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Published in: Digestive Diseases and Sciences 5/2016

01-05-2016 | Review

Fibrosis Assessment in Nonalcoholic Fatty Liver Disease (NAFLD) in 2016

Authors: Dharmesh H. Kaswala, Michelle Lai, Nezam H. Afdhal

Published in: Digestive Diseases and Sciences | Issue 5/2016

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Abstract

Nonalcoholic fatty liver disease (NAFLD) is a spectrum of liver pathologies characterized by hepatic steatosis with a history of little to no alcohol consumption or secondary causes of hepatic steatosis. The prevalence of NAFLD is 20–25 % of the general population in the Western countries and is associated with metabolic risk factors such as obesity, diabetes mellitus, and dyslipidemia. The spectrum of disease ranges from simple steatosis to nonalcoholic steatohepatitis, fibrosis, and cirrhosis. Advanced fibrosis is the most significant predictor of mortality in NAFLD. It is crucial to assess for the presence and degree of hepatic fibrosis in order to make therapeutic decisions and predict clinical outcomes. Liver biopsy, the current gold standard to assess the liver fibrosis, has a number of drawbacks such as invasiveness, sampling error, cost, and inter-/intra-observer variability. There are currently available a number of noninvasive tests as an alternative to liver biopsy for fibrosis staging. These noninvasive fibrosis tests are increasingly used to rule out advanced fibrosis and help guide disease management. While these noninvasive tests perform relatively well for ruling out advanced fibrosis, they also have limitations. Understanding the strengths and limitations of liver biopsy and the noninvasive tests is necessary for deciding when to use the appropriate tests in the evaluation of patients with NAFLD.
Literature
1.
go back to reference Sanyal AJ. AGA technical review on nonalcoholic fatty liver disease. Gastroenterology. 2002;123:1705–1725.CrossRefPubMed Sanyal AJ. AGA technical review on nonalcoholic fatty liver disease. Gastroenterology. 2002;123:1705–1725.CrossRefPubMed
2.
go back to reference Craft S. Insulin resistance syndrome and Alzheimer disease: pathophysiologic mechanisms and therapeutic implications. Alzheimer Dis Assoc Disord. 2006;20:298–301.CrossRefPubMed Craft S. Insulin resistance syndrome and Alzheimer disease: pathophysiologic mechanisms and therapeutic implications. Alzheimer Dis Assoc Disord. 2006;20:298–301.CrossRefPubMed
4.
go back to reference Afdhal NH. Management of nonalcoholic fatty liver disease: a 60-year-old man with probable nonalcoholic fatty liver disease: weight reduction, liver biopsy, or both? JAMA. 2012;308:608–616.CrossRefPubMed Afdhal NH. Management of nonalcoholic fatty liver disease: a 60-year-old man with probable nonalcoholic fatty liver disease: weight reduction, liver biopsy, or both? JAMA. 2012;308:608–616.CrossRefPubMed
5.
go back to reference Marchesini G, Bugianesi E, Forlani G, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology. 2003;37:917–923.CrossRefPubMed Marchesini G, Bugianesi E, Forlani G, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology. 2003;37:917–923.CrossRefPubMed
6.
7.
go back to reference Ogden C, Carroll M, Kit B, Flegal K. Prevalence of obesity and trends in body mass index among US children and adolescents, 1999–2010. JAMA. 2012;307:483–490.CrossRefPubMed Ogden C, Carroll M, Kit B, Flegal K. Prevalence of obesity and trends in body mass index among US children and adolescents, 1999–2010. JAMA. 2012;307:483–490.CrossRefPubMed
8.
go back to reference Fatty NN, Disease L, Mulhall BP, et al. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346:1221–1231.CrossRef Fatty NN, Disease L, Mulhall BP, et al. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346:1221–1231.CrossRef
9.
go back to reference Anstee QM, Targher G, Day CP. Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol. 2013;10:330–344.CrossRefPubMed Anstee QM, Targher G, Day CP. Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol. 2013;10:330–344.CrossRefPubMed
10.
go back to reference Chalasani N, Younossi Z, Lavine J. The diagnosis and management of nonalcoholic fatty liver disease: Practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012;55:2005–2023.CrossRefPubMed Chalasani N, Younossi Z, Lavine J. The diagnosis and management of nonalcoholic fatty liver disease: Practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012;55:2005–2023.CrossRefPubMed
11.
12.
go back to reference Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004;40:1387–1395.CrossRefPubMed Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004;40:1387–1395.CrossRefPubMed
13.
go back to reference Ekstedt M, Hagström H, Nasr P, Fredrikson M, Stål P, Kechagias S, et al. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology. 2015;61:1547–1554.CrossRefPubMed Ekstedt M, Hagström H, Nasr P, Fredrikson M, Stål P, Kechagias S, et al. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology. 2015;61:1547–1554.CrossRefPubMed
14.
go back to reference Brunt EM, Janney CG, Di Bisceglie AM, Neuschwander-Tetri BA, Bacon BR. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol. 1999;94:2467–2474.CrossRefPubMed Brunt EM, Janney CG, Di Bisceglie AM, Neuschwander-Tetri BA, Bacon BR. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol. 1999;94:2467–2474.CrossRefPubMed
15.
go back to reference Nalbantoglu I, Brunt EM. Role of liver biopsy in nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:9026–9037.PubMedPubMedCentral Nalbantoglu I, Brunt EM. Role of liver biopsy in nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:9026–9037.PubMedPubMedCentral
16.
go back to reference Afdhal NH, Nunes D. Evaluation of liver fibrosis: a concise review. Am J Gastroenterol. 2004;99:1160–1174.CrossRefPubMed Afdhal NH, Nunes D. Evaluation of liver fibrosis: a concise review. Am J Gastroenterol. 2004;99:1160–1174.CrossRefPubMed
17.
go back to reference Ratziu V, Charlotte F, Heurtier A, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128:1898–1906.CrossRefPubMed Ratziu V, Charlotte F, Heurtier A, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128:1898–1906.CrossRefPubMed
18.
go back to reference Manning DS, Afdhal NH. Diagnosis and quantitation of fibrosis. Gastroenterology. 2008;134:1670–1681.CrossRefPubMed Manning DS, Afdhal NH. Diagnosis and quantitation of fibrosis. Gastroenterology. 2008;134:1670–1681.CrossRefPubMed
19.
20.
go back to reference McPherson S, Stewart SF, Henderson E, Burt AD, Day CP. Simple non-invasive fibrosis scoring systems can reliably exclude advanced fibrosis in patients with nonalcoholic fatty liver disease. Gut. 2010;59:1265–1269.CrossRefPubMed McPherson S, Stewart SF, Henderson E, Burt AD, Day CP. Simple non-invasive fibrosis scoring systems can reliably exclude advanced fibrosis in patients with nonalcoholic fatty liver disease. Gut. 2010;59:1265–1269.CrossRefPubMed
21.
go back to reference Sheth SG, Flamm SL, Gordon FD, Chopra S. AST/ALT ratio predicts cirrhosis in patients with chronic hepatitis C virus infection. Am J Gastroenterol. 1998;93:44–48.CrossRefPubMed Sheth SG, Flamm SL, Gordon FD, Chopra S. AST/ALT ratio predicts cirrhosis in patients with chronic hepatitis C virus infection. Am J Gastroenterol. 1998;93:44–48.CrossRefPubMed
22.
go back to reference Ohgo H, Yokoyama H, Hirose H, et al. Significance of ALT/AST ratio for specifying subjects with metabolic syndrome in its silent stage. Diabetes Metab Syndr Clin Res Rev. 2009;3:3–6.CrossRef Ohgo H, Yokoyama H, Hirose H, et al. Significance of ALT/AST ratio for specifying subjects with metabolic syndrome in its silent stage. Diabetes Metab Syndr Clin Res Rev. 2009;3:3–6.CrossRef
23.
go back to reference Sorbi D, Boynton J, Lindor KD. The ratio of aspartate aminotransferase to alanine aminotransferase: potential value in differentiating nonalcoholic steatohepatitis from alcoholic liver disease. Am J Gastroenterol. 1999;94:1018–1022.CrossRefPubMed Sorbi D, Boynton J, Lindor KD. The ratio of aspartate aminotransferase to alanine aminotransferase: potential value in differentiating nonalcoholic steatohepatitis from alcoholic liver disease. Am J Gastroenterol. 1999;94:1018–1022.CrossRefPubMed
24.
go back to reference Ruffillo G, Fassio E, Alvarez E, et al. Comparison of NAFLD fibrosis score and BARD score in predicting fibrosis in nonalcoholic fatty liver disease. J Hepatol. 2011;54:160–163.CrossRefPubMed Ruffillo G, Fassio E, Alvarez E, et al. Comparison of NAFLD fibrosis score and BARD score in predicting fibrosis in nonalcoholic fatty liver disease. J Hepatol. 2011;54:160–163.CrossRefPubMed
25.
go back to reference Lee TH, Han SH, Yang JD, Kim D, Ahmed M. Prediction of advanced fibrosis in nonalcoholic fatty liver disease: an enhanced model of BARD score. Gut Liver. 2013;7:323–328.CrossRefPubMedPubMedCentral Lee TH, Han SH, Yang JD, Kim D, Ahmed M. Prediction of advanced fibrosis in nonalcoholic fatty liver disease: an enhanced model of BARD score. Gut Liver. 2013;7:323–328.CrossRefPubMedPubMedCentral
26.
go back to reference Rodrigues S, Rodrigues-Pinto E, Albuquerque A, et al. Significant correlation between liver stiffness, liver histology, and APRI score. Am J Gastroenterol. 2012. doi:10.1038/ajg.2012.271. Rodrigues S, Rodrigues-Pinto E, Albuquerque A, et al. Significant correlation between liver stiffness, liver histology, and APRI score. Am J Gastroenterol. 2012. doi:10.​1038/​ajg.​2012.​271.
27.
go back to reference Pissaia A, Borderie D, Bernard D, Scatton O, Calmus Y, Conti F. APRI and FIB-4 scores are useful after liver transplantation independently of etiology. Transplant Proc. 2009;41:679–681.CrossRefPubMed Pissaia A, Borderie D, Bernard D, Scatton O, Calmus Y, Conti F. APRI and FIB-4 scores are useful after liver transplantation independently of etiology. Transplant Proc. 2009;41:679–681.CrossRefPubMed
28.
go back to reference Tapper EB, Krajewski K, Lai M, et al. Simple non-invasive biomarkers of advanced fibrosis in the evaluation of nonalcoholic fatty liver disease. Gastroenterol Rep. 2014;2:276–280.CrossRef Tapper EB, Krajewski K, Lai M, et al. Simple non-invasive biomarkers of advanced fibrosis in the evaluation of nonalcoholic fatty liver disease. Gastroenterol Rep. 2014;2:276–280.CrossRef
30.
go back to reference Harrison SA, Oliver D, Arnold HL, Gogia S, Neuschwander-Tetri BA. Development and validation of a simple NAFLD clinical scoring system for identifying patients without advanced disease. Gut. 2008;57:1441–1447.CrossRefPubMed Harrison SA, Oliver D, Arnold HL, Gogia S, Neuschwander-Tetri BA. Development and validation of a simple NAFLD clinical scoring system for identifying patients without advanced disease. Gut. 2008;57:1441–1447.CrossRefPubMed
31.
go back to reference Cichoż-Lach H, Celiński K, Prozorow-Król B, Swatek J, Słomka M, Lach T. The BARD score and the NAFLD fibrosis score in the assessment of advanced liver fibrosis in nonalcoholic fatty liver disease. Med Sci Monit. 2012;18:CR735–CR740.PubMedPubMedCentral Cichoż-Lach H, Celiński K, Prozorow-Król B, Swatek J, Słomka M, Lach T. The BARD score and the NAFLD fibrosis score in the assessment of advanced liver fibrosis in nonalcoholic fatty liver disease. Med Sci Monit. 2012;18:CR735–CR740.PubMedPubMedCentral
32.
go back to reference Ratziu V, Giral P, Charlotte F, et al. Liver fibrosis in overweight patients. Gastroenterology. 2000;118:1117–1123.CrossRefPubMed Ratziu V, Giral P, Charlotte F, et al. Liver fibrosis in overweight patients. Gastroenterology. 2000;118:1117–1123.CrossRefPubMed
34.
go back to reference Diab DL, Yerian L, Schauer P, et al. Cytokeratin 18 fragment levels as a noninvasive biomarker for nonalcoholic steatohepatitis in bariatric surgery patients. Clin Gastroenterol Hepatol. 2008;6:1249–1254.CrossRefPubMedPubMedCentral Diab DL, Yerian L, Schauer P, et al. Cytokeratin 18 fragment levels as a noninvasive biomarker for nonalcoholic steatohepatitis in bariatric surgery patients. Clin Gastroenterol Hepatol. 2008;6:1249–1254.CrossRefPubMedPubMedCentral
35.
go back to reference Feldstein AE, Wieckowska A, Lopez AR, Liu YC, Zein NN, McCullough AJ. Cytokeratin-18 fragment levels as noninvasive biomarkers for nonalcoholic steatohepatitis: a multicenter validation study. Hepatology. 2009;50:1072–1078.CrossRefPubMedPubMedCentral Feldstein AE, Wieckowska A, Lopez AR, Liu YC, Zein NN, McCullough AJ. Cytokeratin-18 fragment levels as noninvasive biomarkers for nonalcoholic steatohepatitis: a multicenter validation study. Hepatology. 2009;50:1072–1078.CrossRefPubMedPubMedCentral
36.
go back to reference Cusi K, Chang Z, Harrison S, et al. Limited value of plasma cytokeratin-18 as a biomarker for NASH and fibrosis in patients with nonalcoholic fatty liver disease. J Hepatol. 2014;60:167–174.CrossRefPubMed Cusi K, Chang Z, Harrison S, et al. Limited value of plasma cytokeratin-18 as a biomarker for NASH and fibrosis in patients with nonalcoholic fatty liver disease. J Hepatol. 2014;60:167–174.CrossRefPubMed
37.
go back to reference Pimentel CMG, Jiang Z, Otsubo T, Feldbrügge L, Challies T, Nasser I, et al. Poor inter-test reliability between CK18 kits as a biomarker of NASH. Dig Dis Sci. 2016;61:905–912.CrossRefPubMed Pimentel CMG, Jiang Z, Otsubo T, Feldbrügge L, Challies T, Nasser I, et al. Poor inter-test reliability between CK18 kits as a biomarker of NASH. Dig Dis Sci. 2016;61:905–912.CrossRefPubMed
38.
go back to reference Friedrich-Rust M, Rosenberg W, Parkes J, Herrmann E, Zeuzem S, Sarrazin C. Comparison of ELF, FibroTest and FibroScan for the non-invasive assessment of liver fibrosis. BMC Gastroenterol. 2010;10:103.CrossRefPubMedPubMedCentral Friedrich-Rust M, Rosenberg W, Parkes J, Herrmann E, Zeuzem S, Sarrazin C. Comparison of ELF, FibroTest and FibroScan for the non-invasive assessment of liver fibrosis. BMC Gastroenterol. 2010;10:103.CrossRefPubMedPubMedCentral
39.
go back to reference Guha IN, Parkes J, Roderick P, et al. Noninvasive markers of fibrosis in nonalcoholic fatty liver disease: validating the European liver fibrosis panel and exploring simple markers. Hepatology. 2008;47:455–460.CrossRefPubMed Guha IN, Parkes J, Roderick P, et al. Noninvasive markers of fibrosis in nonalcoholic fatty liver disease: validating the European liver fibrosis panel and exploring simple markers. Hepatology. 2008;47:455–460.CrossRefPubMed
40.
go back to reference Parkes J, Guha IN, Roderick P, et al. Enhanced Liver Fibrosis (ELF) test accurately identifies liver fibrosis in patients with chronic hepatitis C. J Viral Hepat. 2011;18:23–31.CrossRefPubMed Parkes J, Guha IN, Roderick P, et al. Enhanced Liver Fibrosis (ELF) test accurately identifies liver fibrosis in patients with chronic hepatitis C. J Viral Hepat. 2011;18:23–31.CrossRefPubMed
41.
go back to reference Parkes J, Roderick P, Harris S, et al. Enhanced liver fibrosis test can predict clinical outcomes in patients with chronic liver disease. Gut. 2010;59:1245–1251.CrossRefPubMed Parkes J, Roderick P, Harris S, et al. Enhanced liver fibrosis test can predict clinical outcomes in patients with chronic liver disease. Gut. 2010;59:1245–1251.CrossRefPubMed
42.
go back to reference Sumida Y, Yoneda M, Hyogo H, et al. Validation of the FIB4 index in a Japanese nonalcoholic fatty liver disease population. BMC Gastroenterol. 2012;12:2.CrossRefPubMedPubMedCentral Sumida Y, Yoneda M, Hyogo H, et al. Validation of the FIB4 index in a Japanese nonalcoholic fatty liver disease population. BMC Gastroenterol. 2012;12:2.CrossRefPubMedPubMedCentral
43.
go back to reference Adler M, Gulbis B, Moreno C, et al. The predictive value of FIB-4 versus FibroTest, APRI, FibroIndex and Forns index to noninvasively estimate fibrosis in hepatitis C and nonhepatitis C liver diseases. Hepatology. 2008;47:762–763.CrossRefPubMed Adler M, Gulbis B, Moreno C, et al. The predictive value of FIB-4 versus FibroTest, APRI, FibroIndex and Forns index to noninvasively estimate fibrosis in hepatitis C and nonhepatitis C liver diseases. Hepatology. 2008;47:762–763.CrossRefPubMed
44.
go back to reference Lassailly G, Caiazzo R, Hollebecque A, et al. Validation of noninvasive biomarkers (FibroTest, SteatoTest, and NashTest) for prediction of liver injury in patients with morbid obesity. Eur J Gastroenterol Hepatol. 2011;23:499–506.CrossRefPubMed Lassailly G, Caiazzo R, Hollebecque A, et al. Validation of noninvasive biomarkers (FibroTest, SteatoTest, and NashTest) for prediction of liver injury in patients with morbid obesity. Eur J Gastroenterol Hepatol. 2011;23:499–506.CrossRefPubMed
45.
go back to reference Ratziu V, Giral P, Munteanu M, et al. Screening for liver disease using non-invasive biomarkers (FibroTest, SteatoTest and NashTest) in patients with hyperlipidaemia. Aliment Pharmacol Ther. 2007;25:207–218.CrossRefPubMed Ratziu V, Giral P, Munteanu M, et al. Screening for liver disease using non-invasive biomarkers (FibroTest, SteatoTest and NashTest) in patients with hyperlipidaemia. Aliment Pharmacol Ther. 2007;25:207–218.CrossRefPubMed
46.
go back to reference Oh S, Afdhal NH. Hepatic fibrosis: are any of the serum markers useful? Curr Gastroenterol Rep. 2001;3:12–18.CrossRefPubMed Oh S, Afdhal NH. Hepatic fibrosis: are any of the serum markers useful? Curr Gastroenterol Rep. 2001;3:12–18.CrossRefPubMed
47.
go back to reference Ratziu V, Massard J, Charlotte F, et al. Diagnostic value of biochemical markers (FibroTest-FibroSURE) for the prediction of liver fibrosis in patients with nonalcoholic fatty liver disease. BMC Gastroenterol. 2006;6:6.CrossRefPubMedPubMedCentral Ratziu V, Massard J, Charlotte F, et al. Diagnostic value of biochemical markers (FibroTest-FibroSURE) for the prediction of liver fibrosis in patients with nonalcoholic fatty liver disease. BMC Gastroenterol. 2006;6:6.CrossRefPubMedPubMedCentral
48.
go back to reference Leroy V, Sturm N, Faure P, et al. Prospective evaluation of FibroTest®, FibroMeter®, and HepaScore® for staging liver fibrosis in chronic hepatitis B: comparison with hepatitis C. J Hepatol. 2014;61:28–34.CrossRefPubMed Leroy V, Sturm N, Faure P, et al. Prospective evaluation of FibroTest®, FibroMeter®, and HepaScore® for staging liver fibrosis in chronic hepatitis B: comparison with hepatitis C. J Hepatol. 2014;61:28–34.CrossRefPubMed
49.
go back to reference Calès P, Boursier J, Oberti F, et al. FibroMeters: a family of blood tests for liver fibrosis. Gastroenterol Clin Biol. 2008;32:40–51.CrossRefPubMed Calès P, Boursier J, Oberti F, et al. FibroMeters: a family of blood tests for liver fibrosis. Gastroenterol Clin Biol. 2008;32:40–51.CrossRefPubMed
50.
go back to reference Becker L, Salameh W, Sferruzza A, et al. Validation of Hepascore, compared to simple indices of fibrosis, in US patients with chronic hepatitis C virus infection. Clin Gastroenterol Hepatol. 2009;7:696–701.CrossRefPubMed Becker L, Salameh W, Sferruzza A, et al. Validation of Hepascore, compared to simple indices of fibrosis, in US patients with chronic hepatitis C virus infection. Clin Gastroenterol Hepatol. 2009;7:696–701.CrossRefPubMed
51.
go back to reference Bonder A, Tapper EB, Afdhal NH. Contemporary assessment of hepatic fibrosis. Clin Liver Dis. 2015;19:123–134.CrossRefPubMed Bonder A, Tapper EB, Afdhal NH. Contemporary assessment of hepatic fibrosis. Clin Liver Dis. 2015;19:123–134.CrossRefPubMed
52.
go back to reference Suzuki A, Angulo P, Lymp J, Li D, Satomura S, Lindor K. Hyaluronic acid, an accurate serum marker for severe hepatic fibrosis in patients with nonalcoholic fatty liver disease. Liver Int. 2005;25:779–786.CrossRefPubMed Suzuki A, Angulo P, Lymp J, Li D, Satomura S, Lindor K. Hyaluronic acid, an accurate serum marker for severe hepatic fibrosis in patients with nonalcoholic fatty liver disease. Liver Int. 2005;25:779–786.CrossRefPubMed
53.
go back to reference Angulo P, Hui JM, Marchesini G, et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology. 2007;45:846–854.CrossRefPubMed Angulo P, Hui JM, Marchesini G, et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology. 2007;45:846–854.CrossRefPubMed
54.
go back to reference Tanwar S, Trembling PM, Guha IN, et al. Validation of terminal peptide of procollagen III for the detection and assessment of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease. Hepatology. 2013;57:103–111.CrossRefPubMed Tanwar S, Trembling PM, Guha IN, et al. Validation of terminal peptide of procollagen III for the detection and assessment of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease. Hepatology. 2013;57:103–111.CrossRefPubMed
55.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
56.
go back to reference van Werven JR, Marsman HA, Nederveen AJ, et al. Assessment of hepatic steatosis in patients undergoing liver resection: comparison of US, CT, T1-weighted dual-echo MR imaging, and point-resolved 1H MR spectroscopy. Radiology. 2010;256:159–168.CrossRefPubMed van Werven JR, Marsman HA, Nederveen AJ, et al. Assessment of hepatic steatosis in patients undergoing liver resection: comparison of US, CT, T1-weighted dual-echo MR imaging, and point-resolved 1H MR spectroscopy. Radiology. 2010;256:159–168.CrossRefPubMed
57.
go back to reference Saadeh S, Younossi ZM, Remer EM, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology. 2002;123:745–750.CrossRefPubMed Saadeh S, Younossi ZM, Remer EM, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology. 2002;123:745–750.CrossRefPubMed
58.
go back to reference 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.CrossRef 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.CrossRef
59.
go back to reference Hepburn MJ, Vos JA, Fillman EP, Lawitz EJ. The accuracy of the report of hepatic steatosis on ultrasonography in patients infected with hepatitis C in a clinical setting: a retrospective observational study. BMC Gastroenterol. 2005;5:14.CrossRefPubMedPubMedCentral Hepburn MJ, Vos JA, Fillman EP, Lawitz EJ. The accuracy of the report of hepatic steatosis on ultrasonography in patients infected with hepatitis C in a clinical setting: a retrospective observational study. BMC Gastroenterol. 2005;5:14.CrossRefPubMedPubMedCentral
60.
go back to reference Rofsky NM, Fleishaker H. CT and MRI of diffuse liver disease. Semin Ultrasound CT MR. 1995;16:16–33.CrossRefPubMed Rofsky NM, Fleishaker H. CT and MRI of diffuse liver disease. Semin Ultrasound CT MR. 1995;16:16–33.CrossRefPubMed
61.
go back to reference Borra RJH, Salo S, Dean K, et al. Nonalcoholic fatty liver disease: rapid evaluation of liver fat content with in-phase and out-of-phase MR imaging. Radiology. 2009;250:130–136.CrossRefPubMed Borra RJH, Salo S, Dean K, et al. Nonalcoholic fatty liver disease: rapid evaluation of liver fat content with in-phase and out-of-phase MR imaging. Radiology. 2009;250:130–136.CrossRefPubMed
62.
go back to reference Kim D, Kim WR, Talwalkar JA, Kim HJ, Ehman RL. Advanced fibrosis in nonalcoholic fatty liver disease: noninvasive assessment with MR elastography. Radiology. 2013;268:411–419.CrossRefPubMedPubMedCentral Kim D, Kim WR, Talwalkar JA, Kim HJ, Ehman RL. Advanced fibrosis in nonalcoholic fatty liver disease: noninvasive assessment with MR elastography. Radiology. 2013;268:411–419.CrossRefPubMedPubMedCentral
63.
go back to reference Singh S, Venkatesh SK, Wang Z, et al. Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol. 2015;13:440–451.e6.CrossRefPubMedPubMedCentral Singh S, Venkatesh SK, Wang Z, et al. Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol. 2015;13:440–451.e6.CrossRefPubMedPubMedCentral
64.
go back to reference Huwart L, Sempoux C, Vicaut E, et al. Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology. 2008;135:32–40.CrossRefPubMed Huwart L, Sempoux C, Vicaut E, et al. Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology. 2008;135:32–40.CrossRefPubMed
66.
go back to reference Wong VWS, Vergniol J, Wong GLH, et al. Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease. Hepatology. 2010;51:454–462.CrossRefPubMed Wong VWS, Vergniol J, Wong GLH, et al. Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease. Hepatology. 2010;51:454–462.CrossRefPubMed
67.
go back to reference Nobili V, Vizzutti F, Arena U, et al. Accuracy and reproducibility of transient elastography for the diagnosis of fibrosis in pediatric nonalcoholic steatohepatitis. Hepatology. 2008;48:442–448.CrossRefPubMed Nobili V, Vizzutti F, Arena U, et al. Accuracy and reproducibility of transient elastography for the diagnosis of fibrosis in pediatric nonalcoholic steatohepatitis. Hepatology. 2008;48:442–448.CrossRefPubMed
68.
go back to reference Bonder A, Afdhal N. Utilization of FibroScan in clinical practice. Curr Gastroenterol Rep. 2014;16:1–7.CrossRef Bonder A, Afdhal N. Utilization of FibroScan in clinical practice. Curr Gastroenterol Rep. 2014;16:1–7.CrossRef
69.
go back to reference Tapper EB, Castera L, Afdhal NH. FibroScan (vibration-controlled transient elastography): where does it stand in the United States practice. Clin Gastroenterol Hepatol. 2014. doi:10.1016/j.cgh.2014.04.039. Tapper EB, Castera L, Afdhal NH. FibroScan (vibration-controlled transient elastography): where does it stand in the United States practice. Clin Gastroenterol Hepatol. 2014. doi:10.​1016/​j.​cgh.​2014.​04.​039.
70.
go back to reference Cassinotto C, Lapuyade B, Mouries A, et al. Non-invasive assessment of liver fibrosis with impulse elastography: comparison of supersonic shear imaging with ARFI and FibroScan®. J Hepatol. 2014;61:550–557.CrossRefPubMed Cassinotto C, Lapuyade B, Mouries A, et al. Non-invasive assessment of liver fibrosis with impulse elastography: comparison of supersonic shear imaging with ARFI and FibroScan®. J Hepatol. 2014;61:550–557.CrossRefPubMed
71.
go back to reference Coco B, Oliveri F, Maina AM, et al. Transient elastography: a new surrogate marker of liver fibrosis influenced by major changes of transaminases. J Viral Hepat. 2007;14:360–369.CrossRefPubMed Coco B, Oliveri F, Maina AM, et al. Transient elastography: a new surrogate marker of liver fibrosis influenced by major changes of transaminases. J Viral Hepat. 2007;14:360–369.CrossRefPubMed
72.
go back to reference Kim KM, Choi WB, Park SH, et al. Diagnosis of hepatic steatosis and fibrosis by transient elastography in asymptomatic healthy individuals: a prospective study of living related potential liver donors. J Gastroenterol. 2007;42:382–388.CrossRefPubMed Kim KM, Choi WB, Park SH, et al. Diagnosis of hepatic steatosis and fibrosis by transient elastography in asymptomatic healthy individuals: a prospective study of living related potential liver donors. J Gastroenterol. 2007;42:382–388.CrossRefPubMed
73.
go back to reference Castéra L, Vergniol J, Foucher J, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology. 2005;128:343–350.CrossRefPubMed Castéra L, Vergniol J, Foucher J, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology. 2005;128:343–350.CrossRefPubMed
74.
go back to reference Mueller S, Millonig G, Sarovska L, et al. Increased liver stiffness in alcoholic liver disease: differentiating fibrosis from steatohepatitis. World J Gastroenterol. 2010;16:966–972.CrossRefPubMedPubMedCentral Mueller S, Millonig G, Sarovska L, et al. Increased liver stiffness in alcoholic liver disease: differentiating fibrosis from steatohepatitis. World J Gastroenterol. 2010;16:966–972.CrossRefPubMedPubMedCentral
75.
go back to reference Pais R, Lupşor M, Poantă L, et al. Liver biopsy versus noninvasive methods—fibroscan and fibrotest in the diagnosis of nonalcoholic fatty liver disease: a review of the literature. Rom J Intern Med. 2009;47:331–340.PubMed Pais R, Lupşor M, Poantă L, et al. Liver biopsy versus noninvasive methods—fibroscan and fibrotest in the diagnosis of nonalcoholic fatty liver disease: a review of the literature. Rom J Intern Med. 2009;47:331–340.PubMed
76.
go back to reference Myers RP, Pomier-Layrargues G, Kirsch R, et al. Feasibility and diagnostic performance of the FibroScan XL probe for liver stiffness measurement in overweight and obese patients. Hepatology. 2012;55:199–208.CrossRefPubMed Myers RP, Pomier-Layrargues G, Kirsch R, et al. Feasibility and diagnostic performance of the FibroScan XL probe for liver stiffness measurement in overweight and obese patients. Hepatology. 2012;55:199–208.CrossRefPubMed
77.
go back to reference Nahon P, Kettaneh A, Tengher-Barna I, et al. Assessment of liver fibrosis using transient elastography in patients with alcoholic liver disease. J Hepatol. 2008;49:1062–1068.CrossRefPubMed Nahon P, Kettaneh A, Tengher-Barna I, et al. Assessment of liver fibrosis using transient elastography in patients with alcoholic liver disease. J Hepatol. 2008;49:1062–1068.CrossRefPubMed
78.
go back to reference Fraquelli M, Rigamonti C, Casazza G, et al. Etiology-related determinants of liver stiffness values in chronic viral hepatitis B or C. J Hepatol. 2011;54:621–628.CrossRefPubMed Fraquelli M, Rigamonti C, Casazza G, et al. Etiology-related determinants of liver stiffness values in chronic viral hepatitis B or C. J Hepatol. 2011;54:621–628.CrossRefPubMed
79.
go back to reference Arena U, Vizzutti F, Corti G, et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology. 2008;47:380–384.CrossRefPubMed Arena U, Vizzutti F, Corti G, et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology. 2008;47:380–384.CrossRefPubMed
80.
go back to reference Wong VWS, Vergniol J, Wong GLH, et al. Liver stiffness measurement using XL probe in patients with nonalcoholic fatty liver disease. Am J Gastroenterol. 2012;107:1862–1871.CrossRefPubMed Wong VWS, Vergniol J, Wong GLH, et al. Liver stiffness measurement using XL probe in patients with nonalcoholic fatty liver disease. Am J Gastroenterol. 2012;107:1862–1871.CrossRefPubMed
81.
go back to reference Millonig G, Reimann FM, Friedrich S, et al. Extrahepatic cholestasis increases liver stiffness (fibroScan) irrespective of fibrosis. Hepatology. 2008;48:1718–1723.CrossRefPubMed Millonig G, Reimann FM, Friedrich S, et al. Extrahepatic cholestasis increases liver stiffness (fibroScan) irrespective of fibrosis. Hepatology. 2008;48:1718–1723.CrossRefPubMed
82.
go back to reference Millonig G, Friedrich S, Adolf S, et al. Liver stiffness is directly influenced by central venous pressure. J Hepatol. 2010;52:206–210.CrossRefPubMed Millonig G, Friedrich S, Adolf S, et al. Liver stiffness is directly influenced by central venous pressure. J Hepatol. 2010;52:206–210.CrossRefPubMed
83.
go back to reference Goertz RS, Egger C, Neurath MF, Strobel D. Impact of food intake, ultrasound transducer, breathing maneuvers and body position on acoustic radiation force impulse (ARFI) elastometry of the liver. Ultraschall Med. 2012;33:380–385.CrossRefPubMed Goertz RS, Egger C, Neurath MF, Strobel D. Impact of food intake, ultrasound transducer, breathing maneuvers and body position on acoustic radiation force impulse (ARFI) elastometry of the liver. Ultraschall Med. 2012;33:380–385.CrossRefPubMed
84.
go back to reference Tsochatzis EA, Gurusamy KS, Ntaoula S, Cholongitas E, Davidson BR, Burroughs AK. Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol. 2015;54:650–659.CrossRef Tsochatzis EA, Gurusamy KS, Ntaoula S, Cholongitas E, Davidson BR, Burroughs AK. Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol. 2015;54:650–659.CrossRef
85.
go back to reference Crespo G, Fernández-Varo G, Mariño Z, et al. ARFI, FibroScan®, ELF, and their combinations in the assessment of liver fibrosis: a prospective study. J Hepatol. 2012;57:281–287.CrossRefPubMed Crespo G, Fernández-Varo G, Mariño Z, et al. ARFI, FibroScan®, ELF, and their combinations in the assessment of liver fibrosis: a prospective study. J Hepatol. 2012;57:281–287.CrossRefPubMed
86.
go back to reference Rotman Y, Koh C, Zmuda JM, Kleiner DE, Liang TJ. The association of genetic variability in patatin-like phospholipase domain-containing protein 3 (PNPLA3) with histological severity of nonalcoholic fatty liver disease. Hepatology. 2010;52:894–903.CrossRefPubMedPubMedCentral Rotman Y, Koh C, Zmuda JM, Kleiner DE, Liang TJ. The association of genetic variability in patatin-like phospholipase domain-containing protein 3 (PNPLA3) with histological severity of nonalcoholic fatty liver disease. Hepatology. 2010;52:894–903.CrossRefPubMedPubMedCentral
87.
go back to reference Valenti L, Al-Serri A, Daly AK, et al. Homozygosity for the patatin-like phospholipase-3/adiponutrin I148M polymorphism influences liver fibrosis in patients with nonalcoholic fatty liver disease. Hepatology. 2010;51:1209–1217.CrossRefPubMed Valenti L, Al-Serri A, Daly AK, et al. Homozygosity for the patatin-like phospholipase-3/adiponutrin I148M polymorphism influences liver fibrosis in patients with nonalcoholic fatty liver disease. Hepatology. 2010;51:1209–1217.CrossRefPubMed
88.
go back to reference Dongiovanni P, Romeo S, Valenti L. Genetic factors in the pathogenesis of nonalcoholic fatty liver and steatohepatitis. Biomed Res Int. 2015;2015:460190.CrossRefPubMedPubMedCentral Dongiovanni P, Romeo S, Valenti L. Genetic factors in the pathogenesis of nonalcoholic fatty liver and steatohepatitis. Biomed Res Int. 2015;2015:460190.CrossRefPubMedPubMedCentral
89.
go back to reference Liu Y-L, Patman GL, Leathart JBS, et al. Carriage of the PNPLA3 rs738409 C>G polymorphism confers an increased risk of nonalcoholic fatty liver disease associated hepatocellular carcinoma. J Hepatol. 2015;61:75–81.CrossRef Liu Y-L, Patman GL, Leathart JBS, et al. Carriage of the PNPLA3 rs738409 C>G polymorphism confers an increased risk of nonalcoholic fatty liver disease associated hepatocellular carcinoma. J Hepatol. 2015;61:75–81.CrossRef
90.
go back to reference Liu Y-L, Reeves HL, Burt AD, et al. TM6SF2 rs58542926 influences hepatic fibrosis progression in patients with nonalcoholic fatty liver disease. Nat Commun. 2014. doi:10.1038/ncomms5309. Liu Y-L, Reeves HL, Burt AD, et al. TM6SF2 rs58542926 influences hepatic fibrosis progression in patients with nonalcoholic fatty liver disease. Nat Commun. 2014. doi:10.​1038/​ncomms5309.
91.
go back to reference Sookoian S, Castaño GO, Scian R, et al. Genetic variation in transmembrane 6 superfamily member 2 and the risk of nonalcoholic fatty liver disease and histological disease severity. Hepatology. 2015;61:515–525.CrossRefPubMed Sookoian S, Castaño GO, Scian R, et al. Genetic variation in transmembrane 6 superfamily member 2 and the risk of nonalcoholic fatty liver disease and histological disease severity. Hepatology. 2015;61:515–525.CrossRefPubMed
92.
go back to reference Calès P, Lainé F, Boursier J, et al. Comparison of blood tests for liver fibrosis specific or not to NAFLD. J Hepatol. 2009;50:165–173.CrossRefPubMed Calès P, Lainé F, Boursier J, et al. Comparison of blood tests for liver fibrosis specific or not to NAFLD. J Hepatol. 2009;50:165–173.CrossRefPubMed
93.
go back to reference Shah AG, Lydecker A, Murray K, Tetri BN, Contos MJ, Sanyal AJ. Comparison of noninvasive markers of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2009;7:1104–1112.CrossRefPubMedPubMedCentral Shah AG, Lydecker A, Murray K, Tetri BN, Contos MJ, Sanyal AJ. Comparison of noninvasive markers of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2009;7:1104–1112.CrossRefPubMedPubMedCentral
94.
go back to reference Vallet-Pichard A, Mallet V, Nalpas B, et al. FIB-4: An inexpensive and accurate marker of fibrosis in HCV infection. Comparison with liver biopsy and FibroTest. Hepatology. 2007;46:32–36.CrossRefPubMed Vallet-Pichard A, Mallet V, Nalpas B, et al. FIB-4: An inexpensive and accurate marker of fibrosis in HCV infection. Comparison with liver biopsy and FibroTest. Hepatology. 2007;46:32–36.CrossRefPubMed
Metadata
Title
Fibrosis Assessment in Nonalcoholic Fatty Liver Disease (NAFLD) in 2016
Authors
Dharmesh H. Kaswala
Michelle Lai
Nezam H. Afdhal
Publication date
01-05-2016
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 5/2016
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-016-4079-4

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