Non-invasive tests of non-alcoholic fatty liver disease.
Journal
Chinese medical journal
ISSN: 2542-5641
Titre abrégé: Chin Med J (Engl)
Pays: China
ID NLM: 7513795
Informations de publication
Date de publication:
27 Jan 2022
27 Jan 2022
Historique:
pubmed:
29
1
2022
medline:
15
3
2022
entrez:
28
1
2022
Statut:
epublish
Résumé
For the detection of steatosis, quantitative ultrasound imaging techniques have achieved great progress in past years. Magnetic resonance imaging proton density fat fraction is currently the most accurate test to detect hepatic steatosis. Some blood biomarkers correlate with non-alcoholic steatohepatitis, but the accuracy is modest. Regarding liver fibrosis, liver stiffness measurement by transient elastography (TE) has high accuracy and is widely used across the world. Magnetic resonance elastography is marginally better than TE but is limited by its cost and availability. Several blood biomarkers of fibrosis have been used in clinical trials and hold promise for selecting patients for treatment and monitoring treatment response. This article reviews new developments in the non-invasive assessment of non-alcoholic fatty liver disease (NAFLD). Accumulating evidence suggests that various non-invasive tests can be used to diagnose NAFLD, assess its severity, and predict the prognosis. Further studies are needed to determine the role of the tests as monitoring tools. We cannot overemphasize the importance of context in selecting appropriate tests.
Identifiants
pubmed: 35089884
doi: 10.1097/CM9.0000000000002027
pii: 00029330-202203050-00007
pmc: PMC8920457
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
532-546Informations de copyright
Copyright © 2022 The Chinese Medical Association, produced by Wolters Kluwer, Inc. under the CC-BY-NC-ND license.
Références
Powell EE, Wong VWS, Rinella M. Non-alcoholic fatty liver disease. Lancet 2021; 397:2212–2224. doi: 10.1016/S0140-6736(20)32511-3.
doi: 10.1016/S0140-6736(20)32511-3
Younossi Z, Stepanova M, Ong JP, Jacobson IM, Bugianesi E, Duseja A, et al. Nonalcoholic steatohepatitis is the fastest growing cause of hepatocellular carcinoma in liver transplant candidates. Clin Gastroenterol Hepatol 2019; 17:748–755.e3. doi: 10.1016/j.cgh.2018.05.057.
doi: 10.1016/j.cgh.2018.05.057
Taylor RS, Taylor RJ, Bayliss S, Hagstrom H, Nasr P, Schattenberg JM, et al. Association between fibrosis stage and outcomes of patients with nonalcoholic fatty liver disease: a systematic review and meta-analysis. Gastroenterology 2020; 158:1611–1625.e12. doi: 10.1053/j.gastro.2020.01.043.
doi: 10.1053/j.gastro.2020.01.043
Sanyal AJ, Van Natta ML, Clark J, Neuschwander-Tetri BA, Diehl A, Dasarathy S, et al. Prospective study of outcomes in adults with nonalcoholic fatty liver disease. N Engl J Med 2021; 385:1559–1569. doi: 10.1056/NEJMoa2029349.
doi: 10.1056/NEJMoa2029349
Davison BA, Harrison SA, Cotter G, Alkhouri N, Sanyal A, Edwards C, et al. Suboptimal reliability of liver biopsy evaluation has implications for randomized clinical trials. J Hepatol 2020; 73:1322–1332. doi: 10.1016/j.jhep.2020.06.025.
doi: 10.1016/j.jhep.2020.06.025
Zhou YJ, Wong VWS, Zheng MH. Consensus scoring systems for nonalcoholic fatty liver disease: an unmet clinical need. Hepatobiliary Surg Nutr 2021; 10:388–390. doi: 10.21037/hbsn-21-80.
doi: 10.21037/hbsn-21-80
Wong VWS, Adams LA, de Ledinghen V, Wong GLH, Sookoian S. Noninvasive biomarkers in NAFLD and NASH - current progress and future promise. Nat Rev Gastroenterol Hepatol 2018; 15:461–478. doi: 10.1038/s41575-018-0014-9.
doi: 10.1038/s41575-018-0014-9
Chan AWH, Wong GLH, Chan HY, Tong JHM, Yu YH, Choi PCL, et al. Concurrent fatty liver increases risk of hepatocellular carcinoma among patients with chronic hepatitis B. J Gastroenterol Hepatol 2017; 32:667–676. doi: 10.1111/jgh.13536.
doi: 10.1111/jgh.13536
European Association for the Study of the Liver; Clinical Practice Guideline Panel. EASL Clinical Practice Guidelines on non-invasive tests for evaluation of liver disease severity and prognosis - 2021 update. J Hepatol 2021; 75:659–689. doi: 10.1016/j.jhep.2021.05.025.
doi: 10.1016/j.jhep.2021.05.025
Poynard T, Ratziu V, Naveau S, Thabut D, Charlotte F, Messous D, et al. The diagnostic value of biomarkers (SteatoTest) for the prediction of liver steatosis. Comp Hepatol 2005; 4:10doi: 10.1186/1476-5926-4-10.
doi: 10.1186/1476-5926-4-10
Bedogni G, Bellentani S, Miglioli L, Masutti F, Passalacqua M, Castiglione A, et al. The fatty liver index: a simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol 2006; 6:33doi: 10.1186/1471-230X-6-33.
doi: 10.1186/1471-230X-6-33
Lee JH, Kim D, Kim HJ, Lee CH, Yang JI, Kim W, et al. Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig Liver Dis 2010; 42:503–508. doi: 10.1016/j.dld.2009.08.002.
doi: 10.1016/j.dld.2009.08.002
Jeong S, Kim K, Chang J, Choi S, Kim SM, Son JS, et al. Development of a simple nonalcoholic fatty liver disease scoring system indicative of metabolic risks and insulin resistance. Ann Transl Med 2020; 8:1414doi: 10.21037/atm-20-2951.
doi: 10.21037/atm-20-2951
Zhou YJ, Zhou YF, Zheng JN, Liu WY, Van Poucke S, Zou TT, et al. NAFL screening score: a basic score identifying ultrasound-diagnosed non-alcoholic fatty liver. Clin Chim Acta 2017; 475:44–50. doi: 10.1016/j.cca.2017.09.020.
doi: 10.1016/j.cca.2017.09.020
Zhou YJ, Zheng JN, Liu WY, Miele L, Vitale A, Van Poucke S, et al. The NAFL risk score: a simple scoring model to predict 4-y risk for non-alcoholic fatty liver. Clin Chim Acta 2017; 468:17–24. doi: 10.1016/j.cca.2017.01.021.
doi: 10.1016/j.cca.2017.01.021
Yip TCF, Ma AJ, Wong VWS, Tse YK, Chan HLY, Yuen PC, et al. Laboratory parameter-based machine learning model for excluding non-alcoholic fatty liver disease (NAFLD) in the general population. Aliment Pharmacol Ther 2017; 46:447–456. doi: 10.1111/apt.14172.
doi: 10.1111/apt.14172
Hernaez R, Lazo M, Bonekamp S, Kamel I, Brancati FL, Guallar E, et al. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis. Hepatology 2011; 54:1082–1090. doi: 10.1002/hep.24452.
doi: 10.1002/hep.24452
Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, et al. The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol 2007; 102:2708–2715. doi: 10.1111/j.1572-0241.2007.01526.x.
doi: 10.1111/j.1572-0241.2007.01526.x
Ferraioli G, Berzigotti A, Barr RG, Choi BI, Cui XW, Dong Y, et al. Quantification of liver fat content with ultrasound: a WFUMB position paper. Ultrasound Med Biol 2021; 47:2803–2820. doi: 10.1016/j.ultrasmedbio.2021.06.002.
doi: 10.1016/j.ultrasmedbio.2021.06.002
Lee DH, Cho EJ, Bae JS, Lee JY, Yu SJ, Kim H, et al. Accuracy of two-dimensional shear wave elastography and attenuation imaging for evaluation of patients with nonalcoholic steatohepatitis. Clin Gastroenterol Hepatol 2021; 19:797–805.e7. doi: 10.1016/j.cgh.2020.05.034.
doi: 10.1016/j.cgh.2020.05.034
Cerit M, Sendur HN, Cindil E, Erbas G, Yalcin MM, Cerit ET, et al. Quantification of liver fat content with ultrasonographic attenuation measurement function: correlation with unenhanced multidimensional computerized tomography. Clin Imaging 2020; 65:85–93. doi: 10.1016/j.clinimag.2020.04.028.
doi: 10.1016/j.clinimag.2020.04.028
Gao F, He Q, Li G, Huang OY, Tang LJ, Wang XD, et al. A novel quantitative ultrasound technique for identifying non-alcoholic steatohepatitis. Liver Int 2022; 42:80–91. doi: 10.1111/liv.15064.
doi: 10.1111/liv.15064
Karlas T, Petroff D, Sasso M, Fan JG, Mi YQ, de Ledinghen V, et al. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol 2017; 66:1022–1030. doi: 10.1016/j.jhep.2016.12.022.
doi: 10.1016/j.jhep.2016.12.022
Petroff D, Blank V, Newsome PN, Shalimar, Voican CS, Thiele M, et al. Assessment of hepatic steatosis by controlled attenuation parameter using the M and XL probes: an individual patient data meta-analysis. Lancet Gastroenterol Hepatol 2021; 6:185–198. doi: 10.1016/S2468-1253(20)30357-5.
doi: 10.1016/S2468-1253(20)30357-5
Qu Y, Song YY, Chen CW, Fu QC, Shi JP, Xu Y, et al. Diagnostic performance of FibroTouch ultrasound attenuation parameter and liver stiffness measurement in assessing hepatic steatosis and fibrosis in patients with nonalcoholic fatty liver disease. Clin Transl Gastroenterol 2021; 12:e00323doi: 10.14309/ctg.0000000000000323.
doi: 10.14309/ctg.0000000000000323
Zhu SH, Zheng KI, Hu DS, Gao F, Rios RS, Li G, et al. Optimal thresholds for ultrasound attenuation parameter in the evaluation of hepatic steatosis severity: evidence from a cohort of patients with biopsy-proven fatty liver disease. Eur J Gastroenterol Hepatol 2021; 33:430–435. doi: 10.1097/MEG.0000000000001746.
doi: 10.1097/MEG.0000000000001746
Caussy C, Brissot J, Singh S, Bassirian S, Hernandez C, Bettencourt R, et al. Prospective, same-day, direct comparison of controlled attenuation parameter with the M vs the XL probe in patients with nonalcoholic fatty liver disease, using magnetic resonance imaging-proton density fat fraction as the standard. Clin Gastroenterol Hepatol 2020; 18:1842–1850.e6. doi: 10.1016/j.cgh.2019.11.060.
doi: 10.1016/j.cgh.2019.11.060
Wong VWS, Petta S, Hiriart JB, Camma C, Wong GLH, Marra F, et al. Validity criteria for the diagnosis of fatty liver by M probe-based controlled attenuation parameter. J Hepatol 2017; 67:577–584. doi: 10.1016/j.jhep.2017.05.005.
doi: 10.1016/j.jhep.2017.05.005
Audière S, Miette V, Fournier C, Whitehead J, Paredes A, Sandrin L, et al. Continuous CAP algorithm: reduced variability in a prospective cohort. J Hepatol 2020; 73:S436.
van Werven JR, Marsman HA, Nederveen AJ, Smits NJ, ten Kate FJ, van Gulik TM, 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. doi: 10.1148/radiol.10091790.
doi: 10.1148/radiol.10091790
Romeo S, Kozlitina J, Xing C, Pertsemlidis A, Cox D, Pennacchio LA, et al. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat Genet 2008; 40:1461–1465. doi: 10.1038/ng.257.
doi: 10.1038/ng.257
Portillo-Sanchez P, Bril F, Maximos M, Lomonaco R, Biernacki D, Orsak B, et al. High prevalence of nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus and normal plasma aminotransferase levels. J Clin Endocrinol Metab 2015; 100:2231–2238. doi: 10.1210/jc.2015-1966.
doi: 10.1210/jc.2015-1966
Bannas P, Kramer H, Hernando D, Agni R, Cunningham AM, Mandal R, et al. Quantitative magnetic resonance imaging of hepatic steatosis: validation in ex vivo human livers. Hepatology 2015; 62:1444–1455. doi: 10.1002/hep.28012.
doi: 10.1002/hep.28012
Park CC, Nguyen P, Hernandez C, Bettencourt R, Ramirez K, Fortney L, et al. Magnetic resonance elastography vs transient elastography in detection of fibrosis and noninvasive measurement of steatosis in patients with biopsy-proven nonalcoholic fatty liver disease. Gastroenterology 2016; 152:598–607.e2. doi: 10.1053/j.gastro.2016.10.026.
doi: 10.1053/j.gastro.2016.10.026
Stine JG, Munaganuru N, Barnard A, Wang JL, Kaulback K, Argo CK, et al. Change in MRI-PDFF and histologic response in patients with nonalcoholic steatohepatitis: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 2021; 19:2274–2283.e5. doi: 10.1016/j.cgh.2020.08.061.
doi: 10.1016/j.cgh.2020.08.061
Tamaki N, Munaganuru N, Jung J, Yonan AQ, Loomba RR, Bettencourt R, et al. Clinical utility of 30% relative decline in MRI-PDFF in predicting fibrosis regression in non-alcoholic fatty liver disease. Gut 2021; doi: 10.1136/gutjnl-2021-324264. Online ahead of print.
doi: 10.1136/gutjnl-2021-324264.
Bril F, Barb D, Lomonaco R, Lai J, Cusi K. Change in hepatic fat content measured by MRI does not predict treatment-induced histological improvement of steatohepatitis. J Hepatol 2020; 72:401–410. doi: 10.1016/j.jhep.2019.09.018.
doi: 10.1016/j.jhep.2019.09.018
Singh S, Allen AM, Wang Z, Prokop LJ, Murad MH, Loomba R. Fibrosis progression in nonalcoholic fatty liver vs nonalcoholic steatohepatitis: a systematic review and meta-analysis of paired-biopsy studies. Clin Gastroenterol Hepatol 2015; 13:643–654.e1-9. doi: 10.1016/j.cgh.2014.04.014.
doi: 10.1016/j.cgh.2014.04.014
Wong VWS, Chitturi S, Wong GLH, Yu J, Chan HLY, Farrell GC. Pathogenesis and novel treatment options for non-alcoholic steatohepatitis. Lancet Gastroenterol Hepatol 2016; 1:56–67. doi: 10.1016/S2468-1253(16)30011-5.
doi: 10.1016/S2468-1253(16)30011-5
Vilar-Gomez E, Chalasani N. Non-invasive assessment of non-alcoholic fatty liver disease: clinical prediction rules and blood-based biomarkers. J Hepatol 2018; 68:305–315. doi: 10.1016/j.jhep.2017.11.013.
doi: 10.1016/j.jhep.2017.11.013
Kwok R, Tse YK, Wong GLH, Ha Y, Lee AU, Ngu MC, 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 2014; 39:254–269. doi: 10.1111/apt.12569.
doi: 10.1111/apt.12569
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; 43:617–649. doi: 10.3109/07853890.2010.518623.
doi: 10.3109/07853890.2010.518623
Tamimi TIAR, Elgouhari HM, Alkhouri N, Yerian LM, Berk MP, Lopez R, et al. An apoptosis panel for nonalcoholic steatohepatitis diagnosis. J Hepatol 2011; 54:1224–1229. doi: 10.1016/j.jhep.2010.08.023.
doi: 10.1016/j.jhep.2010.08.023
Huang JF, Yeh ML, Huang CF, Huang CI, Tsai PC, Tai CM, et al. Cytokeratin-18 and uric acid predicts disease severity in Taiwanese nonalcoholic steatohepatitis patients. PLoS One 2017; 12:e0174394doi: 10.1371/journal.pone.0174394.
doi: 10.1371/journal.pone.0174394
Younossi ZM, Page S, Rafiq N, Birerdinc A, Stepanova M, Hossain N, et al. A biomarker panel for non-alcoholic steatohepatitis (NASH) and NASH-related fibrosis. Obes Surg 2011; 21:431–439. doi: 10.1007/s11695-010-0204-1.
doi: 10.1007/s11695-010-0204-1
Zheng KI, Liu WY, Pan XY, Ma HL, Zhu PW, Wu XX, et al. Combined and sequential non-invasive approach to diagnosing non-alcoholic steatohepatitis in patients with non-alcoholic fatty liver disease and persistently normal alanine aminotransferase levels. BMJ Open Diabetes Res Care 2020; 8:e001174doi: 10.1136/bmjdrc-2020-001174.
doi: 10.1136/bmjdrc-2020-001174
Verma S, Jensen D, Hart J, Mohanty SR. Predictive value of ALT levels for non-alcoholic steatohepatitis (NASH) and advanced fibrosis in non-alcoholic fatty liver disease (NAFLD). Liver Int 2013; 33:1398–1405. doi: 10.1111/liv.12226.
doi: 10.1111/liv.12226
Barr J, Caballería J, Martínez-Arranz I, Domínguez-Díez A, Alonso C, Muntané J, et al. Obesity-dependent metabolic signatures associated with nonalcoholic fatty liver disease progression. J Proteome Res 2012; 11:2521–2532. doi: 10.1021/pr201223p.
doi: 10.1021/pr201223p
Younossi ZM, Otgonsuren M, Venkatesan C, Mishra A. In patients with non-alcoholic fatty liver disease, metabolically abnormal individuals are at a higher risk for mortality while metabolically normal individuals are not. Metabolism 2013; 62:352–360. doi: 10.1016/j.metabol.2012.08.005.
doi: 10.1016/j.metabol.2012.08.005
Wainwright P, Byrne CD. Bidirectional relationships and disconnects between NAFLD and features of the metabolic syndrome. Int J Mol Sci 2016; 17:367doi: 10.3390/ijms17030367.
doi: 10.3390/ijms17030367
Gao F, Zheng KI, Chen SD, Lee DH, Wu XX, Wang XD, et al. Individualized polygenic risk score identifies NASH in the Eastern Asia Region: a derivation and validation study. Clin Transl Gastroenterol 2021; 12:e00321doi: 10.14309/ctg.0000000000000321.
doi: 10.14309/ctg.0000000000000321
Koo BK, Joo SK, Kim D, Lee S, Bae JM, Park JH, et al. Development and validation of a scoring system, based on genetic and clinical factors, to determine risk of steatohepatitis in Asian patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2020; 18:2592–2599.e10. doi: 10.1016/j.cgh.2020.02.011.
doi: 10.1016/j.cgh.2020.02.011
Castera L, Friedrich-Rust M, Loomba R. Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology 2019; 156:1264–1281.e4. doi: 10.1053/j.gastro.2018.12.036.
doi: 10.1053/j.gastro.2018.12.036
Wu XX, Zheng KI, Boursier J, Chan WK, Yilmaz Y, Romero-Gomez M, et al. acNASH index to diagnose nonalcoholic steatohepatitis: a prospective derivation and global validation study. EClinicalMedicine 2021; 41:101145doi: 10.1016/j.eclinm.2021.101145.
doi: 10.1016/j.eclinm.2021.101145
Dennis A, Kelly MD, Fernandes C, Mouchti S, Fallowfield JA, Hirschfield G, et al. Correlations between MRI biomarkers PDFF and cT1 with histopathological features of non-alcoholic steatohepatitis. Front Endocrinol (Lausanne) 2020; 11:575843doi: 10.3389/fendo.2020.575843.
doi: 10.3389/fendo.2020.575843
Abrigo JM, Shen J, Wong VWS, Yeung DKW, Wong GLH, Chim AML, et al. Non-alcoholic fatty liver disease: spectral patterns observed from an in vivo phosphorus magnetic resonance spectroscopy study. J Hepatol 2013; 60:809–815. doi: 10.1016/j.jhep.2013.11.018.
doi: 10.1016/j.jhep.2013.11.018
Allen AM, Shah VH, Therneau TM, Venkatesh SK, Mounajjed T, Larson JJ, et al. The role of three-dimensional magnetic resonance elastography in the diagnosis of nonalcoholic steatohepatitis in obese patients undergoing bariatric surgery. Hepatology 2020; 71:510–521. doi: 10.1002/hep.30483.
doi: 10.1002/hep.30483
Guimaraes AR, Siqueira L, Uppal R, Alford J, Fuchs BC, Yamada S, et al. T2 relaxation time is related to liver fibrosis severity. Quant Imaging Med Surg 2016; 6:103–114. doi: 10.21037/qims.2016.03.02.
doi: 10.21037/qims.2016.03.02
Cassinotto C, Feldis M, Vergniol J, Mouries A, Cochet H, Lapuyade B, et al. MR relaxometry in chronic liver diseases: comparison of T1 mapping, T2 mapping, and diffusion-weighted imaging for assessing cirrhosis diagnosis and severity. Eur J Radiol 2015; 84:1459–1465. doi: 10.1016/j.ejrad.2015.05.019.
doi: 10.1016/j.ejrad.2015.05.019
Chen ZW, Xiao HM, Ye XJ, Liu K, Rios RS, Zheng KI, et al. A novel radiomics signature based on T2WI accurately predicts hepatic inflammation in individuals with biopsy-proven NAFLD: a derivation and independent validation study. Hepatobiliary Surg Nutr 2021; doi: 10.21037/hbsn-21-23. Online ahead of print.
doi: 10.21037/hbsn-21-23.
Loomba R, Adams LA. Advances in non-invasive assessment of hepatic fibrosis. Gut 2020; 69:1343–1352. doi: 10.1136/gutjnl-2018-317593.
doi: 10.1136/gutjnl-2018-317593
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. doi: 10.1111/j.1572-0241.1998.044_c.x.
doi: 10.1111/j.1572-0241.1998.044_c.x
Shaheen AAM, Myers RP. Diagnostic accuracy of the aspartate aminotransferase-to-platelet ratio index for the prediction of hepatitis C-related fibrosis: a systematic review. Hepatology 2007; 46:912–921. doi: 10.1002/hep.21835.
doi: 10.1002/hep.21835
Wong VWS, Wong GLH, Chim AML, Tse AML, Tsang SWC, Hui AY, et al. Validation of the NAFLD fibrosis score in a Chinese population with low prevalence of advanced fibrosis. Am J Gastroenterol 2008; 103:1682–1688. doi: 10.1111/j.1572-0241.2008.01933.x.
doi: 10.1111/j.1572-0241.2008.01933.x
Sterling RK, Lissen E, Clumeck N, Sola R, Correa MC, Montaner J, et al. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology 2006; 43:1317–1325. doi: 10.1002/hep.21178.
doi: 10.1002/hep.21178
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; 66:1486–1501. doi: 10.1002/hep.29302.
doi: 10.1002/hep.29302
Angulo P, Hui JM, Marchesini G, Bugianesi E, George J, Farrell GC, et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology 2007; 45:846–854. doi: 10.1002/hep.21496.
doi: 10.1002/hep.21496
Wai JW, Fu C, Wong VWS. Confounding factors of non-invasive tests for nonalcoholic fatty liver disease. J Gastroenterol 2020; 55:731–741. doi: 10.1007/s00535-020-01686-8.
doi: 10.1007/s00535-020-01686-8
McPherson S, Hardy T, Dufour JF, Petta S, Romero-Gomez M, Allison M, et al. Age as a confounding factor for the accurate non-invasive diagnosis of advanced NAFLD fibrosis. Am J Gastroenterol 2017; 112:740–751. doi: 10.1038/ajg.2016.453.
doi: 10.1038/ajg.2016.453
Mahady SE, Macaskill P, Craig JC, Wong GLH, Chu WCW, Chan HLY, et al. Diagnostic accuracy of noninvasive fibrosis scores in a population of individuals with a low prevalence of fibrosis. Clin Gastroenterol Hepatol 2017; 15:1453–1460.e1. doi: 10.1016/j.cgh.2017.02.031.
doi: 10.1016/j.cgh.2017.02.031
Ampuero J, Pais R, Aller R, Gallego-Duran R, Crespo J, Garcia-Monzon C, et al. Development and validation of hepamet fibrosis scoring system-a simple, noninvasive test to identify patients with nonalcoholic fatty liver disease with advanced fibrosis. Clin Gastroenterol Hepatol 2020; 18:216–225.e5. doi: 10.1016/j.cgh.2019.05.051.
doi: 10.1016/j.cgh.2019.05.051
Hagström H, Talbäck M, Andreasson A, Walldius G, Hammar N. Repeated FIB-4 measurements can help identify individuals at risk of severe liver disease. J Hepatol 2020; 73:1023–1029. doi: 10.1016/j.jhep.2020.06.007.
doi: 10.1016/j.jhep.2020.06.007
Adams LA, George J, Bugianesi E, Rossi E, De Boer WB, van der Poorten D, et al. Complex non-invasive fibrosis models are more accurate than simple models in non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2011; 26:1536–1543. doi: 10.1111/j.1440-1746.2011.06774.x.
doi: 10.1111/j.1440-1746.2011.06774.x
Vali Y, Lee J, Boursier J, Spijker R, Löffler J, Verheij J, et al. Enhanced liver fibrosis test for the non-invasive diagnosis of fibrosis in patients with NAFLD: a systematic review and meta-analysis. J Hepatol 2020; 73:252–262. doi: 10.1016/j.jhep.2020.03.036.
doi: 10.1016/j.jhep.2020.03.036
Lichtinghagen R, Pietsch D, Bantel H, Manns MP, Brand K, Bahr MJ. The Enhanced Liver Fibrosis (ELF) score: normal values, influence factors and proposed cut-off values. J Hepatol 2013; 59:236–242. doi: 10.1016/j.jhep.2013.03.016.
doi: 10.1016/j.jhep.2013.03.016
Srivastava A, Gailer R, Tanwar S, Trembling P, Parkes J, Rodger A, et al. Prospective evaluation of a primary care referral pathway for patients with non-alcoholic fatty liver disease. J Hepatol 2019; 71:371–378. doi: 10.1016/j.jhep.2019.03.033.
doi: 10.1016/j.jhep.2019.03.033
Parkes J, Roderick P, Harris S, Day C, Mutimer D, Collier J, et al. Enhanced liver fibrosis test can predict clinical outcomes in patients with chronic liver disease. Gut 2010; 59:1245–1251. doi: 10.1136/gut.2009.203166.
doi: 10.1136/gut.2009.203166
Nielsen MJ, Leeming DJ, Goodman Z, Friedman S, Frederiksen P, Rasmussen DGK, et al. Comparison of ADAPT, FIB4 and APRI as non-invasive predictors of liver fibrosis and NASH within the CENTAUR Screening Population. J Hepatol 2021; 75:1292–1300. doi: 10.1016/j.jhep.2021.08.016.
doi: 10.1016/j.jhep.2021.08.016
Daniels SJ, Leeming DJ, Eslam M, Hashem AM, Nielsen MJ, Krag A, et al. ADAPT: an algorithm incorporating PRO-C3 accurately identifies patients with NAFLD and advanced fibrosis. Hepatology 2019; 69:1075–1086. doi: 10.1002/hep.30163.
doi: 10.1002/hep.30163
Feng G, Zheng KI, Li YY, Rios RS, Zhu PW, Pan XY, et al. Machine learning algorithm outperforms fibrosis markers in predicting significant fibrosis in biopsy-confirmed NAFLD. J Hepatobiliary Pancreat Sci 2021; 28:593–603. doi: 10.1002/jhbp.972.
doi: 10.1002/jhbp.972
Zhou YJ, Ye FZ, Li YY, Pan XY, Chen YX, Wu XX, et al. Individualized risk prediction of significant fibrosis in non-alcoholic fatty liver disease using a novel nomogram. United European Gastroenterol J 2019; 7:1124–1134. doi: 10.1177/2050640619868352.
doi: 10.1177/2050640619868352
Gao F, Huang JF, Zheng KI, Pan XY, Ma HL, Liu WY, et al. Development and validation of a novel non-invasive test for diagnosing fibrotic non-alcoholic steatohepatitis in patients with biopsy-proven non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2020; 35:1804–1812. doi: 10.1111/jgh.15055.
doi: 10.1111/jgh.15055
Vali Y, Lee J, Boursier J, Spijker R, Verheij J, Brosnan MJ, et al. FibroTest for evaluating fibrosis in non-alcoholic fatty liver disease patients: a systematic review and meta-analysis. J Clin Med 2021; 10:2415doi: 10.3390/jcm10112415.
doi: 10.3390/jcm10112415
Calès P, Lainé F, Boursier J, Deugnier Y, Moal V, Oberti F, et al. Comparison of blood tests for liver fibrosis specific or not to NAFLD. J Hepatol 2009; 50:165–173. doi: 10.1016/j.jhep.2008.07.035.
doi: 10.1016/j.jhep.2008.07.035
Loong TCW, Wei JL, Leung JCF, Wong GLH, Shu SST, Chim AML, et al. Application of the combined FibroMeter vibration-controlled transient elastography algorithm in Chinese patients with non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2017; 32:1363–1369. doi: 10.1111/jgh.13671.
doi: 10.1111/jgh.13671
Wong GLH. Non-invasive assessments for liver fibrosis: the crystal ball we long for. J Gastroenterol Hepatol 2018; 33:1009–1015. doi: 10.1111/jgh.14103.
doi: 10.1111/jgh.14103
Wong GLH. Update of liver fibrosis and steatosis with transient elastography (Fibroscan). Gastroenterol Rep (Oxf) 2013; 1:19–26. doi: 10.1093/gastro/got007.
doi: 10.1093/gastro/got007
Wong VWS, Vergniol J, Wong GLH, Foucher J, Chan HLY, Le Bail B, et al. Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease. Hepatology 2010; 51:454–462. doi: 10.1002/hep.23312.
doi: 10.1002/hep.23312
Wong VWS, Vergniol J, Wong GLH, Foucher J, Chan AWH, Chermak F, et al. Liver stiffness measurement using XL probe in patients with nonalcoholic fatty liver disease. Am J Gastroenterol 2012; 107:1862–1871. doi: 10.1038/ajg.2012.331.
doi: 10.1038/ajg.2012.331
Wong GLH, Chan HLY, Choi PCL, Chan AWH, Lo AOS, Chim AML, et al. Association between anthropometric parameters and measurements of liver stiffness by transient elastography. Clin Gastroenterol Hepatol 2013; 11:295–302.e1-3. doi: 10.1016/j.cgh.2012.09.025.
doi: 10.1016/j.cgh.2012.09.025
Wong VWS, Irles M, Wong GLH, Shili S, Chan AWH, Merrouche W, et al. Unified interpretation of liver stiffness measurement by M and XL probes in non-alcoholic fatty liver disease. Gut 2019; 68:2057–2064. doi: 10.1136/gutjnl-2018-317334.
doi: 10.1136/gutjnl-2018-317334
Wong GLH, Wong VWS, Choi PCL, Chan AWH, Chim AML, Yiu KKL, et al. Increased liver stiffness measurement by transient elastography in severe acute exacerbation of chronic hepatitis B. J Gastroenterol Hepatol 2009; 24:1002–1007. doi: 10.1111/j.1440-1746.2009.05779.x.
doi: 10.1111/j.1440-1746.2009.05779.x
Zhang X, Wong GLH, Wong VWS. Application of transient elastography in nonalcoholic fatty liver disease. Clin Mol Hepatol 2020; 26:128–141. doi: 10.3350/cmh.2019.0001n.
doi: 10.3350/cmh.2019.0001n
Liu K, Wong VWS, Lau K, Liu SD, Tse YK, Yip TCF, et al. Prognostic value of controlled attenuation parameter by transient elastography. Am J Gastroenterol 2017; 112:1812–1823. doi: 10.1038/ajg.2017.389.
doi: 10.1038/ajg.2017.389
Attia D, Bantel H, Lenzen H, Manns MP, Gebel MJ, Potthoff A. Liver stiffness measurement using acoustic radiation force impulse elastography in overweight and obese patients. Aliment Pharmacol Ther 2016; 44:366–379. doi: 10.1111/apt.13710.
doi: 10.1111/apt.13710
Kiani A, Brun V, Laine F, Turlin B, Morcet J, Michalak S, et al. Acoustic radiation force impulse imaging for assessing liver fibrosis in alcoholic liver disease. World J Gastroenterol 2016; 22:4926–4935. doi: 10.3748/wjg.v22.i20.4926.
doi: 10.3748/wjg.v22.i20.4926
Caussy C, Chen J, Alquiraish MH, Cepin S, Nguyen P, Hernandez C, et al. Association between obesity and discordance in fibrosis stage determination by magnetic resonance vs transient elastography in patients with nonalcoholic liver disease. Clin Gastroenterol Hepatol 2018; 16:1974–1982.e7. doi: 10.1016/j.cgh.2017.10.037.
doi: 10.1016/j.cgh.2017.10.037
Hsu C, Caussy C, Imajo K, Chen J, Singh S, Kaulback K, et al. Magnetic resonance vs transient elastography analysis of patients with nonalcoholic fatty liver disease: a systematic review and pooled analysis of individual participants. Clin Gastroenterol Hepatol 2019; 17:630–637.e8. doi: 10.1016/j.cgh.2018.05.059.
doi: 10.1016/j.cgh.2018.05.059
Barr RG, Ferraioli G, Palmeri ML, Goodman ZD, Garcia-Tsao G, Rubin J, et al. Elastography assessment of liver fibrosis: society of radiologists in ultrasound consensus conference statement. Radiology 2015; 276:845–861. doi: 10.1148/radiol.2015150619.
doi: 10.1148/radiol.2015150619
Hou J, Wong VWS, Jiang B, Wang YX, Wong GLH, Chan AWH, et al. Macromolecular proton fraction mapping based on spin-lock magnetic resonance imaging. Magn Reson Med 2020; 84:3157–3171. doi: 10.1002/mrm.28362.
doi: 10.1002/mrm.28362
Lazarus JV, Anstee QM, Hagstrom H, Cusi K, Cortez-Pinto H, Mark HE, et al. Defining comprehensive models of care for NAFLD. Nat Rev Gastroenterol Hepatol 2021; 18:717–729. doi: 10.1038/s41575-021-00477-7.
doi: 10.1038/s41575-021-00477-7
Kanwal F, Shubrook JH, Adams LA, Pfotenhauer K, Wong VWS, Wright E, et al. Clinical care pathway for the risk stratification and management of patients with nonalcoholic fatty liver disease. Gastroenterology 2021; 161:1657–1669. doi: 10.1053/j.gastro.2021.07.049.
doi: 10.1053/j.gastro.2021.07.049