Multiparametric magnetic resonance for the non-invasive diagnosis of liver disease
Rajarshi Banerjee, Michael Pavlides, Elizabeth M Tunnicliffe, Stefan K Piechnik, Nikita Sarania, Rachel Philips, Jane D Collier, Jonathan C Booth, Jurgen E Schneider, Lai Mun Wang, David W Delaney, Ken A Fleming, Matthew D Robson, Eleanor Barnes, Stefan Neubauer, Rajarshi Banerjee, Michael Pavlides, Elizabeth M Tunnicliffe, Stefan K Piechnik, Nikita Sarania, Rachel Philips, Jane D Collier, Jonathan C Booth, Jurgen E Schneider, Lai Mun Wang, David W Delaney, Ken A Fleming, Matthew D Robson, Eleanor Barnes, Stefan Neubauer
Abstract
Background & aims: With the increasing prevalence of liver disease worldwide, there is an urgent clinical need for reliable methods to diagnose and stage liver pathology. Liver biopsy, the current gold standard, is invasive and limited by sampling and observer dependent variability. In this study, we aimed to assess the diagnostic accuracy of a novel magnetic resonance protocol for liver tissue characterisation.
Methods: We conducted a prospective study comparing our magnetic resonance technique against liver biopsy. The individual components of the scanning protocol were T1 mapping, proton spectroscopy and T2* mapping, which quantified liver fibrosis, steatosis and haemosiderosis, respectively. Unselected adult patients referred for liver biopsy as part of their routine care were recruited. Scans performed prior to liver biopsy were analysed by physicians blinded to the histology results. The associations between magnetic resonance and histology variables were assessed. Receiver-operating characteristic analyses were also carried out.
Results: Paired magnetic resonance and biopsy data were obtained in 79 patients. Magnetic resonance measures correlated strongly with histology (r(s)=0.68 p<0.0001 for fibrosis; r(s)=0.89 p<0.001 for steatosis; r(s)=-0.69 p<0.0001 for haemosiderosis). The area under the receiver operating characteristic curve was 0.94, 0.93, and 0.94 for the diagnosis of any degree of fibrosis, steatosis and haemosiderosis respectively.
Conclusion: The novel scanning method described here provides high diagnostic accuracy for the assessment of liver fibrosis, steatosis and haemosiderosis and could potentially replace liver biopsy for many indications. This is the first demonstration of a non-invasive test to differentiate early stages of fibrosis from normal liver.
Keywords: (1)H MRS; ANOVA; AUROC; Analysis of Variance; Area Under the Receiver Operating Characteristic Curve; BMI; Body Mass Index; CPA; CoV; Coefficient of Variance; Collagen Proportionate Area; HLC; Hepatic Lipid Content; Iron corrected T1; Liver fibrosis; Liver haemosiderosis; Liver steatosis; MR; Magnetic Resonance; Magnetic resonance T1 mapping; Magnetic resonance T2(⁎) mapping; NAFLD; Non-Alcoholic Fatty Liver Disease; Proton Magnetic Resonance Spectroscopy; Proton magnetic resonance spectroscopy; ROI; Region of interest; shMOLLI; shortened Modified Look Locker Inversion.
Copyright © 2013 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.
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References
- Blachier M., Leleu H., Peck-Radosavljevic M., Valla D.-C., Roudot-Thoraval F. The burden of liver disease in Europe: a review of available epidemiological data. J Hepatol. 2013;58:593–608.
- Younossi Z.M., Stepanova M., Afendy M., Fang Y., Younossi Y., Mir H. Changes in the prevalence of the most common causes of chronic liver diseases in the United States from 1988 to 2008. Clin Gastroenterol Hepatol. 2011;9:524–530.
- Poynard T., Lenaour G., Vaillant J.C., Capron F., Munteanu M., Eyraud D. Liver biopsy analysis has a low level of performance for diagnosis of intermediate stages of fibrosis. Clin Gastroenterol Hepatol. 2012;10:657–663.
- Tsochatzis E.A., Gurusamy K.S., Ntaoula S., Cholongitas E., Davidson B.R., Burroughs A.K. Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol. 2011;54:650–659.
- Friedrich-Rust M., Rosenberg W., Parkes J., Herrmann E., Zeuzem S., Sarrazin C. Comparison of ELF, FibroTest, and FibroScan for the non-invasive assessment of liver fibrosis. BMC Gastroenterol. 2010;10:103.
- Grønbaek K., Christensen P.B., Hamilton-Dutoit S., Federspiel B.H., Hage E., Jensen O.J. Interobserver variation in interpretation of serial liver biopsies from patients with chronic hepatitis C. J Viral Hepat. 2002;9:443–449.
- Regev A., Berho M., Jeffers L.J., Milikowski C., Molina E.G., Pyrsopoulos N.T. Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol. 2002;97:2614–2618.
- Ishak K., Baptista A., Bianchi L., Callea F., De Groote J., Gudat F. Histological grading and staging of chronic hepatitis. J Hepatol. 1995;22:696–699.
- Kleiner D.E., Brunt E.M., Van Natta M., Behling C., Contos M.J., Cummings O.W. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41:1313–1321.
- Brunt E.M., Janney C.G., Di Bisceglie A.M., Neuschwander-Tetri B.A., Bacon B.R. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol. 1999;94:2467–2474.
- Scheuer P.J., Williams R., Muir A.R. Hepatic pathology in relatives of patients with haemochromatosis. J Pathol Bacteriol. 1962;84:53–64.
- Rial B. Development of proton magnetic resonance spectroscopy in human heart at 3 Tesla. In: University of Oxford Doctoral thesis; 2010.
- Piechnik S.K., Ferreira V.M., Dall’Armellina E., Cochlin L.E., Greiser A., Neubauer S. 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.
- Ferreira V.M., Piechnik S.K., Dall’Armellina E., Karamitsos T.D., Francis J.M., Choudhury R.P. Non-contrast T1-mapping detects acute myocardial edema with high diagnostic accuracy: a comparison to T2-weighted cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2012;14:42.
- Rial B., Robson M.D., Neubauer S., Schneider J.E. Rapid quantification of myocardial lipid content in humans using single breath-hold 1H MRS at 3 Tesla. Magn Reson Med. 2011;66:619–624.
- Tunnicliffe E. Evaluating liver fibrosis in the presence of elevated iron using MR relaxometry. In: UK Provisional Patent No. 1304728.7 filed on 15th March; 2013.
- Nobili V., Parkes J., Bottazzo G., Marcellini M., Cross R., Newman D. Performance of ELF serum markers in predicting fibrosis stage in pediatric non-alcoholic fatty liver disease. Gastroenterology. 2009;136:160–167.
- Rosenberg W.M., Voelker M., Thiel R., Becka M., Burt A., Schuppan D. Serum markers detect the presence of liver fibrosis: a cohort study. Gastroenterology. 2004;127:1704–1713.
- Mariappan Y.K., Glaser K.J., Ehman R.L. Magnetic resonance elastography: a review. Clin Anat. 2010;23:497–511.
- Sandrin L., Fourquet B., Hasquenoph J.M., Yon S., Fournier C., Mal F. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29:1705–1713.
- Smith F.W., Mallard J.R., Reid A., Hutchison J.M. Nuclear magnetic resonance tomographic imaging in liver disease. Lancet. 1981;1:963–966.
- Aisen A.M., Doi K., Swanson S.D. Detection of liver fibrosis with magnetic cross-relaxation. Magn Reson Med. 1994;31:551–556.
- Alanen A., Komu M., Leino R., Toikkanen S. MR and magnetisation transfer imaging in cirrhotic and fatty livers. Acta Radiol. 1998;39:434–439.
- Kim K.A., Park M.S., Kim I.S., Kiefer B., Chung W.S., Kim M.J. Quantitative evaluation of liver cirrhosis using T1 relaxation time with 3 Tesla MRI before and after oxygen inhalation. J Magn Reson Imaging. 2012;36:405–410.
- Heye T., Yang S.R., Bock M., Brost S., Weigand K., Longerich T. MR relaxometry of the liver: significant elevation of T1 relaxation time in patients with liver cirrhosis. Eur Radiol. 2012;22:1224–1232.
- McPherson S., Jonsson J.R., Cowin G.J., O’Rourke P., Clouston A.D., Volp A. Magnetic resonance imaging and spectroscopy accurately estimate the severity of steatosis provided the stage of fibrosis is considered. J Hepatol. 2009;51:389–397.
- Meisamy S., Hines C.D., Hamilton G., Sirlin C.B., McKenzie C.A., Yu H. Quantification of hepatic steatosis with T1-independent, T2-corrected MR imaging with spectral modeling of fat: blinded comparison with MR spectroscopy. Radiology. 2011;258:767–775.
- Larson S.P., Bowers S.P., Palekar N.A., Ward J.A., Pulcini J.P., Harrison S.A. Histopathologic variability between the right and left lobes of the liver in morbidly obese patients undergoing Roux-en-Y bypass. Clin Gastroenterol Hepatol. 2007;5:1329–1332.
- Wood J.C. Magnetic resonance imaging measurement of iron overload. Curr Opin Hematol. 2007;14:183–190.
- Chandarana H., Lim R.P., Jensen J.H., Hajdu C.H., Losada M., Babb J.S. Hepatic iron deposition in patients with liver disease: preliminary experience with breath-hold multiecho T2⁎-weighted sequence. Am J Roentgenol. 2009;193:1261–1267.
Source: PubMed