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European Radiology

, Volume 29, Issue 12, pp 6499–6507 | Cite as

Assessment of hepatic steatosis by using attenuation imaging: a quantitative, easy-to-perform ultrasound technique

  • Jae Seok Bae
  • Dong Ho LeeEmail author
  • Jae Young Lee
  • Haeryoung Kim
  • Su Jong Yu
  • Jeong-Hoon Lee
  • Eun Ju Cho
  • Yun Bin Lee
  • Joon Koo Han
  • Byung Ihn Choi
Hepatobiliary-Pancreas

Abstract

Objectives

To evaluate the diagnostic performance of attenuation imaging (ATI) in the detection of hepatic steatosis compared with a histopathology gold standard.

Methods

We prospectively enrolled 108 consecutive patients (35 males; median age, 54.0 years) who underwent percutaneous liver biopsy for evaluation of diffuse liver disease between January 2018 and November 2018 in a tertiary academic center. Grayscale ultrasound examination with ATI was performed just before biopsy, and an attenuation coefficient (AC) was obtained from each patient. The degree of hepatic steatosis, fibrosis stage, and necroinflammatory activity were assessed on histopathologic examination. The significant factor associated with the AC was found by a linear regression analysis, and the diagnostic performance of the AC for the classification into each hepatic steatosis stage was evaluated by receiver operating characteristic (ROC) analysis.

Results

The distribution of hepatic steatosis grade on histopathology was 53/11/22/16/6 for none/mild (< 10%)/mild (≥ 10%)/moderate/severe steatosis, respectively. The area under the ROC curve, sensitivity, specificity, and optimal cutoff AC value for detection of hepatic steatosis ranged from 0.843–0.926, 74.5–100.0%, 77.4–82.8%, and 0.635–0.745, respectively. Multivariate analysis revealed that the degree of steatosis was the only significant determinant factor for the AC.

Conclusions

The AC from ATI provided good diagnostic performance in detecting the varying degrees of hepatic steatosis. The degree of steatosis was the only significant factor affecting the AC, whereas fibrosis and inflammation were not.

Key Points

• Attenuation imaging (ATI) is based on two-dimensional grayscale ultrasound images that can incorporate into routine ultrasound examinations with less than 2 min of acquisition time.

• ATI provided good diagnostic performance in detecting the varying degrees of hepatic steatosis with an area under the ROC curves ranging from 0.843 to 0.926, and there was no technical failure in this study indicating high applicability of this technique.

• The degree of hepatic steatosis was the only significant factor affecting the result of ATI examination.

Keywords

Fatty liver Ultrasonography Biopsy Sensitivity and specificity Linear models 

Abbreviations

AC

Attenuation coefficient

ATI

Attenuation imaging

AUC

Area under the receiver operating characteristic curve

BMI

Body mass index

CAP

Controlled attenuation parameter

MR

Magnetic resonance

NAFLD

Nonalcoholic fatty liver disease

NASH

Nonalcoholic steatohepatitis

ROI

Region of interest

SCD

Skin-capsular distance

SD

Standard deviation

TE

Transient elastography

US

Ultrasound

Notes

Acknowledgments

The attenuation imaging method was provided by Canon Medical Systems, and this study was technically supported by Canon Medical Systems.

Funding

The authors state that this work has not received any funding.

Compliance with ethical standards

Guarantor

The scientific guarantor of this publication is Byung Ihn Choi.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

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

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• Prospective

• Diagnostic or prognostic study

• Performed at one institution

Supplementary material

330_2019_6272_MOESM1_ESM.docx (19 kb)
ESM 1 (DOCX 18 kb)

References

  1. 1.
    Browning JD, Szczepaniak LS, Dobbins R et al (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40:1387–1395CrossRefGoogle Scholar
  2. 2.
    Farrell GC (2005) Fatty liver disease: NASH and related disorders. Blackwell Pub., MaldenGoogle Scholar
  3. 3.
    Argo CK, Caldwell SH (2009) Epidemiology and natural history of non-alcoholic steatohepatitis. Clin Liver Dis 13:511–531CrossRefGoogle Scholar
  4. 4.
    Starley BQ, Calcagno CJ, Harrison SA (2010) Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology 51:1820–1832CrossRefGoogle Scholar
  5. 5.
    Noureddin M, Vipani A, Bresee C et al (2018) NASH leading cause of liver transplant in women: updated analysis of indications for liver transplant and ethnic and gender variances. Am J Gastroenterol 113:1649–1659CrossRefGoogle Scholar
  6. 6.
    Mellinger JL, Pencina KM, Massaro JM et al (2015) Hepatic steatosis and cardiovascular disease outcomes: an analysis of the Framingham heart study. J Hepatol 63:470–476CrossRefGoogle Scholar
  7. 7.
    Belfort R, Harrison SA, Brown K et al (2006) A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis. N Engl J Med 355:2297–2307CrossRefGoogle Scholar
  8. 8.
    Brouha SS, Nguyen P, Bettencourt R, Sirlin CB, Loomba R (2018) Increased severity of liver fat content and liver fibrosis in non-alcoholic fatty liver disease correlate with epicardial fat volume in type 2 diabetes: a prospective study. Eur Radiol 28:1345–1355CrossRefGoogle Scholar
  9. 9.
    Bos D, Leening MJG (2018) Leveraging the coronary calcium scan beyond the coronary calcium score. Eur Radiol 28:3082–3087CrossRefGoogle Scholar
  10. 10.
    Bravo AA, Sheth SG, Chopra S (2001) Liver biopsy. N Engl J Med 344:495–500CrossRefGoogle Scholar
  11. 11.
    Ratziu V, Charlotte F, Heurtier A et al (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 128:1898–1906CrossRefGoogle Scholar
  12. 12.
    Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD, American Association for the Study of Liver D (2009) Liver biopsy. Hepatology 49:1017–1044CrossRefGoogle Scholar
  13. 13.
    Noureddin M, Lam J, Peterson MR et al (2013) Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials. Hepatology 58:1930–1940CrossRefGoogle Scholar
  14. 14.
    Lee DH (2017) Imaging evaluation of non-alcoholic fatty liver disease: focused on quantification. Clin Mol Hepatol 23:290–301CrossRefGoogle Scholar
  15. 15.
    Joseph AE, Dewbury KC, McGuire PG (1979) Ultrasound in the detection of chronic liver disease (the “bright liver”). Br J Radiol 52:184–188CrossRefGoogle Scholar
  16. 16.
    Dasarathy S, Dasarathy J, Khiyami A, Joseph R, Lopez R, McCullough AJ (2009) Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol 51:1061–1067CrossRefGoogle Scholar
  17. 17.
    Strauss S, Gavish E, Gottlieb P, Katsnelson L (2007) Interobserver and intraobserver variability in the sonographic assessment of fatty liver. AJR Am J Roentgenol 189:W320–W323CrossRefGoogle Scholar
  18. 18.
    Taylor KJ, Riely CA, Hammers L et al (1986) Quantitative US attenuation in normal liver and in patients with diffuse liver disease: importance of fat. Radiology 160:65–71CrossRefGoogle Scholar
  19. 19.
    Kleiner DE, Brunt EM, Van Natta M et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313–1321CrossRefGoogle Scholar
  20. 20.
    Sharma A, Ashworth A, Behnke M, Cotterell A, Posner M, Fisher RA (2013) Donor selection for adult-to-adult living donor liver transplantation: well begun is half done. Transplantation 95:501–506CrossRefGoogle Scholar
  21. 21.
    Bedossa P, Poynard T (1996) An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology 24:289–29326CrossRefGoogle Scholar
  22. 22.
    Park YN, Chon CY, Park JB et al (1999) Histological grading and staging of chronic hepatitis standardized guideline proposed by the Korean Study Group for the Pathology of Digestive Diseases. Korean J Pathol 33:337–346Google Scholar
  23. 23.
    Deurenberg P, Deurenberg-Yap M, Guricci S (2002) Asians are different from Caucasians and from each other in their body mass index/body fat per cent relationship. Obes Rev 3:141–146CrossRefGoogle Scholar
  24. 24.
    Castera L, Vergniol J, Foucher J et al (2005) Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 128:343–350CrossRefGoogle Scholar
  25. 25.
    Karlas T, Petroff D, Sasso M et al (2017) Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol 66:1022–1030CrossRefGoogle Scholar
  26. 26.
    Rinella ME, Alonso E, Rao S et al (2001) Body mass index as a predictor of hepatic steatosis in living liver donors. Liver Transpl 7:409–414CrossRefGoogle Scholar
  27. 27.
    de Ledinghen V, Vergniol J, Capdepont M et al (2014) Controlled attenuation parameter (CAP) for the diagnosis of steatosis: a prospective study of 5323 examinations. J Hepatol 60:1026–1031CrossRefGoogle Scholar
  28. 28.
    Sasso M, Tengher-Barna I, Ziol M et al (2012) Novel controlled attenuation parameter for noninvasive assessment of steatosis using Fibroscan((R)): validation in chronic hepatitis C. J Viral Hepat 19:244–253CrossRefGoogle Scholar
  29. 29.
    Lin T, Ophir J, Potter G (1988) Correlation of ultrasonic attenuation with pathologic fat and fibrosis in liver disease. Ultrasound Med Biol 14:729–734CrossRefGoogle Scholar
  30. 30.
    Chon YE, Jung KS, Kim SU et al (2014) 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 34:102–109CrossRefGoogle Scholar
  31. 31.
    Chan WK, Nik Mustapha NR, Mahadeva S (2014) Controlled attenuation parameter for the detection and quantification of hepatic steatosis in nonalcoholic fatty liver disease. J Gastroenterol Hepatol 29:1470–1476CrossRefGoogle Scholar
  32. 32.
    Han A, Zhang YN, Boehringer AS et al (2019) Inter-platform reproducibility of ultrasonic attenuation and backscatter coefficients in assessing NAFLD. Eur Radiol.  https://doi.org/10.1007/s00330-019-06035-9

Copyright information

© European Society of Radiology 2019

Authors and Affiliations

  1. 1.Department of RadiologySeoul National University HospitalSeoulRepublic of Korea
  2. 2.Department of RadiologySeoul National University College of MedicineSeoulRepublic of Korea
  3. 3.Institute of Radiation MedicineSeoul National University Medical Research CenterSeoulRepublic of Korea
  4. 4.Department of PathologySeoul National University HospitalSeoulRepublic of Korea
  5. 5.Department of Internal MedicineSeoul National University HospitalSeoulRepublic of Korea
  6. 6.Department of RadiologyChung-Ang University HospitalSeoulRepublic of Korea

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