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Published in: Hepatology International 3/2019

01-05-2019 | Ultrasound | Original Article

Bi-lobar liver biopsy via EUS enhances the assessment of disease severity in patients with non-alcoholic steatohepatitis

Authors: Sandeep Khurana, Waseem Butt, Harshit S. Khara, Amitpal S. Johal, Sara F. West, Zong-Ming E. Chen, Andrea L. Berger, David L. Diehl

Published in: Hepatology International | Issue 3/2019

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Abstract

Background

In patients with non-alcoholic fatty liver disease (NAFLD), all-cause mortality increases with fibrosis stage. Liver biopsy (LB), performed predominantly in the right lobe, assesses fibrosis, however, right lobe LB may not be sufficient due to histological variation in different lobes. Endoscopic ultrasound (EUS) allows for biopsy of right and left liver lobes in the same setting.

Methods

This retrospective study assessed for histologic variability amongst left and right liver lobe (L:R) specimens obtained via EUS at a tertiary care center. Between January 2012 and December 2015, 38 NAFLD patients underwent LB, in whom both lobes were sampled.

Results

L:R agreement was near-perfect for steatosis (κ = 0.816, 95% CI 0.674, 0.958), good for ballooning (κ = 0.740, 95% CI 0.565, 0.916) and moderate for lobular inflammation (κ = 0.401 95% CI 0.110, 0.692) and fibrosis (κ = 0.473, 95% CI 0.275, 0.672). Intra-observer variability assessed by blinded repeat slide readings was almost perfect for fibrosis and steatosis (κ = 1, 95% CI 1, 1 and κ = 0.939, 95% CI 0.881, 0.997 respectively) and substantial for lobular inflammation (κ = 0.725, 95% CI 0.584, 0.866). Only right lobe assessment underestimated fibrosis in 21%, inflammation in 13%, and steatosis and ballooning in 8% cases.

Conclusions

These data indicate that in NAFLD, due to regional variation, EUS-guided bi-lobar LB improves assessment of disease activity and fibrosis.
Literature
1.
go back to reference Williams CD, Stengel J, Asike MI, Torres DM, Shaw J, Contreras M, et al. Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology. 2011;140(1):124–131CrossRefPubMed Williams CD, Stengel J, Asike MI, Torres DM, Shaw J, Contreras M, et al. Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology. 2011;140(1):124–131CrossRefPubMed
2.
go back to reference Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther. 2011;34(3):274–285CrossRef Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther. 2011;34(3):274–285CrossRef
3.
go back to reference Lazo M, Hernaez R, Eberhardt MS, Bonekamp S, Kamel I, Guallar E, et al. Prevalence of nonalcoholic fatty liver disease in the United States: the Third National Health and Nutrition Examination Survey, 1988–1994. Am J Epidemiol. 2013;178(1):38–45CrossRefPubMedPubMedCentral Lazo M, Hernaez R, Eberhardt MS, Bonekamp S, Kamel I, Guallar E, et al. Prevalence of nonalcoholic fatty liver disease in the United States: the Third National Health and Nutrition Examination Survey, 1988–1994. Am J Epidemiol. 2013;178(1):38–45CrossRefPubMedPubMedCentral
4.
5.
go back to reference Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD. American Association for the Study of Liver D Liver biopsy. Hepatology. 2009;49(3):1017–1044CrossRef Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD. American Association for the Study of Liver D Liver biopsy. Hepatology. 2009;49(3):1017–1044CrossRef
6.
go back to reference Kalambokis G, Manousou P, Vibhakorn S, Marelli L, Cholongitas E, Senzolo M, et al. Transjugular liver biopsy–indications, adequacy, quality of specimens, and complications–a systematic review. J Hepatol. 2007;47(2):284–294CrossRefPubMed Kalambokis G, Manousou P, Vibhakorn S, Marelli L, Cholongitas E, Senzolo M, et al. Transjugular liver biopsy–indications, adequacy, quality of specimens, and complications–a systematic review. J Hepatol. 2007;47(2):284–294CrossRefPubMed
7.
go back to reference Chisholm J, Seki Y, Toouli J, Stahl J, Collins J, Kow L. Serologic predictors of nonalcoholic steatohepatitis in a population undergoing bariatric surgery. Surg Obes Relat Dis. 2012;8(4):416–422CrossRef Chisholm J, Seki Y, Toouli J, Stahl J, Collins J, Kow L. Serologic predictors of nonalcoholic steatohepatitis in a population undergoing bariatric surgery. Surg Obes Relat Dis. 2012;8(4):416–422CrossRef
8.
go back to reference Pineda JJ, Diehl DL, Miao CL, Johal AS, Khara HS, Bhanushali A, et al. EUS-guided liver biopsy provides diagnostic samples comparable with those via the percutaneous or transjugular route. Gastrointest Endosc. 2016;83(2):360–365CrossRefPubMed Pineda JJ, Diehl DL, Miao CL, Johal AS, Khara HS, Bhanushali A, et al. EUS-guided liver biopsy provides diagnostic samples comparable with those via the percutaneous or transjugular route. Gastrointest Endosc. 2016;83(2):360–365CrossRefPubMed
9.
go back to reference Diehl DL, Johal AS, Khara HS, Stavropoulos SN, Al-Haddad M, Ramesh J, et al. Endoscopic ultrasound-guided liver biopsy: a multicenter experience. Endosc Int Open. 2015;3(3):E210–E215215CrossRefPubMedPubMedCentral Diehl DL, Johal AS, Khara HS, Stavropoulos SN, Al-Haddad M, Ramesh J, et al. Endoscopic ultrasound-guided liver biopsy: a multicenter experience. Endosc Int Open. 2015;3(3):E210–E215215CrossRefPubMedPubMedCentral
10.
go back to reference Baunsgaard P, Sanchez GC, Lundborg CJ. The variation of pathological changes in the liver evaluated by double biopsies. Acta Pathol Microbiol Scand A. 1979;87(1):51–57PubMed Baunsgaard P, Sanchez GC, Lundborg CJ. The variation of pathological changes in the liver evaluated by double biopsies. Acta Pathol Microbiol Scand A. 1979;87(1):51–57PubMed
11.
go back to reference Abdi W, Millan JC, Mezey E. Sampling variability on percutaneous liver biopsy. Arch Intern Med. 1979;139(6):667–669CrossRefPubMed Abdi W, Millan JC, Mezey E. Sampling variability on percutaneous liver biopsy. Arch Intern Med. 1979;139(6):667–669CrossRefPubMed
12.
go back to reference Labayle D, Chaput JC, Albuisson F, Buffet C, Martin E, Etienne JP. Comparison of the histological lesions in tissue specimens taken from the right and left lobe of the liver in alcoholic liver disease (author's transl). Gastroenterol Clin Biol. 1979;3(3):235–240PubMed Labayle D, Chaput JC, Albuisson F, Buffet C, Martin E, Etienne JP. Comparison of the histological lesions in tissue specimens taken from the right and left lobe of the liver in alcoholic liver disease (author's transl). Gastroenterol Clin Biol. 1979;3(3):235–240PubMed
13.
go back to reference Maharaj B, Maharaj RJ, Leary WP, Cooppan RM, Naran AD, Pirie D, et al. Sampling variability and its influence on the diagnostic yield of percutaneous needle biopsy of the liver. Lancet. 1986;1(8480):523–525CrossRefPubMed Maharaj B, Maharaj RJ, Leary WP, Cooppan RM, Naran AD, Pirie D, et al. Sampling variability and its influence on the diagnostic yield of percutaneous needle biopsy of the liver. Lancet. 1986;1(8480):523–525CrossRefPubMed
14.
go back to reference Regev A, Berho M, Jeffers LJ, Milikowski C, Molina EG, Pyrsopoulos NT, et al. Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol. 2002;97(10):2614–2618CrossRef Regev A, Berho M, Jeffers LJ, Milikowski C, Molina EG, Pyrsopoulos NT, et al. Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol. 2002;97(10):2614–2618CrossRef
15.
go back to reference Bedossa P, Dargere D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology. 2003;38(6):1449–1577CrossRefPubMed Bedossa P, Dargere D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology. 2003;38(6):1449–1577CrossRefPubMed
16.
go back to reference Olsson R, Hagerstrand I, Broome U, Danielsson A, Jarnerot G, Loof L, et al. Sampling variability of percutaneous liver biopsy in primary sclerosing cholangitis. J Clin Pathol. 1995;48(10):933–935CrossRefPubMedPubMedCentral Olsson R, Hagerstrand I, Broome U, Danielsson A, Jarnerot G, Loof L, et al. Sampling variability of percutaneous liver biopsy in primary sclerosing cholangitis. J Clin Pathol. 1995;48(10):933–935CrossRefPubMedPubMedCentral
17.
go back to reference Skripenova S, Trainer TD, Krawitt EL, Blaszyk H. Variability of grade and stage in simultaneous paired liver biopsies in patients with hepatitis C. J Clin Pathol. 2007;60(3):321–324CrossRefPubMed Skripenova S, Trainer TD, Krawitt EL, Blaszyk H. Variability of grade and stage in simultaneous paired liver biopsies in patients with hepatitis C. J Clin Pathol. 2007;60(3):321–324CrossRefPubMed
18.
go back to reference Siddique I, El-Naga HA, Madda JP, Memon A, Hasan F. Sampling variability on percutaneous liver biopsy in patients with chronic hepatitis C virus infection. Scand J Gastroenterol. 2003;38(4):427–432CrossRefPubMed Siddique I, El-Naga HA, Madda JP, Memon A, Hasan F. Sampling variability on percutaneous liver biopsy in patients with chronic hepatitis C virus infection. Scand J Gastroenterol. 2003;38(4):427–432CrossRefPubMed
19.
go back to reference Ratziu V, Charlotte F, Heurtier A, Gombert S, Giral P, Bruckert E, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128(7):1898–1906CrossRefPubMed Ratziu V, Charlotte F, Heurtier A, Gombert S, Giral P, Bruckert E, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128(7):1898–1906CrossRefPubMed
20.
go back to reference Merriman RB, Ferrell LD, Patti MG, Weston SR, Pabst MS, Aouizerat BE, et al. Correlation of paired liver biopsies in morbidly obese patients with suspected nonalcoholic fatty liver disease. Hepatology. 2006;44(4):874–880CrossRef Merriman RB, Ferrell LD, Patti MG, Weston SR, Pabst MS, Aouizerat BE, et al. Correlation of paired liver biopsies in morbidly obese patients with suspected nonalcoholic fatty liver disease. Hepatology. 2006;44(4):874–880CrossRef
21.
go back to reference Larson SP, Bowers SP, Palekar NA, Ward JA, Pulcini JP, Harrison SA. Histopathologic variability between the right and left lobes of the liver in morbidly obese patients undergoing Roux-en-Y bypass. Clin Gastroenterol Hepatol. 2007;5(11):1329–1332CrossRefPubMed Larson SP, Bowers SP, Palekar NA, Ward JA, Pulcini JP, Harrison SA. Histopathologic variability between the right and left lobes of the liver in morbidly obese patients undergoing Roux-en-Y bypass. Clin Gastroenterol Hepatol. 2007;5(11):1329–1332CrossRefPubMed
22.
go back to reference Vuppalanchi R, Unalp A, Van Natta ML, Cummings OW, Sandrasegaran KE, Hameed T, et al. Effects of liver biopsy sample length and number of readings on sampling variability in nonalcoholic Fatty liver disease. Clin Gastroenterol Hepatol. 2009;7(4):481–486CrossRefPubMed Vuppalanchi R, Unalp A, Van Natta ML, Cummings OW, Sandrasegaran KE, Hameed T, et al. Effects of liver biopsy sample length and number of readings on sampling variability in nonalcoholic Fatty liver disease. Clin Gastroenterol Hepatol. 2009;7(4):481–486CrossRefPubMed
23.
go back to reference Hagstrom H, Nasr P, Ekstedt M, Hammar U, Stal P, Hultcrantz R, et al. Fibrosis stage but not NASH predicts mortality and time to development of severe liver disease in biopsy-proven NAFLD. J Hepatol. 2017;67(6):1265–1273CrossRefPubMed Hagstrom H, Nasr P, Ekstedt M, Hammar U, Stal P, Hultcrantz R, et al. Fibrosis stage but not NASH predicts mortality and time to development of severe liver disease in biopsy-proven NAFLD. J Hepatol. 2017;67(6):1265–1273CrossRefPubMed
24.
go back to reference Dulai PS, Singh S, Patel J, Soni M, Prokop LJ, Younossi Z, et al. Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: systematic review and meta-analysis. Hepatology. 2017;65(5):1557–1655CrossRefPubMedPubMedCentral Dulai PS, Singh S, Patel J, Soni M, Prokop LJ, Younossi Z, et al. Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: systematic review and meta-analysis. Hepatology. 2017;65(5):1557–1655CrossRefPubMedPubMedCentral
25.
go back to reference Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41(6):1313–1321CrossRef Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41(6):1313–1321CrossRef
26.
go back to reference Faa G, Nurchi V, Demelia L, Ambu R, Parodo G, Congiu T, et al. Uneven hepatic copper distribution in Wilson's disease. J Hepatol. 1995;22(3):303–308CrossRefPubMed Faa G, Nurchi V, Demelia L, Ambu R, Parodo G, Congiu T, et al. Uneven hepatic copper distribution in Wilson's disease. J Hepatol. 1995;22(3):303–308CrossRefPubMed
27.
go back to reference Stavropoulos SN, Im GY, Jlayer Z, Harris MD, Pitea TC, Turi GK, et al. High yield of same-session EUS-guided liver biopsy by 19-gauge FNA needle in patients undergoing EUS to exclude biliary obstruction. Gastrointest Endosc. 2012;75(2):310–318CrossRefPubMed Stavropoulos SN, Im GY, Jlayer Z, Harris MD, Pitea TC, Turi GK, et al. High yield of same-session EUS-guided liver biopsy by 19-gauge FNA needle in patients undergoing EUS to exclude biliary obstruction. Gastrointest Endosc. 2012;75(2):310–318CrossRefPubMed
28.
go back to reference Mok SRS, Diehl DL, Johal AS, Khara HS, Confer BD, Mudireddy PR, et al. A prospective pilot comparison of wet and dry heparinized suction for EUS-guided liver biopsy (with videos). Gastrointest Endosc. 2018;88(6):919–925CrossRefPubMed Mok SRS, Diehl DL, Johal AS, Khara HS, Confer BD, Mudireddy PR, et al. A prospective pilot comparison of wet and dry heparinized suction for EUS-guided liver biopsy (with videos). Gastrointest Endosc. 2018;88(6):919–925CrossRefPubMed
Metadata
Title
Bi-lobar liver biopsy via EUS enhances the assessment of disease severity in patients with non-alcoholic steatohepatitis
Authors
Sandeep Khurana
Waseem Butt
Harshit S. Khara
Amitpal S. Johal
Sara F. West
Zong-Ming E. Chen
Andrea L. Berger
David L. Diehl
Publication date
01-05-2019
Publisher
Springer India
Published in
Hepatology International / Issue 3/2019
Print ISSN: 1936-0533
Electronic ISSN: 1936-0541
DOI
https://doi.org/10.1007/s12072-019-09945-4

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