The role of fluorescence in situ hybridization in primary diagnosis of distal biliary strictures
Vincent Dansou Zoundjiekpon1, Přemysl Falt Orcid.org 1,2, Jana Zapletalová Orcid.org 3, Daniela Kurfürstová4, Martin Loveček Orcid.org 5, Lumír Kunovský6, Zuzana Slobodová4, Daniela Skanderová4, Gabriela Kořínková4, Pavel Skalický5, Ondřej Urban1, Peter Slodička1, Tomáš Tichý1
+ Affiliation
Summary
Background and aim: Primary diagnosis of the distal biliary stricture can be sometime difficult. Brush cytology (BC) is known to have low diagnostic sensitivity in these cases. Fluorescence in situ hybridization (FISH) has been reported as a useful adjunctive test in patients with biliary strictures. We aimed to determine performance characteristics of BC, FISH and their combination (BC + FISH) in the primary diagnosis of distal biliary strictures. Methods: This single-center prospective study was conducted between April 2019 and January 2021. Consecutive patients with unsampled biliary strictures undergoing first ERCP in our institution were included. Cytological and FISH analysis of tissue specimens from two standardized transpapillary brushings from the distal strictures were provided. Histopathological confirmation after surgery or 12-month follow-up was regarded as the reference standard for the final diagnosis. Results: A total of 109 patients were enrolled. Seven patients were lost from the final analysis and 26 suffered proximal stenosis. Of the 76 remaining patients (61.8% males, mean age 67.6, range 25–89 years) with distal stenosis, the proportions of benign and malignant strictures were 25 (32.9%) and 51 (67.1%), respectively. Of the subgroup of malignant strictures, 17.7% were cholangiocarcinoma, 74.5% were pancreatic tumors and 7.8% others. In comparison to BC alone, FISH increased the sensitivity from 0.373% to 0.706% (p = 0.0007) with a slight decrease in specificity (p = 0.045). Conclusions: Dual modality tissue evaluation using BC + FISH has better sensitivity for the primary diagnosis of distal biliary strictures, compared to BC alone.
Keywords
primary diagnosis of distal biliary strictures, first retrograde cholangiopancreatography, brush cytology, fluorescence in situ hybridizationTo read this article in full, please register for free on this website.
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Literature
1. Pouw RE, Barret M, Biermann K et al. Endoscopic tissue sampling – Part 1: Upper gastrointestinal and hepatopancreatobiliary tracts. European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2021; 53(11): 1174–1188. doi: 10.1055/a-1611-5091.
2. Victor DW, Sherman S, Karakan T et al. Current endoscopic approach to indeterminate biliary strictures. World J Gastroenterol 2012; 18(43): 6197–6205. doi: 10.3748/wjg.v18.i43.6197.
3. Shaib YH, Davila JA, McGlynn K et al. Rising incidence of intrahepatic cholangiocarcinoma in the United States: A true increase? J Hepatol 2004; 40(3): 472–477. doi: 10.1016/ j.jhep.2003.11.030.
4. Urban O, Vanek P, Zoundjiekpon V et al. Endoscopic Perspective in Cholangiocarcinoma Diagnostic Process. Gastroenterol Res Pract 2019; 2019: 9704870. doi: 10.1155/2019/9704870.
5. Van Beers BE. Diagnosis of cholangiocarcinoma. HPB (Oxford) 2008; 10(2): 87–93. doi: 10.1080/13651820801992716.
6. Singh A, Gelrud A, Agarwal B. Biliary strictures: diagnostic considerations and approach. Gastroenterol Rep (Oxf) 2015; 3(1): 22–31. doi: 10.1093/gastro/gou072.
7. Sun B, Moon JH, Cai Q et al. Review article: Asia-Pacific consensus recommendations on endoscopic tissue acquisition for biliary strictures. Aliment Pharmacol Ther 2018; 48(2): 138–151. doi: 10.1111/apt.14811.
8. Dumonceau JM, Delhaye M, Charette N et al. Challenging biliary strictures: Pathophysiological features, differential diagnosis, diagnostic algorithms, and new clinically relevant biomarkers – Part 1. Therap Adv Gastroenterol 2020; 13: 1756284820927292. doi: 10.1177/1756284820927292.
9. Rösch T, Hofrichter K, Frimberger E et al. ERCP or EUS for tissue diagnosis of biliary strictures? A prospective comparative study. Gastrointest Endosc 2004; 60(3): 390–396. doi: 10.1016/s0016-5107(04)01732-8.
10. Moreno Luna LE, Kipp B, Halling KC et al. Advanced cytologic techniques for the detection of malignant pancreatobiliary strictures. Gastroenterology 2006; 131(4): 1064–1072. doi: 10.1053/j.gastro.2006.08.021.
11. Meining A, Chen YK, Pleskow D et al. Direct visualization of indeterminate pancreaticobiliary strictures with probe-based confocal laser endomicroscopy: A multicenter experience. Gastrointest Endosc 2011; 74(5): 961–968. doi: 10.1016/j.gie.2011.05.009.
12. Sun X, Zhou Z, Tian J et al. Is single-operator peroral cholangioscopy a useful tool for the diagnosis of indeterminate biliary lesion? A systematic review and meta-analysis. Gastrointest Endosc 2015; 82(1): 79–87. doi: 10.1016/j.gie.2014.12.021.
13. Sethi A, Tyberg A, Slivka A et al. Digital Single-operator Cholangioscopy (DSOC) Improves Interobserver Agreement (IOA) and Accuracy for Evaluation of Indeterminate Biliary Strictures: The Monaco Classification. J Clin Gastroenterol 2022; 56(2): e94–e97. doi: 10.1097/MCG.0000000000001321.
14. Navaneethan U, Hasan MK, Kommaraju K et al. Digital, single-operator cholangiopancreatoscopy in the diagnosis and management of pancreatobiliary disorders: A multicenter clinical experience (with video). Gastrointest Endosc. 2016; 84(4): 649–655. doi: 10.1016/j.gie.2016.03.789.
15. Shah RJ, Raijman I, Brauer B et al. Performance of a fully disposable, digital, single-operator cholangiopancreatoscope. Endoscopy 2017; 49(7): 651–658. doi: 10.1055/s-0043-106295.
16. Urban O, Evinová E, Fojtík P et al. Digital cholangioscopy: The diagnostic yield and impact on management of patients with biliary stricture. Scand J Gastroenterol 2018; 53(10–11): 1364–1367. doi: 10.1080/00365521.2018.1512649.
17. Caillol F, Bories E, Poizat F et al. Endomicroscopy in bile duct: Inflammation interferes with pCLE applied in the bile duct: A prospective study of 54 patients. United European Gastroenterol J 2013; 1(2): 120–127. doi: 10.1177/2050640613483462.
18. Levy MJ, Baron TH, Clayton AC et al. Prospective evaluation of advanced molecular markers and imaging techniques in patients with indeterminate bile duct strictures. Am J Gastroenterol 2008; 103(5): 1263–1273. doi: 10.1111/j.1572-0241.2007.01776.x.
19. Gonda TA, Glick MP, Sethi A et al. Polysomy and p16 deletion by fluorescence in situ hybridization in the diagnosis of indeterminate biliary strictures. Gastrointest Endosc 2012; 75(1): 74–79. doi: 10.1016/j.gie.2011.08.022.
20. Bergquist A, Tribukait B, Glaumann H et al. Can DNA cytometry be used for evaluation of malignancy and premalignancy in bile duct strictures in primary sclerosing cholangitis? J Hepatol 2000; 33(6): 873–877. doi: 10.1016/s0168-8278(00)80117-8.
21. Kipp BR, Stadheim LM, Halling SA et al. A comparison of routine cytology and fluorescence in situ hybridization for the detection of malignant bile duct strictures. Am J Gastroenterol 2004; 99(9): 1675–1681. doi: 10.1111/j.1572-0241.2004.30281.x.
22. Vlajnic T, Somaini G, Savic S et al. Targeted multiprobe fluorescence in situ hybridization analysis for elucidation of inconclusive pancreatobiliary cytology. Cancer Cytopathol 2014; 122(8): 627–634. doi: 10.1002/cncy.21429.
23. Barr Fritcher EG, Voss JS, Brankley SM et al. An Optimized Set of Fluorescence In situ Hybridization Probes for Detection of Pancreatobiliary Tract Cancer in Cytology Brush Samples. Gastroenterology 2015; 149(7): 1813.e1–1824.e1. doi: 10.1053/j.gastro.2015.08.046.
24. Chaiteerakij R, Barr Fritcher EG, Angsuwatcharakon P et al. Fluorescence in situ hybridization compared with conventional cytology for the diagnosis of malignant biliary tract strictures in Asian patients. Gastrointest Endosc. 2016; 83(6): 1228–1235. doi: 10.1016/j.gie.2015.11.037.
25. Gonda TA, Viterbo D, Gausman V et al. Mutation Profile and Fluorescence in situ Hybridization Analyses Increase Detection of Malignancies in Biliary Strictures. Clin Gastroenterol Hepatol 2017; 15(6): 913.e1–919.e1. doi: 10.1016/j.cgh.2016.12.013.
26. Pitman MB, Centeno BA, Ali SZ et al. Standardized terminology and nomenclature for pancreatobiliary cytology: The Papanicolaou Society of Cytopathology Guidelines. Cytojournal 2014; 11(1): 3. doi: 10.4103/1742-6413.133343.
27. Liew ZH, Loh TJ, Lim TK et al. Role of fluorescence in situ hybridization in diagnosing cholangiocarcinoma in indeterminate biliary strictures. J Gastroenterol Hepatol 2018; 33(1): 315–319. doi: 10.1111/jgh.13824.
28. Han S, Tatman P, Mehrotra S et al. Combination of ERCP-Based Modalities Increases Diagnostic Yield for Biliary Strictures. Dig Dis Sci 2021; 66(4): 1276–1284. doi: 10.1007/s10 620-020-06335-x.
29. Layfield LJ, Schmidt RL, Hirschowitz SL et al. Significance of the diagnostic categories “atypical” and “suspicious for malignancy” in the cytologic diagnosis of solid pancreatic masses. Diagn Cytopathol 2014; 42(4): 292–296. doi: 10.1002/dc.23078.
30. Pitman MB, Layfield LJ. Guidelines for pancreaticobiliary cytology from the Papanicolaou Society of Cytopathology: A review. Cancer Cytopathol 2014; 122(6): 399–411. doi: 10.1002/cncy.21427.
31. Baroud S, Sahakian AJ, Sawas T et al. Impact of trimodality sampling on detection of malignant biliary strictures compared with patients with primary sclerosing cholangitis. Gastrointest Endosc 2022; 95(5): 884–892. doi: 10.1016/ j.gie.2021.11.029.
32. Smoczynski M, Jablonska A, Matyskiel A et al. Routine brush cytology and fluorescence in situ hybridization for assessment of pancreatobiliary strictures. Gastrointest Endosc 2012; 75(1): 65–73. doi: 10.1016/j.gie.2011.08.040.
33. Molitor M, Junker K, Eltze E et al. Comparison of structural genetics of non-schistosoma-associated squamous cell carcinoma of the urinary bladder. Int J Clin Exp Pathol 2015; 8(7): 8143–8158.
34. Biankin AV, Waddell N, Kassahn KS et al. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 2012; 491(7424): 399–405. doi: 10.1038/nature11547.
35. Harbhajanka A, Michael CW, Janaki N et al. Tiny but mighty: Use of next generation sequencing on discarded cytocentrifuged bile duct brushing specimens to increase sensitivity of cytological diagnosis. Mod Pathol 2020; 33(10): 2019–2025. doi: 10.1038/s41379-020-0577-1.
36. Bailey P, Chang DK, Nones K et al. Genomic analyses identify molecular subtypes of pancreatic cancer. Nature 2016; 531(7592): 47–52. doi: 10.1038/nature16965.
37. Navaneethan U, Njei B, Lourdusamy V et al. Comparative effectiveness of biliary brush cytology and intraductal biopsy for detection of malignant biliary strictures: A systematic review and meta-analysis. Gastrointest Endosc 2015; 81(1): 168–176. doi: 10.1016/j.gie.2014.09.017.
38. Tamada K, Tomiyama T, Wada S et al. Endoscopic transpapillary bile duct biopsy with the combination of intraductal ultrasonography in the diagnosis of biliary strictures. Gut 2002; 50(3): 326–331. doi: 10.1136/gut.50.3.326.
39. Arvanitakis M, Hookey L, Tessier G et al. Intraductal optical coherence tomography during endoscopic retrograde cholangiopancreatography for investigation of biliary strictures. Endoscopy 2009; 41(8): 696–701. doi: 10.1055/s-0029-1214950.
40. Sugiyama 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(3): 465–467.
41. Naitoh 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(1): 44–51. doi: 10.1111/1751-2980.12311.
42. Pugliese V, Conio M, Nicolò G et al. Endoscopic retrograde forceps biopsy and brush cytology of biliary strictures: A prospective study. Gastrointest Endosc 1995; 42(6): 520–526. doi: 10.1016/s0016-5107(95)70004-8.
43. Howell DA, Parsons WG, Jones MA et al. Complete tissue sampling of biliary strictures at ERCP using a new device. Gastrointest. Endosc 1996; 43(5): 498–502. doi: 10.1016/ s0016-5107(96)70294-8.
44. Ponchon 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(6): 565–572. doi: 10.1016/s0016-5107(95)70012-9.
45. Schoefl 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(4): 363–368. doi: 10.3109/00365529709007685.
46. Lee YN, Moon JH, Choi HJ et al. Diagnostic approach using ERCP-guided transpapillary forceps biopsy or EUS-guided fine-needle aspiration biopsy according to the nature of stricture segment for patients with suspected malignant biliary stricture. Cancer Med 2017; 6(3): 582–590. doi: 10.1002/cam4.1034.
47. Kamp EJCA, Dinjens WNM, Doukas M et al. Optimal tissue sampling during ERCP and emerging molecular techniques for the differentiation of benign and malignant biliary strictures. Therap Adv Gastroenterol 2021; 14: 17562848211002023. doi: 10.1177/175 62848 211002023.
48. Yang MJ, Hwang JC, Lee D et al. Factors affecting the diagnostic yield of endoscopic transpapillary forceps biopsy in patients with malignant biliary strictures. J Gastroenterol Hepatol 2021; 36(8): 2324–2328. doi: 10.1111/jgh.15497.