Advertisement

NAFLD and NASH pp 115-139 | Cite as

Non-invasive Assessment of Non-alcoholic Fatty Liver Disease: Ultrasound and Transient Elastography

  • Tao Wan
  • Annalisa BerzigottiEmail author
Chapter
  • 96 Downloads

Abstract

Ultrasound (US) is the most common imaging method used to diagnose liver steatosis worldwide due to its wide availability, safety, and relatively low cost. The typical findings include increased a bright liver appearance, attenuation of the ultrasound signal and blurring of the intrahepatic vessels walls. US provides a qualitative assessment of the presence of steatosis >15–20% of hepatocytes, but it has important limitations, including its operator-dependency, poor sensitivity for the detection of very mild steatosis and limited ability of providing a proper quantitative assessment of the fat content. Controlled Attenuation Parameter (CAP) by vibration controlled transient elastography is a quantitative parameter for steatosis obtained simultaneously to liver stiffness. It might be more sensitive than ultrasound for mild steatosis and has an excellent accuracy for severe steatosis. In patients with NAFLD, liver stiffness measurement using transient elastography or other ultrasound elastography techniques is able to rule-out liver fibrosis, and to identify severe fibrosis/cirrhosis. Mild increases of liver stiffness can be due either to liver fibrosis or to inflammation in patients with NASH. This chapter reviews the current evidence regarding the non-invasive diagnosis and characterization of NAFLD/NASH using ultrasound and ultrasound elastography, and provides a short overview of upcoming ultrasound techniques.

Keywords

Liver steatosis Liver fibrosis Cirrhosis Scattering Shear-wave 

Notes

Acknowledgement

Tao Wan is supported by a scholarship by the China Scholarship Council (CSC).

References

  1. 1.
    Angulo P. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346(16):1221–31.CrossRefGoogle Scholar
  2. 2.
    Charlton MR, Burns JM, Pedersen RA, Watt KD, Heimbach JK, Dierkhising RA. Frequency and outcomes of liver transplantation for nonalcoholic steatohepatitis in the United States. Gastroenterology. 2011;141(4):1249–53.CrossRefGoogle Scholar
  3. 3.
    Nascimbeni F, Pais R, Bellentani S, Day CP, Ratziu V, Loria P, et al. From NAFLD in clinical practice to answers from guidelines. J Hepatol. 2013;59(4):859–71.CrossRefGoogle Scholar
  4. 4.
    Leandro G, Mangia A, Hui J, Fabris P, Rubbia-Brandt L, Colloredo G, et al. Relationship between steatosis, inflammation, and fibrosis in chronic hepatitis C: a meta-analysis of individual patient data. Gastroenterology. 2006;130(6):1636–42.CrossRefGoogle Scholar
  5. 5.
    Everhart JE, Lok AS, Kim HY, Morgan TR, Lindsay KL, Chung RT, et al. Weight-related effects on disease progression in the hepatitis C antiviral long-term treatment against cirrhosis trial. Gastroenterology. 2009;137(2):549–57.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Poynard T, Ratziu V, McHutchison J, Manns M, Goodman Z, Zeuzem S, et al. Effect of treatment with peginterferon or interferon alfa-2b and ribavirin on steatosis in patients infected with hepatitis C. Hepatology. 2003;38(1):75–85.CrossRefGoogle Scholar
  7. 7.
    de Meijer VE, Kalish BT, Puder M, Ijzermans JN. Systematic review and meta-analysis of steatosis as a risk factor in major hepatic resection. Br J Surg. 2010;97(9):1331–9.CrossRefGoogle Scholar
  8. 8.
    Spitzer AL, Lao OB, Dick AA, Bakthavatsalam R, Halldorson JB, Yeh MM, et al. The biopsied donor liver: incorporating macrosteatosis into high-risk donor assessment. Liver Transpl. 2010;16(7):874–84.CrossRefGoogle Scholar
  9. 9.
    Hamer OW, Aguirre DA, Casola G, Lavine JE, Woenckhaus M, Sirlin CB. Fatty liver: imaging patterns and pitfalls. Radiographics. 2006;26(6):1637–53.CrossRefGoogle Scholar
  10. 10.
    Ho MC, Lin JJ, Shu YC, Chen CN, Chang KJ, Chang CC, et al. Using ultrasound Nakagami imaging to assess liver fibrosis in rats. Ultrasonics. 2012;52(2):215–22.CrossRefGoogle Scholar
  11. 11.
    Dasarathy S, Dasarathy J, Khiyami A, Joseph R, Lopez R, McCullough AJ. Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol. 2009;51(6):1061–7.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Riley TR 3rd, Mendoza A, Bruno MA. Bedside ultrasound can predict nonalcoholic fatty liver disease in the hands of clinicians using a prototype image. Dig Dis Sci. 2006;51(5):982–5.CrossRefGoogle Scholar
  13. 13.
    Scatarige JC, Scott WW, Donovan PJ, Siegelman SS, Sanders RC. Fatty infiltration of the liver: ultrasonographic and computed tomographic correlation. J Ultrasound Med. 1984;3(1):9–14.CrossRefGoogle Scholar
  14. 14.
    Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, et al. The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol. 2007;102(12):2708–15.CrossRefGoogle Scholar
  15. 15.
    Ballestri S, Lonardo A, Romagnoli D, Carulli L, Losi L, Day CP, et al. Ultrasonographic fatty liver indicator, a novel score which rules out NASH and is correlated with metabolic parameters in NAFLD. Liver Int. 2012;32(8):1242–52.CrossRefGoogle Scholar
  16. 16.
    Magalotti D, Marchesini G, Ramilli S, Berzigotti A, Bianchi G, Zoli M. Splanchnic haemodynamics in non-alcoholic fatty liver disease: effect of a dietary/pharmacological treatment. A pilot study. Dig Liver Dis. 2004;36(6):406–11.PubMedGoogle Scholar
  17. 17.
    Machado MV, Cortez-Pinto H. Non-invasive diagnosis of non-alcoholic fatty liver disease. A critical appraisal. J Hepatol. 2013;58(5):1007–19.CrossRefGoogle Scholar
  18. 18.
    Bril F, Ortiz-Lopez C, Lomonaco R, Orsak B, Freckleton M, Chintapalli K, et al. Clinical value of liver ultrasound for the diagnosis of nonalcoholic fatty liver disease in overweight and obese patients. Liver Int. 2015;35(9):2139–46.CrossRefGoogle Scholar
  19. 19.
    Mathiesen UL, Franzen LE, Aselius H, Resjo M, Jacobsson L, Foberg U, et al. Increased liver echogenicity at ultrasound examination reflects degree of steatosis but not of fibrosis in asymptomatic patients with mild/moderate abnormalities of liver transaminases. Dig Liver Dis. 2002;34(7):516–22.CrossRefGoogle Scholar
  20. 20.
    Cazzo E, de Felice Gallo F, Pareja JC, Chaim EA. Nonalcoholic fatty liver disease in morbidly obese subjects: correlation among histopathologic findings, biochemical features, and ultrasound evaluation. Obes Surg. 2014;24(4):666–8.CrossRefGoogle Scholar
  21. 21.
    Strauss S, Gavish E, Gottlieb P, Katsnelson L. Interobserver and intraobserver variability in the sonographic assessment of fatty liver. AJR Am J Roentgenol. 2007;189(6):W320–3.CrossRefGoogle Scholar
  22. 22.
    Guajardo-Salinas GE, Hilmy A. Prevalence of nonalcoholic fatty liver disease (NAFLD) and utility of FIBROspect II to detect liver fibrosis in morbidly obese Hispano-American patients undergoing gastric bypass. Obes Surg. 2010;20(12):1647–53.CrossRefGoogle Scholar
  23. 23.
    Pozzato C, Botta A, Melgara C, Fiori L, Gianni ML, Riva E. Sonographic findings in type I glycogen storage disease. J Clin Ultrasound. 2001;29(8):456–61.CrossRefGoogle Scholar
  24. 24.
    Berzigotti A, Abraldes JG, Tandon P, Erice E, Gilabert R, Garcia-Pagan JC, et al. Ultrasonographic evaluation of liver surface and transient elastography in clinically doubtful cirrhosis. J Hepatol. 2010;52(6):846–53.CrossRefGoogle Scholar
  25. 25.
    Berzigotti A, Piscaglia F, Education E, Professional Standards C. Ultrasound in portal hypertension—part 2—and EFSUMB recommendations for the performance and reporting of ultrasound examinations in portal hypertension. Ultraschall Med. 2012;33(1):8–32; quiz 0–1.CrossRefGoogle Scholar
  26. 26.
    Ratziu V, Bellentani S, Cortez-Pinto H, Day C, Marchesini G. A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol. 2010;53(2):372–84.CrossRefGoogle Scholar
  27. 27.
    Saadeh S, Younossi ZM, Remer EM, Gramlich T, Ong JP, Hurley M, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology. 2002;123(3):745–50.CrossRefGoogle Scholar
  28. 28.
    Liang RJ, Wang HH, Lee WJ, Liew PL, Lin JT, Wu MS. Diagnostic value of ultrasonographic examination for nonalcoholic steatohepatitis in morbidly obese patients undergoing laparoscopic bariatric surgery. Obes Surg. 2007;17(1):45–56.CrossRefGoogle Scholar
  29. 29.
    Zardi EM, De Sio I, Ghittoni G, Sadun B, Palmentieri B, Roselli P, et al. Which clinical and sonographic parameters may be useful to discriminate NASH from steatosis? J Clin Gastroenterol. 2011;45(1):59–63.CrossRefGoogle Scholar
  30. 30.
    Tarantino G, Conca P, Pasanisi F, Ariello M, Mastrolia M, Arena A, et al. Could inflammatory markers help diagnose nonalcoholic steatohepatitis? Eur J Gastroenterol Hepatol. 2009;21(5):504–11.CrossRefGoogle Scholar
  31. 31.
    Mendes FD, Suzuki A, Sanderson SO, Lindor KD, Angulo P. Prevalence and indicators of portal hypertension in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2012;10(9):1028–33.e2.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Berzigotti A, Castera L. Update on ultrasound imaging of liver fibrosis. J Hepatol. 2013;59(1):180–2.CrossRefGoogle Scholar
  33. 33.
    Mohammadinia AR, Bakhtavar K, Ebrahimi-Daryani N, Habibollahi P, Keramati MR, Fereshtehnejad SM, et al. Correlation of hepatic vein Doppler waveform and hepatic artery resistance index with the severity of nonalcoholic fatty liver disease. J Clin Ultrasound. 2010;38(7):346–52.PubMedGoogle Scholar
  34. 34.
    Oguzkurt L, Yildirim T, Torun D, Tercan F, Kizilkilic O, Niron EA. Hepatic vein Doppler waveform in patients with diffuse fatty infiltration of the liver. Eur J Radiol. 2005;54(2):253–7.CrossRefGoogle Scholar
  35. 35.
    Solhjoo E, Mansour-Ghanaei F, Moulaei-Langorudi R, Joukar F. Comparison of portal vein doppler indices and hepatic vein doppler waveform in patients with nonalcoholic fatty liver disease with healthy control. Hepat Mon. 2011;11(9):740–4.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Balci A, Karazincir S, Sumbas H, Oter Y, Egilmez E, Inandi T. Effects of diffuse fatty infiltration of the liver on portal vein flow hemodynamics. J Clin Ultrasound. 2008;36(3):134–40.CrossRefGoogle Scholar
  37. 37.
    Goyal N, Jain N, Rachapalli V, Cochlin DL, Robinson M. Non-invasive evaluation of liver cirrhosis using ultrasound. Clin Radiol. 2009;64(11):1056–66.CrossRefGoogle Scholar
  38. 38.
    Goceri E, Shah ZK, Layman R, Jiang X, Gurcan MN. Quantification of liver fat: a comprehensive review. Comput Biol Med. 2016;71:174–89.CrossRefGoogle Scholar
  39. 39.
    Webb M, Yeshua H, Zelber-Sagi S, Santo E, Brazowski E, Halpern Z, et al. Diagnostic value of a computerized hepatorenal index for sonographic quantification of liver steatosis. AJR Am J Roentgenol. 2009;192(4):909–14.CrossRefGoogle Scholar
  40. 40.
    Borges VF, Diniz AL, Cotrim HP, Rocha HL, Andrade NB. Sonographic hepatorenal ratio: a noninvasive method to diagnose nonalcoholic steatosis. J Clin Ultrasound. 2013;41(1):18–25.CrossRefGoogle Scholar
  41. 41.
    Marshall RH, Eissa M, Bluth EI, Gulotta PM, Davis NK. Hepatorenal index as an accurate, simple, and effective tool in screening for steatosis. AJR Am J Roentgenol. 2012;199(5):997–1002.CrossRefGoogle Scholar
  42. 42.
    Xia MF, Yan HM, He WY, Li XM, Li CL, Yao XZ, et al. Standardized ultrasound hepatic/renal ratio and hepatic attenuation rate to quantify liver fat content: an improvement method. Obesity. 2012;20(2):444–52.CrossRefGoogle Scholar
  43. 43.
    Martin-Rodriguez JL, Arrebola JP, Jimenez-Moleon JJ, Olea N, Gonzalez-Calvin JL. Sonographic quantification of a hepato-renal index for the assessment of hepatic steatosis in comparison with 3T proton magnetic resonance spectroscopy. Eur J Gastroenterol Hepatol. 2014;26(1):88–94.CrossRefGoogle Scholar
  44. 44.
    Mancini M, Prinster A, Annuzzi G, Liuzzi R, Giacco R, Medagli C, et al. Sonographic hepatic-renal ratio as indicator of hepatic steatosis: comparison with (1)H magnetic resonance spectroscopy. Metab Clin Exp. 2009;58(12):1724–30.CrossRefGoogle Scholar
  45. 45.
    Wang JH, Hung CH, Kuo FY, Eng HL, Chen CH, Lee CM, et al. Ultrasonographic quantification of hepatic-renal echogenicity difference in hepatic steatosis diagnosis. Dig Dis Sci. 2013;58(10):2993–3000.CrossRefGoogle Scholar
  46. 46.
    Ghoshal G, Lavarello RJ, Kemmerer JP, Miller RJ, Oelze ML. Ex vivo study of quantitative ultrasound parameters in fatty rabbit livers. Ultrasound Med Biol. 2012;38(12):2238–48.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Fujiwara Y, Kuroda H, Abe T, Ishida K, Oguri T, Noguchi S, et al. The B-mode image-guided ultrasound attenuation parameter accurately detects hepatic steatosis in chronic liver disease. Ultrasound Med Biol. 2018;44(11):2223–32.CrossRefGoogle Scholar
  48. 48.
    Dioguardi Burgio M, Imbault M, Ronot M, Faccinetto A, Van Beers BE, Rautou PE, et al. Ultrasonic adaptive sound speed estimation for the diagnosis and quantification of hepatic steatosis: a pilot study. Ultraschall Med. 2019;40(6):722–33.Google Scholar
  49. 49.
    Sasso M, Beaugrand M, de Ledinghen V, Douvin C, Marcellin P, Poupon R, et al. Controlled attenuation parameter (CAP): a novel VCTE 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(11):1825–35.CrossRefGoogle Scholar
  50. 50.
    de Ledinghen V, Vergniol J, Capdepont M, Chermak F, Hiriart JB, Cassinotto C, et al. Controlled attenuation parameter (CAP) for the diagnosis of steatosis: a prospective study of 5323 examinations. J Hepatol. 2014;60(5):1026–31.CrossRefGoogle Scholar
  51. 51.
    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(3):626–37.e7.CrossRefGoogle Scholar
  52. 52.
    Wang Y, Fan Q, Wang T, Wen J, Wang H, Zhang T. Controlled attenuation parameter for assessment of hepatic steatosis grades: a diagnostic meta-analysis. Int J Clin Exp Med. 2015;8(10):17654–63.PubMedPubMedCentralGoogle Scholar
  53. 53.
    Shi KQ, Tang JZ, Zhu XL, Ying L, Li DW, Gao J, et al. Controlled attenuation parameter for the detection of steatosis severity in chronic liver disease: a meta-analysis of diagnostic accuracy. J Gastroenterol Hepatol. 2014;29(6):1149–58.CrossRefGoogle Scholar
  54. 54.
    Myers RP, Pollett A, Kirsch R, Pomier-Layrargues G, Beaton M, Levstik M, et al. Controlled Attenuation Parameter (CAP): a noninvasive method for the detection of hepatic steatosis based on transient elastography. Liver Int. 2012;32(6):902–10.CrossRefGoogle Scholar
  55. 55.
    de Ledinghen V, Vergniol J, Foucher J, Merrouche W, le Bail B. Non-invasive diagnosis of liver steatosis using controlled attenuation parameter (CAP) and transient elastography. Liver Int. 2012;32(6):911–8.CrossRefGoogle Scholar
  56. 56.
    Kumar M, Rastogi A, Singh T, Behari C, Gupta E, Garg H, et al. Controlled attenuation parameter for non-invasive assessment of hepatic steatosis: does etiology affect performance? J Gastroenterol Hepatol. 2013;28(7):1194–201.CrossRefGoogle Scholar
  57. 57.
    Shen F, Zheng RD, Mi YQ, Wang XY, Pan Q, Chen GY, et al. Controlled attenuation parameter for non-invasive assessment of hepatic steatosis in Chinese patients. World J Gastroenterol: WJG. 2014;20(16):4702–11.CrossRefGoogle Scholar
  58. 58.
    Chan WK, Nik Mustapha NR, Mahadeva S. Controlled attenuation parameter for the detection and quantification of hepatic steatosis in nonalcoholic fatty liver disease. J Gastroenterol Hepatol. 2014;29(7):1470–6.CrossRefGoogle Scholar
  59. 59.
    Nascimbeni F, Lebray P, Fedchuk L, Oliveira CP, Alvares-da-Silva MR, Varault A, et al. Significant variations in elastometry measurements made within short-term in patients with chronic liver diseases. Clin Gastroenterol Hepatol. 2015;13(4):763–71.e1–6.CrossRefGoogle Scholar
  60. 60.
    Fedchuk L, Nascimbeni F, Pais R, Charlotte F, Housset C, Ratziu V, et al. Performance and limitations of steatosis biomarkers in patients with nonalcoholic fatty liver disease. Aliment Pharmacol Ther. 2014;40(10):1209–22.CrossRefGoogle Scholar
  61. 61.
    Friedrich-Rust M, Romen D, Vermehren J, Kriener S, Sadet D, Herrmann E, et al. Acoustic radiation force impulse-imaging and transient elastography for non-invasive assessment of liver fibrosis and steatosis in NAFLD. Eur J Radiol. 2012;81(3):e325–31.CrossRefGoogle Scholar
  62. 62.
    Masaki K, Takaki S, Hyogo H, Kobayashi T, Fukuhara T, Naeshiro N, et al. Utility of controlled attenuation parameter measurement for assessing liver steatosis in Japanese patients with chronic liver diseases. Hepatol Res. 2013;43(11):1182–9.CrossRefGoogle Scholar
  63. 63.
    Sasso M, Tengher-Barna I, Ziol M, Miette V, Fournier C, Sandrin L, et al. Novel controlled attenuation parameter for noninvasive assessment of steatosis using Fibroscan(®): validation in chronic hepatitis C. J Viral Hepat. 2012;19(4):244–53.CrossRefGoogle Scholar
  64. 64.
    Chon YE, Jung KS, Kim SU, Park JY, Park YN, Kim DY, et al. Controlled attenuation parameter (CAP) for detection of hepatic steatosis in patients with chronic liver diseases: a prospective study of a native Korean population. Liver Int. 2014;34(1):102–9.CrossRefGoogle Scholar
  65. 65.
    Karlas T, Petroff D, Garnov N, Bohm S, Tenckhoff H, Wittekind C, et al. Non-invasive assessment of hepatic steatosis in patients with NAFLD using controlled attenuation parameter and 1H-MR spectroscopy. PLoS One. 2014;9(3):e91987.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Yilmaz Y, Yesil A, Gerin F, Ergelen R, Akin H, Celikel CA, et al. Detection of hepatic steatosis using the controlled attenuation parameter: a comparative study with liver biopsy. Scand J Gastroenterol. 2014;49(5):611–6.CrossRefGoogle Scholar
  67. 67.
    Karlas T, Petroff D, Sasso M, Fan JG, Mi YQ, de Ledinghen V, et al. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol. 2017;66(5):1022–30.CrossRefGoogle Scholar
  68. 68.
    Carvalhana S, Leitao J, Alves AC, Bourbon M, Cortez-Pinto H. How good is controlled attenuation parameter and fatty liver index for assessing liver steatosis in general population: correlation with ultrasound. Liver Int. 2014;34(6):e111–7.CrossRefGoogle Scholar
  69. 69.
    Yilmaz Y, Ergelen R, Akin H, Imeryuz N. Noninvasive detection of hepatic steatosis in patients without ultrasonographic evidence of fatty liver using the controlled attenuation parameter evaluated with transient elastography. Eur J Gastroenterol Hepatol. 2013;25(11):1330–4.CrossRefGoogle Scholar
  70. 70.
    Kwok R, Choi KC, Wong GL, Zhang Y, Chan HL, Luk AO, et al. Screening diabetic patients for non-alcoholic fatty liver disease with controlled attenuation parameter and liver stiffness measurements: a prospective cohort study. Gut. 2016;65(8):1359–68.CrossRefGoogle Scholar
  71. 71.
    Cho Y, Tokuhara D, Morikawa H, Kuwae Y, Hayashi E, Hirose M, et al. Transient elastography-based liver profiles in a hospital-based pediatric population in Japan. PLoS One. 2015;10(9):e0137239.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    de Ledinghen V, Hiriart JB, Vergniol J, Merrouche W, Bedossa P, Paradis V. Controlled Attenuation Parameter (CAP) with the XL Probe of the Fibroscan(®): a comparative study with the M probe and liver biopsy. Dig Dis Sci. 2017;62(9):2569–77.CrossRefGoogle Scholar
  73. 73.
    Chan WK, Nik Mustapha NR, Wong GL, Wong VW, Mahadeva S. Controlled attenuation parameter using the FibroScan® XL probe for quantification of hepatic steatosis for non-alcoholic fatty liver disease in an Asian population. United European Gastroenterol J. 2017;5(1):76–85.CrossRefGoogle Scholar
  74. 74.
    Pathik P, Ravindra S, Ajay C, Prasad B, Jatin P, Prabha S. Fibroscan versus simple noninvasive screening tools in predicting fibrosis in high-risk nonalcoholic fatty liver disease patients from Western India. Ann Gastroenterol. 2015;28(2):281–6.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Siddiqui MS, Yamada G, Vuppalanchi R, Van Natta M, Loomba R, Guy C, et al. Diagnostic accuracy of noninvasive fibrosis models to detect change in fibrosis stage. Clin Gastroenterol Hepatol. 2019;17(9):1877–85.e5.CrossRefGoogle Scholar
  76. 76.
    Castera L. Noninvasive methods to assess liver disease in patients with hepatitis B or C. Gastroenterology. 2012;142(6):1293–302.e4.CrossRefGoogle Scholar
  77. 77.
    Sandrin L, Fourquet B, Hasquenoph JM, Yon S, Fournier C, Mal F, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29(12):1705–13.CrossRefGoogle Scholar
  78. 78.
    Fraquelli M, Rigamonti C, Casazza G, Conte D, Donato MF, Ronchi G, et al. Reproducibility of transient elastography in the evaluation of liver fibrosis in patients with chronic liver disease. Gut. 2007;56(7):968–73.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Foucher J, Chanteloup E, Vergniol J, Castera L, Le Bail B, Adhoute X, et al. Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut. 2006;55(3):403–8.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Castera L, Vergniol J, Foucher J, Le Bail B, Chanteloup E, Haaser M, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology. 2005;128(2):343–50.CrossRefGoogle Scholar
  81. 81.
    Yoneda M, Yoneda M, Mawatari H, Fujita K, Endo H, Iida H, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with nonalcoholic fatty liver disease (NAFLD). Dig Liver Dis. 2008;40(5):371–8.CrossRefGoogle Scholar
  82. 82.
    Yoneda M, Yoneda M, Fujita K, Inamori M, Tamano M, Hiriishi H, et al. Transient elastography in patients with non-alcoholic fatty liver disease (NAFLD). Gut. 2007;56(9):1330–1.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Wong VW, Vergniol J, Wong GL, Foucher J, Chan HL, Le Bail B, et al. Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease. Hepatology. 2010;51(2):454–62.CrossRefGoogle Scholar
  84. 84.
    Kwok R, Tse YK, Wong GL, Ha Y, Lee AU, Ngu MC, et al. Systematic review with meta-analysis: non-invasive assessment of non-alcoholic fatty liver disease—the role of transient elastography and plasma cytokeratin-18 fragments. Aliment Pharmacol Ther. 2014;39(3):254–69.CrossRefGoogle Scholar
  85. 85.
    Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G. 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(5):1486–501.CrossRefGoogle Scholar
  86. 86.
    Chang PE, Goh GB, Ngu JH, Tan HK, Tan CK. Clinical applications, limitations and future role of transient elastography in the management of liver disease. World J Gastrointest Pharmacol Ther. 2016;7(1):91–106.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Petta S, Wong VW, Camma C, Hiriart JB, Wong GL, Marra F, et al. Improved noninvasive prediction of liver fibrosis by liver stiffness measurement in patients with nonalcoholic fatty liver disease accounting for controlled attenuation parameter values. Hepatology. 2017;65(4):1145–55.CrossRefGoogle Scholar
  88. 88.
    Coco B, Oliveri F, Maina AM, Ciccorossi P, Sacco R, Colombatto P, et al. Transient elastography: a new surrogate marker of liver fibrosis influenced by major changes of transaminases. J Viral Hepat. 2007;14(5):360–9.CrossRefGoogle Scholar
  89. 89.
    Wong GL, Wong VW, Choi PC, Chan AW, Chum RH, Chan HK, et al. Assessment of fibrosis by transient elastography compared with liver biopsy and morphometry in chronic liver diseases. Clin Gastroenterol Hepatol. 2008;6(9):1027–35.CrossRefGoogle Scholar
  90. 90.
    Arena U, Vizzutti F, Corti G, Ambu S, Stasi C, Bresci S, et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology. 2008;47(2):380–4.CrossRefGoogle Scholar
  91. 91.
    Sagir A, Erhardt A, Schmitt M, Haussinger D. Transient elastography is unreliable for detection of cirrhosis in patients with acute liver damage. Hepatology. 2008;47(2):592–5.CrossRefGoogle Scholar
  92. 92.
    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(3):828–35.PubMedGoogle Scholar
  93. 93.
    Wong GL, Wong VW, Chim AM, Yiu KK, Chu SH, Li MK, et al. Factors associated with unreliable liver stiffness measurement and its failure with transient elastography in the Chinese population. J Gastroenterol Hepatol. 2011;26(2):300–5.CrossRefGoogle Scholar
  94. 94.
    Petta S, Di Marco V, Camma C, Butera G, Cabibi D, Craxi A. Reliability of liver stiffness measurement in non-alcoholic fatty liver disease: the effects of body mass index. Aliment Pharmacol Ther. 2011;33(12):1350–60.CrossRefGoogle Scholar
  95. 95.
    Myers RP, Crotty P, Pomier-Layrargues G, Ma M, Urbanski SJ, Elkashab M. Prevalence, risk factors and causes of discordance in fibrosis staging by transient elastography and liver biopsy. Liver Int. 2010;30(10):1471–80.CrossRefGoogle Scholar
  96. 96.
    Wong VW, Vergniol J, Wong GL, Foucher J, Chan AW, Chermak F, et al. Liver stiffness measurement using XL probe in patients with nonalcoholic fatty liver disease. Am J Gastroenterol. 2012;107(12):1862–71.CrossRefGoogle Scholar
  97. 97.
    Myers RP, Pomier-Layrargues G, Kirsch R, Pollett A, Beaton M, Levstik M, et al. Discordance in fibrosis staging between liver biopsy and transient elastography using the FibroScan XL probe. J Hepatol. 2012;56(3):564–70.CrossRefGoogle Scholar
  98. 98.
    Myers RP, Pomier-Layrargues G, Kirsch R, Pollett A, Duarte-Rojo A, Wong D, et al. Feasibility and diagnostic performance of the FibroScan XL probe for liver stiffness measurement in overweight and obese patients. Hepatology. 2012;55(1):199–208.CrossRefGoogle Scholar
  99. 99.
    de Ledinghen V, Wong VW, Vergniol J, Wong GL, Foucher J, Chu SH, et al. Diagnosis of liver fibrosis and cirrhosis using liver stiffness measurement: comparison between M and XL probe of FibroScan®. J Hepatol. 2012;56(4):833–9.CrossRefGoogle Scholar
  100. 100.
    Naveau S, Lamouri K, Pourcher G, Njike-Nakseu M, Ferretti S, Courie R, et al. The diagnostic accuracy of transient elastography for the diagnosis of liver fibrosis in bariatric surgery candidates with suspected NAFLD. Obes Surg. 2014;24(10):1693–701.CrossRefGoogle Scholar
  101. 101.
    Suzuki K, Yoneda M, Imajo K, Kirikoshi H, Nakajima A, Maeda S, et al. Transient elastography for monitoring the fibrosis of non-alcoholic fatty liver disease for 4 years. Hepatol Res. 2013;43(9):979–83.CrossRefGoogle Scholar
  102. 102.
    Petta S, Sebastiani G, Bugianesi E, Vigano M, Wong VW, Berzigotti A, et al. Non-invasive prediction of esophageal varices by stiffness and platelet in non-alcoholic fatty liver disease cirrhosis. J Hepatol. 2018;69(4):878–85.CrossRefGoogle Scholar
  103. 103.
    Piscaglia F, Marinelli S, Bota S, Serra C, Venerandi L, Leoni S, et al. The role of ultrasound elastographic techniques in chronic liver disease: current status and future perspectives. Eur J Radiol. 2014;83(3):450–5.CrossRefGoogle Scholar
  104. 104.
    Ebinuma H, Saito H, Komuta M, Ojiro K, Wakabayashi K, Usui S, et al. Evaluation of liver fibrosis by transient elastography using acoustic radiation force impulse: comparison with Fibroscan(®). J Gastroenterol. 2011;46(10):1238–48.CrossRefGoogle Scholar
  105. 105.
    Yoneda M, Suzuki K, Kato S, Fujita K, Nozaki Y, Hosono K, et al. Nonalcoholic fatty liver disease: US-based acoustic radiation force impulse elastography. Radiology. 2010;256(2):640–7.CrossRefGoogle Scholar
  106. 106.
    Yoneda M, Imajo K, Kirikoshi H, Nakajima A. Acoustic radiation force-based shear stiffness and non-invasive panels of tests in Japanese patients with nonalcoholic fatty liver disease. J Hepatol. 2012;56(3):740–1.CrossRefGoogle Scholar
  107. 107.
    Yoon KT, Lim SM, Park JY, Kim DY, Ahn SH, Han KH, et al. Liver stiffness measurement using acoustic radiation force impulse (ARFI) elastography and effect of necroinflammation. Dig Dis Sci. 2012;57(6):1682–91.CrossRefGoogle Scholar
  108. 108.
    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(6):1817–27.CrossRefGoogle Scholar
  109. 109.
    Bota S, Herkner H, Sporea I, Salzl P, Sirli R, Neghina AM, et al. Meta-analysis: ARFI elastography versus transient elastography for the evaluation of liver fibrosis. Liver Int. 2013;33(8):1138–47.CrossRefGoogle Scholar
  110. 110.
    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(11):3040–53.CrossRefGoogle Scholar
  111. 111.
    Herrmann E, de Ledinghen V, Cassinotto C, Chu WC, Leung VY, Ferraioli G, et al. Assessment of biopsy-proven liver fibrosis by two-dimensional shear wave elastography: an individual patient data-based meta-analysis. Hepatology. 2018;67(1):260–72.CrossRefGoogle Scholar
  112. 112.
    Alkhouri N, Feldstein AE. Noninvasive diagnosis of nonalcoholic fatty liver disease: are we there yet? Metab Clin Exp. 2016;65(8):1087–95.CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Petta S, Vanni E, Bugianesi E, Di Marco V, Camma C, Cabibi D, et al. The combination of liver stiffness measurement and NAFLD fibrosis score improves the noninvasive diagnostic accuracy for severe liver fibrosis in patients with nonalcoholic fatty liver disease. Liver Int. 2015;35(5):1566–73.CrossRefGoogle Scholar
  114. 114.
    Tapper EB, Sengupta N, Hunink MG, Afdhal NH, Lai M. Cost-effective evaluation of nonalcoholic fatty liver disease with NAFLD fibrosis score and vibration controlled transient elastography. Am J Gastroenterol. 2015;110(9):1298–304.CrossRefGoogle Scholar
  115. 115.
    Ahmed M. Non-alcoholic fatty liver disease in 2015. World J Hepatol. 2015;7(11):1450–9.CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Mikolasevic I, Milic S, Orlic L, Stimac D, Franjic N, Targher G. Factors associated with significant liver steatosis and fibrosis as assessed by transient elastography in patients with one or more components of the metabolic syndrome. J Diabetes Complicat. 2016;30(7):1347–53.CrossRefGoogle Scholar
  117. 117.
    Lupsor-Platon M, Feier D, Stefanescu H, Tamas A, Botan E, Sparchez Z, et al. Diagnostic accuracy of controlled attenuation parameter measured by transient elastography for the non-invasive assessment of liver steatosis: a prospective study. J Gastrointestin Liver Dis. 2015;24(1):35–42.PubMedGoogle Scholar
  118. 118.
    de Ledinghen V, Wong GL, Vergniol J, Chan HL, Hiriart JB, Chan AW, et al. Controlled attenuation parameter for the diagnosis of steatosis in non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2016;31(4):848–55.CrossRefGoogle Scholar
  119. 119.
    Park CC, Nguyen P, Hernandez C, Bettencourt R, Ramirez K, Fortney L, 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(3):598–607.e2.CrossRefGoogle Scholar
  120. 120.
    Runge JH, Smits LP, Verheij J, Depla A, Kuiken SD, Baak BC, et al. MR spectroscopy-derived proton density fat fraction is superior to controlled attenuation parameter for detecting and grading hepatic steatosis. Radiology. 2018;286(2):547–56.CrossRefGoogle Scholar
  121. 121.
    Naveau S, Voican CS, Lebrun A, Gaillard M, Lamouri K, Njike-Nakseu M, et al. Controlled attenuation parameter for diagnosing steatosis in bariatric surgery candidates with suspected nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol. 2017;29(9):1022–30.CrossRefGoogle Scholar
  122. 122.
    Siddiqui MS, Vuppalanchi R, Van Natta ML, Hallinan E, Kowdley KV, Abdelmalek M, et al. Vibration-controlled transient elastography to assess fibrosis and steatosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2019;17(1):156–63.e2.CrossRefGoogle Scholar
  123. 123.
    Eddowes PJ, Sasso M, Allison M, Tsochatzis E, Anstee QM, Sheridan D, et al. Accuracy of FibroScan controlled attenuation parameter and liver stiffness measurement in assessing steatosis and fibrosis in patients with nonalcoholic fatty liver disease. Gastroenterology. 2019;156(6):1717–30.CrossRefGoogle Scholar
  124. 124.
    Nobili V, Vizzutti F, Arena U, Abraldes JG, Marra F, Pietrobattista A, et al. Accuracy and reproducibility of transient elastography for the diagnosis of fibrosis in pediatric nonalcoholic steatohepatitis. Hepatology. 2008;48(2):442–8.CrossRefGoogle Scholar
  125. 125.
    Lupsor M, Badea R, Stefanescu H, Grigorescu M, Serban A, Radu C, et al. Performance of unidimensional transient elastography in staging non-alcoholic steatohepatitis. J Gastrointestin Liver Dis. 2010;19(1):53–60.PubMedGoogle Scholar
  126. 126.
    Gaia S, Carenzi S, Barilli AL, Bugianesi E, Smedile A, Brunello F, et al. Reliability of transient elastography for the detection of fibrosis in non-alcoholic fatty liver disease and chronic viral hepatitis. J Hepatol. 2011;54(1):64–71.CrossRefGoogle Scholar
  127. 127.
    Kumar R, Rastogi A, Sharma MK, Bhatia V, Tyagi P, Sharma P, et al. Liver stiffness measurements in patients with different stages of nonalcoholic fatty liver disease: diagnostic performance and clinicopathological correlation. Dig Dis Sci. 2013;58(1):265–74.CrossRefGoogle Scholar
  128. 128.
    Tapper EB, Challies T, Nasser I, Afdhal NH, Lai M. The performance of vibration controlled transient elastography in a US cohort of patients with nonalcoholic fatty liver disease. Am J Gastroenterol. 2016;111(5):677–84.CrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    Boursier J, Vergniol J, Guillet A, Hiriart JB, Lannes A, Le Bail B, et al. Diagnostic accuracy and prognostic significance of blood fibrosis tests and liver stiffness measurement by FibroScan in non-alcoholic fatty liver disease. J Hepatol. 2016;65(3):570–8.CrossRefGoogle Scholar
  130. 130.
    Petta S, Wong VW, Camma C, Hiriart JB, Wong GL, Vergniol J, et al. Serial combination of non-invasive tools improves the diagnostic accuracy of severe liver fibrosis in patients with NAFLD. Aliment Pharmacol Ther. 2017;46(6):617–27.CrossRefGoogle Scholar
  131. 131.
    Chen J, Yin M, Talwalkar JA, Oudry J, Glaser KJ, Smyrk TC, 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(2):418–28.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Hepatology, University Clinic for Visceral Surgery and Medicine (UVCM), Inselspital and Department of Biomedical Research (DBMR)University of BernBernSwitzerland
  2. 2.Department of Hepatobiliary SurgeryThe Third Xiangya Hospital, Central South UniversityChangshaChina

Personalised recommendations