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Current Hepatology Reports

, Volume 18, Issue 4, pp 492–502 | Cite as

Quantification of Liver Fat in NAFLD: Available Modalities and Clinical Significance

  • Kee-Huat Chuah
  • Wah-Kheong ChanEmail author
Fatty Liver Disease (V Ajmera, Section Editor)
  • 30 Downloads
Part of the following topical collections:
  1. Topical Collection on Fatty Liver Disease

Abstract

Purpose of Review

To review the available modalities for quantification of liver fat in nonalcoholic fatty liver disease (NAFLD) and their clinical significance.

Recent Findings

Ultrasonography remains the first line imaging used to diagnose NAFLD as it is widely available and relatively inexpensive. Controlled attenuation parameter can be used as a screening tool for fatty liver as it is reasonably accurate and provides simultaneous estimation of hepatic fibrosis. Magnetic resonance imaging proton density fat fraction and magnetic resonance spectroscopy are the most accurate noninvasive modalities for quantification of hepatic steatosis. Liver biopsy remains the gold standard but is limited by the invasive nature of the procedure, and observer and sampling variability. This may be improved with novel computer-assisted stereological analysis or second harmonic generation microscopy.

Summary

Understanding the advantages and disadvantages of each of the modalities will help one choose the most suitable method for quantifying hepatic steatosis in NAFLD.

Keywords

Hepatic steatosis MRI-PDFF MRS CAP 

Notes

Compliance with Ethical Standards

Conflict of Interest

Kee-Huat Chuah declares no potential conflicts of interest.

Wah-Kheong Chan reports speaking for Echosens and a grant from Resonance Health for an investigator-initiated study.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Wah-Kheong C, Khean-Lee G. Epidemiology of a fast emerging disease in the Asia-Pacific region: non-alcoholic fatty liver disease. Hepatol Int. 2013;7:65–71.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    • Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64:73–84 The meta-analysis reporting on the latest global prevalence and clinical and economic burden of NAFLD.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Musso G, Gambino R, Cassader M, Pagano G. Meta-analysis: natural history of non-alcoholic fatty liver disease (NAFLD) and diagnostic accuracy of non-invasive tests for liver disease severity. Ann Med. 2011;43:617–49.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Sayiner M, Otgonsuren M, Cable R, Younossi I, Afendy M, Golabi P, et al. Variables associated with inpatient and outpatient resource utilization among Medicare beneficiaries with nonalcoholic fatty liver disease with or without cirrhosis. J Clin Gastroenterol. 2017;51:254–60.PubMedPubMedCentralGoogle Scholar
  5. 5.
    Wong VW, Chan WK, Chitturi S, Chawla Y, Dan YY, Duseja A, et al. Asia-Pacific Working Party on Non-alcoholic Fatty Liver Disease guidelines 2017-Part 1: definition, risk factors and assessment. J Gastroenterol Hepatol. 2018;33:70–85.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    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;123:745–50.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Lee SS, Park SH, Kim HJ, Kim SY, Kim MY, Kim DY, et al. Non-invasive assessment of hepatic steatosis: prospective comparison of the accuracy of imaging examinations. J Hepatol. 2010;52:579–85.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    • Hernaez R, Lazo M, Bonekamp S, Kamel I, Brancati FL, Guallar E, et al. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis. Hepatology. 2011;54:1082–90 Important major meta-analysis reporting on the reliabilty and accuracy in detecting moderate-to-severe fatty liver, compared with histology.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    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:W320–3.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Lee SS, Park SH. Radiologic evaluation of nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:7392–402.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Kromrey ML, Ittermann T, Berning M, Kolb C, Hoffmann RT, Lerch MM, et al. Accuracy of ultrasonography in the assessment of liver fat compared with MRI. Clin Radiol. 2019;74:539–46.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Lee DH. Imaging evaluation of non-alcoholic fatty liver disease: focused on quantification. Clinical and molecular hepatology. 2017;23:290–301.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    • 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;192:909–14 The original article describing hepatorenal sonograhic index as a sensitive noninvasive method for steatosis quantification.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    de Almeidae Borges VF, ALD D, Cotrim HP, HLOG R, Andrade NB. Sonographic hepatorenal ratio: a noninvasive method to diagnose nonalcoholic steatosis. J Clin Ultrasound. 2013;41:18–25.CrossRefGoogle Scholar
  15. 15.
    Son JY, Lee JY, Yi NJ, Lee KW, Suh KS, Kim KG, et al. Hepatic steatosis: assessment with acoustic structure quantification of US imaging. Radiology. 2016;278:257–64.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Kuroda H, Kakisaka K, Kamiyama N, Oikawa T, Onodera M, Sawara K, et al. Non-invasive determination of hepatic steatosis by acoustic structure quantification from ultrasound echo amplitude. World J Gastroenterol. 2012;18:3889–95.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Lin SC, Heba E, Wolfson T, Ang B, Gamst A, Han A, et al. Noninvasive diagnosis of nonalcoholic fatty liver disease and quantification of liver fat using a new quantitative ultrasound technique. Clin Gastroenterol Hepatol. 2015;13:1337–1345.e1336.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Pickhardt PJ, Park SH, Hahn L, Lee SG, Bae KT, Yu ES. Specificity of unenhanced CT for non-invasive diagnosis of hepatic steatosis: implications for the investigation of the natural history of incidental steatosis. Eur Radiol. 2012;22:1075–82.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Birnbaum BA, Hindman N, Lee J, Babb JS. Multi-detector row CT attenuation measurements: assessment of intra- and interscanner variability with an anthropomorphic body CT phantom. Radiology. 2007;242:109–19.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Park YS, Park SH, Lee SS, Kim DY, Shin YM, Lee W, et al. Biopsy-proven nonsteatotic liver in adults: estimation of reference range for difference in attenuation between the liver and the spleen at nonenhanced CT. Radiology. 2011;258:760–6.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Zhang Y, Wang C, Duanmu Y, Zhang C, Zhao W, Wang L, et al. Comparison of CT and magnetic resonance mDIXON-Quant sequence in the diagnosis of mild hepatic steatosis. Br J Radiol. 2018;91:20170587.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Reeder SB, Cruite I, Hamilton G, Sirlin CB. Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging. 2011;34:729–49.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Chartampilas E. Imaging of nonalcoholic fatty liver disease and its clinical utility. Hormones (Athens). 2018;17:69–81.CrossRefGoogle Scholar
  24. 24.
    Qu Y, Li M, Hamilton G, Zhang YN, Song B. Diagnostic accuracy of hepatic proton density fat fraction measured by magnetic resonance imaging for the evaluation of liver steatosis with histology as reference standard: a meta-analysis. Eur Radiol 2019.Google Scholar
  25. 25.
    •• Bohte AE, van Werven JR, Bipat S, Stoker J. The diagnostic accuracy of US, CT, MRI and 1H-MRS for the evaluation of hepatic steatosis compared with liver biopsy: a meta-analysis. Eur Radiol. 2011;21:87–97 The meta-analysis describing diagnostic accuracy of US, CT, MRI, and MRS, compared with histology in evaluating hepatic steatosis. PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Zheng D, Guo Z, Schroder PM, Zheng Z, Lu Y, Gu J, et al. Accuracy of MR imaging and MR spectroscopy for detection and quantification of hepatic steatosis in living liver donors: a meta-analysis. Radiology. 2017;282:92–102.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Gu J, Liu S, Du S, Zhang Q, Xiao J, Dong Q, et al. Diagnostic value of MRI-PDFF for hepatic steatosis in patients with non-alcoholic fatty liver disease: a meta-analysis. Eur Radiol. 2019;29:3564–73.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Idilman IS, Keskin O, Celik A, Savas B, Elhan AH, Idilman R, et al. A comparison of liver fat content as determined by magnetic resonance imaging-proton density fat fraction and MRS versus liver histology in non-alcoholic fatty liver disease. Acta Radiol. 2016;57:271–8.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Heba ER, Desai A, Zand KA, Hamilton G, Wolfson T, Schlein AN, et al. Accuracy and the effect of possible subject-based confounders of magnitude-based MRI for estimating hepatic proton density fat fraction in adults, using MR spectroscopy as reference. J Magn Reson Imaging. 2016;43:398–406.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Yokoo T, Serai SD, Pirasteh A, Bashir MR, Hamilton G, Hernando D, et al. Linearity, bias, and precision of hepatic proton density fat fraction measurements by using MR imaging: a meta-analysis. Radiology. 2018;286:486–98.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Kang GH, Cruite I, Shiehmorteza M, Wolfson T, Gamst AC, Hamilton G, et al. Reproducibility of MRI-determined proton density fat fraction across two different MR scanner platforms. J Magn Reson Imaging. 2011;34:928–34.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Bachtiar V, Kelly MD, Wilman HR, Jacobs J, Newbould R, Kelly CJ, et al. Repeatability and reproducibility of multiparametric magnetic resonance imaging of the liver. PLoS One. 2019;14:e0214921.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Adams LA. End-points for drug treatment in NASH. Hepatol Int. 2019;13:253–8.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Caussy C, Reeder SB, Sirlin CB, Loomba R. Noninvasive, quantitative assessment of liver fat by MRI-PDFF as an endpoint in NASH trials. Hepatology. 2018;68:763–72.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Siddiqui MS, Harrison SA, Abdelmalek MF, Anstee QM, Bedossa P, Castera L, et al. Case definitions for inclusion and analysis of endpoints in clinical trials for nonalcoholic steatohepatitis through the lens of regulatory science. Hepatology. 2018;67:2001–12.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Loomba R, Sirlin CB, Ang B, Bettencourt R, Jain R, Salotti J, et al. Ezetimibe for the treatment of nonalcoholic steatohepatitis: assessment by novel magnetic resonance imaging and magnetic resonance elastography in a randomized trial (MOZART trial). Hepatology. 2015;61:1239–50.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    •• Noureddin M, Lam J, Peterson MR, Middleton M, Hamilton G, Le TA, et al. Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials. Hepatology. 2013;58:1930–40 The original paper describing MRI-PDFF and MRS correlated well and more sensitive than histology in quantifying steatosis changes.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Patel J, Bettencourt R, Cui J, Salotti J, Hooker J, Bhatt A, et al. Association of noninvasive quantitative decline in liver fat content on MRI with histologic response in nonalcoholic steatohepatitis. Ther Adv Gastroenterol. 2016;9:692–701.CrossRefGoogle Scholar
  39. 39.
    Di Martino M, Pacifico L, Bezzi M, Di Miscio R, Sacconi B, Chiesa C, 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.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    • 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;36:1825–35 The original paper describing controlled attenuation parameter for evaluation of hepatic steatosis in patients with chronic liver disease.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    •• 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((R)): validation in chronic hepatitis C. J Viral Hepat. 2012;19:244–53 The original paper providing validation of controlled attenuation parameter for evaluation of hepatic steatosis.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    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;32:902–10.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    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;32:911–8.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    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;28:1194–201.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    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;34:102–9.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    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;43:1182–9.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    • 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;29:1470–6 The original paper on controlled attenuation parameter for evaluation of hepatic steatosis in NAFLD patients that described reduced accuracy with increased body mass index.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    • Shen F, Zheng RD, Shi JP, Mi YQ, Chen GF, Hu X, et al. Impact of skin capsular distance on the performance of controlled attenuation parameter in patients with chronic liver disease. Liver Int. 2015;35:2392–400 The original paper on controlled attenuation parameter for evaluation of hepatic steatosis that showed reduced accuracy with increased skin capsular distance.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    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;49:611–6.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    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. 2014;20:4702–11.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    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:e91987.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    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;60:1026–31.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Ferraioli G, Tinelli C, Lissandrin R, Zicchetti M, Dal Bello B, Filice G, et al. Controlled attenuation parameter for evaluating liver steatosis in chronic viral hepatitis. World J Gastroenterol. 2014;20:6626–31.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Jung KS, Kim BK, Kim SU, Chon YE, Chun KH, Kim SB, et al. Factors affecting the accuracy of controlled attenuation parameter (CAP) in assessing hepatic steatosis in patients with chronic liver disease. PLoS One. 2014;9:e98689.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Wang CY, Lu W, Hu DS, Wang GD, Cheng XJ. Diagnostic value of controlled attenuation parameter for liver steatosis in patients with chronic hepatitis B. World J Gastroenterol. 2014;20:10585–90.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    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;24:35–42.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Mi YQ, Shi QY, Xu L, Shi RF, Liu YG, Li P, et al. Controlled attenuation parameter for noninvasive assessment of hepatic steatosis using Fibroscan(R): validation in chronic hepatitis B. Dig Dis Sci. 2015;60:243–51.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    • Chan WK, Nik Mustapha NR, Wong GL, Wong VW, Mahadeva S. Controlled attenuation parameter using the FibroScan(R) XL probe for quantification of hepatic steatosis for non-alcoholic fatty liver disease in an Asian population. United European Gastroenterol J. 2017;5:76–85 The original paper on controlled attenuation parameter using XL probe in NAFLD patients, showing similar accuracy for evaluation of hepatic steatosis as the conventional M probe.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Cardoso AC, Beaugrand M, de Ledinghen V, Douvin C, Poupon R, Trinchet JC, et al. Diagnostic performance of controlled attenuation parameter for predicting steatosis grade in chronic hepatitis B. Ann Hepatol. 2015;14:826–36.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    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;31:848–55.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Chen J, Wu D, Wang M, Chen E, Bai L, Liu C, et al. Controlled attenuation parameter for the detection of hepatic steatosis in patients with chronic hepatitis B. Infect Dis (Lond). 2016;48:670–5.CrossRefGoogle Scholar
  62. 62.
    Hong YM, Yoon KT, Cho M, Chu CW, Rhu JH, Yang KH, et al. Clinical usefulness of controlled attenuation parameter to screen hepatic steatosis for potential donor of living donor liver transplant. Eur J Gastroenterol Hepatol. 2017;29:805–10.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Wong VW, Petta S, Hiriart JB, Camma C, Wong GL, Marra F, et al. Validity criteria for the diagnosis of fatty liver by M probe-based controlled attenuation parameter. J Hepatol. 2017;67:577–84.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    • de Ledinghen V, Hiriart JB, Vergniol J, Merrouche W, Bedossa P, Paradis V. Controlled attenuation parameter (CAP) with the XL probe of the fibroscan((R)): a comparative study with the M probe and liver biopsy. Dig Dis Sci. 2017;62:2569–77 The original paper on controlled attenuation parameter using XL probe in patients with chronic liver disease of various aetiologies, showing similar accuracy for evaluation of hepatic steatosis as the conventional M probe.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Andrade P, Rodrigues S, Rodrigues-Pinto E, Gaspar R, Lopes J, Lopes S, et al. Diagnostic accuracy of controlled attenuation parameter for detecting hepatic steatosis in patients with chronic liver disease. GE Port J Gastroenterol. 2017;24:161–8.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Thiele M, Rausch V, Fluhr G, Kjaergaard M, Piecha F, Mueller J, et al. Controlled attenuation parameter and alcoholic hepatic steatosis: diagnostic accuracy and role of alcohol detoxification. J Hepatol. 2018;68:1025–32.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    • Chan WK, Nik Mustapha NR, Mahadeva S, Wong VW, Cheng JY, Wong GL. Can the same controlled attenuation parameter cut-offs be used for M and XL probes for diagnosing hepatic steatosis? J Gastroenterol Hepatol. 2018;33:1787–94 The original paper on controlled attenuation parameter using XL probe in patients with chronic liver disease of various aetiologies, suggesting that the same cutoffs may be used as for the conventional M probe for the diagnosis of the different grades of hepatic steatosis.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Mendes LC, Ferreira PA, Miotto N, Zanaga L, Lazarini MS, Goncales ESL, et al. Controlled attenuation parameter for steatosis grading in chronic hepatitis C compared with digital morphometric analysis of liver biopsy: impact of individual elastography measurement quality. Eur J Gastroenterol Hepatol. 2018;30:959–66.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Yen YH, Kuo FY, Lin CC, Chen CL, Chang KC, Tsai MC, et al. Predicting hepatic steatosis in living liver donors via controlled attenuation parameter. Transplant Proc. 2018;50:3533–8.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    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;156:1717–30.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Rout G, Kedia S, Nayak B, Yadav R, Das P, Acharya SK, et al. Controlled attenuation parameter for assessment of hepatic steatosis in Indian patients. J Clin Exp Hepatol. 2019;9:13–21.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Baumeler S, Jochum W, Neuweiler J, Bergamin I, Semela D. Controlled attenuation parameter for the assessment of liver steatosis in comparison with liver histology: a single-centre real life experience. Swiss Med Wkly. 2019;149:w20077.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Somda S, Lebrun A, Tranchart H, Lamouri K, Prevot S, Njike-Nakseu M, et al. Adaptation of controlled attenuation parameter (CAP) measurement depth in morbidly obese patients addressed for bariatric surgery. PLoS One. 2019;14:e0217093.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Semmler G, Stift J, Scheiner B, Woran K, Schwabl P, Paternostro R, Bucsics T, et al. Performance of controlled attenuation parameter in patients with advanced chronic liver disease and portal hypertension. Dig Dis Sci 2019.Google Scholar
  75. 75.
    Xu L, Lu W, Li P, Shen F, Mi YQ, Fan JG. A comparison of hepatic steatosis index, controlled attenuation parameter and ultrasound as noninvasive diagnostic tools for steatosis in chronic hepatitis B. Dig Liver Dis. 2017;49:910–7.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    •• 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;66:1022–30 The individual patient data meta-analysis that defined the optimal cutoffs for the diagnosis of the different grades of hepatic steatosis.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    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;55:199–208.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Caussy C, Alquiraish MH, Nguyen P, Hernandez C, Cepin S, Fortney LE, et al. Optimal threshold of controlled attenuation parameter with MRI-PDFF as the gold standard for the detection of hepatic steatosis. Hepatology. 2018;67:1348–59.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    •• Boursier J, Zarski JP, de Ledinghen V, Rousselet MC, Sturm N, Lebail B, et al. Determination of reliability criteria for liver stiffness evaluation by transient elastography. Hepatology. 2013;57:1182–91 The original article that defined the reliability criteria for transient elastography.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Ratchatasettakul K, Rattanasiri S, Promson K, Sringam P, Sobhonslidsuk A. The inverse effect of meal intake on controlled attenuation parameter and liver stiffness as assessed by transient elastography. BMC Gastroenterol. 2017;17:50.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Silva M, Costa Moreira P, Peixoto A, Santos AL, Lopes S, Goncalves R, et al. Effect of meal ingestion on liver stiffness and controlled attenuation parameter. GE Port J Gastroenterol. 2019;26:99–104.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Arena U, Lupsor Platon M, Stasi C, Moscarella S, Assarat A, Bedogni G, et al. Liver stiffness is influenced by a standardized meal in patients with chronic hepatitis C virus at different stages of fibrotic evolution. Hepatology. 2013;58:65–72.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    • Kwak MS, Chung GE, Yang JI, Yim JY, Chung SJ, Jung SY, et al. Clinical implications of controlled attenuation parameter in a health check-up cohort. Liver Int. 2018;38:915–23 The original article evaluating the use of CAP in a health check-up population.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Seto WK, Hui RWH, Mak LY, Fung J, Cheung KS, Liu KSH, et al. Association between hepatic steatosis, measured by controlled attenuation parameter, and fibrosis burden in chronic hepatitis B. Clin Gastroenterol Hepatol. 2018;16:575–83 e572.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    • 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;150:626–637 e627 The original article that compared the diagnostic accuracy of MRI-PDFF and CAP for the diagnosis of the different grades of hepatic steatosis in NAFLD patients.CrossRefGoogle Scholar
  86. 86.
    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;286:547–56.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Margini C, Murgia G, Stirnimann G, De Gottardi A, Semmo N, Casu S, et al. Prognostic significance of controlled attenuation parameter in patients with compensated advanced chronic liver disease. Hepatol Commun. 2018;2:929–40.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Scheiner B, Steininger L, Semmler G, Unger LW, Schwabl P, Bucsics T, et al. Controlled attenuation parameter does not predict hepatic decompensation in patients with advanced chronic liver disease. Liver Int. 2019;39:127–35.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Liu K, Wong VW, Lau K, Liu SD, Tse YK, Yip TC, et al. Prognostic value of controlled attenuation parameter by transient elastography. Am J Gastroenterol. 2017;112:1812–23.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    • Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, 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 The latest guidelines from the AASLD on diagnosis and management of NAFLD.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    •• Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41:1313–21 The original article on the histological scoring system for NAFLD, including the grading of hepatic steatosis, which has been used as the reference standard for most studies on diagnostic tests for hepatic steatosis.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Ratziu V, Charlotte F, Heurtier A, Gombert S, Giral P, Bruckert E, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128:1898–906.CrossRefGoogle Scholar
  93. 93.
    • St Pierre TG, House MJ, Bangma SJ, Pang W, Bathgate A, Gan EK, et al. Stereological analysis of liver biopsy histology sections as a reference standard for validating non-invasive liver fat fraction measurements by MRI. PLoS One. 2016;11:e0160789 The original article describing the use of stereological anlaysis as reference standard for measuring hepatic steatosis.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Sun W, Chang S, Tai DC, Tan N, Xiao G, Tang H, et al. Nonlinear optical microscopy: use of second harmonic generation and two-photon microscopy for automated quantitative liver fibrosis studies. J Biomed Opt. 2008;13:064010.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Xu S, Wang Y, Tai DCS, Wang S, Cheng CL, Peng Q, et al. qFibrosis: a fully-quantitative innovative method incorporating histological features to facilitate accurate fibrosis scoring in animal model and chronic hepatitis B patients. J Hepatol. 2014;61:260–9.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    • Goh GB, Leow WQ, Liang S, Wan WK, Lim TKH, Tan CK, et al. Quantification of hepatic steatosis in chronic liver disease using novel automated method of second harmonic generation and two-photon excited fluorescence. Sci Rep. 2019;9:2975 The original article describing the use of second harmonic generation microscopy for measurement of hepatic steatosis.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Pilichiewicz AN, Feltrin KL, Horowitz M, Holtmann G, Wishart JM, Jones KL, et al. Functional dyspepsia is associated with a greater symptomatic response to fat but not carbohydrate, increased fasting and postprandial CCK, and diminished PYY. Am J Gastroenterol. 2008;103:2613–23.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Gastroenterology and Hepatology Unit, Department of Medicine, Faculty of MedicineUniversity of MalayaKuala LumpurMalaysia

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