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Quality in colonoscopy: European perspectives and practice Expert Rev. Gastroenterol. Hepatol. 8(1), 29–47 (2014)

Colin J Rees*1–3, Praveen T Rajasekhar1,3, Matthew D Rutter2–4 and Evelein Dekker5 1 South Tyneside District Hospital, Harton Lane, South Shields, Tyne and Wear, NE34 0PL, UK 2 School of Medicine and Health Sciences, Durham University, University Boulevard, Queens Campus, Stockton-on-Tees, UK 3 Northern Region Endoscopy Group 4 University Hospital of North Tees, Hardwick Road, Stockton-on-Tees, UK 5 Academic Medicxal Centre, Amsterdam, The Netherlands *Author for correspondence: Tel.: +44 191 404 10000; 4028 [email protected]

Colonoscopy is the ‘gold standard’ investigation of the colon. High quality colonoscopy is essential to diagnose early cancer and reduce its incidence through the detection and removal of pre-malignant adenomas. In this review, we discuss the key components of a high quality colonoscopy, review methods for improving quality, emerging technologies that have the potential to improve quality and highlight areas for future work. KEYWORDS: patient experience • polypectomy • quality assurance • safety • training

Colonoscopy is considered the ‘gold standard’ investigation for the detection of colonic neoplasia, currently. The purpose of colonoscopy is to diagnose colonic disease and it also plays a crucial role in colorectal cancer (CRC) prevention. The demand for colonoscopy is increasing. The approximate number of colonoscopies performed per year in the USA, UK and The Netherlands are 14 million [1], 360,000 [201] and 190,000 [202], respectively. Colonoscopy also forms the basis of most CRC screening programs either as the primary or confirmatory test. The aim of CRC screening is to detect cancer at an earlier stage, thereby improving prognosis [2,203]. The majority of CRCs are sporadic and thought to arise from potentially premalignant colorectal adenomas [3–5]. The detection and resection of adenomas at colonoscopy has been shown to significantly reduce the risk of future CRC and this forms an important additional aim of screening programs [6–8]. This review will discuss the important components of a high quality diagnostic colonoscopy, therapeutic procedures as well as the future of colonoscopy. What constitutes a high quality colonoscopy?

Colonoscopy can only be considered the ‘gold standard’ investigation to detect colonic pathology if it is performed safely and to the highest technical standard. In order to achieve this, a colonoscopic examination must include:

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• A complete examination to the cecum; • A thorough examination of the colonic mucosa; • High quality therapeutics; • Measures to ensure patient safety; • Measures to ensure the best overall patient experience. A number of national standards have been produced. TABLE 1 summarizes recommended quality standards from the UK, USA and The Netherlands. Completing colonoscopy

A procedure is considered complete if the colonoscope tip is passed into the cecal pole or terminal ileum (TI). This must be documented in written form and, ideally, supported by a photographic evidence of cecal landmarks or the TI in the majority of cases. Accepted cecal landmarks include the ileocecal valve (ICV), appendix orifice and tri-radiate fold. The cecal intubation rate (CIR) is the proportion of complete colonoscopies which is expressed in percentage. The European Society of Gastrointestinal Endoscopy (ESGE) recommends that for colorectal screening, an unadjusted CIR of 90% should be achieved [2]. In the USA, the US multi-society task force guidelines also recommend a minimum CIR of 90%, as in the UK, for all colonoscopies taken together and 95% for screening colonoscopies [9]. The same standards are also required

 2014 Informa UK Ltd

ISSN 1747-4124

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Table 1. Summary of quality standards and safety from the UK, USA and The Netherlands. USA

The Netherlands†

Quality indicator

UK

CIR

‡90%

‡90% (all cases) ‡95% (screening cases)

‡90%

ADR

>10%

‡25% in men >50 ‡15% in women >50

‡20%

PRR

>90%

‡95%

Good bowel preparation

>90%

Perforation rate

6 min was associated with significantly higher detection for all adenomas and advanced adenomas. Work from the NHS BCSP has demonstrated an increased yield of adenoma detection up to a mean withdrawal time of 11 min in the guaiac-FOB positive population [51]. Dynamic position change

Colonoscopy was traditionally performed with the patient in the left lateral position. The anatomy of the colon, however, dictates that this is often not the ideal position for passage of

Left lateral Supine Right lateral

Figure 2. Optimal patient position for examination of each colonic segment. Reproduced with permission from [52].

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the colonoscope along its entirety as certain segments have a tendency to be collapsed in this position making insertion and mucosal inspection difficult. The benefits of dynamic position change on luminal distension and adenoma detection were studied by East et al. who performed a randomized, crossover trial comparing examination of the colon in the left lateral position with dynamic position changes [52]. Following cecal intubation, the colonoscope was withdrawn to the rectum with patients either in the left lateral position or with dynamic position change (FIGURE 2) as dictated by randomization. The colonoscope was subsequently reinserted to the cecum and withdrawn using the alternative technique to the original. Polyps were only removed after the second withdrawal. The number of adenomas per segment and degree of luminal distension were recorded. The study demonstrated an increase in the number of adenomas detected in the segments where the optimal position for examination differed from the left lateral position. This was statistically significant for examination of the transverse colon. Luminal distension was also significantly better with the use of position change and this was positively correlated with the increase in adenoma detection. Antispasmodic use

Factors that can hinder mucosal inspection are the presence of folds and colonic spasm. The use of antispasmodic agents can relax colonic smooth muscle thereby reducing colonic spasm and the prominence of folds. The most commonly used agent is hyoscine N-butylbromide (Buscopan) although glucagon and peppermint oil (given topically via the colonoscope) are also used. Studies on the use of Buscopan provide conflicting results. There have been four recently published randomized, double-blind, placebo-controlled trials studying the effects of Buscopan use on polyp and adenoma detection. Two studies demonstrated no significant increase in ADR or PDR [53,54]. One reported a significant increase in the total number of polyps detected per patient in the Buscopan group. The PDR and ADR were also higher in the Buscopan group but did not reach statistical significance [55]. Lee et al. [56] studied the colonic spasm scores and number of polyps detected. A statistically significant reduction in spasm score was seen in the Buscopan group. More polyps were detected in patients with moderate to severe spasm receiving Buscopan compared to placebo, however, this didn’t quite reach statistical significance (p = 0.06). One of the studies in which no difference in ADR or PDR was detected found that there was a significantly lower detection of flat or depressed lesions [54]. Whilst this must be borne in mind, the study was not appropriately powered to enable firm conclusions to made regarding this finding. A study examining the effect of Buscopan on colonic surface area visualized through CT colonography demonstrated that significantly more colonic surface, as calculated by the CT software, was visualized in both the supine and prone positions Expert Rev. Gastroenterol. Hepatol. 8(1), (2014)

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Quality in colonoscopy

with Buscopan use compared with when no antispasmodics were used [57]. In their study of evaluating patient and colonoscopy factors that are influencing adenoma detection among patients colonoscoped within the NHS BCSP, Lee et al., reported that Buscopan use correlated positively with adenoma detection among screening colonoscopists [58]. Despite the conflicting results, Buscopan may have a role in improving lesion detection especially when significant colonic spasm is present. Its use is also recommended by experts for lesions that are difficult to detect and resect [59]. Rectal retroflexion

Detection of lesions in the rectum can sometimes be difficult with the colonoscope in the forward viewing position. Better views of the distal rectum can be achieved by retroflexing the colonoscope in the rectum. This may also provide a better position to sample or remove lesions in the lower rectum. A study of 480 patients in whom examination of the distal rectum was performed initially in the forward viewing position and subsequently in the retroflexed position demonstrated that 12 polyps (2.5% of all) were seen only in the retroflexed position, of which four (x3 90% in some series [103–105]. In other cohorts, like in FIT or guaiac-FOBt screening, many large and advanced adenomas are detected and need to be removed. The techniques discussed below are those that should be within the skilled set of all independent colonoscopists. The aim of polypectomy is to remove a polyp completely, safely and retrieve it for histological examination [106]. This is in order to reduce the risk of future CRC incidence and to inform clinical decision making regarding the need for surveillance colonoscopy. [6–8] Patients should receive written information regarding the possible need for polypectomy at colonoscopy for any indication, including the possible risks (bleeding and perforation), and be consented for standard polypectomy during the colonoscopy consent process [106]. Prior to polypectomy, it is important to manage those factors which may increase the potential complications. Most commonly, these are medical conditions or drugs that may increase the risk of bleeding and selecting the appropriate resection technique for each polyp. General principles to consider immediately prior to polypectomy for lesions of all sizes include: • The nature of the lesions: This should include assessment of size, shape and whether the lesion is fixed to the underlying muscle layer or not; • Optimizing luminal view: This should include adequate suctioning of fluid, washing, optimization of luminal distension 37

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with the use of position change and antispasmodics as indicated; • Colonoscope position and manipulation: This should include removal of loops, positioning the polyp close to the accessory channel (at the 5 o’clock position), consideration of the retroflexed position and the use of an assistant to maintain position; • Accessories and diathermy unit: Colonoscopists should be familiar with all equipment prior to attempting polypectomy including settings and understanding of diathermy machines when heat is to be used; • Communication: Good communication between the colonoscopist and endoscopy assistant is vital including clear agreement on instruction and rehearsal outside the patient. Standard polypectomy techniques Hot snare

This technique is most often used for polyps >5 mm in the left colon and for stalked polyps due to the increased likelihood of larger feeding vessels and therefore postpolypectomy bleeding. The electrocautery provided reduces this risk. The snare should always be marked by a pen on its handle to indicate the point at which the snare is fully closed. This helps to avoid grasping normal mucosa at the proximal margin of the polyp, which risks perforation, and also polyp transection prior to the application of current. Clear instructions between the endoscopist and assistant are vital [106,107]. Alternatively, the endoscopist can take control of the snare and ask the assistant to hold the colonoscope [106]. In addition to marking the snare, good communication is important to avoid transection of the polyp prior to the application of heat [107,108]. For larger polyps, injection of the polyp base with adrenaline can be considered or use of an endoloop to reduce the bleeding risk. Some colonoscopists use a submucosal injection at the base of stalked polyps to reduce the risk of heat induced serosal injury. Cold snare

This technique is useful for removing polyps and is recommended in the UK for lesions up to 7 mm in diameter. It is particularly useful in the right colon where thermal methods should be used cautiously due to the thin colonic wall. Cold snaring can be performed with a regular snare or special cold snare with or without the use of submucosal injection, the need for which should be assessed on an individual basis. The snaring technique is identical to that used for hot snaring. The technique has been shown to be safe for polyps smaller than 10 mm in diameter with studies reporting bleeding rates of 0–9%, all of which were immediate. We, however, recommend its use in polyps up to 7 mm only [109–111]. There were no reported perforations in these studies. Cold biopsy

Cold biopsy is used and can be used commonly to remove diminutive polyps, particularly if £3 mm, if they can be removed in a maximum of three bites [106,107,112].

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Hot biopsy

Hot biopsy is a technique that is suitable for removing diminutive polyps but should be used with caution and only in the left colon due to the risk of transmural thermal injury. The tip of the polyp is grasped and tented away from the mucosa and the electrocautery current passed into the polyp. Care should be taken to avoid excess thermal injury by monitoring the spreading of thermal injury [106,107]. The use of hot biopsy has become less common due to concerns of thermal injury. Endoscopic mucosal resection

In this technique, fluid is injected under a flat or sessile polyp, lifting it into a dome. The advantage of this technique is that it makes the lesion easier to grasp with a snare, reduces the risk of transmural thermal injury and also helps to identify the polyps that are tethered to the underlying muscle layer (‘non-lifting sign’) suggesting malignancy. Fluid types used to lift the polyp include saline and colloid. Some colonoscopists choose to add adrenaline and also indigo carmine or methylene blue, the latter aiding identification of the polyp margins [106]. Incomplete polypectomy

The complete adenoma resection (CARE) study demonstrated a significant incomplete proportion of polypectomies [113]. This study prospectively evaluated the proportion of polypectomies that were considered macroscopically complete in which residual neoplastic tissue remained at polypectomy margins determined by the use of post-polypectomy biopsies, the incomplete resection rate (IRR). Of the 346 polyps removed, 10.1% had evidence of residual neoplastic tissue. The rate was higher for large polyps (10–20 mm) compared with small (5–9 mm) polyps (17.3 vs 6.8%, relative risk = 2.1) and for sessile serrated adenomas compared with conventional polyps (31.0 vs 7.2%, relative risk = 3.7). Among colonoscopists performing at least 20 polypectomies, the IRR ranged from 6.5 to 22.7%. Incomplete polyp resection is one of the contributory factors for interval CRC following colonoscopy. It also highlights the need for careful assessment of residual polyp when removing large polyps and sessile serrated lesions. Advanced polypectomy

Removal of larger polyps, in particular flat or sessile polyps ‡20 mm in diameter, requires significant expertise to ensure safe and complete resection. Important issues include the higher associated risk of complications, the higher chance of high grade dysplasia or cancer within the lesion and the increased chance of recurrence. It is important that patients understand the risks associated with removal of large polyps and are consented appropriately. It is also vital that endoscopy lists, on which advanced procedures are to be performed, are structured appropriately including provision of sufficient time, equipment and adequately trained staff. Moreover, these procedures should be done by colonoscopists who regularly undertake such procedures. [114,115].

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Endoscopic mucosal resection of large colonic polyps

Polyp retrieval

The most commonly used technique is the ‘inject and cut’ approach [116]. Lesions are lifted by injection of a solution, most often containing a combination of saline, adrenaline and methylene blue, into the submucosa to separate it so that the lesion can be removed more easily and safely. During this process it is important to observe the ‘non-lifting’ sign, the presence of which suggests tethering of the lesion to structures within the submucosa. This could be a feature of an invasive cancer [117,118] but could also be present if previous resection has been attempted or biopsies have been taken. If present, proceeding to endoscopic mucosal resection (EMR) should be considered very carefully due to the risks of perforation and/or irradical resection in case of an invasive cancer. Resection may be performed en bloc or piecemeal depending on the size of the polyp. Following successful lifting, a snare of appropriate size is placed over the entire polyp or a certain area of the polyp, which is carefully closed and electrocautery applied to transect through the fluid cushion. Argon plasma coagulation (APC) can be used to treat residual polyp tissue at the resection margins. Studies have demonstrated that advanced EMR can be performed safely with low complication rates. Bleeding rates of between 2.2–12.1%, including procedural, early and late bleeding, have been reported [115,119,120]. A perforation rate of between 0.4 and 1.1% was reported in the same studies. Postpolypectomy syndrome (partial thickness burn) was reported in one study at a rate of 1.4%. Local polyp recurrence was highly variable being reported as 4.2 and 7.2%, however, was as high as 27% in one study within the subgroup of patients that underwent endoscopic follow-up which is highlighting the importance of endoscopic surveillance post-procedure. Independent risk factors for recurrence were reported as lesions measuring >4 cm in diameter, ileocaecal valve involvement, the use of APC and previous attempts at resection by one group [121]. The use of APC was not associated with recurrence in another study [117].

Following successful polyp removal, it is important to retrieve it for histological assessment. This is particularly important for polyps whose diameter is >1 cm due to the increased probability of advanced features (high grade dysplasia, villous components) or cancer. Polyps whose diameter is 10 mm, polyps with invasive features, all that have been resected piecemeal and polyps left in situ for removal during a future endoscopy or surgery. Most recommend placement of three tattoos with India ink is 10–20 mm distal to the lesion in question [106]. Similarly, tattooing is recommended for cancers and at the site of larger resected polyps in which the chance of carcinomatous change is higher. This is required so that this area of the colon can be identified by colonoscopy or at the time of surgical resection, respectively. Local policy should be developed and exact notification of the location in relation to the lesion in the endoscopy report is important. Colonic stents

The use of colonic stents to treat large bowel obstruction is increasing most commonly in the context of complete or near complete obstruction due to CRC. Self-expanding metal stents (SEMS) are used, most often, either as palliative treatment or as a bridge to surgery [129]. Preliminary results from one study, also suggests a possible role of SEMS in bridging during administration of neo-adjuvant chemotherapy [130]. The NICE in the UK recommend the use of self-expanding metal stents in the context of acute large bowel obstruction, either complete or near to complete, due to the left sided CRC [129]. Dilatation prior to stent insertion should not be attempted due to the increased risk of perforation [131]. SEMS are not recommended for low rectal cancers, right sided colonic obstruction or if there is a clinical or radiological evidence of perforation or peritonitis. This is because significant tenesmus occurs in low rectal lesions and surgical treatment is the preferred option for right sided cancers and in the context of perforation [132–134]. Furthermore, SEMS can be technically difficult to place in the right colon. Potential complications of SEMS placement include perforation, which can be intra-procedural or late, stent obstruction, stent migration, technical failure and death. In one pooled analysis, rates of perforation were 3.76%, re-obstruction of 7.34%, migration of 11.81 and 0.58% [108]. The median technical and clinical success rate was 94 and 91%, respectively and was higher when palliation was the goal of stent insertion. 39

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Regarding insertion technique, one large UK audit of 334 patients over a 5 year period, reported technical success as significantly better when a through scope technique was used, when compared to radiological insertion and resulted in fewer complications [135]. A UK based multicenter RCT evaluating the use of stents in the management of patients presenting with acute obstruction due to left sided CRC is currently underway and recruiting well [136]. The use of SEMS in the management of benign colonic strictures, such as those related to the diverticular disease and post-operative strictures, has also been evaluated, where the largest experience being in the setting of diverticular strictures. The rate of perforation as a late complication appears to be higher in those with diverticular disease, however, the use of SEMS as a bridge to surgery in this patient group appears to have a role. The ideal timing of surgery can be debated with one group who is suggesting that it should occur within 7 days and another 1 month [137,138] of stent insertion. The outcomes in those with extrinsic compression due to pelvic malignancy are poor. Rates of technical success are low and complication rates high. Furthermore, 30 day mortality rate is up to 36% in some series [139]. Safety & adverse events

As with any invasive procedure, AEs can occur at colonoscopy and are most likely when therapeutic procedures are performed. Bleeding and perforation are the most commonly encountered serious AEs. In The Netherlands CRC screening, acceptable perforation rates for all procedures and for those in which polypectomy is performed are quoted as 90% of sedation practise was in line with current BSG sedation guidelines. More than 10% of procedures were performed without sedation. Nitrous oxide was used as the sole sedative agent in 4.2% of procedures. Reversal agents were required in only 0.1% of procedures. Less than 10% of patients were assessed as they were experiencing severe discomfort assessed using the modified Gloucester comfort score. Similar sedation practise was reported by Rajasekhar et al., who reported that 85.6% of procedures were performed under conscious sedation. All practise was in line with current UK guidelines. Patient discomfort was not reported in this study. These data suggest that conscious sedation can be performed safely and it appears to be satisfactory in the majority, accepting the limitations of current methods of measuring comfort. The administration of propofol by appropriately trained nonanesthetists is endorsed in the USA by the American Society of Gastrointestinal Endoscopy (ASGE) and in Australia by the Australia and New Zealand College of Anaesthetists (ANZCA) in appropriately selected patients [153,154], however, is not supported in the UK. Patients should be at low risk as assessed by American Society of Anaesthesiologists (ASA) grade. The ASGE state those of ASA grade I to II while the ANZCA state those up to ASA grade III can be considered for nonanesthetist propofol use. Consideration of additional ECG and capnography monitoring is recommended. There is now a large body of international evidence supporting these recommendations [155–159]. The use of non-pharmacological adjuncts to sedation has also been studied. The use of music and other audio distractions have consistently been shown to improve comfort levels, www.expert-reviews.com

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reduce anxiety levels and reduce sedation requirements at low cost and, therefore, are worth consideration in cases where low sedation levels or unsedated procedures are preferable[160–162]. Comfort

Colonoscopy is well tolerated in majority of the cases including without sedation [163–165]. The procedure may, however, cause some discomfort or pain and so efforts should be made to minimize this when possible. Non-modifiable factors that increase patient discomfort include female gender, previous abdominal or pelvic surgery, the presence of poor bowel cleansing, diverticulosis, suspected irritable bowel syndrome, anxiety and anticipated discomfort [166,167]. Modifiable factors that can reduce discomfort include appropriate sedation, method of colonic insufflation, early loop resolution and the provision of pre-colonoscopy information in selected patients [168,169]. There are currently few validated measures of comfort in endoscopy and only one for colonoscopy. Challenges faced when deriving universal scores include the wide variation in pain perception, the presence of factors associated with pain (described above) and the variation in sedation practise internationally which alters perception and recall of discomfort. Comfort scores can be either patient or nurse derived. Patient scores are likely to be more representative of their true experience, however, may be influenced by sedation and are unlikely to be able to capture the wide variation. Nurse assessment is likely to be more consistent and reproducible but may be less accurate in representing the patient’s experience. A nurse assessed patient comfort score (NAPCOMS) was developed and validated by an international group. A modified Delphi method [170] was then used and tested by comparing comfort as assessed by an endoscopy nurse, a research nurse, the colonoscopist, and the patient. The colonoscopist and patient provided their scores using a four point Likert scale (no discomfort; minimal discomfort; moderate discomfort; and severe discomfort). All procedures were performed under mild or moderate sedation. This work demonstrated the reliability and reproducibility of the nurse derived score compared with patient reported scores. Further validated scoring systems reliant on patient derived measures are also being developed. Effect of colonoscopy technique & methods of colonic insufflation on comfort

A study in a Norwegian population assessed factors affecting patient discomfort and other outcomes of satisfaction, reporting that higher sedation rates did not necessarily result in a more comfortable procedure. They concluded, therefore, that this is not the only factor in patient comfort and that attention should be paid to good technique [171]. The prevention, early recognition and resolution of loops improve patient comfort and the use of MEI, as discussed above, could be one method of improving this area. Achieving good colonic distension is important to maximize mucosal views, however, prolonged distension can lead to discomfort. CO2 is reabsorbed into the blood stream much more 41

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readily than room air. The use of CO2 for colonic insufflation has been evaluated and has been shown to be safe as well as reducing patient discomfort following colonoscopy [172–174]. Water immersion colonoscopy, as discussed above, may also improve patient comfort in certain patient groups [42,43].

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Expert commentary

The importance of high quality colonoscopy is now much better understood. High quality procedures prevent cancers and reduce the need for surgery without causing harm to the patients. The importance of training and quality assurance are crucial and their role in improving quality can now be supported by evidence. It is important that all aspects of colonoscopy quality are measured. These include diagnostic accuracy, technical expertise for diagnostic and therapeutic procedures and patient experience of colonoscopy. Five-year view

With investment and enthusiastic leadership from its supervisory bodies, the quality of colonoscopy has significantly

improved in recent years. Emphasis on training and quality assurance of diagnostic and therapeutic procedures is crucial to ensure continued delivery of high quality colonoscopy. The future of colonoscopy is exciting. Wider application of current technologies and advances in new technologies will allow in vivo diagnosis and management of colonic lesions. Advances in resection techniques will reduce the need for invasive surgery. Establishing the roles of colonoscopy alongside other screening modalities (FOB testing, CT colonography, flexible sigmoidoscopy) will be important. Computer aided diagnosis and computer assisted evaluation of colonic mucosa may further improve colonoscopy. Financial & competing interests disclosure

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties. No writing assistance was utilized in the production of this manuscript.

Key issues • A high quality colonoscopy must consist of a complete, thorough examination combined with good quality and safe therapeutics and the best possible patient experience. • Investment in training and quality assurance results in significant improvements in completion rates. • The link between adenoma detection rate and interval cancers means that emphasis must now be placed on reducing the variability in adenoma detection rate through improvement in colonoscopy technique and use of advanced imaging where appropriate. • Therapeutics must be performed safely and to the highest technical standard to maximize the potential of colonoscopy to reduce colorectal cancer incidence. • Continued emphasis on patient safety and experience is important.

sequence. Br. J. Surg. 89(7), 845–860 (2002).

References 1

2

3

4

5

42

Seeff LC, Richards TB, Shapiro JA et al. How many endoscopies are performed for colorectal cancer screening? Results from CDC’s survey of endoscopic capacity. Gastroenterology 127(6), 1670–1677 (2004). Rembacken B, Hassan C, Riemann JF et al. Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE). Endoscopy 44(10), 957–968 (2012). Hisabe T, Tsuda S, Matsui T, Iwashita A. Natural history of small colorectal protuberant adenomas. Dig. Endosc. 22(1), 1443–1661 (2010). Jorgensen OD, Kronborg O, Fenger C. The Funen Adenoma Follow-up Study. Incidence and death from colorectal carcinoma in an adenoma surveillance program. Scand. J. Gastroenterol. 28(10), 869–874 (1993). Leslie A, Carey FA, Pratt NR, Steele RJ. The colorectal adenoma-carcinoma

6

Winawer SJ, Zauber AG, Ho MN et al. Prevention of colorectal cancer by colonoscopic polypectomy. The national polyp study workgroup. N. Engl. J. Med. 329(27), 1977–1981 (1993).

7

Citarda F, Tomaselli G, Capocaccia R, Barcherini S, Crespi M. Efficacy in standard clinical practice of colonoscopic polypectomy in reducing colorectal cancer incidence. Gut 48(6), 812–815 (2001).

8

Zauber AG, Winawer SJ, O’brien MJ et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N. Engl. J. Med. 366(8), 687–696 (2012).

9

Sandler RS. Quality of care in gastroenterology: beyond the bell curve. Gastroenterology 128(5), 1158 (2005).

10

Protocol for the authorization and auditing of colonoscopy centres and endoscopists: National screening programme for bowel cancer (2012).

11

Bowles CJ, Leicester R, Romaya C, Swarbrick E, Williams CB, Epstein O. A prospective study of colonoscopy practice in the UK today: are we adequately prepared for national colorectal cancer screening tomorrow? Gut 53(2), 277–283 (2004).

12

Aslinia F, Uradomo L, Steele A, Greenwald BD, Raufman JP. Quality assessment of colonoscopic cecal intubation: an analysis of 6 years of continuous practice at a university hospital. Am. J. Gastroenterol. 101(4), 721–731 (2006).

13

Rex DK, Bond JH, Winawer S et al. Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer. Am. J. Gastroenterol. 97(6), 1296–1308 (2002).

14

Shah HA, Paszat LF, Saskin R, Stukel TA, Rabeneck L. Factors associated with incomplete colonoscopy: a population-based

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Quality in colonoscopy

study. Gastroenterology 132(7), 2297–2303 (2007).

Expert Review of Gastroenterology & Hepatology Downloaded from informahealthcare.com by Chinese University of Hong Kong on 02/21/15 For personal use only.

15

16

17

18

19

Brenner H, Chang-Claude J, Seiler CM, Hoffmeister M. Interval cancers after negative colonoscopy: population-based case-control study. Gut 61(11), 1576–1582 (2012). Bressler B, Paszat LF, Chen Z, Rothwell DM, Vinden C, Rabeneck L. Rates of new or missed colorectal cancers after colonoscopy and their risk factors: a population-based analysis. Gastroenterology 132(1), 96–102 (2007). Gafa R, Maestri I, Matteuzzi M et al. Sporadic colorectal adenocarcinomas with high-frequency microsatellite instability. Cancer 89(10), 2025–2037 (2000). Chou CL, Lin JK, Wang HS, Yang SH, Li AF, Chang SC. Microsatellite instability screening should be done for right-sided colon cancer patients less than 60 years of age. Int. J. Colorectal Dis. 25(1), 47–52 (2010). Lim SB, Jeong SY, Lee MR et al. Prognostic significance of microsatellite instability in sporadic colorectal cancer. Int. J. Colorectal Dis. 19(6), 533–537 (2004).

stage cancer and adenomas in 50% of cases: experience of the prevalent round of screening from two first wave centres in the North East of England. Frontline Gastroenterol. 3(1), 10–15 (2011).

38

Morgan J, Thomas K, Lee-Robichaud H, Nelson RL, Braungart S. Transparent cap colonoscopy versus standard colonoscopy to improve caecal intubation. Cochrane Database Syst. Rev. 12(12)(2012).

27

Wexner SD, Garbus JE, Singh JJ. A prospective analysis of 13,580 colonoscopies. Reevaluation of credentialing guidelines. Surg. Endosc. 15(3), 251–261 (2001).

39

Lee YT, Lai LH, Hui AJ et al. Efficacy of cap-assisted colonoscopy in comparison with regular colonoscopy: a randomized controlled trial. Am. J. Gastroenterol. 104(1), 41–46 (2009).

28

Verma AJ, Mcgrath N, Bennett P et al. Scope to improve: a mutli-centre audit of 16,064 colonoscopies looking at caecal intubation rate, over a 2-year period. Frontline Gastroenterol. (3), 124–129 (2012).

40

Shah SG, Brooker JC, Williams CB, Thapar C, Saunders BP. Effect of magnetic endoscope imaging on colonoscopy performance: a randomised controlled trial. Lancet 356(9243), 1718–1722 (2000).

29

Bernstein C, Thorn M, Monsees K, Spell R, O’connor JB. A prospective study of factors that determine cecal intubation time at colonoscopy. Gastrointest. Endosc. 61(1), 72–75 (2005).

41

Shah SG, Thomas-Gibson S, Lockett M et al. Effect of real-time magnetic endoscope imaging on the teaching and acquisition of colonoscopy skills: results from a single trainee. Endoscopy 35(5), 421–425 (2003).

30

Zuber-Jerger I, Endlicher E, Gelbmann CM. Factors affecting cecal and ileal intubation time in colonoscopy. Med. Klin. 103(7), 477–481 (2008).

42

31

Harewood GC. Relationship of colonoscopy completion rates and endoscopist features. Dig. Dis. Sci. 50(1), 47–51 (2005).

Vemulapalli KC, Rex DK. Water immersion simplifies cecal intubation in patients with redundant colons and previous incomplete colonoscopies. Gastrointest. Endosc. 76(4), 812–817 (2012).

43

Leung CW, Kaltenbach T, Soetikno R, Wu KK, Leung FW, Friedland S. Water immersion versus standard colonoscopy insertion technique: randomized trial shows promise for minimal sedation. Endoscopy 42(7), 557–563 (2010).

44

Chilton A, Rutter MD. Quality Assurance Guidelines for Colonoscopy. Quality Assurance Guidelines for Colonoscopy (2011).

45

Kaminski MF, Regula J, Kraszewska E et al. Quality indicators for colonoscopy and the risk of interval cancer. N. Engl. J. Med. 362(19), 1795–1803 (2010).

20

De Jonge V, Sint Nicolaas J, Cahen DL et al. Quality evaluation of colonoscopy reporting and colonoscopy performance in daily clinical practice. Gastrointest. Endosc. 75(1), 98–106 (2012).

32

Rabeneck L, Paszat LF, Hilsden RJ et al. Bleeding and perforation after outpatient colonoscopy and their risk factors in usual clinical practice. Gastroenterology 135(6), 1899–1906 (2008).

21

Rees CJ, Painter J, Valori R, Barton R. BSG Quality and Safety Indicators for Endoscopy. The JAG Office, London, UK (2007).

33

Haycock AV, Patel JH, Tekkis PP, Thomas-Gibson S. Evaluating changes in gastrointestinal endoscopy training over 5 years: closing the audit loop. Eur. J. Gastroenterol. Hepatol. 22(3), 368–373 (2010).

22

23

Barton JR, Corbett S, Van Der Vleuten CP. The validity and reliability of a Direct Observation of Procedural Skills assessment tool: assessing colonoscopic skills of senior endoscopists. Gastrointest. Endosc. 75(3), 591–597 (2012). Gavin DR, Valori RM, Anderson JT, Donnelly MT, Williams JG, Swarbrick ET. The national colonoscopy audit: a nationwide assessment of the quality and safety of colonoscopy in the UK. Gut 62(2), 242–249 (2013).

24

Rajasekhar PT, Rutter MD, Bramble MG et al. Achieving high quality colonoscopy: using graphical representation to measure performance and reset standards. Colorectal Dis. 14(12), 1538–1545 (2012).

25

Lee TJ, Rutter MD, Blanks RG et al. Colonoscopy quality measures: experience from the NHS bowel cancer screening programme. Gut 61(7), 1050–1057 (2012).

26

Rajasekhar PT, Clifford GM, Lee TJW et al. Bowel cancer screening is safe, detects earlier

www.expert-reviews.com

Review

34

Spier BJ, Benson M, Pfau PR, Nelligan G, Lucey MR, Gaumnitz EA. Colonoscopy training in gastroenterology fellowships: determining competence. Gastrointest. Endosc. 71(2), 319–324 (2010).

46

Van Rijn JC, Reitsma JB, Stoker J, Bossuyt PM, Van Deventer SJ, Dekker E. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am. J. Gastroenterol. 101(2), 343–350 (2006).

35

Sedlack RE, Shami VM, Adler DG et al. Colonoscopy core curriculum. Gastrointest. Endosc. 76(3), 482–490 (2012).

47

36

Othman MO, Bradley AG, Choudhary A, Hoffman RM, Roy PK. Variable stiffness colonoscope versus regular adult colonoscope: meta-analysis of randomized controlled trials. Endoscopy 41(1), 17–24 (2009).

Barclay RL, Vicari JJ, Doughty AS, Johanson JF, Greenlaw RL. Colonoscopic withdrawal times and adenoma detection during screening colonoscopy. N. Engl. J. Med. 355(24), 2533–2541 (2006).

48

Rex DK. Colonoscopic withdrawal technique is associated with adenoma miss rates. Gastrointest. Endosc. 51(1), 33–36 (2000).

49

Lee RH, Tang RS, Muthusamy VR et al. Quality of colonoscopy withdrawal technique and variability in adenoma detection rates (with videos). Gastrointest. Endosc. 74(1), 128–134 (2011).

50

Simmons DT, Harewood GC, Baron TH et al. Impact of endoscopist withdrawal

37

Xie Q, Chen B, Liu L, Gan H. Does the variable-stiffness colonoscope makes colonoscopy easier? A meta-analysis of the efficacy of the variable stiffness colonoscope compared with the standard adult colonoscope. BMC Gastroenterol. 12(151), 12–151 (2012).

43

Review

Rees, Rajasekhar, Rutter & Dekker

speed on polyp yield: implications for optimal colonoscopy withdrawal time. Aliment. Pharmacol. Ther. 24(6), 965–971 (2006).

Expert Review of Gastroenterology & Hepatology Downloaded from informahealthcare.com by Chinese University of Hong Kong on 02/21/15 For personal use only.

51

52

53

54

55

56

Lee TJ, Blanks RG, Rees CJ et al. Longer mean colonoscopy withdrawal time is associated with increased adenoma detection: evidence from the Bowel Cancer Screening Programme in England. Endoscopy 45(1), 20–26 (2013). East JE, Bassett P, Arebi N, Thomas-Gibson S, Guenther T, Saunders BP. Dynamic patient position changes during colonoscope withdrawal increase adenoma detection: a randomized, crossover trial. Gastrointest. Endosc. 73(3), 456–463 (2011). De Brouwer EJ, Arbouw ME, Van Der Zwet WC et al. Hyoscine N-butylbromide does not improve polyp detection during colonoscopy: a double-blind, randomized, placebo-controlled, clinical trial. Gastrointest. Endosc. 75(4), 835–840 (2012). Rondonotti E, Radaelli F, Paggi S et al. Hyoscine N-butylbromide for adenoma detection during colonoscopy: A randomized, double-blind, placebo-controlled study. Dig. Liver Dis. 5(13), 00049–00042 (2013). Corte C, Dahlenburg L, Selby W et al. Hyoscine butylbromide administered at the cecum increases polyp detection: a randomized double-blind placebocontrolled trial. Endoscopy 44(10), 917–922 (2012). Lee JM, Cheon JH, Park JJ et al. Effects of Hyosine N-butyl bromide on the detection of polyps during colonoscopy. Hepatogastroenterology 57(97), 90–94 (2010).

57

East JE, Saunders BP, Burling D et al. Surface Visualisation at CT colonography simulated colonoscope withdrawal: effect of hyoscine butylbromide as antispasmodic. Gut 58(Suppl. 1), A122 (2009).

58

Lee TJW, Rees CJ, Blanks RG et al. Patient and colonoscopy factors influencing adenoma detection in patients undergoing colonoscopy in the NHS bowel cancer screening programme. Gut 60 (Suppl. 1), A68 (2011).

59

60

44

Kiesslich R, Neurath MF. Surveillance colonoscopy in ulcerative colitis: magnifying chromoendoscopy in the spotlight. Gut 53(2), 165–167 (2004). Hanson JM, Atkin WS, Cunliffe WJ et al. Rectal retroflexion: an essential part of lower gastrointestinal endoscopic examination. Dis. Colon Rectum 44(11), 1706–1708 (2001).

61

Hewett DG, Rex DK. Miss rate of right-sided colon examination during colonoscopy defined by retroflexion: an observational study. Gastrointest. Endosc. 74(2), 246–252 (2011).

62

Heresbach D, Barrioz T, Lapalus MG et al. Miss rate for colorectal neoplastic polyps: a prospective multicenter study of back-to-back video colonoscopies. Endoscopy 40(4), 284–290 (2008).

63

64

65

66

67

68

69

70

71

72

Rex DK, Cutler CS, Lemmel GT et al. Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology 112(1), 24–28 (1997). Coe SG, Crook JE, Diehl NN, Wallace MB. An endoscopic quality improvement program improves detection of colorectal adenomas. Am. J. Gastroenterol. 108(2), 219–226 (2013). Imperiali G, Minoli G, Meucci GM et al. Effectiveness of a continuous quality improvement program on colonoscopy practice. Endoscopy 39(4), 314–318 (2007). Francis DL, Rodriguez-Correa DT, Buchner A, Harewood GC, Wallace M. Application of a conversion factor to estimate the adenoma detection rate from the polyp detection rate. Gastrointest. Endosc. 73(3), 493–497 (2011). Rajasekhar PT, Lee TJ, Rutter MD et al. Using a ‘conversion factor’ to estimate adenoma detection rate. Endoscopy 61 (Suppl. 3), A371 (2012). Patel NC, Islam RS, Wu Q et al. Measurement of polypectomy rate by using administrative claims data with validation against the adenoma detection rate. Gastrointest. Endosc. 77(3), 390–394 (2013). Froehlich F, Wietlisbach V, Gonvers JJ, Burnand B, Vader JP. Impact of colonic cleansing on quality and diagnostic yield of colonoscopy: the European Panel of Appropriateness of Gastrointestinal Endoscopy European multicenter study. Gastrointest. Endosc. 61(3), 378–384 (2005). Harewood GC, Sharma VK, De Garmo P. Impact of colonoscopy preparation quality on detection of suspected colonic neoplasia. Gastrointest. Endosc. 58(1), 76–79 (2003). Burke CA, Church JM. Enhancing the quality of colonoscopy: the importance of bowel purgatives. Gastrointest. Endosc. 66(3), 565–573 (2007). Chokshi RV, Hovis CE, Hollander T, Early DS, Wang JS. Prevalence of missed adenomas in patients with inadequate bowel preparation on screening colonoscopy. Gastrointest. Endosc. 75(6), 1197–1203 (2012).

73

Lebwohl B, Kastrinos F, Glick M, Rosenbaum AJ, Wang T, Neugut AI. The impact of suboptimal bowel preparation on adenoma miss rates and the factors associated with early repeat colonoscopy. Gastrointest. Endosc. 73(6), 1207–1214 (2011).

74

Belsey J, Epstein O, Heresbach D. Systematic review: oral bowel preparation for colonoscopy. Aliment. Pharmacol. Ther. 25(4), 373–384 (2007).

75

Belsey J, Epstein O, Heresbach D. Systematic review: adverse event reports for oral sodium phosphate and polyethylene glycol. Aliment. Pharmacol. Ther. 29(1), 15–28 (2009).

76

Khan MA, Waisuddin N, Brown MD. Patient acceptance, convenience and efficacy of one-day versus two-day bowel preparation. Gastrointest. Endosc. 67, AB246 (2008).

77

Desmeules S, Bergeron MJ, Isenring P. Acute phosphate nephropathy and renal failure. N. Engl. J. Med. 349(10), 1006–1007 (2003).

78

Lai EJ, Calderwood AH, Doros G, Fix OK, Jacobson BC. The Boston bowel preparation scale: a valid and reliable instrument for colonoscopy-oriented research. Gastrointest. Endosc. 69(3 Pt 2), 620–625 (2009).

79

Rostom A, Jolicoeur E. Validation of a new scale for the assessment of bowel preparation quality. Gastrointest. Endosc. 59(4), 482–486 (2004).

80

Gupta N, Bansal A, Rao D et al. Prevalence of advanced histological features in diminutive and small colon polyps. Gastrointest. Endosc. 75(5), 1022–1030 (2012).

81

Lieberman D, Moravec M, Holub J, Michaels L, Eisen G. Polyp size and advanced histology in patients undergoing colonoscopy screening: implications for CT colonography. Gastroenterology 135(4), 1100–1105 (2008).

82

Rutter MD, Saunders BP, Schofield G, Forbes A, Price AB, Talbot IC. Pancolonic indigo carmine dye spraying for the detection of dysplasia in ulcerative colitis. Gut 53(2), 256–260 (2004).

83

Marion JF, Waye JD, Present DH et al. Chromoendoscopy-targeted biopsies are superior to standard colonoscopic surveillance for detecting dysplasia in inflammatory bowel disease patients: a prospective endoscopic trial. Am. J. Gastroenterol. 103(9), 2342–2349 (2008).

Expert Rev. Gastroenterol. Hepatol. 8(1), (2014)

Expert Review of Gastroenterology & Hepatology Downloaded from informahealthcare.com by Chinese University of Hong Kong on 02/21/15 For personal use only.

Quality in colonoscopy

84

Brown SR, Baraza W. Chromoscopy versus conventional endoscopy for the detection of polyps in the colon and rectum. Cochrane Database Syst. Rev. 6(10)(2010).

85

Togashi K, Konishi F, Ishizuka T, Sato T, Senba S, Kanazawa K. Efficacy of magnifying endoscopy in the differential diagnosis of neoplastic and non-neoplastic polyps of the large bowel. Dis. Colon Rectum 42(12), 1602–1608 (1999).

86

87

Togashi K, Osawa H, Koinuma K et al. A comparison of conventional endoscopy, chromoendoscopy, and the optimal-band imaging system for the differentiation of neoplastic and non-neoplastic colonic polyps. Gastrointest. Endosc. 69(3 Pt 2), 734–741 (2009). Ignjatovic A, East JE, Suzuki N, Vance M, Guenther T, Saunders BP. Optical diagnosis of small colorectal polyps at routine colonoscopy (Detect InSpect ChAracterise Resect and Discard; DISCARD trial): a prospective cohort study. Lancet Oncol. 10(12), 1171–1178 (2009).

88

Rex DK. Narrow-band imaging without optical magnification for histologic analysis of colorectal polyps. Gastroenterology 136(4), 1174–1181 (2009).

89

Pohl J, Lotterer E, Balzer C et al. Computed virtual chromoendoscopy versus standard colonoscopy with targeted indigocarmine chromoscopy: a randomised multicentre trial. Gut 58(1), 73–78 (2009).

90

91

92

93

94

Hong SN, Choe WH, Lee JH et al. Prospective, randomized, back-to-back trial evaluating the usefulness of i-SCAN in screening colonoscopy. Gastrointest. Endosc. 75(5), 1011–1021 (2012). Lee CK, Lee SH, Hwangbo Y. Narrow-band imaging versus I-Scan for the real-time histological prediction of diminutive colonic polyps: a prospective comparative study by using the simple unified endoscopic classification. Gastrointest. Endosc. 74(3), 603–609 (2011). Pigo F, Bertani H, Manno M et al. i-Scan high-definition white light endoscopy and colorectal polyps: prediction of histology, interobserver and intraobserver agreement. Int. J. Colorectal Dis. 28(3), 399–406 (2013).

endoscopy in patients undergoing screening or surveillance colonoscopy: a meta-analysis. Am. J. Gastroenterol. 107(3), 363–370 (2012). 95

96

Falk GW. Autofluorescence endoscopy. Gastrointest. Endosc. Clin. N. Am. 19(2), 209–220 (2009).

97

Matsuda T, Saito Y, Fu KI et al. Does autofluorescence imaging videoendoscopy system improve the colonoscopic polyp detection rate?–a pilot study. Am. J. Gastroenterol. 103(8), 1926–1932 (2008).

98

99

100

101

102

Nagorni A, Bjelakovic G, Petrovic B. Narrow band imaging versus conventional white light colonoscopy for the detection of colorectal polyps. Cochrane Database Syst. Rev. 18(1) (2012). Pasha SF, Leighton JA, Das A et al. Comparison of the yield and miss rate of narrow band imaging and white light

www.expert-reviews.com

Chung SJ, Kim D, Song JH et al. Efficacy of computed virtual chromoendoscopy on colorectal cancer screening: a prospective, randomized, back-to-back trial of Fuji Intelligent Color Enhancement versus conventional colonoscopy to compare adenoma miss rates. Gastrointest. Endosc. 72(1), 136–142 (2010).

103

Moriichi K, Fujiya M, Sato R et al. Back-to-back comparison of auto-fluorescence imaging (AFI) versus high resolution white light colonoscopy for adenoma detection. BMC Gastroenterol. 12(75), 12–75 (2012). Rotondano G, Bianco MA, Sansone S et al. Trimodal endoscopic imaging for the detection and differentiation of colorectal adenomas: a prospective single-centre clinical evaluation. Int. J. Colorectal Dis. 27(3), 331–336 (2012). Van Den Broek FJ, Fockens P, Van Eeden S et al. Clinical evaluation of endoscopic trimodal imaging for the detection and differentiation of colonic polyps. Clin. Gastroenterol. Hepatol. 7(3), 288–295 (2009). Van Den Broek FJ, Fockens P, Van Eeden S et al. Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions. Gut 57(8), 1083–1089 (2008). Van Den Broek FJ, Van Soest EJ, Naber AH et al. Combining autofluorescence imaging and narrow-band imaging for the differentiation of adenomas from non-neoplastic colonic polyps among experienced and non-experienced endoscopists. Am. J. Gastroenterol. 104(6), 1498–1507 (2009). Lieberman DA, Weiss DG, Harford WV et al. Five-year colon surveillance after screening colonoscopy. Gastroenterology 133(4), 1077–1085 (2007).

Review

104

Chen SC, Rex DK. Endoscopist can be more powerful than age and male gender in predicting adenoma detection at colonoscopy. Am. J. Gastroenterol. 102(4), 856–861 (2007).

105

Gupta N, Bansal A, Rao D et al. Accuracy of in vivo optical diagnosis of colon polyp histology by narrow-band imaging in predicting colonoscopy surveillance intervals. Gastrointest. Endosc. 75(3), 494–502 (2012).

106

Riley SA. Colonoscopic Polypectomy and Endoscopic Mucosal Resection: A Practical Guide. (2008).

107

Fyock CJ, Draganov PV. Colonoscopic polypectomy and associated techniques. World J. Gastroenterol. 16(29), 3630–3637 (2010).

108

Sebastian S, Johnston S, Geoghegan T, Torreggiani W, Buckley M. Pooled analysis of the efficacy and safety of self-expanding metal stenting in malignant colorectal obstruction. Am. J. Gastroenterol. 99(10), 2051–2057 (2004).

109

Ichise Y, Horiuchi A, Nakayama Y, Tanaka N. Prospective randomized comparison of cold snare polypectomy and conventional polypectomy for small colorectal polyps. Digestion 84(1), 78–81 (2011).

110

Paspatis GA, Tribonias G, Konstantinidis K et al. A prospective randomized comparison of cold vs hot snare polypectomy in the occurrence of postpolypectomy bleeding in small colonic polyps. Colorectal Dis. 13(10), 1463–1318 (2011).

111

Repici A, Hassan C, Vitetta E et al. Safety of cold polypectomy for

Quality in colonoscopy: European perspectives and practice.

Colonoscopy is the 'gold standard' investigation of the colon. High quality colonoscopy is essential to diagnose early cancer and reduce its incidence...
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