ORIGINAL ARTICLE: Clinical Endoscopy
Cold snare polypectomy versus cold forceps polypectomy for diminutive and small colorectal polyps: a randomized controlled trial Joon Sung Kim, MD,1 Bo-In Lee, MD,2 Hwang Choi, MD,1 Sun-Young Jun, MD,3 Eun Su Park, MD,3 Jae Myung Park, MD,2 In-Seok Lee, MD,2 Byung-Wook Kim, MD,1 Sang Woo Kim, MD,2 Myung-Gyu Choi, MD2 Seoul, Korea
Background: The optimal technique for removal of diminutive or small colorectal polyps is debatable. Objective: To compare the complete resection rates of cold snare polypectomy (CSP) and cold forceps polypectomy (CFP) for the removal of adenomatous polyps %7 mm. Design: Prospective randomized controlled study. Setting: A university hospital. Patients: A total of 139 patients who were found to have R1 colorectal adenomatous polyps %7 mm. Interventions: Polyps were randomized to be treated with either CSP or CFP. After the initial polypectomy, additional EMR was performed at the polypectomy site to assess the presence of residual polyp tissue. Main Outcome Measurements: Absence of residual polyp tissue in the EMR specimen of the polypectomy site was defined as complete resection. Results: Among a total of 145 polyps, 128 (88.3%) were adenomatous polyps. The overall complete resection rate for adenomatous polyps was significantly higher in the CSP group compared with the CFP group (57/59, 96.6% vs 57/69, 82.6%; P Z .011). Although the complete resection rates for adenomatous polyps %4 mm were not different (27/27, 100% vs 31/32, 96.9%; P Z 1.000), the complete resection rates for adenomatous polyps sized 5 to 7 mm was significantly higher in the CSP group compared with the CFP group (30/32, 93.8% vs 26/37, 70.3%; P Z .013). Limitations: Single-center study. Conclusion: CSP is recommended for the complete resection of colorectal adenomatous polyps %7 mm. (Clinical trial registration number: NCT01665898.) (Gastrointest Endosc 2015;81:741-7.)
Abbreviations: CFP, cold forceps polypectomy; CSP, cold snare polypectomy. DISCLOSURE: This research was supported by a program of the Global Research and Development Center through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT, and Future Planning (NRF-2011-0031644). All other authors disclosed no financial relationships relevant to this article. Copyright ª 2015 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 http://dx.doi.org/10.1016/j.gie.2014.11.048 Received September 29, 2014. Accepted November 18, 2014.
University of Korea, Incheon (1), Division of Gastroenterology, Department of Internal Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul (2), Department of Hospital Pathology, Incheon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Incheon, Korea (3). Reprint requests: Bo-In Lee, MD, Division of Gastroenterology, Department of Internal Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, 222 Banpo-daero, Seocho-gu, Seoul 137-701, Korea. If you would like to chat with an author of this article, you may contact Dr Lee at
[email protected].
Current affiliations: Division of Gastroenterology, Department of Internal Medicine, Incheon St. Mary’s Hospital, College of Medicine, The Catholic
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Cold snare versus cold forceps polypectomy
Colonoscopy is one of the primary screening tests for colorectal cancer because polypectomy during colonoscopy allows for the removal of precursor lesions that may progress to cancer. The majority of polyps found during colonoscopy are !1 cm in size, and the majority of these polyps are %5 mm.1 When neoplastic, most of these small (6-9 mm) and diminutive (1-5 mm) polyps have tubular histology with low-grade dysplasia.2 The polypectomy technique for diminutive and small polyps is highly variable among endoscopists.3 Current techniques include snare and forceps with or without electrocautery. A survey of endoscopists found cold forceps polypectomy (CFP) as the technique of choice for polyps measuring %6 mm.3-5 However, the optimal technique for removing diminutive and small polyps should be directed toward complete polyp removal. A goal of complete resection of all neoplastic polyps should be maintained, because 8.8% to 50.0% of interval colorectal cancer may be related to incomplete polypectomy.6-11 In addition, the risk of removal of small and diminutive polyps should be minimized, because these polyps possess relatively low risks for progression to colorectal cancer. Cold snare polypectomy (CSP) has been shown to be safe and effective for the removal of polyps %7 mm in size and is regarded as the ideal procedure for removal of small polyps.12,13 However, there have been no randomized controlled trials demonstrating complete resection rate by CSP or CFP for diminutive and small polyps. There are a paucity of data regarding which polypectomy technique is recommended according to polyp size. Therefore, this study was performed to compare the efficacy and safety of CSP to CFP in the removal of polyps %7 mm in size.
Kim et al
provide informed consent were excluded. Patients were randomly assigned to either the CSP or CFP technique. If a patient had O1 eligible polyp, it was agreed on that a maximum of 2 were permitted to be included in the study.
Procedure
The study was a single-center, prospective, randomized controlled study involving outpatients who underwent a colonoscopy from January 2012 to July 2014. Inclusion criteria included patients aged O40 years who underwent a screening, surveillance, or diagnostic colonoscopy and were subsequently found to have small colorectal polyps measuring %7 mm in size. Exclusion criteria included patients with a bleeding tendency or those who had taken antiplatelet or anticoagulation therapy within 1 week before undergoing the procedure. Patients with inflammatory bowel disease, polyposis syndrome, or an inability to
Bowel preparation consisted of patients drinking a total of 4 L of polyethylene glycol solution before their procedures. Total colonoscopies were prospectively performed by using a high-definition endoscope (CF-H260AL; Olympus Co, Tokyo, Japan) by 3 highly experienced endoscopists (B.I.L., J.S.K., H.C.). All polyps found during colonoscopy were photographed, and their characteristics, including size and anatomic location, were documented. Polyps that were deemed neoplastic (vessels surrounding oval, tubular, or branched pits under observation by high-definition white-light endoscopy and narrow-band imaging endoscopy) were subjected to polypectomy.14 Polyp size was defined by using the opening width of the biopsy forceps. If the size of the polyp was eligible for the study (%7 mm), polypectomy was performed by one of two randomized methods. Afterward, additional EMR was performed at the polypectomy site to evaluate for the presence of residual polyp tissue. After each procedure, the polypectomy site was observed for 30 seconds to confirm the absence of immediate bleeding. CSP was performed by using a disposable oval snare with a diameter of 10 mm (SD-210U-10; Olympus) under gentle suction to reduce colon wall tension. The tip of the endoscope was deflected toward the polyp base to ensnare 1 to 2 mm of normal mucosa surrounding the polyp. CFP was performed by using biopsy forceps with an ellipsoid cup and needle (FB-24U-1; Olympus). Forceps bites were repeatedly taken until the polyp was thought to be removed on endoscopy. The number of forceps bites was not limited. The procedure time taken for each polypectomy was measured from identification of the polyp to completion of polypectomy by photographic documentation. After each procedure, the specimens were retrieved and stored in formalin. For histologic assessment of residual polyp tissues, the polypectomy site, including an additional 1 to 2 mm clear margin, was resected by the snare and Endocut current (VIO300D; Erbe Elektromedizin GmbH, Tubingen, Germany) after submucosal injection of a mixed solution (normal saline solution þ 0.01% epinephrine). The retrieved specimen was fixed on a plate by using pins. After indigo carmine solution was applied, the specimen was studied under a stereomicroscope with 8power magnification to assess the presence of residual tissue by the endoscopist who performed the polypectomy. The presence of residual tissue was documented, and the plate was marked with a pen to indicate the most probable site of residual tissue. Cross-sections of the EMR specimens were collected at 1-mm intervals; accurate tissue section of the marked site was ensured. All tissue samples
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METHODS The study was approved by the institutional review board at the Catholic University of Korea and registered with ClinicalTrials.gov (NCT01665898). Written informed consent for this study was obtained from all patients. The study concept, hypothesis, and design were all created by the investigator.
Study design
Kim et al
Cold snare versus cold forceps polypectomy
Figure 1. Polypectomy and EMR protocol. A, Polyp detected. B, Polyp observed by narrow-band imaging. C, Polyp size was measured by open width of forceps. D, Polypectomy was done by either cold forceps polypectomy or cold snare polypectomy. E, Submucosal saline solution injection. F, EMR of polypectomy site. G, Resected specimen was fixed on a plate and observed by stereoscope for examination of the presence of residual tissues.
were cross-reviewed by 2 experienced pathologists who were blinded to the clinical information. The process is shown in Figure 1. The patients returned 1 week after each polypectomy to be informed of their pathology results and to be assessed for postprocedural adverse events, such as delayed bleeding. Complete resection was defined as the absence of residual polyp tissue in the EMR sections of the polypectomy site.
Sample size calculations We determined a minimum sample size of 62 polyps per study arm to confirm that the CSP technique would increase the complete polyp resection rate by R15% compared with CFP. This was based on complete resection rates of 80% for CFP and 95% for CSP.15,16 We assumed a dropout rate of 20% with an a value of 0.05 and power of 80%.
Study outcomes Statistical analysis
The primary study outcome was to compare the complete polyp resection rate between groups. Secondary outcomes included rate of postpolypectomy adverse events, including bleeding, perforations, and rate of tissue retrieval.
The chi-square test or the Fisher exact test was used to compare categorical variables. P values of ! .050 were considered to be statistically significant. Continuous or discrete variables between groups were compared by using
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Cold snare versus cold forceps polypectomy
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TABLE 1. Baseline characteristics of patients in each group Parameter Age, mean ( SD), y
CSP (n [ 67)
CFP (n [ 71)
Total (n [ 138)
P value
62.4 ( 8.7)
61.7 ( 10.1)
62.0 ( 9.4)
.653
Sex, no. (%)
.646
Male
38 (56.7)
43 (60.6)
81 (58.7)
Female
29 (43.3)
28 (39.4)
57 (41.3)
Indication, no. (%)
.719*
Screening
32 (47.8)
35 (49.3)
67 (48.6)
Surveillance
14 (20.9)
17 (23.9)
31 (22.5)
For polypectomy
12 (17.9)
7 (9.9)
19 (13.8)
Positive FOBT
3 (4.5)
6 (8.5)
9 (6.5)
Anal bleeding
3 (4.5)
2 (2.8)
5 (3.6)
Other
3 (4.5)
4 (5.6)
7 (5.1)
Bowel preparation, no. (%)
.847*
Excellent
14 (20.9)
16 (22.5)
30 (21.7)
Good
36 (53.7)
38 (53.6)
74 (53.6)
Fair
14 (20.9)
16 (22.5)
30 (21.7)
Poor
3 (4.5)
1 (1.4)
4 (2.9)
CSP, Cold snare polypectomy; CFP, cold forceps polypectomy; SD, standard deviation; FOBT, fecal occult blood test. *Fisher exact test.
the 2-sample t test or z test. All analyses were performed by using SPSS for Windows (version 18, SPSS Inc, Chicago, Ill).
P Z .001). Final pathologic diagnosis revealed tubular adenoma with low-grade dysplasia in 84.3% for the CSP group and 92.0% for the CFP group.
RESULTS
Complete resection rate
Patients and polyp characteristics A total of 138 patients were recruited and enrolled in the study; there were no significant differences in the baseline patient characteristics between groups (Table 1). A total of 145 polyps (70 for CSP and 75 for CFP) were removed by one of two methods (Table 2). In the CSP group, 4.3% (3/70) of polyps were not retrieved, whereas none of the polypectomy samples (0%, 0/75) was lost in the CFP group (P Z .110). The mean size of the polyps was 4.4 mm for each group. The mean ( standard deviation [SD]) number of bites for endoscopic polyp eradication in the CFP group was 2.3 ( 1.0). The mean ( SD) number of forceps bites for polyps in the 5- to 7-mm range was greater than that of polyps in the %4-mm range (3.05 1.4 vs 1.61 0.76; P Z .001). The mean ( SD) procedure time for polypectomy was significantly shorter in the CSP group compared with the CFP group (145.5 64.6 seconds vs 197.0 124.3 seconds; P Z .010). Although the procedure time for polyps %4 mm was not significantly different (157.0 71.2 seconds vs 195.2 140.8 seconds; P Z .060), the procedure time for polyps sized 5 to 7 mm was significantly shorter in the CSP group compared with the CFP group (132.7 54.7 seconds vs 198.9 106.7 seconds, 744 GASTROINTESTINAL ENDOSCOPY Volume 81, No. 3 : 2015
A total of 128 adenomatous polyps were available for assessment. Three hyperplastic polyps were excluded as well as 11 polyps, which were found to be a mucosal tag or inflammation according to the final pathology report. Three polyps that could not be retrieved were excluded (Table 3). The overall complete resection of adenomatous polyps was significantly higher in the CSP group compared with the CFP group (57/59, 96.6% vs 57/69, 82.6%; P Z .011). For adenomatous polyps %4 mm, the complete resection rates were not different between methods (27/27, 100% vs 31/32, 96.9%; P Z 1.000). The complete resection rates for adenomatous polyps 5 to 7 mm was significantly higher in the CSP group when compared with the CFP group (30/32, 93.8% vs 26/37, 70.3%, P Z .013) (Table 3). Univariate analysis revealed that size of the adenomatous polyps and resection methods were related to complete resection rates (Table 4); both factors were statistically significant after binary logistic regression analysis (Table 5).
Postpolypectomy adverse events No immediate postpolypectomy bleeding occurred. After additional EMR for histologic assessment of residual polyp tissues, 2 cases of immediate bleeding were www.giejournal.org
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Cold snare versus cold forceps polypectomy
TABLE 2. Characteristics of polyps Parameter
CSP (n [ 70)
CFP (n [ 75)
Total (n [ 145)
P value
–
2.3 ( 1.0)
–
–
4.4 ( 1.4)
4.4 ( 1.5)
4.4 ( 1.4)
.385
%4
37 (52.9)
38 (50.7)
75 (51.7)
5-7
33 (47.1)
37 (49.3)
70 (48.3)
Right side of colon
43 (61.4)
49 (65.3)
92 (63.4)
Left side of colon and rectum
27 (38.6)
26 (34.7)
53 (36.6)
No. of biopsy, mean ( SD) Size, mean ( SD), mm Size, no. (%), mm
.792
Location, no. (%)
.626
Shape, no. (%)
.684
Sessile
59 (84.3)
65 (86.7)
124 (85.5)
Flat
11 (15.7)
10 (13.3)
21 (14.5)
Pathology*, no. (%)
.193*
Tubular adenoma
59 (84.3)
69 (92.0)
128 (88.3)
Hyperplastic polyp
1 (1.4)
2 (2.7)
3 (2.1)
Mucosal tag or inflammation
7 (10.0)
4 (5.3)
11 (7.6)
Tissue retrieval failure
3 (4.3)
0 (0)
3 (2.0)
CSP, Cold snare polypectomy; CFP, cold forceps polypectomy; SD, standard deviation; –, not applicable. *Fisher exact test.
TABLE 3. Complete resection rates of adenomatous polyps CSP (n [ 59)
CFP (n [ 69)
Total (n [ 128)
P value
57/59 (96.6)
57/69 (82.6)
114/128 (89.1)
.011
%4*
27/27 (100)
31/32 (96.9)
58/59 (98.3)
1.000*
5-7
30/32 (93.8)
26/37 (70.3)
56/69 (81.2)
.013
Parameter, no./No. (%) Complete resection rate of adenomatous polyps Size of adenomatous polyps, mm
CSP, Cold snare polypectomy; CFP, cold forceps polypectomy. *Fisher exact test.
observed in the CSP group and 3 cases in the CFP group, which were controlled by application of hemoclips. There were no cases of delayed bleeding in either group.
Our study clearly demonstrates that CSP is more efficient in complete eradication of adenomatous polyps %7 mm in size as compared with CFP. The largest significant difference is present in 5- to 7-mm polyps. CFP is the preferred technique for removal of diminutive polyps among endoscopists, because cold forceps are immediately available in most endoscopy units, and it is relatively easy to retrieve the resected tissue.4,17 This procedure also requires less coordination between the endoscopist and assistant and is related to fewer postpolypectomy adverse events, such as perforation and bleeding.12,18 However, O1 bite is frequently required to remove even a diminu-
tive polyp, and there are concerns that oozing blood after the initial bite can interfere with accurate aiming of the following bites. Indeed, several studies reported an alarming rate of residual polyp tissue after what was considered a complete polyp removal by cold forceps.4,16,19 Most recently, Efthymiou et al19 found CFP to be inadequate for the removal of diminutive polyps, reporting complete resection rates of 39%. However, Jung et al20 recently used similar techniques and reported complete resection rates of 90% for diminutive polyps. This result poses a disparity regarding the rates of residual adenomatous tissues after CFP. In our study, the complete resection rate of CFP for polyps %5 mm was 92% (46/50), which is more comparable to the Jung et al20 results and suggests that CFP may be an option for the removal of diminutive polyps. Higher complete resection rates in our study, compared with those of the Efthymiou et al19 study, may be related to a greater number of bites taken during
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DISCUSSION
Cold snare versus cold forceps polypectomy
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CFP. Although the median number of bites for complete visual polyp eradication was 2 in the Efthymiou et al19 study, the median number of bites was 2.3 in our study. A recent study found the average number of forceps bites for visual eradication (when the polyp was not completely removed with 1 bite) to be 2.55 even for large-capacity forceps.16 Two bites may not have been sufficient for complete resection of polyps in Efthymiou et al19 study. Although the median number of bites also was 2 in the Jung et al20 study, confirming complete visual eradication by using chromoendoscopy may have led to higher complete resection rates. CSP has been established as an effective method for removal of diminutive and small polyps.18 CSP has the advantage over CFP in that capturing from one to a few millimeters of normal mucosa surrounding the polyp is more likely to yield a higher probability of complete removal. The technique also incurs minimal damage to the submucosal arteries and can be performed safely
for patients taking antiplatelet agents or those with therapeutic levels of anticoagulation.21 Despite these advantages, there were concerns that it would be difficult to retrieve tissues by using the CSP technique. It is now known that tissue retrieval after the CSP technique is successful O94% of the time.22 As is the case with CFP, there has been a paucity of evidence regarding the complete resection rates after CSP and regarding the sizes in which CSP can be efficiently performed. Lee et al15 performed a randomized controlled trial and found CSP to be superior to CFP for the removal of diminutive polyps, especially those in the 4- to 5-mm size range. The complete resection rates of CFP were 91.7% for polyps of 1 to 3 mm and 50.0% for polyps of 4 to 5 mm. The corresponding complete resection rates in our study were 100% and 84.6%, respectively. Only 2 bites for CFP were permitted in the Lee et al15 study, and this may have resulted in the lower eradication rates of CFP, especially in the 4 to 5 mm range. The number of bites for eradication of a polyp is rarely limited in real practice. Although the Lee et al15 study found the CSP technique to be effective for polyps %5 mm, our study found the CSP technique to be effective for complete resection of adenomatous polyps %7 mm. Our study also showed that CSP can remove polyps %7 mm in a shorter time than CFP. Multiple bites for CFP require more passages of biopsy forceps through the working channel. Consequently, CFP would require longer time for polyp removal than CSP. However, we cannot conclude that the total procedure time for CSP is shorter than that for CFP because the time for tissue retrieval was not measured in this study. A recent study reported that jumbo biopsy forceps showed a trend toward higher complete eradication rates compared with standard biopsy forceps.16 The results of our study may have been different if we had used jumbo biopsy forceps. There are several methodologic strengths that add to the validity of our findings. This study has a prospective, randomized, controlled design involving a large number of neoplastic polyps. Although our study was a single-center study, to minimize the introduction of bias the study was performed by 3 endoscopists to account for possible variations of technical skills in performing a polypectomy. Another advantage of our study is that we were meticulous in investigating the presence of residual tissues after polypectomy. After each polypectomy technique, an EMR was performed, and the resected specimen was observed with a stereomicroscope to mark the most probable site of residual tissue and ensure the site was included in the tissue section. The authors of the previous study, who performed EMR of the polypectomy sites, examined the specimens at 1-mm intervals.20 We assumed that the possibility of residual tissues !1 mm can be omitted in the tissue sections and thus decided to observe and mark our specimens under stereoscopic examination.
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TABLE 4. Univariate analysis for predictors of complete resection rate for adenomatous polyps
Variable
Incomplete Complete resection resection Total P (n [ 14) (n [ 114) (n [ 128) value
Sex
.803 Male
9
72
81
Female
5
42
47
%4
1
58
59
5-7
13
56
69
Right side of colon
10
72
82
Left side of colon and rectum
4
42
46
Sessile
12
95
107
Flat
2
19
21
CSP
2
57
59
CFP
12
57
69
Size, mm
.004
Location
.251
Shape
.215
Resection method
.002
CSP, Cold snare polypectomy; CFP, cold forceps polypectomy.
TABLE 5. Binary logistic regression analysis for predictors of complete resection rate for adenomatous polyps Characteristic
OR
95% CI
P value
Size, %4 vs 5-7, mm
.06
.008-.467
.007
Method, CSP vs CFP
6.84
2.045-23.135
.002
OR, Odds ratio; CI, confidence interval; CSP, cold snare polypectomy; CFP, cold forceps polypectomy.
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Other studies performed additional biopsies at the polypectomy site to rule out the presence of residual tissue.15,16,19,23 This method may not have been sufficient for the evaluation of the completeness of the polypectomy. Additionally, performing biopsies after initial biopsies leads to confusion and may introduce inevitable bias as to which biopsy should be regarded as the actual polypectomy procedure. Limitations of the study include the fact that we could not evaluate the complete resection rate of each method for sessile serrated adenomas, because only polyps with neoplastic features on white-light and narrow-band imaging endoscopy were analyzed in the study. The majority of sessile serrated adenomas might have been excluded from this study because they can share many features of hyperplastic polyps.24,25 Delayed postpolypectomy bleeding could not be evaluated because additional EMR was performed to evaluate the presence of residual tissues after each polypectomy. The complete resection rates for adenomatous polyps %4 mm were not significantly different between the CSP group and the CFP group in our study. However, it is unclear whether CFP can be recommended as an alternative method for removal of adenomatous polyps %4 mm because the study number was not powered specifically for this outcome. In conclusion, CSP achieved complete resection rates of 96.6% for adenomatous polyps %7 mm, whereas CFP achieved complete resection rates of 82.6%. CSP is recommended for the complete resection of polyps %7 mm, based on the results of this study.
REFERENCES 1. Pohl H, Srivastava A, Bensen SP, et al. Incomplete polyp resection during colonoscopydresults of the complete adenoma resection (CARE) study. Gastroenterology 2013;144:74-80; e1. 2. Gupta N, Bansal A, Rao D, et al. Prevalence of advanced histological features in diminutive and small colon polyps. Gastrointest Endosc 2012;75:1022-30. 3. Carter D, Beer-Gabel M, Zbar A, et al. A survey of colonoscopic polypectomy practice amongst Israeli gastroenterologists. Ann Gastroenterol 2013;26:135-40. 4. Singh N, Harrison M, Rex DK. A survey of colonoscopic polypectomy practices among clinical gastroenterologists. Gastrointest Endosc 2004;60:414-8. 5. Gellad ZF, Voils CI, Lin L, et al. Clinical practice variation in the management of diminutive colorectal polyps: results of a national survey of gastroenterologists. Am J Gastroenterol 2013;108:873-8.
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Cold snare versus cold forceps polypectomy 6. Farrar WD, Sawhney MS, Nelson DB, et al. Colorectal cancers found after a complete colonoscopy. Clin Gastroenterol Hepatol 2006;4: 1259-64. 7. Pabby A, Schoen RE, Weissfeld JL, et al. Analysis of colorectal cancer occurrence during surveillance colonoscopy in the dietary Polyp Prevention Trial. Gastrointest Endosc 2005;61:385-91. 8. Robertson DJ, Greenberg ER, Beach M, et al. Colorectal cancer in patients under close colonoscopic surveillance. Gastroenterology 2005;129:34-41. 9. Huang Y, Gong W, Su B, et al. Risk and cause of interval colorectal cancer after colonoscopic polypectomy. Digestion 2012;86:148-54. 10. Robertson DJ, Lieberman DA, Winawer SJ, et al. Colorectal cancers soon after colonoscopy: a pooled multicohort analysis. Gut 2014;63: 949-56. 11. le Clercq CM, Bouwens MW, Rondagh EJ, et al. Postcolonoscopy colorectal cancers are preventable: a population-based study. Gut 2014;63: 957-63. 12. Tolliver KA, Rex DK. Colonoscopic polypectomy. Gastroenterol Clin North Am 2008;37:229-51; ix. 13. Tappero G, Gaia E, De Giuli P, et al. Cold snare excision of small colorectal polyps. Gastrointest Endosc 1992;38:310-3. 14. Hewett DG, Kaltenbach T, Sano Y, et al. Validation of a simple classification system for endoscopic diagnosis of small colorectal polyps using narrow-band imaging. Gastroenterology 2012;143:599-607; e1. 15. Lee CK, Shim JJ, Jang JY. Cold snare polypectomy vs. Cold forceps polypectomy using double-biopsy technique for removal of diminutive colorectal polyps: a prospective randomized study. Am J Gastroenterol 2013;108:1593-600. 16. Draganov PV, Chang MN, Alkhasawneh A, et al. Randomized, controlled trial of standard, large-capacity versus jumbo biopsy forceps for polypectomy of small, sessile, colorectal polyps. Gastrointest Endosc 2012;75:118-26. 17. Fyock CJ, Draganov PV. Colonoscopic polypectomy and associated techniques. World J Gastroenterol 2010;16:3630-7. 18. Hewett DG, Rex DK. Colonoscopy and diminutive polyps: hot or cold biopsy or snare? Do I send to pathology? Clin Gastroenterol Hepatol 2011;9:102-5. 19. Efthymiou M, Taylor AC, Desmond PV, et al. Biopsy forceps is inadequate for the resection of diminutive polyps. Endoscopy 2011;43: 312-6. 20. Jung YS, Park JH, Kim HJ, et al. Complete biopsy resection of diminutive polyps. Endoscopy 2013;45:1024-9. 21. Horiuchi A, Nakayama Y, Kajiyama M, et al. Removal of small colorectal polyps in anticoagulated patients: a prospective randomized comparison of cold snare and conventional polypectomy. Gastrointest Endosc 2014;79:417-23. 22. Deenadayalu VP, Rex DK. Colon polyp retrieval after cold snaring. Gastrointest Endosc 2005;62:253-6. 23. Liu S, Ho SB, Krinsky ML. Quality of polyp resection during colonoscopy: Are we achieving polyp clearance? Dig Dis Sci 2012;57:1786-91. 24. Kumar S, Fioritto A, Mitani A, et al. Optical biopsy of sessile serrated adenomas: Do these lesions resemble hyperplastic polyps under narrow-band imaging? Gastrointest Endosc 2013;78:902-9. 25. Yamashina T, Takeuchi Y, Uedo N, et al. Diagnostic features of sessile serrated adenoma/polyps on magnifying narrow band imaging: a prospective study of diagnostic accuracy. J Gastroenterol Hepatol. Epub 2014 Aug 4.
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