Z Gastroenterol 2022; 60(08): 1235-1248
DOI: 10.1055/a-1491-1771
Übersicht

Conventional ultrasound for diagnosis of hepatic steatosis is better than believed

Konventioneller Ultraschall in der Fettleber-Diagnostik ist besser als sein Ruf
1   Department Allgemeine Innere Medizin, Kliniken Hirslanden, Beau Site, Salem und Permanence, Bern, Switzerland,
,
Long Shi
2   Department of Ultrasound, Jingmen No. 2 People’s Hospital, Jingmen, Hubei, China,
,
Axel Löwe
1   Department Allgemeine Innere Medizin, Kliniken Hirslanden, Beau Site, Salem und Permanence, Bern, Switzerland,
,
Yi Dong
3   Ultrasound Department, Zhongshan Hospital Fudan University, Shanghai, China,
,
Andrej Potthoff
4   Gastroenterology and Hepatology and Endocrinology, Hannover Medical School, Hannover, Germany,
,
Zeno Sparchez
5   Department of Internal Medicine-Gastroenterology, University of Medicine and Pharmacy, Cluj-Napoca, Romania,
,
Andreas Teufel
6   Division of Hepatology, Department of Medicine II, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany,
,
Sabine Guth
7   Conradia Medical Prevention Hamburg, Hamburg, Deutschland,
,
Jonas Koch
1   Department Allgemeine Innere Medizin, Kliniken Hirslanden, Beau Site, Salem und Permanence, Bern, Switzerland,
,
Richard G Barr
8   Northeastern Ohio Medical University, Southwoods Imaging, Youngstown, OH, USA,
,
9   Department of Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China,
› Author Affiliations
Supported by: This research was supported by a grant from the National Natural Science Foundation of China (82071953) and the Health Commission of Hubei Province (WJ2019M077).

Abstract

Background Hepatic steatosis is a condition frequently encountered in clinical practice, with potential progression towards fibrosis, cirrhosis, and hepatocellular carcinoma. Detection and staging of hepatic steatosis are of most importance in nonalcoholic fatty liver disease (NAFLD), a disease with a high prevalence of more than 1 billion individuals affected. Ultrasound (US) is one of the most used noninvasive imaging techniques used in the diagnosis of hepatic steatosis. Detection of hepatic steatosis with US relies on several conventional US parameters, which will be described. US is the first-choice imaging in adults at risk for hepatic steatosis. The use of some scoring systems may add additional accuracy especially in assessing the severity of hepatic steatosis.

Summary In the presented paper, we discuss screening and risk stratification, ultrasound features for diagnosing hepatic steatosis, B-mode criteria, focal fatty patterns and Doppler features of the hepatic vessels, and the value of the different US signs for the diagnosis of liver steatosis including classifying the severity of steatosis using different US scores. Limitations of conventional B-mode and Doppler features in the evaluation of hepatic steatosis are also discussed, including those in grading and assessing the complications of steatosis, namely fibrosis and nonalcoholic steatohepatitis.

Key Messages Ultrasound is the first-line imaging examination for the screening and follow-up of patients with liver steatosis. The use of some scoring systems may add additional accuracy in assessing the severity of steatosis. Conventional B-mode and Doppler ultrasound have limitations in grading and assessing the complications of steatosis.

Zusammenfassung

Hintergrund die Fettleber ist eine in der klinischen Praxis häufige Erkrankung mit dem Risiko ein Leberfibrose, Leberzirrhose und auch ein hepatozelluläres Karzinom (HCC) zu entwickeln. Die nicht-alkoholische Fettlebererkrankung (NAFLD) ist eine Krankheit mit hoher Prävalenz und mit mehr als einer Milliarde betroffener Personen. Der Nachweis und die Stadieneinteilung sind von prognostischer Bedeutung.

Ultraschall (US) ist eine weitverbreitete nichtinvasive Bildgebungstechnik, die auch bei der Diagnose der Fettleber eingesetzt werden kann. Der Nachweis einer Fettleber beruht zunächst auf anamnestischen Angaben und konventionellen sonografischen Zeichen. Die Verwendung von Bewertungssystemen kann die diagnostische Genauigkeit erhöhen, insbesondere bei der Beurteilung des Schweregrads.

In dem vorgestellten Artikel diskutieren wir Screening und auch die Risikostratifizierung für die Entwicklung einer Steatohepatitis, Leberfibrose und eines HCC. Die Ultraschallmerkmale zur Diagnose und Differenzialdiagnose der Fettleber inklusive von B-Mode-Kriterien und Doppler-Charakteristika von Lebergefäßen werden erläutert. Die Klassifizierung des Schweregrads der Steatose wird anhand von US-Scores beschrieben und deren Einschränkungen diskutiert.

Kernbotschaft Ultraschall ist die erste bildgebende Untersuchungstechnik für das Screening und Follow-up von Patienten mit Fettleber. Die Verwendung von Bewertungssystemen kann die Diagnostik verbessern.



Publication History

Article published online:
25 June 2021

© 2021. Thieme. All rights reserved.

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  • References

  • 1 Santini F, Giannetti M, Mazzeo S, Fierabracci P. et al. Ultrasonographic evaluation of liver volume and the metabolic syndrome in obese women. J Endocrinol Invest 2007; 30: 104-110
  • 2 Schlottmann K, Baer A, Lock G. et al. The sonographic picture of an echogenic liver is an indicator of pathologic glucose tolerance]. Dtsch Med Wochenschr 2000; 125: 517-522
  • 3 Younossi ZM, Koenig 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
  • 4 Lazarus JV, Ekstedt M, Marchesini G. et al. A cross-sectional study of the public health response to non-alcoholic fatty liver disease in Europe. J Hepatol 2020; 72: 14-24
  • 5 Eslam M, Newsome PN, Sarin SK. et al. A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement. J Hepatol 2020; 73: 202-209
  • 6 Mak LY, Yuen MF, Seto WK. Letter regarding “A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement”. J Hepatol 2020; 73: 1573-1574
  • 7 Dulai PS, Singh S, Patel J. et al. Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: Systematic review and meta-analysis. Hepatology 2017; 65: 1557-1565
  • 8 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: 643-654
  • 9 European Association for Study of Liver, Asociacion Latinoamericana para el Estudio del Higado. EASL-ALEH Clinical Practice Guidelines: non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol 2015; 63: 237-264
  • 10 European Association for the Study of the Liver, European Association for the Study of Diabetes, European Association for the Study of Obesity. EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. Obes Facts 2016; 9: 65-9
  • 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: 328-357
  • 12 Rinella ME, Tacke F, Sanyal AJ. et al. Report on the AASLD/EASL Joint Workshop on Clinical Trial Endpoints in NAFLD. Hepatology 2019; 70: 1424-1436
  • 13 Bacon BR, Farahvash MJ, Janney CG, Neuschwander-Tetri BA. Nonalcoholic steatohepatitis: an expanded clinical entity. Gastroenterology 1994; 107: 1103-1109
  • 14 Mofrad P, Contos MJ, Haque M. et al. Clinical and histologic spectrum of nonalcoholic fatty liver disease associated with normal ALT values. Hepatology 2003; 37: 1286-1292
  • 15 Charatcharoenwitthaya P, Lindor KD, Angulo P. The spontaneous course of liver enzymes and its correlation in nonalcoholic fatty liver disease. Dig Dis Sci 2012; 57: 1925-1931
  • 16 Kautz A, Dorner R, Antoni C. et al. Self-testing for liver disease—response to an online liver test questionnaire. Scand J Gastroenterol 2020; 55: 67-73
  • 17 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: 1486-1501
  • 18 Petta S, Vanni E, Bugianesi E. 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: 1566-1573
  • 19 Petta S, Wong VW, Camma C. 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: 617-627
  • 20 Azzam H, Malnick S. Non-alcoholic fatty liver disease—the heart of the matter. World J Hepatol 2015; 7: 1369-1376
  • 21 Heimbach JK, Kulik LM, Finn RS. et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 2018; 67: 358-380
  • 22 Alberti KG, Eckel RH, Grundy SM. et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009; 120: 1640-1645
  • 23 Adams LA, Anstee QM, Tilg H, Targher G. Non-alcoholic fatty liver disease and its relationship with cardiovascular disease and other extrahepatic diseases. Gut 2017; 66: 1138-1153
  • 24 Lee SS, Park SH. Radiologic evaluation of nonalcoholic fatty liver disease. World J Gastroenterol 2014; 20: 7392-7402
  • 25 Hernaez R, Lazo M, Bonekamp S. et al. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis. Hepatology 2011; 54: 1082-1090
  • 26 Lupşor-Platon M, Stefănescu H, Mureșan D. et al. Noninvasive assessment of liver steatosis using ultrasound methods. Med Ultrason 2014; 16: 236-245
  • 27 Cho CS, Curran S, Schwartz LH. et al. Preoperative radiographic assessment of hepatic steatosis with histologic correlation. J Am Coll Surg 2008; 206: 480-488
  • 28 Uhrig M, Mueller J, Longerich T. et al. Susceptibility based multiparametric quantification of liver disease: non-invasive evaluation of steatosis and iron overload. Magn Reson Imaging 2019; 63: 114-122
  • 29 Schwenzer NF, Springer F, Schraml C. et al. Non-invasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol 2009; 51: 433-445
  • 30 Stern C, Castera L. Non-invasive diagnosis of hepatic steatosis. Hepatol Int 2017; 11: 70-78
  • 31 Castera L, Friedrich-Rust M, Loomba R. Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology 2019; 156: 1264-1281 e1264
  • 32 Pignoli P, Tremoli E, Poli A. et al. Intimal plus medial thickness of the arterial wall: a direct measurement with ultrasound imaging. Circulation 1986; 74: 1399-1406
  • 33 Bots ML, Hoes AW, Koudstaal PJ. et al. Common carotid intima-media thickness and risk of stroke and myocardial infarction: the Rotterdam Study. Circulation 1997; 96: 1432-1437
  • 34 Hong CW, Marsh A, Wolfson T. et al. Reader agreement and accuracy of ultrasound features for hepatic steatosis. Abdom Radiol (NY) 2019; 44: 54-64
  • 35 Décarie PO, Lepanto L, Billiard JS. et al. Fatty liver deposition and sparing: a pictorial review. Insights Imaging 2011; 2: 533-538
  • 36 Sienz M, Ignee A, Dietrich CF. Reference values in abdominal ultrasound—biliopancreatic system and spleen. Z Gastroenterol 2011; 49: 845-870
  • 37 Sienz M, Ignee A, Dietrich CF. Reference values in abdominal ultrasound—liver and liver vessels. Z Gastroenterol 2010; 48: 1141-1152
  • 38 Gerstenmaier JF, Gibson RN. Ultrasound in chronic liver disease. Insights Imaging 2014; 5: 441-455
  • 39 Davies RJ, Saverymuttu SH, Fallowfield M. et al. Paradoxical lack of ultrasound attenuation with gross fatty change in the liver. Clin Radiol 1991; 43: 393-396
  • 40 Jesper D, Klett D, Schellhaas B. et al. Ultrasound-based attenuation imaging for the non-invasive quantification of liver fat—a pilot study on feasibility and inter-observer variability. IEEE J Transl Eng Health Med 2020; 8: 1800409
  • 41 Lee JS, Semela D, Iredale J, Shah VJ. Sinusoidal remodeling and angiogenesis: a new function for the liver-specific pericyte?. Hepatology 2007; 45: 817-825
  • 42 Dasarathy S, Dasarathy J, Khiyami A. et al. Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol 2009; 51: 1061-1067
  • 43 Hirche TO, Ignee A, Hirche H. et al. Evaluation of hepatic steatosis by ultrasound in patients with chronic hepatitis C virus infection. Liver Int 2007; 27: 748-757
  • 44 Arai K, Matsui O, Takashima T. et al. Focal spared areas in fatty liver caused by regional decreased portal flow. AJR Am J Roentgenol 1988; 151: 300-302
  • 45 Dietrich CF, Wehrmann T, Zeuzem S. et al. Analysis of hepatic echo patterns in chronic hepatitis C. Ultraschall in Med 1999; 20: 9-14
  • 46 Dietrich CF, Lee JH, Gottschalk R. et al. Hepatic and portal vein flow pattern in correlation with intrahepatic fat deposition and liver histology in patients with chronic hepatitis C. AJR Am J Roentgenol 1998; 171: 437-443
  • 47 Marchal G, Tshibwabwa-Tumba E, Verbeken E. et al. “Skip areas” in hepatic steatosis: a sonographic-angiographic study. Gastrointest Radiol 1986; 11: 151-157
  • 48 Zezos P, Tatsi P, Nakos A. et al. Focal fatty liver sparing lesion presenting as a “pseudotumor:” case report. Acta Gastroenterol Belg 2006; 69: 323-326
  • 49 Valls C, Iannacconne R, Alba E. et al. Fat in the liver: diagnosis and characterization. Eur Radiol 2006; 16: 2292-2308
  • 50 Hashimoto M, Heianna J, Tate E. et al. Small veins entering the liver. Eur Radiol 2002; 12: 2000-2005
  • 51 Kratzer W, Akinli AS, Bommer M. et al. Prevalence and risk factors of focal sparing in hepatic steatosis. Ultraschall in Med 2010; 31: 37-42
  • 52 Strunk H, Mildenberger P, Jonas J. The incidence of focal liver lesions in patients with colorectal carcinoma. Rofo 1992; 156: 325-327
  • 53 Kester NL, Elmore SG. Focal hypoechoic regions in the liver at the porta hepatis: prevalence in ambulatory patients. J Ultrasound Med 1995; 14: 649-652
  • 54 Koseoglu K, Ozsunar Y, Taskin F, Karaman C. Pseudolesions of left liver lobe during helical CT examinations: prevalence and comparison between unenhanced and biphasic CT findings. Eur J Radiol 2005; 54: 388-392
  • 55 Karcaaltincaba M, Akhan O. Imaging of hepatic steatosis and fatty sparing. Eur J Radiol 2007; 61: 33-43
  • 56 Kyogoku S, Shiraishi A, Ozaki Y, Kurosaki Y. Focal sparing of segment 2 in fatty liver: US appearance. Radiat Med 2004; 22: 342-345
  • 57 Caturelli E, Costarelli L, Giordano M. et al. Hypoechoic lesions in fatty liver. Quantitative study by histomorphometry. Gastroenterology 1991; 100: 1678-1682
  • 58 Dietrich CF, Schall H, Kirchner J. et al. Sonographic detection of focal changes in the liver hilus in patients receiving corticosteroid therapy. Z Gastroenterol 1997; 35: 1051-1057
  • 59 Siegelman ES, Rosen MA. Imaging of hepatic steatosis. Semin Liver Dis 2001; 21: 71-80
  • 60 Bhatnagar G, Sidhu HS, Vardhanabhuti V. et al. The varied sonographic appearances of focal fatty liver disease: review and diagnostic algorithm. Clin Radiol 2012; 67: 372-379
  • 61 Basaran C, Karcaaltincaba M, Akata D. et al. Fat-containing lesions of the liver: cross-sectional imaging findings with emphasis on MRI. AJR Am J Roentgenol 2005; 184: 1103-1110
  • 62 Hamer OW, Aguirre DA, Casola G. et al. Fatty liver: imaging patterns and pitfalls. Radiographics 2006; 26: 1637-1653
  • 63 Farrant P, Meire HB. Hepatic vein pulsatility assessment on spectral Doppler ultrasound. Br J Radiol 1997; 70: 829-832
  • 64 O’Donohue J, Ng C, Catnach S. et al. Diagnostic value of Doppler assessment of the hepatic and portal vessels and ultrasound of the spleen in liver disease. Eur J Gastroenterol Hepatol 2004; 16: 147-155
  • 65 Colli A, Cocciolo M, Riva C. et al. Abnormalities of Doppler waveform of the hepatic veins in patients with chronic liver disease: correlation with histologic findings. AJR Am J Roentgenol 1994; 162: 833-837
  • 66 Arda K, Ofelli M, Calikoglu U. et al. Hepatic vein Doppler waveform changes in early stage (Child-Pugh A) chronic parenchymal liver disease. J Clin Ultrasound 1997; 25: 15-19
  • 67 Bolondi L, Li Bassi S, Gaiani S. et al. Liver cirrhosis: changes of Doppler waveform of hepatic veins. Radiology 1991; 178: 513-516
  • 68 Coulden RA, Britton PD, Farman P. et al. Preliminary report: hepatic vein Doppler in the early diagnosis of acute liver transplant rejection. Lancet 1990; 336: 273-275
  • 69 Jequier S, Jequier JC, Hanquinet S. et al. Orthotopic liver transplants in children: change in hepatic venous Doppler wave pattern as an indicator of acute rejection. Radiology 2003; 226: 105-112
  • 70 von Herbay A, Frieling T, Haussinger D. Association between duplex Doppler sonographic flow pattern in right hepatic vein and various liver diseases. J Clin Ultrasound 2001; 29: 25-30
  • 71 Karabulut N, Kazil S, Yagci B, Sabir N. Doppler waveform of the hepatic veins in an obese population. Eur Radiol 2004; 14: 2268-2272
  • 72 Oguzkurt L, Yildirim T, Torun D. et al. Hepatic vein Doppler waveform in patients with diffuse fatty infiltration of the liver. Eur J Radiol 2005; 54: 253-257
  • 73 Tana C, Schiavone C, Ticinesi A. et al. Hepatic artery resistive index as surrogate marker for fibrosis progression in NAFLD patients: a clinical perspective. Int J Immunopathol Pharmacol 2018; 32: 2058738418781373
  • 74 Tana C, Tana M, Rossi S. et al. Hepatic artery resistive index (HARI) and non-alcoholic fatty liver disease (NAFLD) fibrosis score in NAFLD patients: cut-off suggestive of non-alcoholic steatohepatitis (NASH) evolution. J Ultrasound 2016; 19: 183-189
  • 75 Bucci M, Tana C, Giamberardino MA, Cipollone F. Lp(a) and cardiovascular risk: investigating the hidden side of the moon. Nutr Metab Cardiovasc Dis 2016; 26: 980-986
  • 76 Dietrich CF, Mertens JC, Braden B. et al. Contrast-enhanced ultrasound of histologically proven liver hemangiomas. Hepatology 2007; 45: 1139-1145
  • 77 Guth S, Leise U, Bamberger CM, Windler E. Ultrasonographic hepatic steatosis as a surrogate for atherosclerosis. UIO 2016; 2: E27-E31
  • 78 Ferraioli G, Soares Monteiro LB. Ultrasound-based techniques for the diagnosis of liver steatosis. World J Gastroenterol 2019; 25: 6053-6062
  • 79 Saverymuttu SH, Joseph AE, Maxwell JD. Ultrasound scanning in the detection of hepatic fibrosis and steatosis. Br Med J (Clin Res Ed) 1986; 292: 13-15
  • 80 Saadeh S, Younossi ZM, Remer EM. et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology 2002; 123: 745-750
  • 81 Tominaga K, Kurata JH, Chen YK. et al. Prevalence of fatty liver in Japanese children and relationship to obesity. An epidemiological ultrasonographic survey. Dig Dis Sci 1995; 40: 2002-2009
  • 82 Henschke CI, Goldman H, Teele RL. The hyperechogenic liver in children: cause and sonographic appearance. AJR Am J Roentgenol 1982; 138: 841-846
  • 83 Chan DF, Li AM, Chu WC. et al. Hepatic steatosis in obese Chinese children. Int J Obes Relat Metab Disord 2004; 28: 1257-1263
  • 84 Arslan N, Buyukgebiz B, Ozturk Y, Cakmakci H. Fatty liver in obese children: prevalence and correlation with anthropometric measurements and hyperlipidemia. Turk J Pediatr 2005; 47: 23-27
  • 85 Palmentieri B, de I Sio, La Mura V. et al. The role of bright liver echo pattern on ultrasound B-mode examination in the diagnosis of liver steatosis. Dig Liver Dis 2006; 38: 485-489
  • 86 Lee SS, Park SH, Kim HJ. et al. Non-invasive assessment of hepatic steatosis: prospective comparison of the accuracy of imaging examinations. J Hepatol 2010; 52: 579-585
  • 87 Bril F, Ortiz-Lopez C, Lomonaco R. et al. Clinical value of liver ultrasound for the diagnosis of nonalcoholic fatty liver disease in overweight and obese patients. Liver Int 2015; 35: 2139-2146
  • 88 Hernaez R, Lazo M, Bonekamp S. et al. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis. Hepatology 2011; 54: 1082-1090
  • 89 Mottin CC, Moretto M, Padoin AV. et al. The role of ultrasound in the diagnosis of hepatic steatosis in morbidly obese patients. Obes Surg 2004; 14: 635-637
  • 90 Ferraioli G, Soares Monteiro LB. Ultrasound-based techniques for the diagnosis of liver steatosis. World J Gastroenterol 2019; 25: 6053-6062
  • 91 Hamaguchi M, Kojima T, Itoh Y. 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
  • 92 Zardi EM, De I Sio, Ghittoni G. et al. Which clinical and sonographic parameters may be useful to discriminate NASH from steatosis?. J Clin Gastroenterol 2011; 45: 59-63
  • 93 Webb M, Yeshua H, Zelber-Sagi S. et al. Diagnostic value of a computerized hepatorenal index for sonographic quantification of liver steatosis. AJR Am J Roentgenol 2009; 192: 909-914
  • 94 Tuma J, Novakova B, Schwarzenbach HR. et al. Image analysis in the differential diagnosis of renal parenchyma lesions. Ultraschall in Med 2011; 32: 286-292
  • 95 Marshall RH, Eissa M, Bluth EI. et al. Hepatorenal index as an accurate, simple, and effective tool in screening for steatosis. AJR Am J Roentgenol 2012; 199: 997-1002
  • 96 Shiralkar K, Johnson S, Bluth EI. et al. Improved method for calculating hepatic steatosis using the hepatorenal index. J Ultrasound Med 2015; 34: 1051-1059
  • 97 Khov N, Sharma A, Riley TR. Bedside ultrasound in the diagnosis of nonalcoholic fatty liver disease. World J Gastroenterol 2014; 20: 6821-6825
  • 98 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
  • 99 Perez NE, Siddiqui FA, Mutchnick MG. et al. Ultrasound diagnosis of fatty liver in patients with chronic liver disease: a retrospective observational study. J Clin Gastroenterol 2007; 41: 624-629
  • 100 Macaluso FS, Maida M, Cammà C. et al. Body mass index and liver stiffness affect accuracy of ultrasonography in detecting steatosis in patients with chronic hepatitis C virus genotype 1 infection. Clin Gastroenterol Hepatol 2014; 12: 878-884.e871
  • 101 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: W320-323
  • 102 Pirmoazen AM, Khurana A, El Kaffas A, Kamaya A. Quantitative ultrasound approaches for diagnosis and monitoring hepatic steatosis in nonalcoholic fatty liver disease. Theranostics 2020; 10: 4277-4289
  • 103 Borges VF, Diniz AL, Cotrim HP. et al. Sonographic hepatorenal ratio: a noninvasive method to diagnose nonalcoholic steatosis. J Clin Ultrasound 2013; 41: 18-25
  • 104 Chauhan A, Sultan LR, Furth EE. et al. Diagnostic accuracy of hepatorenal index in the detection and grading of hepatic steatosis. J Clin Ultrasound 2016; 44: 580-586
  • 105 Xia MF, Yan HM, He WY. et al. Standardized ultrasound hepatic/renal ratio and hepatic attenuation rate to quantify liver fat content: an improvement method. Obesity (Silver Spring) 2012; 20: 444-452
  • 106 Wang YS, Zhang GP, Yang X. et al. Assessment of hepatic fat content in using quantitative ultrasound measurement of hepatic/renal ratio and hepatic echo-intensity attenuation rate. Med Ultrason 2020; 22: 393-401
  • 107 Zhang B, Ding F, Chen T. et al. Ultrasound hepatic/renal ratio and hepatic attenuation rate for quantifying liver fat content. World J Gastroenterol 2014; 20: 17985-17992
  • 108 Bae JS, Lee DH, Lee JY. et al. Assessment of hepatic steatosis by using attenuation imaging: a quantitative, easy-to-perform ultrasound technique. Eur Radiol 2019; 29: 6499-6507
  • 109 Fujiwara Y, Kuroda H, Abe T. et al. The B-mode image-guided ultrasound attenuation parameter accurately detects hepatic steatosis in chronic liver disease. Ultrasound Med Biol 2018; 44: 2223-2232
  • 110 Sugimoto K, Moriyasu F, Oshiro H. et al. The role of multiparametric us of the liver for the evaluation of nonalcoholic steatohepatitis. Radiology 2020; 192665
  • 111 Lee DH, Cho EJ, Bae JS. et al. Accuracy of 2-dimensional shear wave elastography and attenuation imaging for evaluation of patients with nonalcoholic steatohepatitis. Clin Gastroenterol Hepatol 2020;
  • 112 Lizardi-Cervera JA-ZD. Nonalcoholic fatty liver disease and its association with cardiovascular disease. Ann Hepatol 2009; 8 (Suppl. 01) S40-S43
  • 113 Ramilli SPS, Muscari A, Pacelli B, Arienti V. Carotid lesions in outpatients with non-alcoholic fatty liver disease. World J Gastroenterol 2009; 15: 4770-4774
  • 114 Targher G, Arcaro G. Non-alcoholic fatty liver disease and increased risk of cardiovascular disease. Atherosclerosis 2007; 191: 235-240
  • 115 Targher G, Bertolini L, Padovani R. et al. Non-alcoholic fatty liver disease is associated with carotid artery wall thickness in diet-controlled type 2 diabetic patients. J Endocrinol Invest 2006; 29: 55-60
  • 116 Choi SY KD, Kang JH, Park MJ. et al. Nonalcoholic fatty liver disease as a risk factor of cardiovascular disease: relation of nonalcoholic fatty liver disease to carotid arteriosclerosis. Korean J Hepatol 2008; 14: 77-88
  • 117 Targher G DC, Bonora E. Risk of cardiovascular disease in patients with non-alcoholic fatty liver disease. N Engl J Med 2010; 363: 1341-1350
  • 118 Lin YC, Lo HM, Chen JD. Sonographic fatty liver, overweight and ischemic heart disease. World J Gastroenterol 2005; 11: 4838-4842
  • 119 Puig J, Blasco G, Daunis IEJ. et al. Nonalcoholic fatty liver disease and age are strong indicators for atherosclerosis in morbid obesity. Clin Endocrinol (Oxf) 2015; 83: 180-186
  • 120 Baumeister SE, Volzke H, Marschall P. et al. Impact of fatty liver disease on health care utilization and costs in a general population: a 5-year observation. Gastroenterology 2008; 134: 85-94
  • 121 Haring R, Wallaschofski H, Nauck M. et al. Ultrasonographic hepatic steatosis increases prediction of mortality risk from elevated serum gamma-glutamyl transpeptidase levels. Hepatology 2009; 50: 1403-1411
  • 122 Jenssen C, Pietsch C, Gottschalk U. et al. Abdominal ultrasonography in patients with diabetes mellitus. Part 1: Liver. Z Gastroenterol 2015; 53: 306-319
  • 123 Ferraioli G, Maiocchi L, Raciti MV. et al. Detection of liver steatosis with a novel ultrasound-based technique: a pilot study using MRI-Derived proton density fat fraction as the gold standard. Clin Transl Gastroenterol 2019; 10: e00081
  • 124 Tamaki N, Koizumi Y, Hirooka M. et al. Novel quantitative assessment system of liver steatosis using a newly developed attenuation measurement method. Hepatol Res 2018; 48: 821-828
  • 125 Lin SC, Heba E, Wolfson T. 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
  • 126 Caussy C, Alquiraish MH, Nguyen P. 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
  • 127 Sasso M, Tengher-Barna I, Ziol M. et al. Novel controlled attenuation parameter for noninvasive assessment of steatosis using Fibroscan: validation in chronic hepatitis C. J Viral Hepat 2012; 19: 244-253
  • 128 Ferraioli G, Tinelli C, Lissandrin R. et al. Controlled attenuation parameter for evaluating liver steatosis in chronic viral hepatitis. World J Gastroenterol 2014; 20: 6626-6631
  • 129 de Ledinghen V, Vergniol J, Foucher J. et al. Non-invasive diagnosis of liver steatosis using controlled attenuation parameter (CAP) and transient elastography. Liver Int 2012; 32: 911-918
  • 130 Lupsor-Platon M, Feier D, Stefanescu H. 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
  • 131 Shen F, Zheng RD, Shi JP. et al. Impact of skin capsular distance on the performance of controlled attenuation parameter in patients with chronic liver disease. Liver Int 2015; 35: 2392-2400
  • 132 Karlas T, Petroff D, Sasso M. et al. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol 2017; 66: 1022-1030
  • 133 Eddowes PJ, Sasso M, Allison M. 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: 1717-1730
  • 134 Dioguardi Burgio M, Imbault M. et al. Ultrasonic adaptive sound speed estimation for the diagnosis and quantification of hepatic steatosis: a pilot study. Ultraschall in Med 2019; 40: 722-733
  • 135 Tada T, Kumada T, Toyoda H. et al. Utility of attenuation coefficient measurement using an ultrasound-guided attenuation parameter for evaluation of hepatic steatosis: comparison with mri-determined proton density fat fraction. AJR Am J Roentgenol 2019; 212: 332-341