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Non-Invasive Assessment of Liver Fibrosis with 31P-Magnetic Resonance Spectroscopy and Dynamic Contrast Enhanced Magnetic Resonance Imaging

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Non-Invasive Assessment of Liver Fibrosis with 31P-Magnetic Resonance Spectroscopy and Dynamic Contrast Enhanced Magnetic Resonance Imaging Linköping University Medical Dissertations No. 1351 Non-Invasive Assessment of Liver Fibrosis with 31P-Magnetic Resonance Spectroscopy and Dynamic Contrast Enhanced Magnetic Resonance Imaging Bengt Norén Faculty of Health Sciences Division of Radiological Sciences Department of Medicine and Health Sciences and Center for Medical Image Science and Visualization Linköping University, Sweden Linköping 2013 Non-Invasive Assessment of Liver Fibrosis with 31P-Magnetic Resonance Spectroscopy and Dynamic Contrast Enhanced Magnetic Resonance Imaging Linköping University Medical Dissertations No. 1351 © Bengt Norén, 2013 Published articles have been reprinted with the permission of the copyright holder ISBN 978-91-7519-705-0N ISSN 0345-0082 Printed by LiU-Tryck, Linköping, Sweden, 2013 CONTENTS Background 1 Diffuse Liver Disease 4 Liver Fibrosis, Cirrhosis, Complications and HCC 4 Evaluation of Liver Function and Prognostic Scores 7 Assessment of Fibrosis: Present ‘Gold Standard’ 8 Assessment of Fibrosis: Non-Invasive Techniques 9 Nuclear Magnetic Resonance 12 Basic Physics 12 The Spectroscopy Technique – MRS 13 Chemical Shift 13 Spin-Spin Coupling 14 Localization Methods 14 Liver Metabolites of Interest in 31P –MRS 14 Dynamic Contrast Enhanced MRI – DCE-MRI 16 Gd- EOB- DTPA (Primovist®) 16 Hepatocyte Uptake and Excretion Mechanisms 17 Quantification Procedures 18 31P –MRS 18 DCE-MRI 19 Aims of the Study 21 Materials and Methods 22 Localized In Vivo 31P NMR Spectroscopy 22 Data Acquisition 22 External Referencing 23 Processing 23 Absolute Quantification of In Vivo Liver Metabolite Concentrations 25 Dynamic Contrast Enhanced MRI – DCE-MRI 26 Data Acquisition 26 Image Analysis 27 Quantitative Measurements of Gd-EOB-DTPA Uptake 27 Visual Assessment of Gd-EOB-DTPA Excretion 30 Subjects, Paper I –IV 32 Clinical Data 33 Laboratory Analysis 33 Liver Biopsy and Histopathological Grading 34 Statistical Analysis 36 Results 38 Localized In Vivo 31P NMR Spectroscopy, Paper I-II 38 Concentrations Determined Using MRS 38 MRS Concentrations Expressed as Anabolic Charge, AC 40 MRS vs Laboratory Data 42 Dynamic Contrast Enhanced MRI, Paper III-IV 43 Final Diagnosis and Fibrosis Scoring 43 Pharmacokinetic Uptake Parameters vs Fibrosis Stage 43 Visually Assessed Contrast Excretion vs Contrast Uptake Parameters, Histopathology and Blood Tests 46 Discussion 48 31P – MR Spectroscopy 48 Dynamic Contrast Enhanced MRI 52 Clinical Significance 56 Conclusions 62 Acknowledgements 63 References 64 Original Papers 73 ABSTRACT The present study aims at demonstrating phosphorus metabolite concentration changes and alterations in uptake and excretion of a hepatocyte specific contrast agent in patients with diffuse - or suspected diffuse - liver disease by applying two non-invasive quantitative MR techniques and to compare the results with histo- pathological findings, with focus on liver fibrosis. In the first study phosphorus-31 MR spectroscopy using slice selection (DRESS) was implemented. Patients with histopathologically proven diffuse liver disease (n = 9) and healthy individuals (n = 12) were examined. The patients had significantly lower concentrations of phosphodiesters (PDE) and ATP compared with controls. Con- structing an ‘anabolic charge’ (AC) based on absolute concentrations, [PME] / ([PME] + [PDE]), the patients had a significant larger AC than the control subjects. The MRS technique was then, in a second study, applied on two distinct groups of patients, one group with steatosis and none-to-moderate inflammation (n = 13) and one group with severe fibrosis or cirrhosis (n = 16). A control group (n = 13) was also included. Lower concentrations of PDE and a higher AC were found in the cirrhosis group compared to the control group. Also compared to the steatosis group, the cir- rhosis group had lower concentrations of PDE and a higher AC. A significant corre- lation between fibrosis stage and PDE and fibrosis stage and AC was found. Using an AC cut-off value of 0.27 to discriminate between mild (stage 0-2) and advanced (stage 3-4) fibrosis yielded an AUROC value of 0.78, similar as for discriminating be- tween F0-1 vs. F2-4. Dynamic contrast enhanced MRI (DCE-MRI) was performed prospectively in a third study on 38 patients referred for evaluation of elevated serum alanine aminotrans- ferase (ALT) and/or alkaline phosphatase (ALP) levels. Data were acquired from re- i gions of interest in the liver and spleen by using single-breath-hold symmetrically sampled two-point Dixon 3D images time-series (non-enhanced, arterial and venous portal phase; 3, 10, 20 and 30 min) following a bolus injection of Gd-EOB-DTPA (0.025 mmol/kg). A new quantification procedure for calculation of the ‘hepatocyte specific uptake rate’, KHep, was applied on a two-compartment pharmacokinetic model. Liver-to-spleen contrast ratios (LSC_N) were also calculated. AUROC values of 0.71, 0.80 and 0.78, respectively, were found for KHep, LSC_N10 and LSC_N20 with regard to severe versus mild fibrosis. Significant group differences were found for KHep (borderline), LSC_N10 and LSC_N20. In study four, no significant correlation was found between visual assessments of bile ducts excretion of Gd-EOB-DTPA and histo-pathological grading of fibrosis or the quantified uptake of Gd-EOB-DTPA defined as KHep and LSC_N. In conclusion 31P-MRS and DCE-MRI show promising results for achieving a non- invasive approach in discriminating different levels of fibrosis from each other. ii LIST OF PAPERS I. Absolute quantification of human liver metabolite concentrations by localized in vivo 31P NMR spectroscopy in diffuse liver disease. Noren, B., Lundberg, P., Ressner, M., Wirell, S., Almer, S., and Smedby, Ö. (2005) Eur Radiol 15(1), 148-157 II. Separation of advanced from mild fibrosis in diffuse liver disease using 31P magnetic resonance spectroscopy Noren B, Dahlqvist O, Lundberg P, Almer S, Kechagias S, Ekstedt M, Franzén L, Wirell S and Smedby Ö. (2008) European Journal of Radiology 66 (2), 313-320, III. Separation of Advanced from mild fibrosis by quantification of the hepatobiliary uptake of Gd-EOB-DTPA. Noren B, Forsgren MF, Dahlqvist Leinhard O, Dahlström N, Kihlberg J, Romu T, Kechagias S, Almer S, Smedby Ö, Lundberg P (2012) Eur Radiol. 23(1), 174-181. IV. Visual assessment of biliary excretion of Gd-EOB-DTPA in patients with suspected diffuse liver disease – a biopsy-controlled prospective study. Norén B, Dahlström N, Forsgren M F, Dahlqvist Leinhard O, Kechagias S, Almer S, Wirell S, Smedby Ö, Lundberg P. (2012) Manuscript. iii AUTHOR CONTRIBUTIONS Paper I I participated in the planning of the study together with radiation physicists and hepatologists. I coordinated the pilot study, assisted in the data analysis and was partly responsible for writing, editing and submitting the manuscript. Paper II I participated in the planning of the study design and was responsible for the man- agement, coordination and partly executing the MRS examinations. I assisted in the data analysis and interpretation, wrote the first and final draft of the manuscript and managed the correspondence with the journal. Paper III I participated in the initial planning. I was responsible for the clinical part of the data processing and assisted in the analysis and interpretation. I wrote the first and final draft of the manuscript and managed the correspondence with the journal Paper IV I participated in the planning of the study design and the image review process. I performed the image review, assisted in the analysis and wrote the first and final draft of the manuscript iv LIST OF ABBREVIATIONS 2,3-DPG 2,3-diphosphoglycerate 99mTc 99mTechnetium AC Anabolic Charge ADC Apparent diffusion coefficient AIH Autoimmune hepatitis ALP Alkaline phosphatase ALT Alanine aminotransferase AMARES Advanced Method for Accurate, Robust and Efficient Spectral fitting AMP Adenosin monophosphate AST Aspartate aminotransferase ATP Adenosine triphosphate AUROC Area under receiver-operating characteristic curve CBD Common bile duct CHC Chronic hepatitis C CLD Chronic liver disease CSI Chemical Shift Imaging CT Computed tomography DCE-MRI Dynamic contrast enhanced MRI DRESS Depth- Resolved Surface coil Spectroscopy DWI Diffusion-weighted imaging ECM Extracellular matrix molecules EES Extracellular extravascular space ER Endoplasmic reticulum ERETIC Electronic Reference To access In vivo Concentrations FA Flip angle FID Free Induction Decay FT Fourier transformation Gd Gadolinium Gd-EOB-DTPA Gadolinium ethoxybenzyl diethylenetriaminepentaacetic acid GGT Gamma glutamic transpeptidase GPC Glycerophosphocholine GPE Glycerophosphoethanolamine GSA Galactosyl human serum albumin HbsAg Hepatitis B surface antigen HBV Hepatitis B virus HCC Hepatocellular carcinoma HCV Hepatitis C virus HSC Hepatic stellate cells ICG(R)-15 Indocyanine green retention at 15 min v ISIS Image Selective In vitro Spectroscopy LSC_N Liver-to-spleen contrast ratio, normalized MANA Multi scale adaptive normalizing averaging MELD Model for end-stage liver disease MeP Methyl Phosphonate MMP Matrix metalloproteinase MP Mobile phospholipids MRE Magnetic Resonance Elastograhpy MRI Magnetic Resonance Imaging MRP Multidrug resistance protein MRUI Magnetic resonance user interface NADH Nicotinamide adenine dinucleotide NAFLD Non-alcoholic fatty liver disease NASH Non alcoholic steatohepatitis NMR Nuclear Magnetic Resonance NTCP Na(+)-taurocholate-cotransporting polypeptide OATP Organic anion transporting polypeptide PBC Primary biliary cirrhosis PC Phosphocholine PCr Phosphocreatine
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