Diagnosis and assessment of disease severity in patients with nonalcoholic fatty liver disease.
NAFLD
hepatocellular carcinoma
liver fibrosis
nonalcoholic fatty liver disease
Journal
United European gastroenterology journal
ISSN: 2050-6414
Titre abrégé: United European Gastroenterol J
Pays: England
ID NLM: 101606807
Informations de publication
Date de publication:
Mar 2024
Mar 2024
Historique:
received:
16
05
2023
accepted:
07
09
2023
pubmed:
21
11
2023
medline:
21
11
2023
entrez:
21
11
2023
Statut:
ppublish
Résumé
Nonalcoholic fatty liver disease (NAFLD) includes simple steatosis, nonalcoholic steatohepatitis (NASH), fibrosis, and eventually cirrhosis and hepatocellular carcinoma (HCC). The diagnosis of NAFLD is based on the detection of excess fat disposition in the liver, which is the first step to trigger further evaluation of NAFLD, including necroinflammation and fibrosis. In this review, we discuss non-invasive biomarkers and imaging tools that are currently and potentially available for different features (steatosis, necroinflammation and fibrosis) and disease severity assessment of NAFLD. In the past 2 decades, advances in non-invasive tests of fibrosis have transformed the management of NAFLD. Blood and imaging biomarkers have already been evaluated in multiple studies for the diagnosis of fibrosis and cirrhosis. Among the various histological features of NAFLD, the degree of fibrosis has the strongest correlation with liver-related morbidity and mortality. Non-invasive tests of fibrosis have been shown to predict liver-related outcomes, both in the general population and among patients with NAFLD. What is lacking, however, is good data to support the use of non-invasive tests as monitoring and response biomarkers. With the conclusion of several large phase 3 studies in the next few years, the availability of paired liver biopsy, non-invasive test and clinical outcome data will likely advance the field and shed light on new biomarkers and the way to use various non-invasive tests in a longitudinal manner.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
219-225Informations de copyright
© 2023 The Authors. United European Gastroenterology Journal published by Wiley Periodicals LLC on behalf of United European Gastroenterology.
Références
Le MH, Yeo YH, Li X, Li J, Zou B, Wu Y, et al. 2019 global NAFLD prevalence: a systematic review and meta‐analysis. Clin Gastroenterol Hepatol. 2022;20(12):2809–2817. https://doi.org/10.1016/j.cgh.2021.12.002
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(4):748–755. https://doi.org/10.1016/j.cgh.2018.05.057
Jiang W, Mao X, Liu Z, Zhang T, Jin L, Chen X. Global burden of nonalcoholic fatty liver disease, 1990 to 2019: findings from the global burden of disease study 2019. J Clin Gastroenterol. 2022.
Wong VW, Adams LA, de Ledinghen V, Wong GL, Sookoian S. Noninvasive biomarkers in NAFLD and NASH ‐ current progress and future promise. Nat Rev Gastroenterol Hepatol. 2018;15(8):461–478. https://doi.org/10.1038/s41575‐018‐0014‐9
Bedossa P, Dargere D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology. 2003;38(6):1449–1457. https://doi.org/10.1053/jhep.2003.09022
Ratziu V, Charlotte F, Heurtier A, Gombert S, Giral P, Bruckert E, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128(7):1898–1906. https://doi.org/10.1053/j.gastro.2005.03.084
Anstee QM, Castera L, Loomba R. Impact of non‐invasive biomarkers on hepatology practice: past, present and future. J Hepatol. 2022;76(6):1362–1378. https://doi.org/10.1016/j.jhep.2022.03.026
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(1):33. https://doi.org/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(7):503–508. https://doi.org/10.1016/j.dld.2009.08.002
Kotronen A, Peltonen M, Hakkarainen A, Sevastianova K, Bergholm R, Johansson LM, et al. Prediction of non‐alcoholic fatty liver disease and liver fat using metabolic and genetic factors. Gastroenterology. 2009;137(3):865–872. https://doi.org/10.1053/j.gastro.2009.06.005
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(1):10. https://doi.org/10.1186/1476‐5926‐4‐10
Yip TC, Ma AJ, Wong VW, Tse Y, Chan HL, Yuen P, 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(4):447–456. https://doi.org/10.1111/apt.14172
Castellana M, Donghia R, Guerra V, Procino F, Lampignano L, Castellana F, et al. Performance of fatty liver index in identifying non‐alcoholic fatty liver disease in population studies. A meta‐analysis. J Clin Med. 2021;10(9):1877. https://doi.org/10.3390/jcm10091877
Mikolasevic I, Domislovic V, Krznaric‐Zrnic I, Krznaric Z, Virovic‐Jukic L, Stojsavljevic S, et al. The accuracy of serum biomarkers in the diagnosis of steatosis, fibrosis, and inflammation in patients with nonalcoholic fatty liver disease in comparison to a liver biopsy. Med Kaunas. 2022;58(2):252. https://doi.org/10.3390/medicina58020252
Wu J, Li H, Xu Z, Ran L, Kong LQ. Population‐specific cut‐off points of fatty liver index for the diagnosis of hepatic steatosis. J Hepatol. 2021;75(3):726–728. https://doi.org/10.1016/j.jhep.2021.05.039
Cen C, Wang W, Yu S, Tang X, Liu J, Liu Y, et al. Development and validation of a clinical and laboratory‐based nomogram to predict nonalcoholic fatty liver disease. Hepatol Int. 2020;14(5):808–816. https://doi.org/10.1007/s12072‐020‐10065‐7
Dasarathy S, Dasarathy J, Khiyami A, Joseph R, Lopez R, McCullough AJ. Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol. 2009;51(6):1061–1067. https://doi.org/10.1016/j.jhep.2009.09.001
Cao YT, Xiang LL, Qi F, Zhang YJ, Chen Y, Zhou XQ. Accuracy of controlled attenuation parameter (CAP) and liver stiffness measurement (LSM) for assessing steatosis and fibrosis in non‐alcoholic fatty liver disease: a systematic review and meta‐analysis. EClinicalMedicine. 2022;51:101547. https://doi.org/10.1016/j.eclinm.2022.101547
Karlas T, Petroff D, Sasso M, Fan JG, Mi YQ, de Lédinghen V, et al. Individual patient data meta‐analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol. 2017;66(5):1022–1030. https://doi.org/10.1016/j.jhep.2016.12.022
Tavaglione F, De Vincentis A, Bruni V, Gallo IF, Carotti S, Tuccinardi D, et al. Accuracy of controlled attenuation parameter for assessing liver steatosis in individuals with morbid obesity before bariatric surgery. Liver Int. 2022;42(2):374–383. https://doi.org/10.1111/liv.15127
Kozlowska‐Petriczko K, Wunsch E, Milkiewicz P. Controlled attenuation parameter in nonalcoholic fatty liver disease: the thresholds do matter. Clin Gastroenterol Hepatol. 2021;19(7):1507–1508. https://doi.org/10.1016/j.cgh.2020.08.055
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(3):185–198. https://doi.org/10.1016/s2468‐1253(20)30357‐5
Gu J, Liu S, Du S, Zhang Q, Xiao J, Dong Q, et al. Diagnostic value of MRI‐PDFF for hepatic steatosis in patients with non‐alcoholic fatty liver disease: a meta‐analysis. Eur Radiol. 2019;29(7):3564–3573. https://doi.org/10.1007/s00330‐019‐06072‐4
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. 2017;152(3):598–607. https://doi.org/10.1016/s0016‐5085(17)30587‐5
Park S, Kwon JH, Kim SY, Kang JH, Chung JI, Jang JK, et al. Cutoff values for diagnosing hepatic steatosis using contemporary MRI‐proton density fat fraction measuring methods. Korean J Radiol. 2022;23(12):1260–1268. https://doi.org/10.3348/kjr.2022.0334
Byra M, Szmigielski C, Kalinowski P, et al. Ultrasound‐ and biomarker‐based assessment of hepatic steatosis in patients with severe obesity. Pol Arch Intern Med. 2023;133(1).
Dillman JR, Thapaliya S, Tkach JA, Trout AT. Quantification of hepatic steatosis by ultrasound: prospective comparison with MRI proton density fat fraction as reference standard. AJR Am J Roentgenol. 2022;219(5):784–791. https://doi.org/10.2214/ajr.22.27878
Boursier J, Guillaume M, Bouzbib C, Lannes A, Pais R, Smatti S, et al. Non‐invasive diagnosis and follow‐up of non‐alcoholic fatty liver disease. Clin Res Hepatol Gastroenterol. 2022;46(1):101769. https://doi.org/10.1016/j.clinre.2021.101769
European Association for the Study of the L, European Association for the Study of D, European Association for the Study of O. EASL‐EASD‐EASO Clinical Practice Guidelines for the management of non‐alcoholic fatty liver disease. J Hepatol. 2016;64(6):1388–1402.
Tada T, Saibara T, Ono M, Takahashi H, Eguchi Y, Hyogo H, et al. Predictive value of cytokeratin‐18 fragment levels for diagnosing steatohepatitis in patients with nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol. 2021;33(11):1451–1458. https://doi.org/10.1097/meg.0000000000002176
Vali Y, Lee J, Boursier J, Petta S, Wonders K, Tiniakos D, et al. Biomarkers for staging fibrosis and non‐alcoholic steatohepatitis in non‐alcoholic fatty liver disease (the LITMUS project): a comparative diagnostic accuracy study. Lancet Gastroenterol Hepatol. 2023;8(8):714–725. https://doi.org/10.1016/s2468‐1253(23)00017‐1
Wong VWS, Zelber‐Sagi S, Cusi K, Carrieri P, Wright E, Crespo J, et al. Management of NAFLD in primary care settings. Liver Int. 2022;42(11):2377–2389. https://doi.org/10.1111/liv.15404
Patel PJ, Connoley D, Rhodes F, Srivastava A, Rosenberg W. A review of the clinical utility of the Enhanced Liver Fibrosis test in multiple aetiologies of chronic liver disease. Ann Clin Biochem. 2020;57(1):36–43. https://doi.org/10.1177/0004563219879962
Boursier J, Vergniol J, Guillet A, Hiriart JB, Lannes A, Le Bail B, 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):570–578. https://doi.org/10.1016/j.jhep.2016.04.023
Sanyal AJ, Foucquier J, Younossi ZM, Harrison SA, Newsome PN, Chan WK, et al. Enhanced diagnosis of advanced fibrosis and cirrhosis in individuals with NAFLD using FibroScan‐based Agile scores. J Hepatol. 2023;78(2):247–259. https://doi.org/10.1016/j.jhep.2022.10.034
Boursier J, Canivet CM, Costentin C, Lannes A, Delamarre A, Sturm N, et al. Impact of type 2 diabetes on the accuracy of noninvasive tests of liver fibrosis with resulting clinical implications. Clin Gastroenterol Hepatol. 2023;21(5):1243–1251. https://doi.org/10.1016/j.cgh.2022.02.059
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(4):630–637. https://doi.org/10.1016/j.cgh.2018.05.059
Villanueva C, Albillos A, Genesca J, Garcia‐Pagan JC, Calleja JL, Aracil C, et al. β blockers to prevent decompensation of cirrhosis in patients with clinically significant portal hypertension (PREDESCI): a randomised, double‐blind, placebo‐controlled, multicentre trial. Lancet. 2019;393(10181):1597–1608. https://doi.org/10.1016/s0140‐6736(18)31875‐0
de Franchis R, Bosch J, Garcia‐Tsao G, Reiberger T, Ripoll C, Abraldes JG, et al. Baveno VII ‐ renewing consensus in portal hypertension. J Hepatol. 2022;76(4):959–974. https://doi.org/10.1016/j.jhep.2021.12.022
Pons M, Augustin S, Scheiner B, Guillaume M, Rosselli M, Rodrigues SG, et al. Noninvasive diagnosis of portal hypertension in patients with compensated advanced chronic liver disease. Am J Gastroenterol. 2021;116(4):723–732. https://doi.org/10.14309/ajg.0000000000000994
Bassegoda O, Olivas P, Turco L, Mandorfer M, Serra‐Burriel M, Tellez L, et al. Decompensation in advanced nonalcoholic fatty liver disease may occur at lower hepatic venous pressure gradient levels than in patients with viral disease. Clin Gastroenterol Hepatol. 2022;20(10):2276–2286. https://doi.org/10.1016/j.cgh.2021.10.023
Dajti E, Ravaioli F, Marasco G, Alemanni LV, Colecchia L, Ferrarese A, et al. A combined Baveno VII and spleen stiffness algorithm to improve the noninvasive diagnosis of clinically significant portal hypertension in patients with compensated advanced chronic liver disease. Am J Gastroenterol. 2022;117(11):1825–1833. https://doi.org/10.14309/ajg.0000000000001887
de Franchis R, VI Faculty B. Expanding consensus in portal hypertension: report of the Baveno VI Consensus Workshop: stratifying risk and individualizing care for portal hypertension. J Hepatol. 2015;63(3):743–752.
Petta S, Sebastiani G, Bugianesi E, Viganò M, Wong VWS, Berzigotti A, et al. Non‐invasive prediction of esophageal varices by stiffness and platelet in non‐alcoholic fatty liver disease cirrhosis. J Hepatol. 2018;69(4):878–885. https://doi.org/10.1016/j.jhep.2018.05.019
Wong GL, Liang LY, Kwok R, Hui AJ, Tse Y, Chan HL, et al. Low risk of variceal bleeding in patients with cirrhosis after variceal screening stratified by liver/spleen stiffness. Hepatology. 2019;70(3):971–981. https://doi.org/10.1002/hep.30522
Taylor RS, Taylor RJ, Bayliss S, Hagström 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(6):1611–1625. https://doi.org/10.1053/j.gastro.2020.01.043
Hagstrom H, Talback 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(5):1023–1029. https://doi.org/10.1016/j.jhep.2020.06.007
Cholankeril G, Kramer JR, Chu J, Yu X, Balakrishnan M, Li L, et al. Longitudinal changes in fibrosis markers are associated with risk of cirrhosis and hepatocellular carcinoma in non‐alcoholic fatty liver disease. J Hepatol. 2023;78(3):493–500. https://doi.org/10.1016/j.jhep.2022.10.035
Boursier J, Hagstrom H, Ekstedt M, Moreau C, Bonacci M, Cure S, et al. Non‐invasive tests accurately stratify patients with NAFLD based on their risk of liver‐related events. J Hepatol. 2022;76(5):1013–1020. https://doi.org/10.1016/j.jhep.2021.12.031
Younossi ZM, Ratziu V, Loomba R, Rinella M, Anstee QM, Goodman Z, et al. Obeticholic acid for the treatment of non‐alcoholic steatohepatitis: interim analysis from a multicentre, randomised, placebo‐controlled phase 3 trial. Lancet. 2019;394(10215):2184–2196. https://doi.org/10.1016/s0140‐6736(19)33041‐7
Newsome PN, Buchholtz K, Cusi K, Linder M, Okanoue T, Ratziu V, et al. A placebo‐controlled trial of subcutaneous semaglutide in nonalcoholic steatohepatitis. N Engl J Med. 2021;384(12):1113–1124. https://doi.org/10.1530/ey.18.15.7
Harrison SA, Bashir MR, Guy CD, Zhou R, Moylan CA, Frias JP, et al. Resmetirom (MGL‐3196) for the treatment of non‐alcoholic steatohepatitis: a multicentre, randomised, double‐blind, placebo‐controlled, phase 2 trial. Lancet. 2019;394(10213):2012–2024. https://doi.org/10.1016/s0140‐6736(19)32517‐6
Francque SM, Bedossa P, Ratziu V, Anstee QM, Bugianesi E, Sanyal AJ, et al. A randomized, controlled trial of the pan‐PPAR agonist lanifibranor in NASH. N Engl J Med. 2021;385(17):1547–1558. https://doi.org/10.1056/nejmoa2036205
Rinella ME, Dufour JF, Anstee QM, Goodman Z, Younossi Z, Harrison SA, et al. Non‐invasive evaluation of response to obeticholic acid in patients with NASH: results from the REGENERATE study. J Hepatol. 2022;76(3):536–548. https://doi.org/10.1016/j.jhep.2021.10.029
Kanwal F, Shubrook JH, Adams LA, Pfotenhauer K, Wai‐Sun Wong V, Wright E, et al. Clinical care pathway for the risk stratification and management of patients with nonalcoholic fatty liver disease. Gastroenterology. 2021;161(5):1657–1669. https://doi.org/10.1053/j.gastro.2021.07.049
European Association for the Study of the Liver. Electronic address eee, Clinical Practice Guideline P, Chair, representative EGB, Panel m. EASL Clinical Practice Guidelines on non‐invasive tests for evaluation of liver disease severity and prognosis ‐ 2021 update. J Hepatol. 2021;75(3):659–689.