Journal of the Neurological Sciences
Volume 206, Issue 2 , Pages 157-164 , 15 February 2003

MRI–clinical correlations in the primary progressive course of MS: new insights into the disease pathophysiology from the application of magnetization transfer, diffusion tensor, and functional MRI

References 

  1. Thompson AJ, Polman CH, Miller DH, et al.  Primary progressive multiple sclerosis. Brain. 1997;120:1085–1096
  2. Cottrell DA, Kremenchutzky M, Rice GPA, et al.  The natural history of multiple sclerosis: a geographically based study. 5. The clinical features and natural history of primary progressive multiple sclerosis. Brain. 1999;122:625–639
  3. Thompson AJ, Kermode AG, MacManus DG, et al.  Patterns of disease activity in multiple sclerosis: clinical and magnetic resonance imaging study. Br. Med. J. 1990;300:631–634
  4. Thompson AJ, Kermode AG, Wicks D, et al.  Major differences in the dynamics of primary and secondary progressive multiple sclerosis. Ann. Neurol. 1991;29:53–62
  5. Kidd D, Thorpe JW, Kendall BE, et al.  MRI dynamics of brain and spinal cord in progressive multiple sclerosis. J. Neurol. Neurosurg. Psychiatry. 1996;60:15–19
  6. Lycklama à Nijeholt GJ, van Walderveen MAA, Castelijns JA, et al.  Brain and spinal cord abnormalities in multiple sclerosis. Correlation between MRI parameters, clinical subtypes and symptoms. Brain. 1998;121:687–697
  7. Stevenson VL, Miller DH, Rovaris M, et al.  Primary and transitional progressive MS. A clinical and MRI cross-sectional study. Neurology. 1999;52:839–845
  8. van Walderveen MAA, Lycklama à Nijeholt GJ, Ader HJ, et al.  Hypointense lesions on T1-weighted spin-echo magnetic resonance imaging. Relation to clinical characteristics in subgroups of patients with multiple sclerosis. Arch. Neurol. 2001;58:76–81
  9. Revesz T, Kidd D, Thompson AJ, Barnard RO, McDonald WI. A comparison of the pathology of primary and secondary progressive multiple sclerosis. Brain. 1994;117:759–765
  10. van Walderveen MAA, Kamphorst W, Scheltens P, et al.  Histopathologic correlate of hypointense lesions on T1-weighted spin-echo MRI in multiple sclerosis. Neurology. 1998;50:1282–1288
  11. Allen IV, McKeown SR. A histological, histochemical and biochemical study of the macroscopically normal white matter in multiple sclerosis. J. Neurol. Sci. 1979;41:81–89
  12. Reddy H, Narayanan S, Arnoutelis R, et al.  Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis. Brain. 2000;123:2314–2320
  13. Rocca MA, Falini A, Colombo B, Scotti G, Comi G, Filippi M. Adaptive functional changes in the cerebral cortex of patients with non-disabling MS correlate with the extent of brain structural damage. Ann. Neurol. 2002;51:330–339
  14. Magnetization transfer in multiple sclerosis. Neurology. 1999;53(Suppl. 3):
  15. Cercignani M, Horsfield MA. The physical basis of diffusion-weighted MRI. J. Neurol. Sci. 2001;186(Suppl. 1):S11–S14
  16. Werring DJ, Bullmore ET, Toosy AT, et al.  Recovery from optic neuritis is associated with a change in the distribution of cerebral response to visual stimulation: a functional magnetic resonance imaging study. J. Neurol. Neurosurg. Psychiatry. 2000;68:441–449
  17. Lee M, Reddy H, Johansen-Berg H, et al.  The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis. Ann. Neurol. 2000;47:606–613
  18. Filippi M, Rocca MA, Colombo B, et al.  Functional magnetic resonance imaging correlates of fatigue in multiple sclerosis. NeuroImage. 2002;15:559–567
  19. McDonald WI, Miller DH, Barnes D. The pathological evolution of multiple sclerosis. Neuropathol. Appl. Neurobiol. 1992;18:319–334
  20. van Waesberghe JH, Kamphorst W, DeGroot CJ, et al.  Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights into substrates of disability. Ann. Neurol. 1999;46:747–754
  21. LeBihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeanter M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology. 1986;161:401–407
  22. Woessner DE. NMR spin-echo self-diffusion measurement on fluids undergoing restricted diffusion. J. Phys. Chem. 1963;67:1365–1367
  23. Le Bihan D, Turner R, Pekar J, Moonen CTW. Diffusion and perfusion imaging by gradient sensitization: design, strategy and significance. J. Magn. Reson. Imaging. 1991;1:7–8
  24. Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys. J. 1994;66:259–267
  25. Pierpaoli C, Basser PJ. Towards a quantitative assessment of diffusion anisotropy. Magn. Reson. Med. 1996;36:893–906
  26. Cercignani M, Iannucci G, Rocca MA, Comi G, Horsfield MA, Filippi M. Pathologic damage in MS assessed by diffusion-weighted and magnetization transfer MRI. Neurology. 2000;54:1139–1144
  27. Ciccarelli O, Werring DJ, Wheeler-Kingshott CAM, et al.  Investigation of MS normal appearing brain using diffusion tensor MRI with clinical correlations. Neurology. 2001;56:926–933
  28. Filippi M, Cercignani M, Inglese M, Horsfield MA, Comi G. Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology. 2001;56:304–311
  29. Filippi M, Iannucci G, Cercignani M, Rocca MA, Pratesi A, Comi G. A quantitative study of water diffusion in MS lesions and NAWM using echo-planar imaging. Arch. Neurol. 2000;57:1017–1021
  30. Werring DJ, Clark CA, Barker GJ, Thompson AJ, Miller DH. Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis. Neurology. 1999;52:1626–1632
  31. Droogan AG, Clark CA, Werring DJ, Barker GJ, McDonald WI, Miller DH. Comparison of multiple sclerosis clinical subgroups using navigated spin echo diffusion-weighted imaging. Magn. Reson. Imaging. 1999;17:653–661
  32. Rocca MA, Cercignani M, Iannucci G, Comi G, Filippi M. Weekly diffusion-weighted imaging study of NAWM in MS. Neurology. 2000;55:882–884
  33. Bammer R, Augustin M, Strasser-Fuchs S, et al.  Magnetic resonance diffusion tensor imaging for characterizing diffuse and focal white matter abnormalities in multiple sclerosis. Magn. Reson. Med. 2000;44:583–591
  34. van Buchem MA, McGowan JC, Kolson DL, Polansky M, Grossman RI. Quantitative volumetric magnetization transfer analysis in multiple sclerosis: estimation of macroscopic and microscopic disease burden. Magn. Reson. Med. 1996;36:632–636
  35. Cercignani M, Inglese M, Pagani E, Comi G, Filippi M. Mean diffusivity and fractional anisotropy histograms of patients with multiple sclerosis. AJNR Am. J. Neuroradiol. 2001;22:952–958
  36. Cercignani M, Bozzali M, Iannucci G, Comi G, Filippi M. Magnetisation transfer ratio and mean diffusivity of normal appearing white and grey matter from patients with multiple sclerosis. J. Neurol. Neurosurg. Psychiatry. 2001;70:311–317
  37. Miller DH, Leary S, Dehmeshki J, et al.  Evidence for grey matter involvement in primary progressive MS: a magnetization transfer imaging study (abstract). J. Neurol. 2001;248(Suppl. 2):27
  38. Bozzali M, Rocca MA, Iannucci G, Pereira C, Comi G, Filippi M. Magnetization transfer histogram analysis of the cervical cord in patients with multiple sclerosis. AJNR Am. J. Neuroradiol. 1999;20:1803–1808
  39. Ogawa S, Menon RS, Tank DW, et al.  Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. Biophys. J. 1993;64:803–812
  40. Jueptner M, Weiller C. Review: does measurement of regional cerebral blood flow reflect synaptic activity? Implications for PET and fMRI. NeuroImage. 1995;2:148–156
  41. Malonek D, Grinvald A. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science. 1996;272:551–554
  42. Vanzetta I, Grinvald A. Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. Science. 1999;286:1555–1558
  43. Ogawa S, Menon RS, Kim SG, Ugurbil K. On the characteristics of functional magnetic resonance imaging of the brain. Annu. Rev. Biophys. Biomol. Struct. 1998;27:447–474
  44. Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS. Processing strategies for time-course data sets in functional MRI of the human brain. Magn. Reson. Med. 1993;30:161–173
  45. Gass A, Barker GJ, Kidd D, et al.  Correlation of magnetization transfer ratio with clinical disability in multiple sclerosis. Ann. Neurol. 1994;36:62–67
  46. Kurtzke JF. Rating neurological impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983;33:1444–1452
  47. Leary SM, Davie CA, Parker GJM, et al.  1H magnetic resonance spectroscopy of normal appearing white matter in primary progressive multiple sclerosis. J. Neurol. 1999;246:1023–1026
  48. Filippi M, Iannucci G, Tortorella C, et al.  Comparison of MS clinical phenotypes using conventional and magnetization transfer MRI. Neurology. 1999;52:588–594
  49. Dehmeshki J, Silver NC, Leary SM, Tofts PS, Thompson AJ, Miller DH. Magnetisation transfer ratio histogram analysis of primary progressive and other multiple sclerosis subgroups. J. Neurol. Sci. 2001;185:11–17
  50. Kalkers NF, Hintzen RQ, van Waesberghe JH, et al.  Magnetization transfer histogram parameters reflect all dimensions of MS pathology, including atrophy. J. Neurol. Sci. 2001;184:155–162
  51. Lublin FD, Reingold SC. The National Multiple Sclerosis Society (USA) advisory committee on clinical trials of new agents in multiple sclerosis. Defining the clinical course of multiple sclerosis: results of an international survey. Neurology. 1996;46:907–911
  52. Tortorella C, Viti B, Bozzali M, et al.  A magnetization transfer histogram study of normal-appearing brain tissue in MS. Neurology. 2000;54:183–186
  53. Bozzali M, Cercignani M, Comi G, Filippi M. Gray matter involvement in multiple sclerosis phenotypes: a diffusion tensor and magnetization transfer imaging study. Proc. Int. Soc. Magn. Reson. Med. 2001;9:95
  54. Rovaris M, Bozzali M, Santuccio G, et al.  In vivo assessment of the brain and cervical cord pathology of patients with primary progressive multiple sclerosis. Brain. 2001;124:2540–2549
  55. Thompson AJ, Montalban X, Barkhof F, et al.  Diagnostic criteria for primary progressive multiple sclerosis: a position paper. Ann. Neurol. 2000;47:831–835
  56. Evangelou N, Konz D, Esiri MM, Smith S, Palace J, Matthews PM. Regional axonal loss in the corpus callosum correlates with cerebral white matter lesion volume and distribution in multiple sclerosis. Brain. 2000;123:1845–1849
  57. Filippi M, Inglese M, Rovaris M, et al.  Magnetization transfer imaging to monitor the evolution of MS: a one-year follow up study. Neurology. 2000;55:940–946
  58. Filippi M, Bozzali M, Horsfield MA, et al.  A conventional and magnetization transfer MRI study of the cervical cord in patients with MS. Neurology. 2000;54:207–213
  59. Lycklama à Nijeholt GJ, Castelijns JA, Lazeron RH, et al.  Magnetization transfer ratio of the spinal cord in multiple sclerosis: relationship to atrophy and neurologic disability. J. Neuroimaging. 2000;10:67–72
  60. Rovaris M, Bozzali M, Santuccio G, et al.  Relative contributions of brain and cervical cord pathology to multiple sclerosis disability: a study with magnetisation transfer ratio analysis. J. Neurol. Neurosurg. Psychiatry. 2000;69:723–727
  61. Wilson M, Morgan PS, Lin X, Turner BP, Blumhardt LD. Quantitative diffusion weighted magnetic resonance imaging, cerebral atrophy and disability in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry. 2001;70:318–322
  62. Bozzali M, Cercignani M, Sormani MP, Comi G, Filippi M. Quantification of brain gray matter damage in different MS phenotypes using diffusion tensor MR imaging. AJNR Am. J. Neuroradiol. 2002; (in press)
  63. Rovaris M, Bozzali M, Iannucci G, et al.  Assessment of normal-appearing white and grey matter in primary progressive multiple sclerosis: a diffusion tensor MR imaging study. Arch. Neurol. 2002; (in press)
  64. Rocca MA, Mastronardo G, Rodegher M, Comi G, Filippi M. Long-term changes of magnetization transfer-derived measures from patients with relapsing–remitting and secondary progressive multiple sclerosis. AJNR Am. J. Neuroradiol. 1999;20:821–827
  65. Kidd D, Barkhof F, McConnell R, Algra PR, Allen IV, Revesz T. Cortical lesions in multiple sclerosis. Brain. 1999;122:17–26
  66. Brownell B, Hughes JT. The distribution of plaques in the cerebrum in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry. 1962;25:315–320
  67. Rocca MA, Matthews PM, Caputo D, et al.  Evidence for widespread movement-associated functional MRI changes in patients with PPMS. Neurology. 2002;58:866–872
  68. Filippi M, Rocca MA, Falini A, et al.  Correlations between structural CNS damage and functional MRI changes in primary progressive MS. NeuroImage. 2002;15:537–546
  69. Martino AM, Strick PL. Corticospinal projections originate from the arcuate premotor area. Brain Res. 1987;404:307–312
  70. Rao SM, Binder JR, Bandettini PA, et al.  Functional magnetic resonance imaging of complex human movements. Neurology. 1993;43:2311–2318
  71. Paus T, Petrides M, Evans AC, Meyer E. Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J. Neurophysiol. 1993;70:453–469
  72. Jenkins IH, Brooks DJ, Nixon PD, et al.  Motor sequence learning: a study with positron emission tomography. J. Neurosci. 1994;14:3775–3790
  73. Mesulam MM, Mufson EJ. The insula of reil in man and monkey: architectonics, connectivity, and function. In:  Peters A,  Jones EG editor. Cerebral cortex: association and auditory cortices. New York: Plenum; 1985;p. 179–226
  74. Cavada C, Goldman-Rakic PS. Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J. Comp. Neurol. 1989;287:422–445

PII: S0022-510X(02)00131-4

Journal of the Neurological Sciences
Volume 206, Issue 2 , Pages 157-164 , 15 February 2003

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