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.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.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
Loomba R, Sanyal AJ (2013) The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol 10:686–690
Bellentani S, Scaglioni F, Marino M, Bedogni G (2010) Epidemiology of non-alcoholic fatty liver disease. Dig Dis 28:155–161
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
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
Rinella ME (2015) Nonalcoholic fatty liver disease: a systematic review. Jama 313:2263–2273
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
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
Friedman SL, Neuschwander-Tetri BA, Rinella M, Sanyal AJ (2018) Mechanisms of NAFLD development and therapeutic strategies. Nat Med 24:908–922
Schuppan D, Afdhal NH (2008) Liver cirrhosis. Lancet 371:838–851
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
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
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
Idilman IS, Ozdeniz I, Karcaaltincaba M (2016) Hepatic steatosis: etiology, patterns, and quantification. Semin Ultrasound CT MR 37:501–510
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
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
Hashimoto E, Taniai M, Tokushige K (2013) Characteristics and diagnosis of NAFLD/NASH. J Gastroenterol Hepatol 28(Suppl 4):64–70
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
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
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
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
Reeder SB (2013) Emerging quantitative magnetic resonance imaging biomarkers of hepatic steatosis. Hepatology 58:1877–1880
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
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
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
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
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
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
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
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
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
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
Schueler S, Schuetz GM, Dewey M (2012) The revised QUADAS-2 tool. Ann Intern Med 156:323 author reply 323-324
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
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
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
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
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
Adams LA, Lindor KD (2007) Nonalcoholic fatty liver disease. Ann Epidemiol 17:863–869
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
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
Ratziu V, Charlotte F, Heurtier A et al (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 128:1898–1906
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
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
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
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
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
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
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
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
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
Ferraioli G, Tinelli C, Lissandrin R et al (2014) Point shear wave elastography method for assessing liver stiffness. World J Gastroenterol 20:4787–4796
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
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
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
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
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
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
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
Corresponding author
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
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-019-06072-4