Non-invasive diagnosis of hepatic steatosis

Hepatology International

Volumn 11, Issue 1, 2017, Pages 70-78

  Stern, Christiane ^a   Castera, Laurent ^a  

^a BEAUJON HOSPITAL   (France)

Author keywords

Biomarkers; NAFLD; NASH; Non invasive tests; Steatosis

Indexed keywords

BIOLOGICAL MARKER;

ALGORITHM; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED ATTENUATION PARAMETER; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST; ECHOGRAPHY; ELASTOGRAPH; FATTY LIVER; HUMAN; LIVER BIOPSY; NON INVASIVE PROCEDURE; NONALCOHOLIC FATTY LIVER; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; RADIATION ATTENUATION; REVIEW; SENSITIVITY AND SPECIFICITY; DIAGNOSTIC IMAGING; FEMALE; LIVER; MALE; METABOLISM; MULTIMODAL IMAGING; PATHOLOGY; PROCEDURES; X-RAY COMPUTED TOMOGRAPHY;

BIOMARKERS; FATTY LIVER; FEMALE; HUMANS; LIVER; MAGNETIC RESONANCE IMAGING; MALE; MULTIMODAL IMAGING; TOMOGRAPHY, X-RAY COMPUTED; ULTRASONOGRAPHY;

EID: 84992392108     PISSN: 19360533     EISSN: 19360541     Source Type: Journal    
DOI: 10.1007/s12072-016-9772-z     Document Type: Review

References (65)

1. 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
2. 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
3. Satapathy SK, Sanyal AJ. Epidemiology and natural history of nonalcoholic fatty liver disease. Semin Liver Dis 2015;35:221–235
4. 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)
5. 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
6. 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)
7. Nalbantoglu IL, Brunt EM. Role of liver biopsy in nonalcoholic fatty liver disease. World J Gastroenterol 2014;20:9026–9037
8. 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
9. 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
10. 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
11. 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
12. 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
13. 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
14. 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
15. 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
16. 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
17. 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
18. 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
19. 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
20. 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
21. 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
22. Castera L, Vilgrain V, Angulo P. Noninvasive evaluation of NAFLD. Nat Rev Gastroenterol Hepatol 2013;10:666–675
23. 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
24. 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
25. 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
26. 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
27. 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
28. 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
29. 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
30. 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
31. 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
32. 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
33. 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
34. 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
35. 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
36. 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
37. 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
38. 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
39. 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
40. 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
41. 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
42. 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
43. 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
44. 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
45. 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
46. 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
47. 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
48. 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)
49. 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
50. 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
51. 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
52. 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
53. 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
54. 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
55. 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
56. 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
57. 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
58. 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
59. 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
60. 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
61. 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
62. 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
63. 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
64. 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
65. 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