Table of Contents Author Guidelines Submit a Manuscript
Multiple Sclerosis International
Volume 2012, Article ID 742018, 13 pages
http://dx.doi.org/10.1155/2012/742018
Research Article

Quantitative Magnetic Resonance Imaging of Cortical Multiple Sclerosis Pathology

1McConnell Brain Imaging Centre, Montreal Neurological Institute, Montreal, Canada
2Small Animal Imaging Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute, Montreal, Canada
3Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmark

Received 4 May 2012; Revised 14 August 2012; Accepted 5 September 2012

Academic Editor: Bruno Stankoff

Copyright © 2012 Christine L. Tardif et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Dawson, “The histology of diseminated sclerosis,” Transactions of the Royal Society of Edinburgh, vol. 50, pp. 517–740, 1916. View at Google Scholar
  2. L. Bø, C. A. Vedeler, H. I. Nyland, B. D. Trapp, and S. J. Mørk, “Subpial demyelination in the cerebral cortex of multiple sclerosis patients,” Journal of Neuropathology and Experimental Neurology, vol. 62, no. 7, pp. 723–732, 2003. View at Google Scholar · View at Scopus
  3. C. Wegner, M. M. Esiri, S. A. Chance, J. Palace, and P. M. Matthews, “Neocortical neuronal, synaptic, and glial loss in multiple sclerosis,” Neurology, vol. 67, no. 6, pp. 960–967, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. J. W. Peterson, L. Bö, S. Mörk, A. Chang, and B. D. Trapp, “Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions,” Annals of Neurology, vol. 50, no. 3, pp. 389–400, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. B. D. Trapp, J. Peterson, R. M. Ransohoff, R. Rudick, S. Mörk, and L. Bö, “Axonal transection in the lesions of multiple sclerosis,” The New England Journal of Medicine, vol. 338, no. 5, pp. 278–285, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Kutzelnigg, C. F. Lucchinetti, C. Stadelmann et al., “Cortical demyelination and diffuse white matter injury in multiple sclerosis,” Brain, vol. 128, Part 11, pp. 2705–2712, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Chard and D. Miller, “Grey matter pathology in clinically early multiple sclerosis: evidence from magnetic resonance imaging,” Journal of the Neurological Sciences, vol. 282, no. 1-2, pp. 5–11, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. J. J. G. Geurts, P. J. W. Pouwels, B. M. J. Uitdehaag, C. H. Polman, F. Barkhof, and J. A. Castelijns, “Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion-recovery MR imaging,” Radiology, vol. 236, no. 1, pp. 254–260, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. M. P. Wattjes, G. G. Lutterbey, J. Gieseke et al., “Double inversion recovery brain imaging at 3T: diagnostic value in the detection of multiple sclerosis lesions,” American Journal of Neuroradiology, vol. 28, no. 1, pp. 54–59, 2007. View at Google Scholar · View at Scopus
  10. W. L. de Graaf, J. J. Zwanenburg, F. Visser et al., “Lesion detection at seven Tesla in multiple sclerosis using magnetisation prepared 3D-FLAIR and 3D-DIR,” European Radiology, vol. 22, no. 1, pp. 221–231, 2012. View at Google Scholar
  11. B. Simon, S. Schmidt, C. Lukas et al., “Improved in vivo detection of cortical lesions in multiple sclerosis using double inversion recovery MR imaging at 3 Tesla,” European Radiology, vol. 20, no. 7, pp. 1675–1683, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Bagnato, J. A. Butman, S. Gupta et al., “In vivo detection of cortical plaques by MR imaging in patients with multiple sclerosis,” American Journal of Neuroradiology, vol. 27, no. 10, pp. 2161–2167, 2006. View at Google Scholar
  13. F. Nelson, A. H. Poonawalla, P. Hou, F. Huang, J. S. Wolinsky, and P. A. Narayana, “Improved identification of intracortical lesions in multiple sclerosis with phase-sensitive inversion recovery in combination with fast double inversion recovery MR imaging,” American Journal of Neuroradiology, vol. 28, no. 9, pp. 1645–1649, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Nelson, A. Poonawalla, P. Hou, J. S. Wolinsky, and P. A. Narayana, “3D MPRAGE improves classification of cortical lesions in multiple sclerosis,” Multiple Sclerosis, vol. 14, no. 9, pp. 1214–1219, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. F. Bagnato, B. Yao, F. Cantor et al., “Multisequence-imaging protocols to detect cortical lesions of patients with multiple sclerosis: observations from a post-mortem 3 Tesla imaging study,” Journal of the Neurological Sciences, vol. 282, no. 1-2, pp. 80–85, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. E. C. Tallantyre, P. S. Morgan, J. E. Dixon et al., “3 Tesla and 7 Tesla MRI of multiple sclerosis cortical lesions,” Journal of Magnetic Resonance Imaging, vol. 32, no. 4, pp. 971–977, 2010. View at Google Scholar · View at Scopus
  17. J. J. G. Geurts, L. Bö, P. J. W. Pouwels, J. A. Castelijns, C. H. Polman, and F. Barkhof, “Cortical lesions in multiple sclerosis: combined postmortem MR imaging and histopathology,” American Journal of Neuroradiology, vol. 26, no. 3, pp. 572–577, 2005. View at Google Scholar · View at Scopus
  18. A. Seewann, H. Vrenken, E.-J. Kooi et al., “Imaging the tip of the iceberg: visualization of cortical lesions in multiple sclerosis,” Multiple Sclerosis, vol. 17, no. 10, pp. 1202–1210, 2011. View at Publisher · View at Google Scholar
  19. A. Seewann, E. J. Kooi, S. D. Roosendaal et al., “Postmortem verification of MS cortical lesion detection with 3D DIR,” Neurology, vol. 78, no. 5, pp. 302–308, 2012. View at Google Scholar
  20. S. D. Roosendaal, B. Moraal, P. J. W. Pouwels et al., “Accumulation of cortical lesions in MS: relation with cognitive impairment,” Multiple Sclerosis, vol. 15, no. 6, pp. 708–714, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Calabrese, F. Agosta, F. Rinaldi et al., “Cortical lesions and atrophy associated with cognitive impairment in relapsing-remitting multiple sclerosis,” Archives of Neurology, vol. 66, no. 9, pp. 1144–1150, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Calabrese, M. A. Rocca, M. Atzori et al., “A 3-year magnetic resonance imaging study of cortical lesions in relapse-onset multiple sclerosis,” Annals of Neurology, vol. 67, no. 3, pp. 376–383, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Kollia, S. Maderwald, N. Putzki et al., “First clinical study on ultra-high-field MR imaging in patients with multiple sclerosis: comparison of 1.5T and 7T,” American Journal of Neuroradiology, vol. 30, no. 4, pp. 699–702, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. A. S. Nielsen, R. P. Kinkel, E. Tinelli, T. Benner, J. Cohen-Adad, and C. Mainero, “Focal cortical lesion detection in multiple sclerosis: 3 tesla DIR versus 7 tesla FLASH-T2,” Journal of Magnetic Resonance Imaging, vol. 35, no. 3, pp. 537–542. View at Publisher · View at Google Scholar
  25. C. Mainero, T. Benner, A. Radding et al., “In vivo imaging of cortical pathology in multiple sclerosis using ultra-high field MRI,” Neurology, vol. 73, no. 12, pp. 941–948, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. J. J. G. Geurts, S. D. Roosendaal, M. Calabrese et al., “Consensus recommendations for MS cortical lesion scoring using double inversion recovery MRI,” Neurology, vol. 76, no. 5, pp. 418–424, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. K. T. Bluestein, D. Pitt, M. V. Knopp et al., “T1 and proton density at 7 T in patients with multiple sclerosis: an initial study,” Magnetic Resonance Imaging, vol. 30, no. 1, pp. 19–25, 2012. View at Publisher · View at Google Scholar
  28. M. Calabrese, F. Rinaldi, D. Seppi et al., “Cortical diffusion-tensor imaging abnormalities in multiple sclerosis: a 3-year Longitudinal study,” Radiology, vol. 261, no. 3, pp. 891–898, 2011. View at Google Scholar
  29. K. Schmierer, H. G. Parkes, P. W. So et al., “High field (9.4 Tesla) magnetic resonance imaging of cortical grey matter lesions in multiple sclerosis,” Brain, vol. 133, Part 3, pp. 858–867, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Pitt, A. Boster, W. Pei et al., “Imaging cortical lesions in multiple sclerosis with ultra-high-field magnetic resonance imaging,” Archives of Neurology, vol. 67, no. 7, pp. 812–818, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. J. J. G. Geurts, E. L. A. Blezer, H. Vrenken et al., “Does high-field MR imaging improve cortical lesion detection in multiple sclerosis?” Journal of Neurology, vol. 255, no. 2, pp. 183–191, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. S. C. L. Deoni, B. K. Rutt, and T. M. Peters, “Rapid combined T1 and T2 mapping using gradient recalled acquisition in the steady state,” Magnetic Resonance in Medicine, vol. 49, no. 3, pp. 515–526, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. J. G. Sled and G. B. Pike, “Correction for B(1) and B(0) variations in quantitative T(2) measurements using MRI,” Magnetic Resonance in Medicine, vol. 43, no. 4, pp. 589–593, 2000. View at Google Scholar
  34. D. L. Collins, P. Neelin, T. M. Peters, and A. C. Evans, “Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space,” Journal of Computer Assisted Tomography, vol. 18, no. 2, pp. 192–205, 1994. View at Google Scholar · View at Scopus
  35. D. L. Collins, C. J. Holmes, T. M. Peters, and A. C. Evans, “Automatic 3-D model-based neuroanatomical segmentation,” Human Brain Mapping, vol. 3, no. 3, pp. 190–208, 1995. View at Google Scholar · View at Scopus
  36. J. Mazziotta, A. Toga, A. Evans et al., “A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM),” Philosophical Transactions of the Royal Society B, vol. 356, no. 1412, pp. 1293–1322, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. A. P. Zijdenbos, R. Forghani, and A. C. Evans, “Automatic "pipeline" analysis of 3-D MRI data for clinical trials: Application to multiple sclerosis,” IEEE Transactions on Medical Imaging, vol. 21, no. 10, pp. 1280–1291, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Tohka, A. Zijdenbos, and A. Evans, “Fast and robust parameter estimation for statistical partial volume models in brain MRI,” NeuroImage, vol. 23, no. 1, pp. 84–97, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. S. F. Eskildsen and L. R. Ostergaard, “Active surface approach for extraction of the human cerebral cortex from MRI,” in Proceedings of the 9th International Conference on Medical Image Computing and Computer-Assisted Intervention (MICCAI '06), vol. 9 of Part 2, pp. 823–830, 2006.
  40. S. F. Eskildsen, L. R. Østergaard, A. B. Rodell et al., “Cortical volumes and atrophy rates in FTD-3 CHMP2B mutation carriers and related non-carriers,” NeuroImage, vol. 45, no. 3, pp. 713–721, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. S. P. Zehntner, M. M. Chakravarty, R. J. Bolovan, C. Chan, and B. J. Bedell, “Synergistic tissue counterstaining and image segmentation techniques for accurate, quantitative immunohistochemistry,” Journal of Histochemistry and Cytochemistry, vol. 56, no. 10, pp. 873–880, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. J. G. Sied, A. P. Zijdenbos, and A. C. Evans, “A nonparametric method for automatic correction of intensity nonuniformity in mri data,” IEEE Transactions on Medical Imaging, vol. 17, no. 1, pp. 87–97, 1998. View at Google Scholar · View at Scopus
  43. L. Bø, “The histopathology of grey matter demyelination in multiple sclerosis,” Acta Neurologica Scandinavica Supplementum, no. 189, pp. 51–57, 2009. View at Google Scholar · View at Scopus
  44. M. Calabrese, M. Battaglini, A. Giorgio et al., “Imaging distribution and frequency of cortical lesions in patients with multiple sclerosis,” Neurology, vol. 75, no. 14, pp. 1234–1240, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Cohen-Adad, T. Benner, D. Greve et al., “In vivo evidence of disseminated subpial T2* signal changes in multiple sclerosis at 7T: A surface-based analysis,” NeuroImage, vol. 57, no. 1, pp. 55–62, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Albert, J. Antel, W. Brück, and C. Stadelmann, “Extensive cortical remyelination in patients with chronic multiple sclerosis,” Brain Pathology, vol. 17, no. 2, pp. 129–138, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. C. F. Lucchinetti, F. G. Bogdan, Popescu et al., “Inflammatory cortical demyelination in early multiple sclerosis,” The New England Journal of Medicine, vol. 365, no. 23, pp. 2188–2197, 2011. View at Google Scholar
  48. B. F. G. Popescu, R. F. Bunyan, J. E. Parisi, R. M. Ransohoff, and C. F. Lucchinetti, “A case of multiple sclerosis presenting with inflammatory cortical demyelination,” Neurology, vol. 76, no. 20, pp. 1705–1710, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. T. M. Shepherd, P. E. Thelwall, G. J. Stanisz, and S. J. Blackband, “Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue,” Magnetic Resonance in Medicine, vol. 62, no. 1, pp. 26–34, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Schmierer, C. A. M. Wheeler-Kingshott, D. J. Tozer et al., “Quantitative magnetic resonance of postmortem multiple sclerosis brain before and after fixation,” Magnetic Resonance in Medicine, vol. 59, no. 2, pp. 268–277, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. K. Schmierer, J. R. Thavarajah, S. F. An, S. Brandner, D. H. Miller, and D. J. Tozer, “Effects of formalin fixation on magnetic resonance indices in multiple sclerosis cortical gray matter,” Journal of Magnetic Resonance Imaging, vol. 32, no. 5, pp. 1054–1060, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. I. R. Levesque, P. S. Giacomini, S. Narayanan et al., “Quantitative magnetization transfer and myelin water imaging of the evolution of acute multiple sclerosis lesions,” Magnetic Resonance in Medicine, vol. 63, no. 3, pp. 633–640, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. A. H. Poonawalla, K. M. Hasan, R. K. Gupta et al., “Diffusion-tensor MR imaging of cortical lesions in multiple sclerosis: initial findings,” Radiology, vol. 246, no. 3, pp. 880–886, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. K. E. Hammond, M. Metcalf, L. Carvajal et al., “Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron,” Annals of Neurology, vol. 64, no. 6, pp. 707–713, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Derakhshan, Z. Caramanos, S. Narayanan et al., “Surface-based techniques reveal regions of reduced cortical magnetization transfer ratio in patients with MS,” in Proceedings of the 17th Scientific Meeting of International Society for Magnetic Resonance in Medicine, Stockholm, Sweeden, 2010.
  56. C. L. Tardif, D. L. Collins, S. F. Eskildsen, J. B. Richardson, G. B. Pike et al., “Segmentation of cortical MS lesions on MRI using automated laminar profile shape analysis,” in Proceedings of the International conference on Medical Image Computing and Computer-Assisted Intervention (MICCAI '10), vol. 13 of Part 3, pp. 181–188, 2010.
  57. A. Schleicher, P. Morosan, K. Amunts, and K. Zilles, “Quantitative architectural analysis: a new approach to cortical mapping,” Journal of Autism and Developmental Disorders, vol. 39, no. 11, pp. 1568–1581, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. N. B. Walters, S. B. Eickhoff, A. Schleicher et al., “Observer-independent analysis of high-resolution MR images of the human cerebral cortex: in vivo delineation of cortical areas,” Human Brain Mapping, vol. 28, no. 1, pp. 1–8, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Geyer, M. Weiss, K. Reimann, G. Lohmann, 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,” Frontiers in Human Neuroscience, vol. 5, p. 19, 2011. View at Google Scholar