Biopsy and Noninvasive Methods to Assess Progression of Nonalcoholic Fatty Liver Disease

Gastroenterology

Volumn 150, Issue 8, 2016, Pages 1811-1822.e4

  Bedossa, Pierre ^a   Patel, Keyur ^b  

^a BEAUJON HOSPITAL   (France)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Antifibrotics; Biomarkers; Hepatic Fibrosis; Histology; Imaging; Steatohepatitis; Steatosis

Indexed keywords

BIOLOGICAL MARKER;

ARTICLE; BLOOD LEVEL; DIAGNOSTIC IMAGING; DISEASE COURSE; HISTOPATHOLOGY; HUMAN; LIVER BIOPSY; MONITORING; NON INVASIVE PROCEDURE; NONALCOHOLIC FATTY LIVER; PREDICTION; PRIORITY JOURNAL; PROGNOSIS; RISK ASSESSMENT; SCORING SYSTEM; ALGORITHM; BIOPSY; BLOOD; COMPLICATION; LIVER; LIVER CIRRHOSIS; PATHOLOGY; SEVERITY OF ILLNESS INDEX;

ALGORITHMS; BIOMARKERS; BIOPSY; DISEASE PROGRESSION; HUMANS; LIVER; LIVER CIRRHOSIS; NON-ALCOHOLIC FATTY LIVER DISEASE; PROGNOSIS; SEVERITY OF ILLNESS INDEX;

EID: 84971350206     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2016.03.008     Document Type: Article

References (147)

1. M.E. Rinella Nonalcoholic fatty liver disease: a systematic review JAMA 313 2015 2263 2273
2. P. Angulo, D.E. Kleiner, S. Dam-Larsen, and et al. Liver fibrosis, but no other histologic features, is associated with long-term outcomes of patients with nonalcoholic fatty liver disease Gastroenterology 149 2015 389 397 e10
3. European Association for Study of Liver EASL-ALEH Clinical Practice Guidelines: non-invasive tests for evaluation of liver disease severity and prognosis J Hepatol 63 2015 237 264
4. K. Patel, P. Bedossa, and L. Castera Diagnosis of liver fibrosis: present and future Semin Liver Dis 35 2015 166 183
5. N. Chalasani, Z. Younossi, J.E. Lavine, and et al. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology Gastroenterology 142 2012 1592 1609
6. I.L. Nalbantoglu, and E.M. Brunt Role of liver biopsy in nonalcoholic fatty liver disease World J Gastroenterol 20 2014 9026 9037
7. V. Ratziu, S. Bellentani, H. Cortez-Pinto, and et al. A position statement on NAFLD/NASH based on the EASL 2009 special conference J Hepatol 53 2010 372 384
8. P. Bedossa, D. Dargere, and V. Paradis Sampling variability of liver fibrosis in chronic hepatitis C Hepatology 38 2003 1449 1457
9. V. Ratziu, F. Charlotte, A. Heurtier, and et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease Gastroenterology 128 2005 1898 1906
10. R. Vuppalanchi, A. Unalp, M.L. Van Natta, and et al. Effects of liver biopsy sample length and number of readings on sampling variability in nonalcoholic fatty liver disease Clin Gastroenterol Hepatol 7 2009 481 486
11. N.S. Goldstein, F. Hastah, M.V. Galan, and et al. Fibrosis heterogeneity in nonalcoholic steatohepatitis and hepatitis C virus needle core biopsy specimens Am J Clin Pathol 123 2005 382 387
12. G. Colloredo, M. Guido, A. Sonzogni, and et al. Impact of liver biopsy size on histological evaluation of chronic viral hepatitis: the smaller the sample, the milder the disease J Hepatol 39 2003 239 244
13. Z.M. Younossi, T. Gramlich, Y.C. Liu, and et al. Nonalcoholic fatty liver disease: assessment of variability in pathologic interpretations Mod Pathol 11 1998 560 565
14. P. Bedossa Consortium FP Utility and appropriateness of the fatty liver inhibition of progression (FLIP) algorithm and steatosis, activity, and fibrosis (SAF) score in the evaluation of biopsies of nonalcoholic fatty liver disease Hepatology 60 2014 565 575
15. E.M. Brunt Pathology of nonalcoholic fatty liver disease Nat Rev Gastroenterol Hepatol 7 2010 195 203
16. M.M. Yeh, and E.M. Brunt Pathological features of fatty liver disease Gastroenterology 147 2014 754 764
17. J.B. Dixon, P.S. Bhathal, and P.E. O'Brien Nonalcoholic fatty liver disease: predictors of nonalcoholic steatohepatitis and liver fibrosis in the severely obese Gastroenterology 121 2001 91 100
18. G.M. Campos, K. Bambha, E. Vittinghoff, and et al. A clinical scoring system for predicting nonalcoholic steatohepatitis in morbidly obese patients Hepatology 47 2008 1916 1923
19. D.G. Tiniakos Nonalcoholic fatty liver disease/nonalcoholic steatohepatitis: histological diagnostic criteria and scoring systems Eur J Gastroenterol Hepatol 22 2010 643 650
20. S. Tandra, M.M. Yeh, E.M. Brunt, and et al. Presence and significance of microvesicular steatosis in nonalcoholic fatty liver disease J Hepatol 55 2011 654 659
21. J.B. Schwimmer, C. Behling, R. Newbury, and et al. Histopathology of pediatric nonalcoholic fatty liver disease Hepatology 42 2005 641 649
22. D.E. Kleiner, E.M. Brunt, M. Van Natta, and et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease Hepatology 41 2005 1313 1321
23. C.A. Matteoni, Z.M. Younossi, T. Gramlich, and et al. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity Gastroenterology 116 1999 1413 1419
24. S. Singh, A.M. Allen, Z. Wang, and et al. Fibrosis progression in nonalcoholic fatty liver vs nonalcoholic steatohepatitis: a systematic review and meta-analysis of paired-biopsy studies Clin Gastroenterol Hepatol 13 2015 643 654 e1-9; quiz e39-e40
25. R. Pais, F. Charlotte, L. Fedchuk, and et al. A systematic review of follow-up biopsies reveals disease progression in patients with non-alcoholic fatty liver J Hepatol 59 2013 550 556
26. S. McPherson, T. Hardy, E. Henderson, and et al. Evidence of NAFLD progression from steatosis to fibrosing-steatohepatitis using paired biopsies: implications for prognosis and clinical management J Hepatol 62 2015 1148 1155
27. J. Ludwig, T.R. Viggiano, D.B. McGill, and et al. Nonalcoholic steatohepatitis: Mayo Clinic experiences with a hitherto unnamed disease Mayo Clin Proc 55 1980 434 438
28. P. Bedossa, C. Poitou, N. Veyrie, and et al. Histopathological algorithm and scoring system for evaluation of liver lesions in morbidly obese patients Hepatology 56 2012 1751 1759
29. C. Lackner, M. Gogg-Kamerer, K. Zatloukal, and et al. Ballooned hepatocytes in steatohepatitis: the value of keratin immunohistochemistry for diagnosis J Hepatol 48 2008 821 828
30. C.K. Argo, Y. Ikura, C. Lackner, and et al. The fat droplet in hepatocellular ballooning and implications for scoring nonalcoholic steatohepatitis therapeutic response Hepatology 63 2016 1056 1057
31. S. Caldwell, Y. Ikura, D. Dias, and et al. Hepatocellular ballooning in NASH J Hepatol 53 2010 719 723
32. C.D. Guy, A. Suzuki, J.L. Burchette, and et al. Costaining for keratins 8/18 plus ubiquitin improves detection of hepatocyte injury in nonalcoholic fatty liver disease Hum Pathol 43 2012 790 800
33. P. Sakhuja Pathology of alcoholic liver disease, can it be differentiated from nonalcoholic steatohepatitis? World J Gastroenterol 20 2014 16474 16479
34. M. Ekstedt, L.E. Franzen, U.L. Mathiesen, and et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes Hepatology 44 2006 865 873
35. M. Ekstedt, H. Hagstrom, P. Nasr, and et al. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up Hepatology 61 2015 1547 1554
36. Y. Ikura Transitions of histopathologic criteria for diagnosis of nonalcoholic fatty liver disease during the last three decades World J Hepatol 6 2014 894 900
37. Z.M. Younossi, M. Stepanova, N. Rafiq, and et al. Pathologic criteria for nonalcoholic steatohepatitis: interprotocol agreement and ability to predict liver-related mortality Hepatology 53 2011 1874 1882
38. M.M. Richardson, J.R. Jonsson, E.E. Powell, and et al. Progressive fibrosis in nonalcoholic steatohepatitis: association with altered regeneration and a ductular reaction Gastroenterology 133 2007 80 90
39. E.M. Brunt, D.E. Kleiner, L.A. Wilson, and et al. Portal chronic inflammation in nonalcoholic fatty liver disease (NAFLD): a histologic marker of advanced NAFLD-clinicopathologic correlations from the nonalcoholic steatohepatitis clinical research network Hepatology 49 2009 809 820
40. C.K. Argo, P.G. Northup, A.M. Al-Osaimi, and et al. Systematic review of risk factors for fibrosis progression in non-alcoholic steatohepatitis J Hepatol 51 2009 371 379
41. E.M. Brunt, C.G. Janney, A.M. Di Bisceglie, and et al. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions Am J Gastroenterol 94 1999 2467 2474
42. E.M. Brunt, D.E. Kleiner, L.A. Wilson, and et al. Nonalcoholic fatty liver disease (NAFLD) activity score and the histopathologic diagnosis in NAFLD: distinct clinicopathologic meanings Hepatology 53 2011 810 820
43. L.L. Listenberger, X. Han, S.E. Lewis, and et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity Proc Natl Acad Sci U S A 100 2003 3077 3082
44. C. Trautwein, S.L. Friedman, D. Schuppan, and et al. Hepatic fibrosis: concept to treatment J Hepatol 62 2015 S15 S24
45. M.W. Russo, R.J. Firpi, D.R. Nelson, and et al. Early hepatic stellate cell activation is associated with advanced fibrosis after liver transplantation in recipients with hepatitis C Liver Transpl 11 2005 1235 1241
46. J. Wattacheril, E.H. Seeley, P. Angel, and et al. Differential intrahepatic phospholipid zonation in simple steatosis and nonalcoholic steatohepatitis PLoS One 8 2013 e57165
47. L. Gailhouste, Y. Le Grand, C. Odin, and et al. Fibrillar collagen scoring by second harmonic microscopy: a new tool in the assessment of liver fibrosis J Hepatol 52 2010 398 406
48. S. Xu, Y. Wang, D.C. Tai, and et al. qFibrosis: a fully-quantitative innovative method incorporating histological features to facilitate accurate fibrosis scoring in animal model and chronic hepatitis B patients J Hepatol 61 2014 260 269
49. A.J. Sanyal, E.M. Brunt, D.E. Kleiner, and et al. Endpoints and clinical trial design for nonalcoholic steatohepatitis Hepatology 54 2011 344 353
50. D.E. Kleiner, and E.M. Brunt Nonalcoholic fatty liver disease: pathologic patterns and biopsy evaluation in clinical research Semin Liver Dis 32 2012 3 13
51. D.E. Kleiner, and P. Bedossa Liver histology and NASH Clinical Trials: two pathologists' perspective Gastroenterology 149 2015 1305 1308
52. A.J. Sanyal, S.L. Friedman, A.J. McCullough, and et al. Challenges and opportunities in drug and biomarker development for nonalcoholic steatohepatitis: findings and recommendations from an American Association for the Study of Liver Diseases-U.S. Food and Drug Administration Joint Workshop Hepatology 61 2015 1392 1405
53. A.J. Sanyal, B.A. Neuschwander-Tetri, and J. Tonascia End points must be clinically meaningful for drug development in nonalcoholic fatty liver disease Gastroenterology 150 2016 11 13
54. R. Belfort, S.A. Harrison, K. Brown, and et al. A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis N Engl J Med 355 2006 2297 2307
55. J.E. Lavine, J.B. Schwimmer, M.L. Van Natta, and et al. Effect of vitamin E or metformin for treatment of nonalcoholic fatty liver disease in children and adolescents: the TONIC randomized controlled trial JAMA 305 2011 1659 1668
56. D.M. Torres, F.J. Jones, J.C. Shaw, and et al. Rosiglitazone versus rosiglitazone and metformin versus rosiglitazone and losartan in the treatment of nonalcoholic steatohepatitis in humans: a 12-month randomized, prospective, open-label trial Hepatology 54 2011 1631 1639
57. R. Loomba, G. Lutchman, D.E. Kleiner, and et al. Clinical trial: pilot study of metformin for the treatment of non-alcoholic steatohepatitis Aliment Pharmacol Ther 29 2009 172 182
58. A.J. Sanyal, N. Chalasani, K.V. Kowdley, and et al. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis N Engl J Med 362 2010 1675 1685
59. B.A. Neuschwander-Tetri, R. Loomba, A.J. Sanyal, and et al. Farnesoid X nuclear receptor ligand obeticholic acid for non-cirrhotic, non-alcoholic steatohepatitis (FLINT): a multicentre, randomised, placebo-controlled trial Lancet 385 2015 956 965
60. L. Castera, V. Vilgrain, and P. Angulo Noninvasive evaluation of NAFLD Nat Rev Gastroenterol Hepatol 10 2013 666 675
61. M.V. Machado, and H. Cortez-Pinto Non-invasive diagnosis of non-alcoholic fatty liver disease. A critical appraisal J Hepatol 58 2013 1007 1019
62. H.K. Luckhoff, F.C. Kruger, and M.J. Kotze Composite prognostic models across the non-alcoholic fatty liver disease spectrum: clinical application in developing countries World J Hepatol 7 2015 1192 1208
63. K. Cusi, Z. Chang, S. Harrison, and et al. Limited value of plasma cytokeratin-18 as a biomarker for NASH and fibrosis in patients with non-alcoholic fatty liver disease J Hepatol 60 2014 167 174
64. R. Kwok, Y.K. Tse, G.L. Wong, and et al. Systematic review with meta-analysis: non-invasive assessment of non-alcoholic fatty liver disease-the role of transient elastography and plasma cytokeratin-18 fragments Aliment Pharmacol Ther 39 2014 254 269
65. Z.M. Younossi, M. Jarrar, C. Nugent, and et al. A novel diagnostic biomarker panel for obesity-related nonalcoholic steatohepatitis (NASH) Obes Surg 18 2008 1430 1437
66. T.I. Tamimi, H.M. Elgouhari, N. Alkhouri, and et al. An apoptosis panel for nonalcoholic steatohepatitis diagnosis J Hepatol 54 2011 1224 1229
67. G. Musso, R. Gambino, M. Cassader, and et al. Meta-analysis: natural history of non-alcoholic fatty liver disease (NAFLD) and diagnostic accuracy of non-invasive tests for liver disease severity Ann Med 43 2011 617 649
68. R. Vuppalanchi, A.K. Jain, R. Deppe, and et al. Relationship between changes in serum levels of keratin 18 and changes in liver histology in children and adults with nonalcoholic fatty liver disease Clin Gastroenterol Hepatol 12 2014 2121 2130 e1-2
69. N.A. Palekar, R. Naus, S.P. Larson, and et al. Clinical model for distinguishing nonalcoholic steatohepatitis from simple steatosis in patients with nonalcoholic fatty liver disease Liver Int 26 2006 151 156
70. T. Poynard, V. Ratziu, F. Charlotte, and et al. Diagnostic value of biochemical markers (NashTest) for the prediction of non alcohol steato hepatitis in patients with non-alcoholic fatty liver disease BMC Gastroenterol 6 2006 34
71. T. Poynard, G. Lassailly, E. Diaz, and et al. Performance of biomarkers FibroTest, ActiTest, SteatoTest, and NashTest in patients with severe obesity: meta analysis of individual patient data PLoS One 7 2012 e30325
72. Y. Sumida, M. Yoneda, H. Hyogo, and et al. A simple clinical scoring system using ferritin, fasting insulin, and type IV collagen 7S for predicting steatohepatitis in nonalcoholic fatty liver disease J Gastroenterol 46 2011 257 268
73. R. Anty, A. Iannelli, S. Patouraux, and et al. A new composite model including metabolic syndrome, alanine aminotransferase and cytokeratin-18 for the diagnosis of non-alcoholic steatohepatitis in morbidly obese patients Aliment Pharmacol Ther 32 2010 1315 1322
74. I.N. Guha, J. Parkes, P. Roderick, and et al. Noninvasive markers of fibrosis in nonalcoholic fatty liver disease: validating the European Liver Fibrosis Panel and exploring simple markers Hepatology 47 2008 455 460
75. V. Nobili, J. Parkes, G. Bottazzo, and et al. Performance of ELF serum markers in predicting fibrosis stage in pediatric non-alcoholic fatty liver disease Gastroenterology 136 2009 160 167
76. P. Cales, F. Laine, J. Boursier, and et al. Comparison of blood tests for liver fibrosis specific or not to NAFLD J Hepatol 50 2009 165 173
77. E. Dincses, and Y. Yilmaz Diagnostic usefulness of FibroMeter VCTE for hepatic fibrosis in patients with nonalcoholic fatty liver disease Eur J Gastroenterol Hepatol 27 2015 1149 1153
78. V. Ratziu, J. Massard, F. Charlotte, and et al. Diagnostic value of biochemical markers (FibroTest-FibroSURE) for the prediction of liver fibrosis in patients with non-alcoholic fatty liver disease BMC Gastroenterol 6 2006 6
79. A.G. Shah, A. Lydecker, K. Murray, and et al. Comparison of noninvasive markers of fibrosis in patients with nonalcoholic fatty liver disease Clin Gastroenterol Hepatol 7 2009 1104 1112
80. Y. Sumida, M. Yoneda, H. Hyogo, and et al. Validation of the FIB4 index in a Japanese nonalcoholic fatty liver disease population BMC Gastroenterol 12 2012 2
81. L.A. Adams, J. George, E. Bugianesi, and et al. Complex non-invasive fibrosis models are more accurate than simple models in non-alcoholic fatty liver disease J Gastroenterol Hepatol 26 2011 1536 1543
82. P. Angulo, J.M. Hui, G. Marchesini, and et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD Hepatology 45 2007 846 854
83. J. Bazick, M. Donithan, B.A. Neuschwander-Tetri, and et al. Clinical model for NASH and advanced fibrosis in adult patients with diabetes and NAFLD: guidelines for referral in NAFLD Diabetes Care 38 2015 1347 1355
84. S. McPherson, S.F. Stewart, E. Henderson, and et al. Simple non-invasive fibrosis scoring systems can reliably exclude advanced fibrosis in patients with non-alcoholic fatty liver disease Gut 59 2010 1265 1269
85. C.F. Subasi, U.E. Aykut, and Y. Yilmaz Comparison of noninvasive scores for the detection of advanced fibrosis in patients with nonalcoholic fatty liver disease Eur J Gastroenterol Hepatol 27 2015 137 141
86. D. Festi, R. Schiumerini, L. Marzi, and et al. Review article: the diagnosis of non-alcoholic fatty liver disease - availability and accuracy of non-invasive methods Aliment Pharmacol Ther 37 2013 392 400
87. S. Petta, E. Vanni, E. Bugianesi, and 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 35 2015 1566 1573
88. L. Castera Noninvasive evaluation of nonalcoholic fatty liver disease Semin Liver Dis 35 2015 291 303
89. M.A. Karsdal, H. Krarup, J.M. Sand, and et al. Review article: the efficacy of biomarkers in chronic fibroproliferative diseases - early diagnosis and prognosis, with liver fibrosis as an exemplar Aliment Pharmacol Ther 40 2014 233 249
90. T. Poynard, G. Lenaour, J.C. Vaillant, and et al. Liver biopsy analysis has a low level of performance for diagnosis of intermediate stages of fibrosis Clin Gastroenterol Hepatol 10 2012 657 663 e7
91. P. Cales, V. de Ledinghen, P. Halfon, and et al. Evaluating the accuracy and increasing the reliable diagnosis rate of blood tests for liver fibrosis in chronic hepatitis C Liver Int 28 2008 1352 1362
92. K. Patel, K.S. Remlinger, T.G. Walker, and et al. Multiplex protein analysis to determine fibrosis stage and progression in patients with chronic hepatitis C Clin Gastroenterol Hepatol 12 2014 2113 2120
93. D. Kim, W.R. Kim, H.J. Kim, and et al. Association between noninvasive fibrosis markers and mortality among adults with nonalcoholic fatty liver disease in the United States Hepatology 57 2013 1357 1365
94. P. Angulo, E. Bugianesi, E.S. Bjornsson, and et al. Simple noninvasive systems predict long-term outcomes of patients with nonalcoholic fatty liver disease Gastroenterology 145 2013 782 789 e4
95. Q.M. Anstee, and C.P. Day The genetics of nonalcoholic fatty liver disease: spotlight on PNPLA3 and TM6SF2 Semin Liver Dis 35 2015 270 290
96. P. Dongiovanni, B. Donati, R. Fares, and et al. PNPLA3 I148M polymorphism and progressive liver disease World J Gastroenterol 19 2013 6969 6978
97. P. Dongiovanni, S. Romeo, and L. Valenti Genetic factors in the pathogenesis of nonalcoholic fatty liver and steatohepatitis Biomed Res Int 2015 2015 460190
98. M.H. Miller, S.V. Walsh, A. Atrih, and et al. Serum proteome of nonalcoholic fatty liver disease: a multimodal approach to discovery of biomarkers of nonalcoholic steatohepatitis J Gastroenterol Hepatol 29 2014 1839 1847
99. Y. Kamada, M. Ono, H. Hyogo, and et al. A novel noninvasive diagnostic method for nonalcoholic steatohepatitis using two glycobiomarkers Hepatology 62 2015 1433 1443
100. Y. Yamasaki, K. Nouso, K. Miyahara, and et al. Use of non-invasive serum glycan markers to distinguish non-alcoholic steatohepatitis from simple steatosis J Gastroenterol Hepatol 30 2015 528 534
101. R. Loomba, O. Quehenberger, A. Armando, and et al. Polyunsaturated fatty acid metabolites as novel lipidomic biomarkers for noninvasive diagnosis of nonalcoholic steatohepatitis J Lipid Res 56 2015 185 192
102. N. Panera, D. Gnani, A. Crudele, and et al. MicroRNAs as controlled systems and controllers in non-alcoholic fatty liver disease World J Gastroenterol 20 2014 15079 15086
103. H. Miyaaki, T. Ichikawa, Y. Kamo, and et al. Significance of serum and hepatic microRNA-122 levels in patients with non-alcoholic fatty liver disease Liver Int 34 2014 e302 e307
104. C.J. Pirola, T. Fernandez Gianotti, G.O. Castano, and et al. Circulating microRNA signature in non-alcoholic fatty liver disease: from serum non-coding RNAs to liver histology and disease pathogenesis Gut 64 2015 800 812
105. A. Zarrinpar, S. Gupta, M.R. Maurya, and et al. Serum microRNAs explain discordance of non-alcoholic fatty liver disease in monozygotic and dizygotic twins: a prospective study Gut 2015 http://dx.doi.org/10.1136/gutjnl-2015-309456
106. S.K. Murphy, H. Yang, C.A. Moylan, and et al. Relationship between methylome and transcriptome in patients with nonalcoholic fatty liver disease Gastroenterology 145 2013 1076 1087
107. S. Lemoinne, D. Thabut, C. Housset, and et al. The emerging roles of microvesicles in liver diseases Nat Rev Gastroenterol Hepatol 11 2014 350 361
108. K. Takahashi, I. Yan, H. Haga, and et al. Long noncoding RNA in liver diseases Hepatology 60 2014 744 753
109. P. Portincasa, I. Grattagliano, B.H. Lauterburg, and et al. Liver breath tests non-invasively predict higher stages of non-alcoholic steatohepatitis Clin Sci (Lond) 111 2006 135 143
110. C. Fierbinteanu-Braticevici, D.A. Plesca, L. Tribus, and et al. The role of (1)(3)C-methacetin breath test for the non-invasive evaluation of nonalcoholic fatty liver disease J Gastrointest Liver Dis 22 2013 149 156
111. H. Korkmaz, G.K. Unler, H.S. Gokturk, and et al. Noninvasive estimation of disease activity and liver fibrosis in nonalcoholic fatty liver disease using anthropometric and biochemical characteristics, including insulin, insulin resistance, and 13C-methionine breath test Eur J Gastroenterol Hepatol 27 2015 1137 1143
112. G. Tribonias, E. Margariti, D. Tiniakos, and et al. Liver function breath tests for differentiation of steatohepatitis from simple fatty liver in patients with nonalcoholic fatty liver disease J Clin Gastroenterol 48 2014 59 65
113. R. Hernaez, M. Lazo, S. Bonekamp, and et al. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis Hepatology 54 2011 1082 1090
114. J.F. Cobbold, D. Patel, and S.D. Taylor-Robinson Assessment of inflammation and fibrosis in non-alcoholic fatty liver disease by imaging-based techniques J Gastroenterol Hepatol 27 2012 1281 1292
115. S.S. Lee, and S.H. Park Radiologic evaluation of nonalcoholic fatty liver disease World J Gastroenterol 20 2014 7392 7402
116. K.Q. Shi, J.Z. Tang, X.L. Zhu, and et al. Controlled attenuation parameter for the detection of steatosis severity in chronic liver disease: a meta-analysis of diagnostic accuracy J Gastroenterol Hepatol 29 2014 1149 1158
117. R.P. Myers, A. Pollett, R. Kirsch, and et al. Controlled attenuation parameter (CAP): a noninvasive method for the detection of hepatic steatosis based on transient elastography Liver Int 32 2012 902 910
118. S. Carvalhana, J. Leitao, A.C. Alves, and et al. How good is controlled attenuation parameter and fatty liver index for assessing liver steatosis in general population: correlation with ultrasound Liver Int 34 2014 e111 e117
119. T. Karlas, D. Petroff, N. Garnov, and et al. Non-invasive assessment of hepatic steatosis in patients with NAFLD using controlled attenuation parameter and 1H-MR spectroscopy PLoS One 9 2014 e91987
120. V. de Ledinghen, J. Vergniol, M. Capdepont, and et al. Controlled attenuation parameter (CAP) for the diagnosis of steatosis: a prospective study of 5323 examinations J Hepatol 60 2014 1026 1031
121. R. Kwok, K.C. Choi, G.L. Wong, and et al. Screening diabetic patients for non-alcoholic fatty liver disease with controlled attenuation parameter and liver stiffness measurements: a prospective cohort study Gut 2015 http://dx.doi.org/10.1136/gutjnl-2015-309265
122. M. Sasso, S. Audiere, A. Kemgang, and 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 42 2016 92 103
123. S.C. Lin, E. Heba, T. Wolfson, and et al. Noninvasive diagnosis of nonalcoholic fatty liver disease and quantification of liver fat using a new quantitative ultrasound technique Clin Gastroenterol Hepatol 13 2015 1337 1345 e6
124. S.B. Reeder, I. Cruite, G. Hamilton, and et al. Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy J Magn Reson Imaging 34 2011 729 749
125. I.S. Idilman, O. Keskin, A. Celik, and et al. 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 57 2016 271 278
126. M. Noureddin, J. Lam, M.R. Peterson, and et al. Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials Hepatology 58 2013 1930 1940
127. N.S. Patel, I. Doycheva, M.R. Peterson, and et al. Effect of weight loss on magnetic resonance imaging estimation of liver fat and volume in patients with nonalcoholic steatohepatitis Clin Gastroenterol Hepatol 13 2015 561 568 e1
128. V.W. Wong, J. Vergniol, G.L. Wong, and et al. Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease Hepatology 51 2010 454 462
129. S. Petta, M. Maida, F.S. Macaluso, and et al. The severity of steatosis influences liver stiffness measurement in patients with nonalcoholic fatty liver disease Hepatology 62 2015 1101 1110
130. R.P. Myers, G. Pomier-Layrargues, R. Kirsch, and et al. Feasibility and diagnostic performance of the FibroScan XL probe for liver stiffness measurement in overweight and obese patients Hepatology 55 2012 199 208
131. G.L. Wong, V.W. Wong, A.M. Chim, and et al. Factors associated with unreliable liver stiffness measurement and its failure with transient elastography in the Chinese population J Gastroenterol Hepatol 26 2011 300 305
132. V.W. Wong, J. Vergniol, G.L. Wong, and et al. Liver stiffness measurement using XL probe in patients with nonalcoholic fatty liver disease Am J Gastroenterol 107 2012 1862 1871
133. R.P. Myers, G. Pomier-Layrargues, R. Kirsch, and et al. Discordance in fibrosis staging between liver biopsy and transient elastography using the FibroScan XL probe J Hepatol 56 2012 564 570
134. E. Ogawa, N. Furusyo, K. Toyoda, and et al. The longitudinal quantitative assessment by transient elastography of chronic hepatitis C patients treated with pegylated interferon alpha-2b and ribavirin Antiviral Res 83 2009 127 134
135. F. Nascimbeni, P. Lebray, L. Fedchuk, and et al. Significant variations in elastometry measurements made within short-term in patients with chronic liver diseases Clin Gastroenterol Hepatol 13 2015 763 771 e1-6
136. R. D'Ambrosio, A. Aghemo, M. Fraquelli, and et al. The diagnostic accuracy of Fibroscan for cirrhosis is influenced by liver morphometry in HCV patients with a sustained virological response J Hepatol 59 2013 251 256
137. H. Liu, J. Fu, R. Hong, and et al. Acoustic radiation force impulse elastography for the non-invasive evaluation of hepatic fibrosis in non-alcoholic fatty liver disease patients: a systematic review & meta-analysis PLoS One 10 2015 e0127782
138. M. Friedrich-Rust, D. Romen, J. Vermehren, and et al. Acoustic radiation force impulse-imaging and transient elastography for non-invasive assessment of liver fibrosis and steatosis in NAFLD Eur J Radiol 81 2012 e325 e331
139. M. Yoneda, K. Suzuki, S. Kato, and et al. Nonalcoholic fatty liver disease: US-based acoustic radiation force impulse elastography Radiology 256 2010 640 647
140. L. Gerber, D. Kasper, D. Fitting, and et al. Assessment of liver fibrosis with 2-D shear wave elastography in comparison to transient elastography and acoustic radiation force impulse imaging in patients with chronic liver disease Ultrasound Med Biol 41 2015 2350 2359
141. J. Cui, B. Ang, W. Haufe, and et al. Comparative diagnostic accuracy of magnetic resonance elastography vs. eight clinical prediction rules for non-invasive diagnosis of advanced fibrosis in biopsy-proven non-alcoholic fatty liver disease: a prospective study Aliment Pharmacol Ther 41 2015 1271 1280
142. R. Loomba, T. Wolfson, B. Ang, and et al. Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study Hepatology 60 2014 1920 1928
143. S. Singh, S.K. Venkatesh, R. Loomba, and 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 26 2016 1431 1440
144. K. Imajo, T. Kessoku, Y. Honda, and et al. Magnetic resonance imaging more accurately classifies steatosis and fibrosis in patients with nonalcoholic fatty liver disease than transient elastography Gastroenterology 150 2016 626 637
145. J. Cui, E. Heba, C. Hernandez, and et al. Magnetic resonance elastography is superior to acoustic radiation force impulse for the diagnosis of fibrosis in patients with biopsy-proven nonalcoholic fatty liver disease: a prospective study Hepatology 63 2016 453 461
146. R. Loomba, C.B. Sirlin, B. Ang, and et al. Ezetimibe for the treatment of nonalcoholic steatohepatitis: assessment by novel magnetic resonance imaging and magnetic resonance elastography in a randomized trial (MOZART trial) Hepatology 61 2015 1239 1250
147. B.C. Fuchs, H. Wang, Y. Yang, and et al. Molecular MRI of collagen to diagnose and stage liver fibrosis J Hepatol 59 2013 992 998