group was finally treated by the C-EMR technique because of repetitive slippage of the snare tip from the small mucosal incision on the oral side; these two patients were excluded from the per-protocol analysis. There was no follow-up loss through patients not visiting to confirm their adverse events, and receive their histological diagnosis and post-polypectomy colonoscopy surveillance plan.
A-EMR, anchoring-endoscopic mucosal resection; C-EMR, conventional-endoscopic mucosal resection.
[Table 1] shows the baseline characteristics of the patients and their polyps in the A-EMR and C-EMR groups. The median size of the polyps was 14 mm in both the A-EMR and C-EMR groups. The polyp was located in the right colon in 72.4 % and 81.1 % of cases in the A-EMR and C-EMR groups, respectively. The morphology was classified as type II in 81.0 % and 76.4 % of the A-EMR and C-EMR group, respectively.
A-EMR, anchoring-endoscopic mucosal resection; C-EMR, conventional endoscopic mucosal resection; IQR, interquartile range.
#
Primary and secondary outcomes
In the intention-to-treat population, the complete resection rate was 89.5 % in the A-EMR group and 74.5 % in the C-EMR group (RR 1.20, 95 %CI 1.04 to 1.38; P = 0.01) ([Table 2]). The en bloc resection rates for the A-EMR and C-EMR groups were 92.4 % vs. 76.4 % (RR 1.21, 95 %CI 1.06 to 1.37; P = 0.005) and the R0 resection rates were 77.1 % vs. 64.2 % (RR 1.18, 95 %CI 0.98 to 1.42; P = 0.07), respectively.
|
A-EMR |
C-EMR |
Relative risk[*] (95 %CI) |
Median difference[*] (95 %CI) |
P [*] |
|
|
Complete resection, n (%) |
94 (89.5) |
79 (74.5) |
1.20 (1.04 to 1.38) |
– |
0.01 |
|
En bloc resection, n (%) |
97 (92.4) |
81 (76.4) |
1.21 (1.06 to 1.37) |
– |
0.005 |
|
R0 resection, n (%) |
81 (77.1) |
68 (64.2) |
1.18 (0.98 to 1.42) |
– |
0.07 |
|
Procedure time until the completion of the first snaring, median (IQR), minutes |
3.2 (2.6–3.9) |
2.7 (2.1–4.0) |
– |
0.5 (0.07 to 0.75) |
0.03 |
|
Total procedure time, median (IQR), minutes |
3.2 (2.6–4.1) |
3.0 (2.2–4.6) |
– |
0.2 (−0.22 to 0.73) |
0.25 |
|
Forceps biopsy for suspicious resection margin, n (%) |
28 (26.7) |
21 (19.8) |
1.35 (0.81–2.22) |
– |
0.25 |
|
Prophylactic clip use, n (%) |
18 (17.1) |
37 (34.9) |
0.48 (0.29–0.80) |
– |
0.005 |
|
Adverse events, n (%) |
|||||
|
Delayed bleeding |
0 (0.0) |
1 (0.9) |
– |
||
|
Perforation |
0 (0.0) |
1 (0.9) |
– |
A-EMR, anchoring-endoscopic mucosal resection; C-EMR, conventional endoscopic mucosal resection; IQR, interquartile range.
* Relative risk, median difference, and P value were calculated by generalized estimating equations.
The median (IQR) procedure time until the completion of the first snaring was longer in the A-EMR group compared with the C-EMR group (3.2 [2.6–3.9] vs. 2.7 [2.1–4.0] minutes; median difference 0.5 minutes, 95 %CI 0.07 to 0.75; P = 0.03). However, the total procedure time was not significantly different between the two groups (3.2 [2.6–4.1] vs. 3.0 [2.2–4.6] minutes; median difference 0.2 minutes, 95 %CI −0.22 to 0.73; P = 0.25).
There was no immediate bleeding. One patient in the C-EMR group had delayed bleeding, which was managed successfully by endoscopic clipping, and one perforation occurred in the C-EMR group ([Table 2]).
In the per-protocol population, the complete resection rate was 90.3 % in the A-EMR group and 74.5 % in the C-EMR group (RR 1.21, 95 %CI 1.05 to 1.39; P = 0.008) (Table 1 s, see online-only Supplementary material). The en bloc resection rates for the A-EMR and C-EMR group were 93.2 % vs. 76.4 % (RR 1.21, 95 %CI 1.06 to 1.38; P = 0.003) and R0 resection rates were 78.6 % vs. 64.2 % (RR 1.20, 95 %CI 1.00 to 1.44; P = 0.049), respectively.
#
Subgroup analysis
Subgroup analysis is shown in [Fig. 3]. A-EMR was better for complete resection of colorectal lesions over 15 mm and lesions located in the right colon. A-EMR was superior to C-EMR for complete resection of both flat and protruded lesions.
† No relative risk owing to small sample size.
#
#
Discussion
In the present study, we clearly showed that the complete resection and en bloc resection rates of A-EMR were higher than those of C-EMR for nonpedunculated polyps of 10–25 mm. The incomplete resection rate of polyps of 10–20 mm has been reported to be as high as 17.3 %–20.8 % in previous studies [6] [20] [21]. Moreover, lesions ≥ 20 mm frequently require piecemeal resection, whereas most lesions < 20 mm typically can be removed en bloc by the EMR technique [3]. It is well known that piecemeal EMR is associated with higher rates of post-polypectomy recurrence [22]. In our study, the incomplete resection rate of A-EMR for nonpedunculated polyps of 10–25 mm was only 10.5 %.
Endoscopic submucosal resection is an effective technique for the en bloc resection of large colorectal lesions; however, the application of the technique is limited to lesions with superficial submucosal invasion or submucosal fibrosis because of the perforation risk, prolonged procedure time, and technical difficulty. A circumferential submucosal incision prior to EMR, a so-called “precut-EMR,” is less time-consuming and technically easier, but our retrospective analyses with propensity score matching have shown that the technique does not increase the complete resection or en bloc resection rates compared with conventional EMR [5].
In our study, the procedure time until the completion of the first snaring was longer in the A-EMR group (3.2 vs. 2.7 minutes; median difference 0.5 minutes, 95 %CI 0.07 to 0.75 minutes; P = 0.03) because the technique required time for anchoring of the snare tip. However, the median difference in the total procedure times between the A-EMR and C-EMR groups was only 0.2 minutes (95 %CI −0.22 to 0.73; P = 0.25), despite the achievement of higher complete resection, en bloc resection, and R0 resection rates. This was because the en bloc resection rate in the A-EMR group was higher than that of the C-EMR group, which resulted in fewer snarings being performed in the A-EMR group. Therefore, A-EMR appears to be an excellent method for the resection of nonpedunculated polyps of 10–25 mm in terms of achieving complete resection and also presenting lower technical difficulty.
A previous Japanese study also showed that A-EMR significantly improved the en bloc resection rate for nonpedunculated lesions of 15–25 mm compared with C-EMR (90.2 % vs. 73.1 %; P = 0.04) [16]; however, there was no statistical difference in the R0 resection rate between their A-EMR and C-EMR groups (73.2 % vs. 58.5 %; P = 0.19), which might have been caused by the relatively small number of study patients (n = 41 in each group). The definition of en bloc resection in the Japanese study was compatible with that of complete resection in our study, and our subgroup analysis also revealed that the complete resection rate in the A-EMR group was higher than that in the C-EMR group, especially when the polyp was ≥ 15 mm (RR 1.39, 95 %CI 1.05 to 1.84).
In the present study, the complete resection rate in the A-EMR group was also higher than that in the C-EMR group when the polyp was located at the right colon. It is assumed that the snare was more likely to slip during ensnaring in the right colon because of the higher transverse folds compared with the left colon. The greatest virtue of A-EMR is that the snare can avoid spillage during ensnaring because its tip is fixed in the incised submucosal layer. This technique enables the snare to capture more of the lesion because it can be deployed in a wider area laterally by pushing the sheath to the oral side. It also prevents the snare tip from lifting when the lesion is located on a convex surface. One of the most important points for successful EMR was anchoring the snare tip in the best position, where the snare could cover the entire lesion with enough normal margin and avoid torque during ensnaring.
In the present study, prophylactic clip use in the C-EMR group was also higher than that in the A-EMR group. We believe that deeper resection occurred more frequently with C-EMR as a wider normal margin needs to be secured, although the depth of resection was not measured prospectively.
A retrospective French study reported that A-EMR was related to a considerable transmural perforation rate (3/125 patients; 2.1 %) and all the perforations occurred when en bloc resection was attempted for a lesion of > 2 cm in size [10]. However, in our study, there were no episodes of perforation or bleeding in the 105 patients in the A-EMR group.
This study had several limitations. First, it was performed in a single center. Second, the polyp recurrence rate was not evaluated by follow-up colonoscopy. Third, the endoscopists could not be blinded to the allocations.
In conclusion, A-EMR was better than C-EMR for complete resection of nonpedunculated polyps of 10–25 mm and can be recommended as a standard method for the resection of large colorectal polyps.
#
#
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgments
Statistical consultation was supported by the Department of Biostatistics of the Catholic Research Coordinating Center.
* Joint first authors
-
References
- 1 Robertson DJ, Lieberman DA, Winawer SJ. et al. Colorectal cancers soon after colonoscopy: a pooled multicohort analysis. Gut 2014; 63: 949-956
- 2 Rutter MD, Beintaris I, Valori R. et al. World Endoscopy Organization consensus statements on post-colonoscopy and post-imaging colorectal cancer. Gastroenterology 2018; 155: 909-925.e903
- 3 Kaltenbach T, Anderson JC, Burke CA. et al. Endoscopic removal of colorectal lesions—recommendations by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2020; 158: 1095-1129
- 4 Ferlitsch M, Moss A, Hassan C. et al. Colorectal polypectomy and endoscopic mucosal resection (EMR): European Society of Gastrointestinal Endoscopy (ESGE) clinical guideline. Endoscopy 2017; 49: 270-297
- 5 Oh CK, Lee BI, Lee SH. et al. Circumferential submucosal incision prior to endoscopic mucosal resection versus conventional endoscopic mucosal resection for colorectal lesions with endoscopic features of sessile serrated lesions. Surg Endosc 2022; 36: 2087-2095
- 6 Djinbachian R, Iratni R, Durand M. et al. Rates of incomplete resection of 1- to 20-mm colorectal polyps: a systematic review and meta-analysis. Gastroenterology 2020; 159: 904-914.e912
- 7 Adler J, Toy D, Anderson JC. et al. Metachronous neoplasias arise in a higher proportion of colon segments from which large polyps were previously removed, and can be used to estimate incomplete resection of 10–20 mm colorectal polyps. Clin Gastroenterol Hepatol 2019; 17: 2277-2284
- 8 Belderbos TD, Leenders M, Moons LM. et al. Local recurrence after endoscopic mucosal resection of nonpedunculated colorectal lesions: systematic review and meta-analysis. Endoscopy 2014; 46: 388-402
- 9 Noh SM, Kim JY, Park JC. et al. Tip-in versus conventional endoscopic mucosal resection for flat colorectal neoplasia 10 mm or larger in size. Int J Colorectal Dis 2020; 35: 1283-1290
- 10 Pioche M, Wallenhorst T, Lepetit H. et al. Endoscopic mucosal resection with anchoring of the snare tip: multicenter retrospective evaluation of effectiveness and safety. Endosc Int Open 2019; 7: E1496-E1502
- 11 Lee CY, Chen MY, Lin HJ. et al. Safety and efficacy of tip‐in endoscopic mucosal resection for large sessile colorectal polyps: A single‐center experience in Taiwan. Adv Dig Med 2020; 7: 58-62
- 12 Toyonaga T, Man-I M, Morita Y. et al. The new resources of treatment for early stage colorectal tumors: EMR with small incision and simplified endoscopic submucosal dissection. Dig Endosc 2009; 21: S31-S37
- 13 Jacques J, Legros R, Charissoux A. et al. Anchoring the snare tip by means of a small incision facilitates en bloc endoscopic mucosal resection and increases the specimen size. Endoscopy 2017; 49: E39-E41
- 14 Chien H, Imai K, Hotta K. et al. Tip-in EMR for R0 resection for a large flat colonic tumor. Gastrointest Endosc 2016; 84: 743
- 15 Shumeiko O, Imai K, Hotta K. Tip‐in endoscopic mucosal resection for R0 resection of a poorly lifted colonic laterally spreading tumor with possible submucosal invasion. Dig Endosc 2020; 32: e15-e16
- 16 Imai K, Hotta K, Ito S. et al. Tip-in endoscopic mucosal resection for 15-to 25-mm colorectal adenomas: a single-center, randomized controlled trial (STAR Trial). Am J Gatroenterol 2021; 116: 1398-1405
- 17 The Paris endoscopic classification of superficial neoplastic lesions. esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 2003; 58: S3-S43
- 18 Yamashina T, Uedo N, Akasaka T. et al. Comparison of underwater vs. conventional endoscopic mucosal resection of intermediate-size colorectal polyps. Gastroenterology 2019; 157: 451-461.e452
- 19 Yoshida N, Inoue K, Dohi O. et al. Efficacy of precutting endoscopic mucosal resection with full or partial circumferential incision using a snare tip for difficult colorectal lesions. Endoscopy 2019; 51: 871-876
- 20 Pohl H, Srivastava A, Bensen SP. et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology 2013; 144: 74-80 e71
- 21 Pedersen IB, Bretthauer M, Kalager M. et al. Incomplete endoscopic resection of colorectal polyps: a prospective quality assurance study. Endoscopy 2021; 53: 383-391
- 22 Woodward TA, Heckman MG, Cleveland P. et al. Predictors of complete endoscopic mucosal resection of flat and depressed gastrointestinal neoplasia of the colon. Am J Gastroenterol 2012; 107: 650-654
Corresponding author
Publication History
Received: 16 February 2022
Accepted after revision: 24 June 2022
Accepted Manuscript online:
24 June 2022
Article published online:
31 August 2022
© 2022. Thieme. All rights reserved.
Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany
-
References
- 1 Robertson DJ, Lieberman DA, Winawer SJ. et al. Colorectal cancers soon after colonoscopy: a pooled multicohort analysis. Gut 2014; 63: 949-956
- 2 Rutter MD, Beintaris I, Valori R. et al. World Endoscopy Organization consensus statements on post-colonoscopy and post-imaging colorectal cancer. Gastroenterology 2018; 155: 909-925.e903
- 3 Kaltenbach T, Anderson JC, Burke CA. et al. Endoscopic removal of colorectal lesions—recommendations by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2020; 158: 1095-1129
- 4 Ferlitsch M, Moss A, Hassan C. et al. Colorectal polypectomy and endoscopic mucosal resection (EMR): European Society of Gastrointestinal Endoscopy (ESGE) clinical guideline. Endoscopy 2017; 49: 270-297
- 5 Oh CK, Lee BI, Lee SH. et al. Circumferential submucosal incision prior to endoscopic mucosal resection versus conventional endoscopic mucosal resection for colorectal lesions with endoscopic features of sessile serrated lesions. Surg Endosc 2022; 36: 2087-2095
- 6 Djinbachian R, Iratni R, Durand M. et al. Rates of incomplete resection of 1- to 20-mm colorectal polyps: a systematic review and meta-analysis. Gastroenterology 2020; 159: 904-914.e912
- 7 Adler J, Toy D, Anderson JC. et al. Metachronous neoplasias arise in a higher proportion of colon segments from which large polyps were previously removed, and can be used to estimate incomplete resection of 10–20 mm colorectal polyps. Clin Gastroenterol Hepatol 2019; 17: 2277-2284
- 8 Belderbos TD, Leenders M, Moons LM. et al. Local recurrence after endoscopic mucosal resection of nonpedunculated colorectal lesions: systematic review and meta-analysis. Endoscopy 2014; 46: 388-402
- 9 Noh SM, Kim JY, Park JC. et al. Tip-in versus conventional endoscopic mucosal resection for flat colorectal neoplasia 10 mm or larger in size. Int J Colorectal Dis 2020; 35: 1283-1290
- 10 Pioche M, Wallenhorst T, Lepetit H. et al. Endoscopic mucosal resection with anchoring of the snare tip: multicenter retrospective evaluation of effectiveness and safety. Endosc Int Open 2019; 7: E1496-E1502
- 11 Lee CY, Chen MY, Lin HJ. et al. Safety and efficacy of tip‐in endoscopic mucosal resection for large sessile colorectal polyps: A single‐center experience in Taiwan. Adv Dig Med 2020; 7: 58-62
- 12 Toyonaga T, Man-I M, Morita Y. et al. The new resources of treatment for early stage colorectal tumors: EMR with small incision and simplified endoscopic submucosal dissection. Dig Endosc 2009; 21: S31-S37
- 13 Jacques J, Legros R, Charissoux A. et al. Anchoring the snare tip by means of a small incision facilitates en bloc endoscopic mucosal resection and increases the specimen size. Endoscopy 2017; 49: E39-E41
- 14 Chien H, Imai K, Hotta K. et al. Tip-in EMR for R0 resection for a large flat colonic tumor. Gastrointest Endosc 2016; 84: 743
- 15 Shumeiko O, Imai K, Hotta K. Tip‐in endoscopic mucosal resection for R0 resection of a poorly lifted colonic laterally spreading tumor with possible submucosal invasion. Dig Endosc 2020; 32: e15-e16
- 16 Imai K, Hotta K, Ito S. et al. Tip-in endoscopic mucosal resection for 15-to 25-mm colorectal adenomas: a single-center, randomized controlled trial (STAR Trial). Am J Gatroenterol 2021; 116: 1398-1405
- 17 The Paris endoscopic classification of superficial neoplastic lesions. esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 2003; 58: S3-S43
- 18 Yamashina T, Uedo N, Akasaka T. et al. Comparison of underwater vs. conventional endoscopic mucosal resection of intermediate-size colorectal polyps. Gastroenterology 2019; 157: 451-461.e452
- 19 Yoshida N, Inoue K, Dohi O. et al. Efficacy of precutting endoscopic mucosal resection with full or partial circumferential incision using a snare tip for difficult colorectal lesions. Endoscopy 2019; 51: 871-876
- 20 Pohl H, Srivastava A, Bensen SP. et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology 2013; 144: 74-80 e71
- 21 Pedersen IB, Bretthauer M, Kalager M. et al. Incomplete endoscopic resection of colorectal polyps: a prospective quality assurance study. Endoscopy 2021; 53: 383-391
- 22 Woodward TA, Heckman MG, Cleveland P. et al. Predictors of complete endoscopic mucosal resection of flat and depressed gastrointestinal neoplasia of the colon. Am J Gastroenterol 2012; 107: 650-654
A-EMR, anchoring-endoscopic mucosal resection; C-EMR, conventional-endoscopic mucosal resection.
† No relative risk owing to small sample size.