#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#
CS
proLékaře.cz / Journals / Czecho-Slovak Pathology / 2024 - 2

How to improve pre-operative diagnostics of pancreatobiliary lesions? From immunohistochemistry to Next Generation Sequencing

Czech version

Authors: Marián Švajdler 1,2,3;  Ondřej Daum 1,2;  Magdaléna Daumová 1,2;  Jiřina Pintová 4;  Robert Procházka 4
Authors‘ workplace: Šiklův ústav patologie, Lékařská fakulta Univerzity Karlovy v Plzni a Fakultní nemocnice Plzeň, Česká republika 1;  Bioptická laboratoř s. r. o., Plzeň, Česká Republika 2;  Cytopathos s. r. o., Bratislava, Slovenská republika 3;  Gastroenterologie, Nemocnice Jablonec nad Nisou, p. o., Česká republika 4
Published in: Čes.-slov. Patol., 60, 2024, No. 2, p. 90-101
Category: Reviews Article

Overview

Preoperative cytopathology of pancreatobiliary neoplastic lesions is a sensitive and specific method and is irreplaceable in the diagnosis and clinical management of these diseases. Pathologists should make every attempt to provide diagnosis as precise as possible and minimize the rate of “atypical” results, which create management dilemmas. The diagnostic accuracy of cytopathology can be significantly improved by judicious use of ancillary studies, including immunohistochemistry and molecular genetics. Next generation sequencing (NGS) is the latest addition to pancreatobiliary cytopathology diagnostic arsenal. NGS is not only a very robust diagnostic tool, but also carries significant prognostic and therapeutic information.

Keywords:

immunohistochemistry – cytology – Genetics – pancreas – biliary tract

Sources
  1. Krejčí D, Pehalová L, Talábová A, et al. Novotvary 2018. Současné epidemiologické trendy novotvarů v České republice. ÚZIS 2021, https://www.uzis.cz/res/f/008352/novot- vary2018.pdf
  2. https://gco.iarc.fr/
  3. Tempero MA, Malafa MP, Benson AB, et al. NCCN Clinical Practice Guidelines in Oncology (NCCN Gudelines). Pancreatic Adenocarcinoma. Guidelines, Version 2.2023, NCCN.org
  4. Greenblatt DY, Kelly KJ, Rajamanickam V, et al. Preoperative factors predict perioperative morbidity and mortality after pancreaticoduodenectomy. Ann Surg Oncol 2011; 18(8): 2126-235.
  5. Hewitt MJ, McPhail MJ, Possamai L, Dhar A, Vlavianos P, Monahan KJ. EUS-guided FNA for diagnosis of solid pancreatic neoplasms: a meta-analysis. Gastrointest Endosc 2012; 75(2): 319-331.
  6. Hébert-Magee S, Bae S, Varadarajulu S, Ramesh J, Frost AR, Eloubeidi MA, Eltoum IA. The presence of a cytopathologist increases the diagnostic accuracy of endoscopic ultrasound-guided fine needle aspiration cytology for pancreatic adenocarcinoma: a meta-analysis. Cytopathology 2013; 24(3): 159-171.
  7. Puli SR, Bechtold ML, Buxbaum JL, Eloubeidi MA. How good is endoscopic ultrasound-guided fine-needle aspiration in diagnosing the correct etiology for a solid pancreatic mass?: A meta-analysis and systematic review. Pancreas 2013; 42(1): 20-26.
  8. Erickson RA, Sayage-Rabie L, Beissner RS. Factors predicting the number of EUS-guided fine-needle passes for diagnosis of pancreatic malignancies. Gastrointest Endosc 2000; 51(2):184-190.
  9. Klapman JB, Logrono R, Dye CE, Waxman I. Clinical impact of on-site cytopathology interpretation on endoscopic ultrasound-guided fine needle aspiration. Am J Gastroenterol 2003; 98(6): 1289-1294.
  10. Wani  S,  Muthusamy  VR,  Komanduri S. EUS-guided tissue acquisition: an evidence-based approach (with videos). Gastrointest Endosc 2014; 80(6): 939-959.e7.
  11. da Cunha Santos G, Ko HM, Saieg MA, Geddie WR. “The petals and thorns” of ROSE (rapid on-site evaluation). Cancer Cytopathol 2013; 121(1): 4-8.
  12. van Riet PA, Larghi A, Attili F, et al. A multicenter randomized trial comparing a 25-gauge EUS fine-needle aspiration device with a 20-gauge EUS fine-needle biopsy device. Gastrointest Endosc 2019; 89(2): 329-339.
  13. Song Z, Trujillo CN, Song H, Tongson-Ignacio JE, Chan MY. Endoscopic Ultrasound-Guided Tissue Acquisition Using Fork-Tip Needle Improves Histological Yield, Reduces Needle Passes, Without On-Site Cytopathological Evaluation. J Pancreat Cancer 2018; 4(1): 75-80.
  14. Wong T, Pattarapuntakul T, Netinatsunton N, et al. Diagnostic performance of endoscopic ultrasound-guided tissue acquisition by EUS-FNA versus EUS-FNB for solid pancreatic mass without ROSE: a retrospective study. World J Surg Oncol 2022; 20(1): 215.
  15. Aziz H, Acher AW, Krishna SG, Cloyd JM, Pawlik TM. Comparison of Society Guidelines for the Management and Surveillance of Pancreatic Cysts: A Review. JAMA Surg 2022; 157(8): 723-730.
  16. Vege SS, Ziring B, Jain R, Moayyedi P; Clinical Guidelines Committee; American Gastroenterology Association. American gastroenterological association institute guideline on the diagnosis and management of asymptomatic neoplastic pancreatic cysts. Gastroenterology 2015; 148(4): 819-822; quize12-13.
  17. Megibow AJ, Baker ME, Morgan DE, et al. Management of Incidental Pancreatic Cysts: A White Paper of the ACR Incidental Findings Committee. J Am Coll Radiol 2017; 14(7): 911-923.
  18. Tanaka M, Fernández-Del Castillo C, et al. Revisions of international consensus Fukuoka guidelines for the management of IPMN of the pancreas. Pancreatology 2017; 17(5): 738-753.
  19. European Study Group on Cystic Tumours of the Pancreas. European evidence-based guidelines on pancreatic cystic neoplasms. Gut 2018; 67(5): 789-804.
  20. Elta GH, Enestvedt BK, Sauer BG, Lennon AM. ACG Clinical Guideline: Diagnosis and Management of Pancreatic Cysts. Am J Gastroenterol 2018; 113(4): 464-479.
  21. Sedlack R, Affi A, Vazquez-Sequeiros E, Norton ID, Clain JE, Wiersema MJ. Utility of EUS in the evaluation of cystic pancreatic lesions. Gastrointest Endosc 2002; 56(4): 543-547.
  22. Brugge WR, Lewandrowski K, Lee-Lewandrowski E, et al. Diagnosis of pancreatic cystic neoplasms: a report of the cooperative pancreatic cyst study. Gastroenterology 2004; 126(5): 1330-1336.
  23. Morris-Stiff G, Lentz G, Chalikonda S, et al. Pancreatic cyst aspiration analysis for cystic neoplasms: mucin or carcinoembryonic antigen--which is better? Surgery 2010; 148(4):638-644; discussion 644-645.
  24. de Jong K, van Hooft JE, Nio CY, et al. Accuracy of preoperative workup in a prospective series of surgically resected cystic pancreatic lesions. Scand J Gastroenterol 2012; 47(8-9):1056-1063.
  25. Cizginer S, Turner BG, Bilge AR, Karaca C, Pitman MB, Brugge WR. Cyst fluid carcinoembryonic antigen is an accurate diagnostic marker of pancreatic mucinous cysts. Pancreas 2011; 40(7): 1024-1028.
  26. Smith AL, Abdul-Karim FW, Goyal A. Cytologic categorization of pancreatic neoplastic mucinous cysts with an assessment of the risk of malignancy: A retrospective study based on the Papanicolaou Society of Cytopathology guidelines. Cancer Cytopathol 2016; 124(4):285-293.
  27. Genevay M, Mino-Kenudson M, Yaeger K, et al. Cytology adds value to imaging studies for risk assessment of malignancy in pancreatic mucinous cysts. Ann Surg 2011; 254(6): 977-983.
  1. Pitman MB, Centeno BA, Daglilar ES, Brugge WR, Mino-Kenudson M. Cytological criteria of high-grade epithelial atypia in the cyst fluid of pancreatic intraductal papillary mucinous neoplasms. Cancer Cytopathol 2014; 122(1): 40-47.
  2. Pitman MB, Layfield LJ. The Papanicolaou Society of Cytopathology System for reporting Pancreatobiliary Cytology. Cham: Springer 2015.
  3. Belsley NA, Pitman MB, Lauwers GY, Brugge WR, Deshpande V. Serous cystadenoma of the pancreas: limitations and pitfalls of endoscopic ultrasound-guided fine-needle aspiration biopsy. Cancer 2008; 114(2): 102-110.
  4. Reid MD, Choi HJ, Memis B, et al. Serous Neoplasms of the Pancreas: A Clinicopathologic Analysis of 193 Cases and Literature Review With New Insights on Macrocystic and Solid Variants and Critical Reappraisal of So-called “Serous Cystadenocarcinoma”. Am J Surg Pathol 2015; 39(12): 1597-1610.
  5. Estrada P, Benson M, Gopal D, Buehler D, Pfau P. Cytology with rapid on-site examination (ROSE) does not improve diagnostic yield of EUS-FNA of pancreatic cystic lesions. Diagn Cytopathol 2019; 47(11): 1184-1189.
  6. McCarty TR, Garg R, Rustagi T. Pancreatic cyst fluid glucose in differentiating mucinous from nonmucinous pancreatic cysts: a systematic review and meta-analysis. Gastrointest Endosc 2021; 94(4): 698-712.
  7. Mohan BP, Madhu D, Khan SR, et al. Intracystic Glucose Levels in Differentiating Mucinous From Nonmucinous Pancreatic Cysts: A Systematic Review and Meta-analysis. J Clin Gastroenterol 2022; 56(2): e131-e136.
  8. Guzmán-Calderón E, Md BM, Casellas JA, Aparicio JR. Intracystic Glucose Levels Appear Useful for Diagnosis of Pancreatic Cystic Lesions: A Systematic Review and Meta-Analysis. Dig Dis Sci 2022; 67(6): 2562-2570.
  9. Itonaga M, Ashida R, Kitano M. The usefulness of liquid-based cytology for endoscopic ultrasound-guided tissue acquisition of solid pancreatic masses. Front Med (Lausanne) 2022; 9:943792.
  10. Mitoro A, Nishikawa T, Yoshida M, et al. Diagnostic Efficacy of Liquid-Based Cytology in Endoscopic Ultrasound-Guided Fine Needle Aspiration for Pancreatic Mass Lesions During the Learning Curve: A Retrospective Study. Pancreas 2019; 48(5): 686-689.
  11. Hashimoto S, Taguchi H, Higashi M, et al. Diagnostic efficacy of liquid-based cytology for solid pancreatic lesion samples obtained with endoscopic ultrasound-guided fine-needle aspiration: Propensity score-matched analysis. Dig Endosc 2017; 29(5): 608-616.
  12. Zhou W, Gao L, Wang SM, et al. Comparison of smear cytology and liquid-based cytology in EUS-guided FNA of pancreatic lesions: experience from a large tertiary center. Gastrointest Endosc 2020; 91(4): 932-942.
  13. LeBlanc JK, Emerson RE, Dewitt J, et al. A prospective study comparing rapid assessment of smears and ThinPrep for endoscopic ultrasound-guided fine-needle aspirates. Endoscopy 2010; 42(5): 389-394.
  14. Lee JK, Choi ER, Jang TH, et al. A prospective comparison of liquid-based cytology and traditional smear cytology in pancreatic endoscopic ultrasound-guided fine needle aspiration. Acta Cytol 2011; 55(5): 401-407.
  15. Yeon MH, Jeong HS, Lee HS, et al. Comparison of liquid-based cytology (CellPrepPlus) and conventional smears in pancreaticobiliary disease. Korean J Intern Med 2018; 33(5): 883-892.
  16. Pan HH, Zhou XX, Zhao F, Chen HY, ZhangY. Diagnostic value of liquid-based cytology and smear cytology in pancreatic endoscopic ultrasound-guided fine needle aspiration: A meta-analysis. World J Clin Cases 2020; 8(14): 3006-3020.
  17. Itonaga M, Murata SI, Hatamaru K, et al. Diagnostic efficacy of smear plus liquid-based cytology for EUS-FNA of solid pancreatic lesions: A propensity-matched study. Medicine (Baltimore) 2019; 98(19): e15575.
  18. Kitagawa K, Mitoro A, Tomooka F, et al. Diagnostic yield of liquid-based cytology in serial pancreatic juice aspiration cytological examination. DEN Open 2022; 3(1): e177.
  19. Miyamoto K, Matsumoto K, Kato H, et al. The efficacy of pancreatic juice cytology with liquid-based cytology for evaluating malignancy in patients with intraductal papillary mucinous neoplasm. BMC Gastroenterol 2020; 20(1): 319.
  20. Yang D, Trindade AJ, Yachimski P, et al. Histologic Analysis of Endoscopic Ultrasound-Guided Through the Needle Microforceps Biopsies Accurately Identifies Mucinous Pancreas Cysts. Clin Gastroenterol Hepatol 2019; 17(8): 1587-1596.
  21. Basar O, Yuksel O, Yang DJ, et al. Feasibility and safety of microforceps biopsy in the diagnosis of pancreatic cysts. Gastrointest Endosc 2018; 88(1): 79-86.
  22. Westerveld DR, Ponniah SA, Draganov PV, Yang D. Diagnostic yield of EUS-guided through-the-needle microforceps biopsy versus EUS-FNA of pancreatic cystic lesions: a systematic review and meta-analysis. Endosc Int Open 2020; 8(5): E656-E667.
  23. Salomao M, Gonda TA, Margolskee E, et al.Strategies for improving diagnostic accuracy of biliary strictures. Cancer Cytopathol 2015; 123(4): 244-252.
  24. Avadhani V, Hacihasanoglu E, Memis B, et al. Cytologic predictors of malignancy in bile duct brushings: a multi-reviewer analysis of 60 cases. Mod Pathol 2017; 30(9): 1273-1286.
  25. Hacihasanoglu E, Memis B, Pehlivanoglu B, et al. Factors Impacting the Performance Characteristics of Bile Duct Brushings: A Clinico-Cytopathologic Analysis of 253 Patients. Arch Pathol Lab Med 2018; 142(7): 863-870.
  26. Draganov PV, Chauhan S, Wagh MS, 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(2): 347-353.
  27. Burnett AS, Calvert TJ, Chokshi RJ. Sensitivity of endoscopic retrograde cholangiopancreatography standard cytology: 10-y review of the literature. J Surg Res 2013; 184(1): 304-311.
  28. Chadwick BE, Layfield LJ, Witt BL, Schmidt RL, Cox RN, Adler DG. Significance of atypia in pancreatic and bile duct brushings: follow-up analysis of the categories atypical and suspicious for malignancy. Diagn Cytopathol 2014; 42(4): 285-291.
  29. Selvaggi SM. Bile duct brushing cytology: Cytohistologic/fine-needle aspiration correlation and diagnostic pitfalls. J Am Soc Cytopathol 2016; 5(5): 296-300.
  30. Mehmood S, Loya A, Yusuf MA. Biliary Brush Cytology Revisited. Acta Cytol 2016; 60(2):167-172.
  31. Pereira P, Morais R, Vilas-Boas F, et al. Brush Cytology Performance for the Assessment of Biliopancreatic Strictures. Acta Cytol 2020; 64(4): 344-351.
  32. Ding SM, Lu AL, Xu BQ, et al. Accuracy of brush cytology in biliopancreatic strictures: a single-center cohort study. J Int Med Res 2021; 49(2):300060520987771.
  33. Varbobitis IC, Booth JC, Griffiths CL, Chandra N. Practical guide to improving diagnostic sensitivity of bile duct brushings. Hepatobiliary Pancreat Dis Int 2021; 20(4): 396-399.
  34. 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.
  35. Tanaka H, Matsusaki S, Baba Y, et al. Usefulness of Endoscopic Transpapillary Tissue Sampling for Malignant Biliary Strictures and Predictive Factors of Diagnostic Accuracy. Clin Endosc 2018; 51(2): 174-180.
  36. Yoon SB, Moon SH, Ko SW, Lim H, Kang HS, Kim JH. Brush Cytology, Forceps Biopsy, or Endoscopic Ultrasound-Guided Sampling for Diagnosis of Bile Duct Cancer: A Meta-Analysis. Dig Dis Sci 2022; 67(7): 3284-3297.
  37. Jo JH, Cho CM, Jun JH, et al.; Research Group for Endoscopic Ultrasonography in KSGE. Same-session endoscopic ultrasound-guided fine needle aspiration and endoscopic retrograde cholangiopancreatography-based tissue sampling in suspected malignant biliary obstruction: A multicenter experience. J Gastroenterol Hepatol 2019; 34(4): 799-805.
  38. Troncone E, Gadaleta F, Paoluzi OA, et al. Endoscopic Ultrasound Plus Endoscopic Retrograde Cholangiopancreatography Based Tissue Sampling for Diagnosis of Proximal and Distal Biliary Stenosis Due to Cholangiocarcinoma: Results from a Retrospective Single-Center Study. Cancers (Basel) 2022; 14(7): 1730.
  39. Sadeghi A, Mohamadnejad M, Islami F, et al. Diagnostic yield of EUS-guided FNA for malignant biliary stricture: a systematic review and meta-analysis. Gastrointest Endosc 2016; 83(2): 290-298.e1.
  40. de Moura DTH, Ryou M, de Moura EGH, Ribeiro IB, Bernardo WM, Thompson CC. Endoscopic Ultrasound-Guided Fine Needle Aspiration and Endoscopic Retrograde Cholangiopancreatography-Based Tissue Sampling in Suspected Malignant Biliary Strictures: A Meta-Analysis of Same-Session Procedures. Clin Endosc 2020; 53(4): 417-428.
  41. Waugh MS, Guy CD, Maygarden SJ, Livasy CA, Jones CK, Volmar KE. Use of the ThinPrep method in bile duct brushings: analysis of morphologic parameters associated with malignancy and determination of interobserver reliability. Diagn Cytopathol 2008; 36(9): 651-656.
  1. Lee MW, Paik WH, Lee SH, et al. Usefulness of Liquid-Based Cytology in Diagnosing Biliary Tract Cancer Compared to Conventional Smear and Forceps Biopsy. Dig Dis Sci 2023; 68(1): 274-283.
  2. Volmar KE, Vollmer RT, Routbort MJ, Creager AJ. Pancreatic and bile duct brushing cytology in 1000 cases: review of findings and comparison of preparation methods. Cancer 2006; 108(4): 231-238.
  3. Nakahara K, Michikawa Y, Morita R, et al. Diagnostic Ability of Endoscopic Bile Cytology Using a Newly Designed Biliary Scraper for Biliary Strictures. Dig Dis Sci 2019; 64(1): 241-248.
  4. Ko SW, Lee SS, So H, et al. A novel method of biopsy for indeterminate pancreaticobiliary strictures: tube-assisted biopsy. Endoscopy 2020; 52(7): 589-594.
  5. Zhuang MQ, Zheng C, Xie WW, et al. Diagnostic value of new biliary biopsy cannulae for malignant bile duct strictures by endoscopic retrograde cholangiopancreatography pathway. Asian J Surg 2023 May 2:S10159584(23)00618-8.
  6. HooKim K, Reid MD. Atypical cells in fine needle aspiration biopsies of pancreas: Causes, work-up, and recommendations for management. Diagn Cytopathol 2022; 50(4):196-207.
  7. Qin SY, Zhou Y, Li P, Jiang HX. Diagnostic efficacy of cell block immunohistochemistry, smear cytology, and liquid-based cytology in endoscopic ultrasound-guided fine-needle aspiration of pancreatic lesions: a single-institution experience. PLoS One 2014; 9(9): e108762.
  8. Pausawasdi N, Hongsrisuwan P, Chalermwai WV, Butt AS, Maipang K, Charatchareonwitthaya P. The diagnostic performance of combined conventional cytology with smears and cell block preparation obtained from endoscopic ultrasound-guided fine needle aspiration for intra-abdominal mass lesions. PLoS One 2022; 17(3): e0263982.
  9. Kim JH, Lee SJ, Moon SH, et al. Incremental value of cell block preparations over conventional smears alone in the evaluation of EUSFNA for pancreatic masses. Hepatogastroenterology 2014; 61(135): 2117-2122.
  10. Nambirajan A, Jain D. Cell blocks in cytopathology: An update. Cytopathology 2018; 29(6): 505-524.
  11. Lin F, Chen ZE, Wang HL. Utility of immunohistochemistry in the pancreatobiliary tract. Arch Pathol Lab Med 2015; 139(1): 24-38.
  12. La Rosa S, Adsay V, Albarello L, et al. Clinicopathologic study of 62 acinar cell carcinomas of the pancreas: insights into the morphology and immunophenotype and search for prognostic markers. Am J Surg Pathol 2012; 36(12): 1782-1795.
  13. Hosoda W, Sasaki E, Murakami Y, Yamao K, Shimizu Y, Yatabe Y. BCL10 as a useful marker for pancreatic acinar cell carcinoma, especially using endoscopic ultrasound cytology specimens. Pathol Int 2013; 63(3): 176-182.
  14. Ishimoto-Namiki U, Ino Y, Esaki M, Shimada K, Saruta M, Hiraoka N. Novel Insights Into Immunohistochemical Analysis For Acinar Cell Neoplasm of The Pancreas: Carboxypeptidase A2, Carboxypeptidase A1, and Glycoprotein 2. Am J Surg Pathol 2023; 47(5): 525-534.
  15. Kim MJ, Jang SJ, Yu E. Loss of E-cadherin and cytoplasmic-nuclear expression of beta-catenin are the most useful immunoprofiles in the diagnosis of solid-pseudopapillary neoplasm of the pancreas. Hum Pathol 2008; 39(2): 251-258.
  16. Din NU, Rahim S, Abdul-Ghafar J, Ahmed A, Ahmad Z. Clinicopathological and immunohistochemical study of 29 cases of solid-pseudopapillary neoplasms of the pancreas in patients under 20 years of age along with detailed review of literature. Diagn Pathol 2020; 15(1): 139.
  17. Li L, Li J, Hao C, Zhang C, Mu K, Wang Y, Zhang T. Immunohistochemical evaluation of solid pseudopapillary tumors of the pancreas: the expression pattern of CD99 is highly unique. Cancer Lett 2011; 310(1): 9-14.
  18. Guo Y, Yuan F, Deng H, Wang HF, Jin XL, Xiao JC. Paranuclear dot-like immunostaining for CD99: a unique staining pattern for diagnosing solid-pseudopapillary neoplasm of the pancreas. Am J Surg Pathol 2011; 35(6): 799-806.
  19. Ardengh JC, Lopes CV, Venco FE, Machado MA. Diagnosis of pancreatic solid pseudopapillary neoplasms using cell-blocks and immunohistochemical evaluation of endoscopic ultrasound-guided fine needle aspiration biopsy specimens. Cytopathology 2021; 32(1):50-56.
  20. Kim EK, Jang M, Park M, Kim H. LEF1, TFE3, and AR are putative diagnostic markers of solid pseudopapillary neoplasms. Oncotarget 2017; 8(55): 93404-93413.
  21. Harrison G, Hemmerich A, Guy C, et al. Overexpression of SOX11 and TFE3 in Solid-Pseudopapillary Neoplasms of the Pancreas. Am J Clin Pathol 2017; 149(1): 67-75.
  22. Dinarvand P, Wang WL, Roy-Chowdhuri S. Utility of SOX11 for the diagnosis of solid pseudopapillary neoplasm of the pancreas on cytological preparations. Cytopathology 2022; 33(2): 216-221.
  23. Tanigawa M, Nakayama M, Taira T, et al. Insulinoma-associated protein 1 (INSM1) is a useful marker for pancreatic neuroendocrine tumor. Med Mol Morphol 2018; 51(1): 32-40.
  24. McHugh KE, Mukhopadhyay S, Doxtader EE, Lanigan C, Allende DS. INSM1 Is a Highly Specific Marker of Neuroendocrine Differentiation in Primary Neoplasms of the Gastrointestinal Tract, Appendix, and Pancreas. Am J Clin Pathol 2020; 153(6): 811-820.
  25. Zhang Q, Huang J, He Y, Cao R, Shu J. Insulinoma-associated protein 1(INSM1) is a superior marker for the diagnosis of gastroenteropancreatic neuroendoerine neoplasms: a meta-analysis. Endocrine 2021; 74(1): 61-71.
  26. González I, Lu HC, Sninsky J, et al. Insulinoma-associated protein 1 expression in primary and metastatic neuroendocrine neoplasms of the gastrointestinal and pancreaticobiliary tracts. Histopathology 2019; 75(4): 568-577.
  27. Konukiewitz B, Jesinghaus M, Kasajima A, Klöppel G. Neuroendocrine neoplasms of the pancreas: diagnosis and pitfalls. Virchows Arch 2022; 480(2): 247-257.
  28. Konukiewitz B, Schlitter AM, Jesinghaus M, et al. Somatostatin receptor expression related to TP53 and RB1 alterations in pancreatic and extrapancreatic neuroendocrine neoplasms with a Ki67-index above 20. Mod Pathol 2017; 30(4): 587-598.
  29. Konukiewitz B, von Hornstein M, Jesing-haus M, et al. Pancreatic neuroendocrine tumors with somatostatin expression and paraganglioma-like features. Hum Pathol 2020; 102: 79-87.
  30. Reid MD, Bhattarai S, Graham RP, et al. Pancreatoblastoma: Cytologic and histologic analysis of 12 adult cases reveals helpful criteria in their diagnosis and distinction from common mimics. Cancer Cytopathol 2019; 127(11): 708-719.
  31. Klimstra DS, Wenig BM, Adair CF, Heffess CS. Pancreatoblastoma. A clinicopathologic study and review of the literature. Am J Surg Pathol 1995; 19(12): 1371-1389.
  32. Tanaka Y, Kato K, Notohara K, et al. Significance of aberrant (cytoplasmic/nuclear) expression of beta-catenin in pancreatoblastoma. J Pathol 2003; 199(2): 185-190.
  33. Nishimata S, Kato K, Tanaka M, et al. Expression pattern of keratin subclasses in pancreatoblastoma with special emphasis on squamoid corpuscles. Pathol Int 2005; 55(6):297-302.
  34. Wood LD, Klimstra DS. Pathology and genetics of pancreatic neoplasms with acinar differentiation. Semin Diagn Pathol 2014; 31(6): 491-497.
  35. Reid MD. Cytologic Assessment of Cystic/ Intraductal Lesions of the Pancreatobiliary Tract. Arch Pathol Lab Med 2022; 146(3): 280-297.
  36. Chi Z, Xu J, Karamchandani DM, Peng L. Pax8 as a useful adjunct marker to differentiate pancreatic serous cystadenoma from clear cell renal cell carcinoma in both cytologic and surgical specimens. Diagn Pathol 2023; 18(1): 54.
  37. Reid MD, Centeno BA. Ancillary Studies, Including Immunohistochemistry and Molecular Studies, in Pancreatic Cytology. Surg Pathol Clin 2014;7(1): 1-34.
  38. Paolino G, Esposito I, Hong SM, et al. Intraductal tubulopapillary neoplasm (ITPN) of the pancreas: a distinct entity among pancreatic tumors. Histopathology 2022; 81(3):297-309.
  39. Lüttges J, Zamboni G, Longnecker D, Klöppel G. The immunohistochemical mucin expression pattern distinguishes different types of intraductal papillary mucinous neoplasms of the pancreas and determines their relationship to mucinous noncystic carcinoma and ductal adenocarcinoma. Am J Surg Pathol 2001; 25(7): 942-948.
  40. Basturk O, Chung SM, Hruban RH, et al. Distinct pathways of pathogenesis of intraductal oncocytic papillary neoplasms and intraductal papillary mucinous neoplasms of the pancreas. Virchows Arch 2016; 469(5): 523-532.
  1. Larghi A, Manfrin E, Fabbri C, et al. Interobserver agreement among expert pathologists on through-the-needle microforceps biopsy samples for evaluation of pancreatic cystic lesions. Gastrointest Endosc 2019; 90(5): 784792.e4.
  2. Cortez N, Berzosa M, Mahfouz M, Dvir K, Galarza Fortuna GM, Ben-David K. Diagnosis and Treatment of Metastatic Disease to the Pancreas. J Laparoendosc Adv Surg Tech A 2020; 30(9): 1008-1012.
  3. Smith AL, Odronic SI, Springer BS, Reynolds JP. Solid tumor metastases to the pancreas diagnosed by FNA: A single-institution experience and review of the literature. Cancer Cytopathol 2015; 123(6): 347-355.
  4. Sekulic M, Amin K, Mettler T, Miller LK, Mallery S, Stewart J Rd. Pancreatic involvement by metastasizing neoplasms as determined by endoscopic ultrasound-guided fine needle aspiration: A clinicopathologic characterization. Diagn Cytopathol 2017; 45(5): 418-425.
  5. Ioakim KJ, Sydney GI, Michaelides C, et al. Evaluation of metastases to the pancreas with fine needle aspiration: A case series from a single centre with review of the literature. Cytopathology 2020; 31(2): 96-105.
  6. Liu H, Shi J, Anandan V, Wang HL, et al. Reevaluation and identification of the best immunohistochemical panel (pVHL, Maspin, S100P, IMP-3) for ductal adenocarcinoma of the pancreas. Arch Pathol Lab Med 2012; 136(6): 601-609.
  7. Luu TT. Review of Immunohistochemistry Biomarkers in Pancreatic Cancer Diagnosis. Front Oncol 2021; 11: 799025.
  8. Sopha SC, Gopal P, Merchant NB, et al. Diagnostic and therapeutic implications of a novel immunohistochemical panel detecting duodenal mucosal invasion by pancreatic ductal adenocarcinoma. Int J Clin Exp Pathol 2013; 6(11): 2476-2486.
  9. Hutchings D, Waters KM, Weiss MJ, et al. Cancerization of the Pancreatic Ducts: Demonstration of a Common and Under-recognized Process Using Immunolabeling of Paired Duct Lesions and Invasive Pancreatic Ductal Adenocarcinoma for p53 and Smad4 Expression. Am J Surg Pathol 2018; 42(11): 1556-1561.
  10. Fukushi K, Yamamiya A, Tominaga K, et al. Usefulness of Adding Maspin Staining to p53 Staining for EUS-FNA Specimens of Pancreatic Ductal Adenocarcinoma. J Clin Med 2022; 11(20): 6097.
  11. Matsuda Y, Esaka S, Suzuki A, et al. Abnormal immunolabelling of SMAD4 in cell block specimens to distinguish malignant and benign pancreatic cells. Cytopathology 2019; 30(2): 201-208.
  12. Giorgadze TA, Peterman H, Baloch ZW, et al. Diagnostic utility of mucin profile in fine-needle aspiration specimens of the pancreas: an immunohistochemical study with surgical pathology correlation. Cancer 2006; 108(3): 186-197.
  13. Hedegaard Jensen G, Mortensen MB, Klöppel G, Nielsen MFB, Nielsen O, Detlefsen S. Utility of pVHL, maspin, IMP3, S100P and Ki67 in the distinction of autoimmune pancreatitis from pancreatic ductal adenocarcinoma. Pathol Res Pract 2020; 216(5): 152925.
  14. Mamdouh MM, Okasha H, Shaaban HAM, Hafez NH, El-Gemeie EH. Role of Maspin, CK17 and Ki-67 Immunophenotyping in Diagnosing of Pancreatic Ductal Adenocarcinoma in Endoscopic Ultrasound-Guided Fine Needle Aspiration Cytology. Asian Pac J Cancer Prev 2021; 22(10): 3299-3307.
  15. Burnett AS, Quinn PL, Ajibade DV, et al. Design of an immunohistochemistry biomarker panel for diagnosis of pancreatic adenocarcinoma. Pancreatology 2019; 19(6): 842-849.
  16. Sweeney J, Rao R, Margolskee E, Goyal A, Heymann JJ, Siddiqui MT. Immunohistochemical staining for S100P, SMAD4, and IMP3 on cell block preparations is sensitive and highly specific for pancreatic ductal adenocarcinoma. J Am Soc Cytopathol 2018; 7(6): 318-323.
  17. Jahng AW, Reicher S, Chung D, et al. Staining for p53 and Ki-67 increases the sensitivity of EUS-FNA to detect pancreatic malignancy. World J Gastrointest Endosc 2010; 2(11): 362-368.
  18. Levy M, Lin F, Xu H, Dhall D, Spaulding BO, Wang HL. S100P, von Hippel-Lindau gene product, and IMP3 serve as a useful immunohistochemical panel in the diagnosis of adenocarcinoma on endoscopic bile duct biopsy. Hum Pathol 2010; 41(9): 1210-1219.
  19. Sasaki M, Sato Y. An immunohistochemical panel of insulin-like growth factor II mRNA-binding protein 3 (IMP3), enhancer of zeste homolog 2 (EZH2), and p53 is useful for a diagnosis in bile duct biopsy. Virchows Arch 2021; 479(4): 697-703.
  20. Lok T, Chen L, Lin F, Wang HL. Immunohistochemical distinction between intrahepatic cholangiocarcinoma and pancreatic ductal adenocarcinoma. Hum Pathol 2014; 45(2):394-400.
  21. Ribeiro A, Peng J, Casas C, Fan YS. Endoscopic ultrasound guided fine needle aspiration with fluorescence in situ hybridization analysis in 104 patients with pancreatic mass. J Gastroenterol Hepatol 2014; 29(8): 1654-1658.
  22. Kubiliun N, Ribeiro A, Fan YS, et al. EUS-FNA with rescue fluorescence in situ hybridization for the diagnosis of pancreatic carcinoma in patients with inconclusive on-site cytopathology results. Gastrointest Endosc 2011; 74(3): 541-547.
  23. Nanda A, Brown JM, Berger SH, et al. Triple modality testing by endoscopic retrograde cholangiopancreatography for the diagnosis of cholangiocarcinoma. Therap Adv Gastroenterol 2015; 8(2): 56-65.
  24. Barr Fritcher EG, Kipp BR, Halling KC, Clayton AC. FISHing for pancreatobiliary tract malignancy in endoscopic brushings enhances the sensitivity of routine cytology. Cytopathology 2014; 25(5): 288-301.
  25. Liew ZH, Loh TJ, Lim TKH, et al. Role of fluorescence in situ hybridization in diagnosing cholangiocarcinoma in indeterminate biliary strictures. J Gastroenterol Hepatol 2018; 33(1):315-319.
  26. Brooks C, Gausman V, Kokoy-Mondragon C, et al. Role of Fluorescent In Situ Hybridization, Cholangioscopic Biopsies, and EUS-FNA in the Evaluation of Biliary Strictures. Dig Dis Sci 2018; 63(3): 636-644.
  27. Zoundjiekpon VD, Falt P, Zapletalova J, et al. Fluorescence In Situ Hybridization in Primary Diagnosis of Biliary Strictures: A Single-Center Prospective Interventional Study. Biomedicines 2023; 11(3): 755.
  28. 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): 1813-1824.e1.
  29. Kipp BR, Barr Fritcher EG, Pettengill JE, Halling KC, Clayton AC. Improving the accuracy of pancreatobiliary tract cytology with fluorescence in situ hybridization: a molecular test with proven clinical success. Cancer Cytopathol 2013; 121(11): 610-619.
  30. Levy MJ, Oberg TN, Campion MB, et al. Comparison of methods to detect neoplasia in patients undergoing endoscopic ultrasound-guided fine-needle aspiration. Gastroenterology 2012; 142(5): 1112-1121.e2.
  31. Boldorini R, Paganotti A, Sartori M, et al. Fluorescence in situ hybridisation in the cytological diagnosis of pancreatobiliary tumours. Pathology 2011; 43(4): 335-339.
  32. Kipp BR, Barr Fritcher EG, Clayton AC, et al. Comparison of KRAS Mutation Analysis and FISH for Detecting Pancreatobiliary Tract Cancer in Cytology Specimens Collected During Endoscopic Retrograde Cholangiopancreatography. J Mol Diagn 2010; 12(6): 780–786.
  33. 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): 913-919.e1.
  34. Kushnir VM, Mullady DK, Das K, et al. The Diagnostic Yield of Malignancy Comparing Cytology, FISH, and Molecular Analysis of Cell Free Cytology Brush Supernatant in Patients With Biliary Strictures Undergoing Endoscopic Retrograde Cholangiography (ERC): A Prospective Study. J Clin Gastroenterol 2019; 53(9): 686-692.
  35. Salek C, Benesova L, Zavoral M, et al. Evaluation of clinical relevance of examining K-ras, p16 and p53 mutations along with allelic losses at 9p and 18q in EUS-guided fine needle aspiration samples of patients with chronic pancreatitis and pancreatic cancer. World J Gastroenterol 2007; 13(27): 3714-3720.
  36. Buscail L, Bournet B, Cordelier P. Role of oncogenic KRAS in the diagnosis, prognosis and treatment of pancreatic cancer. Nat Rev Gastroenterol Hepatol 2020; 17(3): 153-168.
  37. Trisolini E, Armellini E, Paganotti A, et al. KRAS mutation testing on all non-malignant diagnosis of pancreatic endoscopic ultrasound-guided fine-needle aspiration biopsies improves diagnostic accuracy. Pathology 2017; 49(4): 379-386.
  38. Sekita-Hatakeyama Y, Nishikawa T, Takeuchi M, et al. K-ras mutation analysis of residual liquid-based cytology specimens from endoscopic ultrasound-guided fine needle aspiration improves cell block diagnosis of pancreatic ductal adenocarcinoma. PLoS One 2018; 13(3): e0193692.
  1. Park JK, Lee YJ, Lee JK, Lee KT, Choi YL, Lee KH. KRAS mutation analysis of washing fluid from endoscopic ultrasound-guided fine needle aspiration improves cytologic diagnosis of pancreatic ductal adenocarcinoma. Oncotarget 2017; 8(2): 3519-3527.
  2. Hosoda W, Chianchiano P, Griffin JF, et al. Genetic analyses of isolated high-grade pancreatic intraepithelial neoplasia (HG-PanIN) reveal paucity of alterations in TP53 and SMAD4. J Pathol 2017; 242(1): 16-23.
  3. Chen JC, Beal EW, Pawlik TM, Cloyd J, Dillhoff ME. Molecular Diagnosis of Cystic Neoplasms of the Pancreas: a Review. J Gastrointest Surg 2020; 24(5): 1201-1214.
  4. Springer S, Wang Y, Dal Molin M, et al. A combination of molecular markers and clinical features improve the classification of pancreatic cysts. Gastroenterology 2015; 149(6):1501-1510.
  5. Thompson ED, Roberts NJ, Wood LD, et al. The genetics of ductal adenocarcinoma of the pancreas in the year 2020: dramatic progress, but far to go. Mod Pathol 2020; 33(12): 2544-2563.
  6. Shibata T, Arai Y, Totoki Y. Molecular genomic landscapes of hepatobiliary cancer. Cancer Sci 2018; 109(5): 1282-1291.
  7. Nakamura H, Arai Y, Totoki Y, et al. Genomic spectra of biliary tract cancer. Nat Genet 2015; 47(9): 1003-1010.
  8. LaPelusa M, Heumann T, Goff L, Agarwal R. Targeted therapies in advanced biliary tract cancers-a narrative review. Chin Clin Oncol 2023; 12(2): 14.
  9. Takano S, Fukasawa M, Shindo H, et al. Next-generation sequencing of endoscopically obtained tissues from patients with all stages of pancreatic cancer. Cancer Sci 2022; 113(3): 1069-1077.
  10. Chou A, Brown IS, Kumarasinghe MP, et al. RET gene rearrangements occur in a subset of pancreatic acinar cell carcinomas. Mod Pathol 2020; 33(4): 657-664.
  11. Malapelle U, Mayo-de-Las-Casas C, Molina-Vila MA, et al.; Molecular Cytopathology Meeting Group. Consistency and reproducibility of next-generation sequencing and other multigene mutational assays: A worldwide ring trial study on quantitative cytological molecular reference specimens. Cancer Cytopathol 2017; 125(8): 615-626.
  12. Ma W, Brodie S, Agersborg S, Funari VA, Albitar M. Significant Improvement in Detecting BRAF, KRAS, and EGFR Mutations Using Next-Generation Sequencing as Compared with FDA-Cleared Kits. Mol Diagn Ther 2017; 21(5): 571-579.
  13. Park JK, Lee JH, Noh DH, et al. Factors of Endoscopic Ultrasound-Guided Tissue Acquisition for Successful Next-Generation Sequencing in Pancreatic Ductal Adenocarcinoma. Gut Liver 2020; 14(3): 387-394.
  14. Ramani NS, Chen H, Broaddus RR, et al. Utilization of cytology smears improves success rates of RNA-based next-generation sequencing gene fusion assays for clinically relevant predictive biomarkers. Cancer Cytopathol 2021; 129(5): 374-382.
  15. Roy-Chowdhuri S, Pisapia P, Salto-Tellez M, et al. Invited review-next-generation sequencing: a modern tool in cytopathology. Virchows Arch 2019; 475(1): 3-11.
  16. Nikas IP, Mountzios G, Sydney GI, Ioakim KJ, Won JK, Papageorgis P. Evaluating Pancreatic and Biliary Neoplasms with Small Biopsy-Based Next Generation Sequencing (NGS): Doing More with Less. Cancers (Basel) 2022; 14(2): 397.
  17. Dudley JC, Zheng Z, McDonald T, et al. Next-Generation Sequencing and Fluorescence in Situ Hybridization Have Comparable Performance Characteristics in the Analysis of Pancreaticobiliary Brushings for Malignancy. J Mol Diagn 2016; 18(1): 124-130.
  18. Singhi AD, Nikiforova MN, Chennat J, et al. Integrating next-generation sequencing to endoscopic retrograde cholangiopancreatography (ERCP)-obtained biliary specimens improves the detection and management of patients with malignant bile duct strictures.Gut 2020; 69(1): 52-61.
  19. 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.
  20. Rosenbaum MW, Arpin R, Limbocker J, et al. Cytomorphologic characteristics of next-generation sequencing-positive bile duct brushing specimens. J Am Soc Cytopathol 2020; 9(6): 520-527.
  21. Plougmann JI, Klausen P, Toxvaerd A, et al. DNA sequencing of cytopathologically inconclusive EUS-FNA from solid pancreatic lesions suspicious for malignancy confirms EUS diagnosis. Endosc Ultrasound 2020; 9(1):37-44.
  22. Amato E, Molin MD, Mafficini A, et al. Targeted next-generation sequencing of cancer genes dissects the molecular profiles of intraductal papillary neoplasms of the pancreas. J Pathol 2014; 233(3): 217-227.
  23. Jones M, Zheng Z, Wang J, et al. Impact of next-generation sequencing on the clinical diagnosis of pancreatic cysts. Gastrointest Endosc 2016; 83(1): 140-148.
  24. Rosenbaum MW, Jones M, Dudley JC, Le LP, Iafrate AJ, Pitman MB. Next-generation sequencing adds value to the preoperative diagnosis of pancreatic cysts. Cancer Cytopathol 2017; 125(1): 41-47.
  25. Singhi AD, McGrath K, Brand RE, et al. Preoperative next-generation sequencing of pancreatic cyst fluid is highly accurate in cyst classification and detection of advanced neoplasia. Gut 2018; 67(12): 2131-2141.
  26. Schmitz D, Kazdal D, Allgäuer M, et al. KRAS/GNAS-testing by highly sensitive deep targeted next generation sequencing improves the endoscopic ultrasound-guided workup of suspected mucinous neoplasms of the pancreas. Genes Chromosomes Cancer 2021; 60(7): 489-497.
Labels
Anatomical pathology Forensic medical examiner Toxicology
EDITORIAL
INTERVIEW
MONITOR
Intraductal and cystic pancreatic neoplasia
Pitfalls of cytological diagnosis of tumours of the pancreaticobiliary tract
Current diagnostic and treatment options for pancreatic cancer in 2024
Solitary fibrous tumor of thyroid: Case report
Calcific Aortic Stenosis – Inflammatory Disease
Article was published in

Czecho-Slovak Pathology

Issue 2
2024 Issue 2
Most read in this issue
Topics Journals
Login
Forgotten password

Enter the email address that you registered with. We will send you instructions on how to set a new password.

Login

Don‘t have an account?  Create new account

#ADS_BOTTOM_SCRIPTS#