Abstract
Objectives
To quantify and compare the fat fraction of background liver and primary liver lesions using a triple-echo-gradient-echo sequence.
M&M
This IRB-approved study included 128 consecutive patients who underwent a liver MRI for lesion characterization. Fat fraction from the whole lesion volume and the normal liver parenchyma were computed from triple-echo (consecutive in-phase, opposed-phase, in-phase echo times) sequence.
Results
Forty-seven hepatocellular carcinoma (HCCs), 25 hepatocellular adenomas (HCAs), and 56 focal nodular hyperplasia (FNH) were included. The mean intralesional fat fraction for various lesions was 7.1% (range, 0.5–23.6; SD, 5.6) for HCAs, 5.7% (range, 0.8–14; SD, 2.9) for HCCs, and 2.3% (range, 0.8–10.3; SD, 1.9) for FNHs (p = 0.6 for HCCs vs HCA, p < 0.001 for FNH vs HCCs or HCA). A fat fraction threshold of 2.7% enabled distinction between HCA and FNH with a sensitivity of 80% and a specificity of 77%. The mean normal liver parenchyma fat fraction was lower than the intralesional fat fraction in the HCC group (p = 0.04) and higher in the FNH group (p = 0.001), but not significantly different in the HCA group (p = 0.51).
Conclusion
Triple-echo-gradient-echo is a feasible technique to quantify fat fraction of background liver and primary liver lesions. Intralesional fat fraction obtained from lesion whole volume is greater for HCCs and HCA compared to FNH. When trying to distinguish FNH and HCA, an intralesional fat fraction < 2.7% may orient toward the diagnosis of FNH.
Key Points
• Triple-echo technique is feasible to quantify intralesional fat fraction of primary liver lesions.
• Whole volume intralesional fat fraction is greater for HCCs and HCA compared to FNH.
• An intralesional fat fraction < 2.7% may orient toward the diagnosis of FNH.
Similar content being viewed by others
Abbreviations
- FNH:
-
Focal nodular hyperplasia
- HCA:
-
Hepatocellular adenoma
- HCC:
-
Hepatocellular carcinoma
- IP:
-
In-phase
- MRI:
-
Magnetic resonance imaging
- OP:
-
Out of phase
- PDFF:
-
Proton density fat fraction
- ROC:
-
Receiver operating characteristic curves
References
Ratziu V, Charlotte F, Heurtier A et al (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 128:1898–1906
Kramer H, Pickhardt PJ, Kliewer MA et al (2017) Accuracy of liver fat quantification with advanced CT, MRI, and ultrasound techniques: prospective comparison with MR spectroscopy. AJR Am J Roentgenol 208:92–100
Motosugi U, Hernando D, Bannas P et al (2015) Quantification of liver fat with respiratory-gated quantitative chemical shift encoded MRI. J Magn Reson Imaging 42:1241–1248
Satkunasingham J, Besa C, Bane O et al (2015) Liver fat quantification: comparison of dual-echo and triple-echo chemical shift MRI to MR spectroscopy. Eur J Radiol 84:1452–1458
Lin H, Wei H, He N et al (2018) Quantitative susceptibility mapping in combination with water-fat separation for simultaneous liver iron and fat fraction quantification. Eur Radiol 28:3494–3504
Brouha SS, Nguyen P, Bettencourt R, Sirlin CB, Loomba R (2018) Increased severity of liver fat content and liver fibrosis in non-alcoholic fatty liver disease correlate with epicardial fat volume in type 2 diabetes: a prospective study. Eur Radiol 28:1345–1355
Roldan-Valadez E, Favila R, Martinez-Lopez M, Uribe M, Rios C, Mendez-Sanchez N (2010) In vivo 3T spectroscopic quantification of liver fat content in nonalcoholic fatty liver disease: correlation with biochemical method and morphometry. J Hepatol 53:732–737
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
Dixon WT (1984) Simple proton spectroscopic imaging. Radiology 153:189–194
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
Westphalen AC, Qayyum A, Yeh BM et al (2007) Liver fat: effect of hepatic iron deposition on evaluation with opposed-phase MR imaging. Radiology 242:450–455
Reeder SB, Sirlin CB (2010) Quantification of liver fat with magnetic resonance imaging. Magn Reson Imaging Clin N Am 18:337–357 ix
Kuhn JP, Evert M, Friedrich N et al (2011) Noninvasive quantification of hepatic fat content using three-echo Dixon magnetic resonance imaging with correction for T2* relaxation effects. Invest Radiol 46:783–789
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
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
Guiu B, Loffroy R, Cercueil JP, Krause D (2008) Multiecho MR imaging and proton MR spectroscopy for liver fat quantification. Radiology 249:1081
Guiu B, Loffroy R, Petit JM et al (2009) Mapping of liver fat with triple-echo gradient echo imaging: validation against 3.0-T proton MR spectroscopy. Eur Radiol 19:1786–1793
Guiu B, Petit JM, Loffroy R et al (2011) Liver methylene fraction by dual- and triple-echo gradient-echo imaging at 3.0T: correlation with proton MR spectroscopy and estimation of robustness after SPIO administration. J Magn Reson Imaging 33:119–127
Guiu B, Petit JM, Loffroy R et al (2009) Quantification of liver fat content: comparison of triple-echo chemical shift gradient-echo imaging and in vivo proton MR spectroscopy. Radiology 250:95–102
Sacco R, Gadaleta-Caldarola G, Galati G, Lombardi G, Mazza G, Cabibbo G (2014) EASL HCC summit: liver cancer management. Future Oncol 10:1129–1132
European Association for the Study of the Liver (2016) EASL clinical practice guidelines on the management of benign liver tumours. J Hepatol 65:386–398
Szczepaniak LS, Nurenberg P, Leonard D et al (2005) Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 288:E462–E468
Farrell GC, Larter CZ (2006) Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology 43:S99–S112
Qu Y, Li M, Hamilton G, Zhang YN, Song B (2019) Diagnostic accuracy of hepatic proton density fat fraction measured by magnetic resonance imaging for the evaluation of liver steatosis with histology as reference standard: a meta-analysis. Eur Radiol. https://doi.org/10.1007/s00330-019-06071-5
Hernando D, Sharma SD, Aliyari Ghasabeh M et al (2017) Multisite, multivendor validation of the accuracy and reproducibility of proton-density fat-fraction quantification at 1.5T and 3T using a fat-water phantom. Magn Reson Med 77:1516–1524
Serai SD, Dillman JR, Trout AT (2017) Proton density fat fraction measurements at 1.5- and 3-T hepatic MR imaging: same-day agreement among readers and across two imager manufacturers. Radiology 284:244–254
Yokoo T, Serai SD, Pirasteh A et al (2018) Linearity, bias, and precision of hepatic proton density fat fraction measurements by using MR imaging: a meta-analysis. Radiology 286:486–498
Bioulac-Sage P, Balabaud C, Bedossa P et al (2007) Pathological diagnosis of liver cell adenoma and focal nodular hyperplasia: Bordeaux update. J Hepatol 46:521–527
Bioulac-Sage P, Laumonier H, Couchy G et al (2009) Hepatocellular adenoma management and phenotypic classification: the Bordeaux experience. Hepatology 50:481–489
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
van Aalten SM, Thomeer MG, Terkivatan T et al (2011) Hepatocellular adenomas: correlation of MR imaging findings with pathologic subtype classification. Radiology 261:172–181
Funding
The authors state that this work has not received any funding.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Guarantor
The scientific guarantor of this publication is Boris Guiu.
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
One of the authors has significant statistical expertise.
Informed consent
Written informed consent was waived by the Institutional Review Board.
Ethical approval
Institutional Review Board approval was obtained.
Methodology
• Retrospective
• Case-control study
• Performed at one institution
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Nougaret, S., Monsonis, B., Molinari, N. et al. Quantification of liver fat content in liver and primary liver lesions using triple-echo-gradient-echo MRI. Eur Radiol 30, 4752–4761 (2020). https://doi.org/10.1007/s00330-020-06757-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-020-06757-1