American Society for Gastrointestinal Endoscopy guideline on the role of endoscopy in the diagnosis of malignancy in biliary strictures of undetermined etiology: summary and recommendations

This clinical practice guideline from the American Society for Gastrointestinal Endoscopy provides an evidence-based approach for the diagnosis of malignancy in patients with biliary strictures of undetermined etiology. This document was developed using the Grading of Recommendations Assessment, Development and Evaluation framework and addresses the role of fluoroscopic-guided biopsy sampling, brush cytology, cholangioscopy, and EUS in the diagnosis of malignancy in patients with biliary strictures. In the endoscopic workup of these patients, we suggest the use of fluoroscopic-guided biopsy sampling in addition to brush cytology over brush cytology alone, especially for hilar strictures. We suggest the use of cholangioscopic and EUS-guided biopsy sampling especially for patients who undergo nondiagnostic sampling, cholangioscopic biopsy sampling for nondistal strictures and EUS-guided biopsy sampling distal strictures or those with suspected spread to surrounding lymph nodes and other structures. This clinical practice guideline from the American Society for Gastrointestinal Endoscopy provides an evidence-based approach for the diagnosis of malignancy in patients with biliary strictures of undetermined etiology. This document was developed using the Grading of Recommendations Assessment, Development and Evaluation framework and addresses the role of fluoroscopic-guided biopsy sampling, brush cytology, cholangioscopy, and EUS in the diagnosis of malignancy in patients with biliary strictures. In the endoscopic workup of these patients, we suggest the use of fluoroscopic-guided biopsy sampling in addition to brush cytology over brush cytology alone, especially for hilar strictures. We suggest the use of cholangioscopic and EUS-guided biopsy sampling especially for patients who undergo nondiagnostic sampling, cholangioscopic biopsy sampling for nondistal strictures and EUS-guided biopsy sampling distal strictures or those with suspected spread to surrounding lymph nodes and other structures. This guideline document was prepared by the Standards of Practice Committee of the American Society for Gastrointestinal Endoscopy using the best available scientific evidence and considering a multitude of variables including but not limited to adverse events, patient values, and cost implications. The purpose of these guidelines is to provide the best practice recommendations that may help standardize patient care, improve patient outcomes, and reduce variability in practice. We recognize that clinical decision-making is complex. Guidelines, therefore, are not a substitute for a clinician's judgment. Such judgements may at times seem contradictory to our guidance because of many factors that are impossible to fully consider by guideline developers. Any clinical decisions should be based on the clinician's experience, local expertise, resource availability, and patient values and preferences. This document is not a rule and should not be construed as establishing a legal standard of care or as encouraging, advocating for, mandating, or discouraging any particular treatment. Our guidelines should not be used in support of medical complaints, legal proceedings, and/or litigation, as they were not designed for this purpose. Cholangiocarcinoma is a rare malignancy with an approximate incidence of 8000 cases per year in the United States,1American Cancer Society. Key statistics for bile duct cancer. Available at: https://www.cancer.org/cancer/bile-duct-cancer/about/key-statistics.html. Accessed March 11, 2022.Google Scholar although it is increasing in frequency.2Castro F.A. Koshiol J. Hsing A.W. et al.Biliary tract cancer incidence in the United States-Demographic and temporal variations by anatomic site.Int J Cancer. 2013; 133: 1664-1671Crossref PubMed Scopus (78) Google Scholar,3Banales J.M. Marin J.J.G. Lamarca A. et al.Cholangiocarcinoma 2020: the next horizon in mechanisms and management.Nat Rev Gastroenterol Hepatol. 2020; 17: 557-588Crossref PubMed Scopus (1162) Google Scholar The prognosis of cholangiocarcinoma is poor, with an overall 5-year survival rate of about 10%; however, diagnosis at an earlier stage results in a higher likelihood of survival.1American Cancer Society. Key statistics for bile duct cancer. Available at: https://www.cancer.org/cancer/bile-duct-cancer/about/key-statistics.html. Accessed March 11, 2022.Google Scholar Therefore, it is important to diagnose malignancy as soon as possible when patients present with biliary strictures. Patients presenting with biliary strictures of undetermined etiology often pose a diagnostic challenge. It is estimated that the risk of malignancy in patients with a biliary stricture without an obvious mass on cross-sectional imaging is approximately 55%.4Burnett A.S. Calvert T.J. Chokshi R.J. Sensitivity of endoscopic retrograde cholangiopancreatography standard cytology: 10-y review of the literature.J Surg Res. 2013; 184: 304-311Abstract Full Text Full Text PDF PubMed Scopus (89) Google Scholar Benign etiologies of biliary strictures associated with diseases include primary sclerosing cholangitis, IgG subclass 4–related sclerosing cholangitis, fibrotic strictures, and chronic pancreatitis. The appearance of a benign biliary stricture on cross-sectional imaging often mimics the appearance of a malignant biliary stricture. Thus, tissue acquisition is required to distinguish malignant and benign biliary strictures. Diagnostic modalities for biliary strictures are limited; however, endoscopic approaches are preferred over percutaneous sampling approaches, which require an external drain and risk needle-track seeding, or surgical approaches. Tissue acquisition in biliary strictures relies heavily on endoscopic techniques such as ERCP with brush cytology, intraductal biopsy sampling, cholangioscopy, or EUS with FNA or fine-needle biopsy sampling (FNB). However, these techniques have limitations, particularly low sensitivity for the diagnosis of malignancy and needle-track seeding in the setting of EUS-guided FNA of hilar strictures.5Heimbach J.K. Sanchez W. Rosen C.B. et al.Trans-peritoneal fine needle aspiration biopsy of hilar cholangiocarcinoma is associated with disease dissemination.HPB. 2011; 13: 356-360Abstract Full Text Full Text PDF Scopus (192) Google Scholar The diagnosis of malignancy in biliary strictures often requires multiple procedures, resulting in increased cost and patient anxiety as well as delays in diagnosis and potential curative treatment. Therefore, the aim of this guideline is to provide evidence-based recommendations for the endoscopic approach to undetermined biliary strictures. This document was prepared by the Standards of Practice Committee of the American Society for Gastrointestinal Endoscopy (ASGE) and was conceptualized and conducted according to the Grading of Recommendations Assessment, Development and Evaluation framework.6Jackson R. Feder G. Guidelines for clinical guidelines.BMJ. 1998; 317: 427-428Crossref PubMed Scopus (179) Google Scholar, 7Wani S. Sultan S. Qumseya B. et al.The ASGE's vision for developing clinical practice guidelines: the path forward.Gastrointest Endosc. 2018; 87: 932-933Abstract Full Text Full Text PDF PubMed Scopus (15) Google Scholar, 8Guyatt G.H. Oxman A.D. Vist G.E. et al.GRADE: an emerging consensus on rating quality of evidence and strength of recommendations.BMJ. 2008; 336: 924-926Crossref PubMed Google Scholar Evidence was presented to a panel of experts representing various stakeholders, including a surgical oncologist, medical oncologist, and interventional radiologist. A patient advocate was also included. All panel members were required to disclose potential financial and intellectual conflicts of interest, which were addressed according to ASGE policies. In developing these recommendations, we took into consideration the certainty of the evidence, benefits, and harms of different management options, feasibility, patient values and preferences, resource utilization, cost-effectiveness, and health equity. The final wording of the recommendations, including direction and strength, were approved by all members of the panel and the ASGE governing board. Stronger recommendations are typically stated as "we recommend…," whereas weaker recommendations are indicated by phrases such as "we suggest…." These guidelines addressed the following 3 clinical questions using the Grading of Recommendations Assessment, Development and Evaluation format:1.In patients with undetermined biliary strictures, should ERCP with fluoroscopic-guided biopsy sampling be performed versus ERCP with brush cytology to diagnose malignancy?2.In patients with undetermined biliary strictures, should ERCP with cholangioscopic-guided biopsy sampling be performed versus ERCP without cholangioscopy to diagnose malignancy?3.In patients with undetermined biliary strictures, should EUS with FNA/FNB be performed versus ERCP with any form of tissue acquisition to diagnose malignancy? Indeterminate biliary strictures historically have been defined as a stricture in which prior ERCP had inconclusive cytology results. However, this guideline used the term undetermined biliary strictures rather than indeterminate biliary strictures because that term enabled the inclusion of studies of patients undergoing their first ERCP without a prior negative brush cytology. It is important to make this distinction to emphasize the importance of other forms of tissue acquisition that can be used in addition to brush cytology in the initial diagnostic workup of biliary strictures suspected to have underlying malignancy. Relevant clinical outcomes were incremental yield, diagnostic test characteristics (sensitivity, specificity, positive predictive value, and negative predictive value), technical success, specimen adequacy, and adverse events. Technical success was defined as the percentage of cases where the endoscopist was able to perform the desired tissue sampling, whereas specimen adequacy was defined as a pathologic diagnosis with enough cellular components to make a determination of malignant or benign. Details of our literature searches, data analyses, pooled-effects estimates, evidence profiles, forest plots, and panel deliberations for each outcome can be found in the accompany article subtitled "Methodology and Review of Evidence." A summary of our final recommendations is listed in Table 1.Question 1: In patients with biliary strictures of undetermined etiology, should ERCP with fluoroscopic-guided biopsy sampling be performed in addition to brush cytology versus ERCP with brush cytology alone to diagnose malignancy?Recommendation 1. In patients with biliary strictures of undetermined etiology undergoing ERCP, the ASGE suggests the addition of fluoroscopic-guided biopsy sampling with brush cytology versus brush cytology alone to diagnose malignancy.(Conditional recommendation/very low quality of evidence)Table 1Summary of recommendationsQuestionRecommendationQuality of evidenceGeneral concepts1In patients with biliary strictures of undetermined etiology undergoing ERCP, the ASGE suggests the addition of fluoroscopic-guided biopsy sampling with brush cytology versus brush cytology alone to diagnose malignancy.Conditional recommendation, very low quality of evidence•Review all cross-sectional imaging.•Discuss patient in a multidisciplinary board or committee.2In patients with biliary strictures of undetermined etiology undergoing ERCP, the ASGE suggests the use of cholangioscopic-guided biopsy sampling in A, Nondistal biliary strictures where there is a high probability of adequate drainage of the critical liver segment or B, Previous nondiagnostic ERCP without cholangioscopy, and C, Centers with clinical expertise and easy access to the equipment.Otherwise, the ASGE suggests ERCP with or without cholangioscopy in the diagnosis of malignancy.Conditional recommendation, very low quality of evidence•Discuss results with dedicated GI pathologist.•Ensure careful alignment and advancement of forceps into the common bile duct under fluoroscopic guidance.3In patients with biliary strictures of undetermined etiology undergoing ERCP, the ASGE suggests EUS in addition to ERCP for the diagnosis of malignancy in the presence of A, Prior ERCP with nondiagnostic ERCP results,B, Distal biliary stricture, or C, Presence of lymphadenopathy or metastatic disease on cross-sectional imaging,Conditional recommendation, very low quality of evidence•Upfront EUS should be considered in centers with the ability to do EUS and ERCP in the same session.•If EUS is performed in the setting of hilar strictures, it is important for the endoscopist to avoid biopsy sampling of the biliary mass itself.ASGE, American Society for Gastrointestinal Endoscopy. Open table in a new tab Question 1: In patients with biliary strictures of undetermined etiology, should ERCP with fluoroscopic-guided biopsy sampling be performed in addition to brush cytology versus ERCP with brush cytology alone to diagnose malignancy? Recommendation 1. In patients with biliary strictures of undetermined etiology undergoing ERCP, the ASGE suggests the addition of fluoroscopic-guided biopsy sampling with brush cytology versus brush cytology alone to diagnose malignancy. (Conditional recommendation/very low quality of evidence) ASGE, American Society for Gastrointestinal Endoscopy. A de novo systematic review and meta-analysis identified 21 observational studies (20 full text, 1 abstract) with 2726 patients that compared ERCP with fluoroscopic-guided biopsy sampling in combination with brush cytology versus brush cytology alone.9Draganov P.V. Chauhan S. Wagh M.S. et al.Diagnostic accuracy of conventional and cholangioscopy-guided sampling of indeterminate biliary lesions at the time of ERCP: a prospective, long-term follow-up study.Gastrointest Endosc. 2012; 75: 347-353Abstract Full Text Full Text PDF PubMed Scopus (196) Google Scholar, 10Han S. Tatman P. Mehrotra S. et al.Combination of ERCP-based modalities increases diagnostic yield for biliary strictures.Dig Dis Sci. 2021; 66: 1276-1284Crossref PubMed Scopus (10) Google Scholar, 11Hormati A. Jafari S. Jabbari A. et al.Comparison between brush cytology and forceps biopsy under fluoroscopic guidance for the diagnosis of proximal cholangiocarcinoma.Middle East J Dig Dis. 2020; 12: 246-251PubMed Google Scholar, 12Howell D.A. Parsons W.G. Jones M.A. et al.Complete tissue sampling of biliary strictures at ERCP using a new device.Gastrointest Endosc. 1996; 43: 498-502Abstract Full Text Full Text PDF PubMed Google Scholar, 13Jailwala J. Fogel E.L. Sherman S. et al.Triple-tissue sampling at ERCP in malignant biliary obstruction.Gastrointest Endosc. 2000; 51: 383-390Abstract Full Text Full Text PDF PubMed Scopus (301) Google Scholar, 14Kaura K. Sawas T. Bazerbachi F. et al.Cholangioscopy biopsies improve detection of cholangiocarcinoma when combined with cytology and FISH, but not in patients with PSC.Dig Dis Sci. 2020; 65: 1471-1478Crossref PubMed Scopus (24) Google Scholar, 15Kitajima Y. Ohara H. Nakazawa T. et al.Usefulness of transpapillary bile duct brushing cytology and forceps biopsy for improved diagnosis in patients with biliary strictures.J Gastroenterol Hepatol. 2007; 22: 1615-1620Crossref PubMed Scopus (86) Google Scholar, 16Kulaksiz H. Strnad P. Römpp A. et al.A novel method of forceps biopsy improves the diagnosis of proximal biliary malignancies.Dig Dis Sci. 2011; 56: 596-601Crossref PubMed Scopus (14) Google Scholar, 17Moura D.T.H. de Moura E.G.H. Matuguma S.E. et al.EUS-FNA versus ERCP for tissue diagnosis of suspect malignant biliary strictures: a prospective comparative study.Endosc Int Open. 2018; 6: E769-E777Crossref PubMed Google Scholar, 18Naitoh I. Nakazawa T. Kato A. et al.Predictive factors for positive diagnosis of malignant biliary strictures by transpapillary brush cytology and forceps biopsy.J Dig Dis. 2016; 17: 44-51Crossref PubMed Scopus (43) Google Scholar, 19Ponchon T. Gagnon P. Berger F. et al.Value of endobiliary brush cytology and biopsies for the diagnosis of malignant bile duct stenosis: results of a prospective study.Gastrointest Endosc. 1995; 42: 565-572Abstract Full Text Full Text PDF PubMed Scopus (337) Google Scholar, 20Pugliese V. Antonelli G. Vincenti M. et al.Endoductal tissue sampling of biliary strictures through endoscopic retrograde cholangiopancreatography (ERCP).Tumori. 1997; 83: 698-702Crossref PubMed Scopus (8) Google Scholar, 21Pugliese V. Barone D. Saccomanno S. et al.Tissue sampling from the common bile duct through endoscopic retrograde cholangiopancreatography, endoscopic papillo(sphinctero)tomy and drainage in juxtapapillary malignancies.Surg Endosc. 1987; 1: 83-87Crossref PubMed Scopus (24) Google Scholar, 22Ren Y.C. Huang C.L. Chen S.M. et al.Dilation catheter-guided mini-forceps biopsy improves the diagnostic accuracy of malignant biliary strictures.Endoscopy. 2018; 50: 809-812Crossref PubMed Scopus (6) Google Scholar, 23Rösch T. Hofrichter K. Frimberger E. et al.ERCP or EUS for tissue diagnosis of biliary strictures? A prospective comparative study.Gastrointest Endosc. 2004; 60: 390-396Abstract Full Text Full Text PDF PubMed Scopus (281) Google Scholar, 24Sakuma Y. Kodama Y. Sogabe Y. et al.Diagnostic performance of a new endoscopic scraper for malignant biliary strictures: a multicenter prospective study.Gastrointest Endosc. 2017; 85: 371-379Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar, 25Salomao M. Gonda T.A. Margolskee E. et al.Strategies for improving diagnostic accuracy of biliary strictures.Cancer Cytopathol. 2015; 123: 244-252Crossref PubMed Scopus (31) Google Scholar, 26Schoefl R. Haefner M. Wrba F. et al.Forceps biopsy and brush cytology during endoscopic retrograde cholangiopancreatography for the diagnosis of biliary stenoses.Scand J Gastroenterol. 1997; 32: 363-368Crossref PubMed Scopus (168) Google Scholar, 27Sugiyama M. Atomi Y. Wada N. et al.Endoscopic transpapillary bile duct biopsy without sphincterotomy for diagnosing biliary strictures: a prospective comparative study with bile and brush cytology.Am J Gastroenterol. 1996; 91: 465-467PubMed Google Scholar, 28Weber A. von Weyhern C. Fend F. et al.Endoscopic transpapillary brush cytology and forceps biopsy in patients with hilar cholangiocarcinoma.World J Gastroenterol. 2008; 14: 1097-1101Crossref PubMed Scopus (115) Google Scholar, 29Yang X. Guo J.F. Sun L.Q. et al.Assessment of different modalities for repeated tissue acquisition in diagnosing malignant biliary strictures: a two-center retrospective study.J Dig Dis. 2021; 22: 102-107Crossref PubMed Scopus (4) Google Scholar The incremental yield of intraductal biopsy sampling with brush cytology over brush cytology alone was 20% (95% confidence interval [CI], 9-31; I2 = 54.5%) in diagnosing malignancy.13Jailwala J. Fogel E.L. Sherman S. et al.Triple-tissue sampling at ERCP in malignant biliary obstruction.Gastrointest Endosc. 2000; 51: 383-390Abstract Full Text Full Text PDF PubMed Scopus (301) Google Scholar,15Kitajima Y. Ohara H. Nakazawa T. et al.Usefulness of transpapillary bile duct brushing cytology and forceps biopsy for improved diagnosis in patients with biliary strictures.J Gastroenterol Hepatol. 2007; 22: 1615-1620Crossref PubMed Scopus (86) Google Scholar,16Kulaksiz H. Strnad P. Römpp A. et al.A novel method of forceps biopsy improves the diagnosis of proximal biliary malignancies.Dig Dis Sci. 2011; 56: 596-601Crossref PubMed Scopus (14) Google Scholar,20Pugliese V. Antonelli G. Vincenti M. et al.Endoductal tissue sampling of biliary strictures through endoscopic retrograde cholangiopancreatography (ERCP).Tumori. 1997; 83: 698-702Crossref PubMed Scopus (8) Google Scholar,22Ren Y.C. Huang C.L. Chen S.M. et al.Dilation catheter-guided mini-forceps biopsy improves the diagnostic accuracy of malignant biliary strictures.Endoscopy. 2018; 50: 809-812Crossref PubMed Scopus (6) Google Scholar,23Rösch T. Hofrichter K. Frimberger E. et al.ERCP or EUS for tissue diagnosis of biliary strictures? A prospective comparative study.Gastrointest Endosc. 2004; 60: 390-396Abstract Full Text Full Text PDF PubMed Scopus (281) Google Scholar,28Weber A. von Weyhern C. Fend F. et al.Endoscopic transpapillary brush cytology and forceps biopsy in patients with hilar cholangiocarcinoma.World J Gastroenterol. 2008; 14: 1097-1101Crossref PubMed Scopus (115) Google Scholar The miss rate of brush cytology alone was 58% (95% CI, 46-71; I2 = 79.5%) in diagnosing malignancy, whereas the miss rate of biopsy sampling alone was 41% (95% CI, 31-52; I2 = 80.3%).9Draganov P.V. Chauhan S. Wagh M.S. et al.Diagnostic accuracy of conventional and cholangioscopy-guided sampling of indeterminate biliary lesions at the time of ERCP: a prospective, long-term follow-up study.Gastrointest Endosc. 2012; 75: 347-353Abstract Full Text Full Text PDF PubMed Scopus (196) Google Scholar,13Jailwala J. Fogel E.L. Sherman S. et al.Triple-tissue sampling at ERCP in malignant biliary obstruction.Gastrointest Endosc. 2000; 51: 383-390Abstract Full Text Full Text PDF PubMed Scopus (301) Google Scholar,15Kitajima Y. Ohara H. Nakazawa T. et al.Usefulness of transpapillary bile duct brushing cytology and forceps biopsy for improved diagnosis in patients with biliary strictures.J Gastroenterol Hepatol. 2007; 22: 1615-1620Crossref PubMed Scopus (86) Google Scholar,20Pugliese V. Antonelli G. Vincenti M. et al.Endoductal tissue sampling of biliary strictures through endoscopic retrograde cholangiopancreatography (ERCP).Tumori. 1997; 83: 698-702Crossref PubMed Scopus (8) Google Scholar,23Rösch T. Hofrichter K. Frimberger E. et al.ERCP or EUS for tissue diagnosis of biliary strictures? A prospective comparative study.Gastrointest Endosc. 2004; 60: 390-396Abstract Full Text Full Text PDF PubMed Scopus (281) Google Scholar,28Weber A. von Weyhern C. Fend F. et al.Endoscopic transpapillary brush cytology and forceps biopsy in patients with hilar cholangiocarcinoma.World J Gastroenterol. 2008; 14: 1097-1101Crossref PubMed Scopus (115) Google Scholar,30Gerges C. Beyna T. Tang R.S.Y. et al.Digital single-operator peroral cholangioscopy-guided biopsy sampling versus ERCP-guided brushing for indeterminate biliary strictures: a prospective, randomized, multicenter trial (with video).Gastrointest Endosc. 2020; 91: 1105-1113Abstract Full Text Full Text PDF PubMed Scopus (86) Google Scholar The sensitivity of brush cytology alone was .4 (95% CI, .37-.43; I2 = 69.5%).9Draganov P.V. Chauhan S. Wagh M.S. et al.Diagnostic accuracy of conventional and cholangioscopy-guided sampling of indeterminate biliary lesions at the time of ERCP: a prospective, long-term follow-up study.Gastrointest Endosc. 2012; 75: 347-353Abstract Full Text Full Text PDF PubMed Scopus (196) Google Scholar,10Han S. Tatman P. Mehrotra S. et al.Combination of ERCP-based modalities increases diagnostic yield for biliary strictures.Dig Dis Sci. 2021; 66: 1276-1284Crossref PubMed Scopus (10) Google Scholar,12Howell D.A. Parsons W.G. Jones M.A. et al.Complete tissue sampling of biliary strictures at ERCP using a new device.Gastrointest Endosc. 1996; 43: 498-502Abstract Full Text Full Text PDF PubMed Google Scholar, 13Jailwala J. Fogel E.L. Sherman S. et al.Triple-tissue sampling at ERCP in malignant biliary obstruction.Gastrointest Endosc. 2000; 51: 383-390Abstract Full Text Full Text PDF PubMed Scopus (301) Google Scholar, 14Kaura K. Sawas T. Bazerbachi F. et al.Cholangioscopy biopsies improve detection of cholangiocarcinoma when combined with cytology and FISH, but not in patients with PSC.Dig Dis Sci. 2020; 65: 1471-1478Crossref PubMed Scopus (24) Google Scholar, 15Kitajima Y. Ohara H. Nakazawa T. et al.Usefulness of transpapillary bile duct brushing cytology and forceps biopsy for improved diagnosis in patients with biliary strictures.J Gastroenterol Hepatol. 2007; 22: 1615-1620Crossref PubMed Scopus (86) Google Scholar, 16Kulaksiz H. Strnad P. Römpp A. et al.A novel method of forceps biopsy improves the diagnosis of proximal biliary malignancies.Dig Dis Sci. 2011; 56: 596-601Crossref PubMed Scopus (14) Google Scholar, 17Moura D.T.H. de Moura E.G.H. Matuguma S.E. et al.EUS-FNA versus ERCP for tissue diagnosis of suspect malignant biliary strictures: a prospective comparative study.Endosc Int Open. 2018; 6: E769-E777Crossref PubMed Google Scholar, 18Naitoh I. Nakazawa T. Kato A. et al.Predictive factors for positive diagnosis of malignant biliary strictures by transpapillary brush cytology and forceps biopsy.J Dig Dis. 2016; 17: 44-51Crossref PubMed Scopus (43) Google Scholar, 19Ponchon T. Gagnon P. Berger F. et al.Value of endobiliary brush cytology and biopsies for the diagnosis of malignant bile duct stenosis: results of a prospective study.Gastrointest Endosc. 1995; 42: 565-572Abstract Full Text Full Text PDF PubMed Scopus (337) Google Scholar, 20Pugliese V. Antonelli G. Vincenti M. et al.Endoductal tissue sampling of biliary strictures through endoscopic retrograde cholangiopancreatography (ERCP).Tumori. 1997; 83: 698-702Crossref PubMed Scopus (8) Google Scholar,25Salomao M. Gonda T.A. Margolskee E. et al.Strategies for improving diagnostic accuracy of biliary strictures.Cancer Cytopathol. 2015; 123: 244-252Crossref PubMed Scopus (31) Google Scholar, 26Schoefl R. Haefner M. Wrba F. et al.Forceps biopsy and brush cytology during endoscopic retrograde cholangiopancreatography for the diagnosis of biliary stenoses.Scand J Gastroenterol. 1997; 32: 363-368Crossref PubMed Scopus (168) Google Scholar, 27Sugiyama M. Atomi Y. Wada N. et al.Endoscopic transpapillary bile duct biopsy without sphincterotomy for diagnosing biliary strictures: a prospective comparative study with bile and brush cytology.Am J Gastroenterol. 1996; 91: 465-467PubMed Google Scholar,29Yang X. Guo J.F. Sun L.Q. et al.Assessment of different modalities for repeated tissue acquisition in diagnosing malignant biliary strictures: a two-center retrospective study.J Dig Dis. 2021; 22: 102-107Crossref PubMed Scopus (4) Google Scholar,31Reis D.N.F. Freitas C. Marques A. et al.Biopsies in combination with brush cytology can improve the characterization of malignant biliary strictures during ERCP.United Eur Gastroenterol J. 2018; 6: A609Google Scholar The sensitivity of fluoroscopic-guided biopsy sampling was significantly higher at .52 (95% CI, .49-.56; I2 = 79.4%; P = .006), as was the sensitivity of fluoroscopic-guided biopsy sampling in combination with brush cytology at .66 (95% CI, .63-.69; I2 = 48.4%; P < .001)9Draganov P.V. Chauhan S. Wagh M.S. et al.Diagnostic accuracy of conventional and cholangioscopy-guided sampling of indeterminate biliary lesions at the time of ERCP: a prospective, long-term follow-up study.Gastrointest Endosc. 2012; 75: 347-353Abstract Full Text Full Text PDF PubMed Scopus (196) Google Scholar, 10Han S. Tatman P. Mehrotra S. et al.Combination of ERCP-based modalities increases diagnostic yield for biliary strictures.Dig Dis Sci. 2021; 66: 1276-1284Crossref PubMed Scopus (10) Google Scholar, 11Hormati A. Jafari S. Jabbari A. et al.Comparison between brush cytology and forceps biopsy under fluoroscopic guidance for the diagnosis of proximal cholangiocarcinoma.Middle East J Dig Dis. 2020; 12: 246-251PubMed Google Scholar, 12Howell D.A. Parsons W.G. Jones M.A. et al.Complete tissue sampling of biliary strictures at ERCP using a new device.Gastrointest Endosc. 1996; 43: 498-502Abstract Full Text Full Text PDF PubMed Google Scholar, 13Jailwala J. Fogel E.L. Sherman S. et al.Triple-tissue sampling at ERCP in malignant biliary obstruction.Gastrointest Endosc. 2000; 51: 383-390Abstract Full Text Full Text PDF PubMed Scopus (301) Google Scholar,15Kitajima Y. Ohara H. Nakazawa T. et al.Usefulness of transpapillary bile duct brushing cytology and forceps biopsy for improved diagnosis in patients with biliary strictures.J Gastroenterol Hepatol. 2007; 22: 1615-1620Crossref PubMed Scopus (86) Google Scholar, 16Kulaksiz H. Strnad P. Römpp A. et al.A novel method of forceps biopsy improves the diagnosis of proximal biliary malignancies.Dig Dis Sci. 2011; 56: 596-601Crossref PubMed Scopus (14) Google Scholar, 17Moura D.T.H. de Moura E.G.H. Matuguma S.E. et al.EUS-FNA versus ERCP for tissue diagnosis of suspect malignant biliary strictures: a prospective comparative study.Endosc Int Open. 2018; 6: E769-E777Crossref PubMed Google Scholar, 18Naitoh I. Nakazawa T. Kato A. et al.Predictive factors for positive diagnosis of malignant biliary strictures by transpapillary brush cytology and forceps biopsy.J Dig Dis. 2016; 17: 44-51Crossref PubMed Scopus (43) Google Scholar, 19Ponchon T. Gagnon P. Berger F. et al.Value of endobiliary brush cytology and biopsies for the diagnosis of malignant bile duct stenosis: results of a prospective study.Gastrointest Endosc. 1995; 42: 565-572Abstract Full Text Full Text PDF PubMed Scopus (337) Google Scholar, 20Pugliese V. Antonelli G. Vincenti M. et al.Endoductal tissue sampling of biliary strictures through endoscopic retrograde cholangiopancreatography (ERCP).Tumori. 1997; 83: 698-702Crossref PubMed Scopus (8) Google Scholar,22Ren Y.C. Huang C.L. Chen S.M. et al.Dilation catheter-guided mini-forceps biopsy improves the diagnostic accuracy of malignant biliary strictures.Endoscopy. 2018; 50: 809-812Crossref PubMed Scopus (6) Google Scholar,24Sakuma Y. Kodama Y. Sogabe Y. et al.Diagnostic performance of a new endoscopic scraper for malignant biliary strictures: a multicenter prospective study.Gastrointest Endosc. 2017; 85: 371-379Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar, 25Salomao M. Gonda T.A. Margolskee E. et al.Strategies for improving diagnostic accuracy of biliary strictures.Cancer Cytopathol. 2015; 123: 244-252Crossref PubMed Scopus (31) Google Scholar, 26Schoefl