CC BY-NC-ND 4.0 · Endosc Int Open 2020; 08(10): E1280-E1290
DOI: 10.1055/a-1194-4085
Original article

Endoscopic ultrasound-guided through-the-needle microforceps biopsy improves diagnostic yield for pancreatic cystic lesions: a systematic review and meta-analysis

Thomas McCarty
1   Division of Gastroenterology, Hepatology and Endoscopy, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, United States
,
Tarun Rustagi
2   Division of Gastroenterology and Hepatology, University of New Mexico, Albuquerque, New Mexico, United States
› Author Affiliations

Abstract

Background and study aims Given variable diagnostic yield of endoscopic ultrasound (EUS)-guided fine-needle aspiration (FNA) for pancreatic cystic lesions (PCLs), a through-the-needle (TTN) microforceps biopsy device passed through a 19-gauge FNA needle has been devised to improve tissue sampling. This was a systematic review and meta-analysis to evaluate the feasibility, diagnostic yield, and safety of EUS-guided TTN microforceps biopsy for diagnosis of PCLs.

Methods Individualized searches were developed in accordance with PRISMA and MOOSE guidelines. This was a cumulative meta-analysis performed by calculating pooled proportions with rates estimated using random effects models. Measured outcomes included pooled technical success, diagnostic yield, accuracy, and procedure-associated adverse events (AEs) as well as comparison to conventional FNA.

Results Eleven studies (n = 518 patients; mean age 64.13 ± 5.83 years; 58.19 % female) were included. Mean PCL size was 33.39 ± 3.72 mm with the pancreatic head/uncinate (35.50 %) being the most common location. A mean of 2.47 ± 0.92 forceps passes were performed with a mean of 2.79 ± 0.81 microbiopsies obtained per lesion. Pooled technical success was 97.12 % (95 % CI, 93.73–98.71; I2 = 34.49) with a diagnostic yield of 79.60 % (95 % CI, 72.62–85.16; I2 = 56.00), and accuracy of 82.76 % [(95 % CI, 77.80–86.80; I2 = 0.00). The pooled serious adverse event rate was 1.08 % (95 % CI, 0.43–2.69; I2 = 0.00). Compared to conventional FNA, TTN microforceps biopsy resulted in significant improvement in diagnostic yield [OR 4.79 (95 % CI: 1.52–15.06; P = 0.007)] and diagnostic accuracy [OR 8.69 (95 % CI, 1.12–67.12; P = 0.038)], respectively.

Conclusions EUS-guided TTN microforceps biopsy appears to be safe and effective for diagnosis of PCLs with improvement in diagnostic yield and accuracy when compared to FNA alone.

Supplementary material



Publication History

Received: 20 February 2020

Accepted: 09 April 2020

Article published online:
22 September 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/)

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  • References

  • 1 de Jong K, Nio CY, Hermans JJ. et al. High prevalence of pancreatic cysts detected by screening magnetic resonance imaging examinations. Clin Gastroenterol Hepatol 2010; 8: 806-811
  • 2 Laffan TA, Horton KM, Klein AP. et al. Prevalence of unsuspected pancreatic cysts on MDCT. AJR Am J Roentgenol 2008; 191: 802-807
  • 3 Bosman FT, Carneiro F, Hruban RH. et al. WHO classification of tumours of the digestive system. 4th ed. Lyon: International Agency for Research on Cancer; 2010
  • 4 Elta GH, Enestvedt BK, Sauer BG. et al. ACG Clinical Guideline: Diagnosis and Management of Pancreatic Cysts. Am J Gastroenterol 2018; 113: 464-479
  • 5 Khan MA, Grimm IS, Ali B. et al. A meta-analysis of endoscopic ultrasound-fine-needle aspiration compared to endoscopic ultrasound-fine-needle biopsy: diagnostic yield and the value of onsite cytopathological assessment. Endosc Int Open 2017; 5: E363-E75
  • 6 Vege SS, Ziring B, Jain R. et al. American Gastroenterological Association institute guideline on the diagnosis and management of asymptomatic neoplastic pancreatic cysts. Gastroenterology 2015; 148: 819-822; quize12-3
  • 7 Del Chiaro M, Verbeke C, Salvia R. et al. European experts consensus statement on cystic tumours of the pancreas. Dig Liver Dis 2013; 45: 703-711
  • 8 Tanaka M, Fernandez-del Castillo C, Adsay V. et al. International consensus guidelines 2012 for the management of IPMN and MCN of the pancreas. Pancreatology 2012; 12: 183-197
  • 9 Rogart JN, Loren DE, Singu BS. et al. Cyst wall puncture and aspiration during EUS-guided fine needle aspiration may increase the diagnostic yield of mucinous cysts of the pancreas. J Clin Gastroenterol 2011; 45: 164-169
  • 10 Muthusamy VR, Chandrasekhara V. ASGE Standard of Practice Committee. et al. The role of endoscopy in the diagnosis and treatment of cystic pancreatic neoplasms. Gastrointest Endosc 2016; 84: 1-9
  • 11 Liberati A, Altman DG, Tetzlaff J. et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Annals Int Med 2009; 151: W65-W94
  • 12 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
  • 13 Cotton PB, Eisen GM, Aabakken L. et al. A lexicon for endoscopic adverse events: report of an ASGE workshop. Gastrointest Endosc 2010; 71: 446-454
  • 14 DerSimonian R, Laird N. Meta-analysis in clinical trials. Controlled Clin Trials 1986; 7: 177-188
  • 15 Stuart A, Ord JK. Kendall’s Advanced Theory of Statistics. 6th ed. London: Edward Arnold; 1994
  • 16 Riley RD, Higgins JPT, Deeks JJ. Research methods & reporting: interpretation of random effects meta-analyses. Br Med J 2011; 342: d549
  • 17 Higgins JP, Thompson SG, Deeks JJ. et al. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-560
  • 18 Overton RC. A comparison of fixed-effects and mixed (random-effects) models for meta-analysis tests of moderator variable effects. Psycholog Methods 1998; 3: 354-379
  • 19 Wells G, Shea B. et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analysis. 3rd Symposium on Systematic Reviews: Beyond the Basics; July 3–5 2000. Oxford: 2000 Available at (Accessed 24 November 2019): http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
  • 20 Higgins JPT, Altman DG, Sterne JAC. Cochrane Handbook for Systematic Reviews of Interventions. In: Higgins JPT. Available from: www.cochranehandbook.com
  • 21 Borenstein M, Hedges LV, Higgins JP. et al. Introduction to meta-analysis. Hoboken: John Wiley & Sons; 2011
  • 22 Borenstein M, Higgins JP, Hedges LV. et al. Basics of meta-analysis: I(2) is not an absolute measure of heterogeneity. Res Synth Methods 2017; 8: 5-18
  • 23 Egger M, Davey Smith G, Schneider M. et al. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315: 629-634
  • 24 Easterbrook PJ, Berlin JA, Gopalan R. et al. Publication bias in clinical research. Lancet 1991; 337: 867-672
  • 25 Duval S, Tweedie R. Trim and fill: a simple funnel-plot–based method of testing and adjusting for publication bias in metaanalysis. Biometrics 2000; 56: 455-463
  • 26 Kovacevic B, Karstensen JG, Havre RF. et al. Initial experience with EUS-guided microbiopsy forceps in diagnosing pancreatic cystic lesions: A multicenter feasibility study (with video). Endosc Ultrasound 2018; 7: 383-388
  • 27 Mittal C, Obuch JC, Hammad H. et al. Technical feasibility, diagnostic yield, and safety of microforceps biopsies during EUS evaluation of pancreatic cystic lesions (with video). Gastrointest Endosc 2018; 87: 1263-1269
  • 28 Yang D, Samarasena JB, Jamil LH. et al. Endoscopic ultrasound-guided through-the-needle microforceps biopsy in the evaluation of pancreatic cystic lesions: a multicenter study. Endosc Int Open 2018; 6: E1423-E30
  • 29 Zhang ML, Arpin RN, Brugge WR. et al. Moray micro forceps biopsy improves the diagnosis of specific pancreatic cysts. Cancer Cytopathol 2018; 126: 414-420
  • 30 Cheesman AR, Zhu H, Liao X. et al. Impact of EUS-guided microforceps biopsy and needle-based confocal laser endomicroscopy on the diagnostic yield and clinical management of pancreatic cystic lesions. Gastrointest Endosc 2020; 91: 1095-1104
  • 31 Crino SF, Bernardoni L, Brozzi L. et al. Association between macroscopically visible tissue samples and diagnostic accuracy of EUS-guided through-the-needle microforceps biopsy sampling of pancreatic cystic lesions. Gastrointest Endosc 2019; 90: 933-943
  • 32 Hashimoto R, Lee JG, Chang KJ. et al. Endoscopic ultrasound-through-the-needle biopsy in pancreatic cystic lesions: A large single center experience. World J Gastrointest Endosc 2019; 11: 531-540
  • 33 Robles-Medrandra C, Olmos JI, Oleas R. et al. EUS-Through-the-needle technologies in the diagnosis and malignancy detection of pancreatic cysts: a comparative study between different technologies. Gastrointest Endosc 2019; 89: AB608-A609
  • 34 Vestrup Rift C, Melchior LC, Kovacevic B. et al. Next-generation sequencing of endoscopic ultrasound guided microbiopsies from pancreatic cystic neoplasms. Histopathology 2019; 75: 767-771
  • 35 Wilen J, Visrodia K, Lan G. et al. The feasibility and value of cyst wall biopsy using micro forceps in the diagnosis of pancreatic cysts. Gastrointest Endosc 2019; 89: AB605
  • 36 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: 1587-1596
  • 37 Zerboni G, Signoretti M, Crippa S. et al. Systematic review and meta-analysis: Prevalence of incidentally detected pancreatic cystic lesions in asymptomatic individuals. Pancreatology 2019; 19: 2-9
  • 38 Farrell JJ. Prevalence, diagnosis and management of pancreatic cystic neoplasms: current status and future directions. Gut Liver 2015; 9: 571-589
  • 39 Buscarini E. et al. Italian Association of Hospital Gastroenterologists and Endoscopists, Italian Association for the Study of the Pancreas. Italian consensus guidelines for the diagnostic work-up and follow-up of cystic pancreatic neoplasms. Dig Liver Dis 2014; 46: 479-493
  • 40 de Pretis N, Mukewar S, Aryal-Khanal A. et al. Pancreatic cysts: Diagnostic accuracy and risk of inappropriate resections. Pancreatology 2017; 17: 267-272
  • 41 Larino-Noia J, Iglesias-Garcia J, de la Iglesia-Garcia D. et al. EUS-FNA in cystic pancreatic lesions: Where are we now and where are we headed in the future?. Endosc Ultrasound 2018; 7: 102-109
  • 42 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: 1330-1336
  • 43 Cizginer S, Turner BG, Bilge AR. et al. Cyst fluid carcinoembryonic antigen is an accurate diagnostic marker of pancreatic mucinous cysts. Pancreas 2011; 40: 1024-1028
  • 44 Gaddam S, Ge PS, Keach JW. et al. Suboptimal accuracy of carcinoembryonic antigen in differentiation of mucinous and nonmucinous pancreatic cysts: results of a large multicenter study. Gastrointest Endosc 2015; 82: 1060-1069
  • 45 Khalid A, Zahid M, Finkelstein SD. et al. Pancreatic cyst fluid DNA analysis in evaluating pancreatic cysts: a report of the PANDA study. Gastrointest Endosc 2009; 69: 1095-1102
  • 46 Nakai Y, Iwashita T, Park DH. et al. Diagnosis of pancreatic cysts: EUS-guided, through-the-needle confocal laser-induced endomicroscopy and cystoscopy trial: DETECT study. Gastrointest Endosc 2015; 81: 1204-1214
  • 47 Singhi AD, Nikiforova MN, Fasanella KE. et al. Preoperative GNAS and KRAS testing in the diagnosis of pancreatic mucinous cysts. Clin Cancer Res 2014; 20: 4381-4389
  • 48 Iglesias-Garcia J, Larino-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
  • 49 Klapman JB, Logrono R, Dye CE. et al. Clinical impact of on-site cytopathology interpretation on endoscopic ultrasound-guided fine needle aspiration. Am J Gastroenterol 2003; 98: 1289-1294
  • 50 European Study Group on Cystic Tumours of the Pancreas. European evidence-based guidelines on pancreatic cystic neoplasms. Gut 2018; 67: 789-804
  • 51 Aparicio JR, Martinez J, Niveiro M. et al. Direct intracystic biopsy and pancreatic cystoscopy through a 19-gauge needle EUS (with videos). Gastrointest Endosc 2010; 72: 1285-1288
  • 52 Barresi L, Tarantino I, Ligresti D. et al. A new tissue acquisition technique in pancreatic cystic neoplasm: endoscopic ultrasound-guided through-the-needle forceps biopsy. Endoscopy 2015; 47 (Suppl. 01) E297-E298
  • 53 Shakhatreh MH, Naini SR, Brijbassie AA. et al. Use of a novel through-the-needle biopsy forceps in endoscopic ultrasound. Endosc Int Open 2016; 4: E439-E442
  • 54 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
  • 55 Faber T, Ravaud P, Riveros C. et al. Meta-analyses including non-randomized studies of therapeutic interventions: a methodological review. BMC Med Res Methodol 2016; 16: 35
  • 56 Basar O, Yuksel O, Yang DJ. et al. Feasibility and safety of microforceps biopsy in the diagnosis of pancreatic cysts. Gastrointest Endosc 2018; 88: 79-86
  • 57 Kovacevic B, Klausen P, Hasselby JP. et al. A novel endoscopic ultrasound-guided through-the-needle microbiopsy procedure improves diagnosis of pancreatic cystic lesions. Endoscopy 2018; 50: 1105-1111
  • 58 Barresi L, Crino SF, Fabbri C. et al. Endoscopic ultrasound-through-the-needle biopsy in pancreatic cystic lesions: A multicenter study. Dig Endosc 2018; 30: 760-770
  • 59 Samarasena J, Yu A, Lee D. et al. EUS-guided through-the-needle biopsy for pancreatic cystic lesions. VideoGIE 2019; 4: 436-439
  • 60 Kohoutova D, Zar S, Repak R. et al. Pancreatic Cysts: Diagnostic role of EUS-guided microforceps biopsy and confocal laser endomicroscopy. Gastroenterol Res Pract 2019; 2019: 3431048