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Magnetic resonance imaging for the assessment of pathological hepatic findings in nonalcoholic fatty liver disease

Journal of Medical Ultrasonics volume 47, pages 535–548 (2020)Cite this article

Abstract

The prevalence of nonalcoholic fatty liver disease (NAFLD) is expected to increase because of the current epidemics of obesity and diabetes, and NAFLD has become a major cause of chronic liver disease worldwide. Liver fibrosis is associated with poor long-term outcomes in patients with NAFLD. Additionally, increased mortality and liver-related complications are primarily seen in patients with nonalcoholic steatohepatitis (NASH); however, nonalcoholic fatty liver (NAFL) is believed to be benign and non-progressive. Therefore, distinguishing between NASH and NAFL is clinically important. Liver biopsy is the gold standard method for the staging of liver fibrosis and distinguishing between NASH and NAFL. Unfortunately, liver biopsy is an invasive and expensive procedure. Therefore, noninvasive methods, to replace biopsy, are urgently needed for the staging of liver fibrosis and diagnosing NASH. In this review, we discuss the recent studies on magnetic resonance imaging (MRI), including magnetic resonance elastography, proton density fat fraction measurement, and multiparametric MRI (mpMRI) that can be used in the assessment of NASH components such as liver fibrosis, steatosis, and liver injury including inflammation and ballooning.

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References

  1. Younossi ZM, Keonig AB, Abdelatif D, et al. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64:73–84.

    PubMed  Google Scholar 

  2. Li J, Zou B, Yeo YH, et al. Prevalence, incidence, and outcome of non-alcoholic fatty liver disease in Asia, 1999–2019: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2019;4:389–98.

    PubMed  Google Scholar 

  3. Machado MP, Marques-Vidal P, Cortez-Pinto H. Hepatic histology in obese patients undergoing bariatric surgery. J Hepatol. 2006;45:600–6.

    PubMed  Google Scholar 

  4. Milic S, Lulic D, Stimac D. Non-alcoholic fatty liver disease and obesity: biochemical, metabolic and clinical presentations. World J Gastroenterol. 2014;20:9330–7.

    PubMed  PubMed Central  Google Scholar 

  5. Dai W, Ye L, Wen SW, et al. Prevalence of nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus: a meta-analysis. Med (Baltim). 2017;96:e8179.

    Google Scholar 

  6. Estes C, Anstee QM, Arias-Loste MT, et al. Modeling NAFLD disease burden in China, France, Germany, Italy, Japan, Spain, United Kingdom, and United States for the period 2016–2030. J Hepatol. 2018;69:896–904.

    PubMed  Google Scholar 

  7. Angulo P, Kleiner DE, Dam-Larsen S, et al. Liver fibrosis, but no other histologic features, is associated with long-term outcomes of patients with nonalcoholic fatty liver disease. Gastroenterology. 2015;149:e10.

    Google Scholar 

  8. Hagström H, Nasr P, Ekstedt M, et al. Fibrosis stage but not NASH predicts mortality and time to development of severe liver disease in biopsy-proven NAFLD. J Hepatol. 2017;67:1265–73.

    PubMed  Google Scholar 

  9. Cadranel JF. Good clinical practice guidelines for fine needle aspiration biopsy of the liver: past, present and future. Gastroenterol Clin Biol. 2002;26:823–4.

    CAS  PubMed  Google Scholar 

  10. Ratziu V, Charlotte F, Heurtier A, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128:1898–906.

    PubMed  Google Scholar 

  11. Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American association for the study of liver diseases. Hepatology. 2018;67:328–57.

    PubMed  PubMed Central  Google Scholar 

  12. Yoneda M, Imajo K, Takahashi H, et al. Clinical strategy of diagnosing and following patients with nonalcoholic fatty liver disease based on invasive and noninvasive methods. J Gastroenterol. 2018;53:181–96.

    CAS  PubMed  Google Scholar 

  13. Tang A, Cloutier G, Szeverenyi NM, et al. Ultrasound elastography and MR elastography for assessing liver fibrosis: part 2, diagnostic performance, confounders, and future directions. AJR Am J Roentgenol. 2015;205:33–40.

    PubMed  PubMed Central  Google Scholar 

  14. Muthupillai R, Lomas DJ, Rossman PJ, et al. Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science. 1995;269:1854–7.

    CAS  PubMed  Google Scholar 

  15. Venkatesh SK, Yin M, Ehman RL. Magnetic resonance elastography of liver: technique, analysis, and clinical applications. J Magn Reson Imaging. 2013;37:544–55.

    PubMed  PubMed Central  Google Scholar 

  16. Barr RG, Ferraioli G, Palmeri ML, et al. Elastography assessment of liver fibrosis: society of radiologists in ultrasound consensus conference statement. Radiology. 2015;276:845–61.

    PubMed  Google Scholar 

  17. Srinivasa Babu A, Wells ML, Teytelboym OM, et al. Elastography in chronic liver disease: modalities, techniques, limitations, and future directions. RadioGraphics. 2016;36:1987–2006.

    PubMed  PubMed Central  Google Scholar 

  18. Venkatesh SK, Talwalkar JA. When and how to use magnetic resonance elastography for patients with liver disease in clinical practice. Am J Gastroenterol. 2018;113:923–6.

    PubMed  Google Scholar 

  19. Carrión JA, Navasa M, Forns X. MR elastography to assess liver fibrosis. Radiology. 2008;247:591 ((author reply 591–2)).

    PubMed  Google Scholar 

  20. Barr RG. Elastography in clinical practice. Radiol Clin North Am. 2014;52:1145–62.

    PubMed  Google Scholar 

  21. Tan CH, Venkatesh SK. Magnetic resonance elastography and other magnetic resonance imaging techniques in chronic liver disease: current status and future directions. Gut Liver. 2016;10:672–86.

    PubMed  PubMed Central  Google Scholar 

  22. Loomba R, Cui J, Wolfson T, et al. Novel 3D magnetic resonance elastography for the noninvasive diagnosis of advanced fibrosis in NAFLD: a prospective study. Am J Gastroenterol. 2016;111:986–94.

    PubMed  PubMed Central  Google Scholar 

  23. Yin M, Talwalkar JA, Glaser KJ, et al. Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol. 2007;5:e2.

    Google Scholar 

  24. Hines CD, Bley TA, Lindstrom MJ, et al. Repeatability of magnetic resonance elastography for quantification of hepatic stiffness. J Magn Reson Imaging. 2010;31:725–31.

    PubMed  PubMed Central  Google Scholar 

  25. Shire NJ, Yin M, Chen J, et al. Test-retest repeatability of MR elastography for noninvasive liver fibrosis assessment in hepatitis C. J Magn Reson Imaging. 2011;34:947–55.

    PubMed  PubMed Central  Google Scholar 

  26. Trout AT, Serai S, Mahley AD, et al. Liver stiffness measurements with MR elastography: agreement and repeatability across imaging systems, field strengths, and pulse sequences. Radiology. 2016;281:793–804.

    PubMed  Google Scholar 

  27. Yasar TK, Wagner M, Bane O, et al. Interplatform reproducibility of liver and spleen stiffness measured with MR elastography. J Magn Reson Imaging. 2016;43:1064–72.

    PubMed  Google Scholar 

  28. Gill HE, Lisanti CJ, Schwope RB, et al. Technical success rate of MR elastography in a population without known liver disease. Abdom Radiol (NY). 2020. https://doi.org/10.1007/s00261-020-02652-x.

  29. Singh S, Venkatesh SK, Loomba R, 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:e6.

    Google Scholar 

  30. Yin M, Talwalkar JA, Glaser KJ, et al. Dynamic postprandial hepatic stiffness augmentation assessed with MR elastography in patients with chronic liver disease. AJR Am J Roentgenol. 2011;197:64–70.

    PubMed  PubMed Central  Google Scholar 

  31. Kim D, Kim WR, Talwalkar JA, et al. Advanced fibrosis in nonalcoholic fatty liver disease: noninvasive assessment with MR elastography. Radiology. 2013;268:411–9.

    PubMed  PubMed Central  Google Scholar 

  32. Loomba R, Wolfson T, Ang B, et al. Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study. Hepatology. 2014;60:1920–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Singh S, Venkatesh SK, Loomba R, et al. Magnetic resonance elastography for staging liver fibrosis in non-alcoholic fatty liver disease: a diagnostic accuracy systematic review and individual participant data pooled analysis. Eur Radiol. 2016;26:1431–40.

    PubMed  Google Scholar 

  34. Imajo K, Kessoku T, Honda Y, et al. Magnetic resonance imaging more accurately classifies steatosis and fibrosis in patients with nonalcoholic fatty liver disease than transient elastography. Gastroenterology. 2016;150:e7.

    Google Scholar 

  35. Cui J, Heba E, Hernandez C, 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;63:453–61.

    PubMed  Google Scholar 

  36. Park CC, Nguyen P, Hernandez C, et al. Magnetic resonance elastography vs transient elastography in detection of fibrosis and noninvasive measurement of steatosis in patients with biopsy-proven nonalcoholic fatty liver disease. Gastroenterology. 2017;152:e2.

    Google Scholar 

  37. Schwimmer JB, Behling C, Angeles JE, et al. Magnetic resonance elastography measured shear stiffness as a biomarker of fibrosis in pediatric nonalcoholic fatty liver disease. Hepatology. 2017;66:1474–85.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Hsu C, Caussy C, Imajo K, et al. Magnetic resonance vs transient elastography analysis of patients with nonalcoholic fatty liver disease: a systematic review and pooled analysis of individual participants. Clin Gastroenterol Hepatol. 2019;17:e8.

    Google Scholar 

  39. Xiao G, Zhu S, Xiao X, et al. Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology. 2017;66:1486–501.

    CAS  PubMed  Google Scholar 

  40. Dulai PS, Sirlin CB, Loomba R. MRI and MRE for non-invasive quantitative assessment of hepatic steatosis and fibrosis in NAFLD and NASH: clinical trials to clinical practice. J Hepatol. 2016;65:1006–16.

    PubMed  PubMed Central  Google Scholar 

  41. Ajmera VH, Liu A, Singh S, et al. Clinical utility of an increase in magnetic resonance elastography in predicting fibrosis progression in nonalcoholic fatty liver disease. Hepatology. 2020;71:849–60.

    CAS  PubMed  Google Scholar 

  42. Honda Y, Yoneda M, Imajo K, et al. Elastography techniques for the assessment of liver fibrosis in non-alcoholic fatty liver disease. Int J Mol Sci. 2020;21:4039.

    PubMed Central  Google Scholar 

  43. Lee SS, Park SH. Radiologic evaluation of nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:7392–402.

    PubMed  PubMed Central  Google Scholar 

  44. Grimm A, Meyer H, Nicke MD, et al. Evaluation of 2-point, 3-point, and 6-point Dixon magnetic resonance imaging with flexible echo timing for muscle fat quantification. Eur J Radiol. 2018;103:57–64.

    PubMed  Google Scholar 

  45. Negrete LM, Middleton MS, Clark L, et al. Inter-examination precision of magnitude-based MRI for estimation of segmental hepatic proton density fat fraction in obese subjects. J Magn Reson Imaging. 2014;39:1265–71.

    PubMed  Google Scholar 

  46. Tyagi A, Yeganeh O, Levin Y, et al. Intra- and inter-examination repeatability of magnetic resonance spectroscopy, magnitude-based MRI, and complex-based MRI for estimation of hepatic proton density fat fraction in overweight and obese children and adults. Abdom Imaging. 2015;40:3070–7.

    PubMed  PubMed Central  Google Scholar 

  47. Bannas P, Kramer H, Hernando D, et al. Quantitative magnetic resonance imaging of hepatic steatosis: validation in ex vivo human livers. Hepatology. 2015;62:1444–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Vu KN, Gilbert G, Chalut M, et al. MRI-determined liver proton density fat fraction, with MRS validation: comparison of regions of interest sampling methods in patients with type 2 diabetes. J Magn Reson Imaging. 2016;43:1090–9.

    PubMed  Google Scholar 

  49. Permutt Z, Le TA, Peterson MR, et al. Correlation between liver histology and novel magnetic resonance imaging in adult patients with non-alcoholic fatty liver disease: MRI accurately quantifies hepatic steatosis in NAFLD. Aliment Pharmacol Ther. 2012;36:22–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Tang A, Tan J, Sun M, et al. Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology. 2013;267:422–31.

    PubMed  PubMed Central  Google Scholar 

  51. Di Martino M, Pacifico L, Bezzi M, et al. Comparison of magnetic resonance spectroscopy, proton density fat fraction and histological analysis in the quantification of liver steatosis in children and adolescents. World J Gastroenterol. 2016;22:8812–9.

    PubMed  PubMed Central  Google Scholar 

  52. Rung JH, Smits LP, Verheij J, et al. MR spectroscopy-derived proton density fat fraction is superior to controlled attenuation parameter for detecting and grading hepatic steatosis. Radiology. 2018;286:547–56.

    Google Scholar 

  53. Chen J, Talwalkar JA, Yin M, et al. Early detection of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease by using MR elastography. Radiology. 2011;259:749–56.

    PubMed  PubMed Central  Google Scholar 

  54. Singh S, Allen AM, Wang Z, et al. Fibrosis progression in nonalcoholic fatty liver vs. nonalcoholic steatohepatitis: a systematic review and meta-analysis of paired-biopsy studies. Clin Gastroenterol Hepatol. 2015;13:e1.

    Google Scholar 

  55. Castera L, Friedrich-Rust M, Loomba R. Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology. 2019;156:e4.

    Google Scholar 

  56. Harrison SA, Dennis A, Fiore MM, et al. Utility and variability of three non-invasive liver fibrosis imaging modalities to evaluate efficacy of GR-MD-02 in subjects with NASH and bridging fibrosis during a phase-2 randomized clinical trial. PLoS ONE. 2018;13:e0203054.

    PubMed  PubMed Central  Google Scholar 

  57. Chen J, Yin M, Talwalkar JA, et al. Diagnostic performance of MR elastography and vibration-controlled transient elastography in the detection of hepatic fibrosis in patients with severe to morbid obesity. Radiology. 2017;283:418–28.

    PubMed  Google Scholar 

  58. Wagner M, Corcuera-Solano I, Lo G, et al. Technical failure of MR elastography examinations of the liver: experience from a large single-center study. Radiology. 2017;284:401–12.

    PubMed  PubMed Central  Google Scholar 

  59. Harrison SA, Bashir MR, Guy CD, et al. Resmetirom (MGL-3196) for the treatment of non-alcoholic steatohepatitis: a multicentre, randomised, double-blind, placebo-controlled, phase 2 trial. Lancet. 2019;394:2012–24.

    CAS  PubMed  Google Scholar 

  60. Caussy C, Reeder SB, Sirlin CB, et al. Noninvasive, quantitative assessment of liver fat by MRI-PDFF as an endpoint in NASH Trials. Hepatology. 2018;68:763–72.

    PubMed  PubMed Central  Google Scholar 

  61. Dennis A, Mouchti S, Kelly M, Fallowfield JA, Hirschfield G, Pavlides M, Banerjee R. A composite biomarker using multiparametric magnetic resonance imaging and blood analytes accurately identifies patients with non-alcoholic steatohepatitis and significant fibrosis. Sci Rep. 2020;10(1):15308. https://doi.org/10.1038/s41598-020-71995-8.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Jayakumar S, Middleton MS, Lawitz EJ, et al. Longitudinal correlations between MRE, MRI-PDFF, and liver histology in patients with non-alcoholic steatohepatitis: analysis of data from a phase II trial of selonsertib. J Hepatol. 2019;70:133–41.

    PubMed  Google Scholar 

  63. Eddowes PJP, McDonald N, Davies N, et al. Utility and cost evaluation of multiparametric magnetic resonance imaging for the assessment of non-alcoholic fatty liver disease. Aliment Pharmacol Ther. 2018;47:631–44.

    CAS  PubMed  Google Scholar 

  64. Pavlides M, Banerjee R, Sellwood J, et al. Multiparametric magnetic resonance imaging predicts clinical outcomes in patients with chronic liver disease. J Hepatol. 2016;64:308–15.

    PubMed  PubMed Central  Google Scholar 

  65. Bachtiar V, Kelly MD, Wilman HR, et al. Repeatability and reproducibility of multiparametric magnetic resonance imaging of the liver. PLoS ONE. 2019;14:e0214921.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Abrigo JM, Shen J, Wong VW, et al. Non–alcoholic fatty liver disease: spectral patterns observed from an in vivo phosphorus magnetic resonance spectroscopy study. J Hepatol. 2014;60:809–15.

    CAS  PubMed  Google Scholar 

  67. Kim T, Jun HY, Kim K, et al. Hepatic alanine differentiates nonalcoholic steatohepatitis from simple steatosis in humans and mice: a proton MR spectroscopy study with long echo time. J Magn Reson Imaging. 2017;46:1298–310.

    PubMed  Google Scholar 

  68. Leporq B, Lambert SA, Ronot M, et al. Simultaneous MR quantification of hepatic fat content, fatty acid composition, transverse relaxation time and magnetic susceptibility for the diagnosis of non-alcoholic steatohepatitis. NMR Biomed. 2017. https://doi.org/10.1002/nbm.3766.

    Article  PubMed  Google Scholar 

  69. Parente DB, Paiva FF, Neto JA, et al. Intravoxel incoherent motion diffusion weighted MR imaging at 3.0 T: assessment of steatohepatitis and fibrosis compared with liver biopsy in type 2 diabetic patients. PLoS ONE. 2015;10:e0125653.

    PubMed  PubMed Central  Google Scholar 

  70. Dillman JR, Trout AT, Costello EN, et al. Quantitative liver MRI biopsy correlation in pediatric and young adult patients with nonalchohlic fatty liver disease: can one be used to predict the other? AJR Am J Roentgenol. 2018;210:166–74.

    PubMed  Google Scholar 

  71. Parente D, Oliveira Neto J, Brasil P, et al. Preperitoneal fat as a non-invasive marker of increased risk of severe non–alcoholic fatty liver disease in patients with type 2 diabetes. J Gastroenterol Hepatol. 2018;33:511–7.

    CAS  PubMed  Google Scholar 

  72. Gallego-Durán R, Cerro-Salido P, Gomez-Gonzalez E, et al. Imaging biomarkers for steatohepatitis and fibrosis detection in non-alcoholic fatty liver disease. Sci Rep. 2016;6:31421.

    PubMed  PubMed Central  Google Scholar 

  73. Bastati N, Feier D, Wibmer A, et al. Noninvasive differentiation of simple steatosis and steatohepatitis by using gadoxetic acid–enhanced MR imaging in patients with disease: a proof-of-concept study. Radiology. 2014;271:739–47.

    PubMed  Google Scholar 

  74. Smits L, Coolen B, Panno M, et al. Noninvasive differentiation between hepatic steatosis and steatohepatitis with MR imaging enhanced with USPIOs in patients with nonalcoholic fatty liver disease: a proof-of-concept study. Radiology. 2016;278:782–91.

    PubMed  Google Scholar 

  75. Tomita K, Tanimoto A, Irie R, et al. Evaluating the severity of nonalcoholic steatohepatitis with superparamagnetic iron oxide-enhanced magnetic resonance imaging. J Magn Reson Imaging. 2008;28:1444–50.

    PubMed  Google Scholar 

  76. Klatt D, Hamhaber U, Asbach P, et al. Noninvasive assessment of the rheological behavior of human organs using multifrequency MR elastography: a study of brain and liver viscoelasticity. Phys Med Biol. 2007;52:7281–94.

    PubMed  Google Scholar 

  77. Asbach P, Klatt D, Hamhaber U, et al. Assessment of liver viscoelasticity using multifrequency MR elastography. Magn Reson Med. 2008;60:373–9.

    PubMed  Google Scholar 

  78. Meyer GA, McCulloch AD, Lieber RL. A nonlinear model of passive muscle viscosity. J Biomech Eng. 2011;133(9):091007. https://doi.org/10.1115/1.4004993.

    CAS  Article  PubMed  Google Scholar 

  79. Sack I, Beierbach B, Wuerfel J, et al. The impact of aging and gender on brain viscoelasticity. Neuroimage. 2009;46:652–7.

    PubMed  Google Scholar 

  80. Wuerfel J, Paul F, Beierbach B, et al. MR-elastography reveals degradation of tissue integrity in multiple sclerosis. Neuroimage. 2010;49:2520–5.

    PubMed  Google Scholar 

  81. de Franchis R, Baveno VI Faculty. Expanding consensus in portal hypertension: report of the Baveno VI consensus workshop: stratifying risk and individualizing care for portal hypertension. J Hepatol. 2014;63:743–52.

    Google Scholar 

  82. Ronot M, Lambert S, Elkrief L, et al. Assessment of portal hypertension and high-risk oesophageal varices with liver and spleen three-dimensional multifrequency MR elastography in liver cirrhosis. Eur Radiol. 2014;24:1394–402.

    PubMed  Google Scholar 

  83. Sun HY, Lee JM, Han JK, Choi BI. Usefulness of MR elastography for predicting esophageal varices in cirrhotic patients. J Magn Reson Imaging. 2014;39:559–66.

    PubMed  Google Scholar 

  84. Matsui N, Imajo K, Yoneda M, et al. Magnetic resonance elastography increases usefulness and safety of non-invasive screening for esophageal varices. J Gastroenterol Hepatol. 2018;33:2022–8.

    PubMed  Google Scholar 

  85. Ma X, Wang L, Wu H, et al. Spleen stiffness is superior to liver stiffness for predicting esophageal varices in chronic liver disease: a meta-analysis. PLoS ONE. 2016;11:1–15.

    Google Scholar 

  86. Levick C, Phillips-Hughes J, Collier J, et al. Non-invasive assessment of portal hypertension by multi-parametric magnetic resonance imaging of the spleen: a proof of concept study. PLoS ONE. 2019;14:e0221066.

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Nedredal GI, Yin M, McKenzie T, et al. Portal hypertension correlates with splenic stiffness as measured with MR elastography. J Magn Reson Imaging. 2011;34:79–87.

    PubMed  PubMed Central  Google Scholar 

  88. Shin SU, Lee JM, Yu MH, et al. Prediction of esophageal varices in patients with cirrhosis: usefulness of three-dimensional MR elastography with echo-planar imaging technique. Radiology. 2014;272:143–53.

    PubMed  PubMed Central  Google Scholar 

  89. Yin M, Glaser KJ, Talwalkar JA, et al. Hepatic MR elastography: clinical performance in a series of 1377 consecutive examinations. Radiology. 2016;278:114–24.

    PubMed  Google Scholar 

  90. Millonig G, Reimann FM, Friedrich S, et al. Extrahepatic cholestasis increases liver stiffness (FibroScan) irrespective of fibrosis. Hepatology. 2008;48:1718–23.

    PubMed  Google Scholar 

  91. Coco B, Oliveri F, Maina AM, et al. Transient elastography: a new surrogate marker of liver fibrosis influenced by major changes of transaminases. J Viral Hepat. 2007;14:360–9.

    CAS  PubMed  Google Scholar 

  92. European Association for the Study of the Liver (EASL); European Association for the Study of Diabetes (EASD); European Association for the Study of Obesity (EASO). EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64:1388–402.

    Google Scholar 

  93. Sasso M, Beaugrand M, de Ledinghen V, et al. Controlled attenuation parameter (CAP): a novel VCTETM guided ultrasonic attenuation measurement for the evaluation of hepatic steatosis: preliminary study and validation in a cohort of patients with chronic liver disease from various causes. Ultrasound Med Biol. 2010;36:1825–35.

    PubMed  Google Scholar 

  94. Newsome PN, Sasso M, Deeks JJ, et al. FibroScan-AST (FAST) score for the non-invasive identification of patients with non-alcoholic steatohepatitis with significant activity and fibrosis: a prospective derivation and global validation study. Lancet Gastroenterol Hepatol. 2020;5:362–73.

    PubMed  PubMed Central  Google Scholar 

  95. Oeda S, Takahashi H, Imajo K, et al. Diagnostic accuracy of FibroScan-AST score to identify non-alcoholic steatohepatitis with significant activity and fibrosis in Japanese patients with non-alcoholic fatty liver disease: comparison between M and XL probes. Hepatol Res. 2020;50:831–9.

    CAS  PubMed  Google Scholar 

  96. Reeder SB, Robson PM, Yu H, et al. Quantification of hepatic steatosis with MRI: the effects of accurate fat spectral modeling. J Magn Reson Imaging. 2009;29:1332–9.

    PubMed  PubMed Central  Google Scholar 

  97. Yoneda M, Imajo K, Nakajima A. Non-invasive diagnosis of nonalcoholic fatty liver disease. Am J Gastroenterol. 2018;113:1409–11.

    PubMed  Google Scholar 

  98. Chan WK, Treeprasertsuk S, Goh GB, et al. Optimizing use of nonalcoholic fatty liver disease fibrosis score, Fibrosis-4 Score, and liver stiffness measurement to identify patients with advanced fibrosis. Clin Gastroenterol Hepatol. 2019;17:e37.

    Google Scholar 

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  1. Department of Gastroenterology and Hepatology, Yokohama City University Graduate School of Medicine, Yokohama, 236-0004, Japan

    Kento Imajo, Yasushi Honda, Masato Yoneda, Satoru Saito & Atsushi Nakajima

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  1. Kento Imajo
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  2. Yasushi Honda
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Correspondence to Atsushi Nakajima.

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Kento Imajo, Yasushi Honda, Masato Yoneda, Satoru Saito, and Atsushi Nakajima declare that they have no conflicts of interest.

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Imajo, K., Honda, Y., Yoneda, M. et al. Magnetic resonance imaging for the assessment of pathological hepatic findings in nonalcoholic fatty liver disease. J Med Ultrasonics 47, 535–548 (2020). https://doi.org/10.1007/s10396-020-01059-x

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Keywords

  • Magnetic resonance elastography
  • Proton density fat fraction
  • Corrected-T1
  • Nonalcoholic fatty liver disease
  • Nonalcoholic steatohepatitis