Semin Liver Dis 2024; 44(02): 226-238
DOI: 10.1055/a-2334-8525
Review Article

This Is What Metabolic Dysfunction–Associated Steatotic Liver Disease Looks Like: Potential of a Multiparametric MRI Protocol

Anja M. Fischer
1   Boehringer Ingelheim Pharma GmbH & Co. KG, Biberach, Germany
,
Nazim Lechea
1   Boehringer Ingelheim Pharma GmbH & Co. KG, Biberach, Germany
,
Harvey O. Coxson
1   Boehringer Ingelheim Pharma GmbH & Co. KG, Biberach, Germany
› Author Affiliations


Abstract

Metabolic dysfunction–associated steatotic liver disease (MASLD) is a prevalent condition with a broad spectrum defined by liver biopsy. This gold standard method evaluates three features: steatosis, activity (ballooning and lobular inflammation), and fibrosis, attributing them to certain grades or stages using a semiquantitative scoring system. However, liver biopsy is subject to numerous restrictions, creating an unmet need for a reliable and reproducible method for MASLD assessment, grading, and staging. Noninvasive imaging modalities, such as magnetic resonance imaging (MRI), offer the potential to assess quantitative liver parameters. This review aims to provide an overview of the available MRI techniques for the three criteria evaluated individually by liver histology. Here, we discuss the possibility of combining multiple MRI parameters to replace liver biopsy with a holistic, multiparametric MRI protocol. In conclusion, the development and implementation of such an approach could significantly improve the diagnosis and management of MASLD, reducing the need for invasive procedures and paving the way for more personalized treatment strategies.



Publication History

Accepted Manuscript online:
28 May 2024

Article published online:
19 June 2024

© 2024. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Younossi ZM, Golabi P, Paik JM, Henry A, Van Dongen C, Henry L. The global epidemiology of nonalcoholic fatty liver disease (NAFLD) and nonalcoholic steatohepatitis (NASH): a systematic review. Hepatology 2023; 77 (04) 1335-1347
  • 2 Moore JB. Non-alcoholic fatty liver disease: the hepatic consequence of obesity and the metabolic syndrome. Proc Nutr Soc 2010; 69 (02) 211-220
  • 3 Eslam M, Sanyal AJ, George J. International Consensus Panel. MAFLD: a consensus-driven proposed nomenclature for metabolic associated fatty liver disease. Gastroenterology 2020; 158 (07) 1999-2014.e1
  • 4 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 (01) 73-84
  • 5 Haas JT, Francque S, Staels B. Pathophysiology and mechanisms of nonalcoholic fatty liver disease. Annu Rev Physiol 2016; 78: 181-205
  • 6 Cotter TG, Rinella M. Nonalcoholic fatty liver disease 2020: the state of the disease. Gastroenterology 2020; 158 (07) 1851-1864
  • 7 Radu F, Potcovaru CG, Salmen T, Filip PV, Pop C, Fierbințeanu-Braticievici C. The link between NAFLD and metabolic syndrome. Diagnostics (Basel) 2023; 13 (04) 614
  • 8 Ghazanfar H, Javed N, Qasim A. et al. Metabolic dysfunction-associated steatohepatitis and progression to hepatocellular carcinoma: a literature review. Cancers (Basel) 2024; 16 (06) 1214
  • 9 Madir A, Grgurevic I, Tsochatzis EA, Pinzani M. Portal hypertension in patients with nonalcoholic fatty liver disease: current knowledge and challenges. World J Gastroenterol 2024; 30 (04) 290-307
  • 10 Kleiner DE, Brunt EM, Van Natta M. et al; Nonalcoholic Steatohepatitis Clinical Research Network. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005; 41 (06) 1313-1321
  • 11 Bedossa P, Poitou C, Veyrie N. et al. Histopathological algorithm and scoring system for evaluation of liver lesions in morbidly obese patients. Hepatology 2012; 56 (05) 1751-1759
  • 12 Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med 2001; 344 (07) 495-500
  • 13 Cusi K, Isaacs S, Barb D. et al. American Association of Clinical Endocrinology Clinical Practice Guideline for the diagnosis and management of nonalcoholic fatty liver disease in primary care and endocrinology clinical settings: co-sponsored by the American Association for the Study of Liver Diseases (AASLD). Endocr Pract 2022; 28 (05) 528-562
  • 14 Ratziu V, Charlotte F, Heurtier A. et al; LIDO Study Group. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 2005; 128 (07) 1898-1906
  • 15 Merriman RB, Ferrell LD, Patti MG. et al. Correlation of paired liver biopsies in morbidly obese patients with suspected nonalcoholic fatty liver disease. Hepatology 2006; 44 (04) 874-880
  • 16 Larson SP, Bowers SP, Palekar NA, Ward JA, Pulcini JP, Harrison SA. Histopathologic variability between the right and left lobes of the liver in morbidly obese patients undergoing Roux-en-Y bypass. Clin Gastroenterol Hepatol 2007; 5 (11) 1329-1332
  • 17 Grąt K, Grąt M, Rowiński O. Usefulness of different imaging modalities in evaluation of patients with non-alcoholic fatty liver disease. Biomedicines 2020; 8 (09) 298
  • 18 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 (03) 626-637.e7
  • 19 Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 2005; 115 (05) 1343-1351
  • 20 Friedman SL, Neuschwander-Tetri BA, Rinella M, Sanyal AJ. Mechanisms of NAFLD development and therapeutic strategies. Nat Med 2018; 24 (07) 908-922
  • 21 Sanyal AJ, Brunt EM, Kleiner DE. et al. Endpoints and clinical trial design for nonalcoholic steatohepatitis. Hepatology 2011; 54 (01) 344-353
  • 22 Yokoo T, Serai SD, Pirasteh A. et al; RSNA-QIBA PDFF Biomarker Committee. Linearity, bias, and precision of hepatic proton density fat fraction measurements by using MR imaging: a meta-analysis. Radiology 2018; 286 (02) 486-498
  • 23 Park CC, Nguyen P, Hernandez C. 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 (03) 598-607.e2
  • 24 Tang A, Tan J, Sun M. et al. Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology 2013; 267 (02) 422-431
  • 25 Martí-Aguado D, Jiménez-Pastor A, Alberich-Bayarri Á. et al. Automated whole-liver MRI segmentation to assess steatosis and iron quantification in chronic liver disease. Radiology 2022; 302 (02) 345-354
  • 26 McDonald N, Eddowes PJ, Hodson J. et al. Multiparametric magnetic resonance imaging for quantitation of liver disease: a two-centre cross-sectional observational study. Sci Rep 2018; 8 (01) 9189
  • 27 Nogami A, Yoneda M, Iwaki M. et al. Diagnostic comparison of vibration-controlled transient elastography and MRI techniques in overweight and obese patients with NAFLD. Sci Rep 2022; 12 (01) 21925
  • 28 Kim BK, Bernstein N, Huang DQ. et al. Clinical and histologic factors associated with discordance between steatosis grade derived from histology vs. MRI-PDFF in NAFLD. Aliment Pharmacol Ther 2023; 58 (02) 229-237
  • 29 Noureddin M, Lam J, Peterson MR. et al. Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials. Hepatology 2013; 58 (06) 1930-1940
  • 30 Fowler KJ, Venkatesh SK, Obuchowski N. et al. Repeatability of MRI biomarkers in nonalcoholic fatty liver disease: the NIMBLE consortium. Radiology 2023; 309 (01) e231092
  • 31 Hooker JC, Hamilton G, Park CC. et al. Inter-reader agreement of magnetic resonance imaging proton density fat fraction and its longitudinal change in a clinical trial of adults with nonalcoholic steatohepatitis. Abdom Radiol (NY) 2019; 44 (02) 482-492
  • 32 Pournik O, Alavian SM, Ghalichi L. et al. Inter-observer and intra-observer agreement in pathological evaluation of non-alcoholic fatty liver disease suspected liver biopsies. Hepat Mon 2014; 14 (01) e15167
  • 33 Caussy C, Reeder SB, Sirlin CB, Loomba R. Noninvasive, quantitative assessment of liver fat by MRI-PDFF as an endpoint in NASH trials. Hepatology 2018; 68 (02) 763-772
  • 34 Diefenbach MN, Liu C, Karampinos DC. Generalized parameter estimation in multi-echo gradient-echo-based chemical species separation. Quant Imaging Med Surg 2020; 10 (03) 554-567
  • 35 Leporq B, Lambert SA, Ronot M, Vilgrain V, Van Beers BE. Quantification of the triglyceride fatty acid composition with 3.0 T MRI. NMR Biomed 2014; 27 (10) 1211-1221
  • 36 Schneider M, Janas G, Lugauer F. et al. Accurate fatty acid composition estimation of adipose tissue in the abdomen based on bipolar multi-echo MRI. Magn Reson Med 2019; 81 (04) 2330-2346
  • 37 Fridén M, Rosqvist F, Ahlström H. et al. Hepatic unsaturated fatty acids are linked to lower degree of fibrosis in non-alcoholic fatty liver disease. Front Med (Lausanne) 2022; 8: 814951
  • 38 Vilar-Gomez E, Calzadilla-Bertot L, Wai-Sun Wong V. et al. Fibrosis severity as a determinant of cause-specific mortality in patients with advanced nonalcoholic fatty liver disease: a multi-national cohort study. Gastroenterology 2018; 155 (02) 443-457.e17
  • 39 Marti-Aguado D, Rodríguez-Ortega A, Alberich-Bayarri A, Marti-Bonmati L. Magnetic resonance imaging analysis of liver fibrosis and inflammation: overwhelming gray zones restrict clinical use. Abdom Radiol (NY) 2020; 45 (11) 3557-3568
  • 40 Caldwell S, Ikura Y, Dias D. et al. Hepatocellular ballooning in NASH. J Hepatol 2010; 53 (04) 719-723
  • 41 Alsaqal S, Hockings P, Ahlström H. et al. The combination of MR elastography and proton density fat fraction improves diagnosis of nonalcoholic steatohepatitis. J Magn Reson Imaging 2021; DOI: 10.1002/jmri.28040.
  • 42 Loomba R, Neuschwander-Tetri BA, Sanyal A. et al; NASH Clinical Research Network. Multicenter validation of association between decline in MRI-PDFF and histologic response in NASH. Hepatology 2020; 72 (04) 1219-1229
  • 43 Dennis A, Kelly MD, Fernandes C. et al. Correlations between MRI biomarkers PDFF and cT1 with histopathological features of non-alcoholic steatohepatitis. Front Endocrinol (Lausanne) 2021; 11: 575843
  • 44 Jayakumar S, Middleton MS, Lawitz EJ. et al. Longitudinal correlations between MRE, MRI-PDFF, and liver histology in patients with non-alcoholic steatohepatitis: analysis of data from a phase II trial of selonsertib. J Hepatol 2019; 70 (01) 133-141
  • 45 Pepin KM, Welle CL, Guglielmo FF, Dillman JR, Venkatesh SK. Magnetic resonance elastography of the liver: everything you need to know to get started. Abdom Radiol (NY) 2022; 47 (01) 94-114
  • 46 Manduca A, Bayly PJ, Ehman RL. et al. MR elastography: principles, guidelines, and terminology. Magn Reson Med 2021; 85 (05) 2377-2390
  • 47 Allen AM, Shah VH, Therneau TM. 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 (02) 510-521
  • 48 Yin M, Glaser KJ, Manduca A. et al. Distinguishing between hepatic inflammation and fibrosis with MR elastography. Radiology 2017; 284 (03) 694-705
  • 49 Ichikawa S, Motosugi U, Nakazawa T. et al. Hepatitis activity should be considered a confounder of liver stiffness measured with MR elastography. J Magn Reson Imaging 2015; 41 (05) 1203-1208
  • 50 von Ulmenstein S, Bogdanovic S, Honcharova-Biletska H. et al. Assessment of hepatic fibrosis and inflammation with look-locker T1 mapping and magnetic resonance elastography with histopathology as reference standard. Abdom Radiol (NY) 2022; 47 (11) 3746-3757
  • 51 Shi Y, Qi YF, Lan GY. et al. Three-dimensional MR elastography depicts liver inflammation, fibrosis, and portal hypertension in chronic hepatitis B or C. Radiology 2021; 301 (01) 154-162
  • 52 Dzyubak B, Li J, Chen J. et al. Automated analysis of multiparametric magnetic resonance imaging/magnetic resonance elastography exams for prediction of nonalcoholic steatohepatitis. J Magn Reson Imaging 2021; 54 (01) 122-131
  • 53 Breit HC, Block KT, Winkel DJ. et al. Evaluation of liver fibrosis and cirrhosis on the basis of quantitative T1 mapping: Are acute inflammation, age and liver volume confounding factors?. Eur J Radiol 2021; 141: 109789
  • 54 Hoad CL, Palaniyappan N, Kaye P. et al. A study of T1 relaxation time as a measure of liver fibrosis and the influence of confounding histological factors. NMR Biomed 2015; 28 (06) 706-714
  • 55 Eddowes PJ, McDonald N, Davies N. et al. Utility and cost evaluation of multiparametric magnetic resonance imaging for the assessment of non-alcoholic fatty liver disease. Aliment Pharmacol Ther 2018; 47 (05) 631-644
  • 56 Wan Q, Peng H, Lyu J. et al. Water specific MRI T1 mapping for evaluating liver inflammation activity grades in rats with methionine-choline-deficient diet-induced nonalcoholic fatty liver disease. J Magn Reson Imaging 2022; 56 (05) 1429-1436
  • 57 Welle CL, Guglielmo FF, Venkatesh SK. MRI of the liver: choosing the right contrast agent. Abdom Radiol (NY) 2020; 45 (02) 384-392
  • 58 Ulloa JL, Stahl S, Yates J. et al. Assessment of gadoxetate DCE-MRI as a biomarker of hepatobiliary transporter inhibition. NMR Biomed 2013; 26 (10) 1258-1270
  • 59 Yamada T, Obata A, Kashiwagi Y. et al. Gd-EOB-DTPA-enhanced-MR imaging in the inflammation stage of nonalcoholic steatohepatitis (NASH) in mice. Magn Reson Imaging 2016; 34 (06) 724-729
  • 60 Ba-Ssalamah A, Bastati N, Wibmer A. et al. Hepatic gadoxetic acid uptake as a measure of diffuse liver disease: Where are we?. J Magn Reson Imaging 2017; 45 (03) 646-659
  • 61 Eming SA, Wynn TA, Martin P. Inflammation and metabolism in tissue repair and regeneration. Science 2017; 356 (6342) 1026-1030
  • 62 Schuppan D, Surabattula R, Wang XY. Determinants of fibrosis progression and regression in NASH. J Hepatol 2018; 68 (02) 238-250
  • 63 Rohm TV, Meier DT, Olefsky JM, Donath MY. Inflammation in obesity, diabetes, and related disorders. Immunity 2022; 55 (01) 31-55
  • 64 Parthasarathy G, Revelo X, Malhi H. Pathogenesis of nonalcoholic steatohepatitis: an overview. Hepatol Commun 2020; 4 (04) 478-492
  • 65 Schwabe RF, Tabas I, Pajvani UB. Mechanisms of fibrosis development in nonalcoholic steatohepatitis. Gastroenterology 2020; 158 (07) 1913-1928
  • 66 Marra F, Svegliati-Baroni G. Lipotoxicity and the gut-liver axis in NASH pathogenesis. J Hepatol 2018; 68 (02) 280-295
  • 67 De Minicis S, Rychlicki C, Agostinelli L. et al. Dysbiosis contributes to fibrogenesis in the course of chronic liver injury in mice. Hepatology 2014; 59 (05) 1738-1749
  • 68 Lade A, Noon LA, Friedman SL. Contributions of metabolic dysregulation and inflammation to nonalcoholic steatohepatitis, hepatic fibrosis, and cancer. Curr Opin Oncol 2014; 26 (01) 100-107
  • 69 Hagström H, Nasr P, Ekstedt M. et al. Fibrosis stage but not NASH predicts mortality and time to development of severe liver disease in biopsy-proven NAFLD. J Hepatol 2017; 67 (06) 1265-1273
  • 70 Parola M, Pinzani M. Liver fibrosis: pathophysiology, pathogenetic targets and clinical issues. Mol Aspects Med 2019; 65: 37-55
  • 71 Imajo K, Honda Y, Kobayashi T. et al. Direct comparison of US and MR elastography for staging liver fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2022; 20 (04) 908-917.e11
  • 72 Cui J, Heba E, Hernandez C. et al. Magnetic resonance elastography is superior to acoustic radiation force impulse for the diagnosis of fibrosis in patients with biopsy-proven nonalcoholic fatty liver disease: a prospective study. Hepatology 2016; 63 (02) 453-461
  • 73 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 (06) 1920-1928
  • 74 Costa-Silva L, Ferolla SM, Lima AS, Vidigal PVT, Ferrari TCA. MR elastography is effective for the non-invasive evaluation of fibrosis and necroinflammatory activity in patients with nonalcoholic fatty liver disease. Eur J Radiol 2018; 98: 82-89
  • 75 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 (07) 986-994
  • 76 Hoffman DH, Ayoola A, Nickel D, Han F, Chandarana H, Shanbhogue KP. T1 mapping, T2 mapping and MR elastography of the liver for detection and staging of liver fibrosis. Abdom Radiol (NY) 2020; 45 (03) 692-700
  • 77 Huwart L, Sempoux C, Vicaut E. et al. Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology 2008; 135 (01) 32-40
  • 78 Venkatesh SK, Yin M, Ehman RL. Magnetic resonance elastography of liver: technique, analysis, and clinical applications. J Magn Reson Imaging 2013; 37 (03) 544-555
  • 79 Taylor AJ, Salerno M, Dharmakumar R, Jerosch-Herold M. T1 mapping: basic techniques and clinical applications. JACC Cardiovasc Imaging 2016; 9 (01) 67-81
  • 80 Banerjee R, Pavlides M, Tunnicliffe EM. et al. Multiparametric magnetic resonance for the non-invasive diagnosis of liver disease. J Hepatol 2014; 60 (01) 69-77
  • 81 Mózes FE, Tunnicliffe EM. Differences between T1 and corrected T1 cannot be attributed to iron-correction only. Pediatr Radiol 2021; 51 (03) 499-500
  • 82 Pavlides M, Banerjee R, Tunnicliffe EM. et al. Multiparametric magnetic resonance imaging for the assessment of non-alcoholic fatty liver disease severity. Liver Int 2017; 37 (07) 1065-1073
  • 83 Perspectum. (2024). LiverMultiScan v5.0 UK/EU – A Guide to Interpreting LiverMultiScan for Physicians (v1.0 CURRENT) [ENG]. Perspectum. Accessed June 10, 2024, At https://www.perspectum.com/our-products/pdf-library?product-type=LiverMultiScan
  • 84 Beer L, Mandorfer M, Bastati N. et al. Inter- and intra-reader agreement for gadoxetic acid-enhanced MRI parameter readings in patients with chronic liver diseases. Eur Radiol 2019; 29 (12) 6600-6610
  • 85 Verloh N, Utpatel K, Haimerl M. et al. Liver fibrosis and Gd-EOB-DTPA-enhanced MRI: a histopathologic correlation. Sci Rep 2015; 5: 15408
  • 86 Ringe KI, Husarik DB, Gupta RT, Boll DT, Merkle EM. Hepatobiliary transit times of gadoxetate disodium (Primovist®) for protocol optimization of comprehensive MR imaging of the biliary system – what is normal?. Eur J Radiol 2011; 79 (02) 201-205
  • 87 Tsuda N, Okada M, Murakami T. New proposal for the staging of nonalcoholic steatohepatitis: evaluation of liver fibrosis on Gd-EOB-DTPA-enhanced MRI. Eur J Radiol 2010; 73 (01) 137-142
  • 88 Tsuda N, Matsui O. Signal profile on Gd-EOB-DTPA-enhanced MR imaging in non-alcoholic steatohepatitis and liver cirrhosis induced in rats: correlation with transporter expression. Eur Radiol 2011; 21 (12) 2542-2550
  • 89 Chen B-B, Hsu CY, Yu CW. et al. Dynamic contrast-enhanced magnetic resonance imaging with Gd-EOB-DTPA for the evaluation of liver fibrosis in chronic hepatitis patients. Eur Radiol 2012; 22 (01) 171-180
  • 90 Koh D-M, Ba-Ssalamah A, Brancatelli G. et al. Consensus report from the 9th International Forum for Liver Magnetic Resonance Imaging: applications of gadoxetic acid-enhanced imaging. Eur Radiol 2021; 31 (08) 5615-5628
  • 91 Schneider CV, Schneider KM, Raptis A, Huang H, Trautwein C, Loomba R. Prevalence of at-risk MASH, MetALD and alcohol-associated steatotic liver disease in the general population. Aliment Pharmacol Ther 2024; 59 (10) 1271-1281
  • 92 Loomba R, Lawitz EJ, Frias JP. et al. Safety, pharmacokinetics, and pharmacodynamics of pegozafermin in patients with non-alcoholic steatohepatitis: a randomised, double-blind, placebo-controlled, phase 1b/2a multiple-ascending-dose study. Lancet Gastroenterol Hepatol 2023; 8 (02) 120-132
  • 93 Nedrud MA, Chaudhry M, Middleton MS. et al. MRI quantification of placebo effect in nonalcoholic steatohepatitis clinical trials. Radiology 2023; 306 (03) e220743
  • 94 Stine JG, Munaganuru N, Barnard A. 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 (11) 2274-2283.e5
  • 95 Lee SW, Huang DQ, Bettencourt R. et al. Low liver fat in non-alcoholic steatohepatitis-related significant fibrosis and cirrhosis is associated with hepatocellular carcinoma, decompensation and mortality. Aliment Pharmacol Ther 2024; 59 (01) 80-88
  • 96 Ajmera V, Kim BK, Yang K. et al. Liver stiffness on magnetic resonance elastography and the MEFIB index and liver-related outcomes in nonalcoholic fatty liver disease: a systematic review and meta-analysis of individual participants. Gastroenterology 2022; 163 (04) 1079-1089.e5
  • 97 Ajmera V, Nguyen K, Tamaki N, Sharpton S, Bettencourt R, Loomba R. Prognostic utility of magnetic resonance elastography and MEFIB index in predicting liver-related outcomes and mortality in individuals at risk of and with nonalcoholic fatty liver disease. Therap Adv Gastroenterol 2022; 15: 17 562848221093869
  • 98 Kim BK, Bergstrom J, Loomba R. et al. Magnetic resonance elastography-based prediction model for hepatic decompensation in NAFLD: a multicenter cohort study. Hepatology 2023; 78 (06) 1858-1866
  • 99 Nogami A, Yoneda M, Iwaki M. et al. Noninvasive imaging biomarkers for liver steatosis in NAFLD: present and future. Clin Mol Hepatol 2023; 29: S123-S135
  • 100 2_National_schedule_of_NHS_costs_FY21–22_v3.xlsx. https://view.officeapps.live.com/op/view.aspx?src=https%3A%2F%2Fwww.england.nhs.uk%2Fwp-content%2Fuploads%2F2023%2F04%2F2_National_schedule_of_NHS_costs_FY21-22_v3.xlsx&wdOrigin=BROWSELINK
  • 101 Vilar-Gomez E, Lou Z, Kong N, Vuppalanchi R, Imperiale TF, Chalasani N. Cost effectiveness of different strategies for detecting cirrhosis in patients with nonalcoholic fatty liver disease based on United States health care system. Clin Gastroenterol Hepatol 2020; 18 (10) 2305-2314.e12
  • 102 Loomba R, Amangurbanova M, Bettencourt R. et al. MASH Resolution Index: development and validation of a non-invasive score to detect histological resolution of MASH. Gut 2024; DOI: 10.1136/gutjnl-2023-331401.
  • 103 Huang DQ, Sharpton SR, Amangurbanova M, Tamaki N, Sirlin CB, Loomba R. NAFLD Research Study Group. Clinical utility of combined MRI-PDFF and ALT response in predicting histologic response in nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2023; 21 (10) 2682-2685.e4
  • 104 Noureddin M, Truong E, Gornbein JA. et al. MRI-based (MAST) score accurately identifies patients with NASH and significant fibrosis. J Hepatol 2022; 76 (04) 781-787
  • 105 Tamaki N, Imajo K, Sharpton S. et al. Magnetic resonance elastography plus fibrosis-4 versus FibroScan-aspartate aminotransferase in detection of candidates for pharmacological treatment of NASH-related fibrosis. Hepatology 2022; 75 (03) 661-672
  • 106 Noureddin N, Ajmera V, Bergstrom J. et al. MEFIB-Index and MAST-score in the assessment of hepatic decompensation in metabolic dysfunction-associated steatosis liver disease-Individual participant data meta-analyses. Aliment Pharmacol Ther 2023; 58 (09) 856-865
  • 107 Brand T, van den Munckhof ICL, van der Graaf M. et al. Superficial vs deep subcutaneous adipose tissue: sex-specific associations with hepatic steatosis and metabolic traits. J Clin Endocrinol Metab 2021; 106 (10) e3881-e3889
  • 108 Idilman IS, Low HM, Gidener T. et al. Association between visceral adipose tissue and non-alcoholic steatohepatitis histology in patients with known or suspected non-alcoholic fatty liver disease. J Clin Med 2021; 10 (12) 2565
  • 109 Tordjman J, Guerre-Millo M, Clément K. Adipose tissue inflammation and liver pathology in human obesity. Diabetes Metab 2008; 34 (6, Pt 2): 658-663
  • 110 Mauro E, Gadano A. What's new in portal hypertension?. Liver Int 2020; 40 (Suppl. 01) 122-127
  • 111 Ronot M, Lambert S, Elkrief L. et al. Assessment of portal hypertension and high-risk oesophageal varices with liver and spleen three-dimensional multifrequency MR elastography in liver cirrhosis. Eur Radiol 2014; 24 (06) 1394-1402