Abstract
Non-invasive diagnosis and quantification of hepatic steatosis rely on two different but complementary approaches: biomarkers or imaging techniques, either ultrasound-based such as liver ultrasonography and controlled attenuation parameter (CAP), or computed tomography (CT) and magnetic resonance imaging (MRI). Scores for the detection of steatosis have not gained much popularity in clinical practice so far. CAP, using the M probe, is the most promising technique but needs to be implemented with the XL probe and compared to ultrasound that, despite its limitations, remains the most widely used method. CT, owing to its low sensitivity and the fact that it involves a potential radiation hazard, is inappropriate. Finally, proton density fat fraction measurement by MRI is currently the most accurate and sensitive imaging method, simpler and more practical than magnetic resonance spectroscopy, but restricted, up to now, just to research and clinical trials.
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European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD), European Association for the Study of Obesity (EASO). EASL-EASD-EASO clinical practice guidelines for the management of non-alcoholic fatty liver disease. J Hepatol 2016;64:1388–1402
Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, et al. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Am J Gastroenterol 2012;107:811–826
Satapathy SK, Sanyal AJ. Epidemiology and natural history of nonalcoholic fatty liver disease. Semin Liver Dis 2015;35:221–235
Bedossa P, Patel K. Biopsy and noninvasive methods to assess progression of nonalcoholic fatty liver disease. Gastroenterology. 2016. doi:10.1053/j.gastro.2016.03.008 (Epub ahead of print)
Bedossa P, Moucari R, Chelbi E, Asselah T, Paradis V, Vidaud M, Cazals-Hatem D, et al. Evidence for a role of nonalcoholic steatohepatitis in hepatitis C: a prospective study. Hepatology 2007;46:380–387
Singh S, Allen AM, Wang Z, Prokop LJ, Murad MH, Loomba R. 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 (e641–649; quiz e639–640)
Nalbantoglu IL, Brunt EM. Role of liver biopsy in nonalcoholic fatty liver disease. World J Gastroenterol 2014;20:9026–9037
Ratziu V, Charlotte F, Heurtier A, Gombert S, Giral P, Bruckert E, Grimaldi A, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 2005;128:1898–1906
Goldstein NS, Hastah F, Galan MV, Gordon SC. Fibrosis heterogeneity in nonalcoholic steatohepatitis and hepatitis C virus needle core biopsy specimens. Am J Clin Pathol 2005;123:382–387
Vuppalanchi R, Unalp A, Van Natta ML, Cummings OW, Sandrasegaran KE, Hameed T, Tonascia J, et al. Effects of liver biopsy sample length and number of readings on sampling variability in nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2009;7:481–486
European Association for the Study of the 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
Poynard T, Ratziu V, Naveau S, Thabut D, Charlotte F, Messous D, Capron D, et al. The diagnostic value of biomarkers (SteatoTest) for the prediction of liver steatosis. Comp Hepatol 2005;4:10
Poynard T, Lassailly G, Diaz E, Clement K, Caiazzo R, Tordjman J, Munteanu M, et al. Performance of biomarkers FibroTest, ActiTest, SteatoTest, and NashTest in patients with severe obesity: meta analysis of individual patient data. PLoS ONE 2012;7:e30325
Bedogni G, Bellentani S, Miglioli L, Masutti F, Passalacqua M, Castiglione A, Tiribelli C. The fatty liver index: a simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol 2006;6:33
Calori G, Lattuada G, Ragogna F, Garancini MP, Crosignani P, Villa M, Bosi E, et al. Fatty liver index and mortality: the Cremona study in the 15th year of follow-up. Hepatology 2011;54:145–152
Lee JH, Kim D, Kim HJ, Lee CH, Yang JI, Kim W, Kim YJ, et al. Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig Liver Dis 2010;42:503–508
Bedogni G, Kahn HS, Bellentani S, Tiribelli C. A simple index of lipid overaccumulation is a good marker of liver steatosis. BMC Gastroenterol 2010;10:98
Cuthbertson DJ, Weickert MO, Lythgoe D, Sprung VS, Dobson R, Shoajee-Moradie F, Umpleby M, et al. External validation of the fatty liver index and lipid accumulation product indices, using 1H-magnetic resonance spectroscopy, to identify hepatic steatosis in healthy controls and obese, insulin-resistant individuals. Eur J Endocrinol 2014;171:561–569
Otgonsuren M, Estep MJ, Hossain N, Younossi E, Frost S, Henry L, Hunt S, et al. Single non-invasive model to diagnose non-alcoholic fatty liver disease (NAFLD) and non-alcoholic steatohepatitis (NASH). J Gastroenterol Hepatol 2014;29:2006–2013
Kotronen A, Peltonen M, Hakkarainen A, Sevastianova K, Bergholm R, Johansson LM, Lundbom N, et al. Prediction of non-alcoholic fatty liver disease and liver fat using metabolic and genetic factors. Gastroenterology 2009;137:865–872
Fedchuk L, Nascimbeni F, Pais R, Charlotte F, Housset C, Ratziu V, Group LS. Performance and limitations of steatosis biomarkers in patients with nonalcoholic fatty liver disease. Aliment Pharmacol Ther 2014;40:1209–1222
Castera L, Vilgrain V, Angulo P. Noninvasive evaluation of NAFLD. Nat Rev Gastroenterol Hepatol 2013;10:666–675
Hernaez R, Lazo M, Bonekamp S, Kamel I, Brancati FL, Guallar E, Clark JM. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis. Hepatology 2011;54:1082–1090
Webb M, Yeshua H, Zelber-Sagi S, Santo E, Brazowski E, Halpern Z, Oren R. Diagnostic value of a computerized hepatorenal index for sonographic quantification of liver steatosis. AJR Am J Roentgenol 2009;192:909–914
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;199:997–1002
Borges VF, Diniz AL, Cotrim HP, Rocha HL, Andrade NB. Sonographic hepatorenal ratio: a noninvasive method to diagnose nonalcoholic steatosis. J Clin Ultrasound 2013;41:18–25
Shiralkar K, Johnson S, Bluth EI, Marshall RH, Dornelles A, Gulotta PM. Improved method for calculating hepatic steatosis using the hepatorenal index. J Ultrasound Med 2015;34:1051–1059
Sasso M, Beaugrand M, de Ledinghen V, Douvin C, Marcellin P, Poupon R, Sandrin L, 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;36:1825–1835
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;32:911–918
Friedrich-Rust M, Romen D, Vermehren J, Kriener S, Sadet D, Herrmann E, Zeuzem S, 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:e325–e331
Myers RP, Pollett A, Kirsch R, Pomier-Layrargues G, Beaton M, Levstik M, Duarte-Rojo A, et al. Controlled Attenuation Parameter (CAP): a noninvasive method for the detection of hepatic steatosis based on transient elastography. Liver Int 2012;32:902–910
Sasso M, Tengher-Barna I, Ziol M, Miette V, Fournier C, Sandrin L, Poupon R, et al. Novel controlled attenuation parameter for noninvasive assessment of steatosis using Fibroscan((R)): validation in chronic hepatitis C. J Viral Hepat 2012;19:244–253
Kumar M, Rastogi A, Singh T, Behari C, Gupta E, Garg H, Kumar R, et al. Controlled attenuation parameter for non-invasive assessment of hepatic steatosis: does etiology affect performance? J Gastroenterol Hepatol 2013;28:1194–1201
Masaki K, Takaki S, Hyogo H, Kobayashi T, Fukuhara T, Naeshiro N, Honda Y, et al. Utility of controlled attenuation parameter measurement for assessing liver steatosis in Japanese patients with chronic liver diseases. Hepatol Res 2013;43:1182–1189
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:e111–e117
de Ledinghen V, Vergniol J, Capdepont M, Chermak F, Hiriart JB, Cassinotto C, Merrouche W, et al. Controlled attenuation parameter (CAP) for the diagnosis of steatosis: a prospective study of 5323 examinations. J Hepatol 2014;60:1026–1031
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;29:1470–1476
Chon YE, Jung KS, Kim SU, Park JY, Park YN, Kim do Y, Ahn SH, 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;34:102–109
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;20:10585–10590
Karlas T, Petroff D, Garnov N, Bohm S, Tenckhoff H, Wittekind C, Wiese M, 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
Ferraioli G, Tinelli C, Lissandrin R, Zicchetti M, Dal Bello B, Filice G, Filice C. Controlled attenuation parameter for evaluating liver steatosis in chronic viral hepatitis. World J Gastroenterol 2014;20:6626–6631
Jung KS, Kim BK, Kim SU, Chon YE, Cheon KH, Kim SB, Lee SH, 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
Shen F, Zheng RD, Mi YQ, Wang XY, Pan Q, Chen GY, Cao HX, et al. Controlled attenuation parameter for non-invasive assessment of hepatic steatosis in Chinese patients. World J Gastroenterol 2014;20:4702–4711
Yilmaz Y, Yesil A, Gerin F, Ergelen R, Akin H, Celikel CA, Imeryuz N. Detection of hepatic steatosis using the controlled attenuation parameter: a comparative study with liver biopsy. Scand J Gastroenterol 2014;49:611–616
Cardoso AC, Beaugrand M, de Ledinghen V, Douvin C, Poupon R, Trinchet JC, Ziol M, et al. Diagnostic performance of controlled attenuation parameter for predicting steatosis grade in chronic hepatitis B. Ann Hepatol 2015;14:826–836
Mi YQ, Shi QY, Xu L, Shi RF, Liu YG, Li P, Shen F, et al. Controlled attenuation parameter for noninvasive assessment of hepatic steatosis using Fibroscan(R): validation in chronic hepatitis B. Dig Dis Sci 2015;60:243–251
Ledinghen V, Wong GL, Vergniol J, Chan HL, Hiriart JB, Chan AW, Chermak F, et al. Controlled attenuation parameter for the diagnosis of steatosis in non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2016;31:848–855
Imajo K, Kessoku T, Honda Y, Tomeno W, Ogawa Y, Mawatari H, Fujita K, 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)
Shi KQ, Tang JZ, Zhu XL, Ying L, Li DW, Gao J, Fang YX, 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;29:1149–1158
Shen F, Zheng RD, Shi JP, Mi YQ, Chen GF, Hu X, Liu YG, 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
Kwok R, Choi KC, Wong GL, Zhang Y, Chan HL, Luk AO, Shu SS, 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;65:1359–1368
Castera L, Foucher J, Bernard PH, Carvalho F, Allaix D, Merrouche W, Couzigou P, et al. Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology 2010;51:828–835
Sasso M, Audiere S, Kemgang A, Gaouar F, Corpechot C, Chazouilleres O, Fournier C, et al. Liver steatosis assessed by controlled attenuation parameter (cap) measured with the XL probe of the FibroScan: a pilot study assessing diagnostic accuracy. Ultrasound Med Biol 2016;42:92–103
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;25:1330–1334
Limanond P, Raman SS, Lassman C, Sayre J, Ghobrial RM, Busuttil RW, Saab S, et al. Macrovesicular hepatic steatosis in living related liver donors: correlation between CT and histologic findings. Radiology 2004;230:276–280
Schwenzer NF, Springer F, Schraml C, Stefan N, Machann J, Schick F. Non-invasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol 2009;51:433–445
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
Mehta SR, Thomas EL, Bell JD, Johnston DG, Taylor-Robinson SD. Non-invasive means of measuring hepatic fat content. World J Gastroenterol 2008;14:3476–3483
Idilman IS, Keskin O, Celik A, Savas B, Halil Elhan A, Idilman R, Karcaaltincaba M. 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;57:271–278
Szczepaniak LS, Nurenberg P, Leonard D, Browning JD, Reingold JS, Grundy S, Hobbs HH, et al. Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 2005;288:E462–E468
Hines CD, Frydrychowicz A, Hamilton G, Tudorascu DL, Vigen KK, Yu H, McKenzie CA, et al. T(1) independent, T(2) (*) corrected chemical shift based fat-water separation with multi-peak fat spectral modeling is an accurate and precise measure of hepatic steatosis. J Magn Reson Imaging 2011;33:873–881
Permutt Z, Le TA, Peterson MR, Seki E, Brenner DA, Sirlin C, Loomba R. Correlation between liver histology and novel magnetic resonance imaging in adult patients with non-alcoholic fatty liver disease—MRI accurately quantifies hepatic steatosis in NAFLD. Aliment Pharmacol Ther 2012;36:22–29
Idilman IS, Aniktar H, Idilman R, Kabacam G, Savas B, Elhan A, Celik A, et al. Hepatic steatosis: quantification by proton density fat fraction with MR imaging versus liver biopsy. Radiology 2013;267:767–775
Bannas P, Kramer H, Hernando D, Agni R, Cunningham AM, Mandal R, Motosugi U, et al. Quantitative magnetic resonance imaging of hepatic steatosis: validation in ex vivo human livers. Hepatology 2015;62:1444–1455
Tang A, Desai A, Hamilton G, Wolfson T, Gamst A, Lam J, Clark L, 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
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Stern, C., Castera, L. Non-invasive diagnosis of hepatic steatosis. Hepatol Int 11, 70–78 (2017). https://doi.org/10.1007/s12072-016-9772-z
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DOI: https://doi.org/10.1007/s12072-016-9772-z