Measurement of brain and spinal cord atrophy by magnetic resonance imaging as a tool to monitor multiple sclerosis

Journal of Neuroimaging

Volumn 15, Issue 4 SUPPL., 2005, Pages

  Bakshi, Rohit ^a,b   Dandamudi, Venkata S R ^a   Neema, Mohit ^a   De, Chitradeep ^a   Bermel, Robert A ^c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Brain atrophy; Cognitive impairment; Disability; Immunotherapy; Multiple sclerosis; Spinal cord atrophy

Indexed keywords

BETA1A INTERFERON; CORTICOSTEROID; GLATIRAMER; INTERFERON BETA SERINE; METHYLPREDNISOLONE;

BRAIN ATROPHY; BRAIN REGION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CLINICAL TRIAL; COMPARATIVE STUDY; DIAGNOSTIC IMAGING; DISEASE COURSE; FRONTAL LOBE; HUMAN; IMMUNOTHERAPY; MEASUREMENT; MESENCEPHALON; MULTIPLE SCLEROSIS; NEUROPSYCHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL LOBE; PARIETAL LOBE; PHENOTYPE; PONS; REVIEW; SPINAL CORD ATROPHY; TISSUE INJURY;

ATROPHY; BRAIN; DISABILITY EVALUATION; DISEASE PROGRESSION; HUMANS; IMMUNOTHERAPY; MAGNETIC RESONANCE IMAGING; MONITORING, PHYSIOLOGIC; MULTIPLE SCLEROSIS; SPINAL CORD;

EID: 29444447622     PISSN: 10512284     EISSN: 15526569     Source Type: Journal    
DOI: 10.1177/1051228405283901     Document Type: Review

References (110)

1. Bermel RA, Bakshi R. The measurement and clinical relevance of brain atrophy in multiple sclerosis. Lancet Neurol In press.
2. Miller DH, Barkhof F, Frank JA, Parker GJ, Thompson AJ. Measurement of atrophy in multiple sclerosis: pathological basis, methodological aspects and clinical relevance. Brain 2002;125:1676-1695.
3. Rudick RA. Impact of disease-modifying therapies on brain and spinal cord atrophy in multiple sclerosis. J Neuroimaging 2004;14(suppl 3):54S-64S.
4. Zivadinov R, Bakshi R. Central nervous system atrophy and clinical status in multiple sclerosis. J Neuroimaging 2004;14:27S-35S.
5. Benedict RH, Carone DA, Bakshi R. Correlating brain atrophy with cognitive dysfunction, mood disturbances, and personality disorder in multiple sclerosis. J Neuroimaging 2004;14(suppl 3):36S-45S.
6. Lin X, Tench CR, Evangelou N, Jaspan T, Constantinescu CS. Measurement of spinal cord atrophy in multiple sclerosis. J Neuroimaging 2004;(suppl 3);14:20S-26S.
7. Tench CR, Morgan PS, Jaspan T, Auer DP, Constantinescu CS. Spinal cord imaging in multiple sclerosis. J Neuroimaging 2005;15(suppl 1):94S-102S.
8. Minagar A, Toledo EG, Alexander JS, Kelley RE. Pathogenesis of brain and spinal cord atrophy in multiple sclerosis. J Neuroimaging 2004;14(suppl 3):5S-10S.
9. 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.
10. Meier DS, Weiner HL, Khoury SJ, Guttmann CR. Magnetic resonance imaging surrogates of multiple sclerosis pathology and their relationship to central nervous system atrophy. J Neuroimaging 2004;14(suppl 3):46S-53S.
11. Chard DT, Brex PA, Ciccarelli O, et al. The longitudinal relation between brain lesion load and atrophy in multiple sclerosis: a 14 year follow up study. J Neurol Neurosurg Psychiatry 2003;74:1551-1554.
12. Rudick RA, Fisher E, Lee JC, Simon J, Jacobs L. Use of the brain parenchymal fraction to measure whole brain atrophy in relapsing-remitting MS. Multiple Sclerosis Collaborative Research Group. Neurology 1999;53:1698-1704.
13. Ge Y, Grossman RI, Udupa JK, Babb JS, Nyul LG, Kolson DL. Brain atrophy in relapsing-remitting multiple sclerosis: fractional volumetric analysis of gray matter and white matter. Radiology 2001;220:606-610.
14. Quarantelli M, Ciarmiello A, Morra VB, et al. Brain tissue volume changes in relapsing-remitting multiple sclerosis: correlation with lesion load. Neuroimage 2003;18:360-366.
15. Tedeschi G, Lavorgna L, Russo P, et al. Brain atrophy and lesion load in a large population of patients with multiple sclerosis. Neurology 2005;65:280-285.
16. Sanfilipo MP, Benedict RH, Sharma J, Weinstock-Guttman B, Bakshi R. The relationship between whole brain volume and disability in multiple sclerosis: a comparison of normalized gray vs. white matter with misclassification correction. Neuroimage 2005;26:1068-1077.
17. Paolillo A, Pozzilli C, Gasperini C, et al. Brain atrophy in relapsing-remitting multiple sclerosis: relationship with "black holes," disease duration and clinical disability. J Neurol Sci 2000;174:85-91.
18. Bermel RA, Sharma J, Tjoa CW, Puli SR, Bakshi R. A semiautomated measure of whole-brain atrophy in multiple sclerosis. J Neurol Sci 2003;208:57-65.
19. Saindane AM, Ge Y, Udupa JK, Babb JS, Mannon LJ, Grossman RI. The effect of gadolinium-enhancing lesions on whole brain atrophy in relapsing-remitting MS. Neurology 2000;55:61-65.
20. Leist TP, Gobbini MI, Frank JA, McFarland HF. Enhancing magnetic resonance imaging lesions and cerebral atrophy in patients with relapsing multiple sclerosis. Arch Neurol 2001;58:57-60.
21. Zivadinov R, Zorzon M. Is gadolinium enhancement predictive of the development of brain atrophy in multiple sclerosis? A review of the literature. J Neuroimaging 2002;12:302-309.
22. Simon JH, Kinkel RP, Jacobs L, Bub L, Simonian N. A Wallerian degeneration pattern in patients at risk for MS. Neurology 2000;54:1155-1160.
23. Trapp BD, Peterson J, Ransohoff R, Rudick R, Al E. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998;338:278-285.
24. Ge Y, Gonen O, Inglese M, Babb JS, Markowitz CE, Grossman RJ. Neuronal cell injury precedes brain atrophy in multiple sclerosis. Neurology 2004;62:624-627.
25. De Stefano N, Iannucci G, Sormani MP, et al. MR correlates of cerebral atrophy in patients with multiple sclerosis. Neurology 2002;249:1072-1077.
26. Enzinger C, Ropele S, Smith S, et al. Accelerated evolution of brain atrophy and "black holes" in MS patients with APOE-epsilon 4. Ann Neurol 2004;55:563-569.
27. Bakshi R, Dmochowski J, Shaikh ZA, Jacobs L. Gray matter T2 hypointensity is related to plaques and atrophy in the brains of multiple sclerosis patients. J Neurol Sci 2001;185:19-26.
28. Bakshi R, Benedict RH, Bermel RA, et al. T2 hypointensity in the deep gray matter of patients with multiple sclerosis: a quantitative magnetic resonance imaging study. Arch Neurol 2002;59:62-68.
29. Bermel RA, Puli SR, Rudick RA, et al. Prediction of longitudinal brain atrophy in multiple sclerosis by gray matter magnetic resonance imaging T2 hypointensity. Arch Neurol 2005;62:1371-1376.
30. Brex PA, Jenkins R, Fox NC, et al. Detection of ventricular enlargement in patients at the earliest clinical stage of MS. Neurology 2000;54:1689-1691.
31. Fox NC, Jenkins R, Leary SM, et al. Progressive cerebral atrophy in MS: a serial study using registered, volumetric MRI. Neurology 2000;54:807-812.
32. Kalkers NF, Ameziane N, Bot JC, Minneboo A, Polman CH, Barkhof F. Longitudinal brain volume measurement in multiple sclerosis: rate of brain atrophy is independent of the disease subtype. Arch Neurol 2002;59:1572-1576.
33. Redmond IT, Barbosa S, Blumhardt LD, Roberts N. Short-term ventricular volume changes on serial MRI in multiple sclerosis. Acta Neurol Scand 2000;102:99-105.
34. Molyneux PD, Kappos L, Polman C, et al. The effect of interferon beta-1b treatment on MRI measures of cerebral atrophy in secondary progressive multiple sclerosis. European Study Group on Interferon beta-1b in Secondary Progressive Multiple Sclerosis. Brain 2000;123:2256-2263.
35. Ingle GT, Stevenson VL, Miller DH, Thompson AJ. Primary progressive multiple sclerosis: a 5-year clinical and MR study. Brain 2003;126:2528-2536.
36. Ge Y, Grossman RI, Udupa JK, et al. Brain atrophy in relapsing-remitting multiple sclerosis and secondary progressive multiple sclerosis: longitudinal quantitative analysis. Radiology 2000;214:665-670.
37. Zivadinov R, Sepcic J, Nasuelli D, et al. A longitudinal study of brain atrophy and cognitive disturbances in the early phase of relapsing-remitting multiple sclerosis. J Neurol Neurosurg Psychiatry 2001;70:773-780.
38. Filippi M, Rovaris M, Inglese M, et al. Interferon beta-1a for brain tissue loss in patients at presentation with syndromes suggestive of multiple sclerosis: a randomized, double-blind, placebo-controlled trial. Lancet 2004;364:1489-1496.
39. Ge Y, Grossman RI, UdupaJK, et al. Glatiramer acetate (Copaxone) treatment in relapsing-remitting MS: quantitative MR assessment. Neurology 2000;54:813-817.
40. Paolillo A, Piattella MC, Pantano P, et al. The relationship between inflammation and atrophy in clinically isolated syndromes suggestive of multiple sclerosis: a monthly MRI study after triple-dose gadolinium-DTPA. J Neurol 2004;251:432-439.
41. Inglese M, Rovaris M, Giacomotti L, Mastronardo G, Comi G, Filippi M. Quantitative brain volumetric analysis from patients with multiple sclerosis: a follow-up study. J Neurol Sci 1999;171:8-10.
42. Dalton CM, Brex PA, Jenkins R, et al. Progressive ventricular enlargement in patients with clinically isolated syndromes is associated with the early development of multiple sclerosis. J Neurol Neurosurg Psychiatry 2000;68:141-147.
43. Stevenson VL, Miller DH, Leary SM, et al. One year follow up study of primary and transitional progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 2000;68:7l3-7l8.
44. 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;127:1101-1107.
45. Lin X, Blumhardt LD, Constantinescu CS. The relationship of brain and cervical cord volume to disability in clinical subtypes of multiple sclerosis: a three-dimensional MRI study. Acta Neurol Scand 2003;108:401-406.
46. Hohol MJ, Guttmann CR, Orav J, et al. Serial neuropsychological assessment and magnetic resonance imaging analysis in multiple sclerosis. Arch Neurol 1997;54:1018-1025.
47. Losseff NA, Wang L, Lai HM, et al. Progressive cerebral atrophy in multiple sclerosis: a serial MRI study. Brain 1996;119:2009-2019.
48. Turner B. Cerebral atrophy and disability in relapsing-remitting and secondary progressive multiple sclerosis over four years. Mult Scler 2003;9:21-27.
49. Wolinsky JS, Narayana PA, Johnson KP. Multiple Sclerosis Study Group and the MRI Analysis Center. United States open-label glatiramer acetate extension trial for relapsing multiple sclerosis: MRI and clinical correlates. Mult Scler 2001;7:33-41.
50. Gasperini C, Paolillo A, Giugni E, et al. MRI brain volume changes in relapsing-remitting multiple sclerosis patients treated with interferon beta-1a. Mult Scler 2002;8:119-123.
51. Filippi M, Rovaris M, Iannucci G, Mennea S, Sormani MP, Comi G. Whole brain volume changes in patients with progressive MS treated with cladribine. Neurology 2000;55:1714-1718.
52. Bakshi R, Benedict RH, Bermel RA, Jacobs L. Regional brain atrophy is associated with physical disability in multiple sclerosis: semiquantitative magnetic resonance imaging and relationship to clinical findings. J Neuroimaging 2001;11:129-136.
53. Tiberio M, Chard DT, Altmann DR, et al. Gray and white matter volume changes in early RRMS: a 2-year longitudinal study. Neurology 2005;64:1001-1007.
54. De Stefano N, Matthews PM, Filippi M, et al. Evidence of early cortical atrophy in MS: relevance to white matter changes and disability. Neurology 2003;60:1157-1162.
55. Sailer M, Fischl B, Salat D, et al. Focal thinning of the cerebral cortex in multiple sclerosis. Brain 2003;126:1734-1744.
56. Cifelli A, Arridge M, Jezzard P, Esiri MM, Palace J, Matthews PM. Thalamic neurodegeneration in multiple sclerosis. Ann Neurol 2002;52:650-653.
57. Wylezinska M, Cifelli A, Jezzard P, Palace J, Alecci M, Matthews PM. Thalamic neurodegeneration in relapsing-remitting multiple sclerosis. Neurology 2003;60:1949-1954.
58. Taylor I. Serial MRI in multiple sclerosis: a prospective pilot study of lesion load, whole brain volume and thalamic atrophy. J Clin Neurosci 2004;11:153-158.
59. Bermel RA, Innus MD, Tjoa CW, Bakshi R. Selective caudate atrophy in multiple sclerosis: a 3D MRI parcellation study. Neuroreport 2003;14:335-339.
60. Bakshi R, Miletich RS, Kinkel PR, Emmet ML, Kinkel WR. High-resolution fluorodeoxyglucose positron emission tomography shows both global and regional cerebral hypometabolism in multiple sclerosis. J Neuroimaging 1998;8:228-234.
61. Fabiano AJ, Sharma J, Weinstock-Guttman B, et al. Thalamic involvement in multiple sclerosis: a diffusion-weighted magnetic resonance imaging study. J Neuroimaging 2003;13:307-314.
62. Peterson JW, Bo L, Mork S, Chang A, Trapp BD. Transected neuritis, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001;50:389-400.
63. Simon JH, Jacobs LD, Campion MK, et al. A longitudinal study of brain atrophy in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Neurology 1999;53:139-148.
64. Bermel RA, Bakshi R, Tjoa C, Puli SR, Jacobs L. Bicaudate ratio as a magnetic resonance imaging marker of brain atrophy in multiple sclerosis. Arch Neurol 2002;59:275-280.
65. Zivadinov R, Grop A, Sharma J, et al. Reproducibility and accuracy of quantitative magnetic resonance imaging techniques of whole-brain atrophy measurement in multiple sclerosis. J Neuroimaging 2005;15:27-36.
66. Lukas C, Hahn HK, Bellenberg B, et al. Sensitivity and reproducibility of a new fast 3D segmentation technique for clinical MR-based brain volumetry in multiple sclerosis. Neuroradiology 2004;46:906-915.
67. Simon JH. Linear and regional measures of brain atrophy in multiple sclerosis. In: Zivadinov R, Bakshi R, eds. Brain and Spinal Cord Atrophy in Multiple Sclerosis. Hauppauge, NY: Nova Science; 2004:15-27.
68. Benedict RH, Weinstock-Guttman B, Fishman I, Sharma J, Tjoa CW, Bakshi R. Prediction of neuropsychological impairment in multiple sclerosis: comparison of conventional magnetic resonance imaging measures of atrophy and lesion burden. Arch Neurol 2004;61:226-230.
69. Christodoulou C, Krupp LB, Liang Z, et al. Cognitive performance and MR markers of cerebral injury in cognitively impaired MS patients. Neurology 2003;60:1793-1798.
70. Pelletier D, Garrison K, Henry R. Measurement of whole-brain atrophy in multiple sclerosis. J Neuroimaging 2004;14(suppl 3):11S-19S.
71. Sormani MP, Rovaris M, Valsasina P, Wolinsky JS, Comi G, Filippi M. Measurement error of two different techniques for brain atrophy assessment in multiple sclerosis. Neurology 2004;62:1432-1434.
72. Udupa JK, Odhner D, Samarasekera S, et al. 3DVIEWNIX: an open, transportable, multidimensional, multimodality, multiparametric imaging software system. SPIE Proc 1994;2164:58-59, 73.
73. Sanfilipo MP, Benedict RH, Zivadinov R, Bakshi R. Correction for intracranial volume in analysis of whole brain atrophy in multiple sclerosis: the proportion vs. residual method. Neuroimage 2004;22:1732-1743.
74. Smith SM, De Stefano N, Jenkinson M, Matthews PM. Normalized accurate measurement of longitudinal brain change. J Comp Assist Tomogr 2001;25:466-475.
75. Sharma J, Sanfilipo MP, Benedict RH, Weinstock-Guttman B, Munschauer FE III, Bakshi R. Whole-brain atrophy in multiple sclerosis measured by automated versus semiautomated MR imaging segmentation. AJNR Am J Neuroradiol 2004;25:985-996.
76. Barkhof F. MRJ in multiple sclerosis: correlation with expanded disability status scale (EDSS). Mult Scler 1999;5:283-286.
77. Zivadinov R, Leist TP. Clinical-magnetic resonance imaging correlations in multiple sclerosis. J Neuroimaging 2005;15(suppl 1):10S-21S.
78. Dastidar P, Heinonen T, Lehtimaki T, et al. Volumes of brain atrophy and plaques correlated with neurological disability in secondary progressive multiple sclerosis. J Neurol Sci 1999;165:36-42.
79. Fisher E, Rudick RA, Simon JH, et al. Eight-year follow-up study of brain atrophy in patients with MS. Neurology 2002;59:1412-1420.
80. Benedict RHB, Zivadinov R, Carone DA, et al. Regional lobar atrophy predicts memory impairment in multiple sclerosis. AJNR Am J Neuroradiol 2005;26:1824-1831.
81. 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.
82. Sanfilipo MP, Benedict RHB, Weinstock-Guttman B, Bakshi R. Gray and white matter brain atrophy and neuropsychological impairment in multiple sclerosis. Neurology In press.
83. Wei X, Guttmann CR, Warfield SK, Eliasziw M, Mitchell JR. Has your patient's multiple sclerosis lesion burden or brain atrophy actually changed? Mult Scler 2004;4:402-406.
84. Horsfield MA, Rovaris M, Rocca MA, et al. Whole-brain atrophy in multiple sclerosis measured by two segmentation processes from various MRI sequences. J Neurol Sci 2003;216:169-177.
85. Gasperini C, Rovaris M, Sormani MP, et al. Intra-observer, inter-observer and inter-scanner variations in brain MRI volume measurements in multiple sclerosis. Mult Scler 2001;7:27-31.
86. Bentson J, Reza M, Winter J, Wilson G. Steroids and apparent cerebral atrophy on computed tomography scans. J Comput Assist Tomogr 1978;1:16-23.
87. Fox RJ, Fisher E, Tkach J, Lee JC, CohenJA, Rudick RA. Brain atrophy and magnetization transfer ratio following methylprednisolone in multiple sclerosis: short-term changes and long-term implications. Mult Scler 2005;11:140-145.
88. Hoogervorst EL, Polman CH, Barkhof F. Cerebral volume changes in multiple sclerosis patients treated with high-dose intravenous methylprednisolone. Mult Scler 2002;8:415-419.
89. Zivadinov R, Rudick RA, De Masi R, et al. Effects of IV methylprednisolone on brain atrophy in relapsing-remitting MS. Neurology 2001;57:1239-1247.
90. Rudick RA, Fisher E, Lee JC, Duda JT, Simon J. Brain atrophy in relapsing multiple sclerosis: relationship to relapses, EDSS, and treatment with interferon beta-1a. Mult Scler 2000;6:365-372.
91. Rovaris M, Filippi M. Treatment effects on MRI measures of central nervous system atrophy in multiple sclerosis. In: Zivadinov R, Bakshi R, eds. Brain and Spinal Cord Atrophy in Multiple Sclerosis. Hauppauge, NY: Nova Science; 2004:175-190.
92. Hardmeier M, Wagenpfeil S, Freitag P, et al. Rate of brain atrophy in relapsing MS decreases during treatment with IFNbeta-1a. Neurology 2005;64:236-240.
93. Jones CK, Riddehough A, Li DKB, Zhao G, Paty DW. MRI cerebral atrophy in relapsing-remitting MS: results from the PRISMS trial. Neurology 2001;56:A379.
94. Frank JA, Richert N, Bash C, et al. Interferon-beta-1b slows progression of atrophy in RRMS: three-year follow-up in NAb- and NAb+ patients. Neurology 2004;62:719-725.
95. Molyneux PD, Kappos L, Polman C, et al. The effect of interferon beta-1b treatment on MRI measures of cerebral atrophy in secondary progressive multiple sclerosis. European Study Group on Interferon beta-1b in Secondary Progressive Multiple Sclerosis. Brain 2000;123:2256-2263.
96. Rovaris M, Comi G, Rocca MA, Wolinsky JS, Filippi M. European/Canadian Glatiramer Acetate Study Group. Short-term brain volume change in relapsing-remitting multiple sclerosis: effect of glatiramer acetate and implications. Brain 2001;124:1803-1812.
97. Brex PA, Leary SM, O'Riordan JI, et al. Measurement of spinal cord area in clinically isolated syndromes suggestive of multiple sclerosis. J Neurol Neurosurg Psychiatry 2001;70:544-547.
98. Rocca MA, Hickman SJ, Bo L, et al. Imaging spinal cord damage in multiple sclerosis. J Neuroimaging 2005;15:297-304.
99. Bjartmar C, Kidd G, Mork S, Rudick R, Trapp BD. Neurological disability correlates with spinal cord axonal loss and reduced N-acetyl aspartate in chronic multiple sclerosis patients. Ann Neurol 2000;48:893-901.
100. Kidd D, Thorpe JW, Thompson AJ, et al. Spinal cord MRI using multi-array coils and fast spin echo: II. Findings in multiple sclerosis. Neurology 1993;43:2632-2637.
101. Losseff NA, Miller DH. Measures of brain and spinal cord atrophy in multiple sclerosis. J Neurol Neurosurg Psychiatry 1998;64(suppl 1):S102-S105.
102. Stevenson VL, Leary SM, Losseff NA, et al. Spinal cord atrophy and disability in MS: a longitudinal study. Neurology 1998;51:234-238.
103. 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;250:307-315.
104. Hickman SJ, Coulon O, Parker GJ, et al. Application of a B-spline active surface technique to the measurement of cervical cord volume in multiple sclerosis from three-dimensional MR images. J Magn Reson Imaging 2003;18:368-371.
105. Losseff NA, Webb SL, O'Riordan JI, 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;119:701-708.
106. Liu C, Edwards S, Gong Q, Roberts N, Blumhardt LD. Three dimensional MRI estimates of brain and spinal cord atrophy in multiple sclerosis. J Neurol Neurosurg Psychiatry 1999;66:323-330.
107. 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.
108. Lin X, Tench CR, Turner B, Blumhardt LD, Constantinescu CS. Spinal cord atrophy and disability in multiple sclerosis over four years: application of a reproducible automated technique in monitoring disease progression in a cohort of the interferon beta-1a (Rebif) treatment trial. J Neurol Neurosurg Psychiatry 2003;74:1090-1094.
109. Lycklama a 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.
110. Nijeholt GJ, van Walderveen MA, 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.