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Background: Primary sclerosing cholangitis (PSC) is a chronic inflammatory condition causing bile duct strictures. Differentiating inflammatory strictures from malignant transformation is challenging. Cholangioscopy allows direct visualization with the option to biopsy. We describe our experience of cholangioscopy in PSC and propose a novel stricture classification system based on cholangioscopic findings. Methods: All patients with PSC and a dominant stricture referred for cholangioscopy were reviewed. Based on visual characteristics with direct cholangioscopy, we propose a novel classification system for the extrahepatic form of PSC. Results: The proposed Edmonton Classification system for extrahepatic PSC strictures consists of the following phenotypes: 1) ‘inflammatory type’, with mucosal erythema and active inflammatory exudate, 2) ‘fibro-stenotic type’, with concentric fibrotic scars, and 3) ‘nodular or mass-forming type’, with a mass in the involved segment of extrahepatic bile duct. From 2011–2017, 30 patients with PSC and a dominant stricture (21 M, mean age 46 years) underwent 32 cholangioscopy procedures. Cholangioscopy was technically successful in 29 of 32 procedures (91%). In these 29 stricture cases, inflammatory type was seen in 16 (55%), fibro-stenotic type in seven (24%) and nodular or mass-form- ing type in five (17%). In one (4%) procedure, there was no stricture or abnormality identified. Conclusion: Cholangioscopy is effective and safe for the evaluation of dominant biliary strictures in PSC. Based on our experience with cholangioscopy, we propose a novel classification system of extra - hepatic PSC phenotypes: the Edmonton Classification. Keywords: Cholangioscopy, Classification, Primary sclerosing cholangitis, Stricture develop cholangiocarcinoma during the course of their lifetime INTRODUCTION (8). Published literature with respect to biliary tract investigation Primary sclerosing cholangitis (PSC) is a chronic inflammatory in patients with PSC that have worsening liver biochemistry or disease that leads to the formation of multifocal strictures in the identification of a dominant stricture on surveillance imaging, as intrahepatic or extrahepatic bile ducts—or both—and progresses with magnetic resonance cholangiopancreatography (MRCP), to end-stage liver disease (1). There is no effective medical therapy has focused on confirmation or exclusion of cholangiocarcinoma. (2–6), and most patients eventually require liver transplantation Per oral cholangioscopy permits direct visualization of (7). Patients with PSC frequently develop dominant strictures extrahepatic bile duct strictures, and compared to endoscopic with or without recurrent cholangitis, and up to 20% of patients © The Author(s) 2018. Published by Oxford University Press on behalf of the Canadian Association of Gastroenterology. 174 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Downloaded from https://academic.oup.com/jcag/article-abstract/1/4/174/4995069 by Ed 'DeepDyve' Gillespie user on 15 January 2019 Journal of the Canadian Association of Gastroenterology, 2018, Vol. 1, No. 4 175 retrograde cholangiopancreatography (ERCP), has been METHODS shown to improve diagnostic accuracy for malignant biliary At our center, a single-operator per oral direct visualization disease (9). However, cholangioscopy in patients with PSC system (SpyGlass™, Boston Scientific, Marlborough, MA) is and dominant strictures has not been evaluated thoroughly. used for all cholangioscopy procedures, including those for the Protocol screening cholangioscopy with biliary biopsies (sim- evaluation of dominant biliary strictures in PSC. Indications for ilar to yearly colonoscopy in patients with PSC and ulcerative cholangioscopy in this subset of patients include abnormal liver colitis for the early detection of colon cancer) looks like an biochemistry or a ductal caliber change noted on surveillance attractive strategy for PSC patients, especially in patients with imaging with MRCP. Our centre has been performing single-op- a dominant common bile duct (CBD) stricture. However, this erator cholangioscopy since 2011 with the original SpyGlass™ has not been properly evaluated. A prospective study of patients Legacy system but later transitioned to the SpyGlass™ Digital with PSC who had an ERCP indicated for dominant strictures system when it became available in 2015. demonstrated that cholangioscopy did not improve detection Per oral cholangioscopy is performed under general anes- of cholangiocarcinoma more than ERCP alone (10). Other thesia, but if the services of an anesthetist are not available, small studies have only shown mild improvement of cholan- conscious sedation is administered by the endoscopist and gioscopy in detecting cholangiocarcinoma (11, 12). monitored by the assisting nursing sta. ff However, the focus of cholangioscopy in PSC in published Most, but not all, patients had a previous sphincterotomy, literature appears to have been the confirmation or exclu- and wherever possible, free-hand cannulation of the bile duct sion of cholangiocarcinoma when there is a biochemical or with the cholangioscope was performed. If not, a 0.035-inch radiographic suggestion of a ‘new’ or ‘worsening’ dominant stiff guidewire was utilized to assist in cannulating the bile duct. stricture in the CBD. There has been no published report of Our approach is to review any available cross-sectional imag- cholangioscopy in the diagnostic and prognostic stratifica - ing, especially MRCP, before performing cholangioscopy and tion in patients with PSC or dominant strictures of the CBD. to minimize the use of contrast dye before direct visualization. Moreover, it has been shown that the severity of cholangiog- Contrast dye was felt to interfere with optimal visualization, but raphy scores correlates with prognosis in PSC (13–15) and this is not as much of a factor with the current improvements that endoscopic treatment of strictures may affect the natural in digital imaging. W here necessary, a stiff guide-wire was used history of the disease (13, 15, 16). Given that PSC prognosis to access specific areas of the biliary tree, and balloon-dilation seems related to stricture type and extent, it would be useful to of a CBD stricture was performed if there was resistance to the evaluate ways of subtyping and surveying PSC to gain useful passage of the 10-French cholangioscope. Once the cholangio- insights into the natural history and perhaps to help explain scope was at the desired location in the bile duct, visualization the variable response to treatments, in addition to assessing was optimized by minimal amounts of sterile water irrigation for the risk of cholangiocarcinoma development. With the and suctioning. Cholangioscopic features such as erythema, availability of per oral cholangioscopy, we can now directly neo-vascular proliferation, ulceration, presence of fibrinous visualize the bile duct mucosa and have the ability to perform exudate, presence of nodules and scars/rings were described. targeted biopsies in diseases that were previously appreciated All patients with PSC undergoing per oral cholangioscopy only through cholangiographic interpretation. Regardless, it at our centre for the previously mentioned indications were is clear that traditional cholangiography will not address these reviewed for this study. Cases performed at our centre are not subtleties, and perhaps per oral cholangioscopy, along with routinely video-recorded. Most procedures (27 of 30 [90%] histological assessment, will give further insight into targeted patients) were performed by an experienced endoscopist (GS), lines of therapy. and visual characteristics were described and recorded at the The aim of this study is to evaluate the current evidence of time of cholangioscopy. Once the cholangioscopy was com- cholangioscopy for the diagnostic stratification of dominant pleted, cholangiography and any intervention, such as stricture strictures in PSC. Importantly, based on our experience with dilation, were at the discretion of the endoscopist and based on cholangioscopy in dominant strictures in PSC, we would like clinical indication. to propose nomenclature for a classification system to bee tt r understand the variations in phenotypic expression of this dis- RESULTS ease process. To our knowledge, this kind of diagnostic stratifi - Cholangioscopy in PSC Patients cation has not been reported to date. Such stratification could be used to potentially gain prospective insight into the natural A total of 30 patients with PSC were referred to our unit for history of dominant strictures in PSC, assist in developing tar- the investigation of a dominant stricture, and they under- geted therapeutic options and also exclude a small proportion went 32 cholangioscopy procedures (Table 2). There were 21 of patients with PSC mimickers, such as IgG4-associated cho- males, and the mean age was 46 years (range 19–74 years). langitis (17). Twenty-eight patients underwent one cholangioscopy Downloaded from https://academic.oup.com/jcag/article-abstract/1/4/174/4995069 by Ed 'DeepDyve' Gillespie user on 15 January 2019 176 Journal of the Canadian Association of Gastroenterology, 2018, Vol. 1, No. 4 procedure each, whereas two patients underwent cholangios- transplantation (2), it would be ideal to identify these candi- copy twice, at an interval of two years and six months, respec- dates early to optimize outcomes. Since it is challenging to rule tively. Cholangioscopy was technically successful in 29 of 32 out malignancy in these cases, aggressive surveillance cholan- procedures (91%). In three procedures, it was not possible to gioscopy with biopsies are most beneficial here to identify any advance the cholangioscope to the desired segment in question, progression to malignancy (16). and the procedure had to be aborted. Based on the visual characteristics described in Table 1, the remaining 29 procedures were stratified per protocol into Phenotype Stratification System—the Edmonton inflammatory type in 16 cases (55%), fibro-stenotic type in Classification seven cases (24%) and nodular or mass-forming type in five Based on our experience with cholangioscopy in patients cases (17%). In one (4%) procedure, there was no stricture or with PSC, there appear to be distinct phenotypes that occur abnormality identified. among these dominant strictures. We propose the Edmonton Based on the Edmonton Classification, we also propose an Classification system with three distinct phenotypes of dom- algorithm for the management of dominant extrahepatic biliary inant strictures: inflammatory, fibro-stenotic and nodular or strictures in PSC (Figure 4). mass-forming types. The cholangioscopy-based description of characteristic visual features seen in these sub-types is outlined DISCUSSION in Table 1. In addition to the lack of effective treatment, there are no In the ‘inflammatory type’ of stricture, cholangioscopy reveals reliable clinical or biochemical parameters that predict the mucosal erythema and exudate (Figure 1). We have identi- progression of disease in PSC. The Mayo Clinic Risk Score fied a spectrum of disease ranging from acute inflammation provides a statistical assessment of the probability of survival (Figure 1A) to chronic, smoldering inflammation with varying but does not predict pae tt rns in progression of disease or degrees of fibrosis ( Figure 1B). development of cholangiocarcinoma (19). Patients come to The ‘fibro-stenotic type’ of stricture is typically found in medical ae tt ntion either because of jaundice and an increase asymptomatic patients. Cholangioscopy shows circumferential in cholestatic liver enzymes, specifically alkaline phospha - rings or asymmetric cicatrization (Figure 2). These strictures tase or bilirubin, or because of the suggestion of a ‘dominant’ are more appropriate for endoscopic therapy if there is evidence common bile duct (CBD) stricture on surveillance imaging of cholestasis (18). such as MRCP. The finding of a dominant stricture usually Finally, the ‘nodular or mass-forming type’ of stricture is char- warrants further interrogation of the CBD with ERCP and tis- acterized by a focal nodular growth of tissue within a segment sue acquisition with brush cytology to differentiate a benign of extrahepatic bile duct (Figure 3A–D). This subtype is most from a malignant etiology (20). It is reasonable to argue that concerning for evolution to cholangiocarcinoma via a dyspla- ‘indirect’ imaging with cholangiography—whether with sur- sia-to-neoplasia sequence previously suggested (16). With veillance MRCP or interventional ERCP—tends to view promising results from aggressive neoadjuvant therapy and dominant CBD strictures as a single distinct entity with the aim of excluding cholangiocarcinoma. A recent systematic Table 1. The Edmonton Classification of dominant strictures in review and meta-analysis of bile duct brushings for cholangio- PSC by cholangioscopic features carcinoma in PSC assessed 747 patients in 11 studies, with a sensitivity and specificity of 43% and 97%, respectively. The Stricture Type Cholangioscopy features Inflammatory Acute (Figure 1A) Table 2. Patient demographics and cholangioscopy characteristics (Figure 1) 1. Mucosal erythema 2. Ulceration Patients, n 30 2. Fibrinous white exudate Age, years ± SD (range, years) 46 ± 15 (19–74) Chronic (Figure 1B) Gender, M:F (%) 21:9 (70:30) 1. Patchy erythema with early Total procedures, n 32 scar/ring formation Cholangioscopy findings, n (%) 2. No ulceration 1. Unsuccessful procedures 3/32 (9) 3. No exudate 2. Successful procedures 29/32 (91) Fibro-stenotic 1. Fibrotic scars/rings a). Normal 1/29 (4) (Figure 2) 2. No erythema, ulcer or exudate b). Inflammatory type 16/29 (55) Nodular or mass-forming 1. Focal nodular mass c). Fibro-stenotic type 7/29 (24) (Figure 3) d). Nodular/mass-forming type 5/29 (17) Downloaded from https://academic.oup.com/jcag/article-abstract/1/4/174/4995069 by Ed 'DeepDyve' Gillespie user on 15 January 2019 Journal of the Canadian Association of Gastroenterology, 2018, Vol. 1, No. 4 177 Figure 1. Figure 1 demonstrates the inflammatory type of PSC stricture. Figure 1A demonstrates an ulcerated and erythematous bile duct with a fibrinous exudate (acute inflammation) whereas Figure 1B shows chronic, smoldering inflammation (chronic inflammation). (SpyGlass Digital™ was used in these cases.) A review of published literature on the role of cholangios- copy for assessment of dominant CBD strictures in PSC clearly suggests that the focus is either on the performance success of the procedure or the ability to detect cholangiocarcinoma in a localized segment (10–12, 25–27). While some studies make no mention of benign strictures, others have described characteristics of inflammatory strictures; although, there has been no ae tt mpt to formally recognize a pae tt rn of phenotypic expression. The ability to differentiate between a dominant benign stricture from a malignant cholangiocarcinoma has been based on visual characteristics, such as stricture length (benign < 1 cm, malignant > 1 cm) and configuration (benign, regular margin; malignant, irregular margin), (12) or simply based on visual abnormalities such as nodularity, ulceration and neo-vascular proliferation (10). However, in our experi- ence, we know that acute inflammatory strictures can be >1 cm long and can appear varyingly irregular depending upon the degree of inflammatory activity ( Figure 1A and B). One study evaluated if cholangioscopy was useful in differentiating benign Figure 2. This demonstrates circumferential fibrotic scars (fibro-stenotic type) with no iden - strictures in PSC from IgG4-sclerosing cholangitis (IgG4-SC) tia fi ble feature of inflammation. (SpyGlass Digital™ was used in this case.) (26). Cholangioscopy was performed in 33 patients, including obvious limitation in interpretation of this data is the het- patients with PSC, IgG4-SC and cholangiocarcinoma. The inci - erogeneity in the patient population and lack of randomized, dence of dilated and tortuous vessels was significantly higher in controlled trials (21). The lifetime incidence of cholangiocar - IgG4-SC patients than in PSC patients (P = 0.02). Scarring and cinoma in patients with PSC is around 20%, with an annual pseudo-diverticula were found significantly more often in PSC incidence of 1.5%–2% (22–24). Once brush cytology is neg- patients than in IgG4-SC patients (P = 0.001 and P = 0.0007, ative or inconclusive, and it will be for most of these patients, respectively). As expected, cholangioscopy ae ft r corticosteroid there is no further therapy suggested to inter vene for a ‘ benign’ therapy showed resolution of bile duct stenosis; dilated, tortu- inflammatory stricture that has ‘flared’, quite like Crohn’s dis - ous or partially enlarged vessels; and resolution of friability in ease, leading to the luminal narrowing. This may be the reason patients with IgG4-SC. Azeem et al. describe the cholangio- why, in a recent review article, experts have alluded to issues scopic appearances of a benign PSC stricture as being narrower, such as a poor understanding of the pathogenesis, the inability more irregular and whiter, when compared with the normal bile to stratif y patients adequately and a lack of therapeutic targets duct. They also describe a fibrotic, circular ‘ring’ which was seen as potential explanations for why there is no effective therapy in 23 patients either above or below a stricture (11). Published available in this chronic disease (8). literature has not stratified these visual characteristics of benign Downloaded from https://academic.oup.com/jcag/article-abstract/1/4/174/4995069 by Ed 'DeepDyve' Gillespie user on 15 January 2019 178 Journal of the Canadian Association of Gastroenterology, 2018, Vol. 1, No. 4 Figure 3. In the third stricture subtype (nodular or mass-forming), note a normal appearing distal bile duct (3A), followed by a more proximal discrete stricture transitioning to an exophytic lesion (3B-D). (SpyGlass Legacy ™ was used in this case.) Figure 4. Proposed algorithm for classification and management of dominant strictures in PSC. The Edmonton Classification. inflammatory strictures into phenotypic categories. Such a phe- also take targeted biopsies of the mucosal abnormality. Our notypic classification system based on cholangioscopy, how - experience with cholangioscopy in patients with PSC under- ever, was precisely the focus of our study. scores the heterogeneity seen in the phenotypic expression of With single operator cholangioscopy, we have the ability to PSC. Akin to Crohn’s disease of the small and large intestine, not only directly visualize the area of interest in the CBD but we believe there are also distinct phenotypes in the expression Downloaded from https://academic.oup.com/jcag/article-abstract/1/4/174/4995069 by Ed 'DeepDyve' Gillespie user on 15 January 2019 Journal of the Canadian Association of Gastroenterology, 2018, Vol. 1, No. 4 179 of mucosal disease in PSC. Cholangioscopic access is limited variations in their clinical spectrum), a cholangioscopy-based to the CBD, common hepatic duct and perhaps the first- and classification scheme can be extremely vital not only in prog - second-degree radicles of the intrahepatic ducts; therefore, nostication but also in ae tt mpts at directing specific therapeu- cholangioscopic interpretation is limited to dominant strictures tic intervention, whether it be pharmacologic or endoscopic. seen within these larger caliber ducts. Our results show that a For now, cholangioscopy is only indicated for the subset of majority of patients (55%) with dominant strictures present patients that exhibit a clinical indication for intervention, such with an acute inflammatory component, resulting in biochem- as a recent elevation in liver biochemistry or a new change in ical or radiographic abnormalities, whereas fibro-stenotic or luminal caliber as seen on surveillance MRCP. Because cholan- mass-forming subtypes occurred at a lower frequency (24% giocarcinoma is a proven consequence of PSC, however small and 17%, respectively). The natural history of these pheno - the incidence may be, cholangioscopy with visual interrogation types and whether there is progression between one subtype to and biopsies of the dominant stricture is of prime importance another is not known. in confirming or excluding this complication. But there is more Antibiotics have been shown to improve symptoms and bio- we can do to proactively intervene in a disease process we know chemistry in some patients with PSC. In a randomized controlled little of and to change the natural history—rather than wait for trial, vancomycin and metronidazole were shown to significantly an undesirable sequela to warrant intervention. alleviate symptoms and improve biochemistry in a cohort of 35 patients with PSC (6). Patients had evidence of intrahepatic CONCLUSION or extrahepatic manifestation of PSC and were not specifically Even though published literature is limited, cholangioscopy and stratified based on any other parameter. Similarly, corticoste- cholangioscopy-guided sampling can be safely and successfully roids were also shown to benefit a subset of patients with PSC, utilized for the assessment of dominant strictures in patients although there seemed to be an overlap of auto-immune hepatitis with PSC. The diagnostic accuracy of cholangioscopy is supe- in this subgroup (5). The explanation for this possible response rior to endoscopic retrograde cholangiography alone for detec- to antibiotics and steroids may lie in the differences in phenotypic tion of malignancy. Also, cholangioscopy has been shown to be expression of the abnormality seen in the CBD. Cholangioscopy useful in differentiating PSC from IgG4-sclerosing cholangitis. with biopsies has now given us the ability to look at the micro- The Edmonton Classification proposed, based on direct chol - scopic architecture of the CBD. It is conceivable that a dominant angioscopy, aims to stratif y patients with dominant extrahepatic stricture with acute inflammation ( Figure 1A) and a predom- biliary strictures in PSC based on differences in phenotypic inantly acute inflammatory infiltrate (comprising neutrophils expression. Validation of this classification in large multicentre and plasma cells) on biopsies may respond bee tt r to antibiotics, cohorts of PSC patients is warranted with the ultimate goal whereas a stricture with chronic inflammation and a lymphocytic of developing a management algorithm based on a composite infiltrate may respond bee tt r to steroids. Similarly, a br fi otic stric - of patient and biochemical characteristics, cholangiographic ture (Figure 2) with little or no inflammatory infiltrate will likely scores, cholangioscopic subtypes and histopathologic grading. not respond to anti-inflammatories. Balloon dilatation would be We now plan to prospectively enroll patients into this pheno- more worthwhile if there is a clinical or biochemical indication typic stratification and study the histological correlation with for intervention. The lack of patient stratification in previous clin- the cholangioscopic abnormality, hopefully soliciting multi- ical trials may possibly explain the variable response seen with centre involvement. It is time that a consortium of PSC experts either antibiotics or corticosteroids. pool resources and actively seek intervention for a disease pro- We recognize that there are inherent drawbacks with the cess that is poorly understood and has suboptimal treatment design of our study. This is a retrospective review of a sin- options. gle-centre, single-endoscopist experience in a disease process that has not been studied or described in this manner before. At our centre, it is not standard practice to record all procedures, ACKNOWLEDGEMENTS and therefore, a second review was not possible. Moreover, GS conceived the idea, co-wrote, reviewed and edited the manuscript. there is no agreed-upon published consensus on the visual PD co-wrote, reviewed and edited the manuscript. BH reviewed characteristics of inflammatory strictures seen in the bile duct. and edited the manuscript. AML co-wrote, reviewed and edited the Nonetheless, what we propose is a novel classification scheme to manuscript. stratify patients with PSC presenting with dominant strictures. Conflicts of Interest: GS is a Consultant for Boston Scientific Not all PSC patients require cholangioscopic investigation, as a Corporation and has received honoraria for speaking and proctoring significant proportion are symptomatically and biochemically engagements. However, no funding was received for the purposes of quiescent. However, although we recognize the inherent diffi - this study. 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