Skip to main content
Log in

Diagnostic value of MRI-PDFF for hepatic steatosis in patients with non-alcoholic fatty liver disease: a meta-analysis

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

Abstract

Objective

To systematically review studies about the diagnostic accuracy of magnetic resonance imaging proton density fat fraction (MRI-PDFF) in the classification of hepatic steatosis grade in patients with non-alcoholic fatty liver disease (NAFLD).

Methods

Areas under the summary receiver operating characteristic curves (AUROC), sensitivity, specificity, overall diagnostic odds ratio (DOR), diagnostic score, positive likelihood ratio (+LR), and negative likelihood ratio (−LR) for MRI-PDFF in classification of steatosis grades 0 vs. 1–3, 0–1 vs. 2–3, and 0–2 vs. 3 were compared and analyzed.

Results

A total of 6 studies were included in this meta-analysis (n = 635). The summary AUROC values of MRI-PDFF for classifying steatosis grades 0 vs. 1–3, 0–1 vs. 2–3, and 0–2 vs. 3 were 0.98, 0.91, and 0.90, respectively. Pooled sensitivity and specificity of MRI-PDFF for classifying steatosis grades 0 vs. 1–3, 0–1 vs. 2–3, and 0–2 vs. 3 were 0.93 and 0.94, 0.74 and 0.90, and 0.74 and 0.87, respectively. Summary +LR and −LR of MRI-PDFF for classifying steatosis grades 0 vs. 1–3, 0–1 vs. 2–3, and 0–2 vs. 3 were 16.21 (95%CI, 4.72–55.67) and 0.08 (95%CI, 0.04–0.15), 7.19 (95%CI, 5.04–10.26) and 0.29 (95%CI, 0.22–0.38), and 5.89 (95%CI, 4.27–8.13) and 0.29 (95%CI, 0.21–0.41), respectively.

Conclusions

Our meta-analysis suggests that MRI-PDFF has excellent diagnostic value for assessment of hepatic fat content and classification of histologic steatosis in patients with NAFLD.

Key Points

MRI-PDFF has significant diagnostic value for hepatic steatosis in patients with NAFLD.

MRI-PDFF may be used to classify grade of hepatic steatosis with high sensitivity and specificity.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Abbreviations

95%CI:

95% confidence interval

ARFI:

Acoustic radiation force impulse

AUROC:

Areas under summary receiver operating characteristic curves

BMI:

Body mass index

CAP:

Controlled attenuation parameter

CRN:

Clinical Research Network

DOR:

diagnostic odds ratio

ElastPQ:

Elastography point quantification

HCC:

Hepatocellular carcinoma

LR:

Likelihood ratio

MRI:

Magnetic resonance imaging

MRS:

Magnetic resonance spectroscopy

NAFLD:

Non-alcoholic fatty liver disease

NASH:

Non-alcoholic steatohepatitis

PDFF:

Proton density fat fraction

pSWE:

Point shear wave elastography

QUADAS:

Quality assessment of diagnostic accuracy studies

ROC:

Receiver operating characteristic

TE:

Transient elastography

References

  1. Loomba R, Sanyal AJ (2013) The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol 10:686–690

    Article  CAS  PubMed  Google Scholar 

  2. Bellentani S, Scaglioni F, Marino M, Bedogni G (2010) Epidemiology of non-alcoholic fatty liver disease. Dig Dis 28:155–161

    Article  CAS  PubMed  Google Scholar 

  3. Schwimmer JB, Deutsch R, Kahen T, Lavine JE, Stanley C, Behling C (2006) Prevalence of fatty liver in children and adolescents. Pediatrics 118:1388–1393

    Article  PubMed  Google Scholar 

  4. Alswat K, Aljumah AA, Sanai FM et al (2018) Nonalcoholic fatty liver disease burden - Saudi Arabia and United Arab Emirates, 2017–2030. Saudi J Gastroenterol 24:211–219

    Article  PubMed  PubMed Central  Google Scholar 

  5. Rinella ME (2015) Nonalcoholic fatty liver disease: a systematic review. Jama 313:2263–2273

    Article  CAS  PubMed  Google Scholar 

  6. Alexander J, Torbenson M, Wu TT, Yeh MM (2013) Non-alcoholic fatty liver disease contributes to hepatocarcinogenesis in non-cirrhotic liver: a clinical and pathological study. J Gastroenterol Hepatol 28:848–854

    Article  PubMed  Google Scholar 

  7. Singh S, Allen AM, Wang Z, Prokop LJ, Murad MH, Loomba R (2015) Fibrosis progression in nonalcoholic fatty liver vs nonalcoholic steatohepatitis: a systematic review and meta-analysis of paired-biopsy studies. Clin Gastroenterol Hepatol 13:643–654 e641–649; quiz e639–640

    Article  PubMed  Google Scholar 

  8. Friedman SL, Neuschwander-Tetri BA, Rinella M, Sanyal AJ (2018) Mechanisms of NAFLD development and therapeutic strategies. Nat Med 24:908–922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Schuppan D, Afdhal NH (2008) Liver cirrhosis. Lancet 371:838–851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cadranel JF (2002) [Good clinical practice guidelines for fine needle aspiration biopsy of the liver: past, present and future]. Gastroenterol Clin Biol 26:823–824

  11. Bonekamp S, Tang A, Mashhood A et al (2014) Spatial distribution of MRI-determined hepatic proton density fat fraction in adults with nonalcoholic fatty liver disease. J Magn Reson Imaging 39:1525–1532

    Article  PubMed  PubMed Central  Google Scholar 

  12. Merriman RB, Ferrell LD, Patti MG et al (2006) Correlation of paired liver biopsies in morbidly obese patients with suspected nonalcoholic fatty liver disease. Hepatology 44:874–880

    Article  PubMed  Google Scholar 

  13. Idilman IS, Ozdeniz I, Karcaaltincaba M (2016) Hepatic steatosis: etiology, patterns, and quantification. Semin Ultrasound CT MR 37:501–510

    Article  PubMed  Google Scholar 

  14. Kleiner DE, Brunt EM, Van Natta M et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313–1321

    Article  PubMed  Google Scholar 

  15. 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  PubMed  Google Scholar 

  16. Hashimoto E, Taniai M, Tokushige K (2013) Characteristics and diagnosis of NAFLD/NASH. J Gastroenterol Hepatol 28(Suppl 4):64–70

    Article  CAS  PubMed  Google Scholar 

  17. Alisi A, Pinzani M, Nobili V (2009) Diagnostic power of fibroscan in predicting liver fibrosis in nonalcoholic fatty liver disease. Hepatology 50:2048–2049 author reply 2049-2050

    Article  PubMed  Google Scholar 

  18. Chan WK, Nik Mustapha NR, Mahadeva S (2014) Controlled attenuation parameter for the detection and quantification of hepatic steatosis in nonalcoholic fatty liver disease. J Gastroenterol Hepatol 29:1470–1476

    Article  CAS  PubMed  Google Scholar 

  19. Schwimmer JB, Middleton MS, Deutsch R, Lavine JE (2005) A phase 2 clinical trial of metformin as a treatment for non-diabetic paediatric non-alcoholic steatohepatitis. Aliment Pharmacol Ther 21:871–879

    Article  CAS  PubMed  Google Scholar 

  20. Reeder SB, Hu HH, Sirlin CB (2012) Proton density fat-fraction: a standardized MR-based biomarker of tissue fat concentration. J Magn Reson Imaging 36:1011–1014

    Article  PubMed  PubMed Central  Google Scholar 

  21. Reeder SB (2013) Emerging quantitative magnetic resonance imaging biomarkers of hepatic steatosis. Hepatology 58:1877–1880

    Article  CAS  PubMed  Google Scholar 

  22. Le TA, Chen J, Changchien C et al (2012) Effect of colesevelam on liver fat quantified by magnetic resonance in nonalcoholic steatohepatitis: a randomized controlled trial. Hepatology 56:922–932

    Article  CAS  PubMed  Google Scholar 

  23. Bannas P, Kramer H, Hernando D et al (2015) Quantitative magnetic resonance imaging of hepatic steatosis: validation in ex vivo human livers. Hepatology 62:1444–1455

    Article  CAS  PubMed  Google Scholar 

  24. 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 

  25. Kim M, Kang BK, Jun DW (2018) Comparison of conventional sonographic signs and magnetic resonance imaging proton density fat fraction for assessment of hepatic steatosis. Sci Rep 8:7759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Loomba R, Kayali Z, Noureddin M et al (2018) GS-0976 reduces hepatic steatosis and fibrosis markers in patients with nonalcoholic fatty liver disease. Gastroenterology

  27. Patel NS, Peterson MR, Lin GY et al (2013) Insulin resistance increases MRI-estimated pancreatic fat in nonalcoholic fatty liver disease and normal controls. Gastroenterol Res Pract 2013:498296

    Article  PubMed  PubMed Central  Google Scholar 

  28. Idilman IS, Tuzun A, Savas B et al (2015) Quantification of liver, pancreas, kidney, and vertebral body MRI-PDFF in non-alcoholic fatty liver disease. Abdom Imaging 40:1512–1519

    Article  PubMed  Google Scholar 

  29. Yu NY, Wolfson T, Middleton MS et al (2017) Bone marrow fat content is correlated with hepatic fat content in paediatric non-alcoholic fatty liver disease. Clin Radiol 72:425.e429–425.e414

  30. Runge JH, Bakker PJ, Gaemers IC et al (2014) Measuring liver triglyceride content in mice: non-invasive magnetic resonance methods as an alternative to histopathology. MAGMA 27:317–327

    Article  CAS  PubMed  Google Scholar 

  31. Ueno T, Suzuki H, Hiraishi M, Amano H, Fukuyama H, Sugimoto N (2016) In vivo magnetic resonance microscopy and hypothermic anaesthesia of a disease model in Medaka. Sci Rep 6:27188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Schueler S, Schuetz GM, Dewey M (2012) The revised QUADAS-2 tool. Ann Intern Med 156:323 author reply 323-324

    Article  PubMed  Google Scholar 

  33. 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  PubMed  Google Scholar 

  34. Middleton MS, Van Natta ML, Heba ER et al (2017) Diagnostic accuracy of magnetic resonance imaging hepatic proton density fat fraction in pediatric nonalcoholic fatty liver disease. Hepatology 67:858–872

    Article  CAS  Google Scholar 

  35. Middleton MS, Heba ER, Hooker CA et al (2017) Agreement between magnetic resonance imaging proton density fat fraction measurements and pathologist-assigned steatosis grades of liver biopsies from adults with nonalcoholic steatohepatitis. Gastroenterology 153:753–761

    Article  PubMed  Google Scholar 

  36. 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  Google Scholar 

  37. 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 

  38. Adams LA, Lindor KD (2007) Nonalcoholic fatty liver disease. Ann Epidemiol 17:863–869

    Article  PubMed  Google Scholar 

  39. Kim SH, Lee JM, Han JK et al (2006) Hepatic macrosteatosis: predicting appropriateness of liver donation by using MR imaging--correlation with histopathologic findings. Radiology 240:116–129

    Article  PubMed  Google Scholar 

  40. Fernandez-Salazar L, Velayos B, Aller R, Lozano F, Garrote JA, Gonzalez JM (2011) Percutaneous liver biopsy: patients’ point of view. Scand J Gastroenterol 46:727–731

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  42. d’Assignies G, Paisant A, Bardou-Jacquet E et al (2018) Non-invasive measurement of liver iron concentration using 3-Tesla magnetic resonance imaging: validation against biopsy. Eur Radiol 28:2022–2030

    Article  PubMed  Google Scholar 

  43. Reeder SB, Cruite I, Hamilton G, Sirlin CB (2011) Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging 34:729–749

    Article  PubMed  PubMed Central  Google Scholar 

  44. Yokoo T, Shiehmorteza M, Hamilton G et al (2011) Estimation of hepatic proton-density fat fraction by using MR imaging at 3.0 T. Radiology 258:749–759

    Article  PubMed  PubMed Central  Google Scholar 

  45. Di Martino M, Pacifico L, Bezzi M et al (2016) Comparison of magnetic resonance spectroscopy, proton density fat fraction and histological analysis in the quantification of liver steatosis in children and adolescents. World J Gastroenterol 22:8812–8819

    Article  PubMed  PubMed Central  Google Scholar 

  46. Noureddin M, Lam J, Peterson MR et al (2013) Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials. Hepatology 58:1930–1940

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  PubMed  Google Scholar 

  48. Friedrich-Rust M, Romen D, Vermehren J et al (2012) Acoustic radiation force impulse-imaging and transient elastography for non-invasive assessment of liver fibrosis and steatosis in NAFLD. Eur J Radiol 81:e325–e331

    Article  PubMed  Google Scholar 

  49. Cassinotto C, Boursier J, de Ledinghen V et al (2016) Liver stiffness in nonalcoholic fatty liver disease: a comparison of supersonic shear imaging, FibroScan, and ARFI with liver biopsy. Hepatology 63:1817–1827

    Article  PubMed  Google Scholar 

  50. Woo H, Lee JY, Yoon JH, Kim W, Cho B, Choi BI (2015) Comparison of the reliability of acoustic radiation force impulse imaging and supersonic shear imaging in measurement of liver stiffness. Radiology 277:881–886

    Article  PubMed  Google Scholar 

  51. Ferraioli G, Tinelli C, Lissandrin R et al (2014) Point shear wave elastography method for assessing liver stiffness. World J Gastroenterol 20:4787–4796

    Article  PubMed  PubMed Central  Google Scholar 

  52. Ma JJ, Ding H, Mao F, Sun HC, Xu C, Wang WP (2014) Assessment of liver fibrosis with elastography point quantification technique in chronic hepatitis B virus patients: a comparison with liver pathological results. J Gastroenterol Hepatol 29:814–819

    Article  PubMed  Google Scholar 

  53. Fraquelli M, Baccarin A, Casazza G et al (2016) Liver stiffness measurement reliability and main determinants of point shear-wave elastography in patients with chronic liver disease. Aliment Pharmacol Ther 44:356–365

    Article  CAS  PubMed  Google Scholar 

  54. Conti F, Serra C, Vukotic R et al (2017) Accuracy of elastography point quantification and steatosis influence on assessing liver fibrosis in patients with chronic hepatitis C. Liver Int 37:187–195

    Article  CAS  PubMed  Google Scholar 

  55. Mare R, Sporea I, Lupusoru R et al (2017) The value of ElastPQ for the evaluation of liver stiffness in patients with B and C chronic hepatopathies. Ultrasonics 77:144–151

    Article  PubMed  Google Scholar 

  56. Idilman IS, Aniktar H, Idilman R et al (2013) Hepatic steatosis: quantification by proton density fat fraction with MR imaging versus liver biopsy. Radiology 267:767–775

    Article  PubMed  Google Scholar 

  57. McPherson S, Jonsson JR, Cowin GJ et al (2009) Magnetic resonance imaging and spectroscopy accurately estimate the severity of steatosis provided the stage of fibrosis is considered. J Hepatol 51:389–397

    Article  PubMed  Google Scholar 

Download references

Funding

This study has received funding by the National Natural Science Foundation of China (No. 31770837) and the Qingdao, Shinan District Science and Technology Development Project Fund (No. 2016-3-016-YY).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yongning Xin.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Yongning Xin.

Conflict of interest

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

Qing Zhang as an expert in statistics and radiology, who worked at Qingdao Municipal Hospital, gave us much guidance of statistics and biometry.

Informed consent

Written informed consent was not required for this study because this study was a meta-analysis.

Ethical approval

Institutional Review Board approval was not required because this study was a meta-analysis.

Methodology

• Retrospective

• Multicenter study

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gu, J., Liu, S., Du, S. et al. Diagnostic value of MRI-PDFF for hepatic steatosis in patients with non-alcoholic fatty liver disease: a meta-analysis. Eur Radiol 29, 3564–3573 (2019). https://doi.org/10.1007/s00330-019-06072-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-019-06072-4

Keywords

Navigation