The Relevance of Noninvasive Tools To Assess Fibrosis in Non-Alcoholic Fatty Liver Disease

Author(s): Grazia Pennisi*, Ciro Celsa, Antonina Giammanco, Federica Spatola, Salvatore Petta*

Journal Name: Current Pharmaceutical Design

Volume 26 , Issue 32 , 2020


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Abstract:

Non-alcoholic fatty liver disease (NAFLD) is a growing cause of chronic liver diseases worldwide, involving about 25% of people. NAFLD incorporates a large spectrum of pathological conditions, from simple steatosis to non-alcoholic steatohepatitis (NASH), cirrhosis and its complications include hepatic decompensation and hepatocellular carcinoma (HCC). This progression occurs, over many years, in an asymptomatic way, until advanced fibrosis appears. Thus, the differentiation of NASH from simple steatosis and identification of advanced hepatic fibrosis are key issues. To date, the histological assessment of fibrosis with liver biopsy is the gold standard, but obviously, invasiveness is the greater threshold. In addition, rare but potentially life-threatening complications, poor acceptability, sampling variability and cost maybe restrict its use. Furthermore, due to the epidemic of NAFLD worldwide and several limitations of liver biopsy evaluation, noninvasive assessment tools to detect fibrosis in NAFLD patients are needed.

Keywords: NAFLD, NASH, fibrosis, non-invasive tests, FibroScan, MRE, MRI, biomarkers.

[1]
Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 2016; 64(1): 73-84.
[http://dx.doi.org/10.1002/hep.28431] [PMID: 26707365]
[2]
Akbari M, Nayeri H, Nasri H. Relationship of fetuin-A with nonalcoholic fatty liver. J Prev Epidemiol 2018; 3(2) e04
[3]
Cohen JC, Boerwinkle E, Mosley TH Jr, Hobbs HH. Sequence variations in PCSK9, low LDL, and protection against coronary heart disease. N Engl J Med 2006; 354(12): 1264-72.
[http://dx.doi.org/10.1056/NEJMoa054013] [PMID: 16554528]
[4]
Adams LA, Anstee QM, Tilg H, Targher G. Non-alcoholic fatty liver disease and its relationship with cardiovascular disease and other extrahepatic diseases. Gut 2017; 66(6): 1138-53.
[http://dx.doi.org/10.1136/gutjnl-2017-313884] [PMID: 28314735]
[5]
Ekstedt M, Hagström H, Nasr P, 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(5): 1547-54.
[http://dx.doi.org/10.1002/hep.27368] [PMID: 25125077]
[6]
Zhou Y, Orešič M, Leivonen M, et al. Noninvasive detection of nonalcoholic steatohepatitis using clinical markers and circulating levels of lipids and metabolites. Clin Gastroenterol Hepatol 2016; 14(10): 1463-1472.e6.
[http://dx.doi.org/10.1016/j.cgh.2016.05.046] [PMID: 27317851]
[7]
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(4): 1072-8.
[http://dx.doi.org/10.1002/hep.23050] [PMID: 19585618]
[8]
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(4): 846-54.
[http://dx.doi.org/10.1002/hep.21496] [PMID: 17393509]
[9]
McPherson S, Stewart SF, Henderson E, Burt AD, Day CP. Simple non-invasive fibrosis scoring systems can reliably exclude advanced fibrosis in patients with non-alcoholic fatty liver disease. Gut 2010; 59(9): 1265-9.
[http://dx.doi.org/10.1136/gut.2010.216077] [PMID: 20801772]
[10]
Calès P, Lainé F, Boursier J, et al. Comparison of blood tests for liver fibrosis specific or not to NAFLD. J Hepatol 2009; 50(1): 165-73.
[http://dx.doi.org/10.1016/j.jhep.2008.07.035] [PMID: 18977552]
[11]
Fujii H, Enomoto M, Fukushima W, Tamori A, Sakaguchi H, Kawada N. Applicability of BARD score to Japanese patients with NAFLD. Gut 2009; 58(11): 1566-7.
[http://dx.doi.org/10.1136/gut.2009.182758] [PMID: 19834122]
[12]
Wong VW, Wong GL, Chim AM, et al. Validation of the NAFLD fibrosis score in a Chinese population with low prevalence of advanced fibrosis. Am J Gastroenterol 2008; 103(7): 1682-8.
[http://dx.doi.org/10.1111/j.1572-0241.2008.01933.x] [PMID: 18616651]
[13]
Qureshi K, Clements RH, Abrams GA. The utility of the “NAFLD fibrosis score” in morbidly obese subjects with NAFLD. Obes Surg 2008; 18(3): 264-70.
[http://dx.doi.org/10.1007/s11695-007-9295-8] [PMID: 18214632]
[14]
Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G. Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: A meta-analysis. Hepatology 2017; 66(5): 1486-501.
[http://dx.doi.org/10.1002/hep.29302] [PMID: 28586172]
[15]
Fracanzani AL, Valenti L, Bugianesi E, et al. Risk of nonalcoholic steatohepatitis and fibrosis in patients with nonalcoholic fatty liver disease and low visceral adiposity. J Hepatol 2011; 54(6): 1244-9.
[http://dx.doi.org/10.1016/j.jhep.2010.09.037] [PMID: 21145841]
[16]
Sumida Y, Yoneda M, Hyogo H, et al. Japan Study Group of Nonalcoholic Fatty Liver Disease (JSG-NAFLD). Validation of the FIB4 index in a Japanese nonalcoholic fatty liver disease population. BMC Gastroenterol 2012; 12: 2.
[http://dx.doi.org/10.1186/1471-230X-12-2] [PMID: 22221544]
[17]
McPherson S, Hardy T, Dufour JF, et al. Age as a confounding factor for the accurate non-invasive diagnosis of advanced NAFLD fibrosis. Am J Gastroenterol 2017; 112(5): 740-51.
[http://dx.doi.org/10.1038/ajg.2016.453] [PMID: 27725647]
[18]
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(10): 1441-7.
[http://dx.doi.org/10.1136/gut.2007.146019] [PMID: 18390575]
[19]
Raszeja-Wyszomirska J, Szymanik B, Lawniczak M, et al. Validation of the BARD scoring system in Polish patients with nonalcoholic fatty liver disease (NAFLD). BMC Gastroenterol 2010; 10.
[20]
Loaeza-del-Castillo A, Paz-Pineda F, Oviedo-Cárdenas E, Sánchez-Avila F, Vargas-Vorácková F. AST to platelet ratio index (APRI) for the noninvasive evaluation of liver fibrosis. Ann Hepatol 2008; 7(4): 350-7.
[http://dx.doi.org/10.1016/S1665-2681(19)31836-8] [PMID: 19034235]
[21]
Siddiqui MS, Yamada G, Vuppalanchi R, et al. NASH clinical research network. diagnostic accuracy of noninvasive fibrosis models to detect change in fibrosis stage. Clin Gastroenterol Hepatol 2019; 17(9): 1877-85.e5. Epub ahead of print
[http://dx.doi.org/10.1016/j.cgh.2018.12.031] [PMID: 30616027]
[22]
Siddiqui MS, Patidar KR, Boyett S, Luketic VA, Puri P, Sanyal AJ. Performance of non-invasive models of fibrosis in predicting mild to moderate fibrosis in patients with non-alcoholic fatty liver disease. Liver Int 2016; 36(4): 572-9.
[http://dx.doi.org/10.1111/liv.13054] [PMID: 26713759]
[23]
Boursier J, de Ledinghen V, Leroy V, et al. A stepwise algorithm using an at-a-glance first-line test for the non-invasive diagnosis of advanced liver fibrosis and cirrhosis. J Hepatol 2017; 66(6): 1158-65.
[http://dx.doi.org/10.1016/j.jhep.2017.01.003] [PMID: 28088581]
[24]
Demir M, Lang S, Schlattjan M, et al. NIKEI: a new inexpensive and non-invasive scoring system to exclude advanced fibrosis in patients with NAFLD. PLoS One 2013; 8(3) e58360
[http://dx.doi.org/10.1371/journal.pone.0058360] [PMID: 23555578]
[25]
Ampuero J, Aller R, Gallego-Durán R, et al. Hepamet Score: a new non-invasive method for NAFLD-related fibrosis screening in clinical practiceJournal of Hepatology 2018; 68: S65-104.
[26]
Angulo P, Bugianesi E, Bjornsson ES, et al. Simple noninvasive systems predict long-term outcomes of patients with nonalcoholic fatty liver disease. Gastroenterology 2013; 145(4): 782-9.
[http://dx.doi.org/10.1053/j.gastro.2013.06.057]
[27]
Shah AG, Lydecker A, Murray K, Tetri BN, Contos MJ, Sanyal AJ. Nash Clinical Research Network. Comparison of noninvasive markers of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2009; 7(10): 1104-12.
[http://dx.doi.org/10.1016/j.cgh.2009.05.033] [PMID: 19523535]
[28]
Poynard T, Morra R, Halfon P, et al. Meta-analyses of FibroTest diagnostic value in chronic liver disease. BMC Gastroenterol 2007; 7: 40.
[http://dx.doi.org/10.1186/1471-230X-7-40] [PMID: 17937811]
[29]
Poynard T, Lassailly G, Diaz E, et al. FLIP consortium. Performance of biomarkers FibroTest, ActiTest, SteatoTest, and NashTest in patients with severe obesity: Meta analysis of individual patient data. PLoS One 2012; 7(3) e30325
[http://dx.doi.org/10.1371/journal.pone.0030325] [PMID: 22431959]
[30]
Boursier J, Vergniol J, Guillet A, et al. Diagnostic accuracy and prognostic significance of blood fibrosis tests and liver stiffness measurement by FibroScan in non-alcoholic fatty liver disease. J Hepatol 2016; 65(3): 570-8.
[http://dx.doi.org/10.1016/j.jhep.2016.04.023] [PMID: 27151181]
[31]
Munteanu M, Tiniakos D, Anstee Q, et al. FLIP Consortium and the FibroFrance Group. Diagnostic performance of FibroTest, SteatoTest and ActiTest in patients with NAFLD using the SAF score as histological reference. Aliment Pharmacol Ther 2016; 44(8): 877-89.
[http://dx.doi.org/10.1111/apt.13770] [PMID: 27549244]
[32]
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(2): 455-60.
[http://dx.doi.org/10.1002/hep.21984] [PMID: 18038452]
[33]
Yoneda M, Mawatari H, Fujita K, et al. Type IV collagen 7s domain is an independent clinical marker of the severity of fibrosis in patients with nonalcoholic steatohepatitis before the cirrhotic stage. J Gastroenterol 2007; 42(5): 375-81.
[http://dx.doi.org/10.1007/s00535-007-2014-3] [PMID: 17530362]
[34]
Kaneda H, Hashimoto E, Yatsuji S, Tokushige K, Shiratori K. Hyaluronic acid levels can predict severe fibrosis and platelet counts can predict cirrhosis in patients with nonalcoholic fatty liver disease. J Gastroenterol Hepatol 2006; 21(9): 1459-65.
[http://dx.doi.org/10.1111/j.1440-1746.2006.04447.x] [PMID: 16911693]
[35]
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 non-alcoholic fatty liver disease. Liver Int 2005; 25(4): 779-86.
[http://dx.doi.org/10.1111/j.1478-3231.2005.01064.x] [PMID: 15998429]
[36]
Lesmana CR, Hasan I, Budihusodo U, et al. Diagnostic value of a group of biochemical markers of liver fibrosis in patients with non-alcoholic steatohepatitis. J Dig Dis 2009; 10(3): 201-6.
[http://dx.doi.org/10.1111/j.1751-2980.2009.00386.x] [PMID: 19659788]
[37]
Hayes CN, Chayama K. MicroRNAs as biomarkers for liver disease and hepatocellular carcinoma. Int J Mol Sci 2016; 17(3): 280.
[http://dx.doi.org/10.3390/ijms17030280] [PMID: 26927063]
[38]
Lambrecht J, Verhulst S, Reynaert H, van Grunsven LA. The miRFIB-Score: A serological miRNA-based scoring algorithm for the diagnosis of significant liver fibrosis. Cells 2019; 8(9) e1003
[http://dx.doi.org/10.3390/cells8091003] [PMID: 31470644]
[39]
Daniels SJ, Leeming DJ, Eslam M, et al. ADAPT: An algorithm incorporating PRO-C3 accurately identifies patients with NAFLD and advanced fibrosis. Hepatology 2019; 69(3): 1075-86.
[http://dx.doi.org/10.1002/hep.30163] [PMID: 30014517]
[40]
Ratziu V, Massard J, Charlotte F, 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 2006; 6: 6.
[41]
Adams LA, George J, Bugianesi E, et al. Complex non-invasive fibrosis models are more accurate than simple models in non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2011; 26(10): 1536-43.
[42]
Boursier J, Anty R, Vonghia L, et al. Screening for therapeutic trials and treatment indication in clinical practice: MACK-3, a new blood test for the diagnosis of fibrotic NASH. Aliment Pharmacol Ther 2018; 47(10): 1387-96.
[http://dx.doi.org/10.1111/apt.14621] [PMID: 29577364]
[43]
Wong VW, Vergniol J, Wong GL, et al. Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease. Hepatology 2010; 51(2): 454-62.
[http://dx.doi.org/10.1002/hep.23312] [PMID: 20101745]
[44]
Yoneda M, Yoneda M, Mawatari H, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with nonalcoholic fatty liver disease (NAFLD). Dig Liver Dis 2008; 40(5): 371-8.
[http://dx.doi.org/10.1016/j.dld.2007.10.019] [PMID: 18083083]
[45]
Gaia S, Carenzi S, Barilli AL, et al. Reliability of transient elastography for the detection of fibrosis in non-alcoholic fatty liver disease and chronic viral hepatitis. J Hepatol 2011; 54(1): 64-71.
[http://dx.doi.org/10.1016/j.jhep.2010.06.022] [PMID: 20932598]
[46]
Petta S, Di Marco V, Cammà C, Butera G, Cabibi D, Craxì A. Reliability of liver stiffness measurement in non-alcoholic fatty liver disease: the effects of body mass index. Aliment Pharmacol Ther 2011; 33(12): 1350-60.
[http://dx.doi.org/10.1111/j.1365-2036.2011.04668.x] [PMID: 21517924]
[47]
Musso G, Gambino R, Cassader M, Pagano G. Meta-analysis: natural history of non-alcoholic fatty liver disease (NAFLD) and diagnostic accuracy of non-invasive tests for liver disease severity. Ann Med 2011; 43(8): 617-49.
[http://dx.doi.org/10.3109/07853890.2010.518623] [PMID: 21039302]
[48]
Petta S, Maida M, Macaluso FS, et al. The severity of steatosis influences liver stiffness measurement in patients with non-alcoholic fatty liver disease. Hepatology 2015. Epub ahead of print
[49]
Petta S, Wong VW, Cammà C, et al. Improved noninvasive prediction of liver fibrosis by liver stiffness measurement in patients with nonalcoholic fatty liver disease accounting for controlled attenuation parameter values. Hepatology 2017; 65(4): 1145-55.
[http://dx.doi.org/10.1002/hep.28843] [PMID: 27639088]
[50]
Eddowes PJ, Sasso M, Allison M, et al. Accuracy of FibroScan controlled attenuation parameter and liver stiffness measurement in assessing steatosis and fibrosis in patients with nonalcoholic fatty liver disease. Gastroenterology 2019; 156(6): 1717-30.
[http://dx.doi.org/10.1053/j.gastro.2019.01.042] [PMID: 30689971]
[51]
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(1): 199-208.
[http://dx.doi.org/10.1002/hep.24624] [PMID: 21898479]
[52]
de Lédinghen V, Wong VW, Vergniol J, et al. Diagnosis of liver fibrosis and cirrhosis using liver stiffness measurement: comparison between M and XL probe of FibroScan®. J Hepatol 2012; 56(4): 833-9.
[http://dx.doi.org/10.1016/j.jhep.2011.10.017] [PMID: 22173167]
[53]
Vuppalanchi R, Siddiqui MS, Van Natta ML, et al. NASH Clinical Research Network. Performance characteristics of vibration-controlled transient elastography for evaluation of nonalcoholic fatty liver disease. Hepatology 2018; 67(1): 134-44.
[http://dx.doi.org/10.1002/hep.29489] [PMID: 28859228]
[54]
Wong VW, Irles M, Wong GL, et al. Unified interpretation of liver stiffness measurement by M and XL probes in non-alcoholic fatty liver disease. Gut 2019; 68(11): 2057-64.
[http://dx.doi.org/10.1136/gutjnl-2018-317334] [PMID: 30658997]
[55]
Petta S, Wai-Sun Wong V, Bugianesi E, et al. Impact of obesity and alanine aminotransferase levels on the diagnostic accuracy for advanced liver fibrosis of noninvasive tools in patients with nonalcoholic fatty liver disease. Am J Gastroenterol 2019; 114(6): 916-28.
[http://dx.doi.org/10.14309/ajg.0000000000000153] [PMID: 31169533]
[56]
Boursier J, Guillaume M, Leroy V, et al. New sequential combinations of non-invasive fibrosis tests provide an accurate diagnosis of advanced fibrosis in NAFLD. J Hepatol 2019; 71(2): 389-96.
[http://dx.doi.org/10.1016/j.jhep.2019.04.020] [PMID: 31102719]
[57]
Anstee QM, Lawitz EJ, Alkhouri N, et al. Noninvasive tests accurately identify advanced fibrosis due to NASH: Baseline data from the STELLAR Trials. Hepatology 2019; 70(5): 1521-30.
[http://dx.doi.org/10.1002/hep.30842] [PMID: 31271665]
[58]
Bertot LC, Jeffrey GP, de Boer B, et al. Diabetes impacts prediction of cirrhosis and prognosis by non-invasive fibrosis models in non-alcoholic fatty liver disease. Liver Int 2018; 38(10): 1793-802.
[http://dx.doi.org/10.1111/liv.13739] [PMID: 29575516]
[59]
Lupșor-Platon M, Badea R, Gersak M, et al. Noninvasive assessment of liver diseases using 2D shear wave elastography. J Gastrointestin Liver Dis 2016; 25(4): 525-32.
[http://dx.doi.org/10.15403/jgld.2014.1121.254.lup] [PMID: 27981309]
[60]
Barr RG. Shear wave liver elastography. Abdom Radiol (NY) 2018; 43(4): 800-7.
[http://dx.doi.org/10.1007/s00261-017-1375-1] [PMID: 29116341]
[61]
Fang C, Konstantatou E, Romanos O, Yusuf GT, Quinlan DJ, Sidhu PS. Reproducibility of 2-dimensional shear wave elastography assessment of the liver. J Ultrasound Med 2017; 36(8): 1563-9.
[http://dx.doi.org/10.7863/ultra.16.07018] [PMID: 28370146]
[62]
Piscaglia F, Salvatore V, Mulazzani L, Cantisani V, Schiavone C. Ultrasound shear wave elastography for liver disease. A critical appraisal of the many actors on the stage. Ultraschall Med 2016; 37(1): 1-5.
[http://dx.doi.org/10.1055/s-0035-1567037] [PMID: 26871407]
[63]
Foucher J, Chanteloup E, Vergniol J, et al. Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut 2006; 55(3): 403-8.
[http://dx.doi.org/10.1136/gut.2005.069153] [PMID: 16020491]
[64]
Ferraioli G, Tinelli C, Lissandrin R, et al. Point shear wave elastography method for assessing liver stiffness. World J Gastroenterol 2014; 20(16): 4787-96.
[http://dx.doi.org/10.3748/wjg.v20.i16.4787] [PMID: 24782633]
[65]
Mulazzani L, Salvatore V, Ravaioli F, et al. Point shear wave ultrasound elastography with Esaote compared to real-time 2D shear wave elastography with supersonic imagine for the quantification of liver stiffness. J Ultrasound 2017; 20(3): 213-25.
[http://dx.doi.org/10.1007/s40477-017-0260-7] [PMID: 28900522]
[66]
Joo I, Kim SY, Park HS, Lee ES, Kang HJ, Lee JM. Validation of a new point shear-wave elastography method for noninvasine assessment of liver fibrosis: a prospective multicenter study. Korean J Radiol 2019; 20(11): 1527-35.
[http://dx.doi.org/10.3348/kjr.2019.0109] [PMID: 31606957]
[67]
Gani RA, Hasan I, Sanityoso A, et al. Evaluation of acoustic radioation force impulse (ARFI) for fibrosis staging in chronic liver diseases. Acta Med Indones - Indones. J Intern Med 2017; 19(2): 128-35.
[68]
Elhosary YA, Saleh SM, Ezzat WM, Clevert DA. Diagnostic accuracy of acoustic radiation force impulse (ARFI) in diagnosis of liver fibrosis among Egyptian patients with chronic HCV infection. Open Access Maced J Med Sci 2016; 4(3): 374-80.
[http://dx.doi.org/10.3889/oamjms.2016.064] [PMID: 27703558]
[69]
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(2): 281-7.
[http://dx.doi.org/10.1016/j.jhep.2012.03.016] [PMID: 22521355]
[70]
Cassinotto C, Boursier J, de Lédinghen V, et al. Liver stiffness in nonalcoholic fatty liver disease: A comparison of supersonic shear imaging, FibroScan, and ARFI with liver biopsy. Hepatology 2016; 63(6): 1817-27.
[http://dx.doi.org/10.1002/hep.28394] [PMID: 26659452]
[71]
Palmeri ML, Wang MH, Rouze NC, et al. Noninvasive evaluation of hepatic fibrosis using acoustic radiation force-based shear stiffness in patients with nonalcoholic fatty liver disease. J Hepatol 2011; 55(3): 666-72.
[http://dx.doi.org/10.1016/j.jhep.2010.12.019] [PMID: 21256907]
[72]
Cassinotto C, Lapuyade B, Aït-Ali A, et al. Liver fibrosis: noninvasive assessment with acoustic radiation force impulse elastography--comparison with FibroScan M and XL probes and FibroTest in patients with chronic liver disease. Radiology 2013; 269(1): 283-92.
[http://dx.doi.org/10.1148/radiol.13122208] [PMID: 23630312]
[73]
Piscaglia F, Salvatore V, Di Donato R, et al. Accuracy of VirtualTouch Acoustic Radiation Force Impulse (ARFI) imaging for the diagnosis of cirrhosis during liver ultrasonography. Ultraschall Med 2011; 32(2): 167-75.
[http://dx.doi.org/10.1055/s-0029-1245948] [PMID: 21321842]
[74]
Venkatesh SK, Yin M, Ehman RL. Magnetic resonance elastography of liver: technique, analysis, and clinical applications. J Magn Reson Imaging 2013; 37(3): 544-55.
[http://dx.doi.org/10.1002/jmri.23731] [PMID: 23423795]
[75]
Cui J, Ang B, Haufe W, 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 2015; 41(12): 1271-80.
[http://dx.doi.org/10.1111/apt.13196] [PMID: 25873207]
[76]
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: 440-51.
[http://dx.doi.org/10.1016/j.cgh.2014.09.046]
[77]
Loomba R, Wolfson T, Ang B, et al. Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study. Hepatology 2014; 60(6): 1920-8.
[http://dx.doi.org/10.1002/hep.27362] [PMID: 25103310]
[78]
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(2): 411-9.
[http://dx.doi.org/10.1148/radiol.13121193] [PMID: 23564711]
[79]
Singh S, Venkatesh SK, Loomba R, 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 2015; 1431-40.
[PMID: 26314479]
[80]
Chen J, Talwalkar JA, Yin M, Glaser KJ, Sanderson SO, Ehman RL. Early detection of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease by using MR elastography. Radiology 2011; 259(3): 749-56.
[http://dx.doi.org/10.1148/radiol.11101942] [PMID: 21460032]
[81]
Loomba R, Cui J, Wolfson T, et al. Novel 3D magnetic resonance elastography for the noninvasive diagnosis of advanced fibrosis in NAFLD: A prospective study. Am J Gastroenterol 2016; 111(7): 986-94.
[http://dx.doi.org/10.1038/ajg.2016.65] [PMID: 27002798]
[82]
Runge JH, Bohte AE, Verheij J, et al. Comparison of interobserver agreement of magnetic resonance elastography with histopathological staging of liver fibrosis. Abdom Imaging 2014; 39(2): 283-90.
[http://dx.doi.org/10.1007/s00261-013-0063-z] [PMID: 24366108]
[83]
Dulai PS, Sirlin CB, Loomba R. MRI and MRE for non-invasive quantitative assessment of hepatic steatosis and fibrosis in NAFLD and NASH: Clinical trials to clinical practice. J Hepatol 2016; 65(5): 1006-16.
[84]
Asrani SK. Incorporation of noninvasive measures of liver fibrosis into clinical practice: diagnosis and prognosis. Clin Gastroenterol Hepatol 2015; 2190-04.
[85]
Imajo K, Kessoku T, Honda Y, et al. Magnetic resonance imaging more accurately classifies steatosis and fibrosis in patients with nonalcoholic fatty liver disease than transient Elastography Gastroenterology 2016; 150 626-37.
[http://dx.doi.org/10.1053/j.gastro.2015.11.048]
[86]
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 2011; 54(4): 650-9.
[http://dx.doi.org/10.1016/j.jhep.2010.07.033] [PMID: 21146892]
[87]
Tsochatzis EA, Manousou P, Fede G, Dhillon AP, Burroughs AK. Validating non-invasive markers of fibrosis: the need for a new histological reference standard. Gut 2011; 60(10): 1442-3.
[http://dx.doi.org/10.1136/gut.2010.229484] [PMID: 21159895]
[88]
Nierhoff J, Chávez Ortiz AA, Herrmann E, Zeuzem S, Friedrich-Rust M. The efficiency of acoustic radiation force impulse imaging for the staging of liver fibrosis: a meta-analysis. Eur Radiol 2013; 23(11): 3040-53.
[http://dx.doi.org/10.1007/s00330-013-2927-6] [PMID: 23801420]
[89]
Cui J, Philo L, Nguyen P, et al. Sitagliptin versus placebo in the treatment of nonalcoholic fatty liver disease: A randomized controlled trial. J Hepatol 2016.
[http://dx.doi.org/10.1016/j.jhep.2016.04.021]
[90]
Castera L. Noninvasive methods to assess liver disease in patients with hepatitis B or C Gastroenterology 2012; 142: 1293-302.
[91]
Castéra L, Foucher J, Bernard PH, et al. Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology 2010; 51(3): 828-35.
[http://dx.doi.org/10.1002/hep.23425] [PMID: 20063276]
[92]
Bota S, Sporea I, Sirli R, et al. Factors associated with the impossibility to obtain reliable liver stiffness measurements by means of Acoustic Radiation Force Impulse (ARFI) elastography--analysis of a cohort of 1,031 subjects. Eur J Radiol 2014; 83(2): 268-72.
[http://dx.doi.org/10.1016/j.ejrad.2013.11.019] [PMID: 24360231]
[93]
Castera L, Pinzani M. Non-invasive assessment of liver fibrosis: are we ready? Lancet 2010; 375(9724): 1419-20.
[http://dx.doi.org/10.1016/S0140-6736(09)62195-4] [PMID: 20417845]
[94]
Talwalkar JA. Elastography for detecting hepatic fibrosis: options and considerations. Gastroenterology 2008; 135(1): 299-302.
[http://dx.doi.org/10.1053/j.gastro.2008.05.038] [PMID: 18555023]
[95]
Grădinaru-Taşcău O, Sporea I, Bota S, et al. Does experience play a role in the ability to perform liver stiffness measurements by means of supersonic shear imaging (SSI)? Med Ultrason 2013; 15(3): 180-3.
[http://dx.doi.org/10.11152/mu.2013.2066.153.ogt1is2] [PMID: 23979612]
[96]
European Association for Study of Liver. Asociacion Latinoamericana para el Estudio del Higado. EASL-ALEH Clinical Practice Guidelines: Non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol 2015; 63(1): 237-64.
[http://dx.doi.org/10.1016/j.jhep.2015.04.006] [PMID: 25911335]
[97]
Srivastava A, Gailer R, Tanwar S, et al. Prospective evaluation of a primary care referral pathway for patients with non-alcoholic fatty liver disease. J Hepatol 2019; 71(2): 371-8.
[http://dx.doi.org/10.1016/j.jhep.2019.03.033] [PMID: 30965069]


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VOLUME: 26
ISSUE: 32
Year: 2020
Published on: 23 September, 2020
Page: [3928 - 3938]
Pages: 11
DOI: 10.2174/1381612826666200521133307
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