Advertisement

European Radiology

, Volume 29, Issue 12, pp 6477–6488 | Cite as

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

  • 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 TangEmail author
Gastrointestinal

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.

Keywords

Fibrosis Liver Classification Elasticity imaging techniques Prospective studies 

Abbreviations

AIH

Autoimmune hepatitis

AUC

Area under the receiver operating characteristic curve

CLD

Chronic liver disease

HBV

Hepatitis B virus

HCV

Hepatitis C virus

MRE

Magnetic resonance elastography

NAFLD

Nonalcoholic fatty liver disease

NASH

Nonalcoholic steatohepatitis

pSWE

Point shear wave elastography

TE

Transient elastography

Notes

Acknowledgments

We thank and acknowledge Mrs. Assia Belblidia, Mrs. Catherine Huet, and Mr. Walid El Abyad for their assistance in patient enrollment and image post-processing. ACUSON S2000 and S3000 ultrasound systems were lent by Siemens Healthineers. Magnetic resonance elastography hardware and software were provided in-kind by Philips Healthcare for this clinical trial.

Funding information

This study has received funding by grants from the Canadian Institutes of Health Research (CIHR)-Institute of Nutrition, Metabolism and Diabetes (INMD) (CIHR-INMD #273738 and #301520) and Fonds de recherche du Québec en Santé (FRQS) and Fondation de l’association des radiologistes du Québec (FARQ) Clinical Research Scholarship—Junior 1 and 2 Salary Award (FRQS-FARQ #26993 and #34939) to An Tang. Junior 1 Salary Award from (FRQS #27127) and research salary from McGill University to Giada Sebastiani. Junior 1 Salary Award from FRQS to Marie-Pierre Sylvestre (FRQS #34875).

Compliance with ethical standards

Guarantor

The scientific guarantor of this publication is Dr. An Tang.

Conflict of interest

The authors of this manuscript declare relationships with the following company: Philips Healthcare Canada (Guillaume Gilbert is an employee of Philips Healthcare Canada).

Statistics and biometry

Dr. Marie-Pierre Sylvestre is one of the authors and has significant statistical expertise.

Informed consent

Written informed consent was obtained from all subjects in this study.

Ethical approval

Institutional Review Board approval was obtained for the two participating institutions, Centre hospitalier de l’Université de Montréal (CHUM) and McGill University Health Centre (MUHC).

Methodology

• prospective

• cross-sectional study

• multicenter study

Supplementary material

330_2019_6331_MOESM1_ESM.docx (404 kb)
ESM 1 (DOCX 404 kb).

References

  1. 1.
    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 142:1592–1609CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Bedossa P, Dargère D, Paradis V (2003) Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology 38:1449–1457CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    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
  4. 4.
    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 41:1271–1280CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    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 66:1486–1501CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    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 40:818–834CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    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:e0186660CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    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 55:199–208CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Boursier J, Zarski JP, de Ledinghen V et al (2013) Determination of reliability criteria for liver stiffness evaluation by transient elastography. Hepatology 57:1182–1191CrossRefGoogle Scholar
  10. 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–e47Google Scholar
  11. 11.
    Venkatesh SK, Yin M, Ehman RL (2013) Magnetic resonance elastography of liver: technique, analysis, and clinical applications. J Magn Reson Imaging 37:544–555CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Labranche R, Gilbert G, Cerny M et al (2018) Liver iron quantification with MR imaging: a primer for radiologists. Radiographics 38:392–412CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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 106:1460–1465CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Obuchowski NA (2005) Estimating and comparing diagnostic tests’ accuracy when the gold standard is not binary. Acad Radiol 12:1198–1204CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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 51:828–835PubMedPubMedCentralGoogle Scholar
  16. 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 277:881–886CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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–e219CrossRefGoogle Scholar
  18. 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 29:2560–2572CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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 278:114–124CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 284:401–412CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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 211:588–594CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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:e0188321CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Kennedy P, Wagner M, Castéra L et al (2018) Quantitative elastography methods in liver disease: current evidence and future directions. Radiology 286:738–763CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 e446CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 23:3040–3053CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 63:453–461CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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 36:659–666CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 e627CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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 24:638–648CrossRefPubMedPubMedCentralGoogle Scholar
  30. 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–e331CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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 31:151–155CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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
  33. 33.
    Iredale JP (2007) Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ. J Clin Invest 117:539–548CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Yin M, Glaser KJ, Manduca A et al (2017) Distinguishing between hepatic inflammation and fibrosis with MR elastography. Radiology 284:694–705CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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
  36. 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 259:749–756CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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 65:769–775CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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 273:88–98CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Yoneda M, Suzuki K, Kato S et al (2010) Nonalcoholic fatty liver disease: US-based acoustic radiation force impulse elastography. Radiology 256:640–647CrossRefGoogle Scholar
  40. 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 2017:2988–2991Google Scholar
  41. 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 62:1101–1110CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Yin M, Talwalkar JA, Glaser KJ et al (2007) Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 5:1207–1213 e1202CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 39:1–8CrossRefPubMedPubMedCentralGoogle Scholar
  44. 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. 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 274:416–425CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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 286:486–498CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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 66:1022–1030CrossRefGoogle Scholar
  48. 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 67:1348–1359CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 134:960–974CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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 26:3361–3367CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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 26:656–663CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 20:17558–17567CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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 47:976–987CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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 37:35–44CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Zhang E, Wartelle-Bladou C, Lepanto L, Lachaine J, Cloutier G, Tang A (2015) Cost-utility analysis of nonalcoholic steatohepatitis screening. Eur Radiol 25:3282–3294CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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:e0170073CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Ellis EL, Mann DA (2012) Clinical evidence for the regression of liver fibrosis. J Hepatol 56:1171–1180CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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 28:3513–3521CrossRefPubMedPubMedCentralGoogle Scholar
  59. 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 29:2175–2184CrossRefPubMedPubMedCentralGoogle Scholar
  60. 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

Copyright information

© European Society of Radiology 2019

Authors and Affiliations

  • Thierry Lefebvre
    • 1
    • 2
    • 3
  • Claire Wartelle-Bladou
    • 4
  • Philip Wong
    • 5
  • Giada Sebastiani
    • 5
  • Jeanne-Marie Giard
    • 2
    • 4
  • Hélène Castel
    • 2
    • 4
  • Jessica Murphy-Lavallée
    • 1
  • Damien Olivié
    • 1
  • André Ilinca
    • 1
    • 2
  • Marie-Pierre Sylvestre
    • 2
    • 6
  • Guillaume Gilbert
    • 1
    • 7
  • Zu-Hua Gao
    • 8
  • Bich N. Nguyen
    • 9
  • Guy Cloutier
    • 1
    • 10
    • 11
  • An Tang
    • 1
    • 2
    • 10
    Email author
  1. 1.Department of Radiology, Radio-Oncology and Nuclear MedicineUniversité de MontréalMontrealCanada
  2. 2.Centre de recherche du Centre hospitalier de l’Université de Montréal (CRCHUM)MontrealCanada
  3. 3.Medical Physics UnitMcGill UniversityMontrealCanada
  4. 4.Department of Medicine, Division of Hepatology and Liver TransplantationUniversité de MontréalMontrealCanada
  5. 5.Department of Medicine, Division of Gastroenterology and HepatologyMcGill University Health Centre (MUHC)MontrealCanada
  6. 6.Department of Social and Preventive MedicineÉcole de santé publique de l’Université de Montréal (ESPUM)MontrealCanada
  7. 7.MR Clinical SciencePhilips Healthcare CanadaMarkhamCanada
  8. 8.Department of PathologyMcGill UniversityMontrealCanada
  9. 9.Service of PathologyCentre hospitalier de l’Université de Montréal (CHUM)MontrealCanada
  10. 10.Institute of Biomedical EngineeringUniversité de MontréalMontrealCanada
  11. 11.Laboratory of Biorheology and Medical Ultrasonics (LBUM)Centre de recherche du Centre hospitalier de l’Université de Montréal (CRCHUM)MontrealCanada

Personalised recommendations