Magnetic Resonance Imaging in Multiple Sclerosis

Multiple Sclerosis: Diagnosis and Therapy

Volumn , Issue , 2012, Pages 136-162

  Neema, Mohit ^a,b   Ceccarelli, Antonia ^a,b   Jackson, Jonathan S ^a,b   Bakshi, Rohit ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Atrophy; Brain; CNS; Cortical lesion; Diffusion imaging; Gadolinium enhancing lesion; Iron; Magnetization transfer; MR spectroscopy; MRI; Multiple sclerosis; Relaxometry; Spinal cord; T1 black hole; T1 hyperintense lesion; T2 hypointensity; T2 hyperintense lesion

Indexed keywords

EID: 84886967509     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781119963714.ch6     Document Type: Chapter

References (141)

1. Bakshi R, Minagar A, Jaisani Z, Wolinsky JS. Imaging of multiple sclerosis: role in neurotherapeutics. NeuroRx 2005; 2: 277-303.
2. Neema M, Stankiewicz J, Arora A, Guss ZD, Bakshi R. MRI in multiple sclerosis: what's inside the toolbox. Neurotherapeutics 2007; 4: 602-17.
3. Filippi M, Rocca MA. Conventional MRI in multiple sclerosis. J Neuroimag 2007; 17: 3S-9S. 154 Pathology and Diagnosis 4 Bakshi R, Thompson AJ, Rocca MA, Pelletier D, Dousset V, Barkhof F, et al. MRI in multiple sclerosis: current status and future prospects. Lancet Neurol 2008; 7: 615-25.
4. Bruck W, Bitsch A, Kolenda H, Bruck Y, Stiefel M, Lassmann H. Inflammatory central nervous system demyelination: correlation of magnetic resonance imaging findings with lesion pathology. Ann Neurol 1997; 42: 783-93.
5. Geurts JJ, Pouwels PJ, Uitdehaag BM, Polman CH, Barkhof F, Castelijns JA. Intracortical lesions in multiple sclerosis: improved detection with 3D double inversionrecovery MR imaging. Radiology 2005; 236: 254-60.
6. WattjesMP, Barkhof F. High field MRI in the diagnosis of multiple sclerosis: high fieldhigh yield? Neuroradiology 2009; 51: 279-22.
7. Stankiewicz JM, Glanz BI, Healy BC, Arora A, Neema M, Benedict RH, et al. Brain MRI lesion load at 1.5T and 3T versus clinical status in multiple sclerosis. J Neuroimag 2011; 21(2): e50-6.
8. Meier DS, Weiner HL, Guttmann CR. Time-series modeling of multiple sclerosis disease activity: a promising window on disease progression and repair potential? Neurotherapeutics 2007; 4: 485-98.
9. Brex PA, Ciccarelli O, O'Riordan JI, Sailer M, Thompson AJ, Miller DH.Alongitudinal study of abnormalities on MRI and disability from multiple sclerosis. N Engl J Med 2002; 346: 158-64.
10. Li DK, Held U, Petkau J, Daumer M, Barkhof F, Fazekas F, et al. MRI T2 lesion burden in multiple sclerosis: a plateauing relationship with clinical disability. Neurology 2006; 66: 1384-9.
11. Sahraian MA, Radue EW, Haller S, Kappos L. Black holes in multiple sclerosis: definition, evolution, and clinical correlations. Acta Neurol Scand 2010; 122: 1-8.
12. Truyen L, van Waesberghe JH, van Walderveen MA, van Oosten BW, Polman CH, Hommes OR, et al. Accumulation of hypointense lesions ("black holes") on T1 spinecho MRI correlates with disease progression in multiple sclerosis. Neurology 1996; 47: 1469-76.
13. Bitsch A, Kuhlmann T, Stadelmann C, Lassmann H, Lucchinetti C, Brueck W. A longitudinal MRI study of histopathologically defined hypointense multiple sclerosis lesions. Ann Neurol 2001; 49: 793-6.
14. Fisher E, Chang A, Fox RJ, Tkach JA, Svarovsky T, Nakamura K, et al. Imaging correlates of axonal swelling in chronic multiple sclerosis brains. Ann Neurol 2007; 62: 219-28.
15. van Walderveen MA, Lycklama ANijeholt GJ, Adeér HJ, Jongen PJ, Polman CH, Castelijns JA, 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.
16. Molyneux PD, Brex PA, Fogg C, Lewis S, Middleditch C, Barkhof F, et al. The precision of T1 hypointense lesion volume quantification in multiple sclerosis treatment trials: a multicenter study. Mult Scler 2000; 6: 237-40.
17. Filippi M, Rovaris M, Rocca MA, Sormani MP, Wolinsky JS, Comi G. Glatiramer acetate reduces the proportion of new MS lesions evolving into "black holes". Neurology 2001; 57: 731-3.
18. Dalton CM,Miszkiel KA, Barker GJ, MacManusDG, Pepple TI, Panzara M, et al. Effect of natalizumab on conversion of gadolinium enhancing lesions to T1 hypointense lesions in relapsing multiple sclerosis. J Neurol 2004; 251: 407-13.
19. Bakshi R, Neema M, Healy BC, Liptak Z, Betensky RA, Buckle GJ, et al. Predicting clinical progression in multiple sclerosis with the magnetic resonance disease severity scale. Arch Neurol 2008; 65: 1449-53.
20. Waubant E. Biomarkers indicative of blood-brain barrier disruption in multiple sclerosis. Dis Markers 2006; 22: 235-44.
21. Cotton F, Weiner HL, Jolesz FA, Guttmann CR. MRI contrast uptake in new lesions in relapsing-remitting MS followed at weekly intervals. Neurology 2003; 60: 640-6.
22. Soon D, Tozer DJ, Altmann DR, Tofts PS, Miller DH. Quantification of subtle bloodbrain barrier disruption in nonenhancing lesions in multiple sclerosis: a study of disease and lesion subtypes. Mult Scler 2007; 13: 884-94.
23. Masdeu JC, Moreira J, Trasi S, Visintainer P, Cavaliere R, Grundman M. The open ring: a new imaging sign in demyelinating disease. J Neuroimag 1996; 6: 104-7.
24. Bakshi R, Glass J, Louis DN, Hochberg FH. Magnetic resonance imaging features of solitary inflammatory brain masses. J Neuroimag 1998; 8: 8-14.
25. Rovira A, Alonso J, Cucurella G, Nos C, Tintoreé M, Pedraza S, et al. Evolution of multiple sclerosis lesions on serial contrast-enhanced T1-weighted and magnetization- transfer MR images. AJNR Am J Neuroradiol 1999; 20: 1939-45.
26. Minneboo A, Uitdehaag BM, Ader HJ, Barkhof F, Polman CH, Castelijns JA. Patterns of enhancing lesion evolution in multiple sclerosis are uniform within patients. Neurology 2005; 65: 56-61.
27. McFarland HF, Stone LA, Calabresi PA, Maloni H, Bash CN, Frank JA. MRI studies of multiple sclerosis: implications for the natural history of the disease and for monitoring effectiveness of experimental therapies. Mult Scler 1996; 2: 198-205.
28. Kappos L, Moeri D, RadueEW,SchoetzauA, Schweikert K, Barkhof F, et al. Predictive value of gadolinium-enhanced magnetic resonance imaging for relapse rate and changes in disability or impairment in multiple sclerosis: a meta-analysis. Lancet 1999; 353: 964-9.
29. Molyneux PD, Filippi M, Barkhof F, Gasperini C, Yousry TA, Truyen L, et al. Correlations between monthly enhanced MRI lesion rate and changes in T2 lesion volume in multiple sclerosis. Ann Neurol 1998; 43: 332-9.
30. Smith ME, Stone LA, Albert PS, Frank JA, Martin R, Armstrong M, et al. Clinical worsening in multiple sclerosis is associated with increased frequency and area of gadopentetate dimenglumine-enhancing magnetic resonance imaging lesions. Ann Neurol 1993; 33: 480-9.
31. Broome DR, Girguis MS, Baron PW, Cottrell AC, Kjellin I, Kirk GA. Gadodiamideassociated nephrogenic systemic fibrosis: why radiologists should be concerned.AmJ Roentgenol 2007; 188: 586-92.
32. Lovblad KO, Anzalone N, Dorfler A, Essig M, Hurwitz B, Kappos L, et al. MR imaging in multiple sclerosis: review and recommendations for current practice. Am J Neuroradiol 2010; 31: 983-9.
33. Dousset V, Brochet B, Deloire MS, Lagoarde L, Barroso B, Caille JM, et al.MRimaging of relapsing multiple sclerosis patients using ultra-small-particle iron oxide and compared with gadolinium. Am J Neuroradiol 2006; 27: 1000-5.
34. Vellinga MM, Oude Engberink RD, Seewann A, Pouwels PJ, Wattjes MP, van der Pol SM, et al. Pluriformity of inflammation in multiple sclerosis shown by ultra-small iron oxide particle enhancement. Brain 2008; 131: 800-7.
35. Drayer BP. Magnetic resonance imaging of multiple sclerosis. BNI Q 1987; 3: 65-73.
36. Janardhan V, Suri S, Bakshi R. Hyperintense lesions in the brain on noncontrast T1-weighted MR scans (T1 shortening) in multiple sclerosis. Radiology 2007; 244: 823-31.
37. Stankiewicz J, Panter SS, Neema M, Arora A, Batt CE, Bakshi R. Iron in chronic brain disorders: imaging and neurotherapeutic implications. Neurotherapeutics 2007; 4: 371-86.
38. Neema M, Stankiewicz J, Arora A, Dandamudi VS, Batt CE, Guss ZD, et al. T1- and T2-based MRI measures of diffuse gray matter and white matter damage in patients with multiple sclerosis. J Neuroimag 2007; 17: 16S-21S.
39. Smith MA, Castellani R, Napoli S, Perry G, Guttmann CRG, De Girolami U, et al. Gray matter iron deposition in patients with multiple sclerosis: a histochemical study. Neurology 2007; 68: A118.
40. WilliamsR,WangWT, Choi IY, Lee SP, BermanNEJ, Lynch SG, et al. Cerebral vascular changes in an experimental model of multiple sclerosis. Mult Scler 2010; 6: 1010.
41. Ge Y, Jensen JH, Lu H, Helpern JA, Miles L, Inglese M, et al. Quantitative assessment of iron accumulation in the deep gray matter of multiple sclerosis by magnetic field correlation imaging. Am J Neuroradiol 2007; 28: 1639-44.
42. Hammond KE, Metcalf M, Carvajal L, Okuda DT, Srinivasan R, Vigneron D, et al. Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron. Ann Neurol 2008; 64: 707-13.
43. Khalil M, Enzinger C, Langkammer C, Tscherner M, Wallner-Blazek M, Jehna M, et al. Quantitative assessment of brain iron by R(2)-relaxometry in patients with clinically isolated syndrome and relapsing-remitting multiple sclerosis. Mult Scler 2009; 15: 1048-54.
44. Neema M, Arora A, Healy BC, Guss ZD, Brass SD, Duan Y, et al. Deep gray matter involvement on brain MRI scans is associated with clinical progression in multiple sclerosis. J Neuroimag 2009; 19: 3-8.
45. Sajja BR, Wolinsky JS, Narayana PA. Proton magnetic resonance spectroscopy in multiple sclerosis. Neuroimaging Clin N Am 2009; 19: 45-58.
46. De Stefano N, Filippi M, Miller D, Pouwels PJ, Rovira A, Gass A, et al. Guidelines for using protonMRspectroscopy in multicenter clinicalMSstudies. Neurology 2007; 69: 1942-52.
47. Davie CA, Hawkins CP, Barker GJ, Brennan A, Tofts PS, Miller DH, et al. Serial proton magnetic resonance spectroscopy in acute multiple sclerosis lesions. Brain 1994; 117: 49-58.
48. Husted CA, Goodin DS, Hugg JW, Maudsley AA, Tsuruda JS, de Bie SH, et al. Biochemical alterations in multiple sclerosis lesions and normal-appearing white matter detected by in vivo 31P and 1H spectroscopic imaging. Ann Neurol 1994; 36: 157-65.
49. Narayana PA. Magnetic resonance spectroscopy in the monitoring of multiple sclerosis. J Neuroimag 2005; 15: 46S-57S.
50. De Stefano N, Matthews PM, Antel JP, Preul M, Francis G, Arnold DL. Chemical pathology of acute demyelinating lesions and its correlation with disability. Ann Neurol 1995; 38: 901-9.
51. Wattjes MP, Harzheim M, Lutterbey GG, BogdanowM, Schild HH, Traber F. High field MR imaging and 1H-MR spectroscopy in clinically isolated syndromes suggestive of multiple sclerosis: correlation between metabolic alterations and diagnostic MR imaging criteria. J Neurol 2008; 255: 56-63.
52. Ropele S, Fazekas F. Magnetization transfer MR imaging in multiple sclerosis. Neuroimaging Clin N Am 2009; 19: 27-36.
53. Schmierer K, Scaravilli F, Altmann DR, Barker GJ, Miller DH. Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain. Ann Neurol 2004; 56: 407-15.
54. Schmierer K, Tozer DJ, Scaravilli F, Altmann DR, Barker GJ, Tofts PS, et al. Quantitative magnetization transfer imaging in postmortem multiple sclerosis brain. J Magnet Reson Imaging 2007; 26: 41-51.
55. Levesque IR, Giacomini PS, Narayanan S, Ribeiro LT, Sled JG, Arnold DL, et al. Quantitative magnetization transfer and myelin water imaging of the evolution of acute multiple sclerosis lesions. Magnet Reson Med 2010; 63: 633-40.
56. Chen JT, Collins DL, Freedman MS, Atkins HL, Arnold DL; Canadian MS/BMT Study Group. Local magnetization transfer ratio signal inhomogeneity is related to subsequent change in MTR in lesions and normal-appearing white-matter of multiple sclerosis patients. Neuroimage 2005; 25: 1272-8.
57. Chen JT, Kuhlmann T, Jansen GH, Collins DL, Atkins HL, Freedman MS, et al. Voxelbased analysis of the evolution of magnetization transfer ratio to quantify remyelination and demyelination with histopathological validation in a multiple sclerosis lesion. Neuroimage 2007; 36: 1152-8.
58. Sharma J, Zivadinov R, Jaisani Z, Fabiano AJ, Singh B, Horsfield MA, et al. A magnetization transfer MRI study of deep gray matter involvement in multiple sclerosis. J Neuroimag 2006; 16: 302-10.
59. Rocca MA, Agosta F, Sormani MP, Fernando K, TintoreéM, Korteweg T, et al. A threeyear, multi-parametric MRI study in patients at presentation with CIS. J Neurol 2008; 255: 683-91.
60. Filippi M, Rocca MA, Martino G, Horsfield MA, Comi G. Magnetization transfer changes in the normal appearing white matter precede the appearance of enhancing lesions in patients with multiple sclerosis. Ann Neurol 1998; 43: 809-14.
61. Agosta F, RovarisM,Pagani E, SormaniMP,ComiG, FilippiM.Magnetization transfer MRI metrics predict the accumulation of disability 8 years later in patients with multiple sclerosis. Brain 2006; 129: 2620-7.
62. Fisniku LK, Altmann DR, Cercignani M, Tozer DJ, Chard DT, Jackson JS, et al. Magnetization transfer ratio abnormalities reflect clinically relevant grey matter damage in multiple sclerosis. Mult Scler 2009; 15: 668-77.
63. Khaleeli Z, CercignaniM, Audoin B, Ciccarelli O, Miller DH, Thompson AJ. Localized grey matter damage in early primary progressive multiple sclerosis contributes to disability. Neuroimage 2007; 37: 253-61.
64. Agosta F, Pagani E, Caputo D, Filippi M. Associations between cervical cord gray matter damage and disability in patients with multiple sclerosis. Arch Neurol 2007; 64: 1302-5.
65. Bermel RA, Fisher E, Cohen JA. The use of MR imaging as an outcome measure in multiple sclerosis clinical trials. Neuroimaging Clin N Am 2008; 18: 687-701.
66. Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magnet Reson B 1996; 111: 209-19.
67. Goldberg-Zimring D, Mewes AU, Maddah M, Warfield SK. Diffusion tensor magnetic resonance imaging in multiple sclerosis. J Neuroimag 2005; 15: 68S-81S.
68. Rovaris M, Agosta F, Pagani E, Filippi M. Diffusion tensorMRimaging. Neuroimaging Clin N Am 2009; 19: 37-43.
69. Schmierer K, Wheeler-Kingshott CA, Boulby PA, Scaravilli F, Altmann DR, Barker GJ, et al. Diffusion tensor imaging of post mortem multiple sclerosis brain. Neuroimage 2007; 35: 467-77.
70. Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics 2007; 4: 316-29.
71. Rovaris M, Gass A, Bammer R, Hickman SJ, Ciccarelli O, Miller DH, et al. Diffusion MRI in multiple sclerosis. Neurology 2005; 65: 1526-32.
72. Yu CS, Lin FC, Liu Y, Duan Y, Lei H, Li KC. Histogramanalysis of diffusion measures in clinically isolated syndromes and relapsing-remitting multiple sclerosis. Eur J Radiol 2008; 68: 328-34.
73. Rovaris M, Judica E, Ceccarelli A, Ghezzi A, Martinelli V, Comi G, et al. A 3-year diffusion tensor MRI study of grey matter damage progression during the earliest clinical stage of MS. J Neurol 2008; 255: 1209-14.
74. Ceccarelli A, Rocca MA, Valsasina P, Rodegher M, Pagani E, Falini A, et al. A multiparametric evaluation of regional brain damage in patients with primary progressive multiple sclerosis. Hum Brain Mapp 2009; 30: 3009-19.
75. Hecke WV, Nagels G, Leemans A, Vandervliet E, Sijbers J, Parizel PM. Correlation of cognitive dysfunction and diffusion tensor MRI measures in patients with mild and moderate multiple sclerosis. J Magnet Reson Imaging 2010; 31: 1492-8.
76. Bodini B, Khaleeli Z, Cercignani M, Miller DH, Thompson AJ, Ciccarelli O. Exploring the relationship between white matter and gray matter damage in early primary progressive multiple sclerosis: an in vivo study with TBSS and VBM.HumBrain Mapp 2009; 30: 2852-61.
77. Ciccarelli O, Catani M, Johansen-Berg H, Clark C, Thompson A. Diffusion-based tractography in neurological disorders: concepts, applications, and future developments. Lancet Neurol 2008; 7: 715-27.
78. Lin X, Tench CR, Morgan PS, Niepel G, Constantinescu CS. 'Importance sampling' in MS: use of diffusion tensor tractography to quantify pathology related to specific impairment. J Neurol Sci 2005; 237: 13-19.
79. Lin F, Yu C, Jiang T, Li K, Chan P. Diffusion tensor tractography based group mapping of the pyramidal tract in relapsing-remitting multiple sclerosis patients. Am J Neuroradiol 2007; 28: 278-82.
80. Ozturk A, Smith SA, Gordon-Lipkin EM, Harrison DM, Shiee N, Pham DL, et al. MRI of the corpus callosum in multiple sclerosis: association with disability. Mult Scler 2010; 16: 166-77.
81. Fox RJ. Picturing multiple sclerosis: conventional and diffusion tensor imaging. Semin Neurol. 2008; 28: 453-66.
82. Agosta F, Absinta M, Sormani MP, Ghezzi A, Bertolotto A, Montanari E, et al. In vivo assessment of cervical cord damage in MS patients: a longitudinal diffusion tensor MRI study. Brain 2007; 130: 2211-19.
83. Pagani E, Hirsch JG, Pouwels PJ, Horsfield MA, Perego E, Gass A, et al. Intercenter differences in diffusion tensor MRI acquisition. J Magnet Reson Imaging 2010; 31: 1458-68.
84. MacKay AL, Vavasour IM, Rauscher A, Kolind SH,Madler B, Moore GRW, et al. MR relaxation in multiple sclerosis. Neuroimaging Clin N Am 2009; 19: 1-26.
85. Haacke ME, Brown RW, Thompson ME, Venkatesan R. Magnetic Resonance Imaging, Physical Principles and Sequence Design. John Wiley & Sons: New York, 1999.
86. Look DC, Locker DR. Time saving in measurement of NMRand EPR relaxation times. Rev Sci Instrum 1970; 41: 250-1.
87. Vrenken H, Geurts JJG, Knol DL, van Dijk LN, Dattola V, Jasperse B, et al. Wholebrain T1 mapping in multiple sclerosis: global changes of normal-appearing gray and white matter. Radiology 2006; 240: 811-20.
88. Parry A, Clare S, Jenkinson M, Smith S, Palace J, Matthews PM. White matter and lesion T1 relaxation times increase in parallel and correlate with disability in multiple sclerosis. J Neurol 2002; 249: 1279-86.
89. Parry A, Clare S, Jenkinson M, Smith S, Palace J, Matthews PM. MRI brain T1 relaxation time changes in MS patients increase over time in both the white matter and the cortex. J Neuroimag 2003; 13: 234-9.
90. Whittall KP, MacKay AL, Li DK. Are mono-exponential fits to a few echoes sufficient to determine T2 relaxation for in vivo human brain? Magnet Reson Med 1999; 41: 1255-7.
91. Laule C, Kozlowski P, Leung E, Li DKB, Mackay AL, Moore GRW. Myelin water imaging of multiple sclerosis at 7 T: correlations with histopathology. Neuroimage 2008; 40: 1575-80.
92. Neema M, Goldberg-Zimring D, Guss ZD, Healy BC, Guttmann CR, Houtchens MK, et al. 3 T MRI relaxometry detects T2 prolongation in the cerebral normal-appearing white matter in multiple sclerosis. Neuroimage 2009; 46: 633-41.
93. Laule C, Vavasour IM, Moore GR, Oger J, Li DK, Paty DW, et al. Water content and myelin water fraction in multiple sclerosis. A T2 relaxation study. J Neurol 2004; 251: 284-93.
94. Vavasour IM, Laule C, Li DK, Oger J, Moore GR, Traboulsee A, et al. Longitudinal changes in myelin water fraction in two MS patients with active disease. J Neurol Sci 2009; 276: 49-53.
95. Armspach JP, Gounot D, Rumbach L, Chambron J. In vivo determination of multiexponential T2 relaxation in the brain of patients with multiple sclerosis. Magnet Reson Imaging 1991; 9: 107-13.
96. Stevenson VL, Parker GJ, Barker GJ, Birnie K, Tofts PS, Miller DH, et al. Variations in T1 and T2 relaxation times of normal appearing white matter and lesions in multiple sclerosis. J Neurol Sci 2000; 178: 81-7.
97. Oh J, Han ET, Lee MC, Nelson SJ, Pelletier D. Multislice brain myelin water fractions at 3T in multiple sclerosis. J Neuroimag 2007; 17: 156-63.
98. Bermel RA, Bakshi R. The measurement and clinical relevance of brain atrophy in multiple sclerosis. Lancet Neurol 2006; 5: 158-70.
99. Ge Y, Gonen O, Inglese M, Babb JS, Markowitz CE, Grossman RI. Neuronal cell injury precedes brain atrophy in multiple sclerosis. Neurology 2004; 62: 624-7.
100. Davies GR, Altmann DR, Hadjiprocopis A, Rashid W, Chard DT, Griffin CM, et al. Increasing normal-appearing grey and white matter magnetisation transfer ratio abnormality in early relapsing-remitting multiple sclerosis. J Neurol 2005; 252: 1037-44.
101. De Stefano N, Iannucci G, Sormani MP, Guidi L, Bartolozzi ML, Comi G, Federico A, et al. MR correlates of cerebral atrophy in patients with multiple sclerosis. J Neurol 2002; 249: 1072-7.
102. Chard DT, Brex PA, Ciccarelli O, Griffin CM, Parker GJ, Dalton C, et al. The longitudinal relation between brain lesion load and atrophy in multiple sclerosis: a 14 year follow up study. J Neurol Neurosurg Psychiat 2003; 74: 1551-4.
103. Calabrese M, Rocca MA, Atzori M, Mattisi I, Favaretto A, Perini P, et al. A 3-year magnetic resonance imaging study of cortical lesions in relapse-onset multiple sclerosis. Ann Neurol 2010; 67: 376-83.
104. Bakshi R, Dandamudi VSR, Neema M, De C, Bermel RA. Measurement of brain and spinal cord atrophy by magnetic resonance imaging as a tool to monitor multiple sclerosis. J Neuroimag 2005; 15: 30S-45S. 106 Pirko I, Lucchinetti CF, Sriram S, Bakshi R. Gray matter involvement in multiple sclerosis. Neurology 2007; 68: 634-42.
105. Ceccarelli A, Rocca MA, Pagani E, Colombo B, Martinelli V, Comi G. et al. A voxelbased morphometry study of grey matter loss in MS patients with different clinical phenotypes. Neuroimage 2008; 42: 315-22.
106. Sanfilipo MP, Benedict RHB, Sharma J, Weinstock-Guttman B, Bakshi R. The relationship between whole brain volume and disability in multiple sclerosis: a 160 Pathology and Diagnosis comparison of normalized gray vs. white matter with misclassification correction. Neuroimage 2005; 26: 1068-77.
107. Fisher E, Lee JC, Nakamura K, Rudick RA. Gray matter atrophy in multiple sclerosis: a longitudinal study. Ann Neurol 2008; 64: 255-65.
108. Grassiot B, Desgranges B, Eustache F, Defer G. Quantification and clinical relevance of brain atrophy in multiple sclerosis: a review. J Neurol 2009; 256: 1397-1412.
109. Wylezinska M, Cifelli A, Jezzard P, Palace J, Alecci M, Matthews PM. Thalamic neurodegeneration in relapsing-remitting multiple sclerosis. Neurology 2003; 60: 1949-54.
110. Bermel RA, Innus MD, Tjoa CW, Bakshi R. Selective caudate atrophy in multiple sclerosis: a 3D MRI parcellation study. Neuroreport 2003; 14: 335-9.
111. Houtchens MK, Benedict RHB, Killiany R, Sharma J, Jaisani Z, Singh B, et al. Thalamic atrophy and cognition in multiple sclerosis. Neurology 2007; 69: 1213-23.
112. Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 2000; 97: 11050-5.
113. Geurts JJ, Barkhof F. Grey matter pathology in multiple sclerosis. Lancet Neurol 2008; 7: 841-51.
114. Peterson JW, Bo L, Mork S, Chang A, Trapp BD. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001; 50: 389-400.
115. BøL, Vedeler CA,Nyland HI, Trapp BD,Mørk SJ. Subpial demyelinationin the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol 2003; 62: 723-32.
116. Bo L, Geurts JJG, van der Valk P, Polman C, Barkhof F. Lack of correlation between cortical demyelination and white matter pathologic changes in multiple sclerosis. Arch Neurol 2007; 64: 76-80.
117. Bakshi R, Ariyaratana S, Benedict RH, Jacobs L. Fluid-attenuated inversion recovery magnetic resonance imaging detects cortical and juxtacortical multiple sclerosis lesions. Arch Neurol 2001; 58: 742-8.
118. Simon B, Schmidt S, Lukas C, Gieseke J, Traber F, Knol DL, et al. Improved in vivo detection of cortical lesions in multiple sclerosis using double inversion recovery MR imaging at 3 Tesla. Eur Radiol 2010; 20: 1675-83.
119. Nelson F, Poonawalla A, Hou P, Wolinsky JS, Narayana PA. 3D MPRAGE improves classification of cortical lesions in multiple sclerosis. Mult Scler 2008; 14: 1214-19.
120. Calabrese M, Agosta F, Rinaldi F, Mattisi I, Grossi P, Favaretto A, et al. Cortical lesions and atrophy associated with cognitive impairment in relapsing-remitting multiple sclerosis. Arch Neurol 2009; 66: 1144-50.
121. Chard DT, Miller DH. What you see depends on how you look: Gray matter lesions in multiple sclerosis. Neurology 2009; 73: 918-19.
122. Mainero C, Benner T, Radding A, van der Kouwe A, Jensen R, Rosen BR, et al. In vivo imaging of cortical pathology in multiple sclerosis using ultra-high field MRI. Neurology 2009; 73: 941-8.
123. Schmierer K, Parkes HG, So P, An SF, Brandner S, Ordidge RJ, et al. High field (9.4 Tesla) magnetic resonance imaging of cortical grey matter lesions in multiple sclerosis. Brain 2010; 133: 858-67.
124. Bot JC, Barkhof F, Polman CH, Lycklama à Nijeholt GJ, de Groot V, et al. Spinal cord abnormalities in recently diagnosed MS patients: added value of spinal MRI examination. Neurology 2004; 62: 226-33.
125. Thorpe JW, Kidd D, Moseley IF, Kenndall BE, Thompson AJ, MacManus DG, et al. Serial gadolinium-enhanced MRI of the brain and spinal cord in early relapsingremitting multiple sclerosis. Neurology 1996; 46: 373-8.
126. Thorpe JW, Kidd D, Kendall BE, Tofts PS, Barker GJ, Thompson AJ, et al. Spinal cord MRI using multi-array coils and fast spin echo. I. Technical aspects and findings in healthy adults. Neurology 1993; 43: 2625-31.
127. Bot JC, Barkhof F. Spinal-cord MRI in multiple sclerosis: conventional and nonconventional MR techniques. Neuroimag Clin N Am 2009; 19: 81-99.
128. Poonawalla AH, Hou P, Nelson FA, Wolinsky JS, Narayana PA. Cervical spinal cord lesions in multiple sclerosis: T1-weighted inversion-recovery MR imaging with phase-sensitive reconstruction. Radiology 2008; 246: 258-64.
129. Nijeholt GJ, van Walderveen MA, Castelijns JA, van Waesberghe JH, Polman C, Scheltens P, et al. Brain and spinal cord abnormalities in multiple sclerosis. Correlation between MRI parameters, clinical subtypes and symptoms. Brain 1998; 121: 687-97.
130. Kidd D, Thorpe JW, Thompson AJ, Kendall BE, Moseley IF, MacManus DG, et al. Spinal cord MRI using multi-array coils and fast spin echo. II. Findings in multiple sclerosis. Neurology 1993; 43: 2632-7.
131. Nijeholt GJ, Barkhof F, Scheltens P, Castelijns JA, Adeér H, van Waesberghe JH, et al. MR of the spinal cord in multiple sclerosis: relation to clinical subtype and disability. AJNR Am J Neuroradiol 1997; 18: 1041-8.
132. Gilmore CP, Bo L, Owens T, Lowe J, Esiri MM, Evangelou N. Spinal cord gray matter demyelination in multiple sclerosis-a novel pattern of residual plaque morphology. Brain Pathol 2006; 16: 202-8.
133. Stankiewicz JM, Neema M, Alsop DC, Healy BC, Arora A, Buckle GJ, et al. Spinal cord lesions and clinical status in multiple sclerosis: A 1.5 T and 3 T MRI study. J Neurol Sci 2009; 279: 99-105.
134. Bergers E, Bot JC, De Groot CJ, Polman CH, Lycklama à Nijeholt GJ, Castelijns JA, et al. Axonal damage in the spinal cord of MS patients occurs largely independent of T2 MRI lesions. Neurology 2002; 59: 1766-71.
135. Losseff NA, Webb SL, O'Riordan JI, Page R, Wang L, Barker GJ, et al. Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression. Brain 1996; 119: 701-8.
136. Horsfield MA, Sala S, Neema M, Absinta M, Bakshi A, Sormani MP, et al. Rapid semiautomatic segmentation of the spinal cord from magnetic resonance images: application in multiple sclerosis. Neuroimage 2010; 50: 446-55.
137. Liptak Z, Berger AM, Sampat MP, Charil A, Felsovalyi O, Healy BC, et al. Medulla oblongata volume: a biomarker of spinal cord damage and disability in multiple sclerosis. AJNR Am J Neuroradiol 2008; 29: 1465-70.
138. Zackowski KM, Smith SA, Reich DS, Gordon-Lipkin E, Chodkowski BA, Sambandan DR, et al. Sensorimotor dysfunction in multiple sclerosis and column-specific magnetization transfer-imaging abnormalities in the spinal cord. Brain 2009; 132: 1200-9.
139. Mottershead JP, Schmierer K, Clemence M, Thornton JS, Scaravilli F, Barker GJ, et al. High fieldMRIcorrelates of myelin content and axonal density in multiple sclerosis-a post-mortem study of the spinal cord. J Neurol 2003; 250: 1293-1301.
140. Bot JC, Blezer EL, KamphorstW,LycklamaANijeholt GJ, Ader HJ, Castelijns JA, et al. The spinal cord in multiple sclerosis: relationship of high-spatial-resolution quantitative MR imaging findings to histopathologic results. Radiology 2004; 233: 531-40.
141. Vaithianathar L, Tench CR, Morgan PS, Constantinescu CS. Magnetic resonance imaging of the cervical spinal cord in multiple sclerosis-a quantitative T1 relaxation time mapping approach. J Neurol 2003; 250: 307-15.