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      Heterogeneity of Multiple Sclerosis Lesions in Multislice Myelin Water Imaging

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          Abstract

          Purpose

          To assess neuroprotection and remyelination in Multiple Sclerosis (MS), we applied a more robust myelin water imaging (MWI) processing technique, including spatial priors into image reconstruction, which allows for lower SNR, less averages and shorter acquisition times. We sought to evaluate this technique in MS-patients and healthy controls (HC).

          Materials and Methods

          Seventeen MS-patients and 14 age-matched HCs received a 3T Magnetic Resonance Imaging (MRI) examination including MWI (8 slices, 12 minutes acquisition time), T2w and T1mprage pre and post gadolinium (GD) administration. Black holes (BH), contrast enhancing lesions (CEL) and T2 lesions were marked and registered to MWI. Additionally, regions of interest (ROI) were defined in the frontal, parietal and occipital normal appearing white matter (NAWM)/white matter (WM), the corticospinal tract (CST), the splenium (SCC) and genu (GCC) of the corpus callosum in patients and HCs. Mean values of myelin water fraction (MWF) were determined for each ROI.

          Results

          Significant differences (p≤0.05) of the MWF were found in all three different MS-lesion types (BH, CEL, T2 lesions), compared to the WM of HCs. The mean MWF values among the different lesion types were significantly differing from each other. Comparing MS-patients vs. HCs, we found a significant (p≤0.05) difference of the MWF in all measured ROIs except of GCC and SCC. The mean reduction of MWF in the NAWM of MS-patients compared to HCs was 37%. No age, sex, disability score and disease duration dependency was found for the NAWM MWF.

          Conclusion

          MWF measures were in line with previous studies and lesions were clearly visible in MWI. MWI allows for quantitative assessment of NAWM and lesions in MS, which could be used as an additional sensitive imaging endpoint for larger MS studies. Measurements of the MWF also differ between patients and healthy controls.

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          Most cited references23

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          In vivo visualization of myelin water in brain by magnetic resonance.

          A. Mackay, K Whittall, J. Adler … (1994)
          We exploit the intrinsic difference in magnetic resonance spin-spin relaxation time, T2, between water associated with myelin sheaths and water in other central nervous system tissue in order to measure myelin water content within any region of an image or to generate indirectly a myelin map of the brain. In normal volunteers, myelin water maps give the expected myelin distribution. In multiple sclerosis patients, lesions exhibit different myelin water contents providing insight into the demyelination process unavailable from conventional magnetic resonance images. In vivo myelin measurement has important applications in the clinical management of multiple sclerosis and other white matter diseases.
          Article 0 comments Cited 203 times – based on 0 reviews     Review now
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            Water content and myelin water fraction in multiple sclerosis. A T2 relaxation study.

            C Laule, I Vavasour, G R W Moore … (2004)
            Measurements of the T2 decay curve provide estimates of total water content and myelin water fraction in white matter in-vivo, which may help in understanding the pathological progression of multiple sclerosis (MS). Thirty-three MS patients (24 relapsing remitting, 8 secondary progressive, 1 primary progressive) and 18 controls underwent MR examinations. T2 relaxation data were acquired using a 32-echo measurement. All controls and 18 of the 33 MS patients were scanned in the transverse plane through the genu and splenium of the corpus callosum. Five white matter and 6 grey matter structures were outlined in each of these subjects. The remaining 15 MS patients were scanned in other transverse planes. A total of 189 lesions were outlined in the MS patients. Water content and myelin water fraction were calculated for all regions of interest and all lesions. The normal appearing white matter (NAWM) water content was, on average, 2.2% greater than that from controls, with significant differences occurring in the posterior internal capsules, genu and splenium of the corpus callosum, minor forceps and major forceps (p<0.0006). On average, MS lesions had 6.3% higher water content than contralateral NAWM (p<0.0001). Myelin water fraction was 16% lower in NAWM than for controls, with significant differences in the major and minor forceps, internal capsules, and splenium (p<0.05). The myelin water fraction of MS lesions averaged 52 % that of NAWM. NAWM in MS has a higher water content and lower myelin water fraction than control white matter. The cause of the myelin water fraction decrease in NAWM could potentially be due to either diffuse edema, inflammation, demyelination or any combination of these features. We present a simple model which suggests that myelin loss is the dominant feature of NAWM pathology.
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              Histopathologic correlate of hypointense lesions on T1-weighted spin-echo MRI in multiple sclerosis.

              Kiliaan van Wees, F. Barkhof, Peter Valk … (1998)
              Postmortem unfixed whole brains from five multiple sclerosis (MS) patients were examined by MRI using a T2- and T1-weighted spin-echo (SE) sequence and histology to investigate the histopathologic characteristics of hypointense lesions on T1-weighted SE MR images. The degree of hypointensity was scored semiquantitatively by two blinded observers in reference to normal-appearing white matter. Signal intensities of the lesions and the normal-appearing white matter were measured to obtain contrast ratios. Hematoxylin-eosin stain was used to assess degree of matrix destruction (decrease of density of the neuropil) and cellularity of a lesion, Klüver-Barrera stain for degree of demyelination, Bodian stain for axonal density, and immunostaining of glial fibrillary acid protein for reactive astrocytes and fibrillary gliosis. Nineteen lesions were selected for analysis. Nearly all lesions were compatible with the chronic MS plaque: hypocellularity, absence of myelinated axons, in the presence of reactive astrocytes. Contrast ratios of the lesions were highly correlated (R = -0.90; p < 0.01), with degree of hypointensity scored semiquantitatively. Degree of hypointensity on T1-weighted SE images did not correlate with degree of demyelination or number of reactive astrocytes, but was associated with axonal density (R = -0.71; p = 0.001). A trend was found with degree of matrix destruction (R = 0.45; p = 0.052). We conclude that, in our limited sample, hypointense lesions seen on T1-weighted SE MR images are associated histopathologically with severe tissue destruction, including axonal loss. Our results need to be substantiated in a larger study on more varied patient material to evaluate the use of hypointense lesions as a surrogate marker of persistent deficit in MS patients.
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                Author and article information

                Contributors
                Mara Cercignani: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 18 March 2016
                Publication date Collection: 2016
                Volume: 11
                Issue: 3
                Electronic Location Identifier: e0151496
                Affiliations
                [1 ]Department of Diagnostic and Interventional Neuroradiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
                [2 ]Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
                [3 ]Institute of Neuroimmunology and MS (INIMS), University Medical Center Hamburg-Eppendorf, Hamburg, Germany
                Brighton and Sussex Medical School, UNITED KINGDOM
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: TDF CT DK JS JF SS. Performed the experiments: TDF CT SS. Analyzed the data: TDF CT GB DK MG SS. Contributed reagents/materials/analysis tools: TDF CT JPS CH DK SS. Wrote the paper: TDF SS.

                Article
                Publisher ID: PONE-D-15-49902
                DOI: 10.1371/journal.pone.0151496
                PMC ID: 4798764
                PubMed ID: 26990645
                SO-VID: 56096fb4-10f6-4795-8716-d29d3d1f7afb
                Copyright © © 2016 Faizy et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 16 November 2015
                Date accepted : 29 February 2016
                Page count
                Figures: 4, Tables: 3, Pages: 13
                Funding
                This study was supported by the German Federal Ministry of Education and Research (Proposal/Contract 0315610–0315620 NEU2).
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Medicine and Health Sciences
                Subject: Radiology and Imaging
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Nervous System
                Subject: Central Nervous System
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Nervous System
                Subject: Central Nervous System
                Subject: Medicine and Health Sciences
                Subject: Clinical Medicine
                Subject: Clinical Immunology
                Subject: Autoimmune Diseases
                Subject: Multiple Sclerosis
                Subject: Biology and Life Sciences
                Subject: Immunology
                Subject: Clinical Immunology
                Subject: Autoimmune Diseases
                Subject: Multiple Sclerosis
                Subject: Medicine and Health Sciences
                Subject: Immunology
                Subject: Clinical Immunology
                Subject: Autoimmune Diseases
                Subject: Multiple Sclerosis
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Demyelinating Disorders
                Subject: Multiple Sclerosis
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Neurodegenerative Diseases
                Subject: Multiple Sclerosis
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Signs and Symptoms
                Subject: Lesions
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Signs and Symptoms
                Subject: Lesions
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Brain
                Subject: Corpus Callosum
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Brain
                Subject: Corpus Callosum
                Subject: Physical Sciences
                Subject: Astronomical Sciences
                Subject: Celestial Objects
                Subject: Black Holes
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Brain Mapping
                Subject: Brain Morphometry
                Subject: Diffusion Tensor Imaging
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Brain Morphometry
                Subject: Diffusion Tensor Imaging
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Brain Morphometry
                Subject: Diffusion Tensor Imaging
                Subject: Medicine and Health Sciences
                Subject: Radiology and Imaging
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Brain Morphometry
                Subject: Diffusion Tensor Imaging
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Neuroimaging
                Subject: Brain Morphometry
                Subject: Diffusion Tensor Imaging
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Neuroimaging
                Subject: Brain Morphometry
                Subject: Diffusion Tensor Imaging
                Custom metadata
                Data Availability All relevant data are within the paper and its Supporting Information files.

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