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A prospective randomized comparative study of cold forceps polypectomy by using narrow-band imaging endoscopy versus cold snare polypectomy in patients with diminutive colorectal polyps
ORIGINAL ARTICLE: Clinical Endoscopy
A prospective randomized comparative study of cold forceps polypectomy by using narrow-band imaging endoscopy versus cold snare polypectomy in patients with diminutive colorectal polyps Soo-kyung Park, MD, PhD,1 Bong Min Ko, MD,2 Jae Pil Han, MD, PhD,2 Su Jin Hong, MD, PhD,2 Moon Sung Lee, MD, PhD2 Seoul, Republic of Korea
Background and Aims: A previous study reported that cold snare polypectomy (CSP) was superior to cold forceps polypectomy (CFP) for the removal of diminutive colorectal polyps (DCPs) (5 mm) when the techniques were assessed for completeness of resection. However, completeness is expected to be greater with CFP when strict investigation of the remnant polyp is performed. The aim of this study was to assess the efficacy of CFP with narrow-band imaging (NBI) evaluation of polypectomy sites for removal of DCPs, compared with CSP. Methods: This was a randomized, controlled, noninferiority trial at a tertiary-care referral hospital. Of the 380 patients screened, 146 patients with 231 DCPs were enrolled. CFP was used to resect DCPs until no remnant polyp was visible by NBI endoscopy. The primary noninferiority endpoint was histologic eradication of polyps, with a noninferiority margin of -10%. Results: A size of >3 mm was seen in 129 polyps (55.8%). The overall rates of histologic eradication were 90.5% in the CFP group and 93.0% in the CSP group (difference, 2.5%; 95% confidence interval [CI], -9.67 to 4.62). However, when confined to the polyps >3 mm, the histologic eradication rate was 86.8% and 93.4% (95% CI, -17.2 to 3.6), respectively. Polyp size, histology, location, and time taken for polypectomy did not differ between the groups. The failure rate of tissue retrieval was higher in the CSP than in the CFP group (7.8% vs 0.0%, respectively; P Z.001). Conclusions: In this study, >90% of all DCPs were completely resected by using CFP with NBI evaluation of polypectomy sites, showing noninferiority compared with CSP. However, in polyps measuring >3 mm, CFP failed to show noninferiority versus CSP. CFP appears to be the proper method for resection of DCPs 1 to 3 mm in size if no remnant polyp is visible by NBI endoscopy, but CFP is likely to be insufficient for larger polyps. (Clinical trial registration number: NCT02201147.) (Gastrointest Endosc 2016;83:527-32.)
Most colorectal polyps found during colonoscopy are diminutive colorectal polyps (DCPs) (5 mm in size).1,2 At that size, 50% to 64% have been reported to be adenomas,3-5 and advanced neoplasms in DCPs are reportedly rare (<1%).3 A “diagnose and leave” strategy for hyperplastic polyps and a “resect and discard” strategy for adenomatous polyps were proposed recently for
the management of DCPs.6,7 These strategies rely on real-time endoscopic diagnosis of DCPs without a histopathologic assessment and have been shown to save costs.8,9 However, they are based on the presumption that all adenomatous DCPs are completely resected, and the complete resection of DCPs is an issue of concern.
Abbreviations: CFP, cold forceps polypectomy; CSP, cold snare polypectomy; DCP, diminutive colorectal polyp; NBI, narrow-band imaging.
Current affiliations: Department of Internal Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul (1), Digestive Disease Center and Research Institute, Department of Internal Medicine, Soonchunhyang University School of Medicine, Bucheon, Republic of Korea (2).
DISCLOSURE: This work was supported, in part, by the SoonChunHyang University Research Fund. All authors disclosed no financial relationships relevant to this publication. See CME section; p. 637. Copyright ª 2016 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 http://dx.doi.org/10.1016/j.gie.2015.08.053
Reprint requests: Bong Min Ko, MD, Digestive Disease Center and Research Institute, Department of Internal Medicine, Soonchunhyang University School of Medicine, 170 Jomaru-ro, Wonmi-gu, Bucheon, Gyenggi-do 420-767, Republic of Korea.
Received May 2, 2015. Accepted August 19, 2015.
If you would like to chat with an author of this article, you may contact Dr Ko at [email protected].
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Study of cold forceps polypectomy by using narrow-band imaging endoscopy
Among the various endoscopic techniques for removing DCPs, including cold biopsy, hot biopsy, cold snaring, and hot snaring, the use of cold polypectomy techniques has increased in practice because of their safety and efficacy.10,11 Cold forceps polypectomy (CFP) is applied commonly for removal of DCPs because it is quick and easy to perform. However, there is little evidence regarding the efficacy of CFP for removing DCPs,12-14 and a recent study reported that cold snare polypectomy (CSP) was superior to CFP regarding histologic polyp eradication.14 The current study was conducted based on the expectation that the complete resection rate would be increased with CFP when detailed investigation of the remnant polyp by image-enhanced endoscopy, such as narrow-band imaging (NBI), was performed. Thus, we compared the adequacy of DCP resection by using CFP with NBI evaluation of polypectomy sites with that of CSP.
METHODS Study design and patients This was a single-center, prospective, randomized, controlled, noninferiority trial at a tertiary-care referral hospital performed from July to November 2014. The inclusion criteria were adult outpatients undergoing colonoscopy for screening, surveillance, or diagnosis. Exclusion criteria were (1) age <19 years, (2) patients who took antiplatelet or anticoagulant therapy during the week before the procedure, (3) known coagulopathy or thrombocytopenia (platelet count of <100,000/mm3 [normal value for platelet: 160000-362000/mm3]), (4) a history of inflammatory bowel disease, or (5) pregnancy. Patients who agreed to participate were enrolled if they were found to have at least one DCP (5 mm in size). Because the study was interested in the complete resection of diminutive adenomas, DCPs in the rectosigmoid area that appeared macroscopically hyperplastic were excluded from the study. The patients were randomly assigned to either the CFP or CSP group by using a computer-generated random sequence. Written informed consent was obtained from all patients. The study was approved by the institutional review board of Soonchunhyang University Hospital, Bucheon, Korea (SCHBC-IRB 2014-04-041) and was registered at www.clinicaltrials.gov (NCT02201147).
Park et al
was estimated by using the open width of a biopsy forceps (oval spoon-shaped mouth forceps; MTW, Düsseldorf, Germany), regardless of the random allocation (CSP vs CFP). The fully opened gap between the two jaws of the forceps was 7 mm, and the polyps were divided into two groups (3 and >3 mm). The CFP using NBI endoscopy was performed as follows (Fig. 1): (1) CFP was performed to remove DCPs until no remnant polyp was visible by NBI endoscopy, and (2) during CFP, the polypectomy ulcer was rinsed with 1:10,000 epinephrine solution if oozing bleeding from the biopsy site occurred. Oval spoonshaped mouth forceps (MTW) were used throughout the study, and the number of bites required for resection was investigated. The CSP technique was performed as follows (Supplemental Fig. 1): (1) Capturing with the snare a rim of normal mucosa, sized from one to a few millimeters, around the polyp after slight deflation, (2) closing the snare for transection of the polyp without tenting, and (3) suctioning of the transected polyp into the trap.15 In this study, a micro-oval snare (SD-210U-10; Olympus) with a 10-mm opening width was used. The polypectomy procedure time was measured from appearance of the snare or forceps from the colonoscope channel to confirmation of polyp retrieval by an endoscopy nurse. After polypectomy, the polypectomy site was rinsed with saline solution or 1:10,000 epinephrine solution. In the base and margin of the polypectomy ulcer, two additional biopsies were performed to evaluate the histologic eradication of the polyps. Polypectomy specimens and polypectomy site biopsy specimens were sent separately to the histopathology department and blindly analyzed by experienced GI pathologists, based on the World Health Organization criteria.16 All patients were returned to the hospital or followed-up by telephone call within 1 month to assess postprocedure adverse events.
Outcome measures The primary study outcome was comparison of the complete histologic polyp resection rate between the two groups. Secondary outcomes were the tissue retrieval rate, polypectomy procedure time, and procedure-related adverse events rate, including bleeding and perforation.
Statistical analysis
High-definition colonoscopies (CF-H260AL colonoscope; Olympus Optical Co, Tokyo, Japan) were used for polypectomy by two experienced colonoscopists (experience with >10,000 colonoscopies). All patients were underwent bowel preparation with 4 L of polyethylene glycol solution. All colonoscopy procedures were performed from 2 to 7 hours after the last ingestion of polyethylene glycol. During colonoscope withdrawal, polyp size and location were documented. Before the polypectomy, polyp size
Previous studies reported that the complete polyp resection rate was 86.0% to 93.2% by using the CSP technique14,17-19 and a 90.7% by using CFP with chromoendoscopy.20 We assumed that CFP with NBI evaluation of the polypectomy site would not be inferior in terms of the rate of complete histologic polyp eradication compared with CSP, with a noninferiority margin of -10%. The estimated sample size was 112 DCPs, with an a value of 0.05 and power of 80%. Considering a 20% dropout rate, 140 DCPs were required. The c2 test or the Fisher exact test was used to compare categorical variables, and the t test was used for continuous variables. Logistic regression
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Colonoscopic polypectomy protocol
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Study of cold forceps polypectomy by using narrow-band imaging endoscopy
Figure 1. Cold forceps polypectomy protocol. A, Polyp detected with white-light endoscopy. B, Polyp detected with narrow-band imaging (NBI) endoscopy. C, Polyp resected with forceps with NBI. D, E, Remnant polyp suspected at polypectomy site. F, After additional biopsy, the absence of remnant polyp is confirmed by using NBI.
analysis was used to verify significant predictive factors associated with incomplete histologic eradication of DCPs. All data were analyzed by using SPSS software (version 18.0 for Windows; Chicago, Ill).
RESULTS
were removed, and a total of 231 DCPs were available for final assessments after excluding 6 polyps shown to be normal mucosa (Fig. 2). The median age of the patients was 56 (range 32-84) years, and 73.3% (103/146) were men. There was no significant difference in the baseline characteristics of patients between the groups (Table 1).
Baseline characteristics
Polyp characteristics
In total, 380 patients were screened, and 146 patients with DCPs were enrolled. In these patients, 237 DCPs
Table 2 shows the polyp characteristics. The size was >3 mm in 129 polyps (55.8%). DCPs were most often
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Assessed for eligibility (n =380) Excluded (n = 234) Without eligible polyp (n=212) Taking aspirin (n=12) Inflammatory bowel disease (n=10)
CFP group (n =76)
CSP group (n =70)
Eligible polyps (n =118)
Eligible polyps (n =119)
Excluded normal mucosal (n = 2)
Polyps available for assessment (n = 116)
Excluded normal mucosal (n = 4)
Polyps available for assessment (n = 115)
Figure 2. Enrollment flowchart. CFP, cold forceps polypectomy; CSP, cold snare polypectomy.
resected from the descending and sigmoid colon (40.7%). Most polyps evaluated were tubular adenomas (79.6%), and all adenomas displayed low-grade dysplasia. There was no significant difference in the polyp characteristics between the CFP and CSP groups. In the CFP group, the number of bites was 1 in 83 polyps (71.6%), 2 in 31 polyps (26.7%), and 3 in 2 polyps (1.7%).
Primary and secondary outcomes
Risk factors associated with incomplete histologic resection Of the 19 cases of incomplete resection, 11 (57.9%) were in the CFP group and 8 (42.1%) were in the CSP group. The proportion of polyps measuring >3 mm was significantly higher in the incomplete than complete resection subgroup (78.9% vs 21.1%, respectively; P Z .03). There was no difference in polyp location between the incomplete and complete resection subgroups. According to the multivariate analysis, the only significant risk factor for incomplete histologic resection was a polyp size of >3 mm (odds ratio [OR] Z 3.20; 95% CI, 1.02-10.10; P Z.04). Polypectomy type (CFP vs CSP) did not affect the incomplete histologic resection rate (OR Z 0.89; 95% CI, 0.33-2.40).
The overall rate of histologic complete resection was 90.5% in the CFP group and 93.0% in the CSP group (difference 2.5%; 95% confidence interval [CI], -9.67 to 4.62), showing noninferiority (noninferiority margin -10 < -9.67) of CFP versus CSP (Table 3). In the polyps measuring 3 mm, the complete resection rate was 95.8% in the CFP group and 92.6% in the CSP group (95% CI, -6.1 to 12.5), showing noninferiority of CFP compared with CSP. However, in polyps measuring >3 mm, CFP failed to show noninferiority versus CSP (86.8% vs 93.4%, respectively; 95% CI, -17.2 to 3.6). The polypectomy procedure time was 71 seconds in the CFP group and 78 seconds in the CSP group (P Z .15). The failure rates of tissue retrieval were higher in the CSP group than in the CFP group (7.8% vs 0.0%, respectively; P Z .001). The DCPs that were not retrieved were located in the cecum and/or ascending colon (n Z 4) and descending and/or sigmoid colon (n Z 5). There was no immediate or delayed adverse event such as bleeding or perforation in either group.
In this report, we describe a randomized controlled trial comparing CFP by using NBI with CSP for the complete resection of DCPs. Although a recent randomized study reported that CSP was superior to CFP for histologic eradication of DCPs,14 we performed CFP with NBI evaluation of polypectomy sites and showed noninferiority of CFP versus CSP (90.5% vs 93.0%, respectively; 95% CI Z -9.67 to 4.62). In addition, the tissue retrieval rate was higher in the CFP group than in the CSP group. This is the first study that demonstrates that CFP with NBI evaluation of polypectomy sites is not worse than CSP in the complete resection and showed better tissue retrieval.
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DISCUSSION
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Study of cold forceps polypectomy by using narrow-band imaging endoscopy
TABLE 1. Baseline characteristics of patients Characteristic
Overall CFP (n [ 146) (n [ 76)
CSP (n [ 70) P value
Male, no. (%)
106 (73.3)
55 (78.6)
Age, median (range), y
56 (32-84) 54 (36-83) 58 (32-84)
52 (68.4)
Indication, no. (%)
.19 .07 .93
Screening
69 (47.3)
38 (50.0)
31 (44.3)
Surveillance
19 (27.1)
16 (21.1)
15 (21.4)
Abdominal pain
37 (25.3)
18 (23.7)
19 (27.1)
Altered bowel habits
6 (4.1)
3 (3.9)
3 (4.3)
Other
3 (2.1)
1 (1.3)
TABLE 3. Complete resection rate of the cold forceps and cold snare polypectomy techniques Overall
CFP
CSP
95% CI
Overall 212/231 (91.8) 105/116 (90.5) 107/115 (93.0) -9.6 to 4.6 complete resection rate, no. (%) Size, no. (%), mm 3
96/102 (94.1)
46/48 (95.8)
50/54 (92.6) -6.1 to 12.5
>3
116/129 (89.9) 59/68 (86.8)
57/61 (93.4) -17.2 to 3.6
CFP, cold forceps polypectomy; CSP, cold snare polypectomy; CI, confidence interval.
2 (2.9)
CFP, cold forceps polypectomy; CSP, cold snare polypectomy.
CFP is commonly used for removal of DCPs because of its convenience and safety. However, evidence of its efficacy is lacking. Woods et al12 reported that the complete resection rate of CFP was 79%. However, because nonuniform biopsies of residual polypoid material were performed after 3 weeks of treatment, evaluation of the histologic eradication of polyps was limited. More recently, despite the use of biopsy forceps until no remnant polyp was visible, Efthymiou et al13 reported that the complete resection rate of CFP was only 39%. The reason for the discrepancy between our results and those of Efthymiou et al13 probably is the method of assessing the postpolypectomy site. We used NBI to identify residual tissue, thus allowing a more accurate assessment of resection. In addition, more polyps measured >3 mm in the study by Efthymiou et al13 than in the current study (82% vs 55%, respectively). However, the complete resection rate
was notably lower than that in other studies, including the present study. NBI, an equipment-based, image-enhanced endoscopy method, highlights lesions with improved observation of the mucosal epithelium of the microstructure and the capillaries of the lesion.21 Real-time endoscopic diagnosis of colorectal polyp histology has been shown to be highly accurate by using image-enhanced endoscopy.22-25 Similarly, NBI may be helpful in predicting remnant tissue in the margins after polypectomy. One study reported that the prediction of remnant tissue after endoscopic mucosal resection had high overall accuracy with high-magnification chromoscopic colonoscopy by using NBI.26 Another recent study showed that the complete resection rate increased to 90.7% when dye-based image-enhanced endoscopy, chromoendoscopy with indigo carmine, was used to identify remnant tissue after CFP.20 NBI is simpler and safer than chromoendoscopy, and this is the first reported study to investigate the complete resection rate of CFP for DCPs by using NBI. However, one consideration is that blood is dark on NBI and could obscure remnant tissue. In this study, we rinsed with saline solution or 1:10000 epinephrine solution to prevent obscuring remnant tissue by blood. When CFP is performed, epinephrine wash should be considered to ensure complete removal of the polyp. In this report, the failure rate of tissue retrieval was higher in the CSP than CFP group. We transected the polyps without tenting with a 100% tissue retrieval rate in a previous study.15 However, the retrieval rate in the CSP group in the present study (92.2%) was slightly lower than those of recent randomized trials of CSP (93.2%-100.0%) with the same tissue retrieval method.14,15,27 The success rate will increase through careful technique focusing entirely on polyp retrieval. However, forceps biopsy might always be better than CSP for tissue retrieval, showing a 100% retrieval rate. Although we showed noninferiority of CFP versus CSP in terms of the overall complete resection rate, we failed to show noninferiority of CFP for polyps of >3 mm. In addition, a polyp size of >3 mm was the only significant
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TABLE 2. Polyp characteristics Overall CFP CSP (n [ 231) (n [ 116) (n [ 115) P value Size, no. (%), mm
.43
3
102 (44.2)
48 (41.4)
54 (47.0)
>3
129 (55.8)
68 (58.6)
61 (53.0)
Location, no. (%)
.19
Cecum/ascending colon
64 (27.7)
25 (21.6)
39 (33.9)
Transverse colon
53 (22.9)
28 (24.1)
25 (21.7)
Descending/ sigmoid colon
94 (40.7)
51 (44.0)
43 (37.4)
Rectum
20 (8.7)
12 (10.3)
8 (7.0)
Histology, no. (%)*
.99
Adenoma
172 (79.6)
92 (79.3)
80 (80.0)
Hyperplastic polyp
44 (20.4)
24 (20.7)
20 (20.0)
CFP, cold forceps polypectomy; CSP, cold snare polypectomy. *Indicates total of 216 polyps that were retrieved successfully and evaluated pathologically.
Study of cold forceps polypectomy by using narrow-band imaging endoscopy
risk factor for incomplete histologic resection. These results suggest that CSP should be considered in advance for polyps of >3 mm and, if using CFP, a more strict investigation of the polypectomy site is required to ensure complete resection. This study had several limitations. First, only experienced endoscopists performed the polypectomies. Because polypectomy of DCPs, especially when CFP is used, is frequently performed by inexperienced endoscopists. Further trials in various clinical settings are needed. Second, the exact endoscopic findings of remnant polyps were not investigated further. However, it is difficult to describe the endoscopic findings of remnant tissue without a magnifying colonoscope, and we did not use magnification because this requires more time and is not appropriate in regular clinical practice for the removal of DCPs. In a further study, we plan to investigate the endoscopic findings of remnant tissue by CFP of DCPs without magnification. In conclusion, >90% of all DCPs were completely resected by using CFP with NBI evaluation of polypectomy sites, showing noninferiority compared with CSP. However, in polyps measuring >3 mm, CFP failed to show noninferiority versus CSP. CFP appears to be adequate for the resection of DCPs 1 to 3 mm in size if no residual tissue is visible by NBI endoscopy but is likely insufficient for larger polyps.
REFERENCES 1. Church JM. Clinical significance of small colorectal polyps. Dis Colon Rectum 2004;47:481-5. 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. Tsai FC, Strum WB. Prevalence of advanced adenomas in small and diminutive colon polyps using direct measurement of size. Dig Dis Sci 2011;56:2384-8. 4. Kapsoritakis AN, Potamianos SP, Koukourakis MI, et al. Diminutive polyps of large bowel should be an early target for endoscopic treatment. Dig Liver Dis 2002;34:137-40. 5. Rex DK, Overhiser AJ, Chen SC, et al. Estimation of impact of American College of Radiology recommendations on CT colonography reporting for resection of high-risk adenoma findings. Am J Gastroenterol 2009;104:149-53. 6. Abu Dayyeh BK, Thosani N, Konda V, et al. ASGE Technology Committee systematic review and meta-analysis assessing the ASGE PIVI thresholds for adopting real-time endoscopic assessment of the histology of diminutive colorectal polyps. Gastrointest Endosc 2015;81: 502.e1-16. 7. Kaltenbach T, Rastogi A, Rouse RV, et al. Real-time optical diagnosis for diminutive colorectal polyps using narrow-band imaging: the VALID randomised clinical trial. Gut 2015;64:1569-77.
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Park et al 8. Hassan C, Pickhardt PJ, Rex DK. A resect and discard strategy would improve cost-effectiveness of colorectal cancer screening. Clin Gastroenterol Hepatol 2010;8:865-9; 9.e1-3. 9. Kessler WR, Imperiale TF, Klein RW, et al. A quantitative assessment of the risks and cost savings of forgoing histologic examination of diminutive polyps. Endoscopy 2011;43:683-91. 10. 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. 11. Uraoka T, Ramberan H, Matsuda T, et al. Cold polypectomy techniques for diminutive polyps in the colorectum. Dig Endosc 2014;26(suppl 2): 98-103. 12. Woods A, Sanowski RA, Wadas DD, et al. Eradication of diminutive polyps: a prospective evaluation of bipolar coagulation versus conventional biopsy removal. Gastrointest Endosc 1989;35:536-40. 13. Efthymiou M, Taylor AC, Desmond PV, et al. Biopsy forceps is inadequate for the resection of diminutive polyps. Endoscopy 2011;43:312-6. 14. 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. 15. Deenadayalu VP, Rex DK. Colon polyp retrieval after cold snaring. Gastrointest Endosc 2005;62:253-6. 16. Bosman FT, Carneiro F. WHO classification of tumours of the digestive system. Berlin: Springer-Verlag; 2010. 17. Ellis K, Schiele M, Marquis S, et al. Efficacy of hot biopsy forceps. Cold micro-snare and micro-snare with cautery techniques in the removal of diminutive colonic polyps [abstract]. Gastrointest Endosc 1997;45:AB107. 18. Humphris Jeremy L, Tippett Jill, et al. Cold snare polypectomy for diminutive polyps: an assessment of the risk of incomplete removal of small adenomas [abstract]. Gastrointest Endosc 2009;69:AB207. 19. Gonzalez I, Riley DE, Ho SB, et al. Quality colonoscopy: midterm results of a qualitative comparison of cold snare versus cold biopsy forceps for the resection of colonic polyps [abstract]. Gastrointest Endosc 2010;71: AB244. 20. Jung YS, Park JH, Kim HJ, et al. Complete biopsy resection of diminutive polyps. Endoscopy 2013;45:1024-9. 21. Koo JS. Equipment-based image-enhanced endoscopy for differentiating colorectal polyps. Clin Endosc 2014;47:330-3. 22. 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. 23. Rex DK, Kahi C, O'Brien M, et al. The American Society for Gastrointestinal Endoscopy PIVI (Preservation and Incorporation of Valuable Endoscopic Innovations) on real-time endoscopic assessment of the histology of diminutive colorectal polyps. Gastrointest Endosc 2011;73:419-22. 24. McGill SK, Evangelou E, Ioannidis JP, et al. Narrow band imaging to differentiate neoplastic and non-neoplastic colorectal polyps in real time: a meta-analysis of diagnostic operating characteristics. Gut 2013;62:1704-13. 25. Kwon SC, Choi SW, Choi SH, et al. The effect of indigocarmine on improvement of the polyp detection rate during colonoscopic examination with hood cap. Intest Res 2014;12:60-5. 26. Hurlstone DP, Cross SS, Brown S, et al. A prospective evaluation of high-magnification chromoscopic colonoscopy in predicting completeness of EMR. Gastrointest Endosc 2004;59:642-50. 27. Komeda Y, Suzuki N, Sarah M, et al. Factors associated with failed polyp retrieval at screening colonoscopy. Gastrointest Endosc 2013;77:395-400.
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Study of cold forceps polypectomy by using narrow-band imaging endoscopy
Supplemental Figure 1. Cold snare polypectomy protocol. A, Polyp detected. B, Capture of polyp with from one to a few millimeters of surrounding normal mucosa around the polyp. C, Mechanical transection of the polyp without tenting. D, Subsequent suctioning of transected polyp into the trap.
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Volume 83, No. 3 : 2016 GASTROINTESTINAL ENDOSCOPY 532.e1
A prospective randomized comparative study of cold forceps polypectomy by using narrow-band imaging endoscopy versus cold snare polypectomy in patients with diminutive colorectal polyps Soo-kyung Park, MD, PhD,1 Bong Min Ko, MD,2 Jae Pil Han, MD, PhD,2 Su Jin Hong, MD, PhD,2 Moon Sung Lee, MD, PhD2 Seoul, Republic of Korea
Background and Aims: A previous study reported that cold snare polypectomy (CSP) was superior to cold forceps polypectomy (CFP) for the removal of diminutive colorectal polyps (DCPs) (5 mm) when the techniques were assessed for completeness of resection. However, completeness is expected to be greater with CFP when strict investigation of the remnant polyp is performed. The aim of this study was to assess the efficacy of CFP with narrow-band imaging (NBI) evaluation of polypectomy sites for removal of DCPs, compared with CSP. Methods: This was a randomized, controlled, noninferiority trial at a tertiary-care referral hospital. Of the 380 patients screened, 146 patients with 231 DCPs were enrolled. CFP was used to resect DCPs until no remnant polyp was visible by NBI endoscopy. The primary noninferiority endpoint was histologic eradication of polyps, with a noninferiority margin of -10%. Results: A size of >3 mm was seen in 129 polyps (55.8%). The overall rates of histologic eradication were 90.5% in the CFP group and 93.0% in the CSP group (difference, 2.5%; 95% confidence interval [CI], -9.67 to 4.62). However, when confined to the polyps >3 mm, the histologic eradication rate was 86.8% and 93.4% (95% CI, -17.2 to 3.6), respectively. Polyp size, histology, location, and time taken for polypectomy did not differ between the groups. The failure rate of tissue retrieval was higher in the CSP than in the CFP group (7.8% vs 0.0%, respectively; P Z.001). Conclusions: In this study, >90% of all DCPs were completely resected by using CFP with NBI evaluation of polypectomy sites, showing noninferiority compared with CSP. However, in polyps measuring >3 mm, CFP failed to show noninferiority versus CSP. CFP appears to be the proper method for resection of DCPs 1 to 3 mm in size if no remnant polyp is visible by NBI endoscopy, but CFP is likely to be insufficient for larger polyps. (Clinical trial registration number: NCT02201147.) (Gastrointest Endosc 2016;83:527-32.)
Most colorectal polyps found during colonoscopy are diminutive colorectal polyps (DCPs) (5 mm in size).1,2 At that size, 50% to 64% have been reported to be adenomas,3-5 and advanced neoplasms in DCPs are reportedly rare (<1%).3 A “diagnose and leave” strategy for hyperplastic polyps and a “resect and discard” strategy for adenomatous polyps were proposed recently for
the management of DCPs.6,7 These strategies rely on real-time endoscopic diagnosis of DCPs without a histopathologic assessment and have been shown to save costs.8,9 However, they are based on the presumption that all adenomatous DCPs are completely resected, and the complete resection of DCPs is an issue of concern.
Abbreviations: CFP, cold forceps polypectomy; CSP, cold snare polypectomy; DCP, diminutive colorectal polyp; NBI, narrow-band imaging.
Current affiliations: Department of Internal Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul (1), Digestive Disease Center and Research Institute, Department of Internal Medicine, Soonchunhyang University School of Medicine, Bucheon, Republic of Korea (2).
DISCLOSURE: This work was supported, in part, by the SoonChunHyang University Research Fund. All authors disclosed no financial relationships relevant to this publication. See CME section; p. 637. Copyright ª 2016 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 http://dx.doi.org/10.1016/j.gie.2015.08.053
Reprint requests: Bong Min Ko, MD, Digestive Disease Center and Research Institute, Department of Internal Medicine, Soonchunhyang University School of Medicine, 170 Jomaru-ro, Wonmi-gu, Bucheon, Gyenggi-do 420-767, Republic of Korea.
Received May 2, 2015. Accepted August 19, 2015.
If you would like to chat with an author of this article, you may contact Dr Ko at [email protected].
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Volume 83, No. 3 : 2016 GASTROINTESTINAL ENDOSCOPY 527
Study of cold forceps polypectomy by using narrow-band imaging endoscopy
Among the various endoscopic techniques for removing DCPs, including cold biopsy, hot biopsy, cold snaring, and hot snaring, the use of cold polypectomy techniques has increased in practice because of their safety and efficacy.10,11 Cold forceps polypectomy (CFP) is applied commonly for removal of DCPs because it is quick and easy to perform. However, there is little evidence regarding the efficacy of CFP for removing DCPs,12-14 and a recent study reported that cold snare polypectomy (CSP) was superior to CFP regarding histologic polyp eradication.14 The current study was conducted based on the expectation that the complete resection rate would be increased with CFP when detailed investigation of the remnant polyp by image-enhanced endoscopy, such as narrow-band imaging (NBI), was performed. Thus, we compared the adequacy of DCP resection by using CFP with NBI evaluation of polypectomy sites with that of CSP.
METHODS Study design and patients This was a single-center, prospective, randomized, controlled, noninferiority trial at a tertiary-care referral hospital performed from July to November 2014. The inclusion criteria were adult outpatients undergoing colonoscopy for screening, surveillance, or diagnosis. Exclusion criteria were (1) age <19 years, (2) patients who took antiplatelet or anticoagulant therapy during the week before the procedure, (3) known coagulopathy or thrombocytopenia (platelet count of <100,000/mm3 [normal value for platelet: 160000-362000/mm3]), (4) a history of inflammatory bowel disease, or (5) pregnancy. Patients who agreed to participate were enrolled if they were found to have at least one DCP (5 mm in size). Because the study was interested in the complete resection of diminutive adenomas, DCPs in the rectosigmoid area that appeared macroscopically hyperplastic were excluded from the study. The patients were randomly assigned to either the CFP or CSP group by using a computer-generated random sequence. Written informed consent was obtained from all patients. The study was approved by the institutional review board of Soonchunhyang University Hospital, Bucheon, Korea (SCHBC-IRB 2014-04-041) and was registered at www.clinicaltrials.gov (NCT02201147).
Park et al
was estimated by using the open width of a biopsy forceps (oval spoon-shaped mouth forceps; MTW, Düsseldorf, Germany), regardless of the random allocation (CSP vs CFP). The fully opened gap between the two jaws of the forceps was 7 mm, and the polyps were divided into two groups (3 and >3 mm). The CFP using NBI endoscopy was performed as follows (Fig. 1): (1) CFP was performed to remove DCPs until no remnant polyp was visible by NBI endoscopy, and (2) during CFP, the polypectomy ulcer was rinsed with 1:10,000 epinephrine solution if oozing bleeding from the biopsy site occurred. Oval spoonshaped mouth forceps (MTW) were used throughout the study, and the number of bites required for resection was investigated. The CSP technique was performed as follows (Supplemental Fig. 1): (1) Capturing with the snare a rim of normal mucosa, sized from one to a few millimeters, around the polyp after slight deflation, (2) closing the snare for transection of the polyp without tenting, and (3) suctioning of the transected polyp into the trap.15 In this study, a micro-oval snare (SD-210U-10; Olympus) with a 10-mm opening width was used. The polypectomy procedure time was measured from appearance of the snare or forceps from the colonoscope channel to confirmation of polyp retrieval by an endoscopy nurse. After polypectomy, the polypectomy site was rinsed with saline solution or 1:10,000 epinephrine solution. In the base and margin of the polypectomy ulcer, two additional biopsies were performed to evaluate the histologic eradication of the polyps. Polypectomy specimens and polypectomy site biopsy specimens were sent separately to the histopathology department and blindly analyzed by experienced GI pathologists, based on the World Health Organization criteria.16 All patients were returned to the hospital or followed-up by telephone call within 1 month to assess postprocedure adverse events.
Outcome measures The primary study outcome was comparison of the complete histologic polyp resection rate between the two groups. Secondary outcomes were the tissue retrieval rate, polypectomy procedure time, and procedure-related adverse events rate, including bleeding and perforation.
Statistical analysis
High-definition colonoscopies (CF-H260AL colonoscope; Olympus Optical Co, Tokyo, Japan) were used for polypectomy by two experienced colonoscopists (experience with >10,000 colonoscopies). All patients were underwent bowel preparation with 4 L of polyethylene glycol solution. All colonoscopy procedures were performed from 2 to 7 hours after the last ingestion of polyethylene glycol. During colonoscope withdrawal, polyp size and location were documented. Before the polypectomy, polyp size
Previous studies reported that the complete polyp resection rate was 86.0% to 93.2% by using the CSP technique14,17-19 and a 90.7% by using CFP with chromoendoscopy.20 We assumed that CFP with NBI evaluation of the polypectomy site would not be inferior in terms of the rate of complete histologic polyp eradication compared with CSP, with a noninferiority margin of -10%. The estimated sample size was 112 DCPs, with an a value of 0.05 and power of 80%. Considering a 20% dropout rate, 140 DCPs were required. The c2 test or the Fisher exact test was used to compare categorical variables, and the t test was used for continuous variables. Logistic regression
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Colonoscopic polypectomy protocol
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Study of cold forceps polypectomy by using narrow-band imaging endoscopy
Figure 1. Cold forceps polypectomy protocol. A, Polyp detected with white-light endoscopy. B, Polyp detected with narrow-band imaging (NBI) endoscopy. C, Polyp resected with forceps with NBI. D, E, Remnant polyp suspected at polypectomy site. F, After additional biopsy, the absence of remnant polyp is confirmed by using NBI.
analysis was used to verify significant predictive factors associated with incomplete histologic eradication of DCPs. All data were analyzed by using SPSS software (version 18.0 for Windows; Chicago, Ill).
RESULTS
were removed, and a total of 231 DCPs were available for final assessments after excluding 6 polyps shown to be normal mucosa (Fig. 2). The median age of the patients was 56 (range 32-84) years, and 73.3% (103/146) were men. There was no significant difference in the baseline characteristics of patients between the groups (Table 1).
Baseline characteristics
Polyp characteristics
In total, 380 patients were screened, and 146 patients with DCPs were enrolled. In these patients, 237 DCPs
Table 2 shows the polyp characteristics. The size was >3 mm in 129 polyps (55.8%). DCPs were most often
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Study of cold forceps polypectomy by using narrow-band imaging endoscopy
Park et al
Assessed for eligibility (n =380) Excluded (n = 234) Without eligible polyp (n=212) Taking aspirin (n=12) Inflammatory bowel disease (n=10)
CFP group (n =76)
CSP group (n =70)
Eligible polyps (n =118)
Eligible polyps (n =119)
Excluded normal mucosal (n = 2)
Polyps available for assessment (n = 116)
Excluded normal mucosal (n = 4)
Polyps available for assessment (n = 115)
Figure 2. Enrollment flowchart. CFP, cold forceps polypectomy; CSP, cold snare polypectomy.
resected from the descending and sigmoid colon (40.7%). Most polyps evaluated were tubular adenomas (79.6%), and all adenomas displayed low-grade dysplasia. There was no significant difference in the polyp characteristics between the CFP and CSP groups. In the CFP group, the number of bites was 1 in 83 polyps (71.6%), 2 in 31 polyps (26.7%), and 3 in 2 polyps (1.7%).
Primary and secondary outcomes
Risk factors associated with incomplete histologic resection Of the 19 cases of incomplete resection, 11 (57.9%) were in the CFP group and 8 (42.1%) were in the CSP group. The proportion of polyps measuring >3 mm was significantly higher in the incomplete than complete resection subgroup (78.9% vs 21.1%, respectively; P Z .03). There was no difference in polyp location between the incomplete and complete resection subgroups. According to the multivariate analysis, the only significant risk factor for incomplete histologic resection was a polyp size of >3 mm (odds ratio [OR] Z 3.20; 95% CI, 1.02-10.10; P Z.04). Polypectomy type (CFP vs CSP) did not affect the incomplete histologic resection rate (OR Z 0.89; 95% CI, 0.33-2.40).
The overall rate of histologic complete resection was 90.5% in the CFP group and 93.0% in the CSP group (difference 2.5%; 95% confidence interval [CI], -9.67 to 4.62), showing noninferiority (noninferiority margin -10 < -9.67) of CFP versus CSP (Table 3). In the polyps measuring 3 mm, the complete resection rate was 95.8% in the CFP group and 92.6% in the CSP group (95% CI, -6.1 to 12.5), showing noninferiority of CFP compared with CSP. However, in polyps measuring >3 mm, CFP failed to show noninferiority versus CSP (86.8% vs 93.4%, respectively; 95% CI, -17.2 to 3.6). The polypectomy procedure time was 71 seconds in the CFP group and 78 seconds in the CSP group (P Z .15). The failure rates of tissue retrieval were higher in the CSP group than in the CFP group (7.8% vs 0.0%, respectively; P Z .001). The DCPs that were not retrieved were located in the cecum and/or ascending colon (n Z 4) and descending and/or sigmoid colon (n Z 5). There was no immediate or delayed adverse event such as bleeding or perforation in either group.
In this report, we describe a randomized controlled trial comparing CFP by using NBI with CSP for the complete resection of DCPs. Although a recent randomized study reported that CSP was superior to CFP for histologic eradication of DCPs,14 we performed CFP with NBI evaluation of polypectomy sites and showed noninferiority of CFP versus CSP (90.5% vs 93.0%, respectively; 95% CI Z -9.67 to 4.62). In addition, the tissue retrieval rate was higher in the CFP group than in the CSP group. This is the first study that demonstrates that CFP with NBI evaluation of polypectomy sites is not worse than CSP in the complete resection and showed better tissue retrieval.
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DISCUSSION
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Study of cold forceps polypectomy by using narrow-band imaging endoscopy
TABLE 1. Baseline characteristics of patients Characteristic
Overall CFP (n [ 146) (n [ 76)
CSP (n [ 70) P value
Male, no. (%)
106 (73.3)
55 (78.6)
Age, median (range), y
56 (32-84) 54 (36-83) 58 (32-84)
52 (68.4)
Indication, no. (%)
.19 .07 .93
Screening
69 (47.3)
38 (50.0)
31 (44.3)
Surveillance
19 (27.1)
16 (21.1)
15 (21.4)
Abdominal pain
37 (25.3)
18 (23.7)
19 (27.1)
Altered bowel habits
6 (4.1)
3 (3.9)
3 (4.3)
Other
3 (2.1)
1 (1.3)
TABLE 3. Complete resection rate of the cold forceps and cold snare polypectomy techniques Overall
CFP
CSP
95% CI
Overall 212/231 (91.8) 105/116 (90.5) 107/115 (93.0) -9.6 to 4.6 complete resection rate, no. (%) Size, no. (%), mm 3
96/102 (94.1)
46/48 (95.8)
50/54 (92.6) -6.1 to 12.5
>3
116/129 (89.9) 59/68 (86.8)
57/61 (93.4) -17.2 to 3.6
CFP, cold forceps polypectomy; CSP, cold snare polypectomy; CI, confidence interval.
2 (2.9)
CFP, cold forceps polypectomy; CSP, cold snare polypectomy.
CFP is commonly used for removal of DCPs because of its convenience and safety. However, evidence of its efficacy is lacking. Woods et al12 reported that the complete resection rate of CFP was 79%. However, because nonuniform biopsies of residual polypoid material were performed after 3 weeks of treatment, evaluation of the histologic eradication of polyps was limited. More recently, despite the use of biopsy forceps until no remnant polyp was visible, Efthymiou et al13 reported that the complete resection rate of CFP was only 39%. The reason for the discrepancy between our results and those of Efthymiou et al13 probably is the method of assessing the postpolypectomy site. We used NBI to identify residual tissue, thus allowing a more accurate assessment of resection. In addition, more polyps measured >3 mm in the study by Efthymiou et al13 than in the current study (82% vs 55%, respectively). However, the complete resection rate
was notably lower than that in other studies, including the present study. NBI, an equipment-based, image-enhanced endoscopy method, highlights lesions with improved observation of the mucosal epithelium of the microstructure and the capillaries of the lesion.21 Real-time endoscopic diagnosis of colorectal polyp histology has been shown to be highly accurate by using image-enhanced endoscopy.22-25 Similarly, NBI may be helpful in predicting remnant tissue in the margins after polypectomy. One study reported that the prediction of remnant tissue after endoscopic mucosal resection had high overall accuracy with high-magnification chromoscopic colonoscopy by using NBI.26 Another recent study showed that the complete resection rate increased to 90.7% when dye-based image-enhanced endoscopy, chromoendoscopy with indigo carmine, was used to identify remnant tissue after CFP.20 NBI is simpler and safer than chromoendoscopy, and this is the first reported study to investigate the complete resection rate of CFP for DCPs by using NBI. However, one consideration is that blood is dark on NBI and could obscure remnant tissue. In this study, we rinsed with saline solution or 1:10000 epinephrine solution to prevent obscuring remnant tissue by blood. When CFP is performed, epinephrine wash should be considered to ensure complete removal of the polyp. In this report, the failure rate of tissue retrieval was higher in the CSP than CFP group. We transected the polyps without tenting with a 100% tissue retrieval rate in a previous study.15 However, the retrieval rate in the CSP group in the present study (92.2%) was slightly lower than those of recent randomized trials of CSP (93.2%-100.0%) with the same tissue retrieval method.14,15,27 The success rate will increase through careful technique focusing entirely on polyp retrieval. However, forceps biopsy might always be better than CSP for tissue retrieval, showing a 100% retrieval rate. Although we showed noninferiority of CFP versus CSP in terms of the overall complete resection rate, we failed to show noninferiority of CFP for polyps of >3 mm. In addition, a polyp size of >3 mm was the only significant
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Volume 83, No. 3 : 2016 GASTROINTESTINAL ENDOSCOPY 531
TABLE 2. Polyp characteristics Overall CFP CSP (n [ 231) (n [ 116) (n [ 115) P value Size, no. (%), mm
.43
3
102 (44.2)
48 (41.4)
54 (47.0)
>3
129 (55.8)
68 (58.6)
61 (53.0)
Location, no. (%)
.19
Cecum/ascending colon
64 (27.7)
25 (21.6)
39 (33.9)
Transverse colon
53 (22.9)
28 (24.1)
25 (21.7)
Descending/ sigmoid colon
94 (40.7)
51 (44.0)
43 (37.4)
Rectum
20 (8.7)
12 (10.3)
8 (7.0)
Histology, no. (%)*
.99
Adenoma
172 (79.6)
92 (79.3)
80 (80.0)
Hyperplastic polyp
44 (20.4)
24 (20.7)
20 (20.0)
CFP, cold forceps polypectomy; CSP, cold snare polypectomy. *Indicates total of 216 polyps that were retrieved successfully and evaluated pathologically.
Study of cold forceps polypectomy by using narrow-band imaging endoscopy
risk factor for incomplete histologic resection. These results suggest that CSP should be considered in advance for polyps of >3 mm and, if using CFP, a more strict investigation of the polypectomy site is required to ensure complete resection. This study had several limitations. First, only experienced endoscopists performed the polypectomies. Because polypectomy of DCPs, especially when CFP is used, is frequently performed by inexperienced endoscopists. Further trials in various clinical settings are needed. Second, the exact endoscopic findings of remnant polyps were not investigated further. However, it is difficult to describe the endoscopic findings of remnant tissue without a magnifying colonoscope, and we did not use magnification because this requires more time and is not appropriate in regular clinical practice for the removal of DCPs. In a further study, we plan to investigate the endoscopic findings of remnant tissue by CFP of DCPs without magnification. In conclusion, >90% of all DCPs were completely resected by using CFP with NBI evaluation of polypectomy sites, showing noninferiority compared with CSP. However, in polyps measuring >3 mm, CFP failed to show noninferiority versus CSP. CFP appears to be adequate for the resection of DCPs 1 to 3 mm in size if no residual tissue is visible by NBI endoscopy but is likely insufficient for larger polyps.
REFERENCES 1. Church JM. Clinical significance of small colorectal polyps. Dis Colon Rectum 2004;47:481-5. 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. Tsai FC, Strum WB. Prevalence of advanced adenomas in small and diminutive colon polyps using direct measurement of size. Dig Dis Sci 2011;56:2384-8. 4. Kapsoritakis AN, Potamianos SP, Koukourakis MI, et al. Diminutive polyps of large bowel should be an early target for endoscopic treatment. Dig Liver Dis 2002;34:137-40. 5. Rex DK, Overhiser AJ, Chen SC, et al. Estimation of impact of American College of Radiology recommendations on CT colonography reporting for resection of high-risk adenoma findings. Am J Gastroenterol 2009;104:149-53. 6. Abu Dayyeh BK, Thosani N, Konda V, et al. ASGE Technology Committee systematic review and meta-analysis assessing the ASGE PIVI thresholds for adopting real-time endoscopic assessment of the histology of diminutive colorectal polyps. Gastrointest Endosc 2015;81: 502.e1-16. 7. Kaltenbach T, Rastogi A, Rouse RV, et al. Real-time optical diagnosis for diminutive colorectal polyps using narrow-band imaging: the VALID randomised clinical trial. Gut 2015;64:1569-77.
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Park et al 8. Hassan C, Pickhardt PJ, Rex DK. A resect and discard strategy would improve cost-effectiveness of colorectal cancer screening. Clin Gastroenterol Hepatol 2010;8:865-9; 9.e1-3. 9. Kessler WR, Imperiale TF, Klein RW, et al. A quantitative assessment of the risks and cost savings of forgoing histologic examination of diminutive polyps. Endoscopy 2011;43:683-91. 10. 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. 11. Uraoka T, Ramberan H, Matsuda T, et al. Cold polypectomy techniques for diminutive polyps in the colorectum. Dig Endosc 2014;26(suppl 2): 98-103. 12. Woods A, Sanowski RA, Wadas DD, et al. Eradication of diminutive polyps: a prospective evaluation of bipolar coagulation versus conventional biopsy removal. Gastrointest Endosc 1989;35:536-40. 13. Efthymiou M, Taylor AC, Desmond PV, et al. Biopsy forceps is inadequate for the resection of diminutive polyps. Endoscopy 2011;43:312-6. 14. 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. 15. Deenadayalu VP, Rex DK. Colon polyp retrieval after cold snaring. Gastrointest Endosc 2005;62:253-6. 16. Bosman FT, Carneiro F. WHO classification of tumours of the digestive system. Berlin: Springer-Verlag; 2010. 17. Ellis K, Schiele M, Marquis S, et al. Efficacy of hot biopsy forceps. Cold micro-snare and micro-snare with cautery techniques in the removal of diminutive colonic polyps [abstract]. Gastrointest Endosc 1997;45:AB107. 18. Humphris Jeremy L, Tippett Jill, et al. Cold snare polypectomy for diminutive polyps: an assessment of the risk of incomplete removal of small adenomas [abstract]. Gastrointest Endosc 2009;69:AB207. 19. Gonzalez I, Riley DE, Ho SB, et al. Quality colonoscopy: midterm results of a qualitative comparison of cold snare versus cold biopsy forceps for the resection of colonic polyps [abstract]. Gastrointest Endosc 2010;71: AB244. 20. Jung YS, Park JH, Kim HJ, et al. Complete biopsy resection of diminutive polyps. Endoscopy 2013;45:1024-9. 21. Koo JS. Equipment-based image-enhanced endoscopy for differentiating colorectal polyps. Clin Endosc 2014;47:330-3. 22. 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. 23. Rex DK, Kahi C, O'Brien M, et al. The American Society for Gastrointestinal Endoscopy PIVI (Preservation and Incorporation of Valuable Endoscopic Innovations) on real-time endoscopic assessment of the histology of diminutive colorectal polyps. Gastrointest Endosc 2011;73:419-22. 24. McGill SK, Evangelou E, Ioannidis JP, et al. Narrow band imaging to differentiate neoplastic and non-neoplastic colorectal polyps in real time: a meta-analysis of diagnostic operating characteristics. Gut 2013;62:1704-13. 25. Kwon SC, Choi SW, Choi SH, et al. The effect of indigocarmine on improvement of the polyp detection rate during colonoscopic examination with hood cap. Intest Res 2014;12:60-5. 26. Hurlstone DP, Cross SS, Brown S, et al. A prospective evaluation of high-magnification chromoscopic colonoscopy in predicting completeness of EMR. Gastrointest Endosc 2004;59:642-50. 27. Komeda Y, Suzuki N, Sarah M, et al. Factors associated with failed polyp retrieval at screening colonoscopy. Gastrointest Endosc 2013;77:395-400.
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Study of cold forceps polypectomy by using narrow-band imaging endoscopy
Supplemental Figure 1. Cold snare polypectomy protocol. A, Polyp detected. B, Capture of polyp with from one to a few millimeters of surrounding normal mucosa around the polyp. C, Mechanical transection of the polyp without tenting. D, Subsequent suctioning of transected polyp into the trap.
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Volume 83, No. 3 : 2016 GASTROINTESTINAL ENDOSCOPY 532.e1