Assessment of biopsy-proven liver fibrosis by two-dimensional shear wave elastography: An individual patient data-based meta-analysis

Eva Herrmann, Victor de Lédinghen, Christophe Cassinotto, Winnie C-W Chu, Vivian Y-F Leung, Giovanna Ferraioli, Carlo Filice, Laurent Castera, Valérie Vilgrain, Maxime Ronot, Jérôme Dumortier, Aymeric Guibal, Stanislas Pol, Jonel Trebicka, Christian Jansen, Christian Strassburg, Rongqin Zheng, Jian Zheng, Sven Francque, Thomas Vanwolleghem, Luisa Vonghia, Emanuel K Manesis, Pavlos Zoumpoulis, Ioan Sporea, Maja Thiele, Aleksander Krag, Claude Cohen-Bacrie, Aline Criton, Joel Gay, Thomas Deffieux, Mireen Friedrich-Rust, Eva Herrmann, Victor de Lédinghen, Christophe Cassinotto, Winnie C-W Chu, Vivian Y-F Leung, Giovanna Ferraioli, Carlo Filice, Laurent Castera, Valérie Vilgrain, Maxime Ronot, Jérôme Dumortier, Aymeric Guibal, Stanislas Pol, Jonel Trebicka, Christian Jansen, Christian Strassburg, Rongqin Zheng, Jian Zheng, Sven Francque, Thomas Vanwolleghem, Luisa Vonghia, Emanuel K Manesis, Pavlos Zoumpoulis, Ioan Sporea, Maja Thiele, Aleksander Krag, Claude Cohen-Bacrie, Aline Criton, Joel Gay, Thomas Deffieux, Mireen Friedrich-Rust

Abstract

Two-dimensional shear wave elastography (2D-SWE) has proven to be efficient for the evaluation of liver fibrosis in small to moderate-sized clinical trials. We aimed at running a larger-scale meta-analysis of individual data. Centers which have worked with Aixplorer ultrasound equipment were contacted to share their data. Retrospective statistical analysis used direct and paired receiver operating characteristic and area under the receiver operating characteristic curve (AUROC) analyses, accounting for random effects. Data on both 2D-SWE and liver biopsy were available for 1,134 patients from 13 sites, as well as on successful transient elastography in 665 patients. Most patients had chronic hepatitis C (n = 379), hepatitis B (n = 400), or nonalcoholic fatty liver disease (n = 156). AUROCs of 2D-SWE in patients with hepatitis C, hepatitis B, and nonalcoholic fatty liver disease were 86.3%, 90.6%, and 85.5% for diagnosing significant fibrosis and 92.9%, 95.5%, and 91.7% for diagnosing cirrhosis, respectively. The AUROC of 2D-SWE was 0.022-0.084 (95% confidence interval) larger than the AUROC of transient elastography for diagnosing significant fibrosis (P = 0.001) and 0.003-0.034 for diagnosing cirrhosis (P = 0.022) in all patients. This difference was strongest in hepatitis B patients.

Conclusion: 2D-SWE has good to excellent performance for the noninvasive staging of liver fibrosis in patients with hepatitis B; further prospective studies are needed for head-to-head comparison between 2D-SWE and other imaging modalities to establish disease-specific appropriate cutoff points for assessment of fibrosis stage. (Hepatology 2018;67:260-272).

© 2017 The Authors. Hepatology published by Wiley Periodicals, Inc., on behalf of the American Association for the Study of Liver Diseases.

Figures

Figure 1
Figure 1
Flowchart of data collection and individual patient data selection.
Figure 2
Figure 2
Illustration of the heterogeneity of the etiologies of liver diseases (upper panel) as well as of the prevalence of the different fibrosis stages (lower panel) between the clinical sites.
Figure 3
Figure 3
Summarized ROC curves and diagnostic performance by AUROC estimated using a random effect approach for all patients and for HCV, HBV, and NAFLD patients.
Figure 4
Figure 4
Forest plots for the comparison of AUROC as a marker of diagnostic performance between 2D‐SWE and TE. Only results from patients with reported TE success and IQR

References

    1. Lefton HB, Rosa A, Cohen M. Diagnosis and epidemiology of cirrhosis. Med Clin North Am 2009;93:787‐799.
    1. O'Leary JG, Lepe R, Davis GL. Indications for liver transplantation. Gastroenterology 2008;134:1764‐1776.
    1. Castera L, Negre I, Samii K, Buffet C. Pain experienced during percutaneous liver biopsy. Hepatology 1999;30:1529‐1530.
    1. Bedossa P, Dargere D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology 2003;38:1449‐1457.
    1. Friedrich‐Rust M, Poynard T, Castera L. Critical comparison of elastography methods to assess chronic liver disease. Nat Rev Gastroenterol Hepatol 2016;13:402‐411.
    1. Castera L, Chan HLY, Arrese M; for the Clinical Practice Guideline Panel . EASL‐ALEH clinical practice guidelines: non‐invasive tests for evaluation of liver disease severity and prognosis. J Hepatol 2015; 63:237‐264.
    1. Bamber J, Cosgrove D, Dietrich CF, Fromageau J, Bojunga J, Calliada F, et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall Med 2013;34:169‐184.
    1. Friedrich‐Rust M, Ong MF, Martens S, Sarrazin C, Bojunga J, Zeuzem S, et al. Performance of transient elastography for the staging of liver fibrosis: a meta‐analysis. Gastroenterology 2008;134:960‐974.
    1. Chon YE, Choi EH, Song KJ, Park JY, Kim DY, Han KH, et al. Performance of transient elastography for the staging of liver fibrosis in patients with chronic hepatitis B: a meta‐analysis. PloS One 2012;7:e44930.
    1. Tsochatzis EA, Gurusamy KS, Ntaoula S, Cholongitas E, Davidson BR, Burroughs AK. Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta‐analysis of diagnostic accuracy. J Hepatol 2011;54:650‐659.
    1. Talwalkar JA, Kurtz DM, Schoenleber SJ, West CP, Montori VM. Ultrasound‐based transient elastography for the detection of hepatic fibrosis: systematic review and meta‐analysis. Clin Gastroenterol Hepatol 2007;5:1214‐1220.
    1. Castera L, Foucher J, Bernard PH, Carvalho F, Allaix D, Merrouche W, et al. Pitfalls of liver stiffness measurement: a 5‐year prospective study of 13,369 examinations. Hepatology 2010;51:828‐835.
    1. Bercoff J, Tanter M, Fink M. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control 2004;51:396‐409.
    1. Bavu E, Gennisson J‐L, Couade M, Bercoff J, Mallet V, Fink M, et al. Noninvasive in vivo liver fibrosis evaluation using supersonic shear imaging: a clinical study on 113 hepatitis C virus patients. Ultrasound Med Biol 2011;37:1361‐1373.
    1. Cassinotto C, Lapuyade B, Mouries A, Hiriart JB, Vergniol J, Gaye D, et al. Non‐invasive assessment of liver fibrosis with impulse elastography: comparison of supersonic shear imaging with ARFI and FibroScan®. J Hepatol 2014;61:550‐557.
    1. Deffieux T, Gennisson JL, Bousquet L, Corouge M, Cosconea S, Amroun D, et al. Investigating liver stiffness and viscosity for fibrosis, steatosis and activity staging using shear wave elastography. J Hepatol 2015;62:317‐324.
    1. Ferraioli G, Tinelli C, Dal BB, Zicchetti M, Filice G, Filice C. Accuracy of real‐time shear wave elastography for assessing liver fibrosis in chronic hepatitis C: a pilot study. Hepatology 2012;56:2125‐2133.
    1. Guibal A, Renosi G, Rode A, Scoazec JY, Guillaud O, Chardon L, et al. Shear wave elastography: an accurate technique to stage liver fibrosis in chronic liver diseases. Diagn Interv Imaging 2016;97:91‐99.
    1. Leung VY, Shen J, Wong VW, Abrigo J, Wong GL, Chim AM, et al. Quantitative elastography of liver fibrosis and spleen stiffness in chronic hepatitis B carriers: comparison of shear‐wave elastography and transient elastography with liver biopsy correlation. Radiology 2013;269:910‐918.
    1. Zeng J, Liu GJ, Huang ZP, Zheng J, Wu T, Zheng RQ, et al. Diagnostic accuracy of two‐dimensional shear wave elastography for the non‐invasive staging of hepatic fibrosis in chronic hepatitis B: a cohort study with internal validation. Eur Radiol 2014;24:2572‐2581.
    1. Goodman ZD. Grading and staging systems for inflammation and fibrosis in chronic liver diseases. J Hepatol 2007;47:598‐607.
    1. Brunt EM, Janney CG, Di Bisceglie AM, Neuschwander‐Tetri BA, Bacon BR. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol 1999;94:2467‐2474.
    1. Muller M, Gennisson J‐L, Deffieux T, Tanter M, Fink M. Quantitative viscoelasticity mapping of human liver using supersonic shear imaging: preliminary in vivo feasibility study. Ultrasound Med Biol 2009;35:219‐229.
    1. Castera L, Forns X, Alberti A. Non‐invasive evaluation of liver fibrosis using transient elastography. J Hepatol 2008;48: 835‐847.
    1. Obuchowski NA. Estimating and comparing diagnostic tests' accuracy when the gold standard is not binary. Acad Radiol 2005;12:1198‐1204.
    1. Reitsma JB, Glas AS, Rutjes AW, Scholten RJ, Bossuyt PM, Zwinderman AH. Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol 2005;58:982‐990.
    1. DeLong ER, DeLong DM, Clarke‐Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 1988;44:837‐845.
    1. Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, et al. pROC: an open‐source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 2011;12:77.
    1. Cassinotto C, Boursier J, De Ledinghen V, Lebigot J, Lapuyade B, Cales P, et al. Liver stiffness in nonalcoholic fatty liver disease: a comparison of supersonic shear imaging, FibroScan and ARFI with liver biopsy. Hepatology 2016;63:1817‐1827.
    1. Petta S, Maida M, Macaluso FS, Di Marco V, Cammà C, Cabibi D, et al. The severity of steatosis influences liver stiffness measurement in patients with nonalcoholic fatty liver disease. Hepatology 2015;62:1101‐1110.
    1. Ferraioli G, Tinelli C, Zicchetti M, Above E, Poma G, Di Gregorio M, et al. Reproducibility of real‐time shear wave elastography in the evaluation of liver elasticity. Eur J Radiol 2012;81:3102‐3106.
    1. Hudson JM, Milot L, Parry C, Williams R, Burns PN. Inter‐ and intra‐operator reliability and repeatability of shear wave elastography in the liver: a study in healthy volunteers. Ultrasound Med Biol 2013;39:950‐955.
    1. Mehta SH, Lau B, Afdhal NH, Thomas DL. Exceeding the limits of liver histology markers. J Hepatol 2009;50:36‐41.
    1. Talwalkar JA, Yin M, Fidler JL, Sanderson SO, Kamath PS, Ehman RL. Magnetic resonance imaging of hepatic fibrosis: emerging clinical applications. Hepatology 2008;47:332‐342.
    1. Friedrich‐Rust M, Nierhoff J, Lupsor M, Sporea I, Fierbinteanu‐Braticevici C, Strobel D, et al. Performance of acoustic radiation force impulse imaging for the staging of liver fibrosis: a pooled meta‐analysis. J Viral Hepat 2012;19:e212‐e219.
    1. Nierhoff J, Chavez Ortiz AA, Herrmann E, Zeuzem S, Friedrich‐Rust M. The efficiency of acoustic radiation force impulse imaging for the staging of liver fibrosis: a meta‐analysis. Eur Radiol 2013;23:3040‐3053.
    1. Wang QB, Zhu H, Liu HL, Zhang B. Performance of magnetic resonance elastography and diffusion‐weighted imaging for the staging of hepatic fibrosis: a meta‐analysis. Hepatology 2012;56:239‐247.
    1. Singh S, Venkatesh SK, Wang Z, Miller FH, Motosugi U, Low RN, et al. Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta‐analysis of individual participant data. Clin Gastroenterol Hepatol 2015;13:440‐451.
    1. Loomba R, Wolfson T, Ang B, Hooker J, Behling C, Peterson M, et al. Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study. Hepatology 2014;60:1920‐1928.
    1. Imajo K, Kessoku T, Honda Y, Tomeno W, Ogawa Y, Mawatari H, et al. Magnetic resonance imaging more accurately classifies steatosis and fibrosis in patients with nonalcoholic fatty liver disease than transient elastography. Gastroenterology 2016;150:628‐637.
    1. Loomba R, Cui J, Wolfson T, Haufe W, Hooker J, Szeverenyi N, et al. Novel 3D magnetic resonance elastography for the noninvasive diagnosis of advanced fibrosis in NAFLD: a prospective study. Am J Gastroenterol 2016;111:986‐994.
    1. Park CC, Nguyen P, Hernandez C, Bettencourt R, Ramirez K, Fortney L, et al. Magnetic resonance elastography versus transient elastography in detection of fibrosis and noninvasive measurement of steatosis in patients with biopsy‐proven nonalcoholic fatty liver disease. Gastroenterology 2017;152:598‐607.
    1. Bohte AE, de Niet A, Jansen L, Bipat S, Nederveen AJ, Verheij J, et al. Non‐invasive evaluation of liver fibrosis: a comparison of ultrasound‐based transient elastography and MR elastography in patients with viral hepatitis B and C. Eur Radiol 2014;24:638‐648.
    1. Ichikawa S, Motosugi U, Morisaka H, Sano K, Ichikawa T, Tatsumi A, et al. Comparison of the diagnostic accuracies of magnetic resonance elastography and transient elastography for hepatic fibrosis. Magn Reson Imaging 2015;33:26‐30.
    1. Huwart L, Sempoux C, Vicaut E, Salameh N, Annet L, Danse E, et al. Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology 2008;35:299‐302.
    1. Cui J, Heba E, Hernandez C, Haufe W, Hooker J, Andre MP, et al. Magnetic resonance elastography is superior to acoustic radiation force impulse for the diagnosis of fibrosis in patients with biopsy‐proven nonalcoholic fatty liver disease: a prospective study. Hepatology 2016;63:453‐461.
    1. Yoon JH, Lee JM, Joo I, Lee ES, Sohn JY, Jang SK, et al. Hepatic fibrosis: prospective comparison of MR elastography and US shear‐wave elastography for evaluation. Radiology 2014;273:772‐782.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe