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Liver stiffness measurement by magnetic resonance elastography is not affected by hepatic steatosis

  • Gastrointestinal
  • Published:
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Abstract

Objectives

To evaluate the relationship between biopsy-assessed hepatic steatosis, magnetic resonance imaging (MRI)–assessed proton density fat fraction (PDFF), and magnetic resonance elastography (MRE)–assessed liver stiffness measurement (LSM), in patients with or at risk for nonalcoholic fatty liver disease (NAFLD).

Methods

A retrospective study was performed, encompassing 256 patients who had a liver biopsy and MRI/MRE examination performed within 1 year. Clinical and laboratory data were retrieved from the electronic medical record. Hepatic steatosis and fibrosis were assessed by histopathological grading/staging. First, we analyzed the diagnostic performance of PDFF for distinguishing hepatic steatosis with the receiver operating characteristic analyses. Second, variables influencing LSM were screened with univariant analyses, then identified with multivariable linear regression. Finally, the potential relationship between PDFF and LSM was assessed with linear regression after adjustment for other influencing factors, in patients with diagnosed steatosis (PDFF ≥ 5%).

Results

The diagnostic accuracy of PDFF in distinguishing steatosis grades (S0-3) was above 0.82. No significant difference in LSM was found between patients with S1, S2, and S3 steatosis and between all steatosis grades after patients were grouped according to fibrosis stage. No statistically significant relationship was found between the LSM and PDFF (estimate =  − 0.02, p = 0.065) after adjustment for fibrosis stage and age in patients with diagnosed steatosis (PDFF ≥ 5%).

Conclusions

In patients with NAFLD, the severity of hepatic steatosis has no significant influence on the liver stiffness measurement with magnetic resonance elastography.

Key Points

• The MRI-based proton density fat fraction provides a quantitative assessment of hepatic steatosis with high accuracy.

• No significant effect of hepatic steatosis on MRE-based liver stiffness measurement was found in patients with S1, S2, and S3 steatosis and between all steatosis grades after patients were grouped according to fibrosis stage.

• After adjusting for fibrosis stage and age, there was no statistically significant relationship between liver stiffness and proton density fat fraction in patients with hepatic steatosis (p = 0.065).

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Abbreviations

AUROC:

Areas under the receiver operating characteristic curve

LSM:

Liver stiffness measurement

MRE:

Magnetic resonance elastography

NAFLD:

Nonalcoholic fatty liver disease

NASH:

Nonalcoholic 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

    Article  Google Scholar 

  2. Lindenmeyer CC, McCullough AJ (2018) The Natural History of Nonalcoholic Fatty Liver Disease-An Evolving View. Clin Liver Dis 22:11–21

    Article  Google Scholar 

  3. Önnerhag K, Nilsson PM, Lindgren S (2014) Increased risk of cirrhosis and hepatocellular cancer during long-term follow-up of patients with biopsy-proven NAFLD. Scand J Gastroenterol 49:1111–1118

    Article  Google Scholar 

  4. Ekstedt M, Franzén LE, Mathiesen UL et al (2006) Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology 44:865–873

    Article  CAS  Google Scholar 

  5. Pais R, Pascale A, Fedchuck L, Charlotte F, Poynard T, Ratziu V (2011) Progression from isolated steatosis to steatohepatitis and fibrosis in nonalcoholic fatty liver disease. Clin Res Hepatol Gastroenterol 35:23–28

    Article  CAS  Google Scholar 

  6. 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.e310

    Article  Google Scholar 

  7. Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G (2017) Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology 66:1486–1501

    Article  CAS  Google Scholar 

  8. Staufer K, Halilbasic E, Spindelboeck W et al (2019) Evaluation and comparison of six noninvasive tests for prediction of significant or advanced fibrosis in nonalcoholic fatty liver disease. United European Gastroenterol J 7:1113–1123

    Article  Google Scholar 

  9. Xu XY, Wang WS, Zhang QM et al (2019) Performance of common imaging techniques vs serum biomarkers in assessing fibrosis in patients with chronic hepatitis B: a systematic review and meta-analysis. World J Clin Cases 7:2022–2037

    Article  Google Scholar 

  10. 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.e627

    Article  Google Scholar 

  11. Park CC, Nguyen P, Hernandez C et al (2017) 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 152:598-607.e592

    Article  Google Scholar 

  12. Tang A, Cloutier G, Szeverenyi NM, Sirlin CB (2015) Ultrasound elastography and MR elastography for assessing liver fibrosis: Part 2, Diagnostic performance, confounders, and future directions. AJR Am J Roentgenol 205:33–40

    Article  Google Scholar 

  13. Petta S, Maida M, Macaluso FS et al (2015) The severity of steatosis influences liver stiffness measurement in patients with nonalcoholic fatty liver disease. Hepatology 62:1101–1110

    Article  Google Scholar 

  14. Shen F, Mi YQ, Xu L et al (2019) Moderate to severe hepatic steatosis leads to overestimation of liver stiffness measurement in chronic hepatitis B patients without significant fibrosis. Aliment Pharmacol Ther 50:93–102

    Article  Google Scholar 

  15. Karlas T, Petroff D, Sasso M et al (2018) Impact of controlled attenuation parameter on detecting fibrosis using liver stiffness measurement. Aliment Pharmacol Ther 47:989–1000

    Article  CAS  Google Scholar 

  16. Joshi M, Dillman JR, Singh K et al (2018) Quantitative MRI of fatty liver disease in a large pediatric cohort: correlation between liver fat fraction, stiffness, volume, and patient-specific factors. Abdom Radiol (NY) 43:1168–1179

    Article  Google Scholar 

  17. Leitão HS, Doblas S, Garteiser P et al (2017) Hepatic Fibrosis, Inflammation, and Steatosis: Influence on the MR Viscoelastic and Diffusion Parameters in Patients with Chronic Liver Disease. Radiology 283:98–107

    Article  Google Scholar 

  18. Chen J, Talwalkar JA, Yin M, Glaser KJ, Sanderson SO, Ehman RL (2011) Early detection of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease by using MR elastography. Radiology 259:749–756

    Article  Google Scholar 

  19. Ratziu V, Charlotte F, Heurtier A et al (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 128:1898–1906

    Article  Google Scholar 

  20. Longerich T, Schirmacher P (2020) Determining the reliability of liver biopsies in NASH clinical studies. Nat Rev Gastroenterol Hepatol 17:653–654

    Article  Google Scholar 

  21. Reeder SB, Sirlin CB (2010) Quantification of liver fat with magnetic resonance imaging. Magn Reson Imaging Clin N Am 18:337–357 (ix)

    Article  Google Scholar 

  22. Gu J, Liu S, Du S et al (2019) Diagnostic value of MRI-PDFF for hepatic steatosis in patients with non-alcoholic fatty liver disease: a meta-analysis. Eur Radiol 29:3564–3573

    Article  Google Scholar 

  23. Chen J, Yin M, Talwalkar JA et al (2017) Diagnostic performance of MR elastography and vibration-controlled transient elastography in the detection of hepatic fibrosis in patients with severe to morbid obesity. Radiology 283:418–428

    Article  Google Scholar 

  24. Allen AM, Shah VH, Therneau TM et al (2020) The role of three-dimensional magnetic resonance elastography in the diagnosis of nonalcoholic steatohepatitis in obese patients undergoing bariatric surgery. Hepatology 71:510–521

    Article  Google Scholar 

  25. Gidener T, Ahmed OT, Larson JJ et al (2020) Liver stiffness by magnetic resonance elastography predicts future cirrhosis, decompensation and death in NAFLD. Clin Gastroenterol Hepatol. https://doi.org/10.1016/j.cgh.2020.09.044

    Article  PubMed  Google Scholar 

  26. Silva AM, Grimm RC, Glaser KJ et al (2015) Magnetic resonance elastography: evaluation of new inversion algorithm and quantitative analysis method. Abdom Imaging 40:810–817

    Article  Google Scholar 

  27. Dzyubak B, Venkatesh SK, Manduca A, Glaser KJ, Ehman RL (2016) Automated liver elasticity calculation for MR elastography. J Magn Reson Imaging 43:1055–1063

    Article  Google Scholar 

  28. Kleiner DE, Brunt EM, Van Natta M et al (2005) Nonalcoholic Steatohepatitis Clinical Research Network. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 41(6):1313–21. https://doi.org/10.1002/hep.20701. PMID: 15915461

  29. Brunt EM (2016) Nonalcoholic fatty liver disease: pros and cons of histologic systems of evaluation. Int J Mol Sci 13;17(1):97

  30. Eddowes PJ, Sasso M, Allison M et al (2019) Accuracy of FibroScan controlled attenuation parameter and liver stiffness measurement in assessing steatosis and fibrosis in patients with nonalcoholic fatty liver disease. Gastroenterology 156:1717–1730

    Article  Google Scholar 

  31. Hudert CA, Tzschätzsch H, Rudolph B et al (2021) How histopathologic changes in pediatric nonalcoholic fatty liver disease influence in vivo liver stiffness. Acta Biomater 123:178–186

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work has been supported by grant funding from the National Institutes of Health: R37 EB001981 (R.L.E.), R01 EB017197 (M.Y.), K23 DK115594 (A.M.A.), and the US Department of Defense: W81XWH-19-1-0583-01 (M.Y.). The author would like to thank Jennifer Kugel for providing language help for this manuscript.

Funding

This study has received grant funding from the National Institutes of Health: R37 EB001981 (R.L.E.), R01 EB017197 (M.Y.), K23 DK115594 (A.M.A.), and the US Department of Defense: W81XWH-19–1-0583–01 (M.Y.).

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Authors and Affiliations

  1. Department of Radiology, West China Hospital, Sichuan University, No.37 Guoxue Alley, Chengdu, 610041, China

    Jie Chen & Bin Song

  2. Department of Radiology, Mayo Clinic, 200 First Street SW, Rochester, MN, 55905, USA

    Jie Chen, Jun Chen, Jiahui Li, Safa Hoodeshenas, Jingbiao Chen, Xin Lu, Zheng Zhu, Sudhakar K. Venkatesh, Richard L. Ehman & Meng Yin

  3. Division of Gastroenterology and Hepatology, Mayo Clinic, 200 First Street SW, MN, 55905, Rochester, USA

    Alina M. Allen

  4. Division of Biomedical Statistics and Informatics, Mayo Clinic, 200 First Street SW, MN, 55905, Rochester, USA

    Terry M. Therneau

Authors
  1. Jie Chen
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Corresponding author

Correspondence to Meng Yin.

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Guarantor

The scientific guarantor of this publication is Richard L. Ehman (ehman.richard@mayo.edu,Tel: 1-(507)-284–9781, 200 First Street SW, Rochester, Minnesota 55905, United States).

Conflict of interest

The Mayo Clinic, Jun Chen, Richard L. Ehman, and Meng Yin have intellectual property and a financial interest related to our research in this work.

Statistics and biometry

Dr. Terry Therneau provided statistical advice and supervised Dr. Jie Chen to perform the statistical analyses.

Informed consent

Written informed consent was waived by the Institutional Review Board.

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Institutional Review Board approval was obtained.

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• retrospective

• diagnostic or prognostic study

• performed at one institution

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Chen, J., Allen, A.M., Therneau, T.M. et al. Liver stiffness measurement by magnetic resonance elastography is not affected by hepatic steatosis. Eur Radiol 32, 950–958 (2022). https://doi.org/10.1007/s00330-021-08225-w

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