Abstract
Background
Endoscopic ultrasonography (EUS)-guided liver biopsy is a novel technique to obtain adequate liver samples for diagnosis of liver parenchymal diseases. There are studies that have evaluated the feasibility and safety of EUS-guided parenchymal liver biopsy (EUS-LB), however, factors that can influence specimen quality are yet to be determined. Our aim was to determine the diagnostic accuracy of EUS-LB and evaluate factors associated with specimen quality.
Methods
We performed a detailed search of PubMed/MEDLINE and Web of Science™ databases to identify studies in which results of EUS-guided liver parenchymal biopsies were reported published up to July 2020. A random effects model was used to estimate pooled values (mean ± SE) for total specimen length (TSL) and complete portal tracts (CPT). Subgroup analyses were applied to find out the procedural factors associated with better specimen quality using Cochran’s Q test. A total of 10 meta-analyses were done focusing on international studies. Total of 1326 patients who underwent EUS-LB. EUS-LBs performed for suspicion of parenchymal liver disease. Pooled mean values for TSL and CPT with subgroup analyses.
Results
Twenty-three studies with a total of 1326 patients were included in our meta-analysis. Overall pooled mean TSL and CPT were 45.3 ± 4.6 mm and 15.8 ± 1.5, respectively. In subgroup analysis, core biopsy needles proved to better in terms of CPT than fine-needle aspiration needles (18.4 vs 10.99, p = 0.003). FNB with slow-pull or suction technique provided a similar TSL (44.3 vs 53.9 mm, p = 0.40), however, slow-pull technique was better in terms of CPT (30 vs 14.6, p < 0.001). Heterogeneity was present among the studies. Another limitation is the low number randomized control trials.
Conclusion
EUS-guided parenchymal liver biopsy is a good alternative to other methods of liver sampling. Using FNB needles with a slow-pull technique can provide better results.
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References
Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD (2009) American Association for the Study of Liver D. Liver biopsy. Hepatology 49:1017–1044
Boyum JH, Atwell TD, Schmit GD, Poterucha JJ, Schleck CD, Harmsen WS et al (2016) Incidence and risk factors for adverse events related to image-guided liver biopsy. Mayo Clin Proc 91:329–335
Seeff LB, Everson GT, Morgan TR, Curto TM, Lee WM, Ghany MG et al (2010) Complication rate of percutaneous liver biopsies among persons with advanced chronic liver disease in the HALT-C trial. Clin Gastroenterol Hepatol 8:877–883
Kalambokis G, Manousou P, Vibhakorn S, Marelli L, Cholongitas E, Senzolo M et al (2007) Transjugular liver biopsy—indications, adequacy, quality of specimens, and complications—a systematic review. J Hepatol 47:284–294
Nguyen P, Feng JC, Chang KJ (1999) Endoscopic ultrasound (EUS) and EUS-guided fine-needle aspiration (FNA) of liver lesions. Gastrointest Endosc 50:357–361
Jhala NC, Jhala D, Eltoum I, Vickers SM, Wilcox CM, Chhieng DC et al (2004) Endoscopic ultrasound-guided fine-needle aspiration biopsy: a powerful tool to obtain samples from small lesions. Cancer 102:239–246
tenBerge J, Hoffman BJ, Hawes RH, Van Enckevort C, Giovannini M, Erickson RA et al (2002) EUS-guided fine needle aspiration of the liver: indications, yield, and safety based on an international survey of 167 cases. Gastrointest Endosc 55:859–862
Shah ND, Baron TH (2018) Endoscopic ultrasound and the liver: current applications and beyond. J Hepatobiliary Pancreat Sci 25:171–180
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 62:1006–12
McInnes MDF, Moher D, Thombs BD, McGrath TA, Bossuyt PM, the P-DTAG et al (2018) Preferred reporting ıtems for a systematic review and meta-analysis of diagnostic test accuracy studies: the PRISMA-DTA statement. JAMA 319:388–396
Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536
Luo D, Wan X, Liu J, Tong T (2018) Optimally estimating the sample mean from the sample size, median, mid-range, and/or mid-quartile range. Stat Methods Med Res 27:1785–1805
Wan X, Wang W, Liu J, Tong T (2014) Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol 14:135
Shi J, Luo D, Weng H, Zeng XT, Lin L, Chu H et al (2020) Optimally estimating the sample standard deviation from the five-number summary. Res Synth Methods 11:641–654
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560
Deeks JJ (2001) Systematic reviews in health care: systematic reviews of evaluations of diagnostic and screening tests. BMJ 323:157–162
Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558
Nakanishi Y, Mneimneh WS, Sey M, Al-Haddad M, DeWitt JM, Saxena R (2015) One hundred thirteen consecutive transgastric liver biopsies for hepatic parenchymal diseases: a single-institution study. Am J Surg Pathol 39:968–976
Saab S, Phan J, Jimenez MA, Grotts JF, Walters L, Hathaway KA et al (2017) Endoscopic ultrasound liver biopsies accurately predict the presence of fibrosis in patients with fatty liver. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc 15:1477–1478
Johal AS, Khara HS, Maksimak MG, Diehl DL (2014) Endoscopic ultrasound-guided liver biopsy in pediatric patients. Endosc Ultrasound 3:191–194
Aggarwal SN, Magdaleno T, Shah H, Shah S, Goonewardene S (2019) Endoscopıc ultrasound-guıded fıne needle lıver bıopsy: a sıngle-center experıence at a large, quartenary care center. Gastrointest Endosc 89:AB305
Earasi AG, Lynch S, Jahann DA, Sauer BG, Wang AY, Uppal D et al (2019) Transjugular vs. EUS-guıded lıver bıopsy: whıch modalıty ıs better? Gastrointest Endosc 89:AB326
Sampath K, Gordon SR, Toor A, Dinani A, Dickson RC, Suriawinata A et al (2017) Endoscopic ultrasound-guided liver biopsy: comparing the diagnostic yield and safety between the 19-gauge and 22-gauge needle. Gastrointest Endosc 85:AB479
Sarkar A, Shahid H, Tyberg A, Andalib I, Kahaleh M, Gaidhane M et al (1090A) Endoscopic ultrasound (EUS) guided liver biopsy: a single center experience. Hepatology 70:1089A–1090A
Shahshahan M, Gertz H, Fakhreddine AY, Datta A, Eysselein VE, Reicher S et al (2017) Endoscopic ultrasound-guided liver biopsy versus percutaneous and trans-jugular liver biopsy for evaluation of liver parenchyma. Gastrointest Endosc 85:AB490
Mathew A (2007) EUS-guided routine liver biopsy in selected patients. Am J Gastroenterol 102:2354–2355
Phillips B, Lo DY, Forsthoefel K, Speck O, Turner B (2018) Adequacy of endoscopic ultrasound-guided liver fine needle biopsies using a 20-gauge needle. Am J Gastroenterol 113:S1230–S1231
Ali AH, Panchal S, Rao DS, Gan Y, Al-Juboori A, Samiullah S et al (2020) The efficacy and safety of endoscopic ultrasound-guided liver biopsy versus percutaneous liver biopsy in patients with chronic liver disease: a retrospective single-center study. J Ultrasound 23:157–167
Bazerbachi F, Vargas EJ, Matar R, Storm AC, Mounajjed TM, Topazian MD et al (2019) EUS-guided core liver biopsy sampling using a 22-gauge fork-tip needle: a prospective blinded trial for histologic and lipidomic evaluation in nonalcoholic fatty liver disease. Gastrointest Endosc 90:926–932
Ching-Companioni RA, Diehl DL, Johal AS, Confer BD, Khara HS (2019) 19 G aspiration needle versus 19 G core biopsy needle for endoscopic ultrasound-guided liver biopsy: a prospective randomized trial. Endoscopy 51:1059–1065
Diehl DL, Johal AS, Khara HS, Stavropoulos SN, Al-Haddad M, Ramesh J et al (2015) Endoscopic ultrasound-guided liver biopsy: a multicenter experience. Endosc Int Open 3:E210–E215
Gleeson FC, Clayton AC, Zhang L, Clain JE, Gores GJ, Rajan E et al (2008) Adequacy of endoscopic ultrasound core needle biopsy specimen of nonmalignant hepatic parenchymal disease. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc 6:1437–1440
Gor N, Salem SB, Jakate S, Patel R, Shah N, Patil A (2014) Histological adequacy of EUS-guided liver biopsy when using a 19-gauge non-Tru-Cut FNA needle. Gastrointest Endosc 79:170–172
Hasan MK, Kadkhodayan K, Idrisov E, Ali S, Rafiq E, Ben-Ami Shor D et al (2019) Endoscopic ultrasound-guided liver biopsy using a 22-G fine needle biopsy needle: a prospective study. Endoscopy 51:818–824
Hashimoto R, Lee DP, Samarasena JB, Chandan VS, Guo W, Lee JG et al (2020) Comparison of two specialized histology needles for endoscopic ultrasound (EUS)-guided liver biopsy: a pilot study. Dig Dis Sci. https://doi.org/10.1007/s10620-020-06391-3
Mok SRS, Diehl DL, Johal AS, Khara HS, Confer BD, Mudireddy PR et al (2018) A prospective pilot comparison of wet and dry heparinized suction for EUS-guided liver biopsy (with videos). Gastrointest Endosc 88:919–925
Mok SRS, Diehl DL, Johal AS, Khara HS, Confer BD, Mudireddy PR et al (2019) Endoscopic ultrasound-guided biopsy in chronic liver disease: a randomized comparison of 19-G FNA and 22-G FNB needles. Endosc Int Open 7:E62–E71
Nieto J, Dawod E, Deshmukh A, Penn E, Adler D, Saab S (2020) EUS-guided fine-needle core liver biopsy with a modified one-pass, one-actuation wet suction technique comparing two types of EUS core needles. Endosc Int Open 8:E938–E943
Patel HK, Saxena R, Rush N, Patel SK, Dasari CS, Mneimneh W et al (2020) A comparative study of 22G versus 19G needles for EUS-guided biopsies for parenchymal liver disease: are thinner needles better? Dig Dis Sci. https://doi.org/10.1007/s10620-020-06165-x
Sey MS, Al-Haddad M, Imperiale TF, McGreevy K, Lin J, DeWitt JM (2016) EUS-guided liver biopsy for parenchymal disease: a comparison of diagnostic yield between two core biopsy needles. Gastrointest Endosc 83:347–352
Shah ND, Sasatomi E, Baron TH (2017) Endoscopic ultrasound-guided parenchymal liver biopsy: single center experience of a new dedicated core needle. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc 15:784–786
Shuja A, Alkhasawneh A, Fialho A, Fialho A, Shukri A, Harris C et al (2019) Comparison of EUS-guided versus percutaneous and transjugular approaches for the performance of liver biopsies. Dig Liver Dis Off J Ital Soc Gastroenterol Ital Assoc Study Liver 51:826–830
Stavropoulos SN, Im GY, Jlayer Z, Harris MD, Pitea TC, Turi GK et al (2012) High yield of same-session EUS-guided liver biopsy by 19-gauge FNA needle in patients undergoing EUS to exclude biliary obstruction. Gastrointest Endosc 75:310–318
Bhat I, Malvar G, Calmet F, Bonder A, Nasser IA, Sawhney M et al (2019) EUS-guıded lıver bıopsy usıng 22G FNB vs. 19G FNB needles: a prospectıve comparıson of core specımen sıze and dıagnostıc adequacy. Gastrointest Endosc 89:AB293
Ching-Companioni R, Johal AS, Confer B, Khara HS, Forster E, Diehl DL (2018) One versus three needle actuations for EUS-guided liver biopsy: a prospective randomized trial. Am J Gastroenterol 113:S420
El Chafic AH, Mubarak MF, Shah J, Therapondos G, Romero R, Evans J et al (2018) Endoscopic ultrasound-guided liver biopsy compared to percutaneous and transjugular liver biopsy: a tertiary center experience. Am J Gastroenterol 113:S421
Ellis DJ, Therapondos G, Shah JN, Cohen A, Galliano GE, Romero RV et al (2019) Simultaneous biliary and liver parenchymal evaluation in post liver-transplant population using endoscopic ultrasound-guided liver biopsy and endoscopic retrograde cholangiopancreatography in a single session approach. Am J Gastroenterol 114:S501–S502
Foor-Pessin C, Bittner K, Kothari S, Sharma M, Zhou ZR, Sharma A et al (2017) Histologic yield of endoscopic ultrasound guided liver biopsy compared to percutaneous and transjugular approaches: a single-center retrospective review. Gastrointest Endosc 85:AB485–AB486
Rombaoa C, Chen AM (2018) The safety and feasıbılıty of endoscopıc ultrasound-guıded parenchymal lıver bıopsy at a large communıty hospıtal. Gastrointest Endosc 87:AB458
Shimizu T, Fortinsky KJ, Tsujino T, Lu YX, Chin MA, Samarasena JB et al (2018) EUS guıded lıver bıopsy ın benıgn lıver dısease usıng heparanızed needle technıque (HNT). Gastrointest Endosc 87:AB346
Pineda JJ, Diehl DL, Miao CL, Johal AS, Khara HS, Bhanushali A et al (2016) EUS-guided liver biopsy provides diagnostic samples comparable with those via the percutaneous or transjugular route. Gastrointest Endosc 83:360–365
Sporea I, Sirli R, Popescu A, Cornianu M, Manciu C, Focsa M (2007) The quality of the fragment obtained by liver biopsy for staging chronic hepatitis. J Gastrointest Liver Dis 16:263–266
Schiano TD, Azeem S, Bodian CA, Bodenheimer HC Jr, Merati S, Thung SN et al (2005) Importance of specimen size in accurate needle liver biopsy evaluation of patients with chronic hepatitis C. Clin Gastroenterol Hepatol 3:930–935
European Association for Study of L, Asociacion Latinoamericana para el Estudio del H (2015) EASL-ALEH Clinical Practice Guidelines: non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol 63:237–264
Fryer E, Wang LM, Verrill C, Fleming K (2013) How often do our liver core biopsies reach current definitions of adequacy? J Clin Pathol 66:1087–1089
Al Knawy B, Shiffman M (2007) Percutaneous liver biopsy in clinical practice. Liver Int 27:1166–1173
Mohan BP, Shakhatreh M, Garg R, Ponnada S, Adler DG (2019) Efficacy and safety of EUS-guided liver biopsy: a systematic review and meta-analysis. Gastrointest Endosc 89:238–246.e3
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Dr. Nirav Thosani reports other from Boston Scientific, other from Medtronic, primarily as a consultant outside the submitted work. Drs. Bulent Baran, Santosh Kale, Prithvi Patil, Bijun Kannadath, Srinivas Ramireddy, Ricardo Badillo and Tomas Davee have no conflicts of interest or financial ties to disclose.
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464_2020_8053_MOESM1_ESM.tif
Supplementary figure 1. Forrest plots for (a) total specimen length (TSL) and (b) complete portal tracts (CPT) for comparison of suction vs no suction techniques. (TIF 137 kb)
464_2020_8053_MOESM3_ESM.tif
Supplementary figure 2. Forrest plots for (a) total specimen length (TSL) and (b) complete portal tracts (CPT) for comparison of 19G vs 22G EUS needles. (TIF 139 kb)
464_2020_8053_MOESM5_ESM.tif
Supplementary figure 3. Forrest plots for (a) total specimen length (TSL) and (b) complete portal tracts (CPT) for comparison of novel core needles. (TIF 75 kb)
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Baran, B., Kale, S., Patil, P. et al. Endoscopic ultrasound-guided parenchymal liver biopsy: a systematic review and meta-analysis. Surg Endosc 35, 5546–5557 (2021). https://doi.org/10.1007/s00464-020-08053-x
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DOI: https://doi.org/10.1007/s00464-020-08053-x