Abstract
Purpose
To compare liver stiffness measurements obtained from MR elastography with liver T1 relaxation times obtained from T1 mapping and T2 relaxation times obtained from T2 mapping for detection and staging of liver fibrosis.
Materials and methods
223 patients with known or suspected liver disease underwent MRI of the liver with T1 mapping (Look-Locker sequence) and 2D SE-EPI MR elastography (MRE) sequences. 139 of these patients also underwent T2 mapping with radial T2 TSE sequence. Two readers (R1 & R2) measured liver stiffness, T1 relaxation times and T2 relaxation times. T1 and T2 times were correlated with stiffness measurements. ROC analysis was used to compare the performance of both techniques in discriminating fibrosis stage in 23 patients who underwent liver biopsy.
Results
For each reader there was significant moderate positive correlation between liver MRE and liver T1 mapping (r = 0.49 and 0.36). There was significant moderate positive correlation between liver T2 mapping and each of MRE and T1 mapping for one of the readers (r = 0.40 and 0.27). AUC for differentiating early (F0–F2) from advanced (F3–F4) fibrosis in biopsied patients was 0.975 (R1) and 0.925 (R2) for MRE, 0.671 (R1) and 0.642 (R2) for T1 mapping and 0.671 (R1) and 0.743 (R2) for T2 mapping. Inter-reader agreement was good for MRE (ICC = 0.84) substantial for T1 mapping (0.94) and T2 mapping (0.96).
Conclusions
Liver T1 and T2 mapping showed moderate positive correlation with MR elastography. Accuracy of MRE is however superior to T1 and T2 mapping in the subset of patients who underwent liver biopsy. Accuracy of combination of MRE and T1 mapping/T2 mapping was not superior to MRE alone.
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References
Younossi Z, Anstee QM, Marietti M, Hardy T, Henry L, Eslam M, et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol. 2018;15(1):11-20.
Albanis E, Friedman SL. Hepatic fibrosis. Pathogenesis and principles of therapy. Clin Liver Dis. 2001;5(2):315-34, v-vi.
Bataller R, Brenner DA. Liver fibrosis. J Clin Invest. 2005;115(2):209-18.
Ble M, Procopet B, Miquel R, Hernandez-Gea V, Garcia-Pagan JC. Transjugular liver biopsy. Clin Liver Dis. 2014;18(4):767-78.
Chi H, Hansen BE, Tang WY, Schouten JN, Sprengers D, Taimr P, et al. Multiple biopsy passes and the risk of complications of percutaneous liver biopsy. Eur J Gastroenterol Hepatol. 2017;29(1):36-41.
Poynard T, Lenaour G, Vaillant JC, Capron F, Munteanu M, Eyraud D, et al. Liver biopsy analysis has a low level of performance for diagnosis of intermediate stages of fibrosis. Clin Gastroenterol Hepatol. 2012;10(6):657-63 e7.
Manduca A, Oliphant TE, Dresner MA, Mahowald JL, Kruse SA, Amromin E, et al. Magnetic resonance elastography: non-invasive mapping of tissue elasticity. Med Image Anal. 2001;5(4):237-54.
Rustogi R, Horowitz J, Harmath C, Wang Y, Chalian H, Ganger DR, et al. Accuracy of MR elastography and anatomic MR imaging features in the diagnosis of severe hepatic fibrosis and cirrhosis. J Magn Reson Imaging. 2012;35(6):1356-64.
Singh S, Venkatesh SK, Wang Z, Miller FH, Motosugi U, Low RN, et al. Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol. 2015;13(3):440-51 e6.
Srinivasa Babu A, Wells ML, Teytelboym OM, Mackey JE, Miller FH, Yeh BM, et al. Elastography in Chronic Liver Disease: Modalities, Techniques, Limitations, and Future Directions. Radiographics. 2016;36(7):1987-2006.
Marinelli JP, Levin DL, Vassallo R, Carter RE, Hubmayr RD, Ehman RL, et al. Quantitative assessment of lung stiffness in patients with interstitial lung disease using MR elastography. J Magn Reson Imaging. 2017;46(2):365-74.
ElSheikh M, Arani A, Perry A, Boeve BF, Meyer FB, Savica R, et al. MR Elastography Demonstrates Unique Regional Brain Stiffness Patterns in Dementias. AJR Am J Roentgenol. 2017;209(2):403-8.
Arani A, Arunachalam SP, Chang ICY, Baffour F, Rossman PJ, Glaser KJ, et al. Cardiac MR elastography for quantitative assessment of elevated myocardial stiffness in cardiac amyloidosis. J Magn Reson Imaging. 2017;46(5):1361-7.
Li Z, Sun J, Hu X, Huang N, Han G, Chen L, et al. Assessment of liver fibrosis by variable flip angle T1 mapping at 3.0T. J Magn Reson Imaging. 2016;43(3):698-703.
Radenkovic D, Weingartner S, Ricketts L, Moon JC, Captur G. T1 mapping in cardiac MRI. Heart Fail Rev. 2017;22(4):415-30.
Magnetic resonance imaging of parenchymal liver disease: a comparison with ultrasound, radionuclide scintigraphy and X-ray computed tomography. The Clinical NMR Group. Clin Radiol. 1987;38(5):495-502.
Thomsen C, Christoffersen P, Henriksen O, Juhl E. Prolonged T1 in patients with liver cirrhosis: an in vivo MRI study. Magn Reson Imaging. 1990;8(5):599-604.
Hoy AM, McDonald N, Lennen RJ, Milanesi M, Herlihy AH, Kendall TJ, et al. Non-invasive assessment of liver disease in rats using multiparametric magnetic resonance imaging: a feasibility study. Biol Open. 2018;7(7).
Luetkens JA, Klein S, Traber F, Schmeel FC, Sprinkart AM, Kuetting DLR, et al. Quantification of Liver Fibrosis at T1 and T2 Mapping with Extracellular Volume Fraction MRI: Preclinical Results. Radiology. 2018;288(3):748-54.
McDonald N, Eddowes PJ, Hodson J, Semple SIK, Davies NP, Kelly CJ, et al. Multiparametric magnetic resonance imaging for quantitation of liver disease: a two-centre cross-sectional observational study. Sci Rep. 2018;8(1):9189.
Muller A, Hochrath K, Stroeder J, Hittatiya K, Schneider G, Lammert F, et al. Effects of Liver Fibrosis Progression on Tissue Relaxation Times in Different Mouse Models Assessed by Ultrahigh Field Magnetic Resonance Imaging. Biomed Res Int. 2017;2017:8720367.
Banerjee R, Pavlides M, Tunnicliffe EM, Piechnik SK, Sarania N, Philips R, et al. Multiparametric magnetic resonance for the non-invasive diagnosis of liver disease. J Hepatol. 2014;60(1):69-77.
Harrison SA, Dennis A, Fiore MM, Kelly MD, Kelly CJ, Paredes AH, et al. Utility and variability of three non-invasive liver fibrosis imaging modalities to evaluate efficacy of GR-MD-02 in subjects with NASH and bridging fibrosis during a phase-2 randomized clinical trial. PLoS One. 2018;13(9):e0203054.
Piechnik SK, Ferreira VM, Dall’Armellina E, Cochlin LE, Greiser A, Neubauer S, et al. Shortened Modified Look-Locker Inversion recovery (ShMOLLI) for clinical myocardial T1-mapping at 1.5 and 3 T within a 9 heartbeat breathhold. J Cardiovasc Magn Reson. 2010;12:69.
Tunnicliffe EM, Banerjee R, Pavlides M, Neubauer S, Robson MD. A model for hepatic fibrosis: the competing effects of cell loss and iron on shortened modified Look-Locker inversion recovery T1 (shMOLLI-T1) in the liver. J Magn Reson Imaging. 2017;45(2):450-62.
Kazour I, Serai SD, Xanthakos SA, Fleck RJ. Using T1 mapping in cardiovascular magnetic resonance to assess congestive hepatopathy. Abdom Radiol (NY). 2018;43(10):2679-85.
Pan S, Wang XQ, Guo QY. Quantitative assessment of hepatic fibrosis in chronic hepatitis B and C: T1 mapping on Gd-EOB-DTPA-enhanced liver magnetic resonance imaging. World J Gastroenterol. 2018;24(18):2024-35.
Guimaraes AR, Siqueira L, Uppal R, Alford J, Fuchs BC, Yamada S, et al. T2 relaxation time is related to liver fibrosis severity. Quant Imaging Med Surg. 2016;6(2):103-14.
Altbach MI, Bilgin A, Li Z, Clarkson EW, Trouard TP, Gmitro AF. Processing of radial fast spin-echo data for obtaining T2 estimates from a single k-space data set. Magn Reson Med. 2005;54(3):549-59.
Wang Y, Ganger DR, Levitsky J, Sternick LA, McCarthy RJ, Chen ZE, et al. Assessment of chronic hepatitis and fibrosis: comparison of MR elastography and diffusion-weighted imaging. AJR Am J Roentgenol. 2011;196(3):553-61.
Nekolla S, Gneiting T, Syha J, Deichmann R, Haase A. T1 maps by K-space reduced snapshot-FLASH MRI. J Comput Assist Tomogr. 1992;16(2):327-32.
Haimerl M, Verloh N, Zeman F, Fellner C, Muller-Wille R, Schreyer AG, et al. Assessment of clinical signs of liver cirrhosis using T1 mapping on Gd-EOB-DTPA-enhanced 3T MRI. PLoS One. 2013;8(12):e85658.
Aube C, Moal F, Oberti F, Roux J, Croquet V, Gallois Y, et al. Diagnosis and measurement of liver fibrosis by MRI in bile duct ligated rats. Dig Dis Sci. 2007;52(10):2601-9.
Kreft B, Dombrowski F, Block W, Bachmann R, Pfeifer U, Schild H. Evaluation of different models of experimentally induced liver cirrhosis for MRI research with correlation to histopathologic findings. Invest Radiol. 1999;34(5):360-6.
Aisen AM, Doi K, Swanson SD. Detection of liver fibrosis with magnetic cross-relaxation. Magn Reson Med. 1994;31(5):551-6.
Lee MJ, Kim MJ, Yoon CS, Han SJ, Park YN. Evaluation of liver fibrosis with T2 relaxation time in infants with cholestasis: comparison with normal controls. Pediatr Radiol. 2011;41(3):350-4.
Heye T, Yang SR, Bock M, Brost S, Weigand K, Longerich T, et al. MR relaxometry of the liver: significant elevation of T1 relaxation time in patients with liver cirrhosis. Eur Radiol. 2012;22(6):1224-32.
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The authors David H. Hoffman, Abimbola Ayoola, Hersh Chandarana, Krishna Prasad Shanbhogue have nothing to disclose. Dominik Nickel and Fei Han are Employee of Siemens Healthineers.
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Hoffman, D.H., Ayoola, A., Nickel, D. et al. T1 mapping, T2 mapping and MR elastography of the liver for detection and staging of liver fibrosis. Abdom Radiol 45, 692–700 (2020). https://doi.org/10.1007/s00261-019-02382-9
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DOI: https://doi.org/10.1007/s00261-019-02382-9