Abbreviations used in this paper
adjOR
adjusted odds ratio
APC
argon plasma coagulation
CI
confidence interval
CRC
colorectal cancer
EMR
endoscopic mucosal resection
ESD
endoscopic submucosal dissection
GRADE
Grading of Recommendations, Assessment, Development, and Evaluation Ratings of Evidence
LST
laterally spreading tumor
NBI
narrow-band imaging
NICE
Narrow Band Imaging International Colorectal Endoscopic classification
OR
odds ratio
USMSTF
US Multi-Society Taskforce.
Colonoscopy with polypectomy reduces the incidence of and mortality from colorectal cancer (CRC).1,2 3 1,2
The lifetime risk to develop CRC in the United States is approximately 4.3%, with 90% of cases occurring after the age of 50 years.4 5 6 7
Polypectomy techniques have expanded in parallel with advances in endoscopic imaging, technology, and tools. Optimal techniques encompass effectiveness, safety, and efficiency. Colorectal lesion characteristics, including location, size, morphology, and histology, influence the optimal removal method. For example, the applications of cold snare polypectomy for small lesions, which can remove adenomatous tissue en bloc with surrounding normal mucosa, and endoscopic mucosal resection (EMR) for large and flat lesions, which utilizes submucosal injection to lift the lesion before snare resection, have evolved to improve complete and safer resection. The primary aim of polypectomy is the complete and safe removal of the colorectal lesion and the ultimate prevention of CRC. This consensus statement provides recommendations to optimize complete and safe endoscopic removal techniques for colorectal lesions (Table 1 ), based on available literature and experience. The recommendations from the US Multi-Society Task force (USMSTF) on the management of malignant polyps, polyposis syndromes,8 9 Table 2 summarizes abbreviations and definitions of terms utilized in these recommendations.
Table 1.: Statements of Best Practice in This Document
Table 1-A.: Statements of Best Practice in This Document
Table 1-B.: Statements of Best Practice in This Document
Table 2.: Abbreviations, Terms, and Definitions
Table 2-A.: Abbreviations, Terms, and Definitions
Table 2-B.: Abbreviations, Terms, and Definitions
Methods
Process
The USMSTF is composed of 9 gastroenterology specialists who represent the American College of Gastroenterology, the American Gastroenterological Association, and the American Society for Gastrointestinal Endoscopy. We developed the guidance statements by consensus process through e-mail correspondence and multiple joint teleconferences. The final manuscript was reviewed and approval by the governing boards of the 3 respective societies.
Literature Review
We performed a systematic review of the literature based on a defined search by a medical librarian of the Ovid Medline, Embase, and Cochrane databases from 1946 to December 2017, as well as reviews of manual references and scientific meeting abstracts of the American College of Gastroenterology, American Gastroenterology Association, American Society for Gastrointestinal Endoscopy, and United European Gastroenterology Week from 2014–2017. The search was limited to human studies without any language restriction. We framed the search strategy using key words (Appendix 1, https://links.lww.com/AJG/B415 https://links.lww.com/AJG/B416
Grading of Recommendations, Assessment, Development, and Evaluation Ratings of Evidence: Level of Evidence and Strength of Recommendation
The USMSTF group rated the quality of the evidence for each statement as very low quality, low quality, moderate quality, and high quality based on the GRADE (Grading of Recommendations, Assessment, Development, and Evaluation Ratings of Evidence) methodology (Table 3 ).10
Table 3.: Grading of Recommendations Assessment, Development, and Evaluation Ratings of Evidence and Strength of Recommendations
We provide a recommendation as strong or conditional according to modified GRADE criteria.11
Section I: Lesion Assessment
Statement 1: Lesion Assessment and Description
The macroscopic characterization of a lesion provides information to facilitate the lesion’s histologic prediction, and optimal removal strategy.
We recommend the documentation of endoscopic descriptors of the lesion, including location, size in millimeters, and morphology in the colonoscopy procedure report. (Strong recommendation, low-quality evidence)
We suggest the use of the Paris classification to describe the surface morphology in order to provide a common nomenclature (Conditional recommendation, low-quality evidence)
We suggest that for non-pedunculated adenomatous (Paris 0-II and 0-Is) lesions ≥10 mm, surface morphology should be also described as granular or non-granular lateral spreading lesions. (Conditional recommendation, low-quality evidence)
We recommend photo documentation of all lesions ≥10 mm in size before removal, and suggest photo documentation of the post-resection defect (Strong recommendation, low-quality evidence).
We suggest proficiency in the use of electronic- (eg, narrow-band imaging [NBI], i-scan, Fuji Intelligent Chromo Endoscopy or blue light imaging) or dye (chromoendoscopy)-based image enhanced endoscopy techniques to apply optical diagnosis classifications for colorectal lesion histology. (Conditional recommendation, moderate-quality evidence)
We recommend proficiency in the endoscopic recognition of deep submucosal invasion. (Strong recommendation, moderate-quality evidence)
The macroscopic characterization of a colorectal lesion, including its location, size, and shape, combined with the real-time assessment of the suspected histopathology and estimation of the depth of invasion provides information about whether a lesion is amenable to endoscopic resection. In this document, we review key components to the macroscopic characterization of colorectal lesions. A more detailed description of the macroscopic assessment of lesions with submucosal invasion, and a decision-making guide to their optimal management is provided in separate MSTF document on Endoscopic Recognition and Management Strategies for Malignant Colorectal Polyps.
Paris Classification
The Paris classification has been the most used international endoscopic classification of colorectal lesion morphology (Figure 1 ).12 13,14
Figure 1.: Paris Endoscopic Classification of superficial neoplastic lesions in the colon and rectum.
Paris Classification Superficial Lesions, Type 0
The classification of type 0 lesions is based on the distinction between polypoid (type 0-I); and non-polypoid, (type 0-II). The polypoid type consists of pedunculated (type 0-Ip), and sessile (type 0-Is) lesions. The non-polypoid type 0-II lesions are divided by the absence (superficially elevated [type 0-IIa] and flat [type 0-IIb]) or the presence of a depression (type 0-IIc). The non-polypoid, excavated (type 0-III) lesions are rare in the colon. Although depressed (0-IIc) lesions are uncommon (1%–6% of non-polypoid lesions), their risk of submucosal invasion is the highest: the overall risk is reported to be 27%–35.9% compared with 0.7%–2.4% in flat (0-IIa) lesions. More than 40% of small (6–10 mm) depressed (0-IIc) lesions contain submucosal invasive cancer; virtually all large (>20 mm) depressed (0-IIc) lesions have submucosal invasion.15–18
Lateral Spreading Tumors
Non-polypoid lesions 10 mm or larger in diameter are referred to as laterally spreading tumors (LSTs). They have a low vertical axis and extend laterally along the colonic luminal wall. The morphologic subclassifications of LSTs facilitate the endoscopic removal plan, as they inform about submucosal fibrosis or the risk of submucosal invasion. Granular-type LSTs have a nodular surface and are composed of the homogeneous even-sized (LST-G-H) and mixed (LST-G-NM) nodular subtypes. Non-granular type LSTs have a smooth surface and are comprised of the flat elevated (LST-NG-FE) and pseudodepressed (LST-NG-PD) subtypes (Figure 2 ).19 19
Figure 2.: Lateral spreading lesions. Non-polypoid lesions ≥10 mm in diameter are referred to as laterally spreading tumors (LSTs). They have a low vertical axis and extend laterally along the luminal wall. LSTs are morphologically subclassified into granular type (LST-G) (A, B ), which have a nodular surface, and non-granular type (LST-NG), which have a smooth surface (C, D ). This macroscopic distinction is important to facilitate the endoscopic removal plan as it provides information about the risk of cancer or submucosal fibrosis in order to anticipate the technical ease or difficulty of the removal. Overall, LSTs were found to contain submucosal invasion (SMI) in 8.5% of the cases (95% CI, 6.5%–10.5%; I 2 86.8%; 26 studies) and high-grade dysplasia in 36.7% of the cases (95% CI 30.3%–43.2%; I 2 91.9%; 23 studies). Non-granular LSTs more often contained SMI than granular LSTs: 11.7% vs 5.9% (OR, 1.89; 95% CI, 1.48–2.42).
Optical Diagnosis
Endoscopic prediction of the histologic class of a polyp may influence the resection approach to ensure complete removal. A number of studies, including several meta-analyses, have shown that optical diagnosis of colorectal lesions is feasible in routine clinical practice and comparable to the current reference standard, histopathology.20,21
The Narrow Band Imaging International Colorectal Endoscopic (NICE) classification provides a validated criterion for the classification of type 1 (serrated class lesions–hyperplastic and sessile serrated lesions) and type 2 (adenomas), as well as those with deep submucosal invasion (type 3), using real-time NBI during colonoscopy22,23 Figure 3 ). Its application has been shown to be useful in assessing the most clinically relevant approaches: leave hyperplastic diminutive lesions of the rectum and sigmoid colon, remove all adenomas anywhere in the colon and any serrated lesions proximal to sigmoid colon and >5 mm, and biopsy and refer to surgery lesions with deep submucosal invasion. Using this classification, experienced endoscopists have achieved 93% concordance of surveillance intervals made by real-time optical diagnosis and pathology, and a >90% negative predictive value for rectosigmoid lesions when assessments were made with high confidence.21 24
Figure 3.: Optical diagnosis of colorectal lesions, NICE classification. The diagnostic criteria for colorectal lesions using NBI as recommended in the NICE classification. The use of confidence levels (high or low) in making an optical diagnosis is important in its implementation in clinical practice. *Can be applied using colonoscopes with or without optical (zoom) magnification. **These structures (regular or irregular) may represent the pits and the epithelium of the crypt opening. ***In the World Health Organization classification, sessile serrated polyp and sessile serrated adenoma are synonymous. Sessile serrated polyps often demonstrate some dark, dilated crypt orifices. ****Type 2 consists of Vienna classification types 3, 4, and superficial 5 (all adenomas with either low- or high-grade dysplasia, or with superficial submucosal carcinoma). The presence of high-grade dysplasia or superficial submucosal carcinoma may be suggested by an irregular vessel or surface pattern, and is often associated with atypical morphology (eg, depressed area).
The subtle endoscopic appearance of large sessile serrated lesions—predominantly flat in shape with indistinct borders—has been associated with high rates of incomplete removal compared to conventional adenomas (31% vs 7.2%), with even higher rates (47.6%) in large lesions.6 Figure 4 )25 26 27 28
Figure 4.: Morphologic features of sessile serrated lesions. Sessile serrated lesion–like features are defined as (A ) a clouded surface, (B ) indistinctive borders, (C ) irregular shape, or (D ) dark spots inside the crypts. These morphologic features are used to differentiate between sessile serrated lesions and hyperplastic lesions in the type 1 NICE polyps. The presence of at least 2 sessile serrated lesion–like features is hereby considered sufficient to diagnose a sessile serrated lesion.
Unfavorable histologic features of colorectal lesions, such as lymphovascular invasion, tumor budding, or poor differentiation, are not feasible to endoscopically predict before resection. However, the vertical depth of invasion of submucosal cancers can be estimated based on the morphologic appearance using high-definition endoscopy without magnification. Lesion morphology, such as Paris classification 0-IIc and 0-IIa + 0-IIc, non-granular surface particularly pseudodepressed subtype, NICE type 3,23 29 30 https://links.lww.com/AJG/B420 https://links.lww.com/AJG/B421
Section II: Endoscopic Removal Techniques
Statement 2: Lesion Removal
The primary aim of polypectomy is complete removal of the colorectal lesion and the subsequent prevention of CRC. Endoscopists should employ the safest, most complete, and efficient resection techniques based on available evidence.
Polypectomy techniques vary widely in clinical practice. They are often driven by physician preference based on how they were taught and on trial and error, due to the lack of standardized training and the paucity of published evidence. In the past decade, evidence has evolved on the superiority of specific methods. Although more recent practice surveys suggest an increased uptake in the use of cold snare removal techniques for diminutive and small colorectal lesions and EMR for large colorectal lesions, considerable heterogeneity in management techniques persist.31–34 13
Alarmingly, surgery for non-malignant colorectal lesions remains common practice.35–37 38 39 40,41 42 43 44
Therefore, endoscopists should employ techniques that reflect the safest, most complete or effective, and most efficient resection techniques based on available evidence. A suggested management algorithm is presented in Figure 5 .
Figure 5.: Algorithm for the management of colorectal lesions.
2a: Diminutive (≤5 mm) and small (6–9 mm) lesions
We recommend cold snare polypectomy to remove diminutive (≤5 mm) and small (6–9 mm) lesions due to high complete resection rates and safety profile. (Strong recommendation, moderate-quality evidence)
We recommend against the use of cold forceps polypectomy to remove diminutive (≤5 mm) lesions due to high rates of incomplete resection. For diminutive lesions ≤2 mm, if cold snare polypectomy is technically difficult, jumbo or large-capacity forceps polypectomy may be considered. (Strong recommendation, moderate-quality evidence)
We recommend against the use of hot biopsy forceps for polypectomy of diminutive (≤5 mm) and small (6–9 mm) lesions due to high incomplete resection rates, inadequate histopathologic specimens, and complication rates. (Strong recommendation, moderate-quality evidence)
Diminutive (≤5 mm) lesions
Most colorectal lesions are diminutive (≤5 mm). At that size, they are almost always benign,45,46 47–50 48 51
The risk of incomplete removal of diminutive lesions can be reduced with the use of cold snare polypectomy techniques (79%).52 Figure 6 , Video 2, https://links.lww.com/AJG/B443 53,54 52 55
Figure 6.: Cold polypectomy technique. (A ) Diminutive colon lesion in white light. (B ) Lesion characterization as a diminutive colon adenoma with type 2 NICE features using NBI. (C ) Position the lesion at 5 o’clock in line with the colonoscope accessory channel. Engage the snare tip against the mucosa on the proximal side of the lesion and open slowly. (D ) Open the snare until it has normal surrounding tissue and slightly move the endoscope distally as the snare is being opened according to the size of the lesion. (E ) While the snare is initially “closed” in a slow and steady manner, keep the endoscope tip deflection downward to apply gentle pressure against the mucosa (the ensnared polyp should not be lifted or tented during closure). (F ) Continue to maintain some tension on the snare catheter with gentle forward pressure during closure in order to avoid slipping of the snare upwards away from the submucosa and consequent shaving of the lesion. As the snare wire is closed, it will capture normal tissue. (G ) Once you have secured the normal tissue, then the lesion can be “cut.” The snare “close” is slow and steady, the snare “cut” is faster. The normal borders can be seen at the perimeter of the lesion in the cold snare specimen (G ). In the 5 o’clock position, the cut polyp typically remains in place for efficient retrieval. (H ) Minor post–cold snare oozing is expected and self-limiting.
Cold snare polypectomy is a safe, effective, and efficient polypectomy technique for diminutive (≤5 mm) colorectal lesions compared to hot polypectomy techniques. A recent randomized trial on 3–5 mm colorectal lesion removal showed significantly lower incomplete polyp removal rates with cold snare (19.6%) compared to hot forceps polypectomy (53.6%) (P < .0001).56 P < .0001). Another prospective, multicenter, randomized controlled, parallel non-inferiority trial of 796 lesions 4–9 mm in size showed complete resection rates for cold snare polypectomy (98.2%) comparable to those for hot snare polypectomy (97.4%), based on specimens obtained from the resection margin after polypectomy.57
Small (6–9 mm) lesions
Resection methods for small lesions have been highly variable among colonoscopists. The Complete Adenoma Resection (CARE) Study underscored the frequency of incomplete polypectomy, even for small lesions.6 58,59 https://links.lww.com/AJG/B444 60 57,61–63 64 65
Clinical trials have not defined the optimal snare choice for effective cold snare polypectomy. A study of a cold snare (0.3 mm wire, 9 mm diameter, diamond shape, stiff catheter) compared to a conventional snare (0.47 mm, 10 mm diameter oval shape, softer catheter) showed significantly higher complete resection of small lesions (≤10 mm), with dedicated cold snare vs conventional snare (91% vs 79%; P = .015), particularly for lesions 8–10 mm in diameter.66
Cold snare polypectomy has been shown to be a more efficient removal technique for lesions ranging from 3–8 mm in size compared to cold forceps or hot snare polypectomy. The total procedure time was significantly shorter using cold snare (or jumbo forceps) polypectomy compared to cold forceps techniques by an average of 2.66 minutes (95% CI, 0.18–5.14 minutes). Randomized trials of cold snare polypectomy have reported retrieval rates between 81% and 100%.67–69
2c: Non-pedunculated (10–19 mm) lesions
We suggest cold or hot snare polypectomy (with or without submucosal injection) to remove 10–19 mm non-pedunculated lesions. (Conditional recommendation, low-quality evidence)
Optimal methods for removal of sessile lesions measuring 10–19 mm remain uncertain. However, EMR should be considered for non-polypoid and serrated lesions in the 10- to 19-mm size range. Studies have shown that using conventional polypectomy techniques for non-polypoid lesions ≥10 mm70 71 6
2d: Non-pedunculated (≥20 mm) lesions
We recommend EMR as the preferred treatment method of large (≥20 mm) non-pedunculated colorectal lesions. Endoscopic resection can provide complete resection and obviate the higher morbidity, mortality, and cost associated with alternative surgical treatment. (Strong recommendation, moderate-quality evidence)
We recommend an endoscopist experienced in advanced polypectomy to manage large (≥20 mm) non-pedunculated colorectal lesions. (Strong recommendation, low-quality evidence)
We recommend snare resection of all grossly visible tissue of a lesion in a single colonoscopy session and in the safest minimum number of pieces, as prior failed attempts at resection are associated with higher risk for incomplete resection or recurrence. (Strong recommendation, low-quality evidence)
We suggest the use of a contrast agent, such as indigo carmine or methylene blue, in the submucosal injection solution to facilitate recognition of the submucosa from the mucosa and muscularis propria layers. (Conditional recommendation, moderate-quality evidence)
We recommend against the use of tattoo, using sterile carbon particle suspension, as the submucosal injection solution. The carbon particle suspension may result in submucosal fibrosis, and can thus reduce the technical success of future endoscopic resection of residual or recurrent lesion. (Strong recommendation, low-quality evidence)
We suggest the use of a viscous injection solution (eg, hydroxyethyl starch, Eleview, ORISE Gel) for lesions ≥20 mm to removal the lesion in fewer pieces and less procedure time compared to normal saline. (Conditional recommendation, moderate-quality evidence)
We recommend against the use of ablative techniques (eg, argon plasma coagulation [APC], snare tip soft coagulation) on endoscopically visible residual tissue of a lesion, as they have been associated with an increased risk of recurrence. (Strong recommendation, moderate-quality evidence)
We suggest the use of adjuvant thermal ablation of the post-EMR margin, where no endoscopically visible adenoma remains despite meticulous inspection. There is insufficient evidence to recommend a specific modality (ie, APC, snare tip soft coagulation) at this time. (Conditional recommendation, moderate-quality evidence)
We recommend detailed inspection of the post-resection mucosal defect to identify features for immediate or delayed perforation risk, and perform endoscopic clip closure, accordingly. (Strong recommendation, moderate-quality evidence)
We suggest prophylactic closure of resection defects ≥20 mm in size in the right colon, when closure is feasible. (Conditional recommendation; moderate-quality evidence)
We suggest treatment of intraprocedure bleeding using endoscopic coagulation (eg, coagulation forceps or snare-tip soft coagulation) or mechanical therapy (eg, clip), with or without the combined use of dilute epinephrine injection. (Conditional recommendation, low-quality evidence)
We suggest that patients on anti-thrombotics who are candidates for endoscopic removal of a colorectal lesion ≥20 mm receive individualized assessment, balancing the risks of interrupting anticoagulation for colonoscopic polypectomy or mucosal resection against the risks of significant bleeding during and after the procedure. (Conditional recommendation, low-quality evidence)
Endoscopic Mucosal Resection for Flat and Suspected Serrated Lesions
EMR is the preferred treatment method of large (≥20 mm) non-pedunculated colorectal lesions (Figure 7 , Video 4, https://links.lww.com/AJG/B445 https://links.lww.com/AJG/B431 https://links.lww.com/AJG/B432 40,41,44,72–78 43
Figure 7.: Inject-and-cut EMR. (A ) We evaluate a 15-mm superficially elevated serrated–appearing lesion under white light with diluted indigo carmine solution. In preparation for resection, we ensure the targeted lesion to the 5–6 o’clock position and plan the path of injection. (B ) We place the needle catheter next to the lesion to then expose and insert the needle into the submucosa. We rapidly inject the mixture of saline and diluted indigo carmine into the submucosa with simultaneous adjustments of the needle catheter and endoscope tip to ultimately lift the lesion upward. As the injection proceeds to the right, the direction of the injection is slightly altered to the left and then upward again in order to guide the creation of the focal submucosal bleb. (C ) During this process, we slightly suction the lumen in order to decrease wall tension, and then are able to place a snare around the lesion, and (D ) perform complete en bloc resection.
Recurrences were predominantly retreated with endoscopic therapy. There was a 0.3% (95% CI, 0.1%–0.4%) risk of invasive CRC at follow-up. The meta-analysis results, however, may underestimate the true post-endoscopic recurrence rate, as the main discriminator among the individual studies was the adequacy of follow-up. In 17 series it was considered inadequate, mainly due to short duration.
Inject-and-Cut Endoscopic Mucosal Resection Technique
The inject-and-cut EMR is a simple technique that is widely used for removal of large non-pedunculated lesions.79
Submucosal injection is a key step of EMR. Many submucosal injectants are available (Table 4 ). The ideal submucosal injectate should be a widely available inexpensive solution that provides a sustained lift to facilitate safe and efficient piecemeal resection. Normal saline has been used most widely due its availability and low cost. Within a short time, however, saline may dissipate into the surrounding submucosal space. Thus, several colloid plasma volume-expanding solutions, such as sodium hyaluronate,80,81 82 83 84 85 P = .02; I 2- 0%) and lower rates of residual lesions (OR, 0.54; 95% CI, 0.32–0.91; P = .02; I 2- 0%) using a colloid solution compared to normal saline for injection of lesions >20 mm.86
Table 4.: Submucosal Injectants for Endoscopic Resection
More recently, a commercially available emulsion (Eleview; Aries Pharmaceuticals, San Diego, CA) composed of water for injection, medium-chain triglycerides as the oily phase, poloxamer 188 as the bulking/cushioning agent, polyoxyl-15-hydroxystearate as the surfactant, sodium chloride as the osmotic agent, and methylene blue as the dye, has been US Food and Drug Administration–approved for submucosal injection to lift colorectal lesions.87 P < .001) and had a shorter resection time 19.2 minutes, range of 1–100 minutes vs mean of 29.7 minutes, range of 2–687 minutes (P = .326) compared to injection using saline with methylene blue. In addition, when the commercial preparation injection was used, the lesions were removed in fewer pieces (11.9%; P < .052) and with more en bloc resections (58%; P < .125). Another commercially available viscous dyed solution (ORISE Gel, Boston Scientific, Marlborough, MA), which is prefilled into a standard Luer lock syringe, has been US Food and Drug Administration–approved for use in submucosal injection to lift gastrointestinal mucosa during endoscopic resection.
The technique of submucosal injection is a critical factor in the success of the lift and the shape and sustainability of the bleb. Dynamic submucosal injection creates a generous bulge under the lesion (Figure 8 , Video 5, https://links.lww.com/AJG/B446 88
Figure 8.: Dynamic submucosal injection technique. (A ) We evaluate thickened fold under white light and can appreciate a non-polypoid, non-granular lateral spreading lesion overlying the fold. We place the needle catheter next to the lesion to then expose and insert the needle into the submucosa. (B ) We stab the mucosa with the needle to enter the submucosal space and then rapidly inject the mixture of saline and diluted indigo carmine into the submucosa (C ), while simultaneously pulling the needle catheter back into the endoscope and (D ) making adjustments to the needle catheter and endoscope tip to ultimately lift the lesion upward. As the injection proceeds to the right, (E ) the direction of the injection is slightly altered to the left and then upward again in order to guide the creation of the focal submucosal bleb. During this process, we slightly suction the lumen in order to decrease wall tension, and (F ) then are able to ultimately create a polypoid bleb to place the snare around to capture the lesion for endoscopic resection.
A stiff snare is used to facilitate capturing of the tissue. After capturing the lesion with a snare, the lumen is insufflated with air to stretch the wall, and the snare is lifted up while the snare is slightly loosened to release any entrapped muscularis propria. The snare is then closed entirely and the lesion is then transected using microprocessor-controlled cautery. Suggested electrocautery settings are provided in Table 5 .
Table 5.: Suggested Electrocautery Settinga
All grossly visible tissue of a lesion should be resected in a single colonoscopy session and in the safest minimum number of pieces. Prior failed attempts at resection are associated with higher risk for incomplete resection or recurrence. Furthermore, ablative techniques, such as snare tip and APC for the ablation of residual grossly visible tissue, have been associated with an increased risk of recurrence thought to be due to incomplete treatment of deeper layers (Video 6, https://links.lww.com/AJG/B422 https://links.lww.com/AJG/B423 89–91 P = .02; OR, 0.06; 95% CI, 0–0.58, albeit the control arm had very high rates of recurrence (7 of 11).92 P < .001) at first surveillance colonoscopy.93
In one study using conventional hot snare polypectomy techniques, serrated lesions were nearly 4 times more likely to be incompletely resected than adenomas (31.0% vs 7.2%; P ≤ .001), with nearly one-half of all large serrated lesions reported to be resected incompletely.6 71,94–96 71 94,95
Underwater Endoscopic Mucosal Resection
An alternative EMR technique, full water immersion (“underwater”) EMR, has been described recently and obviates the step of submucosal injection before snare resection.97 98 99–102 103 97,99,103 104
Cold Snare Endoscopic Mucosal Resection
Cold snare with injection is a recently described method to remove large lesions without electrocautery to minimize the risk of delayed bleeding and perforation (Video 7, https://links.lww.com/AJG/B447 https://links.lww.com/AJG/B448 105,106 105 106 107 108
Endoscopic Submucosal Dissection
The indications for colorectal endoscopic submucosal dissection (ESD) are relatively few, even at experienced centers, because most colorectal neoplasms are benign and can be resected using piecemeal EMR with minimal risk of recurrence. Large-sized (>20 mm in diameter) lesions that are indicated for endoscopic rather than surgical resection, and in which en bloc resection using inject-and-cut EMR is difficult, may be considered. These include lesions suspected to have submucosal invasion (ie, large depressed lesion or pseudodepressed LST-NG lesion), mucosal lesions with fibrosis, local residual early carcinoma after endoscopic resection, and non-polypoid colorectal dysplasia in patients with inflammatory bowel disease.109
The technique of ESD involves an endoscopic knife for cutting and submucosal injectant for lifting. After submucosal injection, a circumferential incision is performed to isolate the lesion with 3 or 4 mm surrounding normal mucosa. The submucosa under the lesion is injected further. With controlled movements under direct view facilitated with the use of a cap, the ESD knife dissects through the expanded submucosal layer to ultimately resect the lesion in 1 piece.
Hybrid Endoscopic Submucosal Dissection
The colon lumen is narrow and tortuous, and its wall is thin. As such, the risk of complication is relatively high using ESD technique compared to other removal techniques.110–112 113 114 115
Endoscopic Full-Thickness Resection
Endoscopic full-thickness resection in the colon and rectum is a recent approach that allows for better histologic evaluation of resection tissue, as it removes all layers of the colon wall.116,117
The full-thickness resection device system technology is based on a proprietary over the scope clip system (Ovesco Endoscopy AG, Tübingen, Germany). It consists of a cap with a ready-to-use mounted clip and a fitted snare at its tip. The applicator cap is mounted on the endoscope with the snare running on the outside of the scope within a sleeve. By turning the wheel, the clip is released to immobilize the target lesion tissue. The snare is then subsequently closed to cut the tissue. The technique is limited by the cap, which has an outer diameter of 21 mm. The cap size and length limits the amount of tissue that can be grasped, imposes difficulty advancing the endoscope through the colon, and impairs visibility during resection. Successful manipulation of the lesion into the cap also depends on thickness and scarring of the lesion and colonic wall.
A prospective multicenter study of 181 patients in 9 German centers demonstrated that endoscopic full-thickness resection with the full-thickness resection device was effective for difficult-to-resect colorectal lesions, such as non-lifting or challenging locations, especially for lesions ≤20 mm.118 P = .0038). This may partly reflect difficulty assessing whether the lesion margin is fully contained in the cap when the lesion is fully drawn into the cap. Further outcomes studies are needed to better guide patient and lesion selection for this technique to optimize complete resection rates and safety profile.
Special Features
Non-Lifting Lesions
Observation of the lesion during and after submucosal injection is a simple but important method to assess the potential for deeply invasive carcinoma.119–121 Figure 9 ).122 123
Figure 9.: Non-lifting features of colon lesions. Injection of saline or viscous fluid into the submucosa beneath these lesions does not result in lifting of the lesion; instead, the lesions infold, as only the submucosa of the normal surrounding mucosa is expanded. The non-lifting sign may be due to submucosal invasion as shown in lesions (A–C ); or underlying submucosal fibrosis in lateral spreading non-granular type lesions (D ) or from prior polypectomy cautery (lesions E and F ).
In the absence of invasive pathology, non-lifting fibrotic areas of lesion should be treated, but can be a challenge (Figure 10 ). The hot avulsion technique has recently been described for the removal of non-lifting fibrotic areas of colorectal lesions (Video 8, https://links.lww.com/AJG/B424 124,125 126 127,128 129 130
Figure 10.: Hybrid ESD of prior incomplete polypectomy. (A ) A prior incomplete polypectomy site shows macroscopically visible residual lesion within a convergence of folds. (B ) Following submucosal injection, the lesion is non-lifting, likely due to underlying fibrosis from previous cautery. (C ) An ESD knife is used for marginal resection of the periphery of normal mucosa surrounding the lesion. (D ) A stiff snare tip is placed into the cut mucosa. (E ) The snare is slowly opened using a fulcrum approach with the snare closed to fit into the cut perimeter. (F ) The snare is then closed tightly and the lesion cut using endocut electrocautery. (G ) Exposed bleeding superficial vessel is treated with soft coagulation using coagulation forceps. (H ) The defect shows significant fibrosis. (I ) The resected specimen.
Difficult Locations: Appendiceal Orifice, Ileocecal Valve, Near Dentate Line, and Colitis-Associated Dysplasia
Various groups have shown success in the endoscopic removal of lesions in difficult locations, such as an anorectal lesion near the dentate line (Figure 11 ) or at a flexure behind a fold (Figure 12 ), using EMR, ESD, or hybrid methods.113,131–133
Figure 11.: Hybrid ESD of distal rectal lesion involving anal canal. (A ) A 20-mm non-polypoid lateral spreading granular-type lesion on the right wall of the distal rectum is seen in retroflexion, and (B ) extending into the anal canal. (C ) An ESD knife is used to mark the periphery of normal mucosa surrounding the lesion. (D ) We lifted the lesion using dynamic submucosal injection technique and then performed circumferential incision of the normal periphery of the lesion in (E ) antegrade and (F ) retroflexion positions. (G ) A stiff snare tip is placed into the cut mucosa, slowly opened to set within the cut perimeter, and then closed tightly and the lesion cut en bloc using endocut electrocautery. (H ) The post-resection defect. The pathology was tubular adenoma. (I ) The post resection scar site at surveillance showed no local recurrence.
Figure 12.: Use of retroflexion for complete EMR. (A ) A non-polypoid superficially elevated lesion is seen at the hepatic flexion at a prior polypectomy site. (B ) A tattoo is well visualized at the area in retroflexion. (C ) Submucosal injection is performed in retroflexion. (D ) This facilitates visualization of the lesion now in antegrade. (E ) Endoscopic mucosal resection can then be complete. (F ) The post-resection borders are ablated.
2e: Pedunculated lesions
We recommend hot snare polypectomy to remove pedunculated lesions ≥10 mm (Strong recommendation, moderate-quality evidence)
We recommend prophylactic mechanical ligation of the stalk with a detachable loop or clips on pedunculated lesions with head ≥20 mm or with stalk thickness ≥5 mm to reduce immediate and delayed post-polypectomy bleeding. (Strong recommendation, moderate-quality evidence)
We suggest retrieval of large pedunculated polyp specimens en bloc to ensure ability to assess resection margins, rather than dividing polyp heads to facilitate through the scope specimen retrieval. (Conditional recommendation, low-quality evidence)
Large pedunculated lesions should be removed by hot snare polypectomy. Transection should be at the middle to lower stalk in order to provide adequate specimen for histologic assessment of stalk invasion. En bloc resection with marking or pinning of the stalk is a key component to accurate pathologic staging to assess for the level of invasion. A case series of 3 pedunculated (≥30 mm) lesions suggested that injection of 4–8 mL of 1:10,000 epinephrine into both the polyp head and stalk may reduce polyp size and improve en bloc resection rates.134 Table 6 , Video 9, https://links.lww.com/AJG/B425 Figure 13 ).135–138 139,140 140
Table 6.: Studies of Bleeding Prophylaxis for Pedunculated Lesion Removal
Figure 13.: Pedunculated lesion with prophylactic looping. Use of the endoloop in pedunculated polyp to prevent post-polypectomy bleeding. The endoloop is used like a snare except it can be detached after its deployment at the base of the polyp. (A ) A large pedunculated lesion is identified in the sigmoid colon. (B ) The lesion is repositioned to facilitate the endoloop placement around the lesion head. (C ) The loop is closed slightly as it is moved toward the base of the stalk, and (D ) then closed further. (E ) The loop is then closed tightly once at the base of a large pedunculated lesion to ligate the feeding vessel. The lesion starts to become ischemic, purple appearance. (F ) Once the ischemic appearance is confirmed, the cylinder stopper of the loop is then tightened, and (G ) released. (H ) The electrocautery snare is placed above the loop with sufficient room to prevent the endoloop from slipping off after transection. The ideal way to snare a pedunculated polyp that has been looped is to tighten the snare as much as possible to make the snared plane smaller than the plane that has been looped. (I ) Resection site immediately after resection. The loop remains at the base to prevent delayed bleeding.
Lesion Marking
Statement 3: Lesion Marking
We recommend the use of tattoo, using sterile carbon particle suspension, to demarcate any lesion that may require localization at future endoscopic or surgical procedures. (Strong recommendation, low-quality evidence)
We suggest placing the tattoo at 2–3 separate sites located 3–5 cm anatomically distal to the lesion (anal side), particularly when the purpose is to mark the lesion for later endoscopic resection. The carbon particle suspension if injected at or in close approximation to the lesion, may result in submucosal fibrosis, and can thus reduce the technical success and increase the risk of future endoscopic resection. (Conditional recommendation, low-quality evidence)
We suggest endoscopists and surgeons establish a standard location of tattoo injection relative to the colorectal lesion of interest at their institution. (Conditional recommendation, very low-quality evidence)
We recommend documentation of the details of the tattoo injection (ie, material, volume, position relative to the lesions) in the colonoscopy report, as well as photo documentation of the tattoo in relation to the colorectal lesion. (Strong recommendation, low-quality evidence)
Colonoscopic tattooing facilitates identification of a lesion at colonoscopy or surgery.141
Endoscopic tattooing is performed through the submucosal injection of a suspension of highly purified and fine carbon particles that are sterile and biocompatible, although not biologically inert.142 143
Tattoo location is dependent on the anticipated management of a lesion. For example, when marking a lesion for future endoscopic resection, then it is suggested that 2–3 separate injections at 3–5 cm distal (anal side) to the lesion should be performed (Figure 14 ).144
Figure 14.: The bleb technique for tattooing. (A ) A clip is visible protruding from an EMR site proximal to the visible fold. A needle is in the submucosa and tented toward the lumen so that the shape of the needle is visible. Visualization of the needle shape ensures submucosal location of the needle tip. (B ) A small saline bleb is made and the saline bleb is seen immediately after needle withdrawal. (C ) The tattoo-loaded needle is inserted into the saline bleb and 1-mL tattoo is injected. (D ) The finished tattoo.
Pathology Preparation and Assessment
The benefits of polypectomy and mucosal resection can be only fully realized with high-quality pathologic assessment. Orientation of the specimen requires knowledge of the appearance of the lesion before resection. Thus, the orientation of the specimen by the endoscopist, especially in cases of serrated lesions145
Surveillance
Recommendations for surveillance after colonoscopy and polypectomy are available in a recent updated USMSTF document.9
Statement 4: Surveillance
We recommend intensive follow-up schedule in patients after piecemeal EMR (lesions ≥20 mm) with the first surveillance colonoscopy at 6 months, and the intervals to the next colonoscopy at 1 year and then 3 years. (Strong recommendation, moderate-quality evidence)
To assess for local recurrence, we suggest careful examination of the post-mucosectomy scar site using enhanced imaging, such as dye-based (chromoendoscopy) or electronic-based methods, as well as obtaining targeted biopsies of the site. Post-resection scar sites that show both normal macroscopic and microscopic (biopsy) findings have the highest predictive value for long-term eradication. (Conditional recommendation, moderate-quality evidence).
In surveillance cases with suspected local recurrence, we suggest endoscopic resection therapy with repeat EMR, snare or avulsion method, and consider ablation of the perimeter of the post-treatment site. In such cases, subsequent examinations should be performed at 6–12 months until there is no local recurrence. Once a clear resection site is documented by endoscopic assessment and histology, the next follow-ups are performed at 1-year and then 3-year intervals. (Conditional recommendation, low-quality evidence)
In addition to detailed inspection of the post-mucosectomy scar site, we recommend detailed examination of the entire colon at the surveillance colonoscopy to assess for synchronous colorectal lesions. (Strong recommendation, moderate-quality evidence)
After piecemeal resection of non-pedunculated lesions ≥20 mm in size, a repeat colonoscopy is recommended in 6 months to assess for local recurrence and to clear the colon of synchronous lesions. There is a very high prevalence of synchronous disease in patients with lesions ≥20 mm. In a large EMR referral cohort with lesions ≥20 mm, patients had an average of 4 additional conventional adenomas; 40% had an additional advanced adenoma; 20% had an additional lesion ≥20 mm; and 0.8% had a synchronous cancer not detected by the referring physician. Of those referred for removal of a serrated lesion, 30% had unrecognized serrated polyposis.146
The post-mucosectomy scar site should be examined carefully; image-enhanced endoscopy techniques, such as chromoendoscopy147 148 149 150,151 152
In post-EMR surveillance cases with local neoplastic recurrence, appropriate therapy with biopsy or repeat EMR is warranted. In many cases the recurrence is on scar tissue, and EMR may be impossible. Resection of residual tissue using hot snare polypectomy or avulsion is appropriate, and many experts add ablative techniques to the margin of the resection to reduce the risk of further recurrence. Subsequent examinations should be performed at 6- to 12-month intervals, with shorter intervals used for recurrences that are large (≥1 cm) or demonstrated high-grade dysplasia. The majority of recurrences are a few millimeters in size, and the above treatment methods are highly effective, and follow-up 1 year later is adequate. Once a clear resection site is documented by endoscopic assessment and histology, the next follow-ups are performed at 1-year and then 3-year intervals. The rationale for such an intensive follow-up schedule is to treat the local recurrence, particularly after piecemeal polypectomy. Local neoplastic recurrence after endoscopic resection of large colorectal lesions has been reported in several longitudinal outcomes studies to be approximately 16%.89,153,154
Although current recommendations are for close follow-up as we describe, ongoing work to better understand risk for recurrence (eg, lesion >40 mm, use of APC to treat endoscopically visible residual lesion, intraprocedure bleeding, and high-grade dysplasia) is ongoing89,155 156
Adverse Events Associated With Colorectal Lesion Removal
A recent systematic review and meta-analysis of population-based studies from 21 studies including 1,966,340 colonoscopies performed during the period spanning from January 1, 2001 to August 31, 2012 examined the pooled prevalence of complications after colonoscopy with polypectomy.157 158
Bleeding
Bleeding is the most common post-polypectomy–related adverse event. The American Society for Gastrointestinal Endoscopy/American College of Gastroenterology Task Force on Quality in Endoscopy recommends that the post-polypectomy bleeding rate should be ≤1/100 colonoscopies.159,160 157 , and the size and type of lesions resected.
Routine endoscopic treatment of all post-polypectomy sites to prevent bleeding is not cost-effective.161,162 163 162,164
Significant risk factors for post-polypectomy bleeding include polyp size ≥10 mm, pedunculated lesions with thick stalks, LSTs, right-sided colonic lesions,165 https://links.lww.com/AJG/B417 166–168
Recent studies have focused on the role of bleeding prophylaxis after resection in subgroups of lesions, such as large (≥20 mm) non-pedunculated colorectal lesions.162,169 170 P = .02). The benefit was confined to lesions in the proximal colon, where the bleeding risk was significantly lower when clips were applied vs not (9.8% vs 3.3%; P < .001).171
Additionally, prophylactic coagulation of visible vessels in the resection defect of large lesions removed with EMR has not been associated with decreased post-endoscopic resection bleeding. An Australian multicenter randomized trial of 347 patients with average post-endoscopic resection defect of 40 mm did not show any significant reductions in clinically significant bleeding with prophylactic treatment of visible vessel, 5.2% with prophylactic treatment using coagulation forceps (SOFT COAG at 80W Effect 4, ERBE VIO 300D) vs 8.0% no additional therapy (P = .3).172
Post-Polypectomy Coagulation Syndrome
Post-polypectomy coagulation syndrome, also called post-polypectomy syndrome or transmural burn syndrome, is thought to occur when cautery injury causes full-thickness thermal injury of the bowel wall with localized serosal inflammation and peritonitis.173,174 175,176
Perforation
Although rare, 0.08% (95% CI, 0.06%–0.1%),157 43 177 178 179
Techniques to decrease the risk of capturing the muscularis propria have been described, including adequate submucosal injection and avoidance of a large snare size. Confirmation of safe tissue capture of the submucosa can be tested by movement of the snare back and forth. If the muscularis propria is entrapped, the whole wall, as opposed to only the lesion, may be seen to move. In such a scenario, slight loosening of the snare while tenting the mucosa into the lumen and toward the endoscope may help to release potentially entrapped muscularis propria. Alternating forward and backward movements of the snare are also often performed to avoid entrapment of the muscularis propria.79 180
Recognition of partial or full-thickness muscularis propria resection and potential perforation is critical (Video 10, https://links.lww.com/AJG/B426 https://links.lww.com/AJG/B427 https://links.lww.com/AJG/B428 181 177,182 183 184 185 183 https://links.lww.com/AJG/B429 https://links.lww.com/AJG/B449 https://links.lww.com/AJG/B450 https://links.lww.com/AJG/B433 186,187 188,189
Equipment and Tools
Statement 5. Equipment
We recommend the use of carbon dioxide insufflation instead of air during colonoscopy and EMR. (Strong recommendation, moderate-quality evidence.)
We suggest the use of microprocessor-controlled electrosurgical units. (Conditional recommendation, very low-quality evidence)
Carbon dioxide
Randomized controlled trials and a systematic review have demonstrated improved patient satisfaction with reduced pain scores and reduced intestinal distension on plain abdominal radiographs after routine colonoscopy with insufflation of carbon dioxide compared with insufflation of air.190,191 176
Cautery
The majority of US endoscopists perform polypectomy using either a pure coagulating or blended current, with only a minority (3%) using pure cut current, when surveyed regarding polypectomy practices for lesions 7–9 mm in size.192 193
Cap
The use of a soft transparent cap has been shown to facilitate colonoscopic EMR, particularly for flat lesions. It is fitted to the distal tip of the colonoscope insertion tube positioned with 3–4 mm of the cap exposed. This position stabilizes the endoscope distance in relation to the mucosa to maintain a clear, in-focus view, and can make it easier to inspect the lesion behind a fold or at a flexure.194
Statement 6: Quality of Polypectomy
The majority of benign colorectal lesions can be safely and effectively removed using endoscopic techniques. As such, endoscopy should be the first-line management of benign colorectal lesions.
When an endoscopist encounters a suspected benign colorectal lesion that he or she is not confident to remove completely, we recommend referral to an endoscopist experienced in advanced polypectomy for subsequent evaluation and management, in lieu of referral for surgery. (Strong recommendation, low-quality evidence)
We suggest the documentation of the type of resection method (eg, cold snare, hot snare, EMR) used for the colorectal lesion removal in the procedure report. (Strong recommendation, low-quality evidence)
We recommend that non-pedunculated lesions with endoscopic features suggestive of submucosal invasive cancer and that are resected en bloc be retrieved and pinned to a flat surface before submitting the specimen to the pathology laboratory to facilitate pathologic sectioning that is perpendicular to the resection plane. (Strong recommendation, low quality of evidence)
For non-pedunculated colorectal lesions resected en bloc with submucosal invasion, we recommend that pathologists measure and report the depth of invasion, distance of the cancer from the vertical and lateral resection margin, in addition to prognostic histologic features, such as degree of differentiation, presence or absence of lymphovascular invasion, and tumor budding. (Strong recommendation, moderate-quality evidence)
We recommend that endoscopists resect pedunculated lesions en bloc, and that when submucosal invasion is present, pathologists report the distance of cancer from the cautery line, the degree of tumor differentiation, and presence or absence of lymphovascular invasion. (Strong recommendation, moderate-quality evidence)
We recommend endoscopists engage in a local (institution-, hospital-, or practice-based) quality-assurance program, including measuring and reporting of post-polypectomy adverse events. (Strong recommendation, moderate-quality evidence)
We suggest measuring and reporting the proportion of patients undergoing colonoscopy who are referred to surgery for benign colorectal lesion management. (Conditional recommendation, moderate-quality evidence)
We suggest the use of polypectomy competency assessment tools, such as Direct Observation of Polypectomy Skills and/or the Cold Snare Polypectomy Competency Assessment Tool in endoscopic training programs, and in practice improvement programs. (Conditional recommendation, low-quality evidence)
Focused teaching is needed to ensure the optimal endoscopic management of colorectal lesions. Polypectomy competency, however, has been shown to significantly vary among colonoscopists.195 196 https://links.lww.com/AJG/B418 https://links.lww.com/AJG/B419
Ultimately, the majority of colorectal lesions can be safely and effectively removed using endoscopic techniques. The development and implementation of polypectomy quality metrics may be necessary to optimize practice and outcomes. For example, the type of resection method used for the colorectal lesion removal in the procedure report should be documented, and the inclusion of adequate resection technique as a quality indicator in CRC screening programs should be considered.34,198
Conclusions
Endoscopic resection of precancerous lesions reduces the incidence of CRC. Ineffective resection results in residual neoplasia and appears to be the cause of some interval cancers. There is clear evidence that endoscopic resection skills are quite variable, with a substantial need to increase the adoption of proven effective endoscopic resection techniques. Intensive investigation of resection technique in the past 2 decades has made evidenced-based recommendations possible. This report summarizes evidence- and consensus-based recommendations from the MSTF on best practices for endoscopic resection of precancerous colorectal lesions.
CONFLICTS OF INTEREST
The authors disclose no conflicts of interest relative to the current work since 2016. Industry relationships for authors (consulting, research, reimbursement) without conflicts of interest relevant to the current work since 2016: Douglas K. Rex (Olympus, Boston Scientific, Covidien, Lumendi, Salix, Aries, Cook Medical, ERBE, Bausch Health Inc, Novo Nordisk, Endochoice, Braintree Laboratories, Norgine, Endokey, EndoAid, Medivators, Satisfai Health); Sapna Syngal (Chirhoclin, Cook, Myriad Genetics, Inc, DC Health, Inc); David Lieberman (Covidien, Freenome Holdings, Inc, Ironwood, Check-Cap, CEGX); Douglas Robertson (Covidien, Freenome Holdings, Inc, Amadix); Tonya Kaltenbach (Aries Pharmaceuticals, Micro-Tech Endoscopy, Olympus, Boston Scientific, Medtronic); Aasma Shaukat (None); Samir Gupta (Freenome Holdings, Inc, Guardant Health, Inc, Mallinckrodt Pharmaceuticals); Carol Burke (Salix Pharmaceuticals, Ferring Pharmaceuticals, Aries Pharmaceuticals, Intuitive Surgical, Pfizer, Covidien, Boston Scientific, US Endoscopy, Abbvie Cancer Prevention Pharmaceuticals, Janssen Pharmaceuticals; SLA Pharma AG; Freenome Holdings, Inc). Jason Dominitz (None); Joseph C. Anderson (None).
Acknowledgement
The authors thank Christopher Stave, MLS, Lane Medical Library, Stanford University for his assistance with the conduct of the literature search; and Roy Soetikno, MD, MS for his cognitive and technical experienced guidance.
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