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Department of Gastroenterology, Shenzhen People's Hospital (The Second Clinical Medical College, Jinan University, The First Affiliated Hospital, Southern University of Science and Technology), No.1017, Dongmen North Road, Luohu District, Shenzhen, Guangdong 518020, China
Department of Gastroenterology, Shenzhen People's Hospital (The Second Clinical Medical College, Jinan University, The First Affiliated Hospital, Southern University of Science and Technology), No.1017, Dongmen North Road, Luohu District, Shenzhen, Guangdong 518020, China
Department of Gastroenterology, Shenzhen People's Hospital (The Second Clinical Medical College, Jinan University, The First Affiliated Hospital, Southern University of Science and Technology), No.1017, Dongmen North Road, Luohu District, Shenzhen, Guangdong 518020, China
Cold snare polypectomy (CSP) is a promising technique for the removal of sessile serrated polyps (SSPs) ≥ 10 mm. However, the efficacy and safety of this technique remain undetermined.
Aims
We aimed to comprehensively evaluate the efficacy and safety of CSP for SSPs ≥ 10 mm.
Methods
PubMed, EMBASE, Web of Science and Cochrane Library were searched up to January 2021.
Results
A total of 10 studies consisting of 1727 SSPs (range, 10–40 mm) from 1021 patients were included. The overall rates of technical success, adverse events (AEs) and residual SSPs were 100%, 0.7% and 2.9%, respectively. Subgroup analysis showed that the rates of technical success and AEs were comparable between CSP and cold endoscopic mucosal resection (EMR) (99.9% vs. 100% and 1.3% vs. 0.5%, respectively), between the proximal and distal colon (100% vs. 99.9% and 0.3% vs. 0, respectively), and between polyps of 10–19 mm and ≥20 mm (99.8% vs. 100% and 0.9% vs. 0, respectively). However, subgroup analysis showed that the rate of residual SSPs was slightly lower in CSP compared with cold EMR (1.3% vs. 3.9%), as well as in polyps of 10–19 mm compared with those ≥20 mm (3.1% vs. 4.7%).
Conclusion
CSP was an effective and safe technique for removing SSPs ≥ 10 mm.
]. In addition, several studies have demonstrated that SSPs possess the rapid progression potential to invasive carcinomas with lymphatic invasion and metastasis [
Small colonic microsatellite unstable adenocarcinomas and high-grade epithelial dysplasias in sessile serrated adenoma polypectomy specimens: a study of eight cases.
Cold snare polypectomy vs. cold forceps polypectomy using double-biopsy technique for removal of diminutive colorectal polyps: a prospective randomized study.
]. Traditional endoscopic mucosal resection (EMR) and endoscopic submucosal dissection (ESD) are suggested for lesions larger than 20 mm according to international guidelines, while hot polypectomy is recommended for lesions of 10–20 mm [
]. Although traditional EMR is an effective therapeutic technique for the treatment of large SSPs using submucosal injection and electrocautery, it is associated with a risk of serious adverse events (AEs) such as post-EMR bleeding (PEB) and deep mural injury (DMI) [
]. However, two studies have recently shown that routine use of prophylactic clipping can reduce PEBs after removal of large SSPs (more than 20 mm) and may be cost-effective in patients with a high risk of bleeding [
Currently, CSP, including cold snare and cold EMR, is used to treat large SSPs. van Hattem et al. in their prospective study, have demonstrated that piecemeal-CSP (p-CSP) is comparable to EMR for the removal of SSPs ≥20 mm in terms of technical success rate and recurrence rate (100% vs. 99.6%, P = 1 and 4.3% vs. 4.6%, P = 0.9, respectively). However, p-CSP is associated with lower post-procedure bleeding (PPB) (0 vs.5.1%, P = 0.01) [
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
]. Thoguluva Chandrasekar et al. have also reported that for the treatment of SSPs ≥10 mm, CSP has significantly lower rates of PPB and residual rate compared with traditional EMR (0 vs. 2.3%, P-0.03 and 0.9% vs. 5%, P = 0.01, respectively) [
]. However, the current data are limited by relatively smaller sample size and reported mostly from single-center experiences. Therefore, we comprehensively performed a meta-analysis and assessed the efficacy and safety of CSP for the treatment of SSPs ≥10 mm in size.
2. Methods
This study was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) recommendations [
The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration.
Four independent investigators (D-F L, M-F Y, Y Z, and Y-L B) performed a systematic electronic literature search in PubMed, Embase, Web of Science, and Cochrane library for eligible studies from the beginning of indexing for each database to January 31, 2021. The detailed search strategy is available in supplemental materials (Supplement 1). Moreover, additional studies were included by manual searching. Finally, the study protocol was registered in the International Prospective Register of Systematic Reviews (PROSPERO) (No. CRD42021238037).
2.2 Inclusion and exclusion criteria
Inclusion criteria were set as follows: 1. studies involving either cold snare or cold EMR for the treatment of SSPs ≥ 10 mm in size; 2. studies including efficacy or safety data on the removal of SSPs; and 3. full-length articles in English.
Exclusion criteria were set as follows: 1. studies reporting outcomes on SSPs< 10 mm; 2. non-human studies; 3. abstract and case reports; and 4. case series with< 10 patients.
2.3 Data extraction
All included studies were independently reviewed by three reviewers (F X, CW, and B-H W). The following details were extracted from each study: first author, the year of publication, study region, age, gender, number of patients, the number of SSPs, the size of SSPs, the location of SSPs, the method of SSPs resection, follow-up duration, complete resection rate, AE rate, and residual rate. Any conflict or disagreement was resolved by discussion and consensus with a third author (J Y).
2.4 Quality assessment
Two reviewers (Z-L X and D-G Z) independently assessed the methodologic quality using the Newcastle-Ottawa Scale (NOS) for non-randomized studies, and scores of 0–3, 4–6, and 7–9 corresponded to low, medium, and high quality, respectively [
The technical success rate was defined as the rate of complete macroscopic resection. AEs included immediate bleeding, delayed bleeding, and perforation. The immediate bleeding rate was defined as the rate of clinically significant bleeding requiring endoscopic intervention during SSP resection. In contrast, the delayed bleeding rate was defined as the rate of clinically significant bleeding requiring hospitalization, blood transfusion, endoscopy, surgical intervention, or angiography within 14 days of polypectomy. Perforation was evidenced by diffuse gas or intestinal fluid localized in the peritoneum. The residual rate was the proportion of residual SSPs collected at the resection site during follow-up colonoscopy.
2.6 Outcomes
The primary outcome was the technical success rate. The secondary outcomes were rates of AEs and residual SSPs. Beside, subgroup analyses were also performed: 1. outcomes based on techniques for the treatment of SSPs (cold snare vs. cold EMR). 2. outcomes based on the location of SSPs (proximal colon vs. distal colon), and 3. outcomes based on the size of SSPs (10–19 mm vs. ≥ 20 mm).
2.7 Statistical analysis
The effect of interest was pooled rates in the form of proportions of overall included patients (%) with 95% confidence limits. A random-effects model was applied to analyze significant heterogeneity (I2 > 50% and P < 0.05); otherwise, a fixed-effects model was adopted. The corresponding forest plots were constructed to express pooled estimates of the outcomes with the weights of individual studies. A funnel plot and Egger test were used to assess publication bias. Sensitivity analysis was performed by systematically removing individual studies in turn to explore its effect on the rates of technical success, AEs, and residual SSPs. Univariate and multivariate meta-regression was performed to investigate the predictive factors of technical success, AEs, and residual SSPs. All statistical analyses were performed using the meta-package in R Statistics 3.6.1 (Lanzhou, China) by two authors (D-F L and L-S W). All tests were two-sided, and P < 0.05 was considered statistically significant.
3. Results
3.1 Study characteristics
A total of 144 studies were retrieved using the search strategy and manual search. Of these 144 studies, 87 potential studies were retained after 57 duplications were removed. After reviewing the titles, abstracts and full texts, 10 studies matched the selection criteria in the final analysis [
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
]. Only SSPs removed by cold snare or cold EMR were included in the final analysis. A total of 1021 patients were included, with 59.5% of patients being females and a median age of the population of 62 years (Table S1).
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
] reported data on the size stratification of SSPs, 664 SSPs were 10–19 mm in size, and 356 SSPs were ≥ 20 mm in size (Table S2).
3.2 Quality of included studies
Newcastle-Ottawa scores were used to evaluate the methodological quality of non-randomized studies. The results showed that seven studies were moderate-quality studies, and three were low-quality studies (Table S3).
3.3 Technical success rate
The technical success rate was reported in all studies (Table S4). Of these 1727 SSPs, 1726 SSPs were successfully removed using CSP and the overall technical success rate was 100% (95% CI, 99.8–100%) with a low level of heterogeneity (I2 = 0%, P = 1) (Fig. 2A).
Fig. 2Technical success rate. A, Overall technical success rate; B, Technical success rate of the cold snare; C, Technical success rate of cold EMR; D, Technical success rate of the proximal colon; E, Technical success rate of the distal colon; F, Technical success rate of 10–19 mm in size; G, Technical success rate of ≥ 20 mm in size.
Subgroup analysis was performed based on techniques showing that 712 of 713 SSPs were successfully removed using cold snare, and 1014 SSPs were successfully removed using the cold EMR (Table S4). The technical success rate of cold snare and cold EMR was 99.8% (95% CI, 99.0–100%) and 100% (95% CI, 99.8–100%) respectively, with a low level of heterogeneity (Table S4, Fig. 2B, and C).
Subgroup analysis was performed based on the location of SSPs and showed that the technical success rate was 100% (95% CI, 99.6–100%) and 99.9% (95% CI, 99.3–100%) with a low level of heterogeneity (I2 = 0%, P = 1) when SSPs were located in the proximal and distal colon, respectively (Table S4, Fig. 2D, and E).
Subgroup analysis was carried out based on the size of SSPs, showing that the technical success rate was 99.8% (95% CI, 98.9–100%) and 100% (95% CI, 99.3–100%) when the size of SSPs was 10–19 mm and ≥ 20 mm, respectively, with a low level of heterogeneity (I2 = 0%, P = 1) (Table S4, Fig. 2F, and G).
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
]. A total of 17 AEs occurred during CSP including 15 cases of immediate bleeding and two cases of delayed bleeding. However, there were no perforations. Therefore, the overall AEs rate was 0.7% (95% CI, 0.2–1.2%) with a low level of heterogeneity (I2 = 0%, P = 0.55) (Table S5 and Fig. 3A).
Fig. 3Adverse events rate. A, Overall AE rate; B, Adverse events rate of the cold snare; C, AE rate of cold EMR; D, AE rate of the proximal colon; E, AE rate of the distal colon; F, AE rate of 10–19 mm in size; G, AE rate of ≥ 20 mm in size.
Subgroup analysis was conducted based on techniques, and showing that the AE rate was 1.3% (95% CI, 0.4–2.3%) and 0.5% (95% CI, 0–1.1%) when using cold snare and cold EMR, respectively, with a low level of heterogeneity (Table S6, Fig. 3B, and C).
Subgroup analysis was carried out based on the location of SSPs, showing that the AE rate was 0.3% (95% CI, 0–1.0%) and 0% (95% CI, 0–0.9%) when SSPs were located in the proximal and distal colon, respectively, with a low level of heterogeneity (Table S6, Fig. 3D, and E).
Subgroup analysis was carried out based on the size of SSPs, showing that the AE rate was 0.9% (95% CI, 0–3.2%) and 0% (95% CI, 0–0.9%) when the size of SSPs was 10–19 mm and ≥ 20 mm, respectively, with a low level of heterogeneity (Table S6, Fig. 3F, and G).
3.5 Residual SSPs
All studies reported the rate of residual SSPs, and there were 34 residual SSPs for 1129 SSPs with a median follow-up duration of 6 months (range, 3–24 months). The overall rate of residual SSPs was 2.9% (95% CI, 0.8–5.0%) with a high level of heterogeneity (I2 = 72%, P < 0.01) (Table S7 and Fig. 4A).
Fig. 4Residual SSPs rate. A, Overall residual rate; B, Residual rate of the cold snare; C, Residual rate of cold EMR; D, Residual rate of 10–19 mm in size; E, Residual rate of ≥ 20 mm in size.
Subgroup analysis was carried out based on techniques used, revealing that the residual rate was 1.3% (95% CI, 0–3.6%) and 3.9% (95% CI, 0.8–6.9%) when using cold snare and cold EMR, respectively, with a high level of heterogeneity (Table S8, Fig. 4B, and C).
Subgroup analysis was conducted based on the size of SSPs, and indicating that the residual rate was 3.1% (95% CI, 0–6.6%) and 4.7% (95% CI, 0.9–8.5%) when the size of SSPs was 10–19 mm and ≥ 20 mm, respectively, with a low level of heterogeneity (Table S7, Fig. 4D, and E).
3.6 Meta-regression analysis
Univariate meta-regression analysis revealed that the mean size of SSPs was an independent factor for the AE rate [odds ratio (OR), -0.0012; 95% CI, -0.0265 to -0.0001; P = 0.027], whereas the mean size of SSPs was not associated with the rate of technical success and residual SSPs (P = 0.7358 and P = 0.5159, respectively). Univariate meta-regression analysis revealed that the techniques (cold snare or cold EMR) were not associated with the rates of technical success, AEs, and residual SSPs (P = 0.5414, P = 0.1070, and P = 0.2598, respectively). Moreover, multivariate meta-regression analysis revealed that the mean size of SSPs and techniques were not associated with the rates of technical success, AE and residual SSPs (P = 0.9258, P = 0.1223, P = 0.8396, P = 0.6049, P = 0.8002, and P = 0.3576, respectively).
3.7 Publication bias and sensitivity analysis
The funnel plot and Egger test showed no publication bias for the rates of technical success (P = 0.93) and AEs (P = 0.62) (Fig. S1A and B). However, Egger's test indicated a significant difference of publication bias in the rate of residual SSPs (P = 0.014) (Fig. S1C). Beside, the forest plot showed little sensitivity change by systematically removing each study for technical success rate, AE rate and residual rate (Fig. S2A–C).
4. Discussion
To the best of our knowledge, this study was the first systematic analysis of the available studies on the efficacy and safety of CSP (with or without submucosal injection) for the removal of SSPs ≥ 10 mm. The currently available data are limited by smaller sample sizes and reported mainly from single-center studies. Therefore, this systematic review was performed to provide comprehensive outcomes of SSPs removal using CSP and offered comparisons of procedures (cold snare vs. cold EMR), SSPs size (10–19 mm vs. ≥20 mm), and SSPs location (proximal vs. distal colon). In the present study, we found that CSP was an encouraging modality for removing SSPs ≥ 10 mm with a technical success of 100%. At the same time, subgroup analysis showed that the technical success rate was comparable between the cold snare and cold EMR subgroups, between the 10–19 mm and ≥20 mm groups, and between proximal and distal colon subgroups (99.9% vs.100%, 99.8% vs.100% and 100% vs. 99.9%, respectively). Moreover, the AE rate was extremely low at 0.7%. However, subgroup analysis revealed that the AE rate was slightly higher in the cold snare as well as 10–19 mm and proximal colon subgroups (1.3% vs. 0.5%, 0.9% vs. 0 and 0.3% vs. 0, respectively). Furthermore, the residual rate was very low at 2.9%. The subgroup analysis showed the residual rate was slightly lower in the cold snare subgroup compared with the cold EMR subgroup (1.3% vs. 3.9%), as well as in the 10–19 mm subgroup compared with the ≥20 mm subgroup (3.1% vs. 4.7%).
Thoguluva Chandrasekar et al. have performed a meta-analysis to evaluate the efficacy and safety of removal of SSPs ≥10 mm, which includes 1137 SSPs (901 cases of hot EMR and 236 cases of cold snare) and the pooled technical success rate is 99.5%, which is similar to our results (99.5% vs. 100%) [
]. However, hot EMR has significantly higher rates of immediate bleeding, delayed bleeding, and residual SSPs than CSP (2% vs. 0.7%, 2.3% vs. 0 and 5% vs. 0.9%, respectively) [
]. Our pooled cohort had a lower overall AE rate (0.7%) and residual rate (2.9%) in the follow-up of 1593 CSP and 1129 SSPs. These results implied that CSP was superior to hot EMR for the removal of SSPs.
Thoguluva Chandrasekar et al. have performed a systematic review and pooled-analysis to explore the efficacy and safety of cold snare endoscopic resection for removing nonpedunculated colorectal polyps ≥10 mm, which contains 552 polyps (304 adenomas and 248 SSPs), and the pooled technical success rate is 99.3%, with a low AE rate of 1.1% as well as a low residual rate of 4.1% [
]. In our analysis, the rates of technical success and AEs were similar to the above-mentioned study, whereas the rate of residual SSPs was 2.9%, which was slightly higher since we focused only on SSPs (2.9% vs. 1%). This might be attributed to the smaller sample size in the above-mentioned study compared with our study (248 SSPs vs. 1129 SSPs). Nevertheless, the rate of residual SSPs in our study was markedly lower compared with adenomas (2.9% vs. 11.1%), especially for all polyps ≥20 mm (4.7% vs. 22.5%) [
]. Contrary to most adenomas, SSPs tend to be less bulky and protruding beyond the normal surrounding mucosa and are also generally loose with little or no submucosal fibrosis [
]. These results indicated that CSP might be significantly feasible and safe for removing SSPs than adenomas. van Hattem et al. have found that cold EMR is similar to hot EMR when removing SSPs ≥20 mm in terms of technical success rate and recurrence rate (100% vs. 99.6% and 4.3% vs. 4.6%, respectively), which is comparable to our results (100% vs. 99.6% vs. 100% and 4.3% vs. 4.6% vs. 2.9%, respectively) [
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
]. Meanwhile, the cold EMR-related AEs were similar between the study by van Hattem et al. and our study (0 vs. 0.5%), which was significantly lower compared with hot EMR (5%) [
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
]. This could be attributed to the use of electrocautery in hot EMR, which generated a deeper resection plane, leading to an increased risk of encountering and transecting thinker blood vessels in submucosal layers and unintended transmural capture [
]. Kimoto et al. in their prospective study, have reported that cold snare is a feasible and safe modality to remove SSPs ≥10 mm with a satisfactory technical success rate (99.8%) and extremely low rates of AEs and residual SSPs (3% and 0.2%, respectively), which is comparable to our results (99.8% vs 99.9%, 3% vs. 1.3% and 0.2% vs. 1.3%, respectively) [
Tuttici et al. have reported that cold EMR has several advantages: (1) delineating the margins of lesions, (2) expending the submucosal layer, and making tissue transection easier, and (3) preventing the intra-procedure bleeding through a direct tamponade effect [
]. In our sub-group analysis, the rates of technical success and AEs were comparable between the cold snare and cold EMR (99.9% vs. 100% and 1.3% vs. 0.5%, respectively), whereas cold snare had a slightly lower residual rate than cold EMR (1.3% vs. 3.9). However, univariate and multivariate meta-regression analysis showed that procedure methods (cold snare vs. cold EMR) were not associated with technical success, AEs, and residual SSPs. Of note, cold snare without submucosal injection, might be less costly and more efficient than cold EMR.
Previous studies have demonstrated that the immediate bleeding rate is 4.6%, and the delayed bleeding rate is between 2.2% and 6.7% for hot EMR for all polyps. In contrast, the rates of immediate bleeding and delayed bleeding are 11.3% and 6.2% for polyps > 20 mm, respectively [
]. In our pooled analysis, the overall AEs rate was 0.7% for all SSPs when using CSP and 0 for SSPs ≥ 20 mm. Moreover, the overall AE rate was comparable when CSP was used to remove SSPs of 10–19 mm and ≥ 20 mm (0.9% vs. 0). Univariate meta-regression analysis showed that the size of SSPs was an independent factor associated with AEs. However, multivariate meta-regression analysis demonstrated that AEs were not related to the size of SSPs and procedures (cold snare vs. cold EMR). Therefore, CSP was feasible and safe for all SSPs.
Bronsgeest et al. have reported that the residual rate is 18.8% for traditional (hot) EMR when removing all colorectal polyps ≥ 20 mm in size [
Efficacy and adverse events of EMR and endoscopic submucosal dissection for the treatment of colon neoplasms: a meta-analysis of studies comparing EMR and endoscopic submucosal dissection.
]. However, our pooled cohort demonstrated that the residual rate was 2.9% for SSPs ≥ 10 mm in size when using CSP, while the rate for residual SSPs of 10–19 mm and ≥ 20 mm was 2.1% and 4.7%, respectively. Pellise et al. have found that several factors are associated with residual SSPs, such as the size of SSPs (P < 0.001), adjunct modality (P = 0.03), and dysplasia (P = 0.031) [
]. Nevertheless, in our study, univariate and multivariate meta-regression analysis showed that the residual rate was not associated with the size of SSPs and techniques. Therefore, we hypothesized that a meticulous CSP was performed with a wide rim of normal mucosa resection at the peripheral margin. After resection, the margins were carefully checked through narrow-band imaging (NBI). Therefore, CSP appeared to be an efficacious technique for removing SSPs ≥ 10 mm in size.
The strength of our meta-analysis was the sample size since 1727 SSPs were removed by CSP, which was significantly more compared with the individual studies, thus providing a more reliable and clinically relevant inference. In addition, we performed multiple sub-group analyses to assess the outcomes in terms of procedure methods (cold snare vs. cold EMR), location (proximal colon vs. distal colon), and SSPs size (10–19 mm vs. ≥ 20 mm). Most of our outcomes had only none-to-mild heterogeneity, indicating that our results were reliable.
Our study has several limitations. First, most of the studies were retrospective and conducted at a single center. Second, the follow-up duration differed from center to center, leading to inaccuracies in the residual SSP rate. Third, studies from different regions might contribute to selection bias, which was an unmanageable issue. Fourth, the data were unavailable to assess the residual rate based on the location of SSPs (proximal colon vs. distal colon). Fifth, we did not calculate the rates of immediate bleeding, delayed bleeding and perforation because of substantially low overall AEs. Sixth, no single standardized technique was used in the studies to remove the rim of normal mucosa and identify the residual SSPs at the polypectomy site. Seventh, only six studies reported data on the size stratification, which may decrease the relevance of the results reported, especially as the quality of included studies is relatively low. Eighth, the SSPs were removed using piecemeal cold snare resection or cold EMR in included studies. Moreover, these studies mainly focused on the AEs and residual lesions and did not report the rate of en-bloc resection and piecemeal resection. Therefore, the data were limited in comparing the en-bloc resection rate and piecemeal resection rate. Ninth, there was a significant difference of publication bias in the rate of residual SSPs. The main reasons may be as follows. 1. The characteristics of the included studies were different as some were prospective studies and others were retrospective studies. 2. The follow-up duration was different between centers, leading to the inconsistent residual SSPs rate.
Collectively, our meta-analysis demonstrated a high technical success rate of 100% with a low AEs rate of 0.7% as well as a low residual rate of 2.9% when using CSP for the removal of SSPs ≥ 10 mm in size. Therefore, CSP was an efficacious and safe technique for removing SSPs ≥ 10 mm in size.
Conflict of interest
None declared.
Acknowledgments
Thanks very much to Prof. Lode Van Overbeke and Prof. Ken Ohata for providing raw data.
Funding
This work was supported by the Natural Science Foundation of Guangdong Province (No. 2018A0303100024), Three Engineering Training Funds in Shenzhen (No. SYLY201718, SYJY201714 and SYLY201801), Technical Research and Development Project of Shenzhen (No. JCYJ20150403101028164, No. JCYC20170307100911479 and No. JCYJ20190807145617113), National Natural Science Foundation of China (No. 81502040) and Shenzhen Health Planning Commission (No. SZXJ2017030).
Small colonic microsatellite unstable adenocarcinomas and high-grade epithelial dysplasias in sessile serrated adenoma polypectomy specimens: a study of eight cases.
Cold snare polypectomy vs. cold forceps polypectomy using double-biopsy technique for removal of diminutive colorectal polyps: a prospective randomized study.
Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods.
The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration.
Efficacy and adverse events of EMR and endoscopic submucosal dissection for the treatment of colon neoplasms: a meta-analysis of studies comparing EMR and endoscopic submucosal dissection.
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