11/26/2010 Conventional versus hybrid knife endoscopic submucosal dissection in large colorectal laterally spreading tumors: A propensity score analysis Yang B, Shen J, Zhong W, Han H, Lu P, Jiang F, - Saudi J Gastroenterol
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Conventional versus hybrid knife endoscopic submucosal dissection in large colorectal laterally spreading tumors: A propensity score analysis

1 Department of General Surgery, Shanghai Xuhui Center Hospital, Shanghai, China
2 Department of Orthopedics, Shanghai Xuhui Center Hospital, Shanghai, China

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Date of Submission20-Aug-2022
Date of Acceptance08-Nov-2022
Date of Web Publication27-Dec-2022


Background: Colorectal endoscopic submucosal dissection (CR-ESD) has become a promising treatment for laterally spreading tumors (LSTs), but is accompanied by great challenges. This study aimed to evaluate the efficacy and safety of CR-ESD with a hybrid knife, versus the conventional technique for LSTs ≥30 mm in diameter, and analyze the risk factors for piecemeal resection and perforation.
Methods: Patients eligible for CR-ESD were divided into two groups according to the use of the hybrid knife (HK group) or the use of the conventional technique, with an interchange of injection and hook knife (C-group). We performed propensity score matching (PSM) to compare the HK group and the C-group. Risk predictors for perforation and piecemeal resection were identified.
Results: PSM identified 61 (132 patients) and 61 (129 patients) patients in the C-group and the HK group, respectively. Resection speed was significantly faster in the HK group than in the C-group (18.86 vs. 13.33 mm2/min, P < 0.001). The rate of knife exchange was significantly lower in the HK group than in the C-group (1.6% vs. 49.2%, P < 0.001). Multivariate analysis revealed that unfavorable locations, including the splenic flexure, hepatic flexure, or cecum, were predictive of piecemeal resection. The presence of severe fibrosis and a semilunar fold were independent risk factors for perforation.
Conclusions: The use of a hybrid knife appears to increase CR-ESD resection speed. The indicators for piecemeal resection or perforation in CR-ESD identified herein might help to assess the technical difficulties of CR-ESD.

Keywords: Endoscopic submucosal dissection, hybrid knife, lateral spreading tumors

How to cite this URL:
Yang B, Shen J, Zhong W, Han H, Lu P, Jiang F. Conventional versus hybrid knife endoscopic submucosal dissection in large colorectal laterally spreading tumors: A propensity score analysis. Saudi J Gastroenterol [Epub ahead of print] [cited 2023 Feb 2]. Available from: https://www.saudijgastro.com/preprintarticle.asp?id=365752

   Introduction Top

Colorectal cancer (CRC) was the third most common cancer worldwide in 2021 and the second most common cause of cancer-related deaths.[1] Colorectal laterally spreading tumors (LSTs) have been recognized as an important precursor of advanced CRC.[2] A meta-analysis revealed that LST granular mixed type (LST-GM) and LST nongranular type (LST-NG) were related to a substantial risk of submucosal invasion (10.5% and 31.6%, respectively).[3] Additionally, the risk of submucosal invasion increases with tumor size, and LSTs ≥30 mm were associated with 16.5% submucosal invasion. Currently, colorectal endoscopic submucosal dissection (CR-ESD) has become a standard treatment for premalignant and early malignant colorectal tumors.[4]

However, CR-ESD remains technically demanding and has a high risk of perforation mainly due to colorectal anatomical features, including thin walls, peristalsis, semilunar folds, and angulated flexures. Additionally, some tumor characteristics, including submucosal fibrosis, size and location, may increase difficulties. The difficulty mainly stems from the process of submucosal dissection with Endo knives and is demonstrated from the following three perspectives: long procedure time, piecemeal resection, and perforation.[5] First, many devices have been developed to improve the endoscopic submucosal dissection (ESD) techniques.[6] A hybrid knife is a multifunctional device that combines an electrocautery needle and an ultrafine high-pressure fluid jet system in a single instrument, which is reported to reduce rectal ESD difficulties and procedure time.[6],[7],[8] Second, the importance of complete resection for superficial CRC cannot be underestimated, as it is imperative for the evaluation of histopathology, resection margins, and submucosal invasion. The United States National Comprehensive Cancer Network (NCNN) guidelines recommend that additional surgery is required for malignant colorectal polyps after piecemeal resection. Therefore, superficial CRC treated with piecemeal resection still needs radical surgery.[9],[10] In addition, piecemeal resection is associated with a high recurrence rate of approximately 27.5%.[11] Finally, while perforation is common, it is also the most serious complication that can occur during CR-ESD. It may lead to severe peritonitis because of bacterial contamination and fecal leakage. Although most perforations can be endoscopically managed with metal clips or an over-the-scope-clip (OTSC) system, perforations ≥30 mm warrant surgery.[12]

However, there are limited data on the outcomes of CR-ESD with a hybrid knife. In addition, there have been few studies using multivariate analysis of clinical parameters in relation to perforation and piecemeal resection of large LSTs. Thus, in this propensity score matching (PSM) study, we aimed to compare the clinical outcomes between conventional CR-ESD and CR-ESD with a hybrid knife, and clarify the factors predicting perforation and piecemeal resection.

   Materials and Methods Top

Study design

We conducted a retrospective analysis of 261 consecutive patients with LSTs ≥30 mm in diameter, who were treated with CR-ESD, at Shanghai Xuhui Center Hospital between July 2017 and June 2021 [Figure 1]. Subjects who met one or more of the following criteria were excluded: (1) presence of invasion pattern defined as irregular and distorted epithelial crests in a demarcated area; (2) uncorrectable coagulation disorders; (3) American Society of Anesthesiologists grade 3 or above; or (4) certain findings of pathological lymph node on computed tomography scan. Before the operation, each patient involved was informed about the risks and benefits of CR-ESD and the patient provided written informed consent. This protocol was approved by Shanghai Xuhui Center Hospital Ethics Committee (Issue No. 0126 (2022). IRB).
Figure 1: Diagram of the study design. LST, laterally spreading tumor; ESD, endoscopic submucosal dissection; HK, hybrid knife

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Characteristics of LST

According to Kudo's classification system, LSTs were classified into four subtypes based on their endoscopic appearances: LST-granular and homogeneous (LST-GH), LST-GM, LST-nongranular and flat elevated (LST-NG-PE), and LST-nongranular and pseudo depressed (LST-NG-PD).[2] The degree of submucosal fibrosis was categorized into three categories based on findings after injection of mixed solution: F0, no fibrosis; F1, mild fibrosis; and F2, severe fibrosis.[13] The macroscopic type and degree of fibrosis were confirmed by reviews from two independent endoscopists. In cases of disagreement, a third reviewer was consulted until a consensus was reached.

Colorectal ESD operation histological assessment

Endoscopic equipment and accessories of conventional CR-ESD were introduced as described in previous reports.[14],[15] For a brief description, conventional CR-ESD consists of three steps [Figure 2]: (1) submucosal injection of mixed solution, including 5% indigo carmine and saline, using a 23-gauge disposable needle; (2) circumferential mucosal resection with a needle knife 5 mm away from the tumor margin and submucosal dissection with a hook knife (Olympus KD-620LR); and (3) removal of visible blood vessels of artificial colorectal ulcer with an Argo plasma coagulation or hemostatic forceps. However, in cases of large LSTs or LSTs at unfavorable locations, the hybrid knife (Erbe I shape knife) was used at the discretion of endoscopists from the beginning of CR-ESD, after patients provided their consent. All procedures were performed by two highly experienced colonoscopists who had experience with more than 60 conventional CR-ESDs. The pathological diagnosis was established following the revised Vienna classification.[16]
Figure 2: Endoscopic submucosal dissection for a large laterally spreading tumor with a hybrid knife. Endoscopic finding of laterally spreading tumor under (a) white light imaging and with (b) magnifying narrow-band-imaging. (c) after submucosal injection of glycerol, (d) circumferential incision and (e) submucosal dissection with a Hybrid I type knife. (f) artificial ulcer observed after the removal of the tumor. (g) the resected specimen measuring 80mmx100mm

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Study definition

Perforation occurred when mesenteric fat or the intra-abdominal space was directly observed through the colon wall defect during CR-ESD. En bloc resection is a tumor removed in a single piece. A curative resection was R0 removal of lesions without the risk of lymphovascular metastasis.[4] Bleeding was defined as hemorrhage that required blood transfusion or invasive intervention. Stenosis occurred when the colorectal lumen was narrowed to prevent the passage of a 11.8-mm-diameter colonoscope, regardless of symptoms. Local recurrence was defined as neoplasia at the previous resection scar with the same histology as the primary lesion, during follow-up colonoscopy. Knife exchange was defined as the use of more than one knife in the process of submucosal dissection. The resection speed was calculated with the formula πAB/4C, where A is the largest diameter, B the smallest diameter, and C the procedure time.

Statistical analysis

PSM was performed to minimize the effects of potential confounding factors. Propensity scores were estimated using the following variables: age, sex, tumor location and size, macroscopic type, histopathology, fibrosis, submucosal invasion, and presence of convergence and semilunar fold. The 1:1 nearest-neighbor matching from the group subjected to conventional technique with an interchange of injection and hook knife (C-group), and the group in which hybrid knife was used (HK group) was performed using a caliper set at 0.02. Continuous variables are expressed as the median and interquartile range (IQR), and categorical variables are presented as frequencies and percentages. Comparisons between the two groups were performed using Student's t-test and Chi-square tests (or Fisher's exact tests when at least 25% of values showed expected cell frequencies <5). Univariate analysis identified the risk factors for piecemeal resection and perforation, and significant factors were subjected to multivariate logistic analysis to determine independent associations. A P value <0.05 was considered significant. Data were analyzed using commercial software (SPSS Statistics, version 20.0; SPSS Inc.)

   Results Top

Clinicopathological characteristics of patients and lesions

The median age of all patients (before PSM: 261 patients) was 66 (59–72) years, and 50.6% of them were female [Table 1]. Tumors were mainly found in the rectum in 44.1%, cecum in 14.9%, ascending colon in 11.9%, and hepatic flexure in 9.2% of patients. The most common type was granular mixed (33.0%), followed by granular homogenous (30.3%), nongranular flat elevated (23.4%), and nongranular pseudo depressed (13.4%). Fifty-two (19.9%) patients had severe fibrosis. Histopathology demonstrated that 43.3%, 41.8%, and 14.9% of the lesions were low-grade dysplasia, high-grade dysplasia, and adenocarcinoma, respectively, with a median tumor size of 40 mm (35–47). Of 39 adenocarcinomas, 31 (80%) were intramucosal and eight (20%) were submucosal. Noncurative resection occurred in four patients with adenocarcinoma because of deep invasion (two patients) and lymphovascular invasion (two patients). All patients underwent surgical resection with lymphadenectomy immediately after colorectal ESD. These patients had no lymph node metastasis.
Table 1: Clinicopathological characteristics of patients and tumors before and after propensity score matching

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Before PSM, age, sex distribution, submucosal invasion, presence of convergence, presence of fold convergence, and submucosal fibrosis were not significantly different between the C-group and the HK group. However, as the hybrid knife was used for large LSTs or LSTs at unfavorable locations, tumor location and tumor size were significantly different between the two groups (P = 0.01 and P < 0.01, respectively). Additionally, there were significant differences in macroscopic type, histopathology, and the presence of semilunar fold between the two groups (P = 0.03, P < 0.01, and P < 0.01, respectively). PSM did not reveal statistically significant differences in any clinical or pathological characteristic of patients or lesions between the two groups.

The procedural outcomes of colorectal ESD

After PSM, the median resection speed was significantly faster in the HK group (18.86 mm2/min [IQR: 13.70–25]) than in the C-group (13.33 mm2/min [IQR: 9.59–18.05], P < 0.001), whereas en bloc and curative resection rates were not significantly different between the C-group and the HK group (90.2% [55/61] vs. 91.8% [56/61], P = 1 and 86.9% [53/61] vs. 91.8% [56/61], P = 0.398, respectively) [Table 2]. Additionally, the rate of knife replacement during ESD was significantly lower in the HK group than in the C-group (1.6% [1/62] vs. 48.4% [30/62], P < 0.001). Neither the procedure time (43 min [IQR: 36–62] vs. 51 min [IQR: 42–67], P = 0.076) nor the perforation rate (3.3% [2/61] vs. 13.1% [8/61], P = 0.099) differed between the two groups.
Table 2: Clinical outcomes of endoscopic submucosal dissection of large laterally spreading tumors

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Additionally, before PSM, the median resection speed was also significantly faster in the HK group (21.67 mm2/min [IQR: 15.79–27.63]) than in the C-group (13.07 mm2/min [IQR: 9.60–15.72]). The resection speed in the rectum was the fastest (22.38 mm2/min [16.67–28.53]), while the resection speed in the sigmoid was the slowest (9.14 mm2/min [7.57–13.68]). Internal traction with double band and a clip was used for 18 patients. Stenosis occurred in three patients, and all lesions had ≥90% circumferential mucosal defects after rectal ESD. They were successfully treated with standard balloon dilation and had a standard endoscope passed at subsequent surveillance. Local recurrence was observed in three patients who underwent piecemeal resection and all of them were treated endoscopically.

Risk factors for perforation and piecemeal resection

The potential risk factors for perforation and piecemeal resection were analyzed by univariate and multivariate regression and are shown in [Table 3]. In the univariate logistic regression analysis, unfavorable location, including splenic flexure, hepatic flexure, or cecum, was the leading risk factor for piecemeal resection (odds ratio [OR] 6.75, 95% confidence interval [CI] 2.53, 18.05, P < 0.001). In contrast, age, sex, tumor size ≥60 mm, procedure time ≥60 min, macroscopic type, submucosal fibrosis, histopathology, resection method, and submucosal invasion were not associated with piecemeal resection.
Table 3: Univariate and multivariate analyses of risk factors for piecemeal resection and perforation in all lesions (before propensity score matching; n=261)

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Submucosal fibrosis, histopathology, submucosal invasion, tumor size ≥60 mm, and the presence of a semilunar fold were found to be significant risk factors for perforation in the univariate analysis, with ORs of 8.0 (95% CI 3.43, 18.6), 3.4 (1.4, 8.26), 10 (2.34, 42.66), 3.06 (1.17, 7.99), and 7.36 (3.12, 17.38), respectively. Multivariate analysis revealed that fibrosis and semilunar fold were significant risk factors for perforation, with ORs of 6.15 (2.39, 15.80) and 7.42 (2.49, 21.04). No statistically significant correlation was observed between perforation and location, macroscopic type, or the resection method.

   Discussion Top

To the best of our knowledge, this was the first large-sample study to compare the efficacy and safety of a water jet-assisted hybrid knife and the conventional technique with needle knives and an injection needle in CR-ESD procedures using PSM, which decreased the effect of selection biases. We found that the use of the hybrid knife improved the resection speed. Additionally, the results showed that unfavorable locations, including the splenic flexure, hepatic flexure, or cecum, were risk factors for piecemeal resection. Furthermore, the presence of severe fibrosis and a semilunar fold were risk factors for perforation.

The results of the present study were comparable with a prospective study of 50 experimental gastric ESDs, with a hybrid knife, in animals.[8] The resection speed in the HK group was significantly faster than that in the C-group. Several possibilities might explain why the hybrid knife achieved faster speed. The major advantage of the HK group over the C-group is that the hybrid knife also has the function of submucosal injection and coagulation, which significantly decreased the rate of knife exchange in the HK group (1.6%).[6] Another possible reason was that the hybrid knife can create a long-lasting and adequate cushion with the ultrafine high-pressure water jet. The sufficient space between mucosa and muscularis propria enables endoscopists to clearly visualize the submucosa being resected. Additionally, the hybrid knife can reduce difficulties in maintaining a stable and desired position throughout ESD, particularly when the effect of diaphragmatic movement is prominent. However, 14 cases in the HK group warranted additional hemostatic forceps to address spurting intraoperative bleeding. Given these findings, we concluded that hemostatic forceps should be used in cases of large vessels, instead of the hybrid knife. Despite similar procedure time between both groups, the dissection speed was faster for the HK group. This was because the mean tumor size of the HK group was significantly larger than that of the C-group. In the HK group, there were 42 cases of LSTs ≥50 mm and seven cases of LSTs ≥100 mm.

Considering the low risk of submucosal invasion of LST-GH, endoscopic piecemeal mucosal resection is acceptable.[17] In contrast, LST-GM ≥30 mm and LST-NG have high risk of submucosal invasion and warrant en bloc removal.[3] Piecemeal resection of these tumors may lead to local cancerous recurrence and even distant metastasis. Kobayashi et al.[18] reported a fairly low rate (3%) of piecemeal resection of CR-ESD in Japan, while our findings showed that piecemeal resection occurred in 7.3% of patients. This disparity may be driven by the lightweight mucosal flap and large tumor size. The lightweight mucosal flap does not move away from the muscle layer by gravity.[19] In addition, a large tumor size is associated with fold convergence and semilunar folds. The presence of fold convergence and semilunar folds are the risk factors for severe fibrosis and increase the rate of piecemeal resection.[20] Iacopini et al.[21] indicated that colon location was a risk factor for piecemeal resection. Our study showed that an unfavorable location, including the splenic flexure, hepatic flexure, or cecum, was an independent risk factor for piecemeal resection, consistent with results of Hori et al.[5] The great angulation of flexure leads to poor visualization of the oral part of the lesion, particularly for those lesions in the inner curve of flexure.[22] Inaccurate submucosal injection may cause the lesion to turn more towards the oral side and increase maneuverability difficulties.[23] As the endoscope is placed vertically to the cecum wall, LSTs at the cecum are associated with poor maneuverability. Additionally, the thin wall of the cecum and the presence of the ileocecal valve and appendiceal orifice may contribute to the high rate of piecemeal resection of LSTs in the cecum.[24],[25] Regarding local recurrence after CR-ESD, piecemeal resection is the only established risk factor. The recurrence rate rises suddenly to 16.7% when there are more than three resected specimens.[26]

Another concern about CR-ESD is perforation, which limits its widespread diffusion. Previous studies have described that large tumor size, fold convergence, underlying semilunar folds, colonic location, and inexperienced endoscopists are preoperative risk factors for perforation.[27],[28],[29] The present study demonstrated that the presence of a semilunar fold was an independent preoperative risk factor for perforation. The presence of severe fibrosis is a well-known intraoperative risk factor for perforation,[28],[30],[31] which agrees with our study results. However, preoperative evaluation of fibrosis is challenging and makes limited contributions to reducing perforation. Recent studies have found that lesions across the fold, with protruded morphology or scars, were correlated with severe fibrosis.[20],[21],[32] Due to the friability of invasive tissue, submucosal invasion is relevant for high rate of perforation.[31] Hong et al.[28] developed a SELF (tumor size, endoscopist experience, tumor location, submucosal fibrosis) scoring system which could identify patients at high risk of perforation (score >4) before CR-ESD, in order to develop better preventive strategies including selection of expert endoscopists and adequate preparation of devices. As CR-ESD is an operator-dependent procedure, the perforation rate decreases with greater clinical experience in CR-ESD.[13] Risk factors predicting perforation also vary with endoscopists' increasing experience in CR-ESD. Kenichiro et al.[27] demonstrated that location of the lesion within the colon was a significant predictor for failure of ESD or perforation for inexperienced colonoscopists. Similarly, Hori et al.[5] reported that flexure location was a factor for perforation for beginners, but not for experienced endoscopists. All current studies focused on the analysis of preoperative and intraoperative risk factors for perforations.[29],[33] However, there is no risk prediction model of perforation stratified according to endoscopists' experience in CR-ESD.

Although we conducted this study with a relatively large sample, there were still several limitations. First, it was a single-center retrospective and nonrandomized study. The hybrid knife was used for large LSTs or LSTs at unfavorable locations. Thus, we performed PSM to reduce selection biases. Second, it was conducted as a post hoc analysis. Finally, our follow-up length was too short to evaluate long-term recurrence.

In conclusion, the hybrid knife could safely and effectively improve resection speed. The presence of severe fibrosis and a semilunar fold were independent risk factors for perforation. Unfavorable locations, including the splenic flexure, hepatic flexure, and cecum, were independent risk factors for piecemeal resection.

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Conflicts of interest

There are no conflicts of interest.

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Correspondence Address:
Fei Jiang,
966 Huaihai Rd (M), Xuhui District, Shanghai - 200041
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/sjg.sjg_373_22


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  [Table 1], [Table 2], [Table 3]


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