Top

Published in:

01-12-2019 | Gastrointestinal

Prospective comparison of transient, point shear wave, and magnetic resonance elastography for staging liver fibrosis

Authors: Thierry Lefebvre, Claire Wartelle-Bladou, Philip Wong, Giada Sebastiani, Jeanne-Marie Giard, Hélène Castel, Jessica Murphy-Lavallée, Damien Olivié, André Ilinca, Marie-Pierre Sylvestre, Guillaume Gilbert, Zu-Hua Gao, Bich N. Nguyen, Guy Cloutier, An Tang

Published in: European Radiology | Issue 12/2019

Abstract

Objectives

To perform head-to-head comparisons of the feasibility and diagnostic performance of transient elastography (TE), point shear-wave elastography (pSWE), and magnetic resonance elastography (MRE).

Methods

This prospective, cross-sectional, dual-center imaging study included 100 patients with known or suspected chronic liver disease caused by hepatitis B or C virus, nonalcoholic fatty liver disease, or autoimmune hepatitis identified between 2014 and 2018. Liver stiffness measured with the three elastographic techniques was obtained within 6 weeks of a liver biopsy. Confounding effects of inflammation and steatosis on association between fibrosis and liver stiffness were assessed. Obuchowski scores and AUCs for staging fibrosis were evaluated and the latter were compared using the DeLong method.

Results

TE, pSWE, and MRE were technically feasible and reliable in 92%, 79%, and 91% subjects, respectively. At univariate analysis, liver stiffness measured by all techniques increased with fibrosis stages and inflammation and decreased with steatosis. For classification of dichotomized fibrosis stages, the AUCs were significantly higher for distinguishing stages F0 vs. ≥ F1 with MRE than with TE (0.88 vs. 0.71; p < 0.05) or pSWE (0.88 vs. 0.73; p < 0.05), and for distinguishing stages ≤ F1 vs. ≥ F2 with MRE than with TE (0.85 vs. 0.75; p < 0.05). TE, pSWE, and MRE Obuchowski scores for staging fibrosis stages were respectively 0.89 (95% CI 0.85–0.93), 0.90 (95% CI 0.85–0.94), and 0.94 (95% CI 0.91–0.96).

Conclusion

MRE provided a higher diagnostic performance than TE and pSWE for staging early stages of liver fibrosis.

Trial registration

NCT02044523

Key Points

• The technical failure rate was similar between MRE and US-based elastography techniques.

• Liver stiffness measured by MRE and US-based elastography techniques increased with fibrosis stages and inflammation and decreased with steatosis.

• MRE provided a diagnostic accuracy higher than US-based elastography techniques for staging of early stages of histology-determined liver fibrosis.

Available only for authorised users

Chalasani N, Younossi Z, Lavine JE et al (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology. Gastroenterology 142:1592–1609PubMedCrossRef

Bedossa P, Dargère D, Paradis V (2003) Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology 38:1449–1457PubMedCrossRef

Younossi ZM, Loomba R, Anstee QM et al (2017) Diagnostic modalities for non-alcoholic fatty liver disease (NAFLD), non-alcoholic steatohepatitis (NASH) and associated fibrosis. Hepatology. https://doi.org/10.1002/hep.29721 PubMedCrossRef

Cui J, Ang B, Haufe W et al (2015) Comparative diagnostic accuracy of magnetic resonance elastography vs. eight clinical prediction rules for non-invasive diagnosis of advanced fibrosis in biopsy-proven non-alcoholic fatty liver disease: a prospective study. Aliment Pharmacol Ther 41:1271–1280PubMedPubMedCentralCrossRef

Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G (2017) Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology 66:1486–1501PubMedCrossRef

Guo Y, Parthasarathy S, Goyal P, McCarthy RJ, Larson AC, Miller FH (2015) Magnetic resonance elastography and acoustic radiation force impulse for staging hepatic fibrosis: a meta-analysis. Abdom Imaging 40:818–834PubMedCrossRef

Xiao H, Shi M, Xie Y, Chi X (2017) Comparison of diagnostic accuracy of magnetic resonance elastography and FibroScan for detecting liver fibrosis in chronic hepatitis B patients: a systematic review and meta-analysis. PLoS One 12:e0186660PubMedPubMedCentralCrossRef

Myers RP, Pomier-Layrargues G, Kirsch R et al (2012) Feasibility and diagnostic performance of the FibroScan XL probe for liver stiffness measurement in overweight and obese patients. Hepatology 55:199–208PubMedCrossRef

Boursier J, Zarski JP, de Ledinghen V et al (2013) Determination of reliability criteria for liver stiffness evaluation by transient elastography. Hepatology 57:1182–1191PubMedCrossRef

10.

Dietrich CF, Bamber J, Berzigotti A et al (2017) EFSUMB guidelines and recommendations on the clinical use of liver ultrasound elastography, update 2017 (long version). Ultraschall Med 38:e16–e47PubMed

11.

Venkatesh SK, Yin M, Ehman RL (2013) Magnetic resonance elastography of liver: technique, analysis, and clinical applications. J Magn Reson Imaging 37:544–555PubMedPubMedCentralCrossRef

12.

Labranche R, Gilbert G, Cerny M et al (2018) Liver iron quantification with MR imaging: a primer for radiologists. Radiographics 38:392–412PubMedCrossRef

13.

Wood JC, Enriquez C, Ghugre N et al (2005) MRI R2 and R2* mapping accurately estimates hepatic iron concentration in transfusion-dependent thalassemia and sickle cell disease patients. Blood 106:1460–1465PubMedPubMedCentralCrossRef

14.

Obuchowski NA (2005) Estimating and comparing diagnostic tests’ accuracy when the gold standard is not binary. Acad Radiol 12:1198–1204PubMedCrossRef

15.

Castéra L, Foucher J, Bernard PH et al (2010) Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology 51:828–835PubMed

16.

Woo H, Lee JY, Yoon JH, Kim W, Cho B, Choi BI (2015) Comparison of the reliability of acoustic radiation force impulse imaging and supersonic shear imaging in measurement of liver stiffness. Radiology 277:881–886PubMedCrossRef

17.

Friedrich-Rust M, Nierhoff J, Lupsor M et al (2012) Performance of acoustic radiation force impulse imaging for the staging of liver fibrosis: a pooled meta-analysis. J Viral Hepat 19:e212–e219PubMedCrossRef

18.

Kim DW, Park C, Yoon HM et al (2019) Technical performance of shear wave elastography for measuring liver stiffness in pediatric and adolescent patients: a systematic review and meta-analysis. Eur Radiol 29:2560–2572PubMedCrossRef

19.

Yin M, Glaser KJ, Talwalkar JA, Chen J, Manduca A, Ehman RL (2016) Hepatic MR elastography: clinical performance in a series of 1377 consecutive examinations. Radiology 278:114–124PubMedCrossRef

20.

Wagner M, Corcuera-Solano I, Lo G et al (2017) Technical failure of MR elastography examinations of the liver: experience from a large single-center study. Radiology 284:401–412PubMedCrossRef

21.

Felker ER, Choi KS, Sung K et al (2018) Liver MR elastography at 3 T: agreement across pulse sequences and effect of liver R2* on image quality. AJR Am J Roentgenol 211:588–594PubMedCrossRef

22.

Lee MS, Bae JM, Joo SK et al (2017) Prospective comparison among transient elastography, supersonic shear imaging, and ARFI imaging for predicting fibrosis in nonalcoholic fatty liver disease. PLoS One 12:e0188321PubMedPubMedCentralCrossRef

23.

Kennedy P, Wagner M, Castéra L et al (2018) Quantitative elastography methods in liver disease: current evidence and future directions. Radiology 286:738–763PubMedCrossRef

24.

Singh S, Venkatesh SK, Wang Z et al (2015) Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol 13:440–451 e446PubMedCrossRef

25.

Nierhoff J, Chávez Ortiz AA, Herrmann E, Zeuzem S, Friedrich-Rust M (2013) The efficiency of acoustic radiation force impulse imaging for the staging of liver fibrosis: a meta-analysis. Eur Radiol 23:3040–3053PubMedCrossRef

26.

Cui J, Heba E, Hernandez C et al (2016) 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 63:453–461PubMedCrossRef

27.

Dyvorne HA, Jajamovich GH, Bane O et al (2016) Prospective comparison of magnetic resonance imaging to transient elastography and serum markers for liver fibrosis detection. Liver Int 36:659–666PubMedPubMedCentralCrossRef

28.

Imajo K, Kessoku T, Honda Y et al (2016) Magnetic resonance imaging more accurately classifies steatosis and fibrosis in patients with nonalcoholic fatty liver disease than transient elastography. Gastroenterology 150:626–637 e627PubMedCrossRef

29.

Bohte AE, de Niet A, Jansen L et al (2014) 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 24:638–648PubMedCrossRef

30.

Friedrich-Rust M, Romen D, Vermehren J et al (2012) Acoustic radiation force impulse-imaging and transient elastography for non-invasive assessment of liver fibrosis and steatosis in NAFLD. Eur J Radiol 81:e325–e331PubMedCrossRef

31.

Goertz RS, Zopf Y, Jugl V et al (2010) Measurement of liver elasticity with acoustic radiation force impulse (ARFI) technology: an alternative noninvasive method for staging liver fibrosis in viral hepatitis. Ultraschall Med 31:151–155PubMedCrossRef

32.

Rizzo L, Calvaruso V, Cacopardo B et al (2011) Comparison of transient elastography and acoustic radiation force impulse for non-invasive staging of liver fibrosis in patients with chronic hepatitis C. Am J Gastroenterol. https://doi.org/10.1038/ajg.2011.341 PubMedCrossRef

33.

Iredale JP (2007) Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ. J Clin Invest 117:539–548PubMedPubMedCentralCrossRef

34.

Yin M, Glaser KJ, Manduca A et al (2017) Distinguishing between hepatic inflammation and fibrosis with MR elastography. Radiology 284:694–705PubMedCrossRef

35.

Salameh N, Larrat B, Abarca-Quinones J et al (2009) Early detection of steatohepatitis in fatty rat liver by using MR elastography. Radiology. https://doi.org/10.1148/radiol.2523081817 PubMedCrossRef

36.

Chen J, Talwalkar JA, Yin M, Glaser KJ, Sanderson SO, Ehman RL (2011) Early detection of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease by using MR elastography. Radiology 259:749–756PubMedPubMedCentralCrossRef

37.

Hartl J, Denzer U, Ehlken H et al (2016) Transient elastography in autoimmune hepatitis: timing determines the impact of inflammation and fibrosis. J Hepatol 65:769–775PubMedCrossRef

38.

Shi Y, Guo Q, Xia F et al (2014) MR elastography for the assessment of hepatic fibrosis in patients with chronic hepatitis B infection: does histologic necroinflammation influence the measurement of hepatic stiffness? Radiology 273:88–98PubMedCrossRef

39.

Yoneda M, Suzuki K, Kato S et al (2010) Nonalcoholic fatty liver disease: US-based acoustic radiation force impulse elastography. Radiology 256:640–647PubMedCrossRef

40.

Yanrong Guo, Haoming Lin, Xinyu Zhang, Huiying Wen, Siping Chen, Xin Chen (2017) The influence of hepatic steatosis on the evaluation of fibrosis with non-alcoholic fatty liver disease by acoustic radiation force impulse. Conf Proc IEEE Eng Med Biol Soc 2017:2988–2991

41.

Petta S, Maida M, Macaluso FS et al (2015) The severity of steatosis influences liver stiffness measurement in patients with nonalcoholic fatty liver disease. Hepatology 62:1101–1110PubMedCrossRef

42.

Yin M, Talwalkar JA, Glaser KJ et al (2007) Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 5:1207–1213 e1202PubMedPubMedCentralCrossRef

43.

Venkatesh SK, Wang G, Teo LL, Ang BW (2014) Magnetic resonance elastography of liver in healthy Asians: normal liver stiffness quantification and reproducibility assessment. J Magn Reson Imaging 39:1–8PubMedCrossRef

44.

Kazemirad S, Zhang E, Nguyen BN et al (2016) Detection of steatohepatitis in a rat model by using spectroscopic shear-wave US elastography. Radiology. https://doi.org/10.1148/radiol.2016160308:160308

45.

Tang A, Desai A, Hamilton G et al (2015) Accuracy of MR imaging-estimated proton density fat fraction for classification of dichotomized histologic steatosis grades in nonalcoholic fatty liver disease. Radiology 274:416–425PubMedCrossRef

46.

Yokoo T, Serai SD, Pirasteh A et al (2018) Linearity, bias, and precision of hepatic proton density fat fraction measurements by using MR imaging: a meta-analysis. Radiology 286:486–498PubMedCrossRef

47.

Karlas T, Petroff D, Sasso M et al (2017) Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol 66:1022–1030CrossRefPubMed

48.

Caussy C, Alquiraish MH, Nguyen P et al (2018) Optimal threshold of controlled attenuation parameter with MRI-PDFF as the gold standard for the detection of hepatic steatosis. Hepatology 67:1348–1359PubMedCrossRef

49.

Friedrich-Rust M, Ong MF, Martens S et al (2008) Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology 134:960–974CrossRefPubMed

50.

Shin HJ, Kim MJ, Kim HY, Roh YH, Lee MJ (2016) Comparison of shear wave velocities on ultrasound elastography between different machines, transducers, and acquisition depths: a phantom study. Eur Radiol 26:3361–3367PubMedCrossRef

51.

Yoshimitsu K, Mitsufuji T, Shinagawa Y et al (2016) MR elastography of the liver at 3.0 T in diagnosing liver fibrosis grades; preliminary clinical experience. Eur Radiol 26:656–663PubMedCrossRef

52.

Park HS, Kim YJ, Yu MH, Choe WH, Jung SI, Jeon HJ (2014) Three-tesla magnetic resonance elastography for hepatic fibrosis: comparison with diffusion-weighted imaging and gadoxetic acid-enhanced magnetic resonance imaging. World J Gastroenterol 20:17558–17567PubMedPubMedCentralCrossRef

53.

Wang J, Glaser KJ, Zhang T et al (2018) Assessment of advanced hepatic MR elastography methods for susceptibility artifact suppression in clinical patients. J Magn Reson Imaging 47:976–987PubMedCrossRef

54.

Zou X, Zhu MY, Yu DM et al (2017) Serum WFA(+) -M2BP levels for evaluation of early stages of liver fibrosis in patients with chronic hepatitis B virus infection. Liver Int 37:35–44PubMedCrossRef

55.

Zhang E, Wartelle-Bladou C, Lepanto L, Lachaine J, Cloutier G, Tang A (2015) Cost-utility analysis of nonalcoholic steatohepatitis screening. Eur Radiol 25:3282–3294PubMedPubMedCentralCrossRef

56.

Zhao J, Zhai F, Cheng J et al (2017) Evaluating the significance of viscoelasticity in diagnosing early-stage liver fibrosis with transient elastography. PLoS One 12:e0170073PubMedPubMedCentralCrossRef

57.

Ellis EL, Mann DA (2012) Clinical evidence for the regression of liver fibrosis. J Hepatol 56:1171–1180PubMedCrossRef

58.

Lee DH, Lee JM, Chang W et al (2018) Prognostic role of liver stiffness measurements using magnetic resonance elastography in patients with compensated chronic liver disease. Eur Radiol 28:3513–3521PubMedCrossRef

59.

Tang A, Destrempes F, Kazemirad S, Garcia-Duitama J, Nguyen BN, Cloutier G (2019) Quantitative ultrasound and machine learning for assessment of steatohepatitis in a rat model. Eur Radiol 29:2175–2184PubMedCrossRef

60.

Yin Z, Murphy MC, Li J et al (2019) Prediction of nonalcoholic fatty liver disease (NAFLD) activity score (NAS) with multiparametric hepatic magnetic resonance imaging and elastography. Eur Radiol. https://doi.org/10.1007/s00330-019-06076-0 PubMedCrossRefPubMedCentral

Title: Prospective comparison of transient, point shear wave, and magnetic resonance elastography for staging liver fibrosis
Authors: Thierry Lefebvre
Claire Wartelle-Bladou
Philip Wong
Giada Sebastiani
Jeanne-Marie Giard
Hélène Castel
Jessica Murphy-Lavallée
Damien Olivié
André Ilinca
Marie-Pierre Sylvestre
Guillaume Gilbert
Zu-Hua Gao
Bich N. Nguyen
Guy Cloutier
An Tang
Publication date: 01-12-2019
Publisher: Springer Berlin Heidelberg
Published in: European Radiology / Issue 12/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI: https://doi.org/10.1007/s00330-019-06331-4

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Prospective comparison of transient, point shear wave, and magnetic resonance elastography for staging liver fibrosis

Abstract

Objectives

Methods

Results

Conclusion

Trial registration

Key Points

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objectives

Methods

Results

Conclusion

Trial registration

Key Points

Please log in to get access to this content

Other articles of this Issue 12/2019

Estimation of the radiation dose in pregnancy: an automated patient-specific model using convolutional neural networks

Prevalence of inflammatory posterior arch abnormalities on lumbar spine MRI in spondyloarthritis patients compared with low back pain patients

Correction to: An analysis of 11.3 million screening tests examining the association between recall and cancer detection rates in the English NHS breast cancer screening programme

Structural and functional MRI correlates of T2 hyperintensities of brain white matter in young neurologically asymptomatic adults

Inter-vendor reproducibility and accuracy of segmental left ventricular strain measurements using CMR feature tracking

Correction to: Epicardial fat volume measured on nongated chest CT is a predictor of coronary artery disease