MR imaging of gray matter involvement in multiple sclerosis: Implications for understanding disease pathophysiology and monitoring treatment efficacy

American Journal of Neuroradiology

Volumn 31, Issue 7, 2010, Pages 1171-1177

  Filippi, Massimo ^a   Rocca, M A ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTERFERON; GLATIRAMER; PIOGLITAZONE;

BRAIN ATROPHY; BRAIN DAMAGE; DIFFUSION TENSOR IMAGING; DISEASE COURSE; DRUG EFFICACY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; MOTOR PERFORMANCE; MULTIPLE SCLEROSIS; NEUROIMAGING; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PATIENT MONITORING; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; VOXEL BASED MORPHOMETRY;

CENTRAL NERVOUS SYSTEM; DRUG MONITORING; HUMANS; MAGNETIC RESONANCE IMAGING; MULTIPLE SCLEROSIS;

EID: 77955603930     PISSN: 01956108     EISSN: 1936959X     Source Type: Journal    
DOI: 10.3174/ajnr.A1944     Document Type: Review

References (81)

1. Bo L, Vedeler CA, Nyland HI, et al. Subpial demyelination in the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol 2003;62:723-32 (Pubitemid 36870458)
2. Geurts JJ, Barkhof F. Grey matter pathology in multiple sclerosis. Lancet Neurol 2008;7:841-51
3. Bo L, Vedeler CA, Nyland H, et al. Intracortical multiple sclerosis lesions are not associated with increased lymphocyte infiltration. Mult Scler 2003;9:323-31 (Pubitemid 36958014)
4. Filippi M, Rocca MA. Functional MR imaging in multiple sclerosis. Neuroimaging Clin N Am 2009;19:59-70
5. Filippi M, Rocca MA. Conventional MRI in multiple sclerosis. J Neuroimaging 2007;17(suppl 1):3S-9S
6. Kidd D, Barkhof F, McConnell R, et al. Cortical lesions in multiple sclerosis. Brain 1999;122(pt 1):17-26
7. Bakshi R, Ariyaratana S, Benedict RH, et al. Fluid-attenuated inversion recovery magnetic resonance imaging detects cortical and juxtacortical multiple sclerosis lesions. Arch Neurol 2001;58:742-48
8. Geurts JJ, Pouwels PJ, Uitdehaag BM, et al. Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion-recovery MR imaging. Radiology 2005;236:254-60
9. Calabrese M, De Stefano N, Atzori M, et al. Detection of cortical inflammatory lesions by double inversion recovery magnetic resonance imaging in patients with multiple sclerosis. Arch Neurol 2007;64:1416-22
10. Calabrese M, Rocca MA, Atzori M, et al. Cortical lesions in primary progressive multiple sclerosis: a 2-year longitudinal MR study. Neurology 2009;72:1330-36
11. Calabrese M, Filippi M, Rovaris M, et al. Evidence for relative cortical sparing in benign multiple sclerosis: a longitudinal magnetic resonance imaging study. Mult Scler 2009;15:36-41
12. Calabrese M, Filippi M, Rovaris M, et al. Morphology and evolution of cortical lesions in multiple sclerosis: a longitudinal MRI study. Neuroimage 2008;42:1324-28
13. Pouwels PJ, Kuijer JP, Mugler JP 3rd, et al. Human gray matter: feasibility of single-slab 3D double inversion-recovery high-spatial-resolution MR imaging. Radiology 2006;241:873-79
14. Nelson F, Poonawalla AH, Hou P, et al. Improved identification of intracortical lesions in multiple sclerosis with phase-sensitive inversion recovery in combination with fast double inversion recovery MR imaging. AJNR Am J Neuroradiol 2007;28:1645-49
15. Nelson F, Poonawalla A, Hou P, et al. 3D MPRAGE improves classification of cortical lesions in multiple sclerosis. Mult Scler 2008;14:1214-19
16. Kangarlu A, Bourekas EC, Ray-Chaudhury A, et al. Cerebral cortical lesions in multiple sclerosis detected by MR imaging at 8 Tesla. AJNR Am J Neuroradiol 2007;28:262-66
17. Mainero C, Benner T, Radding A, et al. In vivo imaging of cortical pathology in multiple sclerosis using ultra-high field MRI. Neurology 2009;73:941-48. Epub 2009 Jul 29
18. Calabrese M, De Stefano N, Atzori M, et al. Extensive cortical inflammation is associated with epilepsy in multiple sclerosis. J Neurol 2008;255:581-86
19. Roosendaal SD, Moraal B, Pouwels PJ, et al. Accumulation of cortical lesions in MS: relation with cognitive impairment. Mult Scler 2009;15:708-14
20. Ormerod IE, Miller DH, McDonald WI, et al. The role of NMR imaging in the assessment of multiple sclerosis and isolated neurological lesions: a quantitative study. Brain 1987;110(pt 6):1579-616
21. Roosendaal SD, Moraal B, Vrenken H, et al. In vivo MR imaging of hippocampal lesions in multiple sclerosis. J Magn Reson Imaging 2008;27:726-31 (Pubitemid 351508085)
22. Filippi M, Agosta F. Magnetization transfer MRI in multiple sclerosis. J Neuroimaging 2007;17(suppl 1):22S-26S
23. Hayton T, Furby J, Smith KJ, et al. Grey matter magnetization transfer ratio independently correlates with neurological deficit in secondary progressive multiple sclerosis. J Neurol 2009;256:427-35
24. Rovaris M, Judica E, Sastre-Garriga J, et al. Large-scale, multicentre, quantitative MRI study of brain and cord damage in primary progressive multiple sclerosis. Mult Scler 2008;14:455-64 (Pubitemid 351943857)
25. Ranjeva JP, Audoin B, Au Duong MV, et al. Local tissue damage assessed with statistical mapping analysis of brain magnetization transfer ratio: relationship with functional status of patients in the earliest stage of multiple sclerosis. AJNR Am J Neuroradiol 2005;26:119-27 (Pubitemid 43079834)
26. Agosta F, Rovaris M, Pagani E, et al. Magnetization transfer MRI metrics predict the accumulation of disability 8 years later in patients with multiple sclerosis. Brain 2006;129:2620-27 (Pubitemid 44522095)
27. Khaleeli Z, Altmann DR, Cercignani M, et al. Magnetization transfer ratio in gray matter: a potential surrogate marker for progression in early primary progressive multiple sclerosis. Arch Neurol 2008;65:1454-59
28. Rovaris M, Agosta F, Pagani E, et al. Diffusion tensor MR imaging. Neuroimaging Clin N Am 2009;19:37-43
29. Rovaris M, Iannucci G, Falautano M, et al. Cognitive dysfunction in patients with mildly disabling relapsing-remitting multiple sclerosis: an exploratory study with diffusion tensor MR imaging. J Neurol Sci 2002;195:103-09
30. Rovaris M, Judica E, Gallo A, et al. Grey matter damage predicts the evolution of primary progressive multiple sclerosis at 5 years. Brain 2006;129:2628-34
31. De Stefano N, Filippi M, Miller D, et al. Guidelines for using proton MR spectroscopy in multicenter clinical MS studies. Neurology 2007;69:1942-52
32. Cifelli A, Arridge M, Jezzard P, et al. Thalamic neurodegeneration in multiple sclerosis. Ann Neurol 2002;52:650-53
33. Inglese M, Liu S, Babb JS, et al. Three-dimensional proton spectroscopy of deep gray matter nuclei in relapsing-remitting MS. Neurology 2004;63:170-72 (Pubitemid 38943801)
34. Geurts JJ, Reuling IE, Vrenken H, et al. MR spectroscopic evidence for thalamic and hippocampal, but not cortical, damage in multiple sclerosis. Magn Reson Med 2006;55:478-83 (Pubitemid 43352544)
35. Sijens PE, Mostert JP, Oudkerk M, et al. (1)H MR spectroscopy of the brain in multiple sclerosis subtypes with analysis of the metabolite concentrations in gray and white matter: initial findings. Eur Radiol 2006;16:489-95. Epub 2005 Jul 19
36. Caramanos Z, DiMaio S, Narayanan S, et al. (1)H-MRSI evidence for cortical gray matter pathology that is independent of cerebral white matter lesion load in patients with secondary progressive multiple sclerosis. J Neurol Sci 2009;282:72-79. Epub 2009 Feb 20
37. Sastre-Garriga J, Ingle GT, Chard DT, et al. Metabolite changes in normal-appearing gray and white matter are linked with disability in early primary progressive multiple sclerosis. Arch Neurol 2005;62:569-73
38. Neema M, Stankiewicz J, Arora A, et al. T1- and T2-based MRI measures of diffuse gray matter and white matter damage in patients with multiple sclerosis. J Neuroimaging 2007;17(suppl 1):16S-21S
39. Niepel G, Tench ChR, Morgan PS, et al. Deep gray matter and fatigue in MS: a T1 relaxation time study. J Neurol 2006;253:896-902. Epub 2006 Mar 13
40. Dalton CM, Chard DT, Davies GR, et al. Early development of multiple sclerosis is associated with progressive grey matter atrophy in patients presenting with clinically isolated syndromes. Brain 2004;127:1101-07
41. Tiberio M, Chard DT, Altmann DR, et al. Gray and white matter volume changes in early RRMS: a 2-year longitudinal study. Neurology 2005;64:1001-07 (Pubitemid 40388451)
42. Valsasina P, Benedetti B, Rovaris M, et al. Evidence for progressive gray matter loss in patients with relapsing-remitting MS. Neurology 2005;65:1126-28 (Pubitemid 41429650)
43. Sastre-Garriga J, Ingle GT, Chard DT, et al. Grey and white matter volume changes in early primary progressive multiple sclerosis: a longitudinal study. Brain 2005;128:1454-60 (Pubitemid 40826197)
44. Tedeschi G, Lavorgna L, Russo P, et al. Brain atrophy and lesion load in a large population of patients with multiple sclerosis. Neurology 2005;65:280-85
45. Chen JT, Narayanan S, Collins DL, et al. Relating neocortical pathology to disability progression in multiple sclerosis using MRI. Neuroimage 2004;23:1168-75
46. Fisher E, Lee JC, Nakamura K, et al. Gray matter atrophy in multiple sclerosis: a longitudinal study. Ann Neurol 2008;64:255-65
47. Amato MP, Bartolozzi ML, Zipoli V, et al. Neocortical volume decrease in relapsing-remitting MS patients with mild cognitive impairment. Neurology 2004;63:89-93
48. Benedict RH, Bruce JM, Dwyer MG, et al. Neocortical atrophy, third ventricular width, and cognitive dysfunction in multiple sclerosis. Arch Neurol 2006;63:1301-06
49. Henry RG, Shieh M, Okuda DT, et al. Regional grey matter atrophy in clinically isolated syndromes at presentation. J Neurol Neurosurg Psychiatry 2008;79:1236-44
50. Prinster A, Quarantelli M, Orefice G, et al. Grey matter loss in relapsing-remitting multiple sclerosis: a voxel-based morphometry study. Neuroimage 2006;29:859-67
51. Bendfeldt K, Kuster P, Traud S, et al. Association of regional gray matter volume loss and progression of white matter lesions in multiple sclerosis: a longitudinal voxel-based morphometry study. Neuroimage 2009;45:60-67
52. Ceccarelli A, Rocca MA, Pagani E, et al. A voxel-based morphometry study of grey matter loss in MS patients with different clinical phenotypes. Neuroimage 2008;42:315-22
53. Sepulcre J, Sastre-Garriga J, Cercignani M, et al. Regional gray matter atrophy in early primary progressive multiple sclerosis: a voxel-based morphometry study. Arch Neurol 2006;63:1175-80
54. Mesaros S, Rocca MA, Absinta M, et al. Evidence of thalamic gray matter loss in pediatric multiple sclerosis. Neurology 2008;70:1107-12
55. Morgen K, Sammer G, Courtney SM, et al. Evidence for a direct association between cortical atrophy and cognitive impairment in relapsing-remitting MS. Neuroimage 2006;30:891-98
56. Benedict RH, Zivadinov R, Carone DA, et al. Regional lobar atrophy predicts memory impairment in multiple sclerosis. AJNR Am J Neuroradiol 2005;26:1824-31
57. Sicotte NL, Kern KC, Giesser BS, et al. Regional hippocampal atrophy in multiple sclerosis. Brain 2008;131:1134-41
58. Sepulcre J, Masdeu JC, Goni J, et al. Fatigue in multiple sclerosis is associated with the disruption of frontal and parietal pathways. Mult Scler 2009;15:337-44
59. Anderson V, Fisniku L, Altmann D, et al. MRI measures show significant cerebellar gray matter volume loss in multiple sclerosis and are associated with cerebellar dysfunction. Mult Scler 2009;15:811-17
60. Sailer M, Fischl B, Salat D, et al. Focal thinning of the cerebral cortex in multiple sclerosis. Brain 2003;126:1734-44 (Pubitemid 36917333)
61. Mesaros S, Rovaris M, Pagani E, et al. A magnetic resonance imaging voxel-based morphometry study of regional gray matter atrophy in patients with benign multiple sclerosis. Arch Neurol 2008;65:1223-30
62. Audoin B, Ranjeva JP, Au Duong MV, et al. Voxel-based analysis of MTR images: a method to locate gray matter abnormalities in patients at the earliest stage of multiple sclerosis. J Magn Reson Imaging 2004;20:765-71
63. Davies GR, Altmann DR, Rashid W, et al. Emergence of thalamic magnetization transfer ratio abnormality in early relapsing-remitting multiple sclerosis. Mult Scler 2005;11:276-81 (Pubitemid 40775182)
64. Audoin B, Fernando KT, Swanton JK, et al. Selective magnetization transfer ratio decrease in the visual cortex following optic neuritis. Brain 2006;129:1031-39
65. Khaleeli Z, Cercignani M, Audoin B, et al. Localized grey matter damage in early primary progressive multiple sclerosis contributes to disability. Neuroimage 2007;37:253-61 (Pubitemid 47068988)
66. Ceccarelli A, Rocca MA, Valsasina P, et al. A multiparametric evaluation of regional brain damage in patients with primary progressive multiple sclerosis. Hum Brain Mapp 2009;30:3009-19
67. Bodini B, Khaleeli Z, Cercignani M, et al. Exploring the relationship between white matter and gray matter damage in early primary progressive multiple sclerosis: an in vivo study with TBSS and VBM. Hum Brain Mapp 2009;30:2852-61
68. Ciccarelli O, Wheeler-Kingshott CA, McLean MA, et al. Spinal cord spectroscopy and diffusion-based tractography to assess acute disability in multiple sclerosis. Brain 2007;130:2220-31 (Pubitemid 47236629)
69. Agosta F, Pagani E, Caputo D, et al. Associations between cervical cord gray matter damage and disability in patients with multiple sclerosis. Arch Neurol 2007;64:1302-05 (Pubitemid 47403085)
70. Rocca MA, Colombo B, Falini A, et al. Cortical adaptation in patients with MS: a cross-sectional functional MRI study of disease phenotypes. Lancet Neurol 2005;4:618-26 (Pubitemid 41317296)
71. Mezzapesa DM, Rocca MA, Rodegher M, et al. Functional cortical changes of the sensorimotor network are associated with clinical recovery in multiple sclerosis. Hum Brain Mapp 2008;29:562-73
72. Filippi M, Rocca MA, Falini A, et al. Correlations between structural CNS damage and functional MRI changes in primary progressive MS. Neuroimage 2002;15:537-46 (Pubitemid 34852521)
73. Penner IK, Rausch M, Kappos L, et al. Analysis of impairment related functional architecture in MS patients during performance of different attention tasks. J Neurol 2003;250:461-72 (Pubitemid 36459754)
74. Rocca MA, Agosta F, Colombo B, et al. fMRI changes in relapsing-remitting multiple sclerosis patients complaining of fatigue after IFNbeta-1a injection. Hum Brain Mapp 2007;28:373-82
75. Fazekas F, Soelberg-Sorensen P, Comi G, et al. MRI to monitor treatment efficacy in multiple sclerosis. J Neuroimaging 2007;17(suppl 1):50S-55S (Pubitemid 46558270)
76. Kaiser CC, Shukla DK, Stebbins GT, et al. A pilot test of pioglitazone as an add-on in patients with relapsing remitting multiple sclerosis. J Neuroimmunol 2009;211:124-30. Epub 2009 May 15
77. Rocca MA, Agosta F, Sormani MP, et al. A three-year, multi-parametric MRI study in patients at presentation with CIS. J Neurol 2008;255:683-91
78. Narayana PA, Wolinsky JS, Rao SB, et al. Multicentre proton magnetic resonance spectroscopy imaging of primary progressive multiple sclerosis. Mult Scler 2004;10(suppl 1):S73-78
79. Sajja BR, Narayana PA, Wolinsky JS, et al. Longitudinal magnetic resonance spectroscopic imaging of primary progressive multiple sclerosis patients treated with glatiramer acetate: multicenter study. Mult Scler 2008;14:73-80. Epub 2007 Sep 19
80. Wegner C, Filippi M, Korteweg T, et al. Relating functional changes during hand movement to clinical parameters in patients with multiple sclerosis in a multi-centre fMRI study. Eur J Neurol 2008;15:113-22
81. Rocca MA, Absinta M, Valsasina P, et al. Abnormal connectivity of the sensorimotor network in patients with MS: a multicenter fMRI study. Hum Brain Mapp 2009;30:2412-25