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Liver surface nodularity on non-contrast MRI identifies advanced fibrosis in patients with NAFLD

  • Gastrointestinal
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An Editorial Comment to this article was published on 27 January 2022

Abstract

Objectives

To evaluate the diagnostic performance of liver surface nodularity (LSN) for the assessment of advanced fibrosis in patients with non-alcoholic fatty liver disease (NAFLD).

Methods

We retrospectively analysed patients with pathologically proven NAFLD who underwent liver MRI. Demographic, clinical, and laboratory data (including FIB-4 scores) were gathered. The SAF score was used to assess NAFLD. MRI-proton density fat fraction (PDFF) and LSN were determined on pre-contrast MR sequences. ROC curve analysis was performed to evaluate the diagnostic performance of MRI-LSN for the diagnosis of advanced (F3-F4) liver fibrosis.

Results

The final population included 142 patients. Sixty-seven (47%) patients had non-alcoholic steatohepatitis (NASH), and 52 (37%) had advanced fibrosis. The median MRI-PDFF increased with the grades of steatosis: 8.1%, 18.1%, and 31% in S1, S2, and S3 patients, respectively (p < 0.001). The area under the ROC curve (AUC) of MRI-LSN ≥ 2.50 was 0.838 (95%CI 0.767–0.894, sensitivity 67.3%, specificity 88.9%, positive and negative predictive values 77.8% and 82.5%, respectively) for the diagnosis of advanced fibrosis. Combining FIB-4 and MRI-LSN correctly classified 103/142 (73%) patients. This was validated in an external cohort of 75 patients.

Conclusions

MRI-LSN has good diagnostic performance in diagnosis of advanced fibrosis in NAFLD patients. A combination of FIB-4 and MRI-LSN derived from pre-contrast MRI could be helpful to detect advanced fibrosis.

Key Points

• MRI-LSN ≥ 2.5 was accurate for the diagnosis of advanced hepatic fibrosis in NAFLD patients.

• The combination of FIB-4 and MRI-LSN improved the detection of advanced fibrosis.

• MRI-LSN can be easily derived by unenhanced MRI sequences that are routinely acquired.

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Abbreviations

FIB-4:

Fibrosis-4

LSN:

Liver surface nodularity

MRI:

Magnetic resonance imaging

NAFLD:

Non-alcoholic fatty liver disease

NASH:

Non-alcoholic steatohepatitis

PDFF:

Proton density fat fraction

References

  1. Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M (2016) Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 64:73–84. https://doi.org/10.1002/hep.28431

    Article  PubMed  Google Scholar 

  2. Bedossa P (2014) Utility and appropriateness of the fatty liver inhibition of progression (FLIP) algorithm and steatosis, activity, and fibrosis (SAF) score in the evaluation of biopsies of nonalcoholic fatty liver disease. Hepatology 60:565–575. https://doi.org/10.1002/hep.27173

    Article  CAS  PubMed  Google Scholar 

  3. Sheka AC, Adeyi O, Thompson J, Hameed B, Crawford PA, Ikramuddin S (2020) Nonalcoholic steatohepatitis: a review. JAMA 323:1175–1183. https://doi.org/10.1001/jama.2020.2298

    Article  CAS  PubMed  Google Scholar 

  4. Schattenberg JM, Lazarus JV, Newsome PN et al (2021) Disease burden and economic impact of diagnosed non-alcoholic steatohepatitis in five European countries in 2018: a cost-of-illness analysis. Liver Int 41:1227–1242. https://doi.org/10.1111/liv.14825

    Article  PubMed  PubMed Central  Google Scholar 

  5. Caussy C, Reeder SB, Sirlin CB, Loomba R (2018) Noninvasive, quantitative assessment of liver fat by MRI-PDFF as an endpoint in NASH trials. Hepatology 68:763–772. https://doi.org/10.1002/hep.29797

    Article  PubMed  Google Scholar 

  6. Berzigotti A, Tsochatzis E, Boursier J et al (2021) EASL Clinical Practice Guidelines on non-invasive tests for evaluation of liver disease severity and prognosis – 2021 update. J Hepatol. https://doi.org/10.1016/j.jhep.2021.05.025

    Article  PubMed  Google Scholar 

  7. Allen AM, Shah VH, Therneau TM et al (2018) The role of three-dimensional magnetic resonance elastography in the diagnosis of nonalcoholic steatohepatitis in obese patients undergoing bariatric surgery. Hepatology. https://doi.org/10.1002/hep.30483

    Article  PubMed  Google Scholar 

  8. van Werven JR, Schreuder TCMA, Aarts EO et al (2011) Hepatic steatosis in morbidly obese patients undergoing gastric bypass surgery: assessment with open-system 1H-MR spectroscopy. AJR Am J Roentgenol 196:W736-742. https://doi.org/10.2214/AJR.10.5215

    Article  PubMed  Google Scholar 

  9. Angulo P, Kleiner DE, Dam-Larsen S et al (2015) Liver fibrosis, but no other histologic features, is associated with long-term outcomes of patients with nonalcoholic fatty liver disease. Gastroenterology 149:389-397.e10. https://doi.org/10.1053/j.gastro.2015.04.043

    Article  PubMed  Google Scholar 

  10. Ekstedt M, Hagström H, Nasr P et al (2015) Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology 61:1547–1554. https://doi.org/10.1002/hep.27368

    Article  CAS  PubMed  Google Scholar 

  11. Imajo K, Kessoku T, Honda Y et al (2016) Magnetic resonance imaging more accurately classifies steatosis and fibrosis in patients with nonalcoholic fatty liver disease than transient elastography. Gastroenterology 150:626-637.e7. https://doi.org/10.1053/j.gastro.2015.11.048

    Article  PubMed  Google Scholar 

  12. Akkaya HE, Erden A, Kuru Öz D, Ünal S, Erden İ (2018) Magnetic resonance elastography: basic principles, technique, and clinical applications in the liver. Diagn Interv Radiol 24:328–335. https://doi.org/10.5152/dir.2018.18186

    Article  PubMed  PubMed Central  Google Scholar 

  13. Smith AD, Branch CR, Zand K et al (2016) Liver surface nodularity quantification from routine CT images as a biomarker for detection and evaluation of cirrhosis. Radiology 280:771–781. https://doi.org/10.1148/radiol.2016151542

    Article  PubMed  Google Scholar 

  14. Sartoris R, Rautou P-E, Elkrief L et al (2018) Quantification of liver surface nodularity at CT: utility for detection of portal hypertension. Radiology 289:698–707. https://doi.org/10.1148/radiol.2018181131

    Article  PubMed  Google Scholar 

  15. De Vos N, Sartoris R, Cauchy F, Rautou PE, Vilgrain V, Ronot M (2020) Performance of liver surface nodularity quantification for the diagnosis of portal hypertension in patients with cirrhosis: comparison between MRI with hepatobiliary phase sequences and CT. Abdom Radiol (NY) 45:365–372. https://doi.org/10.1007/s00261-019-02355-y

    Article  Google Scholar 

  16. Besa C, Wagner M, Lo G et al (2018) Detection of liver fibrosis using qualitative and quantitative MR elastography compared to liver surface nodularity measurement, gadoxetic acid uptake, and serum markers. J Magn Reson Imaging 47:1552–1561. https://doi.org/10.1002/jmri.25911

    Article  PubMed  Google Scholar 

  17. EASL-EASD-EASO (2016) Clinical practice guidelines for the management of non-alcoholic fatty liver disease. J Hepatol 64:1388–402. https://doi.org/10.1016/j.jhep.2015.11.004

    Article  Google Scholar 

  18. Kim WR, Berg T, Asselah T et al (2016) Evaluation of APRI and FIB-4 scoring systems for non-invasive assessment of hepatic fibrosis in chronic hepatitis B patients. J Hepatol 64:773–780. https://doi.org/10.1016/j.jhep.2015.11.012

    Article  CAS  PubMed  Google Scholar 

  19. Brunt EM, Kleiner DE, Wilson LA et al (2011) The NAS and the histopathologic diagnosis in NAFLD: distinct clinicopathologic meanings. Hepatology 53:810–820. https://doi.org/10.1002/hep.24127

    Article  CAS  PubMed  Google Scholar 

  20. Kleiner DE, Brunt EM, Natta MV et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313–1321. https://doi.org/10.1002/hep.20701

    Article  PubMed  Google Scholar 

  21. Smith AD, Zand KA, Florez E et al (2016) Liver surface nodularity score allows prediction of cirrhosis decompensation and death. Radiology 283:711–722. https://doi.org/10.1148/radiol.2016160799

    Article  PubMed  Google Scholar 

  22. Sartoris R, Lazareth M, Nivolli A, Burgio MD, Vilgrain V, Ronot M (2020) CT-based liver surface nodularity for the detection of clinically significant portal hypertension: defining measurement quality criteria. Abdom Radiol (NY). https://doi.org/10.1007/s00261-020-02519-1

    Article  Google Scholar 

  23. Mózes FE, Lee JA, Selvaraj EA et al (2021) Diagnostic accuracy of non-invasive tests for advanced fibrosis in patients with NAFLD: an individual patient data meta-analysis. Gut. https://doi.org/10.1136/gutjnl-2021-324243

    Article  PubMed  Google Scholar 

  24. Castera L, Friedrich-Rust M, Loomba R (2019) Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology 156:1264-1281.e4. https://doi.org/10.1053/j.gastro.2018.12.036

    Article  PubMed  Google Scholar 

  25. Costa-Silva L, Ferolla SM, Lima AS, Vidigal PVT, de Abreu Ferrari TC (2018) MR elastography is effective for the non-invasive evaluation of fibrosis and necroinflammatory activity in patients with nonalcoholic fatty liver disease. Eur J Radiol 98:82–89. https://doi.org/10.1016/j.ejrad.2017.11.003

    Article  PubMed  Google Scholar 

  26. Yin M, Talwalkar JA, Glaser KJ et al (2007) Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 5:1207-1213.e2. https://doi.org/10.1016/j.cgh.2007.06.012

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kim DW, Kim SY, Yoon HM, Kim KW, Byun JH (2020) Comparison of technical failure of MR elastography for measuring liver stiffness between gradient-recalled echo and spin-echo echo-planar imaging: a systematic review and meta-analysis. J Magn Reson Imaging 51:1086–1102. https://doi.org/10.1002/jmri.26918

    Article  PubMed  Google Scholar 

  28. Wagner M, Corcuera-Solano I, Lo G et al (2017) Technical failure of MR elastography examinations of the liver: experience from a large single-center study. Radiology 284:401–412. https://doi.org/10.1148/radiol.2016160863

    Article  PubMed  Google Scholar 

  29. Kim T-H, Kim JE, Ryu J-H, Jeong C-W (2019) Development of liver surface nodularity quantification program and its clinical application in nonalcoholic fatty liver disease. Sci Rep 9:9994. https://doi.org/10.1038/s41598-019-46442-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Catania R, Furlan A, Smith AD, Behari J, Tublin ME, Borhani AA (2020) Diagnostic value of MRI-derived liver surface nodularity score for the non-invasive quantification of hepatic fibrosis in non-alcoholic fatty liver disease. Eur Radiol. https://doi.org/10.1007/s00330-020-07114-y

    Article  PubMed  Google Scholar 

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Funding

The authors state that this work has not received any funding.

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Authors and Affiliations

  1. INSERM U1149 “Centre de Recherche Sur L’inflammation”, CRI, Université de Paris, 75018, Paris, France

    Marco Dioguardi Burgio, Riccardo Sartoris, Pierre-Emmanuel Rautou, Valérie Paradis, Valérie Vilgrain & Maxime Ronot

  2. Department of Radiology, AP-HP.Nord, Hôpital Beaujon, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Marco Dioguardi Burgio, Riccardo Sartoris, Jules Grégory, Valérie Vilgrain & Maxime Ronot

  3. Department of Pathology, AP-HP.Nord, Hôpital Beaujon, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Aurélie Beaufrere & Valérie Paradis

  4. INSERM, UMR1153, Epidemiology and Biostatistics Sorbonne Paris Cité Center (CRESS), METHODS team, Hôpital Hôtel Dieu, F-75004, Paris, France

    Jules Grégory

  5. Department of Radiology, St-Éloi University Hospital, 34980, Montpellier, France

    Boris Guiu & Chloé Guillot

  6. Department of Hepatology, AP-HP.Nord, Hôpital Beaujon, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Pierre-Emmanuel Rautou & Laurent Castera

  7. Department of Digestive Oncology, AP-HP.Nord, Hôpital Beaujon, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Mohamed Bouattour

Authors
  1. Marco Dioguardi Burgio
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  7. Pierre-Emmanuel Rautou
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  9. Mohamed Bouattour
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  10. Valérie Paradis
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  11. Valérie Vilgrain
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  12. Maxime Ronot
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Corresponding author

Correspondence to Marco Dioguardi Burgio.

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The scientific guarantor of this publication is Maxime Ronot.

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The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors has significant statistical expertise; moreover, no complex statistical methods were necessary for this paper.

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• retrospective

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• multicenter study

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Dioguardi Burgio, M., Sartoris, R., Beaufrere, A. et al. Liver surface nodularity on non-contrast MRI identifies advanced fibrosis in patients with NAFLD. Eur Radiol 32, 1781–1791 (2022). https://doi.org/10.1007/s00330-021-08261-6

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