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1 Digestive Endoscopy 2018; 30: doi: /den Review Efficacy and safety of cold versus hot snare polypectomy for resecting small colorectal polyps: Systematic review and meta-analysis Satoshi Shinozaki, 1,2 Yasutoshi Kobayashi, 2 Yoshikazu Hayashi, 2 Hirotsugu Sakamoto, 2 Alan Kawarai Lefor 3 and Hironori Yamamoto 2 1 Shinozaki Medical Clinic, Utsunomiya, 2 Division of Gastroenterology, Departments of Medicine, and 3 Surgery, Jichi Medical University, Shimotsuke, Japan Background and Aim: Safety and effectiveness of cold snare polypectomy (CSP) compared with hot snare polypectomy (HSP) has been reported. The aim of the present study is to carry out a meta-analysis of the efficacy and safety of HSP and CSP. Methods: Randomized controlled trials were reviewed to compare HSP with CSP for resecting small colorectal polyps. Outcomes reviewed include complete resection rate, polyp retrieval, delayed bleeding, perforation and procedure time. Outcomes were documented by pooled risk ratios (RR) with 95% confidence intervals (CI) using the Mantel-Haenszel random effect model. Results: Eight studies were reviewed in this meta-analysis, including 1665 patients with 3195 polyps. Complete resection rate using HSP was similar to CSP (RR: 1.02, 95% CI: , P = 0.31). Polyp retrieval after HSP was similar to CSP (RR: 1.00, 95% CI: , P = 0.60). Delayed bleeding rate after HSP was higher than after CSP, although not significantly (patient basis: RR: 7.53, 95% CI: , P = 0.06; polyp basis: RR: 7.35, 95% CI: , P = 0.06). Perforation was not reported in all eight studies. Total colonoscopy time for HSP was significantly longer than CSP (mean difference 7.13 min, 95% CI: , P < 0.001). Specific polypectomy time for HSP was significantly longer than CSP (mean difference s, 95% CI: , P = 0.005). Conclusion: This meta-analysis shows significantly shorter procedure time using CSP compared with HSP. CSP tends toward less delayed bleeding compared with HSP. We recommend CSP as the standard treatment for resecting small benign colorectal polyps. Key words: colonic polyp, colorectal neoplasm, endoscope, therapeutics, treatment outcome INTRODUCTION RESECTION OF COLORECTAL polyps decreases the prevalence of colorectal cancer and subsequent mortality. 1 Eradication of colorectal polyps, even diminutive ones, is routine practice for colonoscopists. In the 20th century, snare polypectomy with electrocautery, so-called hot snare polypectomy (HSP), became widely used. However, a <1% rate of delayed bleeding is considered inevitable, regardless of the techniques used by the endoscopist because of the delayed cauterization effect that extends ulceration and injures arteries in the submucosal layer. 2,3 In the 21st century, snare polypectomy without electrocautery, so-called cold snare polypectomy (CSP), Corresponding: Satoshi Shinozaki, Shinozaki Medical Clinic, Kiyoharadai, Utsunomiya, Tochigi, , Japan. shinozaki-s@aqua.ocn.ne.jp Received 16 January 2018; accepted 5 April has become widely disseminated from western to eastern countries, because of its safety and shortened procedure time. 3,4 There are several recent reports about the safety and effectiveness of CSP compared with HSP. Although a low incidence of delayed bleeding with CSP has been reported, 2,5 the low complete resection rate has become a recent concern. 6 A low complete resection rate has the potential to increase the rate of local recurrence, which may require lengthy and invasive procedures for adequate treatment. Needless to say, polypectomy throughout the gastrointestinal tract requires an R0 resection, defined as an en bloc resection with negative pathological margins. Regarding safety, a <1% incidence of delayed bleeding after HSP is considered unavoidable. 4 As a result of the low malignant potential of small colorectal polyps, zero adverse events are an important goal. The aim of the present study is to compare the efficacy and safety of HSP with CSP. 592

2 Digestive Endoscopy 2018; 30: Cold vs hot snare polypectomy 593 METHODS THIS SYSTEMATIC REVIEW and meta-analysis was carried out after registration with the International Prospective Register of Systematic Reviews (PROSPERO) and according to protocol (ID: CRD ). We included only randomized controlled trials (RCT) and compared HSP with CSP for resecting small colorectal polyps. Outcome measures include complete resection rate, polyp retrieval, delayed bleeding, perforation and procedure time. Search strategy On 20 February 2018, Medline (PubMed), EMBASE, ISI the Web of Science and Cochrane Library were searched using the key words: ( colon [MeSH Terms] OR colonic polyps [MeSH Terms]) and ( humans [MeSH Terms] AND English [LA] OR Japanese [LA]) and ( adult [MeSH Terms]) and ( endoscopy, gastrointestinal [MeSH Terms]) and ( therapeutics [MeSH Terms]). Meeting abstracts including Digestive Disease Week (USA), United European Gastroenterology Week and Asian Pacific Digestive Week were also searched. Languages were restricted to English and Japanese. Study selection Two authors (S.S. and Y.K.) independently reviewed the titles and abstracts of screened articles. Duplicate publications and studies were excluded. The full text of the selected articles was then reviewed and eligibility independently determined. When disagreement occurred, we discussed with another co-author to reach a consensus. Data extraction and quality assessment The following data were abstracted: first author, year of publication, study period, type of study, country, number of patients, age, gender, method of endoscopic resection, type of snare, number of colorectal polyps, size, submucosal injection, resection area, complete resection rate, polyp retrieval rate, incidence of delayed bleeding and perforation, total colonoscopy time and specific polypectomy time. Unclear or non-assessable pathological margins were not categorized as complete resection. Total colonoscopy time was defined as the interval between colonoscope insertion in the anus and removal from the anus. A second co-author verified the data. When the data were not clear in an article, we requested as much detailed information as possible from the authors of the study by direct contact. Risk of bias We carried out an estimation of risk of bias based on the Cochrane risk of bias criteria. 7 These criteria include random sequence generation, allocation concealment, blinding of participants and personnel, blinding of outcome assessment, incomplete outcome data, selective reporting and other forms of bias. Statistical analysis To assess the effect of an intervention and risk of bias, we used Review Manager 5.3 statistical software (Cochrane, Copenhagen, Denmark). Outcomes were documented by pooled risk ratios (RR) with 95% confidence intervals (CI). We calculated overall RR with the Mantel-Haenszel random effect model because of expected strong diversities among studies. Interstudy heterogeneity among studies was described by the chi-squared test and I 2 statistic. P < 0.05 was considered statistically significant. RESULTS Study selection THE PROCESS FOR selecting papers to review for this meta-analysis is shown in Figure 1. Initial database searches identified 832 studies. Based on the title and abstract, 816 irrelevant studies were excluded. Evaluation of the full text of the remaining studies excluded eight more: observational studies (n = 4), 8 11 comparison with cold forceps (n =3) and comparison with hot forceps (n = 1). 15 The remaining eight studies were included in this meta-analysis. 2,5,16 21 Characteristics of studies The studies reviewed were conducted in China, 20 Greece, 16,21 Japan 2,5,18,19 and the USA. 17 The year of publication ranges from 2011 to 2018, and study periods were from 2008 to One study was a triple-arm study including HSP, CSP and cold forceps polypectomy. 18 Data regarding HSP versus CSP were extracted from this study. The other studies had two arms, including HSP and CSP. The majority of polyps were 5 7 mm in size. Seven studies were evaluated for complete resection rate, eight for polyp retrieval, seven for delayed bleeding, three for total colonoscopy time and two for specific polypectomy time

3 594 S. Shinozaki et al. Digestive Endoscopy 2018; 30: Identification Records identified by database search (n = 832) Records identified by manual search (n = 0) Screening Records screened by title and abstract (n = 832) Records excluded (n = 816) Eligibility Records screened by full text articles for eligibility (n = 16) Records excluded (n = 8) Included Studies included in quantitative synthesis (meta analysis) (n = 8) Figure 1 Flow diagram of studies included in the present meta-analysis. (Table 1). In total, this meta-analysis includes 1665 patients with 3195 polyps. Type of snare Type of snare used in each study is listed in Table 2. One study partially used a dedicated snare for CSP. 21 Each study used a different type of snare, except three studies that used the Captivator II (Boston Scientific, Natick, MA, USA). 18,19,21 Complete resection rate Complete resection rate is the main outcome measure of this meta-analysis. As three out of eight studies did not report a complete resection rate, we contacted the corresponding Table 1 Characteristics of the eight studies included in the present meta-analysis First author [Reference] Patients, n Methods Submucosal injection, n Polyps, n Size of polyp, mm Hyperplastic Resection area Complete polyps resection Ichise [5] 80 HSP None Included Not reported Negative margin CSP None Paspatis [16] 414 HSP None Not reported Extended Not reported CSP None Horiuchi [2] 70 HSP None Included Not reported Negative margin CSP None Gomez [17] 60 HSP None 18 Not reported Included Extended Negative margin CSP None 21 Kawamura [18] 476 HSP Partially Excluded Not reported Negative biopsy CSP None Papastergiou 155 HSP All Included Extended Negative biopsy [21] CSP All Suzuki [19] 52 HSP None Excluded Extended Negative margin CSP None Zhang [20] 358 HSP All Excluded Extended Negative biopsy CSP None Inclusion/Exclusion of hyperplastic polyps in complete resection analysis. Extended resection defined as a polyp resected with a more than 1-mm circumferential margin. Patients allocated to hot and cold snare polypectomy are included. Biopsy specimen obtained from the margin of the polypectomy site. CSP, cold snare polypectomy; HSP, hot snare polypectomy.

4 Digestive Endoscopy 2018; 30: Cold vs hot snare polypectomy 595 Table 2 Snare used for colorectal polypectomy First author [Reference] Snare Size of snare, mm Company Ichise [5] SD-7P-1 or SD-BP-1 23 Olympus, Tokyo, Japan Paspatis [16] Sensation Polypectomy Snare 13 Boston Scientific, Natick, MA, USA Horiuchi [2] Dual-loop wire snare 16 or 33 Medico s Hirata Inc., Osaka, Japan Gomez [17] Captiflex Extra Small Oval Flexible 11 Boston Scientific, Natick, MA, USA Kawamura [18] Captivator II 10 Boston Scientific, Natick, MA, USA Papastergiou [21] Snare Master 10 or 15 Olympus, Tokyo, Japan AcuSnare 10 or 15 Cook Medical, Bloomington, IN, USA Captivator II 10 or 15 Boston Scientific, Natick, MA, USA Exacto Cold Snare 9 US Endoscopy, Mentor, OH, USA Suzuki [19] Captivator II 10 Boston Scientific, Natick, MA, USA Zhang [20] Snare Master 10 Olympus, Tokyo, Japan Used for cold snare polypectomy only. authors and obtained data for the complete resection rate for two of these studies. 2,5 Therefore, we included seven studies in this analysis (Fig. 2a). Three of seven studies included HSP after submucosal injection, and one study 21 did CSP after submucosal injection (Table 1). Three of the seven studies excluded hyperplastic polyps, and the remaining four studies included them (Table 1). The definition of extended resection is a polyp resected with a more than 1-mm circumferential margin. 22 Carrying out of an extended resection was stated in the Methods section in five of eight studies (Table 1), and the remaining three studies do not state whether or not circumferential normal mucosa was resected. Three of seven studies 18,20,21 defined complete resection as a negative biopsy from the edge of the polypectomy site and the remaining four studies defined complete resection as an en bloc resection with negative pathological margins (R0 resection) 2,5,17,19 (Table 1). The HSP group had a similar complete resection rate compared with the CSP group (95% vs 94%, RR: 1.02, 95% CI: , P = 0.31) with strong heterogeneity (I 2 = 61%; Fig. 2a). Polyp retrieval All eight studies reported a polyp retrieval rate. The HSP group had a similar polyp retrieval rate compared with the CSP group (97% vs 97%, RR: 1.00, 95% CI: , P = 0.60) with no heterogeneity (I 2 = 0%; Fig. 2b). Delayed bleeding Seven studies reported a rate of delayed bleeding, but delayed bleeding actually occurred in two of the seven studies. Although the HSP group had a higher delayed bleeding rate than the CSP group, there is no statistically significant difference (patient basis: 0.8% vs 0%, RR: 7.53, 95% CI: , P = 0.06 [Fig. 2c] and polyp basis: 0.4% vs 0%, RR: 7.35, 95% CI: , P = 0.06 [Fig. 2d]) with no heterogeneity (I 2 = 0%). Perforation Perforation was not reported in any of the eight studies. Therefore, no comparison was carried out. Procedure time Procedure time was analyzed for five studies, including three that reported total colonoscopy time and two that reported specific polypectomy time. These studies were analyzed separately. Total colonoscopy time was significantly longer in the HSP group than in the CSP group (mean difference 7.13 min, 95% CI: , P < 0.001) with moderate heterogeneity (I 2 = 41%; Fig. 2e). As only one study reported median specific polypectomy time, 18 we contacted the corresponding author and obtained the mean polypectomy time with standard deviation. One of the two studies defined specific polypectomy time as the interval between snare insertion into the working channel and completion of the polypectomy, 18 and the other defined it as the interval between identification of a polyp and completion of the polypectomy. 20 Specific polypectomy time was significantly longer in the HSP group than in the CSP group (mean difference s, 95% CI: , P = 0.005) with moderate heterogeneity (I 2 = 53%; Fig. 2f). DISCUSSION RESULTS OF THE present meta-analysis show a similar complete resection rate for both HSP and CSP. The

5 596 S. Shinozaki et al. Digestive Endoscopy 2018; 30:

6 Digestive Endoscopy 2018; 30: Cold vs hot snare polypectomy 597 Figure 2 Forest plots of the meta-analysis of hot snare polypectomy (HSP) vs cold snare polypectomy (CSP). (a) Complete resection rate. (b) Polyp retrieval rate. (c) Delayed bleeding rate (per patient basis). (d) Delayed bleeding rate (per polyp basis). (e) Total colonoscopy time (min). (f) Specific polypectomy time (s). CI, confidence interval; IV, inverse variance; M-H, Mantel- Haenszel; SD, standard deviation. Risks of bias: A, Random sequence generation (selection bias); B, Allocation concealment (selection bias); C, Blinding participants and personnel (performance bias); D, Blinding of outcome assessment (detection bias); E, Incomplete outcome data (attrition bias); F, Selective reporting (reporting bias); G, other bias. Symbols for risk of bias: +, low risk;, high risk; blank, unclear risk. polyp retrieval rate is also similar between the two groups. The HSP group had a higher delayed bleeding rate than the CSP group, although it does not reach a statistical significance. The CSP group had a significantly shorter procedure time than the HSP group. Complete resection is important to confirm curability. Even if the pathological diagnosis of a small polyp shows an adenoma, unclear or positive lateral margins shorten the colonoscopic follow-up period which increases patient burden and medical costs. CSP has significant superiority to yield a complete resection compared with cold forceps polypectomy, without increasing procedure time. 23,24 Cold forceps polypectomy is not recommended to resect small colorectal polyps because of the low histological eradication rate. In this meta-analysis, the complete resection rate for the HSP group is similar to the CSP group. This meta-analysis shows strong heterogeneity in the complete resection rate. First, this may be explained by the size of the resection area (mucosal defect). In HSP, the size of the resection area and degree of cauterization vary among endoscopists, which influences the complete resection rate. The resection technique may be more important for CSP than for HSP because the lack of a cautery effect obscures the resection margin at the time of histopathological evaluation. We previously reported the usefulness of extended CSP defined as CSP with a >1-mm circumferential margin resulting in significant improvement of the R0 resection rate without increasing the incidence of delayed bleeding. 22 Of the seven studies reviewed in this metaanalysis, four studies described carrying out an extended CSP, and the remaining studies did not specify the resection technique (Table 1). Second, three of seven studies included HSP done after submucosal injection. Generally, submucosal injection and mucosal elevation facilitate to obtain a wide surrounding margin. However, a recent RCT from China reported that HSP after injection did not improve the complete resection rate compared to HSP without injection. 25 Therefore, the exact influence of submucosal injection on the complete resection rate remains unclear. Nevertheless, the use of submucosal injection before polypectomy may enhance the heterogeneity of this metaanalysis. Third, the definition of complete resection is different among the seven studies included. Three of the seven studies defined complete resection as a negative biopsy from the edge of the polypectomy site and the remaining four studies defined complete resection as an en bloc resection with negative pathological margins (R0 resection). The mixed definition of complete resection may increase the heterogeneity. Fourth, the snares used in the studies differed, as shown in Table 2. A recent Japanese RCT reported that use of a dedicated snare for CSP (Exacto Cold Snare; US Endoscopy, Mentor, Ohio, USA) increased the R0 resection rate compared with the use of a traditional snare (Snare Master; Olympus, Tokyo, Japan). 26 Fifth, the inclusion or exclusion of hyperplastic polyps varied among the studies. These factors may explain the strong heterogeneity observed for complete resection rate. Polyp retrieval after polypectomy is important for histological evaluation and to determine the optimal subsequent colonoscopic follow-up interval as well as the need for any additional treatment. This meta-analysis shows a similar polyp retrieval rate comparing the HSP and CSP groups. Recently, a predict-resect-and-discard policy has been developed, because of the evolution of magnifying endoscopy and image-enhanced endoscopy such as narrow-band imaging or flexible integrated color enhancement that is helpful to distinguish neoplastic lesions from hyperplastic lesions. 27 However, this policy risks overlooking incomplete resection of advanced neoplastic lesions. Even if the malignant potential of small colorectal polyps is low, it should not be ignored. Repici et al. 28 reported that 9% (43/ 492) of 5 mm colorectal polyp contained advanced neoplastic lesions. Polyp retrieval for complete pathological examination is an important consideration for endoscopists. Delayed bleeding after colorectal polypectomy usually requires emergent colonoscopy to establish hemostasis in a poor visual field with a blood-filled lumen. Delayed bleeding may result in emergency hospitalization and/or the need for blood transfusion. An increased likelihood of bleeding during polypectomy using CSP has been reported compared with HSP. 16 In general, bleeding during polypectomy is not important, because bleeding during the procedure is readily controlled by clip application or electrocautery. Delayed bleeding after HSP is considered

7 598 S. Shinozaki et al. Digestive Endoscopy 2018; 30: to be caused by use of the electrocautery, resulting in tissue degradation and necrosis within a few days. Suzuki et al. 19 compared the mucosal defects with HSP and CSP 1 day after polypectomy, and found expansion of the mucosal defect when using HSP and diminution of the defect after CSP. Also, the resected specimen after HSP had more submucosal tissue than CSP. 19 Horiuchi et al. 2 reported that histological evaluation showed more damaged arteries in the submucosa after HSP than after CSP. Therefore, HSP is prone to damage submucosal tissue and arteries as a result of the use of electrocautery and results in an expanded mucosal defect after polypectomy, resulting in delayed bleeding. Unlike a recent large retrospective study with propensity score matched data which reported a significantly lower rate of delayed bleeding after HSP than after CSP, 11 this metaanalysis did not demonstrate a significant difference regarding delayed bleeding between the two study groups. Although CSP is usually considered to result in a lower rate of delayed bleeding, the occurrence of delayed bleeding is relatively rare and the number of patients in randomized studies is often small. Further studies are needed to determine whether CSP results in significantly less delayed bleeding than HSP. In this meta-analysis, three of the included studies reported total colonoscopy time and two studies reported specific polypectomy time. All studies showed significantly shorter procedure times for CSP compared with HSP. CSP can omit some HSP-specific procedures such as preparation of the electrocautery, fitting a disposable split return electrode to the patient and using electrocautery at the polypectomy site. CSP also saves the cost of the electrode. Prolonged colonoscopy leads to abdominal discomfort and pain for patients, and a shorter procedure time can increase the number of procedures carried out in a day. A shorter procedure time is favorable for both patients and medical institutions. As a matter of course, indications for CSP should be limited to small colorectal polyps without findings suspicious for malignancy. Small colorectal polyps with findings suspicious for malignancy should be carefully treated by HSP after submucosal injection because CSP does not always resect the muscularis mucosa. 29 A shallow resection by CSP may result in a positive or non-assessable vertical margin in patients with advanced neoplastic lesions. A recent case report documented that a 5-mm sessile rectal polyp resected by CSP was followed by a local recurrence 3 months after polypectomy and eventually developed advanced cancer at the local recurrence site. 30 Careful endoscopic observation before CSP is important, and the routine use of magnifying endoscopy with color enhancement is recommended to clarify mucosal irregularities. There are some acknowledged limitations to the present study. First, the number of studies included (n =8) is comparatively small. Second, the type of snare, size of polyps, polypectomy method, submucosal injection and skill of the endoscopists and pathologists varied among the included studies. Third, long-term outcomes, such as recurrence rate, were not evaluated. An R0 resection does not always exclude the possibility of local recurrences. Carrying out an R0 resection may be more important in CSP than in HSP, because the delayed burning effect after HSP may eliminate microscopic remnants of a lesion. Pathological examination with a 2-mm margin of a small colorectal polyp cannot completely exclude the presence of a remnant. Therefore, surveillance for local recurrences with a longterm program of follow-up colonoscopy may be more important than an R0 resection. Fourth, there is one study that included patients being treated with anticoagulants which showed a statistically significant difference in the rate of delayed bleeding. 2 In conclusion, this meta-analysis shows a shorter procedure time for CSP compared with HSP. CSP tends to decrease the rate of delayed bleeding compared with HSP. As CSP has become the standard procedure to resect small benign colorectal polyps, improvements to increase the complete resection rate such as extended CSP with a dedicated snare should be considered. To resect small colorectal polyps, CSP is recommended as a reduced-time procedure, as long as advanced neoplasia is excluded by careful endoscopic observation. ACKNOWLEDGMENTS THE AUTHORS ARE grateful for detailed unpublished data provided by Dr Akira Horiuchi (Digestive Disease Center, Showa Inan General Hospital, Komagane, Japan) and by Dr Takuji Kawamura (Department of Gastroenterology, Kyoto Second Red Cross Hospital, Kyoto, Japan). CONFLICTS OF INTEREST AUTHORS DECLARE NO conflicts of interest for this article. REFERENCES 1 Zauber AG, Winawer SJ, O Brien MJ et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N. Engl. J. Med. 2012; 366: Horiuchi A, Nakayama Y, Kajiyama M, Tanaka N, Sano K, Graham DY. Removal of small colorectal polyps in anticoagulated patients: a prospective randomized comparison of cold

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