Quantitative Magnetic Resonance Imaging of Cortical Multiple Sclerosis Pathology

Although significant improvements have been made regarding the visualization and characterization of cortical multiple sclerosis (MS) lesions using magnetic resonance imaging (MRI), cortical lesions (CL) continue to be under-detected in vivo, and we have a limited understanding of the causes of GM pathology. The objective of this study was to characterize the MRI signature of CLs to help interpret the changes seen in vivo and elucidate the factors limiting their visualization. A quantitative 3D high-resolution (350 μm isotropic) MRI study at 3 Tesla of a fixed post mortem cerebral hemisphere from a patient with MS is presented in combination with matched immunohistochemistry. Type III subpial lesions are characterized by an increase in T1, T2 and M0, and a decrease in MTR in comparison to the normal appearing cortex (NAC). All quantitative MR parameters were associated with cortical GM myelin content, while T1 showed the strongest correlation. The histogram analysis showed extensive overlap between CL and NAC for all MR parameters and myelin content. This is due to the poor contrast in myelin content between CL and NAC in comparison to the variability in myelo-architecture throughout the healthy cortex. This latter comparison is highlighted by the representation of T1 times on cortical surfaces at several laminar depths.

[1]  D. Louis Collins,et al.  Automatic 3‐D model‐based neuroanatomical segmentation , 1995 .

[2]  Leif Østergaard,et al.  Cortical volumes and atrophy rates in FTD-3 CHMP2B mutation carriers and related non-carriers , 2009, NeuroImage.

[3]  F. Barkhof,et al.  Does high-field MR imaging improve cortical lesion detection in multiple sclerosis? , 2008, Journal of Neurology.

[4]  David H. Miller,et al.  Effects of formalin fixation on magnetic resonance indices in multiple sclerosis cortical gray matter , 2010, Journal of magnetic resonance imaging : JMRI.

[5]  B. Scheithauer,et al.  Inflammatory cortical demyelination in early multiple sclerosis. , 2011, The New England journal of medicine.

[6]  Alessandra Bertoldo,et al.  Cortical diffusion-tensor imaging abnormalities in multiple sclerosis: a 3-year longitudinal study. , 2011, Radiology.

[7]  Julien Cohen-Adad,et al.  In vivo evidence of disseminated subpial T2* signal changes in multiple sclerosis at 7T: A surface-based analysis , 2011, NeuroImage.

[8]  H. Merkle,et al.  Multisequence-imaging protocols to detect cortical lesions of patients with multiple sclerosis: Observations from a post-mortem 3 Tesla imaging study , 2009, Journal of the Neurological Sciences.

[9]  P. Narayana,et al.  Improved Identification of Intracortical Lesions in Multiple Sclerosis with Phase-Sensitive Inversion Recovery in Combination with Fast Double Inversion Recovery MR Imaging , 2007, American Journal of Neuroradiology.

[10]  Stephen J Blackband,et al.  Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue , 2009, Magnetic resonance in medicine.

[11]  F. Barkhof,et al.  Accumulation of cortical lesions in MS: relation with cognitive impairment , 2009, Multiple sclerosis.

[12]  Khader M Hasan,et al.  Diffusion-tensor MR imaging of cortical lesions in multiple sclerosis: initial findings. , 2008, Radiology.

[13]  P. Matthews,et al.  Neocortical neuronal, synaptic, and glial loss in multiple sclerosis , 2006, Neurology.

[14]  F. Barkhof,et al.  Postmortem verification of MS cortical lesion detection with 3D DIR , 2012, Neurology.

[15]  David H. Miller,et al.  High field (9.4 Tesla) magnetic resonance imaging of cortical grey matter lesions in multiple sclerosis. , 2010, Brain : a journal of neurology.

[16]  David Pitt,et al.  Imaging cortical lesions in multiple sclerosis with ultra-high-field magnetic resonance imaging. , 2010, Archives of neurology.

[17]  David H. Miller,et al.  Quantitative magnetic resonance of postmortem multiple sclerosis brain before and after fixation , 2008, Magnetic resonance in medicine.

[18]  L. Bø,et al.  The histopathology of grey matter demyelination in multiple sclerosis , 2009, Acta neurologica Scandinavica. Supplementum.

[19]  Alan C. Evans,et al.  Automatic "pipeline" analysis of 3-D MRI data for clinical trials: application to multiple sclerosis , 2002, IEEE Transactions on Medical Imaging.

[20]  M Riva,et al.  In vivo detection of cortical plaques by MR imaging in patients with multiple sclerosis. , 2006, AJNR. American journal of neuroradiology.

[21]  Mike P. Wattjes,et al.  Lesion detection at seven Tesla in multiple sclerosis using magnetisation prepared 3D-FLAIR and 3D-DIR , 2011, European Radiology.

[22]  J. Dawson,et al.  XVIII.–The Histology of Disseminated Sclerosis , 1916, Transactions of the Royal Society of Edinburgh.

[23]  G. B. Pike,et al.  Quantitative magnetization transfer and myelin water imaging of the evolution of acute multiple sclerosis lesions , 2010, Magnetic resonance in medicine.

[24]  Katrin Amunts,et al.  Observer‐independent analysis of high‐resolution MR images of the human cerebral cortex: In vivo delineation of cortical areas , 2007, Human brain mapping.

[25]  Nassir Navab,et al.  Medical Image Computing and Computer-Assisted Intervention - MICCAI 2010, 13th International Conference, Beijing, China, September 20-24, 2010, Proceedings, Part III , 2010, MICCAI.

[26]  F. Barkhof,et al.  Imaging the tip of the iceberg: visualization of cortical lesions in multiple sclerosis , 2011, Multiple sclerosis.

[27]  J. Wolinsky,et al.  3D MPRAGE improves classification of cortical lesions in multiple sclerosis , 2008, Multiple sclerosis.

[28]  Christine Stadelmann,et al.  Extensive Cortical Remyelination in Patients with Chronic Multiple Sclerosis , 2007, Brain pathology.

[29]  Massimo Filippi,et al.  Cortical lesions and atrophy associated with cognitive impairment in relapsing-remitting multiple sclerosis. , 2009, Archives of neurology.

[30]  B. Trapp,et al.  Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions , 2001, Annals of neurology.

[31]  Caterina Mainero,et al.  In vivo imaging of cortical pathology in multiple sclerosis using ultra-high field MRI , 2009, Neurology.

[32]  T. Benner,et al.  Focal cortical lesion detection in multiple sclerosis: 3 tesla DIR versus 7 tesla FLASH‐T2* , 2012, Journal of magnetic resonance imaging : JMRI.

[33]  B. Trapp,et al.  Subpial Demyelination in the Cerebral Cortex of Multiple Sclerosis Patients , 2003, Journal of neuropathology and experimental neurology.

[34]  B. Bedell,et al.  Synergistic Tissue Counterstaining and Image Segmentation Techniques for Accurate, Quantitative Immunohistochemistry , 2008, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[35]  F. Barkhof,et al.  Improved in vivo detection of cortical lesions in multiple sclerosis using double inversion recovery MR imaging at 3 Tesla , 2010, European Radiology.

[36]  Lasse Riis Østergaard,et al.  Active Surface Approach for Extraction of the Human Cerebral Cortex from MRI , 2006, MICCAI.

[37]  Frederik Barkhof,et al.  Cortical lesions in multiple sclerosis: combined postmortem MR imaging and histopathology. , 2005, AJNR. American journal of neuroradiology.

[38]  R. Turner,et al.  Microstructural Parcellation of the Human Cerebral Cortex – From Brodmann's Post-Mortem Map to in vivo Mapping with High-Field Magnetic Resonance Imaging , 2011, Front. Hum. Neurosci..

[39]  D. Chard,et al.  Grey matter pathology in clinically early multiple sclerosis: Evidence from magnetic resonance imaging , 2009, Journal of the Neurological Sciences.

[40]  M. Schlamann,et al.  First Clinical Study on Ultra-High-Field MR Imaging in Patients with Multiple Sclerosis: Comparison of 1.5T and 7T , 2009, American Journal of Neuroradiology.

[41]  B. Rutt,et al.  Rapid combined T1 and T2 mapping using gradient recalled acquisition in the steady state , 2003, Magnetic resonance in medicine.

[42]  David Pitt,et al.  T1 and proton density at 7 T in patients with multiple sclerosis: an initial study. , 2012, Magnetic resonance imaging.

[43]  M. Filippi,et al.  A 3‐year magnetic resonance imaging study of cortical lesions in relapse‐onset multiple sclerosis , 2009, Annals of neurology.

[44]  G. Pike,et al.  Correction for B1 and B0 variations in quantitative T2 measurements using MRI , 2000, Magnetic resonance in medicine.

[45]  D. Collins,et al.  Surface-based techniques reveal regions of reduced cortical magnetization transfer ratio in patients with MS , 2009 .

[46]  F Träber,et al.  Double inversion recovery brain imaging at 3T: diagnostic value in the detection of multiple sclerosis lesions. , 2007, AJNR. American journal of neuroradiology.

[47]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[48]  J. Parisi,et al.  A case of multiple sclerosis presenting with inflammatory cortical demyelination , 2011, Neurology.

[49]  S. Nelson,et al.  Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron , 2008, Annals of neurology.

[50]  Nikos Evangelou,et al.  3 Tesla and 7 Tesla MRI of multiple sclerosis cortical lesions , 2010, Journal of magnetic resonance imaging : JMRI.

[51]  Frederik Barkhof,et al.  Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion-recovery MR imaging. , 2005, Radiology.

[52]  S. B. Eickhoff,et al.  Quantitative architectural analysis: a new approach to cortical mapping , 2005, Anatomy and Embryology.

[53]  R. Rudick,et al.  Axonal transection in the lesions of multiple sclerosis. , 1998, The New England journal of medicine.

[54]  A Giorgio,et al.  Imaging distribution and frequency of cortical lesions in patients with multiple sclerosis , 2010, Neurology.

[55]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[56]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[57]  Hans Lassmann,et al.  Cortical demyelination and diffuse white matter injury in multiple sclerosis. , 2005, Brain : a journal of neurology.

[58]  Alan C. Evans,et al.  Fast and robust parameter estimation for statistical partial volume models in brain MRI , 2004, NeuroImage.

[59]  D. Louis Collins,et al.  Segmentation of Cortical MS Lesions on MRI Using Automated Laminar Profile Shape Analysis , 2010, MICCAI.

[60]  O. Ciccarelli,et al.  Consensus recommendations for MS cortical lesion scoring using double inversion recovery MRI , 2011, Neurology.