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Quantitative Ultrasound Radiofrequency Data Analysis for the Assessment of Hepatic Steatosis in Nonalcoholic Fatty Liver Disease Using Magnetic Resonance Imaging Proton Density Fat Fraction as the Reference Standard

  • Sun Kyung Jeon (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Jeong Min Lee (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Ijin Joo (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Sae-Jin Park (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine)
  • Received : 2020.10.20
  • Accepted : 2020.11.16
  • Published : 2021.07.01

Abstract

Objective: To investigate the diagnostic performance of quantitative ultrasound (US) parameters for the assessment of hepatic steatosis in patients with nonalcoholic fatty liver disease (NAFLD) using magnetic resonance imaging proton density fat fraction (MRI-PDFF) as the reference standard. Materials and Methods: In this single-center prospective study, 120 patients with clinically suspected NAFLD were enrolled between March 2019 and January 2020. The participants underwent US examination for radiofrequency (RF) data acquisition and chemical shift-encoded liver MRI for PDFF measurement. Using the RF data analysis, the attenuation coefficient (AC) based on tissue attenuation imaging (TAI) (AC-TAI) and scatter-distribution coefficient (SC) based on tissue scatter-distribution imaging (TSI) (SC-TSI) were measured. The correlations between the quantitative US parameters (AC and SC) and MRI-PDFF were evaluated using Pearson correlation coefficients. The diagnostic performance of AC-TAI and SC-TSI for detecting hepatic fat contents of ≥ 5% (MRI-PDFF ≥ 5%) and ≥ 10% (MRI-PDFF ≥ 10%) were assessed using receiver operating characteristic (ROC) analysis. The significant clinical or imaging factors associated with AC and SC were analyzed using linear regression analysis. Results: The participants were classified based on MRI-PDFF: < 5% (n = 38), 5-10% (n = 23), and ≥ 10% (n = 59). AC-TAI and SC-TSI were significantly correlated with MRI-PDFF (r = 0.659 and 0.727, p < 0.001 for both). For detecting hepatic fat contents of ≥ 5% and ≥ 10%, the areas under the ROC curves of AC-TAI were 0.861 (95% confidence interval [CI]: 0.786-0.918) and 0.835 (95% CI: 0.757-0.897), and those of SC-TSI were 0.964 (95% CI: 0.913-0.989) and 0.935 (95% CI: 0.875-0.972), respectively. Multivariable linear regression analysis showed that MRI-PDFF was an independent determinant of AC-TAI and SC-TSI. Conclusion: AC-TAI and SC-TSI derived from quantitative US RF data analysis yielded a good correlation with MRI-PDFF and provided good performance for detecting hepatic steatosis and assessing its severity in NAFLD.

Keywords

Acknowledgement

This study was supported by a research grant from Samsung Medison Co., Ltd (06-2018-4010) and a grant from the SNUH research fund (03-2018-02-30).

References

  1. Castera L, Friedrich-Rust M, Loomba R. Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology 2019;156:1264-1281.e4 
  2. Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 2011;34:274-285 
  3. Friedman SL, Neuschwander-Tetri BA, Rinella M, Sanyal AJ. Mechanisms of NAFLD development and therapeutic strategies. Nat Med 2018;24:908-922 
  4. Pais R, Barritt AS 4th, Calmus Y, Scatton O, Runge T, Lebray P, et al. NAFLD and liver transplantation: current burden and expected challenges. J Hepatol 2016;65:1245-1257 
  5. Machado MV, Cortez-Pinto H. Non-invasive diagnosis of non-alcoholic fatty liver disease. A critical appraisal. J Hepatol 2013;58:1007-1019 
  6. Reeder SB, Cruite I, Hamilton G, Sirlin CB. Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging 2011;34:729-749 
  7. Tang A, Desai A, Hamilton G, Wolfson T, Gamst A, Lam J, et al. Accuracy of MR imaging-estimated proton density fat fraction for classification of dichotomized histologic steatosis grades in nonalcoholic fatty liver disease. Radiology 2015;274:416-425 
  8. 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;286:486-498 
  9. Kramer H, Pickhardt PJ, Kliewer MA, Hernando D, Chen GH, Zagzebski JA, et al. Accuracy of liver fat quantification with advanced CT, MRI, and ultrasound techniques: prospective comparison with MR spectroscopy. AJR Am J Roentgenol 2017;208:92-100 
  10. Zhou Z, Zhang Q, Wu W, Lin YH, Tai DI, Tseng JH, et al. Hepatic steatosis assessment using ultrasound homodyned-K parametric imaging: the effects of estimators. Quant Imaging Med Surg 2019;9:1932-1947 
  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;51:1061-1067 
  12. 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.e6 
  13. Paige JS, Bernstein GS, Heba E, Costa EAC, Fereirra M, Wolfson T, et al. A pilot comparative study of quantitative ultrasound, conventional ultrasound, and MRI for predicting histology-determined steatosis grade in adult nonalcoholic fatty liver disease. AJR Am J Roentgenol 2017;208:W168-W177 
  14. Yang KC, Liao YY, Tsui PH, Yeh CK. Ultrasound imaging in nonalcoholic liver disease: current applications and future developments. Quant Imaging Med Surg 2019;9:546-551 
  15. Jeon SK, Joo I, Kim SY, Jang JK, Park J, Park HS, et al. Quantitative ultrasound radiofrequency data analysis for the assessment of hepatic steatosis using the controlled attenuation parameter as a reference standard. Ultrasonography 2021;40:136-146 
  16. 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;102:2708-2715 
  17. Reeder SB, Robson PM, Yu H, Shimakawa A, Hines CD, McKenzie CA, et al. Quantification of hepatic steatosis with MRI: the effects of accurate fat spectral modeling. J Magn Reson Imaging 2009;29:1332-1339 
  18. Hamilton G, Yokoo T, Bydder M, Cruite I, Schroeder ME, Sirlin CB, et al. In vivo characterization of the liver fat 1H MR spectrum. NMR Biomed 2011;24:784-790 
  19. Tang A, Tan J, Sun M, Hamilton G, Bydder M, Wolfson T, et al. Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology 2013;267:422-431 
  20. Han A, Zhang YN, Boehringer AS, Montes V, Andre MP, Erdman JW Jr, et al. Assessment of hepatic steatosis in nonalcoholic fatty liver disease by using quantitative US. Radiology 2020;295:106-113 
  21. 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;67:1348-1359 
  22. Lee DH, Lee JM, Yi NJ, Lee KW, Suh KS, Lee JH, et al. Hepatic stiffness measurement by using MR elastography: prognostic values after hepatic resection for hepatocellular carcinoma. Eur Radiol 2017;27:1713-1721 
  23. Yoon JH, Lee JM, Woo HS, Yu MH, Joo I, Lee ES, et al. Staging of hepatic fibrosis: comparison of magnetic resonance elastography and shear wave elastography in the same individuals. Korean J Radiol 2013;14:202-212 
  24. Singh S, Venkatesh SK, Loomba R, Wang Z, Sirlin C, Chen J, 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;26:1431-1440 
  25. Youden WJ. Index for rating diagnostic tests. Cancer 1950;3:32-35 
  26. Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 2016;15:155-163 
  27. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986;1:307-310 
  28. Kim H, Varghese T. Attenuation estimation using spectral cross-correlation. IEEE Trans Ultrason Ferroelectr Freq Control 2007;54:510-519 
  29. Wan YL, Tai DI, Ma HY, Chiang BH, Chen CK, Tsui PH. Effects of fatty infiltration in human livers on the backscattered statistics of ultrasound imaging. Proc Inst Mech Eng H 2015;229:419-428 
  30. 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;29:3564-3573 
  31. Tsui PH, Ho MC, Tai DI, Lin YH, Wang CY, Ma HY. Acoustic structure quantification by using ultrasound Nakagami imaging for assessing liver fibrosis. Sci Rep 2016;6:33075 
  32. Yamada H, Ebara M, Yamaguchi T, Okabe S, Fukuda H, Yoshikawa M, et al. A pilot approach for quantitative assessment of liver fibrosis using ultrasound: preliminary results in 79 cases. J Hepatol 2006;44:68-75 
  33. Jeon SK, Lee JM, Joo I, Yoon JH, Lee DH, Lee JY, et al. Prospective evaluation of hepatic steatosis using ultrasound attenuation imaging in patients with chronic liver disease with magnetic resonance imaging proton density fat fraction as the reference standard. Ultrasound Med Biol 2019;45:1407-1416 
  34. Tada T, Kumada T, Toyoda H, Yasuda S, Sone Y, Hashinokuchi S, et al. Liver stiffness does not affect ultrasound-guided attenuation coefficient measurement in the evaluation of hepatic steatosis. Hepatol Res 2020;50:190-198 
  35. Lin T, Ophir J, Potter G. Correlation of ultrasonic attenuation with pathologic fat and fibrosis in liver disease. Ultrasound Med Biol 1988;14:729-734