PDF herunterladen
CC BY-NC-ND 4.0 · Endosc Int Open 2020; 08(11): E1611-E1622
DOI: 10.1055/a-1240-0027
Original article

Comparison of EUS-guided conventional smear and liquid-based cytology in pancreatic lesions: A systematic review and meta-analysis

Saurabh Chandan‡
 1   Division of Gastroenterology and Hepatology, CHI Creighton University Medical Center, Omaha, Nebraska, USA
,
Babu P. Mohan‡
 2   Division of Gastroenterology and Hepatology, University of Utah School of Medicine, Salt Lake City, Utah, USA
,
Shahab R. Khan
 3   Section of Gastroenterology, Rush University Medical Center, Chicago, Illinois, USA
,
Andrew Ofosu
 4   Division of Gastroenterology & Hepatology, Stanford University, Stanford, California, United States
,
Amaninder S. Dhaliwal
 5   Division of Digestive Diseases & Nutrition, University of South Florida, Tampa, Florida, USA
,
Aun R. Shah
 6   Gastroenterology and Hepatology, University of Nebraska Medical Center, Omaha, Nebraska, USA
,
Neil Bhogal
 6   Gastroenterology and Hepatology, University of Nebraska Medical Center, Omaha, Nebraska, USA
,
Harmeet S. Mashiana
 6   Gastroenterology and Hepatology, University of Nebraska Medical Center, Omaha, Nebraska, USA
,
Simran S. Mashiana
 7   Pathology & Microbiology, University of Nebraska Medical Center, Omaha, Nebraska, USA
,
Lena L. Kassab
 8   Internal Medicine, Mayo Clinic, Rochester, Minnesota, USA
,
Suresh Ponnada
 9   Internal Medicine, Carilion Roanoke Memorial Hospital, Roanoke, Virginia, USA
,
Antonio Facciorusso
10   Gastroenterology Unit, Department of Medical Sciences, University of Foggia, Foggia, Italy
,
Ishfaq Bhat
 6   Gastroenterology and Hepatology, University of Nebraska Medical Center, Omaha, Nebraska, USA
,
Shailender Singh
 6   Gastroenterology and Hepatology, University of Nebraska Medical Center, Omaha, Nebraska, USA
,
Benjamin L. Witt
11   Cytopathology Section, University of Utah School of Medicine, Salt Lake City, Utah, USA
,
Douglas G. Adler
 2   Division of Gastroenterology and Hepatology, University of Utah School of Medicine, Salt Lake City, Utah, USA
› Institutsangaben
› Weitere Informationen
Auch verfügbar auf
   Lizenzen und Reprints

Abstract

Background and study aims Endoscopic ultrasound (EUS)-guided fine-needle aspiration (EUS-FNA) has limitations of inadequate sampling and false-negative results for malignancy. It has been performed using conventional smear (CS) cytology with rapid on-site evaluation (ROSE) with reasonable diagnostic accuracy. An alternative to ROSE is liquid-based cytology (LBC). Commonly used LBC techniques include precipitation-based (SurePath™) and filtration-based (ThinPrep®, CellPrep®). Data regarding the diagnostic efficacy of LBC compared with CS are limited.

Methods Multiple databases were searched through March 2020 to identify studies reporting diagnostic yield of EUS-guided CS and LBC in pancreatic lesions. Pooled diagnostic odds and rates of performance for the cytologic diagnoses of benign, suspicious, and malignant lesions were calculated. Diagnostic efficacy was evaluated by pooled rates of accuracy, sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV).

Results Nine studies with a total of 1308 patients were included in our final analysis. Pooled diagnostic odds of CS cytology were 1.69 (CI 1.02–2.79) and 0.39 (CI 0.19–0.8) for malignant lesions when compared to filtration-based and precipitation-based LBC techniques, respectively. For CS, precipitation-based and filtration-based LBC, pooled diagnostic accuracy was 79.7 %, 85.2 %, 77.3 %, sensitivity was 79.2 %, 83.6 %, 68.3 %, and specificity was 99.4 %, 99.5 %, 99.5 %, respectively.

Conclusions The precipitation-based LBC technique (SurePath™) had superior diagnostic odds for malignant pancreatic lesions compared with CS cytology in the absence of ROSE. It showed superior accuracy and sensitivity, but comparable specificity and PPV. Diagnostic odds of CS cytology in the absence of ROSE were superior to the filtration-based LBC technique (ThinPrep®, Cellprep®) for diagnosing malignant pancreatic lesions.

Supplementary material



Publikationsverlauf

Eingereicht: 06. Mai 2020

Angenommen: 07. Juli 2020

Artikel online veröffentlicht:
22. Oktober 2020

© 2020. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Tharian B, Tsiopoulos F, George N. et al. Endoscopic ultrasound fine needle aspiration: Technique and applications in clinical practice. World J Gastrointest Endosc 2012; 4: 532-544
    CrossrefPubMedGoogle Scholar
  • 2 Weston BR, Bhutani MS. Optimizing diagnostic yield for EUS-guided sampling of solid pancreatic lesions: a technical review. Gastroenterol Hepatol (NY) 2013; 9: 352-363
    PubMedGoogle Scholar
  • 3 Santo E, Bar-Yishay I. Pancreatic solid incidentalomas. Endosc Ultrasound 2017; 6: S99-S103
    CrossrefPubMedGoogle Scholar
  • 4 Bray F, Ferlay J, Soerjomataram I. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 394-424
    CrossrefPubMedGoogle Scholar
  • 5 Ferlay J, Ervik M, Lam F. et al. Global cancer Observatory: cancer today. Lyon, France: International agency for research on cancer, Cancer Today; 2018
    Google Scholar
  • 6 DeWitt J, McGreevy K, Sherman S. et al. Utility of a repeated EUS at a tertiary-referral center. Gastrointest Endosc 2008; 67: 610-619
    CrossrefPubMedGoogle Scholar
  • 7 Iglesias-Garcia J, Dominguez-Munoz E, Lozano-Leon A. et al. Impact of endoscopic ultrasound-guided fine needle biopsy for diagnosis of pancreatic masses. World J Gastroentero 2007; 13: 289
    CrossrefPubMedGoogle Scholar
  • 8 Bang JY, Hebert-Magee S, Trevino J. et al. Randomized trial comparing the 22-gauge aspiration and 22-gauge biopsy needles for EUS-guided sampling of solid pancreatic mass lesions. Gastrointest Endosc 2012; 76: 321-327
    CrossrefPubMedGoogle Scholar
  • 9 Hucl T, Wee E, Anuradha S. et al. Feasibility and efficiency of a new 22G core needle: a prospective comparison study. Endoscopy 2013; 45: 792-798
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 10 Berzosa M, Villa N, El-Serag HB. et al. Comparison of endoscopic ultrasound guided 22-gauge core needle with standard 25-gauge fine-needle aspiration for diagnosing solid pancreatic lesions. Endosc Ultrasound 2015; 4: 28
    CrossrefPubMedGoogle Scholar
  • 11 Syed A, Babich O, Rao B. et al. Endoscopic ultrasound guided fine‐needle aspiration vs core needle biopsy for solid pancreatic lesions: Comparison of diagnostic accuracy and procedural efficiency. Diagnostic cytopathology 2019; 47: 1138-1144
    CrossrefPubMedGoogle Scholar
  • 12 Sweeney J, Soong L, Goyal A. Endoscopic ultrasound-guided tissue acquisition of solid mass lesions of the pancreas: A retrospective comparison study of fine-needle aspiration and fine-needle biopsy. Diagn Cytopathol 2020; 48: 322-329
    CrossrefPubMedGoogle Scholar
  • 13 Petrone MC, Arcidiacono PG. Basic technique in endoscopic ultrasound-guided fine needle aspiration for solid lesions: How many passes?. Endosc Ultrasound 2014; 3: 22-27
    CrossrefPubMedGoogle Scholar
  • 14 Matynia AP, Schmidt RL, Barraza G. et al. Impact of rapid on‐site evaluation on the adequacy of endoscopic‐ultrasound guided fine‐needle aspiration of solid pancreatic lesions: a systematic review and meta‐analysis. J Gastroenterol Hepatol 2014; 29: 697-705
    CrossrefPubMedGoogle Scholar
  • 15 Hewitt MJ, McPhail MJ, Possamai L. et al. EUS-guided FNA for diagnosis of solid pancreatic neoplasms: a meta-analysis. Gastrointest Endosc 2012; 75: 319-331
    CrossrefPubMedGoogle Scholar
  • 16 Haba S, Yamao K, Bhatia V. et al. Diagnostic ability and factors affecting accuracy of endoscopic ultrasound-guided fine needle aspiration for pancreatic solid lesions: Japanese large single center experience. J Gastroenterol 2013; 48: 973-981
    CrossrefPubMedGoogle Scholar
  • 17 da Cunha Santos G, Saieg MA. Preanalytic specimen triage: Smears, cell blocks, cytospin preparations, transport media, and cytobanking. Cancer Cytopathol 2017; 125: 455-464
    CrossrefPubMedGoogle Scholar
  • 18 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: 883-892
    CrossrefPubMedGoogle Scholar
  • 19 Bernstein SJ, Sanchez-Ramos L, Ndubisi B. Liquid-based cervical cytologic smear study and conventional Papanicolaou smears: a metaanalysis of prospective studies comparing cytologic diagnosis and sample adequacy. Am J Obstet Gynecol 2001; 185: 308-317
    CrossrefPubMedGoogle Scholar
  • 20 Meara RS, Jhala D, Eloubeidi MA. et al. Endoscopic ultrasound-guided FNA biopsy of bile duct and gallbladder: analysis of 53 cases. Cytopathology 2006; 17: 42-49
    CrossrefPubMedGoogle Scholar
  • 21 Stroup DF, Berlin JA, Morton SC. et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000; 283: 2008-2012
    Google Scholar
  • 22 Moher D, Liberati A, Tetzlaff J. et al. Preferred reporting items for systematic reviews and meta-analyses: The prisma statement. Ann Intern Med 2009; 151: 264-269
    CrossrefPubMedGoogle Scholar
  • 23 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 Cytologica 2011; 55: 401-407
    CrossrefPubMedGoogle Scholar
  • 24 Lee KJ, Kang YS, Cho MY. et al. Comparison of cytologic preparation methods in endoscopic ultrasound-guided fine needle aspiration for diagnosis of pancreatic adenocarcinoma. Pancreatology 2016; 16: 824-828
    CrossrefPubMedGoogle Scholar
  • 25 Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010; 25: 603-605
    CrossrefPubMedGoogle Scholar
  • 26 DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7: 177-188
    CrossrefPubMedGoogle Scholar
  • 27 Sutton AJ AK, Jones DR. et al. Methods for meta-analysis in medical research. New York: J. Wiley; 2000
    Google Scholar
  • 28 Higgins JP, Thompson SG, Deeks JJ. et al. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-560
    Google Scholar
  • 29 Mohan BP, Adler DG. Heterogeneity in systematic review and meta-analysis: how to read between the numbers. Gastrointest Endosc 2019; 89: 902-903
    CrossrefPubMedGoogle Scholar
  • 30 Duval S, Tweedie R. Trim and Fill: a simple funnel-plot–based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000; 56: 455-463
    CrossrefPubMedGoogle Scholar
  • 31 Rothstein HR, Sutton AJ, Borenstein M. Publication bias in meta-analysis: Prevention, assessment and adjustments. John Wiley & Sons; 2006
    Google Scholar
  • 32 Chun JW, Lee K, Lee SH. et al. Comparison of liquid-based cytology with conventional smear cytology for EUS-guided FNA of solid pancreatic masses: a prospective randomized noninferiority study. Gastrointest Endosc 2020; 91: 837-846.e831
    CrossrefPubMedGoogle Scholar
  • 33 Zhou W, Gao L, Wang S-M. et al. Comparison of smear cytology and liquid-based cytology in EUS-guided fine-needle aspiration of pancreatic lesion: experience from a large tertiary center. Gastrointest Endosc 2020; 91: 932-942
    CrossrefPubMedGoogle Scholar
  • 34 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. Digest Endosc 2017; 29: 608-616
    CrossrefPubMedGoogle Scholar
  • 35 de Luna R, Eloubeidi MA, Sheffield MV. et al. Comparison of ThinPrep and conventional preparations in pancreatic fine-needle aspiration biopsy. Diagnostic Cytopathology 2004; 30: 71-76
    CrossrefPubMedGoogle Scholar
  • 36 Lee YS, Son JH, Kim NH. et al. Diagnostic efficacy of liquid-based cytology in endoscopic ultrasoundguided fine-needle aspiration for solid pancreas lesion: Single academic institution experience. Pancreatology 2018; 18: S42
    CrossrefPubMedGoogle Scholar
  • 37 Qin SY, Zhou Y, Li P. et al. 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: e108762
    CrossrefPubMedGoogle Scholar
  • 38 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: 401-407
    CrossrefPubMedGoogle Scholar
  • 39 van Riet PA, Quispel R, Cahen DL. et al. Diagnostic yield and agreement on fine-needle specimens from solid pancreatic lesions : comparing the smear technique to liquid-based cytology. Endosc Int Open 2020; 8: E155-E162
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 40 Qin SY, Jiang HX, Zhang XL. et al. Evaluation of endoscopic ultrasound-guided fine-needle aspiration biopsy of cell block with immunostaining for panceatic lesions. J Digest Dis 2014; 1: 109
    PubMedGoogle Scholar
  • 41 Uehara H, Ikezawa K, Kawada N. et al. Diagnostic accuracy of endoscopic ultrasound-guided fine needle aspiration for suspected pancreatic malignancy in relation to the size of lesions. J Gastroenterol Hepatol 2011; 26: 1256-1261
    CrossrefPubMedGoogle Scholar
  • 42 Iglesias-Garcia J, Lariño-Noia J, Abdulkader I. et al. Rapid on-site evaluation of endoscopic-ultrasound-guided fine-needle aspiration diagnosis of pancreatic masses. World J Gastroenterol 2014; 20: 9451-9457
    CrossrefPubMedGoogle Scholar
  • 43 Iglesias-Garcia J, Dominguez-Munoz JE, Abdulkader I. et al. Influence of on-site cytopathology evaluation on the diagnostic accuracy of endoscopic ultrasound-guided fine needle aspiration (EUS-FNA) of solid pancreatic masses. Am J Gastroenterol 2011; 106: 1705-1710
    CrossrefPubMedGoogle Scholar
  • 44 Hocke M, Topalidis T, Braden B. et al. “Clinical” cytology for endoscopists: A practical guide. Endosc Ultrasound 2017; 6: 83-89
    CrossrefPubMedGoogle Scholar
  • 45 Biermann K, Escario MDL, Hebert-Magee S. et al. How to prepare, handle, read, and improve EUS-FNA and fine-needle biopsy for solid pancreatic lesions: The pathologist's role. Endoscopic Ultrasound 2017; 6: S95-S98
    CrossrefPubMedGoogle Scholar
  • 46 Chen J, Yang R, Lu Y. et al. Diagnostic accuracy of endoscopic ultrasound-guided fine-needle aspiration for solid pancreatic lesion: a systematic review. J Cancer Res Clin Oncol 2012; 138: 1433-1441
    CrossrefPubMedGoogle Scholar
  • 47 Hébert-Magee S, Bae S, Varadarajulu S. et al. 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: 159-171
    CrossrefPubMedGoogle Scholar
  • 48 van Riet PA, Cahen DL, Poley JW. et al. Mapping international practice patterns in EUS-guided tissue sampling: outcome of a global survey. Endosc Int Open 2016; 4: E360-E370
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 49 Biscotti CV, Hollow JA, Toddy SM. et al. ThinPrep versus conventional smear cytologic preparations in the analysis of thyroid fine-needle aspiration specimens. Am J Clinic Pathol 1995; 104: 150-153
    CrossrefPubMedGoogle Scholar
  • 50 Rossi ED, Raffaelli M, Zannoni GF. et al. Diagnostic efficacy of conventional as compared to liquid-based cytology in thyroid lesions: evaluation of 10,360 fine needle aspiration cytology cases. Acta Cytolog 2009; 53: 659-666
    CrossrefPubMedGoogle Scholar
  • 51 Michael CW. Liquid-Based Cytology Technique for Thyroid Cytology . . In Thyroid FNA Cytology: Springer 2019: 101-112
    PubMedGoogle Scholar
  • 52 Rivera R, Madera J. EP1086 Diagnostic accuracy of conventional cervical cytology (Papanicolau smear), liquid based cytology and visual inspection with acetic acid in detecting premalignant and malignant cervical lesions among Filipino women in a tertiary hospital. BMJ Special J 2019; 29: A569
    PubMedGoogle Scholar
  • 53 Hing E, Saraiya M, Roland K. Liquid-based cytology test use by office-based physicians: United States, 2006–2007. Nat Health Stat Rep 2011; 40: 1-6
    PubMedGoogle Scholar
  • 54 Arbyn M, Herbert A, Schenck U. et al. European guidelines for quality assurance in cervical cancer screening: recommendations for collecting samples for conventional and liquid‐based cytology. Cytopathology 2007; 18: 133-139
    CrossrefPubMedGoogle Scholar
  • 55 Hoda RS, VandenBussche C, Hoda SA. Liquid-Based Specimen Collection, Preparation, and Morphology. In, Diagnostic Liquid-Based Cytology: Springer 2017: 1-12
    PubMedGoogle Scholar
  • 56 Nayar R, Wilbur DC. The Bethesda System for Reporting Cervical Cytology. Acta Cytol 2017; 61: 359-372
    CrossrefPubMedGoogle Scholar
  • 57 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: 686-689
    CrossrefPubMedGoogle Scholar
  • 58 Gao L, Zhang M, He X. et al. Liquid-based cytology diagnosis of endoscopic ultrasound-guided fine needle aspiration of pancreatic lesions. Chinese J Pathol 2016; 45: 43-46
    PubMedGoogle Scholar
  • 59 Ohtani M, Ofuji K, Nosaka T. et al. Diagnostic utility of liquid-based cytology in EUS-FNA for pancreatic lesion and subepithelial tumor. Gastrointest Endosc 2018; 87: AB340
    CrossrefPubMedGoogle Scholar
  • 60 Pannala R, Hallberg-Wallace KM, Smith AL. et al. Endoscopic ultrasound-guided fine needle aspiration cytology of metastatic renal cell carcinoma to the pancreas: A multi-center experience. Cytojournal 2016; 13: 24
    CrossrefPubMedGoogle Scholar