Skip to main content
SpringerLink
Log in

Feasibility of a three-step magnetic resonance imaging approach for the assessment of hepatic steatosis in an asymptomatic study population

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To determine the feasibility of a multi-step magnetic resonance imaging (MRI) approach for comprehensive assessment of hepatic steatosis defined as liver fat content of ≥5 % in an asymptomatic population.

Methods

The study was approved by the institutional review board and written informed consent of all participants was obtained. Participants of a population-based study cohort underwent a three-step 3-T MRI-based assessment of liver fat. A dual-echo Dixon sequence was performed to identify subjects with hepatic steatosis, followed by a multi-echo Dixon sequence with proton density fat fraction estimation. Finally, single-voxel T2-corrected multi-echo spectroscopy was performed.

Results

A total of 215 participants completed the MRI protocol (56.3 % male, average age 57.2 ± 9.4 years). The prevalence of hepatic steatosis was 55 %. Mean liver proton density fat fraction was 9.2 ± 8.5 % by multi-echo Dixon and 9.3 ± 8.6 % by multi-echo spectroscopy (p = 0.51). Dual-echo Dixon overestimated liver fat fraction by 1.4 ± 2.0 % (p < 0.0001). All measurements showed excellent correlations (r ≥ 0.9, p < 0.001). Dual-echo Dixon was highly sensitive for the detection of hepatic steatosis (sensitivity 0.97, NPV 0.96) with good specificity and PPV (0.75 and 0.81, respectively).

Conclusions

A multi-step MRI approach may enable rapid and accurate identification of subjects with hepatic steatosis in an asymptomatic population.

Key Points

• Dual-echo Dixon can rapidly and reliably exclude hepatic steatosis without complex post-processing.

• Multi-echo Dixon and multi-echo spectroscopy yield similar results regarding hepatic fat quantification.

• Each sequence can be performed in one breath-hold.

• These sequences can be implemented in routine abdominal MRI protocols.

• Thus hepatic fat can be evaluated without relevant increase in scan time.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

BMI:

body mass index

95 % CI:

95 % confidence interval

HISTO:

high-speed T2-corrected multi-echo single-voxel spectroscopy

H MRS:

1H magnetic resonance spectroscopy

ICC:

Intra-class correlation coefficient

MRI:

Magnetic resonance imaging

NAFLD:

non-alcoholic fatty liver disease

NPV:

negative predictive value

PPV:

positive predictive value

PRESS:

point-resolved spectroscopy

STEAM:

stimulated-echo acquisition mode

VIBE:

volumetric interpolated breath-hold examination

KORA:

Cooperative Health Research in the Region of Augsburg

References

  1. Chalasani N, Younossi Z, Lavine JE et al (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology. Gastroenterology 142:1592–1609

    Article  PubMed  Google Scholar 

  2. Cusi K (2009) Nonalcoholic fatty liver disease in type 2 diabetes mellitus. Curr Opin Endocrinol Diabetes Obes 16:141–149

    Article  PubMed  Google Scholar 

  3. Lee JY, Kim KM, Lee SG et al (2007) Prevalence and risk factors of non-alcoholic fatty liver disease in potential living liver donors in Korea: a review of 589 consecutive liver biopsies in a single center. J Hepatol 47:239–244

    Article  PubMed  Google Scholar 

  4. Marcos A, Fisher RA, Ham JM et al (2000) Selection and outcome of living donors for adult to adult right lobe transplantation. Transplantation 69:2410–2415

    Article  CAS  PubMed  Google Scholar 

  5. Vernon G, Baranova A, Younossi ZM (2011) Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 34:274–285

    Article  CAS  PubMed  Google Scholar 

  6. Williams CD, Stengel J, Asike MI et al (2011) Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology 140:124–131

    Article  PubMed  Google Scholar 

  7. Browning JD, Szczepaniak LS, Dobbins R et al (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40:1387–1395

    Article  PubMed  Google Scholar 

  8. Machado M, Marques-Vidal P, Cortez-Pinto H (2006) Hepatic histology in obese patients undergoing bariatric surgery. J Hepatol 45:600–606

    Article  PubMed  Google Scholar 

  9. OECD (2014) Obesity update 2014. OECD, Paris. http://www.oecd.org/health/Obesity-Update-2014.pdf. Accessed 26 Oct 2014

  10. Schwenzer NF, Springer F, Schraml C, Stefan N, Machann J, Schick F (2009) Non-invasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol 51:433–445

    Article  PubMed  Google Scholar 

  11. Bohte AE, van Werven JR, Bipat S, Stoker J (2011) The diagnostic accuracy of US, CT, MRI and 1H-MRS for the evaluation of hepatic steatosis compared with liver biopsy: a meta-analysis. Eur Radiol 21:87–97

    Article  PubMed  PubMed Central  Google Scholar 

  12. Bashir MR, Merkle EM, Smith AD, Boll DT (2012) Hepatic MR imaging for in vivo differentiation of steatosis, iron deposition and combined storage disorder: single-ratio in/opposed phase analysis vs. dual-ratio Dixon discrimination. Eur J Radiol 81:e101–e109

    Article  PubMed  Google Scholar 

  13. Bashir MR, Zhong X, Dale BM, Gupta RT, Boll DT, Merkle EM (2013) Automated patient-tailored screening of the liver for diffuse steatosis and iron overload using MRI. AJR Am J Roentgenol 201:583–588

    Article  PubMed  Google Scholar 

  14. Zhong X, Nickel MD, Kannengiesser SA, Dale BM, Kiefer B, Bashir MR (2014) Liver fat quantification using a multi-step adaptive fitting approach with multi-echo GRE imaging. Magn Reson Med 72:1353–1365

    Article  PubMed  Google Scholar 

  15. Bashir MR, Zhong X, Nickel MD et al (2015) Quantification of hepatic steatosis with a multistep adaptive fitting MRI approach: prospective validation against MR spectroscopy. AJR Am J Roentgenol 204:297–306

    Article  PubMed  Google Scholar 

  16. Pineda N, Sharma P, Xu Q, Hu X, Vos M, Martin DR (2009) Measurement of hepatic lipid: high-speed T2-corrected multiecho acquisition at 1H MR spectroscopy–a rapid and accurate technique. Radiology 252:568–576

    Article  PubMed  Google Scholar 

  17. Fischer MA, Raptis DA, Montani M et al (2012) Liver fat quantification by dual-echo MR imaging outperforms traditional histopathological analysis. Acad Radiol 19:1208–1214

    Article  PubMed  Google Scholar 

  18. Tang A, Desai A, Hamilton G et al (2015) Accuracy of MR imaging-estimated proton density fat fraction for classification of dichotomized histologic steatosis grades in nonalcoholic fatty liver disease. Radiology 274:416–425

    Article  PubMed  PubMed Central  Google Scholar 

  19. Yokoo T, Bydder M, Hamilton G et al (2009) Nonalcoholic fatty liver disease: diagnostic and fat-grading accuracy of low-flip-angle multiecho gradient-recalled-echo MR imaging at 1.5 T. Radiology 251:67–76

    Article  PubMed  PubMed Central  Google Scholar 

  20. Meisamy S, Hines CD, Hamilton G et al (2011) Quantification of hepatic steatosis with T1-independent, T2-corrected MR imaging with spectral modeling of fat: blinded comparison with MR spectroscopy. Radiology 258:767–775

    Article  PubMed  PubMed Central  Google Scholar 

  21. Tang A, Tan J, Sun M et al (2013) Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology 267:422–431

    Article  PubMed  PubMed Central  Google Scholar 

  22. Xiang QS, An L (1997) Water-fat imaging with direct phase encoding. J Magn Reson Imaging 7:1002–1015

    Article  CAS  PubMed  Google Scholar 

  23. Ma J (2004) Breath-hold water and fat imaging using a dual-echo two-point Dixon technique with an efficient and robust phase-correction algorithm. Magn Reson Med 52:415–419

    Article  PubMed  Google Scholar 

  24. Yu H, Reeder SB, Shimakawa A, Brittain JH, Pelc NJ (2005) Field map estimation with a region growing scheme for iterative 3-point water-fat decomposition. Magn Reson Med 54:1032–1039

    Article  PubMed  Google Scholar 

  25. DeFilippis AP, Blaha MJ, Martin SS et al (2013) Nonalcoholic fatty liver disease and serum lipoproteins: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis 227:429–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Baumeister SE, Volzke H, Marschall P et al (2008) Impact of fatty liver disease on health care utilization and costs in a general population: a 5-year observation. Gastroenterology 134:85–94

    Article  PubMed  Google Scholar 

  27. Koehler EM, Schouten JN, Hansen BE et al (2012) Prevalence and risk factors of non-alcoholic fatty liver disease in the elderly: results from the Rotterdam study. J Hepatol 57:1305–1311

    Article  PubMed  Google Scholar 

  28. German National Cohort (GNC) Consortium (2014) The German National Cohort: aims, study design and organization. Eur J Epidemiol 29:371–382

    Article  Google Scholar 

  29. Henninger B, Zoller H, Rauch S et al (2015) Automated two-point Dixon screening for the evaluation of hepatic steatosis and siderosis: comparison with R2-relaxometry and chemical shift-based sequences. Eur Radiol 25:1356–1365

    Article  CAS  PubMed  Google Scholar 

  30. Kukuk GM, Hittatiya K, Sprinkart AM et al (2015) Comparison between modified Dixon MRI techniques, MR spectroscopic relaxometry, and different histologic quantification methods in the assessment of hepatic steatosis. Eur Radiol. doi:10.1007/s00330-015-3703-6

    Google Scholar 

Download references

Acknowledgments

We thank Xiaodong Zhong and Radhouene Neji of Siemens Healthcare as principal authors of the prototype sequences and software packages.

The scientific guarantor of this publication is Holger Hetterich. The authors of this manuscript declare relationships with the following companies: Stephan A.R. Kannengießer is an employee of Siemens Healthcare. This study has received funding by The KORA research platform (Cooperative Research in the Region of Augsburg) and was initiated and financed by the Helmholtz Zentrum München - German Research Center for Environmental Health, which is funded by the German Federal Ministry of Education and Research and by the State of Bavaria. The KORA-MRI substudy received funding by the German Research Foundation (DFG, Deutsche Forschungsgemeinschaft). The KORA-MRI substudy was supported by an unrestricted research grant from Siemens Healthcare.

One of the authors has significant statistical expertise. Institutional review board approval was obtained. Written informed consent was obtained from all subjects in this study. Methodology: prospective, cross sectional, diagnostic study, performed at one institution.

Author information

Authors and Affiliations

  1. Institute of Clinical Radiology, Ludwig-Maximilian University Hospital, Marchioninistraße 15, 81377, Munich, Germany

    Holger Hetterich, Christian Bayerl, Sigrid Auweter, Harald Kramer, Birgit Ertl-Wagner & Fabian Bamberg

  2. Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany

    Annette Peters, Margit Heier, Birgit Linkohr & Christa Meisinger

  3. KORA Myocardial Infarction Registry, Central Hospital of Augsburg, Augsburg, Germany

    Margit Heier & Christa Meisinger

  4. Siemens Healthcare, Erlangen, Germany

    Stephan A. R. Kannengießer

  5. Department of Radiology, University of Wisconsin – Madison, Madison, WI, USA

    Harald Kramer

  6. Department of Radiology, University Hospital Tübingen, Tübingen, Germany

    Fabian Bamberg

Authors
  1. Holger Hetterich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christian Bayerl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Annette Peters
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Margit Heier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Birgit Linkohr
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christa Meisinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sigrid Auweter
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Stephan A. R. Kannengießer
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Harald Kramer
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Birgit Ertl-Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Fabian Bamberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Holger Hetterich.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hetterich, H., Bayerl, C., Peters, A. et al. Feasibility of a three-step magnetic resonance imaging approach for the assessment of hepatic steatosis in an asymptomatic study population. Eur Radiol 26, 1895–1904 (2016). https://doi.org/10.1007/s00330-015-3966-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-015-3966-y

Keywords

Search

Navigation