PATIENTS WITH LONG-STANDING inflammatory

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1 Digestive Endoscopy 2016; 28: doi: /den Review Paradigm Shift in the Surveillance and Management of Dysplasia in Inflammatory Bowel Disease (West) Roy Soetikno, 1 Tonya Kaltenbach, 2 Kenneth R McQuaid, 3 Venkataraman Subramanian, 5 Rahul Kumar, 6 Alan N Barkun 7 and Loren Laine 4 1 Division of Gastroenterology, Stanford University, 2 Endoscopy Unit, VA Palo Alto, Palo Alto, 3 Department of Gastroenterology, VA San Francisco, UCSF, San Francisco, 4 Section of Digestive Diseases, Yale University School of Medicine, New Haven, USA, 5 Gastroenterology Department, University of Leeds, Leeds, UK, 6 Department of Gastroenterology, SingHealth, Singapore, and 7 Division of Gastroenterology, The McGill University Health Centre, Montreal, Canada Patients with long-standing inflammatory bowel disease (IBD) colitis have a 2.4-fold higher risk of developing colorectal cancer (CRC) than the general population, for both ulcerative colitis (UC) and Crohn s disease (CD) colitis. Surveillance colonoscopy is recommended to detect early CRC and dysplasia. Most dysplasia discovered in patients with IBD is actually visible. Recently published SCENIC (Surveillance for Colorectal Endoscopic Neoplasia Detection and Management in Inflammatory Bowel Disease Patients: International Consensus Recommendations) consensus statements provide unifying recommendations for the optimal surveillance and management of dysplasia in IBD. SCENIC followed the prescribed processes for guideline development from the Institute of Medicine (USA), including systematic reviews, full synthesis of evidence and deliberations by panelists, and incorporation of the GRADE methodology. The new surveillance paradigm involves high-quality visual inspection of the mucosa, using chromoendoscopy and highdefinition colonoscopy, with endoscopic recognition of colorectal dysplasia. Lesions are described according to a new classification, which replaces the term dysplasia associated lesion or mass (DALM) and its derivatives. Targeted biopsies are subsequently done on areas suspicious for dysplasia, and resections are carried out for discrete, resectable lesions. Key words: chromoendoscopy, colon cancer, colonoscopy, dysplasia, inflammatory bowel disease INTRODUCTION PATIENTS WITH LONG-STANDING inflammatory bowel disease (IBD) colitis have a higher risk of developing colorectal cancer (CRC) than the general population, approximately 2.4-fold higher in ulcerative colitis (UC) 1 and a similar risk in Crohn s disease (CD) colitis. 2 Surveillance colonoscopy is recommended to detect dysplasia, the precursor of CRC, in order to potentially prevent or cure CRC. In the present review, we will focus on the recently published SCENIC (Surveillance for Colorectal Endoscopic Neoplasia Detection and Management in Inflammatory Bowel Disease Patients: International Consensus Recommendations) consensus statements as they provide a unifying consensus recommendation on the surveillance and management of dysplasia in IBD. 3,4 Corresponding: Roy Soetikno, Gastroenterology Department, Singapore General Hospital, National Cancer Center Singapore and Duke-NUS, Singapore. soetikno@earthlink.net Received 20 November 2015; accepted 8 February THE NEED FOR A NEW AND UNIFYING GUIDELINE COLONOSCOPY, THE GOLD standard examination to screen for colorectal neoplasms in patients without IBD, has relied on careful examination of the mucosa. In contrast, colonoscopy for surveillance of dysplasia in IBD has relied on extensive random biopsies to identify invisible dysplasia. The American Gastroenterological Association guidelines published in 2010 recommend obtaining at least 32 random biopsy specimens from all segments of the colon as the foundation of endoscopic surveillance. 5,6 These biopsies sample <0.1% of the surface mucosa. Conceptually, the technique of random biopsy is unlikely to be efficacious. Practically, only approximately one dysplasia is detected per 1000 biopsies and approximately 9% of patients with dysplasia are diagnosed. A population study using the United States Medicare database shows that the rate of interval CRC in patients with IBD is three-fold higher than in those without IBD. 7 A new approach is needed. The goal of SCENIC was to determine the optimal practice for the detection and management of dysplasia in IBD. The universal recommendation that surveillance to detect neoplasia be carried out was accepted as the starting point (SCENIC was 266 bs_bs_banner

2 Digestive Endoscopy 2016; 28: Surveillance for dysplasia in IBD 267 not designed to determine whether surveillance to detect neoplasia be carried out). The practice of random biopsy arose from knowledge, technology and techniques that were developed in the early 1980s the era of fiberoptic and early video endoscopy. Investigators in the early 1980s biopsied areas of colon that appeared nodular, but without a lesion being visible and, to their surprise, found dysplasia. Thus, the term invisible dysplasia was coined. Blackstone and others subsequently described that patients who had endoscopic biopsy of a lesion or a mass were often found to have CRC. Thus, he coined the term dysplasia associated lesion or mass (DALM). 8 Significant progress has been made since then. Recent studies of chromoendoscopy or highdefinition white light report that invisible dysplasia accounts only for a minority (10%) of patients diagnosed with dysplasia. The majority of dysplasia is visible. 9 Techniques and technology to visualize dysplasia are now available. 10 Chromoendoscopy using diluted indigocarmine or methylene blue can be very useful to delineate the border and surface topography of non-polypoid dysplasia, which accounts for the majority of dysplasia. The high-definition colonoscope, which is equipped with more than 1 million pixels and brighter lighting, allows endoscopists to visualize the colonic mucosa with details that were not available in the era of fiberoptic or early video endoscope. Note that chromoendoscopy and high definition provide different functions contrast and resolution, respectively. They are not interchangeable. Most importantly, current medical practice has shifted to evidence-based medicine. Currently available literature supports the use of chromoendoscopy with targeted biopsy rather than random biopsy. In fact, a number of gastrointestinal societies have recommended the use of chromoendoscopy with targeted biopsy Thus, the aim of SCENIC was to develop a unifying, evidence-based, guideline for the surveillance and management of dysplasia in IBD. THE SCENIC INTERNATIONAL CONSENSUS STATEMENT THE SCENIC INTERNATIONAL Consensus sought to address two issues: (i) how should surveillance colonoscopy for detection of dysplasia be carried out; and (ii) how should dysplasia identified be managed? In addition, in order to be able to ultimately implement the statements into clinical practice, SCENIC also developed two recommendations on the following topics: (i) how should dysplasia be described Figure 1 Schematic and timeline of the SCENIC (Surveillance for Colorectal Endoscopic Neoplasia Detection and Management in Inflammatory Bowel Disease Patients: International Consensus Recommendations) international consensus process.

3 268 R. Soetikno et al. Digestive Endoscopy 2016; 28: macroscopically; and (ii) how should the statement be implemented into practice? The development process of SCENIC meticulously adhered to the suggested standards for guideline development from the Institute of Medicine (USA) 14 and others 15 and used the Grading of Recommendations Assessment, Development and Evaluation (GRADE) methodology. 16 The SCENIC international multidisciplinary group represented a wide spectrum of stakeholders ([general gastroenterology, endoscopy, IBD, outcomes methodology, nurse, pathology, patient group, surgery] and practices [academic, government and private practice]), and attitudes regarding IBD surveillance and management of dysplasia. A schematic of the process that was undertaken is shown in Figure 1. We based our inclusion and exclusion criteria on nine PICO (P: patient, problem or population; I: intervention; C: comparison, control or comparator; O: outcomes)-formatted question statements. We carried out a systematic review of the literature with a defined search strategy using MEDLINE and EMBASE databases, as well as manual reference and scientific meeting abstract reviews. Two reviewers independently assessed over 5000 identified abstracts. Multiple systematic reviews were carried out for each focused question to synthesize the available data, and meta-analyses were done when appropriate. We carried out quality assessment of the evidence using modified JADAD (for randomized clinical trials) and QUADAS-2 (for diagnostic tests). The strength of the recommendation follows that of the GRADE methodology. The stakeholders deliberated using a well-developed online platform (Fig. 2) prior to having a face-to-face meeting in San Francisco in March SCENIC Consensus Statement was reviewed and endorsed by the American Gastroenterological Association, American Figure 2 Example of the screen view of the online consensus platform that was used to facilitate most aspects of the SCENIC (Surveillance for Colorectal Endoscopic Neoplasia Detection and Management in Inflammatory Bowel Disease Patients: International Consensus Recommendations) consensus process. Stakeholders received evidence reports for each statement along with the pertinent original studies. Two rounds of voting prior to a face-to-face meeting were conducted using the platform to determine consensus on the recommendation. A five-point scale (1, strongly disagree; 2, disagree; 3, neutral; 4, agree; 5, strongly agree) was used.

4 Digestive Endoscopy 2016; 28: Surveillance for dysplasia in IBD 269 Society of Gastrointestinal Endoscopy (ASGE), Asian Pacific Association of Gastroenterology, British Society of Gastroenterology, Canadian Association of Gastroenterology, and European Society of Gastrointestinal Endoscopy, and the Japanese Gastroenterological Endoscopy Society and published simultaneously in Gastrointestinal Endoscopy and Gastroenterology in March ,4 SCENIC Classification (Nomenclature) of IBD Colorectal Dysplasia The term DALM can be very confusing as it is not specific. A DALM can be a polyp, non-polypoid or mass. A subgroup of SCENIC panelists therefore developed a new set of terms to describe the macroscopic appearance of dysplasia (Fig. 3). They recommended using the descriptive terms that are derived from the Paris classification 17 with modifications to describe ulceration and border of the lesion. The SCENIC panelists also recommended abandoning the term DALM and its derivations. The term endoscopically resectable was also defined in order to indicate: (i) distinct margins of the lesion could be identified; (ii) the lesion appears to be completely removed on visual inspection after endoscopic resection; (iii) histological examination of the resected specimen is consistent with complete removal; and (iv) biopsy specimens taken from mucosa immediately adjacent to the resection site are free of dysplasia on histological examination. 3 How should surveillance colonoscopy for detection of dysplasia be carried out? The SCENIC recommendations are listed in Table 1, along with the proportion of panelists in agreement, the strength of the recommendation, and the quality of the evidence. Note that the criterion for accepting a statement for recommendation was defined as 80% of participants voting agree or strongly agree (or disagree or strongly disagree), and that the strength of the recommendation was voted to be strong or conditional by the panelist according to GRADE criteria. The words recommend and suggest were used for strong and conditional recommendations, respectively. 16 SCENIC international consensus statement recommends (with standard definition) and suggests (with high definition) the use of chromoendoscopy, rather than white-light endoscopy, when carrying out surveillance in patients with IBD. Thus, a paradigm clinical practice shift from the random biopsy technique. The summary statistics of studies that compared chromoendoscopy with white-light standard definition colonoscopy alone shows that a significantly greater proportion of patients with dysplasia will be identified using chromoendoscopy (relative risk = 1.8 [ ]). Additionally, the use of chromoendoscopy will lead to detection of significantly more patients with visible dysplasia, dysplasia, and visible dysplasia. There was only one study available in which high-definition colonoscopy was used. Thus, the SCENIC recommendation included a conditional Figure 3 SCENIC (Surveillance for Colorectal Endoscopic Neoplasia Detection and Management in Inflammatory Bowel Disease Patients: International Consensus Recommendations) classification of irritable bowel disease (IBD) dysplasia.

5 270 R. Soetikno et al. Digestive Endoscopy 2016; 28: Table 1 Summary Recommendations for Surveillance and Management of Dysplasia in Patients with IBD Statement 1 Statement 2 Statement 3 Statement 4 Statement 5 Statement 6 Statement 7 Statement 8 Statement 9 When performing surveillance with white-light colonoscopy, high definition is recommended rather than standard definition.(80% agreement; strong recommendation; low-quality evidence) When performing surveillance with standard-definition colonoscopy, chromoendoscopy is recommended rather than white-light colonoscopy.(85% agreement; strong recommendation; moderate-quality evidence) When performing surveillance with high-definition colonoscopy, chromoendoscopy is suggested rather than white-light colonoscopy.(84% agreement; conditional recommendation; low-quality evidence) When performing surveillance with standard-definition colonoscopy, narrow-band imaging (NBI) is not suggested in place of white-light colonoscopy.(84% agreement; conditional recommendation; low-quality evidence) When performing surveillance with high-definition colonoscopy, narrow-band imaging is not suggested in place of white-light colonoscopy.(80% agreement; conditional recommendation; moderate-quality evidence) When performing surveillance with image-enhanced high-definition colonoscopy, narrow-band imaging is not suggested in place of chromoendoscopy.(90% agreement; conditional recommendation; moderate-quality evidence) After complete removal of endoscopically resectable polypoid dysplastic lesions, surveillance colonoscopy is recommended rather than colectomy.(100% agreement; strong recommendation; very low-quality evidence) After complete removal of endoscopically resectable non-polypoid dysplastic lesions, surveillance colonoscopy is suggested rather than colectomy.(80% agreement; conditional recommendation; very low-quality evidence) For patients with endoscopically invisible dysplasia (confirmed by a GI pathologist) referral is suggested to an endoscopist with expertise in IBD surveillance using chromoendoscopy with high-definition colonoscopy. (100% agreement; conditional recommendation; very-low-quality evidence) recommendation for the use of chromoendoscopy, rather than white light, when carrying out surveillance with highdefinition colonoscopy. The procedure time increased, on average, by 10.7 min, but the additional time measured was not specific to carrying out chromoendoscopy (i.e. included time of random biopsies). SCENIC addresses the question of the use of equipmentbased image-enhanced endoscopy. Because narrow band imaging (NBI) was the only enhanced imaging technology that had been studied in IBD surveillance, the statements pertain to NBI only. The use of NBI is not suggested in place of white-light endoscopy standard or high definition system. Last, NBI is also not suggested in place of chromoendoscopy because meaningful benefit of NBI over chromoendoscopy is unlikely. 3 Meta-analysis of four randomized trials failed to show a significant difference. (absolute difference of 6% (95% CI: 1% to 14%) in the proportion of patients with dysplasia with chromoendoscopy over NBI). 3 How should dysplasia identified be managed? The SCENIC statement addresses the management of dysplasia detected on surveillance colonoscopy. Traditionally, the finding of dysplasia led to colectomy. SCENIC statements describe the management of polypoid, non-polypoid, and endoscopically invisible dysplasia (Table 1). Surveillance colonoscopy rather than colectomy is recommended for removal of endoscopically resectable polypoid dysplastic lesions. Data are limited on the management of non-polypoid dysplasia. Thus, the SCENIC statement for the management of non-polypoid endoscopically resectable dysplasia included surveillance is suggested for non-polypoid dysplastic lesions. after complete endoscopic resection. Finally, referral to an endoscopist with expertise in surveillance using chromoendoscopy with high-definition colonoscopy is suggested for patients with endoscopically invisible dysplasia after confirmation by a gastrointestinal (GI) pathologist. The specific technique required to remove the dysplasia was not part of the SCENIC. Roadmap to the Implementation of the SCENIC Statement A subgroup of SCENIC stakeholders have developed a document that describes the steps for the integration of chromoendoscopy in routine IBD surveillance practice and proposed solutions to potential barriers to widespread implementation. 18 The steps include the following. To use the standardized terminology. To familiarize gastroenterologists with standard chromoendoscopy protocols. The findings of SCENIC, including the chromoendoscopy and targeted biopsy techniques, have been disseminated widely. Information on how to obtain the free online resources has been made available through gastroenterology and endoscopy journals. Multiple lectures during regional and international endoscopy courses, symposia during a regional gastroenterology course, and Digestive Disease Week have been conducted. More recently, an

6 Digestive Endoscopy 2016; 28: Surveillance for dysplasia in IBD 271 ASGE day-long course to train key experts in IBD from throughout the USA has been conducted. To train in chromoendoscopy using standardized algorithms. Free online resources have been developed to support training: algorithms, 19 endoscopic videos, 20 atlases, 19,21,22 and books. 23 It has been suggested that partnered learning on the first five cases is a simple and efficient method. To practice using quality reporting including photodocumentation. To develop quality measures in IBD surveillance. To develop reimbursement for chromoendoscopy and targeted biopsy. CARRYING OUT CHROMOENDOSCOPY WITH TARGETED BIOPSY A VIDEO DESCRIBING the technique of chromoendoscopy and targeted biopsy is available free online. 20 In brief, the technique can be summarized as follows. Avoid active disease. Excellent bowel preparation is a prerequisite. Wash the residue during insertion. Chromoendoscopy begins in the cecum. Starting at the cecum, spray dilute indigocarmine through the water jet during withdrawal. Dilute indigocarmine is made to achieve a concentration of 0.03%. If dilute methylene blue is used, the concentration is 0.04%. To view in detail a suspect area, spray through the accessory channel a more concentrated indigocarmine (0.13%) or methylene blue (0.2%) solution. Examine all lesions closely to determine whether the border is well defined. Target biopsies to abnormal-appearing areas. When in doubt, biopsy the lesion. Superficial lesions with well-defined borders are potentially endoscopically resectable. If lesion is resectable, when possible, remove en-bloc; biopsy the adjacent mucosa. If lesion is unresectable, biopsy and tattoo. Biopsy the most amorphous region of the lesion; anything that looks amorphous in the colon is generally of concern. Areas that are slightly elevated or depressed, friable, have obscure vascular pattern, discolored (uneven redness), contain villous-appearing mucosa and are nodular are targeted for further detailed viewing and examination. They may be biopsied or resected. The immediate surrounding tissue needs to be biopsied as well. Chromoendoscopy and targeted biopsies have limitations. Presence of mucosal inflammation or multiple pseudopolyps may affect interpretation of chromoendoscopy and, in these circumstances, the need for random biopsy is still justified. EFFORTS POST-SCENIC The New ASGE guidelines THE SCENIC CONSENSUS statement and other SCENIC-related efforts ushered the field forward as it entered a new era in the surveillance and management of dysplasia in patients with IBD. Perhaps reflecting the transition as we move to implement the new paradigm into clinical practice, the SCENIC consensus group was unable to reach a consensus (requiring 80% agreement or disagreement) as to whether random biopsies can be abandoned once chromoendoscopy is used (60% disagreed with carrying out random biopsies when using chromoendoscopy). The new ASGE guidelines, 24 published after SCENIC, state that chromoendoscopy with targeted biopsies are sufficient for dysplasia surveillance. The random biopsies technique may be continued while becoming familiar with chromoendoscopy. Discussions pertaining to SCENIC SCENIC efforts have opened discussions as to how the surveillance and management of dysplasia in IBD can be improved. Editorials, 25 based on narrative review or retrospective study, 26 have been published that have questioned the SCENIC statements. For example, concerns have been raised that chromoendoscopy and targeted biopsy have not been shown to reduce important clinical outcomes such as colorectal cancer mortality. 27 These points are correct and ideally, improvements in surveillance techniques will be shown to improve such clinical outcomes. Nevertheless, despite the lack of direct evidence that colonoscopic surveillance decreases important outcomes such as colorectal cancer mortality, surveillance to detect neoplasia is universally recommended. Until data that directly document that colonoscopic surveillance and incorporation of techniques such as high-definition endoscopy and chromoendoscopy improve clinical outcomes such as colorectal cancer mortality, endoscopists will continue to perform surveillance and will ask what techniques are most likely to optimize the detection of dysplasia. CONCLUSIONS THE NEW PARADIGM of colonoscopy for surveillance of dysplasia in patients with IBD places the emphasis on chromoendoscopy to allow high-quality visual inspection of the mucosa. Targeted biopsies are subsequently carried

7 272 R. Soetikno et al. Digestive Endoscopy 2016; 28: out on areas suspicious for dysplasia and resections are done for endoscopically resectable suspicious lesions. Lesions are described according to a new classification, which replaces the term DALM and its derivatives. The SCENIC international consensus statement and other SCENIC-related efforts mark a new beginning in the surveillance and management of dysplasia in patients with IBD. CONFLICTS OF INTEREST R. SOETIKNO IS a consultant and has received research support from Olympus. T. Kaltenbach is a consultant and has received research support from Olympus. The other authors declare no conflicts of interest for this article. REFERENCES 1 Jess T, Rungoe C, Peyrin-Biroulet L. Risk of colorectal cancer in patients with ulcerative colitis: a meta-analysis of populationbased cohort studies. Clin. Gastroenterol. Hepatol. 2012; 10: Bleday R, Lee E, Jessurun J, et al. 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